Compendium of Trace Metals and Marine Biota Volume 1: Plants and Invertebrates
This page intentionally left blank
Compendium of Trace Metals and Marine Biota Volume 1: Plants and Invertebrates by
Ronald Eisler
Amsterdam • Boston • Heidelberg • London • New York • Oxford Paris • San Diego • San Francisco • Singapore • Sydney • Tokyo
Elsevier The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, UK Radarweg 29, PO Box 211, 1000 AE Amsterdam, The Netherlands First edition 2010 Copyright
#
2010 Elsevier BV. All rights reserved
No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means electronic, mechanical, photocopying, recording or otherwise without the prior written permission of the publisher Permissions may be sought directly from Elsevier’s Science & Technology Rights Department in Oxford, UK: phone (þ44) (0) 1865 843830; fax (þ44) (0) 1865 853333; email:
[email protected]. Alternatively you can submit your request online by visiting the Elsevier web site at http://elsevier.com/locate/permissions, and selecting Obtaining permission to use Elsevier material Notice No responsibility is assumed by the publisher for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein. British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress ISBN (Set): 978-0-444-53439-2 ISBN (Vol 1): 978-0-444-53436-1 For information on all Elsevier publications visit our website at books.elsevier.com Printed and bound in Great Britain 10 11 12 10 9 8 7 6 5 4 3
2 1
This volume is dedicated to the memory of my mentors: Yohay Bin-Nun Lauren R. Donaldson Clarence P. Idyll Morton I. Grossman Frank G. Lowman James E. Lynch Lionel A. Walford
This page intentionally left blank
Contents Acknowledgments ........................................................................................... xvii Books by Ronald Eisler..................................................................................... xix About the Author ............................................................................................ xxi List of Tables – Vol. 1....................................................................................xxiii Chapter 1 Introduction ...................................................................................... 1 1.1 Literature Cited...........................................................................................................6
Chapter 2 Algae and Macrophytes...................................................................... 7 2.1 2.2 2.3 2.4 2.5 2.6 2.7 2.8 2.9 2.10 2.11 2.12 2.13 2.14 2.15 2.16 2.17 2.18 2.19 2.20 2.21 2.22 2.23
Aluminum...................................................................................................................7 Americium ..................................................................................................................8 Antimony ....................................................................................................................8 Arsenic........................................................................................................................9 Barium ......................................................................................................................14 Beryllium ..................................................................................................................14 Bismuth.....................................................................................................................15 Boron ........................................................................................................................15 Cadmium ..................................................................................................................16 Cerium ......................................................................................................................22 Cesium ......................................................................................................................22 Chromium .................................................................................................................23 Cobalt........................................................................................................................26 Copper.......................................................................................................................28 Gallium .....................................................................................................................36 Germanium ...............................................................................................................37 Gold ..........................................................................................................................37 Iron............................................................................................................................38 Lead ..........................................................................................................................42 Lithium .....................................................................................................................48 Manganese ................................................................................................................48 Mercury.....................................................................................................................51 Molybdenum.............................................................................................................55
vii
viii
Contents 2.24 2.25 2.26 2.27 2.28 2.29 2.30 2.31 2.32 2.33 2.34 2.35 2.36 2.37 2.38 2.39 2.40 2.41 2.42 2.43
Nickel........................................................................................................................56 Plutonium..................................................................................................................60 Radium......................................................................................................................61 Rhenium....................................................................................................................61 Rubidium ..................................................................................................................61 Ruthenium.................................................................................................................61 Selenium ...................................................................................................................62 Silicon .......................................................................................................................62 Silver.........................................................................................................................64 Strontium ..................................................................................................................66 Technetium ...............................................................................................................67 Tin.............................................................................................................................67 Titanium....................................................................................................................69 Tungsten....................................................................................................................69 Uranium ....................................................................................................................69 Vanadium..................................................................................................................70 Yttrium......................................................................................................................71 Zinc ...........................................................................................................................72 Zirconium .................................................................................................................79 Literature Cited.........................................................................................................80
Chapter 3 Protists .......................................................................................... 99 3.1 3.2 3.3 3.4 3.5 3.6 3.7 3.8 3.9 3.10 3.11 3.12 3.13 3.14 3.15 3.16 3.17 3.18 3.19 3.20
Aluminum.................................................................................................................99 Arsenic......................................................................................................................99 Barium ....................................................................................................................101 Cadmium ................................................................................................................101 Cesium ....................................................................................................................102 Chromium...............................................................................................................102 Cobalt......................................................................................................................102 Copper ....................................................................................................................102 Gallium ...................................................................................................................103 Iron..........................................................................................................................103 Lead ........................................................................................................................103 Manganese ..............................................................................................................104 Mercury...................................................................................................................104 Nickel......................................................................................................................107 Silver.......................................................................................................................107 Strontium ................................................................................................................108 Tin...........................................................................................................................108 Titanium..................................................................................................................109 Zinc .........................................................................................................................109 Literature Cited.......................................................................................................109
Contents ix
Chapter 4 Sponges........................................................................................ 115 4.1 4.2 4.3 4.4 4.5 4.6 4.7 4.8 4.9 4.10 4.11 4.12 4.13 4.14 4.15 4.16 4.17 4.18 4.19 4.20 4.21
Aluminum...............................................................................................................115 Antimony ................................................................................................................115 Arsenic....................................................................................................................115 Barium ....................................................................................................................118 Cadmium ................................................................................................................118 Cobalt......................................................................................................................119 Copper ....................................................................................................................119 Gallium ...................................................................................................................119 Iron..........................................................................................................................119 Lead ........................................................................................................................120 Manganese ..............................................................................................................120 Mercury...................................................................................................................120 Nickel......................................................................................................................120 Plutonium................................................................................................................120 Ruthenium...............................................................................................................120 Selenium .................................................................................................................120 Silver.......................................................................................................................121 Strontium ................................................................................................................121 Vanadium................................................................................................................121 Zinc .........................................................................................................................121 Literature Cited.......................................................................................................121
Chapter 5 Coelenterates ................................................................................ 123 5.1 5.2 5.3 5.4 5.5 5.6 5.7 5.8 5.9 5.10 5.11 5.12 5.13 5.14 5.15 5.16 5.17 5.18
Aluminum...............................................................................................................123 Antimony ................................................................................................................123 Arsenic....................................................................................................................123 Barium ....................................................................................................................124 Bismuth...................................................................................................................125 Boron ......................................................................................................................125 Cadmium ................................................................................................................126 Cesium ....................................................................................................................127 Chromium...............................................................................................................127 Cobalt......................................................................................................................127 Copper.....................................................................................................................127 Gallium ...................................................................................................................129 Iron..........................................................................................................................131 Lead ........................................................................................................................131 Lithium ...................................................................................................................133 Manganese ..............................................................................................................133 Mercury...................................................................................................................134 Molybdenum...........................................................................................................134
x
Contents 5.19 5.20 5.21 5.22 5.23 5.24 5.25 5.26 5.27 5.28 5.29 5.30 5.31 5.32 5.33
Nickel......................................................................................................................134 Radium....................................................................................................................134 Rubidium ................................................................................................................134 Ruthenium...............................................................................................................134 Scandium ................................................................................................................135 Silicon .....................................................................................................................135 Silver.......................................................................................................................135 Strontium ................................................................................................................137 Thorium ..................................................................................................................137 Tin...........................................................................................................................137 Titanium..................................................................................................................137 Uranium ..................................................................................................................139 Vanadium................................................................................................................140 Zinc .........................................................................................................................140 Literature Cited.......................................................................................................141
Chapter 6 Molluscs ....................................................................................... 143 6.1 6.2 6.3 6.4 6.5 6.6 6.7 6.8 6.9 6.10 6.11 6.12 6.13 6.14 6.15 6.16 6.17 6.18 6.19 6.20 6.21 6.22 6.23 6.24 6.25 6.26 6.27
Aluminum...............................................................................................................144 Americium ..............................................................................................................147 Antimony ................................................................................................................148 Arsenic....................................................................................................................150 Barium ....................................................................................................................155 Bismuth...................................................................................................................157 Boron ......................................................................................................................157 Cadmium ................................................................................................................157 Cerium ....................................................................................................................175 Cesium ....................................................................................................................175 Chromium ...............................................................................................................177 Cobalt......................................................................................................................186 Copper.....................................................................................................................192 Europium ................................................................................................................224 Gallium ...................................................................................................................224 Gold ........................................................................................................................224 Hafnium ..................................................................................................................226 Iron..........................................................................................................................226 Lanthanum ..............................................................................................................237 Lead ........................................................................................................................237 Lithium ...................................................................................................................255 Manganese ..............................................................................................................255 Mercury...................................................................................................................266 Molybdenum...........................................................................................................280 Neptunium ..............................................................................................................282 Nickel......................................................................................................................282 Niobium ..................................................................................................................292
Contents xi 6.28 6.29 6.30 6.31 6.32 6.33 6.34 6.35 6.36 6.37 6.38 6.39 6.40 6.41 6.42 6.43 6.44 6.45 6.46 6.47 6.48 6.49 6.50 6.51 6.52 6.53 6.54 6.55
Plutonium................................................................................................................292 Polonium.................................................................................................................293 Protactinium............................................................................................................293 Radium....................................................................................................................293 Rhenium..................................................................................................................294 Rubidium ................................................................................................................294 Ruthenium...............................................................................................................295 Samarium ................................................................................................................295 Scandium ................................................................................................................295 Selenium .................................................................................................................295 Silicon .....................................................................................................................299 Silver.......................................................................................................................299 Strontium ................................................................................................................312 Tantalum .................................................................................................................312 Technetium .............................................................................................................312 Tellurium ................................................................................................................315 Terbium...................................................................................................................315 Thallium..................................................................................................................315 Thorium ..................................................................................................................316 Tin...........................................................................................................................316 Titanium..................................................................................................................329 Tungsten..................................................................................................................329 Uranium ..................................................................................................................329 Vanadium................................................................................................................329 Ytterbium ................................................................................................................329 Zinc .........................................................................................................................329 Zirconium ...............................................................................................................363 Literature Cited.......................................................................................................363
Chapter 7 Crustaceans .................................................................................. 399 7.1 7.2 7.3 7.4 7.5 7.6 7.7 7.8 7.9 7.10 7.11 7.12 7.13 7.14 7.15
Aluminum...............................................................................................................399 Antimony ................................................................................................................399 Arsenic....................................................................................................................399 Barium ....................................................................................................................406 Beryllium ................................................................................................................407 Bismuth...................................................................................................................407 Boron ......................................................................................................................407 Cadmium ................................................................................................................407 Cerium ....................................................................................................................417 Cesium ....................................................................................................................418 Chromium ...............................................................................................................418 Cobalt......................................................................................................................423 Copper.....................................................................................................................424 Dysprosium.............................................................................................................438 Erbium ....................................................................................................................438
xii Contents 7.16 7.17 7.18 7.19 7.20 7.21 7.22 7.23 7.24 7.25 7.26 7.27 7.28 7.29 7.30 7.31 7.32 7.33 7.34 7.35 7.36 7.37 7.38 7.39 7.40 7.41 7.42 7.43 7.44 7.45 7.46 7.47 7.48 7.49 7.50 7.51 7.52 7.53 7.54 7.55 7.56 7.57 7.58
Europium ................................................................................................................439 Gadolinium .............................................................................................................439 Gallium ...................................................................................................................439 Germanium .............................................................................................................440 Gold ........................................................................................................................440 Holmium .................................................................................................................440 Iron..........................................................................................................................440 Lanthanum ..............................................................................................................443 Lead ........................................................................................................................443 Lithium ...................................................................................................................448 Lutetium..................................................................................................................448 Manganese ..............................................................................................................449 Mercury...................................................................................................................452 Molybdenum...........................................................................................................460 Neodymium ............................................................................................................461 Neptunium ..............................................................................................................461 Nickel......................................................................................................................461 Niobium ..................................................................................................................463 Plutonium................................................................................................................463 Polonium.................................................................................................................464 Praseodymium ........................................................................................................464 Protactinium............................................................................................................464 Radium....................................................................................................................464 Rhenium..................................................................................................................464 Rubidium ................................................................................................................465 Ruthenium...............................................................................................................465 Samarium ................................................................................................................465 Scandium ................................................................................................................465 Selenium .................................................................................................................468 Silicon .....................................................................................................................469 Silver.......................................................................................................................469 Strontium ................................................................................................................470 Terbium...................................................................................................................472 Thallium..................................................................................................................472 Thorium ..................................................................................................................472 Thulium...................................................................................................................472 Tin...........................................................................................................................472 Titanium..................................................................................................................476 Tungsten..................................................................................................................476 Uranium ..................................................................................................................476 Vanadium................................................................................................................476 Ytterbium ................................................................................................................476 Yttrium....................................................................................................................477
Contents xiii 7.59 Zinc .........................................................................................................................477 7.60 Zirconium ...............................................................................................................495 7.61 Literature Cited.......................................................................................................495
Chapter 8 Insects.......................................................................................... 517 8.1 8.2 8.3 8.4 8.5 8.6 8.7 8.8 8.9
Cadmium...................................................................................................................517 Chromium .................................................................................................................517 Copper.......................................................................................................................519 Iron............................................................................................................................520 Lead ..........................................................................................................................520 Manganese ................................................................................................................520 Nickel........................................................................................................................520 Zinc ...........................................................................................................................520 Literature Cited ........................................................................................................520
Chapter 9 Chaetognaths ................................................................................ 521 9.1 9.2 9.3 9.4 9.5 9.6 9.7 9.8 9.9 9.10 9.11 9.12 9.13 9.14 9.15 9.16 9.17 9.18 9.19 9.20 9.21
Arsenic....................................................................................................................521 Barium ....................................................................................................................521 Boron ......................................................................................................................524 Cadmium ................................................................................................................524 Chromium...............................................................................................................524 Cobalt......................................................................................................................524 Copper ....................................................................................................................524 Gallium ...................................................................................................................524 Iron..........................................................................................................................525 Lead ........................................................................................................................525 Lithium ...................................................................................................................525 Molybdenum...........................................................................................................525 Nickel......................................................................................................................525 Silver.......................................................................................................................525 Strontium ................................................................................................................525 Tin...........................................................................................................................525 Titanium..................................................................................................................526 Vanadium................................................................................................................526 Zinc .........................................................................................................................526 Zirconium ...............................................................................................................526 Literature Cited.......................................................................................................526
Chapter 10 Annelids ..................................................................................... 527 10.1 10.2 10.3 10.4 10.5 10.6
Aluminum .............................................................................................................527 Americium ............................................................................................................527 Antimony ..............................................................................................................528 Arsenic ..................................................................................................................528 Barium...................................................................................................................529 Cadmium...............................................................................................................529
xiv
Contents 10.7 10.8 10.9 10.10 10.11 10.12 10.13 10.14 10.15 10.16 10.17 10.18 10.19 10.20 10.21 10.22 10.23 10.24 10.25 10.26
Cesium ..................................................................................................................532 Chromium .............................................................................................................532 Cobalt ....................................................................................................................534 Copper...................................................................................................................535 Iron........................................................................................................................537 Lead ......................................................................................................................537 Manganese ............................................................................................................537 Mercury.................................................................................................................537 Nickel....................................................................................................................540 Plutonium..............................................................................................................540 Ruthenium.............................................................................................................541 Samarium ..............................................................................................................541 Scandium ..............................................................................................................542 Selenium ...............................................................................................................542 Silver.....................................................................................................................542 Strontium ..............................................................................................................542 Tin.........................................................................................................................543 Zinc .......................................................................................................................543 Zirconium .............................................................................................................547 Literature Cited.....................................................................................................547
Chapter 11 Echinoderms................................................................................ 553 11.1 11.2 11.3 11.4 11.5 11.6 11.7 11.8 11.9 11.10 11.11 11.12 11.13 11.14 11.15 11.16 11.17 11.18 11.19 11.20 11.21 11.22
Aluminum.............................................................................................................553 Antimony ..............................................................................................................553 Arsenic..................................................................................................................553 Barium ..................................................................................................................556 Boron ....................................................................................................................556 Cadmium ..............................................................................................................556 Cerium ..................................................................................................................558 Cesium ..................................................................................................................558 Chromium.............................................................................................................559 Cobalt....................................................................................................................559 Copper...................................................................................................................561 Europium ..............................................................................................................563 Gallium .................................................................................................................564 Iron........................................................................................................................564 Lead ......................................................................................................................565 Manganese ............................................................................................................566 Mercury.................................................................................................................568 Molybdenum.........................................................................................................569 Nickel....................................................................................................................569 Plutonium..............................................................................................................569 Rubidium ..............................................................................................................571 Scandium ..............................................................................................................571
Contents xv 11.23 11.24 11.25 11.26 11.27 11.28 11.29
Selenium ...............................................................................................................571 Silver.....................................................................................................................571 Strontium ..............................................................................................................573 Technetium ...........................................................................................................575 Tin.........................................................................................................................575 Zinc .......................................................................................................................575 Literature Cited.....................................................................................................578
Chapter 12 Tunicates.................................................................................... 583 12.1 12.2 12.3 12.4 12.5 12.6 12.7 12.8 12.9 12.10 12.11 12.12 12.13 12.14 12.15 12.16 12.17 12.18 12.19 12.20 12.21 12.22 12.23 12.24 12.25 12.26
Antimony ..............................................................................................................583 Arsenic..................................................................................................................583 Barium ..................................................................................................................585 Boron ....................................................................................................................585 Cadmium ..............................................................................................................585 Cesium ..................................................................................................................585 Chromium.............................................................................................................586 Cobalt....................................................................................................................587 Copper ..................................................................................................................587 Iron........................................................................................................................589 Lead ......................................................................................................................589 Manganese ............................................................................................................589 Mercury.................................................................................................................589 Nickel....................................................................................................................589 Niobium ................................................................................................................589 Rubidium ..............................................................................................................591 Ruthenium.............................................................................................................592 Scandium ..............................................................................................................592 Selenium ...............................................................................................................592 Silver.....................................................................................................................592 Strontium ..............................................................................................................592 Tin.........................................................................................................................593 Titanium................................................................................................................593 Vanadium..............................................................................................................593 Zinc .......................................................................................................................595 Literature Cited.....................................................................................................596
Chapter 13 Concluding Remarks .................................................................... 599 13.1 13.2 13.3 13.4
General....................................................................................................................599 Breadth of Coverage ..............................................................................................600 Depth of Coverage .................................................................................................600 Literature Cited.......................................................................................................602
This page intentionally left blank
Acknowledgments Early work on this project was conducted at research libraries of the United States Environmental Protection Agency, the United States Department of the Interior, and the National Library of Medicine. During the past several years, all work was conducted at the National Agricultural Library (NAL) of the United States Department of Agriculture, located in Beltsville, Maryland. I thank the librarians and staff of the NAL for their assistance in procuring needed research materials.
xvii
This page intentionally left blank
Books by Ronald Eisler 2010. Compendium of Trace Metals and Marine Biota. Volume 2: Vertebrates, Elsevier, Amsterdam, 522 pp. 2007. Eisler’s Encyclopedia of Environmentally Hazardous Priority Chemicals, Elsevier, Amsterdam, 950 pp. 2006. Mercury Hazards to Living Organisms, CRC Press, Boca Raton, Florida, 312 pp. 2004. Biogeochemical, Health, and Ecotoxicological Perspectives on Gold and Gold Mining, CRC Press, Boca Raton, Florida, 356 pp. 2000. Handbook of Chemical Risk Assessment: Health Hazards to Humans, Plants, and Animals. Vol. 1, Metals; Vol. 2, Organics; Vol.3, Metalloids, Radiation, Cumulative Index to Chemicals and Species, Lewis Publishers, Boca Raton, Florida, 1903 pp. 1981. Trace Metal Concentrations in Marine Organisms, Pergamon Press, Elmsford, New York, 687 pp.
xix
This page intentionally left blank
About the Author Ronald Eisler received the B.A. degree from New York University, and the M.S. and Ph.D. degrees from the University of Washington. As a federal research scientist, he served with the United States Department of the Interior in the Territory of Alaska (Egegik), New Jersey (Highlands), Maryland (Laurel), and Washington, DC; the United States Environmental Protection Agency in Rhode Island (Narragansett); and the United States Army Medical Service Corps in Colorado (Denver). In addition to federal service, he was a research assistant at the University of Miami Marine Laboratory (Coral Gables, Florida), a radiochemist at the Laboratory of Radiation Ecology at the University of Washington (Seattle), an aquatic biologist at the New York State Department of Environmental Conservation (Raybrook), and the senior science advisor to the American Fisheries Society (Bethesda, Maryland). Dr. Eisler participated in research and monitoring studies in the Pacific Northwest, the Territory of Alaska, Colorado, the Marshall and Marianas Islands, all along the eastern seaboard of the United States Atlantic coast, the Adirondacks region of New York, the Gulf of Aqaba in the Red Sea, and the Gulf of Mexico. Since 1955 he has authored more than 150 technical articles—including several books and 16 book chapters— mainly on contaminant hazards to plants, animals, and human health, with emphasis on trace metals. He has held a number of adjunct professor appointments and taught for extended periods at the Graduate School of Oceanography of the University of Rhode Island, and the Department of Biology of American University in Washington, DC. He also served as Visiting Professor and Resident Director of Hebrew University’s Marine Biology Laboratory in Eilat, Israel. In retirement, he actively consults and writes on chemical risk assessment. Eisler resides in Potomac, Maryland, with his wife, Jeannette, a teacher of French and Spanish.
xxi
This page intentionally left blank
List of Tables – Vol. 1 Table 1.1: Symbol, Atomic Number, and Atomic Weight of the Known Elements Table 2.1: Aluminum Concentrations in Field Collections of Algae and Macrophytes Table 2.2: Antimony Concentrations in Field Collections of Algae and Macrophytes Table 2.3: Arsenic Concentrations in Field Collections of Algae and Macrophytes Table 2.4: Barium Concentrations in Field Collections of Algae and Macrophytes Table 2.5: Beryllium, Bismuth, and Boron Concentrations in Field Collections of Algae and Macrophytes Table 2.6: Cadmium Concentrations in Field Collections of Algae and Macrophytes Table 2.7: Cesium Concentrations in Field Collections of Algae and Macrophytes Table 2.8: Chromium Concentrations in Field Collections of Algae and Macrophytes Table 2.9: Cobalt Concentrations in Field Collections of Algae and Macrophytes Table 2.10: Copper Concentrations in Field Collections of Algae and Macrophytes Table 2.11: Gallium, Germanium, and Gold Concentrations in Field Collections of Algae and Macrophytes Table 2.12: Iron Concentrations in Field Collections of Algae and Macrophytes Table 2.13: Lead Concentrations in Field Collections of Algae and Macrophytes Table 2.14: Lithium Concentrations in Field Collections of Algae and Macrophytes Table 2.15: Manganese Concentrations in Field Collections of Algae and Macrophytes Table 2.16: Mercury Concentrations in Field Collections of Algae and Macrophytes Table 2.17: Molybdenum Concentrations in Field Collections of Algae and Macrophytes Table 2.18: Nickel Concentrations in Field Collections of Algae and Macrophytes Table 2.19: Rubidium Concentrations in Field Collections of Algae and Macrophytes Table 2.20: Selenium and Silicon Concentrations in Field Collections of Algae and Macrophytes Table 2.21: Silver Concentrations in Field Collections of Algae and Macrophytes
xxiii
xxiv List of Tables – Vol. 1 Table 2.22: Strontium Concentrations in Field Collections of Algae and Macrophytes Table 2.23: Tin Concentrations in Field Collections of Algae and Macrophytes Table 2.24: Titanium Concentrations in Field Collections of Algae and Macrophytes Table 2.25: Vanadium Concentrations in Field Collections of Algae and Macrophytes Table 2.26: Zinc Concentrations in Field Collections of Algae and Macrophytes Table 3.1: Trace Element Concentrations in Field Collections of Protists Table 4.1: Trace Element Concentrations in Field Collections of Sponges Table 5.1: Aluminum, Antimony, and Arsenic Concentrations in Field Collections of Coelenterates Table 5.2: Barium, Bismuth, and Boron Concentrations in Field Collections of Coelenterates Table 5.3: Cadmium Concentrations in Field Collections of Coelenterates Table 5.4: Chromium and Cobalt Concentrations in Field Collections of Coelenterates Table 5.5: Copper Concentrations in Field Collections of Coelenterates Table 5.6: Iron Concentrations in Field Collections of Coelenterates Table 5.7: Lead and Lithium Concentrations in Field Collections of Coelenterates Table 5.8: Manganese and Mercury Concentrations in Field Collections of Coelenterates Table 5.9: Molybdenum and Nickel Concentrations in Field Collections of Coelenterates Table 5.10: Scandium, Silicon, and Silver Concentrations in Field Collections of Coelenterates Table 5.11: Strontium, Thorium, Tin, and Titanium Concentrations in Field Collections of Coelenterates Table 5.12: Uranium and Vanadium Concentrations in Field Collections of Coelenterates Table 5.13: Zinc Concentrations in Field Collections of Coelenterates Table 6.1: Aluminum Concentrations in Field Collections of Molluscs Table 6.2: Antimony Concentrations in Field Collections of Molluscs Table 6.3: Arsenic Concentrations in Field Collections of Molluscs Table 6.4: Barium, Bismuth, and Boron Concentrations in Field Collections of Molluscs Table 6.5: Cadmium Concentrations in Field Collections of Molluscs Table 6.6: Cesium Concentrations in Field Collections of Molluscs Table 6.7: Chromium Concentrations in Field Collections of Molluscs Table 6.8: Cobalt Concentrations in Field Collections of Molluscs Table 6.9: Copper Concentrations in Field Collections of Molluscs
List of Tables – Vol. 1
xxv
Table 6.10: Europium, Gallium, Gold, and Hafnium Concentrations in Field Collections of Molluscs Table 6.11: Iron Concentrations in Field Collections of Molluscs Table 6.12: Lead Concentrations in Field Collections of Molluscs Table 6.13: Manganese Concentrations in Field Collections of Molluscs Table 6.14: Mercury Concentrations in Field Collections of Molluscs Table 6.15: Molybdenum Concentrations in Field Collections of Molluscs Table 6.16: Nickel Concentrations in Field Collections of Molluscs Table 6.17: Rubidium Concentrations in Field Collections of Molluscs Table 6.18: Scandium Concentrations in Field Collections of Molluscs Table 6.19: Selenium Concentrations in Field Collections of Molluscs Table 6.20: Silver Concentrations in Field Collections of Molluscs Table 6.21: Strontium Concentrations in Field Collections of Molluscs Table 6.22: Thorium, Tin, Titanium, Tungsten, and Uranium Concentrations in Field Collections of Molluscs Table 6.23: Vanadium Concentrations in Field Collections of Molluscs Table 6.24: Zinc Concentrations in Field Collections of Molluscs Table 7.1: Aluminum Concentrations in Field Collections of Crustaceans Table 7.2: Antimony Concentrations in Field Collections of Crustaceans Table 7.3: Arsenic Concentrations in Field Collections of Crustaceans Table 7.4: Barium, Beryllium, and Boron Concentrations in Field Collections of Crustaceans Table 7.5: Cadmium Concentrations in Field Collections of Crustaceans Table 7.6: Cerium and Cesium Concentrations in Field Collections of Crustaceans Table 7.7: Chromium Concentrations in Field Collections of Crustaceans Table 7.8: Cobalt Concentrations in Field Collections of Crustaceans Table 7.9: Copper Concentrations in Field Collections of Crustaceans Table 7.10: Europium, Gallium, Germanium, and Gold Concentrations in Field Collections of Crustaceans Table 7.11: Iron Concentrations in Field Collections of Crustaceans Table 7.12: Lead Concentrations in Field Collections of Crustaceans Table 7.13: Manganese Concentrations in Field Collections of Crustaceans Table 7.14: Mercury Concentrations in Field Collections of Crustaceans
xxvi List of Tables – Vol. 1 Table 7.15: Molybdenum Concentrations in Field Collections of Crustaceans Table 7.16: Nickel Concentrations in Field Collections of Crustaceans Table 7.17: Scandium, Selenium, and Silver Concentrations in Field Collections of Crustaceans Table 7.18: Strontium Concentrations in Field Collections of Crustaceans Table 7.19: Tin, Titanium, and Tungsten Concentrations in Field Collections of Crustaceans Table 7.20: Vanadium Concentrations in Field Collections of Crustaceans Table 7.21: Zinc Concentrations in Field Collections of Crustaceans Table 8.1:
Trace Element Concentrations in Field Collections of Marine Insects
Table 9.1:
Trace Element Concentrations in Field Collections of Chaetognaths
Table 10.1: Antimony, Arsenic, Barium, and Cadmium Concentrations in Field Collections of Annelids Table 10.2: Chromium, Cobalt, and Copper Concentrations in Field Collections of Annelids Table 10.3: Iron, Lead, and Manganese in Field Collections of Annelids Table 10.4: Mercury and Nickel Concentrations in Field Collections of Annelids Table 10.5: Samarium, Scandium, Silver, and Strontium in Field Collections of Annelids Table 10.6: Zinc Concentrations in Field Collections of Annelids Table 11.1: Aluminum Concentrations in Field Collections of Echinoderms Table 11.2: Antimony Concentrations in Field Collections of Echinoderms Table 11.3: Arsenic Concentrations in Field Collections of Echinoderms Table 11.4: Cadmium Concentrations in Field Collections of Echinoderms Table 11.5: Chromium Concentrations in Field Collections of Echinoderms Table 11.6: Cobalt Concentrations in Field Collections of Echinoderms Table 11.7: Copper Concentrations in Field Collections of Echinoderms Table 11.8: Iron Concentrations in Field Collections of Echinoderms Table 11.9: Lead Concentrations in Field Collections of Echinoderms Table 11.10: Manganese Concentrations in Field Collections of Echinoderms Table 11.11: Mercury Concentrations in Field Collections of Echinoderms Table 11.12: Nickel Concentrations in Field Collections of Echinoderms Table 11.13: Rubidium Concentrations in Field Collections of Echinoderms Table 11.14: Selenium Concentrations in Field Collections of Echinoderms Table 11.15: Silver Concentrations in Field Collections of Echinoderms Table 11.16: Strontium and Tin Concentrations in Field Collections of Echinoderms
List of Tables – Vol. 1
xxvii
Table 11.17: Zinc Concentrations in Field Collections of Echinoderms Table 12.1: Antimony, Arsenic, Barium, Boron, and Cadmium Concentrations in Field Collections of Tunicates Table 12.2: Cesium, Chromium, and Cobalt Concentrations in Field Collections of Tunicates Table 12.3: Copper, Iron, and Lead Concentrations in Field Collections of Tunicates Table 12.4: Manganese, Mercury, Nickel, and Niobium Concentrations in Field Collections of Tunicates Table 12.5: Rubidium, Scandium, Selenium, and Silver Concentrations in Field Collections of Tunicates Table 12.6: Strontium, Tin, and Titanium Concentrations in Field Collections of Tunicates Table 12.7: Vanadium Concentrations in Field Collections of Tunicates Table 12.8: Zinc Concentrations in Field Collections of Tunicates Table 13.1: Trace Metals and Marine Biota: Breadth of Coverage Table 13.2: Trace Metals and Marine Biota: Depth of Coverage
This page intentionally left blank
CHAPTER 1
Introduction The first major attempt to systematically summarize all that was known about trace metal and metalloid content of marine biota was Vinogradov’s classic The Elementary Chemical Composition of Marine Organisms (Vinogradov, 1953) and the last was Trace Metal Concentrations in Marine Organisms (Eisler, 1981). At that time, I recommended major revision in about 25 years owing to a growing technical literature and to a greater availability of atomic absorption spectroscopy and newer analytical techniques that accurately measure trace metal concentrations in tissues of marine plants and animals at biologically significant levels. This volume on plants and invertebrates—and the companion volume on marine vertebrates (Eisler, 2009)—has two main objectives. The first is to summarize the available world literature on trace metal and metalloid concentrations in tissues of representative field populations of marine, estuarine, and oceanic algae and macrophytes, bacteria and protozoans, sponges, coelenterates, molluscs, arthropods, chaetognaths, annelids, echinoderms, and tunicates, and their significance to organism health and to their consumers. The database in this subject area alone has more than doubled in the past several decades. Information on the following elements are presented: aluminum, americium, antimony, arsenic, barium, beryllium, bismuth, boron, cadmium, cerium, cesium, chromium, cobalt, copper, dysprosium, erbium, gadolinium, gallium, germanium, gold, hafnium, holmium, iron, lanthanum, lead, lithium, lutetium, manganese, mercury, molybdenum, nickel, niobium, plutonium, polonium, praseodymium, protactinium, radium, rhenium, rubidium, ruthenium, samarium, scandium, selenium, silicon, silver, strontium, tantalum, technetium, tellurium, terbium, thallium, thorium, thulium, tin, titanium, tungsten, uranium, vanadium, ytterbium, yttrium, zinc, and zirconium (Table 1.1). Information on sodium, potassium, calcium, and magnesium were especially abundant, but these were excluded as their concentrations in marine organisms were almost always in excess of the 100.0 mg/kg dry weight limit that I set arbitrarily as a trace concentration. The second objective is to synthesize selected information on biological, chemical, and physical factors known to modify uptake, retention, and translocation of each element by representative groups of marine plants and invertebrates under field and laboratory
1
2 Chapter 1 Table 1.1: Symbol, Atomic Number, and Atomic Weight of the Known Elements Element
Symbol
Atomic Number
Atomic Weight
Actinium
Ac
89
227a
Aluminum
Al
13
26.98
Americium
Am
95
243a
Antimony
Sb
51
121.76
Argon
Ar
18
39.95
Arsenic
As
33
74.92
Astatine
At
85
210a
Barium
Ba
56
137.33
Berkelium
Bk
97
247a
Beryllium
Be
4
9.01
Bismuth
Bi
83
Bohrium
Bh
197
Boron
B
5
10.81
Bromine
Br
35
79.90
Cadmium
Cd
48
112.41
Calcium
Ca
20
40.01
Californium
Cf
98
251a
Carbon
C
6
12.01
Cerium
Ce
58
140.12
Cesium
Cs
55
132.90
Chlorine
Cl
17
35.45
Chromium
Cr
24
52.00
Cobalt
Co
27
58.93
Copper
Cu
29
63.54
Curium
Cm
96
247a
Dubnium
Db
105
262a
Dysprosium
Dy
66
162.50
Einsteinium
Es
99
252a
208.98 264a
(Continues)
Introduction 3 Table 1.1: Element
Symbol
Cont’d Atomic Number
Atomic Weight
Erbium
Er
68
167.26
Europium
Eu
63
151.96
Fermium
Fm
100
Fluorine
F
9
19.00
Francium
Fr
87
223a
Gadolinium
Gd
64
157.25
Gallium
Ga
31
69.72
Germanium
Ge
32
72.61
Gold
Au
79
196.97
Hafnium
Hf
72
178.49
Hassium
Hs
108
269a
Helium
He
2
4.00
Holmium
Ho
67
Hydrogen
H
1
Indium
In
49
114.82
Iodine
I
53
126.90
Iridium
Ir
77
192.22
Iron
Fe
26
55.85
Krypton
Kr
36
83.80
Lanthanum
La
57
138.91
Lawrencium
Lr
103
Lead
Pb
82
Lithium
Li
3
Lutetium
Lu
71
174.97
Magnesium
Mg
12
24.31
Manganese
Mn
25
54.94
Meitnerium
Mt
109
268a
Mendelevium
Md
101
258a
257a
164.93 1.01
262a 207.20 6.94
(Continues)
4 Chapter 1 Table 1.1:
Cont’d
Element
Symbol
Atomic Number
Atomic Weight
Mercury
Hg
80
200.59
Molybdenum
Mo
42
95.94
Neodymium
Nd
60
144.24
Neon
Ne
10
20.18
Neptunium
Np
93
237a
Nickel
Ni
28
58.69
Niobium
Nb
41
92.91
Nitrogen
N
7
14.01
Nobelium
No
102
Osmium
Os
76
190.23
Oxygen
O
8
16.00
Palladium
Pd
46
106.42
Phosphorus
P
15
30.97
Platinum
Pt
78
195.08
Plutonium
Pu
94
244a
Polonium
Po
84
210a
Potassium
K
19
39.10
Praseodymium
Pr
59
140.91
Promethium
Pm
61
145a
Protactinium
Pa
91
231.04
Radium
Ra
88
226a
Radon
Rn
86
222a
Rhenium
Re
75
186.21
Rhodium
Rh
45
102.91
Rubidium
Rb
37
85.47
Ruthenium
Ru
44
101.07
Rutherfordium
Rf
104
Samarium
Sm
62
259a
261a 150.36 (Continues)
Introduction 5 Table 1.1: Element
Symbol
Cont’d Atomic Number
Atomic Weight
Scandium
Sc
21
44.96
Seaborgium
Sg
106
266a
Selenium
Se
34
78.96
Silicon
Si
14
28.09
Silver
Ag
47
107.87
Sodium
Na
11
23.00
Strontium
Sr
38
87.62
Sulfur
S
16
32.07
Tantalum
Ta
73
180.95
Technetium
Tc
43
98a
Tellurium
Te
52
127.6
Terbium
Tb
65
158.92
Thallium
Tl
81
204.38
Thorium
Th
90
232.04
Thulium
Tm
69
168.93
Tin
Sn
50
118.71
Titanium
Ti
22
47.88
Tungsten
W
74
183.84
Ununbium
Unb
112
Ununennium
Uue
119
–
Ununhexium
Uuh
116
–
Ununnilium
Uun
110
269a
Ununoctiium
Uuo
118
–b
Ununpentium
Uup
115
–b
Ununquadium
Uuq
114
–b
Ununseptium
Uus
117
–b
Ununtriium
Uut
113
–b
Unununium
Unn
111
272a
277a
(Continues)
6 Chapter 1 Table 1.1: Element
Symbol
Cont’d Atomic Number
Atomic Weight
Uranium
U
92
238.03
Vanadium
V
23
50.94
Xenon
Xe
54
131.29
Ytterbium
Yb
70
173.04
Yttrium
Y
39
88.91
Zinc
Zn
30
65.39
Zirconium
Zr
40
91.22
a
Most stable or best known isotope. Yet to be reported.
b
conditions. Recognition of the importance of these modifiers and their accompanying interactions is essential to the understanding of metals kinetics in marine systems and to the interpretation of baseline residue data in marine biota. In many cases, the relation between concentrations of these elements in tissues had little relation to concentrations of the same element in the organisms’s immediate biogeophysical environment including sediments, sediment interstitial waters, diet, and water column. The reasons for this are explored, and their role examined in formulation of proposed criteria by regulatory agencies to protect sensitive natural resources and their consumers. It is emphasized that major changes are now being recorded in global climate extremes and in the amounts of metals, metalloids, and other contaminants discharged into the biosphere as a result of human activities; these changes, and others, may ultimately render obsolete certain terms—now used liberally in this volume—such as “controls,” “reference site,” and “environmentally pristine area.” The organization of this book is similar to that of my earlier work on trace metal concentrations in marine biota (Eisler, 1981): chapters are arranged in evolutionary order starting with most primitive to most advanced; within each chapter, metals and metalloids are arranged in alphabetical order; and, finally, all concentrations are listed in milligrams per kilogram (mg/kg ¼ parts per million) on a fresh weight (FW), dry weight (DW), or ash weight (AW) basis. In all tables, concentrations shown in parentheses represent the range of values documented; others, the means.
1.1 Literature Cited Eisler, R., 1981. Trace Metal Concentrations in Marine Organisms. Pergamon, Elmsford, NY, 687 pp. Eisler, R., 2009. Compendium of Trace Metals and Marine Biota. Volume 2: Vertebrates. Elsevier, Amsterdam. Vinogradov, A.P., 1953. The elementary chemical composition of marine organisms. Sears Foundation for Marine Research, Memoir 2. Yale University, New Haven, CT, 647 pp.
CHAPTER 2
Algae and Macrophytes This group is ubiquitous in aquatic environments with distribution usually limited only by available light and nutrients. It is generally acknowledged that photosynthetic plants form the base of marine food pyramids and that highest biomass is linked to our most productive fisheries, especially biomass of unicellular algae. Continuing interest in the role of algae and macrophytes as indicators of trace metal contaminants, their role in transferring these substances to other environmental compartments, and their potential in removing toxic metals from impacted ecosystems, is reflected by a growing technical literature on this subject.
2.1 Aluminum Aluminum is common in the aquatic environment, but is comparatively harmless to biota under circumneutral or alkaline conditions typical of marine ecosystems (Sparling and Lowe, 1996). Relatively high concentrations of aluminum were evident in marine plants, with many species containing more than 200.0 mg Al/kg dry weight (DW) whole plant and some more than 3000.0 mg Al/kg DW (Table 2.1). More than 90% of the total aluminum was associated with water insoluble and water soluble organic fractions from the cell wall (Bohm, 1972). Laboratory studies with the euryhaline alga Suaeda maritima showed that aluminum accumulations were lower and growth better among saline-reared algae (Yeo and Flowers, 1977). In saline waters, growth was stimulated at 1.0 mg Al/L; after 14 days of exposure, roots contained 0.75 mg Al/kg DW and shoots 0.24 mg Al/kg DW. In nonsaline waters, growth was inhibited under the same dose-time regimen; roots contained 1.59 mg Al/kg DW after 14 days and shoots 0.24 mg Al/kg DW. Higher concentrations of 4.0-16.0 mg Al/L medium inhibited growth, regardless of ambient salinity. After 14 days, Suaeda exposed in saline waters to 16.0 mg Al/L had 4.1 and 0.4 mg Al/kg DW in roots and shoots, respectively. Suaeda immersed for 14 days in fresh water containing 16.0 mg Al/L had elevated levels of 36.7 mg Al/kg DW in roots, and 3.7 mg Al/kg DW in shoots (Yeo and Flowers, 1977).
7
8 Chapter 2 Table 2.1: Aluminum Concentrations in Field Collections of Algae and Macrophytes Organism
Concentration
Reference
Algae, whole
34.0-4200.0 DW
1, 2
Algae, whole, 15 species 12 species 3 species
118.0-490.0 DW 330.0-1750.0 DW
3 3
Alga, Enteromorpha sp. Chesapeake Bay, Maryland San Francisco Bay, California
22,830.0 DW 16,020.0 DW
6 6
Phytoplankton; organic fractions vs. siliceous frustules No titanium group Titanium group Strontium-concentrated group
110.0 DW vs. 620.0 DW 444.0 DW vs. 2550.0 DW 38.0 DW vs. 80.0-110.0 DW
4 4 4
Sargassum spp., whole
33.0-13,450.0 DW
7
Seaweeds, whole, 30 species
533.0 (57.0-3290.0) DW
5
a
Values are in mg Al/kg dry weight (DW). a 1, Culkin and Riley, 1958; 2, Tijoe et al., 1977; 3, Riley and Roth, 1971; 4, Martin and Knauer, 1973; 5, Yamamoto et al., 1976; 6, as quoted in Sparling and Lowe, 1996; 7, Trefry and Presley, 1976.
2.2 Americium Accumulation of americium in marine vegetation is similar to that of plutonium; however, some marine plants, such as Sargassum and Fucus, selectively accumulate plutonium over americium, while others, such as Desmaidetta, Daisia, and Chondrus, accumulate americium over plutonium (Livingston and Bowen, 1976). The reasons for this are not known.
2.3 Antimony Algae reportedly concentrate the antimony content of the surrounding seawater by factors that range from 110 to 340 (Van As et al., 1973). However, the highest antimony levels recorded in whole marine plants were 0.47 mg Sb/kg on a fresh weight (FW) basis and 2.5 mg/kg on a DW basis (Table 2.2). Antimony trioxide is at least six times more toxic to freshwater algae than marine algae. For example, the marine alga Skeletonema costatum had normal chlorophyll a production and normal growth during 96-h exposure to antimony trioxide concentrations less than
Algae and Macrophytes 9 Table 2.2: Antimony Concentrations in Field Collections of Algae and Macrophytes Organism
Concentration
Reference
Algae, whole; 6 species
0.02-0.08 DW
1
Macrophytes; whole; 5 species
0.08-0.47 FW
2
Macrophytes; whole; 3 species
0.07-0.22 FW
5
Macrophytes; whole; 4 spp.; Strait of Magellan, Chile; 2000-2001
<0.2-1.98 DW
6
0.08-0.24 FW 0.05-2.5 DW
3 4
Seaweeds Whole, 5 species Whole
a
Values are in mg Sb/kg fresh weight (FW) or dry weight (DW). a 1, Leatherland and Burton, 1974; 2, Van As et al., 1973; 3, Van As et al., 1975; 4, Lunde, 1970; 5, Strohal et al., 1975; 6, Astorga-Espana et al., 2008.
4.2 mg Sb/L, whereas adverse effects in these variables were observed in freshwater algae during 96-h exposure to 0.01-0.63 mg Sb/L (USEPA, 1989).
2.4 Arsenic Field collections of algae and macrophytes show considerable variation in arsenic content, with known modifiers that include proximity to arsenic mining activities, arsenic valence state, fractions analyzed, and geographic location (Table 2.3). Arsenosugars were the most abundant arsenic species in 8 of 10 species of Adriatic Sea littoral zone algae sampled in 2004; however, Cystoseira and Ceramium (the two species that contained the highest concentrations of total arsenic at 17.6 and 28.1 mg/kg FW, respectively) contained high amounts of mainly inorganic arsenic (Slejkovec et al., 2006). Total arsenic concentrations in the Antarctic region macroalgae ranged from 5.8 mg/kg DW in Myriogramme sp. to 152.0 mg/kg DW in Himantothallus grandfolius (Farias et al., 2007); in general, total arsenic concentrations in brown algae were higher than those in red algae, and this confirms observations in non-Antarctic species of macroalgae (Almela et al., 2006; Cullen and Reimer, 1989). Arsenate reduction to arsenite in seawater is dependent on pentavalent phosphorus in solution and algal biomass (Johnson and Burke, 1978). During algal growth, as phosphate is depleted and the P5+/As5+ ratio decreases, arsenate reduction occurs at an increasing rate. The resultant arsenite (As3+), after an initial peak, is rapidly oxidized to arsenate, suggesting the biological catalysis of oxidation as well as mediation of arsenate reduction. Although most investigators agree that arsenite is more toxic than arsenate to higher organisms, it seems
10 Chapter 2 Table 2.3: Arsenic Concentrations in Field Collections of Algae and Macrophytes Organism
Concentration
Adriatic Sea; 2004; littoral zone; total arsenic Ulva sp. Enteromorpha sp. Padina sp. Gelidium spp. Fucus sp. Cystoseira sp. Ceramium sp.
1.4 FW 1.4 FW 1.9 FW 1.7-2.4 FW 8.4-12.1 FW 17.6 FW 28.1 FW
Algae, whole Green Brown 11 species Various species
0.5-5.0 DW Max. 30.0 DW 2.0-58.0 DW 10.0-100.0 DW
1 1 2 3
17.2 DW vs. 9.8-12.1 DW
7
Algae; whole; 2 species; near arsenic waste outfall vs. sites 5-300 km distant Antarctic region macroalgae; whole; summer 2002; total arsenic vs, inorganic arsenic Brown algae; 6 species Red algae; 3 species
Reference
a
14 14 14 14 14 14 14
33.0-152.0 DW vs. 0.25-0.84 DW 5.8-28.0 DW vs. 0.12-0.55 DW
15 15
Argentina; 3 sites; summer 2002; Porphyra columbina vs. Ulva sp.; whole
22.9-33.8 DW vs. 3.0-5.6 DW
12
Seaweed, Chondrus crispus
5.2 DW
Seaweed, Fucus sp.; whole; arsenic-contaminated site at Seal Harbour, Nova Scotia vs. reference site Total arsenic Inorganic arsenic Trivalent arsenic Pentavalent arsenic Bioaccessible fraction
23.0-43.0 FW vs. 6.0-10.0 FW
11
3.1 FW vs. 0.31 FW 10.1 FW vs. 0.62 FW 18.0-29.0 FW vs. 0.7-1.0 FW
11 11 11
Alga, Fucus sp.; oil vs. fatty acid
6.0-27.0 FW vs. 5.0-6.0 FW
1
Brown alga, Fucus vesiculosus Whole Whole Oil
94.0 DW 35.2-80.0 DW 155.0-221.0 DW
1 4 1
1
(Continues)
Algae and Macrophytes 11 Table 2.3: Organism Fatty acid
Cont’d
Concentration
Reference
8.0-36.0 DW
1
12.2 (2.0-25.0) DW
8
94.0 DW 42.0-50.0 DW 155.0-221.0 DW 8.0-36.0 DW
1 4 1 1
Alga, Laminaria hyperborea; total arsenic vs. organic arsenic
142.0 DW vs. 139.0 DW
2
Seaweed, Padina sp.; Guam; June 1998-1999; fronds
5.3-32.2 DW; max. 38.1 DW
9
Seagrass, Posidonia oceanica; Mediterranean Sea, Spain; 2001-2003; leaves
0.69 (0.2-1.6) DW
Shoalgrass, Halodule wrightii; rhizomes; south Texas, Lower Laguna Madre; 1986-1987 Brown alga, Laminaria digitata Whole Whole Oil Fatty acid
a
13
Sargassum weed, Sargassum fluvitans Total arsenic As3+ As5+ Organoarsenicals
19.5 FW 1.8 FW 17.7 FW 0.2 FW
5 5 5 5
Seaweed, Sargassum sp. Total arsenic As3+ As5+ Organoarsenicals
4.1-8.7 FW 0.14-0.35 FW 1.9-7.3 FW Max. 0.1 FW
6 6 6 6
Seaweeds Whole Whole Oil fraction
3.8-93.8 DW 10.0-109.0 DW 5.7-221.0 FW
1 2 2
Eelgrass, Zostera marina; Oregon Leaf Rhizome Root
4.6 DW 4.8 DW 12.0 DW
10 10 10
Values are in mg As/kg fresh weight (FW) or dry weight (DW). a 1, NAS, 1977; 2, Eisler, 1981; 3, Pershagen and Vahter, 1979; 4, Jenkins, 1980a; 5, Woolson, 1975; 6, NRCC, 1978; 7, Penrose et al., 1975; 8, Custer and Mitchell, 1993; 9, Denton et al., 2006; 10, Kaldy, 2006; 11, Koch et al., 2007; 12, Perez et al., 2007; 13, Fourqurean et al., 2007; 14, Slejkovec et al., 2006; 15, Farias et al., 2007.
12 Chapter 2 that arsenate has a more profound effect than arsenite on growth and morphology of marine algae. It is suggested that marine algae erect a barrier against the absorption of arsenite, but not arsenate; within the cell, arsenate could be reduced to the comparatively toxic arsenite (Johnson and Burke, 1978). Thus,Tetraselmis chui and Hymenomonas carterae cultured in media containing various concentrations of arsenate or arsenite took up arsenate that was partially released by both species; differences between rates of uptake and release of arsenicals suggest that arsenate undergoes chemical changes after incorporation into algal cells (Bottino et al., 1978). Methylated arsenicals such as monomethyl arsonate (MMA) and dimethylarsinate (DMA) are about 1000 times less toxic than inorganic arsenites and arsenates to Chlorella salina; uptake of organoarsenicals is similarly reduced (Karadjova et al., 2008). Seawater enrichment with phosphate—up to 1.3 mg P/L—reduced both intracellular content and toxicity due to inorganic trivalent and pentavalent species, although MMA and DMA were unaffected. The release of inorganic arsenate and arsenite, together with bioreduction of arsenate and subsequent methylation of inorganic arsenite, may be a detoxification mechanism for this alga (Karadjova et al., 2008). In Charlotte Harbor, Florida, a region that has become phosphate enriched due to agricultural activity, virtually all of the arsenic taken up by phytoplankton was biomethylated and returned to the estuary, usually as methylarsonic acid and dimethylarsenic acid (Froelich et al., 1985). The ability of marine phytoplankton to methylate arsenic and release the products to a surrounding environment varies between species and even within a particular species in relation to their possession of necessary methylating enzymes (Sanders, 1985). The process involved in detoxifying arsenate after its absorption by phytoplankton are not firmly established, but seem to be nearly identical in all plants, suggesting a similar evolutionary development (Benson, 1984). Like phosphates and sulfates, arsenate may be fixed with ADP, reduced to the arsonous level, and successfully methylated and adenosylated, ultimately producing the 5-dimethylarsenosoribosyl derivatives accumulating in algae (Benson, 1984). The former kelp industry is considered a probable cause of present day arsenic contamination in remote Scottish islands (Riekie et al., 2006). Burning seaweed to produce kelp was in years past a significant industry in remote coastal areas of Scotland and elsewhere, and may have caused arsenic contamination of soils to 10.7 mg As/kg soil versus 1.7 mg As/kg in reference areas. From 1764 to 1772, an estimated 4900 metric tons of kelp was produced commercially in Scotland, and in 1770-1820 another 2500 tons of kelp was produced on Orkney. Seaweeds containing up to 100.0 mg As/kg DW were burned, transforming lowtoxicity arsenosugars to highly toxic inorganic forms, mainly arsenate (Riekie et al., 2006). The ability of marine phytoplankton to accumulate high concentrations of inorganic arsenicals and transform them to methylated arsenicals that are later efficiently transferred in the food chain is well documented (Benson, 1984; Freeman, 1985; Froelich et al., 1985;
Algae and Macrophytes 13 Irgolic et al., 1977; Maeda et al., 1985; Matsuto et al., 1984; Norin et al., 1985; Sanders, 1985; Yamaoka and Takimura, 1986). In a three-step food chain consisting of Dunaliella marina (alga), brine shrimp Artemia salina (grazer), and a carnivorous shrimp Lysmata seticaudata, organic forms of arsenic are derived from an in vivo synthesis by Dunaliella and efficiently transferred along the food chain (Wrench et al., 1979). Arsenic is taken up from seawater by a variety of organisms, but there is no evidence of magnification along the aquatic food chain (Hallacher et al., 1985; Lindsay and Sanders, 1990; NAS, 1977; NRCC, 1978; Woolson, 1975). In a marine ecosystem based on the alga Fucus vesiculosus, arsenate at 7.5 mg As5+/L was taken up by all biota. After 3 months, arsenic was accumulated most efficiently by Fucus (120.0 mg/kg DW in apical fronds) and filamentous algal species; little or no accumulation occurred in invertebrates, although arsenic seemed to be retained by gastropods and mussels (Rosemarin et al., 1985). Microcosms of a Delaware cordgrass (Spartina alterniflora), salt marsh exposed to elevated levels of As5+, showed that virtually all arsenic was incorporated into plant tissue or strongly sorbed to cell surfaces (Sanders and Osman, 1985). In general, arsenic concentrations are significantly higher in marine plants and animals than in freshwater counterparts because of their ability to accumulate arsenic from seawater or food sources, and not because of localized arsenic pollution (Eisler, 2000; Maher, 1985). The great majority of arsenic in marine biota exists as water-soluble and lipid-soluble organoarsenicals that include arsenolipids, arsenosugars, arsenocholine, arsenobetaine [(CH3)3AsCH2COOH], MMA [CH3AsO(OH)2], DMA [CH3)2AsO(OH)], and other forms (Edmonds et al., 1993). Arsenosugars (arsenobetaine precursors) are the dominant arsenic species in brown kelp, Ecklonia radiata, and certain molluscs and crustaceans (Eisler, 2000). Adverse effects of arsenites are reported in marine plants at 0.019-0.58 mg As3+/L and of arsenates at 0.013-100.0 mg As5+/L. Among the most sensitive of all marine species of plants and animals tested were three species of algae, which had reduced growth during exposure to 0.019-0.022 mg As3+/L (USEPA, 1985a). Arrested spore development was documented in the red alga Plumaria elegans 7 days after exposure to 0.58 mg As3+/L for 18 h (Sanders, 1986). Normal sexual reproduction was documented in the red alga Champia parvula at concentrations <0.065 mg As3+/L; however, sexual reproduction ceased at 0.095 mg As3+/L and death occurred at 0.3 mg As3+/L (Thursby and Steele, 1984). For Champia and pentavalent arsenic, normal growth—but no sexual reproduction—was observed at 10.0 mg As5+/L (Thursby and Steele, 1984). Chronic studies with mass cultures of natural phytoplankton communities exposed to low levels of arsenate (0.001-0.015 mg As5+/L) showed that As5+ differentially inhibits certain plants, causing a marked change in species composition, succession, and predator-prey relations; the significance of these changes on carbon transfer between trophic levels is unknown (Sanders, 1986; Sanders and Cibik, 1985). Growth inhibition occurred in S. costatum at
14 Chapter 2 0.013 mg As5+/L (USEPA, 1985a) and reduced chlorophyll a production was observed in Thalassiosira aestivales at 0.075 mg As5+/L (USEPA, 1985a). Sargassum communities seemed normal during exposure to 0.028 mg As5+/L (Blake and Johnson, 1976). Results from laboratory studies with five species of euryhaline algae grown in freshwater or in seawater show that all five species synthesize fat-soluble and water-soluble organoarsenicals from both arsenate and arsenite. Arsenic concentration factors over seawater among the five species ranged from 200 to 3000, with accumulations highest in lipid phases (Lunde, 1973).
2.5 Barium The maximum barium concentrations in whole marine plants were 12.0 mg Ba/kg FW and 287.0 mg/kg DW (Table 2.4). The highest concentration of 287.0 mg Ba/kg DW was measured in a phytoplankton organic fraction containing high strontium content (Martin and Knauer, 1973), emphasizing the importance of interactions.
2.6 Beryllium Beryllium concentrations in marine algae ranged from a low of 1.1 mg Be/kg DW in Dunaliella tertiolecta to 8.4 mg Be/kg DW in Heteromastix longifillis (Riley and Roth, 1971; Table 2.5). Table 2.4: Barium Concentrations in Field Collections of Algae and Macrophytes Organism
Concentration
Reference
Algae, whole, 15 species 9 species 5 species 1 species
34.5-76.0 DW 80.0-145.0 DW 262.0 DW
1 1 1
Algae, whole Chlorophycae Phaeophyceae Rhodophyceae
0.09-0.44 FW 0.05-0.38 FW 0.05-0.36 FW
2 2 2
Phytoplankton, organic reactions No titanium group With titanium group Strontium-concentrated group
33.0 DW 19.0 DW 287.0 DW
3 3 3
Seaweeds, whole, 5 species May June
13.0-44.0 DW 16.0-64.0 DW; 3.1-12.0 FW
4 4
a
Values are mg Ba/kg fresh weight (FW) or dry weight (DW). a 1, Riley and Roth, 1971; 2, Mauchline and Templeton, 1966; 3, Martin and Knauer, 1973; 4, Black and Mitchell, 1952.
Algae and Macrophytes 15 Table 2.5: Beryllium, Bismuth, and Boron Concentrations in Field Collections of Algae and Macrophytes Element and Organism
Concentration
Reference
a
Beryllium Algae, whole, 14 species 6 species 4 species 2 species 2 species
1.1-2.0 DW 2.1-3.0 DW 3.1-4.0 DW 5.7-8.4 DW
1 1 1 1
2.0-7.7 DW
1
Seaweeds, whole, 41 species
106.0 (16.0-319.0) DW
2
Algae
4.0-120.0 DW
3
Argentina; summer 2002; 3 sites; Porphyra columbina vs. Ulva sp.; whole
12.6-16.5 DW vs. 37.9-58.3 DW
4
Bismuth Algae, whole, 6 species Boron
Values are in mg element/kg dry weight (DW). a 1, Riley and Roth, 1971; 2, Yamamoto et al., 1971; 3, Jenkins, 1980b; 4, Perez et al., 2007.
2.7 Bismuth Bismuth concentrations in field collections of marine algae ranged from 2.0 mg Bi/kg DW in Monochrysis lutheri to 7.7 mg Bi/kg DW in Chlamydomonas sp. (Riley and Roth, 1971; Table 2.5).
2.8 Boron Boron content among 41 species of seaweeds collected from Wakayama Prefecture, Japan, ranged from 16.0 to 319.0 mg B/kg DW (Table 2.5). Boron is an essential trace element for the diatom Cylindrotheca fusiformis (Lewin and Chen, 1976) and probably other marine plants. Boron interactions with water temperature, nitrates, phosphates, and silicates are important governors of phytoplankton growth (Rao, 1981). At 30.0 mg B/L, at low temperatures and high concentrations of nitrates, phosphates, and silicates, marine phytoplankton show increased primary production and carbon assimilation. At 30.0 mg B/L, under conditions of high temperatures and low nutrients, photosynthesis is inhibited up to 62% (Rao, 1981). Cylindrotheca grown in boron-deficient medium of 0.02 mg B/L had a generation time of 90 h compared to only 11 h when
16 Chapter 2 cultured in complete medium containing 0.5 mg B/L (Lewin and Chen, 1976). Borondeficient Cylindrotheca accumulate rubidium, phenolic compounds, nitrates, and phosphates, and show increased activity of various enzymes, especially glucose-6-phosphate dehydrogenase; however, respiratory adjustment is negligible until nutrient stress becomes irreversible in about 48 h (Smyth and Dugger, 1980, 1981). Phytoplankton are comparatively resistant to high boron concentrations, and no measurable effects were observed during exposure to media containing 5.0-10.0 mg B/L; however, growth inhibition of 25% was documented at 50.0 mg B/L, and about 40% were killed at 100.0 mg B/L (Antia and Cheng, 1975).
2.9 Cadmium The grossly elevated levels of 22.0-220.0 mg Cd/kg DW in algae (Table 2.6) were almost always directly associated with cadmium pollution from human activities. The ability of algae and macrophytes to accumulate cadmium from ambient seawater is well documented. Concentration factors ranged from 4200 to 11,000 for field collections (Melhuus et al., 1978) and from 11 to 36 in laboratory studies with radiocadmium (Hiyama and Shimizu, 1964) and stable cadmium (Sivalingam, 1978b). Marine algae accumulated more cadmium at lower salinities than at higher salinities; algae bound only free cadmium ions, and these were inversely related to the concentration of suspended particulate matter (Favero et al., 1996). Ulva reticulata showed a 36-fold increase in 48 h over seawater containing 50.0 mg Cd/L (Sivalingam, 1978b). Others have shown that diatoms held in seawater containing 1.0 mg Cd/L for 12 days had 8300.0 mg Cd/kg FW (Cossa, 1976), S. alterniflora seedlings reared in media containing 100.0 mg Cd/L for 8 weeks contained 94.0 mg Cd/kg FW (Dunstan et al., 1975), and 85-95% uptake was measured among two algal species held in 1.8 mg Cd/L for 24 h (Maclean et al., 1972). Up to 80% of accumulated cadmium was retained for at least 13 days in Ulva sp. (Ueda et al., 1978). Sporophytes of the kelp, Laminaria saccharina, when placed in cadmium-seawater solutions begin to accumulate cadmium almost immediately without apparent regulation (Markham et al., 1980). Saturation was not reached within 6 days suggesting the potential for high accumulations. Slower growing plants and slower growing regions of the thallus, such as the stipe, holdfast, and distal blade regions, accumulated more cadmium than did other portions of the plant (Markham et al., 1980). The sea rush, Juncus maritimus, a saltmarsh plant, accumulated cadmium in roots continuously throughout the year in the Douro River estuary in Portugal, and is considered a major photostabilizer in cadmium regulation in that area (Almeida et al., 2006). Cadmium-copper antagonism in seaweeds inhabiting coastal Chile affected by copper mine wastes is reported (Andrade et al., 2006). High copper accumulations in various species of
Algae and Macrophytes 17 Table 2.6: Cadmium Concentrations in Field Collections of Algae and Macrophytes Organism Algae, whole Chlorophycae; 5 spp. Phaeophyceae; 4 spp. Rhodophyceae, 10 spp. Rio Tinto estuary, Spain West Norway coast Israel; Mediterranean Sea coast; 2 spp. United Kingdom, Solant region; 2 spp. Argentina; 3 sites; summer 2002; Porphyra columbina vs. Ulva sp.; whole
Concentration 8.3-16.3 DW 5.6-13.8 DW 3.7-13.2 DW Max. 7.4 DW Max. 20.0 DW 0.9-2.1 DW 0.3-0.4 DW
a
Reference 1 1 1 2 20 3 4
2.8-3.5 DW vs. 0.2-1.0 DW
27
6.0-15.0 DW 3.5-5.7 DW <1.0 DW <1.0-4.0 DW
9 10 10 10
1.8 DW 1.5 DW <0.7 DW <0.7-1.0 DW 0.7-16.0 DW 0.1-0.6 DW
11 11 12 12 12 33
0.29 (0.08-0.62) DW <0.1 DW 0.19 DW; max. 0.39 DW
28 28 28
Green alga, Enteromorpha sp.; whole; 2000-2003; Gulf of Gdansk, Baltic Sea
0.44 (0.03-1.08) DW
24
Alga, Skeletonema costatum, whole; water content 0.01 mg Cd/L
4.0 DW
17
Fucus distichus, whole
0.7-1.8 DW
13
Brown alga, Ascophyllum nodosum; whole Sorfjorden, Norway Eikhamrane, Norway Flak, Norway Transferred from Eikhamrane to Flak for 120 days Menai Straits, United Kingdom Dulas Bay, United Kingdom Lofoten, Norway Trondheimsfjord, Norway Hardangerfjord, Norway Coast of Ireland; 1999-2000 Green alga, Cladophora sp.; 2000-2003; Baltic Sea Gulf of Gdansk Vistula Lagoon Reference site
(Continues)
18 Chapter 2 Table 2.6:
Cont’d
Organism
Concentration
Fucus serratus, whole Sorfjorden, Norway Portland, Dorset, United Kingdom Severn estuary, United Kingdom
22.0-29.0 DW 0.3 DW 53.0 DW
Fucus vesiculosus, whole Sorfjorden, Norway Tamar estuary, United Kingdom Menai Straits, United Kingdom Dulas Bay, United Kingdom Severn estuary, United Kingdom Irish Sea
8.6-10.6 DW 4.8 (1.8-9.0) DW 2.1 DW 1.8 DW 220.0 DW 1.4 DW
9 14 11 11 15 16
Halophytes; 2 spp.; leaves, Tamil Nadu, India; anuary 2007
<0.31 DW
38
Macroalgae (6 spp). vs. phytoplankton; Gulf of California, Mexico; 1998-1999; whole
0.13-0.87 DW vs. 0.27 DW
25
Macroalgae; 3 spp.; epiphytic on estuarine mangrove aerial roots; Sydney region, Australia; sites
Not detectable
29
0.59 vs. 0.17 DW 0.12 DW vs. 0.1 DW 0.29 DW vs. 0.25 DW
25 25 25
0.27 DW
35
0.23 DW vs. 0.87 DW
35
0.17 DW 0.1 DW 0.25 DW
35 35 35 35
0.07-0.26 DW
21
Mangroves; Gulf of California, Mexico; 1998-1999; twigs vs. leaves Rhizophora mangle Avicennia germinans Laguncularia racemosa Mexico; Gulf of California; 19992000 Microalgae, Coscinodiscus centralis; whole Macroalgae; Gracilaria sp. vs. Polysiphonia sp.; whole Mangroves; leaves Rhizophora mangle Avicennia germinans Laguncularia racemosa Seaweed, Padina sp.; Guam; 1998-1999; fronds
Reference
a
9 4 9
(Continues)
Algae and Macrophytes 19 Table 2.6: Organism Macrophyte, Posidonia oceanica Italy Sheath Rhizome Mediterranean Sea; blade; summers 2004-2005 Corsica, France; summer 2003; adult leaves; blades vs. sheaths Mangrove, Rhizophora mangle; Natal, Brazil; summer 2001; leaves
Cont’d
Concentration
a
Reference
0.6-2.0 DW 0.8-2.4 DW 2.1-5.4 DW
23 23 31
2.8 (1.5-4.0) DW vs. 1.0 (0.7-1.7) DW
34, 36
1.1-1.4 DW
3
Saltmarsh grass, Spartina alterniflora Whole Leaves and stalks
0.6 DW 0.5 DW
18 17, 19
Seaweed, Ulva lactuca Gulf of California, Mexico; 2002; whole Summer Winter
1.3-1.5 DW 2.6 DW
26 26
India; 2004-2005; industrial area
38.1 (21.7-59.6) DW
32
Seaweeds Australia, 3 spp. Japan, 5 spp. Korea 17 spp. 20 spp. Eelgrass, Zostera marina Baja California, Mexico; March 2000; reference site vs. salt mining site; whole Oregon Leaf Rhizome Root
0.03-85.0 DW 0.1-0.3 DW
6 5
0.02-1.5 DW 0.2-3.4 DW
7 8
1.6 (0.03-3.4) DW vs. 6.2 (0.008-66.0) DW
37
1.7 DW 0.8 DW 6.4 DW
22 22 22
Values are in mg Cd/kg dry weight (DW) or fresh weight (FW). a 1, Sivalingam, 1978b; 2, Stenner and Nickless, 1975; 3, Roth and Hornung, 1977; 4, Leatherland and Burton, 1974; 5, Ishibashi et al., 1964a; 6, Harris et al., 1979; 7, Kim, 1972; 8, Pak et al., 1977; 9, Melhuus et al., 1978; 10, Myklestad et al., 1978; 11, Foster, 1976; 12, Haug et al., 1974; 13, Bohn, 1979; 14, Bryan and Uysal, 1978; 15, Butterworth et al., 1972; 16, Preston et al., 1972; 17, Windom et al., 1976; 18, Dunstan et al., 1975; 19, Windom, 1975; 20, Stenner and Nickless, 1974; 21, Denton et al., 2006, 22, Kaldy, 2006; 23, Baroli et al., 2001; 24, Zbikowski et al., 2006; 25, Ruelas-Inzunza and Paez-Osuna, 2006; 26, Orduna-Rojas and Longoria-Espinoza, 2006; 27, Perez et al., 2007; 28, Zbikowski et al., 2007; 29, Melville and Pulkownik, 2007; 30, Silva et al., 2006; 31, Lafabrie et al., 2007b; 32, Kamala-Kannan et al., 2008; 33, Morrison et al., 2008; 34, Lafabrie et al., 2008a; 35, RuelasInzunza and Paez-Osuna, 2008; 36, Lafabrie et al., 2008b; 37, Marcias-Zamora et al., 2008; 38, Agoramoorthy et al., 2008.
20 Chapter 2 seaweeds collected in 2003-2004 appear to suppress cadmium burdens, and seaweeds from copper-contaminated sites had lower burdens (0.1-1.9 mg Cd/kg DW) than did reference sites (2.5-17.8 mg Cd/kg DW). Transplants of Lessonia nigrescens from a reference site to a copper-contaminated site resulted in cadmium depuration; however, cadmium loss occurs more slowly than copper uptake (Andrade et al., 2006). Studies on accumulation of cadmium by eelgrass, Zostera marina, under laboratory conditions, show active transport across cell membranes, as opposed to passive diffusion (Faraday and Churchill, 1979). Most, if not all, of the cadmium uptake occurred through the roots, and this was directly related to cadmium concentration and exposure time. Cadmium uptake by the root rhizomes was similar at dissolved oxygen concentrations of 6% or 90% saturation. In separate studies, cadmium could also accumulate in Zostera leaves, with increasing translocation to the root rhizomes over time, where it remained. It was concluded that Z. marina is not important in cycling of cadmium from sediments into the water column, but may be very important in removing cadmium from the water column and returning it to the sediments via translocation to the root rhizomes. Maximum cadmium concentrations recorded in roots rhizomes and leaves after immersion for 72 h in 1.0 mg Cd/L were 48.0 mg Cd/kg DW in roots and 94.0 mg Cd/kg DW in leaves (Faraday and Churchill, 1979). C. salina, a euryhaline alga, can accumulate up to 142.0 mg Cd/kg FW after exposure for 14 days to 0.1 mg Cd/L in fresh water; however, cadmium uptake is drastically reduced at lower ambient cadmium concentrations and at salinities of 5 ppt, which was the lowest test salinity examined (Wong et al., 1979). Salt marsh plants accumulated higher concentrations of cadmium from contaminated soils under oxidizing conditions: however, well-oxidized soils amended with up to 50.0 mg Cd/kg were associated with reduced yields (Gambrell et al., 1977). Algae can also accumulate cadmium from sewage sludge as shown in 120-day exposure studies with Thalassiosira testudinum (Montgomery et al., 1978). Seagrass, T. testudinum, exposed to graded concentrations of cadmium for 96 h took up cadmium in proportion to the dose, with concentrations highest in green blades (max. 150.0 mg Cd/kg DW), roots and rhizomes (17.8 mg/Cd kg DW), and live sheaths (8.0 mg/kg DW); all tissues had increases in thiolcontaining compounds as a response to cadmium exposure (Alvarez-Legorreta et al., 2008). Below ground portions of two species of saltmarsh plants collected from the Tagus estuary, Portugal, in March 2004, had elevated concentrations of cadmium when compared to aerial portions (Reboreda and Cacador, 2007). Cadmium values in Spartina maritima, in mg Cd/m2 DW, were 19.3 for roots, 0.8 for stems, and 0.2 for leaves. For Halimione portulacoides, these values were 22.4 for roots, 2.3 in stems, and 0.7 in leaves. Authors conclude that areas colonized by Spartina are effective sinks for cadmium in the estuary and those colonized mainly by Halimione are more effective sources (Reboreda and Cacador, 2007). Sensitivity of algae to cadmium varied considerably. Growth inhibition in the diatom Phaeodactylum tricornutum occurred at 5.4 mg Cd/L in 72 h; however, growth stimulation
Algae and Macrophytes 21 was recorded at 0.16-1.0 mg Cd/L (Horvatic and Persic, 2007), although this requires verification. Growth inhibition was evident at cadmium concentrations in excess of 0.45 mg Cd/L over a 10-day period for Pelvetia sp., Fucus spp., and Ascophyllum nodosum (Stromgren, 1980). At lower concentrations, growth was significantly enhanced in Pelvetia and Ascophyllum (Stromgren, 1980). Berland et al. (1976) with reports that concentrations of 0.051.0 mg Cd/L killed 18 species of algae in 17 days, with growth inhibition reported in the range of 0.005-0.25 mg Cd/L. Concentrations of 0.01-0.025 mg Cd/L depressed the growth of P. tricornutum (Cossa, 1976) and S. costatum (Berland et al., 1977). However, no deleterious effects were observed at 11.2 mg Cd/L and lower among four species grown in batch culture (Bentley-Mowat and Reid, 1977), and among Spartina seedlings held in 100.0 mg Cd/L for 8 weeks (Dunstan et al., 1975); concentrations up to 100.0 mg Cd/L had no measurable effect on oxygen uptake of most species of algae tested (Mills and Colwell, 1977). But concentrations of 112.0 mg Cd/L inhibited photosynthesis within 15 min in the four species of alga tested (Overnell, 1976). It is probable that some of this variability in cadmium sensitivity was attributable to biological availability. For example, chelated cadmium had no demonstrable effect on P. tricornutum (Cossa, 1976). Macroalgae, Enteromorpha prolifera and Enteromorpha linza stressed by 0.1 or 0.2 mg Cd/L react differently (Malea et al., 2006). In E. linza, glutathione pools increased, but were susceptible to Cd-induced oxidative stress. In E. prolifera, cadmium was actively detoxified by phytochelatins (Malea et al., 2006). Red alga, Audouinella saviana, was exposed to lethal concentrations of cadmium for up to 15 days (Talarico, 2002). Among survivors, thalli of treated algae—when compared to controls—had abnormal plasmalemna, enhanced protein and carbohydrate biosynthesis, and smooth and thick cell walls. Chloroplasts did not accumulate cadmium and were the least affected organelles. Cadmium toxicity is reduced in this cadmium-tolerant species by formation of polysaccharides and structural proteins as a cell wall barrier blocking Cd2+ ions in the cell wall by negatively charged groups, cytoplasmic ion detoxification by chelating proteins and cytoplasmic sequestering, and by accumulation of metal complexes into large vacuoles (Talarico, 2002). Mixtures of cadmium and zinc ions were more effective in the inhibition of growth of Thalassiosira pseudonana, and of clone Skel-5 of S. costatum than either metal alone (Braek et al., 1980). However, cadmium-zinc mixtures were less than additive in producing growth inhibition of P. tricornutum and S. costatum, clone Skel-0. The relative resistance of the latter two species is attributed to competition for uptake sites by different chemical forms of cadmium and zinc. In the most resistant alga, P. tricornutum, sorption of cadmium as well as zinc was dependant on magnesium concentration of the medium. It was concluded that high levels of nontoxic divalent cations, such as calcium, magnesium, and strontium in seawater, compete with the same uptake sites as toxic divalent cations such as cadmium, copper, and zinc, and may, therefore, protect against metal poisoning in marine organisms (Braek et al., 1980).
22 Chapter 2
2.10 Cerium Radiocerium-144 was concentrated from the medium by six species of algae by factors of 300-3000 within 30 min and by factors of 2000-4500 after 24 h (Rice and Willis, 1959); similar results are reported by Ancellin and Vilquin (1968). Dead algae continue to adsorb 144Ce, as was the case for Cystoseira barbata (Polikarpov, 1961), suggesting that residue levels in algae dead on collection should be viewed with reservation (Eisler, 1981). Uptake and retention of cerium by algae is variable. Nondividing cells of Nitzchia closterium kept in the dark continue to accumulate 144Ce for as long as 3 days, and particulate cerium became associated with the cells more rapidly than did ionic cerium (Rice and Willis, 1959); further, chelating compounds added to the medium reduced uptake of radiocerium by Nitzchia (Rice and Willis, 1959), and other species (Hiyama and Shimizu, 1964). Loss rate of cerium from algae is variable; about 25% in 5 h on transfer to cerium-free media; this effect was accelerated when the transfer medium contained chelating agents (Rice and Willis, 1959). The greatest loss of 144Ce was from biological dilution as a result of cell division; this loss amounted to 50% of the contained activity of the cells at each division (Rice and Willis, 1959).
2.11 Cesium The highest concentration of stable cesium recorded in a marine plant is 0.071 mg/kg DW in whole Sargassum thunbergii collected off the coast of Japan (Ishii et al., 1978). On a DW basis, cesium values in other species of marine plants ranged from 0.031 to 0.061 mg/kg (Table 2.7).
Table 2.7: Cesium Concentrations in Field Collections of Algae and Macrophytes Organism
Concentration
Algae, whole, 6 species
0.037-0.061 DW
1
Alga, Hizakia fusiforme, whole; varying lengths up to 10 cm 10.1-20 cm 20.1-30 cm
0.031 DW 0.036 DW 0.051 DW
1 1 1
Sargassum spp., whole, 5 species
0.037-0.071 DW
1
Seaweeds, whole, 5 species
0.003-0.023 FW
2, 3
Values are in mg Cs/kg fresh weight (FW) or dry weight (DW). a 1, Ishii et al., 1978; 2, Van As et al., 1973; 3, Van As et al., 1975.
Reference
a
Algae and Macrophytes 23 Radiocesium accumulation rates by marine plants vary significantly among species. Concentration factors up to 2 are listed with equilibrium reached in 24 h (Hiyama and Shimizu, 1964), up to 3 (Ueda et al., 1978), up to 6 (Ichikawa, 1961), 4 to 30 (Gutknecht, 1965), up to 30 (Ishii et al., 1978), up to 40 (Ancellin and Vilquin, 1968), 8 to 70 (Van As et al., 1973), and 2740 to 3360 in algulose and alginic acid fractions (Ryndina, 1976). Accumulations were higher in fresh than in decaying samples of Cystoseira and other species; however, the opposite was observed for C. barbata (Polikarpov, 1961). Light, nitrogen, oxygen, dissolved cesium concentrations, and chemical form affect cesium dynamics in seaweeds (Gutknecht, 1965). Uptake and loss of 137Cs by seaweeds were stimulated by light, although some activity occurred in the dark. Previous exposure to light stimulated radiocesium-137 uptake in the dark; exposure to nitrogen in the dark inhibited both influx and efflux of 137Cs. Neither darkness nor anoxia caused appreciable loss of 137Cs. Radiocesium was not extensively adsorbed by cell walls or killed tissues. Influx and efflux of cesium were proportional, respectively, to the external and internal radiocesium concentrations. Finally, intracellular cesium appears to be largely ionic, with cesium movements closely related to metabolism (Gutknecht, 1965).
2.12 Chromium High concentrations of chromium were recorded in marine algae and other biota near electroplating plants, tanneries, oil drilling operations, sewage outfalls, drift cooling towers, dump sites, and other sources of chromium-containing wastes that were being discharged into the environment (Eisler, 2000c). Marine plants can accumulate chromium from seawater by factors ranging from 5890 to 10,930 (El Ati-Hellal et al., 2007; Van As et al., 1973), from solutions containing 50.0 mg Cr/L by a factor of 18 in 49 h (Sivalingam, 1978a), and from sewage sludge containing 25.0 mg Cr/kg DW by a factor of 2.2 (Montgomery et al., 1978). The unusually high chromium concentrations observed among some species of algae and macrophytes from Puerto Rico (Bernhard and Zattera, 1975) and from Narragansett Bay, Rhode Island, United States (Phelps et al., 1975), were almost certainly due to chromium wastes discharged into the Bay from electroplaters in the case of Rhode Island and from other anthropogenic sources in Puerto Rico. A similar situation probably exists wherever grossly elevated chromium levels are documented in marine algae and macrophytes (Table 2.8). Accidental contamination of field-collected samples is another source of elevated chromium residues that has been investigated (Martin and Knauer, 1973). They found that chromium contamination of phytoplankton samples collected under field conditions comes from metal particles in samples (up to 150.0 mg Cr/kg), rust from stainless hydrowire (up to 460.0 mg Cr/kg), and from hull paint (up to 1.0 mg/kg). Dead biomass of the brown seaweed Ecklonia sp. can reduce the toxic hexavalent chromium ion to the less-toxic trivalent chromium ion; the rate of reduction was most rapid at pH < 3.0 (Park et al., 2007).
24 Chapter 2 Table 2.8: Chromium Concentrations in Field Collections of Algae and Macrophytes Organism Algae, whole Sea of Japan, 12 spp. United Kingdom, 11 spp. Monaco, 4 spp. Soviet Union, 4 spp. Egypt; Mex Bay, Alexandria; 2 pp. Puerto Rico, 18 spp. Argentina; summer 2002; 3 sites; Porphyra columbina vs. Ulva sp.; whole,
Concentration
Reference
1.0-140.0 DW 2.8-30.0 DW 0.4-4.2 DW 6.7-13.4 DW 1.9-3.5 DW
1 2 3, 4 5 17
0.4-110.0 DW
6
0.65-0.73 DW vs. 0.84-1.14 DW
21
4.0 DW 1.1-10.0 DW 0.05-1.1 DW
7 8, 9 26
Mangrove, Avicennia marina; pneumatophores; Queensland, Australia
<1.0-4.0 DW
29
Shoalgrass, Halodule wrighti; rhizomes; Texas; Laguna Madre; 1986-1987
13.0 (5.0-149.0) DW
15
39.0 DW 9.0 DW 61.0 DW
22 22 22
0.6-14.0 DW
18
Macrophyte, Phragmites sp,; New Jersey; Hackensack River wetlands vs. reference site; AugustNovember 1991 Roots Shoots
240.0 DW vs. 65.0 DW 0.3 DW vs. 0.2 DW
16 16
Phytoplankton, whole; Narragansett Bay, Rhode Island
4.3-73.3 DW
10
Knotted wrack, Ascophyllum nodosum, whole Norway England Coast of Ireland; 1999-2000
Macroalgae; epiphytic on estuarine mangrove aerial roots; Sydney, Australia Caloglossa leprieurii Caloglossa nipae Bostrychia sp. Seaweed, Patina sp.; Guam; 1998-1999; ronds
a
(Continues)
Algae and Macrophytes 25 Table 2.8: Organism Seagrass, Posidonia oceanica Blades; Mediterranean Sea; summers 2004-2005; 3 sites Corsica, France; summer 2003; adult leaves; blades vs. sheaths
Cont’d
Concentration
Reference
0.2-1.3 DW
24
0.32 (0.15-1.1) DW vs. 0.84 (0.2-3.8) DW
27, 28
0.1-2.5 DW 0.7-7.4 DW
11 12
0.7-1.8 DW 0.7-3.7 DW; 0.14-0.68 FW
13 13
2.3-3.1 DW 31.0-44.0 DW
14 14
Macroalgae; Tunisia; 2 spp.; Mediterranean Sea coast; whole
2.2-17.0 DW
20
Salt marsh plants; Venice lagoon; June-December 2001; aerial portions; maximum concentration; Phragmites australis vs. Bolboschoenus maritimus
120.0 DW vs. 28.0 DW
26
Seaweed, Ulva lactuca; whole; India; 2004-2005
22.7 (10.5-45.7) DW
25
7.2 DW 7.4 DW 38.0 DW
19 19 19
Seaweeds, whole Japan, 44 spp. Korea, 20 spp. United Kingdom, 5 spp. May June Cordgrass, Spartina spp., whole Reference areas Areas treated with sewageamended sludge at 10,300 mg Cr/m2 over a 7-year period
Eelgrass, Zostera marina; Oregon Leaf Rhizome Root
a
Values are in mg Cr/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Gryzhankova et al., 1973; 2, Riley and Roth, 1971; 3, Fukai, 1965; 4, Fukai and Broquet, 1965; 5, Khristoforova et al., 1976; 6, Bernhard and Zattera, 1975; 7, Lande, 1977; 8, Foster, 1976; 9, Bryan and Uysal, 1978; 10, Phelps et al., 1975; 11, Ishibashi and Yamamoto, 1960; 12, Pak et al., 1977; 13, Black and Mitchell, 1952; 14, Giblin et al., 1980; 15, Custer and Mitchell, 1993; 16, Hall and Pulliam, 1995; 17, Dahab et al., 1990; 18, Denton et al., 2006; 19, Kaldy, 2006; 20, El Ati-Hellal et al., 2007; 21, Perez et al., 2007; 22, Melville and Pulkownik, 2007; 23, Bragato et al., 2006; 24, Lafabrie et al., 2007b; 25, Kamala-Kannan et al., 2008; 26, Morrison et al., 2008; 27, Lafabrie et al., 2008a; 28, Lafabrie et al., 2008b; 29, Preda and Cox, 2002.
26 Chapter 2 Chromium concentrations in blades of the seagrass, Posidonia oceanica, were positively correlated with chromium concentrations in the surrounding sediments (Lafabrie et al., 2007b). Although chromium is abundant in primary producers, there is little evidence of biomagnification through marine food chains consisting of herbivores and carnivores (Osterberg et al., 1964). In an experimental food chain consisting of phytoplankton, brine shrimp, postlarval fish, and adult fish, chromium was successfully transferred through each trophic level, with concentrations declining up the food chain (Baptist and Lewis, 1969). Based on laboratory studies, it was concluded that chromium uptake from diet was usually more efficient than uptake from seawater (Baptist and Lewis, 1969). Among sensitive species of marine algae, concentrations of 0.01 mg/L of hexavalent chromium (Cr6+) partially inhibited growth of Olisthodiscus leucas. All cultures, including those in which growth was inhibited, contained viable, active (>75%) cells at the end of 10 days. Inhibitory effects were reversed by chelators such as EDTA (Mahoney, 1982), suggesting that naturally occurring ligands and sequestering agents in seawater may alleviate the toxicity of Cr6+, and perhaps other metals. In the giant kelp, Macrocystis pyrifera, photosynthesis was inhibited 20% in 5 days at 1.0 mg/L of Cr6+, and 50% in 4 days at 5.0 mg/L (USEPA, 1980d); this kelp seems to be one of the more chromium-resistant plants. Euryhaline species of algae tested show increasing resistance to hexavalent chromium at increasing salinities (Wong and Trevors, 1988). Less than 0.05 mg Cr6+/L is proposed as safe for marine biota (USEPA, 1999).
2.13 Cobalt Cobalt concentrations in algal field collections seldom exceed 15.0 mg/kg DW, with most values notably lower (Table 2.9). The average cobalt content in 38 species of seaweeds from Japan was 0.8 mg/kg DW, with values ranging from 0.1 for Eisenia bicyclis to 4.5 mg/kg DW for S. thunbergii (Ishibashi et al., 1964c). Differences in cobalt content of Japanese seaweeds were not attributable to season of collection or habitat. Green seaweeds were comparatively high in cobalt when compared to red seaweeds. Most brown seaweeds were low in cobalt, but some species such as S. thunbergii, S. hemiphyllum, and Padina arborescens contained high cobalt residues. Seaweeds with high cobalt concentrations also contain high iron concentrations and vice versa (Ishibashi et al., 1964c), and this could account for some of the observed variation. Six species of macrophytes collected from the southwest coast of India between 1999 and 2001 had elevated concentrations in summer monsoon and hot seasons (up to 10.1 mg Co/kg DW), with little difference between species in ability to accumulate cobalt from seawater (Kalesh and Nair, 2006). Cobalt concentrations in the seagrass, P. oceanica, from the Mediterranean Sea in summers of 2004-2005 were positively correlated with cobalt concentrations in the surrounding sediments, suggesting that this species may be useful as a biomonitor for cobalt and other trace metals (Lafabrie et al., 2007b).
Algae and Macrophytes 27 Table 2.9: Cobalt Concentrations in Field Collections of Algae and Macrophytes a
Organism
Concentration
Algae, whole Sea of Japan Reds and browns, 9 spp. Greens, 3 spp. Iceland, 10 spp. Goa, India, 33 spp. Canada, Atlantic Provinces, 11 spp.
2.0-147.0 DW 2.0-31.0 DW 0.3-11.9 DW 1.3-15.2 DW 0.1-6.3 DW
1 1 2 3 4
Algae and macrophytes; whole, 10 spp.
0.1-0.4 DW
5
Argentina; summer 2004; 3 sites; Porphyra columbina vs. Ulva sp.; whole
0.38-0.55 DW vs. 0.27-0.73 DW
15
Seaweed, Ascophyllum nodosum; whole; Ireland; 1999-2000
0.11-0.92 DW
17
Fucus vesiculosus; whole; United Kingdom
4.8 (1.8-9.0) DW
Macrophytes; 6 spp.; whole; India; 1999–2001
0.8-10.1 DW
Marsh plants; whole; Texas, Harbour Island, 14 spp.
0.06-0.065 DW
7
Porphyra spp., whole
0.5-2.6 DW
2
1.7-12.1 DW
16
3.8 (1.8-7.7) DW vs. 0.2 (0.1-0.3) DW
18
0.9-2.4 DW 0.1-5.2 DW 0.006-0.075 FW 0.8 (0.1-4.5) DW
8 9 10, 11 12
0.7-1.4 DW 0.6-2.0 DW; 0.1-0.4 FW
13 13
Seagrass, Posidonia oceanica, blades Mediterranean Sea; summers 2004-2005; 3 sites Corsica, France; summer 2003; adult leaves; blades vs. sheaths Seaweeds. Whole Korea; 20 spp. Norway South Africa; 7 spp. Sea of Japan; 38 spp. Irish Sea; United Kingdom; 5 spp. May June
Reference
6 14
Values are in mg Co/kg fresh weight (FW) or dry weight (DW). a 1, Gryzhankova et al., 1973; 2, Munda, 1978; 3, Agadi et al., 1978; 4, Young and Langille, 1958; 5, Ishii et al., 1978; 6, Bryan and Uysal, 1978; 7, Lytle et al., 1973; 8, Pak et al., 1977; 9, Lunde, 1970; 10, Van As et al., 1973; 11, Van As et al., 1975; 12, Ishibashi et al., 1964c; 13, Black and Mitchell, 1952; 14, Kalesh and Nair, 2006; 15, Perez et al., 2007; 16, Lafabrie et al., 2007b; 17, Morrison et al., 2008; 18, Lafabrie et al., 2008a.
28 Chapter 2 Bioconcentration of cobalt from ambient seawater under laboratory conditions ranged from 15 (Ichikawa, 1961) to 136 (Sivalingam, 1978a); the latter value was derived from immersion for 48 h of U. reticulata in solutions containing 50.0 mg Co/L. Under field conditions, cobalt bioconcentration was variously estimated for different species at 215-1600 (Van As et al., 1973), 2000 (Ishii et al., 1978), and 990 and 9710 in algulose and barium-complexed fucoidan fractions, respectively, for Cystoseira spp. (Ryndina, 1976). Cobalt is considered an essential trace element for most organisms, including algae. Normal growth was evident in Cricosphaera carterae at concentrations less than 0.6 mg Co/L; however, higher concentrations up to 6.0 mg Co/L inhibited cell division, and still higher concentrations up to 12.0 mg Co/L drastically reduced protein synthesis (Blankenship and Wilbur, 1975). In the diatom, P. tricornutum, growth stimulation occurred at 0.08-12.5 mg Co/L, and growth inhibition at 19.6 mg Co/L (Horvatic and Persic, 2007).
2.14 Copper Large variability in copper concentrations of marine plants is due, in part, to proximity to heavily populated or industrialized areas, fraction or tissue analyzed, copper concentration of the surrounding seawater, season of collection, geographic area, interspecies variations, and age of the plant (Almeida et al., 2006; Eisler, 1981, 2000g; Kalesh and Nair, 2006; Table 2.10). Algae reared or found in high-copper environments can tolerate additional levels of copper more readily than algae from low-copper environments. It is not clear if these differences are adaptive or genetic. In one case, Ectocarpus siliculosus collected from the hulls of ocean-going freighters—that had been treated with copper-based antifouling paints— were an order of magnitude more resistant to dissolved CuCl2 over a 5-week period than were conspecifics collected from an uncontaminated rocky shore (Russell and Morris, 1970). Copper tolerance in various strains of E. siliculosus is attributed to a copper-exclusion mechanism (Hall et al., 1979). Changes in the cell membrane, possibly in combination with intracellular changes, are the most probable causes of the exclusion mechanism rather than extracellular releases of organic matter (Hall et al., 1979). Copper is readily accumulated from seawater by algae and macrophytes by factors estimated at 2060 for Enteromorpha spp. (El Ati-Hellal et al., 2007), 6000-20,000 for A. nodosum (Foster, 1976; Melhuus et al., 1978), 2000 for Sargassum (Ishii et al., 1978), 1070-27,000 for F. vesiculosus (Bryan and Hummerstone, 1973; El Ati-Hellal et al., 2007; Foster, 1976; Seeliger and Edwards, 1977), and 4700-200,000 for other species (Kim and Won, 1974; Seeliger and Edwards, 1977; Yoshimura et al., 1976). Of all marine organisms examined, algae—together with certain bivalve molluscs—have the greatest ability to accumulate copper from the surrounding environment (Eisler, 1979). Copper in sewage sludge is also readily mobilized by marine plants (Montgomery et al., 1978). Field collections of marine algae may be subjected to contamination. For example, copper contamination of
Algae and Macrophytes 29 Table 2.10: Copper Concentrations in Field Collections of Algae and Macrophytes Organism Alga, Ascophyllum nodosum, whole England: polluted bay vs. reference site Norway; polluted fjord vs. reference ite Algae and macrophytes, whole Canada; Atlantic Provinces; 11 spp. Iceland, 10 spp. Goa, India; 39 spp. Irish Sea Sea of Japan; 12 spp. Norway; west coast Spain; Rio Tinto estuary Israel; Mediterranean Sea coast; 2 spp. United Kingdom; 13 spp. Argentina; summer 2002; 3 sites; Porphyra columbina vs. Ulva sp.; whole Chile; 2003-2004; seaweeds Copper-contaminated site from copper mine wastes; 4 spp. Reference site; 8 spp. Ulva compressa; reference site vs. coppercontaminated site Mangrove, Avicennia marina Hong Kong Sediment Root Leaf Western Australia Sediment Root Leaf Shenzhen, China Sediment Root Leaf Southeast Australia Sediment Root Leaf Pneumatophore
Concentration 68.0 (46.0-96.0) DW vs. 12.0 (6.0-18.0) DW 45.0-240.0 DW vs. 5.5 (4.0-8.0) DW
Reference
a
1 1
6.0-62.0 DW 1.8-8.8 DW 3.2-80.4 DW 5.6-86.0 DW 2.0-8.0 DW Max. 170.0 DW Max. 26.0 DW 2.9-7.6 DW 25.0-210.0 DW
2 3 4, 5 6 7 8 8 9 10
1.9-6.9 DW vs. 1.7-3.8 DW
32
93.5-1609.2 DW
37
1.7-27.1 DW 4.2-6.1 DW vs. 93.5-790.6 DW
37 37
13.0 DW 13.0 DW 16.0 DW
38 38 38
16.0 DW 18.0 DW 7.3 DW
39 39 39
36.0 DW 13.0-14.0 DW 5.0-5.2 DW
40, 41 40, 41 40, 41
61.0 DW 101.0 DW 9.0 DW 6.0-12.0 DW
42 42 42 45 (Continues)
30 Chapter 2 Table 2.10: Cont’d Organism
Concentration
Reference
Green alga, Cladophora sp.; 2000-2003; Baltic Sea Gulf of Gdansk Vistula Lagoon Reference site
5.3 (1.1-11.2) DW 8.4 DW; max. 11.4 DW 5.1 DW; max. 7.2 DW
33 33 33
Chlorophyceae, whole, 14 spp.
9.2-27.7 DW
11, 12
Green alga, Enteromorpha sp.; whole; 2000-2003; Gulf of Gdansk, Baltic Sea
4.9 (1.8-11.6) DW
26
Fucus serratus Near desalinization plant outfall vs. reference site Tips May August Thallus May August
5.9 DW vs. 6.7 DW 204.0 DW vs. 4.3 DW
13 13
17.0 DW vs. 6.7 DW 104.0 DW vs. 4.7 DW
13 13
Fucus spiralis; near desalination plant outfall vs. reference site; August Tips Thallus
231.0 DW vs. 2.8 DW 231.0 DW vs. 3.8 DW
13 13
Microalgae, Haslea ostrearia Adsorbed onto cell surface Incorporated into cell; soluble vs. insoluble
0.06 DW 0.017 DW vs. 0.023 DW
47 47
India; Tamil Nadu; leaves; January 2007 Mangroves; 8 spp. Halophytes; 5 spp.
24.1 (8.1-95.1) DW 14.4 (7.8-32.2) DW
46 46
Macroalgae; Tunisia; Mediterranean Sea coast; 2 spp.; whole
1.3-8.2 DW
29
Macroalgae (6 spp.) vs. phytoplankton; Gulf of California, Mexico; 1998-1999; whole
7.5-24.6 DW vs. 30.0 DW
27
200.0 DW 34.0 DW 86.0 DW
31 31 31
Macroalgae; epiphytic on estuarine mangrove aerial roots; Sydney region, Australia Caloglossa leprieurii Caloglossa nipae Bostrychia sp.
a
(Continues)
Algae and Macrophytes 31 Table 2.10:
Cont’d
Organism
Concentration
Mangroves; Gulf of California, Mexico; 1998-1999; twigs vs. leaves Rhizophora mangle Avicennia germinans Laguncularia racemosa
3.0 DW vs. 7.4 DW 18.1 DW vs. 4.6 DW 5.0 DW vs. 2.3 DW
27 27 27
New Jersey, United States; Raritan Bay; water content 0.002 mg Cu/L vs. 0.022 mg Cu/L Blidingia minima Enteromorpha linza Fucus vesiculosus Ulva spp.
2.0 DW vs. 160.0 DW 17.0 DW vs. 77.0 DW 8.0 DW vs. 48.0 DW 14.0 DW vs. 38.0 DW
14 14 14 14
Macrophytes; 6 spp.; whole; India; 1999-2001
0.6-14.6 DW
30
Phaeophyceae, whole, 23 spp.
4.5-49.7 DW
11, 12
Brown alga, Pelvetia canaliculata; whole Norway Scotland
35.0 DW 5.0-16.0 DW
1 1
Macrophyte, Posidonia oceanica; Italy Sheath Rhizome
6.0-17.0 DW 5.4-15.3 DW
25 25
1.1-2.7 DW
35
14.0 DW 6.5 DW 3.7 DW
39 39 39
19.0 DW 1.1 DW 0.6 DW
43 43 43
Mangrove, Rhizophora mangle; Natal, Brazil; summer 2001; leaves Mangrove, Rhizophora stylosa Western Australia Sediment Root Leaf Yingluo Bay, China Sediment Root Leaf Rhodophyceae, whole, 29 spp.
2.0-13.4 DW
Saltmarsh macrophytes; 3 spp.; Yangtze River estuary, China; July 2005 Above ground portions Below ground portions
30.0 DW 100.0 DW
Reference
a
7,11,12
34 34 (Continues)
Table 2.10: Cont’d Organism
Concentration
Salt marsh plants; Venice lagoon; 2001; aerial portions Phragmites australis Bolboschoenus maritimus
Max. 14.0 DW Max. 5.0 DW
36 36
Sargassum spp., whole Japan Texas Korea
Max. 10.0 DW 4.1 (2.8-7.0) DW 5.7 (3.6-13.1) DW
15 16 17
Seaweed, Ulva lactuca; Gulf of California, Mexico; 2002; whole Summer Winter
23.0 DW 44.0 DW
28 28
Seaweeds, whole Korea, 17 spp. Korea, 20 spp. Norway United Kingdom, 5 spp.; May vs. June
0.9-17.0 DW; 0.2-4.0 FW 5.0-54.0 DW 6.0-63.0 DW 4.0-7.0 DW vs. 6.0-31.0 DW
18 19 20 21
2.9 (1.3-14.0) DW vs. 4.0 (3.8-15.0) DW
44
10.0 DW 8.3 DW 47.0 DW
24 24 24
9.0-13.0 DW vs. 5.0-6.0 DW 27.4 DW vs. 6.0-7.0 DW Max. 1350.0 DW vs. 9.0-36.0 DW
22 1 23
Eelgrass, Zostera marina Baja California, Mexico; March 2000; whole; reference site vs. salt mining site Oregon Leaf Rhizome Root Eelgrass, Zostera spp. Denmark; 1979-80; metalscontaminated site vs. reference site Leaves Roots Portugal and Spain; metals-contaminated site vs. reference site
Reference
a
Values are in mg Cu/kg fresh weight (FW) or dry weight (DW). a 1, Jenkins, 1980b; 2, Young and Langille, 1958; 3, Munda, 1978; 4, Agadi et al., 1978; 5, Zingde et al., 1976; 6, Culkin and Riley, 1958; 7, Gryzhankova et al., 1973; 8, Stenner and Nickless, 1974; 9, Roth and Hornung, 1977; 10, Riley and Roth, 1971; 11, Sivalingam, 1978b; 12, Ishibashi et al., 1962; 13, Romeril, 1977; 14, Seeliger and Edwards, 1977; 15, Ishii et al., 1978; 16, Horowitz and Presley, 1977; 17, Kim and Won, 1974; 18, Kim, 1972; 19, Pak et al., 1977; 20, Lunde, 1970; 21, Black and Mitchell, 1952; 22, Brix and Lyngby, 1982; 23, Stenner and Nickless, 1975; 24, Kaldy, 2006; 25, Baroli et al., 2001; 26, Zbikowski et al., 2006; 27, Ruelas-Inzunza and Paez-Osuna, 2006; 28, OrdunaRojas and Longoria-Espinoza, 2006; 29, El Ati-Hellal et al., 2007; 30, Kalesh and Nair, 2006; 31,Melville and Pulkownik, 2007; 32, Perez et al., 2007; 33, Zbikowski et al., 2007; 34, Quan et al., 2007; 35, Silva et al., 2006; 36, Bragato et al., 2006; 37, Andrade et al., 2006; 38, Chen et al., 2003; 39, Alongi et al., 2003; 40, Peng et al., 1997; 41, Zheng and Lin, 1996; 42, MacFarlane et al., 2003; 43, Zheng et al., 1997; 44, Marcias-Zamora et al., 2008; 45, Preda and Cox, 2002; 46, Agoramoorthy et al., 2008; 47, Amiard-Triquet et al., 2006.
Algae and Macrophytes 33 phytoplankton samples by metal particles in samples, rust from stainless and nonstainless hydrowire, hull paint, and open ocean tar balls are all documented (Martin and Knauer, 1973). Bioconcentration and biomagnification of copper occurs in the food chain of diatom (S. costatum) to clams (Donax cuneatus) to prawns (Penaeus indicus). All species accumulate copper from the medium, and clams and shrimp from the diet. Maximum concentrations after exposure to 0.2 mg Cu/L and diets for 10 days, in mg Cu/kg FW, are 2.8 in whole diatoms, 13.6 in clam soft parts, and 33.9 in whole shrimps (Rao and Govindarajan, 1992). Transfer of copper from wood treated with chromated copper arsenate (CCA) occurs in estuarine algae (Ulva sp., Enteromorpha sp.), American oysters, mud snails, and fiddler crabs (Weis and Weis, 1992). Algae from CCA-treated lumber show elevated concentrations of copper when compared to reference sites (Weis and Weis, 1992). Bioavailability of copper determined from metal speciation in diet permits an accurate prediction of trophic transfer in some cases (Amiard-Triquet et al., 2006). In the case of the microalga Haslea ostrearia, which was exposed to 0.03 mg Cu/L until exponential growth was achieved and then fed to Pacific oysters, Crassostrea gigas, for 3 weeks, only the exchangeable copper was available, that is, copper adsorbed onto cell surface and soluble copper incorporated into the cell. Copper-loaded Haslea had 0.23 mg Cu/kg DW adsorbed onto the cell surface, 0.085 mg Cu/kg DW in incorporated soluble fractions, and 0.035 mg Cu/kg DW as insoluble copper within the cell. Thus, 90% of the copper in Haslea was exchangeable and similar to the 93% stored by oysters (Amiard-Triquet et al., 2006). In the case of copperloaded diatoms, Tetraselmis suecica, only half (21% of the potentially available copper of 0.067 mg Cu/kg DW) was incorporated by oysters (Amiard-Triquet et al., 2006). Below ground portions of two species of saltmarsh plants collected from the Tagus estuary, Portugal, in March 2004 had elevated concentrations of copper when compared to aerial portions (Reboreda and Cacador, 2007). For S. maritima, copper concentrations, in mg Cu/m2 DW, were 230.1 for roots, 1.8 for stems, and 0.8 for leaves. For H. portulacoides, these values were 660.9 for roots, 3.9 for stems, and 1.8 for leaves, suggesting that Spartina is a more effective sink for copper and Halimione a more effective source (Reboreda and Cacador, 2007). Saltmarsh plants, including H. portulacoides, can increase the potential mobility of metals, especially copper, from sediments to pore water and sometimes to the water column when rhizosediments are resuspended (Almeida et al., 2008). High transfer of copper from Halimione-colonized sediments to pore waters occurs with attendant risks to biota; however, strong copper-complexing organic ligands in water and elutriates reduce metal bioavailability. In areas not colonized by Halimione, sediments remove copper and other metals to pore waters (Almeida et al., 2008). Although mangroves are a taxonomically diverse group, copper accumulation and partitioning is similar across genera and families (MacFarlane et al., 2007). Patterns of copper accumulation are also similar for salt-secreting and nonsecreting species. Copper is accumulated in roots to concentrations similar to
34 Chapter 2 adjacent sediments, and copper concentrations in leaves are usually less than half that of roots. Leaf copper concentrations decreased as environmental copper concentrations increased, suggesting regulation. A similar case is made for zinc, another essential metal (MacFarlane et al., 2007). Copper residue data in photosynthetic organisms should be interpreted with the knowledge that numerous intrinsic and extrinsic variables significantly affect copper uptake, as well as growth and survival. Thus, increasing temperatures were positively associated with copper uptake and biomass in Coccochloris elegans, D. tertiolecta, and S. costatum (Mandelli, 1969). Growth rate and copper content of T. pseudonana and Nannochloris atomus were altered independently of medium copper concentrations by varying pH (Sunda and Guillard, 1976). Chelators reduced the availability of copper to algae (Davey et al., 1973; Erickson, 1972; Erickson et al., 1970; Morris and Russell, 1974). In one instance, the presence of decomposed natural plankton and detritus decreased toxicity of copper to T. pseudonana, probably by complexation or chelation of the copper to a biologically unavailable form (Erickson, 1972). In another instance, effects of potentially inhibitory levels of cupric ion in seawater on marine algae can be reduced or eliminated depending on the degree of copper complexation by natural organic ligands (Sunda and Guillard, 1976). The anionic constituent must also be considered when evaluating algal copper kinetics, with differences observable in chloride and sulfate salts (Nielsen and Wium-Anderson, 1970). High concentrations of iron or citrate in seawater both reportedly reduced the biocidal properties of copper to algae (Nielsen and Kamp-Nielsen, 1970), presumably by complexation. In laboratory studies, thalli of two species of benthic red algae, Ceramium pedicellatum and Neogardhiella baileyi accumulated copper from media containing 0.0014, 0.0064, or 0.011 mg Cu/L by factors ranging from 4540 and 6864 (Seeliger and Edwards, 1979). Up to 22% of the copper was excreted in organic matter, but less than 10% was released in the inorganic form. Dead algae released 80-90% of the copper in organic fractions, both dissolved and particulate. Copper was thus present to a large extent in both dissolved and detrital fractions, components which are readily consumed by marine heterotrophs, and only to a small extent in dissolved inorganic form (Seeliger and Edwards, 1979). Copper tolerance of the diatom N. closterium was measured after copper acclimatization to 0.005 or 0.025 mg Cu/L for 100 days; there were no significant changes over a 72-h period in growth rate or tolerance to zinc or copper when compared to nonacclimatized algae (Johnson et al., 2007). Seagrass (Heterozostera tasmanica) held in seawater containing 0.042 mg Cu/L for several weeks had 2700.0 mg Cu/kg DW; sea grasses in media containing 0.0003 mg Cu/L had 2.5 mg Cu/kg DW, and intermediate values are reported for 0.01 mg Cu/L (306.0-564.0 mg/kg DW) and 0.02 mg Cu/L (1280.0 mg Cu/kg DW; Ahsanullah and Williams, 1991). Brown alga, Sargassum linearifolium, experimentally contaminated in the laboratory with 0.3 mg Cu/L for 24 h and transferred to the field, had greatly reduced colonial epifauna taxa (Roberts et al., 2006).
Algae and Macrophytes 35 Ionic copper (Cu2+) is phytotoxic. Copper was the most toxic metal tested to five species of fucoid algae, followed by ionic mercury, zinc, lead, and cadmium, in that order (Stromgren, 1980). The biocidal properties of copper were evident among complex metal mixtures. In one study using the diatom Thalassiosira aestivalis, effects of a mixture of 10 metals (copper, zinc, nickel, chromium, lead, cadmium, mercury, arsenic, selenium, and antimony) were investigated at metals concentrations expected to occur in a moderately polluted estuary. Diatom growth was not inhibited under laboratory conditions. But growth was inhibited when all metals concentrations were increased by a factor of 5 or 10. Growth inhibition was due solely to copper with normal growth evident when copper was deleted from the mixture (Thomas et al., 1980). In another study, three species of algae were grown in situ in Norwegian fjords contaminated to various degrees with copper and other metals in solution including cadmium, zinc, lead, and mercury. In every case, growth was significantly reduced and metals uptake increased in the most heavily contaminated fjord when compared to a less-polluted fjord, and especially to reference sites (Eide and Jensen, 1979). It is probable that copper was the primary agent responsible for the observed deleterious effects. Copper toxicity in a diatom, Thalassiosira weissflogii, is predictable, in part, by the intracellular copper and its subcellular distribution as compared with the currently used free Cu2+ ion activity model (Miao and Wang, 2007). Antifouling paints containing mixtures of zinc pyrithione and copper (as a replacement for tributyltin, TBT) were more than additive in toxicity during 96-h survival tests than either alone, and this should be considered in developing copper and zinc water quality criteria (Bao et al., 2008). Increased production of phytochelatins in the diatom P. tricornutum is a useful indicator of free copper in the medium, suggesting that phytochelatins can serve as biomarkers of exposure to the bioavailable copper fraction (Morelli and Fantozzi, 2008). A linear doseresponse relation between metal exposure—including cadmium, lead, and especially copper—and phytochelatin synthesis was found in seawater enriched with known amounts of metal (Morelli and Fantozzi, 2008). Copper sensitivity of 13 species of marine microalgae—as judged by 50% inhibition of growth rate in 72 h—ranged from 0.0006 mg Cu/L for Minutocellus polymorphus, a centric diatom, to 0.53 mg/L for D. tertiolecta, a green algae; values for most other species tested were less than 0.015 mg Cu/L (Levy et al., 2007). Interspecies sensitivity to copper was attributed to differences in uptake rates across the plasma membrane, differences in internal binding mechanisms, and variability in detoxification mechanisms between species (Levy et al., 2007). However, use of internal copper concentrations and net uptake rates alone cannot satisfactorily account for differences in species sensitivity to copper, suggesting that cellular detoxification mechanisms merit additional research (Levy et al., 2008). Considerable variability in sensitivity to copper was documented among algal species. For example, exposure of algae to very low sublethal concentrations of copper (0.00003 mg/L) increases their sensitivity toward additional copper challenge and to cadmium salts (Visviki
36 Chapter 2 and Rachlin, 1994a). Adverse effects on growth, survival, and development were documented for sensitive species of algae at nominal copper concentrations of 0.005-0.01 mg Cu/L (Davey, 1976; Jensen et al., 1976; Saifullah, 1978; Saward et al., 1975; USEPA, 1980a), and at 0.011-0.05 mg/L (Braek et al., 1976; Gnassi-Barelli et al., 1978; Havens, 1994; Hopkins and Kain, 1971; Pace et al., 1977; Sunda and Guillard, 1976; Visviki and Rachlin, 1994a). Growth inhibition (50% in 96 h) is reported for Chlorella pyrenoidosa at 0.51 (0.39-0.63) mg Cu/L (Wang et al., 2007). Among resistant species, adverse effects were evident at comparatively high nominal copper concentrations of greater than 0.1-100.0 mg Cu/L (as quoted in Abalde et al., 1995; Coppellotti, 1989; Eisler, 1981; Visviki and Rachlin, 1994b). Minor effects on lipid metabolism of Dunaliella salina was reported at 0.000031 mg Cu/L after exposure for 8 months (Visviki and Rachlin, 1994a), but this requires verification. A proposed criterion to protect algal life is less than 0.0031 mg Cu/L (El Ati-Hellal et al., 2007).
2.15 Gallium Gallium concentrations in algae and seaweeds ranged from 0.01 to 0.64 mg/kg DW, and up to 20.0 on an ash weight (AW) basis (Table 2.11). The role of gallium in plant physiology is imperfectly understood.
Table 2.11: Gallium, Germanium, and Gold Concentrations in Field Collections of Algae and Macrophytes Element and Organism
Concentration
Reference
a
Gallium Algae, whole, Irish Sea
0.01 DW
1
Diatoms, whole, Black Sea
20.0 AW
2
Seaweeds, whole, Japan, 30 spp.
0.14 (0.02-0.64) DW
3
0.003-0.032 FW
4
0.015-0.093 AW 0.021-0.035 DW
5 6
Germanium Sargassum sp., whole, Gulf of Mexico Gold Seaweeds, whole, Japan Ulva sp. Ulva sp. and Porphyra sp.
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Culkin and Riley, 1958; 2, Vinogradova and Koual’skiy, 1962; 3, Yamamoto et al., 1976; 4, Johnson and Braman, 1975; 5, Fukai and Meinke, 1959; 6, Fukai and Meinke, 1962.
Algae and Macrophytes 37
2.16 Germanium Germanium concentrations in Sargassum collected from the Gulf of Mexico ranged from 0.003 to 0.032 mg/kg FW (Table 2.11). Marine diatoms under laboratory conditions were more sensitive to germanium salts than were other groups of phytoplanktons (Azam et al., 1973; Lewin, 1966; Thomas and Dodson, 1974). In one study, four species of diatoms accumulated radiogermanium from their growth media and incorporated up to 80% into the silica of cell walls (Azam et al., 1973). Uptake and incorporation of germanic acid was dependent upon the Ge/Si ratio; at a ratio of 0.01, no inhibition of growth or silicic acid uptake was observed (Lewin, 1966). At a Ge/Si ratio of 0.1, growth and silicic acid uptake in diatoms was reduced by 95%. Lewin (1966) concluded that high levels of germanium interfered with silicate utilization by diatoms. Thomas and Dodson (1974) demonstrated that 0.5 and 1.0 mg Ge/L as Ge(OH)4 interfered with diatom photosynthesis, with degree of inhibition proportional to Si(OH)4 concentrations in the medium; however, at 5.0 and 10.0 mg Ge/L, inhibition was independent of Si(OH)4 concentration.
2.17 Gold Unlike certain species of terrestrial plants that routinely accumulate gold to concentrations greater than 0.1 mg Au/kg DW (Eisler, 2004), maximum values recorded in seaweeds from Japan were 0.035 mg/kg on a DW basis and 0.093 mg/kg on an AW basis (Table 2.11). Gold is not an essential element for living organisms (Brown and Smith, 1980). Trivalent gold is considered the most toxic gold species tested. Trivalent gold as tetrachloroaurate (AuCl4) depressed chlorophyll concentrations, photosynthetic rates, and thiol levels at concentrations greater than 0.0985 mg Au3+/L over a 21-day period in Amphora coffeaeformis, a marine diatom (Robinson et al., 1997). Cells were able to recover at concentrations <0.985 mg Au3+/L due to cellular and photoreduction of AuCl4. Adverse effects were exacerbated by Cu2+. Uptake of Au3+ by Amphora is not an energy-dependent process. At 0.394-0.985 mg Au3+/L, only 30% of the total gold uptake after 24 h was internal. Robinson et al. (1997) concluded that algal cells, alive or dead, rapidly accumulate Au3+ and start to reduce it within 2 days to elemental gold (Auo) and monovalent gold (Au+). Gold can be sequestered from acid solutions by dead biomass of the brown alga Sargassum natans and deposited in its elemental form (Kuyucak and Volesky, 1989). The cell wall of Sargassum was the major site for gold deposition, with carbonyl groups (C ¼ O) playing a major role in binding, and N-containing groups a lesser role. Like activated carbon, the biomass of S. natans is extremely porous and this accounts, in part, for its ability to accumulate gold (Kuyucak and Volesky, 1989). Ground-dried seaweeds representing species of Sargassum, Gracilaria, Eisenia, and Ulva, accumulated gold from solution (Zhao et al., 1994). Seaweeds can remove 75-90% of gold within 60 min at pH 2 from solutions containing 5.0 mg Au3+/L.
38 Chapter 2
2.18 Iron Open ocean marine diatoms are bioindicators of available iron originating from atmospheric dust. Depending on the physicochemical characteristics of the dust, phytoplankton growth is stimulated (Visser et al., 2003). In the laboratory, Arctic diatoms (Actinocyclus sp., Thalassiosira sp.) were exposed to road dust containing FeCl3. Diatom growth was positively correlated with dissolution rate of iron in seawater and concentration of amorphous iron in dust (Visser et al., 2003). Iron concentrations in marine algae and macrophytes are elevated (Table 2.12) when compared to other trace elements; substantial variability in iron content was evident, even among closely related species. The high iron content is probably due to several factors. First, is the established need of iron by marine plants for normal growth (Davies, 1970; Goldberg, 1952; Lewin and Chen, 1971; Smith, 1970). Davies (1970) studied the growth of D. tertiolecta under iron-limiting conditions and concluded that cells maintained in culture under iron-deficient conditions gradually adapt to that situation. Moreover, growth rate of Table 2.12: Iron Concentrations in Field Collections of Algae and Macrophytes Organism
Concentration
Reference
Algae and macrophytes; whole Admiralty Bay, Antarctica; January 2004; 3 spp. Irish Sea Japan; 11 spp. Japan; 44 spp. Sea of Japan; 12 spp. Goa, India; 33 spp.
91.0-4450.0 DW
30
34.0-4680.0 DW 25.0-590.0 DW 74.0-3410.0 DW 82.0-886.0 DW 130.0-1796.0 DW
1 2 4 5 6
Argentina; summer 2002; 3 sites; Porphyra columbina vs. Ulva sp.; whole
213.0-440.0 DW vs. 201.0-532.0 DW
Brown alga, Ascophyllum nodosum; whole Trondheimsfjord, Norway United Kingdom Menai Straits Dulas Bay Mangrove, Avicennia marina; Queensland, Australia; pneumatophores
34
52.0-291.0 DW
7
86.0 DW 30.0 DW
8 8
184.0-4687.0 DW
a
37
Alga, Chaetomorpha brychagona; whole Near iron-ore tailings Reference site
7624.0-10,346.0 DW 114.0 DW
9 9
Chlorophyceae; whole; 5 spp.
4735.0-13,816.0 DW
10 (Continues)
Algae and Macrophytes 39 Table 2.12:
Cont’d
Organism
Concentration
Reference
Alga, Enteromorpha cunita; whole Near iron-ore tailings Reference site
2491.0-6772.0 DW 143.0 DW
9 9
140.0 DW
7
Fucus vesiculosus Whole; Norway Whole; United Kingdom Coastal waters Menai Straits Dulas Bay Tamar estuary Thallus
249.0 DW 218.0 DW 75.0 DW 808.0 (401.0-1300.0) DW 506.0-1920.0 DW
11 8 8 12 13
Halimeda spp., whole
24.0-27.6 DW
14, 15
Hizakia fusiforme; whole; varying lengths up to 10 cm 10-20 cm 20-30 cm
91.0 DW 82.0 DW 72.0 DW
India; Tamil Nadu; leaves; January 2007 Mangroves; 8 spp. Halophytes; 5 spp.
193.6 (103.8-293.0) DW 418.6 (311.2-977.3) DW
38 38
Mangroves; Gulf of California, Mexico; 998-1999; twigs vs. leaves Rhizophora mangle Avicennia germinans Laguncularia racemosa
41.0 DW vs. 115.0 DW 77.0 DW vs. 171.0 DW 28.8 DW vs. 97.0 DW
31 31 31
Marsh plants; whole; 14 spp.
47.0-200.0 DW
16
Macroalgae (6 spp.) vs. phytoplankton; Gulf of California, Mexico; 1998-1999; whole
318.0-2131.0 DW vs. 889.0 DW
31
Macroalgae; epiphytic on estuarine mangrove aerial roots; Sydney region, Australia Caloglossa leprieurii Caloglossa nipae Bostrychia sp.
23,000.0 DW 3100.0 DW 18,000.0 DW
33 33 33
Padina australis, whole
Max. 504.0 DW
17
Padina gymnospora, whole
Max. 4100.0 DW
18
Phaeophyceae, whole, 4 spp.
348.0-15,743.0 DW
10
a
2 2 2
(Continues)
40 Chapter 2 Table 2.12: Cont’d Organism Phytoplankton Whole Organic fractions No titanium group Titanium group Strontium-concentrated group Siliceous frustules No titanium group Titanium group Strontium-concentrated group
Concentration
Reference
624.0 (280.0-1290.0) DW
19
224.0 DW 1510.0 DW 231.0 DW
20 20 20
220.0 DW 560.0 DW 180.0-500.0 DW
20 20 20
0.5-4.8 DW 0.09-0.1 DW
29 29
Spain; Mediterranean Sea; leaves; 2001-2003
72.7 (31.1-167.7) DW
36
Mangrove, Rhizophora mangle; summer 2001; Natal, Brazil; leaves
76.7-120.0 DW
35
Rhodophyceae, whole, 9 spp.
486.0-2301.0 DW
10
Sargassum fulvellum, whole
130.0-265.0 DW; 1137.0-1950.0 AW
21
Macrophyte, Posidonia oceanica Italy Sheath Rhizome
Sargassum horneri Whole Whole; varying lengths up to 50 cm 50-100 cm 100-150 cm Lamina Air bladder Stipe Receptacle Seaweeds, whole South Africa; 11 spp. Coast of Japan; 38 spp. Norway Japan; 30 spp. Korea; 20 spp. May vs. June; 5 spp.
98.0 DW
2
137.0 DW 80.0 DW 58.8 DW 335.0 DW 61.0 DW 41.0 DW 18.0 DW
2 2 2 2 2 2 2
3.3-230.0 FW 52.0-3296.0 DW 33.0-931.0 DW 501.0 DW (47.0-3310.0) DW 148.0-2343.0 DW Max. 638.0 DW vs. Max. 3380.0 DW
a
22, 23 21 24 25 26 27 (Continues)
Algae and Macrophytes 41 Table 2.12:
Cont’d
Organism
Concentration
Reference
Spartina alterniflora Sprout Mature plant Dead plant Leaves and stalks
700.0-4800.0 DW 320.0-2600.0 DW 2250.0-10,500.0 DW 750.0 DW
Seaweed, Ulva lactuca; Gulf of California, Mexico; 2002; whole August Rest of year
3652.0 DW 500.0-1500.0 DW
32 32
Eelgrass, Zostera marina; Oregon Leaf Rhizome Root
2422.0 DW 1584.0 DW 11,933.0 DW
28 28 28
a
3 3 3 3
Values are in mg Fe/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Culkin and Riley, 1958; 2, Ishii et al., 1978; 3, Williams and Murdock, 1969; 4, Ishibashi and Yamamoto, 1960; 5, Gryzhankova et al., 1973; 6, Agadi et al., 1978; 7, Lande, 1977; 8, Foster, 1976; 9, Wong et al., 1979; 10, Sivalingam, 1978b; 11, Preston et al., 1972; 12, Bryan and Uysal, 1978; 13, Bryan and Hummerstone, 1973; 14, Bohn, 1979; 15, Khristoforova and Bogdanova, 1980; 16, Lytle et al., 1973; 17, Pillai, 1956; 18, Stevenson and Ufret, 1966; 19, Horowitz and Presley, 1977; 20, Martin and Knauer, 1973; 21, Ishibashi et al., 1964a; 22, Van As et al., 1973; 23, Van As et al., 1975; 24, Lunde, 1970; 25, Yamamoto et al., 1976; 26, Pak et al., 1977; 27, Black and Mitchell, 1952; 28, Kaldy, 2006; 29, Baroli et al., 2001; 30, Santos et al., 2006; 31, Ruelas-Inzunza and Paez-Osuna, 2006; 32, Orduna-Rojas and Longoria-Espinoza, 2006; 33, Melville and Pulkownik, 2007; 34, Perez et al., 2007; 35, Silva et al., 2006; 36, Fourqurean et al., 2007; 37, Preda and Cox, 2002; 38, Agoramoorthy et al., 2008.
cells may be expressed mathematically in terms of the metabolic iron content of the cells, and that chlorophyll production by phytoplankton may be governed by the supply of organoiron complexes. Second, is the ability of most algal species to bioconcentrate iron from the surrounding environment. Typical concentration factors ranged from 810,000 for thallus of F. vesiculosus (Bryan and Hummerstone, 1973) to a low of 100-300 for Ceramium and Enteromorpha (Taylor and Odum, 1960); intermediate values for various species were also documented (Ichikawa, 1961; Ishii et al., 1978; Ryndina, 1976; Van As et al., 1973; Young, 1975; Yoshimura et al., 1976). Davies (1967) reports that iron is present in a particulate form, probably as hydrous ferric oxide, which can scavenge isotopes of other elements. The ability of a diatom P. tricornutum to adsorb iron from the medium at high ambient iron levels was documented (Davies, 1967). Third, is the possibility of accidental contamination of samples during collection. Martin and Knauer (1973) observed that iron contamination associated with field samples of phytoplankton included metal particles in samples, rust form stainless hydrowire, hull paint, and open ocean tar balls. Fourth, and most likely, iron contamination as a result of industrial and other anthropogenic activities may account for a significant amount of the variability observed in Table 2.12, especially among
42 Chapter 2 estuarine species. For example, the highest iron (and manganese) concentrations in salt marsh plants grown on contaminated soils occurred under acid-reducing conditions, and this is in accord with effects of reducing conditions on chemical speciation of iron and manganese and their bioavailability (Gambrell et al., 1977). In another study, thalli of marine algae from intertidal environments, especially P. elegans and Cladophora rupestris, retained about 29% of their FW as iron after shaking for 6 h in solutions containing 5000.0 mg iron ore dust/L. On this basis, Boney (1978) concluded that marine algae have potential as bioindicators of ore dust loading of seawater due to accidental spillage at ore unloading terminals. Bryan and Hummerstone (1973) state that other factors should be considered when interpreting the significance of iron loadings in marine plants, such as seasonal changes, location of the plant in the intertidal zone, age of the plant, and portion analyzed. Ishibashi et al. (1964b) showed that iron content in 38 species of dried seaweeds from Japan ranged from a low of 52.0 mg/kg in Sargassum gigantifoleum to 3296.0 mg/kg Caulerpa okamurai; however, these differences were not attributable to season or habitat. Green seaweeds usually contained the highest iron concentrations and red seaweeds the lowest; however in almost every case, high iron content was positively associated with high cobalt content, and low iron content with low cobalt loadings (Ishibashi et al., 1964b), suggesting a possible complexation mechanism.
2.19 Lead Lead is not essential for photosynthetic organisms, and excessive amounts cause growth inhibition as well as a reduction in mitosis, photosynthesis, and water absorption (Demayo et al., 1982). Mangroves as a group tend to operate as excluder species for nonessential metals and as regulators of essential metals. Unlike essential metals, such as copper and zinc, the nonessential lead is excluded from leaf tissues regardless of environmental concentrations (MacFarlane et al., 2007; Table 2.13). Many factors can modify lead concentrations in field-collected algae, including geographic location, proximity to anthropogenic lead sources, water lead concentrations, association with strontium and titanium, and season of collection (Eisler, 1981; Table 2.13). In addition, low pH and high phosphate levels of the surrounding medium may inhibit lead uptake in Ulva lactuca (Shiber and Washburn, 1978). Differences in concentrations of lead—as well as copper, iron, manganese, and zinc—among Caulerpaceae seaweeds from shallows of coral islands in the southwestern Pacific Ocean were associated with differences in naturally occurring geochemical properties of island waters (Khristoforova and Bogdanova, 1980). Lead concentrations in field-collected phytoplankton samples may be contaminated by sampling devices. Contamination from sampling is estimated to approach 1500.0 mg Pb/kg from metal particles, 660.0 mg/kg stainless hydrowire, and 485.0 mg/kg from hull paint (Martin and Knauer, 1973). In addition, tetramethyllead (TML) was 4-10 times more effective than tetraethyllead (TEL) salts in producing deleterious effects in Dunaliella spp. (Marchetti, 1978), and this is presumably reflected in lead-uptake kinetics.
Algae and Macrophytes 43 Table 2.13: Lead Concentrations in Field Collections of Algae and Macrophytes Organism Algae, whole India, Goa; 33 spp. Norway; west coast Spain; Rio Tinto estuary United Kingdom; 11 spp. Argentina; summer 2002; 3 sites; Porphyra columbina vs. Ulva sp.; whole Brown alga, Ascophyllum nodosum; whole Norway Eikhamrane Flak Transferred from Eikhamrane to Flak for 120 days Sorfjorden Hardangerfjord United Kingdom Menai Straits Dulas Bay Irish coast; 1999-2000
Concentration usually 6.1-28.3 DW; max. 197.5 DW Max. 1200.0 DW Max. 22.0 DW 8.1-56.6 DW <0.5 DW vs. 0.8-1.7 DW
Reference
a
1 2 2 3 23
11.0-54.0 DW <3.0 DW <3.0-5.0 DW
4 4 4
10.4-85.0 DW <3.0-95.0 DW
5 6
2.3 DW 2.2 DW 0.12-2.1 DW
7 7 34
31.0-34.0 DW 3.4-3.5 DW 1.8-1.9 DW
28, 29 28, 29 28, 29
Mangrove, Avicennia marina Shenzhen, China Sediment Root Leaf Hong Kong Sediment Root Leaf Southeast Australia Sediment Root Leaf
33.0 DW 15.0 DW 8.0 DW
30 30 30
100.0 DW 164.0 DW 5.0 DW
31 31 31
Alga, Blidingia minima; whole; Raritan Bay, New Jersey, United States; water lead content of 0.002 mg Pb/L or 0.01 mg Pb/L 0.002 mg/L 0.01 mg/L
12.0 DW 172.0 DW
8 8 (Continues)
44 Chapter 2 Table 2.13: Cont’d Organism
Concentration
Chesapeake, Bay; submerged aquatic vegetation; 5 spp.; 1989-1981; whole
7.4 (0.5-30.0) DW
18
Green alga, Cladophora sp.; Baltic Sea; 2000-2003 Gulf of Gdansk Vistula Lagoon Reference site
5.1 (1.8-13.2) DW 8.4 DW; max. 11.4 DW 4.3 DW; max. 6.2 DW
24 24 24
Alga, Enteromorpha linza; whole; Raritan Bay; water lead content of 0.002 or 0.01 mg Pb/L 0.002 mg/L 0.01 mg/L
18.0 DW 68.0 DW
8 8
Chlorophyceae, whole, 5 spp.
13.0-58.0 DW
9
Green alga, Enteromorpha sp.; whole; 2000-2003; Gulf of Gdansk, Baltic Sea
3.8 (0.9-10.4) DW
20
8.5 DW 2.3 DW 3.2 DW 4.0 DW 26.5 (5.9-109.0) DW 27.5-163.3 DW
10 7 7 11 12 5
Alga, Fucus vesiculosus; whole United Kingdom Severn estuary Dulas Bay Menai Straits Irish Sea Tamar estuary Norway, Sorfjorden United States, Raritan Bay; water content of 0.002 or 0.01 mg Pb/L 0.002 mg/L 0.01 mg/L India; Tamil Nadu; leaves; January 2007 Mangroves; 8 spp. Halophytes; 5 spp.
8.0 DW 38.0 DW
Reference
a
8 8
16.7 (2.2-27.3) DW 12.6 (10.6-17.0) DW
39 39
Macroalgae; whole; 4 spp.; Strait of Magellan, Chile; 2000-2001
<0.5-11.2 DW
36
Macroalgae (6 spp.) vs. phytoplankton; Gulf of California, Mexico; 1998-1999; whole
0.29-3.1 DW vs. 23.0 DW
21
(Continues)
Algae and Macrophytes 45 Table 2.13:
Cont’d
Organism
Concentration
Macroalgae; epiphytic on estuarine mangrove aerial roots; Sydney region, Australia Caloglossa leprieurii Caloglossa nipae Bostrychia sp.
257.0 DW 61.0 DW 264.0 DW
25 25 25
Mangroves; Gulf of California, Mexico; 1998-1999; twigs vs. leaves Rhizophora mangle Avicennia germinans Laguncularia racemosa
0.9 DW vs. 2.1 DW 0.4 DW vs. 2.2 DW 0.4 DW vs. 0.94 DW
21 21 21
0.83-4.2 DW
13
2.3 DW
37
Marsh plants, whole, 4 spp.; Texas, United States
Reference
Mexico; Gulf of California; 1999-2000 Microalgae, Coscinodiscus centralis; whole Macroalgae; Gracilaria sp. vs. Polysiphonia sp.; whole Mangroves; 3 spp.; leaves
4.9 DW vs. 3.1 DW
37
0.9-2.2 DW
37
Phaeophyceae, whole, 4 spp.
5.2-49.7 DW
9
Macrophyte, Posidonia oceanica Blade; Mediterranean Sea; summers 2004-2005; 3 sites Italy Sheath Rhizome Corsica, France; summer 2003; adult leaves; blades vs. sheaths
1.4-1.8 DW
27
5.2-11.2 DW 0.8-2.4 DW 2.2 (1.3-3.4) DW vs. 0.3 (0.2-0.5) DW
19 19 35
Mangrove, Rhizophora stylosa; Yingluo Bay, China Sediment Root Leaf
10.0 DW 0.9 DW 0.8 DW
32 32 32
Rhodophyceae, whole, 8 spp.
1.7-44.8 DW
Saltmarsh macrophytes; 3 spp.; July 2005; Yangtze River estuary, China Above ground portions Below ground portions
14.0 DW 28.0 DW
a
9
26 26 (Continues)
46 Chapter 2 Table 2.13: Cont’d Organism
Concentration
Seaweeds, whole Korea, 17 spp. Korea, 20 spp. May vs. June, 5 spp.
0.2-1.3 DW; 0.05-0.3 FW 1.7-82.0 DW 2.0-10.0 DW vs. 4.0-13.0 DW
14 15 16
Seaweed, Ulva lactuca Gulf of California, Mexico; 2002; whole August (low) February (high) India; whole; 2004-2005
94.0 DW 259.0 DW 11.6 (5.9-20.3) DW
22 22 33
1.0-2.0 DW
17
Ulva spp., whole Puget Sound, Washington, United States Raritan Bay, New Jersey Water content 0.002 mg Pb/L Water content 0.01 mg Pb/L Eelgrass, Zostera marina; whole; Baja California, Mexico; March 2000; reference site vs. salt mining site
20.0 DW 76.0 DW 14.9 (2.6-46.0) DW vs. 8.8 (4.5–18.8) DW
Reference
a
8 8 38
Values are in mg Pb/kg dry weight (DW) or fresh weight (FW). a 1, Agadi et al., 1978; 2, Stenner and Nickless, 1974; 3, Riley and Roth, 1971; 4, Myklestad et al., 1978; 5, Melhuus et al., 1978; 6, Haug et al., 1974; 7, Foster, 1976; 8, Seeliger and Edwards, 1977; 9, Sivalingam, 1978b; 10, Butterworth et al., 1972; 11, Preston et al., 1972; 12, Bryan and Uysal, 1978; 13, Lytle et al., 1973; 14, Kim, 1972; 15, Pak et al., 1977; 16, Black and Mitchell, 1952; 17, Schell and Nevissi, 1977; 18, Di Giulio and Scanlon, 1985; 19, Baroli et al., 2001; 20, Zbikowski et al., 2006; 21, Ruelas-Inzunza and Paez-Osuna, 2006; 22, Orduna-Rojas and Longoria-Espinoza, 2006; 23, Perez et al., 2007; 24, Zbikowski et al., 2007; 25, Melville and Pulkownik, 2007; 26, Quan et al., 2007; 27, Lafabrie et al., 2007b; 28, Tam et al., 1995; 29, Zheng and Lin, 1996; 30, Chen et al., 2003; 31, MacFarlane et al., 2003; 32, Zheng et al., 1997; 33, Kamala-Kannan et al., 2008; 34, Morrison et al., 2008; 35, Lafabrie et al., 2008a; 36, Astorga-Espana et al., 2008; 37, Ruelas-Inzunza and Paez-Osuna, 2008; 38, Marcias-Zamora et al., 2008; 39, Agoramoorthy et al., 2008.
High bioconcentration factors (BCFs) for lead from ambient seawater by marine plants is documented by several investigators. BCFs ranged from 13,000 to 82,000 for algae from Raritan Bay, New Jersey (Seeliger and Edwards, 1977), and from 1200 to 26,000 for algae from Sorfjorden, Norway (Melhuus et al., 1978). Under laboratory conditions, U. reticulata held in seawater for 48 h containing 50.0 mg Pb/L had a BCF of 124 (Sivalingam, 1978b). The ability of mangrove Rhizophora mangle and the macrophyte Thallassium testinudum to accumulate lead from sewage sludge is reported by Montgomery et al. (1978). After exposure for 120 days, mangrove roots contained up to 5.0 mg/kg more lead than controls; for Thallassium this value was 80.0 mg/kg.
Algae and Macrophytes 47 Saltmarsh plants contribute significantly to lead budgets in estuaries (Reboreda and Cacador, 2007). Below ground portions of two species of saltmarsh plants collected from the Tagus estuary, Portugal, in March 2004 had elevated concentrations of lead when compared to aerial portions. Values for S. maritima, in mg Pb/m2 DW, were 670.0 in roots, 7.9 in stems, and 3.0 in leaves. For H. portulacoides, these values were 1147.1 in roots, 22.5 in stems, and 7.7 in leaves (Reboreda and Cacador, 2007). Differential sensitivity of algal species to lead is well documented. Growth rate and biomass of the comparatively sensitive S. costatum were inhibited by dissolved lead concentrations between 0.00005 and 0.01 mg/L (Rivkin, 1979; USEPA, 1985b). Growth enhancement was observed among five species of intertidal algae at concentrations between 0.045 and 0.81 mg Pb/L (Stromgren, 1980); higher lead concentrations were associated with growth inhibition over a 10-day period in Pelvetia canaliculatum, three species of Fucus, and A. nodosum. At 0.1-1.0 mg Pb/L, photosynthesis and respiration were significantly reduced in several species (Woolery and Lewin, 1976; Zavodnik, 1977). In another study, D. salina was relatively unaffected at 0.3 mg Pb/L, but showed reduced growth and other adverse effects at 0.9 mg Pb/L and higher (Pace et al., 1977). In the range 0.25-2.0 mg Pb/L, growth was inhibited in 18 species of unicellular algae (Berland et al., 1976) and in D. tertiolecta (Stewart, 1977a). At 0.5 mg Pb/L, Tiffaniella snyderae showed reduced growth and reduced cell division rate over 28 days, and at 10.0 mg Pb/L slower growth occurred for Platythamnion and Plenosporium (Stewart, 1977b). At more than 10.0 mg Pb/L, kelp M. pyrifera showed 50% inhibition of photosynthesis in 4 days (Clendenning and North, 1959). However, algal cultures of Phaeodactylum, Tetraselmis, Cricosphaera, and Dunaliella all grew well at <20.0 mg Pb/L with adverse effects at higher concentrations (Bentley-Mowat and Reid, 1977). At 25.0100.0 mg Pb/L, reduced oxygen uptake was measured in three species of unicellular algae (Mills and Colwell, 1977), and at 100.0 mg Pb/L S. alterniflora seedlings failed to grow with most dying within 8 weeks (Dunstan et al., 1975). Organolead compounds were more toxic to P. tricornutum than were inorganic lead compounds, and organoethylleads were more toxic than organomethylleads (Maddock and Taylor, 1980). Concentrations of various lead compounds causing 50% mortality in 96 h were greater than 5.0 mg/L for inorganic lead, 1.3 mg/L for TML, 0.8 mg/L for trimethyllead, and 0.1 mg/L for both triethyllead and TEL (Maddock and Taylor, 1980). A similar pattern held for growth inhibition of D. tertiolecta: 50% inhibition in 96 h at 0.15 mg TEL/L versus 1.65 mg TML/L (USEPA, 1985b). Studies on lead uptake and retention in P. tricornutum and Platymonas subcordiformes showed that both species accumulated lead from the medium at ambient concentrations of 0.02 mg Pb/L and higher (Schulz-Baldes and Lewin, 1976). In the first phase, usually completed within minutes after lead addition, cells of Phaeodactylum became saturated when the lead burden reached a remarkable 11,640.0 mg/kg DW. In the second phase, the lead content of Platymonas continued to rise slowly, whereas that of Phaeodactylum declined after 2-3 days. The addition of chelating agents, such as EDTA, inhibited lead uptake by
48 Chapter 2 Phaeodactylum. In both species, the content of bound lead increased with increasing exposure time, suggesting that during prolonged exposure to lead solutions the metal ions are first adsorbed to the cell surface and then translocated to within the cell wall, to the plasma membrane, and eventually to the cytoplasm.
2.20 Lithium Available data indicate that lithium concentrations in plant tissues ranged from 4.0 to 8.0 mg Li/kg DW (Table 2.14). Diminished rhizoid development was observed in eggs of Fucus evanescens subsequent to rearing in 500.0 mg Li/L as LiI or LiCl (Nakazawa, 1977).
2.21 Manganese Early interest in manganese was stimulated by the observation that 54Mn, a common fallout product from early nuclear tests, was preferentially accumulated by marine algae over other radioisotopes examined (Slowey et al., 1965). Stable manganese is also readily accumulated by algae from seawater. Manganese BCFs of 3900 are reported for A. nodosum (Foster, 1976), 4600-26,000 for F. vesiculosus (Foster, 1976), 10,000-200,000 for Laminaria japonica (Yoshimura et al., 1976), and 9000 for Sargassum spp. (Ishii et al., 1978). Similar concentration factors are for other algal species (Ichikawa, 1961; Ryndina, 1976; Van As et al., 1973). Manganese is an essential element for normal growth of D. tertiolecta, and probably other species, and adverse effects occur in Dunaliella when manganese concentrations in the growth medium were less than 0.1 mg Mn/L (Noro, 1978). Manganese concentrations in field collections of marine algae collected worldwide ranged from 3.8 to 3421.0 Mn/kg DW (Table 2.15). The high variability between and among species are attributed to a variety of biotic and extrinsic modifiers, including accidental contamination during the sampling process (Martin and Knauer, 1973), season of collection (Bryan and Hummerstone, 1973; Pillai, 1956), plant part analyzed (Bryan and Hummerstone, 1973; Khristoforova et al., 1976), tidal fluctuations (Sanders, 1978), Table 2.14: Lithium Concentrations in Field Collections of Algae and Macrophytes Organism
Concentration
Algae, whole, 3 spp.
4.0-6.0 DW
1
Diatoms, whole
150.0 AW
2
Laminaria cloustini; frond; sterile vs. sporing
6.0 DW vs. 4.0 DW
1
Laminaria digitata; frond vs. stipe
8.0 DW vs. 4.0 DW
1
Values are in mg Li/kg dry weight (DW) or ash weight (AW). a 1, Black and Mitchell, 1952; 2, Vinogradova and Koual’skiy, 1962.
Reference
a
Algae and Macrophytes 49 Table 2.15: Manganese Concentrations in Field Collections of Algae and Macrophytes Organism
Concentration
Reference
Algae and macrophytes; whole Sea of Japan; 12 spp. Canada, Atlantic Provinces; 11 spp. United Kingdom; coastal waters; 15 spp. Goa, India; 33 spp. Japan; 12 spp. East Indies; 19 spp. Iceland; 12 spp.
5.0-805.0 DW 20.0-50.0 DW 3.8-73.0 DW
1 2 3
25.0-3421.0 DW 4.4-41.0 DW 23.7-316.0 DW 13.0-680.0 DW
4 5 6 7
Argentina; summer 2002; 3 sites; Porphyra columbina vs. Ulva sp.; whole
31.7-41.8 DW vs. 8.1–51.4 DW
25
Brown alga, Ascophyllum nodosum, whole; United Kingdom
16.0-21.0 DW
8
Mangrove, Avicennia marina; SE Australia; pneumatophores
4.0-163.0 DW
30
Green alga, Enteromorpha sp.; whole; 2000-2003; Gulf of Gdansk, Baltic Sea
172.7 (30.7-384.1) DW
23
Near iron-ore tailings site vs. reference site Chaetomorpha brychagona Enteromorpha crinita
392.0-592.0 DW vs. 57.0 DW 96.0-226.0 DW vs. 4.0 DW
9 9
Green alga, Cladophora sp.; Baltic Sea; 2002-2003 Gulf of Gdansk Vistula Lagoon Reference site
298.0 (48.7-740.0) DW 1185.0 DW; max. 1930.0 DW 253.0 DW; max. 428.0 DW
26 26 26
Fucus vesiculosus, whole; United Kingdom Menai straits Dulas Bay Irish Sea Tamar estuary
103.0 DW 71.0 DW 99.0 DW 204.0 (85.0-393.0) DW
8 10 11
India; Tamil Nadu; leaves; January 2007 Mangroves; 8 spp. Halophytes; 5 spp.
168.7 (51.1-391.0) DW 38.3 (11.7-88.6) DW
31 31
a
(Continues)
50 Chapter 2 Table 2.15: Cont’d Organism
Concentration
Macroalgae (6 spp.) vs. Phytoplankton; Gulf of California, Mexico; 1998-1999; whole
29.0-120.0 DW vs. 289.0 DW
24
Macroalgae; epiphytic on estuarine mangrove aerial roots; Sydney region, Australia Caloglossa leprieurii Caloglossa nipae Bostrychia sp.
1400.0 DW 1600.0 DW 1800.0 DW
27 27 27
Mangroves; Gulf of California, Mexico; 1998-1999; twigs vs. leaves Rhizophora mangle Avicennia germinans Laguncularia racemosa
47.0 DW vs. 30.0 DW 11.1 DW vs. 64.0 DW 106.0 DW vs. 28.0 DW
24 24 24
9.2-170.0 DW
12
99.0 DW 49.0 DW
13 13
21.7 (4.4-41.5) DW 35.0 DW
14 15
6.1 DW vs. not detected 13.3 DW vs. 4.3 DW 7.7 DW vs. 1.2-22.0 DW
16 16 16
190.0-550.0 DW
28
Marsh plants; whole; Harbour Island, Texas; 14 spp. Puerto Rico; whole Padina gymnospora Thalassia testudinium Phytoplankton Whole Texas Continental Shelf Monterey Bay, California Organic fractions vs. siliceous frustules No titanium group Titanium group Strontium- concentrated group Mangrove, Rhizophora mangle; summer 2001; Natal, Brazil; leaves Sargassum horneri Lamina Air bladder Stipe Receptacle Whole, varying lengths Up to 50 cm 50-100 cm 100-150 cm
Reference
12.7 DW 7.0 DW 4.3 DW 3.4 DW
5 5 5 5
9.9 DW 8.4 DW 8.7 DW
5 5 5
a
(Continues)
Algae and Macrophytes 51 Table 2.15:
Cont’d
Organism
Concentration
Sargassum spp.; whole; south Texas Continental Shelf Seaweeds; whole Korea; 20 spp. South Africa; 5 spp. Norway United Kingdom; 5 spp.; May vs. June
31.4 (12.0-89.5) DW
14
15.0-191.0 DW 0.3-6.1 FW 4.0-164.0 DW 22.0-155.0 DW vs. 36.0-121.0 DW, 8.9-24.0 FW
17 18, 19 20 21
Spartina alterniflora Sprout Mature plant Dead plant Leaves and stalks
50.0-130.0 DW 30.0-95.0 DW 90.0-330.0 DW 50.0 DW
22 22 22 22
61.0 (7.2-476.0) DW vs. 40.0 (18.0–73.0) DW
29
Eelgrass, Zostera marina; whole; Baja California, Mexico; reference site vs. salt mining site
Reference
a
Values are in mg Mn/kg fresh weight (FW) or dry weight (DW). a 1, Gryzhankova et al., 1973; 2, Young and Langille, 1958; 3, Riley and Roth, 1971; 4, Agadi et al., 1978; 5, Ishii et al., 1978; 6, Sivalingam, 1978b; 7, Munda, 1978; 8, Foster, 1976; 9, Wong et al., 1979; 10, Preston et al., 1972; 11, Bryan and Uysal, 1978; 12, Lytle et al., 1973; 13, Stevenson and Ufret, 1966; 14, Horowitz and Presley, 1977; 15, Knauer and Martin, 1973; 16, Martin and Knauer, 1973; 17, Pak et al., 1977; 18, Van As et al., 1973; 19. Van As et al., 1975; 20, Lunde, 1970; 21, Black and Mitchell, 1952; 22, Williams and Murdock, 1969; 23, Zbikowski et al., 2006; 24, Ruelas-Inzunza and PaezOsuna, 2006; 25, Perez et al., 2007; 26, Zbikowski et al., 2007; 27, Melville and Pulkownik, 2007; 28, Silva et al., 2006; 29, Marcias-Zamora et al., 2008; 30, Preda and Cox, 2002; 31, Agoramoorthy et al., 2008.
abundance of lithogenic materials in the immediate environment (Lowman et al., 1967), and proximity to anthropogenic sources (Table 2.15). For example, tidal fluctuations of 0.6-0.8 m were stimulatory to manganese-loaded phytoplankton, but the reverse was observed at higher tidal fluctuations of 1.0-1.2 m (Sanders, 1978). Lowered manganese burdens and lowered ash content occur in various species of Posidonia, Sargassum, Dictyota, and Dictyopterus collected long distances from the mouths of rivers in Puerto Rico when compared to conspecifics collected nearer the river mouth; these differences were attributed to the relatively high concentrations of lithogenic materials in riverine discharges to the sea (Lowman et al., 1967).
2.22 Mercury The highest mercury concentration recorded in marine plants is 51.5 mg/kg DW in leaves of the marine flowering plant, P. oceanica, collected from a sewer outfall in Marseille, France (Table 2.16; Augier et al., 1978b). Concentrations of total mercury in marine flora
52 Chapter 2 Table 2.16: Mercury Concentrations in Field Collections of Algae and Macrophytes Organism Algae and macrophytes, whole Admiralty Bay, Antarctica; 2004; 3 spp. Malaysia, 26 spp. Korea, 17 spp. Aleutian Islands; 2003-2004; used as food; 4 spp. Brown alga, Ascophyllum nodosum, whole 60 cm length vs. 100-140 cm length Eikhamrane, Norway vs. Flak, Norway Transplanted from Eikhamrane to Flak for 4 months Lofoten, Norway Trondheimsfjord, Norway Hardangerfjord, Norway
Concentration
a
Reference
0.024-0.047 DW
21
Max. 0.35 DW 0.02-0.52 DW 0.001-0.005 FW; max. 0.039 FW
1 2 23
0.07 FW vs. 0.11 FW 0.012-1.09 DW vs. 0.02-0.03 DW 0.04-0.95 DW
3 4
0.05-0.08 DW 0.05-0.18 DW 0.05-20.0 DW
5 5 5
4
Seaweeds, Fucus spp.; NW Portugal; September 2002 Receptacles Stipes Holdfasts
0.012-0.061 DW 0.028-0.221 DW 0.029-0.287 DW
22 22 22
India; Tamil Nadu; January 2007; leaves Mangroves; 8 spp. Halophytes; 5 spp.
0.06 (0.03-0.07) DW 0.43 (0.09-0.94) DW
28 28
Kelp, Laminaria digitata, whole Firth of Tay, Scotland Solent region, England
0.13 FW; 0.79 DW 0.17 DW
Macroalgae; whole; 4 spp.; Strait of Magellan, Chile; 2000-2001 Phytoplankton, whole Antarctica, Terra Nova Bay; 1989-91 Chesapeake Bay, Maryland North Atlantic Ocean; offshore Japan, Minamata Bay; 1974 Spain and Portugal Norway, west coast Laver, Porphyra umbilicalus; whole; United Kingdom
6 7
<0.001-0.02 DW
27
0.04 DW 0.11-0.13 DW 0.05 FW Max. 0.32 DW Max. 1.2 DW 0.6-25.2 DW
8 9 10 20 11 12
0.5 FW; 2.4 DW
13 (Continues)
Algae and Macrophytes 53 Table 2.16: Organism Marine flowering plant, Posidonia oceanica Near sewer outfall; Marseille, France Rhizomes Leaves Roots Dead sheaths of shoots; mercurycontaminated site (Tuscany, Italy) vs. reference site (Corsica, France) 1995 1996 1997 2003 Mediterranean Sea; 3 sites; summers 2004-2005; blades Corsica, France; summer 2003; adult leaves; blades vs. sheaths
Cont’d
Concentration
Reference
2.5 DW 51.5 DW 0.6 DW
19 19 19
0.21 DW vs. 0.05 DW 0.23 DW vs. 0.05 DW 0.3 DW vs. 0.06 DW 0.32 DW vs. 0.05 DW 0.05-0.13 DW
24 24 24 24 25
0.05 (0.03-0.07) DW vs. 0.04 (0.01-0.05) DW
26
Saltmarsh grass, Spartina alterniflora; Brunswick, Georgia, United States Whole Leaves and stalks Rhizomes Roots Base of stalk Stalk Leaves
Max. 1.4 DW 0.2 DW 0.5-0.7 DW 0.7-8.7 DW 0.6-1.2 DW 0.4-1.1 DW 0.4-1.1 DW
14 14, 15 16 16 16 16 16
Alga, Ulva spp., whole Firth of Tay, Scotland Minamata Bay, Japan Puget Sound, Washington State
6.3 FW; 25.5 DW Max. 14.0 DW 0.005-0.011 DW
6 17 18
a
Values are in mg Hg/kg fresh weight (FW) or dry weight (DW). a 1, Sivalingam, 1980; 2, Kim, 1972; 3, Augier et al., 1978a; 4, Myklestad et al., 1978; 5, Haug et al., 1974; 6, Jones et al., 1972; 7, Leatherland and Burton, 1974; 8, Bargagli et al., 1998; 9, Cocoros et al., 1973; 10, Greig et al., 1975; 11, Stenner and Nickless, 1975; 12, Skei et al., 1976; 13, Preston et al., 1972; 14, Windom et al., 1976; 15, Windom, 1975; 16, Windom, 1973; 17, Matida and Kumada, 1969; 18, Schell and Nevissi, 1977; 19, Augier et al., 1978b; 20, Nishimura and Kumagi, 1983; 21, Santos et al., 2006; 22, Cairrao et al., 2007; 23, Burger et al., 2007; 24, Lafabrie et al., 2007a; 25, Lafabrie et al., 2007b; 26, Lafabrie et al., 2008a; 27, Astorga-Espana et al., 2008; 28, Agoramoorthy et al., 2008.
54 Chapter 2 were usually less than 1.0 mg/kg DW; higher concentrations were almost always associated with contamination from environmental releases of mercury due to human activities (Table 2.16; Eisler, 2006). In general, mercury concentrations were highest in marine plants collected from sewage lagoons, near chloralkali plants, and proximity to industrialized areas (Augier et al., 1978a; Chigbo et al., 1982; Eisler, 2006). The macrophyte P. oceanica is proposed for use in reconstructing past mercury contamination of coastal sites by measuring mercury concentrations in the dead sheaths of shoots and taking into account degradation of the sheaths (Lafabrie et al., 2007a,b). A mercury budget for estuaries along the Georgia, United States, coast indicates that the dominant salt marsh plant S. alterniflora exerts a strong control on mercury migration (Gardner et al., 1975; Windom, 1973; Windom et al., 1976). Mercury entered the estuary mainly in solution, delivering about 1.5 mg of mercury annually to each square meter of salt marsh surface. Annual uptake of mercury by Spartina alone was about 0.7 mg/m2 salt marsh. Mangrove vegetation plays a similar role in mercury cycling in the Florida Everglades (Lindberg and Harriss, 1974; Tripp and Harriss, 1976). Another salt marsh macrophyte, H. portulacoides, accumulates mercury in the below ground part of the plant (Valega et al., 2008). However, this fraction is mobile and able to return mercury to the sediment pool throughout the mineralization process, thus contributing to reactive mercury concentrations in pore waters (Valega et al., 2008). Rapid accumulation of mercury, especially organomercury compounds, by various species of algae under controlled conditions is documented (Davies, 1974; Fang, 1973; Laumond et al., 1973). However, mercury uptake rates and accumulations by marine algae are modified by mercury concentration (Sick and Windom, 1975; Windom et al., 1976), duration of exposure (Sick and Windom, 1975), salinity of the medium (Gambrell et al., 1977), biological surface area (Sick and Windom, 1975), variability in mercury detoxification mechanisms (Davies, 1976), cell density (Delcourt and Mestre, 1978), and accumulation after death (Glooschenko, 1969). For example, Croomonas salina took up 1400.0 mg Hg/kg DW after 48 h in a solution containing 0.164 mg Hg/L (Parrish and Carr, 1976); Chaetoceros galvestonensis and P. tricornutum contained 7400.0 and 2400.0 mg Hg/kg DW, respectively, when cultured in media containing 0.1 mg Hg/L (Chaetoceros) or 0.05 mg Hg/L (Phaeodactylum) (Hannan et al., 1973); and Isochrysis sp. contained up to 1000.0 mg Hg/kg DW after exposure to 0.015 mg Hg/L (Davies, 1974). Salt marsh plants show enhanced mercury accumulation in roots at lower salinities and higher pH (Gambrell et al., 1977). Phytotoxic effects of mercurials include reduced growth, developmental abnormalities, photosynthesis inhibition, and death. Effects in sensitive species, such as Scripsiella faroense (Kayser, 1976) and Nitzchia spp. (Saboski, 1977), were measured at 0.001 mg Hg2+/L. In one case, reduced growth was documented at 0.001-0.005 mg Hg/L in natural phytoplankton
Algae and Macrophytes 55 from Saanach Inlet, British Columbia, using artificial ecosystems; however, recovery to above-control levels occurred in 21 days (Thomas et al., 1980). Sensitivity to mercurials was documented for many species of algae and macrophytes in the range 0.005-0.03 mg/L (Berland et al., 1976, 1977; Davies, 1976; Delcourt and Mestre, 1978; Harrison et al., 1978; Hopkins and Kain, 1971; Horvatic and Persic, 2007; Stromgren, 1980). It is emphasized that phytotoxic effects of mercury are always more pronounced when mercury is present as an organomercurial than in the inorganic form (Boney, 1971; Boney and Corner, 1959; Boney et al., 1959; Delcourt and Mestre, 1978; Eisler, 1987, 2006; Ukeles, 1962).
2.23 Molybdenum All plants contain molybdenum and it is probably essential for growth (Schroeder et al., 1970), although the concentrations required for marine plants are not known with certainty. The highest molybdenum value recorded for any marine plant is 5.8 mg/kg DW (Table 2.17). Among 11 species of seaweeds collected from Palk Bay, Norway, molybdenum values were highest in August and highest among the Rhodophyceae (Lunde, 1970). Molybdenum occurs naturally in seawater as molybdate ion, MoO42, at about 0.01 mg/L (Abbott, 1977). Despite the high concentrations of dissolved molybdenum in offshore waters, phytoplanktons from these locales contain extremely low molybdenum concentrations, almost typical of molybdenum-deficient terrestrial plants (Howarth and Cole, 1985).
Table 2.17: Molybdenum Concentrations in Field Collections of Algae and Macrophytes Organism
Concentration
Reference
Algae, whole; Canada; 11 spp.
0.23-1.36 DW
1
Argentina; summer 2002; 3 sites; Porphyra columbina vs. Ulva sp.; whole
1.1-2.0 DW vs. 0.54-0.67 DW
8
Marsh plants, whole; Texas, United States; 14 spp.
0.36-2.5 DW
2
Porphyra spp., whole; Japan
Max. 1.0 DW; Max. 17.0 AW
3, 4
United Kingdom, 5 spp.
0.2-1.3 DW; 0.04-0.2 FW
5
Norway, 11 spp.
0.3-5.8 DW
6, 7
a
Seaweeds, whole
Values are in mg Mo/kg fresh weight (FW), dry weight (DW) or ash weight (AW). a 1, Young and Langille, 1958; 2, Lytle et al., 1973; 3, Fukai and Meinke, 1959; 4, Fukai and Meinke, 1962; 5, Black and Mitchell, 1952; 6, Lunde, 1970; 7, Friberg et al., 1975; 8, Perez et al., 2007.
56 Chapter 2 The low molybdenum levels are attributed to the high concentrations of sulfate in seawater; sulfate inhibits molybdate assimilation by phytoplankton, making it less available in seawater. As one result, nitrogen fixation and nitrate assimilation—processes that require molybdenum— may require greater energy expenditure in marine waters than in freshwaters and may explain, in part, why marine ecosystems are usually nitrogen limited and lakes are not (Howarth and Cole, 1985). Laboratory studies on uptake of 99Mo by Fucus serratus and Laminaria digitata show that Fucus accumulates twice as much molybdenum at 15 C than at 0 C, with light intensity having little apparent effect (Penot and Videau, 1975). Laminaria, under similar conditions, took up more than 5 times as much molybdenum as did Fucus; however, molybdenum uptake was reduced dramatically on addition of about 0.6 mg KCN/L (Penot and Videau, 1975). Experimentally increasing the ratio of sulfate to molybdate inhibits molybdate uptake by marine algae, slows nitrogen fixation rates, and slows the growth of organisms that use nitrate as a nitrogen source (Howarth and Cole, 1985). Proposed molybdenum criteria to protect marine plants indicate that 0.0177 mg/L seawater and lower are associated with deficiency (Steeg et al., 1986; Vaishampayan, 1983), 0.000014 mg/L and higher are associated with high uptake (Short et al., 1971), and concentrations greater than 50.0 mg Mo/L are associated with growth reduction and other adverse effects (Eisler, 2000b; Sakaguchi et al., 1981).
2.24 Nickel In general, nickel concentrations in plants, other living organisms, and abiotic materials are elevated in the vicinity of nickel smelters and refineries, nickel-cadmium battery plants, sewage outfalls, electroplating plants, coal ash disposal basins, and heavily populated areas (Eisler, 2000d). Nickel concentrations in marine algae and macrophytes from pollution-free locales, on a DW basis, ranged from 0.2 to 39.1 mg/kg, with most values less than 10.0 mg/kg (Table 2.18). High concentrations up to 60.3 mg Ni/kg DW blade were also reported for the seagrass, P. oceanica, and were positively correlated with sediment nickel concentrations (Lafabrie et al., 2007b). Algae reportedly bioconcentrate nickel from seawater by factors that range from 146 to over 1000 (Black and Mitchell, 1952; NAS, 1975; Sivalingam, 1978b). Accordingly, elevated levels of nickel were expected in algae in samples collected near heavily populated areas (Bernhard and Zattera, 1975), especially in the vicinity of sewage outfalls (Montgomery et al., 1978). For example, turtle grass, Thalassia testudinium, contained up to 45.0 mg Ni/kg DW in leaves over controls during exposure for 120 days in sewage sludge; for mangrove, R. mangle, this value was 10.0 mg Ni/kg DW higher in roots over conspecifics from a reference site (Montgomery et al., 1978). Concentrations of nickel in Spartina sp. roots from the vicinity of a discharge from a nickel-cadmium battery plant ranged from 30.0 to 500.0 mg/kg DW, and reflected sediment
Algae and Macrophytes 57 Table 2.18: Nickel Concentrations in Field Collections of Algae and Macrophytes Organism Algae and macrophytes, whole Japan; coastal waters; 60 spp. India; Goa; 27 spp. Canada, Atlantic Ocean coast; 11 spp. Sea of Japan; 12 spp. England; coastal waters; 14 spp. Israel; Mediterranean Sea coast; 2 spp. Nickel-contaminated areas vs. reference site Puerto Rico; 2 spp. Texas; Harbour Island; 14 spp.
Concentration
Reference
2.2-6.9 (0.2-31.0) DW 3.5-39.1 DW 0.3 >2.0DW
1, 21 2 3
5.0-31.0 DW 2.7-10.3 DW 5.2-5.8 DW
4 5 6
150.0 DW vs. <15.0 DW
20
20.0-27.0 DW 0.2-2.6 DW
7 21
0.7-1.5 DW vs. 1.0-4.1 DW
26
Brown alga, Ascophyllum nodosum, whole Trondheimsfjord, Norway Menai Straits; United Kingdom Dulas Bay; United Kingdom Nova Scotia Former Soviet Union Scotland
1.0-22.0 DW 22.0 DW 4.6 DW 0.6 DW 0.4 DW 0.9 FW; 1.5-6.3 DW
8 9 9 19 19 19
Green alga, Cladophora sp.; Baltic Sea; 2000-2003 Gulf of Gdansk Vistula Lagoon Reference site
3.5 (0.8-9.2) DW 11.4 DW; max. 17.1 DW 6.4 DW; max. 10.6 DW
27 27 27
Diatoms, whole, Black Sea
150.0 AW
10
Green alga, Enteromorpha sap.; whole; 2000-2003; Gulf of Gdansk, Baltic Sea
3.6 (0.1-7.1) DW
25
45.0 DW
23
10.0 DW
23
Argentina; summer 2002; 3 sites; Porphyra columbina vs. Ulva sp.; whole
Florida; near sewage outfall; exposure for 120 days Turtle grass, Thalassia testudinium; leaves Mangrove, Rhizophora mangle; roots
a
(Continues)
58 Chapter 2 Table 2.18: Cont’d Organism
Concentration
Reference
Bladder wrack, Fucus vesiculosus, whole Norway United Kingdom Tamar estuary Dulas Bay Menai Straits Irish Sea England Greenland Nova Scotia Scotland
3.5 (0.7-4.8) DW 6.0 DW 8.1 DW 6.7 DW 1.2-29.6 DW 0.6-2.3 DW 2.0 DW 1.4 FW; 4.9 DW
11 9 9 12 19 19 19 19
Macroalgae; epiphytic on estuarine mangrove aerial roots; Sydney region, Australia Caloglossa leprieurii Caloglossa nipae Bostrychia sp.
10.0 DW 4.0 DW 5.0 DW
28 28 28
Marsh plants; whole Harbour Island, Texas; 14 spp.
0.21-2.6 DW
13
<1.0-12.6 DW
33
1.9-7.8 DW 5.5 DW
14 15
4.4 (2.2-7.5) DW
16
27.5-60.3 DW
32
24.4 (13.0-50.0) DW vs. 4.3 1.8-10.0 DW
31, 34
0.24-0.58 DW
29
60.0 DW 10.0 DW
30 30
Macroalgae; whole; 4 spp.; Strait of Magellan; Chile; 2000-2001 Phytoplankton Organic fractions Whole, Puget Sound, Washington state South Texas coast Seagrass, Posidonia oceanica Mediterranean Sea; summers 2004-2005; 3 sites; blades Corsica, France; summer 2003; adult leaves; blades vs. sheaths Mangrove, Rhizophora mangle; summer 2001; Natal, Brazil; leaves Salt marsh plants; Venice lagoon; 2001; aerial parts Phragmites australis Bolboschoenus maritimus
2.0-7.0 DW
a
8, 19
(Continues)
Algae and Macrophytes 59 Table 2.18: Organism
Concentration
Sargassum, Sargassum horneri Whole, varying lengths Up to 50 cm 50-100 cm 100-150 cm Receptacle Lamina Air bladder Stipe
2.1 DW 1.9 DW 2.3 DW 2.0 DW 2.9 DW 1.7 DW 2.0 DW
Cont’d Reference
1 1 1 1 1 1 1
Sargassum, Sargassum spp.; Gulf of Mexico; whole
0.9-15.6 DW
21
Sargassum weed, Sargassum sp.; Texas; outer continental shelf; whole
5.2 DW
16
Seaweeds, whole United Kingdom; 5 spp. Japan; Tomogashima; 38 spp.
3.2-9.3 DW; 0.9-1.4 FW 2.8 (0.2-10.9) DW
17 18
Eelgrass, Zostera marina; Oregon Leaf Rhizome Root
20.0 DW 25.0 DW 40.0 DW
24 24 24
3.2 DW
22
Algae, Zygnema sp.; Arctic Ocean; Spitsbergen, Svalbard; JulyAugust 1988; whole
a
Values are in mg Ni/kg fresh weight (FW), dry weight (DW), or ash weight. a 1, Ishii et al., 1978; 2, Agadi et al., 1978; 3, Young and Langille, 1958; 4, Gryzhankova et al., 1973; 5, Riley and Roth, 1971; 6, Roth and Hornung, 1977; 7, Stevenson and Ufret, 1966; 8, Lande, 1977; 9, Foster, 1976; 10, Vinogradova and Koual’skiy, 1962; 11, Bryan and Uysal, 1978; 12, Preston et al., 1972; 13, Lytle et al., 1973; 14, Martin and Knauer, 1973; 15, Laevastu and Thompson, 1956; 16, Horowitz and Presley, 1977; 17, Black and Mitchell, 1952; 18, Ishibashi et al., 1964a; 19, Jenkins, 1980b; 20, WHO, 1991; 21, Eisler, 1981; 22, Drbal et al., 1992; 23, Montgomery et al., 1978; 24, Kaldy, 2006; 25, Zbikowski et al., 2006; 26, Perez et al., 2007; 27, Zbikowski et al., 2007; 28, Melville and Pulkownik, 2007; 29, Silva et al., 2006; 30, Bragato et al., 2006; 31, Lafabrie et al., 2007b; 32, Lafabrie et al., 2008a; 33, AstorgaEspana et al., 2008; 34, Lafabrie et al., 2008b.
nickel concentrations that ranged up to 7000.0 mg/kg DW (Kniep et al., 1974). Dumping of sewage sludge in coastal tropical waters may result in elevated concentrations of nickel and other trace metals by turtle grass and other members of that ecosystem. The influence of airborne nickel species from automobile exhausts on coastal communities has not been addressed adequately.
60 Chapter 2 Nickel is ubiquitous in the biosphere and is considered essential for the normal growth of many species of microorganisms and photosynthetic plants (Eisler, 2000d; USPHS, 1993, 1995). In higher plants, magnesium is the usual competitor for nickel in biological ionexchange reactions; active binding sites are the carboxylic and hydroxycarboxylic groups fixed on the cell wall (Kasprzak, 1987). There is little convincing evidence for the biomagnification of nickel in the food chain. Most authorities agree that nickel concentrations did not increase with ascending trophic levels of food chains and that predatory animals do not have higher concentrations (Chau and KulikovskyCordeiro, 1995; Eisler, 2000d; Jenkins, 1980a; WHO, 1991). The potential for biomagnification exists because algae and macrophytes have comparatively elevated concentrations of nickel; however, animals seem to be able to regulate the nickel content of their tissues by controlled intake and increased excretion (Eisler, 2000d; Outridge and Scheuhammer, 1993). The alga Thalassiosira rotula can accumulate as much as 90.0 mg Ni/kg DW from the ambient medium; however, growth was inhibited at 0.03 mg Ni/L and was toxic at 0.3 mg Ni/L (Dongmann and Nurnberg, 1982). For the diatom Navicula pelliculosa, 50% growth inhibition occurred in 14 days at 0.1 mg Ni/L (WHO, 1991), and reduced growth was reported in P. tricornutum at 1.0 mg Ni/L (USEPA, 1980b). Photosynthesis inhibition of 50% was reported in the comparatively resistant giant kelp, M. pyrifera, at 2.0 mg Ni/L (USEPA, 1980e). To protect marine plants and other biota, it is proposed that the 24-h average for total recoverable nickel should not exceed 0.0071 mg Ni/L and the maximum concentration should not exceed 0.14 mg/L at any time (USEPA, 1980e); however, this needs to be re-examined because 0.03 mg Ni/L adversely affects growth of marine diatoms (Dongmann and Nurnberg, 1982).
2.25 Plutonium Marine algae and macrophytes concentrate radioplutonium isotopes from ambient seawater by factors up to 660 for dinoflagellates, 770 for the kelp M. pyrifera, 1080 for Eisenia pyrifera, and 1570 for Enteromorpha sp. (Pillai et al., 1964). Among Atlantic Ocean organisms examined for 239Pu, Sargasso weed had the highest concentrations of radioplutonium on a FW basis, higher than mixed zooplankton, starfish Asterias forbesi, shell and meats of mussels and clams, shark liver and bone, and fish tissues, in that order (Wong, 1971). Marine algae may have potential in scavenging radioisotopes of plutonium and other fallout products, and heavy metals in general, from contaminated environments (Wong, 1971). It is alleged that there is negligible hazard to public health from the consumption of plutonium-contaminated algae, fish, or shellfish from the vicinity of the Windscale (United Kingdom) nuclear fuel reprocessing plant (Hetherington et al., 1976; Mitchell, 1977). Porphyra seaweed, as one instance, is processed into flour and subsequently sold as a baked product called laverbread. The radioactive dose to bone of people eating laverbread made from
Algae and Macrophytes 61 Porphyra harvested near Windscale at a rate of 130 g daily was estimated at less than 7.5 millirems annually, which is considered a negligible risk (Hetherington et al., 1976; Mitchell, 1977).
2.26 Radium Phytoplankton from various locations, including coastal Sweden, the Mediterranean Sea, and the Pacific Ocean contained about 6.0 107 mg Ra/kg calcium (Koczy and Titze, 1958). Radium, and possibly thorium, is concentrated by tropical marine algae through two mechanisms: (1) ion exchange or coprecipitation of the ion with the calcium carbonate matrix and (2) complex formation with either the protein nitrogen or some other component of he organic fraction (Edgington et al., 1970). For the Rhodophta and the highly calcified Chlorophyta, radium as well as uranium is concentrated by the first mechanism. For the Phaeophyta, radium is taken up by the second mechanism (Edgington et al., 1970).
2.27 Rhenium Rhenium concentrations in marine plants ranged from 0.046 to 0.073 mg Re/kg AW in Ulva spp. collected from the coast of Japan, and from 0.011 to 0.016 mg Re/kg DW in Ulva spp. and Porphyra spp. from the same location (Fukai and Meinke, 1959, 1962).
2.28 Rubidium Rubidium concentrations in marine photosynthetic organisms ranged from 11.0 to 250.0 mg Rb/kg DW (Table 2.19). Accumulation over ambient seawater by 40-fold is reported for field collections of Sargassum spp. from Japan (Ishii et al., 1978). Under laboratory conditions, F. serratus accumulated 1.7 mg Rb/kg DW; however, accumulation was reduced 50% in 5 h by 103 M dinitrophenol (Penot and Videau, 1975). L. digitata took up 1.0 mg Rb/ kg DW in 2 h at 15 C, with uptake halved at 0 C (Penot and Videau, 1975). Up to 26% retention of radiorubidium is reported after 14 days for Ulva pertussa (Nakamura et al., 1977).
2.29 Ruthenium Algae accumulated radioruthenium-106 from seawater solutions by factors of 100-200 times those of the medium (Ancellin et al., 1967; Ancellin and Vilquin, 1968; Ueda et al., 1978), and retained about 25% of the 106Ru after 14 days (Nakamura et al., 1977). The chemical form in which 106Ru is administered, especially its solubility, will significantly alter bioavailability to algae and other biota (Ancellin and Bovard, 1971). Uptake of 106Ru by marine algae is a surface phenomenon associated mainly with extracellular polysaccharides (Jones, 1960). The presence of ferric hydroxide on sand and silt particles in the medium enhances algal accumulation of ruthenium (Jones, 1960).
62 Chapter 2 Table 2.19: Rubidium Concentrations in Field Collections of Algae and Macrophytes Organism
Concentration
Reference
Algae and macrophytes, whole Coast of Japan; 12 spp. Coastal United Kingdom; 3 spp.
11.0-52.0 DW 80.0-170.0 DW
1 2
Laminaria cloustini; frond Sterile Sporing
250.0 DW 130.0 DW
2 2
Laminaria digitata Frond Stipe
240.0 DW 240.0 DW
2 2
a
Values are in mg Rb/kg dry weight (DW). a 1, Ishii et al., 1978; 2, Black and Mitchell, 1952.
2.30 Selenium Limited data show that selenium concentrations in field collections of algae and macrophytes range from 0.04 to 0.84 mg Se/kg DW (Table 2.20). Studies on the metabolic transformation of inorganic selenium by Tetraselmis tetrathele and Dunaliella minuta demonstrate that the majority of accumulated selenium becomes associated with cellular protein, with the main selenium fraction integrated into the primary protein structure (Wrench, 1978). In marine algae, this may represent a form of storage prior to detoxification (Boisson et al., 1995). Accumulation, transfer, and release of selenium by aquatic biota may affect the speciation and toxicity of dissolved selenium (Besser et al., 1993, 1994). Depletion of dissolved selenite and increased concentration of organoselenium compounds occur during seasonal peaks in phytoplankton abundance. For example, green algae previously exposed to inorganic radioselenium-75 produced increasing concentrations of organoselenium species during population blooms and crashes.
2.31 Silicon Silicon is essential for the growth of many species of algae, especially diatoms (Borowitzka and Volcani, 1977; Morel et al., 1978). Silicon is readily accumulated from seawater by marine algae and macrophytes (Goering et al., 1977; Nelson and Goering, 1978; Yoshimura et al., 1976), and this may account, in part, for the elevated
Algae and Macrophytes 63 Table 2.20: Selenium and Silicon Concentrations in Field Collections of Algae and Macrophytes Element and Organism
Concentration
Reference
Algae, whole
0.19-0.84 DW
1, 2
Argentina; summer 2002; 3 sites; Porphyra columbina vs. Ulva sp.; whole
1.1-1.7 DW vs. 0.5-0.7 DW
8
0.04-0.24 DW 0.16-0.39 DW; 0.047 FW
3 6
<0.2 DW
7
Halimeda opuntia, whole, Jamaica
2000.0 DW
4
Phytoplankton, whole, mostly diatoms, Japan
195,000.0 DW
5
a
Selenium
Seaweeds, whole Norway Seaweeds eaten by humans Shoalgrass, Halodule wrightii; rhizomes; Texas, Lower Laguna Madre; 1986-1987 Silicon
Values are in mg element/kg fresh weight (FW) or dry weight (DW). a 1, Tijoe et al., 1977; 2, Chau and Riley, 1965; 3, Lunde, 1973; 4, Bohm, 1972; 5, Fujita, 1971; 6, Noda et al., 1979; 7, Custer and Mitchell, 1993; 8, Perez et al., 2007.
silicon levels in marine plants of 2000.0-195,000.0 mg Si/kg DW (Table 2.20). About 90% of the silicon in the cell wall of Halimeda opuntia, and presumably other algal species, was associated the water-soluble and water-insoluble organic fractions (Bohm, 1972). Silicon is an important structural component of diatoms, silicoflagellates, some higher plants, sponges, and other organisms. It is necessary for DNA polymerase in diatoms. Silicified algal species are assumed to have an obligate concentration-dependent silicon requirement for growth, and transport systems for the accumulation of silicic acid in these species are well documented (Fuhrman et al., 1978). Phytoplankton growth in coastal waters is likely to become limited only when most of the silicate originally present has been removed in the course of diatom blooms (Paasche, 1973a,b). However, some nonsilicified algae, including Platymonas spp., can accumulate significant amounts of silicon without apparent requirement. Since silicon is a potentially limiting nutrient for diatoms, the removal of available silicon from the environment by organisms that do not require it could affect phytoplankton competition, succession, and eventually the cycling of silicon in the ocean (Fuhrman et al., 1978).
64 Chapter 2
2.32 Silver The highest silver concentration reported in field collections of marine photosynthetic organisms is 14.1 mg Ag/kg DW (Table 2.21). Silver accumulations in marine algae are due mainly to adsorption rather than active uptake (Ratte, 1999; USPHS, 1990). Dissolved silver speciation and bioavailability were important in determining silver uptake and retention by aquatic plants (Connell et al., 1991). Silver availability was controlled by the concentration of free silver ion (Ag+) and the concentrations of other silver complexes, such as AgCl (Sanders and Abbe, 1989). Silver uptake by phytoplankton was rapid in proportion to silver concentration and inversely proportional to water salinity. The availability of free silver ion in marine environments is strongly controlled by salinity of the medium owing to the affinity of silver for the chloride ion (Sanders et al., 1991). Silver sorbs readily to phytoplankton and to suspended sediments. As salinity increases, the degree of sorption decreases. Nearly 80% of silver sorbed to suspended sediments at low salinities desorb at higher salinities; however, desorption
Table 2.21: Silver Concentrations in Field Collections of Algae and Macrophytes Organism
Concentration
Reference
Algae and macrophytes; whole; United Kingdom; 15 spp.
3.7-14.1 DW
1
Diatoms, whole, Black Sea
30.0 AW
2
Fucus vesiculosus, whole Irish Sea Tamar estuary
0.35 DW 0.23 (<0.1-0.36) DW
3 4
Macroalgae; whole; 4 spp.; Strait of Magellan, Chile; 2000-2001
<0.02-0.3 DW
9
Seaweed, Padina sp.; Guam; 1998-1999; fronds
Not detectable to 0.89 DW
8
Phytoplankton, organic fractions
0.2-0.6 DW
5
Seaweeds whole United Kingdom; 5 spp., May vs. June Arabian Sea; 4 spp.; whole; near Pakistan; 1987-88
0.2-0.3 DW vs. 0.1-0.4 DW, 0.03-0.07 FW 0.4-0.76 FW
6
a
7
Values are in mg Ag/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Riley and Roth, 1971; 2, Vinogradova and Koual’skiy, 1962; 3, Preston et al., 1972; 4, Bryan and Uysal, 1978; 5, Martin and Knauer, 1973; 6, Black and Mitchell, 1952; 7, Tariq et al., 1993; 8, Denton et al., 2006; 9, Astorga-Espana et al., 2008.
Algae and Macrophytes 65 does not occur when silver is associated with phytoplankton. Thus, silver incorporation in or on cellular materials increases the retention of silver in the estuary, reducing the rate of transport (Sanders and Abbe, 1987, 1989). Diatoms, Thalassiosira spp., for example, readily accumulated silver from the medium. Once incorporated, silver was tightly bound to the cell membrane, even after the cells were mechanically disrupted (Connell et al., 1991). High bioconcentration of silver from the ambient medium is documented for various species of marine plants. BCFs (mg Ag per kg FW organism/mg Ag per L medium) for silver and diatoms is 210 and for brown algae 240 (USEPA, 1980f). Recovery of silver from industrial and other waste outfalls using marine plants has not yet been evaluated. Marine algae held in solutions containing various concentrations of silver can accumulate the metal from the medium by factors of 13,000-66,000 at equilibrium (Fisher and Reinfelder, 1995; Fisher et al., 1984). Under laboratory conditions, algae held for 38 days in seawater containing radiosilver-110 concentrated 110Ag by a factor of 2800 (Pouvreau and Amiard, 1974). Three species of marine algae subjected to 0.002 mg Ag/L for 24 h contained 27.8-58.6 mg Ag/kg DW at 10 ppt salinity, 16.4-33.4 mg/kg at 15 ppt salinity, and 9.8-25.2 mg Ag/kg DW at 20 ppt salinity (Sanders and Abbe, 1987). Silver is comparatively phytotoxic to marine plants (Boney et al., 1959). Free silver ion is lethal to representative species of aquatic plants at concentrations of 0.0012-0.0049 mg/L; sublethal effects were documented at 0.0004-0.0006 mg/L (Eisler, 2000e). However, toxicity is reduced at increased salinities. For example, ionic silver produced 50% growth reduction in 5 days in the marine alga Prorocentrum mariae-lebouriae at 7.5 ppt and 0.0033 mg Ag/L; at 15.0-22.5 ppt and 30.0 ppt, these values were 0.0067 and 0082 mg Ag/L, respectively (Sanders and Abbe, 1989). Similar results are shown for S. costatum at 0.006-0.02 mg Ag/L (Sanders and Abbe, 1989). At 0.1-0.2 mg Ag/L, Scenedesmus sp. failed to grow (USEPA, 1980f). Species composition and species succession in Chesapeake Bay phytoplankton communities were significantly altered in experimental ecosystems continuously stressed by low concentrations (0.0003-0.0006 mg/L) of silver (Sanders and Cibik, 1985; Sanders et al., 1990). At higher concentrations of 0.002-0.007 mg/L for 3-4 weeks, silver inputs caused disappearance of Anacystis marina, a mat-forming blue-green alga; increased dominance by S. costatum, a chain-forming centric diatom; and caused cell burdens of 8.6-43.7 mg Ag/kg DW (Sanders and Cibak, 1988). The proposed silver criterion of 0.0023 mg total recoverable silver/L (maximum)at any time to protect marine life (USEPA, 1980f) needs to be reconsidered because phytoplankton species competition and succession are significantly altered at 0.0003-0.0006 mg total Ag/L, and some species of marine algae show extensive accumulations at 0.001-0.002 mg total Ag/L (Eisler, 2000e).
66 Chapter 2
2.33 Strontium The highest concentration of strontium recorded in field collections of algae and macrophytes was 7770.0 mg Sr/kg DW in the tropical calcareous alga H. opuntia (Table 2.22). Marked discrimination for strontium over calcium is recorded in several species of marine flora (Gogate et al., 1975; Weiss et al., 1976). This, and the observations that marine plants readily accumulate strontium from seawater (Hiyama and Shimizu, 1964; Ichikawa, 1961; Rice, 1956; Ryndina, 1976; Skipnes et al., 1975; Zlobin, 1966) and that there is an established need for strontium in normal algal metabolism (Weiss et al., 1976), may account, in part, for the elevated strontium content in Halimeda. Marine plants were unable to discriminate between radiostrontium-90 and stable strontium (Parchevskii et al., 1965), but this pattern was not evident for strontium-89. For example, of 12 species of planktonic algae grown in media containing both strontium-89 and strontium-90, only Carteria and Thoracomonas took up 90Sr, the others took up 89Sr (Rice, 1956). In another case, an increase in stable strontium in seawater up to 160.0 mg Sr/L caused a threefold reduction in the uptake of 89Sr by F. serratus (Zlobin, 1966). Polikarpov (1961) cautioned against use of dead algae in assessing strontium risk owing to loss of all accumulated strontium after death, as was documented for C. barbata and other species.
Table 2.22: Strontium Concentrations in Field Collections of Algae and Macrophytes Organism
Concentration
Reference
Algae and macrophytes, whole India; west coast; 9 spp. England; coastal waters; 10 spp. Irish Sea
19.0-646.0 DW; Max, 1458.0 DW 5.8-39.0 DW 0.02-6.2 FW
1 2 3
Diatoms; whole Mediterranean Sea Black Sea
Max. 1500.0 AW Max. 15,000.0 AW
4 5
Halimeda opuntia; whole; Jamaica
7700.0 DW
6
Phytoplankton; organic fractions No titanium group With titanium group Strontium-concentrated group
147.0 DW 119.0 DW 697.0 DW
7 7 7
Sargassum enerve, whole
2200.0 AW
4
a
Values are in mg Sr/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Gogate et al., 1975; 2, Riley and Roth, 1971; 3, Mauchline and Templeton, 1966; 4, Fukai et al., 1962; 5, Vinogradova and Koual’skiy, 1962; 6, Bohm, 1973; 7, Martin and Knauer, 1973.
Algae and Macrophytes 67 Strontium availability probably influences the distribution of many macrophytes. Thus, mangrove vegetation comprising species of Laguncularia, Conocarpus, and Rhizophora— normally associated with brackish saline waters—were found in inland stations on Barbuda, West Indies, having no connection with the sea (Stoddart et al., 1973). Analysis of the inland waters showed higher concentrations of strontium and calcium, and lowered concentrations of sodium, potassium, and magnesium when compared with seawater having the same chloride content, with the higher strontium and calcium levels associated with changes in limestone composition.
2.34 Technetium The brown seaweed A. nodosum was used to biomonitor the spatial distribution of technetium-99 in Wales (Oliver et al., 2006). During the period August 1999 to June 2000, eight sites containing Ascophyllum were selected 45-650 km from the Sellafield nuclear reprocessing facility, the putative source of the 99Tc. Ascophyllum 99Tc content decreased with increasing distance from the facility, being 202 times higher in June 2000 at the closest site than at the most distant site. Discharges of 99Tc from the facility continue to decrease (Oliver et al., 2006).
2.35 Tin Tin concentrations in field collections of marine algae and macrophytes ranged from 0.5 to 101.0 mg Sn/kg DW whole plant (Table 2.23), suggesting high bioconcentration potential over ambient seawater. BCFs were highest when ambient tin levels were <0.001 mg/L, when exposure times were comparatively lengthy, and when organism lipid content was elevated (Champ, 1986; Laughlin et al., 1986; Thain and Waldock, 1986; Thompson et al., 1985). BCFs for inorganic tin and marine algae were about 1900 (Eisler, 2000f). A BCF of 20,000 was reported after 7 days at 0.002 mg total Sn/L (Maguire et al., 1984). Partitioning or binding may control uptake of TBT by marine phytoplankton. A linear relation is documented for external concentrations of TBT compounds and cell burdens in Nannochloris sp. and Chaetoceros gracilis, but was not linear for Isochrysis galbana (Chiles et al., 1989). Leaves of mangroves and halophytes collected on January 8, 2007 from a mangrove forest preserve in Tamil Nadu, India, had unusually high concentrations of total tin: up to 2516.7 mg/Sn kg DW (Table 2.23; Agoramoorthy et al., 2008). The reasons for this are unknown, but tin concentrations were positively correlated with iron and mercury (Agoramoorthy et al., 2008), and could have been a contaminant associated with these metals.
68 Chapter 2 Table 2.23: Tin Concentrations in Field Collections of Algae and Macrophytes Organism
Concentration
Reference
Algae; whole; 12 spp.; United Kingdom
11.0-101.0 DW
1
Seaweeds, whole, 5 spp.
0.5-1.8 DW; 0.1-0.5 FW
2
Green alga, Enteromorpha spp. Inorganic tin Monomethyltins Dimethyltins Trimethyltins Tetramethyltins Monobutyltins Tributyltins
0.4 FW; 4.4 DW 0.5 FW 0.5 FW <0.001 FW <0.001 FW 0.006 FW; 0.4 DW 0.05 FW; 0.6 DW
3 3 3 3 3 3 3
India; Tamil Nadu; January 2007; leaves Mangroves; 8 spp. Halophytes; 5 spp.
1187.6 (354.2-1333.5) DW 1871.2 (1655.8-2516.7) DW
5 5
Phytoplankton; Bohai Bay, North China; May-September, 2002 Monobutyltins Dibutyltins Tributyltins Triphenyltins
0.007 FW 0.019 FW 0.013 FW 0.001 FW
4 4 4 4
a
Values are in mg Sn/kg fresh weight (FW), dry weight (DW), and ash weight (AW). a 1, Riley and Roth, 1971; 2, Black and Mitchell, 1952; 3, Donard et al., 1987; 4, Hu et al., 2006; 5, Agoramoorthy et al., 2008.
TBTs are highly toxic to aquatic plants and are present in some harbors where their release from antifouling paints is the putative source (Laughlin et al., 1986; USEPA, 1986; Walsh et al., 1985). The ability of algae to reduce various organotins to less-toxic metabolites that can be excreted rapidly seems to preclude biomagnification (Cardwell and Sheldon, 1986). Marine plants are important in the cycling of tin. Living algae are effective in immobilizing tin from seawater and regulating the formation and degradation of toxic methyltin compounds (Donard et al., 1987). Some species of algae, including two species of Chlorella, can degrade TBT when present in a high-growth medium (Tam et al., 2002; Tsang et al., 1999). Dead and decaying algae, however, accumulate inorganic and organic tin compounds, release them, and ultimately remove tin from the estuary to the atmosphere by formation of tetramethyltins (Donard et al., 1987; Tam et al., 2002). Comparatively elevated concentrations of inorganic tin (>1.5 mg Sn/L) were associated with frustule abnormalities in Nitzschia lierethrutti after 14-day exposure (Saboski, 1977). In
Algae and Macrophytes 69 general, inorganic tins were always less toxic to marine flora than all organotins tested, and TBTs were the most toxic triorganotin compounds tested (Argese et al., 1998). In order of toxicity of triorganotins to marine plants, TBTs were the most toxic followed by tripropyltins, triphenyltins, trimethyltins, and tripentyltins (Eisler, 2000f). For algae, 50% growth inhibition in 72 h was reported for diatoms at 0.31 mg Sn (as inorganic tin)/L; for TBT compounds, growth inhibition occurred at 0.0001-0.0003 mg/L (Beaumont and Newman, 1986; Walsh et al., 1985), they inhibited photosynthesis at 0.003 mg/L (Hall and Pinkney, 1985) and death at 0.015 mg/L (Walsh et al., 1985). Resistance to tin is variable. A marine diatom, T. pseudonana, showed no adaptation or resistance to triphenyltins or TBTs (Walsh et al., 1985), but another diatom, A. coffeaeformis, was extremely resistant (Thomas and Robinson, 1986, 1987).
2.36 Titanium Titanium concentrations in marine plants are variable and may reach as high as 10,000.0 mg Ti/kg DW in dinoflagellates under bloom conditions (Table 2.24; Collier, 1953). Phytoplanktons in Monterey Bay, California, were analyzed for various metals based on three arbitrary groupings in organic fractions and frustules: titanium not detected and strontium not concentrated; titanium detected and strontium not concentrated; and strontium concentrated (Martin and Knauer, 1973). Concentrations of most metals were higher in the latter two groups, especially iron, manganese, aluminum, and titanium. It was speculated that these samples represented phytoplankton populations with reduced growth rate, and because of slow turnover rates sufficient time had elapsed for greater uptake of several metals. However, titanium is relatively abundant in many species of marine plants, especially in early summer (Table 2.24), and this does not support the scenario proposed by Martin and Knauer (1973).
2.37 Tungsten On an AW basis, tungsten concentrations in Ulva spp. from Japanese waters ranged from 0.13 to 0.18 mg/kg whole plant (Fukai and Meinke, 1959). On a DW basis, Porphyra spp. and Ulva spp. from Japan contained between 0.029 and 0.042 mg W/kg whole plant (Fukai and Meinke, 1962).
2.38 Uranium Accumulation of uranium salts in Scenedesmus quadricauda under laboratory conditions was highest at pH 6.0, 24 C, and algal biomass of 30 mg/L (Pribil and Marvan, 1976). Lowest uptake was observed at pH 4.0, 3 C, and biomass of 2290 mg/L; intermediate values were recorded for pH 8.0, 50 C, and biomass of 840 mg/L. At optimal pH and temperature, mean
70 Chapter 2 Table 2.24: Titanium Concentrations in Field Collections of Algae and Macrophytes Organism
Concentration
Reference
Algae and macrophytes, whole Sea of Japan; 12 spp. United Kingdom; 15 spp.
5.0-147.0 DW 7.8-99.5 DW
1 2
Diatoms, Black Sea
20,000.0 AW
3
Dinoflagellate, Gymnodinium breve
100.0-1000.0 DW
4
not detected 27.0 DW not detected
5 5 5
115.0 DW 400.0 DW Max. 221.0 DW
5 5 5
20.0-38.0 DW 7.0-308.0 DW; 1.4-57.0 FW
6 6
33.9 DW 40.0 DW 21.8 DW
7 7 7
Phytoplankton Organic fraction No titanium group With titanium group With strontium- concentrated group Siliceous frustules No titanium group With titanium group With strontiumconcentrated group Seaweeds Whole; 5 spp. May June Whole Brown Green Red
a
Values are in mg Ti/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Gryzhankova et al., 1973; 2, Riley and Roth, 1971; 3, Vinogradova and Koual’skiy, 1962; 4, Collier, 1953; 5, Martin and Knauer, 1973; 6, Black and Mitchell, 1952; 7, Yamamoto et al., 1970.
accumulations in Scenedesmus held in solutions containing less than 1.0 mg U/L with biomass greater than 500.0 mg/L for 6 h was 3300.0 mg U/kg DW; at higher nominal concentrations of 3.5-10.0 mg U/L, and lower initial biomass of less than 100.0 mg/L and uranium content was 100,500.0 mg/kg DW (Pribil and Marvan, 1976), suggesting that decontamination of uraniumimpacted areas by selected species of algae should be given serious consideration.
2.39 Vanadium Vanadium content of saline photosynthetic organisms ranged between 0.9 and 24.0 mg/kg DW (Table 2.25). Acute toxicity bioassays with vanadium as sodium metavanadate and
Algae and Macrophytes 71 Table 2.25: Vanadium Concentrations in Field Collections of Algae and Macrophytes Organism
Concentration
Algae, whole Sea of Japan; 12 spp. Sea of Japan Coastal waters; United Kingdom; 10 spp.
4.0-24.0 DW 2.8-3.4 Max. 5.7 DW
1 2 3, 4
Argentina; summer 2002; 3 sites; Porphyra columbina vs. Ulva sp; whole
3.5-4.5 DW vs. 2.2-5.6 DW
9
Mangrove, Avicennia marina; Queensland, Australia; pneumatophores
<0.5-8.0 DW
Diatoms, whole, Black Sea
60.0 AW
Macroalgae; whole; 4 spp.; Strait of Magellan, Chile; 2000-2001
<1.2-11.3 DW
Seaweeds, whole 3 spp. 5 spp. May June
Reference
a
11
5 10
Max. 3.1 DW; Max. 262.0 AW
6, 7
1.5-2.6 DW 0.6-11.9 DW; 0.12-2.2 FW
8 8
Values are in mg V/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Gryzhankova et al., 1973; 2, Yamamoto et al., 1970; 3, Chau and Riley, 1965; 4, Riley and Roth, 1971; 5, Vinogradova and Koual’skiy, 1962; 6, Fukai and Meinke, 1959; 7, Fukai and Meinke, 1962; 8, Black and Mitchell, 1952; 9, Perez et al., 2007; 10, Astorga-Espana et al., 2008; 11, Preda and Cox, 2002.
D. marina, Prorocentrum micans, and Asterionella japonica showed that algal populations were reduced by 50% in 9 days at nominal concentrations of 0.5-3.0 mg V/L (Miramand and Unsal, 1978). Algae were more sensitive to vanadium than were marine annelids (10.0 mg V/L), crabs (35.0 mg V/L), and mussels (65.0 mg V/L) during a similar period (Miramand and Unsal, 1978).
2.40 Yttrium Yttrium accumulations in algae were apparently independent of yttrium concentrations in the medium (Parchevskii et al., 1965). Highest accumulations were consistently found in algulose fractions, followed by the fucoidan barium complex fraction, and the alginic acid fraction in the general ratio of 32:8:1 (Ryndina, 1976).
72 Chapter 2 Selective discrimination of 90Sr over 90Y by U. lactuca occurred during exposure for 3 h (Hampson, 1967). Since 90Sr has a physical half life of about 30 years and 90Y only about 65 h, and this is unfortunate from the viewpoint of radiological damage control. The addition of 0.15 mg Y/L led to equilibrium within 3 h, with Ulva accumulating yttrium from the medium by a factor of about 500. Without added carrier, 90Y remained on the outer surface of Ulva; however, with the addition of stable yttrium, 90Y entered the cells in the region of protoplasmic inclusions (Hampson, 1967). Uptake of yttrium as well as strontium was enhanced as the pH of the medium decreased from 8.0 to 6.5 (Hampson, 1967). The influence of chelating agents on 91Y uptake by Porphyra umbilicalis was demonstrated by Vosjan (1969). Porphyra accumulated 91Y from seawater to a concentration factor of 288 in 6 h. The accumulated yttrium was removed with seawater-EDTA washing, suggesting that yttrium is adsorbed onto outer layers of the thallus. When stable yttrium is added, the concentration factor decreases in concentrations greater than 0.008 mg Y/L owing to precipitation. From seawater containing low concentrations of EDTA, uptake of yttrium by Porphyra is negligible because the yttrium is chelated and biologically unavailable.
2.41 Zinc Many species of marine algae and macrophytes contain more than 1000.0 mg Zn/kg DW (Table 2.26). These grossly elevated levels are usually associated with nearby industrial or domestic outfalls containing substantial amounts of zinc (Eisler, 1981, 2000a). Zinc residues from algae already dead on collection are of limited worth. For example, dead Ulva lactosa accumulate zinc more rapidly than live Ulva during a 6-h period (Gutknecht, 1965); a similar pattern was observed in A. nodosum (Skipnes et al., 1975). It was Table 2.26: Zinc Concentrations in Field Collections of Algae and Macrophytes Organism Algae and macrophytes, whole Admiralty Bay, Antarctica; 2004; 3 spp. Canada, Atlantic Ocean coast; 11 spp. Iceland; 10 spp. Panama and Columbia India, Goa; 33 spp. India; 11 spp. East Indies; 18 spp. Japan; 50 spp. Norway, west coast Spain, Rio Tinto estuary
Concentration 27.7-39.6 DW 35.0-97.0 DW 2.5-73.0 DW Max. 2150.0 AW Usually <25.0 DW; max. 203.9 DW 10.8-80.0 DW 14.2-210.0 DW 110.0-3950.0 FW Max. 2370.0 DW Max. 160.0 DW
Reference
a
41 1 2 3 4 5 6 7 8 9 (Continues)
Algae and Macrophytes 73 Table 2.26: Organism United Kingdom; coastal waters; 14 spp. United States; Newport River estuary, North Carolina Argentina; summer 2002; 3 sites; Porphyra columbina vs. Ulva sp.; whole Ascophyllum nodosum, whole Norway Flak Eikhamrane Transferred from Eikhamrane to Flak for 4 months Sorfjorden Lofoton Trondheimsfjord Hardangerfjord United Kingdom Menai Straits Dulas Bay Coastal waters Mangrove, Avicennia marina Western Australia Sediment Root Leaf Hong Kong Sediment Root Leaf Shenzhen, China Sediment Root Leaf Southeast Australia Sediment Root Leaf Pneumatophore
Cont’d
Concentration
Reference
75.0-410.0 DW 33.0-120.0 DW
10 11
21.1 DW vs.17.4-31.3 DW
47
90.0-265.0 DW 825.0-2640.0 DW 70.0-1430.0 DW
12 12 12
2028.0-3700.0 DW 60.0-110.0 DW 66.0-640.0 DW 240.0-3700.0 DW
13 14 14 14
149.0 DW 199.0 DW 60.0-103.0 DW
15 15 16
34.0 DW 16.0 DW 14.0 DW
52 52 52
55.0 DW 16.0 DW 15.0 DW
54 54 54
99.0-106.0 DW 70.0-79.0 DW 23.0 DW
55,56 55,56 55,56
243.0 DW 295.0 DW 25.0 DW 29.0-60.0 DW
57 57 57 60
a
(Continues)
74 Chapter 2 Table 2.26: Cont’d Organism
Concentration
Reference
Green alga, Cladophora sp.; Baltic Sea; 2000-2003 Gulf of Gdansk Vistula Lagoon Reference site
63.0 (21.7-146.4) DW 73.1 DW; max. 105.0 DW 67.5 DW; max. 94.1 DW
46 46 46
Eisenia bicyclis, whole, Japan
39.0-127.0 DW
17, 18
Green alga, Enteromorpha sp.; whole; 2000-2003; Gulf of Gdansk, Baltic Sea
64.1 (13.6-175.9) DW
40
Fucus distichus; whole Distance from zinc ore deposit in km 0.1 1 2 7 18 Greenland Near Pb/Zn flotation mill outfall Reference site
138.0 DW 88.0 DW 43.0 DW 33.0 DW 27.0 DW
19 19 19 19 19
300.0 FW 8.0 FW
37 37
Fucus serratus, whole United Kingdom Norway
70.0-600.0 DW 3500.0-4400.0 DW
16, 20 13
Fucus vesiculosus; whole Sorfjorden, Norway Tamar estuary, United Kingdom Irish Sea Wales, United Kingdom Severn estuary, United Kingdom Menai Straits, United Kingdom Dulas Bay, United Kingdom
2207.0-3090.0 DW 379.0 (138.0-1330.0) DW 171.0 DW 216.0-507.0 DW Max. 800.0 DW 116.0 DW 306.0 DW
13 21 22 23 24 15 15
India; Tamil Nadu; January 2007; leaves Mangroves; 8 spp. Halophytes; 5 spp.
56.0 (9.3-116.9) DW 52.9 (19.0-71.1) DW
61 61
Laminaria cloustini; frond Sterile, winter Sporing, winter Spring
117.0 DW 136.0 DW 76.0 DW
16 16 16
a
(Continues)
Algae and Macrophytes 75 Table 2.26:
Cont’d
Organism
Concentration
Laminaria digitata Frond Stipe; winter Stipe; spring Whole
64.0-99.0 DW Not detectable 62.0 DW 4.0-10.0 FW
16 16 16 16
Macroalgae; whole; 4 spp.; Strait of Magellan, Chile; 2000-2001
14.1-79.0 DW
57
Macroalgae (6 spp.) vs. phytoplankton; Gulf of California, Mexico; 1998-1999; whole
26.2-103.0 DW vs. 117.0 DW
42
Macroalgae; epiphytic on estuarine mangrove aerial roots; Sydney, Australia Caloglossa leprieurii Caloglossa nipae Bostrychia sp.
407.0 DW 250.0 DW 394.0 DW
48 48 48
Macrocystis integrifolia Frond Stipe
97.0 (14.0-335.0) DW 21.0 (10.0-34.0) DW
25 25
5.5-83.9 DW
45
10.1 DW vs. 8.7 DW 11.0 DW vs. 64.0 DW 11.0 DW vs. 15.0 DW
42 42 42
117.0 DW 36.0 DW vs. 34.0 DW
58 58
8.7-21.0 DW
58
Mangrove, Rhizophora mangle; summer 2001; Natal, Brazil; leaves
4.2-6.9 DW
50
Marsh plants; whole; 14 spp.; Harbour Island, Texas
3.4-50.0 DW
26
90.8 (42.0-158.0) DW 590.0 DW 750.0 DW
28 29 30
Macrophytes; 6 spp.; whole; India; 1999-2001 Mangroves; Gulf of California, Mexico; 1998-1999; twigs vs. leaves Rhizophora mangle Avicennia germinans Laguncularia racemosa Mexico; Gulf of California; 1999-2000 Microalgae, Coscinodiscus centralis; whole Macroalgae; Gracilaria sp. vs. Polysiphonia sp.; whole Mangroves; 3 spp.; leaves
Phytoplankton; whole Texas Continental Shelf Japan Monterey Bay, California
Reference
a
(Continues)
76 Chapter 2 Table 2.26: Cont’d Organism Puerto Rico Cymodocea sp. Thalassia testudinum Udotea flabellum Mangrove, Rhizophora stylosa Western Australia Sediment Root Leaf Yingluo Bay, China Sediment Root Leaf
Concentration 3.6-8.7 FW, 45.0-92.0 DW, 120.0-250.0 AW 5.5-12.0 FW, 35.0-82.0 DW, 75.0-200.0 AW 4.9-800.0 FW, 16.0-1900.0 AW
Reference 27 27 27
29.0 DW 15.0 DW 6.6 DW
52 52 52
47.0 DW 6.2 DW 5.9 DW
58 58 58
Saltmarsh macrophytes 3 spp.; Yangtze River estuary; July 2005 Above ground portions Below ground portions 2 spp.; Venice lagoon; 2001; aerial portions Phragmites australis Bolboschoenus maritimus
110.0 DW 160.0 DW
49 49
Max. 14.0 DW Max. 7.5 DW
51 51
Seaweeds; whole Australia; 5 spp.; various distances from lead smelter outfall 2.5-5.2 km 18.0-18.8 km South Africa; 7 spp. Norway Korea; 10 spp. Tunisia; 2 spp.
823.0 DW; max. 3540.0 DW Max. 72.0 DW 1.2-12.0 FW 53.0-520.0 DW 7.0-82.0 DW 27.0-327.0 DW
36 36 31 32 33 44
1580.0-7350.0 DW 95.0-6233.0 DW
13 13
11.0-20.0 DW 7.0-12.0 DW 14.0-37.0 DW
34 34 34
Sorfjorden, Norway; whole Chorda sp. Enteromorpha sp. Spartina alterniflora Sprout Mature plant Dead plant
a
(Continues)
Algae and Macrophytes 77 Table 2.26:
Cont’d
Organism
Concentration
Seaweed, Ulva lactuca; Gulf of California, Mexico; 2002; whole August (low) April (high)
98.0 DW 547.0 DW
43 43
Eelgrass, Zostera spp., whole Australia Spain United States, North Carolina
21.0-670.0 DW Max. 1480.0 DW 49.0 DW
35 9 11
Max. 195.0 DW Max. 70.0 DW Max. 155.0 DW Max. 85.0 DW 27.0 (1.7-221.0) DW vs. 38.0 (0.8-157.0) DW
38 38 38 38 59
29.0 DW 18.0 DW 52.0 DW
39 39 39
Eelgrass, Zostera marina Leaf Rhizome Root Stem Baja California, Mexico; whole; March 2000; reference site vs. salt mining site Oregon Leaf Rhizome Root
Reference
a
Values are in mg Zn/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Young and Langille, 1958; 2, Munda, 1978; 3, Lowman et al., 1970; 4, Agadi et al., 1978; 5, Pillai, 1956; 6, Sivalingam, 1978b; 7, Ishibashi et al., 1965; 8, Stenner and Nickless, 1974; 9, Stenner and Nickless, 1975; 10, Riley and Roth, 1971; 11, Wolfe, 1974; 12, Myklestad et al., 1978; 13, Melhuus et al., 1978; 14, Haug et al., 1974; 15, Foster, 1976; 16, Black and Mitchell, 1952; 17, Ishibashi et al., 1965; 18, Ishii et al., 1978; 19, Bohn, 1979; 20, Leatherland and Burton, 1974; 21, Bryan and Uysal, 1978; 22, Preston et al., 1972; 23, Ireland, 1973; 24, Butterworth et al., 1972; 25, Wort, 1955; 26, Lytle et al., 1973; 27, Lowman et al., 1966; 28, Horowitz and Presley, 1977; 29, Fujita, 1972; 30, Knauer and Martin, 1973; 31, Van As et al., 1975; 32, Lunde, 1970; 33, Pak et al., 1977; 34, Williams and Murdock, 1969; 35, Harris et al., 1979; 36, Ward et al., 1986; 37, Loring and Asmund, 1989; 38, Brix and Lyngby, 1982; 39, Kaldy, 2006; 40, Zbikowski et al., 2006; 41, Santos et al., 2006; 42, Ruelas-Inzunza and Paez-Osuna, 2006; 43, OrdunaRojas and Longoria-Espinoza, 2006; 44, El Ati-Hellal et al., 2007; 45, Kalesh and Nair, 2006; 46, Zbikowski et al., 2007; 47, Perez et al., 2007; 48, Melville and Pulkownik, 2007; 49, Quan et al., 2007; 50, Silva et al., 2006; 51, Bragato et al., 2006; 52, Alongi et al., 2003; 54, Chen et al., 2003; 55, Zheng and Lin, 1996; 56, Peng et al., 1997; 57, MacFarlane et al., 2003, 58, Zheng et al., 1997; 57, Astorga-Espana et al., 2008; 58, Ruelas-Inzunza and Paez-Osuna, 2008; 59, Marcias-Zamora et al., 2008; 60, Preda and Cox, 2002; 61, Agoramoorthy et al., 2008.
suggested that algal zinc-binding substances, presumably proteinaceous compounds (Parry and Hayward, 1973), are directly accessible to ambient zinc ions in seawater prior to death (Skipnes et al., 1975). Zinc concentrations in field collections of marine algae and macrophytes are usually—but not always—at least several orders of magnitude higher than zinc concentrations of the surrounding seawater (Eisler, 1981). BCFs for Enteromorpha spp. and F. vesiculosus
78 Chapter 2 from the Mediterranean Sea near Tunisia were 9930 and 4980, respectively, and were attributed to harbor activities and urban discharges (El Ati-Hellal et al., 2007). Of 16 species of seaweeds analyzed, at least 3 did not markedly concentrate zinc over ambient seawater levels and only 7 species showed marked concentration (Saenko et al., 1976). In general, zinc concentrations in marine flora were elevated when seawater zinc concentrations were elevated; however, the relation was not linear. Marine flora, especially red and brown algae, are among the most effective marine zinc accumulators. Increasing accumulations of zinc in marine algae were associated with decreasing light intensity, decreasing pH, increasing water temperature, decreasing levels of DDT, and increasing oxygen; ionic zinc was accumulated more readily than other forms (Eisler, 1981). Mean BCFs for three species of marine algae were 1530 in 12 days, 4680 in 34 days, and 16,600 in 140 days (USEPA, 1980c). The maximum net daily accumulation rate for the alga A. nodosum was 1.3 mg Zn/kg FW for whole alga (Eisler, 1980). Season of collection is another important variable governing uptake: zinc concentrations in six species of macrophytes collected from the southwest coast of India between 1999 and 2001 were consistently highest during winter and summer monsoon seasons (Kalesh and Nair, 2006). Zinc interacts with numerous chemicals, often producing greatly different patterns of accumulation, toxicity, and metabolism when compared to zinc alone. For example, cadmium-zinc interactions sometimes act to the organisms’s advantage, and sometimes not, depending on nutritional status and other variables. In the case of marine algae, cadmium promotes the growth of zinc-limited phytoplankton (Price and Morel, 1990). Substitution of trace metals or metalloenzymes could be a common strategy for phytoplankton in trace-metal impoverished environments, such as the ocean, and could result in an effective limitation of phytoplankton growth by several bioactive elements. Thus, zinc-deficient diatoms T. weissflogii can grow at 90% of the maximum rate when supplied with cadmium, which substitutes for zinc in certain macromolecules; a similar case is made for cobalt, although less efficiently when compared to cadmium (Price and Morel, 1990). Zinc is almost certainly required for normal growth and metabolism of all marine organisms, including the flora. Zinc deficiency in algae is associated with growth inhibition. For example, T. weissflogii grows best in the range 0.0007-0.065 mg Zn/L, but not at all at less than 0.0007 mg Zn/L (Anderson et al., 1978). In the diatom P. tricornutum, growth stimulation was observed at 0.08-0.31 mg Zn/L and growth inhibition at 5.4 mg Zn/L (Horvatic and Persic, 2007). Adverse effects of zinc—including growth reduction, altered lipid metabolism, and photosynthesis inhibition—were reported in sensitive species of algae at 0.005-0.01 mg Zn/L for Schroederella and Thalassiosira and 0.05-0.1 mg Zn/L for Amphidinium, Skeletonema,
Algae and Macrophytes 79 and others (Braek et al., 1976; Eisler, 2000a; Malea et al., 2006; Spear, 1981; USEPA, 1980c, 1987). However, many species of algae are comparatively resistant to elevated zinc levels of 1.0-2.0 mg Zn/L, and higher (Eisler, 2000a; Stromgren, 1979; USEPA, 1980c, 1987). Specific effects of zinc on sensitive species of marine algae are documented at 0.00880.0095 mg/L (altered lipid metabolism and BCF of 10,770 in 140 days of brown macroalgae F. serratus; USEPA, 1987); at 0.015-0.025 mg/L (photosynthesis reduction in Rhizoselenia sp.; Spear, 1981); 0.019 mg/L (50% growth reduction in 48-96 h of the diatom Schroederella schroederi; USEPA, 1987); 0.02 mg/L (chlorophyll reduction of 65% in 2 days in the dinoflagellate Glenodinium halli; USEPA, 1987); 0.05-0.1 mg/L (growth reduced 23% in 15 days of the diatom S. costatum; USEPA, 1987); 0.065 mg/L (BCF of 255 in 6 days of green macroalgae U. lactuca; USEPA, 1987); 0.1 mg/L (growth inhibition of Glenodinium splendens in 38 days and 5 other species in 48 h; Spear, 1981; USEPA, 1987); 0.1 mg/L (growth stimulation of the diatom Nitzschia longissima during exposure for 1-5 days; USEPA, 1987); and 0.25 mg/L (decreased growth rate of brown alga A. nodosum in 10 days; USEPA, 1987). Unlike algae, submerged macrophytes play a minor role in cycling zinc (Lyngby et al., 1982). Rooted aquatic macrophytes may participate in heavy metal cycling in the aquatic environment either as a source or as a sink; however, studies with eelgrass, Z. marina, show that zinc exchange between the water and sediment is negligible (Lyngby et al., 1982). Although most species of marine algae and macrophytes are not adversely affected at less than 1.4 mg Zn/L (Eisler, 2000a), others show varying degrees of resistance. To protect sensitive species of algae and other marine life, the United States Environmental Protection Agency recommends that total recoverable zinc in seawater should average less than 0.056 mg/L and never exceed 0.17 mg/L (USEPA, 1980a); for acid-soluble zinc, these values are 0.086 and 0.095 mg/L, respectively (USEPA, 1987). More recently, saltwater zinc criteria were set at less than 0.081 mg Zn/L (USEPA, 1999). However, as shown earlier, several sensitive species of marine plants are adversely affected at zinc concentrations between 0.009 and 0.05 mg Zn/L, or significantly below the proposed criteria for marine life protection (Eisler, 2000a; Spear, 1981; USEPA, 1987).
2.42 Zirconium Zirconium concentrations in Gymnodinium brevis, the dinoflagellate associated with “red tide” blooms in the Gulf of Mexico and elsewhere, contained 10.0-100.0 mg Zr/kg DW (Collier, 1953). Diatoms from the Black Sea contained up to 50.0 mg Zr/kg AW (Vinogradova and Koual’skiy, 1962). U. pertussa accumulated up to 41% of all 95Zr after exposure for 14 days in solutions containing radiozirconium-95 (Nakamura et al., 1977).
80 Chapter 2
2.43 Literature Cited Abalde, J., Aid, A., Reisiz, S., Torres, E., Herrero, C., 1995. Response of the marine macroalga Dunaliella tertiolecta (Chlorophycea) to copper toxicity in short time experiments. Bull. Environ. Contam. Toxicol. 54, 317–324. Abbott, O.J., 1977. The toxicity of ammonium molybdate to marine invertebrates. Mar. Pollut. Bull. 8, 204–205. Agadi, V.V., Bhosle, N.B., Untawale, A.G., 1978. Metal concentration in some seaweeds of Goa (India). Botanica Marina 21, 247–250. Agoramoorthy, G., Chen, F.A., Hsu, M.J., 2008. Threat of heavy metal pollution in halophytic and mangrove plants of Tamil Nadu, India. Environ. Pollut. 155, 320–326. Ahsanullah, M., Williams, A.R., 1991. Sublethal effects and bioaccumulation of cadmium, chromium, copper and zinc in the marine amphipod Allorchestes compressa. Mar. Biol. 108, 59–65. Almeida, C.M.R., Mucha, A.P., Vasconcelos, M.T.S.D., 2006. Variability of metal contents in the sea rush Juncus maritimus-estuarine sediment system through one year of plant’s life. Mar. Environ. Res. 61, 424–438. Almeida, C.M.R., Mucha, A.P., Bordalo, A.A., Vasconcelos, M.T.S.D., 2008. Influence of a salt marsh plant (Halimione portulacoides) on the concentrations and potential mobility of metals in sediments. Sci. Total Environ. 403, 188–195. Almela, C., Clemente, M.J., Velez, D., Montoro, R., 2006. Total arsenic, lead and cadmium contents in edible seaweeds sold in Spain. Food Chem. Toxicol. 44, 1901–1908. Alongi, D.M., Clough, B.F., Dixon, P., Tirendi, F., 2003. Nutrient partitioning and storage in arid-zone forests of the mangroves Rhizophora stylosa and Avicennia marina. Trees 17, 51–60. Alvarez-Legorreta, T., Mendoza-Cozatl, D., Moreno-Sanchez, R., Gold-Bouchot, G., 2008. Thiol peptides induction in the seagrass Thalassia testudinum (Banks ex Konig) in response to cadmium exposure. Aquat. Toxicol. 86, 12–19. Amiard-Triquet, C., Berthet, B., Joux, L., Perrein-Ettajani, H., 2006. Significance of physicochemical forms of storage in microalgae in predicting copper transfer to filter-feeding oysters (Crassostrea gigas). Environ. Toxicol. 21, 1–7. Ancellin, J., Bovard, P., 1971. Observations concernant les contaminations experimentales et les contaminations “in situ” d’especes marine par le ruthenium 106. Rev. Int. Oceanogr. Med. 21, 85–92. Ancellin, J., Vilquin, A., 1968. Nouvelles etudes de contaminations experimentales d’especes marines par le cesium 137, le ruthenium 106 et le cerium 144. Radioprotection 3, 185–213. Ancellin, J., Bovard, P., Vilquin, A., 1967. In: New studies on experimental contamination of marine species by ruthenium-106. Actes du Congres Int. sur la Radioprotection du Milieu. Soc. Franc. de Radioprot, Toulouse, France, 14-16 January, 1967, pp. 213–214. Anderson, M.A., Morel, F.M.M., Guillard, R.R.L., 1978. Growth limitation of a coastal diatom by low zinc ion activity. Nature 276, 70–71. Andrade, S., Medina, M.H., Moffett, J.W., Correa, J.A., 2006. Cadmium-copper antagonism in seaweeds inhabiting coastal areas affected by copper mine waste disposals. Environ. Sci. Technol. 40, 4382–4387. Antia, N.J., Cheng, J.Y., 1975. Culture studies on the effects from borate pollution on the growth of marine phytoplankters. J. Fish. Res. Board Can. 32, 2487–2494. Argese, E., Bettiol, C., Ghirardini, A.V., Fasolo, M., Giurin, G., Ghetti, P.F., 1998. Comparison of in vitro submitochondrial particle and Microtox assays for determining the toxicity of organotin compounds. Environ. Toxicol. Chem. 17, 1005–1012. Astorga-Espana, M.S., Calisto-Ulloa, N.C., Guerrero, S., 2008. Baseline concentrations of trace metals in macroalgae from the Strait of Magellan, Chile. Bull. Environ. Contam. Toxicol. 80, 97–101. Augier, H., Gilles, G., Ramonda, G., 1978a. Studies on the mercury content in the thallus and in a commercial product of agricultural use of the brown algae Ascophyllum nodosum (Linne) Le Jois manufactured in Brittany. Botanica Marina 21, 41–416. Augier, H., Gilles, G., Ramonda, G., 1978b. Recherche sur la pollution mercurielle du milieu maritime dans le region de Marseille (Mediterranee, France): Partie 1. Degre de contamination par le mercure de la phanerograme marine Posidonia oceanica delile a proximite du complexe portuaire et dans le zone de reject due grand collecteur d’egouts de la ville de Marseille. Environ. Pollut. 17, 269–285.
Algae and Macrophytes 81 Azam, R., Hemmingsen, B.B., Volcani, B.E., 1973. Germanium incorporation into the silica of diatom cell walls. Arch. Microbiol. 92, 11–20. Bao, V.W.W., Leung, K.M.Y., Kwok, K.W.H., Zhang, A.Q., Lui, G.C.S., 2008. Synergistic toxic effects of zinc pyrithione and copper to three marine species: implications on setting appropriate water quality criteria. Mar. Pollut. Bull. 57, 616–623. Baptist, J.P., Lewis, C.W., 1969. Transfer of 65Zn and 51Cr through an estuarine food chain. In: Proceedings 2nd National Symposium on Radioecology. US Atomic Enerergy Community, Conference 670503, pp. 420–430. Bargagli, R., Monaci, F., Sanchez-Hernandez, J.C., Cateni, D., 1998. Biomagnification of mercury in an Antarctic marine coastal food web. Mar. Ecol. Prog. Ser. 169, 65–76. Baroli, M., Cristini, A., Cossu, A., De Falco, G., Gzale, V., Pergent-Martini, C., et al., 2001. Concentrations of trace metals (Cd, Cu, Fe, Pb) in Posidonia oceanica seagrass of Liscia Bay, Sardinia (Italy). In: Faranda, G.L., Guglielmo, G.L., Spezie, G. (Eds.), Mediterranean Ecosystems: Structures and Processes. Springer-Verlag, Milano, Italy, pp. 95–99. Beaumont, A.R., Newman, P.B., 1986. Low levels of tributyltin reduce growth of marine micro-algae. Mar. Pollut. Bull. 17, 457–461. Benson, A.A., 1984. Phytoplankton solved the arsenate-phosphate problem. In: Holm-Hansen, O., Bolis, R., Giles, R. (Eds.), Lecture Notes on Coastal and Estuarine Ecology. 8. Marine Phytoplankton and Productivity. Springer-Verlag, Berlin, pp. 55–59. Bentley-Mowat, J.A., Reid, S.M., 1977. Survival of marine phytoplankton in high concentrations of heavy metals, and uptake of copper. J. Exp. Mar. Biol. Ecol. 16, 249–264. Berland, D.R., Bonin, D.J., Kapkov, V.I., Maestrini, S.Y., Arlhac, D.P., 1976. Action toxique de quatre metaux lourds sur la croissance d’algues unicellulaires marines. CR Acad. Sci. Paris 282D, 633–636. Berland, B.R., Bonin, D.J., Guerin-Ancey, O.J., Kapkov, V.I., Arlhac, D.P., 1977. Action de metaux lourds a des doses subletales sur les caracteristiques de la croisssance chez la diatomee. Skeletonema costatum. Mar. Biol. 42, 17–30. Bernhard, M., Zattera, A., 1975. Major pollutants in the marine environment. In: Pearson, E.A., Frangipane, E.D. (Eds.), Marine Pollution and Marine Waste Disposal. Pergamon Press, Elmsford, NY, pp. 195–300. Besser, J.M., Canfield, T.J., La Point, T.W., 1993. Bioaccumulation of organic and inorganic selenium in a laboratory food chain. Environ. Toxicol. Chem. 12, 57–72. Besser, J.M., Huckins, J.N., Clark, R.C., 1994. Separation of selenium species released from Se-exposed algae. Chemosphere 29, 771–780. Black, W.A.P., Mitchell, R.L., 1952. Trace elements in the common brown algae and in seawater. J. Mar. Biol. Assoc. UK 30, 575–584. Blake, N.J., Johnson, D.L., 1976. Oxygen production-consumption of the pelagic Sargassum community in a flow-through system with arsenic additions. Deep Sea Res. 23, 773–778. Blankenship, M.L., Wilbur, E.M., 1975. Cobalt effects on cell division and calcium uptake in the coccolithophorid Cricosphaera carterae (Haptophyceae). J. Phycol. 11, 211–219. Bohm, E.L., 1972. Concentration and distribution of Al, Fe, and Si in the calcareous alga, Halimeda opuntia (L) (Chlorophyta, Udoteaceae). Int. Rev. Ges. Hydrobiol. 57, 631–636. Bohm, E.L., 1973. Studies on the mineral content of calcareous algae. Bull. Mar. Sci. 23, 177–190. Bohn, A., 1979. Trace metals in fucoid algae and purple sea urchins near a high Arctic lead/zinc ore deposit. Mar. Pollut. Bull. 10, 325–327. Boisson, F., Gnassia-Barelli, M., Romeo, M., 1995. Toxicity and accumulation of selenite and selenate in the unicellular marine alga Cricosphaera elongata. Arch. Environ. Contam. Toxicol. 28, 487–493. Boney, A.D., 1971. Sub-lethal effects of mercury on marine algae. Mar. Pollut. Bull. 2, 69–71. Boney, A.D., 1978. Marine algae as collectors of iron ore dust. Mar. Pollut. Bull. 9, 175–180. Boney, A.D., Corner, E.D.S., 1959. Application of toxic agents in the study of the ecological resistance of intertidal red algae. J. Mar. Biol. Assoc. UK 38, 267–275. Boney, A.D., Corner, E.D.S., Sparrow, B.W.P., 1959. The effects of various poisons on the growth and viability of sporelings of the red alga Plumaria elegans (Bonnem). Biochem. Pharmacol. 2, 37–49.
82 Chapter 2 Borowitzka, L.J., Volcani, B.E., 1977. Role of silicon in diatom metabolism. Arch. Microbiol. 112, 147–152. Bottino, N.R., Newman, R.D., Cox, E.R., Stockton, R., Hoban, M., Zingaro, R.A., et al., 1978. The effects of arsenate and arsenite on the growth and morphology of the marine unicellular algae Tetraselmis chui (Chlorophyta) and Hymenomonas carterae (Chrysophyta). J. Exp. Mar. Biol. Ecol. 33, 153–168. Braek, G.S., Jensen, A., Mohus, A., 1976. Heavy metal tolerance of marine phytoplankton. III. Combined effects of copper and zinc ions on cultures of four common species. J. Exp. Mar. Biol. Ecol. 25, 37–50. Braek, G.S., Malnes, D., Jensen, A., 1980. Heavy metal tolerance of marine phytoplankton. IV. Combined effect of zinc and cadmium on growth and uptake in some marine diatoms. J. Exp. Mar. Biol. Ecol. 42, 39–54. Bragato, C., Brix, H., Malagoli, M., 2006. Accumulation of nutrients and heavy metals in Phragmites australis (Cav.) Tri. ex Steudel and Bolboschoenus maritimus (L.) Palla in a constructed wetland of the Venice lagoon watershed. Environ. Pollut. 144, 967–975. Brix, H., Lyngby, J.E., 1982. The distribution of cadmium, copper, lead, and zinc in eelgrass (Zostera marina L.). Sci. Total Environ. 24, 51–63. Brown, D.H., Smith, W.E., 1980. The chemistry of the gold drugs used in the treatment of rheumatoid arthritis. Chem. Soc. Rev. 9, 217–240. Bryan, G.W., Hummerstone, L.G., 1973. Brown seaweed as an indicator of heavy metals in estuaries in southwest England. J. Mar. Biol. Assoc. UK 53, 705–720. Bryan, G.W., Uysal, H., 1978. Heavy metals in the burrowing bivalve Scrobicularia plana from the Tamar estuary in relation to environmental levels. J. Mar. Biol. Assoc. UK 58, 89–108. Burger, J., Gochfeld, M., Jeitner, C., Burke, S., Stamm, T., Snigaroff, R., et al., 2007. Mercury levels and potential risk from subsistence foods from the Aleutians. Sci. Total Environ. 384, 93–105. Butterworth, J., Lester, P., Nickless, G., 1972. Distribution of heavy metals in the Severn estuary. Mar. Pollut. Bull. 3, 72–74. Cairrao, E., Pereira, M.J., Pastorinho, M.R., Morgado, F., Soares, A.M.V.M., Guilhermano, L., 2007. Fucus spp. as a mercury contamination bioindicator in coastal areas (northwestern Portugal). Bull. Environ. Contam. Toxicol. 79, 388–395. Cardwell, R.D., Sheldon, A.W., 1986. A risk assessment concerning the fate and effects of tributyltins in the aquatic environment. In: Maton, G.L. (Ed.), Proceedings Oceans 86 Conference, Washington, DC, September 23-25, 1986, vol. 4, Organotin Symposium, pp. 1117–1129. Available from Marine Technology Society, Florida Avenue, Washington, DC. Champ, M.A., 1986. Organotin symposium: introduction and review. In: Maton, G.L. (Ed.), Proceedings Oceans 86 Conference, Washington, DC, September 23-25, 1986, vol. 4, Organotin Symposium, 1093–1100. Available from Marine Technology Society, Florida Avenue, Washington, DC. Chau, Y.K., Kulikovsky-Cordeiro, O.T.R., 1995. Occurrence of nickel in the Canadian environment. Environ. Res. 3, 95–120. Chau, Y.K., Riley, J.P., 1965. The determination of selenium in sea water, silicates and marine organisms. Anal. Chim. Acta 33, 36–49. Chen, X.Y., Tsang, E.P.K., Chan, A.L.W., 2003. Heavy metal contents in sediments, mangroves and bivalves from Ting Kok, Hong Kong. China Environ. Sci. 23, 480–484. Chigbo, F.E., Smith, R.W., Shore, F.L., 1982. Uptake of arsenic, cadmium, lead and mercury from polluted waters by the water hyacinth Eichornia crassipes. Environ. Pollut. 27A, 31–36. Chiles, T.C., Pendoley, P.D., Laughlin Jr., R.B., 1989. Mechanisms of tri-n-butyltin accumulation by marine phytoplankton. Can. J. Fish. Aquat. Sci. 46, 859–862. Clendenning, K.A., North, W.J., 1959. Effects of wastes on the giant kelp, Macrocystis pyrifera. In: Pearson, E.A. (Ed.), Proceedings of the 1st Conference on Waste Disposal in the Marine Environment, Berkeley, CA, pp. 82–91. Cocoros, G.P., Cahn, H., Siler, W., 1973. Mercury concentrations in fish, plankton and water from three western Atlantic estuaries. J. Fish Biol. 5, 641–647. Collier, A., 1953. Titanium and zirconium in bloom of Gymnodinium breve Davis. Science 118, 328. Connell, D.B., Sanders, J.G., Reidel, G.F., Abbe, G.R., 1991. Pathways of silver uptake and trophic transfer in estuarine organisms. Environ. Sci. Technol. 25, 921–924.
Algae and Macrophytes 83 Coppellotti, O., 1989. Glutathione, cysteine, and acid-soluble thiol levels in Euglena gracilis cells exposed to copper and cadmium. Comp. Biochem. Physiol. 94C, 35–40. Cossa, D., 1976. Sorption du cadmium par une population de la diatomee Phaeodactylum tricornutum en culture. Mar. Biol. 34, 163–167. Culkin, F., Riley, J.P., 1958. The occurrence of gallium in marine organisms. J. Mar. Biol. Assoc. UK 37, 607–615. Cullen, W., Reimer, K.J., 1989. Arsenic speciation in the environment. Chem. Rev. 89, 713–764. Custer, T.W., Mitchell, C.A., 1993. Trace elements and organochlorines in the shoalgrass community of the lower Laguna Madre, Texas. Environ. Monit. Assess. 25, 235–246. Dahab, O.A., Khalil, A.N., Halim, Y., 1990. Chromium fluxes through Mex Bay inshore waters. Mar. Pollut. Bull. 21, 68–73. Davey, E.W., 1976. Potential roles of metal-ligands in the marine environment. In: Andrew, R.W., Hodson, P.V., Konesewigh, E.E. (Eds.), Toxicity to Biota of Metal Forms in Natural Water, Great Lakes Res. Adv. Bd., Stand. Comm. Sci. Basis Water Qual. Criteria, Inter. Jt. Comm. Res. Adv. Bd, pp. 197–209. Davey, E.W., Morgan, M.J., Erickson, S.J., 1973. A biological measurement of the copper complexation capacity of seawater. Limnol. Oceanogr. 18, 993–997. Davies, A.G., 1967. In: Studies on the accumulation of radio-iron by a marine diatom. Proceedings of an International Symposium on Radioecological Concentration Processes, Stockholm, 1966, pp. 983–991. Davies, A.G., 1970. Iron, chelation and the growth of marine phytoplankton. I. Growth kinetics and chlorophyll production in cultures of the euryhaline flagellate Dunaliella tertiolecta under iron-limiting conditions. J. Mar. Biol. Assoc. UK 50, 65–86. Davies, A.G., 1974. The growth kinetics of Isochrysis galbana in cultures containing sublethal concentrations of mercuric chloride. J. Mar. Biol. Assoc. UK 54, 157–169. Davies, A.G., 1976. An assessment of the basis of mercury tolerance in Dunaliella tertiolecta. J. Mar. Biol. Assoc. UK 56, 39–57. Delcourt, A., Mestre, J.C., 1978. The effects of phenylmercuric acetate on the growth of Chlamydomonas variabilis Dang. Bull. Environ. Contam. Toxicol. 20, 145–148. Demayo, A., Taylor, M.C., Taylor, K.W., Hodson, P.V., 1982. Toxic effects of lead and lead compounds on human health, aquatic life, wildlife, plants, and livestock. CRC Crit. Rev. Environ. Control 12, 257–305. Denton, G.R.W., Concepcion, L.R., Wood, H.R., Morrison, R.J., 2006. Trace metals in marine organisms from four harbours in Guam. Mar. Pollut. Bull. 52, 1784–1804. Di Giulio, R.T., Scanlon, P.F., 1985. Heavy metals in aquatic plants, clams, and sediments from the Chesapeake Bay, U.S.A. Implications for waterfowl. Sci. Total Environ. 41, 259–274. Donard, O.X.F., Short, F.T., Weber, J.H., 1987. Regulation of tin and methyltin compounds by the green alga Enteromorpha under simulated estuarine conditions. Can. J. Fish. Aquat. Sci. 44, 140–145. Dongmann, G., Nurnberg, H.W., 1982. Observations with Thalassiosira rotula (Menier) on the toxicity and accumulation of cadmium and nickel. Ecotoxicol. Environ. Safety 6, 535–544. Drbal, K., Elster, J., Komarek, J., 1992. Heavy metals in water, ice and biological material from Spitsbergen, Svalbard. Polar Res. 11, 99–101. Dunstan, W.M., Windom, H.L., McIntire, G.L., 1975. The role of Spartina alterniflora in the flow of lead, cadmium and copper through the salt-marsh ecosystem. In: Howell, F.G., Gentry, J.B., Smith, M.H. (Eds.), Mineral Cycling in Southeastern Ecosystems. US Energy Res. Dev. Admin. CONF-740513, pp. 250–256. Edgington, D.N., Gordon, S.A., Thommus, M.M., Almodovar, L.R., 1970. The concentration of radium, thorium, and uranium by tropical marine algae. Limnol. Oceanogr. 15, 945–955. Edmonds, J.S., Francesconi, K.A., Stick, R.V., 1993. Arsenic compounds from marine organisms. Nat. Prod. Rep. 10, 421–428. Eide, I., Jensen, A., 1979. Application of in situ cage cultures of phytoplankton for monitoring heavy metal pollution in two Norwegian fjords. J. Exp. Mar. Biol. Ecol. 37, 271–286. Eisler, R., 1979. Copper accumulations in coastal and marine biota. In: Nriagu, J.O. (Ed.), Copper in the Environment, Part I: Ecological Cycling. John Wiley, New York, pp. 383–449.
84 Chapter 2 Eisler, R., 1980. Accumulation of zinc by marine biota. In: Nriagu, J.O. (Ed.), Zinc in the Environment. Part II. Health Effects. John Wiley, New York, pp. 259–351. Eisler, R., 1981. In: Trace Metal Concentrations in Marine Organisms. Pergamon Press, Elmsford, NY, 687 pp. Eisler, R., 1987. Mercury hazards to fish, wildlife, and invertebrates: a synoptic review. US Fish Wildl. Serv. Biol. Rep. 85 (1.10), 1–90. Eisler, R., 2000. Arsenic. In: Handbook of Chemical Risk Assessment. Health Hazards to Humans, Plants, and Animals, vol. 3. Lewis Publishers, Boca Raton, FL, pp. 1501–1566. Eisler, R., 2000a. Zinc. In: Handbook of Chemical Risk Assessment. Health hazards to Humans, Plants, and Animals, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 605–714. Eisler, R., 2000b. Molybdenum. In: Handbook of Chemical Risk Assessment. Health Hazards to Humans, Plants, and Animals, vol. 3. Lewis Publishers, Boca Raton, FL, pp. 1613–1647. Eisler, R., 2000c. Chromium. In: Handbook of Chemical Risk Assessment. Health Hazards to Humans, Plants, and Animals, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 45–92. Eisler, R., 2000d. Nickel. In: Handbook of Chemical Risk Assessment. Health Hazards to Humans, Plants, and Animals, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 411–497. Eisler, R., 2000e. Silver. In: Handbook of Chemical Risk Assessment. Health Hazards to Humans, Plants, and Animals, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 499–550. Eisler, R., 2000f. Tin. In: Handbook of Chemical Risk Assessment. Health Hazards to Humans, Plants, and Animals, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 551–603. Eisler, R., 2000g. Copper. In: Handbook of Chemical Risk Assessment. Health Hazards to Humans Plants and Animals, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 93–200. Eisler, R., 2004. Biogeochemical, Health, and Ecotoxicological Perspectives on Gold and Gold Mining. CRC Press, Boca Raton, FL, 355 pp. Eisler, R., 2006. Mercury Hazards to Living Organisms. CRC Press, Boca Raton, FL, 312 pp. El Ati-Hellal, M., Hedhili, A., Dachraoui, M., 2007. Contents of trace metals in water and macroalgae along the Mediterranean coast of Tunisia. Bull. Environ. Contam. Toxicol. 78, 33–37. Erickson, S.J., 1972. Toxicity of copper to Thalassiosira pseudonana in unenriched inshore seawater. J. Phycol. 8, 318–323. Erickson, S.J., Lackie, N., Maloney, T., 1970. A screening technique for estimating copper toxicity to estuarine phytoplankton. J. Water Pollut. Control Fed. 42 (8), Part 2, R270–R278. Fang, S.C., 1973. Uptake and biotransformation of phenylmercuric acetate by aquatic organisms. Arch. Environ. Contam. Toxicol. 1, 18–26. Faraday, W.E., Churchill, A.C., 1979. Uptake of cadmium by the eelgrass Zostera marina. Mar. Biol. 53, 293–298. Farias, S., Smichowski, P., Velez, D., Montoro, R., Curtosi, A., Vodopivez, C., 2007. Total and inorganic arsenic in Antarctic macroalgae. Chemosphere 69, 1017–1024. Favero, N., Cattalini, F., Bertaggia, D., Albergoni, V., 1996. Metal accumulation in a biological indicator (Ulva rigida) from the lagoon of Venice (Italy). Arch. Environ. Contam. Toxicol. 31, 9–18. Fisher, N.S., Reinfelder, J.R., 1995. The trophic transfer of metals in marine systems. In: Tessier, A., Turner, D.R. (Eds.), Metal Speciation and Bioavailability in Aquatic Systems. John Wiley & Sons, New York, pp. 363–406. Fisher, N.S., Bohe, M., Teyssie, J.L., 1984. Accumulation and toxicity of Cd, Zn, Ag, and Hg in four marine phytoplankters. Mar. Ecol. Prog. Ser. 18, 201–213. Foster, P., 1976. Concentrations and concentration factors of heavy metals in brown algae. Environ. Pollut. 10, 45–53. Fourqurean, J.W., Marba, N., Duarte, C.M., Diaz-Almela, E., Ruiz-Halpern, S., 2007. Spatial and temporal variation in the elemental and stable isotopic content of the seagrasses Posidonia oceanica and Cymodocea nodosa from the Illes Balears, Spain. Mar. Biol. 151, 219–232. Freeman, M.C., 1985. The reduction of arsenate to arsenite by an Anabaena bacteria assemblage isolated from the Waikato River. NZ J. Mar. Freshw. Res. 19, 277–282.
Algae and Macrophytes 85 Friberg, L., Boston, P., Nordberg, G., Piscator, M., Robert, K.H., 1975. Molybdenum: a toxicological appraisal. US Environ. Protect. Agen. Rep. 600/1-75-004, 142 pp. Froelich, P.N., Kaul, L.W., Byrd, J.T., Andreas, M.O., Roe, K.K., 1985. Arsenic, barium, germanium, tin, dimethylsulfide and nutrient biogeochemistry in Charlotte Harbor, Florida, a phosphorus-enriched estuary. Estuar. Coast. Shelf Sci. 20, 239–264. Fuhrman, J.A., Chisholm, S.W., Guillard, R.R.L., 1978. Marine alga Platymonas sp. accumulates silicon without apparent requirement. Nature 272, 244–246. Fujita, T., 1971. Concentration of major chemical elements in marine plankton. Geochem. J. 4, 143–156. Fujita, T., 1972. The zinc content in marine plankton. Rec. Oceangr. Works Jpn. 11 (2), 73–79. Fukai, R., 1965. Analysis of trace amounts of chromium in marine organisms by the isotope dilution of Cr-51. In: Radiochemical Methods of Analysis. International Atomic Energy Agency, Vienna, pp. 335–351. Fukai, R., Broquet, D., 1965. Distribution of chromium in marine organisms. Bull. Inst. Oceanogr. 65 (1336), 1–19. Fukai, R., Meinke, W.W., 1959. Some activation analyses of six trace elements in marine biological ashes. Nature 184, 815–816. Fukai, R., Meinke, W.W., 1962. Activation analyses of vanadium, arsenic, molybdenum, tungsten, rhenium, and gold in marine organisms. Limnol. Oceanogr. 7, 186–200. Fukai, R., Suzuki, H., Watanake, K., 1962. Strontium-90 in marine organisms during the period 1857-1961. Bull. Inst. Oceanogr. Monaco 1251, 1–16. Gambrell, R.P., Collard, V.R., Reddy, C.N., Patrick Jr., W.H., 1977. Trace and toxic metal uptake by marsh plants as affected by Eh, pH, and salinity. Dredged Mat. Res. Prog. Tech. Rep. D-77-40. U.S. Army Corps Engineer Waterways Experiment Station, Vicksburg, MS, pp. 1–124. Gardner, W.S., Windom, H.L., Stephens, J.A., Taylor, F.E., Stickney, R.R., 1975. Concentrations of total mercury in fish and other coastal organisms: implications to mercury cycling. In: Howell, F.G., Gentry, J. B., Smith, M.H. (Eds.), Mineral Cycling in Southeastern Ecosystems. U.S. Energy Res. Dev. Admin. Available as CONF-740513 from NTIS. US Department of Commerce, Springfield, VA, pp. 268–278. Giblin, A.E., Bourg, A., Valiela, I., Teal, J.M., 1980. Uptake and losses of metals in sewage sludge by a New England salt marsh. Am. J. Bot. 67, 1059–1068. Glooschenko, W.A., 1969. Accumulation of 203Hg by the marine diatom Chaetoceros costatum. J. Phycol. 5, 224–226. Gnassi-Barelli, M., Romeo, M., Laumond, F., Pesando, D., 1978. Experimental studies on the relationship between natural copper complexes and their toxicity to phytoplankton. Mar. Biol. 47, 15–19. Goering, J.J., Boisseau, D., Hattori, A., 1977. Effects of copper on silicic acid uptake by a marine phytoplankton population controlled ecosystem pollution experiment. Bull. Mar. Sci. 27, 58–65. Gogate, S.S., Shah, S.M., Unni, C.K., 1975. Strontium, calcium and magnesium contents of some marine algae from the west coast of India. J. Mar. Biol. Assoc. UK 17, 28–33. Goldberg, E.D., 1952. Iron assimilation by marine diatoms. Biol. Bull. 102, 243–248. Greig, R.A., Wenzloff, D., Shelpuk, C., 1975. Mercury concentrations in fish, North Atlantic offshore waters— 1971. Pestic. Monit. J. 9, 15–20. Gryzhankova, L.N., Sayenko, G.N., Karyakin, A.V., Laktionova, N.V., 1973. Concentrations of some metals in the algae of the Sea of Japan. Oceanology 13, 206–210. Gutknecht, J., 1965. Uptake and retention of cesium-137 and zinc-65 by seaweeds. Limnol. Oceanogr. 6, 426–431. Hall Jr., L.W., Pinkney, A.E., 1985. Acute and sublethal effects of organotin compounds on aquatic biota: an interpretive literature evaluation. CRC Crit. Rev. Toxicol. 14, 159–209. Hall, W.S., Pulliam, G.W., 1995. An assessment of metals in an estuarine wetlands ecosystem. Arch. Environ. Contam. Toxicol. 29, 164–173. Hall, A., Fielding, A.H., Butler, M., 1979. Mechanisms of copper tolerance in the marine fouling alga Ectocarpus siliculosis-evidence for an exclusion mechanism. Mar. Biol. 54, 195–199.
86 Chapter 2 Hallacher, L.E., Kho, E.B., Bernard, N.D., Orcutt, A.M., Dudley Jr., W.C., Hammond, T.M., 1985. Distribution of arsenic in the sediments and biota of Hilo Bay, Hawaii. Pac. Sci. 39, 266–273. Hampson, M.A., 1967. Uptake of radioactivity by aquatic plants and location in the cells. I. The effect of pH on the Sr-90 and Y-90 uptake by the green alga Ulva lactuca and the effect of stable yttrium on Y-90 uptake. J. Exp. Bot. 18, 17–53. Hannan, P.J., Wilkniss, P.E., Patouillet, C., Carr, R.A., 1973. Measurements of mercury sorption by algae. US Naval Res. Lab., Washington, DC. Rep. 7628, pp. 1–26. Harris, J.E., Fabris, G.J., Statham, P.J., Tawfik, F., 1979. Biogeochemistry of selected heavy metals in Western Port, Victoria, and use of invertebrates as indicators with emphasis on Mytilus edulis planulatus. Aust. J. Mar. Freshw. Res. 30, 159–178. Harrison, W.G., Renger, E.H., Eppley, R.W., 1978. Controlled ecosystem pollution experiment: effect of mercury on enclosed water columns. VII. Inhibition of nitrogen assimilation and ammonia regeneration by plankton in seawater samples. Mar. Sci. Comm. 4, 13–22. Haug, A., Melsom, S., Omang, S., 1974. Estimation of heavy metal pollution on two Norwegian fjord areas by analysis of the brown alga Ascophyllum nodosum. Environ. Pollut. 7, 179–192. Havens, K.E., 1994. An experimental comparison of the effects of two chemical stressors on a freshwater zooplankton assemblage. Environ. Pollut. 84, 245–251. Hetherington, J.A., Jefferies, D.F., Mitchell, N.T., Pentreath, R.J., Woodhead, D.S., 1976. Environmental and public health consequences of the controlled disposal of transuranic elements to the marine environment. In: Transuranium Nuclides in the Environment. IAEA-SM-199/11. International Atomic Energy Agency, Vienna, pp. 139–154. Hiyama, Y., Shimizu, M., 1964. On the concentration factors of radioactive Cs, Sr, Cd, Zn, and Ce in marine organisms. Rec. Oceangr. Works Jpn. 7(2), 43–77. Hopkins, R., Kain, J.M., 1971. The effect of marine pollutants on Laminaria hyperborea. Mar. Pollut. Bull. 2, 75–77. Horowitz, A., Presley, B.J., 1977. Trace metal concentrations and partitioning in zooplankton, neuston, and benthos from the south texas outer continental shelf. Arch. Environ. Contam. Toxicol. 5, 241–255. Horvatic, J., Persic, V., 2007. The effect of Ni2+, Co2+, Zn2+, Cd2+and Hg2+on the growth rate of marine diatom Phaeodactylum tricornutum Bohlin: microplate growth inhibition test. Bull. Environ. Contam. Toxicol. 79, 494–498. Howarth, R.W., Cole, J.J., 1985. Molybdenum availability, nitrogen limitation, and phytoplankton growth in natural waters. Science 229, 653–655. Hu, H., Zhen, H., Wan, Y., Gao, H., An, W., An, L., et al., 2006. Trophic magnification of triphenyltin in a marine food web of Bohai Bay, North China: comparison to tributyltin. Environ. Sci. Technol. 40, 3142–3147. Ichikawa, R., 1961. On the concentration factors of some important radionuclides in marine food organisms. Bull. Jpn. Soc. Sci. Fish. 27, 66–74. Ireland, M.P., 1973. Result of fluvial zinc pollution on the zinc content of littoral and sublittoral organisms in Cardigan Bay, Wales. Environ. Pollut. 4, 27–35. Irgolic, K.J., Woolson, E.A., Stockton, R.A., Newman, R.D., Bottino, N.R., Zingaro, R.A., et al., 1977. Characterization of arsenic compounds formed by Daphnia magna and Tetraselmis chuii from inorganic arsenate. Environ. Health Perspect. 19, 61–66. Ishibashi, M., Yamamoto, T., 1960. Inorganic constituents in seaweeds. Rec. Oceangr. Works Jpn. 5(2), 55–62. Ishibashi, M., Yamamoto, T., Morii, F., 1962. Chemical studies on the ocean (part 85). Chemical studies on the seaweeds (11). Copper content in seaweeds. Rec. Oceangr. Works Jpn. 6, 157–162. Ishibashi, M., Fujinaga, T., Morii, F., Kanchiku, Y., Kamiyama, F., 1964a. Chemical studies on the ocean (part 94). Chemical studies on the seaweeds (19). Determination of zinc, copper, lead, cadmium and nickel in seaweeds using dithizone extraction and polarographic method. Rec. Oceangr. Works Jpn. 7(2), 33–36. Ishibashi, M., Yamamoto, T., Fujita, T., 1964b. Chemical studies on the ocean (part 93). Chemical studies on the seaweeds (18). Nickel content in seaweeds. Rec. Oceangr. Works Jpn. 7, 25–32.
Algae and Macrophytes 87 Ishibashi, M., Yamamoto, T., Fujita, T., 1964c. Cobalt content in seaweeds. Rec. Oceangr. Works Jpn. 7(2), 17–24. Ishibashi, M., Fujinaga, T., Yamamoto, T., Fujita, T., Watanabe, K., 1965. Zinc and iron in seaweeds. J. Chem. Soc. Jpn. 86, 728–733. Ishii, T., Suzuki, H., Koyanagi, T., 1978. Determination of trace elements in marine organisms-I. Factors for variation of concentration of trace element. Bull. Jpn. Soc. Sci. Fish. 44, 155–162. Jenkins, D.W., 1980a. Biological monitoring of toxic trace metals. Vol. 2. Toxic trace metals in plants and animals of the world. Part 1. US Environ. Protect. Agen. Rep. 600/3-80-090, pp. 30–138. Jenkins, D.W., 1980b. Biological monitoring of toxic trace metals. Vol. 2. Toxic trace metals in plants and animals of the world. Part 3. US Environ. Protect. Agen. Rep. 600/3-80-092, p. 290. Jensen, A., Rystad, B., Melsom, S., 1976. Heavy metal tolerance of marine phytoplankton. II. Copper tolerance of three species in dialysis and batch cultures. J. Exp. Mar. Biol. Ecol. 22, 249–256. Johnson, D.L., Braman, R.S., 1975. The speciation of arsenic and the content of germanium and mercury in members of the pelagic Sargassum community. Deep Sea Res. 22, 503–507. Johnson, D.L., Burke, R.M., 1978. Biological mediation of chemical speciation. II. Arsenate reduction during marine phytoplankton blooms. Chemosphere 8, 645–648. Johnson, H.L., Stauber, J.L., Adams, M.S., Jolley, D.F., 2007. Copper and zinc tolerance of two tropical microalgae after copper acclimation. Environ. Toxicol. 22, 234–244. Jones, R.F., 1960. The accumulation of nitrosyl ruthenium by fine particles and marine organisms. Limnol. Oceanogr. 5, 312–325. Jones, A.M., Jones, Y., Stewart, W.D.P., 1972. Mercury in marine organisms of the Tay region. Nature 238, 164–165. Kaldy, J.E., 2006. Carbon, nitrogen, phosphorus and heavy metal budgets: how large is the eelgrass (Zostera marina L.) sink in a temperate estuary? Mar. Pollut. Bull. 52, 342–353. Kalesh, N.S., Nair, S.M., 2006. Spatial and temporal variability of copper, zinc, and cobalt in marine macroalgae from the southwest coast of India. Bull. Environ. Contam. Toxicol. 76, 293–300. Kamala-Kannan, S., Batvari, B.P.D., Lee, K.J., Kannan, N., Krishnamoorthy, R., Shanthi, K., et al., 2008. Assessment of heavy metals (Cd, Cr and Pb) in water, sediment and seaweed (Ulva lactuca) in the Pulicat Lake, South East India. Chemosphere 71, 1233–1240. Karadjova, I.B., Slaveykova, V.I., Tsalev, D.L., 2008. The biouptake and toxicity of arsenic species on the green microalga Chlorella salina in seawater. Aquat. Toxicol. 87, 264–271. Kasprzak, K.S., 1987. Nickel. Adv. Mod. Environ. Toxicol. 11, 145–183. Kayser, H., 1976. Waste-water assay with continuous algal culture: the effect of mercuric acetate on the growth of some marine dinoflagellates. Mar. Biol. 36, 61–72. Khristoforova, N.R., Bogdanova, N.N., 1980. Mineral composition of seaweeds from coral islands of the Pacific Ocean as a function of environmental conditions. Mar. Ecol. Prog. Ser. 3, 25–29. Khristoforova, N.K., Sin’kov, N.A., Saenko, G.N., Koryakova, M.D., 1976. Contents of the trace elements Fe, Mn, Ni, Cr, Cu and Zn in the proteins of marine algae. Sov. J. Mar. Biol. 2(2), 124–128. Kim, C.Y., 1972. Studies on the contents of mercury, cadmium, lead and copper in edible seaweeds in Korea. Bull. Korean Fish. Soc. 5(3), 88–96. Kim, C.Y., Won, J.H., 1974. Concentrations of mercury, cadmium, lead and copper in the surrounding seawater and in seaweeds, Undaria pinnatifida and Sargassum fulvellum, from Suyeong Bay in Busan. Bull. Korean Fish. Soc. 7, 169–178. Knauer, G.A., Martin, J.H., 1973. Seasonal variations of cadmium, copper, manganese, lead, and zinc in water and phytoplankton in Monterey Bay, California. Limnol. Oceanogr. 18, 597–604. Kniep, T.J., Re, G., Hernandez, T., 1974. Cadmium in an aquatic ecosystem: distribution and effects. In: Hemphill, D.D. (Ed.), Trace Substances in Environmental Health—VIII: Proceedings of University of Missouri’s 8th Annual Conference on Trace Substances in Environmental Health. University of Missouri, Columbia, MO, pp. 173–177.
88 Chapter 2 Koch, I., McPherson, K., Smith, P., Easton, L., Doe, K.G., Reimer, K.J., 2007. Arsenic bioaccessibility and speciation in clams and seaweed from a contaminated marine environment. Mar. Pollut. Bull. 54, 586–594. Koczy, F.F., Titze, H., 1958. Radium content of carbonate shells. J. Mar. Res. 17, 302–311. Kuyucak, N., Volesky, B., 1989. The mechanism of gold biosorption. Biorecovery 1, 219–235. Laevastu, T., Thompson, T.G., 1956. The determination and occurrence of nickel in seawater, marine organisms, and sediments. J. du Conseil 21, 125–143. Lafabrie, C., Pergent, G., Pergent-Martini, C., Capiomont, A., 2007a. Posidonia oceanica: a tracer of past mercury contamination. Environ. Pollut. 148, 688–692. Lafabrie, C., Pergent, G., Kantin, R., Pergent-Martini, C., Gonzalez, J.L., 2007b. Trace metals assessment in water, sediment, mussel and seagrass species—validation of the use of Posidonia oceanica as a metal biomonitor. Chemosphere 68, 2033–2039. Lafabrie, C., Pergent-Martini, C., Pergent, G., 2008a. Metal contamination of Posidonia oceanica meadows along the Corsican coastline (Mediterranean). Environ. Pollut. 151, 262–268. Lafabrie, C., Pergent-Martini, C., Pergent, G., 2008b. First results on the study of metal contamination along the Corsican coastline using Posidonia oceanica. Mar. Pollut. Bull. 57, 155–159. Lande, E., 1977. Heavy metal pollution in Trondheimsfjorden, Norway, and the recorded effects on the fauna and flora. Environ. Pollut. 12, 187–198. Laughlin Jr., R.B., French, W., Guard, H.E., 1986. Accumulation of bis(tributyltin) oxide by the marine mussel Mytilus edulis. Environ. Sci. Technol. 20, 884–890. Laumond, F., Neuburger, M., Donnier, B., Fourcy, A., Bittel, R., Aubert, M., 1973. Experimental investigations, at laboratory, on the transfer of mercury in marine trophic chains. In: 6th International Symposium on Medical Oceanography. Portoroz, Yugoslavia, September 26-30, 1973, pp. 47–53. Leatherland, T.M., Burton, J.D., 1974. The occurrence of some trace metals in coastal organisms with particular reference to the Solent region. J. Mar. Biol. Assoc. UK 54, 457–468. Levy, J.L., Stauber, J.L., Jolley, D.J., 2007. Sensitivity of marine microalgae to copper: the effect of biotic factors on copper adsorption and toxicity. Sci. Total Environ. 387, 141–154. Levy, J.L., Angel, B.M., Stauber, J.L., Poon, W.L., Simpson, S.L., Cheng, S.H., et al., 2008. Uptake and internalisation of copper by three marine macroalgae: comparison of copper-sensitive and copper-tolerant species. Aquat. Toxicol. 89, 82–93. Lewin, J., 1966. Silicon metabolism in diatoms. V. Germanium dioxide, a specific inhibitor of diatom growth. Phycologia 6, 1–12. Lewin, J., Chen, C.H., 1971. Available iron: a limiting factor for marine phytoplankton. Limnol. Oceanogr. 16, 670–675. Lewin, J., Chen, C.H., 1976. Effects of boron deficiency on the chemical composition of a marine diatom. J. Exp. Bot. 27, 916–921. Lindberg, E., Harriss, C., 1974. Mercury enrichment in estuarine plant detritus. Mar. Pollut. Bull. 5, 93–95. Lindsay, D.M., Sanders, J.G., 1990. Arsenic uptake and transfer in a simplified estuarine food chain. Environ. Toxicol. Chem. 9, 391–395. Livingston, H.D., Bowen, V.T., 1976. Americium in the marine environment—relationships to plutonium. In: Miller, M.W., Stannard, J.N. (Eds.), Environmental Toxicity of Aquatic Radionuclides: Models and Mechanisms. Ann Arbor Science Publishers, Ann Arbor, MI, pp. 107–130. Loring, D.H., Asmund, G., 1989. Heavy metal contamination of a Greenland fjord system by mine wastes. Environ. Geol. Water Sci. 14, 61–71. Lowman, F.G., Phelps, D.K., Ting, R.Y., Escalera, R.M., 1966. In: Progress Summary Report No. 4, Marine Biology Program June 1965-June 1966. Puerto Rico Nucl. Cen., Rep. PRNC 85, pp. 1–57. Lowman, F.G., Stevenson, R.A., Escalera, R.M., Ufret, S.L., 1967. The effects of river outflows upon the distribution patterns of fallout radioisotopes in marine organisms. In: Proceedings of an International Symposium on Radioecological Concentration Processes. Stockholm, 1966, pp. 735–752.
Algae and Macrophytes 89 Lowman, F.G., Martin, J.H., Ting, R.Y., Barnes, S.S., Swift, D.J.P., Seiglie, G.A., et al., 1970. Bioenvironmental and radiological-safety feasibility studies, Atlantic-Pacific interoceanic canal. Estuar. Mar. Ecol. I-IV, Prepared for Battelle Memorial Institute, 505 King Avenue, Columbus, OH, contract AT (26-1)-171. Lunde, G., 1970. Analysis of trace elements in seaweed. J. Sci. Food Agric. 21, 416–418. Lunde, G., 1973. The synthesis of fat and water soluble arseno organic compounds in marine and limnetic algae. Acta Chem. Scand. 27, 1586–1594. Lyngby, J.E., Brix, H., Schierup, H.H., 1982. Absorption and translocation of zinc in eelgrass (Zostera marina L.). J. Exp. Mar. Biol. Ecol. 58, 259–270. Lytle, T.F., Lytle, J.S., Parker, P.L., 1973. A geochemical study of a marsh environment. Gulf Res. Rep. 4(2), 214–232. MacFarlane, G.R., Pulkownik, A., Burchett, M.D., 2003. Accumulation and distribution of heavy metals in the grey mangrove, Avicennia marina (Forsk) Vierh.: biological indication potential. Environ. Pollut. 123, 139–151. MacFarlane, G.R., Koller, C.E., Blomberg, S.P., 2007. Accumulation and partitioning of heavy metals in mangroves: a synthesis of field-based studies. Chemosphere 69, 1454–1564. Maclean, F.I., Lucis, O.J., Shakh, Z.Z., Jansz, E.R., 1972. The uptake and subcellular distribution of Cd and Zn in microorganisms. Fed. Proc. Fed. Am. Soc. Exp. Biol. 31, 699. Maddock, B.G., Taylor, D., 1980. The acute toxicity and bioaccumulation of some lead alkyl compounds in marine animals. In: Branica, M., Konrad, Z. (Eds.), Lead in the Marine Environment. Pergamon, Oxford, UK, pp. 233–261. Maeda, S., Nakashima, S., Takeshita, T., Higashi, S., 1985. Bioaccumulation of arsenic by freshwater algae and the application to the removal of inorganic arsenic from the aqueous phase. II. By Chlorella vulgaris isolated from arsenic-polluted environment. Sep. Sci. Technol. 20, 153–161. Maguire, R.J., Wong, P.T.S., Rhamey, J.S., 1984. Accumulation and metabolism of tri-n-butyltin cation by a green alga, Ankistrodesmus falcatus. Can. J. Fish. Aquat. Sci. 41, 537–540. Maher, W.A., 1985. The presence of arsenobetaine in marine animals. Biochem. Physiol. 80C, 199–201. Mahoney, J.B., 1982. The effects of trace metals on growth of a phytoflagellate Olisthodiscus luteus, which blooms in lower New York Bay. Bull. N. J. Acad. Sci. 27, 53–57. Malea, P., Rijstenbil, J.W., Haritondis, S., 2006. Effects of cadmium, zinc and nitrogen on non-protein thiols in the macroalgae Enteromorpha spp. From the Scheldt Estuary (SW Netherlands, Belgium) and Thermaikos Gulf (N Aegean Sea, Greece). Mar. Environ. Res. 62, 45–60. Mandelli, E.F., 1969. The inhibitory effects of copper on marine phytoplankton. Mar. Sci. 14, 47–57. Marchetti, R., 1978. Acute toxicity of alkyl leads to some marine organisms. Mar. Pollut. Bull. 9, 206–207. Marcias-Zamora, J.V., Sanchez-Osorio, J.L., Rios-Mendoza, L.M., Ramirez-Alvarez, N., Huerta-Diaz, M.A., Lopez-Sanchez, D., 2008. Trace metals in sediments and Zostera marina of San Ignacio and Ojo de Liebre Lagoons in the central Pacific coast of Baja California, Mexico. Arch. Environ. Contam. Toxicol. 55, 218–228. Markham, J.W., Kremer, B.P., Sperling, K.R., 1980. Effects of cadmium on Laminaria saccharina in culture. Mar. Ecol. Prog. Ser. 3, 31–90. Martin, J.H., Knauer, G.A., 1973. The elemental composition of plankton. Geochim. Cosmochim. Acta 37, 1639–1653. Matida, Y., Kumada, H., 1969. Distribution of mercury in water, bottom mud and aquatic organisms of Minamata Bay, the River Agano and other water bodies in Japan. Bull. Freshw. Fish. Res. Lab. Tokyo 19(2), 73–93. Matsuto, S., Kasuga, H., Okumoto, H., Takahashi, A., 1984. Accumulation of arsenic in blue-green alga, Phormidium sp. Comp. Biochem. Physiol. 78C, 377–382. Mauchline, J., Templeton, W.L., 1966. Strontium, calcium and barium in marine organisms from the Irish Sea. J. Cons. Perm. Int. Explor. Mer. 30, 161–170. Melhuus, A., Seip, K.L., Seip, M., Myklestad, S., 1978. A preliminary study on the use of benthic algae as biological indicators of heavy metal pollution in Sorfjorden, Norway. Environ. Pollut. 15, 101–107. Melville, F., Pulkownik, A., 2007. Investigation of mangrove macroalgae as biomonitors of estuarine metal contamination. Sci. Total Environ. 387, 301–309.
90 Chapter 2 Miao, A.J., Wang, W.X., 2007. Predicting copper toxicity with its intracellular or subcellular concentration and the thiol synthesis in a marine diatom. Environ. Sci. Technol. 41, 1777–1782. Mills, A.L., Colwell, R.R., 1977. Microbiological effects of metal ions in Chesapeake Bay water and sediment. Bull. Environ. Contamin. Toxicol. 18, 99–103. Miramand, P., Unsal, M., 1978. Acute toxicity of vanadium to some marine benthic and phytoplanktonic species. Chemosphere 10, 827–832. Mitchell, N.T., 1977. Radioactivity in the surface and coastal waters of the British Isles, 1976. Part I. The Irish Sea and its environs. Tech. Rep. Fish. Radiobiol. Lab., MAFF Direct. Fish. Res., (FRL 13), Lowestoft, 15 pp. Montgomery, J.R., Price, M., Thurston, J., de Castro, G.L., Cruz, L.L., Zimmerman, D.D., 1978. Biological availability of pollutants to marine organisms. US Environ. Protect. Agen. Narragansett, Rhode Island Rep. EPA600/3-78-035, 134 pp. Morel, N.M.L., Rueter, J.G., Morel, F.M.M., 1978. Copper toxicity to Skeletonema costatum (Bacillarophyceae). J. Phycol. 14, 43–48. Morelli, E., Fantozzi, L., 2008. Phytochelatins in the diatom Phaeodactylum tricornutum Bohlin: an evaluation of their use as biomarkers of metal exposure in marine waters. Bull. Environ. Contam. Toxicol. 81, 236–241. Morris, O.P., Russell, G., 1974. Inter-specific differences in responses to copper by natural populations of Ectocarpus. Br. Phycol. J. 269–272. Morrison, L., Baumann, H.A., Stengel, D.B., 2008. An assessment of metal contamination along the Irish coast using the seaweed Ascophyllum nodosum (Fucales, Phaeophyceae). Environ. Pollut. 152, 293–303. Munda, I.M., 1978. Trace metal concentrations in some Icelandic seaweeds. Botanica Marina 21, 261–263. Myklestad, S., Eide, I., Melsom, S., 1978. Exchange of heavy metals in Ascophyllum nodosum (L.) Le Jod. in situ by means of transplanting experiments. Environ. Pollut. 16, 277–284. Nakamura, R., Suzuki, Y., Ueda, T., 1977. Distribution of radionuclides among green alga, marine sediments and seawater. J. Radiat. Res. 18, 322–330. Nakazawa, S., 1977. Development of Fucus eggs, as affected by iodine, lithium, and nitroprusside. Bull. Jpn. Soc. Phycol. 25 (Suppl.), 215–220. National Academy of Sciences (NAS), 1975. Medical and Biological Effects of Environmental Pollutants. Nickel. National Research Council, NAS, Washington, DC, 277 pp. NAS, 1977. Arsenic. National Academy of Sciences, Washington, DC, 332 pp. National Research Council of Canada (NRCC), 1978. Effects of Arsenic in the Canadian Environment. Natl. Res. Coun. Canada Publ. No. NRCC 15391, 349 pp. Nelson, D.M., Goering, J.J., 1978. Assimilation of silicic acid by phytoplankton in the Baja California and northwest Africa upwelling systems. Limnol. Oceanogr. 23, 508–517. Nielsen, E.S., Kamp-Nielsen, L., 1970. Influence of deleterious concentrations of copper on the growth of Chlorella pyrenoidosa. Physiol. Plant. 23, 828–840. Nielsen, E.S., Wium-Andersen, S., 1970. Copper ions as poison in the sea and in freshwater. Mar. Biol. 6, 93–97. Nishimura, H., Kumagi, M., 1983. Mercury pollution of fishes in Minamata Bay and surrounding water: analysis of pathway of mercury. Water Air Soil Pollut. 20, 401–411. Noda, K., Hirai, S., Sunayashiki, K., Danbara, H., 1979. Neutron activation analysis of selenium and mercury in marine products along the coast of Shikoku Island. Agric. Biol. Chem. 47, 1381–1386. Norin, H., Vahter, M., Christakopoulos, A., Sandstrom, M., 1985. Concentration of inorganic and total arsenic in fish from industrially polluted water. Chemosphere 14, 325–334. Noro, T., 1978. Effect of Mn on the growth of a marine green alga. Dunaliella tertiolecta. Jpn. J. Phycol. 26, 69–72. Oliver, L.R., Perkins, W.T., Mudge, S.M., 2006. Detection of technetium-99 in Ascophyllum nodosum from around the Welsh coast. Chemosphere 65, 2297–2303. Orduna-Rojas, J., Longoria-Espinoza, R.M., 2006. Metal content in Ulva lactuca (Linnaeus) from Navachiste Bay (Southeast Gulf of California) Sinaloa, Mexico. Bull. Environ. Contam. Toxicol. 77, 574–580. Osterberg, C., Pearcy, W.G., Curl, H.J., 1964. Radioactivity and its relationship to oceanic food chains. J. Mar. Res. 22, 2–12.
Algae and Macrophytes 91 Outridge, P.M., Scheuhammer, A.M., 1993. Bioaccumulation and toxicology of nickel: implications for wild mammals and birds. Environ. Rev. 1, 172–197. Overnell, J., 1976. Inhibition of marine algal photosynthesis by heavy metals. Mar. Biol. 38, 335–342. Paasche, E., 1973a. Silicon and the ecology of marine plankton diatoms. I. Thalassiosira pseudonana (Cyclotella nana) grown in a chemostat with silicate as a limiting nutrient. Mar. Biol. 19, 117–126. Paasche, E., 1973b. Silicon and the ecology of marine plankton diatoms. II. Silicate-uptake kinetics in five diatom species. Mar. Biol. 19, 262–269. Pace, F., Ferrara, R., Del Carratore, G., 1977. Effects of sublethal doses of copper sulfate and lead nitrate on growth and pigment composition of Dunaliella salina Teod. Bull. Environ. Contam. Toxicol. 17, 679–685. Pak, C.K., Yang, K.R., Lee, I.K., 1977. Trace metals in several edible marine algae of Korea. J. Oceanol. Soc. Korea 12, 41–47. Parchevskii, V.P., Polikarpov, G.G., Zabarunova, I.S., 1965. Certain regularities in the accumulation of yttrium and strontium by marine organisms. Dokl. Akad. Nauk. SSSR 164, 913–916. Park, D., Yun, Y.S., Ahn, C.K., Park, J.M., 2007. Kinetics of the reduction of hexavalent chromium with the brown seaweed. Ecklonia biomass. Chemosphere 66, 939–946. Parrish, K.M., Carr, R.A., 1976. Transport of mercury through a laboratory two-level marine food chain. Mar. Pollut. Bull. 7, 90–91. Parry, G.D.R., Hayward., J., 1973. The uptake of 65Zn by Dunaliella tertiolecta Butcher.. J. Mar. Biol. Assn. UK 53, 915–922. Peng, L., Zheng, W., Li, Z., 1997. Distribution and accumulation of heavy metals in Avicennia marina community in Shenzhen, China. J. Environ. Sci. (China) 9, 427–429. Penot, M., Videau, C., 1975. Absorption du 86Rb et du 99Mo par deux algues marines: le Laminaria digitata et le Fucus serratus. Z. Pflanzenphysiol. 76 (Suppl.), 285–293. Penrose, W.R., Black, R., Hayward, M.J., 1975. Limited arsenic dispersion in seawater, sediments, and biota near a continuous source. J. Fish. Res. Board Can. 32, 1275–1281. Perez, A.A., Farias, S.S., Strobl, A.M., Perez, L.B., Lopez, C.M., Pineiro, A., et al., 2007. Levels of essential and toxic elements in Porphyra columbina and Ulva sp. from San Jorge Gulf, Patagonia, Argentina. Sci. Total Environ. 376, 51–59. Pershagen, G., Vahter, M., 1979. Arsenic—A Toxicological and Epidemiological Appraisal. Naturvaardsverket Rapp. SNV PM 1128. Liber Tryck, Stockholm, Sweden, 265 pp. Phelps, D.K., Telek, G., Lapan Jr., R.L., 1975. Assessment of heavy metal distribution within the food web. In: Pearson, E.A., Frangipane, E.D. (Eds.), Marine Pollution and Marine Waste Disposal. Pergamon Press, Elmsford, NY, pp. 341–348. Pillai, V.K., 1956. Chemical studies on Indian seaweeds. I. Mineral constituents. Proc. Indian Acad. Sci. 44(1), Sec. B, 3–29. Pillai, K.C., Smith, R.C., Folsom, T.R., 1964. Plutonium in the marine environment. Nature 203, 568–571. Polikarpov, G.G., 1961. The role of detritus formation in the migration of strontium-90, cesium-137, and cerium144. Experiments with the seaweed Cystoseira barbata. CR Acad. Sci. URSS 136, 921–923 (Nucl. Sci. Abstr. 1961, 15, 1872). Pouvreau, B., Amiard, J.C., 1974. Etude experimentale de l’accumulation de l’argent 110m chez divers organismes marins. Comm. Atom. France, 19 pp. Rep. CEA-R-4571. Preda, M., Cox, M.E., 2002. Trace metal occurrence and distribution in sediments and mangroves, Pumicestone region, southeast Queensland, Australia. Environ. Int. 28, 433–439. Preston, A., Jeffries, D.F., Dutton, J.W.R., Harvey, B.R., Steele, A.K., 1972. British isles coastal waters: the concentrations of selected heavy metals in sea water, suspended matter and biological indicators—a pilot survey. Environ. Pollut. 3, 69–82. Pribil, S., Marvan, P., 1976. Accumulation of uranium by the chlorococcal alga Scenedesmus quadricauda. Arch. Hydrobiol. (Suppl. 49), 214–225. Price, N.M., Morel, F.M.M., 1990. Cadmium and cobalt substitution for zinc in a marine diatom. Nature 344, 658–660.
92 Chapter 2 Quan, W.M., Han, J.D., Shen, A.L., Ping, X.Y., Qian, P.L., Li, C.J., et al., 2007. Uptake and distribution of N, P and heavy metals in three dominant salt marsh macrophytes from Yangtze River estuary, China. Mar. Environ. Res. 64, 21–37. Rao, D.V.S., 1981. Effect of boron on primary productivity of nanoplankton. Can. J. Fish. Aquat. Sci. 38, 52–58. Rao, V.N.R., Govindarajan, S., 1992. Transfer of copper and zinc through a marine food chain. Acta Bot. Indica 20, 71–75. Ratte, H.T., 1999. Bioaccumulation and toxicity of silver compounds: a review. Environ. Toxicol. Chem. 18, 89–108. Reboreda, R., Cacador, I., 2007. Halophyte vegetation influences in salt marsh retention capacity for heavy metals. Environ. Pollut. 146, 147–154. Rice, T.R., 1956. The accumulation and exchange of strontium by marine planktonic algae. Limnol. Oceanogr. 1, 123–138. Rice, T.R., Willis, V.M., 1959. Uptake, accumulation, and loss of radioactive cerium-144 by marine planktonic algae. Limnol. Oceanogr. 4, 277–290. Riekie, G.J., Williams, P.N., Raab, A., Meharg, A.A., 2006. The potential for kelp manufacture to lead to arsenic pollution of remote Scottish islands. Chemosphere 65, 332–342. Riley, J.P., Roth, I., 1971. The distribution of trace elements in some species of phytoplankton grown in culture. J. Mar. Biol. Assoc. UK 51, 63–72. Rivkin, R.B., 1979. Effects of lead on the growth of the marine diatom Skeletonema costatum. Mar. Biol. 50, 239–247. Roberts, D.A., Poore, A.G.B., Johnston, E.L., 2006. Ecological consequences of copper contamination in macroalgae: effects on epifauna and associated herbivores. Environ. Toxicol. Chem. 25, 2470–2479. Robinson, M.G., Brown, L.N., Hall, B.D., 1997. Effect of gold (III) on the fouling diatom Amphora coffeaeformis: uptake, toxicity and interactions with copper. Biofouling 11, 59–79. Romeril, M.G., 1977. Heavy metal accumulation in the vicinity of a desalination plant. Mar. Pollut. Bull. 8, 84–87. Rosemarin, A., Notine, M., Holmgren, K., 1985. The fate of arsenic in the Baltic Sea Fucus vesiculosus ecosystem. Ambio 14, 342–345. Roth, I., Hornung, H., 1977. Heavy metal concentrations in water, sediments and fish from Mediterranean coastal area, Israel. Environ. Sci. Technol. 11, 265–269. Ruelas-Inzunza, J., Paez-Osuna, P., 2006. Trace metal concentrations in different primary producers from AltataEnsenada del Pabellon and Guaymas Bay (Gulf of California). Bull. Environ. Contam. Toxicol. 76, 327–333. Ruelas-Inzunza, J., Paez-Osuna, F., 2008. Trophic distribution of Cd, Pb, and Zn in a food web from Alata-Ensenada del Pabellon subtropical lagoon, SE Gulf of California. Arch. Environ. Contam. Toxicol. 54, 584–596. Russell, G., Morris, O.P., 1970. Copper tolerance in the marine fouling alga Ectocarpus siliculosus. Nature 228, 288–289. Ryndina, D.D., 1976. Accumulation and fixation of radionuclides by algal polysaccharides. Hydrobiol. J. 9, 16–20. Saboski, E.M., 1977. Effects of mercury and tin on frustular ultrastructure of the marine diatom Nitzschia liebethrutti. Water Air Soil Pollut. 8, 461–466. Saenko, G.N., Koryakova, M.D., Makienko, V.F., Dobrosmyslova, I.G., 1976. Concentration of polyvalent metals by seaweeds in Vostok Bay, Sea of Japan. Mar. Biol. 34, 169–176. Saifullah, S.M., 1978. Inhibitory effects of copper on marine dinoflagellates. Mar. Biol. 44, 299–308. Sakaguchi, T., Nakajima, A., Horikoshi, T., 1981. Studies on the accumulation of heavy metal elements in biological systems. Accumulation of molybdenum by green microalgae. Eur. J. Appl. Microbiol. Biotechnol. 12, 84–89. Sanders, J.G., 1978. Enrichment of estuarine phytoplankton by the addition of dissolved manganese. Mar. Environ. Res. 1, 59–66. Sanders, J.G., 1985. Arsenic geochemistry in Chesapeake Bay: dependence upon anthropogenic inputs and phytoplankton species composition. Mar. Chem. 17, 329–340.
Algae and Macrophytes 93 Sanders, J.G., 1986. Direct and indirect effects of arsenic on the survival and fecundity of estuarine zooplankton. Can. J. Fish. Aquat. Sci. 43, 694–699. Sanders, J.G., Abbe, G.R., 1987. The role of suspended sediments and phytoplankton in the partitioning and transport of silver in estuaries. Continent. Shelf Res. 7, 1357–1361. Sanders, J.G., Abbe, G.R., 1989. Silver transport and impact in estuarine and marine systems. In: Suter II, G.W., Lewis, M.A. (Eds.), Aquatic Toxicology and Environmental Fate: Eleventh Volume. Amer. Soc., Testing Mater., Spec. Tech. Publ. 1007, Philadelphia, PA, pp. 5–18. Sanders, J.G., Cibak, S.J., 1988. Response of Chesapeake Bay phytoplankton communities to low levels of toxic substances. Mar. Pollut. Bull. 19, 439–444. Sanders, J.G., Cibik, S.J., 1985. Adaptive behavior of euryhaline phytoplankton communities to arsenic stress. Mar. Ecol. Prog. Ser. 22, 195–205. Sanders, J.G., Osman, R.W., 1985. Arsenic incorporation in a salt marsh ecosystem. Estuar. Coast. Shelf Sci. 20, 387–392. Sanders, J.G., Abbe, G.F., Reidel, G.F., 1990. Silver uptake and subsequent effects on growth and species composition in an estuarine community. Sci. Total Environ. 97/98, 761–769. Sanders, J.G., Riedel, G.F., Abbe, G.R., 1991. Factors controlling the spatial and temporal variability of trace metal concentrations in Crassostrea virginica (Gmelin). In: Elliott, M., Ducrotoy, J.P. (Eds.), Estuaries and Coasts: Spatial and Temporal Comparison. ECSA Sympos. 19 (Univ. Caen, France, 1989). Olsen and Olsen, Fredensborg, Denmark, pp. 335–339. Santos, I.R., Silva-Filho, E.V., Schaefer, C., Sella, S.M., Silva, C.A., Gomes, V., et al., 2006. Baseline mercury and zinc concentrations in terrestrial and coastal organisms of Admiralty Bay, Antarctica. Environ. Pollut. 140, 304–311. Saward, D., Stirling, A., Topping, G., 1975. Experimental studies on the effects of copper on a marine food chain. Mar. Biol. 29, 351–356. Schell, W.R., Nevissi, A., 1977. Heavy metals from waste disposal in Central Puget Sound. Environ. Sci. Technol. 11, 887–893. Schroeder, H.A., Balassa, J.J., Tipton, I.H., 1970. Essential trace metals in man: molybdenum. J. Chronic Dis. 23, 481–499. Schulz-Baldes, M., Lewin, R.A., 1976. Lead uptake in two marine phytoplankton organisms. Biol. Bull. 150, 118–127. Seeliger, U., Edwards, P., 1977. Correlation coefficients and concentration factors of copper and lead in seawater and benthic algae. Mar. Pollut. Bull. 8, 16–19. Seeliger, U., Edwards, P., 1979. Fate of biologically accumulated copper in growing and decomposing thalli of two benthic red marine algae. J. Mar. Biol. Assoc. UK 59, 227–238. Shiber, J., Washburn, E., 1978. Lead, mercury, and certain nutrient elements in Ulva lactuca (Linnaeus) from Ras Beirut, Lebanon. Hydrobiologia 61, 187–192. Short, Z.F., Olson, P.R., Palumbo, R.F., Donaldson, J.R., Lowman, F.G., 1971. Uptake of molybdenum marked with 99Mo, by the biota of Fern Lake, Washington, in a laboratory and field experiment. In: Nelson, D.J. (Ed.), Radionuclides in Ecosystems. Proceedings of the Third National Symposium on Radioecology, vol. 1, Oak Ridge, TN, May 10-12, 1971, pp. 474–485. Sick, L.V., Windom, H.L., 1975. Effects of environmental levels of mercury and cadmium on rates of metal uptake and growth physiology of selected genera of marine phytoplankton. In: Howell, F.G., Gentry, J.B., Smith, M.H. (Eds.), Mineral Cycling in Southeastern Ecosystems. U.S. Energy Res. Dev. Admin., CONF740513, Washington, DC, pp. 239–249. Silva, C.A.R., Smith, B.D., Rainbow, P.S., 2006. Comparative biomonitors of coastal trace metal contamination in tropical South America (N. Brazil). Mar. Environ. Res. 61, 439–455. Sivalingam, P.M., 1978a. Effects of high concentration stress of trace metals on their biodeposition modes in Ulva reticulata forskal. Jpn. J. Phycol. 26, 157–160. Sivalingam, P.M., 1978b. Biodeposited trace metals and mineral content studies of some tropical marine algae. Botanica Marina 21, 327–330.
94 Chapter 2 Sivalingam, P.M., 1980. Mercury contamination in tropical algal species of the Island of Penang, Malaysia. Mar. Pollut. Bull. 11, 106–107. Skei, J.M., Saunders, M., Price, N.B., 1976. Mercury in plankton from a polluted Norwegian fjord. Mar. Pollut. Bull. 7, 34–35. Skipnes, O., Roald, T., Haug, A., 1975. Uptake of zinc and strontium by brown algae. Physiol. Plant. 34, 314–320. Slejkovec, Z., Kapolna, E., Ipolyi, I., van Elteren, J.T., 2006. Arsenosugars and other arsenic compound in littoral zone algae from the Adriatic Sea. Chemosphere 63, 1098–1105. Slowey, J.F., Hayes, D., Dixon, B., Hood, D.W., 1965. Distribution of gamma-emitting radionuclides in the Gulf of Mexico. Occ. Publs. Narragansett Mar. Lab., Univ. Rhode Island, Kingston, Rhode Island, 3, pp. 109–129. Smith, W.G., 1970. Spartina “die-back” on Louisiana marshlands. Coast. Stud. Bull. 5, 89–96. Smyth, D.A., Dugger, W.M., 1980. Effects of boron deficiency on 86rubidium uptake and photosynthesis in the diatom Cylindrotheca fusiformis. Plant Physiol. 51, 111–117. Smyth, D.A., Dugger, W.M., 1981. Cellular changes during boron-deficient culture of the diatom. Cylindrotheca fusiformis. Physiol. Plant. 66, 692–695. Sparling, D.W., Lowe, T.P., 1996. Environmental hazards of aluminum to plants, invertebrates, fish and wildlife. Rev. Environ. Contam. Toxicol. 145, 1–127. Spear, P.A., 1981. Zinc in the aquatic environment: chemistry, distribution, and toxicology. Natl. Res. Coun. Can. Publ. NRCC 17589, 145 pp. Steeg, P.F.T., Hanson, P.J., Paerl, H.W., 1986. Growth-limiting quantities and accumulation of molybdenum in Anabaena oscillaroides (Cyanobacteria). Hydrobiologia 140, 143–147. Stenner, R.D., Nickless, G., 1974. Distribution of some heavy metals in organisms in Hardangerfjord and Skjerstadfjord, Norway. Water Air Soil Pollut. 3, 279–291. Stenner, R.D., Nickless, G., 1975. Heavy metals in organisms of the Atlantic coast of S.W. Spain and Portugal. Mar. Pollut. Bull. 6, 89–92. Stevenson, R.A., Ufret, S.L., 1966. Iron, manganese and nickel in skeletons and food of the sea urchins Tripneustes esculentus and Echinometra lucunter. Limnol. Oceanogr. 11, 11–17. Stewart, J.G., 1977a. Relative sensitivity to lead of a naked green flagellate Dunaliella tertiolecta. Water Air Soil Pollut. 8, 243–247. Stewart, J.G., 1977b. Effects of lead on the growth of four species of red algae. Phycologia 16, 31–36. Stoddart, D.R., Bryan, G.W., Gibbs, P.E., 1973. Inland mangroves and water chemistry, Barbuda, West Indies. J. Nat. Hist. 7, 33–46. Strohal, P., Huljev, D., Lulic, S., Picer, M., 1975. Antimony in the coastal marine environment, North Adriatic. Estuar. Coast. Mar. Sci. 3, 119–123. Stromgren, T., 1979. The effect of zinc on the increase in length of five species of intertidal fucales. J. Exp. Mar. Biol. Ecol. 40, 95–102. Stromgren, T., 1980. The effect of lead, cadmium, and mercury on the increase in length of five intertidal fucales. J. Exp. Mar. Biol. Ecol. 43, 107–119. Sunda, W., Guillard, R.R., 1976. The relationship between cupric ion activity and the toxicity of copper to phytoplankton. J. Mar. Res. 34, 511–529. Talarico, L., 2002. Fine structure and X-ray microanalysis of a red macrophyte cultured under cadmium stress. Environ. Pollut. 120, 813–821. Tam, N.F.Y., Li, S.H., Lan, C.Y., Chen, G.Z., Li, M.S., Wong, Y.S., 1995. Nutrients and heavy metal contamination of plants and sediments in Futian mangrove forest. Hydrobiologia 295, 149–158. Tam, N.R., Chong, A.M., Wong, Y.S., 2002. Removal of tributyltin (TBT) by live and dead microalgal cells. Mar. Pollut. Bull. 45, 362–371. Tariq, J., Jaffar, M., Ashraf, M., Moazzam, M., 1993. Heavy metal concentrations in fish, shrimp, seaweed, sediment, and water from the Arabian Sea. Mar. Pollut. Bull. 26, 644–647. Taylor, W.R., Odum, E.P., 1960. Uptake of iron-59 by marine benthic algae. Biol. Bull. 119, 343.
Algae and Macrophytes 95 Thain, J.E., Waldock, M.J., 1986. The impact of tributyl tin (TBT) antifouling paints on molluscan fisheries. Water Sci. Technol. 18, 193–202. Thomas, W.H., Dodson, A.N., 1974. Inhibition of diatom photosynthesis by germanic acid: separation of diatom productivity from total marine primary productivity. Mar. Biol. 27, 11–19. Thomas, T.E., Robinson, M.G., 1986. The physiological effects of the leachates from a self-polishing organotin antifouling paint on marine diatoms. Mar. Environ. Res. 18, 215–229. Thomas, T.E., Robinson, M.G., 1987. Initial characterization of the mechanisms responsible for the tolerance of Amphora coffeaeformis to copper and tributyltin. Bot. Mar. 30, 47–53. Thomas, W.H., Hollibaugh, J.T., Siebert, D.L.R., Wallace Jr, G.T., 1980. Toxicity of a mixture of ten metals to phytoplankton. Mar. Ecol. Prog. Ser. 2, 213–220. Thompson, J.A.J., Sheffer, M.G., Pierce, R.C., Chau, Y.K., Cooney, J.J., Cullen, W.R., et al., 1985. Organotin compounds in the aquatic environment: scientific criteria for assessing their effects on environmental quality. Natl. Res. Coun. Can. Publ., NRCC 22404, pp. 1–284. Thursby, G.B., Steele, R.L., 1984. Toxicity of arsenite and arsenate to the marine macroalgae Champia parvula (Rhodophyta). Environ. Toxicol. Chem. 3, 391–397. Tijoe, P.S., de Goeij, J.J.M., de Bruin, M., 1977. Determination of Trace Elements in Dried Sea-Plant Homogenate (SP-M-1) and in Dried Copepod Homogenate (MA-A-1) by Means of Neutron Activation Analysis. Interuniversity Reactor Institute, Rep., 133-77-05, Delft, Nederlands, 14 pp. Trefry, J.H., Presley, B.J., 1976. Heavy metal transport from the Mississippi River to the Gulf of Mexico. In: Windom, H.L., Duce, R.A. (Eds.), Marine Pollutant Transfer. D.C. Heath, Lexington, MA, pp. 39–76. Tripp, M., Harriss, R.C., 1976. Role of mangrove vegetation in mercury cycling in the Florida everglades. In: Nriagu, J.D. (Ed.), Environmental Biogeochemistry. Vol. 2. Metals Transfer and Ecological Mass Balances. Ann Arbor Science Publishers, Ann Arbor, MI, pp. 489–497. Tsang, C.K., Lau, P.S., Tam, N.F.Y., Wong, Y.S., 1999. Biodegradation capacity of tributyltin by two Chlorella species. Environ. Pollut. 105, 289–297. Ueda, T., Nakamura, R., Suzuki, Y., 1978. Comparison of influence of sediments and sea water on accumulation of radionuclides by marine organisms. J. Radiat. Res. 19, 93–99. Ukeles, R., 1962. Growth of pure cultures of marine phytoplankton in the presence of toxicants. Appl. Microbiol. 10, 512–537. U.S. Environmental Protection Agency (USEPA), 1980a. Ambient water quality criteria for copper. USEPA Rep. 440/5-80-036, 162 pp. USEPA, 1980b. Ambient water quality criteria for nickel. USEPA Rep. 440/5-80-060, 206 pp. USEPA, 1980c. Ambient water quality criteria for zinc. USEPA Rep. 440/5-80-079, 158 pp. USEPA, 1980d. Ambient water quality criteria for chromium. USEPA Rep. 440/5-80-035 pp. USEPA, 1980e. Ambient water quality criteria for nickel. USEPA Rep. 440/5-80-060, pp. 1–206. USEPA, 1980f. Ambient water quality criteria for silver. USEPA, Rep. 440/5-80-071, pp. 1–212. USEPA, 1985a. Ambient water quality criteria for arsenic—1984. USEPA Rep. 440/5-84-033, 66 pp. USEPA, 1985b. Ambient water quality criteria for lead—1984. USEPA Rep. 440/5-84-027, 81 pp. USEPA, 1986. Initiation of a special review of certain pesticide products containing tributyltins used as antifoulants; availability of support document. Fed. Regis. 51(5), 778–779 pp. USEPA, 1987. Ambient water quality criteria for zinc—1987. USEPA Rep. 440/5-87-003, 207 pp. USEPA, 1989. Ambient water quality criteria for antimony. USEPA Rep. 440/5-80-120, 103 pp. USEPA, 1999. National recommended water quality criteria—correction. USEPA 822-Z-99-001. Office of Water, Washington, DC. US Public Health Service (USPHS), 1990. Toxicological profile for silver. Agen. Toxic Subs. Dis. Regis. TP-90-124, 145 pp. USPHS, 1993. Toxicological profile for nickel. USPHS, Agen. Toxic Subs. Dis. Regis., Atlanta, GA, pp. Rep. TP-92/14, 1–158 pp. USPHS, 1995. Toxicological profile for nickel (update). USPHS, Agen. Toxic Subs. Dis. Regis., Atlanta, GA, pp. 1–244.
96 Chapter 2 Vaishampayan, A., 1983. Mo-V interactions during N2- and NO3-metabolism in a N2-fixing blue-green alga Nostoc muscorum. Experientia 39, 358–360. Valega, M., Lillebo, A.I., Cacador, I., Pereira, M.E., Duarte, A.C., Pardal, M.A., 2008. Mercury mobility in a salt marsh colonised by Halimione portulacoides. Chemosphere 72, 1607–1613. Van As, D., Fourie, H.O., Vlegaar, C.M., 1973. Accumulation of certain trace elements in the marine organisms from the sea around the Cape of Good Hope. In: Radioactive Contamination of the Marine Environment. International Atomic Energy Agency, Vienna, Austria, pp. 615–624. Van As, D., Fourie, H.O., Vlegaar, C.M., 1975. Trace element concentrations in marine organisms for the Cape West Coast. S. Afr. J. Sci. 71, 151–154. Vinogradova, Z.A., Koual’skiy, V.V., 1962. Elemental composition of the Black Sea plankton. Dokl. Acad. Sci. USSR Earth Sci. Sec. 147, 217–219. Visser, F., Gerringa, J.A., Van der Gaast, S.J., de Baar, H.J.W., Timmermans, K.R., 2003. The role of the reactivity and content of iron of aerosol dust on growth rates of two Antarctic diatom species. J. Phycol. 39, 1085–1094. Visviki, L., Rachlin, J.W., 1994a. Acute and chronic exposure of Dunaliella salina and Chlamydomonas bullosa to copper and cadmium: effects on growth. Arch. Environ. Contam. Toxicol. 26, 149–153. Visviki, L., Rachlin, J.W., 1994b. Acute and chronic exposure of Dunaliella salina and Chlamydomonas bullosa to copper and cadmium: effects on ultrastructure. Arch. Environ. Contam. Toxicol. 26, 154–162. Vosjan, J.H., 1969. Effect of chelation on the uptake and loss of yttrium-91 by Porphyra. Neth. J. Sea Res. 4, 310–316. Walsh, G.E., McLaughlin, L.L., Lores, E.M., Louie, M.K., Deans, C.H., 1985. Effects of organotins on growth and survival of two marine diatoms, Skeletonema costatum and Thalassiosira pseudonana. Chemosphere 14, 383–392. Wang, Z.S., Kong, H.N., Wu, D.Y., 2007. Reproductive toxicity of dietary copper to a saltwater cladoceran, Moina monogolica Daday. Environ. Toxicol. Chem. 26, 126–131. Ward, T.J., Correll, R.L., Anderson, R.B., 1986. Distribution of cadmium, lead and zinc amongst the marine sediments, sea grasses and fauna, and the selection of sentinel accumulators, near a lead smelter in South Australia. Aust. J. Mar. Freshw. Res. 37, 567–585. Weis, J.S., Weis, P., 1992. Transfer of contaminants for CCA-treated lumber to aquatic biota. J. Exp. Mar. Biol. Ecol. 161, 189–199. Weiss, R.E., Blackwelder, P.L., Wilbur, K.M., 1976. Effects of calcium, strontium and magnesium on the coccolithophorid Cricosphaera (Hymenomonas) carterae. II. Cell division. Mar. Biol. 34, 17–22. Williams, R.B., Murdock, M.B., 1969. The potential importance of Spartina alterniflora in conveying zinc, manganese, and iron into estuarine food chains. In: Proceedings of 2nd National Symposium on Radioecology. USAEC Conf. 670503, pp. 431–440. Windom, H.L., 1973. Mercury distribution in estuarine-nearshore environment. J. Am. Soc. Civ. Eng. Waterways Harbors Coast. Eng. Div. 99 (WW2), 257–264. Windom, H., 1975. Heavy metal fluxes through salt marsh estuaries. In: Cronin, L.E. (Ed.), Estuarine Research, Vol. 1. Chemistry, Biology, and the Estuarine System. Academic Press, New York, pp. 137–152. Windom, H.L., Gardner, W., Dunstan, W.M., Paffenhofer, G.A., 1976. Cadmium and mercury transfer in a coastal marine ecosystem. In: Windom, H.L., Duce, R.A. (Eds.), Marine Pollutant Transfer. D.C. Heath, Lexington, MA, pp. 135–157. Wolfe, D.A., 1974. The cycling of zinc in the Newport River estuary, North Carolina. In: Vernberg, F.J., Vernberg, W.J. (Eds.), Pollution and Physiology of Marine Organisms. Academic Press, New York, pp. 79–99. Wong, K.M., 1971. Radiochemical determination of plutonium in sea water, sediments and marine organisms. Anal. Chim. Acta, 56, 355–364. Wong, K.H., Chan, K.Y., Ng, S.L., 1979. Cadmium uptake by the unicellular green alga Chlorella salina CU-1 from culture media with high salinity. Chemosphere 11/12, 887–891. Wong, P.T.S., Trevors, J.T., 1971. Chromium toxicity to algae and bacteria. In: Nriagu, J.O., Nieboer, E. (Eds.), Chromium in Natural and Human Environments. John Wiley, New York, pp. 305–315.
Algae and Macrophytes 97 Woolery, M.L., Lewin, R.A., 1976. The effects of lead on algae. IV. Effects of Pb on respiration and photosynthesis of Phaeodactylum tricornutum (Bacillariophyceae). Water Air Soil Pollut. 6, 25–31. Woolson, E.A. (Ed.), 1975. Arsenical Pesticides. Amer. Chem. Soc. Sympos. Ser. 7. 176 pp. World Health Organization (WHO), 1991. Nickel. Environ. Health Crit. 108, 383. Wort, D.J., 1955. The seasonal variation in chemical composition of Macrocystis integrifolia and Nereocystis luetkeana in British Columbia coastal waters. Can. J. Bot. 33, 323–340. Wrench, J.J., 1978. Selenium metabolism in the marine phytoplankters Tetraselmis tetrathele and Dunaliella minuta. Mar. Biol. 49, 231–236. Wrench, J., Fowler, S.W., Unlu, M.Y., 1979. Arsenic metabolism in a marine food chain. Mar. Pollut. Bull. 10, 18–20. Yamamoto, Y., Fujita, T., Ishibashi, M., 1970. Chemical studies on the seaweeds (25). Vanadium and titanium contents in seaweeds. Rec. Oceangr. Works Jpn. 10(2), 125–135. Yamamoto, T., Yamaoka, T., Fujita, T., Isoda, C., 1971. Chemical studies on the seaweeds (26). Boron content of seaweeds. Rec. Oceangr. Works Jpn. 11(1), 7–13. Yamamoto, T., Otsuka, Y., Uemura, K., 1976. Gallium content in seaweeds. J. Ocean. Soc. Jpn. 32, 182–186. Yamaoka, Y., Takimura, O., 1986. Marine algae resistant to inorganic arsenic. Agric. Biol. Chem. 50, 185–186. Yeo, A.R., Flowers, T.J., 1977. Salt tolerance in the halophyte Suaeda maritima (L.) Dum.: interaction between aluminum and salinity. Ann. Bot. 41, 331–339. Yoshimura, A., Tada, H., Sakai, M., Harada, T., Oishi, K., 1976. Distribution of inorganic constituents of kombu blade-III. Inorganic constituents of acceleratedly cultured ma-kombu at various growth stages. Bull. Jpn. Soc. Sci. Fish. 42, 661–664. Young, M.L., 1975. The transfer of 65Zn and 59Fe along a Fucus serratus (L.)/Littorina obtusa food chain. J. Mar. Biol. Assoc. UK 55, 583–610. Young, E.G., Langille, W.M., 1958. The occurrence of inorganic elements in marine algae of the Atlantic provinces of Canada. Can. J. Bot. 36, 301–310. Zavodnik, N., 1977. Note on the effects of lead on oxygen production of several littoral seaweeds of the Adriatic Sea. Botanica Marina 20, 167–170. Zbikowski, R., Szefer, P., Latala, A., 2006. Distribution and relationships between selected chemical elements in green alga Enteromorpha sp. from the southern Baltic. Environ. Pollut. 143, 435–448. Zbikowski, R., Szefer, P., Latala, A., 2007. Comparison of green algae Cladophora sp. and Enteromorpha sp. as potential biomonitors of chemical elements in the southern Baltic. Sci. Total Environ. 387, 320–332. Zhao, Y., Hao, H., Ramelow, G.J., 1994. Evaluation of treatment techniques for increasing the uptake of metal ions from solution by nonliving seaweed algal biomass. Environ. Monit. Assess. 33, 61–70. Zheng, W., Lin, P., 1996. Accumulation and distribution of Cu, Pb, Zn and Cd in Avicennia marina mangrove community of Futian in Shenzhen. Oceanol. Limnol. Sinica 1996, 77. Zheng, W.J., Chen, X.Y., Lin, P., 1997. Accumulation and biological cycling of heavy metal elements in Rhizophora stylosa mangroves in Yingluo Bay, China. Mar. Ecol. Prog. Ser. 159, 293–301. Zingde, M.D., Singbal, S.Y.S., Moraes, C.F., Reddy, C.V.G., 1976. Arsenic, copper, zinc & manganese in the marine flora & fauna of coastal & estuarine waters around Goa. Indian J. Mar. Sci. 5, 212–217. Zlobin, U.S., 1966. Accumulations of radioactive strontium by the brown seaweeds. Gig. Sanit. 31(12), 86–88 (Nucl. Sci. Abstr. 1967, 21, 2349).
This page intentionally left blank
CHAPTER 3
Protists This group comprises all marine nonphotosynthetic unicellular organisms, such as protozoans, bacteria, yeasts, and fungi. Trace metal concentrations in protists are known initially from the results of three studies: Culkin and Riley (1958), who collected the foraminiferan Ramulina sp. from the Irish Sea; Krinsley (1960), who analyzed planktonic foraminiferan tests from Atlantic Ocean cores; and Martin and Knauer (1973), who sampled radiolarians from the Pacific Ocean near and between Hawaii, California, and Oregon.
3.1 Aluminum Concentrations ranged from 137.0 to 3008.0 mg Al/kg DW (dry weight) (Table 3.1). Endosymbiotic bacteria (sulfur and methane oxidizers) from gills of a hydrothermal vent mussel, Bathymodiolus azoricus, collected in 2002 contained 209.0 mg Al/kg DW (Table 3.1). Authors aver that endosymbiotic bacteria sequester aluminum (and to a lesser extent manganese and mercury) from host gill and contribute to its removal (Kadar et al., 2006).
3.2 Arsenic Organoarsenicals were less toxic to Vibrio fischeri marine bacteria than were inorganic arsenicals, based on luminescence tests (Fulladosa et al., 2007). In most cases, adverse effects of dimethylarsinic acid, monomethylarsonic acid, and 4-hydroxy-3-nitrobenzene arsonic acid could not be determined because of the low toxicity of these compounds. Arsenobetaine and monomethylarsonic acid, however, can stimulate bacterial growth (Fulladosa et al., 2007). Bacterial cultures from the Sargasso Sea and from marine waters of Rhode Island were grown in media with added trivalent arsenic. During log growth phase, bacteria reduced all available pentavalent arsenic and used As3þ, presumably as an essential nutrient. The arsenate reduction rate was estimated at 75 1011 mg As/cell/min (Johnson, 1972). Since As3þ is considered a threat to human health, while As5þ by all accounts remains comparatively innocuous, these findings have important toxicological implications. 99
100 Chapter 3 Table 3.1: Trace Element Concentrations in Field Collections of Protists Element and Organism
Concentration
Reference
a
Aluminum Endosymbiotic bacteria from gills of a hydrothermal vent mussel, Bathymodiolus azoricus
209.0 DW
4
Foraminiferan tests
1269.0-3008.0 DW
1
Radiolarians
137.0 DW
2
Ramulina sp.
973.0 DW
3
17.0 DW
2
Endosymbiotic bacteria from gills of mussel
0.3 DW
4
Radiolarians
6.4 DW
2
0.2 DW
4
Foraminiferan tests
8.0-30.4
1
Radiolarians
6.5 (4.4-11.4) DW
2
Ramulina sp.
111.0 DW
3
0.18 DW
3
Radiolarians
315.0 DW
2
Ramulina sp.
1148.0 DW
3
2.1 DW
2
Endosymbiotic bacteria from mussel gills
1.4 DW
4
Foraminiferan tests
9.3-63.3 DW
1
Barium Radiolarians Cadmium
Cobalt Endosymbiotic bacteria from mussel gills Copper
Gallium Ramulina sp. Iron
Lead Radiolarians Manganese
(Continues)
Protists Table 3.1:
101
Cont’d
Element and Organism
Concentration
Reference
Radiolarians
6.4 DW
2
Endosymbiotic bacteria from mussel gills
0.9 DW
4
Radiolarians
0.14 DW
2
Foraminiferan tests
15.4-23.0 DW
1
Radiolarians
3.7 DW
2
Foraminiferan tests
933.9-1782.9 DW
1
Radiolarians
163.0 DW
2
186.0-360.0 DW
1
63.0-279.0 DW
2
a
Mercury
Nickel
Strontium
Titanium Foraminiferan tests Zinc Radiolarians
Values are in mg element/kg dry weight (DW). a 1, Krinsley, 1960; 2, Martin and Knauer, 1973; 3, Culkin and Riley, 1958; 4, Kadar et al., 2006.
3.3 Barium A single datum was available of 17.0 mg Ba/kg DW (Table 3.1).
3.4 Cadmium Limited data show that cadmium ranged from 0.3 to 6.4 mg Cd/kg DW (Table 3.1). Cadmium uptake by a gram-positive bacterium, Bacillus firmus, isolated from Hong Kong sediments is best predicted by Cd2þ activity and passive diffusion through the plasma membrane (Keung et al., 2008). The trypanosomid flagellate Crithidia fasciculate, grown in culture media containing 1.79 mg Cd/L, removed 95% of the cadmium (Maclean et al., 1972). Under similar conditions, Escherichia coli bacteria from sediments of Corpus Christi Harbor, Texas, took up 70% of the metal (McLerran and Holmes, 1974). The use of protists as possible decontaminators of cadmium-impacted environments is suggested. Extracts from cadmium-exposed clams, Scapharca inaequivalvis, inhibited the bacterial luminescence of Vibrio logei; the inhibition decreased as time of clam exposure to cadmium increased, suggesting a reduction of the biological component (Girotti et al., 2006).
102 Chapter 3
3.5 Cesium A foraminiferan, Elphidium crispum, showed a maximum concentration factor of 16 for radiocesium (Bryan, 1963). Accumulation rates were similar for dead and living Elphidium, suggesting that cesium metabolism by this species may be governed by the same mechanisms responsible for potassium balance (Bryan, 1963).
3.6 Chromium A hexavalent chromium-resistant strain of Enterobacter cloacae can remove up to 70% of the chromium in solution and show enhanced growth and exopolysaccharide production at concentrations as high as 100.0 mg Cr6þ/L (Iyer et al., 2004). V. fischeri bacteria are comparatively resistant to hexavalent chromium owing to its capacity to reduce the toxic Cr6þ to the comparatively innocuous Cr3þ; the reducing capacity is attributed to unidentified thermostable nonproteic molecules (Fulladosa et al., 2006).
3.7 Cobalt Bacteria from gills of mussels contained 0.2 mg Co/kg DW (Table 3.1). Cobalt uptake into cells of E. coli was inhibited by 0.24 mg magnesium/L and higher, and energy-dependent transport of Mg2þ into cells was inhibited by 0.59 mg Co2þ/L and higher (Nelson and Kennedy, 1971). Cobalt-magnesium interactions and energy transport mechanisms of protists merit additional research.
3.8 Copper Concentrations in field collections ranged from 4.4 to 111.0 mg Cu/kg DW (Table 3.1). Extracts from copper-exposed clams inhibited the natural luminescence of V. logei bacteria (Girotti et al., 2006). A bacterial copper-resistant strain of Vibrio sp.—resistant to 50.0 mg Cu/L— was isolated from the scallop Argopecten purpuratus (Miranda and Rojas, 2006). On exposure to 15.0 mg Cu/L for 24 h, the Vibrio strain accumulated copper in cellular and loosely bound copper burdens of 201.1 and 493.2 mg/kg DW, respectively. Scallop larvae subjected to Cu-enriched Vibrio took up 20.4 mg Cu/kg DW after 12 h and 30.1 mg Cu/kg DW after 24 h, and suggest that bacterial copper accumulation could be active in copper transfer among marine food chains (Miranda and Rojas, 2006). Resistance mechanisms, such as accumulation of copper by resistant cells or reduced permeability to Cu2þ owing to the synthesis of new membrane proteins, could be active in aerobic aquatic environments (Cha and Cooksey, 1991; Harwood-Sears and Gordon, 1990, 1994). As a group, the bacteria are important agents in determining the form and distribution of copper in marine environments, playing a major role in the modification, activation, and detoxification of copper (Gordon et al., 2000).
Protists
103
The bacterial community of silty estuarine sediments withstands high concentrations of copper at the cost of reduced bacterial organic matter degradation and reduced bacterial production (Almeida et al., 2007). In one study, bacteria-containing silty estuarine sediments were spiked with 200.0 mg Cu/kg DW. After 21 days, bacterial abundance decreased by 98.6% when compared to controls, and leucine turnover rate decreased by 87%. The toxic effects caused by copper on protein and carbohydrate degradation were not rapidly repaired by erosion and oxygenation; however, bacterial biomass production and leucine turnover were rapidly reactivated (Almeida et al., 2007). The marine protozoan Euplotes vannus subjected to various concentrations of copper for 6 days showed stimulated growth at low concentrations (0.1 mg/L), normal growth at 0.2 mg Cu/L, and adverse effects at 0.4 mg Cu/L, such as depressed growth, morphological cell alterations, and copper accumulations of 239.0 mg/kg DW (Coppellotti, 1998). Copper-zinc mixtures are frequently more than additive in toxicity to marine biota; however, mixtures of copper (up to 0.09 mg/L) and zinc (up to 1.2 mg/L) are only additive in action to a marine bacterium (Photobacterium phosphoreum), decreasing its luminescence after exposure for 30 min (Parrott and Sprague, 1993). Phosphate interfered with the inhibitory effects of copper on marine bacteria and yeasts under conditions of manganese deficiency (Button and Dunker, 1971). It is probable that the complexed copper was not biologically available. High concentrations of copper had no apparent effect on Cristigera, a ciliate protozoan, but this may be due to the complexation or chelation of ionic copper with organic matter (Gray and Ventilla, 1971). Iron-reducing bacteria from copper-contaminated sediment were more tolerant to copper adsorbed on hydrous ferric oxide (HFO) than were pristine-sediment bacteria (Markwiese et al., 1998). Copper-tolerant bacteria were more efficient in reducing contaminated HFO, with greater potential for copper mobilization in aquatic sediments (Markwiese et al., 1998).
3.9 Gallium A single datum was available of 0.18 mg Ga/kg DW (Table 3.1).
3.10 Iron Iron concentrations in protists ranged from 315.0 to 1148.0 mg Fe/kg DW (Table 3.1).
3.11 Lead A single datum was available of 2.1 mg Pb/kg DW in radiolarians (Table 3.1). Reduced growth was documented in the protozoan Cristigera sp. after immersion for 12 h in seawater containing 0.15 mg inorganic Pb/L (USEPA, 1985a). Organolead compounds are,
104 Chapter 3 in general, more toxic than inorganic lead compounds to aquatic organisms. Ethyl derivatives were more toxic than methyl derivatives, and toxicity increased with increasing degree of alkylation, tetraethyllead being the most toxic (Babich and Borenfreund, 1990; Chau et al., 1980). Mixed species of coastal marine bacteria show marked reduction in oxygen consumption during exposure to tetramethyllead salts; however, tetraethyllead salts were more effective at doses only 10% that of tetramethyllead (Marchetti, 1978). It is reasonable to assume that lead is more readily accumulated by these species in the tetraethyl form than the tetramethyl form. Interaction of lead with mercury and zinc are documented for Cristigera (Gray, 1974). At 0.3 mg Pb/L, about 12% growth reduction was observed; similar results occur at 0.005 mg Hg/L or 0.25 mg Zn/L. However, when mixtures containing 0.3 mg Pb/L plus 0.005 mg Hg/L plus 0.25 mg Zn/L were tested, the growth reduction was 67% rather than the expected 36%. It is possible that several physiologically active sites are involved.
3.12 Manganese Concentrations in field collections ranged from 1.4 to 63.3 mg Mn/kg DW (Table 3.1). Manganese is essential for normal metabolism of some marine bacteria. For example, bacteria isolated from ferromanganese nodules synthesized ATP at rates governed by available manganese in the ratio of 1 to 2 moles of ATP for each mole of Mn2þ oxidized (Ehrlich, 1976).
3.13 Mercury Limited data show 0.14-0.9 mg Hg/kg DW, being highest in bacteria isolated from gills of mussels (Table 3.1). Common features of foraminiferal assemblages in polluted environments include reduced foraminiferal population diversity and density, stunting of adult tests, frequent presence of deformed tests, and an increase in percentage of individuals belonging to a few opportunistic species (Di Leonardo et al., 2007). For example, sediment cores collected off Sicily in 2003-2004 near industrialized areas showed highly enriched mercury concentrations as well as polycyclic aromatic hydrocarbon burdens, and this was associated with a reduction in the abundance of benthic foraminifera, an increasing percentage of tests with morphological deformities, and the dominance of opportunistic species in the more recent sediments associated with human activities (Di Leonardo et al., 2007). Mercury discharged into rivers, bays, or estuaries as metallic mercury, inorganic divalent mercury, or organomercurial can all be converted to water soluble methylmercury compounds of high toxicity (Jernelov, 1969). Mercury-resistant strains of bacteria that have been developed
Protists
105
or discovered may have application in mercury mobilization or fixation from mercurycontaminated waters to the extent that polluted areas become innocuous (Colwell and Nelson, 1975; Eisler, 2006; Nelson et al., 1973; Vosjan and Van der Hoek, 1972). For example, a mercury-reducing strain of Pseudomonas reduced 0.025 mg of HgCl2 to elemental mercury from solutions containing 6.0 mg HgCl2/L (Colwell et al., 1976). Mercury-resistant strains of bacteria are common, and 364 strains resistant to HgCl2 have been isolated from Chesapeake Bay alone; most were pseudomonads and almost all from seven genera (Colwell et al., 1976). The percentage of mercury-resistant strains in bay sediments was highest in the spring of the year (Colwell and Nelson, 1974). Some strains were not only mercury resistant, but were reported to also degrade petroleum (Walker and Colwell, 1974). Mercury-resistant and metabolizing strains of bacteria showed a wide range of metabolic rates depending on the chemical species of mercury, the bacterial biomass (Colwell and Nelson, 1975; Nelson and Colwell, 1975), and species competition in the case of E. coli and Staphylococcus aureus (Stutzenberger and Bennet, 1965). Other groups of bacteria that influence mercury fluxes include strains of E. coli that convert inorganic divalent mercury to metallic mercury (Summers and Silver, 1972), and strains of anaerobic methanogenic bacteria that enhance the transfer of methylcobalamin to Hg2þ in mild reducing conditions (Wood et al., 1968). In the case of Minamata Bay, Japan, a site initially contaminated by inorganic mercury, the mercury was methylated chemically with methylcobalamin as the carbon methyl group donor (Baldi et al., 1993; Choi and Bartha, 1993). The methylcobalamin is synthesized by a range of bacterial species, especially Desulfovibrio desulfuricans, which is considered a major methylating source in anaerobic sediments (Choi and Bartha, 1993). At low (0.1 mg Hg2þ/ kg) sediment mercury concentrations, up to 37% of the added mercury was methylated during fermentative growth of D. desulfuricans. But under conditions of sulfate reduction, mercury methylation was less efficient. The fermentative mercury methylating cultures were comparatively sensitive to Hg2þ, whereas the sulfate-reducing cultures that did not methylate at a high rate were more resistant to Hg2þ (Choi and Bartha, 1993). Some strains of D. desulfuricans, in addition to producing methylmercury, can also convert methylmercury to methane and Hgo, as was true for aerobic species of bacteria isolated from Minamata Bay sediments (Baldi et al., 1993). In Minamata Bay, 72 strains of mercury-resistant Pseudomonas spp. bacteria were isolated from sediments near the drainage outlet to the bay (Nakamura et al., 1986). Pseudomonas spp. dominated the bacteria with the highest resistance to mercury, although Bacillus spp. strains were the most numerous among all bacterial species isolated from Minamata Bay sediments. Total bacterial concentrations in Minamata Bay were the same as a nearby reference site, but mercury-resistant bacteria were found in higher numbers in Minamata Bay. In 1984, additional bacteria were isolated. Bacillus strains dominated in sediments containing up to 23.0 mg total Hg/kg and Pseudomonas strains in sediments with higher (>52.0 mg total Hg/kg) mercury concentrations. The mercury-resistant Pseudomonas strains, when compared to Bacillus strains, were
106 Chapter 3 more resistant to inorganic mercury, methylmercury, and phenylmercury (Nakamura et al., 1986). Multiple organomercurial-volatilizing bacteria that can volatilize Hgo from methylmercury chloride, ethylmercury chloride, phenylmercury acetate, and fluorescein mercuric acetate, and p-chloromercuric benzoate were found in the sediments of Minamata Bay (Nakamura, 1994; Nakamura and Silver, 1994). The bacteria detoxify mercury compounds by two separate enzymes—organomercurial lyase and mercuric reductase— acting sequentially. Organomercurial lyase cleaves the C-Hg bond of certain mercurials, and mercuric reductase then reduces Hg2þ to volatile Hgo; bacteria remove mercury from the environment as mercury vapor (Nakamura, 1994). In 1988, a total of 4604 bacterial strains were isolated from Minamata Bay (1428 strains) and a reference site (3176 strains) and screened for their ability to volatilize mercuric chloride (Nakamura, 1994). Up to 38% of all bacterial strains isolated from Minamata Bay could grow on agar media containing 40.0 mg MgCl2/L versus only 0.8% of bacteria from reference locations. A total of 67 Pseudomonas strains and 91 Bacillus strains from Minamata Bay were significantly more resistant to mercuric chloride than were Bacillus spp., both detoxify the mercury compounds in Minamata Bay by organomercurial lyase and mercuric reductase enzymes. The organomercurials-volatilizing bacteria strains were found only in sediments of Minamata Bay. A total of 78 strains of Bacillus that can degrade both inorganic and organic mercurials were collected from Minamata Bay and were identified as Bacillus subtilis, B. firmus, B. lentus, B. bodius, and two unidentified strains. The ability to detoxify mercury compounds is chromosomally encoded and similar to that of Bacillus spp. isolated from Boston Harbor, Massachusetts (Nakamura, 1994). Enzymatic detoxification was determined as the major resistance mechanism in all species of mercury-resistant bacteria (Furukawa and Tonomura, 1971; Komura and Izaki, 1971; Summers and Silver, 1972). For example, mercuric reductase was essential for volatilization of Hgo from Hg2þ, and various organomercurial hydrolases were responsible for volatilization of methane (CH4) from methylmercury, for ethane (C2H5) from ethylmercury, and for benzene from phenylmercury (Silver et al., 1994). Minamata Bay bacterial isolates can also volatilize Hgo from added inorganic and organic mercurials (Nakamura, 1989; Nakamura et al., 1988, 1990). Genes that govern the chemistry of mercury detoxification were abundant in bacteria found in Minamata Bay and other mercury-polluted sites; these genetic strains of mercury-resistant bacteria show promise for bioremediation of mercury pollution (Misra, 1992; Nakamura, 1994; Silver and Waldrhaug, 1992; Silver et al., 1994). Mercury was the most toxic metal tested to the ciliated marine protozoan Uronema marinum, with 50% survival in 24 h at 0.006 mg Hg/L (Parker, 1979). Similar values for lead and zinc were 60.0 and 400.0 mg/L, respectively. Interaction effects among the three were evident. Attempts to acclimatize the ciliates to trace metals over an 18-week period were unsuccessful (Parker, 1979). However, the marine ciliate Uronema nigricans did acquire tolerance to mercury after eating mercury-laden bacteria, although survival was lower than controls
Protists
107
(Berk et al., 1978). Acquired mercury tolerance was demonstrated within a single generation. Ciliates fed with mercury-free bacteria and subsequently exposed to increasing levels of mercury in solution show an elevated tolerance to concentrations that initially killed 83% of the ciliates (Berk et al., 1978).
3.14 Nickel Concentrations in field collections ranged from 3.7 to 23.0 mg Ni/kg DW (Table 3.1). Nickel is essential for the normal growth of many species of microorganisms and plants, and several species of mammals (USPHS, 1993, 1995; WHO, 1991). Nickel introduced into the environment from natural or human sources is circulated through the system by chemical and physical processes and though biological transport mechanisms of living organisms (NAS, 1975; WHO, 1991). In microorganisms, nickel binds mainly to the phosphate groups of the cell wall. From this site, an active transport mechanism designed for magnesium transport transports the nickel (Kasprzak, 1987). Nickel salts gave no evidence of mutagenesis in tests with viruses (USPHS, 1977), and bacterial tests of nickel compounds have consistently yielded negative or inconclusive results (Sunderman, 1981; Sunderman et al., 1984; USPHS, 1977; WHO, 1991). However, nickel chloride and nickel sulfate were judged to be mutagenic or weakly mutagenic in certain bacterial eukaryotic test systems (USEPA, 1985b). Nickel subsulfide was positively mutagenic to the protozoan Paramecium sp. at 0.5 mg Ni/L (WHO, 1991). Ionic Ni2þ was mutagenic to E. coli; mutagenesis was enhanced by the addition of both hydrogen peroxide and tripeptide glycyl-Lhistidine, suggesting that short-lived oxygen free radicals are generated (Tkeshelashvili et al., 1993). Nickel chloride hexahydrate induced respiratory deficiency in yeast cells, but this may be a cytotoxic effect rather than a gene mutation (USPHS, 1977; WHO, 1991). Marine bacteria are comparatively tolerant of nickel, with growth inhibition evident at concentrations greater than 10.0 mg Ni/L (Babich and Stotzky, 1982).
3.15 Silver Silver was lethal to sensitive protozoans at 0.009-0.015 mg/L (Nalecz-Jawecki et al., 1993). The ciliate protozoan Fabrea salina held in seawater solution containing radiosilver 110 m accumulated silver from the medium by factors that ranged from 7000 to 40,000 within 24 h (Fisher et al., 1995). Marine bacteria isolated from tubes of deep-sea polychaete annelids were comparatively resistant to silver salts; 3.0 mg Ag/L was the lowest concentration tested that inhibited growth in 50% of strains tested during exposure for 10 days (Jeanthon and Prieur, 1990).
108 Chapter 3 Silver-resistant strains (55% of all strains tested) survived at least 24 h during exposure to 20.0 mg Ag/L, and some strains survived exposure to 40.0 mg Ag/L (Jeanthon and Prieur, 1990).
3.16 Strontium Concentrations of strontium were comparatively high in field collections, ranging from 163.0 to 1782.0 mg Sr/kg DW (Table 3.1). Calcium is an important variable mediating strontium accumulations in foraminiferans. Two studies show that the Sr/Ca ratios range from 0.0012-0.0015 (Bender et al., 1975) and 0.028-0.038 (Thompson and Chow, 1955), respectively.
3.17 Tin Total tin accumulations in marine algae, molluscs, and crustaceans seldom exceeded 100.0 mg Sn/kg DW; however, certain species of tin-resistant bacteria contained a remarkable 3700.0-7700.0 mg Sn/kg DW (Eisler, 2000; Maguire, 1991; Maguire et al., 1984). Tributyltin (TBT)-resistant strains of Pseudoalteromonas sp. were unable to degrade the comparatively toxic TBT to the less toxic dibutyltin (DBT) and monobutyltin (MBT); resistance in this strain was attributed to the unique cell surface containing membranebinding proteins that can pump TBT from the cytoplasm (Mimura et al., 2008). Inorganic tin can be biomethylated by microorganisms in the aquatic environment and subsequently mobilized in the ecosystem (Tugrul et al., 1983; Yemenicioglu et al., 1987). The process is slow and usually does not proceed beyond the monomethyltin stage (Zuckerman et al., 1978), although dimethyltin formation by Pseudomonas bacteria is reported (Roy et al., 2004; Smith, 1978). The fungus Cunninghamella elegans can degrade TBTs to less toxic derivatives, that is, DBTs and MBTs; up to 89% of TBT is degraded within 3 days in oxygenated media containing glucose, ammonium chloride, potassium diphosphate, and magnesium sulfate (Bernat and Dlugonski, 2006). The ability of microorganisms to reduce various organotins to less toxic, easily excreted, metabolites seems to preclude food-chain biomagnification (Cardwell and Sheldon, 1986). Strains of Pseudomonas isolated from Chesapeake Bay were about 100 times more sensitive to divalent tin salts than to tetravalent tin salts (Iverson et al., 1973). Organotins can be highly toxic to many prokaryotic and eukaryotic organisms and have been identified as immune system inhibitors and endocrine disruptors in humans (Dubey and Roy, 2003; Dubey et al., 2006). Mechanisms involved in TBT resistance in bacteria include transformation into less-toxic compounds, such as DBT and MBT, by abiotic and biotic processes (Clark et al., 1988; Pain and Cooney, 1998a). Marine bacteria that are resistant to TBT and can degrade TBT to less-toxic metabolites were isolated from water and sediments near Aveiro, Portugal (Cruz et al., 2007). Of the 50 TBT-resistant strains, an isolate of Aeromonas veronii
Protists
109
AV27 was highly resistant to TBT (about 330.0 mg TBT/L), uses TBT as a carbon source and degrades it to less-toxic compounds, including DBT and MBT (Cruz et al., 2007). Antifouling paints containing organotin compounds are associated with reductions in natural bacterial assemblages (Prior and Riemann, 1998). Among the triorganotin compounds, tripropyltins (TPTs) were highly toxic to gram-negative bacteria, and TBTs to gram-positive bacteria (Eisler, 2000; Maguire, 1991; Mendo et al., 2003). Antifouling paints containing TPTs will not be a suitable substitute for TBTs in paints designed to inhibit microbial biofilms (Pain and Cooney, 1998b). Up to 98% of bacteria resistant to six organotins, including TBTs, isolated from estuarine sediments of Boston Harbor, Massachusetts, were also resistant to TPTs. All bacteria were resistant to at least six of eight metals tested, suggesting that resistance to metals—including nickel, cadmium, lead, mercury, copper, and zinc—may be associated with resistance to organotins (Pain and Cooney, 1998a,b).
3.18 Titanium A single datum was available of 186.0-360.0 mg Ti/kg DW in tests of foraminiferans (Table 3.1).
3.19 Zinc A single datum was available of 63.0-279.0 mg Zn/kg DW in radiolarians (Table 3.1). Zinc uptake by a gram-positive bacterium, B. firmus, isolated from Hong Kong sediments, is best predicted by free Zn2þ ion activity and passive diffusion through the plasma membrane (Keung et al., 2008). Bacteria compete actively with sediments and higher trophic levels regarding zinc uptake in salt marsh ecosystems (Pomeroy et al., 1966). Bacteria and their metabolic byproducts also play an important role in removal of zinc and other metals from seawater and subsequent deposition in sediments. In one study, mixed cultures of bacteria removed up to 85% of 65Zn from seawater in 120 h (McLerran and Holmes, 1974). Interaction effects of zinc with salts of other metals on protozoan growth are documented. Cristigera, a ciliate protozoan, had reduced growth—and presumably altered zinc uptake—when held in media containing salts of zinc, lead, and mercury (Gray, 1974). Growth reduction was observed in Cristigera during 5 h exposure in solutions containing 0.05-0.12 mg Zn/L (USEPA, 1980, 1987); other species of protists tested were more resistant to zinc (Spear, 1981).
3.20 Literature Cited Almeida, A., Cunha, A., Fernandes, S., Sobral, P., Alcantara, F., 2007. Copper effects on bacterial activity of estuarine silty sediments. Estuar. Coastal Shelf Sci. 73, 743–752. Babich, H., Borenfreund, E., 1990. In vitro cytotoxicities of inorganic lead and di- and trialkyl lead compounds to fish cells. Bull. Environ. Contam. Toxicol. 44, 456–460. Babich, H., Stotzky, G., 1982. Nickel toxicity to microbes: Effect of pH and implications for acid rain. Environ. Res. 29, 335–350.
110 Chapter 3 Baldi, F., Pepi, M., Filipelli, M., 1993. Methylmercury resistance in Desulfovibrio desulfuricans in relation to methylmercury degradation. Appl. Environ. Microbiol. 59, 2479–2485. Bender, M.L., Lorens, R.B., Williams, D.F., 1975. Sodium, magnesium, and strontium in the tests of planktonic foraminifera. Micropaleontology 21, 448–459. Berk, S.K., Mills, A.L., Henricks, D.L., Colwell, R.R., 1978. Effects of ingesting mercury containing bacteria on mercury tolerance and growth in ciliates. Microb. Ecol. 4, 319–330. Bernat, P., Dlugonski, J., 2006. Acceleration of tributyltin chloride (TBT) degradation in liquid cultures of the filamentous fungus Cunninghamella elegans. Chemosphere 62, 3–8. Bryan, G.W., 1963. The accumulation of radioactive caesium by marine invertebrates. J. Mar. Biol. Assoc. UK 43, 519–539. Button, D.K., Dunker, S.S., 1971. Biological effects of copper and arsenic pollution. U.S. Environmental Protection Agency Contract 18050 DLW, Report R71-8. University of Alaska (College), Alaska, 59 pp. Cardwell, R.D., Sheldon, A.W., 1986. A risk assessment concerning the fate and effects of tributyltins in the aquatic environment. In: Maton, G.L. (Ed.), Proceedings Oceans 86 Conference, September 23-25, 1986, vol. 4, Organotin Symposium. Available from Marine Technology Society, 2000 Florida Avenue NW, Washington, DC, pp. 1117–1129. Cha, J.S., Cooksey, D.A., 1991. Copper resistance in Pseudomonas syringae mediated by periplasmic and outer mechanism proteins. Proc. Natl. Acad. Sci. USA 88, 8915–8919. Chau, Y.K., Wong, P.T.S., Kramer, O., Bengert, G.A., Cruz, R.B., Kinrade, J.O., et al., 1980. Occurrence of tetraalkyllead compounds in the aquatic environment. Bull. Environ. Contam. Toxicol. 24, 265–269. Choi, S.C., Bartha, R., 1993. Cobalamin-mediated mercury methylation by Desulfovibrio desulfuricans LS. Appl. Environ. Microbiol. 59, 290–295. Clark, E.A., Sterritt, R.M., Lester, J.N., 1988. The fate of tributyltin in the aquatic environment. Environ. Sci. Technol. 22, 600–604. Colwell, R.R., Nelson Jr., J.D., 1974. Bacterial mobilization of mercury in Chesapeake Bay. In: Proceedings of an International Conference on Transport of Persistent Chemicals in Aquatic Ecosystems, Ottawa, Canada, pp. 1–10. Colwell, R.R., Nelson Jr., J.D., 1975. In: Metabolism of Mercury Compounds in Microorganisms. Report 600/3-75-077. U.S. Environmental Protection Agency, Narragansett, RI, pp. 1–84. Colwell, R.R., Sayler, G.S., Nelson Jr., J.D., Justice, A., 1976. Microbial mobilization of mercury in the aquatic environment. In: Nriagu, J.O. (Ed.), Environmental Biogeochemistry, Vol. 2. Metals Transfer and Ecological Mass Balances. Ann Arbor Science Publication, Ann Arbor, MI, pp. 437–487. Coppellotti, O., 1998. Sensitivity to copper in a ciliate as a possible component of biological monitoring in the Lagoon of Venice. Arch. Environ. Contam. Toxicol. 35, 417–425. Cruz, A., Caetano, T., Suzuki, S., Mendo, S., 2007. Aeromonas veronii, a tributyltin (TBT)-degrading bacterium isolated from an estuarine environment, Rio de Aveiro in Portugal. Mar. Environ. Res. 64, 639–650. Culkin, F., Riley, J.P., 1958. The occurrence of gallium in marine organisms. J. Mar. Biol. Assoc. UK 37, 607–615. Di Leonardo, R., Bellanca, A., Capotondi, L., Cundy, A., Neri, R., 2007. Possible impacts of Hg and PAH contamination on benthic foraminiferal assemblages: An example from the Sicilian coast, central Mediterranean. Sci. Total Environ. 388, 168–183. Dubey, S.K., Roy, U., 2003. Biodegradation of tributyltins (organotins) by marine bacteria. Appl. Organomet. Chem. 17, 3–8. Dubey, S.K., Tokashiki, T., Suzuki, S., 2006. Microarray-mediated transcriptome analysis of the tributyltin (TBT)-resistant bacterium Pseudomonas aeruginosa 25W in the presence of TBT. J. Microbiol. 44, 200–205. Ehrlich, H.L., 1976. Manganese as an energy source for bacteria. In: Nriagu, J.O. (Ed.), Environmental Biogeochemistry, Vol. 2. Metals Transfer and Ecological Mass Balances. Ann Arbor Science Publication, Ann Arbor, MI, pp. 633–644. Eisler, R., 2000. Tin. In: Handbook of Chemical Risk Assessment. Health Hazards to Humans, Plants, and Animals. Vol. 1, Metals. Lewis Publishers, Boca Raton, FL, pp. 551–603. Eisler, R., 2006. Mercury Hazards to Living Organisms. CRC Press, Boca Raton, FL, p. 312.
Protists
111
Fisher, N.S., Breslin, V.T., Levandowsky, M., 1995. Accumulation of silver and lead in estuarine microzooplankton. Mar. Ecol. Prog. Ser. 116, 207–215. Fulladosa, E., Desjardin, V., Murat, J.C., Gourdon, R., Villaescusa, I., 2006. Cr(VI) reduction into Cr(III) as a mechanism to explain the low sensitivity of Vibrio fischeri bioassay to detect chromium pollution. Chemosphere 65, 644–650. Fulladosa, E., Murat, J.C., Bollinger, J.C., Villaescusa, I., 2007. Adverse effects of organic arsenical compounds towards Vibrio fischeri bacteria. Sci. Total Environ. 377, 207–213. Furukawa, A., Tonomura, K., 1971. Enzyme system involved in the decomposition of phenyl mercuric acetate by mercury-resistant Pseudomonas. Agric. Biol. Chem. 35, 604–610. Girotti, S., Botelli, L., Fini, F., Monari, M., Andreani, G., Isani, G., et al., 2006. Trace metals in arcid clam Scapharca inaequivalvis: Effects of molluscan extracts on bioluminescent bacteria. Chemosphere 65, 627–633. Gordon, A.S., Donat, J.R., Kango, R., Dyer, B., Stuart, L., 2000. Dissolved copper-complexing ligands in cultures of marine bacteria and estuarine water. Mar. Chem. 70, 149–160. Gray, J.S., 1974. Synergistic effects of three heavy metals on growth rates of a marine ciliate protozoan. In: Vernberg, F.J., Vernberg, W.B. (Eds.), Pollution and Physiology of Marine Organisms. Academic Press, New York, pp. 465–485. Gray, J.S., Ventilla, R.J., 1971. Pollution effects on micro- and meiofauna of sand. Mar. Pollut. Bull. 2, 39–43. Harwood-Sears, V., Gordon, A.S., 1990. Copper-induced production of copper-binding supernatant proteins by the marine bacterium Vibrio alginolyticus. Appl. Environ. Microbiol. 56, 1327–1332. Harwood-Sears, V., Gordon, A.S., 1994. Regulation of extracellular copper-binding proteins in copper-resistant and copper-sensitive mutants of Vibrio alginolyticus. Appl. Environ. Microbiol. 60, 1749–1753. Iverson, W.P., Huey, C., Brinckman, F.E., Jewett, K.L., Blair, W., 1973. Biological and nonbiological transformations of mercury in aquatic systems. In: Krenkel, P.A. (Ed.), Heavy Metals in the Aquatic Environment. Pergamon, Elmsford, NY, pp. 193–195. Iyer, A., Mody, K., Jha, B., 2004. Accumulation of hexavalent chromium by an exopolysaccharide producing marine Enterobacter cloaceae. Mar. Pollut. Bull. 49, 974–977. Jeanthon, C., Prieur, D., 1990. Susceptibility to heavy metals and characterization of heterotrophic bacteria isolated from two hydrothermal vent polychaete annelids. Appl. Environ. Microbiol. 56, 3308–3314. Jernelov, A., 1969. Conversion of mercury compounds. In: Miller, C.W., Berg, G.G. (Eds.), Chemical Fallout, Current Research on Persistent Pesticides. Chas. C. Thomas, Springfield, IL, pp. 68–74. Johnson, D.L., 1972. Bacterial reduction of arsenate in seawater. Nature 240, 44–45. Kadar, E., Santos, R.S., Powell, J.J., 2006. Biological factors influencing tissue compartmentalization of trace metals in the deep-sea hydrothermal vent bivalve Bathymodiolus azoricus at geochemically distinct vents sites of the mid-Atlantic Ridge. Environ. Res. 101, 221–229. Kasprzak, K.S., 1987. Nickel. Adv. Mod. Environ. Toxicol. 11, 145–183. Keung, C.F., Guo, F., Qian, P., Wang, W.X., 2008. Influences of metal-ligand complexes on the cadmium and zinc biokinetics in the marine bacterium, Bacillus firmus. Environ. Toxicol. Chem. 27, 131–137. Komura, I., Izaki, K., 1971. Mechanism of mercuric chloride resistance in microorganisms. I. Vaporization of a mercury compound from mercuric chloride by multiple drug resistant strains of Escherichia coli. J. Biochem. (Tokyo) 70, 885–893. Krinsley, D., 1960. Trace elements in the tests of planktonic foraminifera. Micropaleontology 6, 297–300. Maclean, F.I., Lucis, O.J., Shakh, Z.Z., Jansz, E.R., 1972. The uptake and cellular distribution of Cd and Zn in microorganisms. Fed. Proc. FASEB 31, 699. Maguire, R.J., 1991. Aquatic environmental aspects of non-pesticidal organotin compounds. Water Pollut. Res. J. Can. 26, 243–360. Maguire, R.J., Wong, P.T.S., Rhamey, J.S., 1984. Accumulation and metabolism of tri-n-butyltin cation by a green alga, Ankistrodesmus falcatus. Can. J. Fish Aquat. Sci. 41, 537–540. Marchetti, R., 1978. Acute toxicity of alkyl leads to some marine organisms. Mar. Pollut. Bull. 9, 206–207. Markwiese, J.T., Meyer, J.S., Colberg, P.J.S., 1998. Copper tolerance in iron-reducing bacteria: Implications for copper mobilization in sediments. Environ. Toxicol. Chem. 17, 675–678.
112 Chapter 3 Martin, J.H., Knauer, G.A., 1973. The elemental composition of plankton. Geochim. Cosmochim. Acta 37, 1639–1653. McLerran, C.J., Holmes, C.W., 1974. Deposition of zinc and cadmium by marine bacteria in estuarine sediments. Limnol. Oceanol. 19, 988–1001. Mendo, S.A., Nogueira, P.R., Ferreira, S.C.N., Silva, R.G., 2003. Tributyltin and triphenyltin toxicity on benthic estuarine bacteria. Fresenius Environ. Bull. 12, 1361–1367. Mimura, H., Sato, R., Furyama, Y., Taniike, A., Yagi, M., Yoshida, K., 2008. Adsorption of tributyltin by tributyltin resistant marine Pseudoalteromonas sp. Cells. Mar. Pollut. Bull. 57, 877–882. Miranda, C.D., Rojas, R., 2006. Copper accumulation by bacteria and transfer to scallop larvae. Mar. Pollut. Bull. 52, 293–300. Misra, T.K., 1992. Bacterial resistance to inorganic mercury salts and organomercurials. Plasmid 27, 4–16. Nakamura, K., 1989. Volatilization of fluorescein mercuric acetate by marine bacteria from Minamata Bay. Bull. Environ. Contam. Toxicol. 42, 785–790. Nakamura, K., 1994. Mercury compounds-decomposing bacteria in Minamata Bay. In: Proceedings of the International Symposium on Assessment of Environmental Pollution and Health Effects from Methylmercury, Kumamoto, Japan, October 8-9, 1993. National Institute for Minamata Disease, Minamata City, Kumamoto, Japan, pp. 198–209. Nakamura, K., Silver, S., 1994. Molecular analysis of mercury-resistant Bacillus isolates from sediment of Minamata Bay, Japan. Appl. Environ. Microbiol. 60, 4599–4956. Nakamura, K., Fujisaki, T., Tamashiro, H., 1986. Characteristics of Hg-resistant bacteria isolated from Minamata Bay sediment. Environ. Res. 40, 58–67. Nakamura, K., Fujisaki, T., Shibata, Y., 1988. Mercury-resistant bacteria in the sediment of Minamata Bay. Nippon Suisan Gakkashi 54, 1359–1363. Nakamura, K., Sakamoto, M., Uchiyama, H., Yagi, O., 1990. Organomercurial-volatilizing bacteria in the mercury-polluted sediment of Minamata Bay, Japan. Appl. Environ. Microbiol. 56, 304–305. Nalecz-Jawecki, G., Demkowicz-Dobrzanski, K., Sawicki, J., 1993. Protozoan Spirostomum ambiguum as a highly sensitive bioindicator for rapid and easy determination of water quality. Sci. Total Environ. 2 (Suppl.), 1227–1234. National Academy of Sciences (NAS), 1975. Medical and Biological Effects of Environmental Pollutants: Nickel. National Research Council, NAS, Washington, DC, 277 pp. Nelson Jr., J.D., Colwell, R.R., 1975. The ecology of mercury-resistant bacteria in Chesapeake Bay. Microbiol. Ecol. 1, 191–218. Nelson, D.L., Kennedy, E.P., 1971. Magnesium transport in Escherichia coli. J. Biol. Chem. 246, 3042–3049. Nelson, J.D., Blair, W., Brinckman, F.E., Colwell, R.R., Iverson, W.P., 1973. Biodegradation of phenylmercuric acetate by mercury-resistant bacteria. Appl. Microbiol. 26, 321–326. Pain, A., Cooney, J.J., 1998a. Characterization of organotin-resistant bacteria from Boston Harbor sediments. Arch. Environ. Contam. Toxicol. 35, 412–416. Pain, A., Cooney, J.J., 1998b. Characterization of organotin-resistant bacteria from Boston Harbor sediments. Arch. Environ. Contam. Toxicol. 35, 412–416. Parker, J.G., 1979. Toxic effects of heavy metals upon cultures of Uronema marinum (Ciliophora: uronematidae). Mar. Biol. 54, 17–24. Parrott, J.L., Sprague, J.B., 1993. Patterns in toxicity of sublethal mixtures of metals and organic chemicals determined by rmicrotox and by DNA, RNA, and protein content of fathead minnows (Pimephales promelas). Can. J. Fish. Aquat. Sci. 50, 2245–2253. Pomeroy, L.R., Odum, E.P., Johannes, R.E., Roffman, B., 1966. Flux of phosphorus-32 and zinc-65 through a salt-marsh ecosystem. Proc. Symp. IAEA 177–188. Prior, S., Riemann, B., 1998. Effects of tributyltin, linear alkylbenzenesulfonates, and nutrients (nitrogen and phosphorus) on nucleoid-containing bacteria. Environ. Toxicol. Chem. 17, 1473–1480. Roy, U., Dubey, S.K., Bhosle, S., 2004. Tributyltin chloride-utilizing bacteria from marine ecosystem of west coast of India. Curr. Sci. 86(5), 702–705.
Protists
113
Silver, S., Waldrhaug, M., 1992. Gene regulation of plasmid and chromosome-determined inorganic ion transport in bacteria. Microbiol. Rev. 56, 195–228. Silver, S., Endo, G., Nakamura, K., 1994. Mercury in the environment and in the laboratory. J. Jpn. Soc. Water Environ. 17, 235–243. Smith, P.J., 1978. Structure/Activity Relationships for Di- and Triorganotin Compounds. I.T.R.I. Rep. 569. Available from International Tin Research Institute, Greenford, Middlesex, UK, 16 pp. Spear, P.A., 1981. Zinc in the aquatic environment: Chemistry, distribution, and toxicology. Natl. Res. Coun. Can. Publ., NRCC 17589, 145. Stutzenberger, F.J., Bennet, E.O., 1965. Sensitivity of mixed populations of Staphylococcus aureus and Escherichia coli to mercurials. Appl. Microbiol. 13, 570–574. Summers, A.O., Silver, S., 1972. Mercury resistance in a plasmid-bearing strain of Escherichia coli. J. Bacteriol. 112, 1228–1236. Sunderman Jr., F.W., 1981. Recent research on nickel carcinogenesis. Environ. Health Perspect. 40, 131–141. Sunderman Jr., F.W., Aito, A., Berlin, A., Bishop, C., Buringh, E., Davis, W., et al. (Eds.), 1984. Nickel in the Human Environment. IARC Sci. Publ. No. 53. International Agency for Research on Cancer, Oxford University Press, Oxford, 530 pp. Thompson, T.G., Chow, T.J., 1955. The strontium-calcium atom ratio in carbonate-secreting marine organisms. Deep Sea Res. 3 (Suppl.), 20–39. Tkeshelashvili, L.K., Reid, T.M., McBride, T.J., Loeb, L.A., 1993. Nickel induces a signature mutation for oxygen free radical damage. Cancer Res. 53, 4172–4174. Tugrul, S., Balkas, T.I., Goldberg, E.D., 1983. Methyltins in the marine environment. Mar. Pollut. Bull. 14, 297–303. U.S. Environmental Protection Agency (USEPA), 1980. Ambient water quality criteria for zinc. USEPA Rep. 440/5-80-079, 158 pp. USEPA, 1985a. Ambient water quality criteria for lead—1984. USEPA Rep. 440/5-84-027, 81 pp. USEPA, 1985b. Drinking water criteria document for nickel. USEPA Rep. 600/X-84-193-1, pp. 1–64. USEPA, 1987. Ambient water quality criteria for zinc—1987. USEPA Rep. 440/5-87-003, 207 pp. U.S. Public Health Service (USPHS), 1977. Criteria for a recommended standard: occupational exposure to inorganic nickel. U.S. Dept. Health Educ. Welfare, PHS, Center Dis. Control. Nat. Inst. Occupat. Safety Health, DHEW (NIOSH), Publ. No. 77-164, pp. 1–282. USPHS, 1993. In: Toxicological profile for nickel. Rep. TP-92/14. USPHS, Agen. Toxic Subs. Dis Regis., Atlanta, GA, pp. 1–158. USPHS, 1995. Toxicological profile for nickel (update). USPHS, Agen. Toxic Subs. Dis. Regis., Atlanta, GA, pp. 1–244. Vosjan, J.H., Van de Hoek, G.J., 1972. A continuous culture of Desulfovibrio on a medium containing mercury and copper ions. Neth. J. Sea Res. 5, 440–444. Walker, J.D., Colwell, R.R., 1974. Mercury-resistant bacteria and petroleum degradation. Appl. Microbiol. 27, 285–287. Wood, J.M., Kennedy, F.S., Rosen, C.G., 1968. Synthesis of methylmercury compounds by extracts of a methanogenic bacterium. Nature 220, 173–174. World Health Organization (WHO), 1991. Nickel. Environ. Health Crit. 18, 1–383. Yemenicioglu, D.R., Saydam, C., Salihoglu, I., 1987. Distribution of tin in the northeastern Mediterranean. Chemosphere 16, 429–443. Zuckerman, J.J., Reisdorf, R.P., Ellis III, H.V., Wilkinson, R.R., 1978. Organotins in biology and the environment. In: Brinckman, F.E., Bellama, J.M. (Eds.), Organometals and Organometalloids, Occurrence and Fate in the Environment. American Chemical Society Symposium Series 82, Washington, DC, pp. 388–424.
This page intentionally left blank
CHAPTER 4
Sponges There are approximately 5000 species in this group, most of them marine. The largest, the loggerhead sponge Spheciospongia vesparum, may reach 2 m in diameter. These multicellular organisms are sessile and aquatic, with a single body cavity lined in part or almost wholly by collared flagellate cells. Sponges possess numerous body pores in the body wall through which water enters, and one or more larger pores through which it exits. In general, sponges have a calcareous, horny, or siliceous skeleton. Sponges have been proposed as heavy metal biomonitors owing to their ability to accumulate metals (Cebrian et al., 2003; Hansen et al., 1995; Olesen and Weeks, 1994; Patel et al., 1985; Perez et al., 2005) and because they show biological and biochemical responses when submitted to metal insult (Agell et al., 2001; Berthet et al., 2005; Cebrian et al., 2003, 2006; Philp, 1999; Rao et al., 2006; Schroeder et al., 2000). For example, high accumulations of metals alter the composition of sugars, proteins, and lipids, especially in near-shore sponges which usually have higher accumulations than offshore conspecifics (Rao et al., 2006). Despite their widespread geographic distribution, comparatively little is known of the trace metal composition of this group (Table 4.1).
4.1 Aluminum Aluminum content ranges from 37.3 to 3700.0 mg Al/kg DW (dry weight) whole sponge (Table 4.1), being higher in polluted areas.
4.2 Antimony A single datum is available of 0.089 mg Sb/kg DW whole sponge (Table 4.1).
4.3 Arsenic Arsenic seems to concentrate in lipid extracts of sponges (6400.0 mg As/kg; Table 4.1); however, of all groups examined by Vaskovsky et al. (1972), the annelids, molluscs, and asteroid echinoderms had the highest arsenic contents, and sponges had the lowest. 115
116 Chapter 4 Table 4.1: Trace Element Concentrations in Field Collections of Sponges Element and Organism
Concentration
Reference
a
Aluminum Halichondria panicea, whole Petrosia testudinaria
b
3700.0 DW 205.9 DW vs. 37.3 DW
1 10
Antimony Halichondria panicea, whole
0.089 DW
2
<0.11-47.7 DW
9
Halichondria panacea Lipid extract; whole Whole
6400.0 FW 2.8 DW
3 2
Petrosia testudinariab
2.3 DW vs. 1.3 DW
Arsenic Guam; 11 spp.; 4 locales; 1998-1999; whole
10
Barium Sponges; whole
0.22 FW
4
Guam; 11 spp.; 4 locales; 1998-1999; whole
0.13-0.86 DW
9
Halichondria panicea; whole
0.85 DW
2
Sponges; whole
0.17-1.0 FW; 1.2-4.5 DW
5
Cadmium
Cobalt Petrosia testudinariab
3.0 DW vs. 0.1 DW
10
Copper Sponges; whole
0.99-5.0 FW; 8.5-31.0 DW
6
Crambe crambe; Spain; contaminated site (97.0 mg Cu/kg DW sediment) vs. reference site (6.0 mg Cu/kg DW)
Max. 280.0 DW vs. <20.0 DW
Sponges; whole; 3 spp.
13.0-34.0 DW
8
Sponges; whole; 4 spp.; 3 sites; Catalonia, Spain; 2003-2004 Chondrosia reniformis Crambe crambe
8.2-11.3 DW 9.1-42.2 DW
11 11
12
(Continues)
Sponges Table 4.1: Element and Organism Phorbas tenacior Dysidea avara Petrosia testudinariab
117
Cont’d
Concentration 34.0-91.0 DW 97.4-299.3 DW 2.5 DW vs. 2.0 DW
Reference
a
11 11 10
Gallium Halichondria panicea; whole
0.93 FW
1
4040.0 DW
1
Iron Halichondria panicea; whole b
305.5 DW vs. 66.3 DW
10
1.5-2.1 DW 0.3-1.8 DW 0.5-0.8 DW 0.1-0.8 DW
11 11 11 11
Crambe crambe; Spain; contaminated site vs. reference site
Max. 130.0 DW vs. <60.0 DW
12
Guam; 11 spp.; 4 locales; 1998-1999; whole
(0.25-8.1) DW
Petrosia testudinariab
0.3 DW vs. no data
10
91.0 DW vs. 2.0 DW
10
Petrosia testudinaria Lead
Catalonia, Spain; summer; 2003-2004; 3 sites; whole Chondrosia reniformis Crambe crambe Phorbas tenacior Dysidea avara
9
Manganese Petrosia testudinariab Mercury Halichondria panicea; whole
0.33 DW
2
22.0 DW
8
Nickel Halichondria sp.; whole; Sweden b
5.0 DW vs. 4.0 DW
10
Petrosia testudinariab
1.0 DW vs. 0.7 DW
10
Petrosia testudinaria Selenium
Silver Guam; 11 spp; 4 locales; 1998-1999; whole
<0.11-0.47 DW
9 (Continues)
118 Chapter 4 Table 4.1: Element and Organism
Cont’d
Concentration
Reference
a
Strontium Sponges; whole
0.31 FW
4
Vanadium Crambe crambe; Spain; contaminated site vs. reference site
Max. 15.0 DW vs. <6.0 DW
12
Petrosia testudinariab
0.6 DW vs. no data
10
Zinc Halichondria panicea; whole
89.0-152.0 DW
7
Sponges; whole
4.7-30.0 FW; 63.0-180.0 DW; 93.0-360.0 AW
6
Petrosia testudinariab
0.6 DW vs. no data
10
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Culkin and Riley, 1958; 2, Leatherland and Burton, 1974; 3, Vaskovsky et al., 1972; 4, Mauchline and Templeton, 1966; 5, Bernhard and Zattera, 1975; 6, Lowman et al., 1966; 7, Ireland, 1973; 8, Jenkins, 1980; 9, Denton et al., 2006; 10, Rao et al., 2006; 11, Cebrian et al., 2007; 12, Cebrian et al., 2003. b Gulf of Mannar; India; 2004; polluted area; whole less calcareous spicules; 0.5-1.0 km from shore vs. 5.0-7.0 km from shore.
4.4 Barium A single datum is available of 0.22 mg Ba/kg FW (fresh weight) whole sponge (Table 4.1).
4.5 Cadmium Maximum concentrations of 4.5 mg Cd/kg DW and 1.0 mg Cd/kg FW are reported in whole sponges (Table 4.1). Isolated cells of the sponge Scopalina lyphropoda subjected for 3 h to 0.005 or 0.010 mg Cd/L showed enhanced pseudopodia formation, cell motility, and cell aggregation at the concentrations tested (Cebrian and Uriz, 2007a). Larvae of two Mediterranean Sea sponges Cranke cranke and Scopalina lophyropoda exposed to 0.005 mg Cd/L for 1 week had normal settlement and juvenile survival (Cebrian and Uriz, 2007c). Calcium is important in cadmium uptake (Cebrian and Uriz, 2007b). Isolated cells of Scopalina lophyropoda were held for 3 h and larvae for 7 days in calcium-free seawater (CFSW), seawater (SW), or SW with 0.005 mg Cd/L (CdCFSW). Sponge cells incubated in CdCFSW took up as much cadmium as SW controls, but little uptake in CFSW. Cadmium initially appeared to accelerate larval settlement, but after 5 days mortality increased and settlement decreased (Cebrian and Uriz, 2007b).
Sponges
119
4.6 Cobalt The maximum concentration of cobalt in sponges from polluted areas is 3.0 mg Co/kg DW (Table 4.1). The introduction of lithogenic material into the sea from the rivers of the west coast of Puerto Rico, and fallout, had a direct effect on cobalt burdens in Spheciospongia sp. and Iricinia sp. (Lowman et al., 1967). Sponges distant from the outflows contained lower amounts of total ash and fallout radioisotopes of cobalt, cerium, zirconium, and ruthenium (Lowman et al., 1967). In general, organisms of a single species that is widely distributed geographically have lower trace metal concentrations with increasing distance from land masses.
4.7 Copper Highest values recorded for copper in sponges are 5.0 mg/kg FW and 299.3 mg/kg DW (Table 4.1). High concentrations of copper in Crambe crambe, were associated with inhibited growth and decreased fecundity (Cebrian et al., 2003). Isolated cells of Scopalina lophyropoda subjected to 0.03 and 0.1 mg Cu/L for 3 h, as was true for cadmium, showed enhanced pseudopodia formation, cell motility, and cell aggregation at the concentrations tested (Cebrian and Uriz, 2007a). Calcium seems to control copper metabolism in sponges. Isolated cells of Scopalina lophyropoda were subjected for 3 h and larvae for 7 days to CFSW, SW, or CFSW with copper (CuCFSW) at 0.03 mg Cu/L (Cebrian and Uriz, 2007b). Sponge cells incubated in CuCFSW took up Cu as SW controls, with little uptake in CFSW. In the short term, copper accelerated larval settlement but decreased larval settlement and increased mortality after 5 days (Cebrian and Uriz, 2007b). Larvae of two Mediterranean Sea sponges, Crambe crambe and Scopalina lophyropoda exposed to 0.03 mg Cu/L for 1 week had normal settlement and juvenile survival (Cebrian and Uriz, 2007c). However, copper (0.03 mg/L) in combination with 0.005 mg/L of a mixture of polycyclic aromatic hydrocarbons (benzo(a)pyrene, benzo(e)pyrene, benzo(a)anthracene), benzo(b)fluoranthene, benzo(j)fluoranthene, and benzo(k) fluoranthene) acted more than additively to inhibit the development of sponge larvae with resultant population declines expected (Cebrian and Uriz, 2007c).
4.8 Gallium A single datum was available of 0.93 mg Ga/kg FW whole sponge (Table 4.1)
4.9 Iron Iron content in whole sponges ranged from 66.3 to 4040.0 mg Fe/kg DW (Table 4.1).
120 Chapter 4
4.10 Lead The maximum lead concentration recorded of 130.0 mg Pb/kg DW was in Crambe crambe from a lead-contaminated site in Spain (Table 4.1). Concentrations in whole sponges collected from various locations in Guam ranged up to 8.1 mg Pb/kg DW; this animal was collected near a fuel station and commercial port (Denton et al., 2006).
4.11 Manganese Manganese concentrations in whole sponge, Petrosia testudinaria, taken in 2004 from an industrialized area in the Gulf of Mannar, India, were significantly higher in specimens collected 0.5-1.0 km from shore than those collected 5.0-7.0 km from shore: 91.0 mg Mn/kg DW vs. 2.0 mg Mn/kg DW (Rao et al., 2006; Table 4.1).
4.12 Mercury A single datum was available of 0.33 mg Hg/kg DW whole sponge (Table 4.1). Isolated cells of a Mediterranean Sea sponge, Scopalina lyphropoda, held in 0.001 or 0.005 mg Hg/L for 3 h, showed enhanced cell aggregation, a reduction in cell motility, and the absence of pseudopodia (Cebrian and Uriz, 2007a).
4.13 Nickel Whole sponges, Halichondria sp., from Sweden contained an average of 22.0 m Ni/kg DW (Table 4.1).
4.14 Plutonium Sponges reportedly concentrate et al., 1971).
239
Pu from seawater by as much as 2300-fold (Noshkin
4.15 Ruthenium Soluble radioruthenium-106 was accumulated by sponges 5-10 times more rapidly than insoluble forms; similar observations were noted for shrimps, mussels, sea anemones, and algae (Ancellin and Bovard, 1971).
4.16 Selenium Whole Petrosia testudinaria from the Gulf of Mannar, India, in 2004 contained up to 1.0 mg Se/kg DW (Rao et al., 2006; Table 4.1).
Sponges
121
4.17 Silver The maximum concentration recorded in whole sponges from Guam is 0.47 mg/kg DW whole animal (Denton et al., 2006; Table 4.1).
4.18 Strontium A single datum was available of 0.31 mg Sr/kg FW whole sponge (Table 4.1).
4.19 Vanadium Whole sponges contained up to 15.0 mg V/kg DW (Table 4.1; Cebrian et al., 2003).
4.20 Zinc Limited data indicate that maximum zinc concentrations in whole sponges are 30.0 mg/kg fresh weight, 180.0 mg/kg dry weight, and 360.0 mg/kg ash weight (Table 4.1).
4.21 Literature Cited Agell, G., Uriz, M.J., Cebrian, E., Marti, R., 2001. Does stress protein induction modify natural toxicity in sponges? Environ. Toxicol. Chem. 20, 2588–2593. Ancellin, J., Bovard, P., 1971. Observations concernant les contaminations experimentales et les contaminations “in situ” d’especes marines par le ruthenium 106. Rev. Int. Ocean. Med. 21, 85–92. Bernhard, M., Zattera, A., 1975. Major pollutants in the marine environment. In: Pearson, E.A., Frangipane, E.D. (Eds.), Marine Pollution and Marine Waste Disposal. Pergamon, Elmsford, New York, pp. 195–300. Berthet, B., Mouneyrac, C., Perez, T., Amiard-Triquet, C., 2005. Metallothionein concentration in sponges (Spongia officinalis) as a biomarker of metal contamination. Comp. Biochem. Physiol. 141C, 306–313. Cebrian, E., Uriz, M.J., 2007a. Contrasting effects of heavy metals on sponge cell behavior. Arch. Environ. Contam. Toxicol. 53, 552–558. Cebrian, E., Uriz, M.J., 2007b. Do heavy metals play an active role in sponge cell behaviour in the absence of calcium? Consequences in larval settlement. J. Exp. Mar. Biol. Ecol. 346, 60–65. Cebrian, E., Uriz, M.J., 2007c. Contrasting effects of heavy metals and hydrocarbons on larval settlement and juvenile survival in sponges. Aquat. Toxicol. 81, 137–143. Cebrian, E., Marti, R., Uriz, M.J., Turon, X., 2003. Sublethal effects of contamination on the Mediterranean sponge Crambe crambe: metal accumulation and biological responses. Mar. Pollut. Bull. 46, 1273–1284. Cebrian, E., Marti, R., Agell, G., Uriz, M.J., 2006. Response of the Mediterranean sponge Chondrosia reniformis Nardo to heavy metal pollution. Environ. Pollut. 141, 452–458. Cebrian, E., Uriz, M.J., Turon, X., 2007. Sponges as biomonitors of heavy metals in spatial and temporal surveys in northwestern Mediterranean: multispecies comparison. Environ. Toxicol. Chem. 26, 2430–2439. Culkin, F., Riley, J.P., 1958. The occurrence of gallium in marine organisms. J. Mar. Biol. Assoc. UK 37, 607–615. Denton, G.R.W., Concepcion, L.P., Wood, H.R., Morrison, R.J., 2006. Trace metals in marine organisms from four harbours in Guam. Mar. Pollut. Bull. 52, 1784–1804. Hansen, I.V., Weeks, J.M., Depledge, M.H., 1995. Accumulation of copper, zinc, cadmium and chromium by the marine sponge Halichondria panicea Pallas and the implications for biomonitoring. Mar. Pollut. Bull. 31, 133–138.
122 Chapter 4 Ireland, M.P., 1973. Result of fluvial zinc pollution on the zinc content of littoral and sublittoral organisms in Cardigan Bay, Wales. Environ. Pollut. 4, 27–35. Jenkins, D.W., 1980. Biological monitoring of toxic trace metals. Volume 2. Toxic trace metals in plants and animals of the world. Part II. U.S. EPA Report 600/3-80-091, pp. 505–618. Leatherland, T.M., Burton, J.D., 1974. The occurrence of some trace metals in coastal organisms with particular reference to the Solent region. J. Mar. Biol. Assoc. UK 54, 457–468. Lowman, F.G., Phelps, D.K., Ting, R.Y., Escalera, R.M., 1966. Progress Summary Report No. 4, Marine Biology Program June 1965-June 1966. Puerto Rico Nuclear Center Report PRNC 85, pp. 1–57. Lowman, F.G., Stevenson, R.A., Escalera, R.M., Ufret, S.L., 1967. The effects of river outflows upon the distribution patterns of fallout radioisotopes in marine organisms. In: Proceedings of an International Symposium on Radioecological Concentration Processes, 1966. Stockholm, Int. Atom. Ener. Agency, pp. 735–752. Mauchline, J., Templeton, W., 1966. Strontium, calcium, and barium in marine organisms from the Irish Sea. J. Cons. Perm. Int. Explor. Mer. 30, 161–170. Noshkin, V.E., Bowen, V.T., Wong, K.M., Barke, J.C., 1971. Plutonium in North Atlantic ocean organisms: ecological relationships. In: Nelson, D.J. (Ed.), Radionuclides in Ecosystems. Proceedings of the Third National Symposium on Radioecology, May 10-12, 1971, Oak Ridge, Tennessee, Vol. 2, pp. 681–688. Available from NTIS Springfield, Virginia. Olesen, T.M.E., Weeks, J.M., 1994. Accumulation of Cd by the marine sponge Halichondria panicea Pallas: effects upon filtration rate and its relevance for biomonitoring. Bull. Environ. Contam. Toxicol. 52, 722–728. Patel, B., Balani, M.C., Patel, S., 1985. Sponge “sentinel” of heavy metals. Sci. Total. Environ. 41, 143–152. Perez, T., Longet, D., Schembri, T., Rebouillon, P., Vacelet, J., 2005. Effects of 12 years’ operation of a sewage treatment plant on trace metal occurrence within a Mediterranean commercial sponge (Spongia officinalis, Demospongiae). Mar. Pollut. Bull. 50, 301–309. Philp, R.B., 1999. Cadmium content of the marine sponge Microciona prolifera, other sponges, water and sediment from the eastern Florida panhandle: possible effects on Microciona cell aggregation and potential roles of low pH and low salinity. Comp. Biochem. Physiol. 124C, 41–49. Rao, J.V., Kavitha, P., Reddy, N.C., Rao, T.G., 2006. Petrosia testudinaria as a biomarker for metal contamination at Gulf of Mannar, southeast coast of India. Chemosphere 65, 634–638. Schroeder, H.C., Shostak, K., Gamulin, V., Skorokhod, A., Kavsan, V., Muller, I.M., et al., 2000. Purification, cDNA cloning and expression of cadmium-inducible cysteine-rich metallothionein-like protein from the marine sponge Suberites domuncula. Mar. Ecol. Prog. Ser. 200, 149–157. Vaskovsky, V.E., Korotchenko, O.D., Kosheleva, L.P., Levin, V.S., 1972. Arsenic in the lipid extracts of marine invertebrates. Comp. Biochem. Physiol. 41B(4), 777–784.
CHAPTER 5
Coelenterates This phylum includes all diploblastic animals. Two distinct groups comprise this phylum: the Cnidarians, characterized by muscular movements, nematocyst presence, and occurrence as polyp or medusa; and the Ctenophores which retain the ciliary locomotion of the planula, are without nematocysts, and are not assigned either to the polyp or medusa type. There are about 9000 species of Cnidarians; the largest solitary Cnidarian is a sea anemone, Stoichactis sp., 0.5 m high and 1.5 m in diameter. Major subgroups within the Cnidaria include the Hydrozoa (about 2700 species of which 700 are free-living medusa, or jellyfish) and the Anthozoa. There are about 6000 species of Anthozoans, including anemones, corals, and sea pens; all are polyps, either solitary or colonial, and all are marine. There are about 80 species of Ctenophores, of which the largest is Cestus veneris, 1.5 m in length. Ctenophores, also known popularly as comb jellies or sea walnuts, have an apical statocyst, eight rows of combs, and usually two tentacles armed with numerous adhesive cells.
5.1 Aluminum Highest values recorded for aluminum in different species of coelenterates are 453.0 mg/kg DW (dry weight), and 3600.0 mg/kg AW (ash weight) (Table 5.1). The significance of aluminum in coelenterates and other marine organisms is imperfectly understood.
5.2 Antimony Limited data indicate that antimony concentrations range from 0.022 to 0.043 mg/kg DW (Table 5.1).
5.3 Arsenic Maximum concentrations of arsenic recorded in coelenterates were 2200.0 mg/kg FW (fresh weight) in lipid extracts from a jellyfish and 72.0 mg/kg DW in whole anemones (Table 5.1). 123
124 Chapter 5 Table 5.1: Aluminum, Antimony, and Arsenic Concentrations in Field Collections of Coelenterates Element and Organism
Concentration
Reference
a
Aluminum Coral, Alcyonium digitatum
90.0 DW
1
Coral, Alcyonium digitatum
453.0 DW
2
Jellyfish, Aurelia sp.
0.6 FW
3
Coral, Montastrea annularis, skeleton deposits
<125.0 DW
4
Anemone, Tealia felina
80.0 DW
1
Jellyfish, Velella lata
1600.0-3600.0 AW
5
Jellyfish, Pelagia sp.
0.043 DW
6
Anemone, Tealia felina
0.022 DW
7
Anemone
6.6 DW
8
Jellyfish, Cyanea arctica, lipid extract of whole organism
2200.0 FW
9
Antimony
Arsenic
Guam; 1998-1999; 4 locales; whole Soft coral, Sinularia sp. Hard coral, Pocilopora damicornis Hard coral, Fungia sp. Hard coral, Acropora formosa Jellyfish, Pelagia sp. Anemone, Tealia felina
0.01-2.33 DW <0.01-67.1 DW
10 10
0.19-0.25 DW 0.14 DW 11.0 DW 72.0 DW
10 10 6 7
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Riley and Segar, 1970; 2, Culkin and Riley, 1958; 3, Matsumoto et al., 1964; 4, Goreau, 1977; 5, Bieri and Krinsley, 1958; 6, Leatherland et al., 1973; 7, Leatherland and Burton, 1974; 8, Gorgy et al., 1948; 9, Vaskovsky et al., 1972; 10, Denton et al., 2006.
5.4 Barium Corals, especially hermatypic inshore species, appear to selectively accumulate barium to a maximum of 85.0 mg Ba/kg DW (Table 5.2). Corals reportedly lose barium after death (Livingston and Thompson, 1971). As will be seen later, post-mortem changes in metal and metalloid content of many groups of organisms are well documented and contraindicate
Coelenterates 125 Table 5.2: Barium, Bismuth, and Boron Concentrations in Field Collections of Coelenterates Element and organism
Concentration
Reference
Coelenterates
0.03-0.55 FW
1
Corals, 34 spp. Deep open ocean Shallow open ocean Shallow coastal zone
16.0-60.0 DW 15.0-30.0 DW 9.0-85.0 DW
2 2 2
Ctenophore, Pleurobrachia pileus
60.0 AW
3
Jellyfish, Velella lata
<100.0 AW
4
<2.0 DW
2
Ctenophore, Beroe cucumis
115.0 AW
5
Corals, 34 spp. Deep open ocean Shallow open ocean Shallow coastal zone
50.0-85.0 DW 65.0-100.0 DW 40.0-110.0 DW
2 2 2
Jellyfish, Cyanea capillata
100.0 AW
5
a
Barium
Bismuth Corals, 34 spp. Boron
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Mauchline and Templeton, 1966; 2, Livingston and Thompson, 1971; 3, Vinogradova and Koual’skiy, 1962; 4, Bieri and Krinsley, 1958; 5, Nicholls et al., 1959.
the collection of dead organisms, including corals, for baseline residue purposes. Barium was initially incorporated into the coral skeleton along with calcium at the time of skeleton formation; this was also true for other elements including strontium, vanadium, copper, boron, lithium, and zinc (Livingston and Thompson, 1971).
5.5 Bismuth All available data indicate that bismuth levels are less than 2.0 mg Bi/kg DW in all tissues analyzed (Table 5.2).
5.6 Boron As was true for barium, corals accumulated boron from ambient seawater to a maximum of 110.0 mg B/kg DW (Table 5.2).
126 Chapter 5
5.7 Cadmium Cadmium concentrations in representative species of coelenterates ranged from 0.01 to 5.3 mg/kg DW whole organism (Table 5.3). In laboratory studies, sea anemones, Bundosoma cavernata, held in seawater containing high sublethal concentrations of 7.0 mg Cd/L for up to 7 days had significant increases in glutamate and alanine (Kasschau et al., 1980); also, ambient concentrations as low as 0.04 mg Cd/L were associated with disrupted enzyme metabolism in the hydroid Campanularia flexuosa (Moore, 1977; Moore and Stebbing, 1976). The hydrozoan Laomedea loveni experienced 50% irreversible polyp retraction in 7 days at 0.003 mg Cd/L at 10 ppt salinity; organisms were comparatively resistant at elevated salinities and reduced temperatures (Theede et al., 1979). Colonies of the tropical coral Pocillopora damicornis were exposed to 0, 0.005, or 0.05 mg Cd/L for up to 14 days (Mitchelmore et al., 2007). All corals exposed to 0.05 mg Cd/L
Table 5.3: Cadmium Concentrations in Field Collections of Coelenterates Organism
Concentration
Reference
Corals; 5 spp.; Arabian Sea Skeleton Tissues
0.3-2.6 DW 0.04-2.2 DW
7 7
Coral, Alcyonium digitatum
4.1 DW
1
Jellyfish, Aurelia sp.
0.1 FW
2
Corals, 34 spp.
<2.0 DW
3
Guam; 1998-1999; 4 locales; whole Soft coral, Sinularia sp. Hard coral, Pocilopora damicornis Hard coral, Fungia sp. Hard coral, Acropora formosa
<0.05-0.16 DW <0.04-0.24 DW 0.01-0.08 DW 0.09 DW
6 6 6 6
Jellyfish, Pelagia sp.
5.3 DW
4
Anemone, Tealia felina
0.07 DW
5
Anemone, Tealia felina
0.7 DW
1
a
Values are in mg Cd/kg fresh weight (FW) or dry weight (DW). a 1, Riley and Segar, 1970; 2, Matsumoto et al., 1964; 3, Livingston and Thompson, 1971; 4, Leatherland et al., 1973; 5, Leatherland and Burton, 1974; 6, Denton et al., 2006; 7, Anu et al., 2007.
Coelenterates 127 died by day 4 of exposure. After 14 days, cadmium concentrations, in mg Cd/kg DW, were 0.005 in controls and 0.0086 in the 0.005 mg Cd/L group (Mitchelmore et al., 2007). Exposure of temperate water sea anemones, Anthopleura elegantissima to 0.02 mg Cd/L for 14 days resulted in concentrations of 0.003 mg Cd/kg DW (Mitchelmore et al., 2003a), and this is similar to findings for the same species exposed to 0.10 mg Cd/L for 7 days (Mitchelmore et al., 2003b).
5.8 Cesium Radiocesium accumulation in Actinia equina, Tealia felina, Metridium senile, and Calliactes parasitica was documented by Bryan (1963). In all cases, accumulation increased with increasing exposure time, suggesting that equilibrium may not be reached for months or years. Highest concentrations were observed in tentacles from all four species, with concentration values over the ambient medium ranging from 16.6 to 19.6. In general, the lowest concentration factors measured were in whole organism, with values between 4.2 and 11.6 (Bryan, 1963).
5.9 Chromium Chromium concentrations in field collections of coelenterates ranged from <0.12 to 35.0 mg/ kg DW (Table 5.4). Chromium, and also scandium and titanium, were largely associated with detrital phases in corals from chromium-rich areas (Livingston and Thompson, 1971).
5.10 Cobalt Cobalt values were low among near-shore coral species from Hawaii, Tahiti, Samoa, and other areas, seldom exceeding 0.04 mg Co/kg DW (Table 5.4). Higher values were measured in medusa and especially among some species of deep-ocean ahermatypic corals (Table 5.4).
5.11 Copper Copper concentrations in coelenterates were comparatively low except for anemones T. felina (52.0 mg/kg DW) and jellyfish Cyanea capillata (68.0 mg/kg DW) (Table 5.5). Highest accumulations of copper in marine invertebrate organisms were observed in molluscan tissues and soft parts, followed by crustaceans, macrophytes, annelids, tunicates, algae, echinoderms, and coelenterates, in that general sequence (Eisler, 1979). Lowest concentrations of copper were consistently found among the marine vertebrate groups examined (Eisler, 1979).
128 Chapter 5 Table 5.4: Chromium and Cobalt Concentrations in Field Collections of Coelenterates Element and Organism
Concentration
Reference
Corals; 5 spp.; Arabian Sea Skeleton Tissues
0.82-5.44 DW 2.8-15.9 DW
8 8
Coral, Alcyonium digitatum
<0.4 DW
1
Corals, 34 spp. Deep open ocean Shallow open ocean Shallow coastal zone
0.8-3.0 DW 2.0-35.0 DW 0.2-23.0 DW
2 2 2
Guam; 1998-1999; 4 locations; whole Soft coral, Sinularia sp. Hard coral, Pocilopora damicornis Hard coral, Fungia sp. Hard coral, Acropora formosa
<0.15-0.31 DW <0.12-0.33 DW 0.24-0.34 DW 0.27 DW
7 7 7 7
Ctenophore, Pleurobrachia pileus
10.0 AW
3
Anemone, Tealia felina
0.37 DW
1
Jellyfish, Velella lata
>100.0 AW
4
Corals; 5 spp.; Arabian Sea Skeleton Tissues
0.79-9.82 DW 0.2-8.9 DW
8 8
Coral, Acropora sp.; exoskeleton Samoa Tahiti
0.004 DW 0.004 DW
5 5
Coral, Alcyonium digitatum
0.6 DW
1
Corals, 34 spp. Deep open ocean Shallow open ocean Shallow coastal zone
0.4-105.0 DW 0.2-3.0 DW 0.04-2.0 DW
2 2 2
Jellyfish, Cyanea capillata
3.0 AW
6
Coral, Favia sp.; exoskeleton
0.011 DW
5
a
Chromium
Cobalt
(Continues)
Coelenterates 129 Table 5.4:
Cont’d
Element and Organism
Concentration
Reference
Coral, Fungia sp. Septa Base
0.002 DW 0.001 DW
5 5
Coral, Leptastrea spp.; exoskeleton
0.012 DW
5
Coral, Leptoria spp.; exoskeleton
0.002 DW
5
Coral, Pocillopora sp.; exoskeleton Hawaii Tahiti
0.007 DW 0.001 DW
5 5
Anemone, Tealia felina
<0.2 DW
1
a
Values are in mg element/kg dry weight (DW) or ash weight (AW). a 1, Riley and Segar, 1970; 2, Livingston and Thompson, 1971; 3, Vinogradova and Koual’skiy, 1962; 4, Bieri and Krinsley, 1958; 5, Veek and Turekian, 1968; 6, Nicholls et al., 1959; 7, Denton et al., 2006; 8, Anu et al., 2007.
Laboratory studies demonstrate that marine hydroid coelenterates were quite sensitive to copper salts, and this may account, in part, for the low uptake of copper by coelenterates. Colonies of the tropical coral P. damicornis were exposed to 0, 0.005, or 0.05 mg Cu/L for up to 9 days (Mitchelmore et al., 2007). All corals exposed to 0.05 mg Cu/L died by day 9. Copper concentrations at day 4, in mg Cu/kg DW were 0.004 in controls, 0.013 in the 0.005 mg Cu/L group, and 0.13 in the 0.05 mg Cu/L group (Mitchelmore et al., 2007). Serious adverse effects to hydroids were observed at nominal concentrations of 0.0012-0.05 mg Cu/L (Moore, 1977; Moore and Stebbing, 1976; Stebbing, 1976). The ctenophore, Pleurobrachia pileus, held in seawater containing 0.033 mg Cu/L for 24 h had a 50% death rate (USEPA, 1980). The coral, Acropora formosa, exposed to 0.01-0.04 mg Cu/L for 48 h lost most of their symbiotic algae (Jones, 1997). The sea anemone. Anemonia viridis, held in seawater containing 0.05-0.2 mg Cu/L for 5 days exhibited immediate tentacle retraction, copious production of mucus, progressive visible bleaching, and loss of zooxanthellae (Harland and Nganro, 1990). Zooxanthellae accumulate copper and their expulsion is considered a form of copper regulation (Harland and Nganro, 1990).
5.12 Gallium A single value for gallium was available of 0.05 mg Ga/kg DW in a whole coral, Alcyonium digitatum (Culkin and Riley, 1958).
130 Chapter 5 Table 5.5: Copper Concentrations in Field Collections of Coelenterates Organism
Concentration
Reference
Coral, Alcyonium digitatum
6.2 DW
1
Alcyonium digitatum
9.7 DW
2
Jellyfish, Aurelia sp.
0.7 FW
3
Ctenophore, Beroe cucumis
700.0 AW
4
Corals; 5 spp.; Arabian Sea Skeleton Tissues
0.49-1.88 DW 0.18-6.48 DW
14 14
Corals, 34 spp. Deep open ocean Shallow open ocean Shallow coastal zone
<2.0-14.0 DW 2.0-10.0 DW <2.0-10.0 DW
5 5 5
Jellyfish, Cyanea capillata; whole Pacific Ocean New England Sweden
13.0 AW 8.2 DW 68.0 DW
6 10 10
Guam; 1998-1999; 4 locales; whole Soft coral, Sinularia sp. Hard coral, Pocilopora damicornis Hard coral, Fungia sp. Hard coral, Acropora formosa
0.4-0.9 DW Max. 0.2 DW 0.4-1.0 DW <0.1 DW
13 13 13 13
Coral, Meandrina meandrites
22.0 (14.0-33.0) FW
Octacorals; Venezuela; whole; 5 spp.
0.9-3.1 DW
Ctenophore, Pleurobrachia pileus
300.0 AW
8
Anemone, Tealia felina
57.0 DW
2
Jellyfish, Velella lata
71.0-220.0 AW
9
Wales; 1989; coastal area Anemones; whole Soft corals; whole
0.6 FW 1.0 FW
a
7 11
12 12
Values are in mg Cu/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Culkin and Riley, 1958; 2, Riley and Segar, 1970; 3, Matsumoto et al., 1964; 4, Nicholls et al., 1959; 5, Livingston and Thompson, 1971; 6, Nicholls et al., 1959; 7, Lowman et al., 1966; 8, Vinogradova and Koual’skiy, 1962; 9, Bieri and Krinsley, 1958; 10, Jenkins, 1980; 11, Jaffe et al., 1992; 12, Morris et al., 1989; 13, Denton et al., 2006; 14, Anu et al., 2007.
Coelenterates 131
5.13 Iron On a DW basis, the highest concentrations of iron recorded were among ahermatypic deep ocean corals (up to 6500.0 mg Fe/kg) and lowest values (<5.0 mg Fe/kg) among reefbuilding corals and jellyfish (Table 5.6).
5.14 Lead In general, deep-sea ahermatypic corals contained the highest concentrations of lead recorded among coelenterates, while jellyfishes and coastal zone corals contained the lowest (Table 5.7). Between 1954 and 1980—prior to the wide-spread use of unleaded gasoline products—there were significant increases in lead concentrations in marine corals and other biota as a direct result of increased global lead availability during that period (Dodge and Gilbert, 1984). The lead concentration in exoskeleton of Porites spp. corals from Ogasawara Island, Japan, gradually increased over the past 108 years with steep increases in the 1950s owing to Table 5.6: Iron Concentrations in Field Collections of Coelenterates Organism
Concentration
Reference
Corals; 5 spp.; Arabian Sea Skeletons Tissues
0.53-12.8 DW 1.2-62.9 DW
8 8
Coral, Alcyonium digitatum
438.0 DW
1
Alcyonium digitatum
250.0 DW
2
Jellyfish, Aurelia sp.
0.9 FW
3
Corals Deep open ocean Shallow open ocean Shallow coastal zone
30.0-6500.0 DW 14.0-780.0 DW <5.0-880.0 DW
4 4 4
Coral, Montastrea annularis
363.0-506.0 DW
5
Ctenophore, Pleurobrachia pileus
5000.0 AW
6
Anemone, Tealia felina
730.0 DW
2
Jellyfish, Velella lata
>10.0 AW
7
a
Values are in mg Fe/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Culkin and Riley, 1958; 2, Riley and Segar, 1970; 3, Mauchline and Templeton, 1966; 4, Livingston and Thompson, 1971; 5, Goreau, 1977; 6, Vinogradova and Koual’skiy, 1962; 7, Bieri and Krinsley, 1958; 8, Anu et al., 2007.
132 Chapter 5 Table 5.7: Lead and Lithium Concentrations in Field Collections of Coelenterates Element and Organism
Concentration
Reference
a
Lead Coral, Alcyonium digitatum
24.0 DW
1
Jellyfish, Aurelia sp.
0.8 FW
2
Ctenophore, Beroe cucumis
6.0 AW
3
Corals Deep open ocean Shallow open ocean Shallow coastal zone
<2.0-42.0 DW <2.0-9.0 DW <2.0-4.0 DW
4 4 4
Corals; 5 spp.; Arabian Sea Skeletons Tissues
0.7-23.8 DW 0.3-20.7 DW
7 7
Jellyfish, Cyanea capillata
6.0 AW
3
Ctenophore, Pleurobrachia pileus
40.0 AW
6
Coral, Porites spp.; exoskeleton Japan; 1994-2000 Hong Kong; 1990-1993 Bermuda; 1980-1983 St. Croix; 1954-1980
0.400 DW 0.222 DW 0.01-0.134 DW 0.021-0.207 DW
6 6 7 8
Anemone, Tealia felina
2.6 DW
1
Jellyfish, Velella lata
>10.0 AW
5
Corals, 23 spp. Deep open ocean Shallow open ocean Shallow coastal zone
1.0-3.0 DW 1.0 DW 0.5-2.0 DW
4 4 4
Ctenophore, Pleurobrachia pileus
600.0 AW
6
Lithium
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Riley and Segar, 1970; 2, Matsumoto et al., 1964; 3, Nicholls et al., 1959; 4, Livingston and Thompson, 1971; 5, Bieri and Krinsley, 1958; 6, Vinogradova and Koual’skiy, 1962; 7, Anu et al., 2007; 8, Inoue et al., 2006; 7, Shen and Boyle, 1987; 8, Dodge and Gilbert, 1984.
lead-containing industrial discharges from Japan (Inoue et al., 2006). In Porites spp. exoskeletons from Hainan Island, China, there is a marked decline in lead content in recent years attributed to the introduction of unleaded gasoline in China and Indonesia (Inoue et al., 2006).
Coelenterates 133
5.15 Lithium Lithium was selectively accumulated by corals (Livingston and Thompson, 1971). Concentrations among corals on a DW basis show little variability with all values measured in the range 0.5-3.0 mg Li/kg (Table 5.7).
5.16 Manganese Manganese concentrations were highest among the corals—especially non-reef-building species that frequented the deep open ocean—and lowest, in general, among polyps (Table 5.8).
Table 5.8: Manganese and Mercury Concentrations in Field Collections of Coelenterates Element and Organism
Concentration
Reference
a
Manganese Coral, Alcyonium digitatum
3.7 DW
1
Anemone, Anemonia sulcata
21.3 AW
2
Corals; 5 spp.; Arabian Sea Skeleton Tissue
0.3-4.7 DW 0.2-2.5 DW
9 9
Corals, 34 spp. Deep open ocean Shallow open ocean Shallow coastal zone
2.0-2100.0 DW <2.0-465.0 DW 2.0-130.0 DW
3 3 3
Ctenophore, Pleurobrachia pileus
20.0 AW
4
Anemone, Tealia felina
9.3 DW
1
Jellyfish, Velella lata
7.0-41.0 AW
5
Jellyfish, Pelagia sp.
0.07 DW
6
Anemone; Minamata Bay, Japan
41.0 DW
7
Anemone, Tealia felina
0.86 DW
8
Mercury
Values are in mg element/kg dry weight (DW) or ash weight (AW). a 1, Riley and Segar, 1970; 2, Chipman and Thommeret, 1970; 3, Livingston and Thompson, 1971; 4, Vinogradova and Koual’skiy, 1962; 5, Bieri and Krinsley, 1958; 6, Leatherland et al., 1973; 7, Matida and Kumada, 1969; 8, Leatherland and Burton, 1974; 9, Anu et al., 2007.
134 Chapter 5
5.17 Mercury Mercury concentrations were low among coelenterates except for species collected from the mercury-contaminated Minamata Bay, Japan (Table 5.8). Mercury is among the most toxic metals known to marine organisms including coelenterates; this point will be developed in detail later in this volume. In the case of coelenterates, concentrations as low as 0.0017 mg Hg/L depressed the growth of the hydrozoan C. flexuosa; moreover, concentrations an order of magnitude lower adversely affected metabolism of various lysosomal enzymes in that species (Moore, 1977; Moore and Stebbing, 1976; Stebbing, 1976). Higher sublethal concentrations of 1.2 mg Hg/L were associated with increased concentrations of free amino acids in the anemone B. cavernata following exposure for up to 7 days (Kasschau et al., 1980).
5.18 Molybdenum Concentrations of molybdenum in coelenterates examined were uniformly low and near the detection limits of the analytical procedures used (Table 5.9).
5.19 Nickel Accumulations of nickel up to 23.0 mg Ni/kg DW are documented in corals, especially among nonhermatypic corals and selected medusa (Table 5.9).
5.20 Radium Corals appear to reflect environmental levels of radium. The radium/calcium ratio in corals is reportedly similar to that of seawater (Moore et al., 1973).
5.21 Rubidium Corals from different habitats and geographic areas all contained less than 10.0 mg Rb/kg DW whole organism (Livingston and Thompson, 1971).
5.22 Ruthenium Laboratory studies with radioruthenium-106 and selected species of invertebrates, including coelenterates, demonstrated that all organisms examined accumulated 106Ru over ambient seawater levels by 30- to 50-fold factors in 10 days (Ancellin et al., 1967).
Coelenterates 135 Table 5.9: Molybdenum and Nickel Concentrations in Field Collections of Coelenterates Element and Organism
Concentration
Reference
a
Molybdenum Beroe cucumis
3.0 AW
1
Corals, 34 spp.
<2.0 DW
2
Jellyfish, Cyanea capillata
3.0 AW
1
Jellyfish, Velella lata
>10.0 AW
3
Coral, Alcyonium digitatum
17.0 DW
4
Corals; 5 spp.; Arabian Sea Skeleton Tissue
2.07-12.7 DW 0.5-10.1 DW
6 6
Corals, 24 spp. Deep open ocean Shallow open ocean Shallow coastal zone
<2.0-23.0 DW 2.0-19.0 DW <2.0-3.0 DW
2 2 2
Pleurobranchia pileus
50.0 AW
5
Anemone, Tealia felina
3.3 DW
4
Jellyfish, Velella lata
33.0-220.0 AW
3
Nickel
Values are in mg element/kg dry weight (DW) or ash weight (AW). a 1, Nicholls et al., 1959; 2, Livingston and Thompson, 1971; 3, Bieri and Krinsley, 1958; 4, Riley and Segar, 1970; 5, Vinogradova and Koual’skiy, 1962; 6, Anu et al., 2007.
5.23 Scandium Scandium concentrations in corals never exceeded 0.25 mg Sc/kg DW (Table 5.10).
5.24 Silicon Silicon was relatively abundant in nonhermatypic as well as reef-building corals, with concentrations up to 2000.0 mg Si/kg DW documented (Table 5.10).
5.25 Silver All silver concentrations were less than 0.26 mg Ag/kg DW except for a single value of 2.7 mg/kg DW in Sinularia sp., a soft coral (Table 5.10). Measurable differences in silver accumulations were evident between tissues, and between geographic areas (Table 5.10).
136 Chapter 5 Table 5.10: Scandium, Silicon, and Silver Concentrations in Field Collections of Coelenterates Element and Organism
Concentration
Reference
0.01-0.17 DW 0.01-0.24 DW 0.005-0.25 DW
1 1 1
Corals, 34 spp. Deep open ocean Shallow open ocean Shallow coastal zone
15.0-2000.0 DW 45.0->2000.0 DW 20.0->2000.0 DW
1 1 1
Jellyfish, Velella lata
>10.0 AW
2
Coral, Acropora spp.; exoskeleton Samoa Tahiti
0.014 DW 0.022 DW
3 3
Coral, Alcyonium digitatum
<0.03 DW
4
Corals, 34 spp.
<1.0 DW
1
Coral, Favia spp.; exoskeleton
0.024 DW
3
Coral, Fungia spp. Septa Base
0.065 DW 0.022 DW
3 3
Guam; 1998-1999; 4 locations; whole Soft coral, Sinularia sp. Hard coral, Pocilopora damicornis Hard coral, Fungia sp. Hard coral, Acropora formosa
<0.11-2.7 DW <0.10-0.26 DW 0.14-0.24 DW <0.11 DW
6 6 6 6
Hard coral, Leptastrea spp.; exoskeleton
0.10 DW
3
Hard coral, Leptoria spp.; exoskeleton
0.057 DW
3
Pleurobranchia pileus
4.0 AW
5
a
Scandium Corals, 34 spp. Deep open ocean Shallow open ocean Shallow coastal zone Silicon
Silver
(Continues)
Coelenterates 137 Table 5.10:
Cont’d
Element and Organism
Concentration
Reference
Hard coral, Pocilopora spp.; exoskeleton Hawaii Tahiti
0.034 DW 0.018 DW
3 3
Anemone, Tealia felina
0.05 DW
4
Jellyfish, Velella lata
>3.0 AW
2
a
Values are in mg element/kg dry weight (DW) or ash weight (AW). a 1, Livingston and Thompson, 1971; 2, Bieri and Krinsley, 1958; 3, Veek and Turekian, 1968; 4, Riley and Segar, 1970; 5, Vinogradova and Koual’skiy, 1962; 6, Denton et al., 2006.
5.26 Strontium Strontium was especially abundant among coelenterates with calcified exoskeletons and concentrations >6300.0-10,800.0 mg Sr/kg DW were not uncommon in that group; however, strontium concentrations were significantly lower among polyps and medusa (Table 5.11).
5.27 Thorium Thorium concentrations were always less than 0.01 mg Th/kg DW (Table 5.11). This was attributed primarily to the very low thorium content of seawater (Moore et al., 1973).
5.28 Tin Tin concentrations in coelenterates ranged between 4.0 and 20.0 mg Sn/kg AW (Table 5.11). Tributyltins are the most toxic of all tin compounds tested. In the case of the hydroid, C. flexuosa, complete growth inhibition occurred in 11 days during exposure to 0.001 mg Sn (as tributyltin)/L (Hall and Pinkney, 1985).
5.29 Titanium Titanium residues in coelenterates ranged up to 330.0 mg Ti/kg on a DW basis and up to 1400.0 on an AW basis (Table 5.11). The significance of these very considerable titanium accumulations in coelenterates is unknown.
138 Chapter 5 Table 5.11: Strontium, Thorium, Tin, and Titanium Concentrations in Field Collections of Coelenterates Element and Organism
Concentration
Reference
a
Strontium Coral, Alcyonium digitatum
220.0 DW
1
Coelenterates
0.02-1.4 FW
2
Corals, 14 spp. Deep open ocean Shallow open ocean Shallow coastal zone
8200.0-10,000.0 DW 8200.0-9320.0 DW 7070.0-8680.0 DW
3 3 3
Coral, Montastrea annularis
6300.0-7160.0 DW
4
Ctenophore, Pleurobrachia pileus
1000.0 AW
5
Coral, Porites sp., skeletal parts
2500.0-10,800.0 DW
6
Anemone, Tealia felina
9.5 DW
1
Jellyfish, Velella lata
>200.0 AW
7
<0.01 DW
8
Ctenophore, Beroe cucumis
7.0 AW
9
Corals, 34 spp.
<5.0 DW
3
Jellyfish, Cyanea capillata
4.0 AW
9
Ctenophore, Pleurobrachia pileus
20.0 AW
5
Corals, 34 spp. Deep open ocean Shallow open ocean Shallow coastal zone
<50.0-330.0 DW <20.0-60.0 DW <20.0-80.0 DW
3 3 3
Jellyfish, Cyanea capillata
3.0 AW
9
Ctenophore, Pleurobrachia pileus
30.0 AW
5
Jellyfish, Velella lata
460.0-1400.0 AW
7
Thorium Coelenterates Tin
Titanium
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Riley and Segar, 1970; 2, Mauchline and Templeton, 1966; 3, Livingston and Thompson, 1971; 4, Goreau, 1977; 5, Vinogradova and Koual’skiy, 1962; 6, Polyakov and Krasnov, 1976; 7, Bieri and Krinsley, 1958; 8, Moore et al., 1973; 9, Nicholls et al., 1959.
Coelenterates 139
5.30 Uranium Uranium values of 1.5-4.8 mg/kg coral DW were not unusual (Table 5.12). Uranium values in corals reflected seawater values, with nonhermatypic corals of the open ocean containing more uranium than most near-shore hermatypes (Livingston and Thompson, 1971). Uranium content in corals also varied as a function of growth rate. For example, rapidly growing reef corals incorporated up to 60% more uranium and up to 9% more strontium than did ahermatypic corals (Moore et al., 1973).
Table 5.12: Uranium and Vanadium Concentrations in Field Collections of Coelenterates Element and Organism
Concentration
Reference
a
Uranium Coral, Acropora sp.; exoskeleton Samoa Tahiti
2.82 DW 1.95 DW
1 1
Corals, 34 spp. Deep open ocean Shallow open ocean Shallow coastal zone
Max. 4.8 DW Max. 4.7 DW Max. 4.8 DW
2 2 2
Coral, Favia sp.; exoskeleton
1.52 DW
1
Coral, Fungia spp. Septa Base
2.06 DW 2.19 DW
1 1
Coral, Leptastrea spp.; exoskeleton
2.83 DW
1
Coral, Leptoria spp.; exoskeleton
2.00 DW
1
Coral, Pocilopora spp.; exoskeleton Hawaii Tahiti
2.11 DW 2.17 DW
1 1
Ctenophore, Beroe cucumis
8.0 AW
3
Corals, 34 spp.
<10.0 DW
2
Jellyfish, Cyanea capillata
5.0 AW
3
Jellyfish, Velella lata
>70.0 AW
4
Vanadium
Values are in mg element/kg dry weight (DW) or ash weight (AW). a 1, Veek and Turekian, 1968; 2, Livingston and Thompson, 1971; 3, Nicholls et al., 1959; 4, Bieri and Krinsley, 1958.
140 Chapter 5
5.31 Vanadium Vanadium concentrations in coelenterates were usually at or near the detection limits of the analytical methodologies used (Table 5.12).
5.32 Zinc Zinc residues in coelenterates ranged widely (Table 5.13). The highest zinc residue reported of 603.0 mg Zn/kg DW in the anemone Actina equina was from specimens collected from a metalscontaminated area (Ireland, 1973); however, most values were substantially lower (Table 5.13). Table 5.13: Zinc Concentrations in Field Collections of Coelenterates Organism
Concentration
Reference
Anemone, Actina equina
167.0-603.0 DW
1
Soft coral, Alcyonia alcyonium; whole
9.6 FW
9
Coral, Alcyonium digitatum
46.0 DW
2
Jellyfish, Aurelia sp.
3.4 FW
3
Corals; 5 spp.; Arabian Sea Skeleton Tissue
1.2-2.6 DW 0.7-9.3 DW
Corals Deep open ocean, 7 spp. Shallow open ocean, 8 spp. Shallow coastal zone, 8 spp.
2.0-9.0 DW <2.0-70.0 DW 2.0-7.0 DW
4 4 4
Coral, Eusmilia fastigata
74.0-80.0 FW; 75.0-80.0 DW; 77.0-83.0 AW
5
Coral, Manicina aerolata
59.0-63.0 FW; 60.0-68.0 DW; 65.0-69.0 AW
5
Coral, Meandrina meandrites
54.0-120.0 FW; 55.0-120.0 DW; 56.0-120.0 AW
5
Ctenophores; whole; Calcasieu River Estuary
(31.0-64.0) DW
Plumose anemone, Metridium senile; whole
18.0 FW
9
Jellyfish, Pelagia sp.
28.0 DW
6
Ctenophore, Pleurobrachia pileus
900.0 AW
7
Anemone, Tealia felina
200.0 DW
8
Anemone, Tealia felina
280.0 DW
2
a
11 11
10
Values are in mg Zn/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Ireland, 1973; 2, Riley and Segar, 1970; 3, Matsumoto et al., 1964; 4, Livingston and Thompson, 1971; 5, Lowman et al., 1966; 6, Leatherland et al., 1973; 7, Vinogradova and Koual’skiy, 1962; 8, Leatherland and Burton, 1974; 9, Morris et al., 1989; 10, Ramelow et al., 1989; 11, Anu et al., 2007.
Coelenterates 141
5.33 Literature Cited Ancellin, J., Bovard, P., Vilquin, A., 1967. New studies on experimental contamination of marine species by ruthenium-106. In: Actes du Congress Internationale Radioprotection Milieu. Soc. Franc. Radioprotect., Toulouse, France, January 14–16, 1967, pp. 213–234. Anu, G., Kumar, N.C., Jayalakshmi, K.V., Nair, S.M., 2007. Monitoring of heavy metal partitioning in reef corals of Lakshadweep Archipelago, Indian Ocean. Environ. Monit. Assess. 128, 195–208. Bieri, R., Krinsley, D.M., 1958. Trace elements in the pelagic coelenterate, Velella lata. J. Mar. Res. 16, 246–254. Bryan, G.W., 1963. The accumulation of radioactive caesium by marine invertebrates. J. Mar. Biol. Assoc. UK 43, 519–539. Chipman, W., Thommeret, J., 1970. Manganese content and the occurrence of fallout 54Mn in some marine benthos of the Mediterranean. Bull. Inst. Oceanol. 69(1402), 1–15. Culkin, F., Riley, J.P., 1958. The occurrence of gallium in some marine organisms. J. Mar. Biol. Assoc. UK 37, 607–615. Denton, G.R.W., Concepcion, L.P., Wood, H.R., Morrison, R.J., 2006. Trace metals in marine organisms from four harbours in Guam. Mar. Pollut. Bull. 52, 1784–1804. Dodge, R.E., Gilbert, T.R., 1984. Chronology of lead pollution contained in banded coral skeletons. Mar. Biol. 82, 9–13. Eisler, R., 1979. Copper accumulations in coastal and marine biota. In: Nriagu, J.O. (Ed.), Copper in the Environment, Part 1: Ecological Cycling. John Wiley, New York, pp. 383–449. Goreau, T.T., 1977. Coral skeletal chemistry: Physiological and environmental regulation of stable isotopes and trace metals in Montastrea annularis. Proc. R. Soc. Lond. B 196, 291–315. Gorgy, S., Rakestraw, N.W., Fox, D.L., 1948. Arsenic in the sea. J. Mar. Res. 7, 22–32. Hall Jr., L.W., Pinkney, A.E., 1985. Acute and sublethal effects of organotin compounds on aquatic biota: An interpretive literature evaluation. CRC Crit. Rev. Toxicol. 14, 159–209. Harland, A.D., Nganro, N.R., 1990. Copper uptake by the sea anemone Anemonia viridis and the role of zooxanthellae in metal regulation. Mar. Biol. 104, 297–301. Inoue, M., Hata, A., Suzuki, A., Nohara, M., Shikazono, N., Yim, W.W.S., et al., 2006. Distribution and temporal changes of lead in the surface seawater in the western Pacific and adjacent seas derived from coral skeletons. Environ. Pollut. 144, 1045–1052. Ireland, M.P., 1973. Result of fluvial zinc pollution on the zinc content of littoral and sublittoral organisms in Cardigan Bay, Wales. Environ. Pollut. 4, 27–35. Jaffe, R., Fernandez, C.A., Alvarado, J., 1992. Trace metal analyses in octacorals by microwave acid digestion and graphite furnace atomic-absorption spectrometry. Talanta 39, 113–117. Jenkins, D.W., 1980. Biological Monitoring of Toxic Trace Metals. Volume 2. Toxic Trace Metals in Plants and Animals of the World. Part II. U.S. Environmental Protection Agency Report 600/3-80-091, pp. 505–618. Jones, R.J., 1997. Zooxanthellae loss as a bioassay for assessing stress in corals. Mar. Ecol. Prog. Ser. 149, 163–171. Kasschau, M.R., Skaggs, M.M., Chen, E.C.M., 1980. Accumulation of glutamate in sea anemones exposed to heavy metals and organic amines. Bull. Environ. Contam. Toxicol. 25, 873–878. Leatherland, T.M., Burton, J.D., 1974. The occurrence of some trace metals in coastal organisms with particular reference to the Solent region. J. Mar. Biol. Assoc. UK 54, 457–468. Leatherland, T.M., Burton, J.D., Culkin, F., McCartney, M.J., Morris, R.J., 1973. Concentrations of some trace metals in pelagic organisms and of mercury in Northeast Atlantic Ocean water. Deep Sea Res. 20, 679–685. Livingston, H.D., Thompson, G., 1971. Trace element concentrations in some modern corals. Limnol. Oceanol. 16, 786–795. Lowman, F.G., Phelps, D.K., Ting, R.Y., Escalera, R.M., 1966. Progress Summary Report No. 4, Marine Biology Program, June 1965-June 1966, Puerto Rico Nuclear Center Report PRNC 85, pp. 1–57. Matida, Y., Kumada, H., 1969. Distribution of mercury in water, bottom mud, and aquatic organisms of Minamata Bay, the River Agano, and other water bodies in Japan. Bull. Freshw. Fish. Res. Lab. Tokyo 19(2), 73–93. Matsumoto, T., Satake, M., Yamamoto, J., Haruna, S., 1964. On the micro constituent elements in marine invertebrates. J. Oceanol. Soc. Jpn. 20(3), 15–19.
142 Chapter 5 Mauchline, J., Templeton, W.L., 1966. Strontium, calcium, and barium in marine organisms from the Irish Sea. J. Cons. 39, 161–170. Mitchelmore, C.L., Ringwood, A.H., Weis, V.M., 2003a. Differential accumulation of cadmium and changes in glutathione levels as a function of symbiotic state in the sea anemone Anthopleura elegantissima. J. Exp. Mar. Biol. Ecol. 284, 71–85. Mitchelmore, C.L., Verde, E.A., Ringwood, A.H., Weis, V.M., 2003b. Differential accumulation of heavy metals in the sea anemone Anthopleura elegantissima as a function of symbiotic state. Aquat. Toxicol. 64, 317–329. Mitchelmore, C.L., Verde, E.A., Weis, V.M., 2007. Uptake and partitioning of copper and cadmium in the coral Pocillopora damicornis. Aquat. Toxicol. 85, 48–56. Moore, N.N., 1977. Lysosomal responses to environmental chemicals in some marine invertebrates. In: Giam, C.S. (Ed.), Pollutant Effects on Marine Organisms. D.C. Heath, Lexington, MA, pp. 143–154. Moore, M.N., Stebbing, A.R.D., 1976. The quantitative cytochemical effects of three metal ions on a lysosomal hydrolase of a hydroid. J. Mar. Biol. Assoc. UK 56, 995–1005. Moore, W.S., Krishnaswami, S., Bhat, S.G., 1973. Radiometric determinations of coral growth rates. Bull. Mar. Sci. 23, 157–176. Morris, R.J., Law, R.J., Allchin, C.R., Kelly, C.A., Fileman, C.F., 1989. Metals and organochlorines in dolphins and porpoises of Cardigan Bay, West Wales. Mar. Pollut. Bull. 20, 512–523. Nicholls, G.D., Curl Jr., H., Bowen, V.T., 1959. Spectrographic analyses of marine plankton. Limnol. Oceanol. 4, 472–476. Polyakov, D.M., Krasnov, E.V., 1976. Determination of the growth rate and age of corals Porites by the strontium and sodium content in their skeletons. Sov. J. Mar. Biol. 2(1), 391–396. Ramelow, G.J., Webre, C.L., Mueller, C.S., Beck, J.N., Young, J.C., Langley, M.P., 1989. Variations of heavy metals and arsenic in fish and other organisms from the Calcasieu River and Lake, Louisiana. Arch. Environ. Contam. Toxicol. 18, 804–818. Riley, J.P., Segar, D.A., 1970. The distribution of the major and minor elements in marine animals. I. Echinoderms and coelenterates. J. Mar. Biol. Assoc. UK 50, 721–730. Shen, G.T., Boyle, E.A., 1987. Lead in corals: Reconstruction of historical industrial fluxes to the surface ocean. Earth Planet. Sci. Lett. 82, 289–304. Stebbing, A.R.D., 1976. The effects of low metal levels on a colonial hydroid. J. Mar. Biol. Assoc. UK 56, 977–994. Theede, H., Scholz, N., Fisher, H., 1979. Temperature and salinity effects on the acute toxicity of cadmium to Laomedea loveni (Hydrozoa). Mar. Ecol. Prog. Ser. 1, 13–19. U.S. Environmental Protection Agency (USEPA), 1980. Ambient water quality criteria for copper. USEPA Rep. 440/5-80-036, pp. 1–162. Vaskovsky, V.E., Korotchenko, O.D., Kosheleva, L.P., Levin, V.S., 1972. Arsenic in the lipid extracts of marine invertebrates. Comp. Biochem. Physiol. 41B(4), 777–784. Veek, H.H., Turekian, K.K., 1968. Cobalt, silver, and uranium concentrations of reef-building corals in the Pacific Ocean. Limnol. Oceanol. 13, 304–308. Vinogradova, Z.A., Koual’skiy, V.V., 1962. Elemental composition of the Black Sea plankton. Doklady Acad. Sci. USSR Earth Sci. Sec. 147, 217–219.
CHAPTER 6
Molluscs Molluscs are unsegmented coelomate animals with a well-developed head, a ventral muscular foot, and a dorsal visceral hump; with soft skin, partly covering the visceral hump, the mantle, and often secreting a calcareous shell. Molluscs are characterized by a complex anatomy and highly diverse specializations. Many are of large size, especially the giant squids. There are about 128,000 species of molluscs. There are five major groups in this phylum: the pelycopods, with 20,000 recent species, including clams, oysters, mussels, cockles, and scallops; gastropods, comprising 105,000 species, such as the drills, conchs, cowries, whelks, nudibranchs, and mud snails; about 750 species of cephalopods, including octopus, squid, and cuttlefish; 305 species of scaphopods; and about 1000 species of amphineurans, including the chitons. Bivalves exhibit several characteristics of ideal indicator organisms (Darracott and Watling, 1975; Eisler, 1981; Phillips, 1977a). This includes an ability to accumulate high concentrations of metals without dying, a sedentary life history, high numerical abundance, a lengthy life span that permits sampling of more than 1 year class throughout the monitoring period, a large size so that ample tissue is available for analysis, and good adaptation to laboratory conditions. Extensive monitoring programs have been implemented, mainly with mussels, to assess potentially toxic metals and other contaminants in marine environments (Goldberg et al., 1978; Phillips, 1976b). Although mussels are recommended as indicator organisms, additional biological variables need to be investigated (Eisler, 1981; Phillips, 1977a; Westernhagen et al., 1978), along with water and sediment analyses. The model of Goldberg et al. (1978), for example, is based on the equation dM=dt ¼ KMsw TM where M is metal concentration in bivalve tissue, t is age of organism, K is constant, T is biological half-life of metal, and Msw is concentration of metal in seawater. The age of the organism was correlated with shell thickness, and this relation appears valid. The variables T and M are easily measured. However, K, the uptake constant at time t may be dependent upon the age of the bivalve; further, the uptake constant assumes linearity, and this 143
144 Chapter 6 has not been established even today. The basic flaw in the equation is the assumption that Msw is constant over time. It is probable that Msw is variable, with pulses in Msw due to variations in outfall discharge rates, as well as the changing composition of the waste effluent. It is likely, in many cases, that only during surges in metal concentrations above a given level will the sentinel organism bioconcentrate, and even this process is modified significantly by biological and abiotic variables. Accordingly, pending further refinement of this and similar models, predicted data on KMsw derived from TM, and the reverse, should be accepted with caution. In general, the highest concentrations of all metals and metalloids examined in marine molluscs were in gut and digestive gland, with moderate enrichment in gills, mantle, and gonads, and lowest residuals in muscle and shell (Eisler, 1981; Segar et al., 1971). Most of the initial literature on trace metal composition of molluscs was devoted to the filter-feeding bivalves, especially mussels and oysters. Bivalves have received—and continue to receive—extensive treatment in the literature owing to their reported ability to reflect environmental levels of trace metals in marine and estuarine ecosystems. It is now generally accepted that mussels from highly industrialized areas contain significantly higher levels in tissues of copper, lead, cobalt, chromium, nickel, iron, manganese, and other elements (Karouna-Renier et al., 2007; Szefer et al., 2006). Variability in metal concentrations in mussels from impacted environments is attributed mainly to variability in byssus metal concentrations: byssus, as was true for soft tissues, selectively and sensitively reflects variations of certain metals in ambient seawater and may prove useful as a reliable biomonitor of these metals in a variety of coastal and estuarine areas (Szefer et al., 2006). The presence of other contaminants—such as polychlorinated biphenyls (PCBs), dioxins, and dibenzofurans—in areas contaminated by metals, may present difficulty in the interpretation of tissue metal residues in molluscs (Karouna-Renier et al., 2007).
6.1 Aluminum Aluminum concentrations in molluscan tissues were variable, especially among conspecifics collected from different portions of its range (Table 6.1). Byssus threads had aluminum concentrations more than an order of magnitude greater than soft tissues and appears to be an important detoxification route by sequestration of aluminum (and to a lesser degree for cadmium, cobalt, and manganese) within its proteinaceous fibers (Kadar et al., 2006; Table 6.1). Highest concentrations reported on a dry weight (DW) basis were 12,475.0 mg Al/kg in soft parts, 470.0 in shell, and 860.0 in gut and digestive gland; however, most values were substantially lower (Table 6.1). Most of this variability is attributable to proximity to anthropogenic sources and some to differences in sample preparation techniques. In the case of Pecten maximus, for example, washing the sample prior to analysis lowers measured aluminum concentrations by more than half in mantle and gill samples, and by 10% in gonad (Segar et al., 1971).
Molluscs 145 Table 6.1: Aluminum Concentrations in Field Collections of Molluscs Organism
Concentration
Mussel, Anodonta sp. Shell Soft parts
173.0 DW 107.0 DW
1 1
Mussel, Bathymodiolus azoricus; 2002; mid-Atlantic Ridge; 3 sites Gill Mantle Digestive gland Byssus threads
1.6-8.4 DW 3.1-4.5 DW 5.9-28.8 DW 274.8-304.6 DW
9 9 9 9
Waved whelk, Buccinum undatum Shell Soft parts
84.0 DW 300.0 DW
1 1
Cockle, Cardium edule Shell Soft parts
84.0 DW 2700.0 DW
1 1
Scallop, Chlamys opercularis Soft parts Kidneys Digestive gland Shell
49.0 DW 58.0 DW 43.0 DW 300.0-430.0 DW
2 2 2 2
American oyster, Crassostrea virginica Soft parts Soft parts; Savannah, Georgia; 9 sites; November 2000 and 2001
20.0-540.0 DW 309.0-1460.0 DW
Reference
3 10, 12
Slipper limpet, Crepidula fornicata Shell Soft parts
80.0 DW 150.0 DW
1 1
Ribbed mussel, Geukensia demissa; soft parts Southern Chesapeake Bay, Maryland San Francisco Bay, California
450.0 DW 1435.0 DW
7 7
Periwinkle, Littoraria scabra; soft parts; Tanzania; winter 2005 Polluted site Reference site
55.0 DW 15.0 DW
Baltic clam, Macoma nasuta; soft parts Chesapeake Bay, Maryland; northern portion vs. southern portion San Francisco Bay, California
a
11 11
1994.0 DW vs. 3010.0 DW
7
12,475.0 DW
7 (Continues)
146 Chapter 6 Table 6.1:
Cont’d
Organism
Concentration
Hardshell clam, Mercenaria mercenaria Shell Soft parts
71.0 DW 615.0 DW
1 1
Mussel, Modiolus modiolus Shell Soft parts Mantle and gills Muscle Gonad Gut and digestive gland
150.0 DW 210.0-260.0 DW 210.0 DW 95.0 DW 230.0 DW 860.0 DW
1 1 1 1 1 1
Bivalves Shell Soft parts
32.0-174.0 DW 186.0-346.0 DW
4 4
California mussel, Mytilus californianus Soft parts
6.0-440.0 DW
3
Common mussel, Mytilus edulis Shell Shell; Baltic Sea; 2005; 12 sites Soft parts Soft parts Soft parts; Scheldt estuary; March 2000
76.0 DW 119.0-214.0 DW 1230.0 DW 24.0-420.0 DW 925.0 DW
Reference
1 13 1 3 14
Dog whelk, Nucella lapillus Shell Soft parts
170.0 DW 160.0 DW
1 1
Octopus, Octopus sp., whole
4.0 FW
5
Common limpet, Patella vulgata Shell Soft parts
470.0 DW 160.0 DW
1 1
610.0 DW 53.0 DW 340.0 DW
1 1 1
200.0 DW 95.0 DW
1 1
130.0 DW
1
Scallop, Pecten maximus Soft parts Muscle Gut and digestive gland Mantle and gills Unwashed Washed Gonad Unwashed
a
(Continues)
Molluscs 147 Table 6.1: Organism Washed Shell Soft parts Kidneys Digestive gland
Cont’d
Concentration
Reference
95.0 DW 190.0-230.0 DW 55.0 DW 53.5 DW 173.0 DW
1 1 2 2 2
Sea scallop, Placopecten magellanicus; soft parts
338.0 DW
8
Pteropods; shell
3.0-8.0 DW
6
Cuttlefish, Sepia sp.; whole
1.7 FW
5
a
Values are in mg Al/kg fresh weight (FW) or dry weight (DW). a 1, Segar et al., 1971; 2, Bryan, 1973; 3, Goldberg et al., 1978; 4, Culkin and Riley, 1958; 5, Matsumoto et al., 1964; 6, Krinsley and Bieri, 1959; 7, Sparling and Lowe, 1996; 8, Reynolds, 1979; 9, Kadar et al., 2006; 10, Kumar et al., 2008; 11, De Wolf and Rashid, 2008; 12, Sajwan et al., 2008; 13, Protasowicki et al., 2008; 14, Wepener et al., 2008.
Scallops, P. maximus, subjected to aluminum loading via the ambient medium under controlled conditions show high bioconcentration factors (BCFs) in digestive gland (9000), kidneys (2100), and total soft parts (1400); however, in the case of Chlamys opercularis, another scallop, concentration factors were different: 2600 in kidney, 2300 in digestive gland, and 1100 in soft parts (Bryan, 1973). The softshell clam Mya arenaria, and the American oyster Crassostrea virginica, remove aluminum particles from the medium by filtering activity; however, there were no measurable increases in aluminum content of tissues when compared to controls (Hanks, 1965). High aluminum concentrations in shellfish may have some beneficial impact on human consumers. Thus, in butter clam, Saxidomus giganteus, the amount of PSP (paralytic shellfish poisoning) bound to clam melanin decreased by 68% in the presence of Al3+, and 57% with Ba2 +(Price and Lee, 1972). These results confirmed an earlier conclusion by the same authors that the PSP-melanin interaction was reversible and electrostatic in nature.
6.2 Americium Measurable levels of 241Am were found in the rock jingle Pododesmus macroschisma, blue mussel Mytilus trossulus, and horse mussel Modiolus modiolus from Amchitka Island in the Aleutian chain during summer 2004; Amchitka was the site of nuclear tests between 1965 and 1971 (Burger et al., 2007b). In laboratory studies, newly hatched juvenile cuttlefish (Sepia officinalis) were exposed for 29 days to 241Am-spiked sediments (Bustamante et al., 2006a,b, 2008), and also uptake of 241 Am from seawater over 36 h by newly hatched juveniles and 8-h exposure by adults, both followed by 29 days in clean seawater. A final set of studies involved feeding newly hatched
148 Chapter 6 juveniles 241Am-labeled mussels and brine shrimp for 1 h followed by 29 days in clean seawater. There was very little uptake from spiked sediments after 29 days, although digestive gland had 47% of the total radioactivity at that time. In seawater exposure, whole juveniles had a BCF of 6.2 after 36 h; 29 days later, 27% of the 241Am was retained in digestive glands. Adults exposed to 241Am via seawater for 8 h had a BCF of 42 in branchial hearts and 16 in branchial heart appendages; the biological half-time persistence of 241Am in seawater-exposed adults was about 14 days. In the 1-h diet route study, 89% of the total radioactivity was in digestive gland after 24 h, and 98% after 29 days; half-time persistence of 241Am via the diet was 28 days (Bustamante et al., 2006b, 2008). Gravid cuttlefish were fed crabs radiolabeled with 241Am over a 2 week period to determine the rate of maternal transfer into eggs; there was no significant transfer of 241Am (Lacoue-Labarthe et al., 2008b).
6.3 Antimony Five species of bivalves from the Aegean Sea concentrated antimony over ambient seawater levels by factors that ranged from 13 in Spondylus gaederopus to 2600 for Chama placentina (Papadopoulu, 1973). In North America, most species of molluscs had antimony residues that ranged from 0.5 to 2.0 mg/kg fresh weight (FW) edible tissues (Hall et al., 1978; Table 6.2); among European collections, antimony residues were somewhat lower in similar tissues (Table 6.2).
Table 6.2: Antimony Concentrations in Field Collections of Molluscs Organism
Concentration
Reference
Mussel, Anodonta sp.; soft parts; United Kingdom Southampton area Chertsey area
0.029 DW 0.054 DW
1 1
Cockle, Cardium edule Soft parts Mantle cavity fluid
0.034-0.063 DW 0.18 DW
1 1
Mussel, Choromytilus meridionalis; soft parts
0.20 FW
2
Clam, Donax serra; soft parts
0.27 FW
2
Clam, Ensis arcuatus; soft parts
0.028 DW
3
Clam, Ensis siliqua; shell
0.014 DW
3
a
(Continues)
Molluscs 149 Table 6.2:
Cont’d
Organism
Concentration
Reference
Gastropods; 5 spp; soft parts
0.007-0.124 DW
1
Abalone, Haliotis midea; soft parts
0.083 FW
2
Hardshell clam or Quahaug, Mercenaria mercenaria; soft parts; age in years 3 4 10 15
0.014 DW 0.011 DW 0.008 DW 0.006 DW
1 1 1 1
Molluscs; commercial species; edible tissues; 21 spp. 3 spp. 3 spp. 3 spp. 4 spp. 5 spp. 3 spp.
<0.1 FW 0.08-0.20 0.5-0.7 FW 0.7-0.9 FW 0.0-1.0 FW 1.0-2.0 FW
4 5 4 4 4 4
Common mussel, Mytilus edulis Soft parts Shell Soft parts
0.042-0.047 DW 0.022 DW 0.11 DW
1 6 3
European oyster, Ostrea edulis; soft parts
0.010-0.015 DW
1
Pen shell, Pinna nobilis Soft parts Mantle and gills Muscle Nervous system Stomach and intestines Gonad Hepatopancreas Byssus Byssus gland
1.1 DW 0.9 DW 1.0 DW 0.9 DW 1.3 DW 0.3 DW 0.6 DW 1.2 DW 0.5 DW
7 7 7 7 7 7 7 7 7
Cuttlefish, Sepia sp. Gills Mantle
0.026 DW 0.01 DW
1 1
Squid, whole
0.46 AW
8
a
Values are in mg Sb/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Leatherland and Burton, 1974; 2, Van As et al., 1973; 3, Bertine and Goldberg, 1972; 4, Hall et al., 1978; 5, Van As et al., 1975; 6, Bertine and Goldberg 1972; 7, Papadopoulu, 1973; 8, Robertson, 1967.
150 Chapter 6
6.4 Arsenic Early analytical interest in arsenic was prompted by a rash of arsenic homicides in the early 1900s. Subsequently, it was determined that seafoods, especially molluscs and crustaceans, were unusually rich in arsenic compounds, although these were present almost always in a nontoxic form, that is, as arsenobetaine or as an organic pentavalent compounds, with little risk to human consumers. The relation between arsenic transformation rates between nontoxic and toxic forms of arsenic, such as inorganic trivalent arsenites, is discussed later. It is clear from Table 6.3 that arsenic concentrates in lipid extracts of representative molluscs, that wastes containing arsenic compounds raised biogenic arsenic levels in mussels and gastropods, that arsenic content in molluscs varied with the age of the organism as well as tissue analyzed, and that mean levels of arsenic in edible portions of commercially important North American molluscs do not exceed 20.0 mg As/kg FW. Unusually high levels of arsenic are reported in filter feeding bivalves from the vicinity of Athens, Greece (Papadopoulu, 1973). It was subsequently determined that Pinna nobilis concentrated arsenic from seawater by a factor of 46,000 and that concentration factors for other species of bivalves from the same Aegean area ranged from 1500 to 18,000 (Papadopoulu, 1973). Cultured Pacific oysters, Crassostrea gigas, from Taiwan contained up to 33.4 mg total arsenic/kg FW; however, less than 2% of the total arsenic was in the form of inorganic arsenicals (Table 6.3), and the remainder was in the form of arsenobetaine and other comparatively harmless organoarsenicals with little risk to health of human consumers (Liu et al., 2006). Trivalent arsenic was lethal to embryos of the Pacific oyster, C. gigas, at 0.33 mg As3+/L, with 50% dead in 96 h (USEPA, 1985a). And 2.0 mg As3+/L depressed oxygen consumption of mud snails, Nassarius obsoletus within 72 h (USNAS, 1977). Bryant et al. (1985) showed that pentavalent As5+ was 15 times more toxic at 15 C than at 5 C to clams, Macoma balthica during exposure for 7 days. Studies with radioarsenic and Mytilus galloprovincialis show that accumulation was modified at nominal arsenic concentrations in the medium, with tissue, with age of the mussel, and with temperature and salinity of the medium (Unlu and Fowler, 1979). Uptake of arsenate arsenic, increased with increasing arsenate concentration in the medium; however, the response was not linear, with accumulation suppressed at higher external arsenate concentrations. Smaller mussels accumulated more arsenic than larger mussels; in both size groups, highest levels were in byssus and digestive gland. In general, uptake and loss of arsenate was enhanced at higher temperatures, and lower salinities (19 vs. 38 ppt). Loss rate was the same at both salinities. Radioarsenic loss followed a biphasic pattern with biological half-times of 3 and 32 days for the fast and slow compartments, respectively. Byssal thread secretion played a key role in arsenic elimination from M. galloprovincialis (Unlu and Fowler, 1979).
Molluscs 151 Table 6.3: Arsenic Concentrations in Field Collections of Molluscs Organism
Concentration
Reference
Alaska; Cook Inlet; summer 1997; clams; soft parts; maximum values Total arsenic Dimethylarsinic acid As3+ plus As5+ Monomethylarsinic acid
5.0 FW 0.6 FW 0.01 FW <0.001 FW
17 17 17 17
1.0 DW 48.0 DW vs. 44.0 DW
42 42
Clam, Asaphis violascens; soft parts; American Samoa; 2001-2002; total arsenic vs. inorganic arsenic Industrialized sites Reference sites
4.7-5.9 FW vs. 0.21-0.24 FW 1.2-1.5 FW vs. 0.07-0.10 FW
38 38
Bivalves; California; 1984-1985; soft parts Clam, Corbicula sp. Clam, Macoma balthica
5.4-11.5 DW 7.6-12.1 DW
18 18
Bivalves; East China Sea; 5 spp.; soft parts; August 2002
0.50 (0.22-0.81) FW
31
Clam, Anodonta cygnea; soft parts
4.3 DW
Ivory shell, Buccinum striatissimum; total arsenic vs. arsenobetaine Muscle Midgut gland
38.0 FW vs. 24.2 FW 18.0 FW vs. 10.8 FW
Channeled whelk, Busycon canaliculatum
9.0 FW
3
Cockle, Cardium edule Soft parts Mantle cavity fluids
5.1-6.3 DW 8.4 DW
2 2
Scallop, Comptopallium radula; New Caledonia; October 2004; Santa Marie Bay Soft parts Kidney
44.7 (39.3-53.6) DW 116.0 DW
Giant squid, Architeuthis dux; 2001-2005 Gill; Bay of Biscay Hepatopancreas; Bay of Biscay vs. Mediterranean Sea
a
2
19 19
36 36
Pacific oyster, Crassostrea gigas Taiwan; cultured; 4 sites; soft parts Total arsenic (Continues)
152 Chapter 6 Table 6.3: Organism All sites April vs. February As5+ As3+ Monomethylarsonic acid Dimethylarsinic acid Taiwan; soft parts; 2002; 4 sites, 4 seasons Total arsenic Arsenite Arsenate Dimethylarsinic acid Monomethylarsonic acid Arsenobetaine American oyster, Crassostrea virginica Soft parts Soft parts Soft parts; Pensacola, Florida: 2003-2004 Soft parts; Savannah, Georgia; 2000-2001; 9 sites
Cont’d
Concentration
Reference
8.4-9.5 (3.1-33.4) FW 22.9 FW vs. 4.2 FW 0.038-0.087 FW 0.071-0.125 FW 0.052-0.124 FW 0.3(0.06-0.47) FW
32 32 32 32 32 32
9.9 (8.5-10.7) DW 0.09 (0.06-0.12) DW 0.03 (0.02-0.05) DW 0.53 (0.47-0.62) DW 0.04 (0.03-0.05) DW 3.9 DW
37 37 37 37 37 37
10.3 DW 2.9 FW Max. 2.8 FW
20 26 34
0.2-3.0 DW
35, 40
Oyster, Crassostrea spp; soft parts
(0.3-3.4) FW; (1.3-10.0) DW
2,4,5,6
Gastropods, 5 spp.; soft parts
8.1-38.0 DW
2
Periwinkle, Littoraria scabra; soft parts Industrial zone; 1998 vs. 2005 Reference site; 2005
6.5 DW vs. 1.4 DW 1.1 DW
39 39
Max. 500.0 FW vs. <0.5 FW
21
Spindle shell, Hemifusus spp.; Hong Kong; 1984; muscle; total arsenic vs. inorganic arsenic Limpet. Littorina littorea; soft parts Near arsenic source Offshore
11.5 DW 4.0 DW
Squid, Loligo vulgaris; soft parts
(0.8-7.5) FW
Hardshell clam, Mercenaria mercenaria; soft parts; age in years 3 4 10 15
3.8 DW 4.7 DW 9.3 DW 8.4 DW
a
7 7 26
2 2 2 2 (Continues)
Molluscs 153 Table 6.3:
Cont’d
Organism
Concentration
Clam, Meretrix casta; soft parts
10.9 DW
5
Molluscs; soft parts; lipid extracts; 7 spp.
4600.0-39,300.0 FW
1
2.0-3.0 FW 3.0-4.0 FW 4.0-5.0 FW 7.0-20.0 FW
8 8 8 8
7.1-83.8 (1.3-129.6) DW
9
Molluscs; commercial; edible tissues; North America 6 spp. 8 spp. 3 spp. 4 spp. Molluscs; commercial; edible portions; various locations; 21 spp. Molluscs; edible tissues Hong Kong, 1976-1978 Bivalves Gastropods Cephalopods Yugoslavia; northern Adriatic Sea; summer 1986 Softshell clam, Mya arenaria; soft parts; arsenic-contaminated sites at Seal Harbour, Nova Scotia vs. reference sites Total arsenic Inorganic arsenic Trivalent arsenic Pentavalent arsenic Bioaccessible fraction Common mussel, Mytilus edulis Soft parts Soft parts Soft parts Soft parts; Scheldt estuary; March 2000 Pacific blue mussel, Mytilus edulis trossulus; 2004; Adak Island, Alaska; soft parts; 5 sites
Reference
a
3.2-39.6 FW 19.0-176.0 FW 0.7-5.5 FW 21.0-31.0 FW
22 22 22 23
218.0-228.0 FW vs. 7.0-7.9 FW
28
22.0 FW vs. 0.37 FW 57.0 FW vs <0.25 FW 89.2 FW vs. 6.0 FW
28 28 28
1.6-16.0 DW 2.5 (1.4-4.6) FW Max. 20.0 DW 61.0 DW
2,7,10,11 24 30 41
9.0 FW; max. 32.2 FW; 6.0-19.0 DW
33
(Continues)
154 Chapter 6 Table 6.3: Organism
Cont’d
Concentration
Reference
Mussel, Mytilus galloprovincialis; soft parts Western Mediterranean Sea; Balearic Islands; Port of Mahon; 1991-2005 Adriatic Sea; 2001-2005; winter vs. summer
5.4 (0.8-11.0) DW
29
11.8-17.0 DW vs. 10.8-37.6 DW
44
Mytilus spp.; soft parts
3.0 FW; (8.2-9.6) DW
North Sea; 1997-1998; soft parts Whelk, Buccinum undatum Giant scallop, Pecten maximus
Max. 65.0 FW 1.0-3.6 FW
43 43
96.4 DW vs. 44.3 DW
27
23.8-56.0 DW 12.0-32.0 DW 16.0-59.0 DW 33.0-56.0 DW
45 45 45 45
2.8-6.2 DW 10.6 (0.8-19.0) DW
2 29
Scallop, Pecten maximus; soft parts
11.6 DW
13
Pen shell, Pinna nobilis Soft parts Mantle, gills Muscle Nervous system Stomach, intestine Gonads Hepatopancreas Byssus Byssus gland
670.0 DW 120.0 DW 95.0 DW 180.0 DW 1100.0 DW 90.0 DW 210.0 DW 57.0 DW 37.0 DW
14 14 14 14 14 14 14 14 14
1.6 (1.3-2.4) FW
26
Octopus, Octopus cyanea; Guam; June 1998; tentacle vs. liver Octopus, Octopus vulgaris Portugal; 1999-2002; 3 sites Digestive gland Branchial heart Gill Muscle European flat oyster, Ostrea edulis Soft parts Soft parts; Balearic Islands; western Mediterranean Sea; Port of Mahon; 1991-2005
Scallop, Placopecten magellanicus; soft parts Cuttlefish, Sepia officinalis Gills Mantle
198.0 DW 73.0 DW
a
5,12
2 2 (Continues)
Molluscs 155 Table 6.3:
Cont’d
Organism
Concentration
Reference
Surf clam, Spisula solidissima; muscle
1.3 FW
Taiwan; 1995-1996; soft parts Clam, Meretrix lusoria Pacific oyster, Crassostrea gigas
13.7 (9.5-20.1) DW 11.8 (7.2-16.3) DW
25 25
Clam, Tapes japonica; soft parts
<0.004 to <0.05 AW
15,16
a
3
Values are in mg As/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Vaskovsky et al., 1972; 2, Leatherland and Burton, 1974; 3, Greig et al., 1977; 4, Mackay et al., 1975; 5, Zingde et al., 1976; 6, Sims and Presley, 1976; 7, Penrose et al., 1975; 8, Hall et al., 1978; 9, Costa and da Fonseca 1967; 10, Karbe et al., 1977; 11, Bohn, 1975; 12, Vecchio et al., 1962; 13, Lunde, 1970; 14, Papadopoulu, 1973; 15, Fukai and Meinke, 1959; 16, Fukai and Meinke, 1962; 17, Bigler and Crecelius, 1998; 18, Johns and Luoma, 1990, Shiomi et al., 1984; 20, Zaroogian and Hoffman, 1982; 21, Phillips and Depledge, 1986; 22, Phillips et al., 1982; 23, Ozretic et al., 1990; 24, Vos and Hovens, 1986; 25, Han et al., 1998; 26, Jenkins, 1980; 27, Denton et al., 2006; 28, Koch et al., 2007; 29, Deudero et al., 2007; 30, Mubiana and Blust, 2006; 31, Huang et al., 2007; 32, Liu et al., 2006; 33, Burger and Gochfeld, 2006; 34, KarounaRenier et al., 2007; 35, Kumar et al., 2008; 36, Metian et al., 2008; 37, Liu et al., 2008; 38, Peshut et al., 2008; 39, De Wolf and Rashid, 2008; 40, Sajwan et al., 2008; 41, Wepener et al., 2008; 42, Bustamante et al., 2008; 43, De Gieter et al., 2002; 44, Fattorini et al., 2008; 45, Napoleao et al., 2005.
Experimental work with molluscs suggest only minor accumulations of stable arsenic, although arsenic seemed to be retained by gastropods and mussels (Rosemarin et al., 1985). American oysters, C. virginica, held in seawater containing 0.005 mg As5+/L for 112 days concentrated arsenic by a factor of 350 (Zaroogian and Hoffman, 1982). There was no relation between oyster body burdens of arsenic and exposure concentrations; however, diet contributed more to arsenic uptake than did seawater concentrations (Zaroogian and Hoffman, 1982). In another study, neither soft parts nor shell of Mytilus edulis retained more than 0.01 mg of arsenic during immersion in solutions containing 100,000.0 mg As/L. By contrast, the byssus accumulated up to 0.5 mg and the excreta contained up to 0.8 mg arsenic in an insoluble form (Sautet et al., 1964). Juveniles of bay scallops, Argopecten irradians, contained 29.2 mg As/kg FW soft parts after exposure to 20.0 mg As/L for 96 h, again suggesting little bioconcentration (Nelson et al., 1976).
6.5 Barium Most of the information on barium in molluscs is restricted to residues in shell (Table 6.4). Factors known to modify incorporation of barium and other alkaline earths into shells include the ambient salinity of the medium (Pilkey and Goodell, 1963), direct relation to shell strontium (Pearce and Mann, 2006), and the chemical form of barium, with ionic species most readily incorporated (Turekian and Armstrong, 1960). Barium incorporation from seawater into soft tissues is reported: concentration factors for barium in four bivalve species from polluted waters of Greece ranged from 200 to 1100 (Papadopoulu, 1973).
156 Chapter 6 Table 6.4: Barium, Bismuth, and Boron Concentrations in Field Collections of Molluscs Element and Organism
Concentration
Reference
a
Barium Gastropods; shell
4.0-15.0 DW
1
Molluscs Tissues and shell Shells, 7 spp.
0.02-0.1 FW 3.0-48.0 DW
2 3
Common mussel, Mytilus edulis; soft parts
0.8-26.0 DW
4
Mussel, Mytilus galloprovincialis; soft parts; Adriatic Sea; 2001-2005; winter vs. summer
1.3-7.6 DW vs. 1.5-3.4 DW
Scallop, Pecten sp.; shell
6.0-12.0 DW
1
Pelycopods; shell
4.0-41.0 DW
1
Gastropod, Pinna nobilis Soft parts Mantle and gills Muscle Nervous system Stomach and intestine Gonads Hepatopancreas Byssus Byssus gland
120.0 AW 150.0 AW 100.0 AW 140.0 AW 140.0 AW 79.0 AW 66.0 AW 63.0 AW 120.0 AW
5 5 5 5 5 5 5 5 5
Mussel, Choromytilus meridionalis; soft parts
5.0-6.0 DW
6
Pacific oyster, Crassostrea gigas; soft parts
4.0 DW
6
Bivalve molluscs; soft parts; 11 spp.
2.0-4.5 FW
7
Bivalve molluscs; soft parts; 2 spp.
50.0-90.0 AW
8
American oyster, Crassostrea virginica; soft parts; Savannah, Georgia; 2000-2001
Max. 254.0 DW
9, 10
Octopus, Polypus bimaculatus; whole
1.3 FW
7
Squid, Ommastrephes illicebrosa; whole
420.0 AW
8
11
Bismuth
Boron
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Turekian and Armstrong, 1960; 2, Mauchline and Templeton, 1966; 3, Pilkey and Goodel 1963; 4, Karbe et al., 1977; 5, Papadopoulu, 1973; 6, Watling and Watling 1976a,b; 7, Thompson et al., 1976; 8, Nicholls et al., 1959; 9, Kumar et al., 2008; 10, Sajwan et al., 2008; 11, Fattorini et al., 2008.
Molluscs 157 Barium concentrations in shell of razor clam, Ensis siliqua, collected from the west coast of England tended to be elevated where sewage sludge dumping was operative during shell growth (Pearce and Mann, 2006).
6.6 Bismuth The highest bismuth concentration recorded was 6.0 mg/kg DW in soft parts of a mussel (Table 6.4). Bismuth concentrations in mussels, Choromytilus meridionalis, from South Africa were positively correlated with the age, sex, zinc content, and degree of metals contamination in the immediate environment. Bismuth accumulation rates were higher in larger mussels, in females, in mussels with elevated zinc content, and lower in mussels collected from waters of low metal content (Watling and Watling, 1976a).
6.7 Boron The maximum boron concentration recorded of 254.0 mg B/kg DW was in soft parts of an American oyster, C. virginica, from Savannah, Georgia (Table 6.4). The significance of this high concentration on oyster health is unknown and merits additional research. Boron concentrations in soft tissues of Pacific Northwest molluscs ranged from 1.6 to 4.5 mg B/kg FW (Table 6.4; Thompson et al., 1976). Oysters show little bioaccumulation potential or prolonged retention of boron after cessation of exposure to 10.0 mg B/L. Boron concentrations in industrial waste outfalls seldom exceed 1.0 mg B/L, and this concentration presents little risk to fish or oysters (Thompson et al., 1976).
6.8 Cadmium Cadmium has no known biological function in molluscs and other living organisms. A criterion of 1.0 mg Cd/kg FW diet is proposed for human health protection (Burger and Gochfeld, 2006; Glynn et al., 2003; Julshamn et al., 2008; Sankar et al., 2006), although some localities suggest less than 2.0 mg Cd/kg FW in seafoods (Lekhi et al., 2008). Accordingly, the elevated concentrations of cadmium in some molluscan tissues (Table 6.5) is of concern to consumers, including humans. It is generally acknowledged that there is a high positive correlation between cadmium concentrations in molluscan tissues and proximity to heavily urbanized areas, especially areas featuring electroplating and mining operations (Bloom and Ayling, 1977; Eisler, 1981, 2000g; Eisler et al., 1978; Eustace, 1973a; Fowler and Oregioni, 1976; Graham, 1972; Maanan, 2007; Phillips, 1979; Talbot et al., 1976b; Thrower and Ratkowsky et al., 1974).
158 Chapter 6 Table 6.5: Cadmium Concentrations in Field Collections of Molluscs Organism
Concentration
Reference
Abalone, Korea Muscle Viscera
Max. 0.1 FW 1.3-2.0 FW
26 26
Cockle, Anadara trapezia; soft parts; April 2000; New South Wales, Australia
Max. 11.0 DW
75
Giant squid, Architeuthis dux; hepatopancreas; 2001-2005; Bay of Biscay vs. Mediterranean Sea
60.8 DW vs. 90.7 DW
Bay scallop, Argopecten irradians Soft parts Adductor muscle Kidney concretion Hydrothermal vent mussel, Bathymodiolus azoricus; mid-Atlantic ridge 2002; 3 sites Gills Mantle Digestive gland Byssus threads 2001; shell; 4 sites 2001; 5 sites Gills Mantle Digestive gland Bivalves; 5 spp.; soft parts; East China Sea; August 2002 Mussel, Brachidontes pharaonis; Mersin coast, Turkey; 2002-2003; max. concentrations Muscle Gill Hepatopancreas Cephalopods; Brazil; June-September 2004; digestive gland Slender inshore squid, Loligo plei; adult Argentine short-finned squid, Illex argentinus
a
102
43.0 AW; 1.1 FW; 7.5 DW 49.2 AW; 1.4 FW 19.7 DW
14, 27 14 22
8.2-28.6 DW 0.01-2.1 DW 13.3-28.8 DW 11.4-89.8 DW 0.4-1.4 (0.2-2.4) DW
80 80 80 80 90
1.8-47.2 DW 0.04-2.4 DW 1.5-4.5 DW
91 91 91
0.12 (0.01-0.33) FW
66
2.2 DW 8.0 DW 3.3 DW
60 60 60
19.6 FW
78
(Continues)
Molluscs 159 Table 6.5: Organism
Cont’d
Concentration
Reference
18.5 FW 1002.9 FW
78 78
Cockle, Cerastoderma glaucum; Gulf of Gabes, Tunisia; February 2001; max. concentrations Gill Digestive gland Remainder Soft parts, 7 sites
3.5 DW 0.5 DW 0.4 DW 0.08-2.5 DW
59 59 59 59
Scallop, Comptopallium radula; Santa Marie Bay, New Caledonia; October 2004 Soft parts Kidney
1.1 (0.5-1.9) DW 57.8 DW
86 86
Oyster, Crassostrea angulata; soft parts
0.35-1.4 FW
28
Sydney rock oyster, Crassostrea commercialis Soft parts Soft parts
0.4-18.6 FW 0.1-1.0 FW
1 2
Immature Mature
Oyster, Crassostrea corteziensis; soft parts; Gulf of California; 1999-2000 Pacific oyster, Crassostrea gigas Soft parts Soft parts Soft parts Soft parts; China; November 2003; impacted by industrial effluents; 3 sites Mangrove oyster, Crassostrea rhizophorae Sepetiba Bay, Brazil; soft parts; near zinc smelting plant closed in 1996; max. concentrations 1978 1980 1983 1989 1996 (after a tailings spill following heavy rains) 1997
7.2 DW
96
0.2-2.1 FW Max. 30.7 FW 3.7-9.0 DW 11.0-25.0 DW
34 1 5 61
10.9 DW 1.9 DW 20.5 DW 4.6 DW 29.0 DW
52 52 52 52 52
4.0 DW
52
a
(Continues)
160 Chapter 6 Table 6.5: Organism
Cont’d
Concentration
Reference
5.4 DW 1.3 DW 2.0 DW 1.3-2.4 DW; max. 3.1 DW vs. 1.5-2.5 DW; max. 3.1 DW
52 52 52 72
Max. 0.61 FW
77
<1.5 to 2.9 DW
85
3.6-66.0 DW
74
1780.0 DW vs. 84.0-119.0 DW 25.0 DW vs. 1.6-1.9 DW
74 74
0.18-1.2 (0.04-1.40) FW
62
0.2-0.5 DW 5.1-10.0 DW 25.7 DW 127.0-156.0 DW
53 53 53 53
0.4-3.3 FW
50
Abalone, Haliotis corrugata Digestive gland Muscle
Max. 82.2 FW 0.3 FW
31 31
Red abalone, Haliotis rufescens Gill Mantle Digestive gland Foot
4.0-10.0 DW 2.8-12.8 DW 183.0-1163.0 DW 0.2-0.5 DW
Periwinkle, Littoraria scabra; soft parts; Tanzania Industrial sites; 1998 vs. 2005 Reference site; 2005
10.0 DW vs. 1.7 DW 1.0 DW
1999 2001 2002 Near Natal, Brazil; summer 2001; soft parts; contaminated estuary vs. reference site American oyster, Crassostrea virginica Soft parts; Pensacola, Florida; 2003-2004 Soft parts; Savannah, Georgia; November 2000-2001; 9 sites Mussel, Crenomytilus grayanus Soft parts; world wide Okhotsk Sea and Sea of Japan; summer 2001; upwelling region vs reference sites Kidney Digestive gland Mussel, Elliptio buckleyi; soft parts; Marmara Sea, Turkey; 2004-2005 Razor clam, Ensis siliqua; shell; 23 stations; west coast of England 18 stations 2 stations 1 station 2 stations Greenland; 1975-1991; bivalves; 5 spp.; soft parts
a
6 6 6 6
88 88 (Continues)
Molluscs 161 Table 6.5:
Cont’d
Organism
Concentration
Periwinkle, Littorina littorea Soft parts Soft parts Soft parts
0.9-1.5 DW 0.0-0.5 FW 210.0 DW
7 8 9
Squid, Loligo opalescens; liver; California coast Central region Southern region
85.0 DW 121.0 DW
10 10
Clam, Macoma balthica Whole Soft parts
0.05 FW 0.2-0.5 FW; 0.21-0.85 DW
32 33, 34
Horse mussel, Modiolus modiolus; Norway; 2007 Kidney Digestive gland Gills Gonad Muscle Total soft parts
7.2 (2.5-12.0) FW 0.6 (0.2-1.3) FW 0.9 (0.5-1.7)FW 0.3 (0.1-0.6) FW 0.15 (0.06-0.23) FW 0.86 (0.34-1.52) FW
92 92 92 92 92 92
Mexico; Sinaloa; 2004-2005; soft parts; rainy season vs. dry season Oyster, Crassostrea corteziensis Mussel, Mytella strigata Clam, Megapitaria squalida
7.3 DW vs. 6.0 DW 7.1 DW vs. 5.1 DW 4.1 DW vs. 2.6 DW
93 93 93
0.04-2.0 FW 0.17-1.9 DW 0.13-0.92 FW
36 37 76
<0.1 to 0.3 FW 0.3-1.0 FW 1.0-3.0 FW 0.1 FW
38 38 38 83
0.5 DW 0.7 DW
95 95
Molluscs Soft parts 12 spp. 3 spp. 5 spp.; Strait of Magellan, Chile; 2001; 17 stations Edible tissues 11 spp. 3 spp. 4 spp. 2 spp. Morocco; 2001; clams; soft parts Scrobicularia plana Cerastoderma edule
Reference
a
(Continues)
162 Chapter 6 Table 6.5:
Cont’d a
Organism
Concentration
Reference
Morocco; 2004-2005; soft parts Mussel, Mytilus galloprovincialis Clam, Venerupis decussatus Pacific oyster, Crassostrea gigas
7.2 (1.3-25.3) DW 2.2 (1.4-3.7) DW 4.5 (0.7-9.4) DW
87 87 87
Softshell clam, Mya arenaria Soft parts Soft parts Whole
0.3 (0.1-0.9) FW 0.34-0.6 DW 0.1 FW
3, 40 41 42
Common mussel, Mytilus edulis; soft parts United States West Coast United States East Coast Port Phillip Bay, Australia Western Port Bay, Australia Scottish waters Looe estuary, United Kingdom Tasmania Corio Bay, Australia The Netherlands; summer 2002 Scheldt estuary; March 2000
2.3-10.5 DW 0.6-6.2 DW 0.2-1.3 FW Max. 18.2 FW 0.1-2.0 FW 0.8-2.6 DW 5.5 FW 2.0-63.0 DW Max. 6.0 DW 4.0 DW
Common mussel, Mytilus edulis Shell Shell; Baltic Sea; 2005; 12 sites Hepatopancreas
0.95-5.5 DW 0.009-0.11 DW Max. 18.0 DW
19, 35, 43 98 44
Mussel, Mytilus edulis planulatus; total dry weight soft parts 0.09 g 0.39 g 0.48 g 0.69 g
0.6 DW 0.8 DW 1.1 DW 1.3 DW
18 18 18 18
0.99 FW; max. 2.98 FW; 3.7-7.3 DW
70
1.3 FW 1.9 DW 1.1 FW
45 46 58
0.03 DW vs. 0.01 DW
99
Pacific blue mussel, Mytilus edulis trossulus; Adak Island, Alaska; 2004; soft parts; 5 sites Mussel, Mytilus galloprovincialis Soft parts Soft parts Soft parts; Marmara Sea, Turkey; 2005 Soft parts; Izmir Bay, Turkey; 2004; near shore vs. mid-bay
12 12 13 13 14 15 16 17 67 100
(Continues)
Molluscs 163 Table 6.5: Organism Soft parts; Gulf of Gemlik, Turkey; 2004 Soft parts; Adriatic Sea, Italy; 2 sites Soft parts; Sardinia; 2004 vs. 2006 Soft parts; Adriatic Sea; 2001-2005; winter vs. summer Greece; 2004-2006; contaminated sites; max. mean concentrations; mantle vs. gills Summer Autumn Winter Spring Soft parts; Adriatic Sea; 2001-2002; summer vs. winter Industrialized sites Reference sites Soft parts; Venice lagoon, Italy; 2005-2006; San Giuliano vs. Sacca Sessola April July October February Western Mediterranean Sea; Balearic Islands; Port of Mahon; 1991-2005 Aegean Sea; Turkey; 2002-2003 Soft parts; NW Mediterranean Sea; May 2003 Italy; Genova and environs France; Marseille and vicinity Spain; Barcelona and vicinity Soft parts; Mediterranean Sea; summer 2004-2005; 3 sites Octopus, Octopus cyanea; Guam; June 1998; tentacle vs. liver Octopus, Octopus vulgaris Portugal; digestive gland Portugal; digestive gland; 2005-2006; northwest region vs. south coast
Cont’d
Concentration
Reference
2.4 DW
106
0.26-0.35 FW 2.8 DW vs. 1.1 DW 0.9-1.5 DW vs. 0.4-1.3 DW
97 101 104
0.09 FW 0.04 FW 0.07 FW 0.05 FW
vs. 0.41 FW vs. 0.42 FW vs 0.43 FW vs. 0.36 FW
97 97 97 97
0.54-0.59 DW vs. 0.44-0.63 DW 1.1 DW vs. 0.95 DW
69
6.6 DW vs. 2.5 DW 1.2 DW vs. 0.8 DW 2.0 DW vs. 1.2 DW 2.7 DW vs. 3.6 DW 0.66 (0.25-1.7) DW
81 81 81 81 56
0.25 (0.04-0.52) FW
64
0.27-0.55 DW 0.40-0.62 DW 0.63-0.89 DW 1.1-1.8 DW
55 55 55 84
0.06 DW vs. 7.82 DW
57
19.6-761.5 DW
79
a
69
(Continues)
164 Chapter 6 Table 6.5: Organism Whole Nuclei Mitochondria Lysosomes Microsomes Squid, Ommastrephes bartrami Liver Muscle Gonad
Cont’d
Concentration
Reference
150.0 (57.0-250.0) DW vs. 15.0 (10.0-30.0) DW 120.0 (28.0-500.0) DW vs. 22.0 (20.0-210.0) DW 150.0 (36.0-360.0) DW vs. 21.0 (17.0-45.0) DW 120.0 DW vs. 25.0 DW 230.0 (190.0-1080.0) DW vs. 21.0 (15.0-450.0) DW
94 94 94 94 94
81.0-782.0 DW 0.7 DW 0.4 DW
10, 11 10, 11 10, 11
1.3 (0.3-3.9) DW
56
Oyster, 5 species of Ostrea Soft parts Soft parts Soft parts Soft parts
0-21.4 DW 0.2-2.3 FW 36.0-174.0 DW Max. 10.7 FW
51 18 17 39
Limpet, Patella candei gomesii; soft parts; 1997; Azores Near hydrothermal vent Reference site
0.65-1.0 DW 1.7-2.8 DW
89 89
0.36 (0.02-0.94) DW
65
13.0 DW 1.9 DW 96.0 DW 3.2-17.0 DW 2.5 DW 0.0 DW 54.0-79.0 DW 546.6 DW 321.0 DW 5.1-23.0 FW
19 19 19 19 19 19 20, 21 22 20 14
European flat oyster, Ostrea edulis; soft parts; 1991-2005; western Mediterranean Sea; Balearic Islands; Port of Mahon
Gastropod, Patella piperata; Canary Islands, Spain; soft parts; March-April 2003 Scallop, Pecten maximus Soft parts Muscle Gut and digestive gland Mantle and gills Gonad Shell Kidney Kidney concretion Digestive gland Edible tissues
a
(Continues)
Molluscs 165 Table 6.5:
Cont’d
Organism
Concentration
Reference
Giant scallop, Pecten maximus; Norway; 2006 Digestive gland Kidney Muscle Gonad Total soft parts
52.0 (40.0-68.0) FW 4.7 (2.3-8.8) FW 0.15 (0.11-0.21) FW 0.13 (0.07-0.20) FW 5.4 (3.7-8.4) FW
92 92 92 92 92
Scallop, Pecten novae-zelandiae Stomach Gonad Adductor muscle Soft parts Soft parts Visceral mass Other tissues
137.0 FW 1.5 FW 0.5 FW 0.2 FW 249.0 DW 2000.0 DW <20.0 DW
36 36 36 36 49 49 49
Green mussel, Perna viridis Hong Kong; juveniles vs. adults Reference sites Soft parts Byssus Polluted sites Soft parts Byssus India; 28 sites; January 2002; soft parts False quahog, Pitar morrhuana; soft parts; near electroplating plant outfall vs. distant site Giant scallop, Placopecten magellanicus Muscle; March vs. rest of year Viscera; max. values March August February June Gonad Viscera Clam, Protothaca staminea Shell Soft parts
3.1 DW vs. 5.4 DW 1.5 DW vs 1.5 DW
105 105
1.3 DW vs. 1.1 DW 0.8 DW vs. 1.3 DW 1.1-1.3 FW
105 105 73
3.3 DW vs. <0.07 DW
29
Max. 8.8 DW vs. <3.7 DW
23
104.1 DW 121.2 DW 161.8 DW 105.3 DW 0.5-3.2 FW 3.7-27.0 FW
23 23 23 23 24 24
2.9 DW 5.7 DW
35 35
a
(Continues)
166 Chapter 6 Table 6.5:
Cont’d
Organism
Concentration
Reference
Manila clam, Ruditapes philippinarum; Korea; soft parts; 2002-2003 Females vs. males Postspawn vs. prespawn Jiaozhou Bay, China; November 2004; sediments vs. soft parts
0.86 DW vs. 0.85 DW 1.4 DW vs. 0.86 DW 0.2 mg/kg DW vs. 0.51-0.67 DW
54 54 67
39.8 DW 1.7 DW 5.6 DW
25 25 25
21.0 DW
25
0.59 DW 0.76 DW 0.4 DW
71 71 71
0.5 DW 0.8 DW
71 71
1.2 DW 15.0 DW 0.06 DW
71 71 71
2.0 DW 22.0 DW 0.22 DW
71 71 71
1.1 DW 25.0 DW 0.03 DW
71 71 71
Squid, Sepia spp. Gills Mantle Whole
0.11 DW 0.03 DW 0.7 FW
7 7 30
Whelk, Thais lapillus; soft parts
425.0 DW
9
Clam, Scrobicularia plana; digestive gland Gannel estuary, United Kingdom Camel estuary, United Kingdom Transferred from Camel to Gannel estuary for 352 days Transferred from Gannel to Camel estuary for 352 days Common cuttlefish, Sepia officinalis Egg Eggshell Embryo Yolk Hatchlings Whole Cuttlebone Juveniles, age 1 month Whole Digestive gland Cuttlebone Immatures, age 12 months Whole Digestive gland Cuttlebone Adults, age 18 months Whole Digestive gland Cuttlebone
a
(Continues)
Molluscs 167 Table 6.5:
Cont’d
Organism
Concentration
Reference
Japanese common squid, Todarodes pacificus; liver
336.0 DW
103
Clam, Trivela mactroidea; Venezuela; 2002; 14 sites; soft parts
<1.0 to 1.9 DW
a
82
Values are in mg Cd/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Ratkowsky et al., 1974; 2, Mackay et al., 1975; 3, Pringle et al., 1968; 4, Kopfler and Mayer, 1967; 5, Watling and Watling 1976; 6, Anderlini, 1974; 7, Leatherland and Burton, 1974; 8, Topping, 1973; 9, Butterworth et al., 1972; 10, Martin and Flegal, 1975; 11, Hamanaka et al., 1977; 12, Goldberg et al., 1978; 13, Phillips 1976; 14, Eisler et al., 1972; 15, Bryan and Hummerstone 1973; 16, Eustace, 1974; 17, Talbot et al., 1976b; 18, Harris et al., 1979; 19, Segar et al., 1971; 20, Bryan, 1973; 21, George et al., 1980; 22, Carmichael et al., 1979; 23, Reynolds, 1979; 24, Greig et al., 1978; 25, Bryan and Hummerstone, 1978; 26, Won, 1973; 27, Pesch and Stewart, 1980; 28, Establier, 1977; 29, Eisler et al., 1978; 30, Matsumoto et al., 1964; 31, Vattuone et al., 1976; 32, White et al., 1979; 33, Bryan and Hummerstone, 1977; 34, Miettinen and Verta, 1978; 35, Graham, 1972; 36, Nielsen and Nathan, 1975; 37, Greig, 1979; 38, Hall et al., 1978; 39, Eustace, 1974; 40, Shuster and Pringle, 1968; 41, Eisler 1977b; 42, White et al., 1979; 43, Lande, 1977; 44, Young et al., 1979; 45, Uysal, 1978a; 46, Fowler and Oregioni, 1976; 47, Fukai et al., 1978; 48, Thomson, 1979; 49, Brooks and Rumsby, 1965; 50, Dietz et al., 1996; 51, Denton et al., 2006; 52, Lacerda and Molisani, 2006; 53, Pearce and Mann, 2006; 54, Ji et al., 2006; 55, Zorita et al., 2007; 56, Deudero et al., 2007; 57, Vlahogianni et al., 2007; 58, Keskin et al., 2007; 59, Machreki-Ajmi and Hamza-Chaffai, 2006; 60, Karayakar et al., 2007; 61, Liu and Deng, 2007; 62, Yarsan et al., 2007; 63, Mubiana and Blust, 2006; 64, Sunlu, 2006; 65, Bergasa et al., 2007; 66, Huang et al., 2007; 67, Li et al., 2006; 68, Liang et al., 2004a; 69, Scancar et al., 2007; 70, Burger and Gochfeld, 2006; 71, Miramand et al., 2006; 72, Silva et al., 2006; 73, Sasikumar et al., 2006; 74, Podgurskaya and Kavun, 2006; 75, Burt et al., 2007; 76, Espana et al., 2007; 77, KarounaRenier et al., 2007; 78, Dorneles et al., 2007; 79, Raimundo et al., 2004; 80, Kadar et al., 2006; 81, Nesto et al., 2007; 82, LaBrecque et al., 2004; 83, Sankar et al., 2006; 84, Lafabrie et al., 2007; 85, Kumar et al., 2008; 86, Metian et al., 2008; 87, Maanan, 2008; 88, De Wolf and Rashid, 2008; 89, Cunha et al., 2008; 90, Cravo et al., 2008; 91, Cosson et al., 2008; 92, Julshamn et al., 2008; 93, Frias-Espericueta et al., 2008; 94, Raimundo et al., 2008; 95, Anajjar et al., 2008; 96, Ruelas-Inzunza and Paez-Osuna, 2008; 97, Conti et al., 2008; 98, Protasowicki et al., 2008; 99, Kucuksezgin et al., 2008; 100, Wepener et al., 2008; 101, Schintu et al., 2008; 102, Bustamante et al., 2008; 103, Arai et al., 2004; 104, Fattorini et al., 2008; 105, Nicholson and Szefer, 2003; 106, Unlu et al., 2008.
High BCFs of 10,000 and greater were recorded for most species of field-collected molluscs, with highest concentrations in digestive gland, kidney, and kidney concretions (Table 6.5; Belcheva et al., 2006; Bowen, 1958; Brooks and Rumsby, 1965; Bryan, 1973; Ketchum and Majori and Petronio, 1973; Podgurskaya and Kavun, 2006; Vattuone et al., 1976). Some of the observed variations in cadmium content from field collections of molluscs were attributable to the following: age and size of mollusc (Belcheva et al., 2006; Cossa et al., 1979; Nielsen, 1975; Noel-Lambot et al., 1980; Peden et al., 1973); moisture content (Phillips, 1976a); seasonal changes (Belcheva et al., 2006; Eisler, 1977b; Fowler and Oregioni, 1976; Phillips, 1976a); salinity of the medium (Huggett et al., 1973; Larsen, 1979; Phillips, 1976a, 1977); presence of other metals in solution (Huggett et al., 1973); chelating agents (George and Coombs, 1977); cadmium content of ambient seawater (Peden et al., 1973; Stenner and Nickless, 1974a); the diet (Peden et al., 1973; Phillips, 1977; Thorsson et al., 2008); the chemical form of cadmium (Chou et al., 1978); metabolic changes associated with increasing cadmium concentrations in tissues (Shore et al., 1975); calcium
168 Chapter 6 content of shell (Belcheva et al., 2006); and vertical concentration gradients (Nielsen, 1974; Podgurskaya and Kavun, 2006). Selected examples of biotic and abiotic modifiers of tissue cadmium concentrations follow.
6.8.1 Size of Organism In the Manila clam, Ruditapes philippinarum, there is a positive correlation between cadmium concentration in soft tissues on a DW basis and increasing shell length (Ji et al., 2006). Cadmium in the oyster Ostrea lutaria increased with increasing body weight up to about 10 g; in larger oysters, concentrations were independent of body weight (Nielsen, 1975). In mussels, M. edulis, older specimens from the Gulf of St. Lawrence contained less cadmium per unit weight than younger stages; however, the correlations were variable with increasing age and may have been related to biochemical changes during the sexual cycle (Cossa et al., 1979). In mussels, M. galloprovincialis, cadmium increased in soft parts with increasing weight (Conti et al., 2008). Clams, Gafrarium tumidum, of shell width 3.5 cm held for 15 days in seawater containing 109Cd, took up about 50 times more radiocadmium in soft parts on a weight/weight basis than in the medium; smaller clams of 2.5 cm took up more cadmium and larger clams of 5.0 cm took up the least radiocadmium (Hedouin et al., 2006). Limpets, Patella vulgata, from a metal-contaminated environment show a positive correlation between cadmium concentration and body weight (Noel-Lambot et al., 1980). Most of the cadmium present in limpets with high burdens was bound to thioneine. Because prolonged exposure of limpets to cadmium insult results in an increase in both tissue cadmium concentrations and in metallothioneins, authors conclude that the induced production of metallothioneins is responsible for the cumulative absorption of cadmium in limpets from the Bristol Channel, United Kingdom (Noel-Lambot et al., 1980); these findings have important implications in studies on ageing processes.
6.8.2 Tissue Specificity Digestive gland of squid, Illex argentinus, contains up to 1002.9 mg Cd/kg FW (Dorneles et al., 2007). Authors suggest that upwelling, cannibalism, and cadmium pollution of the studied area are possible reasons for the comparatively elevated cadmium burden in digestive gland. Tissues from other species also contained elevated cadmium burdens: up to 2000.0 mg/kg DW in visceral mass of scallops; 1780.0 mg Cd/kg DW in mussel kidney; 1163.0 mg/kg in digestive gland of abalone; and 782.0 mg/kg DW in squid liver (Table 6.5). Byssus threads from the hydrothermal vent mussel, Bathymodiolus azoricus, contained a maximum of 89.8 mg Cd/kg DW, or more than three times the level of any other tissue (Table 6.5); The role of byssus in cadmium metabolism of mussels is unknown.
Molluscs 169
6.8.3 Moisture Content Variations in wet weight of mussels, M. edulis, have been recorded, with lowest weights in winter; however, the total cadmium content of individual mussels remains almost constant throughout the year, with weight fluctuations producing much of the observed seasonality of cadmium concentrations in mussels (Phillips, 1976a).
6.8.4 Seasonality Significant differences between seasons in cadmium content of mussels from the Mersin coast, Turkey in 2002-2003(Karayakar et al., 2007), in three species of bivalves from Mexico in 2004-2005 (Frias-Espericueta et al., 2008) and in M. galloprovincialis from Morocco in 2004-2005 (Maanan, 2007) were documented (Table 6.5). Mean cadmium concentrations in mussels, M. galloprovincialis, from the NW Mediterranean Sea were similar to those measured in other species from different localities throughout the world (Fowler and Oregioni, 1976). Seasonal maxima in cadmium concentrations of mussels were observed, but this coincided with periods of high precipitation and runoff with a simultaneous increase in the suspended load in coastal waters. This increase could enhance the ambient concentrations of cadmium and other trace metals in both the soluble and particulate forms (Fowler and Oregioni, 1976). They concluded that the overall seasonal increase in metal content of mussels was more likely to be related to natural climatological conditions than to effects of local pollution.
6.8.5 Salinity Salt content of the medium was inversely associated with cadmium body burdens. At low salinities, comparatively high cadmium concentrations were measured in M. edulis (Mubiana and Blust, 2006; Phillips, 1976a) and Mercenaria (Larsen, 1979). There is significant interaction between temperature, salinity, and cadmium burdens in M. edulis. Body burdens of cadmium were relatively constant at low temperatures and high salinities, elevated at low salinities and high temperatures, and lowest at low temperatures and low salinities (Phillips, 1976a). Cadmium concentrations in mussels from low salinity waters were, in general, considerably higher than conspecifics from relatively high salinity waters (Phillips, 1977). This was not attributed to cadmium concentrations in seawater or to availability of algal food, but to the greater accumulation of cadmium by algae in low salinity waters (Phillips, 1977). Clams, Scrobicularia plana, reportedly bioaccumulate cadmium more efficiently at higher salinities within the range 16-32 ppt (Garcia-Luque et al., 2007), but this needs verification. Assimilation efficiency (AE) of 109Cd-labeled phytoplankton by the Pacific blue mussel, M. trossulus, was significantly lower at higher salinities (Widmeyer and Bendell-Young, 2007). Differences in salinity, rather than ingestion rate or food quality—as percent organic
170 Chapter 6 carbon content—seemed to best define observed differences in (Widmeyer and Bendell-Young, 2007).
Cd AE by M. trossulus
109
6.8.6 Other Metals The presence of other metals in solution, such as zinc, lead, and copper, had no effect on net uptake of cadmium from the medium by mussels (Phillips, 1976a) and this is consistent with the theory that no interaction occurred between these metals in molluscs during uptake. Also, unusually high levels of copper in whole body of American oysters, C. virginica, did not influence cadmium content of eggs. The two populations of oysters with different levels of cadmium and copper both contained less than 1.6 mg Cd/kg DW eggs (Greig et al., 1975). In digestive gland of M. galloprovincialis, superoxide dismutase enzyme activity was significantly higher at inshore stations than offshore stations while the reverse was found for glutathione peroxidase activity; this may reflect significantly different concentrations of cadmium and other metals (lead, chromium, copper, zinc, and manganese) between the two sites (Kucuksezgin et al., 2008).
6.8.7 Chemical Form Different chemical forms of cadmium exist in molluscan tissues, and these may be important in cadmium detoxification mechanisms. In scallop muscle that had 5.3 mg total Cd/kg FW, no cadmium was present in free form; however, soft parts of oysters with 0.8 mg C/kg FW contained up to 50% of the cadmium in free form (Chou et al., 1978).
6.8.8 Diet Dietary cadmium toxicity in gastropods is low, even when accumulated cadmium body burdens are high; however, metal fractionation in prey can alter the subsequent cellular metal distribution in predators (Cheung et al., 2006). Thus, predatory gastropods, Thais clavigera, fed cadmium-contaminated rock oysters, Saccostrea cucullata, for up to 4 weeks, show increases in soft parts from 3.1 mg Cd/kg DW at start to 41.8 mg/kg DW after 4 weeks. Oysters and gastropods had been exposed to dissolved cadmium for 2 weeks (0.03-0.15 mg Cd/L) before oysters were fed to gastropods; oysters had up to 90.9 mg Cd/kg DW soft parts at that time. In gastropods, an increasing proportion of cadmium was distributed in metallothionein-like proteins and organelle fractions, but the metal-rich granule fraction decreased when gastropods were fed Cd-exposed prey; metallothionein content in these gastropods was significantly higher than controls (Cheung et al., 2006). Dog whelks, Nucella lapillus, which feed extensively on limpets, P. vulgata, had more than twice as much cadmium in whole body than did whelks which do not feed on limpets or those
Molluscs 171 which include them only occasionally in the diet (Peden et al., 1973). This was attributed to the observation that limpets rapidly reflected environmental cadmium levels. American oysters and hardshell clams show a continual increase in tissue cadmium concentrations during exposure to seawater and algae contaminated with cadmium. Algae were the main source of accumulation while direct absorption of soluble cadmium from seawater was another pathway of accumulation in molluscs (Kerfoot, 1979). Cadmium uptake in fed mussels, M. edulis, was significantly higher from the medium than starved mussels. The elevated cadmium concentrations measured were not attributed to cadmium-contaminated food but to increased pumping rate when food is available. Highest cadmium concentrations and major body burdens were in the mid-gut gland (Janssen and Scholz, 1979). Transport via hemolymph, and selective discrimination at the basement lamina of mid-gut gland tubuli appears to be the main accumulation route. In the tubuli, cadmium is immobilized in membrane-bound vesicles and eventually excreted (Janssen and Scholz, 1979). Green mussels, Perna viridis, exposed to 0.005, 0.02, 0.05, or 0.2 mg Cd/L for 7 days, 16 h daily, all had higher metallothionein synthesis rates when compared to controls; dietary assimilation of cadmium increased by a factor of 2 at 0.02 mg Cd/L and higher (Ng et al., 2007). Dissolved cadmium is the main source of cadmium to cultured Pacific oysters, C. gigas, where it concentrated mainly in gut tissues, with accumulation lower during summer; particulate matter was not a source of cadmium in oysters (Lekhi et al., 2008).
6.8.9 Ambient Cadmium Concentrations Transplantation of molluscs from cadmium-free waters to areas heavily contaminated by cadmium and other metals wastes was reflected in elevated tissue concentrations of cadmium. For example, dog whelks transplanted from Beer, Dorset, United Kingdom, to Bristol Channel, United Kingdom, showed a rise in tissue levels from 36.0 mg Cd/kg DW at the start to 211.0 mg Cd/kg DW after 5 months; the rise was even more dramatic (from 11.0 to 220.0) for Patella sp. transplanted for 8 months (Stenner and Nickless, 1974a). Cadmium sediment concentrations of 0.2 mg/kg DW in Jiaozhou Bay, China, were much lower than were cadmium concentrations in soft parts of clams, R. philippinarum (0.51-0.67 mg/kg DW); this was not the case for copper, zinc, lead, manganese, and chromium (Li et al., 2006). The reverse was true for cockles, Anadara trapezia, from a metals-contaminated estuary in New South Wales, Australia in April 2000: in that case, cadmium—as well as zinc and lead—concentrations in soft parts of the cockle were highly correlated with cadmium, zinc, and lead sediment burdens, respectively (Burt et al., 2007). Sediment composition dramatically affects cadmium accumulation by softshell clams, M. arenaria, during the first 24 h (Phelps, 1979). Virtually all radiocadmium-109 sorbed to
172 Chapter 6 bentonite was taken up; for humic acid-109Cd, this value was 60%; for mud sediment-Cd, 33%; and for albumin-Cd, only 12%. Shell sorbed twice as much cadmium than soft tissues during the first 230 min of exposure (Phelps, 1979). Availability of sediment-bound cadmium to cockles, Cerastoderma edule, is dependent on whether cadmium was bound to biogenic calcium carbonate (readily available) or precipitated calcium carbonate (low availability) (Cooke et al., 1979). Also, cadmium bound to iron oxide and manganese oxide was unavailable to cockles, at least in short-term exposure. In general, cadmium availability to cockles seems to be a function of the ability of cadmium to desorb from the sediment (Cooke et al., 1979).
6.8.10 Metabolism Increasing body burdens of cadmium were associated with metabolic changes. In one case, as cadmium increased in digestive gland of limpets, P. vulgata, from 27.0 to 537.0 mg/kg DW, there was a significant decrease in glycolytic rate and corresponding increase in hemolymph glucose (Shore et al., 1975).
6.8.11 Depth Vertical concentration gradients of heavy metals, including cadmium, in mussels, Perna canaliculis, are reported in some locations, but not others (Nielsen, 1974). Differences in mixing of the water column, which in turn causes variations in the type of food organisms with depth, or variations in the ratio of particulate/dissolved metal levels with depth, could account for this phenomenon (Nielsen, 1974). Similar findings were reported for M. edulis (Talbot et al., 1976b). Near freshwater inputs of trace metals, concentrations of cadmium in M. edulis varied with water depth of collection, being greater in shallower waters; however, this effect was absent in summer when freshwater runoff was reduced (Phillips, 1976a).
6.8.12 Laboratory Studies Accumulation of cadmium by bivalve molluscs under controlled conditions is the subject of several investigations (Alquezar et al., 2007; Brooks and Rumsby, 1967; Chuang and Wang, 2006; Eisler et al., 1972; Hiyama and Shimizu, 1964; Mubiana and Blust, 2007; Nelson et al., 1976; Ng et al., 2007; Noel-Lambot, 1976; Pesch and Stewart, 1980; Pringle et al., 1968; Shuster and Pringle, 1969; Sturesson, 1978; Zaroogian, 1979; Zaroogian and Cheer, 1976). Brooks and Rumsby (1967) report that oysters, Ostrea sinuata, held in high (50.0 mg Cd/L) concentrations of cadmium for 100 h accumulated this metal strongly in gills, visceral mass, and heart; high cadmium accumulations in oyster tissues had relatively little effect on concentrations of silver, manganese, lead, vanadium, or zinc in the same tissues, although
Molluscs 173 some displacement may have occurred in visceral mass. Uptake was attributed to nonselective adsorption of cadmium, possibly by coordination to organic ligands (Brooks and Rumsby, 1967). American oysters, C. virginica, and scallops, Aquipecten irradians, that were immersed in flowing seawater containing 0.01 mg Cd/L for 21 days bioconcentrated cadmium by factors of 5.6 and 2.4 respectively in whole soft parts (Eisler et al., 1972). It has been stated that it is the concentration of cadmium in water and food and not the absolute amount that determines acute cadmium poisoning as indicated by vomiting (USPHS, 1962). On this basis, American oysters quickly accumulated emetic thresholds concentrations of cadmium, that is 13.0-15.0 mg Cd/kg FW, when cadmium levels in the medium exceeded 0.01 mg Cd/L. Emetic thresholds were surpassed in 5 and 2 weeks at cadmium water levels of 0.025 and 0.1 mg Cd/L, respectively (Shuster and Pringle, 1969). Similar results were documented in other species of oysters (Casterline and Yip, 1975) and in clams (Shuster and Pringle, 1968). Rates of accumulation in bivalve molluscs were not linearly related to ambient cadmium concentrations. For softshell clam, M. arenaria, daily accumulation rates, in mg Cd/kg FW, were 0.16 for clams held in solutions of 0.1 mg Cd/L, and 0.1 for those immersed in 0.05 mg Cd/L (Pringle et al., 1968). Concentrations as low as 0.005 mg Cd/L in flowing seawater were also accumulated to potentially hazardous levels (13.6 mg Cd/kg FW soft parts) by American oysters after an extended exposure of 40 weeks (Zaroogian and Cheer, 1976). Cadmium-loaded oysters retained virtually all accumulated cadmium (12.5 mg Cd/kg FW soft parts) during a period of 16 weeks immersion in clean seawater (Zaroogian, 1979), with attendant risk to human consumers. Glycoproteins reportedly protect bivalve molluscs against cadmium (Ivanina and Sokolova, 2008). American oysters, C. virginica, exposed to 0.05 mg Cd/L for 30-40 days produced a 2.0- to 2.5-fold increase in glycoprotein content on cell membrane and mitochondria of gills and hepatopancreas, and a 3.5- to 7.0-fold increase in transport rate (Ivanina and Sokolova, 2008). Scallops, A. irradians, held for 6 weeks in seawater solutions containing 0.06 mg Cd/L contained up to 1253.0 mg Cd/kg DW soft parts versus 7.6 in controls; higher residues were observed in scallops that survived 0.12, 0.25, and 0.5 mg Cd/L for a similar period (Pesch and Stewart, 1980). Mussels, M. edulis, subjected to alternate immersion and emersion characteristic of tidal cycles accumulated significantly less cadmium that did continually immersed mussels (Coleman, 1980). It is noteworthy that mussels held 15 days in seawater solutions containing 0.035 mg Cd/L always accumulated more than 2.0 mg Cd/kg FW soft parts, which is the maximum safe value specified by Australian authorities for edible shell fish (Coleman, 1980); this value has since been modified for shellfish to <2.0 mg Cd/kg on a DW basis (Machreki-Ajmi and Hamza-Chaffai, 2006). Shells from M. edulis held in seawater solutions containing 0.2 mg Cd/L for 50 days had 75.0 mg Cd/kg DW in shell periostracum, 17.0 mg/kg
174 Chapter 6 in the nacreous layer, and 13.0 mg Cd/kg DW in newly formed calcite (Sturesson, 1978). In untreated M. edulis, cadmium was associated with molecular proteins of high weight, but after exposure of 90 days in 0.005 mg Cd/L, cadmium was bound to low-molecularweight proteins, similar to vertebrate metallothioneins and apparently synthesized in a like manner as vertebrates (Noel-Lambot, 1976). Isolated gills of the common mussel, M. edulis, were held for 28 days in seawater containing 0.003 mg Cd/L at water temperatures between 6 and 26 C (Mubiana and Blust, 2007). Increasing cadmium concentrations were measured at increasing water temperatures; whole mussels showed the same trend, but elimination was independent of water temperature (Mubiana and Blust, 2007). Uptake and elimination patterns for isolated gills and whole mussel were the same for lead exposures. Cobalt and copper uptake and elimination patterns in whole mussels were different from those of copper and lead, and it is not possible to generalize (Mubiana and Blust, 2007). Mussels, Mytilopsis sallei, all survived immersion in 0.05 mg Cd/L for 96 h; however, 0.71 mg Cd/L was fatal to 50% in that same time period (Devi, 1996). Adaptation to environmental cadmium stress is reported for M. sallei exposed to sublethal concentrations >0.05 mg Cd/L for at least 96 h (Devi, 1996). The decrease in oxygen consumption and the increased metabolism of glycogen and carbohydrates during cadmium exposure suggest that M. sallei could shift to anaerobic metabolism to counter the environmental cadmium stress (Devi, 1996). Uptake and retention of radiocadmium-109 was studied in the pygmy mussel, Xenostrobus securis (Alquezar et al., 2007). Mussels were held for 385 h in seawater spiked with 109Cd followed by 189 h in 109Cd-free media. During uptake, whole mussels concentrated radiocadmium by a factor of 81 over seawater; during the loss phase, 77% of the accumulated radiocadmium was excreted in a biphasic pattern. The biological half-time of the short-lived component was 11 h; for the long-lived component, it was 2140 h (about 89 days; Alquezar et al., 2007). Uptake of ligand-bound 109Cd by the green mussel, P. viridis, indicates that metal-ligand complexes were available for uptake independent of free cadmium concentration (Chuang and Wang, 2006). Scallops, Comptopallium radula, exposed to 109Cd for four days had a BCF of 62 in soft parts; however, uptake was greater in kidney with a BCF of 169 (Metian et al., 2008). Eggs of the cuttlefish, S. officinalis, exposed to 109 Cd during embryonic development and also stable cadmium at 0.001 mg Cd/L did not accumulate cadmium in yolk material; both stable cadmium and radiocadmium were mainly associated with eggshell, indicating that the eggshell acted as an efficient shield against penetration (Lacoue-Labarthe et al., 2008a,b). Eggs of the European squid developed normally at 0.01-0.1 mg Cd/L; however, effects on survival and development were demonstrable at 1 mg Cd/L and higher (Sen and Sunlu, 2007). Feeding rate of clams, Donax trunculus, was inhibited 60% during immersion in seawater containing 0.1 mg Cd/L for 24 h (Neuberger-Cywiak et al., 2007).
Molluscs 175
6.9 Cerium Concentrations of stable cerium in the tests of six species of pteropod molluscs ranged between 0.26 and 3.03 mg Ce/kg DW (Turekian et al., 1973). All species of molluscs examined accumulated cerium from ambient seawater by factors that ranged from 100 to 1200 (Avargues et al., 1968; LeGall and Ancellin, 1971). The addition of chelating agents to the medium reduced concentration factors to <1 for the clam Venerupis philippinarum (Hiyama and Shimizu, 1964). Radiocerium-144 concentrations in tissues of the clam Anadara granosa reflected sediment 144Ce concentrations (Patel et al., 1978). On reaching maximum accumulations, the concentration of 144Ce (and also cesium-137 and ruthenium-106) decreased exponentially over time, although 144Ce was still available in sediments.
6.10 Cesium Stable cesium concentrations in molluscan tissues never exceeded 0.13 mg Cs/kg DW, or 0.007 mg Cs/kg FW (Table 6.6).
Table 6.6: Cesium Concentrations in Field Collections of Molluscs Organism
Concentration
Reference
Mussel, Choromytilus meridionalis; soft parts
0.0070 FW
1
Clam, Donax serra; soft parts
0.0049 FW
1
Abalone, Haliotis midea; soft parts
0.0002 FW
1
Clam, Meretrix lamarckii; soft parts
0.022 DW
2
Molluscs, 3 spp; edible flesh
0.001-0.007 FW
3
Mussel, Mytilus corscum; soft parts
0.023 DW
2
Common mussel, Mytilus edulis; soft parts
0.0004-0.13 DW
4
Abalone, Notohaliotis discus; soft parts less viscera
0.029 DW
2
Limpet, Patella candei gomesii; soft parts; 2007; Azores Near hydrothermal vent Reference site
0.05-0.13 DW 0.02 DW
5 5
Squid, Sepia esculenta; trunk
0.016 DW
2
a
Values are in mg Cd/kg fresh weight (FW) or dry weight (DW). a 1, Van As et al., 1973; 2, Ishii et al., 1978; 3, Van As et al., 1975; 4, Karbe et al., 1977; 5, Cunha et al., 2008.
176 Chapter 6 As a result of the Chernobyl nuclear reactor plant accident on April 26, 1986 (Eisler, 1995b, 2003), radiocesium-137 levels (but not 134Cs levels) in seven species of molluscs collected near a nuclear plant increased by a factor up to 6 (Lowe and Horrill, 1991). Mussels, M. galloprovincialis, accumulated 134Cs and 137Cs in soft parts following the Chernobyl nuclear reactor accident; however, between May 6 and August 14, 1986, mussels lost 98.4% of the accumulated 134Cs and 94.4% of the 137Cs (Whitehead et al., 1988). Using M. galloprovincialis as an indicator or 137Cs activity in the Mediterranean Sea and Black Sea during 2004-2006, mussels with the highest radioactivity levels were confined to the Black Sea and North Aegean Sea and reflect fallout from Chernobyl (Thebault et al., 2008). In summer 2004, 137Cs activity above minimum detectable levels was measured in Pacific octopus, Enteroctopus dofleini, from Amchitka Island in the Aleutian chain; Amchitka Island was the site of three nuclear tests between 1965 and 1971 (Burger et al., 2007). However, no 137Cs activity was detected in summer 2004 samples of chiton, Cryptochiton stelleri, rock jingle, P. macroschisma, or plate limpet, Tectura scutum from Amchitka Island (Burger et al., 2007b). Studies on radiocesium-137 accumulation and retention by marine molluscs under controlled environments (Argiero et al., 1966; Avargues et al., 1968; Bryan, 1963a,b; Hiyama and Shimizu, 1964; LeGall and Ancellin, 1971; Ueda et al., 1978; Van As et al, 1973) show similar results. In one of the more exhaustive studies, Bryan (1963b) established that six species of marine gastropods and bivalves reached equilibrium with ambient 137Cs levels between 300 and 1400 h, that concentration factors for any tissue in any species never exceeded 15.3, that highest accumulations were usually in muscle and digestive gland, and the lowest concentration factors were in plasma, shell, and mucous. In one species, Archidoris pseudoargus, gonad was the second most active site of 137Cs, next to digestive gland (Bryan, 1963b). Data seem needed on effect of cesium translocation to sex products on molluscan embryonic development. Accumulation of 137Cs was measured in the cephalopods Octopus vulgaris and Doryteuthis bleekeri (Ueda et al., 1978). Concentration factors for Octopus after 14 days were highest for liver (12.8), ovotestis (10.9), kidney, funnel, branchial heart (8.0-8.3), heart, anus, tentacles, buccal bulb, ctenidia, gastric caecum (6.1-7.5) stomach, sucker, esophagus, salivary gland (4.7-5.7), and mantle (3.5), in that order. Most, that is, 90–95%, of the radioactivity was eliminated in 75 days. Concentration factors for Doryteuthis after 6 days ranged between 8 and 11 for the tissues examined (Ueda et al., 1978). Salinity of the medium affects cesium uptake mechanisms in the euryhaline clam Rangia cuneata. In one study, Rangia contained lower cesium concentrations in waters of higher salinities (Wolfe, 1970). Studies on the interaction of salinity with temperature on radiocesium-137 uptake by Rangia show that uptake in soft parts was lower with increasing salinity, as expected, but uptake increased with increasing temperature; in shell, however, the proportion of cesium decreased as both salinity or temperature was increased (Wolfe and Coburn, 1970).
Molluscs 177 Recent uptake studies (Bustamante et al., 2006) on 134Cs uptake by different developmental stages of cuttlefish, S. officinalis, via the sediments, medium, and diet demonstrate that uptake from sediments was negligible compared to seawater and diet. In the seawater portion, for example, whole juveniles exposed to 134Cs for 36 h had a BCF of 4.1; after 29 days in clean seawater; 61% of the radioactivity was retained in digestive gland. Adults held for 8 h in 134Cs-spiked seawater, had a BCF <2 for all tissues, with half-time persistence of 6 days. Cuttlefish fed a radiolabeled 134Cs diet of mussels and brine shrimp for 1 h then transferred to clean seawater for 29 days still retained 54% of the 134Cs in digestive gland; the calculated half-time persistence of 134Cs was 5 days (Bustamante et al., 2006). Gravid cuttlefish fed crabs radiolabeled with 134Cs over a 2 week period to determine rate of maternal transfer into eggs showed no significant transfer (Lacoue-Labarthe et al., 2008b).
6.11 Chromium Chromium concentrations were usually elevated in molluscs and other marine biota in the vicinity of electroplating plants, tanneries, ocean dump sites, oil drilling operations, sewage outfalls, and other sources of chromium-containing wastes (Eisler, 2000a; Maanan, 2007; Table 6.7). Edible tissues of commercially important North American species of marine molluscs contained between 0.1 and 0.6 mg Cr/kg FW (Hall et al., 1978), and this is in general agreement with molluscan data from other geographic areas (Table 6.7). However, higher chromium values of 3.4 mg Cr/kg FW are documented in edible portions of American oysters, C. virginica, 5.8 mg Cr/kg FW in hardshell clam, Mercenaria, and 5.0 mg Cr/kg FW in softshell clam, M. arenaria (Shuster and Pringle, 1968). The ability of marine molluscs to accumulate chromium far in excess of ambient seawater concentrations is documented in five species of bivalves from Greek waters; concentration factors ranged from 16,000 in P. nobilis to 260,000 in Astralium rogosum (Papadopoulu, 1973). No deleterious health effects are documented among consumers of molluscs with occasional high chromium content. Anthropogenic and natural chromium gradients in water column or sediments are reflected in the wide range of values reported for this element in field collections of Mercenaria mercenaria (Phelps et al., 1975), M. edulis (Karbe et al., 1977; Lande, 1977); Pitar morrhuana (Eisler et al., 1978), Mytilus californianus (Alexander and Young, 1976), and M. galloprovincialis (Fowler and Oregioni, 1976). Two variables linked to chromium accumulations in tissues of field-collected molluscs are the weight of the organism and the salinity of the medium. For example, decreasing concentrations of chromium in R. cuneata tissues occur with increasing body weight and increasing salinities (Olson and Harrel, 1973).
178 Chapter 6 Table 6.7: Chromium Concentrations in Field Collections of Molluscs Organism
Concentration
Reference
Gastropod, Acmaea digitalis Shell Soft parts
<5.7 DW 7.1-24.2 DW
1 1
Mussel, Anodonta sp. Shell Soft parts
0.45 DW 0.84 DW
2 2
Giant squid, Architeuthis dux; 2001-2005; hepatopancreas Bay of Biscay Mediterranean Sea
0.9 DW 0.5 DW
67 67
Ocean quahaug (clam), Arctica islandica; soft parts
0.3-2.5 FW
3
Bay scallop, Argopecten irradians; kidney concretion
49.3 DW
4
Cockle, Austrovenus stutchburyi; soft parts; 1993-1994; New Zealand
1.0-44.0 DW
50
Mussel, Brachydontes pharaonis; Mersin coast, Turkey; 2002-2003; max. concentrations Muscle Gill Hepatopancreas
8.9 DW 19.0 DW 6.5 DW
47 47 47
Whelk, Busycon canaliculatum Muscle Digestive gland Digestive diverticula Gills
<0.8 FW <0.8 FW 0.24 DW 4.2 DW
5 5 6 6
Cockle, Cerastoderma edule; soft parts
1.3-2.5 DW
7
Scallop, Chlamys opercularia Soft parts Kidneys Digestive gland
2.2 DW 6.6 DW 4.7 DW
8 8 8
Mussel, Choromytilus meridionalis Soft parts Soft parts
1.4 DW 0.10-0.13 FW
a
9 10, 11 (Continues)
Molluscs 179 Table 6.7:
Cont’d
Organism
Concentration
Scallop, Comptopallium radula; Santa Marie Bay, New Caledonia; October 2004 Soft parts Digestive gland
3.3 (2.4-5.0) DW 16.8 DW
60 60
Pacific oyster, Crassostrea gigas; soft parts
0.1-0.3 FW
12
0.04-3.4 FW 1.8-7.3 FW Max. 0.71 FW
13 14 54
<1.5 to 8.0 DW
59
American oyster, Crassostrea virginica Soft parts Shell Soft parts; Pensacola, Florida; 2003-2004 Soft parts; Savannah, Georgia; 2000-2001
Reference
Limpet, Crepidula fornicata; soft parts
2.0 DW
Clam, Donax serra; soft parts
0.19-0.24 FW
10, 11
Clam, Ensis arcuatus; shell
0.14 DW
15
Clam, Ensis siliqua; shell
0.13 DW
15
Abalone, Haliotis midea; soft parts
0.44-0.5 FW
10, 11
Red abalone, Haliotis rufescens Gill Mantle Digestive gland Foot
0.6-4.0 DW 0.0-12.6 DW 2.0-13.2 DW not detectable
16 16 16 16
Periwinkle, Littoraria scabra; soft parts; Tanzania Industrial sites; 1998 vs. 2005 Reference site; 2005
7.0 DW vs. 8.5 DW 4.0 DW
62 62
Limpet, Littorina littorea Soft parts plus operculum Soft parts; United Kingdom
0.1-1.0 DW <0.1 to 1.6 DW
7 40
Clam, Macoma balthica; soft parts
1.9-3.3 DW
7
Hardshell clam, Mercenaria mercenaria Soft parts Soft parts Soft parts Shell
3.3-24.7 DW 0.2-5.8 FW 0.8 DW 0.37 DW
17 13 2 2
a
2
(Continues)
180 Chapter 6 Table 6.7:
Cont’d
Organism
Concentration
Mussel, Modiolus modiolus Soft parts Mantle and Gills Muscle Gonad Gut and digestive gland
0.14 DW 0.15 DW 0.2 DW 0.2 DW 0.19 DW
Molluscs; commercially important; edible tissues 3 spp. 5 spp. 8 spp. 2 spp. 6 spp.; Spain; April-May 1990; Mediterranean Sea 3 spp.; India; 2003
Reference
a
2 2 2 2 2
0.1-0.2 FW 0.2-0.3 FW 0.3-0.4 FW 0.4-0.6 FW 0.06-0.39 FW
18 18 18 18 39
0.3-0.9 FW
57
Morocco; 2001; clams; soft parts Scrobicularia plana Cerastoderma edule
6.0 DW 1.0 DW
63 63
Morocco; 2004-2005; soft parts Mussel, Mytilus galloprovincialis Clam, Venerupis decussatus Pacific oyster, Crassostrea gigas
8.8 (4.0-20.6) DW 9.6 (4.3-15.3) DW 7.1 (1.2-15.3) DW
61 61 61
Gastropod, Murex trunculus; soft parts
1.3 DW
19
Softshell clam, Mya arenaria Soft parts Soft parts
1.8-4.4 DW 0.1-0.5 FW
20 13
California mussel, Mytilus californianus Digestive gland Shell Soft parts
1.0-61.0 DW <5.7 to 14.2 DW <1.5 to 7.8 DW
21 1 1
Common mussel, Mytilus edulis Digestive gland Gonad Muscle Shell Shell Shell; Baltic Sea; 2005; 12 sites Hepatopancreas
7.4 FW 3.0 FW 11.0 FW 1.0-2.0 DW 0.1 DW 1.1-1.4 DW 3.5-15.0 DW
22 22 22 24 15 64 25 (Continues)
Molluscs 181 Table 6.7: Organism Soft parts; Scheldt estuary; March 2000 Soft parts Soft parts Soft parts Soft parts Soft parts Gills; near leather tannery effluent vs. reference site; Ireland; River Calligan; 1992-1994 Mussel, Mytilus edulis-aoteanus Soft parts Gill Visceral mass Pacific blue mussel, Mytilus edulis trossulus; soft parts; 2004; 5 sites; Adak Island, Alaska Mussel, Mytilus galloprovincialis Soft parts; Venice lagoon, Italy; 2005-2006; San Giuliano vs. Sacca Sessola April July October February Soft parts Soft parts Soft parts; 1991-2005; western Mediterranean Sea; Balearic Islands; Port of Mahon Soft parts; May 2003; NW Mediterranean Sea Italy; near Genova France; near Marseille Spain; near Barcelona Soft parts; summers 2004-2005; Mediterranean Sea; 3 sites Soft parts; Adriatic Sea; 2001-2005; winter vs. summer Mantle vs. gills; Saronikos Gulf of Greece; 2004-2006; max. mean concentrations; contaminated sites
Cont’d
Concentration
Reference
5.8 DW
66
1.0-1.5 DW 0.9-2.7 DW <1.0 to 7.6 DW 4.0-49.0 DW Max. 3.0 DW 400.0-1000.0 DW vs. max. 6.0 DW
25 7 1 24 48 41
16.0 DW 10.0 DW 29.0 DW
26 26 26
20.7 FW; max. 148.0 FW; 62.0-170.0 DW
52
2.8 DW vs. 1.6 DW 0.2 DW vs. 0.7 DW 0.5 DW vs. 0.7 DW 0.8 DW vs. 2.0 DW 7.5 DW 4.4 FW 4.6 (0.7-14.8) DW
55 55 55 55 27 28 45
1.7-5.1 DW 0.71-3.3 DW 3.2-24.4 DW 0.4-3.0 DW
44 44 44 58
1.1-2.3 DW vs. 0.4-0.8 DW
68
a
(Continues)
182 Chapter 6 Table 6.7: Organism Summer Autumn Winter Spring Soft parts; Adriatic Sea; 2001-2002; summer vs. winter Industrialized sites Reference site Soft parts; Izmir Bay, Turkey; 2004; near shore vs. mid-bay Soft parts; Gulf of Gemlik, Turkey; 2004
Cont’d
Concentration
Reference
2.3 FW vs. 4.2 FW 0.39 FW vs. 0.57 FW 0.2 FW vs. 0.4 FW 1.4 FW vs. 0.55 FW
47 47 47 47
3.7-4.7 DW vs. 4.4-10.3 DW 3.4 DW vs. 2.7 DW 0.17 DW vs. 0.12 DW
51 51 65
2.3 DW
70
Octopus, Octopus cyanea; Guam; June 1998; tentacle vs. liver
<0.16 DW vs. 1.87 DW
42
Oyster, Ostrea edulis; soft parts
0.1-2.1 DW
29
Oyster, Ostrea sinuata Soft parts Heart
3.0 DW 9.0 DW
26 26
Scallop, Pecten maximus Soft parts Kidneys Digestive gland Mantle and gills Gonad
1.3-1.8 DW 3.9 DW 8.1 DW 0.76 DW 0.45 DW
Scallop, Pecten novae-zelandiae Soft parts Gills Intestine Kidney Foot
10.0 DW 145.0 DW 24.0 DW 17.0 DW 8.0 DW
26 26 26 26 26
Pen shell, Pinna nobilis Soft parts Mantle and gills Muscle Nervous system Stomach and intestine Gonads Hepatopancreas
5.8 DW 16.0 DW 3.9 DW 6.3 DW 6.2 DW 22.0 DW 150.0 DW
30 30 30 30 30 30 30
a
2, 8 8 8 2 2
(Continues)
Molluscs 183 Table 6.7: Organism Byssus Byssus gland
Cont’d
Concentration
Reference
32.0 DW 12.0 DW
30 30
False quahaug, Pitar morrhuana; soft parts
3.1-14.2 DW
31
Pteropods; 9 spp.; tests
0.43-4.9 DW
32
Clam, Rangia cuneata; whole
0.32 FW
33
Manila clam, Ruditapes philippinarum; soft parts; Korea; 2002-2003 Females vs. males Postspawn vs. prespawn
1.05 DW vs. 1.07 DW 1.6 DW vs. 1.1 DW
43 43
Clam, Spisula solidissima; muscle
0.7-2.7 DW
6
Whelk, Nucella lapillus; soft parts plus operculum
0.4-5.6 DW
7
0.5-2.6 DW 7.0-17.0 DW 1.0-2.0 DW
7 24 24
3.3 (0.8-11.0) DW
45
0.09 FW 0.07 FW 0.01 FW
53 53 53
1.1 DW vs. 1.0 DW 0.9 DW vs. 2.4 DW
69 69
1.7 DW vs. 1.5 DW 4.2 DW vs. 2.4 DW
69 69
3.1 DW <0.3 to 0.6 FW
34 35
Limpet, Patella vulgata Soft parts Soft parts Shell European flat oyster, Ostrea edulis; soft parts; Balearic Islands; western Mediterranean Sea; 1991-2005; Port of Mahon Green mussel, Perna viridis India; 28 sites; January 2002; soft parts Small Medium Large Hong Kong; juveniles vs. adults Reference site Soft parts Byssus Polluted site Soft parts Byssus Scallop, Placopecten magellanicus Soft parts Muscle
a
(Continues)
184 Chapter 6 Table 6.7: Organism Gonad Visceral mass Soft parts
Cont’d
Concentration
Reference
0.3-1.7 FW 0.4-4.0 FW 0.2-2.4 FW
35 35 3
65.3 DW vs. <0.01 DW
49
0.14-0.63 DW
49
2.8 (1.1-3.9) DW
37
2.1 (0.5-4.2) DW 6.9 (3.9-12.8) DW
36 36
1.5-2.2 DW 3.6 DW 2.1 DW 1.1 DW
37 37 37 37
1.2-1.3 DW 2.9 DW 1.4 DW 0.6 DW 2.3 DW
37 37 37 37 37
6.3 DW 1.2 DW
37 37
3.7 DW 1.2 DW
37 37
Squid Muscle Muscle with skin Viscera Pen
5.4 DW 4.7 DW 3.9 DW 3.1 DW
38 38 38 38
Clam, Tapes semidecussata Shell Soft parts
10.3 DW 10.3 DW
1 1
Clam, Ruditapes philippinarum Jiaozhou Bay, China; sediments vs. soft parts; November 2004 Bohai Sea, China; soft parts Clam, Scrobicularia plana Looe estuary, England; soft parts Tamar estuary, England Soft parts Digestive gland Gannel estuary, England Soft parts Digestive gland Mantle and siphons Foot and gonad Camel estuary, England Soft parts Digestive gland Mantle and siphons Foot and gonad Gills and palps Transferred from Camel estuary to Gannel estuary for 352 days Digestive gland Remaining tissues Transferred from Gannel estuary to Camel estuary for 352 days Digestive gland Remaining tissues
a
(Continues)
Molluscs 185 Table 6.7:
Cont’d
Organism
Concentration
Gastropod, Thais emarginata Shell Soft parts
<5.7 to 10.5 DW <1.5 DW
1 1
<1.0 to 6.2 DW
56
Clam, Trivela mactroidea; Venezuela; 2002; 14 sites; soft parts
Reference
a
Values are in mg Cr/kg fresh weight (FW) or dry weight (DW). a 1, Graham, 1972; 2, Segar et al., 1971; 3, Palmer and Rand, 1977; 4, Carmichael et al., 1979; 5, Greig et al., 1977; 6, Greig, 1975; 7, Bryan and Hummerstone, 1977; 8, Bryan, 1973; 9, Watling and Watling, 1976a; 10, Van As et al., 1973; 11, Van As et al., 1975; 12, Pringle et al., 1968; 13, Shuster and Pringle, 1968; 14, Ferrell et al., 1973; 15, Bertine and Goldberg, 1972; 16, Anderlini, 1974; 17, Phelps et al., 1975; 18, Hall et al., 1978; 19, Fukai, 1965; 20, Eisler, 1977b; 21, Alexander and Young, 1976; 22, Young and McDermott, 1975; 23, Karbe et al., 1977; 24, Lande, 1977; 25, Young et al., 1979; 26, Brooks and Rumsby, 1965; 27, Fowler and Oregioni, 1976; 28, Uysal, 1978a; 29, Fukai et al., 1978; 30, Papadopoulu, 1973; 31, Eisler et al., 1978; 32, Turekian et al., 1973; 33, White et al., 1979; 34, Reynolds, 1979; 35, Greig et al., 1978; 36, Bryan and Uysal, 1978; 37, Bryan and Hummerstone, 1978; 38, Horowitz and Presley, 1977; 39, Schuhmacher et al., 1992; 40, Bryan et al., 1983; 41, Walsh and O’Halloran, 1998; 42, Denton et al., 2006; 43, Ji et al., 2006; 44, Zorita et al., 2007; 45, Deudero et al., 2007; 46, Vlahogianni et al., 2007; 47, Karayakar et al., 2007; 48, Mubiana and Blust, 2006; 49, Li et al., 2006; 50, Peake et al., 2006; 51, Scancar et al., 2007; 52, Burger and Gochfeld, 2006; 53, Sasikumar et al., 2006; 54, Karouna-Renier et al., 2007; 55, Nesto et al., 2007; 56, LaBrecque et al., 2004; 57, Sankar et al., 2006; 58, Lafabrie et al., 2007; 59, Kumar et al., 2008; 60, Metian et al., 2008; 61, Maanan, 2008; 62, De Wolf an Rashid, 2008; 63, Anajjar et al., 2008; 64, Protasowicki et al., 2008; 65, Kucuksezgin et al., 2008; 66, Wepener et al., 2008; 67, Bustamante et al., 2008; 68, Fattorini et al., 2008; 69, Nicholson and Szefer, 2003; 70, Unlu et al., 2008.
Hexavalent chromium accumulation rates by oysters, C. virginica, were studied over a 20 week period (Shuster and Pringle, 1968). Oysters were continuously subjected to seawater solutions containing 0.05 or 0.1 mg Cr6+/L. After 5, 10, or 20 weeks in 0.05 mg Cr/L, maximum soft parts concentrations in mg total Cr/kg FW were 2.4, 3.7, and 6.3, respectively, up from control values of <0.12. Oysters held in 0.1 mg Cr/L contained 4.4 mg/kg FW after 5 weeks, 6.4 after 10 weeks, and 11.5 after 20 weeks (Shuster and Pringle, 1968). Preston (1971) concluded that C. virginica, under laboratory conditions, accumulated chromium more readily by direct absorption from the medium than from diet, using radiochromiumlabeled algae, Chlamydomonas spp. However, in nature, chromium is likely to be greater in the food supply than in the water, and food supply would be the main source of chromium to oysters even though accumulation occurs more readily by direct absorption (Preston, 1971). Studies with 51Cr and clams, G. tumidum, of 3.5 cm shell width show that soft parts of clams after 15 days took up 10 to 40 times more radiochromium than in seawater; concentration factors were higher for clams of 2.5 cm shell width and lower at 5.0 cm shell width (Hedouin et al., 2006). Clams, oysters, and mussels take up chromium from seawater or from chromium-contaminated sediments at comparatively low concentrations. For example, American oysters subjected to 0.005 mg Cr6+/L for 12 weeks contained 3.1 mg Cr/kg DW in
186 Chapter 6 soft parts and retained 52% of the accumulated chromium after they were transferred to chromium-free seawater for 28 weeks (Zaroogian and Johnson, 1983). Common mussels subjected to the same dose-time regimen contained 4.8 mg/kg but retained only 39% after 28 weeks of depuration. Both oysters and mussels contained higher residues after exposure to 0.01 mg Cr/L for 12 weeks—5.6 and 9.4 mg Cr/kg DW in soft parts, respectively—and both contained substantial (30-58%) residues after 28 weeks in a chromium-free environment (Zaroogian and Johnson, 1983). Chromium residues in cockle, Austrovenus stutchburyi, soft parts collected over the period 1993-1994 ranged between 1.0 and 44.0 mg Cr/kg DW; however, residues were highest in August (Peake et al., 2006). It is emphasized that trivalent chromium (Cr3+), probably because of its very low solubility in seawater, seems to have a much lower bioavailability to molluscs and other groups of marine animals than hexavalent chromium, which is more water soluble (Carr et al., 1982). The clam, R. cuneata, appears to be an exception: it accumulated up to 19.0 mg Cr/kg in soft parts, on a DW basis, during exposure for 16 days to chromium-contaminated muds, and retained most of it for an extended period; the estimated biological half-time was 11 days (Carr et al., 1982). Studies with the green mussel, P. viridis, and Cr3+ show that 1.0 mg Cr3+/L is not fatal in 96 h, but oxygen consumption, filtration rate, and ATPase activity were all significantly decreased (Vijayavel et al., 2007). Proposed national chromium criteria in seawater for marine life protection include <0.018 mg Cr6+/L as 24 h average, not to exceed 1.26 mg/L at any time (USEPA, 1980a). For California, the following are proposed: <0.002 mg/L total chromium, 6 month median; <0.008 mg/L total chromium, daily maximum; <0.02 mg/L instantaneous mix (Ecological Analysts, 1981); and <0.005 mg total chromium/L for 50% of measurements, and <0.01 mg/L for 10% of measurements (Reish, 1977). To protect human consumers of molluscan shellfish, tissues should not exceed 13.0 mg Cr/kg FW (Sankar et al., 2006), although some locales now propose concentrations as low as 0.3-0.4 mg Cr/kg DW molluscan tissues (Kucuksezgin et al., 2008).
6.12 Cobalt Maximum cobalt values recorded in molluscan tissues were 7.2 mg Co/kg on a FW basis and 121.0 mg Co/kg on a DW basis (Table 6.8), although most values were substantially lower. Cobalt content of soft tissues of clams increases with increasing shell length (Ji et al., 2006). Accumulation of cobalt and its isotopes from the medium is reported in many species of bivalve molluscs (Ichikawa, 1961; Papadopoulu, 1973; Shimizu et al., 1970, 1971; Van As et al., 1973; Weiss and Shipman, 1957). Among five species of bivalves collected from Greek waters, for example, cobalt concentration factors in tissues were 1000 to 9300 that of ambient seawater (Papadopoulu, 1973). Enhanced cobalt uptake occurs in mussels at lower salinities (Mubiana and Blust, 2006).
Molluscs 187 Table 6.8: Cobalt Concentrations in Field Collections of Molluscs Organism
Concentration
Mussel, Anodonta sp. Shell Soft parts
0.2 DW 0.4 DW
1 1
Gastropod, Aplysia benedicti Ctenidium Gonad Parapodia Hepatopancreas Buccal mass Intestine Gut content Shell
3.0-4.0 DW 5.0-8.0 DW 3.0-4.0 DW 19.0-22.0 DW 10.0-14.0 DW 21.0 DW 22.0 DW 4.0-11.0 DW
2 2 2 2 2 2 2 2
Giant squid, Architeuthis dux; hepatopancreas; 2001-2005; Bay of Biscay vs. Mediterranean Sea
Reference
3.3 DW vs. 4.8 DW
33
Mussel, Bathymodiolus azoricus; 2002; mid-Atlantic Ridge; 3 sites Gill Mantle Digestive gland Byssus threads
0.18-0.91 DW 0.19-0.3 DW 0.5-2.1 DW 0.48-9.6 DW
28 28 28 28
Whelk, Buccinum undatum Shell Soft parts
0.2 DW 0.8 DW
1 1
Cockle, Cerastoderma edule; soft parts
1.3-2.9 DW
3
Scallop, Chlamys opercularis Soft parts Body fluid Mantle Gills Digestive gland Striated muscle Gonad and foot Kidneys Shell
0.33 DW 0.2 DW 0.2 DW 0.45 DW 1.03 DW 0.03 DW 0.2 DW 15.1 DW 0.3 DW
4 4 4 4 4 4 4 4 4
Mussel, Choromytilus meridionalis Soft parts Soft parts
0.037 FW 2.0-3.0 DW
5 6
a
(Continues)
188 Chapter 6 Table 6.8:
Cont’d
Organism
Concentration
Scallop, Comptopallium radula; Santa Marie Bay, New Caledonia; October 2004 Soft parts Kidney
1.8 (1.0-2.8) DW 179.0 DW
Pacific oyster, Crassostrea gigas Soft parts Soft parts
0.1-0.2 FW 1.0 DW
7 6
0.06-0.2 FW
7
Limpet, Crepidula fornicata Shell Soft parts
0.2 DW 17.0 DW
1 1
Clam, Donax serra; soft parts
0.04 FW
5
Clam, Ensis sp.; shell
0.03 DW
8
Abalone, Haliotis midea; soft parts
0.023 FW
5
Limpet, Littorina littorea; soft parts plus operculum
0.8-3.0 DW
11
Clam, Macoma balthica; soft parts
3.7-6.8 DW
11
Hardshell clam, Mercenaria mercenaria Soft parts Soft parts Shell
0.1-0.2 FW 4.3 DW 1.2 DW
7 1 1
Clam, Meretrix lamarcki; soft parts
0.63 DW
9
Clam, Meretrix meretrix; soft parts
0.09-0.52 FW
Mussel, Modiolus modiolus Shell Soft parts Mantle and gills Muscle Gonad Gut and digestive gland
0.3 DW 0.5-5.5 DW 2.9 DW 0.3 DW 0.7 DW 1.1 DW
1 1 1 1 1 1
Softshell clam, Mya arenaria; soft parts
0.1-0.2 FW
7
Mussel, Mytilus corscum; soft parts
0.64 DW
9
Common mussel, Mytilus edulis Shell Soft parts
0.029 DW 1.7 DW
8 8
American oyster, Crassostrea virginica; soft parts
Reference
a
30 30
10
(Continues)
Molluscs 189 Table 6.8: Organism
Cont’d
Concentration
Reference
0.1-2.4 DW 0.2 DW 1.6 DW 0.02-1.1 DW Max. 3.0 DW 2.8 DW
12 1 1 11 25 32
2.0 DW
35
7.2 FW 2.8 DW
13 14
1.2-1.3 DW vs. 1.1-2.1 DW 0.3 DW vs. 1.3 DW 0.06-1.5 DW
26 26 29
Mussel, Mytilus viridis; soft parts
1.0-8.7 DW
15
Whelk, Nucella lapillus Soft parts plus operculum Shell Soft parts
0.2-1.2 DW 0.3 DW 0.3 DW
11 1 1
Squid, Ommastrephes illicebrosa; whole
3.0 AW
16
Oyster, Ostrea edulis; soft parts
0.26-0.54 DW
17
Limpet, Patella candei gomesii; soft parts; 2007; Azores Near hydrothermal vent Reference site
0.9-1.2 DW 0.4-0.7 DW
31 31
Limpet, Patella vulgata Shell Soft parts Soft parts
0.8 DW 0.4 DW 0.2-1.6 DW
1 1 11
Scallop, Pecten maximus Soft parts Body fluid Mantle Gills Digestive gland
0.25 DW 0.07 DW 0.14 DW 0.23 DW 1.28 DW
Soft parts Shell Soft parts Soft parts Soft parts Soft parts; Scheldt estuary; March 2000 Soft parts; Gulf of Gemlik, Turkey; 2004 Mussel, Mytilus galloprovincialis Soft parts Soft parts Soft parts; Adriatic Sea; 2001-2002; summer vs. winter Industrialized sites Reference site Soft parts; summers 2004-2005; Mediterranean Sea; 3 sites
a
4 4 4 4 4 (Continues)
190 Chapter 6 Table 6.8: Organism Striated muscle Gonad and foot Kidneys Soft parts Muscle Gut and digestive gland Mantle and gills Unwashed Washed Gonad Unwashed Washed Shell
Cont’d
Concentration
Reference
0.009 DW 0.1 DW 9.05 DW 8.5 DW 0.3 DW 0.7 DW
4 4 4 1 1 1
0.6 DW 0.4 DW
1 1
2.7 DW 0.2 DW 0.3 DW
1 1 1
Green mussel, Perna viridis; Hong King; juveniles vs. adults Reference site Soft parts Byssus Polluted site Soft parts Byssus
1.9 DW vs. 0.6 DW 0.7 DW vs. 3.9 DW
34 34
1.5 DW vs. 2.8 DW 26.2 DW vs. 7.3 DW
34 34
Pen shell, Pinna nobilis Soft parts Mantle and gills Muscle Nervous system Stomach and intestines Gonads Hepatopancreas
6.8 DW 11.0 DW 10.0 DW 10.0 DW 6.4 DW 6.0 DW 61.0 DW
18 18 18 18 18 18 18
Clam, Pitar morrhuana; soft parts
0.6-6.1 DW
19
Scallop, Placopecten magellanicus; soft parts
0.6 DW
20
Pteropods, 9 spp.; tests
0.064-1.01 DW
21
Manila clam, Ruditapes philippinarum; soft parts; Korea; 2002-2003 Females vs. males Postspawn vs. prespawn
1.06 DW v. 1.05 DW 3.7 DW vs. 1.1 DW
24 24
Clam, Scrobicularia plana Gannel estuary, England Soft parts
19.0-66.0 DW
22
a
(Continues)
Molluscs 191 Table 6.8: Organism Digestive gland Mantle and siphons Foot and gonad Gills and palps Adductor muscle Kidney Camel estuary, England Soft parts Digestive gland Mantle and siphons Foot and gonad Gills and palps Adductor muscle Kidney Transferred from Camel estuary to Gannel estuary for 352 days Digestive gland Remaining tissues Transferred from Gannel estuary to Camel estuary for 352 days Digestive gland Remaining tissues Tamar estuary, England Soft parts Digestive gland Looe estuary, England; soft parts Squid, Sepia esculata; trunk Common cuttlefish, Sepia officinalis Egg shell Embryo Digestive gland Juveniles, age 1 month Immatures, age 12 months Adults, age 18 months
Cont’d
Concentration
Reference
156.0 DW 6.3 DW 1.4 DW 2.3 DW 0.5 DW 1.1 DW
22 22 22 22 22 22
4.3-5.3 DW 15.9 DW 1.2 DW 0.8 DW not detectable 0.3 DW 4.3 DW
22 22 22 22 22 22 22
39.0 DW 1.9 DW
22 22
66.0 DW 2.7 DW
22 22
3.0-37.2 DW 27.0-121.0 DW 2.4-17.7 DW
23 23 11
0.06 DW
9
1.2 DW 0.25 DW
27 27
2.6 DW 6.8 DW 10.0 DW
27 27 27
a
Values are in mg Co/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Segar et al., 1971; 2, Patel et al., 1973; 3, Bryan and Hummerstone, 1973; 4, Bryan, 1973; 5, Van As et al., 1973; 6, Watling and Watling, 1976a; 7, Pringle et al., 1968; 8, Bertine and Goldberg, 1972; 9, Ishii et al., 1978; 10, Bhatt et al., 1968; 11, Bryan and Hummerstone, 1977; 12, Karbe et al., 1977; 13, Uysal, 1978a; 14, Fowler and Oregioni, 1976; 15, Bhosle and Matondkar, 1978; 16, Nicholls et al., 1959; 17, Fukai et al., 1978; 18, Papadopoulu, 1973; 19, Eisler et al., 1978; 20, Reynolds, 1979; 21, Turekian et al., 1973; 22, Bryan and Hummerstone, 1978; 23, Bryan and Uysal, 1978; 24, Ji et al., 2006; 25, Mubiana and Blust, 2006; 26, Scancar et al., 2007; 27, Miramand et al., 2006; 28, Kadar et al., 2006; 29, Lafabrie et al., 2007; 30, Metian et al., 2008; 31, Cunha et al., 2008; 32, Wepener et al., 2008; 33, Bustamante et al., 2008; 34, Nicholson and Szefer, 2003; 35, Unlu et al., 2008.
192 Chapter 6 Radiocobalt-60 was not detectable in mussels and chitons collected in summer 2004 from Amchitka Island in the Aleutian chain, the site of nuclear tests between 1965 and 1971 (Burger et al., 2007b). Laboratory studies with 57Co and clams, G. tumidum, of various shell widths show that soft parts from 3.5 cm shell width clams contained 40-100 times more radiocobalt than seawater after 15 days; concentration factors were higher for clams of 2.5 cm shell width and lowest for those of 5.0 cm shell width (Hedouin et al., 2006). Scallops, C. radula, held in seawater containing 57Co for four days had a BCF of 15 in total soft parts and 603 in kidney (Metian et al., 2008). Gravid cuttlefish, S. officinalis, fed crabs radiolabeled with 60Co over a 2 week period to determine rate of maternal transfer into eggs showed no significant transfer (Lacoue-Labarthe et al., 2008b). Results of laboratory studies in which American oysters were immersed for 20 weeks in 0.05 or 0.1 mg Co/L showed high tissue concentrations of 6.0-11.0 mg Co/kg FW soft parts (Shuster and Pringle, 1968); these values were significantly higher than those recorded in field populations. Cobalt most frequently accumulated in molluscan kidney or digestive gland tissues (Amiard-Triquet and Amiard, 1976; Bryan, 1973; Patel et al., 1973; Pentreath, 1973; Young and Folsom, 1967, 1973). In oceanic squid, Stenoteuthis bartrami, for example, 90 percent of all cobalt in the animal was found in digestive gland, which contributed less than 5 percent of the total body weight (Folsom and Young, 1965). Uptake of cobalt in molluscs is influenced by diet (Amiard-Triquet and Amiard, 1976; Pentreath, 1973), by the physicochemical form of cobalt (Lowman and Ting, 1973; Pentreath, 1973), by season of year (Bryan, 1973; Patel et al., 1973), by ambient sediment lithology in the case of burrowing bivalves (Luoma and Jenne, 1977), and by the number and types of protein binding materials (Shimizu et al., 1971). In general, molluscs accumulate cobalt mainly from the diet, with only minor accumulation from water; soluble forms of cobalt were preferred to particulates; and bivalves living on calcareous substrates accumulated cobalt more readily than those living on substrates of iron oxide, manganese oxide, or detrital organics (Eisler, 1981).
6.13 Copper Molluscs tend to accumulate copper from seawater. For example, bivalve tissues from Greece had 10,000-15,000 times more copper than the ambient medium (Papadopoulu, 1973). In general, molluscs contain more copper in soft tissues than other marine groups examined, including plants, other invertebrate groups, and vertebrates (Eisler, 1979, 1981, 2000b). Among the molluscs, highest accumulations were generally observed in cephalopods and in ostreid and crassostreid oysters; blood, digestive gland, and kidney appeared to contain the highest copper concentrations (Table 6.9). Several species of molluscs other than cephalopods or oysters also had elevated copper burdens; in many cases, the high copper concentrations were associated with proximity to anthropogenic point sources of copper, and secondarily to various biological and abiotic variables that modify copper uptake and retention. Recognition of the importance of these variables and their interactions is essential to an understanding of copper kinetics in marine systems. Selected examples follow.
Molluscs 193 Table 6.9: Copper Concentrations in Field Collections of Molluscs Organism
Concentration
Abalones Muscle Viscera
1.8-3.4 FW 4.2-17.2 FW
1 1
Gastropod, Acmaea digitalis Shell Soft parts
7.5 DW 12.0 DW
2 2
Antarctic scallop, Adamussium colbecki Ross Sea; 1987-1988 vs. 1990 Digestive gland Gills Gonads Kidneys Mantle Muscle
12.6 DW vs. 3.5 FW 6.5 DW vs. 1.4 FW 2.7 DW vs. Not detectable (ND) 4.0 DW vs. ND 3.5 DW vs. ND 1.6 DW vs. ND
106, 107 106, 107 106 106 106 106
0.7-0.8 FW; 6.3 4.5-8.0 DW
108, 109
Blood clam, Anadara granosa; soft parts; Malaysia
Reference
Mussel, Anodonta sp. Shell Soft parts
7.6 DW 3.0 DW
4 4
Gastropod, Aplysia benedicti Ctenidium Gonad Parapodia Hepatopancreas Buccal mass Intestine Gut content Shell
160.0-232.0 DW 18.0-25.0 DW 12.0 DW 7.0-9.0 DW 11.0 DW 23.0 DW 16.0 DW 19.0-20.0 DW
5 5 5 5 5 5 5 5
Giant squid, Architeuthis dux; 2001-2005; hepatopancreas Bay of Biscay Mediterranean Sea
108.0 DW 1218.0 DW
Ocean quahog, Arctica islandica Soft parts March August February June
6.6-11.3 DW 4.5-13.2 DW 4.4-7.5 DW 4.5-9.3 DW
a
185 185
6 6 6 6 (Continues)
194 Chapter 6 Table 6.9: Organism Block Island Sound Chesapeake Bay Georges Bank New York Bight Western Baltic Sea; 1992-1993 Adductor muscle Digestive gland Foot Gills Kidney Mantle Soft parts
Cont’d
Concentration
Reference
10.0 DW 5.4 DW 3.5-10.3 DW 11.3 DW
110 110 110 110
1.8-2.2 DW 13.5 DW 3.1 DW 6.7 DW 40.1 DW 5.0 DW 14.3-15.3 DW
110 110 110 110 110 110 110
Scallop, Argopecten gibbus; kidney concretion
490.0 DW
7
Scallop, Argopecten irradians; kidney concretion
8.9 DW
7
Cockle, Austrovenus stutchburyi; soft parts; 1993-1994; Otago, New Zealand
3.0-60.0 DW
147
52.0-130.0 DW 1.0-81.0 DW 11.0-172.0 DW
176 176 176
22.0 DW 47.0 DW 10.0 DW
169 169 169
5.2 DW 70.0 DW 13.0 DW
169 169 169
18.0 DW 67.0 DW 4.0 DW 0.6-1.7 (0.1-2.7) DW
169 169 169 175
Hydrothermal vent mussel, Bathymodiolus azoricus; mid-Atlantic ridge; 2001 5 sites Gills Mantle Digestive gland Various depths 840 m deep Digestive gland Gills Mantle 1700 m deep Digestive gland Gills Mantle 2300 m deep Digestive gland Gills Mantle Shell Summer 2002; start vs. 30 days in metals-free seawater
a
(Continues)
Molluscs 195 Table 6.9: Organism
Cont’d
Concentration
Reference
37.0 FW vs. 20.0 FW 30.0 FW vs. 15.0 FW 80.0 FW vs. 30.0 FW 500.0 FW vs. 10.0 FW
149 149 149 149
3.1 (1.3-9.1) FW
144
Mussel, Brachydontes pharaonis; Turkey; 2002-2003; max. concentrations Muscle Gill Hepatopancreas
44.0 DW 245.0 DW 62.0 DW
138 138 138
Whelk, Buccinum undatum Shell Soft parts Soft parts; Irish Sea vs. Scotland
9.1 DW 180.0 DW 180.0 DW vs. 78.0 DW
4 4 111
Gill Mantle Digestive gland Byssus threads Bivalves; 5 spp.; soft parts; East China Sea; August 2002
Channeled whelk, Busycon canaliculatum Soft parts Digestive gland Summer months Winter months Blood Summer months Winter months Kidney Foot Osphradium Gill Summer months Winter months Gut Liver Kidney Pancreas Buccal mass Gill Gonad Heart Foot Blood Hemocyanin
76.0 (58.0-116.0) FW
9
400.0-900.0 FW 62.0-120.0 FW
9 9
316.0 FW 19.0 FW 171.0 FW 20.0 FW 40.0 FW
9 9 9 9 9
70.0-80.0 FW 15.0-30.0 FW 248.0 FW 146.0 FW 76.0 FW 76.0 FW 44.0 FW 40.0 FW 21.0 FW 16.0 FW 8.0 FW 35.0-83.0 FW 67.0-137.0 FW
a
9 9 10 10 10 10 10 10 10 10 10 10 10 (Continues)
196 Chapter 6 Table 6.9: Organism
Cont’d
Concentration
Reference
0.0023 mg per capsule FW 11.9-21.0 FW
11 12
32.4 FW 1080.0-1135.0 FW
12 12
Cockle, Cardium edule Soft parts Shell Soft parts
5.0 FW 3.0 DW 11.0 DW
13 4 4
Cockle, Cerastoderma edule Soft parts Soft parts
4.0-9.0 DW 9.8 (5.2-27.2) DW
14 15
Scallop, Chlamys opercularis Soft parts Body fluid Mantle Gills Digestive gland Striated muscle Unstriated muscle Gonad and foot Kidney Shell
15.4 DW 5.6 DW 5.6 DW 16.7 DW 36.7 DW 1.3 DW 3.1 DW 9.7 DW 1285.0 DW 0.38-0.7 DW
16 16 16 16 16 16 16 16 16 4
7.0-14.0 DW
17
Eggs Muscle Digestive gland Virginia Long Island Sound, New York
Mussel, Choromytilus meridionalis; soft parts Scallop, Comptopallium radula; New Caledonia; October 2004 Soft parts Digestive gland
3.7 (2.9-5.1) DW 15.0 DW
Oyster, Crassostrea angulata; soft parts; Spain Sanlucar Sancti-Petri Barbate Rio Piedras Ayamonte
264.7 FW 28.0 FW 35.0 FW 200.3 FW 120.1 FW
18 18 18 18 18
Oyster, Crassostrea commercialis Soft parts Soft parts
18.7 FW 3.0-48.0 FW
19 20
a
171 171
(Continues)
Molluscs 197 Table 6.9:
Cont’d
Organism
Concentration
Reference
Oyster, Crassostrea cucullata Soft parts Soft parts
251.0-480.0 DW 20.6 FW
21 22
9.4-192.2 FW 200.0-853.0 DW 513.0-1655.0 DW 6.6-37.9 FW 19.0-482.0 FW 47.0-900.0 DW 18.0-61.0 DW 110.0-643.0 DW Up to 6480.0 DW in power station cooling water 19.0 (1.0-55.0) FW 33.0 DW 32.0 DW 1.6-2.9 DW
19 14 14 23 24 24 24 25 26 27 17 28 111
340.0-6480.0 DW 33.0 DW 9.4-84.4 DW 7.8-38.0 FW 389.0-1411.0 DW
111 111 111 111 139
840.0 DW 509.0 DW 750.0 DW 344.0-422.0 DW; max. 1071.0 DW 383.0 DW
112 112 112 112
48.3-63.8 DW 67.7-116.2 DW 101.8-135.0 DW
113 113 113
4401.0 DW; green in color
114
909.0 (113.0-2805.0) DW 2225.0 DW
116 115
Pacific oyster, Crassostrea gigas Soft parts Soft parts Gill Soft parts Soft parts Mantle Digestive diverticula Soft parts Soft parts Soft parts Soft parts Soft parts Shell Soft parts England South Africa Tasmania United States China; November 2003; impacted by industrial effluents; 3 sites Hong Kong; 1989; various locations Gill Mantle Muscle Soft parts Visceral mass Arcachon Bay, France; soft parts 1979-1982 1983-1987 1988-1991 Taiwan; soft parts 1989; from discharge of copper recycling facility containing 0.0050.024 mg Cu/L 1995-1996 From Cu-contaminated environment
a
112
(Continues)
198 Chapter 6 Table 6.9: Organism As above; after 6 days in clean seawater As above; after 32 days in clean seawater Oyster, Crassostrea gryphoides; soft parts American oyster, Crassostrea virginica Soft parts Alabama Atlantic Ocean; northwestern areas Chesapeake Bay East coast, United States East coast, United States Georgia Savannah, Georgia; 2000-2001; 9 sites Gulf coast, United States Gulf coast, United States Pensacola, Florida; 2003-2004 West coast, United States Maryland North Carolina; Newport River estuary Rhode Island Texas Virginia, Rappahannock River estuary Virginia; 1972-1973; various salinities 7.5 ppt 9.5 ppt 12 ppt 13.5 ppt Purdy, Washington State, United States March-June 1965 July-December 1965 December-June 1966 July-October 1966 October-March 1967 May-July 1967
Cont’d
Concentration
Reference
746.0 DW
115
344.0 DW
115
175.0-210.0 DW
a
21
20.0 (4.0-78.0) FW 46.0 (11.0-100.0) DW
111 111
5.0-240.0 FW 91.5 (7.0-517.0) FW 21.0-220.0 DW 48.0-261.0 DW 67.0-121.0 DW
111 29 39 111 170, 177
23.0-410.0 DW 16.0 (6.0-27.0) FW Max. 56.0 FW 7.8-37.5 FW Max. 1120.0 DW 2.2-6.2 FW
39 111 165 29 111 36
121.0 (92.0-140.0) FW 161.0 DW 3.0-29.0 FW
111 111 36
29.0 FW 16.0 FW 12.0 FW 3.0 FW
36 36 36 36
20.2 FW 20.3 FW 14.2 FW 19.2 FW 12.5 FW 14.3 FW
29 29 29 29 29 29 (Continues)
Molluscs 199 Table 6.9: Organism Manchester, Washington State March-June 1965 July-December 1965 December-June 1966 July-October 1966 October-March 1967 May-July 1967 Shell Soft parts Mantle Soft parts Florida; soft parts From a canal lined with chromated-copper-arsenate wood vs. reference site
Reference site oysters transplanted into above canal After 3 months After 4 months
North Carolina; soft parts Marina sites Open water sites At 12 ppt salinity At 33 ppt salinity Soft parts Soft parts Soft parts Summer Autumn Shell Soft parts; metals-contaminated site vs. reference site Soft parts Soft parts Oyster, Crassostrea rhizophorae; soft parts; near Natal Brazil; summer 2001; contaminated estuary vs. reference site
Cont’d
Concentration
Reference
24.0 FW 22.4 FW 20.6 FW 25.8 FW 17.4 FW 18.3 FW 42.7-69.8 FW 290.0-913.0 DW 968.0 DW Max. 200.0 FW
29 29 29 29 29 29 30 24 24 31
150.0-200.0 FW vs. 10.0 FW; elevated concentrations associated with greenish color and higher frequency of histopathology of digestive gland diverticula
118
130.0 FW 220.0 FW; no increase in frequency of digestive gland lesions
118 118
36.7 FW 7.1 FW 6.0 FW 2.0 FW 55.0-261.0 DW Mean 180.0 FW; Max. 584.0 FW
119 119 36 36 32 33
a
250.0 DW 50.0 DW 0.2 DW 450.0 DW vs. 6.0 DW
34 34 34 35
1.0-702.0 FW 161.0 DW
27, 37, 38 40
18.0-39.0 DW vs. 16.9-28.2 DW
161
(Continues)
200 Chapter 6 Table 6.9:
Cont’d
Organism
Concentration
Limpet, Crepidula fornicata Shell Soft parts
1.8 DW 270.0 DW
Octopus, Eledone cirrhosa; English Channel; October, 1987 Branchial hearts Digestive gland Genital tract Gill Kidney Mantle Muscle Whole
335.0 DW 448.0-463.0 DW 60.0-66.0 DW 268.0 DW 594.0 DW 102.0 DW 17.0 DW 122.0 DW
120 120 120 120 120 120 120 120
1.2-1.7 (0.51-2.99) FW
140
Mussel, Elliptio buckleyi; soft parts; Marmara Sea, Turkey; 2004-2005
Reference 4 4
Red abalone, Haliotis rufescens Gills Mantle Digestive gland Foot
18.0-123.0 DW 8.0-20.0 DW 11.0-78.0 DW 1.4-12.8 DW
41 41 41 41
Abalone, Haliotis sp.; soft parts
8.0 FW
13
28.0 DW 68.0 DW 15.4 DW 20.7 DW
42 42 42 42
39.0 DW 77.0 DW 22.4 DW 17.6 DW
42 42 42 42
560.0 DW 12.1 DW 103.0 DW 374.0 DW 24.2 DW
42 42 42 42 42
Abalone, Haliotis tuberculata; United Kingdom locations Cobo Bay Soft parts Viscera Foot Digestive gland Fermain Bay Soft parts Viscera Foot Digestive gland All stations Blood Muscle Gills Left kidney Right kidney
a
(Continues)
Molluscs 201 Table 6.9:
Cont’d
Organism
Concentration
Reference
Scallop, Hinnites multirugosus; power plant outfall vs. reference site Digestive gland Gonad Adductor muscle
190.0 FW vs. 64.0 FW 3.2 FW vs. 2.2 FW 0.4 FW vs. 0.2 FW
43 43 43
Mud snail, Ilyanassa obsoleta; soft parts; North Carolina Marina sites Open water sites
402.2 FW 219.5 FW
119 119
Periwinkle, Littoraria scabra; soft parts; Tanzania Industrialized sites; 1998 vs. 2005 Reference sites; 2005
9.0 DW vs. 62.0 DW 8.0 DW
173 173
Limpet, Littorina littorea Soft parts Whole Soft parts plus operculum Soft parts Digestive gland and gonad Shell
6.2-20.0 FW 23.8-36.1 FW 124.0 (62.0-194.0) DW 42.7-248.8 DW 91.4-92.5 DW 2.1-3.5 DW
44 45 15 46 46 46
Squid, Loligo opalescens; liver; California Central coast Southern coast
5350.0 DW 8370.0 DW
47 47
Baltic clam, Macoma balthica Shell; Sweden West coast Baltic coast Soft parts Soft parts Soft parts; 1996-1997; Gulf of Gdansk; age 3-4 years Soft parts; the Netherlands; 1990-1992; acid-soluble fraction vs. total copper Hardshell clam, Mercenaria mercenaria Soft parts April 3+ age group 4+ age group 5+ age group
41.0 FW 117.0 FW 300.0 (96.0-615.0) DW 5.0-12.0 FW 25.0-150.0 DW
48 48 15 49 164
4.1 (2.7-6.7) DW vs. 13.8-22.6 DW
121
42.0 DW 40.0 DW 35.0 DW
a
50 50 50 (Continues)
202 Chapter 6 Table 6.9: Organism
Cont’d
Concentration
Reference
23.0 DW 28.0 DW 27.0 DW 1.7 DW 25.0 DW 2.6 FW 1.0-16.5 FW 1.1-7.9 FW
50 50 50 4 4 29 37 51
Clam, Meretrix casta; soft parts
16.1 DW
21
Clam, Meretrix lamarckii; soft parts
15.0 DW
52
Mexico; Sinaloa; 2004-2005; soft parts; rainy season vs. dry season Oyster, Crassostrea corteziensis Mussel, Mytella strigata Clam, Megapitaria squalida
73.2 DW vs. 70.3 DW 27.8 DW vs. 20.5 DW 11.1 DW vs. 6.3 DW
Mussel, Modiolus modiolus Shell Soft parts Mantle and gills Muscle Gonads Gut
1.9 DW 10.0-44.0 DW 42.0 DW 14.0 DW 19.0 DW 45.0 DW
August 3+ age group 4+ age group December; 5+ age group Shell Soft parts Soft parts Soft parts Soft parts
Molluscs Soft parts West Norway coast Rio Tinto estuary, Spain 5 spp; Chile, Strait of Magellan; 2001; 17 stations 3 spp.; India; 2003 Shell Soft parts Soft parts, 12 spp. Edible tissues; commercial species; 18 spp. 3 spp. 5 spp. 3 spp. 4 spp. 3 spp.
178 178 178 4 4 4 4 4 4
Max. 190.0 DW Max. 26.0 DW 0.7-7.5 FW
53 54 163
4.4-6.5 FW 1.6-7.9 DW 37.0-102.0 DW 1.0-40.0 FW
168 55 55 57
0.1-0.4 FW 0.6-0.8 FW 1.0-3.0 FW 3.0-8.0 FW 10.0-40.0 FW
a
56 56 56 56 56 (Continues)
Molluscs 203 Table 6.9:
Cont’d
Organism
Concentration
Reference
Morocco; 2001; clams; soft parts Scrobicularia plana Cerastoderma edule
50.0 DW 10.0 DW
180 180
Morocco; 2004-2005; soft parts Mussel, Mytilus galloprovincialis Clam, Venerupis decussatus Pacific oyster, Crassostrea gigas
26.8 (4.4-142.2) DW 11.1 (6.2-18.3) DW 25.9 (3.6-42.1) DW
172 172 172
1.2 FW
117
Mussels; various species; soft parts; Wales; 1989; coastal area Softshell clam, Mya arenaria Soft parts Soft parts Lagoon mussel, Mytella strigiata; soft parts; Baja California; Mexico; 1989-1991
5.8 (1.2-90.0) FW 9.8-14.6 DW
a
29, 37 58
Max. 3.9 DW
122
Mussel, Mytilus californianus Shell Soft parts Digestive gland Soft parts
8.1-18.6 DW 9.0-30.3 DW 14.0-69.0 DW 4.6-11.0 DW
2 2 59 39
Common mussel, Mytilus edulis Soft parts Whole Gill Foot Mantle Kidney Digestive gland Muscle Soft parts Shell Soft parts Shell Shell; Baltic Sea; 2005; 12 sites Soft parts Whole Soft parts Soft parts
3.7-65.4 DW 8.3-11.5 DW 6.9-10.8 DW 4.2-7.2 DW 5.4-5.8 DW 7.4-8.7 DW 6.8-7.0 DW 2.7-3.7 DW 5.0 FW 2.0 DW 9.6 DW Max. 8.6 DW 2.2-4.2 DW 5.0-11.2 DW 1.9-2.3 FW 3.1 FW 0.6-0.9 FW
14 60 60 60 60 60 60 60 13 4 4 2 182 2 45 61 62 (Continues)
204 Chapter 6 Table 6.9: Organism Soft parts Soft parts Soft parts Digestive gland Gonad Muscle Hepatopancreas San Diego Harbor Offshore Protein fractions Soft parts Soft parts Shell Shell California England Japan New Zealand Soft parts United States West coast sites United States East coast sites Looe estuary, England California Canada; Halifax England Long Island Sound, New York 1983 1986-1987 Norway Portugal and Spain Mussel, Mytilus edulis aoteanus Soft parts Mantle Gills Muscle Visceral mass Intestine Foot Gonads Shell
Cont’d
Concentration
Reference
Max. 1.4 FW 0.5-5.0 FW 9.0-17.0 DW Max. 77.0 FW Max. 23.0 FW Max. 53.0 FW
63 44 64 65 65 65
39.0-73.0 DW 17.0-22.0 DW 0.1-0.2 FW Max. 28.0 DW 5.0-88.0 DW 4.0-8.0 DW
66 66 67 141 68 68
Max. 8.6 DW 9.6 DW 1.2-2.8 DW 3.0 DW
111 111 111 111
3.5-8.6 DW 6.7-13.2 DW 9.5 (3.9-13.6) DW 5.0-11.2 DW 13.7-154.3 DW 7.0-11.0 DW
39 39 15 111 123 111
1.0-2.3 FW 15.0 DW 3.0-130.0 DW 6.5-14.0 DW
124 125 111 111
9.0 (5.0-11.0) DW 11.0 DW 20.0 DW 1.0 DW 19.0 DW 15.0 DW 13.0 DW 6.0 DW 3.0 DW
a
69 69 69 69 69 69 69 69 69 (Continues)
Molluscs 205 Table 6.9: Organism Mussel, Mytilus edulis planulatus Soft parts Dry weight 0.09 g Dry weight 0.39 g Dry weight 0.48 g Dry weight 0.69 g Soft parts June January Mussel, Mytilus galloprovincialis Protein extracts; Bulgarian Black Sea coast; polluted vs. reference site Soft parts; purged for 48 h in synthetic seawater vs. not purged Soft parts Soft parts Soft parts; May 2003; NW Mediterranean Sea Near Genova, Italy Near Marseille, France Near Barcelona, Spain Soft parts; 1991-2005; western Mediterranean Sea; Balearic Islands; Port of Mahon Soft parts; Marmara Sea, Turkey; 2005 Soft parts; Izmir Bay, Turkey; 2004; near shore vs. mid-bay Soft parts; Gulf of Gemlik, Turkey; 2004 Soft parts; Adriatic Sea; 2001-2002; summer vs. winter Industrialized sites Reference site Soft parts; Adriatic Sea, Italy; 2 sites Soft parts; Adriatic Sea; 2001-2005; winter vs. summer Soft parts; Sardinia; 2004 vs. 2006
Cont’d
Concentration
Reference
7.5 DW 6.9 DW 6.2 DW 6.0 DW
3 3 3 3
19.6 FW 0.8 FW
70 70
23.2 DW vs. 12.9 DW
150
6.9 DW vs. 13.1 DW
126
18.0 DW 7.3 FW
a
71 72
5.7-40.0 DW 5.5-8.5 DW 5.7-74.8 DW 21.2 (5.9-58.3) DW
134 134 134 135
1.2 FW
137
5.3 DW vs. 3.7 DW
183
5.5 DW
189
6.5-11.7 DW vs. 8.3-49.0 DW 7.6 DW vs. 9.7 DW 0.74-0.82 FW
148 148 181
5.1-8.9 DW vs. 1.1-4.5 DW
186
17.0 DW vs. 14.0 DW
184 (Continues)
206 Chapter 6 Table 6.9: Organism
Cont’d
Concentration
Reference
1.5 (0.95-1.8) FW
142
1.4 FW 1.3 FW 0.0 FW 1.1 FW
vs. vs. vs. vs.
1.5 FW 2.2 FW 2.2 FW 2.2 FW
136 136 136 136
9.3 DW 3.6 DW 4.7 DW 9.0 DW
vs. vs. vs. vs.
10.8 DW 4.4 DW 6.3 DW 8.7 DW
166 166 166 166
20.2 DW vs. 1.8 DW
115
Mussels, Mytilus spp.; soft parts; United States; 1970s vs. 1980s Bodega Bay, California Narragansett Bay, Rhode Island
6.9 DW vs. 7.7 DW 11.0 DW vs. 14.0 DW
127 127
Mussel, Mytilus viridis Soft parts Soft parts Soft parts
2.3 FW 3.0-16.0 DW 8.6-26.0 DW
73 74 21
17.0 DW
52
70.0 DW 170.0 DW
75 75
0.29 DW 150.0 DW 110.0 (51.0-141.0) DW
4 4 15
Soft parts; Aegean Sea, Turkey; 2002-2003 Mantle vs. gills; 2004-2006; Saronikos Gulf of Greece; max. mean concentrations; contaminated sites Summer Autumn Winter Spring Soft parts; Venice lagoon, Italy; 2005-2006; San Giuliano vs. Sacca Sessola April July October February Mussel, Mytilus smarangdium; soft parts; copper-contaminated environment vs. 6 days in clean seawater
Abalone, Notohaliotis discus; soft parts less viscera Whelk, Nucella lapillus Soft parts Reference site After transfer for 5 months to Cu-contaminated area Shell Soft parts Soft parts plus operculum
a
(Continues)
Molluscs 207 Table 6.9:
Cont’d
Organism
Concentration
Reference
Octopus, Octopus sp. Viscera Whole Whole
300.0 FW 7.0 FW 39.0 FW
1 61 76
Octopus, Octopus cyanea; Guam; June 1998 Tentacle Liver
12.1 DW 5680.0 DW
132 132
2550.0 DW 4880.0 DW 93.0 DW 111.0 DW 43.0 DW 48.0 DW 28.0 DW 2450.0 DW
77 78 77 77 77 77 77 77
Octopus, Octopus vulgaris Hepatopancreas Hepatopancreas Branchial heart Gill Central heart Kidney Muscle Hemolymph Portugal; 2005-2006; digestive gland; northwest region vs. south coast Whole Nuclei Mitochondria Lysosomes Microsomes Portugal; 1999-2002; 3 sites Digestive gland Branchial heart Gill Muscle
860.0 (64.0-1490.0) DW vs. 1390.0 (1120.0-1600.0) DW 1100.0 (90.0-1210.0) DW vs. 1160.0 (310.0-1670.0) DW 740.0 (520.0-3260.0) DW vs. 890.0 (410.0-1280.0) DW 620.0 (220.0-13,020.0) DW vs. 910.0 (440.0-2000.0) DW 950.0 (600.0-2890.0) DW vs. 1310.0 (720.0-1,570.0) DW
179
1411.0-2515.0 DW 155.0-221.0 DW 100.0-151.0 DW 26.0-36.0 DW
187 187 187 187
a
179 179 179 179
Squid, Ommastrephes bartrami; liver
195.0 DW
47
Squid, Ommastrephes illicebrosa; whole
2700.0 AW
79
Oyster, Ostrea angasi Whole Soft parts
39.0-104.0 DW 4.0-80.5 FW
3 19 (Continues)
208 Chapter 6 Table 6.9: Organism Soft parts Soft parts June January Oyster, Ostrea circumpicta; soft parts; Japan; Nobeoka Bay South coast North coast European flat oyster, Ostrea edulis Soft parts; Balearic Islands; western Mediterranean Sea; 1991-2005; Port of Mahon Soft parts Gill Soft parts Soft parts Soft parts Wales, United Kingdom vs. Cornwall, England Gills Mantle Kidney Viscera Muscle Hemolymph Whole Cell-free Oyster, Ostrea equestris; soft parts; United States East coast Gulf coast Oyster, Ostrea gigas Soft parts; Japan; Nobeoka Bay South coast North coast Soft parts Reference site; seawater Cu levels 0.0005-0.0023 mg/L
Cont’d
Concentration
Reference
57.9 FW
61
20.6 FW 7.5 FW
70 70
356.0-686.8 FW 93.0 FW
80 80
451.7 (0.8-1444.0) DW
a
135
86.0-597.0 DW 380.0-1420.0 DW 6.0 FW 38.0 DW 245.0-405.0 DW
14 14 13 28 82
253.0 FW vs. 2395.0 FW 207.0 FW vs. 2175.0 FW 124.0 FW vs. 500.0 FW 77.0 FW vs. 1184.0 FW 64.0 FW vs. 315.0 FW
81 81 81 81 81
2.0 FW vs. 21.0 FW 0.6 FW vs. 8.0 FW
81 81
660.0 DW 21.0-220.0 DW
39 39
320.2-434.6 FW 60.9-86.9 FW
80 80
25.0 FW
83 (Continues)
Molluscs 209 Table 6.9: Organism
Cont’d
Concentration
Reference
65.0 FW 205.0 FW 255.0 FW 1237.0 FW
84 84 84 84
5.0 FW 14.0 FW 15.0 FW 18.0 FW
85 85 85 85
Oyster, Ostrea sinuata Soft parts Mantle Gills Muscle Striated muscle Visceral mass Kidney Heart Shell
41.0 (21.0-53.0) DW 34.0 DW 100.0 DW 23.0 DW 6.0 DW 49.0 DW 22.0 DW 59.0 DW <1.0 DW
69 69 69 69 69 69 69 69 69
Oyster, Ostrea spinosa; soft parts
40.0 FW
80
Oysters Soft parts Soft parts; from area of metal pollution vs. reference site
Max. 123.0 FW Max. 450.0 FW vs. Max. 100.0 FW
86 86
Transplanted for 120 days to seawater Cu levels of 0.001-0.0064 mg/L Muscle Mantle Gill Labial palps Transplants after depletion for 116 days in control waters Muscle Mantle Gill Labial palps
Clam, Paphia undulata; soft parts; Malaysia; 1993
0.9-1.1 FW
Limpet, Patella caerulea: soft parts
2.7-9.7 FW; 11.3-38.0 DW
Limpet, Patella candei gomesii; soft parts; 2007; Azores Near hydrothermal vent Reference site
6.4-7.2 DW 5.2-5.7 DW
174 174
2.1 (0.6-5.0) DW
143
Gastropod, Patella piperata; Canary Islands, Spain; soft parts; March-April 2003
a
108 8
(Continues)
210 Chapter 6 Table 6.9:
Cont’d
Organism
Concentration
Reference
Limpet, Patella sp.; soft parts Reference site Transplants to high copper areas for 8 months
7.0 DW 30.0 DW
75 75
2.7 FW 8.1 FW
87 87
Limpet, Patella vulgata Bristol Channel, United Kingdom Foot Viscera Soft parts Near desalination plant outfall; May vs. August Reference site; May vs. August Soft parts Shell Soft parts Soft parts Shell Soft parts
25.4 vs. 282.0 DW
88
8.7 DW vs. 6.6 DW 14.4 DW 42.0 DW 7.7 DW 12.0-30.0 DW 1.0-6.0 DW 19.0 (10.0-27.0) DW
88 89 4 4 68 68 15
Scallop, Pecten jacobeus, Adriatic Sea; June 1988 Digestive gland Gills Gonad Kidney Mantle Muscle
16.6 DW 6.3 DW 10.3 DW 17.5 DW 3.3 DW 1.1 DW
Scallop, Pecten maximus Soft parts Shell Soft parts Muscle Gut Mantle and gills Gonad Soft parts Body fluid mantle Gills Digestive gland Striated muscle
0.4-0.9 FW 1.1 DW 3.3 DW 1.2 DW 25.0 DW 2.8 DW 14.0 DW 8.9 DW 2.5 DW 2.7 DW 6.7 DW 57.9 DW 0.8 DW
a
106 106 106 106 106 106 44 4 4 4 4 4 4 16 16 16 16 16 16 (Continues)
Molluscs 211 Table 6.9: Organism Unstriated muscle Gonad and foot Kidney Kidney Scallop, Pecten novae-zelandiae Soft parts Mantle Gills Muscle Visceral mass Intestine Kidney Gonad Shell Soft parts Stomach Gonad Adductor muscle Green mussel, Perna viridis Hong Kong; soft parts; March 1986 India; January 2002; soft parts; 28 sites Small Medium Large Hong Kong; juveniles vs. adults Reference site Soft parts Byssus Shell Polluted site Soft parts Byssus Shell
Cont’d
Concentration
Reference
1.6 DW 17.4 DW 20.8 DW 21.0 FW
16 16 16 90
9.0 (2.0-14.0) DW 15.0 DW 36.0 DW 1.0 DW 24.0 DW 131.0 DW 78.0 DW 9.0 DW 2.0 DW 1.5 FW 10.0 FW 2.1 FW 6.6 FW
69 69 69 69 69 69 69 69 69 57 57 57 57
Max. 35.1 DW
128
0.6 FW 0.6 FW 0.23 FW
162 162 162
10.1 DW vs. 14.9 DW 40.4 DW vs. 35.4 DW 11.8 DW vs. 12.3 DW
188 188 188
17.5 DW vs. 16.4 DW 60.2 DW vs. 96.3 DW 13.5 DW vs. 12.8 DW
188 188 188
Pearl oyster, Pinctada fucata Mantle Foot
2.3 DW 3.7 DW
190 190
Pen shell, Pinna nobilis Soft parts Mantle and gills
860.0 AW 700.0 AW
a
91 91 (Continues)
212 Chapter 6 Table 6.9: Organism Muscle Nervous system Stomach and intestines Gonads Hepatopancreas Byssus Byssus gland Clam, Pitar morrhuana; soft parts Scallop, Placopecten magellanicus Soft parts Muscle March August February June Viscera March August February June Muscle Gonad Visceral mass
Cont’d
Concentration
Reference
680.0 AW 370.0 AW 610.0 AW 460.0 AW 800.0 AW 960.0 AW 700.0 AW
91 91 91 91 91 91 91
2.3-29.6 DW
92
7.3 DW
6
0.9-14.8 DW 0.8-4.4 DW 1.1-6.6 DW 0.9-2.6 DW
6 6 6 6
7.0-14.3 DW 8.0-20.1 DW 7.9-15.8 DW 7.2-9.6 DW 0.27-1.1 FW 1.1-10.6 FW 1.3-5.6 FW
6 6 6 6 93 93 93
Clam, Protothaca staminea Shell Soft parts
11.5 DW 7.5 DW
Pteropods; shells
Max. 20.0 DW
94
Clam, Rangia cuneata Soft parts Soft parts Whole
0.7-1.4 FW 25.0 DW 4.0 FW
95 40 96
Manila clam, Ruditapes philippinarum Soft parts; Korea; 2002-2003 Females vs. males Postspawn vs. prespawn Jiaozhou Bay, China; sediments vs. soft parts; November 2004 Bohai Sea; soft parts
a
2 2
8.6 DW vs. 8.1 DW 8.9 DW vs. 8.4 DW 25.8 DW vs. 6.4-19.8 DW
133 133 145
1.3-4.4 DW
146 (Continues)
Molluscs 213 Table 6.9:
Cont’d
Organism
Concentration
Reference
Tropical rock oyster, Saccostrea cucullata; soft parts Australia; 1983-1984; near sewage discharge vs. reference site Hong Kong; March 1986
285.0 DW vs. 34.0 DW
129
Max. 556.0 DW
128
Sydney rock oyster, Saccostrea commercialis; soft parts; Georges River, Australia; 1970s vs. 1980s
20.0-46.0 FW vs. 14.0-93.0 FW
130
Oyster, Saccostrea glomerata; soft parts
315.0-1146.0 DW
97
25.0-86.0 DW 92.0 DW 29.0 DW 48.0 DW 36.0 DW 5.3 DW 37.0 DW
98 98 98 98 98 98 98
25.0-77.0 DW 51.0 DW 30.0 DW 19.0 DW 45.0 DW 8.3 DW 28.0 DW
98 98 98 98 98 98 98
170.0 DW 27.0 DW
98 98
35.0 DW 16.0 DW
98 98
13.0-52.0 DW 26.0-102.0 DW
99 99
16.0-365.0 DW
15
35.0 DW
52
Clam, Scrobicularia plana Gannel estuary, England Soft parts Digestive gland Mantle and siphons Foot and gonads Gills and palps Adductor muscle Kidney Camel estuary, England Soft parts Digestive gland Mantle and siphons Foot and gonads Gills and palps Adductor muscle Kidney Transplants from Camel estuary to Gannel estuary for 352 days Digestive gland Remaining tissues Transplants from Gannel estuary to Camel estuary for 352 days Digestive gland Remaining tissues Tamar estuary, England Soft parts Digestive gland Looe estuary, England Soft parts Squid, Sepia esculenta; trunk
a
(Continues)
214 Chapter 6 Table 6.9: Organism Common cuttlefish, Sepia officinalis Embryos Mantle Dorsal shield Beak Gills Liver Ink Blood Not dialyzed Dialyzed Liver Not dialyzed Dialyzed Gut Not dialyzed Dialyzed Branchial gland Not dialyzed Dialyzed Arterial heart Not dialyzed Dialyzed Ovary Not dialyzed Dialyzed Blood Hepatopancreas Branchial gland Branchial heart Branchial heart appendage Heart ventricle Pancreatic appendages English Channel; October 1987 Branchial hearts Digestive gland Genital tract Gill Kidney Mantle Muscle Whole Egg Eggshell
Cont’d
Concentration
Reference
0.0038 mg/embryo FW 1.5 FW 16.2 FW 2.9 FW 49.9 FW 1025.0 FW 4.6 FW
100 18 18 18 18 18 18
175.0 DW 73.0 DW
102 102
165.0 DW 73.0 DW
102 102
42.0 DW 33.0 DW
102 102
70.0 DW 63.0 DW
102 102
30.0 DW 22.0 DW
102 102
21.0 DW 18.0 DW 157.0 DW 100.0 FW 22.0 FW 20.0 FW 28.0 FW 23.0 FW 20.0 FW
102 102 103 103 103 103 103 103 103
256.0 DW 313.0-317.0 DW 55.0-56.0 DW 183.0 DW 185.0 DW 141.0 DW 9.0 DW 59.0 DW
131 131 131 131 131 131 131 131
14.0 DW
160
a
(Continues)
Molluscs 215 Table 6.9: Organism Embryo Yolk Hatchlings Whole Cuttlebone Juveniles, age 1 month Whole Digestive gland Cuttlebone Immatures, age 12 months Whole Digestive gland Cuttlebone Adults, age 18 months Whole Digestive gland Cuttlebone
Cont’d
Concentration
Reference
31.0 DW 19.0 DW
160 160
60.0 DW 38.0 DW
160 160
73.0 DW 450.0 DW 12.0 DW
160 160 160
104.0 DW 760.0 DW 8.0 DW
160 160 160
70.0 DW 600.0 DW 5.0 DW
160 160 160
Squid, Sepia sp.; whole
23.0 FW
Clam, Spisula sp.; whole
0.7-1.1 FW
104
Clam, Spisula solidissima; muscle
0.9-1.1 FW
12
Squid Flesh Flesh with skin Viscera Pen
15.0 DW 65.7 DW 162.0 DW 65.0 DW
105 105 105 105
5.3-39.0 FW; 11.0-40.0 DW 0.3-39.0 FW 0.5-0.7 FW; 1.8-3.1 DW 240.0-480.0 FW; 1500.0-2000.0 DW
101 101 101 101
Gastropod, Strombus gigas Shell Foot Muscle Viscera
a
76
Squid, Symplectoteuthis oualaniensis; liver
1720.0 DW
47
Clam, Tapes decussatus; soft parts
2.0-7.1 FW
18
Clam, Tapes semidecussata Shell Soft parts
19.2 DW 19.2 DW
2 2
Gastropod, Thais emarginata Shell Soft parts
5.9-8.2 DW 571.0 DW
2 2 (Continues)
216 Chapter 6 Table 6.9:
Cont’d
Organism
Concentration
Reference
Gastropod, Thais lapillus Soft parts Digestive gland and gonad Shell
167.6-458.1 DW 506.7-554.0 DW 2.6-3.6 DW
46 46 46
Clam, Trivela mactroidea; Venezuela; 2002; 14 sites; soft parts
11.0-49.0 DW
167
Clam, Venus mercenaria; whole
0.91-19.2 FW
104
a
Values are in mg Cu/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Won, 1973; 2, Graham, 1972; 3, Harris et al., 1979; 4, Segar et al., 1971; 5, Patel et al., 1973; 6, Reynolds, 1979; 7, Carmichael et al., 1979; 8, Shiber and Shatila, 1978; 9, Betzer and Pilson, 1974; 10, Townsley, 1954; 11, Betzer, 1972; 12, Greig et al., 1977; 13, George and Coombs, 1975; 14, Boyden, 1974; 15, Bryan and Hummerstone, 1977; 16, Bryan, 1973; 17, Watling and Watling, 1976b; 18, Establier, 1977; 19, Ratkowsky et al., 1974; 20, Mackay et al., 1975; 21, Zingde et al., 1976; 22, D’Silva and Quasim, 1979; 23, Jeng and Huang, 1973; 24, Ruddell and Rains, 1975; 25, Thornton et al., 1975; 26, Boyden and Romeril, 1974; 27, Kopfler and Mayer, 1967; 28, Watling and Watling, 1976a; 29, Pringle et al., 1968; 30, Ferrell et al., 1973; 31, Huggett et al., 1973; 32, Windom and Smith, 1972; 33, Drifmeyer, 1974; 34, Frazier, 1975; 35, Frazier, 1976; 36, Huggett et al., 1975; 37, Shuster and Pringle, 1968; 38, Greig and Wenzloff, 1978; 39, Goldberg et al., 1978; 40, Sims and Presley, 1976; 41, Anderlini, 1974; 42, Bryan et al., 1977; 43, Young and Jan, 1976; 44, Topping, 1973; 45, Wharfe and Van Den Broek, 1977; 46, Ireland and Wooton, 1977; 47, Martin and Flegal, 1975; 48, Sturesson and Reyment, 1971; 49, Miettinen and Verta, 1978; 50, Larsen, 1979; 52, Ishii et al., 1978; 53, Stenner and Nickless, 1974b; 54, Stenner and Nickless, 1975; 55, Culkin and Riley, 1958; 56, Hall et al., 1978; 57, Nielsen and Nathan, 1975; 58, Eisler, 1977b; 59, Alexander and Young, 1976; 60, Delhaye and Cornet, 1975; 61, Eustace, 1974; 62, Phillips, 1976a; 63, Phillips, 1976b; 64, Simpson, 1979; 65, Young and McDermott, 1975; 66, Young et al., 1979; 67, Talbot and Magee, 1978; 68, Lande, 1977; 69, Brooks and Rumsby, 1965; 70, Thomson, 1979; 71, Fowler and Oregioni, 1976; 72, Uysal, 1978a; 73, D’Silva and Kureishy, 1978; 74; Bhosle and Matondkar, 1978; 75, Stenner and Nickless, 1974a; 76, Matsumoto et al., 1964; 77, Ghiretti-Magaldi et al., 1958; 78, Rocca, 1969; 79, Nicholls et al., 1959; 80, Ikuta, 1967; 81, George et al., 1978; 82, Fukai et al., 1978; 83, Ikuta et al., 1968a; 84, Ikuta et al,. 1968b; 85, Ikuta et al., 1968c; 86, Thrower and Eustace, 1973a; 87, Noel-Lambot et al., 1980; 88, Romeril, 1977; 89, Preston et al., 1972; 90, George et al., 1980; 91, Papadopoulu, 1973; 92, Eisler et al., 1978; 93, Greig et al., 1978; 94, Krinsley and Bieri, 1959; 95, Wolfe and Jennings, 1973; 96, White et al., 1979; 97, Phillips, 1979; 98, Bryan and Hummerstone, 1978; 99, Bryan and Uysal, 1978; 100, Decleir et al., 1970; 101, Lowman et al., 1966; 102, Decleir et al., 1978; 103, Schipp and Hevert, 1978; 104, Craig, 1967; 105, Horowitz and Presley, 1977; 106, Mauri et al., 1990; 107, Viarengo et al., 1993; 108, Mat, 1994; 109; Mat et al., 1994;110, Swaileh and Adelung, 1994; 111, Jenkins, 1980; 112, Cheung and Wong, 1992; 113, Claisse and Alzieu, 1993; 114, Han and Hung, 1990; 115, Han et al., 1993; 116, Han et al., 1998; 117, Morris et al., 1989; 118, Weis et al., 1993a; 119, Byers, 1993; 120, Miramand and Bentley, 1992; 121, Bordin et al., 1994; 122, Paez-Osuna et al., 1994; 123, Ward, 1990; 124, Greig and Sennefelder, 1985; 125, Turgeon and O’Connor, 1991; 126, Fagioli et al., 1994; 127, Lauenstein et al., 1990; 128, Chu et al., 1990; 129, Talbot et al., 1985; 130, Brown and McPherson, 1992; 131, Miramand and Bentley, 1992; 132, Denton et al., 2006; 133, Ji et al., 2006; 134, Zorita et al., 2007; 135, Deudero et al., 2007; 136, Vlahogianni et al., 2007; 137, Keskin et al., 2007; 138, Karayakar et al., 2007; 139, Liu and Deng, 2007; 140, Yarsan et al., 2007; 141, Mubiana and Blust, 2006; 142, Sunlu, 2006; 143, Bergasa et al., 2007; 144, Huang et al., 2007; 145, Li et al., 2006; 146, Liang et al., 2004a; 147, Peake et al., 2006; 148, Scancar et al., 2007; 149, Kadar, 2007; 159, Gorinstein et al., 2006; 160, Miramand et al., 2006; 161, Silva et al., 2006; 162, Sasikumar et al., 2006; 163, Espana et al., 2007; 164, Sokolowski et al., 2007; 165, Karouna-Renier et al., 2007; 166, Nesto et al., 2007; 167, LaBrecque et al., 2004; 168, Sankar et al., 2006; 169, Colaco et al., 2006; 170, Kumar et al., 2008; 171, Metian et al., 2008; 172, Maanan, 2008; 173, De Wolf and Rashid, 2008; 174, Cunha et al., 2008; 175, Cravo et al., 2008; 176, Cosson et al., 2008; 177, Sajwan et al., 2008; 178, Frias-Espericueta et al., 2008; 179, Raimundo et al., 2008; 180, Anajjar et al., 2008; 181, Conti et al., 2008; 182, Protasowicki et al., 2008; 183, Kucuksezgin et al., 2008; 184, Schintu et al., 2008; 185, Bustamante et al., 2008; 186, Fattorini et al., 2008; 187, Napoleao et al., 2005; 188, Nicholson and Szefer, 2003; 189, Unlu et al., 2008; 190, Jing et al., 2007.
Molluscs 217
6.13.1 Age and Size Most authorities agree that copper accumulations or rates of accumulation vary with the age of the organism, but even within the same species the pattern was not always predictable. In mussels there was an increase in copper per unit tissue weight with increasing size (Marks, 1938). In a cockle, C. edule, copper concentrations in tissues decreased with increasing age (Savari et al., 1991). In octopus, Polypus, however, copper levels were similar for all size groups (Marks, 1938). Decreasing copper concentrations with increasing body weight is reported for the clams P. morrhuana (Eisler et al., 1978) and M. mercenaria (Larsen, 1979), for the oyster S. cucullata (Mackay et al., 1975) and for the mussel C. meridionalis (Watling and Watling, 1976a). But copper was positively correlated with increasing body weight for other bivalve molluscs, including M. edulis, M. mercenaria, and Venerupis decussata (Boyden, 1974). Small oysters and other bivalve molluscs that have higher copper concentrations in soft tissues than larger bivalves reportedly take up copper at a greater rate and excrete it more slowly than larger conspecifics (Weis et al., 1993a). Younger and smaller bivalve molluscs are more sensitive to copper insult. Juveniles of Asiatic clams (Corbicula fluminea) are more sensitive than adults to ionic copper (Belanger et al., 1990). And embryos of the common mussel are more sensitive to copper than older veliger larvae or postlarval spat (Hoare et al., 1995b).
6.13.2 Chelators Chelators reduced the availability of potentially harmful levels of copper in seawater to molluscs and other marine groups. EDTA reduced toxic and behavioral effects of copper to the clam V. decussata, by making copper ions biologically unavailable (Stephenson and Taylor, 1975). Mussels, M. edulis, collected from the field contained almost as much copper as those subjected to high concentrations in the laboratory, suggesting that copper in field-collected mussels was in a relatively harmless organically bound form (Scott and Major, 1972). Reduced uptake of radiocopper-64 by Baltic clams, M. balthica, occurs at high concentrations of dissolved organic ligands (Absil et al., 1993).
6.13.3 Depth Effects Mussels, M. edulis, collected near shore had nine times more copper in soft tissues than did conspecifics collected offshore in deeper waters (Young and McDermott, 1975). A similar pattern has been observed in other species with different metals and is attributed, in part, to salinity differences and food availability (Nielsen, 1974; Phillips, 1976a,b).
218 Chapter 6
6.13.4 Inherent Species Differences Copper concentrations in cephalopod molluscs are, in general, higher than those in bivalves; in cephalopods, 50-80% of the copper is localized in the digestive gland (Miramand and Bentley, 1992). For crassostreid oysters, which strongly take up copper, green coloration is attributable to excessive accumulation of copper salts (Herdman and Boyce, 1899; Roosenburg, 1969). These oysters, which reportedly have a bitter taste, contain >1000.0 mg Cu/kg DW and have been observed to occur in areas close to steam electric stations (Roosenburg, 1969). Of three species of bivalves collected from Chesapeake Bay, Maryland, oysters contained up to 20 times more copper than clams and up to 200 times more copper than mussels (McFarren et al., 1962). In the mussel, M. edulis, copper was mainly associated with high-molecular weight proteins (Noel-Lambot, 1976); a similar pattern is reported for O. vulgaris hepatopancreas (Rocca, 1969). Loss rates of copper from molluscs varied widely. The gastropod, Busycon canaliculatum, depleted at the rate of 0.07 mg Cu/kg FW daily (Betzer and Pilson, 1975). For Mercenaria, this rate was about 0.05 mg Cu/kg FW daily (Pringle et al., 1968); and for C. virginica it was 3.95 mg Cu/kg FW daily (Mandelli, 1975). In all cases the copper depletion rates were independent of total body copper concentrations.
6.13.5 Interactions with Other Metals Copper concentrations in soft parts of the green mussel, P. viridis, were significantly and positively correlated with concentrations of iron, nickel, lead, manganese, and zinc (Sasikumar et al., 2006). Copper uptake by mussels was erratic and seems to be influenced by available concentrations of zinc, cadmium, and lead salts (Phillips, 1976). Silver, at 0.0005-0.0155 mg Ag/L, enhances adverse effects of copper to embryos of the Pacific oyster when copper concentrations exceed 0.006 mg Cu/L (Coglianse and Martin, 1981). Benthic communities near wooden bulkheads treated with chromated copper arsenate (CCA) had elevated concentrations of these elements, reduced species richness and diversity, and reduced numbers of total organisms when compared to reference sites (Weis and Weis, 1994; Weis et al., 1993b). Transfer of copper from CCA-treated wood occurs in estuarine algae, American oysters, mud snails (N. obsoletus), mussels, and crabs (Weis and Weis, 1992). American oysters (C. virginica) from a canal lined with CCA-treated wood had 150.0 mg Cu/kg FW soft parts versus 20.0 mg Cu/kg FW in conspecifics from a reference site (Weis and Weis, 1993). Copper is trophically transferred from CCA-exposed American oysters to predatory gastropods (Thais spp.), resulting in reduced gastropod feeding and growth (Weis and Weis, 1993).
Molluscs 219
6.13.6 Salinity Copper concentrations in American oyster tissues are higher in low salinity waters than in high salinity (Roesijadi, 1994). Copper uptake by Baltic clams is higher at 10 ppt salinity than at 30 ppt (Absil et al., 1993). Clams, R. cuneata, were 20 times more sensitive to biocidal properties of ionic copper2þ at 1 ppt salinity than at 5 or 22 ppt (Olson and Harrel, 1973), and this was presumably reflected in tissue residues.
6.13.7 Proximity to Point Sources Higher concentrations of copper are found in molluscan tissues near waste outfalls containing copper than in conspecifics from reference sites (Eisler, 1981). Mussels from the most polluted zones had altered enzyme chemistry and enlarged lysosomes (Zorita et al., 2007). Proximity to sewage discharge outfalls is associated with elevated copper burdens in mussels, Mytilus spp. (Lauenstein et al., 1990; Ward, 1990). Elevated copper concentrations in soft tissues of Baltic clams in San Francisco Bay are associated with anthropogenic inputs form nearby sources (Cain and Luoma, 1990). Copper concentrations in rock oysters, Saccostrea glomerata, collected from many locations in Hong Kong were highest in the vicinity of anthropogenic outfalls (Phillips, 1979). In the case of ocean-going and coastal vessels coated with several layers of antifouling paint—containing copper, and sometimes chromium, lead, mercury, tin, or zinc and designed for continual controlled release of toxicants—one result was elevated levels of copper and other paint components in harbor populations of M. edulis when compared to offshore populations (Young et al., 1979). Pacific oysters near a copper recycling facility in Taiwan contained up to 4400.0 mg Cu/kg DW soft parts, a characteristic green color, and low survival after exposure to effluents for 3-7 months (Hung et al., 1990). Oysters in proximity to Australian urban and industrial discharge outfalls frequently exceed the recommended limit of 70.0 mg Cu/kg FW in shellfish edible tissues for protection of human health in than country (Brown and McPherson, 1992). Elevated copper concentrations in Pacific oysters (135.0 mg Cu/kg DW soft parts) near a marina in Arcachon Bay, France, are attributed to a ban on tributyltin (TBT) antifouling paints in 1982 and the subsequent growth in use of copper-based antifouling paints (Claisse and Alzieu, 1993).
6.13.8 Seasonal Variations Copper burdens of bivalves in 2004-2005 from Sinaloa, Mexico, were higher in the rainy season than in the dry season (Frias-Espericueta et al., 2008). Copper accumulations in oysters, mussels, and scallops were highest in summer (Bryan, 1973; Hill and Helz, 1973; Karayakar et al., 2007; Roesijadi, 1994); similar results were observed in clams (Eisler, 1977b; Lee et al., 1975). Tissues of cockles, however, had lower concentrations in summer
220 Chapter 6 when compared to other seasons (Savari et al., 1991). Baltic clams, M. balthica, had highest concentrations in tissues in autumn and winter, and lowest in spring and summer (Sokolowski et al., 2007). These differences were not wholly explainable on the basis of thermal regimes. Possible causes of seasonal variation are attributed to reproductive cycle (Bryan, 1973), variations in moisture content of molluscs (Cain and Luoma, 1990; Phillips, 1976), food availability (Bryan, 1973), local pollution (Fowler and Oregioni, 1976), and drainage from land (Bryan, 1973; Fowler and Oregioni, 1976; Pentreath, 1973; Phillips, 1976).
6.13.9 Gender Concentrations of copper that inhibit reproduction in the common mussel, M. edulis, from unpolluted or mildly contaminated sites did not inhibit embryonic development of mussels from copper-contaminated sites; cross-breeding of mussels from these sites suggest that copper tolerance in mussels in mostly maternally controlled (Hoare et al., 1995a). Female C. meridionalis contain significantly more copper in whole soft parts than males, with copper concentrations positively correlated with zinc concentrations (Watling and Watling, 1976a). Copper does not necessarily translocate to sex products. In one case, Pacific oysters, C. gigas, from two geographic locations had significantly different tissue levels of copper; both groups were induced to spawn, and eggs from the two groups contained similar amount of copper: 28.0 and 29.0 mg Cu/kg DW (Greig et al., 1975). However, in the case of mussels, M. californianus, gonads of females contained up to twice as much copper as testes, with no-sex related differences in copper content of digestive gland or muscle (Alexander and Young, 1976).
6.13.10 Sediments Copper concentrations in Baltic clam (M. balthica) and cockle (C. edule) tissues are positively correlated with copper concentrations in the surrounding sediments (Cain and Luoma, 1990; Savari et al., 1991; Sokolowski et al., 2007). However, copper burdens in tissues of another cockle (Anadara trapezium) are independent of sediment copper concentrations (Scanes, 1993). Larvae of Pacific oyster, C. gigas, accumulate copper and other metals from elutriates of metals-contaminated sediments (Geffard et al., 2007). Proposed sediment copper criteria for protection of sensitive marine molluscs include <5.0 mg/kg DW to prevent avoidance by clams and <15.0 mg/kg DW to allow burrowing (Roper and Hickey, 1994). For more resistant species, less than 40.0 mg Cu/kg DW sediment is considered safe (Fagioli et al., 1994), but more than 200.0 mg Cu/kg DW may cause reduced species diversity and the disappearance of sensitive species (Bryan and Langston, 1992). Sediments containing more than 2000.0 mg Cu/kg DW are considered lethal to juvenile bivalve molluscs (Bryan and Langston, 1992).
Molluscs 221
6.13.11 Temperature Groups of softshell clams, M. arenaria, had greatly reduced survival during immersion in given concentrations of copper salts at ambient summer temperatures (22 C) that were nonlethal, and at autumn (17 C) or winter (4 C) thermal regimes (Eisler, 1977a). At 22 C, 0.035 mg Cu/L was fatal to 50% of M. arenaria in 168 h; however, at 3.0 mg/L and 4 C, none died in 336 h (Eisler, 1995a). Copper was also accumulated more rapidly by Mya at ambient summer temperatures than other seasonal thermal regimes (Eisler, 1977b). Embryos of the giant clam, Tridacna derasa, were extremely sensitive to copper: at 27 C and 0.0001 mg Cu/L, 50% died in 72 h (Soria-Dengg and Ochavillo, 1990). Copper is more toxic to embryos of the tropical giant clam than to bivalve embryos in temperate regions, possibly because many tropical species of shellfish live near their upper lethal thermal limits and are unable to withstand additional environmental stressors. Isolated gills of the common mussel, M. edulis, took up copper from the medium (0.004 mg/L) over a 28 day period at temperatures between 6 and 26 C; accumulations were directly proportional to increasing temperature (Mubiana and Blust, 2007). When the study was repeated with whole mussels, copper levels were inversely related to water temperature. In gills, temperature effects on uptake are due mainly to changes in solution chemistry and physical kinetics, which favor higher uptake at higher temperatures. At the whole organism level, however, complex physiological responses appear to mask the relationship, particularly for biologically essential metals such as copper (Mubiana and Blust, 2007).
6.13.12 Tissue Specificity Copper concentrations in excess of 1000.0 mg/kg DW in molluscan tissues are documented, although tissues differ among groups (Table 6.9). For example, highest elevated copper burdens were in liver and hepatopancreas of octopods, squids, and gastropods; kidney in scallops; soft parts, gills, viscera, and mantle of oysters; and hemolymph of octopods (Table 6.9). In cuttlefish, S. officinalis, copper tends to increase exponentially in digestive gland with increasing age and may contain up to 90% of the organisms total metal burden (Miramand et al., 2006). Highest accumulations of copper in the bivalve, Meretrix casta, were in gill tissues (Nambisan et al., 1977). In the gastropod, B. canaliculatum, copper concentrated in gill and osphradium, with histopathology observed at these sites (Betzer and Yevich, 1975). In the scallop, P. maximus, copper accumulated in digestive gland; however, copper was mainly in kidneys of the closely related C. opercularis (Bryan, 1973). In mussels, M. edulis, the digestive gland is the primary site of copper accumulation (Young and McDermott, 1975). Adverse effects of copper stress are not necessarily accompanied by measurable
222 Chapter 6 copper accumulations in tissues. Thus, copper-induced death was reported for the hardshell clam, Mercenaria, with no measured accumulations in tissues (Shuster and Pringle, 1968). Copper accumulations, both natural and experimentally induced, in the gastropod Littorina littorea, shows copper in four types of cells, as determined by histochemical, spectrographic, and ion emission techniques (Martoja et al., 1980). Excretory cells of conjunctive tissues, in vascular conjunctive tissue and myocardium, contained precipitated CuS; older gastropods contained increasing concentrations of CuS and is interpreted as the result of hemocyanin degradation. Perivascular cells surrounding the aorta and arteries contain copper inside the spherocrystals; copper was associated with other elements, mainly magnesium and calcium, and intoxication by Cu2+ results in deposits at the periphery of these crystals. Hepatopancreas digestive cells are a third type; copper, in an unidentified unstable form, is found along the boundaries of these cells. Finally, the axial conjunctive cells of kidney lamellae contain copper overlying the sulfyrillated proteins, with highest concentrations in gastropods from copper-impacted areas; however, stress was not associated with environmental levels of copper. Progressive accumulation of copper sulfide (CuS), independent of environmental copper levels, makes Littorina an unreliable indicator of copper stress (Martoja et al., 1980).
6.13.13 Toxicity Dissolved organic carbon, administered as humic acid, affects copper speciation and toxicity to embryos of the Pacific oyster, C. gigas (Brooks et al., 2007). Increasing humic acid concentration up to 1.0 mg/L reduces the toxicity of total copper by about 50%; however, the labile copper component—comprised of free ion and inorganic copper complexes—was unaffected. This finding suggests that the labile copper fraction—not total copper—is responsible for the observed toxicity to oyster embryos, and this is consistent with the freeion activity model for copper toxicity (Brooks et al., 2007). Copper was fatal at 0.005 mg Cu/L (50% dead in 119 days) to the bay scallop, A. irradians, at 0.025 mg Cu/L to the hardshell clam, M. mercenaria (53% dead in 77 days; USEPA, 1980b), and at 0.087 mg Cu/L (50% dead in 96 h) to the abalone, Haliotis rubra (Gorski and Nugegoda, 2006). Sublethal concentrations of copper to various shellfish species were associated with cytotoxicity (Zaroogian et al., 1992) and abnormal metabolism (Chelomin and Belcheva, 1992). Adverse effects of copper to mussels include: inhibited mucous production at 0.01 mg Cu/L (Davies, 1992);reduced growth in 0.01-0.032 mg Cu/L (Calabrese et al., 1984; Sanders et al., 1991a, 1994); disrupted metabolism (Viarengo et al., 1981, 1990) and increased oxygen consumption (Mathew and Menon, 1993) at 0.015 mg Cu/L; a significant reduction in spawning frequency at 0.002-0.006 mg/L during immersion for 30 days (Stromgren and Nielsen, 1991); and death at 0.086 mg Cu/L (Krishnakumar et al., 1990). In mussels, copper
Molluscs 223 impairs the structure and function of cellular membranes by stimulating the peroxidation of membrane lipids causing increased formation of lipofuscins (Viarengo et al., 1981, 1990). Copper-induced lysosomal lipofuscin accumulations, together with metallothioneins, control copper residues at the cellular levels and are responsible for the short half-time persistence (6-8 days) of copper in the digestive gland of mussels (Viarengo et al., 1990). Juvenile clams, Macoma liliana, die when kept in sediments containing more than 30.0 mg Cu/kg DW; avoid sediments containing more than 25.0 mg Cu/kg DW (0.113 mg Cu/L sediment interstitial water); and show a reduction in ability to bury in sediments containing more than 15.0 mg Cu/kg DW (Roper and Hickey, 1994).
6.13.14 Accumulations by Laboratory Populations Initial effects of copper on mussels (Mytilus spp.) include valve closure, a reduction in filtration rate, and cardiac inhibition; all of these responses serve to slow copper uptake through reduction in mussel contact with the ambient environment and a reduction in blood flow within the organism (Gainey and Kenyon, 1990). Eggs and larvae of the mussel, M. galloprovincialis, accumulate copper from the medium, but adverse effects on development occur only at seawater concentrations of 0.00946 mg Cu/L and higher, when whole embryos contain 47.8 mg Cu/kg DW, and when shell contains 26.8 mg Cu/kg DW or soft parts have more than 76.9 mg Cu/kg DW (Rosen et al., 2008). BCFs for marine bivalve molluscs (ratio of mg Cu/kg FW soft parts to mg Cu/L medium) vary from 85 to 28,200. BCFs for copper are high for American oysters after exposure for 140 days (20,200-28,200) and lower (3100-3300) for bay scallops and softshell clams after exposure for 35-112 days (USEPA, 1980b). Accumulations in Pacific oysters held on copper-loaded sediments are similar to those of oysters contaminated through ingestion of diatoms (Haslea ostrearia); however, accumulations are highest in oysters when exposed through the medium (Ettajani et al., 1992). In that study, a concentration of 0.03 mg Cu/L seawater for 21 days resulted in copper burdens of 137.0 mg/kg DW in whole diatoms and 1320.0 mg/kg DW in oyster soft tissues. Oysters fed contaminated diatoms in the study had 419.0 mg Cu/kg DW soft parts. Oysters held on sediments containing 108.0 mg Cu/kg DW had 401.0 mg Cu/kg DW (Ettajani et al., 1992). Han and Hung (1990) aver that diet is the major pathway by which greenish-colored Pacific oysters contain up to 4000.0 mg Cu/kg DW soft tissues. Initial daily accumulation rates up to 214.0 mg Cu/kg DW soft parts are reported (Han and Hung, 1990). Elimination of 50% of the copper from green Pacific oysters with elevated copper burdens takes only 11.6 days versus 25.1 days in reference oysters (Han et al., 1993). Copper uptake kinetics in rock oysters, Crassostrea cucullata, was investigated (D’Silva and Quasim, 1979) and showed that exposure in media containing 0.01 mg Cu/L resulted in an
224 Chapter 6 increase in soft parts from 10.6 mg Cu/kg FW at start to 60.4 mg Cu/kg FW after 7 weeks. After 7 weeks in copper-free seawater, oysters lost 38% of the accumulated copper. Authors concluded that copper loss was closely correlated with total internal copper concentration rather than uptake rate as proposed by Pringle et al. (1968). However, copper uptake rate is considered an important variable in predicting copper toxicity to mussels, M. edulis, together with medium copper concentration (Martin, 1979). High accumulations of copper in soft tissues were measured in several species of bivalves under various concentration/time regimes: M. edulis in 0.010-0.04 mg Cu/L for 2-30 days (Adema et al., 1972; Bordin et al., 1994); Tellina tenuis in 0.01 mg Cu/L for 100 days (Saward et al., 1975); M. arenaria in 0.01 mg Cu/L for 6 weeks at 0-10 C temperatures and 7 days at 20-22 C (Eisler, 1977a,b); Haliotis spp. in 0.01 mg Cu/L for 96 h (Martin et al., 1977); and Mytilus viridis in 0.01 mg Cu/L for 5 weeks (D’Silva and Kureishy, 1978). At higher copper concentrations and longer exposure periods, copper residues in molluscs were higher, survival lower, and damage effects more pronounced (Clarke, 1947; Eisler, 1977b; Jing et al., 2007; Martin et al., 1977; Pringle et al., 1968; Scott and Major, 1972). Most investigators now support the premise that copper in trace quantities is required by marine molluscs and that small increments above the required level are highly toxic.
6.14 Europium The highest value known for stable europium in marine molluscs is 0.123 mg Eu/kg DW in pteropod tests (Table 6.10). No radioeuropium-152 activity was found in various species of molluscs collected in summer 2004 near Amchitka Island in the Aleutian chain; Amchitka Island was the site of three nuclear tests between 1965 and 1971 (Burger et al., 2007b).
6.15 Gallium The highest value reported for gallium in marine molluscs is 0.16 mg Ga/kg DW in soft parts (Table 6.10).
6.16 Gold The highest values known for gold concentrations in marine molluscs are 0.038 mg Au/kg DW and 0.079 mg Au/kg AW, both in soft parts (Table 6.10). High bioconcentration of gold was reported in three species of bivalves from the Aegean Sea. Although tissue gold concentrations were 770-2400 times higher than seawater levels (Papadopoulu, 1973), maximum values recorded in bivalves did not exceed 0.052 mg Au/kg AW soft parts (Table 6.10).
Molluscs 225 Table 6.10: Europium, Gallium, Gold, and Hafnium Concentrations in Field Collections of Molluscs Metal and Organism
Concentration
Reference
a
Europium Bivalve molluscs; 4 species; Aegean Sea Soft parts Muscle Mantle and gills Stomach and intestines Gonads Hepatopancreas Byssus
0.020-0.044 DW 0.009-0.03 DW 0.011-0.061 DW 0.012-0.048 DW 0.011-0.039 DW 0.012-0.017 DW 0.014-0.056 DW
1 1 1 1 1 1
Common mussel, Mytilus edulis; soft parts
0.0005-0.11 DW
2
Pteropods; tests
0.007-0.123 DW
3
0.008-0.036 DW 0.007-0.16 DW
4 4
Molluscs; 3 species; soft parts
0.049-0.052 AW
5
Mytilus edulis; soft parts
0.002-0.038 DW
2
Clam, Tapes japonica Soft parts Soft parts
0.079 AW 0.0057 DW
6 7
0.0006-0.1000 DW
2
Gallium Molluscs Shell Soft parts Gold
Hafnium Mytilus edulis; soft parts
Values are in mg element/kg dry weight (DW) or ash weight (AW). a 1, Papadopoulu and Hadzistelios, 1977; 2, Karbe et al., 1977; 3, Turekian et al., 1973; 4, Culkin and Riley, 1958; 5, Papadopoulu, 1973; 6, Fukai and Meinke, 1959; 7, Fukai and Meinke, 1962.
Common mussels, M. edulis, exposed for 24 h to gold-citrate nanoparticles had increased catalase activity in digestive gland and mantle, and other signs of oxidative stress (Tedesco et al., 2008). Smaller gold nanoparticles of about 1 nm in diameter are potentially toxic when compared to nanoparticles about 18 nm in diameter (Tedesco et al., 2008).
226 Chapter 6
6.17 Hafnium The only datum found on hafnium in molluscs is 0.0006-0.1 mg Hf/kg DW in mussel soft tissues (Table 6.10).
6.18 Iron Iron concentrations in excess of 2000.0 mg/kg DW are documented for soft parts, mantle and digestive gland of clams; for shell, soft parts, gills, and visceral mass of mussels; for shell and soft parts of gastropods; and for shell, soft parts, gills, digestive gland, striated muscle, intestine, and kidney of scallops (Table 6.11). Substantial variations in iron content between and among field-collected species are attributed, in part, to diet and pollution. For example, proximity to anthropogenic point sources such as electroplating plants, iron works, and waste outfalls was almost always associated with elevated iron concentrations in molluscs (Eisler et al., 1978; Fowler and Oregioni, 1976; Phillips, 1978, 1979; Sankaranarayanan et al., 1978). Diet was acknowledged as an important source of iron in marine molluscs. In the case of Littorina obtusata, food chain accounted for 42% of daily iron intake equivalent to 910.0 mg Fe/kg tissue/day to the total tissue concentration of 34,600.0 mg/kg DW (Young, 1975). Among predatory gastropods, such as N. lapillus, diet was the major source of iron, the input from food being about 100 times greater than seawater (Young, 1977). In N. lapillus, the fraction of iron assimilated from food was similar to rate of excretion, with relative iron concentrations reflecting the relative concentrations in prey organisms (Young, 1977). Mussels, M. edulis, may preferentially accumulate soluble forms of iron from seawater over particulates; however, accumulation of iron from the medium is relatively minor compared with that of dietary accumulation (Pentreath, 1973). Organism size and salinity of the medium also confound interpretation of residues: iron in soft tissues of clams is significantly correlated with increasing shell length (Ji et al., 2006), and with decreasing salinity of the medium (Mubiana and Blust, 2006). In the pearl oyster, Pinctada fucata, iron was most abundant in digestive gland, followed by mantle, and gill tissues in the ratio of 11:4:1 (Gonzalez et al., 2008). M. edulis accumulates radiolabeled ferric hydroxide in linear proportion to concentrations in seawater in the range 0.007-0.5 mg Fe/L; iron uptake rates in whole soft parts were constant during exposure for 25 days although iron levels in some tissues show a tendency to equilibrate, presumably by transfer of iron from these tissues to a growing store elsewhere (George et al., 1976). Many mollusc cell types are rich in lysosomes and these have the ability to sequester—or otherwise bind—metals. Iron was demonstrated histochemically in cytoplasmic inclusions shown to be lysosomes in a number of cell types of M. edulis (Lowe and Moore, 1979). Exponential, rather than linear, uptake of radioiron from seawater by Mytilus was observed with equilibrium reached for individual tissues in 21-42 days (Pentreath, 1973).
Molluscs 227 Table 6.11: Iron Concentrations in Field Collections of Molluscs Organism
Concentration
Clam, Andara trapezia; whole
745.0-1285.0 DW
1
Mussel, Anodonta sp. Shell Soft parts
2600.0 DW 5500.0 DW
2 2
Gastropod, Aplysia benedicti Ctenidium Gonad Parapodia Hepatopancreas Buccal mass Intestine Gut Content Shell
320.0-750.0 DW 194.0-325.0 DW 48.0-175.0 DW 261.0-280.0 DW 400.0-2300.0 DW 456.0 DW 541.0 DW 647.0 DW
3 3 3 3 3 3 3 3
Giant squid, Architeuthis dux; 2001-2005; hepatopancreas; Bay of Biscay vs. Mediterranean Sea
497.0 DW vs. 158.0 DW
Scallop, Argopecten irradians; kidney concretion
608.3 DW
Reference
a
72
4
Hydrothermal vent mussel, Bathymodiolus azoricus; mid-Atlantic ridge Summer 2002; start vs. 30 days in metals-free seawater Gill Mantle Digestive gland Byssus thread Shell; 2001 2001; 5 sites Gills Mantle Digestive gland
120.0 FW vs. 75.0 FW 60.0 FW vs. 70.0 FW 260.0 FW vs. 200.0 FW 1400.0 FW vs. <10.0 FW 20.6-55.0 (15.6-62.1) DW
55 55 55 55 66
83.0-2066.0 DW 28.0-229.0 DW 198.0-1854.0 DW
67 67 67
Waved whelk, Buccinum undatum Shell Soft parts
470.0 DW 110.0 DW
2 2
Cockle, Cardium edule Shell Soft parts
1600.0 DW 590.0 DW
2 2 (Continues)
228 Chapter 6 Table 6.11: Cont’d Organism
Concentration
Cockle, Cerastoderma edule Soft parts Soft parts
390.0-1327.0 DW 406.0-991.0 DW
5 6
Scallop, Chlamys opercularis Shell Soft parts Body fluid Mantle Gills Digestive gland Striated muscle Unstriated muscle Gonad and foot Kidneys
64.0-120.0 DW 113.0 DW 32.1 DW 67.1 DW 134.0 DW 853.0 DW 10.7 DW 16.3 DW 132.0 DW 330.0 DW
2 7 7 7 7 7 7 7 7 7
Mussel, Choromytilus meridionalis Soft parts Soft parts
18.0 FW 60.0 DW
8 9
Scallop, Comptopallium radula; New Caledonia; October 2004 Soft parts Digestive gland
221.0 (162.0-375.0) DW 1195.0 DW
63 63
Pacific oyster, Crassostrea gigas Soft parts Soft parts
15.3-91.4 FW 128.0 DW
10 11
Oyster, Crassostrea margaritacea; soft parts
57.0 DW
11
Oyster, Crassostrea rhizophorae; soft parts; summer 2001; Brazil; contaminated estuary vs. reference site
152.0-519.0 DW vs. 242.0-299.0 DW
57
31.0-238.0 FW 510.0 DW vs. 150.0 DW 19.0 DW 140.0-800.0 DW 15.0-79.0 DW 233.0-738.0 DW 140.0-690.0 DW 232.0-1357.0 DW
12 13 13 14 15 15 16 62, 68
American oyster, Crassostrea virginica Soft parts Soft parts; October vs. December Shell Soft parts Shell Soft parts Soft parts Soft parts; Savannah, Georgia; 2000-2001; 9 sites
Reference
a
(Continues)
Molluscs 229 Table 6.11:
Cont’d
Organism
Concentration
Slipper limpet, Crepidula fornicata Shell Soft parts
1600.0 DW 2000.0 DW
2 2
Clam, Donax serra; soft parts
47.0 FW
8
Clam, Ensis arcuatus; shell
66.0 DW
17
Clam, Ensis siliqua; shell
75.0 DW
17
Gastropods Flesh Shell Viscera Operculum
13,000.0 AW 680.0 AW 6100.0 AW 50,000.0 AW
18 18 18 18
Abalone, Haliotis midea; soft parts
27.0 FW
Abalone, Haliotis tuberculata; soft parts
306.0-474.0 DW
19
Periwinkle, Littoraria scabra; soft parts; Tanzania Industrialized sites; 1998 vs. 2005 Reference sites; 2005
350.0 DW vs. 350.0 DW 110.0 DW
64 64
Limpet, Littorina littorea; soft parts plus operculum Squid, Loligo opalescens; liver; California Central coast Southern coast
227.0-784.0 DW
Reference
8
6
111.0 DW 87.0 DW
20 20
502.0-1540.0 DW 650.0-1800.0 DW
6 60
Hardshell clam, Mercenaria mercenaria Soft parts Soft parts Shell Soft parts Soft parts Mantle Gills Muscle
9.0-83.0 FW 18.0-81.0 FW 1600.0 DW 5400.0 DW 810.0 AW 740.0 AW 1480.0 AW 800.0 AW
12 5 2 2 21 21 21 21
Clam, Meretrix lamarckii; soft parts
130.0 DW
22
Clam, Macoma balthica Soft parts Soft parts; 1996-1997; Gulf of Gdansk
a
(Continues)
230 Chapter 6 Table 6.11: Cont’d Organism
Concentration
Mussel, Modiolus modiolus Shell Soft parts Mantle and gills Muscle Gonad Gut and digestive gland
15.0 DW 300.0-350.0 DW 220.0 DW 51.0 DW 130.0 DW 1100.0 DW
2 2 2 2 2 2
41.0-239.0 DW 86.0-1415.0 DW 25.2-551.0 FW
23 23 59
18.0-59.0 FW
24
4834.0 DW vs. 230.0-317.0 DW 49.7-1710.0 FW
25
Mussel, Mytilus californianus; soft parts
59.0-630.0 DW
26
Mussel, Mytilus corscum; soft parts
150.0 DW
22
Molluscs Shell Soft parts Soft parts; 5 spp.; Chile, Strait of Magellan; 2001; 17 stations Edible portions, 3 spp. Softshell clam, Mya arenaria Soft parts; winter vs. summer Soft parts
Reference
a
12
Common mussel, Mytilus edulis Soft parts; Scheldt estuary; March 2000 Soft parts Soft parts Shell Shell; Baltic Sea; 2005; 12 sites Soft parts Soft parts Soft parts Shell Soft parts Soft parts Soft parts Soft parts Shell Soft parts
3800.0 DW
71
14.0-1367.0 DW 112.0-1623.0 DW 17.0-55.0 DW 5.5-22.2 DW 81.0-710.0 DW 17.0-31.0 DW 152.0-401.0 DW 8.9 DW 64.0-589.0 DW 776.0 DW 41.0-707.0 DW Max. 400.0 DW 290.0 DW 1700.0 DW
27 28 28 69 26 29 6 17 30 17 31 54 2 2
Mussel, Mytilus edulis aoteanus Soft parts Mantle Gill
1960.0 DW 180.0 DW 2940.0 DW
32 32 32 (Continues)
Molluscs 231 Table 6.11: Organism Muscle Visceral mass Intestine Foot Gonad Shell Mussel, Mytilus edulis planulatus; soft parts; various dry weights 0.09 g 0.39 g 0.48 g 0.69 g Mussel, Mytilus galloprovincialis Soft parts; Venice lagoon, Italy; 2005-2006; San Giuliano vs. Sacca Sessola April July October February Soft parts Soft parts Soft parts; Izmir Bay, Turkey; 2004 Soft parts; Gulf of Gemlik, Turkey; 2004 Soft parts; Adriatic Sea; 2001-2005; winter vs. summer Mantle vs, gills; 2004-2006; Greece; max. mean concentrations; contaminated sites Summer Autumn Winter Spring
Cont’d
Concentration 82.0 DW 13,650.0 DW 570.0 DW <10.0 DW 93.0 DW <10.0 DW
1198.0 DW 671.0 DW 601.0 DW 616.0 DW
Reference 32 32 32 32 32 32
1 1 1 1
207.9 DW vs. 234.9 DW 3.9 DW vs. 3.8 DW 131.6 DW vs. 131.0 DW 306.3 DW vs. 271.9 DW 443.0 DW 26.9 FW 49.3 DW 205.4 DW
61 61 61 61 33 34 70 81
348.0-460.0 DW vs. 58.6-177.0 DW
73
98.4 FW 90.0 FW 22.2 FW 30.0 FW
53 53 53 53
vs. vs. vs. vs.
a
151.0 FW 130.0 FW 32.9 FW 43.8 FW
Mussel, Mytilus viridis; soft parts
549.0-2751.0 DW
35
Abalone, Notohaliotis discus; soft parts
110.0 DW
22
Gastropod, Nucella conccina; soft parts; Antarctica; 2004
2756.0 DW
52 (Continues)
232 Chapter 6 Table 6.11: Cont’d Organism
Concentration
Gastropod, Nucella lapillus Soft parts with operculum Shell Soft parts
193.0-270.0 DW 4.5 DW 65.0 DW
Octopus, Octopus sp.; whole
37.0 FW
36
1920.0 DW 399.0 DW 188.0 DW 160.0 DW 112.0 DW 47.0 DW not detectable
37 37 37 37 37 37 37
636.0-844.0 DW 464.0-690.0 DW 33.0-47.0 DW 23.0-27.0 DW
79 79 79 79
Squid, Ommastrephes bartrami; liver
399.0 DW
20
Oyster, Ostrea angasi; whole
612.0-2585.0 DW
1
Oyster, Ostrea edulis Soft parts Soft parts
232.0-352.0 DW 167.0 DW
38 11
Oyster, Ostrea sinuata Soft parts Mantle Gill Muscle, nonstriated Muscle, striated Visceral mass Kidney Heart Shell
682.0 DW 840.0 DW 620.0 DW 274.0 DW 2880.0 DW 1156.0 DW 384.0 DW 247.0 DW 570.0 DW
32 32 32 32 32 32 32 32 32
1535.6-5915.6 DW; 442.3-1283.7 FW
39
1635.0-2670.0 DW 1024.0-1995.0 DW
65 65
Octopus, Octopus vulgaris Hepatopancreas Branchial heart Gill Central heart Kidney Body muscle Hemolymph Portugal; 1999-2002; 3 sites Digestive gland Branchial heart Gill Muscle
Limpet, Patella coerulea; soft parts Limpet, Patella candei gomesii; soft parts; 2007; Azores Near hydrothermal vent Reference site
Reference
a
6 2 2
(Continues)
Molluscs 233 Table 6.11:
Cont’d
Organism
Concentration
Reference
Limpet, Patella vulgata Soft parts Soft parts Shell Shell Soft parts Soft parts
2454.0 DW 1289.0-2505.0 DW 39.0-64.0 DW 430.0 DW 150.0 DW 891.0-2330.0 DW
40 28 28 2 2 6
Scallop, Pecten maximus Shell Soft parts Muscle Gut and digestive gland Mantle and gills Gonad Soft parts Body fluid Mantle Gills Digestive gland Striated muscle Unstriated muscle Gonad and foot Kidney Kidney
37.0-49.0 DW 170.0 DW 30.0 DW 2900.0 DW 570.0 DW 100.0 DW 196.0 DW 26.4 DW 86.4 DW 137.0 DW 1295.0 DW 13.1 DW 17.1 DW 143.0 DW 149.0 DW 42.0 FW
2 2 2 2 2 2 7 7 7 7 7 7 7 7 7 41
Scallop, Pecten novae-zelandiae Soft parts Mantle Gills Muscle Visceral mass Intestine Kidney Foot Shell Gonad
2915.0 DW 1540.0 DW 21,600.0 DW 34.0 DW 2200.0 DW 6090.0 DW 2470.0 DW 2380.0 DW 2000.0 DW 228.0 DW
32 32 32 32 32 32 32 32 32 32
Pelycopods Soft parts Shell
500.0 AW 142.0 AW
18 18
Green mussel, Perna viridis Soft parts; India; January 2002 Small
81.0 FW
58
a
(Continues)
234 Chapter 6 Table 6.11: Cont’d Organism Medium Large Hong Kong; juveniles vs. adults Reference site Soft parts Byssus Shell Polluted site Soft parts Byssus Shell
Concentration
Reference
64.9 FW 40.3 FW
58 58
144.0 DW vs. 97.2 DW 899.0 DW vs. 230.0 DW 4.9 DW vs. 5.2 DW
80 80 80
345.0 DW vs. 354.0 DW 527.0 DW vs. 1162.0 DW 12.4 DW vs. 8.9 DW
80 80 80
Clam, Pitar morrhuana; soft parts
250.0-799.0 DW
42
Scallop, Placopecten magellanicus; soft parts
803.0 DW
43
Pteropods; 9 spp.; tests
48.0-741.0 DW
44
Manila clam, Ruditapes philippinarum; soft parts; Korea; 2002-2003 Females vs. males Postspawn vs. prespawn
573.0 DW vs. 571.0 DW 740.0 DW vs. 572.0 DW
51 51
Oyster, Saccostrea glomerata; soft parts
202.0-731.0 DW
45
Clam, Scrobicularia plana Looe estuary, England; soft parts Tamar estuary, England Soft parts Digestive gland Gannel estuary, England Soft parts Digestive gland Mantle and siphons Foot and gonad Gills and palps Adductor muscle Kidney Camel estuary, England Soft parts Digestive gland Mantle and siphons Foot and gonad Gills and palps
1090.0 (559.0-3010.0) DW
6
2370.0 (441.0-7280.0) DW 1170.0 (676.0-2400.0) DW
46 46
1120.0-1240.0 DW 872.0 DW 3480.0 DW 342.0 DW 848.0 DW 236.0 DW 819.0 DW
47 47 47 47 47 47 47
699.0-840.0 DW 604.0 DW 971.0 DW 298.0 DW 680.0 DW
47 47 47 47 47
a
(Continues)
Molluscs 235 Table 6.11: Organism Adductor muscle Kidney Transferred from Camel estuary to Gannel estuary for 352 days Digestive gland Other tissues Transferred from Gannel estuary to Camel estuary for 352 days Digestive gland Other tissues
Cont’d
Concentration
Reference
177.0 DW 1090.0 DW
47 47
1940.0 DW 1020.0 DW
47 47
728.0 DW 1290.0 DW
47 47
Squid, Sepia esculenta; trunk
16.0 DW
22
Cuttlefish, Sepia officinalis Blood Liver Gut Branchial gland Arterial heart Ovary Blood Hepatopancreas Branchial gland Branchial heart Branchial heart appendage Heart ventricle Pancreatic appendages
1.0 FW 37.0-42.0 DW 16.0-36.0 DW 19.0-27.0 DW 22.0-31.0 DW 5.0-8.0 DW 26.0 FW 152.0 FW 22.0 FW 46.0 FW 67.0 FW 37.0 FW 36.0 FW
48 48 48 48 48 48 49 49 49 49 49 49 49
Squid, Sepia sp.; whole
8.0 FW
36
398.0 DW 14.0 DW 1.1 DW
56 56 56
80.0 DW 21.0 DW
56 56
38.0 DW 210.0 DW 28.0 DW
56 56 56
41.0 DW
56
Common cuttlefish, Sepia officinalis Egg Eggshell Embryo Yolk Hatchlings Whole Cuttlebone Juveniles, age 1 month Whole Digestive gland Cuttlebone Immature, age 12 months Whole
a
(Continues)
236 Chapter 6 Table 6.11: Cont’d Organism Digestive gland Cuttlebone Adults, age 18 months Whole Digestive gland Cuttlebone
Concentration
Reference
340.0 DW 15.0 DW
56 56
30.0 DW 390.0 DW 2.5 DW
56 56 56
Squid Muscle Muscle with skin Viscera Pen
107.0 DW 19.3 DW 60.6 DW 160.0 DW
50 50 50 50
Squid, Symplectoteuthis oualaniensis; liver
319.0 DW
20
a
Values are in mg Fe/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Harris et al., 1979; 2, Segar et al., 1971; 3, Patel et al., 1973; 4, Carmichael et al., 1979; 5, Romeril, 1974; 6, Bryan and Hummerstone, 1977; 7, Bryan, 1973; 8, Van As et al., 1973; 9, Watling and Watling, 1976b; 10, Pringle et al., 1968; 11, Watling and Watling, 1976a; 12, Shuster and Pringle, 1968; 13, Frazier, 1975; 14, Galtsoff, 1953; 15, Windom and Smith, 1972; 16, Goldberg et al., 1978; 17, Bertine and Goldberg, 1972; 18, Lowman et al., 1970; 19, Bryan et al., 1977; 20, Martin and Flegal, 1975; 21, Eisler and Weinstein, 1967; 22, Ishii et al., 1978; 23, Culkin and Riley, 1958; 24, Van As et al., 1975; 25, Eisler, 1977b; 26, Goldberg et al, 1978; 27, Phillips, 1978; 28, Lande, 1977; 29, Hobden, 1967; 30, Simpson, 1979; 31, Karbe et al., 1977; 32, Brooks and Rumsby, 1965; 33, Fowler and Oregioni, 1976; 34, Uysal, 1978a,b; 35, Bhosle and Matondkar, 1978; 36, Matsumoto et al., 1964; 37, Ghiretti-Magaldi et al., 1958; 38, Fukai et al., 1978; 39, Shiber and Shatila, 1978; 40, Preston et al., 1972; 41, George et al., 1980; 42, Eisler et al., 1978; 43, Reynolds, 1979; 44, Turekian et al., 1973; 45, Phillips, 1979; 46, Bryan and Uysal, 1978; 47, Bryan and Hummerstone, 1978; 48, Decleir et al., 1978; 49, Schipp and Hevert, 1978; 50, Horowitz and Presley, 1977; 51, Ji et al., 2006; 52, Santos et al., 2006; 53, Vlahogianni et al., 2007; 54, Mubiana and Blust, 2006; 55, Kadar, 2007; 56, Miramand et al., 2006; 57, Silva et al., 2006; 58, Sasikumar et al., 2006; 59, Espana et al., 2007; 60, Sokolowski et al., 2007; 61, Nesto et al., 2007; 62, Kumar et al., 2008; 63, Metian et al., 2008; 64, De Wolf and Rashid, 2008; 65, Cunha et al., 2008; 66, Cravo et al., 2008; 67, Cosson et al., 2008; 68, Sajwan et al., 2008; 69, Protasowicki et al., 2008; 70, Kucuksezgin et al., 2008; 71, Wepener et al., 2008; 72, Bustamante et al., 2008; 73, Fattorini et al., 2008; 79, Napoleao et al., 2005; 80, Nicholson and Szefer, 2003; 81, Unlu et al., 2008.
The concentration of iron in feces of M. arenaria and Mercenaria is increased by several orders of magnitude over that in seawater, that is, 15,400 for Mercenaria, 1000 for Mya and may represent an important factor in the transfer of iron to bottom sediments (Andrews and Warren, 1969). Studies on the compartmentalization of iron in M. edulis (Hobden, 1967) showed that iron concentrations in whole mussels from Southampton, England, usually ranged between 20.0 and 40.0 mg Fe/kg DW, occasionally rising to 100.0 mg Fe/kg DW in the spring. Prolonged starvation in seawater of low iron content did not reduce average iron below 20.0 mg Fe/kg DW, as this represents a permanent store. Higher iron values were produced by a temporary store that was lost rapidly on starvation. Digestive gland was the major repository of the temporary store of iron, most of which was subjected to digestive processes. In a second
Molluscs 237 study (Hobden, 1969), it was demonstrated that Mytilus absorbed soluble iron from citrated seawater either directly of by adsorption onto mucous used in feeding. Absorption slowed or ceased after 3-7 days at which time the total iron uptake was about 1% of the total body iron burden. Byssus threads had the highest iron concentration, followed by kidney, digestive gland, gut epithelia, gill, heart, gonad, and muscle, in that order. Accumulated iron persisted over a period of 10 days when the mussels were transferred to clean seawater (Hobden, 1969). Pteropods, unlike mussels, eliminated radioiron rapidly, at elimination rates of 5-6%/h (Kuenzler, 1969). Iron-mercury interactions were observed in M. mercenaria. In the range 0.0-0.1 mg Hg/L in the medium there were significant decreases in iron content of mantle fringe tissues (Fowler et al., 1975). Other factors reported to modify iron accumulations in molluscs included gender, season of collection, and water turbidity, salinity, and depth. Thus, iron concentrations were higher in females of C. meridionalis than in males (Watling and Watling, 1976b); higher in M. edulis from waters of comparatively low salinity (Phillips, 1978); higher in oysters during winter than other seasons (Sankaranarayanan et al., 1978); higher in bivalves collected from relatively turbulent waters with high suspended solids content (Raymont, 1972); and higher in mussels Perna canaliculus held at increasing water depths (Nielsen, 1974).
6.19 Lanthanum Limited data on lanthanum concentrations in molluscs indicate that tests of pteropods from the Red Sea contained lower concentrations than did pteropod tests from the South Atlantic Ocean, namely, 0.34-1.72 mg La/kg DW versus 5.28-6.09 mg La/kg DW (Turekian et al., 1973).
6.20 Lead Maximum lead concentrations—in mg Pb/kg DW—in excess of 450.0 mg/kg DW among field collections of molluscs were 452.0 in soft parts of a mussel, M. edulis planulatus; 827.0 in kidneys of the scallop, C. opercularis; 820.0 in soft parts of the clam, S. plana; 931.0 in soft parts of the gastropod, Acmaea digitalis; 1130.0 in digestive gland of S. plana; and 3100.0 in soft parts of M. edulis (Table 6.12). The elevated levels reported in some species were almost always positively associated with degree of industrial or other anthropogenic lead discharges to the biosphere (Bloom and Ayling, 1977; Eisler, 2000c; Eisler et al., 1978; Fowler and Oregioni, 1976; Graham, 1972; Phillips, 1978; Schulz-Baldes, 1973). In one case, lead concentrations in the common mussel, M. edulis, exceeded the World Health Organization food standard of 10.0 mg Pb/kg DW in 19 of the 22 locations sampled in Port Phillip Bay, Australia; stormwater runoff and tidal movements were contributory causes to elevated lead
238 Chapter 6 Table 6.12: Lead Concentrations in Field Collections of Molluscs Organism
Concentration
Reference
Abalone Muscle Viscera
0.33-0.39 FW 0.6-2.5 FW
1 1
Gastropod, Acmaea digitalis Shell Soft parts
<9.0 to 108.0 DW 7.5-931.0 DW
2 2
Cockle, Anadara trapezia; April 2000; soft parts; New South Wales, Australia
Max. 11.0 DW
87
Clam, Anodonta sp. Shell Soft parts
0.6 DW 1.2 DW
4 4
Giant squid, Architeuthis dux; 2001-2005; hepatopancreas Bay of Biscay Mediterranean Sea
0.4 DW 0.8 DW
108 108
Bivalves; 5 spp.; soft parts; East China Sea; August 2002
0.09 (0.003-0.24) FW
80
Mussel, Brachydontes pharaonis; Mersin coast, Turkey; 2002-2003; max. concentrations Muscle Gill Hepatopancreas
2.0 DW 8.0 DW 3.9 DW
74 74 74
Whelk, Buccinum undatum Shell Soft parts
0.5 DW 5.4 DW
4 4
Channeled whelk, Busycon canaliculatum Muscle Digestive gland
<0.7 to 0.9 FW 1.1-1.7 FW
6 6
Cockle, Cardium edule Shell Soft parts
0.4 DW 0.8 DW
4 4
4.7-15.6 DW
7
Cockle, Cerastoderma edule Soft parts Gulf of Gabes, Tunisia; February 2001 Gill Digestive gland
Max. 14.0 DW Max. 2.0 DW
a
73 73 (Continues)
Molluscs 239 Table 6.12: Organism Remainder Soft parts; 7 sites Chesapeake Bay; bivalves; 3 spp.; soft parts; 1979-1981 Scallop, Chlamys opercularis Soft parts Body fluid Mantle Gills Digestive gland Striated muscle Gonad and foot Kidneys Shell
Cont’d
Concentration
Reference
Max. 1.0 DW 0.13-1.1 DW
73 73
5.0 (0.6-27.0) DW
26
12.0 DW 1.1 DW 1.0 DW 2.1 DW 10.2 DW 0.6 DW 2.5 DW 827.0 DW 0.6-1.7 DW
8 8 8 8 8 8 8 8 4
Mussel, Choromytilus meridionalis; soft parts
2.0-5.0 DW
9
Oyster, Crassostrea commercialis; soft parts
0.3-1.3 FW
10
0.1-4.5 FW 1.0 DW 3.0-37.0 DW
11 12 75
Pacific oyster, Crassostrea gigas Soft parts Soft parts Soft parts; China; November 2003; contaminated sites Oyster, Crassostrea corteziensis; soft parts; Gulf of California; 1999-2000 American oyster, Crassostrea virginica Soft parts San Antonio Bay, Texas Galveston Bay, Texas; 1992-1993; summer vs. winter and spring United States East coast United States Gulf coast Pensacola, Florida; 2003-2004 Mississippi estuaries United States Atlantic Ocean coast Savannah, Georgia; 2000-2001 Shell Soft parts
3.4 DW
a
102
<0.8 DW 1.0-1.5 DW vs. 0.3-0.5 DW
13 63
<0.1 to 0.5 DW 0.1-3.5 DW Max. 0.42 FW 0.63-1.6 FW 0.1-2.3 FW
14 14 90 15 16
<1.5 to 4.0 DW 35.9-40.9 FW <1.0 DW
94 17 18 (Continues)
240 Chapter 6 Table 6.12: Cont’d Organism
Concentration
Limpet, Crepidula fornicata Shell Soft parts
0.4 DW 3.9 DW
Mussel, Elliptio buckleyi; soft parts; Turkey
Reference 4 4
0.13-0.68 (0.08-0.96) FW
76
<10.0 DW 10.1-20.0 DW 21.0-30.0 DW 32.2 DW
67 67 67 67
0.07-0.09 FW
64
0.1 DW 0.6-1.5 DW
89 89
Abalone, Haliotis rufescens Digestive gland Remaining tissues
9.0-40.0 DW <0.1 DW
20 20
Periwinkle, Littoraria scabra; soft parts; Tanzania Industrialized sites; 1998 vs. 2005 Reference site; 2005
8.2 DW vs. 1.6 DW 0.8 DW
96 96
Limpet, Littorina littorea Soft parts Digestive gland and gonad Shell Soft parts Soft parts Soft parts
4.0-15.0 DW 3.7-10.0 DW 28.8-41.5 DW <0.1 to 2.8 FW 3.0 DW 19.0 (3.7-70.0) DW
21 21 21 22 23 7
0.56 FW 34.0 (15.0-61.0) DW 0.7-1.5 FW 0.2-8.5 DW
24 7 25 88
Razor clam, Ensis siliqua; shell; 23 stations; west coast of England 5 stations 14 stations 3 stations 1 station Greenland; 5 spp.; soft parts; 1978-1993 Gulf of Mexico; Coatzacoalcos estuary; 2005-2006; soft parts Asiatic clam, Corbicula fluminea Carolina marsh clam, Polymesoda caroliniana
Baltic clam, Macoma balthica Whole Soft parts Soft parts Soft parts; 1996-1997; Gulf of Gdansk
a
(Continues)
Molluscs 241 Table 6.12:
Cont’d
Organism
Concentration
Clam, Macoma mitchelli; whole
0.28 FW
24
Hardshell clam, Mercenaria mercenaria Soft parts Soft parts Soft parts Shell Soft parts
0.5 (0.1-7.5) FW 1.9 (<0.1 to 8.6) DW 18.0 DW 0.4 DW 3.5 DW
11 27 4 4 18
Bivalve, Mesidotea entomon; soft parts
0.3-1.5 FW
25
Mexico; Sinaloa; 2004-2005; soft parts; rainy season vs. dry season Oyster, Crassostrea corteziensis Mussel, Mytella strigata Clam, Megapitaria squalida
7.7 DW vs. 8.8 DW 4.5 DW vs. 6.3 DW 6.6 DW vs. 8.4 DW
99 99 99
Mussel, Modiolus demissus; soft parts
3.2 DW
18
Horse mussel, Modiolus modiolus Shell Soft parts Mantle and gills Muscle Gonad Gut and digestive gland Norway; 2007 Kidney Digestive gland Gills Gonad Muscle Total soft parts Molluscs North America; 18 commercial species; edible tissues 4 spp. 12 spp. 2 spp. Korea; edible tissues East coast South coast West coast Soft parts; 12 spp.
1.9 DW 23.0-42.0 DW 18.0 DW 7.5 DW 25.0 DW 22.0 DW
Reference
a
4 4 4 4 4 4
44.5 (16.0-85.0) FW 0.88 (0.16-2.2) FW 0.23 (0.05-0.49) FW 0.15 (0.05-0.29) FW 0.12 (0.04-0.32) FW 3.3 (1.4-6.6) FW
98 98 98 98 98 98
0.2-0.5 FW 0.5-0.7 FW 0.7-0.9 FW
28 28 28
0.59 (0.25-1.2) FW 1.25 (0.32-3.2) FW 0.98 (0.11-3.8) FW 0.04-1.8 FW
1 1 1 29 (Continues)
242 Chapter 6 Table 6.12: Cont’d Organism
Concentration
Morocco; 2001; clams; soft parts Scrobicularia plana Cerastoderma plana
11.0 DW 1.0 DW
Morocco; 2004-2005; soft parts Mussel, Mytilus galloprovincialis Clam, Venerupis decussatus Pacific oyster, Crassostrea gigas
9.6 (0.5-34.2) DW 4.1 (1.2-6.7) DW 4.2 (1.2-7.4) DW
95 95 95
Clam, Mulinia lateralis; whole
0.02 FW
24
Softshell clam, Mya arenaria Soft parts Soft parts Whole
0.1-10.2 FW 6.6-7.6 DW 0.3 FW
16 30 24
Mussel, Mytilus californianus Soft parts Near urban areas Near rural areas United States West coast Shell Soft parts Digestive gland
8.0 DW 0.3-0.8 DW 0.1-12.0 DW <9.0 to 19.4 DW <2.2 to 23.4 DW 2.4-38.0 DW
31 31 14 2 2 36
<9.0 to 21.2 DW <2.2 to 7.9 DW 1.9-6.4 DW 0.4 DW 0.01-0.43 DW 9.1 DW
2 2 33 4 104 4
1.9-8.8 DW <0.4 to 9.5 DW 3.0-264.0 DW 54.0 (30.0-105.0) DW 13.0 DW
14 14 34 7 106
Common mussel, Mytilus edulis Shell Soft parts Soft parts Shell Shell; Baltic Sea; 2005; 12 sites Soft parts Soft parts United States West coast United States East coast Scandinavia Looe estuary, England Scheldt estuary, Europe; March 2000 Netherlands; summer 2002 Puget Sound, Washington state Anaheim Bay, California Port Phillip Bay, Australia Scotland New Zealand
Max. 9.0 DW 1.5-2.2 DW 33.0 DW up to 10.0 FW <0.2 to 5.5 FW 12.0 (3.0-25.0) DW
Reference
a
101 101
77 35 31 36, 37 22 39 (Continues)
Molluscs 243 Table 6.12: Organism Florida Germany Norway England Spain Greenland Mantle Gills Muscle Visceral mass Intestine Foot Gonads Shell Foot Gills Stomach Mantle Muscle Shell Soft parts Soft parts Hepatopancreas San Diego Harbor Offshore Mussel, Mytilus edulis aoteanus Soft parts Gill Visceral mass Intestine Gonad Other tissues Mussel, Mytilus edulis planulatus Soft parts Soft parts June January Soft parts Pacific blue mussel, Mytilus edulis trossulus; 2004; soft parts; Adak Island, Alaska; 5 sites
Cont’d
Concentration
Reference
0.02-0.04 FW 2.0-6.0 DW 2.0-3100.0 DW 9.0 DW; 0.5-3.0 FW 2.0-15.0 DW 2.0-21.0 FW <5.0 DW 36.0 DW <5.0 DW 26.0 DW 69.0 DW <5.0 DW 7.0 DW <5.0 DW Max. 8.2 DW Max. 32.6 DW Max. 22.9 DW Max. 14.5 DW Max. 17.8 DW Max. 81.0 DW Max. 18.9 DW 30.0-138.0 DW
38 66 66 66 66 66 39 39 39 39 39 39 39 39 40 40 40 40 40 40 40 41
6.9-22.0 DW <2.3 to 13.0 DW
42 42
12.0 DW 36.0 DW 26.0 DW 69.0 DW 7.0 DW <5.0 DW
39 39 39 39 39 39
3.1-452.0 DW
19
4.1 FW 0.5 FW 0.4-1.2 DW
43 43 3
Max. 47.6 FW; 1.2-5.1 DW
84
a
(Continues)
244 Chapter 6 Table 6.12: Cont’d Organism Mussel, Mytilus galloprovincialis Soft parts; Venice lagoon, Italy; 2005-2006; San Giuliano vs. Sacca Sessola April July October February Soft parts Soft parts Soft parts; Adriatic Sea, Italy; 2 sites Soft parts; Adriatic Sea; 2001-2005; winter vs. summer Soft parts; Marmara Sea, Turkey; 2005 Soft parts; Gulf of Gemlik, Turkey; 2004 Soft parts; Izmir Bay, Turkey; 2004; near shore vs. mid-bay Soft parts; 2002-2003; Aegean Sea, Turkey Soft parts; 2001-2002; Adriatic Sea; summer vs. winter Industrialized sites Reference site Soft parts; May 2003; NW Mediterranean Sea Near Genova, Italy Near Marseille, France Near Barcelona, Spain Soft parts; Sardinia; 2004 vs. 2006 Soft parts; 1991-2005; Balearic Islands; western Mediterranean Sea; Port of Mahon Mantle vs. gills; 2004-2006; Saronikos Gulf of Greece; max. mean concentrations; contaminated sites Summer Autumn Winter Spring Soft parts; Mediterranean Sea; 3 sites; summers 2004-2005 Mussel, Mytilus viridis; soft parts
Concentration
Reference
4.3 DW vs. 3.2 DW 1.5 DW vs. 1.1 DW 2.3 DW vs. 1.9 DW 3.6 DW vs. 3.2 DW 13.4 FW 21.5 DW 0.10-0.16 FW 1.2-2.0 DW vs. 0.2-1.0 DW
91 91 91 91 44 45 103 109
0.82 FW 0.5 DW
72 112
0.4 DW vs. 0.08 DW
105
0.98 (0.49-1.7) FW
78
1.9-3.1 DW vs. 0.8-11.5 DW 1.6 DW vs. 1.6 DW
83 83
1.9-29.8 DW 2.2-4.0 DW 1.8-38.5 DW 18.0 DW vs. 7.5 DW 10.0 (3.3-18.6) DW
69 69 69 107 70
10.5 FW vs. 21.0 FW 5.4 FW vs. 8.7 FW 0.38 FW vs. 9.8 FW 0.34 FW vs. 0.95 FW 1.0-1.4 DW
71 71 71 71 93
1.1-12.7 DW
46
a
(Continues)
Molluscs 245 Table 6.12:
Cont’d
Organism
Concentration
Whelk, Nucella lapillus Shell Soft parts Soft parts
0.5 DW 4.9 DW 1.9-7.1 DW
Octopus, Octopus sp.; whole
1.0 FW
Octopus, Octopus vulgaris Portugal; 1999-2002; 3 sites Digestive gland Branchial heart Digestive gland; Portugal; 2005-2006; northwest region vs. south coast Whole Nuclei Mitochondria Lysosomes Microsomes Squid, Ommastrephes illicebrosa; whole
Reference 4 4 7 47
4.8-7.2 DW 3.1-10.0 DW
110 110
2.4 (1.5-4.1) DW vs. 4.8 (3.0-7.2) DW 5.4 (4.5-22.0) DW vs. 8.6 (2.7-16.0) DW 6.4 (1.9-31.0) DW vs. 12.0 (4.7-21.0) DW 3.2 (1.4-5.7) DW vs. 10.0 (2.4-26.0) DW 6.4 (1.5-25.0) DW vs. 7.0 (2.5-34.0) DW
100 100 100 100 100
5.0 AW
48
1.4-84.0 DW
19
2.0 FW 0.6 FW 0.5-1.9 DW
43 43 3
0.2-2.3 DW 7.5 (2.1-17.3) DW
49 70
Oyster, Ostrea gigas; soft parts United States East coast United States Gulf coast
1.4 DW 0.1-0.3 DW
14 14
Oyster, Ostrea sinuata Soft parts Heart Other tissues
10.0 DW 15.0 DW 5.0 DW
39 39 39
Oyster, Ostrea angasi Soft parts Soft parts June January Whole European flat oyster, Ostrea edulis Soft parts Soft parts; 1991-2005; Balearic Islands; western Mediterranean Sea; Port of Mahon
a
(Continues)
246 Chapter 6 Table 6.12: Cont’d Organism
Concentration
Limpet, Patella candei gomesii; soft parts; 2007; Azores Near hydrothermal vent Reference site
0.24-0.35 DW 0.30-0.94 DW
Reference
97 97
Limpet, Patella coerulea; soft parts
<7.0 to 95.6 DW; <1.7 to 27.5 FW
Gastropod, Patella piperata; Canary Islands, Spain; soft parts; March-April 2003
1.6 (0.3-10.2) DW
79
5.1-38.0 DW 9.5 DW 7.9 DW 46.0 DW 32.0 DW
7 23 51 4 4
<0.1 to 1.0 FW 2.0 DW 0.9 DW 0.7 DW 0.8 DW 3.9 DW 0.2 DW 1.7 DW 159.0 DW 44.0 FW 8.3 DW 17.0 DW 1.7 DW 1.5-2.8 DW
22 8 8 8 8 8 8 8 8 52 4 4 4 4
Limpet, Patella vulgata Soft parts Soft parts Soft parts Shell Soft parts Giant scallop, Pecten maximus Soft parts Soft parts Body fluid Mantle Gills Digestive gland Striated muscle Gonad and foot Kidney Kidney Soft parts Muscle Gut and digestive gland Mantle and gills Gonad Unwashed Washed Shell Norway; 2006 Digestive gland Kidney Muscle Gonad Total soft parts
31.0 DW 0.4 DW 0.6-2.4 DW 0.29 (0.17-0.50) FW 8.2 (4.0-12.4) FW <0.01 (<0.01 to 0.02) FW 0.07 (0.05-0.09) FW 0.12 (0.09-0.14) FW
a
5
4 4 4 98 98 98 98 98 (Continues)
Molluscs 247 Table 6.12:
Cont’d
Organism
Concentration
Scallop, Pecten novaezelandiae Stomach Gonad Abductor muscle Soft parts Soft parts Gill Intestine Kidney Foot Gonad
1.2 FW 0.3 FW 0.5 FW 1.1 FW 16.0 DW 52.0 DW 28.0 DW 137.0 DW 14.0 DW 78.0 DW
29 29 29 29 39 39 39 39 39 39
0.5 FW 0.25 FW 0.09 FW
86 86 86
Green mussel, Perna viridis India; January 2002; 28 sites; soft parts Small Medium Large Hong Kong; juveniles vs. adults Reference site Soft parts Byssus Polluted site Soft parts Byssus
Reference
3.7 DW vs. 3.3 DW 5.4 DW vs. 7.3 DW
111 111
4.2 DW vs. 7.0 DW 4.9 DW vs. 7.7 DW
111 111
Pearl oyster, Pinctada fucata Gills Mantle Digestive gland Foot
3.2 DW 1.4 DW 2.1 DW 1.3 DW
113 113 113 113
Clam, Pitar morrhuana; soft parts
11.1-29.4 DW
53
Scallop, Placopecten magellanicus Soft parts Muscle Gonad Visceral mass
3.6 DW <0.4 to 1.7 FW <0.4 to 1.5 FW 0.45-1.6 FW
54 55 55 55
Clam, Protothaca staminea Shell Soft parts
<9.0 DW 5.2 DW
2 2
Clam, Rangia cuneata Soft parts Whole
1.1 DW 0.37 FW
56 24
a
(Continues)
248 Chapter 6 Table 6.12: Cont’d Organism
Concentration
Manila clam, Ruditapes philippinarum Soft parts; Korea; 2002-2003 Females vs. males Postspawn vs. prespawn Jiaozhou Bay, China; sediments vs. soft parts; November 2004 Bohai Sea; soft parts
0.78 DW vs. 0.73 DW 1.1 DW vs. 0.76 DW 34.8 DW vs. 0.31-1.0 DW
68 68 81
0.13-0.33 DW
82
8.0-327.0 DW 189.0 (62.0-473.0) DW
57 7
12.0-21.0 DW 37.8 DW 3.7 DW not detectable
58 58 58 58
234.0-828.0 DW 1130.0 DW 90.0 DW 8.0 DW 29.0 DW 9.0 DW 74.0 DW
58 58 58 58 58 58 58
402.0 DW 35.0 DW
58 58
486.0 DW 20.0 DW
58 58
94.0 (26.0-296.0) DW 384.0 (235.0-983.0) DW
59 59
1.4 DW <0.1 DW <0.1 DW
85 85 85
<0.1 DW 0.6 DW
85 85
Clam, Scrobicularia plana Soft parts Soft parts Camel estuary, England Soft parts Digestive gland Mantle and siphons Remaining tissues Gannel estuary, England Soft parts Digestive gland Mantle and siphons Foot and gonads Gills and palps Adductor muscles Kidneys Transferred from Camel estuary to Gannel estuary for 352 days Digestive gland Remaining tissues Transferred from Gannel estuary to Camel estuary for 352 days Digestive gland Remaining tissues Tamar estuary, England Soft parts Digestive gland Common cuttlefish, Sepia officinalis Egg Eggshell Embryo Yolk Hatchlings Whole Cuttlebone
Reference
a
(Continues)
Molluscs 249 Table 6.12: Organism Juveniles, age 1 month Whole Digestive gland Cuttlebone Immatures, age 12 months Whole Digestive gland Cuttlebone Adults, age 18 months Whole Digestive gland Cuttlebone
Cont’d
Concentration
Reference
<0.1 DW 1.6 DW 0.5 DW
85 85 85
0.65 DW 2.4 DW 0.9 DW
85 85 85
0.2 DW 2.2 DW 0.3 DW
85 85 85
Squid, Sepia sp.; whole
0.4 FW
47
Spain; Tarragona coast; commercial species; edible portions
Max. 2.4 FW
65
Clam, Spisula sp.; soft parts; United States Delaware Massachusetts
7.4 FW 1.2 DW
60 60
Squid Flesh Flesh with skin Viscera Pen
1.3 DW 2.0 DW 2.7 DW 2.3 DW
61 61 61 61
Gastropod, Strombus pugilis Shell Muscle Soft parts
88.0 (79.0-98.0) DW 8.0 (7.3-8.6) DW 24.0 DW
62 62 62
1.9-152.0 DW
19
Chiton, Sypharochiton pellis-serpentis; soft parts Clam, Tapes semidecussata Shell Soft parts
<9.0 DW <2.0 DW
Gastropod, Thais lapillus Soft parts Soft parts Digestive gland and gonad Shell
Max. 27.0 DW 3.9-19.6 DW 4.2-11.0 DW 28.4-44.9 DW
a
2 2 23 21 21 21 (Continues)
250 Chapter 6 Table 6.12: Cont’d Organism
Concentration
Clam, Trivela mactroidea; Venezuela; 2002; 14 sites; soft parts
<1.5 to 4.9 DW
92
1.1 FW 2.6 FW
60 60
Clam, Venus mercenaria; soft parts Delaware Massachusetts
Reference
a
Values are in mg Pb/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Won, 1973; 2, Graham, 1972; 3, Harris et al., 1979; 4, Segar et al., 1971; 5, Shiber and Shatila, 1978; 6, Greig et al., 1977; 7, Bryan and Hummerstone, 1977; 8, Bryan, 1973; 9, Watling and Watling, 1976b; 10, Mackay et al., 1975; 11, Pringle et al., 1968; 12, Watling and Watling, 1976a; 13, Sims and Presley, 1976; 14, Goldberg et al., 1978; 15, Harvey and Knight, 1978; 16, Shuster and Pringle, 1968; 17, Ferrell et al., 1973; 18, Valiela et al., 1974; 19, Bloom and Ayling, 1977; 20, Anderlini, 1974; 21, Ireland and Wooton, 1977; 22, Topping, 1973; 23, Butterworth et al., 1972; 24, White et al., 1979; 25, Miettinen and Verta, 1978; 26, Di Giulio and Scanlon, 1985; 27, Genest, 1979; 28, Hall et al., 1978; 29, Nielsen and Nathan, 1975; 30, Eisler, 1977b; 31, Chow et al., 1976; 32, Alexander and Young, 1976; 33, Schulz-Baldes, 1973; 34, Phillips, 1978; 35, Schell and Nevissi, 1977; 36, Phillips, 1976a; 37, Phillips, 1976b; 38, Horvath et al., 1972; 39, Brooks and Rumsby, 1965; 40, Talbot et al., 1976a; 41, Simpson, 1979; 42, Young et al., 1979; 43, Thomson, 1979; 44, Uysal, 1978a; 45, Fowler and Oregioni, 1976; 46, Bhosle and Matondkar, 1978; 47, Matsumoto et al., 1964; 48, Nicholls et al., 1959; 49, Fukai et al., 1978; 50, Hayashi, 1960; 51, Preston et al., 1972; 52, George et al., 1980; 53, Eisler et al., 1978; 54, Reynolds, 1979; 55, Greig et al., 1978; 56, Sims and Presley, 1976; 57, Luoma and Bryan, 1978; 58, Bryan and Hummerstone, 1978; 59, Bryan and Uysal, 1978; 60, Craig, 1967; 61, Horowitz and Presley, 1977; 62, Lowman et al., 1966; 63, Jiann and Presley, 1997; 64,Dietz et al., 1996; 65, Schuhmacher et al., 1990; 66, Jenkins, 1980; 67, Pearce and Mann, 2006; 68, Ji et al., 2006; 69, Zorita et al., 2007; 70, Deudero et al., 2007; 71, Vlahogianni et al., 2007; 72, Keskin et al., 2007; 73, Machreki-Ajmi and Hamza-Chaffai, 2006; 74, Karayakar et al., 2007; 75, Liu and Deng, 2007; 76, Yarsan et al., 2007; 77, Mubiana and Blust, 2006; 78, Sunlu, 2006; 79, Bergasa et al., 2007; 80, Huang et al., 2007; 81, Li et al., 2006; 82, Liang et al., 2004a; 83, Scancar et al., 2007; 84, Burger and Gochfeld, 2006; 85, Miramand et al., 2006; 86, Sasikumar et al., 2006; 87, Burt et al., 2007; 88, Sokolowski et al., 2007; 89, Ruelas-Inzunza et al., 2007; 90, Karouna-Renier et al., 2007; 91, Nesto et al., 2007; 92, LaBrecque et al., 2004; 93, Lafabrie et al., 2007; 94, Kumar et al., 2008; 95, Maanan, 2008; 96, De Wolf and Rashid, 2008; 97, Cunha et al., 2008; 98, Julshamn et al., 2008; 99, Frias-Espericueta et al., 2008; 100, Raimundo et al., 2008; 101, Anajjar et al., 2008; 102, Ruelas-Inzunza and Paez-Osuna, 2008; 103, Conti et al., 2008; 104, Protasowicki et al., 2008; 105, Kucuksezgin et al., 2008; 106, Wepener et al., 2008; 107, Schintu et al., 2008; 108, Bustamante et al., 2008; 109, Fattorini et al., 2008; 110, Napoleao et al., 2005; 111, Nicholson and Szefer, 2003; 112, Unlu et al., 2008; 113, Jing et al., 2007.
concentrations in mussels (Talbot et al., 1976a). Proposed lead criteria to protect human health include less than 5.0 mg Pb/kg DW in marine mollusks (Kucuksezgin et al., 2008), less than 1.5 mg Pb/kg FW in seafood products (Julshamn et al, 2008), less than 1.0 mg Pb/kg FW diet (Glynn et al., 2003; Ruelas-Inzunza et al., 2007), less than 1.5 mg Pb/kg DW diet (Unlu et al., 2008), and less than 0.5 mg Pb/kg FW in molluscan soft tissues (Burger and Gochfeld, 2006; Huang et al., 2007). High lead concentrations were especially common in bivalves collected near industrialized and populated areas subject to continual atmospheric fallout of lead from automobile exhaust during the period preceding wide-scale use of lead-free gasoline. In general, shellfish collected near sewer outfalls, in regions near heavy vehicular traffic, and in proximity to bridges coated with lead-based paints, had especially high lead burdens (Eisler, 2000c;
Molluscs 251 Graham, 1972). Mytilus and Acmaea, two organisms that live on and feed from rock surfaces in the intertidal zone, had comparatively elevated lead content; incomplete rinsing during high tides may be a contributing factor in specimens living near point sources of lead contamination (Graham, 1972). Mussels from the most impacted zones showed enlarged lysosomes accompanied by reduced labilization period of lysosomal membranes, indicating disturbed health (Zorita et al., 2007). In general, highest accumulations of lead in bivalve tissues were in kidney, gills, and digestive gland, and lowest concentrations in gonads, mantle and muscle (Table 6.12). Accumulation studies with M. edulis demonstrated that kidney contained 50-70% of the total lead while accounting for only 6-8% of the total biomass (Schulz-Baldes, 1973, 1974). Similar distributions were found in scallops (Brooks and Rumsby, 1965; Bryan, 1973), oysters (Pringle et al., 1968), and cephalopods (Heyraud and Cherry, 1979). Digestive gland was the major repository of lead in the abalone Haliotis rufescens (Stewart and SchulzBaldes, 1976) and in the mussel M. californianus (Alexander and Young, 1976). Newly formed carbonate fractions of M. edulis shell contained 6-10 times more lead than older carbonate fractions; however, older periostracum contains more lead than newly formed periostracum (Sturesson, 1976). Age and gender of the organism, and other variables influence lead content in tissues. For example, lead concentrations in soft parts of American oysters (C. virginica) were higher in smaller oysters than in larger ones, much lower than the lead burden of the surrounding sediments, and strongly correlated with iron content of the geochemical environment (Jiann and Presley, 1997). In the mussel, M. galloprovincialis, lead concentrations in soft parts decreased with increasing weight (Conti et al., 2008). Among various species of mussels, smaller and younger organisms had significantly higher lead uptake rates and lower loss rates than did larger, older conspecifics (Schulz-Baldes, 1973, 1974; Watling and Watling, 1976b); a similar pattern was observed among several species of bivalves from Greenland (Dietz et al., 1996). Lead concentrations were higher in soft tissues of male C. meridionalis than in females; lead was inversely related to iron concentrations in females and this may account for the depressed lead levels in females (Watling and Watling, 1976b). In M. californianus, lead concentrations were 1.7 times higher in testicular tissue than in ovarian tissue, although no sex-related differences were documented in lead content of digestive gland or muscle (Alexander and Young, 1976). Temperature of ambient seawater in the 10-18 C range made little difference in lead content in tissues of M. edulis (Phillips, 1976a). However, salinity of the medium was significant and lead residues were higher in mussels from lower salinity waters (Mubiana and Blust, 2006; Phillips, 1976a,b, 1978). The higher lead concentrations in mussels from low salinity waters are not correlated with water lead concentrations; differences are attributed to the biological availability of lead, that exists mainly in particulate form in seawater (Phillips, 1978).
252 Chapter 6 Selectivity for lead and other metals among various molluscan species depends, in part, upon its availability in the environment, its chemical and physical properties, the kind and number of ligands available for chelation, its transportation and storage, and the stability of the complex formed. The relative toxicities of these compounds also play a prominent role (Pringle et al., 1968). For the clam S. plana, the biological availability of lead in the sediments is controlled mainly by the concentration of iron. The concentration of lead in S. plana may be predicted from the Pb/Fe ratio in acid extracts of surficial sediments (Luoma and Bryan, 1978). Mussels, M. edulis, show a linear relation between body burdens and lead in ambient seawater (Schulz-Baldes, 1973, 1974). However, Phillips (1976a,b) states that this relation is not valid for tetraethyllead salts owing to differences in uptake kinetics of this molecule and those of inorganic lead or other lead salts. Diet, seasonality, depth of collection, and presence of other metals salts affect lead accumulations. Among abalones, H. rufescens, substantial uptake via diet occurred after ingestion of algae Egretia laevigata pretreated in solutions containing 1.0 mg Pb/L; abalones accumulated up to 21.0 mg Pb/kg FW soft parts, almost wholly in digestive gland (Stewart and Schulz-Baldes, 1976). Among mussels, however, there was no significant difference in lead uptake between lead offered via diet (algae) or by way of the medium (Schulz-Baldes, 1974). Seasonal variations in lead content of bivalves are attributed to seasonal variations in phytoplankton trace metals (Bryan, 1973) or to high precipitation and attendant runoff rather than to local pollution (Fowler and Oregioni, 1976). Phillips (1976a) maintains that the trace metal content of individual mussels remains constant throughout the year and that weight (moisture) fluctuations produced much of the seasonality in mussel lead concentrations. Differences in lead content of cultured mussels P. canaliculus with depth of collection is a function of food availability and to the ratio of particulate to dissolved lead with increasing vertical concentration gradients. Either or both of these conditions could influence the bioavailability of lead and other metals with increasing depth (Nielsen, 1974). The concentrations of zinc, lead, and cadmium attained in mussels are consistent with a theory that no interactions occurred between these metals during uptake (Phillips, 1977a,b); however, Phillips cautions that this relation does not hold for all metals, especially copper. In green mussel, P. viridis, lead content in soft parts is positively correlated with cadmium and chromium burdens, as well as proximity to industrial sites (Sasikumar et al., 2006). Mussels are capable of acting as efficient, time-integrated indicators of lead and other metals over a wide range of environmental conditions, and are recommended as an alternative to the analysis of sediment and water (Phillips, 1976a,b,c 1977a,b,c, 1978). Fowler and Oregioni (1976) report that poor correlations between metals in mussel soft parts and metals in ambient seawater may arise from either of two conditions. First, filter feeders ingest particulates which could result in enhanced metal content during periods of high runoff; thus, metal concentrations in filtered seawater (used in some laboratory studies) may not be
Molluscs 253 representative of total metal available to mussels in their immediate biosphere. Second, metal uptake and excretion kinetics in mussels may be slow relative to short-term fluctuations in metal concentrations occurring in the water; thus, metal concentrations in mussels at any given point in time will not reflect exactly those measured in seawater sampled at the same time. Clearly, care should be taken when using Mytilus and other filter-feeding bivalves to infer metal concentrations in ambient waters. Many laboratory studies have been conducted to measure accumulation and loss of lead in various species of bivalves under controlled environmental conditions. At 0.01 mg Pb/L medium, there was no significant difference in lead uptake by M. edulis whether lead was offered via the diet or via the medium (Schulz-Baldes, 1974); the highest values recorded were in kidney (135.8 mg Pb/kg DW) after immersion for 63 days when compared to the start (10.0 mg Pb/kg DW kidney). For total mussel soft parts after 63 days immersed in seawater solutions containing 0.01 mg Pb/L, lead content was 18.3 mg Pb/kg DW versus 2.5 in controls. Schulz-Baldes (1974) showed that lead uptake was a linear function of lead concentrations in the medium for the first 40 days over the range of lead concentrations tested: 0.005, 0.01, 0.05, 0.1, 0.2, 0.5, 1.0, and 5.0 mg Pb/L. For all groups, lead burdens were similar at 0.26-0.31 mg Pb/kg daily, regardless of amount accumulated or route of administration (Schulz-Baldes, 1974). Mussels, M. galloprovincialis, exposed to 0.1 mg Pb/L for 60 days as Pb(NO3)2 had highest concentrations in gills, palps, and digestive gland, specifically in various lysosomal structures within these tissues (Dimitriadis et al., 2003). Remarkable lead accumulations of 12,840.0 mg Pb/kg DW soft parts were measured in M. edulis following exposure for 150 days in 0.5 mg Pb/L; controls contained 8.4 mg Pb/kg DW (Schulz-Baldes, 1972). Softshell clams, M. arenaria, in 0.014 mg Pb/L, accumulated up to 2.9 mg Pb/kg FW soft parts in 6 weeks under ambient winter thermal regimes versus 0.68 mg Pb/kg FW in controls. At 0.07 mg Pb/L, Mya took up 13.3 mg Pb/kg FW soft parts under similar conditions (Eisler, 1977b). At summer thermal regimes, these values in Mya were about 5.6 mg Pb/kg FW soft parts after 14 days in 0.014 mg Pb/L and 17.3 in 7 days in 0.07 mg Pb/L (Eisler, 1977b). Hardshell clams, M. mercenaria, contained 70.0 mg Pb/kg FW soft parts after exposure for 20 weeks in 0.2 mg Pb/L (Shuster and Pringle, 1968). American oysters, C. virginica, held in seawater solutions containing 0.025 mg Pb/L for 5 weeks contained up to 17.0 mg Pb/kg FW soft parts; after 10 weeks, oysters had 35.1 mg Pb/kg FW (Shuster and Pringle, 1968, 1969). Higher nominal lead concentrations and increasing periods of exposure in the above studies were always associated with higher lead body burdens in oysters. In another study with American oysters, Zaroogian et al. (1979) showed significant accumulations after long-term exposure to extremely low lead concentrations. At ambient levels of 0.001 mg Pb/L, oyster tissues contained 6.6 mg Pb/kg DW soft parts after 20 weeks; for 0.0033 mg Pb/L, this value was 11.4 mg Pb/kg DW. In all studies, the oysters and their progeny appeared normal. Zaroogian et al. (1979) maintain that 85-90% of the lead added to seawater was detected in the particulate fraction. The remainder is suggested to occur in
254 Chapter 6 a complex inorganic and a chelated form in the soluble fraction. The adsorptive behavior of lead is probably strongly pH dependent. Thus, when the pH is lowered, lead could be released from the particulates and a shift might occur in the equilibrium between the chemical species of lead. This change in equilibrium could favor ionic lead in the oyster digestive tract that has a pH range of 5.5-6.0. Pearl oysters, P. fucata, exposed to 0.1 mg Pb/L for 72 h had 29.1 mg Pb/kg DW in gills (up from 3.2 mg Pb/kg DW at start), 11.1 mg Pb/kg DW in mantle (up from 1.4), 9.4 mg/kg DW in digestive gland (up from 2.1) and 9.8 mg Pb/kg DW in foot (up from 1.3 mg Pb/kg DW at start) (Jing et al., 2007). Mantle tissue was especially sensitive, with altered activities of antioxidant and immune enzymes (Jing et al., 2007). Mechanisms to account for lead uptake and retention by molluscan soft tissues are proposed by Romeril (1971) and Bryan (1971). Uptake mechanisms, according to Romeril (1971), include adsorption of ions at membrane-water interfaces; absorption by active or passive diffusion of metal ions across semipermeable membranes into body fluids and subsequent distribution to other organs; and ingestion of ions with food or in combination with particulate matter or mucous, and absorption through the gut wall. Despite having no direct connection with the medium or intestine, the mussel kidney takes up lead most rapidly of all tissues and organs, presumably via the blood. It is likely that initial uptake is via gills and adductor muscle into the blood, with eventual deposition in the kidney. According to the last proposed mechanism of Romeril (1971), lead is taken up by stomach and digestive gland; however, gills accumulate lead rapidly, possibly owing to the high blood flow at that site. Bryan (1971) proposed three mechanisms for metals loss: excretion across the body surface or gills; excretion via the gut; and excretion via urine. It is probable that all three mechanisms are used by mussels in lead depuration. In general, alkyl leads are more toxic than inorganic lead compounds, and tetraalkyl leads are more toxic than trialkyl lead compounds. For example, adverse effects of lead on the survival of the common mussel, M. edulis, include 50% dead in 96 h at 0.1 mg tetraethyllead/L, 0.27 mg tetramethyllead/L, 0.5 mg trimethyllead/L, 1.1 mg triethyllead/L (Maddock and Taylor, 1980), and 0.5 mg inorganic lead/L for mussel larvae (USEPA, 1985b). Shell has been proposed as a suitable indicator of lead exposure in the Akoya pearl oyster, Pinctada imbricata (MacFarlane et al., 2006). Under controlled conditions, oysters were subjected to 0.18 mg Pb/L (as lead nitrate) for 9 weeks, or to two short term exposures of 0.18 mg Pb/L, namely, 3 weeks each, with an intervening depuration period of 3 weeks. Soft tissues after 9 week exposure had 539.0 mg Pb/kg DW; the 2 3 week exposure had 603.0 mg Pb/kg DW, and the controls 0.2 mg Pb/kg DW; for shell, these values were 249.0 mg Pb/kg DW, 207.0 mg/kg DW, and 6.0 mg Pb/kg DW, respectively. Lead accumulated in successively deposited nacreous layers of shell; patterns of deposition reflected the extent and frequency of lead insult (MacFarlane et al., 2006).
Molluscs 255
6.21 Lithium Shells of the common mussel, M. edulis, collected from the Baltic Sea in 2005 at 12 sites contained 0.29-3.48 mg Li/kg DW (Protasowicki et al., 2008).
6.22 Manganese Manganese concentrations in various molluscan tissues on a FW basis ranged from 0.5 to 110,000.0 mg Mn/kg; major sites of accumulation were in kidney concretions, kidney, shell, gill, and digestive gland (Table 6.13). In addition to tissue specific differences in ability to accumulate and retain manganese, other factors should be considered when interpreting manganese concentrations in field collections of molluscs. Elevated levels of manganese and other metals in flesh of mussels, for example, was linked to contamination from automobiles, small crafts, and to substrate composition, especially muddy substrates (Graham, 1972). It is generally acknowledged that mussels collected near industrialized port areas had higher manganese concentrations than did conspecifics collected some distance from these areas (Fowler and Oregioni, 1976; Sasikumar et al., 2006); however, manganese residues in mussels collected in Sweden showed little relation to proximity to known industrial areas (Phillips, 1978). Chemical availability of manganese to Swedish mussels is secondary to that of biological availability, and the latter is influenced by the presence of other metals in solution and water salinity (Phillips, 1978). Variations in manganese content of oyster shell and soft parts were attributed to fluctuations in water salinity; residues in shell (Rucker and Valentine, 1961) and soft tissues (Mubiana and Blust, 2006) being higher at lower salinities. Among common mussels, M. edulis, it seems that manganese is regulated in soft parts to some extent in waters of low salinity (Phillips, 1978). Seasonal variations in manganese content of molluscan tissues, as distinct from changes in thermal regimes, are documented (Bryan, 1973; Patel et al., 1973). In soft tissues of the green mussel, P. viridis, manganese concentrations were positively correlated with copper, iron, and nickel contents (Sasikumar et al., 2006). Soft tissues of the Baltic clam, M. balthica, collected from the Gulf of Gdansk in 1996-1997 had highest concentrations in autumn and spring, and lowest in winter (Sokolowski et al., 2007). The main source of manganese was suspended and deposited particles. Uptake was inhibited by increasing concentrations of iron in the immediate biosphere. Uptake was higher at increasing depths, which was a function of extractable manganese and iron in the sediments (Sokolowski et al., 2007). Diet is the major route of manganese accumulation in mussels; the role of seawater in manganese accumulation is minor when compared with food (Pentreath, 1973). Soluble chemical species of manganese were taken up by mussels more rapidly than particulate forms (Pentreath, 1973); the reverse was true for clams, D. trunculus (Orlando and Mauri, 1978).
256 Chapter 6 Table 6.13: Manganese Concentrations in Field Collections of Molluscs Organism
Concentration
Reference
Gastropod, Acmaea digitalis Shell Soft parts
19.3-30.7 DW 24.5-25.1 DW
1 1
Gastropod, Aplysia benedicti Ctenidium Gonad Parapodia Hepatopancreas Buccal mass Intestine Gut content Shell
13.0-15.0 DW 14.0-21.0 DW 5.0-7.0 DW 4.0-7.0 DW 5.0-8.0 DW 5.0 DW 8.0 DW 101.0-106.0 DW
2 2 2 2 2 2 2 2
Giant squid, Architeuthis dux; Spain; 2001-2005 Hepatopancreas Oviduct gland Skin
2.3-2.7 DW 27.0 DW 9.0 DW
67 67 67
Scallop, Argopecten gibbus; kidney concretion
24,000.0 DW
3
Scallop, Argopecten irradians; kidney concretion
23,643.0 DW
3
Cockle, Austrovenus stutchburyi; soft parts; New Zealand; 1993-1994
2.0-12.0 DW
45
4.0-24.6 DW 3.1-21.5 DW 5.9-17.7 DW 12.4-208.5 DW 3.7-31.4 (0.1-62.1) DW
52 52 52 52 60
6.3-9.5 DW 2.4-8.4 DW 2.1-8.1 DW
61 61 61
Hydrothermal vent mussel, Bathymodiolus azoricus; mid-Atlantic Ridge 2002; 3 sites Gill Mantle Digestive gland Byssus threads Shell; 2001; 4 sites 2001; 5 sites Gill Mantle Digestive gland Whelk, Buccinum undatum Shell Soft parts
1.2 DW 1.7 DW
a
4 4 (Continues)
Molluscs 257 Table 6.13:
Cont’d
Organism
Concentration
Reference
Whelk, Busycon canaliculatum Muscle Digestive gland
2.4-3.5 FW 3.5-5.7 FW
5 5
Cockle, Cardium edule Shell Soft parts
2.0 DW 6.3 DW
4 4
Cockle, Cerastoderma edule; soft parts
6.2-44.6 DW
6
Scallop, Chlamys opercularis Shell Soft parts Body fluid Gills Mantle Digestive gland Striated muscle Unstriated muscle Gonad and foot Kidneys
17.0-18.0 DW 158.0 DW 2.0 DW 105.0 DW 18.6 DW 29.7 DW 4.0 DW 4.4 DW 12.5 DW 17,300.0 DW
4 7 7 7 7 7 7 7 7 7
Mussel, Choromytilus meridionalis Soft parts Soft parts
1.7 FW 9.0-11.0 DW
8 9
Scallop, Comptopallium radula; New Caledonia; October 2004 Soft parts Kidney
6.1 (2.8-8.7) DW 187.0 DW
56 56
Pacific oyster, Crassostrea gigas Soft parts Soft parts
0.9-16.0 FW 12.0-16.0 DW
10 9, 11
Oyster, Crassostrea gryphoides; soft parts
4.9 (4.2-5.7) FW
12
Oyster, Crassostrea margaritacea; soft parts
2.0 DW
11
Oyster, Crassostrea rhizophorae; soft parts; summer 2001; Brazil; contaminated estuary vs. reference site
28.1-60.9 DW; max. 81.9 DW vs. 33.9-50.0 DW; max. 67.8 DW
48
American oyster, Crassostrea virginica Soft parts Shell Soft parts
4.3 (0.1-15.0) FW 33.0-121.0 DW 24.0-51.0 DW
10 13 13
a
(Continues)
258 Chapter 6 Table 6.13: Cont’d Organism Soft parts; United States Gulf coast New England Chesapeake Bay October December Soft parts; Savannah, Georgia; 2000-2001 Shell Shell Soft parts Winter Summer Ovaries, mature Testes, mature Gills Winter Summer Mantle Winter Summer Adductor muscle
Concentration
Reference
5.9-41.9 DW 9.0-60.0 DW
14 15
30.0 DW 2.0 DW 17.0-54.0 DW
16 16 55
21.0-227.0 DW 505.0 DW
17 16
7.0-11.0 DW 38.6 DW 51.0-59.6 DW 4.6-7.3 DW
18 18 18 18
17.1 DW 38.6 DW
18 19
8.7 DW 17.0 DW 3.6-9.2 DW
18 18 18
Limpet, Crepidula fornicata Shell Soft parts
2.1 DW 17.0 DW
4 4
Clam, Donax serra; soft parts
0.84 FW
8
Gastropods Muscle Shell Viscera Operculum
370.0 AW 140.0 AW 23.0 AW 17,000.0 AW
Abalone, Haliotis midea; soft parts
0.27 FW
Periwinkle, Littoraria scabra; soft parts; Tanzania Industrial sites; 1998 vs. 2005 Reference site; 2005
300.0 DW vs. 50.0 DW 15.0 DW
58 58
Limpet, Littorina littorea Soft parts Digestive gland and gonad
18.6-59.8 DW 68.8-104.6 DW
20 20
a
19 19 19 19 8
(Continues)
Molluscs 259 Table 6.13: Organism Shell Soft parts with operculum
Cont’d
Concentration
Reference
5.5-8.3 DW 18.0-133.0 DW
20 6
19.0-24.0 DW 10.0-50.0 DW
6 51
Hardshell clam, Mercenaria mercenaria Shell Soft parts
1.5 DW 5.8 (0.7-29.7) FW
4 10
Clam, Meretrix lamarckii; soft parts
5.4 DW
21
Clam, Meretrix meretrix; soft parts
11.5 (3.3-27.6) FW
12
Mussel, Modiolus modiolus Shell Soft parts Mantle and gills Muscle Gonad Gut and digestive gland
20.0 DW 47.0-150.0 DW 160.0 DW 71.0 DW 49.0 DW 140.0 DW
Molluscs Edible tissues of 15 commercial species 5 spp. 2 spp. 2 spp. 3 spp. 3 spp. 3 spp. Edible tissues; 3 spp.; India; 2003
0.1-0.3 FW 0.3-0.5 FW 0.5-0.7 FW 0.8-2.0 FW 2.0-5.0 FW 6.0-8.0 FW 1.1-2.8 FW
22 22 22 22 22 22 54
1.5-10.4 FW
50
Morocco; 2004-2005; soft parts Mussel, Mytilus galloprovincialis Clam, Venerupis decussatus Pacific oyster, Crassostrea gigas
20.8 (8.7-34.8) DW 18.8 (12.1-27.8) DW 26.4 (5.3-38.9) DW
57 57 57
Softshell clam, Mya arenaria Soft parts Soft parts
29.0-70.0 DW 6.7 (0.1-29.9) FW
23 10, 24
Clam, Macoma balthica Soft parts Soft parts; 1996-1997; Gulf of Gdansk; age 3-4 years
Molluscs; 5 spp; soft parts; Chile, Strait of Magellan; September-December 2001; 17 stations
a
4 4 4 4 4 4
(Continues)
260 Chapter 6 Table 6.13: Cont’d Organism
Concentration
Mussel, Mytilus californianus Shell Soft parts Soft parts
8.4-14.2 DW 5.9-7.8 DW 2.5-17.0 DW
1 1 14
Mussel, Mytilus corscum; soft parts
7.7 DW
21
3.6 DW 23.4-74.4 DW 3.5 DW 9.3-45.8 DW 6.1-28.4 DW 21.0-22.0 DW
4 62 4 1 1 25
8.2-25.0 DW 8.9-18.0 DW 5.2-35.4 DW 4.9-91.7 DW 130.0 DW 2.5 FW Max. 32.0 DW
14 14 6 26 64 27 77
27.0 DW 2.0 DW 28.0 DW <1.0 DW 105.0 DW <1.0 DW 6.0 DW <1.0 DW
28 28 28 28 28 28 28 28
3.5-12.3 DW
29
11.2 DW 8.9 DW 7.8 DW 7.1 DW
29 29 29 29
3.6 FW; max. 47.6 FW; 3.0-36.0 DW
37
Common mussel, Mytilus edulis Shell Shell; Baltic Sea; 2005; 12 sites Soft parts Shell Soft parts Soft parts Soft parts United States West coast United States East coast Looe estuary, England Scandinavia Scheldt estuary; March 2000 Tasmania Netherlands; summer 2002 Mussel, Mytilus edulis aoteanus Soft parts Mantle Gill Muscle Visceral mass Foot Gonad Shell Mussel, Mytilus edulis planulatus Whole Soft parts Dry weight 0.09 g Dry weight 0.39 g Dry weight 0.48 g Dry weight 0.69 g Pacific blue mussel, Mytilus edulis trossulus; soft parts; 2004; Adak Island, Alaska; 5 sites
Reference
a
(Continues)
Molluscs 261 Table 6.13: Organism Mussel, Mytilus galloprovincialis Soft parts; Venice lagoon, Italy; 2005-2006; San Giuliano vs. Sacca Sessola April July October February Soft parts Soft parts; Izmir Bay, Turkey; 2004; near shore vs. mid-bay Soft parts; Gulf of Gemlik, Turkey; 2004 Soft parts; Adriatic Sea; 2001-2002; summer vs. winter Industrialized sites Reference site Soft parts; Adriatic Sea; 2002-2005; winter vs. summer
Cont’d
Concentration
Reference
10.9 DW vs. 11.9 DW 7.4 DW vs. 5.3 DW 4.7 DW vs. 4.7 DW 9.2 DW vs. 8.7 DW 21.1 DW 4.5 DW vs. 2.7 DW
53 53 53 53 30 63
5.8 DW
68
9.6-10.9 DW vs. 14.0-29.8 DW 12.9 DW vs. 14.0 DW 10.2-16.4 DW vs. 4.4-12.7 DW
46 46 66
Mussel, Mytilus viridis Soft parts Soft parts
6.1 (4.2-8.1) FW 24.2-94.1 DW
12 31
Whelk, Nucella lapillus Shell Soft parts Soft parts and operculum
1.1 DW 12.0 DW 11.4-16.8 DW
Octopus, Octopus sp.; whole
0.6 FW
27
Octopus, Octopus vulgaris Portugal; 1999-2002; 3 sites Digestive gland Branchial heart Gill Muscle
4.6-6.0 DW 6.3-9.6 DW 5.0-7.1 DW 1.6-1.9 DW
67 67 67 67
Oyster, Ostrea angasi Soft parts Whole
2.5 FW 7.8-16.7 DW
27 29
Oyster, Ostrea edulis; soft parts Mediterranean Sea South Africa
6.1-85.0 DW 6.0 DW
32 11
a
4 4 6
(Continues)
262 Chapter 6 Table 6.13: Cont’d Organism
Concentration
Oyster, Ostrea sinuata Soft parts Mantle Gill Muscle Visceral mass Kidney Heart Shell
8.0 DW 4.0 DW 11.0 DW 2.0 DW 2.0 DW 2.0 DW 2.0 DW 1.0 DW
28 28 28 28 28 28 38 28
Limpet, Patella candei gomesii; soft parts; 2007; Azores Near hydrothermal vent Reference site
77.2-204.5 DW 6.8-20.9 DW
59 59
Limpet, Patella vulgata Shell Soft parts Soft parts Soft parts
8.6 DW 13.0 DW 5.4-36.0 DW 42.0 DW
4 4 6 33
Scallop, Pecten maximus Soft parts Muscle Gut and digestive gland Mantle and gills Unwashed Washed Gonad Unwashed Washed Shell Upper valve Lower valve Kidney Soft parts Excretory granules Kidney Soft parts Body fluid Mantle Gills Digestive gland
Reference
140.0 DW 22.0 DW 410.0 DW
4 4 4
200.0 DW 4.0 DW
4 4
31.0 DW 8.6 DW
4 4
12.0 DW 4.9 DW
4 4
3206.0 FW 110,000.0 FW 15,300.0 DW 107.0 DW 1.0 DW 8.8 DW 45.5 DW 15.6 DW
a
34 34 7 7 7 7 7 7 (Continues)
Molluscs 263 Table 6.13: Organism Striated muscle Unstriated muscle Gonad and foot Scallop, Pecten novae-zelandiae Soft parts Mantle Gill Muscle Visceral mass Kidney Foot Gonad Shell Green mussel, Perna viridis Soft parts; India; January 2002; 28 sites Hong Kong; juveniles vs. adults Reference site Soft parts Byssus Shell Polluted site Soft parts Byssus Shell Pen shell (bivalve), Pinna nobilis Kidney Byssus Hepatopancreas Gonads Soft tissues Shell Mantle Gill Byssus Hepatopancreas Muscle Body liquids Soft parts Muscle
Cont’d
Concentration 1.8 DW 0.8 DW 9.9 DW
Reference
a
7 7 7
110.0 DW 45.0 DW 353.0 DW 2.0 DW 24.0 DW 2660.0 DW 27.0 DW 5.0 DW 1.0 DW
28 28 28 28 28 28 28 28 28
5.05-5.24 FW
49
26.6 DW vs. 27.3 DW 13.2 DW vs. 24.2 DW 6.8 DW vs. 4.5 DW
68 68 68
26.6 DW vs. 43.0 DW 146.0 DW vs. 215.0 DW 9.0 DW vs. 8.2 DW
68 68 68
39,000.0 DW 950.0 DW 20.0 DW 10.0 DW 22,600.0 AW 34.0 AW 4070.0 AW 730.0 AW 820.0 AW 32,000.0 AW 1720.0 AW 1480.0 AW 5500.0 AW 4900.0 AW
35 35 35 35 36 36 36 36 36 36 36 36 37 37 (Continues)
264 Chapter 6 Table 6.13: Cont’d Organism Nervous system Intestine Gonads Hepatopancreas Byssus Byssus gland
Concentration
Reference
2700.0 AW 5200.0 AW 500.0 AW 3200.0 AW 4700.0 AW 4200.0 AW
37 37 37 37 37 37
Clam, Pitar morrhuana; soft parts
38.0-159.0 DW
38
Clam, Protothaca staminea Shell Soft parts
16.8 DW 11.5 DW
Manila clam, Ruditapes philippinarum Soft parts; Korea; 2002-2003 Females vs. males Postspawn vs. prespawn Jiaozhou Bay, China; sediments vs. soft parts; November 2004 Clam, Scrobicularia plana Looe estuary, England; soft parts Gannel estuary, England Soft parts Digestive gland Mantle and siphons Foot and gonads Camel estuary, England Soft parts Digestive gland Mantle and siphons Foot and gonads Transferred from Camel estuary to Gannel estuary for 352 days Digestive gland Remaining tissues Transferred from Gannel estuary to Camel estuary for 352 days Digestive gland Remaining tissues Tamar estuary, England Soft parts Digestive gland
37.7 DW vs. 32.7 DW 82.3 DW vs. 35.5 DW 433.0 DW vs. 27.5-67.6 DW
43.0 (25.0-100.0) DW
a
1 1
42 42 44
6
57.0-87.0 DW 190.0 DW 360.0 DW 15.0 DW
39 39 39 39
19.0-22.0 DW 79.8 DW 14.4 DW 4.0 DW
39 39 39 39
271.0 DW 134.0 DW
39 39
111.0 DW 36.0 DW
39 39
48.0 (18.0-97.0) DW 131.0 (72.0-183.0) DW
40 40 (Continues)
Molluscs 265 Table 6.13:
Cont’d
Organism
Concentration
Reference
Squid, Sepia esculenta; trunk
1.4 DW
Clam, Spisula solidissima; muscle
0.5-1.9 FW
Squid Flesh Flesh with skin Viscera Pen
6.5 DW 1.8 DW 3.3 DW 2.1 DW
41 41 41 41
Clam, Tapes decussata Shell Mantle Gill Muscle
3.0 AW 77.0 AW 61.0 AW 96.0 AW
36 36 36 36
Clam, Tapes semidecussata Shell Soft parts
24.7 DW 24.7 DW
1 1
Gastropod, Thais emarginata Shell Soft parts
5.3-6.0 DW 8.8 DW
1 1
Gastropod, Thais lapillus Soft parts Digestive gland and gonad Shell
5.9-17.3 DW 5.9-8.5 DW 2.8-4.2 DW
20 20 20
a
21 5
Values are in mg Mn/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Graham, 1972; 2, Patel et al., 1973; 3, Carmichael et al., 1979; 4, Segar et al., 1971; 5, Greig et al., 1977; 6, Bryan and Hummerstone, 1977; 7, Bryan, 1973; 8, Van As et al., 1973; 9, Watling and Watling, 1976b; 10, Pringle et al., 1968; 11, Watling and Watling, 1976a; 12, Bhatt et al., 1968; 13, Windom and Smith, 1972; 14, Goldberg et al., 1978; 15, Galtsoff, 1953; 16, Frazier, 1975; 17, Rucker and Valentine, 1961; 18, Galtsoff, 1942; 19, Lowman et al., 1970; 20, Ireland and Wooton, 1977; 21, Ishii et al., 1978; 22, Hall et al., 1978; 23, Eisler, 1977b; 24, Shuster and Pringle, 1968; 25, Simpson, 1979; 26, Phillips, 1978; 27, Eustace, 1974; 28, Brooks and Rumsby, 1965; 29, Harris et al., 1979; 30, Fowler and Oregioni, 1976; 31, Bhosle and Matondkar, 1978; 32, Fukai et al., 1978; 33, Preston et al., 1972; 34, George et al., 1980; 35, Ghiretti et al., 1972; 36, Chipman and Thommeret, 1970; 37, Papadopoulu, 1973; 38, Eisler et al., 1978; 39, Bryan and Hummerstone, 1978; 40, Bryan and Uysal, 1978; 41, Horowitz and Presley, 1977; 42, Ji et al., 2006; 43, Mubiana and Blust, 2006; 44, Li et al., 2006; 45, Peake et al., 2006; 46, Scancar et al., 2007; 47, Burger and Gochfeld, 2006; 48, Silva et al., 2006; 49, Sasikumar et al., 2006; 50, Espana et al., 2007; 51, Sokolowski et al., 2007; 52, Kadar et al., 2006; 53, Nesto et al., 2007; 54, Sankar et al., 2006; 55, Kumar et al., 2008; 56, Metian et al., 2008; 57. Maanan, 2008; 58, De Wolf and Rashid, 2008; 59, Cunha et al., 2008; 60, Cravo et al., 2008; 61, Cosson et al., 2008; 62, Protasowicki et al., 2008; 63, Kucuksezgin et al., 2008; 64, Wepener et al., 2008; 65, Bustamante et al., 2008; 66, Fattorini et al., 2008; 67, Napoleao et al., 2005; 68, Nicholson and Szefer, 2003; 68, Unlu et al., 2008.
266 Chapter 6 Manganese tends to accumulate in specific tissues, but this is not necessarily the same tissue among closely related species of molluscs. In mussels, for example, greatest manganese burdens were measured in stomach and digestive gland of M. edulis, and in musculature and digestive gland of M. californianus (Young and Folsom, 1967, 1973). In scallops, however, more than 90% of all manganese concentrated in kidney (Bryan, 1973); this was also the case in the clam D. trunculus (Orlando and Mauri, 1978). Age, sex, and body weight all modify manganese uptake and retention in molluscs. Unlike several other metals, manganese concentrations in American oysters were not related to age or to body weight (Downes, 1957). In other species, however, increasing tissue concentrations of manganese were associated with increasing body weight in clams P. morrhuana (Eisler et al., 1978). Females of C. meridionalis contained significantly more manganese than males of similar size; these differences were especially pronounced for zinc to which manganese was positively correlated (Watling and Watling, 1976b). Manganese uptake in molluscs under laboratory conditions is the subject of many studies. In one study, bivalves from the Baltic Sea did not accumulate manganese in tissues at ambient seawater concentrations of 5.0 mg Mn/L; at higher concentrations of 17.0-20.0 mg Mn/L, manganese accumulated in gonads, liver, and heart, accompanied by adverse metabolic effects, and finally death in about two months (Karpevich and Shurin, 1977). This contrasts sharply with known bioconcentration potential of field-collected molluscs. Thus, P. nobilis from Greek waters had manganese levels in soft tissues that were 180,000 times higher than seawater concentrations; lower concentration factors occurred in four other species of bivalves from the same area (Papadopoulu, 1973). In another study, Chipman and Thommeret (1970) found that high radioactivity from fallout 54Mn was generally related to high manganese content in the organism; however, the specific activity of 54Mn (the ratio of 54Mn to stable manganese) varied widely. The manganese content in molluscs was more than twice that of tunicates, though the total 54Mn radioactivity was the same in both groups. Scallops C. radula exposed to seawater containing 54Mn for 96 h had BCFs of 15 for total soft parts, and about 30 for gill, 30 for kidney, and 30 for digestive gland tissues (Metian et al., 2008). Gravid cuttlefish fed crabs radiolabeled with 54Mn over a 2 week period to determine rate of maternal transfer into eggs showed no significant transfer (Lacoue-Labarthe et al., 2008b).
6.23 Mercury Toxicological aspects of mercury and mercury compounds in coastal and offshore environments as a result of anthropogenic or natural processes have been reviewed extensively (D’Itri, 1972; Eisler, 2000, 2006; Friberg and Vostal, 1972; Gavis and Ferguson, 1972; Harriss, 1971; Holden, 1973; Jernelov et al., 1975; Keckes and Miettinen, 1972). Most of these authorities agree on five points. First, forms of mercury with relatively
Molluscs 267 low toxicity can be transformed into forms with very high toxicity through biological and abiotic processes. Second, uptake of mercury directly from seawater or through the diet returns mercury directly to upper level trophic consumers, including humans. Third, mercury uptake may result in genetic changes. Fourth, elevated levels of mercury in some marine fishes, such as tunas and swordfishes, emphasize the complexity of both natural mercury cycles and anthropogenic impacts on those cycles. Finally, human use of mercury should be curtailed because the difference between tolerable natural background levels of mercury and harmful effects in the environment is exceptionally small. Any review of mercury hazards in the marine environment should include the Minamata Bay incident in southwestern Kyushu, Japan. This extensively documented case (Eisler, 2006; Fujiki, 1963; Irukayama, 1967; Irukayama et al., 1961, 1962a,b; Kiyoura, 1963; Kurland et al., 1960; Matida and Kumada, 1969; Matida et al., 1972; Takevich, 1972; Tsubaki et al., 1967) reveals effects on humans of chronic discharges of low-level methyl mercury wastes into coastal waters. The source of the mercury was waste discharged from an acetaldehyde plant into Minamata Bay beginning in 1952. Several years later, the mercury levels in sediments near the plant outfall were about 2010.0 mg/kg FW; this decreased sharply with increasing distance from the plant. Sediments in Bay contained between 0.4 and 3.4 mg Hg/kg FW. Concentrations of mercury in fish and shellfish decreased with increasing distance from the point of effluence and appeared to reflect sediment mercury levels. Late in 1953, a severe neurological disorder was recognized among inhabitants of the Minamata Bay region. By 1956, the outbreak had reached epidemic proportions: 111 cases of poisoning were diagnosed by the end of 1960, and 41 deaths by August 1965. The poisoning was caused by eating fish and shellfish from the Bay and environs, except for 19 congenital cases in children born of mothers who had eaten the same diet. In addition to humans, cats and waterfowl living near the Bay succumbed to the disease. Laboratory cats and rats fed fish and shellfish collected from the Bay developed the same signs as animals spontaneously affected. Signs included cerebellar ataxia, constriction of visual fields, dysarthria, and, in congenital cases, disturbance of physical and mental development. Pathological findings included regressive changes in the cerebellum and the cerebral complexes. The clinicopathological features resembled alkylmercury poisoning. Abnormal mercury content, namely more than 30.0 mg Hg/kg FW, was measured in fish, molluscs, and muds from the Bay and in organs of necropsied humans and cats that died of the disease. Years after the waste discharge situation was corrected, fish and shellfish still contained levels of mercury considered hazardous to human health. Mercury levels in sediments vary widely and tend to be elevated near sewer outfalls (Klein and Goldberg, 1970), sludge disposal areas, and especially areas impacted by mercury wastes from industrial operations, such as Minamata Bay, Japan (Eisler, 2006; Irukayama, 1967). Vucetic et al. (1974) reported sediment mercury levels ranging from 0.13 to 1.5 mg/kg in the Adriatic Sea, and Williams and Weiss (1973) found 0.39 mg/kg in pelagic clays collected
268 Chapter 6 430 km southeast of San Diego, California. It is reported that mercury in seawater exists almost entirely bound to suspended particles (Jernelov et al., 1972), that the surface area of sediment granules is instrumental in determining final mercury content (Renzoni et al., 1973), that conversion and transformation occur in the surface layer of the sediment or on suspended organic particles in the water (Dean, 1972; Fagerstrom and Jernelov, 1972; Jernelov et al., 1972), and that mercury-containing sediments require many decades to purge themselves naturally to background levels (Langley, 1973). Mercury-sediment-water interactions affect uptake by marine biota. It is generally acknowledged that marine organisms feeding in direct contact with sediment have higher overall mercury levels than those feeding above the sediment-water interface (Klemmer et al., 1976). Bivalves accumulate mercury directly from seawater; however, mercury concentrations were higher with increasing water turbidity (Raymont, 1972). Molluscs sampled before and immediately after their substrate was extensively dredged had significantly higher mercury concentrations postdredging; elevated concentrations persisted for at least 18 months (Rosenberg, 1977). Some investigators report that mercury from point-source discharges, including sewer outfalls and chlor-alkali plants, is taken up by sediments; sediment mercury levels were eventually reflected by an increased mercury content in epibenthic fauna (Dehlinger et al., 1975; Hoggins and Brooks, 1973; Klein and Goldberg, 1970; Klemmer et al., 1973; Parsons et al., 1973; Takevich, 1972). Analysis of the effluent from the Hyperion sewer outfall in Los Angeles showed mercury content slightly below 0.001 mg/L (Klein and Goldberg, 1970). Concentrations of mercury in sediments near this outfall were as high as 0.82 mg/kg but decreased with increasing distance from the outfall; mercury levels in epibenthic fauna, including whelks and scallops, were also highest near the discharge and lowest at tens of kilometers distant. De Wolf (1975) found that mercury burdens in mussels along European coasts tend to reflect mercury levels in water and sediments to a greater degree than size of the mussel, season of collection, or position in the intertidal zone. Rapid accumulation of mercury, especially organomercury compounds, by representative species of molluscs is documented (Cunningham and Tripp, 1975a,b; Fang, 1973; Fowler et al., 1975; Irukayama et al., 1962a; Laumond et al., 1973; Nelson et al., 1976). Mercury accumulation from seawater by molluscs is modified by many factors, including the chemical form of mercury administered (Cunningham and Tripp, 1975a; Irukayama et al., 1962a); water temperature (Cunningham and Tripp, 1975b; Fowler et al., 1978; Lee et al., 1975; Nelson et al., 1977); salinity of the medium (Dillon, 1977; Dillon and Neff, 1978; Olson and Harrel, 1973); presence of selenium (Fowler and Benayoun, 1976a; Glickstein, 1978); sexual condition (Cunningham and Tripp, 1975b; De Wolf, 1975; Norum et al., 2005); tissue specificity (Cunningham and Tripp, 1975a; Dimitriadis et al., 2003; Fowler et al., 1975, 1978; Wrench, 1978); previous acclimatization to mercury salts (Dillon, 1977); season of year (De Wolf, 1975); soluble protein content of organism (Wrench, 1978); and presence of mercury-resistant strains of bacteria (Nelson et al., 1971; Colwell and Nelson, 1975;
Molluscs 269 Colwell et al., 1976; Sayler et al., 1975). Although certain trends were evident among individual modifiers, the results were not applicable to all groups of molluscs examined, with two exceptions. First, there was general agreement that organomercury compounds were more toxic and taken up more rapidly than were inorganic mercury compounds. Second, that salinity stress, especially abnormally low salinities, reduced significantly the survival time of mercury-exposed molluscs. Jones (1973), suggests that species adapted to a fluctuating estuarine environment could be more vulnerable to the added stresses of heavy metal pollution, including mercury, than species inhabiting more uniformly stable environments. Among cephalopods, total mercury concentrations are higher in the digestive gland than in the remaining tissues (Table 6.14). The percent of total body mercury burden of cephalopods that is organic is 67-93%; for digestive gland it is 3-16%, and for remaining tissues 84-98% (Bustamante et al., 2006). Marine molluscs, unlike certain species of marine mammals, teleosts, and elasmobranchs accumulate mercury only when the environment is contaminated with this element as a direct result of human activities. In every case reported wherein mercury levels in molluscan tissues exceed about 1.0 mg Hg/kg FW, this residue was associated with mercury pollution (Eisler, 1981, 2000, 2006; Table 6.14). In general, salts of mercury and its organic compounds were more toxic to marine biota during short term bioassays than were salts of other trace metals tested (Berland et al., 1976; Connor, 1972; Eisler and Hennekey, 1977; Kobayashi, 1971; Reish et al., 1976; Schneider, 1972). To oyster embryos, for example, mercury salts were more toxic than were salts of silver, copper, zinc, nickel, lead, cadmium, arsenic, chromium, manganese, or aluminum (Calabrese et al., 1973); to clam embryos, mercury was the most toxic metal tested, followed by silver, zinc, nickel, and lead, in that order (Calabrese and Nelson, 1974). Mercury was extremely toxic to Pacific oyster embryos with 50% mortality reported at 0.0057 mg Hg/L; embryos were relatively insensitive to mercury 24 h postfertilization and survival was affected by a variety of factors including selenium concentrations in the ambient medium (Glickstein, 1978). Juveniles of bay scallops, A. irradians, subjected to 0.04 mg Hg/L for 96 h contained 48.9 mg Hg/kg FW, a concentration far in excess of the 0.5 mg Hg/kg FW limit considered hazardous to human health (Nelson et al., 1976). A concentration of 0.089 mg Hg/L was lethal to juvenile bay scallops in 96 h (Nelson et al., 1976). Immunotoxic effects of mercuric chloride were reported in adult common mussels, M. edulis after exposure for 7 days at 0.21 mg Hg/L with 29% dead in 21 days; no deaths or immunotoxic effects occurred at 0.02 mg Hg/L and lower (Duchemin et al., 2008). Two studies, both on adult American ousters, C. virginica, are worth emphasizing. (Cunningham and Tripp, 1973; Kopfler, 1974). Cunningham and Tripp (1973) held oysters in seawater containing 0.01 mg Hg/L as mercuric acetate. After 45 days the total body mercury concentration of exposed oysters was 28.0 mg Hg/kg FW versus less than 0.02 mg Hg/kg FW in control oysters. Mercury burden in exposed oysters dropped to 18.0 mg/kg by
270 Chapter 6 Table 6.14: Mercury Concentrations in Field Collections of Molluscs Organism
Concentration
Abalone Muscle Viscera
0.12 FW 0.13 FW
Reference 1 1
Aleutian Islands; 2004-2005; edible portions; 6 spp.
0.010-0.038 FW; max. 0.096 FW
Clam, Anadara tuberculosa; soft parts
0.02-0.1 FW
2
Clam, Anodonta cygnea; soft parts; United Kingdom Southampton area Chertsey area
0.07 DW 0.76 DW
3 3
Giant squid, Architeuthis dux; 2001-2005 Hepatopancreas Branchial heart Muscle
0.47-1.6 DW 2.2 DW 2.4 DW
77 77 77
4.6 DW 4.4 DW 0.8 DW 0.8 DW
69 69 69 69
2.4 DW 4.1 DW 0.4 DW 0.2 DW
69 69 69 69
1.3 DW 1.0 DW 0.3 DW 0.2 DW
69 69 69 69
2.4-8.2 DW 0.27-0.44 DW 2.2-12.5 DW 1.6-5.1 DW
67 67 67 67
Mussel, Bathymodiolus azoricus Mid-Atlantic Ridge; hydrothermal vent fields; 2001 840 m deep Digestive gland Gills Mantle Foot 1700 m deep Digestive gland Gills Mantle Foot 2300 m deep Digestive gland Gills Mantle Foot Mid-Atlantic Ridge; 3 sites; 2002 Gill Mantle Digestive gland Byssus threads Bivalves and gastropods; 5 commercial spp.; edible portions
0.04 FW
a
65
4 (Continues)
Molluscs 271 Table 6.14:
Cont’d
Organism
Concentration
Bivalves; 5 spp.; soft parts; East China Sea; August 2002
0.012 (0.006-0.022) FW
a
Reference 61
Whelk, Busycon canaliculatum Muscle Digestive gland
0.06-0.14 FW 0.16-0.52 FW
5 5
Cockle, Cardium edule Soft parts Soft parts
0.8 DW 0.03-0.04 FW
3 6
Cephalopods; 3 spp.; edible portions
0.06 FW
4
Cephalopods; northeastern Atlantic Ocean between Bay of Biscay and Faroe Islands; 1996-2003 Total mercury; 20 spp. Whole Digestive gland Remaining tissues Organomercury compounds; 7 spp. Whole Digestive gland Remaining tissues
0.06-0.62 (0.035-1.2) DW 0.05-1.95 (0.01-3.6) DW 0.07-0.5 (0.04-1.0) DW
63 63 63
0.07-0.8 DW 0.04-0.71 DW 0.08-0.82 DW
63 63 63
China Coastal sites along Bohai Sea and Huangshi Sea; commercial species; soft parts; gastropods vs. bivalves Zhejiang coastal area; May 1998 Cephalopods; mantle; 2 spp. Bivalve molluscs; soft parts; 4 spp.
0.03 (0.002-0.09) FW vs. 0.01-0.08 FW
38
0.016-0.024 (0.009-0.0047) FW 0.013-0.023 (0.009-0.044) FW
45 45
Spiny scallop, Chlamys hastata; British Columbia, Canada; July 1999-February 2000; males vs. females Gonad Gill Mantle Muscle
0.4 DW vs. 0.2 DW 0.0 DW vs. 0.9 DW 0.1 DW vs. 0.08 DW 0.03 DW vs. 0.03 DW
46 46 46 46
Clams Soft parts Soft parts
0.005-0.012 DW 0.05-0.3 FW
8 9 (Continues)
272 Chapter 6 Table 6.14: Cont’d Organism
Concentration
Oyster, Crassostrea amasa; soft parts
0.07 FW
10
Oyster, Crassostrea angulata Soft parts Soft parts
0.56 DW 0.03-0.05 FW
3 11
Oyster, Crassostrea commercialis Soft parts Soft parts
0.001-0.1 FW 0.01-0.1 FW
12 13
0.2 (0.03-1.3) DW
47
0.081 FW 0.165 FW 0.137 FW 0.08 FW 0.018 FW 0.131 FW
14 14 14 14 14 14
0.089 FW
15
0.01-0.06 FW 0.05 DW 0.02-0.08 FW Max. 0.06 FW 0.13-0.91 DW
2 16 17 66 71
Mussel, Elliptio buckleyi; soft parts; Marmara Sea, Turkey; 2004-2005
0.23-0.75 (0.07-0.90) FW
60
Clam, Ensis arcuatus; shell
0.11 DW
18
Clam, Ensis siliqua; shell
0.1 DW
18
Gastropods; 5 spp.; soft parts
0.07-0.8 DW
2
Greenland; 1983-1991; bivalves; 5 spp.; soft parts
0.01-0.02 FW
48
Abalone, Haliotis ruber; muscle
0.01-0.04 FW
13
Abalone, Haliotis rufescens Gills Mantle Digestive gland Foot
0.08-0.27 DW 0.02-0.33 DW 0.12-4.64 DW 0.03-0.09 DW
19 19 19 19
Pacific oyster, Crassostrea gigas; Thailand; 1995-96; soft parts Oyster, Crassostrea glomerata Soft parts Gills Mantle Muscle Shell Viscera American oyster, Crassostrea virginica Shell Soft parts Mexico Texas Mississippi Pensacola, Florida; 2003-2004 Savannah, Georgia; 2000-2001
Reference
a
(Continues)
Molluscs 273 Table 6.14:
Cont’d a
Organism
Concentration
Reference
Italy; summer 1986-1987; soft parts Mussel, Mytilus galloprovincialis Gastropod, Murex trunculus
0.01-0.07 FW 0.03-0.15 FW
50 50
Squid, Illex illicebrosa Whole Soft parts Soft parts
<0.05 to 0.06 FW 0.04 FW; 0.11 DW 0.06-0.16 DW
23 25 6
Limpet, Littorina sp.; soft parts
2.6 DW
26
Squid, Loligo sp.; muscle Total Hg Organic Hg
0.014 (0.006-0.027) FW 0.008 (0.003-0.017) FW
27 27
Squid, Loligo vulgaris; edible portions
0.01-0.22 FW
28
Clam, Macoma balthica Soft parts Soft parts
0.03-0.07 FW 0.04-0.1 FW
6 29
0.056 0.146 0.041 0.277
55
Marine mammal food items; whole; Atlantic Ocean vs. Mediterranean Sea Squid, Loligo vulgaris Squid, Illex coindeti Hardshell clam, Mercenaria mercenaria Soft parts Soft parts; various ages 3 years 4 years 10 years 15 years Minamata Bay, Japan; site of massive chronic mercury pollution easing in 1950s Scallop, Chlamys ferrei nipponensis; soft tissue Pacific oyster, Crassostrea gigas; soft tissues Clam, Hormomya mutabilis Soft tissues Soft parts December 1959 January 1960
(0.024-0.097) FW vs. (0.068-0.250) FW (0.014-0.069) FW vs. (0.110-0.490) FW
0.03-0.12 FW; 0.18-0.57 DW
55
30
0.16 DW 0.2 DW 0.22 DW 0.22 DW
3 3 3 3
48.0 DW
7
10.0 DW
7
18.0-48.0 DW
7
100.0 DW 85.0 DW
20 21 (Continues)
274 Chapter 6 Table 6.14: Cont’d Organism April 1960 August 1960 January 1961 April 1961 December 1961 October 1963 Ganglion Gills Ligament Mantle Muscle Byssus Digestive gland Genital gland Octopus, Octopus vulgaris Abdomen Tentacles Clam, Pinctada martensii; soft parts Bivalve, Pinna attenuata; soft parts
Concentration 50.0 DW 31.0 DW 56.0 DW 30.0 DW 9.0 DW 12.0 DW 181.0 DW 87.0 DW 62.0 DW 63.0 DW 25.0 DW 20.0 DW 73.0 DW 64.0 DW
Reference 21 21 21 21 21 21 22 22 22 22 22 22 22 22
62.0 DW 39.0 DW 5.2-32.0 DW 11.0-25.0 DW
7 7 7 7
Molluscs; commercial species; soft parts 6 spp. 18 spp.
0.04-0.23 FW <0.1 FW
11 31
Morocco; 2001; clams; soft parts Scrobicularia plana Cerastoderma edule
0.4 DW 0.1 DW
74 74
Morocco; 2004-2005; soft parts Mussel, Mytilus galloprovincialis Clam, Venerupis decussatus Pacific oyster, Crassostrea gigas
0.6 (0.02-2.3) DW 0.3 (0.08-0.58) DW 0.4 (0.08-0.84) DW
72 72 72
Softshell clam, Mya arenaria; soft parts
0.04 FW
Mussel, Mytilus californianus Digestive gland Muscle Gonad Transferred to proximity of wastewater discharge for 24 weeks Digestive gland; start vs. end Muscle; start vs. end Gonads; start vs. end
a
6
0.023-0.063 FW 0.019-0.062 FW 0.005-0.014 FW
32 32 32
0.025 FW vs. 0.040-0.063 FW 0.027 FW vs. 0.032-0.046 FW 0.005 FW vs. 0.009-0.018 FW
32 32 32 (Continues)
Molluscs 275 Table 6.14:
Cont’d a
Organism
Concentration
Common mussel, Mytilus edulis Soft parts; Norway Soft parts Soft parts Soft parts Visceral mass Foot muscle Mantle Ctenidia Shell Shell; Baltic Sea; 2005; 12 sites Soft parts Soft parts
Max. 0.04 FW 0.03-1.4 DW 0.42-1.9 DW 0.64 FW; 2.1 DW 0.28 FW; 1.35 DW 0.36 FW; 0.77 DW 0.87 FW; 4.26 DW 3.41 FW; 19.95 DW 0.49 DW 0.002-0.008 DW 0.97 DW 0.006-0.012 DW
51 33 3 25 25 25 25 25 18 75 16 8
Mussel, Mytilus edulis planulatus; soft parts
0.66-10.6 DW
34
Pacific blue mussel, Mytilus edulis trossulus; soft parts; 2004; Adak Island, Alaska; 5 sites
0.016 FW; max. 0.04 FW
62
0.44-1.35 DW 0.24-0.32 DW 0.24-0.38 DW
64 64 64
0.16 DW Max. 0.09 DW Max. 0.04 DW 0.12 FW 0.78 (0.013-2.2) DW
64 64 64 35 58
0.04-0.19 DW vs. 0.02-0.03 DW 0.18 DW 1.75 FW
79
Mussel, Mytilus galloprovincialis Cultured mussels (<0.15 mg/kg soft parts DW) transplanted to Kastela Bay, Croatia (Hgcontaminated 1950-1990), in 2000-2001 for 6 months Total mercury Digestive gland Soft tissues (all) Gills Methylmercury Digestive gland Soft tissues (all) Gills Soft parts Soft parts; 1991-2005; western Mediterranean Sea; Balearic Islands; Port of Mahon Soft parts; Adriatic Sea; 2001-2005; winter vs. summer Soft parts; Izmir Bay, Turkey; 2004 Soft parts; Marmara Sea, Turkey; 2005
Reference
76 59 (Continues)
276 Chapter 6 Table 6.14: Cont’d Organism
Concentration
Reference
0.08-0.31 DW 0.11-0.26 DW 0.13-0.55 DW 0.09-0.12 DW
57 57 57 70
0.02-0.31 FW
36
0.07-1.01 DW vs. 0.06-0.83 DW; 52% organomercury 0.12-0.65 DW; 75-93% organomercury 0.031-0.037 DW; 5-22% organomercury 0.008-0.013 DW; 1.9-2.5% organomercury
54
New Jersey (United States) supermarkets; July-October 2003; scallops; edible tissues
0.01 (0.007-0.02) FW
52
Gastropod, Nucella conccina; soft parts; Antarctica; 2004
0.026 DW
56
Whelk, Nucella lapillus; soft parts
0.48 FW; 1.47 DW
25
Octopus, Octopus cyanea; June 1998; Guam; 4 stations; tentacle vs. liver
0.1 DW vs. 0.1 DW
53
Octopus, Octopus vulgaris Tentacle muscle Digestive gland Kidney Gill Brain Gonad Edible portions
0.75-2.32 FW 15.5-202.0 FW 4.0-7.5 FW 0.48-1.9 FW 0.99-1.24 FW 0.40-1.03 FW 0.05-0.37 FW
37 37 37 37 37 37 28
Squid, Ommastrephes sloani pacificus Muscle Liver
0.020-0.07 FW 0.03-0.13 FW
39 39
Oyster, Ostrea angasi; soft parts
1.5-8.2 DW
34
Soft parts; May 2003; NW Mediterranean Sea Near Genova, Italy Near Marseille, France Near Barcelona, Spain Soft parts; summers 2004-2005; Mediterranean Sea; 3 sites Mussel, Mytilus spp.; soft parts Netted whelk, Nassarius reticulatus; Portugal; 2000; total mercury Soft parts; males vs. females
Soft tissues Operculum Shell
a
54 54 54
(Continues)
Molluscs 277 Table 6.14: Organism European flat oyster, Ostrea edulis Soft parts Soft parts Soft parts; 1991-2005; Balearic Islands; western Mediterranean Sea; Port of Mahon
Cont’d
Concentration 0.36-1.2 DW 0.08-0.28 DW 0.9 (0.15-2.2) DW
a
Reference 3 40 58
Oysters; soft parts
0.01-0.05 FW
9
Clam, Paphies australe Soft parts Foot Gill Mantle Muscle Shell Viscera
0.023 FW 0.009 FW 0.02 FW 0.013 FW 0.014 FW 0.012 FW 0.012 FW
14 14 14 14 14 14 14
Limpet, Patella cerulea Soft parts Shell Foot Visceral mass
0.10-2.72 FW 0.08-0.25 FW 0.13-0.62 FW 2.04-5.92 FW
37 37 37 37
Limpet, Patella candei gomesii; soft parts; 2007; Azores Near hydrothermal vent Reference site
0.01 DW 0.02-0.03 DW
73 73
Limpet, Patella vulgata; soft parts
0.19 FW; 0.54 DW
25
Mussel, Perna canaliculus Soft parts Foot Gills Mantle Shell Viscera
0.017 FW 0.021 FW 0.032 FW 0.028 FW 0.005 FW 0.023 FW
14 14 14 14 14 14
Bivalve, Pinna nobilis Soft parts Mantle and gills Muscle Nerve tissue Stomach and intestines Gonads
6.0 DW 1.1 DW 3.1 DW 1.4 DW 14.0 DW 3.0 DW
41 41 41 41 41 41 (Continues)
278 Chapter 6 Table 6.14: Cont’d Organism Hepatopancreas Byssus Byssus gland
Concentration
Reference
7.6 DW 3.3 DW 1.0 DW
41 41 41
Scallop, Placopecten magellanicus Muscle Muscle Gonad Visceral mass
<0.05 FW <0.08 to 0.18 FW <0.08 to 0.18 FW <0.08 to 0.18 FW
25 42 42 42
Cuttlefish, Sepia officinalis Gills Mantle Edible portions Edible portions
0.9 DW 0.67 DW 0.10-0.13 FW 0.03-0.19 FW
3 3 43 35
Sepia sp.; India; 2003; edible portions
0.4 FW
68
Spain; Catalonia; November 1992February 1993; edible tissues Cephalopods; 3 spp. Noncephalopods; 5 spp.
0.003-0.27 FW 0.001-0.019 FW
49 49
Clam, Spisula solidissima; muscle
<0.05 FW
Clam, Spisula sp.; soft parts
0.8 FW
44
Clam, Tapes decussata; soft parts
0.03-0.06 FW
11
Japanese common squid, Todarodes pacificus; liver
0.19 DW
78
a
5
Values are in mg Hg/kg fresh weight (FW) or dry weight (DW). a 1, Won, 1973; 2, Reimer and Reimer, 1975; 3, Leatherland and Burton, 1974; 4, Kumagi and Saeki, 1978; 5, Greig et al., 1977; 6, Zauke, 1977; 7, Matida and Kumada, 1969; 8, Schell and Nevissi, 1977; 9, Hung and Lin, 1976; 10, Sorentino, 1979; 11, Establier, 1977; 12, Hussain and Bleiler, 1973; 13, Williams et al., 1976; 14, Hoggins and Brooks, 1973; 15, Ferrell et al., 1973; 16, Sims and Presley, 1976; 17, Harvey and Knight, 1978; 18, Bertine and Goldberg, 1972; 19, Anderlini, 1974; 20, Irukayama et al., 1961; 21, Irukayama, 1967; 22, Irukayama et al., 1962a; 23, Greig et al., 1975; 24, Windom et al., 1976; 25, Jones et al., 1972; 26, Windom et al., 1976; 27, Cheevaparanapivat and Menasveta, 1979; 28, Cumont et al., 1975; 29, Miettinen and Verta, 1978; 30, Burton and Leatherland, 1971; 31, Hall et al., 1978; 32, Eganhouse and Young, 1978; 33, Karbe et al., 1977; 34, Bloom and Ayling, 1977; 35, Uysal, 1978b; 36, Thibaud, 1973; 37, Renzoni et al, 1973; 38, Liang et al., 2004b; 39, Doi and Ui, 1975; 40, Fukai et al., 1978; 41, Papadopoulu, 1973; 42, Greig et al., 1978; 43, Yannai and Sachs, 1978; 44, Craig, 1967; 45, Fang et al., 2004; 46, Norum et al., 2005; 47, Han et al., 1998; 48, Dietz et al., 1996; 49, Schuhmacher et al., 1994; 50, Giordno et al., 1991; 51, Airas et al., 2004; 52, Burger et al., 2005; 53, Denton et al., 2006; 54, Coelho et al., 2006a,b; 55, Lahaye et al., 2006; 56, Santos et al., 2006; 57, Zorita et al., 2007; 58, Deudero et al., 2007; 59, Keskin et al., 2007; 60, Yarsan et al., 2007; 61, Huang et al., 2007; 62, Burger and Gochfeld, 2006; 63, Bustamante et al., 2006; 64, Kljakovic-Gaspic et al., 2006; 65, Burger et al., 2007a,b; 66, Karouna-Renier et al., 2007; 67. Kadar et al., 2006; 68, Sankar et al., 2006; 69, Colaco et al., 2006; 70, Lafabrie et al., 2007; 71, Kumar et al., 2008; 72 Maanan, 2008; 73, Cunha et al., 2008; 74, Anajjar et al., 2008; 75, Protasowicki et al., 2008; 76, Kucuksezgin et al., 2008; 77, Bustamante et al., 2008; 78, Arai et al., 2004; 79, Fattorini et al., 2008.
Molluscs 279 day 60, probably from loss owing to spawning. At day 60, oysters were transferred to mercury-free seawater for 160 days. During the first 18.0 days postexposure mercury levels declined to 15.0 mg/kg, but remained at that level for the next 142 days. Authors concluded that oysters concentrated 0.01 mg Hg/L by a factor of 2800 and that total self-purification was not achieved over a 6-month cleansing period. Kopfler (1974) found that continuous exposure to only 0.001 mg Hg/L in any of the three mercury compounds tested resulted in rapid accumulation in excess of 0.5 mg Hg/kg FW, that is, to concentrations potentially hazardous to humans ingesting these oysters, according to the action guideline established by the USFDA at that time. (Note: this action level is now 0.3 mg Hg/kg FW, as reviewed by Eisler, 2006). In China, the maximum allowable concentration of mercury in tissues of marine bivalves used as human food is 0.3 total mercury/kg FW (Huang et al., 2007). Details of Kopfler’s study (1974) follow. Accumulation of mercury compounds was determined in two experiments, each using three groups of 100 oysters. In the first experiment, conducted between 0 and 10 C, mercury concentrations were maintained at 0.05 mg/L with flow rate adjusted to 1 L/oyster/h. In the second experiment, mercury levels were reduced to 0.001 mg/L, the water temperature varied between 25 and 35 C, and flow rates maintained at 2 L/oyster/h because of the increased temperature. Controls were maintained for each study. In the first experiment, the administration of organic mercury compounds was terminated after 19 days because many of the oysters in groups receiving either methylmercury or phenylmercury salts were dead or moribund. Oysters classified as moribund had slow, incomplete valve closure when disturbed. When oysters in these groups (surviving 19 days exposure) were placed in mercury-free flowing seawater, about half in each group died within a week and all oysters exposed to either methylmercury or phenylmercury died within 14 days. However, oysters exposed to inorganic mercuric chloride had no apparent adverse effects over a 42-day exposure to 0.05 mg Hg/L; mean mercury levels in exposed oysters after exposure for 7 days were 15.0-17.0 mg/kg FW versus 0.02 mg/ kg FW for controls. Copper and zinc metabolism was significantly altered in all exposure groups. In the second experiment, methylmercury and phenylmercury compounds were both significantly elevated in oyster tissues when compared to inorganic mercury; concentrations of organomercury compounds were about 20.0 mg Hg/kg FW after 20 days of exposure, and 30.0 mg/kg FW after 60 days—a final concentration factor of about 30,000; for inorganic mercuric chloride, these values ware about 2.0 mg Hg/kg FW after exposure for 20 days and about 10.0 mg Hg/kg FW after 60 days (Kopfler, 1974). Mercury is also accumulated from seawater by other marine molluscs. In radiotracer studies, clams Tapes decussatus, contained 10 times more 203Hg per unit weight over the medium within 24 h (Unlu et al., 1972). Mercury can also be accumulated through food webs. Bacteria have a marked effect on mercury in food chains that include filter feeders. Thus, whole oyster accumulation of mercury more than doubled in the presence of mercuryresistant strains of Pseudomonas spp. (Colwell and Nelson, 1975; Colwell et al., 1976; Sayler
280 Chapter 6 et al., 1975). In clams, radiomercury seems to have a biological half-life of 10 days if accumulated via the food chain but only 5 days via the medium (Unlu et al., 1972). Retention times of radiomercury-203 in most marine species were comparatively lengthy, up to 1000 days for mussels, M. galloprovincialis (Miettinen et al., 1969, 1972). Miettinen and coworkers found that phylogenetically related species follow a similar pattern of methylmercury excretion, with biological half-life depending on water temperature and mode of entry into organisms; half-life is longer after intramuscular injection than after peroral administration. Three points are with emphasizing at this juncture. first, mercury discharged into rivers, bays, or estuaries as metallic mercury, inorganic divalent mercury, phenylmercury, or alkoxyalkyl mercurials, can all be converted to methylmercurials by natural processes (Jernelov, 1969). Second, organomercury complexes are rapidly accumulated in tissues with high lipid content (Wood, 1973). Finally, mercury-resistant strains of bacteria which have been developed or discovered may have application in mercury mobilization of fixation from mercury-contaminated waters to the extent that polluted areas become innocuous (Colwell and Nelson, 1975; Nelson et al., 1983; Vosjan and Van der Hoek, 1972). Establishment of mercury criteria for the protection of human health and sensitive marine resources includes abatement of existing discharges, development of technologies to decontaminate contaminated waterways, monitoring of bivalve molluscs and other sensitive indicators of mercury insult, and establishing predictive models of mercury stress in marine ecosystems (Eisler, 1978, 2000, 2006; Johnels and Westermark, 1969; USEPA, 1977; USNAS, 1973). Reduced mercury inputs to coastal area as a result of legislation and effective enforcement actions is reflected in mercury levels of common mussels, M. edulis, in Bergen Harbor, Norway. In 2002, mussels from Bergen Harbor contained a maximum of 0.04 mg Hg/kg FW soft parts; this was about 60% lower than mercury concentrations in mussels collected from the same area in 1993. The reduced mercury was attributed to reductions in mercury content to Bergen Harbor of municipal wastewater, urban runoff, and especially of mercury-containing dental wastes (Airas et al., 2004).
6.24 Molybdenum Maximum concentrations of molybdenum recorded in molluscan tissues, in mg Mo/kg DW, are 240.0 in mantle and gills of Arca noae and 464.0 in branchial heart of O. vulgaris, although most values were significantly lower (Table 6.15). A. noae and P. nobilis collected from coastal waters of Greece exhibited unusually high bioconcentration up to 1300-fold over seawater molybdenum concentrations (Papadopoulu, 1973). Lower concentration factors were reported for mussels, scallops, and oysters; these groups contained
Molluscs 281 Table 6.15: Molybdenum Concentrations in Field Collections of Molluscs Organism
Concentration
Bivalve, Arca noae Soft parts Mantle and gills
88.0 DW 240.0 DW
1 1
Max. 0.64 DW
6
<0.1 to 0.2 FW 0.2-0.4 FW 0.4-0.6 FW 0.7-0.8 FW 3.0-4.0 FW
2 2 2 2 2
<1.9 DW
5
Mussel, Mytilus edulis aoteanus Soft parts Gills Visceral mass Shell
0.6 DW 0.6 DW 1.9 DW 11.0 DW
3 3 3 3
Octopus, Octopus vulgaris; Portugal; 1999-2002; 3 sites Digestive gland Branchial heart
2.7-19.0 DW 233.0-464.0 DW
7 7
Squid, Ommastrephes illicebrosa; whole
4.0 AW
4
Oyster, Ostrea sinuata Soft parts Heart Visceral mass Gill
0.9 DW 1.3 DW 0.5 DW 0.4 DW
3 3 3 3
Scallop, Pecten novae-zelandiae Soft parts Mantle Gill Intestine Kidney Foot
0.9 DW 1.8 DW 3.1 DW 3.6 DW 3.4 DW 0.4 DW
3 3 3 3 3 3
American oyster, Crassostrea virginica; soft parts; Savannah, Georgia; 2000-2001 Molluscs; commercial species; edible tissues 3 spp. 9 spp. 3 spp. 2 spp. 1 spp. Common mussel, Mytilus edulis; soft parts; southeast Alaska; 1980-1982
Reference
a
(Continues)
282 Chapter 6 Table 6.15: Cont’d Organism
Concentration
Bivalve, Pinna nobilis Mantle and gills Other tissues
20.0 DW <0.1 DW
Reference
a
1 1
Values are in mg Mo/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Papadopoulu, 1973; 2, Hall et al., 1978; 3, Brooks and Rumsby, 1965; 4, Nicholls et al., 1959; 5, Franson et al., 1995; 6, Kumar et al., 2008; 7, Napoleao et al., 2005.
30-90 times the level of molybdenum normally encountered in ambient seawater (Brooks and Rumsby, 1965). Molluscs are relatively resistant to molybdenum. Laboratory studies with larvae of the common mussel, M. edulis, show that 147.0 mg Mo/L was required for 50% inhibition of development in 48 h based on reduced survival and increased frequency of abnormalities (Morgan et al., 1986), and that 1375.0 mg Mo/L was associated with a 50% reduction in shell growth in 96 h of adult American oysters, C. virginica (Knothe and Van Riper, 1988). There is some evidence that pH of the medium directly affects molybdenum residues and biocidal properties in Venerupis pallustra, with higher residues and lower survival reported in the pH range 5.1-6.2 (Abbott, 1977).
6.25 Neptunium During exposure of M. galloprovincialis for 58 days to 237Np, about 90% of the accumulated isotope concentrated in the shell. The remainder was located in viscera, gill, mantle, and muscle, in descending order of accumulation (Guary and Fowler, 1978).
6.26 Nickel Nickel concentrations in marine molluscs varied with season of collection, with geographic area, and among tissues examined (Table 6.16). Maximum nickel concentrations recorded in molluscan tissues, in mg Ni/kg DW, were 200.0 in byssus gland of P. nobilis, 342.0 in brachial heart of O. vulgaris, 850.0 in soft parts of Crepidula fornicata, and 876.0 in kidney of C. radula (Table 6.16), and were probably associated with industrial nickel wastes. BCFs for nickel of 800 in soft parts and 40 in shell of marine bivalve molluscs and 500 in brown algae suggest that some food chain biomagnification may occur (USNAS, 1975). For marine mussels and oysters, typical BCF values in soft tissues ranged between 279 and 414 (USEPA, 1980c). However, interpretation of nickel concentrations in molluscs is confounded by interspecies variations in uptake potential. For example, Astralium rugosum can bioconcentrate nickel up to 120,000 times that of ambient seawater levels (Papadopoulu,
Molluscs 283 Table 6.16: Nickel Concentrations in Field Collections of Molluscs Organism
Concentration
Mussel, Anodonta sp. Shell Soft parts
1.2 DW 0.4 DW
1 1
Gastropod, Aplysia benedicti Ctenidium Gonad Parapodia Hepatopancreas Buccal mass Intestine Gut content
8.0-10.0 DW 6.0-10.0 DW 5.0 DW 15.0-20.0 DW 6.0-10.0 DW 13.0 DW 15.0 DW
2 2 2 2 2 2 2
Giant squid, Architeuthis dux; 20012005; Spain Hepatopancreas Branchial heart
0.6-1.4 DW 1.4 DW
62 62
4.2-13.4 DW 4.0-18.4 DW 5.4-29.3 DW 4.0-18.0 DW 3.1-22.7 DW 1.1-7.0 FW
3 3 3 3 3 34
Cockle, Austrovenus stutchburyi; soft parts; 1993-1994; New Zealand
5.0-35.0 DW
46
Mussel, Brachydontes variabilis; soft parts
Max. 19.5 FW; max 98.4 DW
Whelk, Buccinum undatum Shell Soft parts Soft parts; near sludge dump site vs. reference site
0.1 DW 0.6 DW 8.5 DW vs. 0.6 DW
Ocean quahog, Arctica islandica; soft parts New England; offshore August February March June Long Island, New York; 1974-1975; offshore
Reference
a
4 1 1 36
Cockle, Cardium edule Shell Soft parts
0.1 DW 7.0 DW
1 1
Mussel, Cerastoderma edule; soft parts
34.0-62.0 DW
5 (Continues)
284 Chapter 6 Table 6.16: Cont’d Organism
Concentration
Scallop, Chlamys opercularis Soft parts Body fluid Mantle Gills Digestive gland Striated muscle Gonad and foot Kidneys Shell
1.6 DW 0.9 DW 0.6 DW 1.6 DW 4.3 DW 0.2 DW 0.6 DW 78.2 DW 0.2-7.2 DW
6 6 6 6 6 6 6 6 1
2.0-3.0 DW
7
Mussel, Choromytilus meridionalis; soft parts Scallop, Comptopallium radula; Santa Marie Bay (metals-contaminated), New Caledonia; October 2004 Soft parts Kidney Pacific oyster, Crassostrea gigas Soft parts Soft parts Soft parts South Africa United Kingdom United States
12.8 (8.6-17.2) DW 876.0 DW 1.0-1.6 DW 0.1-0.2 FW Max. 2.0 DW 1.0-10.0 DW Max. 0.2 DW
Reference
56 56 7, 8 9 36 36 36
Oyster, Crassostrea margaritacea; soft parts
1.6 DW
Oyster, Crassostrea rhizophorae; soft parts; Brazil; summer 2001; contaminated estuary vs. reference site
0.5-2.1 DW; max. 9.0 DW vs. 1.2-1.8 DW; max. 4.3 DW
48
0.2 (0.08-1.8) FW 0.9-5.4 DW <1.0 DW vs. (0.9-5.4) DW; no data vs. 0.19 (0.08-1.8) FW Max. 0.69 FW
9 10 35, 36
<1.5 to 2.5 DW
55
American oyster, Crassostrea virginica Soft parts Soft parts Shell vs. soft parts Soft parts; Pensacola, Florida; 2003-2004 Soft parts; Savannah, Georgia; 2000-2001
a
8
52
(Continues)
Molluscs 285 Table 6.16:
Cont’d
Organism
Concentration
Limpet, Crepidula fornicata Shell Soft parts
1.6 DW 850.0 DW
Abalone, Haliotis rufescens Gills Mantle Digestive gland Foot
69.0-112.0 DW 19.0-57.0 DW 2.5-10.6 DW 0.2-1.6 DW
11 11 11 11
13.6-15.9 DW
37
6.9-7.9 DW 0.5-9.0 DW
5 51
Abalone, Haliotis tuberculata; soft parts; England Clam, Macoma balthica Soft parts Soft parts; 1996-1997; Gulf of Gdansk Hardshell clam, Mercenaria mercenaria Shell Soft parts Soft parts Soft parts United Kingdom United States
2.4 DW 11.0 DW 0.2 (0.1-2.4) FW
Reference 1 1
1 1 9
2.2 FW; 6.5-19.2 DW 1.2 (0.1-2.4) FW
36 36
Clam, Meretrix lamarckii; soft parts
3.1 DW
12
Mussel, Modiolus modiolus Shell Soft parts Mantle and gills Muscle Gonad Gut and digestive gland
0.2 DW 9.4-133.0 DW 3.2 DW 2.0 DW 1.2 DW 0.6 DW
Molluscs; 21 commercial species; edible portions 5 spp. 4 spp. 6 spp. 3 spp. 3 spp.
0.2-0.3 FW 0.3-0.5 FW 0.5-0.8 FW 1.0-3.0 FW 0.65-3.4 FW
Molluscs; 3 spp.; soft parts; Lebanon, near Ras Beirut
27.4-40.1 DW
a
1 1 1 1 1 1
13 13 13 13 14 4 (Continues)
286 Chapter 6 Table 6.16: Cont’d Organism
Concentration
Molluscs; 5 spp; soft parts; Chile, Strait of Magellan; 2001; 17 stations
0.16-0.8 FW
50
Morocco; 2001; clams; soft parts Scrobicularia plana Cerastoderma edule
6.0 DW 17.0 DW
58 58
Morocco; 2004-2005; soft parts Mussel, Mytilus galloprovincialis Clam, Venerupis decussatus Pacific oyster, Crassostrea gigas;
32.8 (12.7-94.3) DW 22.4 (14.6-34.2) DW 25.8 (6.0-37.8) DW
57 57 57
Softshell clam, Mya arenaria Soft parts Soft parts
0.3 (0.1-2.3) FW 1.8-4.1 DW
9 15
Mussel, Mytilus californianus Digestive gland Soft parts
3.0-20.0 DW 0.7-5.3 DW
16 10
Max. 7.4 DW <6.0 FW <2.6 FW <14.0 FW 2.1 DW 1.5-2.2 DW 3.7 DW 0.5-9.5 DW 0.0-3.5 DW 26.0-53.0 DW 0.4-6.3 DW
17 18
Common mussel, Mytilus edulis Hepatopancreas Digestive gland Gonads Muscle Shell Shell; Baltic Sea; 2005; 12 sites Soft parts Soft parts Soft parts Soft parts Soft parts Soft parts France Norway United Kingdom Scheldt estuary, Europe; March 2000 The Netherlands 1985-1990 Summer, 2002 Mussel, Mytilus edulis aoteanus Soft parts Gills
Reference
a
18 1 59 1 19 5 20 10
0.5 FW; 2.4 DW 6.0-43.0 DW 0.4 FW; max. 53.0 FW; 3.7 (5.0-12.0) DW 23.0 DW
36 36 36
0.33-0.52 FW Max. 6.0 DW
41 45
7.0 DW 8.0 DW
21 21
60
(Continues)
Molluscs 287 Table 6.16: Organism Visceral mass Gonads Intestine
Cont’d
Concentration
Reference
32.0 DW 5.0 DW 42.0 DW
21 21 21
4.3 DW 6.8 (0.7-35.2) DW
22 43
26.0 DW vs. 7.0 DW 1.1-3.7 DW
61 54
1.3 DW
66
2.8-3.6 DW vs. 3.7-5.6 DW 4.3 DW vs. 3.3 DW 2.6-6.5 DW vs. 1.8-2.6 DW
47 47 63
0.27 FW vs. 0.53 FW 0.34 FW vs. 0.5 FW 0.3 FW vs. 0.6 FW 0.74 FW vs. 1.87 FW
44 44 44 44
Mussel, Mytilus viridis; soft parts
1.1-15.1 DW
23
Abalone, Notohaliotis discus; soft parts less viscera
2.4 DW
12
Mussel, Mytilus galloprovincialis Soft parts Soft parts; 1991-2005; western Mediterranean Sea Soft parts; Sardinia; 2004 vs. 2006 Soft parts; summers 2004-2005; Mediterranean Sea; 3 sites Soft parts; Gulf of Gemlik, Turkey; 2004 Soft parts; Adriatic Sea; 2001-2002; summer vs. winter Industrialized sites Reference site Soft parts; Adriatic Sea; 2001-2005; winter vs. summer Mantle vs. gills; 2004-2006; Greece; max. mean concentrations; contaminated sites Summer Autumn Winter Spring
Whelk, Nucella lapillus Shell Soft parts Soft parts plus operculum
0.3 DW 2.4 DW 1.4-4.1 DW
Octopus, Octopus vulgaris; Portugal; 1999-2002; 3 sites Digestive gland Branchial heart Gill Muscle
3.9-7.6 DW 205.0-342.0 DW 1.5-1.6 DW 1.5-2.2 DW
64 64 64 64
Squid, Ommastrephes illicebrosa; whole
<1.0 AW
24
a
1 1 5
(Continues)
288 Chapter 6 Table 6.16: Cont’d Organism European flat oyster, Ostrea edulis Soft parts Soft parts; 1991-2005; Balearic Islands; Port of Mahon; western Mediterranean Sea
Concentration
Reference
1.7 DW 3.6 (0.8-7.5) DW
8 43
Oyster, Ostrea equestris; soft parts; United States East coast West coast
<0.1 DW 1.4-7.3 DW
10 10
Oyster, Ostrea sinuata Soft parts Muscle Visceral mass Heart
2.0 DW 8.0 DW 12.0 DW 2.0 DW
21 21 21 21
Limpet, Patella coerulea; soft parts
Max. 15.3 FW; max. 75.9 DW
Common limpet, Patella vulgata Shell Soft parts Shell Soft parts Soft parts Norway United Kingdom Israel; near sewage discharge vs. reference site Scallop, Pecten maximus Soft parts Body fluid Mantle Gills Digestive gland Striated muscle Gonad and foot Kidneys Soft parts Muscle Gut and digestive gland Mantle and gills; washed vs. unwashed Gonad; washed vs. unwashed Shell; upper valve vs. lower valve
a
4
0.5 DW 2.5 DW 3.0-7.0 DW 1.7-3.7 DW
1 1 26 5
4.0-11.0 DW 7.3 (2.5-24.0) DW 12.0 DW vs. 5.0-9.0 DW
26, 36 25, 36 36
0.8 DW 0.7 DW 0.4 DW 0.7 DW 3.6 DW 0.04 DW 0.3 DW 22.9 DW 49.0 DW 1.7 DW 1.0 DW 0.3 DW vs. 0.8 DW
6 6 6 6 6 6 6 6 1 1 1 1
0.4 DW vs. 1.5 DW 1.2 DW vs. 2.4 DW
1 1 (Continues)
Molluscs 289 Table 6.16:
Cont’d
Organism
Concentration
Scallop, Pecten novae-zelandiae Soft parts Gills Intestine Kidney Foot Gonads Shell
6.0 DW 68.0 DW 52.0 DW 106.0 DW 22.0 DW <2.0 DW <2.0 DW
21 21 21 21 21 21 21
0.24-0.31 FW
49
5.4 DW vs. 2.8 DW 10.0 DW vs. 10.4 DW
65 65
6.5 DW vs. 13.4 DW 12.6 DW vs. no data
65 65
Bivalve, Pinna nobilis Soft parts Nervous system Stomach and intestine Gonads Hepatopancreas Byssus gland
21.0 DW 18.0 DW 170.0 DW 74.0 DW 170.0 DW 200.0 DW
27 27 27 27 27 27
Clam, Pitar morrhuana; soft parts
7.4-37.5 DW
28
Green mussel, Perna viridis Soft parts; India; January 2002; 28 sites Hong Kong; juveniles vs. adults Reference site Soft parts Byssus Polluted site Soft parts Byssus
Sea scallop, Placopecten magellanicus Soft parts Muscle March August February June Viscera March August February June Muscle Gonad
Reference
4.4 DW
3
0.0-22.3 DW 0.0-4.9 DW 0.0-0.3 DW 0.0 DW
3 3 3 3
1.5-13.1 DW 1.2-8.8 DW 1.5-7.6 DW 1.6-3.7 DW <0.28 to 0.68 FW 0.23-2.5 FW
a
3 3 3 3 29 29 (Continues)
290 Chapter 6 Table 6.16: Cont’d Organism Visceral mass Soft parts; Long Island, New York; 1974-1975 North Atlantic Ocean coast; 42 stations Gonads Muscle Viscera Soft parts; near ocean disposal sites Manila clam, Ruditapes philippinarum; soft parts; Korea; 2002-2003 Females vs. males Postspawn vs. prespawn Clam, Scrobicularia plana Bidaron estuary, France-Spain border; April 1993; soft parts Looe estuary, England; soft parts Camel estuary, England Soft parts Digestive gland Mantle and siphons Foot and gonad Gills and palps Gannel estuary, England Soft parts Digestive gland Mantle and siphons Foot and gonad Transferred from Camel Estuary to Gannel estuary for 352 days Digestive gland Remaining tissues Transferred from Gannel Estuary to Camel estuary for 352 days Digestive gland Remaining tissues Tamar estuary, England Soft parts Digestive gland Squid, Sepia esculenta; trunk
Concentration
Reference
0.31-1.6 FW 0.5-3.3 FW
29 34
0.2-2.5 FW <0.3 to 0.7 FW 0.3-1.6 FW 4.4 DW
38 38 38 39
4.9 DW vs. 4.9 DW 21.0 DW vs. 4.9 DW
42 42
4.1 (2.9-5.7) DW
40
5.3-13.9 DW
5
3.4-4.5 DW 10.6 DW 1.4 DW 4.0 DW 10.5 DW
30 30 30 30 30
9.8-11.9 DW 43.1 DW 3.2 DW 3.9 DW
30 30 30 30
32.0 DW 2.3 DW
30 30
29.0 DW 1.9 DW
30 30
1.6-9.1 DW 6.6-25.0 DW
31 31
1.1 DW
12
a
(Continues)
Molluscs 291 Table 6.16:
Cont’d
Organism
Concentration
Squid; muscle; Texas outer continental shelf
2.5 DW
33
Clam, Siliqua patula; soft parts
0.74 DW
32
Squid Flesh Flesh with skin Viscera Pen
2.5 DW 2.5 DW 1.7 DW 0.8 DW
33 33 33 33
6.0-15.0 DW
53
Clam, Trivela mactroidea; Venezuela; 2002; 14 sites; soft parts
Reference
a
Values are in mg Ni/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Segar et al., 1971; 2, Patel et al., 1973; 3, Reynolds, 1979; 4, Shiber and Shatila, 1978; 5, Bryan and Hummerstone, 1977; 6, Bryan, 1973; 7, Watling and Watling, 1976b; 8, Watling and Watling, 1976a; 9, Pringle et al., 1968; 10, Goldberg et al., 1978; 11, Anderlini, 1974; 12, Ishii et al., 1978; 13, Hall et al., 1978; 14, Ikebe and Tanaka, 1979; 15, Eisler, 1977b; 16, Alexander and Young, 1976; 17, Young et al., 1979; 18, Young and McDermott, 1975; 19, Karbe et al., 1977; 20, Simpson, 1979; 21, Brooks and Rumsby, 1965; 22, Fowler and Oregioni, 1976; 23, Bhosle and Matondkar, 1978; 24, Nicholls et al., 1959; 25, Preston et al., 1972; 26, Lande, 1977; 27, Papadopoulu, 1973; 28, Eisler et al., 1978; 29, Greig et al., 1978; 30, Bryan and Hummerstone, 1978; 31, Bryan and Uysal, 1978; 32, Laevastu and Thompson, 1956; 33, Horowitz and Presley, 1977; 34, Palmer and Rand, 1977; 35, Eisler, 1981; 36, Jenkins, 1980; 37, Bryan et al., 1977; 38, Greig et al., 1978; 39, Pesch et al., 1977; 40, Saiz-Salinas et al., 1996; 41, Stronkhorst, 1992; 42, Ji et al., 2006; 43, Deudero et al., 2007; 44, Vlahogianni et al., 2007; 45, Mubiana and Blust, 2006; 46, Peake et al., 2006; 47, Scancar et al., 2007; 48, Silva et al., 2006; 49, Sasikumar et al., 2006; 50, Espana et al., 2007; 51, Sokolowski et al., 2007; 52, Karouna-Renier et. al., 2007; 53, LaBrecque et al., 2004; 54, Lafabrie et al., 2007; 55, Kumar et al., 2008; 56, Metian et al., 2008; 57, Maanan, 2008; 58, Anajjar et al., 2008; 59, Protasowicki et al., 2008; 60, Wepener et al., 2008; 61, Schintu et al., 2008; 62, Bustamante et al., 2008; 63, Fattorini et al., 2008; 64, Napoleao et al., 2005; 65, Nicholson and Szefer, 2003; 66, Unlu et al., 2008.
1973), far greater than most species. Nickel concentrations in soft tissues of clams, R. philippinarum, increase significantly with increasing shell length (Ji et al., 2006). In cockles, A. stutchburyi, nickel burdens were lowest in soft parts during summer—unlike copper, chromium, and zinc (Peake et al., 2006). In soft parts of the green mussel, P. viridis, nickel content was positively correlated with chromium, copper, and manganese contents (Sasikumar et al., 2006). Laboratory studies on nickel accumulation by the common mussel, M. edulis, were conducted by Freidrich and Felice (1976). At nominal seawater concentrations of 0.03 mg Ni/L and lower, they found that mussels did not accumulate nickel in soft parts after exposure for 28 days. At 0.056 mg Ni/L, however, mussels contained up to 33.0 mg Ni/kg DW soft parts after 28 days; at 0.107 mg Ni/L this was 41.0 mg Ni/kg DW after 28 days. At higher concentrations of 20.0, 40.0, and 80.0 mg Ni/L and exposure for 96 h, mussels contained
292 Chapter 6 420.0, 450.0, and 820.0 mg Ni/kg DW, respectively. All mussels survived exposure for 96 h at all nickel concentrations tested, including 80.0 mg Ni/L (Freidrich and Felice, 1976). Nickel at 0.05 mg/L was accumulated from seawater by softshell clams, M. arenaria, more rapidly during summer at water temperatures of 16-22 C than during winter at 0-10 C; no accumulation occurred at 0.01 mg Ni/L in winter although clams took up twice as much nickel over controls in summer (Eisler, 1977a). At present, latent sublethal effects of short-term exposure to nickel salts have not been evaluated adequately in marine molluscs. Clam embryos were comparatively sensitive to ionic nickel. The LC-50 (48 h) value for nickel and embryos of the hardshell clam, M. mercenaria, was 0.31 mg Ni/L (Calabrese and Nelson, 1974). Embryos of the American oyster, C. virginica, were more resistant: the LC-50 (48 h) value for that life stage was 1.18 mg Ni/L (Calabrese and Nelson, 1974). No deaths occurred among adult softshell clams exposed to 100.0-500.0 mg Ni/L for 168 h (Eisler, 1977b; Eisler and Hennekey, 1977). Three species of bivalves were exposed for 14 days to radionickel-63 via seawater or food (Hedouin et al., 2007). In the seawater portion of the study, oysters (Isognomon isognomon, Malleus regula) and a clam (G. tumidum) were subjected to stable nickel concentrations up to 0.0014 mg Ni/L; uptake was proportional to nickel concentration in the medium. Most of the accumulated nickel was lost within a few days; however, 7-47% of the 63Ni was retained in tissues indefinitely. Feeding studies showed that 63Ni ingested with phytoplankton was assimilated more efficiently in the clam (61%) than in oysters (17%) and was retained in tissues of all bivalves with an estimated biological half-life of more than 35 days (Hedouin et al., 2007). To protect marine life, the USEPA has proposed a 24 h average of total recoverable nickel at less than 0.007 mg Ni/L and a maximum of 0.14 mg Ni/L that should not be exceeded at any time (USEPA, 1980c). However, 0.056 mg Ni/L is associated with nickel accumulations in mussels (Freidrich and Felice, 1976), suggesting reexamination of the 0.14 mg Ni/L proposed maximum criterion. To protect human consumers, edible portions of molluscs should not exceed 80.0 mg Ni/kg FW (Sankar et al., 2006).
6.27 Niobium The single datum available on niobium in marine molluscs indicates that the common mussel, M. edulis contains less than 0.001 mg Nb/kg DW soft parts (Carlisle, 1958).
6.28 Plutonium Plutonium was present in three species of molluscs as 239 + 240Pu—but not 238Pu—in samples collected during summer 2004 near Amchitka Island in the Aleutians; Amchitka was the site of nuclear tests between 1965 and 1971 (Burger et al., 2007b). Elevated levels
Molluscs 293 of plutonium were measured in gastropod and bivalve molluscs collected in the vicinity of French nuclear installations when compared to conspecifics collected 50 km distant (Guary and Frazier, 1977). Elevated plutonium levels were also recorded in the bivalve Macoma sp. and other benthic fauna from Bylot Sound, Greenland, following accidental contamination of that area with nuclear weapons in 1968; organisms lost about 90% of the accumulated 239 + 240Pu by 1970, but loss was negligible over the next few years (Aarkrog, 1971, 1977, 1990). Benthic bivalves reportedly can accumulate plutonium isotopes to a greater degree than all other marine biota (Aarkrog, 1971; Pillai et al., 1964). Radioplutonium concentrations in the common mussel, M. edulis, seem to reflect global fallout levels (Crowley et al., 1990). Accumulation of transuranic elements, including 238 + 239 + 240 Pu, and also americium-241, in M. edulis from the vicinity of a uranium processing plant is documented (Hamilton and Clifton, 1980). Uptake was probably from seawater rather than ingested sediments. Highest enrichment of plutonium and americium occurred in byssal threads and periostracum; lowest in shell with periostracum removed. Transuranics retained within the intestinal tract were excreted in feces, but those which enter the systemic circulation were widely diffused (Hamilton and Clifton, 1980).
6.29 Polonium BCFs values for 210Po from seawater to tissues of squids, Todarodes pacificus, from the East Japan Sea ranged from 6400 for muscle to 14 million for hepatopancreas; intermediate values were estimated for gill (2.4 million) and stomach (240,000) (Waska et al., 2008). Polonium-210 was measured in whole squid, muscle, and hepatopancreas (Heyraud and Cherry, 1979). The concentration factors from seawater to whole squid were about 1000, but were significantly lower in muscle, and higher in hepatopancreas. In general, 210Po accumulations were highest in crustaceans and lowest in fish, cephalopods being intermediate (Heyraud and Cherry, 1979).
6.30 Protactinium Lucu et al. (1969) showed that M. galloprovincialis held for 20 days in seawater solutions containing 233Pa took up this isotope by factors of 2500 in byssus, 150 in shell, up to 200 in digestive tract, 60 in gill, 15 in gonad, and 10 in muscle.
6.31 Radium Concentrations of radium in 18 species of molluscs collected from various locales parallel those of calcium; for all species, radium content ranged from 359.0 1010 to 3580.0 1010 mg/kg calcium (Koczy and Titze, 1958).
294 Chapter 6
6.32 Rhenium Clams, Tapes japonicus, contained 0.064 mg Re/kg ash weight (AW) soft parts; on a DW basis, this value was 0.0046 (Fukai and Meinke, 1959, 1962).
6.33 Rubidium Rubidium concentrations in molluscan tissues ranged from 3.2 to 14.0 mg Rb/kg DW (Table 6.17). Eversole (1978) studied rubidium uptake in hardshell clams, M. mercenaria. Clams held in seawater solutions containing 0.01 mg Rb/L and higher for 96 h had significantly more rubidium than controls. Clams held in 1.0 mg Rb/L for 96 h, showed measurable rubidium levels in tissues for periods up to 3 weeks postexposure when held in rubidium-free seawater. Clam embryos held for 96 h in vessels containing diatoms previously exposed to 1000.0 mg Rb/L took up more rubidium than embryos subjected to unlabeled diatoms, suggesting that diet is important as a source of rubidium for Mercenaria.
Table 6.17: Rubidium Concentrations in Field Collections of Molluscs Organism
Concentration
Clam, Meretrix lamarckii; soft parts
4.5 DW
1
Mussel, Mytilus corscum; soft parts
4.2 DW
1
Common mussel, Mytilus edulis; soft parts
3.4-14.0 DW
2
Abalone, Notohaliotis discus; soft parts less viscera
3.2 DW
1
Octopus, Octopus vulgaris; Portugal; 1999-2000; 3 sites Digestive gland Branchial heart
5.0-7.1 DW 9.1-9.5 DW
4 4
Limpet, Patella candei gomesii; soft parts; 2007; Azores Near hydrothermal vent Reference site
8.2-8.4 DW 5.8-5.9 DW
3 3
Squid, Sepia esculenta; trunk
3.4 DW
1
Values are in mg Rb/kg dry weight (DW). a 1, 1, Ishii et al., 1978; 2, Karbe et al., 1977; 3, Cunha et al., 2008; 4, Seixas and Pierce, 2005.
Reference
a
Molluscs 295
6.34 Ruthenium Ruthenium-106 concentrations in seven species of molluscs increased by a factor of at least 2.6 following release of 106Ru and other isotopes from the Chernobyl nuclear reactor accident (Lowe and Horrill, 1991). Mussels, M. galloprovincialis, rapidly accumulated 103Ru and 106 Ru after the Chernobyl incident in April 1986; however, loss was rapid, and between May 6 and August 14 the loss rate from mussel soft parts was 98% for 103Ru and 91% for 106 Ru (Whitehead et al., 1988). Molluscs accumulated radioruthenium from seawater by factors up to 200 (Ueda et al., 1978). However, uptake by clams was different for anionic, cationic, and neutral fractions of ruthenium; the cationic fraction was accumulated by an order of magnitude higher than the other fractions (Ishikawa et al., 1973, 1976). Similar results were observed in various species of mussels. In one case, M. galloprovincialis held for 5 days in seawater containing a 106 Ru-nitrate complex had ruthenium concentration factors of 50 in soft parts and 4 in shell; however, a 106Ru-chloride complex had concentration factors of only 5 in soft parts and 1 in shell (Keckes et al., 1966). Uptake of 106Ru-chloride fractions was faster than that of 106Ru nitrosyl-nitrate fractions and uptake was greater in soft tissues than in shell (Keckes et al., 1966). On the other hand, several investigations on ruthenium distribution in mussels show that most of the ruthenium accumulated in shells (Jones, 1973; Zesenko and Polikarpov, 1965) with negligible uptake in edible meats (Avargues et al., 1968; LeGall and Ancellin, 1971).
6.35 Samarium Samarium concentrations in tests of pteropods ranged from 0.04 to 0.72 mg Sm/kg DW (Turekian et al., 1973).
6.36 Scandium The highest scandium concentration recorded in marine molluscs was 0.76 mg Sc/kg DW in mussel soft parts (Table 6.18).
6.37 Selenium Maximum selenium concentrations in molluscan tissues were 11.1 mg Se/kg FW in mussel soft parts and 16.0 mg Se/kg DW in squid liver (Table 6.19). Selenium reportedly protects against mercury damage. Mercury-induced DNA damage in hemocytes of mussels, M. edulis, was produced in three days at 0.02 mg Hg2+/L; however, effects were reduced with added selenium, as selenite, at 0.004 mg Se/L (Tran et al., 2007). Selenium pre-exposure also provided some protection against mercury-induced DNA damage. Glutathione peroxidase
296 Chapter 6 Table 6.18: Scandium Concentrations in Field Collections of Molluscs Organism
Concentration
Reference
Clam, Ensis arcuatus; shell
0.005 DW
1
Clam, Ensis siliqua; shell
0.008 DW
1
Common mussel, Mytilus edulis Shell Soft parts Soft parts
0.004 DW 0.019 DW 0.005-0.76 DW
1 1 2
Pteropods; tests
0.028-0.247 DW
2
Squid, whole
0.01 AW
3
a
Values are in mg Sc/kg dry weight (DW) or ash weight (AW). a 1, Bertine and Goldberg, 1972; 2, Turekian et al., 1973; 3, Robertson, 1967.
Table 6.19: Selenium Concentrations in Field Collections of Molluscs Organism
Concentration
Reference
Cockle, Anadara trapezia; soft parts; April 2000; New South Wales, Australia
Max. 3.7 DW
11
Giant squid, Architeuthis dux; 2001-2005; Spain Hepatopancreas Branchial heart
13.0 DW 9.0 DW
16 16
Bivalves Muscle Viscera
1.1-2.3 DW 1.6-2.5 DW
9 9
Bivalves; edible portions; 3 spp. Total selenium Selenate Selenite plus selenide
0.22 (0.16-0.31) FW 0.05 FW 0.17 FW
6 6 6
American oyster, Crassostrea virginica; soft parts; Pensacola, Florida; 2003-2004
Max. 0.95 FW
Clam, Ensis arcuatus; shell
0.06 DW
1
Clam, Ensis siliqua; shell
0.03 DW
1
Greenland; bivalves; 1975-1991; 3 spp.; soft parts
0.2-0.9 FW
8
a
13
(Continues)
Molluscs 297 Table 6.19:
Cont’d
Organism
Concentration
Molluscs; commercial species; edible tissues 2 spp. 9 spp. 7 spp.
0.1-0.3 FW 0.3-0.5 FW 0.5-0.9 FW
Molluscs; 5 spp.; soft parts; 2001; Chile, Strait of Magellan; 17 stations
a
Reference 2 2 2
0.15-0.29 FW
12
Common mussel, Mytilus edulis Shell Soft parts Soft parts Gills Viscera
0.046 DW 4.5 DW 1.3-9.9 DW 2.0-16.0 DW Max. 5.0 DW
1 1 3 7 7
Pacific blue mussel, Mytilus edulis trossulus; 2004; soft parts; Adak Island, Alaska; 5 sites
0.9 FW; max. 11.1 FW; 2.2-8.8 DW
10
Mussel, Mytilus galloprovincialis; Adriatic Sea; 2001-2005; winter vs. summer
3.3-4.4 DW vs. 1.7-2.0 DW
18
Octopus, Octopus vulgaris; Portugal; 1999-2002; 3 sites Digestive gland Branchial heart Gill Muscle
8.3-11.0 DW 6.9-9.8 DW 1.9-2.2 DW 1.3-1.7 DW
19 19 19 19
Oyster, Ostrea edulis Soft parts Soft parts
1.7-2.9 DW <0.5 FW
4 5
Limpet, Patella candei gomesii; soft parts; 2007; Azores Near hydrothermal vent Reference site
0.40-0.45 DW 0.8 DW
14 14
Squid, Todarodes pacificus; Japan Sea; summer Muscle Gill Stomach Hepatopancreas Liver
1.6 DW 0.4 DW 4.9 DW 4.1 DW 16.0 DW
15 15 15 15 16
Values are in mg Se/kg fresh weight (FW) or dry weight (DW). a 1, Bertine and Goldberg, 1972; 2, Hall et al., 1978; 3, Karbe et al., 1977; 4, Fukai et al., 1978; 5, Lande, 1977; Cappon and Smith, 1982; 7, Stump et al., 1979; 8, Dietz et al., 1996; 9, Maher, 1983; 10, Burger and Gochfeld, 2006; 11, Burt et al., 2007; 12, Espana et al., 2007; 13, Karouna-Renier et al., 2007; 14, Cunha et al., 2008; 15, Waska et al., 2008; 16, Bustamante et al., 2008; 17, Arai et al., 2004; 18, Fattorini et al., 2008; 19, Napoleao et al., 2005.
298 Chapter 6 activity increased with added selenite, suggesting that selenium availability could offset the antioxidant status of mussels and levels of DNA damage (Tran et al., 2007). Dietary uptake is the dominant pathway for selenium accumulation in clams; interspecies differences are attributed, in part, to different food ingestion rates (Lee et al., 2006). Radioselenium-75 uptake from diet or medium and subsequent retention was determined for the clams C. fluminea and Potamocorbula amurensis (Lee et al., 2006). Corbicula assimilated 75Se from labeled diatoms more efficiently (66-87%) than selenium associated with sediments (20-37%); for Potamocorbula, there was no difference between food types (19-60%). Temperature and selenium of the medium had little effect on selenium assimilation from ingested food, but were significant in uptake from the medium. Influx of selenite increased by a factor of 3 when temperature increased from 5 to 21 C for Corbicula, but salinity between 4 and 21 ppt had no effect; for Potamocorbula, uptake decreased with increasing salinity (Lee et al., 2006). Diet is also the major route of selenium intake by the common mussel (M. edulis). Studies with radioselenium-75 demonstrated that selenium efficiency was 28-34% from the diet and 0.03% from the medium (Wang et al., 1996). It was concluded that 96% of the selenium in mussels is obtained from ingested food under conditions typical of coastal waters (Wang et al., 1996). Uptake from seawater by tissues of the squid, T. pacificus, captured in the East Japan Sea during summers—as judged by BCF values—ranged from 20,000 in muscle to 110,000 in hepatopancreas; intermediate values were estimated for stomach (62,000) and gill (84,000) (Waska et al., 2008). Uptake and retention of radioselenium-75 was studied in the pygmy mussel, X. securis (Alquezar et al., 2007). During the uptake phase of 388 h, whole mussels concentrated 75Se from seawater by a factor of 162. During the loss phase of 189 h in 75Se-free media, 71% was lost. The short-lived component had a biological halftime of 34 h; for the long-lived component, this was 555 h (Alquezar et al., 2007). Gravid cuttlefish, S. officinalis, were fed crabs radiolabeled with 75Se for 2 weeks to determine rate of maternal transfer into eggs; during embryonic development 75Se was progressively transferred to the embryo, and also to juveniles after hatching (Lacoue-Labarthe et al., 2008b). Residue data for selenium in bivalve molluscs should be interpreted with caution. For example, Fowler and Benayoun (1976a,b) in studies on selenium uptake by M. galloprovincialis demonstrated the following: mussels selectively accumulate tetravalent selenium salts over hexavalent species; the smallest mussels (2.1 g FW) concentrate selenium from solution by a factor of 46 versus 29 for intermediate weight (13.2 g), and 13 for the largest (21.8 g) mussels; visceral mass had the highest selenium burdens, followed by gill, muscle, and mantle tissues, in that order; and mussels did not reach equilibrium with the medium during exposure for 9 weeks. Differences among molluscan species should also be considered in the interpretation of selenium residues. Adult oysters, as one case, accumulate radioselenium to a greater degree than other species of
Molluscs 299 bivalve filter feeders examined, and this may prove useful in monitoring pollution due to selenium radionuclides (Patel and Ganguly, 1973). Incidentally, embryos of the Pacific oyster, C. gigas, were relatively insensitive to selenium salts; concentrations required to produce 50% abnormalities in 48 h being greater than 10.0 mg Se/L (Glickstein, 1978). The accuracy and precision of analytical methodologies in trace metal and metalloid determination needs to be considered. In one interlaboratory analysis of selenium in homogenates of oyster, Ostrea edulis, from France, involving 87 laboratories, “acceptable” (viz., within two standard deviations of the mean) results ranged from 1.7 to 2.9 mg Se/kg DW (Fukai et al., 1978). On this basis, at least one laboratory would have reported a result near 1.1 or 3.3 mg Se/kg DW homogenate, and these values may have little worth in enforcement or abatement actions regarding water quality criteria for selenium. However, additional laboratory intercalibration studies are continually in progress using a variety of biological matrices, sample preparation techniques, and instrumentations.
6.38 Silicon Soft parts of the American oyster, C. virginica, from Savannah, Georgia in November 2000 and November 2001 collected at nine sites contained 241.0-381.0 mg Si/kg DW (Kumar et al., 2008; Sajwan et al., 2008).
6.39 Silver Of all trace metals tested to marine bivalve molluscs, silver is the most strongly accumulated (Luoma, 1994). Highest silver concentrations reported in tissues of marine molluscs, in mg Ag/kg DW, were 113.0 in soft parts of the mussel P. canaliculus, 129.0 in gills of the abalone H. rufescens, 133.0 in soft parts of the Baltic clam M. balthica, 166.0 in kidney of the scallop C. radula, 185.0 in soft parts of the clam S. plana, and 320.0 in digestive diverticula of the whelk B. canaliculatum (Table 6.20). Silver content in molluscan tissues varies widely among closely related species as well as conspecifics collected from different locations (Table 6.20). In general, the highest silver concentrations were in samples collected nearest port cities and river discharges (Berrow, 1991; Fowler and Oregioni, 1976), electroplating plant outfalls (Eisler et al., 1978; Stephenson and Leonard, 1994), ocean dumpsites (Greig, 1979), urban point sources (Alexander and Young, 1976; Anderlini, 1992; Crecelius, 1993; Martin et al., 1988), and from calcareous sediments rather than detrital organic or iron oxide sediments (Luoma and Jenne, 1977). Seasonal (Fowler and Oregioni, 1976) and latitudinal (Anderlini, 1974) trends were also in evidence. Seasonal variations in silver concentrations of the Baltic clam, M. balthica, were associated with seasonal variations in moisture content of soft tissues, and frequently (66-87%) reflected the silver content in the surrounding sediments (Cain and
300 Chapter 6 Table 6.20: Silver Concentrations in Field Collections of Molluscs Organism
Concentration
Gastropod, Acmaea digitalis Shell Soft parts
6.3-11.1 DW 2.4-2.6 DW
1 1
Clam, Anodonta sp. Shell Soft parts
0.15 DW 0.28 DW
2 2
Giant squid, Architeuthis dux; 2001-2005; Spain Gill Hepatopancreas; Bay of Biscay vs. Mediterranean Sea
Reference
1.0 DW 1.9 DW vs. 14.0 DW
58 58
Hydrothermal vent mussel, Bathymodiolus azoricus; mid-Atlantic ridge; 2001; 5 sites Gills Mantle Digestive gland
1.8-5.2 DW 0.1-0.7 DW 0.5-0.9 DW
56 56 56
Whelk, Buccinum undatum Shell Soft parts
0.11 DW 0.58 DW
2 2
Whelk, Busycon canaliculatum Muscle Digestive gland Gills Digestive diverticula
0.1-0.18 FW 6.4-19.7 FW 0.53 DW 320.0 DW
3 3 4 4
Cockle, Cardium edule Shell Soft parts
0.11 DW 0.04 DW
2 2
Cockle, Cerastoderma edule; soft parts
1.5 (0.11-6.5) DW
5
Scallop, Chlamys opercularis Soft parts Kidneys Digestive gland
10.4 DW 35.0 DW 77.0 DW
6 6 6
Mussel, Choromytilus meridionalis; soft parts
0.3 DW
7
Scallop, Comptopallium radula; Santa Marie Bay (metals-contaminated), New Caledonia; October 2004 Soft parts Kidney
5.2 (3.9-6.5) DW 160.0 DW
a
55 55 (Continues)
Molluscs 301 Table 6.20:
Cont’d
Organism
Concentration
Reference
Clam, Corbicula sp.; San Francisco Bay; 1983-1986; soft parts
0.07-0.2 DW
Pacific oyster, Crassostrea gigas; soft parts
1.9 DW
8
Oyster, Crassostrea margaritacea; soft parts
2.6 DW
8
American oyster, Crassostrea virginica Soft parts; United States East coast Gulf coast Connecticut Georgia Northeast Louisiana Gulf coast Maryland, Chesapeake Bay; 1986-1988 Gills
0.3-5.0 DW 0.59-6.0 DW 6.1 FW 28.0-82.0 DW 0.8-2.3 FW 1.0-5.0 DW 0.6-6.0 DW; max. 7.0 DW 2.0-6.0 DW 5.9 FW
9, 9 10, 11 12 32, 9, 37 10
Cephalopods; 7 spp.; digestive gland
3.0-46.0 DW
33
a
34
Cephalopods; coast of France on English Channel; October 1978 Octopus, Eledone cirrhosa Digestive gland Digestive tract Other tissues Whole Cuttlefish, Sepia officinalis Digestive gland Kidney Other tissues Whole
2.0-4.4 DW 0.6 DW <0.3 DW 0.8 DW
33 33 33 33
4.9-7.4 DW 0.7 DW <0.3 DW 0.7 DW
33 33 33 33
Limpet, Crepidula fornicata Shell Soft parts
0.1 DW 0.97 DW
2 2
Clam, Ensis arcuata; shell
0.022 DW
13
Clam, Ensis siliqua; shell
0.017 DW
13
Abalone, Haliotis rufescens Gills Mantle Digestive gland Foot
13.0-129.0 DW 16.0-54.0 DW 14.0-60.0 DW 1.1-44.4 DW
14 14 14 14
45 50
39 35, 36
(Continues)
302 Chapter 6 Table 6.20: Cont’d Organism
Concentration
Reference
Abalone, Haliotis tuberculata; soft part
2.9 DW
15
Limpet, Littorina littorea Soft parts Soft parts; Looe estuary, United Kingdom, vs. reference site; 1988
19.6 (3.2-73.0) DW 10.7 (3.1-17.4) DW vs. 4.1 (3.4-5.0) DW
5 38
Squid, Loligo opalescens; liver; California Central coast Southern coast
25.0 DW 45.0 DW
16 16
Baltic clam, Macoma balthica Soft parts Soft parts; San Francisco Bay; near sewage site vs. reference site
85.0 (19.0-128.0) DW 32.0-133.0 DW vs. <1.0 DW
5 39, 40
Hardshell clam, Mercenaria mercenaria Body Gills Shell Soft parts
0.4 FW 1.6 FW 0.21 DW 1.3 DW
10 10 2 2
Mussel, Modiolus modiolus Soft parts Mantle and gills Muscle Gonad Gut and digestive gland
0.26 DW 0.24 DW 0.03 DW 0.07 DW 0.81 DW
2 2 2 2 2
Molluscs; 21 commercial species; edible portions 10 spp. 5 spp. 3 spp. 3 spp.
<0.1 FW 0.1-0.3 FW 0.3-0.7 FW 0.44-3.8 DW
17 17 17 18
Molluscs; South San Francisco Bay; 1982; soft parts; maximum values Mud snail, Nassarius obsoletus Clam, Macoma nasuta Softshell clam, Mya arenaria Clam, Tapes japonica
320.0 DW 5.1 DW 34.0 DW 65.0 DW
40 40 40 40
Softshell clam, Mya arenaria; soft parts
0.3 FW
10
a
(Continues)
Molluscs 303 Table 6.20: Organism California mussel, Mytilus californianus Soft parts California United States West coast Digestive gland Shell Soft parts; California Bodega Bay; 1976-1978 vs. 1986-1988 Coast; 1977-1981 vs. 1989-1991 San Diego Bay; near municipal wastewater outfall vs. reference sites in northern California and Baja California, Mexico San Francisco Bay; 1987; North Bay vs. South Bay Common mussel, Mytilus edulis Soft parts North Sea United States West coast United States West coast; rural sites vs. urban areas United States East coast United States East coast; rural sites vs. urban areas Rhode Island; Narragansett Bay; 1976-1978 vs. 1986-1988 Scheldt estuary, Europe; March 2000 Belgium Connecticut, United States Looe estuary, United Kingdom United Kingdom Norway California, United States Ireland; February 1990; contaminated site (Cork Harbour) vs. reference sites (east coast of Ireland) Shell Shell Shell Shell
Cont’d
Concentration
Reference
<1.0-5.5 DW 0.1-2.0 DW 0.7-33.0 DW 5.0-7.9 DW
1 9 19 1
0.15 DW vs. 0.1 DW
41
Max. 10.0-70.0 DW vs. <2.0 DW 59.0 DW vs. 0.08-0.22 DW
42
a
43
0.04-0.16 DW vs. 0.7-2.9 DW
40
0.02-1.2 DW 0.3-2.3 DW 0.1 DW vs. max. 5.0 DW
20 9 45
0.04-0.7 DW 0.3 DW vs. max. 2.0 DW
9 45
0.2 DW vs. 0.22 DW
41
1.5 DW 0.15 DW 0.2 FW 0.23 (0.10-0.55) DW 0.03 DW 1.0-6.0 DW <1.0-1.3 DW 0.08-4.3 DW vs. <0.05-1.0 DW
57 13 10 5 2 21 1 44
0.006 DW 0.1 DW 2.0-4.0 DW 4.4-6.3 DW
13 2 21 1 (Continues)
304 Chapter 6 Table 6.20: Cont’d Organism
Concentration
Reference
Mussel, Mytilus edulis aoteanus Soft parts Mantle Gill Visceral mass Gonad Soft parts; New Zealand; 1986-1987; various distances (meters) from sewage outfall 50 100 200 750 1500 3000
0.1 DW 0.4 DW 1.0 DW 0.2 DW 0.1 DW
22 22 22 22 22
5.3-7.7 DW 4.2 DW 3.9 DW 3.5-4.1 DW 2.9 DW 2.7-3.4 DW
46 46 46 46 46 46
Mussel, Mytilus galloprovincialis Soft parts Soft parts
0.76 DW 0.9 (0.3-7.1) DW
23 53
Whelk, Nucella lapillus; soft parts
2.7 (1.3-4.2) DW
5
Squid, Ommastrephes bartrami; liver
12.0 DW
16
Oyster, Ostrea edulis Soft parts Homogenate
6.4 DW 4.9-7.7 DW
8 24
Octopus, Octopus cyanea; June 1998; Guam; tentacle vs. liver
<0.12 DW vs. 4.4 DW
52
European flat oyster, Ostrea edulis; soft parts
2.9 (0.4-9.7) DW
53
Oyster, Ostrea equestris; soft parts; United States East coast West coast
18.9 DW 0.7-1.6 DW
Oyster, Ostrea sinuata Soft parts Mantle Gill Muscle Visceral mass Kidney
5.6 DW 4.8 DW 4.6 DW 1.8 DW 68.0 DW 1.0 DW
a
9 9 22 22 22 22 22 22 (Continues)
Molluscs 305 Table 6.20: Organism Heart Shell
Cont’d
Concentration
Reference
48.0 DW <0.1 DW
22 22
Limpet, Patella vulgata. Soft parts Shell Soft parts Soft parts Soft parts vs. shell; Israel; 1973 Near sewage outfalls Reference site 80 km north of outfall
<0.1-4.0 DW 4.0-5.0 DW 3.0 (1.5-6.0) DW 2.1 DW
21 21 5 25
6.7 DW vs. 5.7 DW 1.2 DW vs. 5.3 DW
47 47
Scallop, Pecten maximus Soft parts Kidneys Digestive gland Gut and digestive gland Mantle and gills
2.7 DW 4.3 DW 13.6 DW 8.9 DW 0.4 DW
6 6 6 2 2
Scallop, Pecten novae-zelandiae Soft parts Mantle Gills Muscle Visceral mass Intestine Kidney Foot Gonad Shell
0.7 DW 0.2 DW 1.0 DW <0.1 DW 1.8 DW 2.9 DW 4.8 DW 1.1 DW 0.2 DW <0.1 DW
22 22 22 22 22 22 22 22 22 22
Mussel, Perna canaliculus; soft parts; New Zealand; 1986-1987; distance from sewage outfall, in meters 200 750 1500-3000
35.0-113.0 DW 49.0-85.0 DW 8.0-13.0 DW
46 46 46
Clam, Pitar morrhuana; soft parts
1.2-4.6 DW
26
Giant scallop, Placopecten magellanicus Soft parts Muscle Gonads Visceral mass
1.8 DW <0.08-0.24 FW 0.13-0.69 FW 0.22-1.9 FW
27, 28 29 29 29
a
(Continues)
306 Chapter 6 Table 6.20: Cont’d Organism
Concentration
Reference
Max. 9.1 DW vs. <0.1 DW
39
Clam, Potamocorbula amurensis; San Francisco Bay; 1991-1992
2.2 (0.3-7.0) DW; BCF of about 366,000
48
Clam, Protothaca staminea Soft parts Shell
<1.0 DW 5.8 DW
Soft parts; ocean disposal site vs. reference site
Oysters, Saccostrea spp.; Australia; 1980-1983; soft parts
a
1 1
Max. 0.4 FW
49
0.8 DW 0.4 DW 0.1-1.5 (0.03-2.1) DW vs. 4.0-5.8 (1.1-185.0) DW 0.2 (0.03-0.38) DW 0.38 (<0.1 to 1.1) DW 0.23-1.2 DW 1.4 DW 0.5 DW 0.67 DW 1.58 DW <0.1 DW 0.24 DW
33 33 5, 30, 37, 38, 51 30 30 31 31 31 31 31 31 31
0.55 DW 0.35 DW
31 31
1.8 DW 0.25 DW
31 31
Clam, Scrobicularia plana Digestive gland Kidney Soft parts; reference site vs. silvercontaminated estuary Soft parts Digestive gland Soft parts Digestive gland Mantle and siphons Foot and gonad Gills and palps Adductor muscle Kidney Camel estuary Digestive gland Remaining tissues Transferred from Camel estuary to Gannel estuary for 352 days Digestive gland Remaining tissues Gannel estuary Digestive gland Remaining tissues Transferred from Gannel estuary to Camel estuary for 352 days Digestive gland Remaining tissues
2.0 DW 0.28 DW
31 31
0.43 DW 0.22 DW
31 31
Common cuttlefish, Sepia officinalis Egg Eggshell
0.07 DW
54 (Continues)
Molluscs 307 Table 6.20: Organism Embryo Yolk Hatchlings Whole Cuttlebone Juveniles age 1 month Whole Digestive gland Cuttlebone Immatures, age 12 months Whole Digestive gland Cuttlebone Adults, age 18 months Whole Digestive gland Cuttlebone
Cont’d
Concentration
Reference
0.16 DW 0.22 DW
54 54
1.8 DW 0.03 DW
54 54
1.4 DW 14.0 DW 0.1 DW
54 54 54
1.8 DW 19.0 DW 0.08 DW
54 54 54
0.6 DW 13.4 DW 0.08 DW
54 54 54
Clam, Spisula solidissima; muscle
0.39-1.3 DW
Squid, Symplectoteuthis oualaniensis; liver
24.0 DW
16
Clam, Tapes semidecussata Shell Soft parts
7.3 DW 7.3 DW
1 1
Gastropod, Thais emarginata Shell Soft parts
6.4-11.1 DW 2.1 DW
1 1
a
3, 4
Values are in mg Ag/kg fresh weight (FW) or dry weight (DW). a 1, Graham, 1972; 2, Segar et al., 1971; 3, Greig et al., 1977; 4, Greig, 1975; 5, Bryan and Hummerstone, 1977; 6, Bryan, 1973; 7, Watling and Watling, 1976b; 8, Watling and Watling, 1976a; 9, Goldberg et al., 1978; 10, Thurberg et al., 1974; 11, Windom and Smith, 1972; 12, Greig and Wenzloff, 1978; 13, Bertine and Goldberg, 1972; 14, Anderlini, 1974; 15, Bryan et al., 1977; 16, Martin and Flegal, 1975; 17, Hall et al., 1978; 18, Greig, 1979; 19, Alexander and Young, 1976; 20, Karbe et al., 1977; 21, Lande, 1977; 22, Brooks and Rumsby, 1965; 23, Fowler and Oregioni, 1976; 24, Fukai et al., 1978; 25, Preston et al., 1972; 26, Eisler, 1977b; 27, Pesch et al., 1977; 28, Reynolds, 1979; 29, Greig et al., 1978; 30, Bryan and Uysal, 1978; 31, Bryan and Hummerstone, 1978; 32, Ramelow et al., 1989; 33, Miramand and Bentley, 1992; 34, Luoma et al., 1990; 35, Morse et al., 1993; 36, Presley et al., 1990; 37, Sanders et al., 1991b; 38. Truchet et al., 1990; 39, USPHS, 1990; 40, Luoma and Phillips, 1988; 41, Lauenstein et al., 1990; 42, Stephenson and Leonard, 1994; 43, Martin et al., 1988; 44, Berrow, 1991; 45, Crecelius, 1993; 46, Anderlini, 1992; 47, Navrot et al., 1974; 48, Brown and Luoma, 1995; 49, Talbot, 1985; 50, Thurberg et al, 1974; 51, Bryan and Hummerstone, 1977; 52, Denton et al., 2006; 53, Deudero et al., 2007; 54, Miramand et al., 2006; 55, Metian et al., 2008; 56, Cosson et al., 2008; 57, Wepener et al., 2008; 58, Bustamante et al., 2008.
308 Chapter 6 Luoma, 1990). Inherent differences among species in ability to accumulate silver from seawater are well-documented, with oysters >> scallops >> mussels (Brooks and Rumsby, 1965). Even closely related species of scallops collected from the same area differed in silver content of individual tissues by 3- to 9-fold (Bryan, 1973). Internal organs, especially digestive gland and kidney, usually contained the highest burdens of silver in all species of molluscs examined (Table 6.20). Studies with radiosilver-110 m suggest that the half-time persistence of silver is 27 days in mussels, 44-80 days in clams, and more than 180 days in oysters (Fisher et al., 1994; Preston et al., 1968). In oysters and other bivalve molluscs, the major pathway of silver accumulation was from dissolved silver. Uptake was negligible from silver adsorbed onto suspended sediments and algal cells, with elimination of adsorbed silver by oysters via the feces (Abbe and Sanders, 1990; Sanders et al., 1990). In oysters, silver associated with food was unavailable for incorporation, which may be due to the ability of silver to adsorb rapidly to cell surfaces and to remain tightly bound despite changes in pH or enzymatic activity (Connell et al., 1991). Studies with 110mAg and clams, G. tumidum, held for 15 days in seawater containing radiosilver had concentration factors of 4000-15,000 in soft parts; concentration factors were lower for smaller clams and higher for larger clams— which differs significantly from studies with the same species and isotopes of cadmium, cobalt, chromium, and zinc, wherein smaller clams had highest concentration factors (Hedouin et al., 2006). Uptake of dissolved silver by oysters was higher at elevated temperatures in the 15-25 C range tested (Abbe and Sanders, 1990). American oysters, C. virginica, maintained near a nuclear power plant in Maryland that discharged radionuclides on a daily basis into Chesapeake Bay accumulated 110mAg; accumulations were higher in summer and fall than in winter or spring (Rose et al., 1988). Oysters from the Gulf of Mexico vary considerably in whole-body content of silver and other trace metals. Variables known to modify silver concentrations in oyster tissues include the age, size, gender, reproductive stage, general health and metabolism of the oyster, water temperature and salinity, dissolved oxygen and turbidity of the medium, natural and anthropogenic inputs to the biosphere, and chemical species and interactions with other compounds (Presley et al., 1990). For example, silver concentrations in American oysters from the Chesapeake Bay were reduced in summer and at increasing water salinities, and were elevated near sites of human activity; chemical forms of silver taken up by oysters included the free ion (Ag+)and the uncharged AgCl0 (Daskalakis, 1995; Sanders et al., 1991a). Declines in tissue silver concentrations of the California mussel, M. californianus, were significant between 1977 and 1990; body burdens decreased from 10.0-70.0 mg Ag/kg DW to less than 2.0 mg/kg DW and seem to be related to the termination of metal-plating facilities in 1974 and decreased mass emission rates by wastewater treatment facilities (Stephenson and Leonard, 1994). Laboratory studies on silver accumulation and effects in marine gastropods, mussels, clams, scallops, and oysters is the subject of a growing number of studies. In one series, Thurberg
Molluscs 309 et al. (1974) immersed American oysters, C. virginica, common mussels, M. edulis, and hardshell clams, M. mercenaria, in seawater solutions containing 1.0 mg Ag/L for 96 h. Whole-body silver burdens—in mg Ag/kg FW—rose during this period from 0.2 to 5.2 in mussels, from 0.4 to 1.0 in clams, and from 6.1 to 14.9 in oysters. Silver content in gill tissues during this interval rose from 5.9 mg/kg FW to 33.9 in oysters, and from 1.6 to 6.9 in clams. In a second series, Thurberg et al. (1975) exposed adult surf clams, Spisula solidissima, to 0.01 or 0.1 mg Ag/L for 96 h. Whole-body tissue concentrations in surf clams rose from 0.08 mg Ag/kg FW in controls to 1.0 in the low dose group and 2.0 in the high dose group; for gills, silver values were 5.7 mg/kg FW in the low dose group and 8.5 in the high dose group. Bivalve molluscs, especially oysters, took up radiosilver-110 from the medium by factors as high as 500- to 32,000-fold (Pouvreau and Amiard, 1974); these values were lower for gastropods. Gastropod sea hares Aplysia californica were exposed to 0.001 or 0.01 mg Ag/L for 48 h (Bianchini et al., 2007). Afterwards, digestive gland contained 3.6 mg Ag/kg FW in the high dose group. Silver burdens in the high dose group were lowest in hemolymph, muscle, ganglia, and gills in that order, and highest in digestive gland (Bianchini et al., 2007). Slipper limpets (Gastropoda), C. fornicata, subjected to silver concentrations as low as 0.001 mg/L for up to 24 months showed histopathological damage and accumulations up to 34.0 mg Ag/kg FW soft parts; higher exposure concentrations of 0.005 and 0.01 mg Ag/L were associated with inhibited reproduction and whole-body burdens as high as 87.0 mg Ag/ kg FW (Nelson et al., 1983). Maximum silver concentrations for the 0.005 mg Ag/L group after 6 months was 54.1 mg Ag/kg FW soft parts versus 2.8 in controls; after 24 months this was less than 8.0 mg/kg FW soft parts (Nelson et al., 1983). Respiration rate in gastropods was depressed by ionic silver; however, the reverse was observed in six species of bivalves tested (Gould and MacInnes, 1977). In marine gastropods, L. littorea, silver is stored in the basement membrane of the digestive system (Truchet et al., 1990). Asiatic clams, C. fluminea, held in seawater containing 0.0045 mg Ag/L for 21 days showed growth inhibition; residues of 1.65 mg Ag/kg FW soft parts and higher were associated with reduced growth (Diamond et al., 1990). The LC50 (96 h) value for juveniles of the Asiatic clam followed by a 96 h observation period was 0.155 mg Ag/L (Diamond et al., 1990). Juveniles of the surf clam, S. solidissima, had increased oxygen consumption at 0.01 mg Ag/L after 96 h (Calabrese et al., 1977b) and abnormal embryo development at 0.014 mg/L following 1 h exposure after fertilization (Bryan and Langston, 1992); 0.1 mg/L was lethal to juveniles in 96 h (Calabrese et al., 1977a,b). In clams, S. plana, silver is stored in the basement membrane of the outer fold of the mantle edge and in the amoebocytes (Truchet et al., 1990). Juvenile bay scallops, A. irradians, held in 0.01 mg Ag/L for 96 h contained 3.1 mg Ag/kg FW (Nelson et al., 1976). It is noteworthy that ionic silver is extremely toxic to molluscs, with concentrations lethal to 50% of bay scallops in 96 h as low as 0.033 mg Ag+/L (Nelson
310 Chapter 6 et al., 1976); similar results were reported for clams and oysters (Calabrese et al., 1977b). Scallops, Chlamys varia, held in seawater containing 0.02 mg Ag/L for 14 days had 18.0 mg Ag/kg DW in soft tissues versus 1.7 in controls (Berthet et al., 1992). The LC50 (115 h) value for C. varia is 0.1 mg Ag/L (Berthet et al., 1992). In scallops and mussels, silver was stored in basement membranes and pericardial gland. In all species of bivalve molluscs, sequestered silver was in the form of silver sulfide (Berthet et al., 1992). Trophic transfer of silver in mussels is dependent on the silver assimilation efficiency (AE) from ingested food particles, feeding rate, and silver efflux rate (Fisher and Wang, 1998). Silver AE is usually less than 30%, and is lower for sediment than for phytoplankton. Silver AE and distribution from ingested phytoplankton particles is modified by gut passage time, extracellular and intracellular digestion rates, and metal desorption at lowered pH. The kinetic model of Fisher and Wang (1998) for mussels predicts that either the solute or particulate pathway can dominate and is dependent on silver partition coefficients for suspended particles, and silver AE. Common mussels, M. edulis, exposed continuously for 21 months to 0.0 (controls), 0.001, 0.005, or 0.01 mg Ag/L from age 2.5 months, were observed for growth, accumulations, and histopathology (Calabrese et al., 1984). Growth was not affected. Silver burdens, in mg Ag/kg FW soft parts, for controls ranged from 0.2 to 0.7; maximum concentrations in the 0.001 mg/L group (9.1) occurred a 18 months; for the 0.005 mg/L group, residues were highest (11.9) at 18 months; for the 0.01 mg/L group, Concentrations were highest (15.3) at 12 months. All silver-exposed groups had histopathology of basement membranes and connective tissues; histopathology was typical of argyria in humans and other mammals that have absorbed organic or inorganic silver compounds (Calabrese et al., 1984). Adults of M. galloprovincialis had normal growth after 21-month exposure to 0.01 mg Ag/L; mussels held in 0.02 mg Ag/L for 28 days had 15.0 mg Ag/kg DW soft parts versus 0.08 in controls (Berthet et al., 1992). The LC50 (110 h) for M. galloprovincialis adults was 0.1 mg Ag/L (Berthet et al., 1992). Eggs of the cuttlefish, S. officinalis were exposed to both 110mAg and stable silver at 0.002 mg Ag/L during embryonic development; both stable silver and radiosilver continued to increase in eggs beginning at day 30 of embryonic development, owing to eggshell permeability to silver at that time (Lacoue-Labarthe et al., 2008a,b). Silver concentrations in juvenile cuttlefish, S. officinalis, were much higher than those in embryos (Table 6.20), suggesting efficient incorporation from seawater (Miramand et al., 2006). Silver concentrations in digestive gland, unlike other metals analyzed wherein burdens increase exponentially with age, decreases as soon as adult cuttlefish migrate to the open sea; suggesting that silver is excreted from digestive gland on contact with less contaminated environments (Miramand et al., 2006). Embryos of the Pacific oyster, C. gigas, held in 0.0020.01 mg Ag/L for 48 h had retarded shell growth, reduced size, and erratic swimming behavior in 5.8% of exposed groups versus 1% in controls (Coglianse and Martin, 1981).
Molluscs 311 Juvenile Pacific oysters held in 0.02 mg Ag/L for 14 days then transferred to uncontaminated seawater for 23 days had impaired glycogen storage capacity during exposure (Berthet et al., 1990). During depuration, silver concentrations decreased from 31.3 mg/kg DW soft parts to 12.8 versus <10.0 in controls. Most (69%-89%) of the insoluble accumulated silver was sequestered in amoebocytes and basement membranes as silver sulfide (Ag2S), a stable mineral form that is not degradable, thereby limiting the risk of silver transfer through the food chain (Berthet et al., 1990). The LC50 (209 h) value for silver and adult Pacific oysters was 0.1 mg/L (Berthet et al., 1992). Adults of the American oyster, C. virginica, held in 0.002 mg Ag/L for 14 days in natural enclosures containing phytoplankton showed reduced growth; phytoplankton had 8.6 mg Ag/kg DW (vs. 0.03 in controls) and oyster soft parts 2.8 mg/kg DW (vs. 0.8 in controls). Oysters and phytoplankton held in 0.005 or 0.007 mg Ag/L under similar conditions had 24.0-44.0 mg Ag/kg DW phytoplankton and 4.8-6.8 mg Ag/kg DW soft part oysters (Abbe and Sanders, 1990; Sanders et al., 1990). The LC50 (48 h) value for American oyster embryos was 0.0058 mg Ag/L (Calabrese et al., 1977b; Ratte, 1999). American oysters excrete about 60% of their accumulated excess silver in soft tissues within 30 days of transfer to silver-free seawater; soluble forms were preferentially eliminated and insoluble forms retained (Berthet et al., 1992). Interspecies differences in ability to retain silver among bivalve molluscs are large, even among closely related species of crassostreid oysters. For example, the half-time persistence of silver was 149 days in American oysters but only 26 days in Pacific oysters (USPHS, 1990). Silver interactions with other metals and compounds in solution are not well defined. For example, mixtures of salts of silver and copper markedly increased the survival of oyster embryos, but only when copper concentrations were less than 0.006 mg/L and total silver less than 0.011 mg/L (Coglianse and Martin, 1981). Silver interacts with salts of copper and cadmium in the green mussel, P. viridis in 2 week exposure studies (Ng et al., 2007). Mussels subjected to 0.005 mg Ag/L plus 0.02 mg Cd/L accumulated each metal in soft tissues, but independently. Interaction was observed at the subcellular level wherein 25% of the silver shifted from the insoluble fraction to the metallothionein-like protein in the presence of cadmium. Exposure to silver alone (0.005 mg Ag/L), for 2 weeks increased the dietary uptake of silver by 30%, although the effect was reduced in the presence of cadmium. Co-exposure of mussels to 0.005 mg Ag/L plus 0.03 mg Cu/L increased both silver and copper concentrations in soft parts by up to fivefold. Silver and copper subcellular distributions in co-exposed and singly exposed mussels were similar (Ng et al., 2007). Other studies with the green mussel show that 2.0 mg Ag/L is not fatal to adults in 96 h; however, there were significant decreases in filtration rate, oxygen consumption, and ATPase activity in gills, hepatopancreas, ovary, and muscle (Vijayavel et al., 2007). Water quality criteria for silver for the protection of marine molluscs are proposed. Bryan and Langston (1992) state that tissue concentrations less than 1.0 mg total Ag/kg DW soft
312 Chapter 6 parts is normal and presumably safe for marine clams; however, more than 100.0 mg total Ag/kg DW is stressful and possibly fatal. This needs to be further refined. The proposed silver criterion of 0.0023 mg total Ag/L to protect marine molluscs needs to be reconsidered because some species of molluscs show extensive accumulations at 0.001-0.002 mg total Ag/L (Eisler, 2000d).
6.40 Strontium Strontium concentrations in molluscs are highest in calcareous tissues, such as shell, and lowest in soft tissues (Table 6.21). Since the mean strontium to calcium ratios in pelycopods, amphineurans, scaphopods, and cephalopods all fall within the same narrow range of 0.00185-0.00806 (Thompson and Chow, 1955), it is probable that strontium residues closely parallel those of calcium concentrations in molluscan tissues. Mussels, M. galloprovincialis, show increasing concentrations of strontium with increasing growth; moreover, this species reportedly can distinguish between stable strontium and radiostrontium-90, with selective accumulation of the stable form (Parchevskii et al., 1965). No 90Sr activity was detectable in various species of molluscs collected near Amchitka Island in summer 2004; Amchitka Island was a nuclear test site between 1965 and 1971 (Burger et al., 2007b). Some molluscs were inefficient accumulators of strontium. Among five species of bivalves taken from coastal waters of Greece, strontium concentration factors in soft tissues ranged from 1 to 15 (Papadopoulu, 1973). This is not the case with fecal materials of some species. Feces of bivalves contribute significantly to the transfer of strontium to bottom sediments. The concentration of strontium in feces of hardshell clams, as one example, is increased by a factor of 670 over that in seawater; for softshell clams, however, this value was only 14 (Andrews and Warren, 1969).
6.41 Tantalum Soft tissues of the common mussel, M. edulis, contained between 0.004 and 0.33 mg Ta/kg DW (Karbe et al., 1977).
6.42 Technetium No 99Tc activity was detected in molluscs from the Aleutian Islands during summer 2004; Amchitka Island in the Aleutian chain was used for nuclear tests between 1965 and 1971 (Burger et al., 2007b).
Molluscs 313 Table 6.21: Strontium Concentrations in Field Collections of Molluscs Organism
Concentration
Reference
Mussel, Anodonta sp.; shell
150.0 DW
1
Gastropod, Aplysia benedicti Ctenidium Gonad Parapodia Hepatopancreas Buccal mass Gut content Shell
0.6-0.9 DW 2.5-3.0 DW 0.3 DW 5.0-7.0 DW 1.9 DW 0.8 DW 1300.0-1600.0 DW
2 2 2 2 2 2 2
Hydrothermal vent mussel, Bathymodiolus azoricus; mid-Atlantic ridge Shell; 2001; 4 sites
871.0-1063.0 (536.0-1261.0) DW
Whelk, Buccinum undatum Shell Soft parts
750.0 DW 13.0 DW
Cockle, Cardium edule Shell Soft parts
1300.0 DW 17.0 DW
Scallop, Chlamys opercularis; shell
270.0-410.0 DW
1
American oyster, Crassostrea virginica Shell Soft parts
1142.0-1648.0 DW 13.0-28.0 DW
3 4
Limpet, Crepidula fornicata Shell Soft parts
100.0 DW 20.0 DW
1 1
Gastropods Flesh Shell Viscera Operculum Shell
510.0 AW 2194.0 AW 84.0 AW 200.0 AW 860.0-2700.0 AW
5 5 5 5 6
Hardshell clam, Mercenaria mercenaria Shell Soft parts
170.0 DW 13.0 DW
1 1
Mussel, Modiolus modiolus Shell Soft parts
73.0 DW 30.0-47.0 DW
1 1
a
16 1 1
(Continues)
314 Chapter 6 Table 6.21: Cont’d Organism Mantle and gills Muscle Gonad Gut and digestive gland
Concentration
Reference
41.0 DW 23.0 DW 33.0 DW 41.0 DW
1 1 1 1
Molluscs Shell Shell Soft parts
1000.0 to <5000.0 DW 1540.0-4097.0 DW 0.04-0.77 FW
6 7 8
Softshell clam, Mya arenaria; soft parts
63.0-163.0 DW
9
Mussel, Mytilus californianus; soft parts
16.0-48.0 DW
4
Common mussel, Mytilus edulis Soft parts Soft parts Soft parts
18.0-100.0 DW 19.0-56.0 DW 24.0 DW
10 4 1
Whelk, Nucella lapillus Shell Soft parts
1200.0 DW 79.0 DW
Limpet, Patella candei gomesii; soft parts; 2007; Azores Near hydrothermal vent Reference site
63.3-84.7 DW 111.3-154.3 DW
Limpet, Patella vulgata Shell Soft parts
570.0 DW 23.0 DW
1 1
Scallop, Pecten maximus Soft parts Muscle Gut and digestive gland Mantle and gills Gonad Shell
12.0 DW 9.9 DW 13.0 DW 11.0-16.0 DW 12.0-23.0 DW 270.0-660.0 DW
1 1 1 1 1 1
Scallop, Pecten sp.; shell
660.0-1200.0 DW
6
Bivalve, Pinna nobilis Soft parts Mantle and gills Muscle Nervous system
2300.0 AW 830.0 AW 1400.0 AW 3300.0 AW
a
1 1
15 15
11 11 11 11 (Continues)
Molluscs 315 Table 6.21: Organism Stomach and intestine Gonads Hepatopancreas Byssus Byssus gland
Cont’d
Concentration
Reference
2900.0 AW 1600.0 AW 600.0 AW 2200.0 AW 4700.0 AW
11 11 11 11
Pteropods Shell Shell
220.0-620.0 DW 950.0-1400.0 DW
12 13
Clam, Tapes japonica Soft parts Shell
110.0-360.0 AW 1700.0-1900.0 AW
14 14
a
Values are in mg Sr/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Segar et al., 1971; 2, Patel et al., 1973; 3, Rucker and Valentine, 1961; 4, Goldberg et al., 1978; 5, Lowman et al., 1970; 6, Turekian and Armstrong, 1960; 7, Pilkey and Goodell, 1963; 8, Mauchline and Templeton, 1966; 9, Eisler, 1977b; 10, Karbe et al., 1977; 11, Papadopoulu, 1973; 12, Pyle and Tieh, 1970; 13, Krinsley and Bieri, 1959; 14, Fukai and Meinke, 1962; 15, Cunha et al., 2008; 16, Cravo et al., 2008.
6.43 Tellurium Tellurium concentrations in tissues of the squid, T. pacificus, captured in the East Japan Sea near Korea during summer were highest in hepatopancreas (0.0025 mg Te/kg DW) and stomach (0.0024 mg/kg DW), and lowest in muscle (0.0006 mg Te/kg DW) and gill (0.0001 mg/kg DW) (Waska et al., 2008). BCF values from seawater are estimated at 5800 for muscle, 5900 for stomach, 16,000 for gill, and 22,000 for hepatopancreas (Waska et al., 2008).
6.44 Terbium Terbium concentrations in soft tissues of the common mussel ranged from 0.006 to 0.03 mg Tb/kg DW (Karbe et al., 1977).
6.45 Thallium Laboratory studies on thallium accumulation from the medium by the softshell clam and the common mussel were conducted by Zitko and Carson (1975). These studies demonstrated that clams accumulated 6.0 mg Tl/kg DW soft parts in 88 days from solutions containing 0.05 mg Tl/L; this value was 12.5 mg Tl/kg DW when environmental thallium levels were doubled to 0.1 mg/L. On transfer to thallium-free media for 30 days, clam
316 Chapter 6 soft parts contained less than 0.5 mg Tl/kg DW. Exposure of M. edulis for 40 days in seawater solutions containing 0.05 or 0.1 mg Tl/l produced thallium accumulations of 4.3 and 6.3 mg Tl/kg DW soft parts, respectively; thallium levels in mussels fell to less than 0.5 mg/kg DW within 7 days postexposure (Zitko and Carson, 1975).
6.46 Thorium The maximum thorium concentration recorded in field collections of molluscs was 0.26 mg Th/kg DW in mussel soft parts (Table 6.22).
6.47 Tin Inorganic tin concentrations up to 2.0 mg Sn/kg FW were recorded in edible tissues of commercial species of North American molluscs, and up to 35.0 mg Sn/kg FW in smoked canned oysters (Table 6.22). Organotin concentrations in edible tissues of 10 species of molluscs sold commercially in France in 2005 were usually less than 0.0076 mg total organotins/kg FW, but were somewhat higher in squid (0.0133 mg/kg FW) and scallop (0.0098 mg/kg FW); in all cases, TBTs accounted for the majority of all organotins (Table 6.22; Guerin et al., 2007). Larger bivalves (D. trunculus) collected from Alexandria, Egypt in 2004 have elevated concentrations of organotins and total tin when compared to smaller bivalves; intermediate sized groups had intermediate values (Table 6.22; Said et al., 2006). Organic tin compounds are used extensively in antifouling marine paints and in molluscicides (Crowe, 1987). The use of antifoulants on ships was necessitated by the damage some organisms cause to wooden structures and by the reduced fuel efficiency and speed due to drag when vessels become heavily fouled (Laughlin et al., 1984). Organotins replaced copper in antifouling paints because copper has a short effective life and is comparatively expensive. Organic compounds of arsenic, mercury, and lead have also been used in antifouling paints, but present unacceptable toxicological risks during preparation and to the environment (Blunden et al., 1985; Hall et al., 1987). Organotin coatings were promoted because of their efficient antifouling action, long lifetime (up to 4 years) and lack of corrosion (Messiha and Ikladious, 1986). Use of organotin antifouling paints on recreational and commercial vessels has increased markedly. In Maryland, for example, at least 50% and up to 75% of the recreational boats used in Chesapeake Bay are covered with organotin paints (Hall et al., 1988). However, organotin coatings, especially TBTs, present potential environmental problems to nontarget aquatic biota due to their extreme toxicity (Eisler, 2000e; Maguire, 1991). The organotin biocide released by hydrolysis from the surface of the paint film into seawater provides the antifoulant action. In consequence, the depleted outer layer of paint film, containing hydrophilic carboxylate groups, is easily eroded by moving
Molluscs 317 Table 6.22: Thorium, Tin, Titanium, Tungsten, and Uranium Concentrations in Field Collections of Molluscs Element and Organism
Concentration
Reference
a
Thorium Common mussel, Mytilus edulis; soft parts
0.0003-0.26 DW
1
Pteropods; tests
0.023-0.147 DW
2
Tin Bohai Bay, North China; May-September, 2002; soft parts Bay scallop, Argopecten irradians Monobutyltins Dibutyltins Tributyltins Triphenyltins Veined rapa whelk, Rapana venosa Monobutyltins Dibutyltins Tributyltins Triphenyltins Short-necked clam, Ruditapes philippinarum Monobutyltins Dibutyltins Tributyltins Triphenyltins Pacific oyster, Crassostrea gigas Arcachon Bay, France; July; soft parts; total tin vs. organotins; max. values 1982 1983 1985 Soft parts; reared for 16 weeks in sea cages painted with tributyltin Total tin Tributyltin Total tin (unpainted) Tributyltin; soft parts; coastal United Kingdom estuaries 1986 1987 1988 1989
0.009 FW 0.017 FW 0.025 FW 0.004 FW
32 32 32 32
0.004 FW 0.009 FW 0.005 FW 0.005 FW
32 32 32 32
0.004 FW 0.005 FW 0.004 FW 0.003 FW
32 32 32 32
7.0 DW vs. 1.6 DW 4.0 DW vs. 0.8 DW 0.9 DW vs. 0.4 DW
10 10 10
1.4 FW 0.9 FW 0.1 FW
11 11 11
0.2-6.4 DW 0.3-3.7 DW 0.1-5.6 DW 0.1-1.3 DW
12 12 12 12 (Continues)
318 Chapter 6 Table 6.22: Cont’d Element and Organism Korea; January 1995; soft parts Tributyltins Triphenyltins American oyster, Crassostrea virginica Soft parts; Gulf of Mexico; 1989-1991; max. values Monobutyltins Dibutyltins Tributyltins Soft parts; Pensacola, Florida; 20032004 Bivalve, Donex trunculus; Alexandria, Egypt; 2004; soft parts; shell length 1.5 cm vs. 2.5 cm Dibutyltins Tributyltins Diphenyltins Total tin
Concentration
Reference
0.1-0.9 DW; 28% of total body burden in gonads 0.16-0.7 DW; 19% of total body burden in gonads
13
0.15 DW 0.2 DW 1.2 DW Max. 0.6 FW
12 12 12 28
0.011 DW vs. 0.028 DW 0.16 DW vs. 0.25 DW 0.041 DW vs. 0.066 DW 0.37 DW vs. 0.58 DW
24 24 24 24
a
13
France; January-April 2005; edible portions Total organotins; 8 spp. Squid Total organotins Butyltins Phenyltins Octyltins
<0.0076 FW
26
0.0133 FW 0.0123 FW 0.0006 FW 0.0003 FW
26 26 26 26
Scallop Total organotins Butyltins Phenyltins Octyltins
0.0098 FW 0.0086 FW 0.0008 FW 0.0003 FW
26 26 26 26
Gastropod, Hexaplex trunculus; December 2002-2003; Venice lagoon, Italy (organotin antifouling paints banned in 1990) vs. Istrian region, Croatia (no restrictions on organotin antifouling paints) Visceral coil Tributyltin
0.1 DW vs. 0.41 DW
23 (Continues)
Molluscs 319 Table 6.22: Element and Organism Dibutyltin Monobutyltin Monophenyltin Diphenyltin Triphenyltin Rest of soft parts Tributyltin Dibutyltin Monobutyltin Monophenyltin Diphenyltin Triphenyltin Japan; northern Kyushu; coastal areas; soft parts; maximum concentrations Common mussel, Mytilus edulis; 1998 Manila clam, Ruditapes philippinarum; 1998 vs. 2001 Pen shell, Atrina pectinata; 2001 Molluscs; commercial species; edible portions; 18 species 3 spp. 7 spp. 4 spp. 4 spp. Softshell clam, Mya arenaria; soft parts; Bohai Sea, China; summer 2002; total butyltins Common mussel, Mytilus edulis Soft parts Soft parts; Lisbon, Portugal; max. values Monomethyltins Dimethyltins Trimethyltins Soft parts; Tokyo Bay; 1989; max. values Monobutyltins Dibutyltins Tributyltins Soft parts; Osaka Bay, Japan; 1986; tributyltins
Cont’d
Concentration
Reference
0.21 DW vs. 1.53 DW 0.12 DW vs. 2.4 DW <0.0005 DW vs. 0.134 DW 0.004 DW vs. 0.064 DW 0.037 DW vs. 0.131 DW
23 23 23 23 23
0.12 DW vs. 0.33 DW 0.12 DW vs. 0.73 DW 0.05 DW vs. 1.5 DW <0.0005 DW vs. 0.026 DW <0.0004 DW vs. 0.035 DW 0.03 DW vs. 0.029 DW
23 23 23 23 23 23
0.135 FW 0.125 FW vs. 0.033 FW
34 34
0.095 FW
34
0.3-0.5 FW 0.5-0.7 FW 0.7-0.9 FW 0.9-2.0 FW
3 3 3 3
Max. 0.99 FW
a
31
1.3-7.1 DW
1
0.007 DW 0.01 DW 0.023 DW
14 14 14
0.12 FW 0.15 FW 0.24 FW 0.02-0.39 DW
12 12 12 15 (Continues)
320 Chapter 6 Table 6.22: Cont’d Element and Organism Soft parts; transplanted from reference site to River Tyne (United Kingdom), a TBT-impacted site for 6 months; March-September 2001 Tributyltins; start vs. end Dibutyltins; start vs. end Soft parts; British Columbia; 1990; max. values Monobutyltins Dibutyltins Tributyltins Soft parts; tributyltins United States; 1986-1987 Maine; 1989 Perth, Australia; 1991 San Diego Bay; 1988 Hepatopancreas; tributyltins San Diego Harbor Offshore Mussel, Mytilus galloprovincialis; soft parts Adriatic Sea; 2001-2002; summer vs. winter Monobutyltins Industrialized sites Reference site Dibutyltins Industrialized sites Reference sites Tributyltins Industrialized sites Reference site Monophenyltins Industrialized sites Reference site Diphenyltins Industrialized sites Reference site Triphenyltins Industrialized sites Reference site
Concentration
Reference
Max. 0.009 FW vs. 0.48 FW Max. 0.011 FW vs. 0.49 FW
27 27
0.05 DW 0.08 DW 0.31 DW
12 12 12
<0.005-1.4 FW 2.4 DW <0.001-0.33 FW 0.86 FW
12 12 12 16
1.9-3.5 DW <0.7-2.0 DW
a
4 4
0.4-0.6 DW vs. <0.01-0.27 DW 0.03 DW vs. 0.4 DW
25 25
1.2-2.2 DW vs. 0.09-1.1 DW 0.34 vs. 1.2 DW
25 25
1.2-1.7 DW vs. 1.5-7.9 DW 0.34 vs. 1.1 DW
25 25
0.04-0.07 DW vs. <0.01 DW <0.01 DW vs. 0.07 DW
25 25
<0.005 DW vs. <0.005 DW <0.005 DW vs. <0.005 DW
25 25
<0.005-0.028 DW vs. <0.005-0.007 DW <0.005 DW vs. 0.005 DW
25 25 (Continues)
Molluscs 321 Table 6.22: Element and Organism Korea; 2004-2005; reference site vs. transplantation for 126 days near shipyard; 3 stations Monobutyltins Dibutyltins Tributyltins Gastropod, Nassarius nitidus Venice lagoon, Italy; 2004-2004; soft parts Tributyltins Dibutyltins Monobutyltins Southern Venice lagoon; 2004; soft parts Tributyltins Dibutyltins Common dogwhelk, Nucellus lapillus Soft parts; reference sites Total tin Total tin Tributyltins Dibutyltins Soft parts; transplanted to TBTimpacted site for 6 months (River Tyne estuary, United Kingdom) Tributyltins; start vs. end Dibutyltins; start vs. end Squid, Ommastrephes illicebrosa; whole European oyster, Ostrea edulis Reference site; all tissues River Crouch, United Kingdom Soft parts Eggs Larvae Oysters; smoked; canned; soft parts; Canada Limpet, Patella caerulea; NE Mediterranean Sea; 1980; shell
Cont’d
Concentration
Reference
0.006-0.012 DW vs. 0.001-0.018 DW 0.013-0.017 DW vs. 0.008-0.07 DW 0.006-0.017 DW vs. 0.016-0.155 DW
33
Max. 0.244 DW Max. 0.132 DW Max. 0.082 DW
29 29 29
<0.004-0.976 DW <0.004-1.43 DW
30 30
Max. 0.3 FW 0.1-0.2 DW 0.1-0.2 DW 0.01-0.05 DW
17 18 18 18
Max. 0.006 FW vs. 0.056 FW Max. 0.005 FW vs. 0.049 FW
27 27
3.0 AW
a
33 33
5
<0.1 FW
19
0.27-0.33 FW 0.33 FW 0.3 FW
19 19 19
25.0-35.0 FW
6
(Continues)
322 Chapter 6 Table 6.22: Cont’d Element and Organism Total tin Methyltins Dimethyltins Trimethyltins Scallop, Pecten maximus Reared for 3 weeks in sea pens with tributyltin-coated netting; total tin vs. tributyltin Gonad Adductor muscle Gills Digestive gland Green mussel, Perna viridis Soft parts; Thailand; 1994-1995 Monobutyltins Dibutyltins Tributyltins Soft parts; tributyltins Hong Kong; 1989 Malaysia; 1992 Portugal; Rio de Aveiro; May-June 2005 (2 years after European Union ban on TBT anti-fouling paints); whelk, Nassarius reticulatus vs. mussel, Mytilus galloprovincialis; soft parts; max. concentrations Monobutyltins Dibutyltins Tributyltins Monophenyltins Diphenyltins Triphenyltins Monooctyltins Dioctyltins Trioctyltins
Concentration
Reference
0.013 DW 0.0004 DW 0.0002 DW 0.0009 DW
20 20 20 20
0.6 FW 0.6 FW 0.6 FW 1.0 FW
11 11 11 11
vs. vs. vs. vs.
0.4 FW 0.5 FW 0.6 FW 0.5 FW
0.014 (0.003-0.045) FW 0.013 (0.001-0.008) FW 0.1 (0.004-0.8) FW
12 12 12
0.06-0.12 FW 0.01-0.02 FW
12 12
0.071 DW vs. 0.163 DW 0.05 DW vs. 0.094 DW 0.073 DW vs. 0.5 DW <0.0097 DW vs. 0.051 DW <0.00016 DW vs. 0.00016 DW 0.0025 DW vs. 0.00054 DW 0.0118 DW vs. <0.0031 DW 0.0081 DW vs. <0.0036 DW <0.00043 DW vs. <0.00043 DW
22 22 22 22 22 22 22 22 22
a
Titanium Squid, Ommastrephes illicebrosa; whole
6.0 AW
5
Scallop, Pecten magellanicus; soft parts
9.8 (1.1-26.2) DW
7 (Continues)
Molluscs 323 Table 6.22: Element and Organism
Cont’d
Concentration
Reference
a
Tungsten Clam, Tapes japonica Soft parts Soft parts
0.46 AW 0.03 DW
8 9
Uranium Razor clam, Ensis siliqua; shell; 23 stations; west coast of England 17 stations 4 stations 2 stations
<0.5-1.0 DW 1.1-2.0 DW 3.1-4.7 DW
21 21 21
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Karbe et al., 1977; 2, Turekian et al., 1973; 3, Hall et al., 1978; 4, Young et al., 1979; 5, Nicholls et al., 1959; 6, Dick and Pugsley, 1950; 7, Reynolds, 1979; 8, Fukai and Meinke, 1959; 9, Fukai and Meinke, 1962; 10, Alzieu et al., 1986; 11, Davies et al., 1986; 12, Kanatireklap et al., 1997; 13, Shim et al., 1998; 14, Hamasaki et al., 1995; 15, Harino et al., 1998; 16, Harrington, 1991; 17,Davies et al., 1987; 18, Bryan et al., 1986; 19, Thain and Waldock, 1986; 20, Tugrul et al., 1983; 21, Pearce and Mann, 2006; 22, Sousa et al., 2007; 23, Garaventa et al., 2007; 24, Said et al., 2006; 25, Scancar et al., 2007; 26, Guerin et al., 2007; 27, Smith et al., 2006; 28, Karouna-Renier et al., 2007; 29, Pavoni et al., 2007; 30, Berto et al., 2007; 31, Yang et al., 2006; 32, Hu et al., 2006; 33, Kim et al., 2008; 34, Inoue et al., 2006a.
seawater exposing a fresh surface layer or organotin acrylate polymer. In continuing tests by the United States Navy, ablative organotin fouling coatings have demonstrated more than 48 months of protection (Blunden et al., 1985). Organotin compounds are more toxic than inorganic tin compounds; triorganotins are more toxic than mono-, di-, or tetraorgano forms; and TBT (TBT) compounds were the most toxic triorganotin compounds tested (Argese et al., 1998). TBTs cause adverse biological effects at levels far below those of any reported marine pollutant (Lawler and Aldrich, 1987; Matthiessen and Gibbs, 1998; van Slooten and Tarradellas, 1994), and, arguably, are the most toxic synthetic chemicals discharged into the marine environment (Eisler, 2000e). TBTs are highly toxic to aquatic plants and invertebrates, readily accumulate in molluscs from contaminated localities, and present in harbors where their release from antifouling paints—found usually on small boats and recreational craft—is the putative source (Chan et al., 2008; Horiguchi et al., 2006; Kim et al., 2008; Laughlin et al., 1986; USEPA, 1986; Walsh et al., 1985). TBT is a contributory factor and probably a major cause for the reproductive failure of the European flat oyster (O. edulis) in some locations (Thain and Waldock, 1986). Many organotins are slow-acting poisons; accordingly, short-term toxicity tests seriously underestimate the lethality of these compounds (Laughlin and Linden, 1985; Laughlin et al., 1988). Molluscs were the most sensitive group tested to TBT, especially gastropod and bivalve molluscs (Eisler, 2000e). Larvae of the Manila clam,
324 Chapter 6 R. philippinarum, exposed to TBT for 13 days had abnormal development at all TBT concentrations tested (0.000033-0.0006 mg/L) when compared to controls (<0.000001 mg TBT/L; Inoue et al., 2007b). In a maternal exposure test, clams were exposed to 0.000061 or 0.00031 mg TBT/L for 3 weeks. No maternal effect on veliger larvae were observed, suggesting that declines in Manila clam populations attributed to TBT were due to inhibited development and reduced survival of veliger larvae (Inoue et al., 2007b). Adverse effects of TBT are recorded at 0.00001-0.00002 mg/L on growth of Pacific oysters (C. gigas) after 2-8 weeks (Lawler and Aldrich, 1987; Waldock and Thain, 1983) and concentrations of 0.001-0.0016 mg/L were lethal (Champ, 1986; Thompson et al., 1985). TBT was lethal to the common mussel (M. edulis) at 0.00005-0.00097 mg/L (Cardwell and Sheldon, 1986; Dixon and Prosser, 1986; Valkirs et al., 1987). Similar results are recorded in European oysters, American oysters, and mud snails (Eisler, 2000e). Energy metabolism of the pen shell, Atrina pectinata japonica, is disrupted by TBT subjected to 0.0001 mg TBT/L for 72 h under aerobic conditions; later, half the pen shells were subjected to anaerobic conditions for 12 h (Inoue et al., 2007a). Exposure to TBT under aerobic conditions significantly raised lactate, pyruvate, and fumarate concentrations over controls. Clams held under anaerobic conditions had slightly lower succinate concentration than controls (Inoue et al., 2007a). In laboratory studies, crassostreid oysters, C. cucullata and C. gryphoides, reportedly accumulated radioisotopes of tin to a higher degree than other species of bivalve molluscs; this characteristic may be useful in the event of contamination from 113Sn (Patel and Ganguly, 1973). Mussels exposed to organotins through a diet of algae showed slow accumulation when compared to exposure from the medium; the reverse was observed for crabs (Evans and Laughlin, 1984; Hall et al., 1987; Laughlin et al., 1986). Uptake of organotins by molluscs was highest when ambient tin concentrations were less than 0.001 mg/L, when exposure duration was comparatively lengthy, and when organism lipid content was elevated (Champ, 1986; Laughlin et al., 1986; Thain and Waldock, 1986; Thompson et al., 1985). Limpets (Patella caerula), for example, contain 35-75% of their total tin body burden as organotin (Tugrul et al., 1983). Studies on TBT uptake and depuration from seawater by crabs, oysters, and fish demonstrated that all species accumulate and metabolize TBT, at least partly, within 48 h to dibutyltins, monobutyltins, and more polar metabolites. However, American oysters, C. virginica, metabolize less TBT than other species tested (Lee, 1985). The accumulation of TBT compounds in different tissues correlated positively with lipid content and supports a partitioning mode of uptake (Laughlin et al., 1986). The mixed function oxygenase system from hepatic tissues was able to metabolize TBT by forming hydroxylated metabolites (Lee, 1985). TBT and its degradation products were measurable in tissues of American oysters from the Gulf of Mexico ten years after the use of TBT-based paints was regulated. The likely sources of the TBT compounds include sediments, TBT-based paints on vessels longer than 25 m,
Molluscs 325 and shipyard wastes (Sericano et al., 1999). Softshell clams, M. arenaria, that were exposed to TBT concentrations of 0.00005-0.0008 mg Sn/L for 28 days showed high uptake, mostly in gills, and lengthy retention (Yang et al., 2006). Total maximum butyltin concentrations—mostly TBT —in soft parts at start was 0.19 mg/kg DW; after 28 days, maximum concentrations ranged between 4.6 and 12.4 mg total butyltins/kg DW, in a dose-dependent manner. The maximum total butyltin concentration value in clam soft parts after a 28 day-depuration period was 9.14 mg/kg DW, with a calculated half-time retention period of 94 days (Yang et al., 2006). TBTs were not genotoxic to larvae of the common mussel as judged by results of sister chromatid exchange and analysis of chromosomal aberrations (Dixon and Prosser, 1986). However, genotoxicity was demonstrated in other species tested. Organotin-induced strand breakage in erythrocytes as an indicator of DNA damage was evaluated in the bivalve Scapharca inaequivalvis (Gabbianelli et al., 2006). Significant DNA damage was evident in 30 min of in vitro incubation with about 0.004 mg/L of various organotins. Tributyltin chloride was the most genotoxic compound followed by monobutyltin chloride and dibutyltin chloride. Molluscs exposed in vivo to 0.05 mg tributyltin chloride/kg FW for 11 days showed exacerbated damage effects (Gabbianelli et al., 2006). Imposex—the superimposition of male characteristics onto a functionally normal female reproductive anatomy—is a phenomenon documented in populations of marine gastropods in the vicinity of yacht basins and marinas and is a sensitive indicator of TBT contamination. A female with imposex displays one or more male characteristics, such as a penis, a vas deferens, or convolution of the normally straight gonadal oviduct. Imposex is prevalent in mud snails (N. obsoletus) near estuarine marinas and has been induced experimentally in that species by exposure to TBT compounds at concentrations of 0.0045-0.0055 mg/L (Smith, 1981a,b). Imposex is documented extensively in declining populations of the common dogwhelk (N. lapillus), especially in southwestern England (Bryan et al., 1986, 1987b, Davies et al., 1987; Gibbs and Bryan, 1986; Gibbs et al., 1987; Smith et al., 2006). These authorities agree on six points: (1) dogwhelk populations near centers of boating and shipping show the highest frequency of imposex, coinciding with the introduction and increasing use of antifouling paints containing TBT compounds; (2) imposex is not correlated with tissue burdens of arsenic, cadmium, copper, lead silver, or zinc but is correlated with increasing concentrations of TBT and dibutyltin fractions; (3) transplantation of dogwhelks from a locality with little boating activity to a site near a heavily used marina caused a marked increase in frequency of imposex and in tissue accumulations of TBT; (4) imposex can be induced in female dogwhelks by exposure to 0.00002 mg Sn/L leached from a TBT antifouling paint; after exposure for 120 days, 41% of the females had male characteristics and whole-body burdens of 1.65 mg S/kg DW soft parts (vs. 0.1 in controls); concentrations as low as 0.0000015 mg TBT/L can initiate imposex in immature females; (5) declining dogwhelk populations were characterized by a moderate to high degree of imposex, relatively
326 Chapter 6 fewer functional females, few juveniles, and a general scarcity of deposited egg capsules. Many females in late imposex contained aborted capsules as a result of oviduct blockage, causing sterility and premature death; and (6) there was no evidence that loss of tin leads to any remission of imposex; in fact, all evidence indicates that gross morphological changes that occur in late imposex are irreversible. Additional studies with the common dogwhelk and TBT concentrations between 0.000001 and 0.00002 mg/L show that 13% of females develop male characteristics in 31 days, 27% in 91 days, and 41% in 120 days. BCFs from the medium were about 19,000 in 31 days, 36,000 in 91 days, and 78,000 in 120 days (Bryan et al., 1986). Others have shown that exposure of dogwhelks to TBT concentrations of 0.000002-0.000128 mg/L for 6-12 months resulted in a dose-related increase in frequency of imposex (Davies et al., 1997). There was no effect on feeding rate (predation on M. edulis), activity patterns, or male growth rate; however, female growth rate was inhibited. BCF values ranged from 7400 to 25,000 and decreased with increasing TBT exposure concentrations. Diet (mussels) accounted for about 40% of the accumulated TBT in whelks; the maximum concentration of TBT recorded in soft tissues of the 0.000128 mg/L group was 1.04 mg/kg FW after 12 months (Davies et al., 1997). Significant accumulation of butyltins—up to 0.196 mg/kg DW—in gastropod tissues along the western Iberian Peninsula plus high imposex frequency in the vicinity of shipping routes shows that organotin contamination is not confined to coastal areas (Gomez-Ariza et al., 2006; Rato et al., 2006). A similar situation is documented in areas of high shipping activity along the central west coast of India in which imposex frequency reached 100% in populations of the gastropod Gyrineum natator (Vishwakiran et al., 2006). Signs of severe imposex documented in some populations of whelks (Thais spp., Vasum turbinellus) sampled in eastern Indonesia in 1993 are attributed to unrestricted use of paints containing TBT (Evans et al., 1995). Imposex frequency in soft parts of the gastropod, Nassarius nitidus, from the Lagoon of Venice in 2004-2005 increased with increasing concentrations of TBTs over the range 0.025-0.100 mg TBT/kg DW (Pavoni et al., 2007). Studies show that imposex in gastropods is caused by elevated testosterone levels that masculinized TBT-exposed females owing to inhibition of cytochrome P450-mediated aromatase (Matthiessen and Gibbs, 1998). TBT-induced masculinization in gastropods (imposex and intersex) is a convincing example of endocrine disruption described in invertebrates that is unequivocally linked to an environmental contaminant (Matthiessen and Gibbs, 1998). Imposex is also induced in the mud snail, Ilyanassa obsoleta, through injection or via the medium by tin compounds other than TBT (McClellan-Green et al., 2006). Mud snails held in seawater for 45 days containing 0.000005-0.00005 mg/L of either trioctyltin chloride, dioctyltin chloride, or tin tetrachloride show a dose-dependent increase in imposex frequency over controls (McClellan-Green et al., 2006). In the gastropod predatory muricid drill, Stramonita haemastoma, frequency of imposex and organotin concentrations in tissues were correlated (Limaverde et al., 2007). Body burden threshold of TBTs associated with
Molluscs 327 33–80% imposex frequency is 0.005-0.024 mg Sn/kg FW; for triphenyltins, 0.023 mg Sn/kg FW produced 50% imposex. Organotin uptake by drills via the medium or via a diet of contaminated mussels seem possible (Limaverde et al., 2007). Once plentiful, no gastropods of the genus Nucella were found in locales near Vancouver, Canada in May-June 1999 owing to suspected TBT contamination from continuous use of TBT in antifouling paints and high (0.17 mg TBT/kg FW)concentrations of TBT in tissues of the mussel, M. trossulus (Horiguchi et al., 2003). During that same period, Nucella spp. from Victoria, and from Mission Point–where TBT contamination had decreased–seemed to be recovering from imposex; maximum TBT levels in tissues were 0.029 mg TBT/kg FW in Nucella lima and 0.044 in N. lamellosa (Horiguchi et al., 2003). Although TBT-antifouling paints are acknowledged causes of imposex in gastropod molluscs, this phenomenon has been recorded in more than 120 species of gastropods before the advent of TBT-antifouling paints (Garaventa et al., 2006). Factors other than TBT that can alter endocrine control of imposex development include exposure to heavy metals, changes in environmental conditions (Nias et al., 1993), infestation by parasites (Gorbushin, 1997), and the influence of other androgenic compounds (Cajaraville et al., 2000). More research is recommended on the imposex phenomenon in molluscs and its implications for vertebrates and other taxonomic groups (Eisler, 2000e). Imposex frequency in Thais spp. gastropod populations in Hong Kong was positively correlated with butyltin body burdens (Leung et al., 2006). Risks associated with use of organotin compounds include imposex, growth inhibition, and impairment of immune function (Chan et al., 2008; Coelho et al., 2006a,b; Inoue et al., 2006b; Kim et al., 2008; Leung et al., 2006). TBT concentrations as low as 0.00005 mg/L were associated with abnormal shell growth and reduced weight gain rate of juvenile clams Ruditapes decussatus exposed for up to two years (Coelho et al., 2006a,b). Embryonic development of the Manila clam, R. philippinarum, was adversely affected when egg-bearing females were held for 3 weeks in seawater containing 0.00006 mg TBT/L (Inoue et al., 2006b). In a waterborne exposure test, 4-h-old zygotes experienced decreased developmental success at concentrations as low as 0.000062 mg TBT/L (Inoue et al., 2006b). Antifouling paints containing TBT compounds are also used widely on netting panels of sea cages at fish and shellfish aquaculture units in order to minimize the obstruction of water change through the cages (Davies et al., 1987). Under these conditions, TBT paints were detrimental to the growth and survival of juvenile scallops and to calcium metabolism and growth of adult oysters (Paul and Davies, 1986). Scallops (P. maximus) reared in sea pens for 31 weeks on nets coated with TBT oxide contained 2.5 mg total Sn/kg FW soft parts (1.9 mg TBT/kg FW), but lost up to 40% during a 10 week depuration period (Davies et al., 1986). Scallop adductor muscle had 0.53 mg TBT/kg FW, suggesting that this tissue (the one consumed by humans) is a probable tin storage site (Davies et al., 1986). Pacific
328 Chapter 6 oysters (C. gigas) reared for 31 weeks on TBT-treated nets had up to 1.4 mg TBT/kg FW at week 16 (vs. 0.12 in controls), but lost 90% during a 10 week depuration period (Davies et al., 1986). In 1979, due to the increasing use of the organotin compounds as a class, the Canadian government placed organotins on Canada’s Category III Contaminant List, a designation requiring that more data be gathered on their occurrence, persistence, and toxicity in order to prepare informed environmental and human health risk assessments (Chau et al., 1984). In 1982, the use of TBT paints was curtailed in France, and in 1985 the United Kingdom introduced regulations to limit sales of TBT paints that released the biocide at high rates (Huggett et al., 1992). In 1985, tin and organotin concentrations in seawater and Pacific oysters in France were 5-10 times lower than 1982 (Alzieu et al., 1986). In Arcachon Bay, France, there was a decrease in the incidence and extent of anomalies in oyster calcification mechanisms that were correlated with decreases in tin contamination (Alzieu et al., 1986). In April 1987, the United Kingdom banned the retail sale of antifouling paints containing organotin concentrations greater than 4000.0 mg total tin/L (Side, 1987); continued monitoring of TBT was recommended, especially in areas of extensive boating activities (Simmonds, 1986). In 1990, Japan banned the use of TBT-containing paints (Horiguchi et al., 2006); however declining bivalve populations in coastal areas in northern Kyushu in 19982001 has been linked, in part to continued TBT contamination of bivalves (Inoue et al., 2006a). In 1992, field work on the River Crouch Estuary showed that sediments from areas most contaminated with TBT in 1987 contained 0.16 mg TBT/kg DW, but by 1992 this had declined to 0.02 mg TBT/kg DW. TBT declines were accompanied by increases in abundance and diversity of benthic fauna, especially bivalve molluscs (Rees et al., 1999; Waldock et al., 1999). The United States Navy has implemented fleet wide use of organotin antifouling paints that contain TBT in order to reduce fuel consumption by up to 15%, and increase ship speed up to 40% as a direct result of reduced drag (USN, 1984). Since naval vessels seldom remain moored for extended periods in coastal areas, hazard effects to the environment should be minimal—despite the size of the vessel—when compared to boating practices at local marinas (USN, 1984). Accordingly, civilian use of marine paints containing TBT compounds has been severely restricted. The State of Virginia enacted legislation that prohibits the use of TBT paints on nonaluminum vessels under 25 m in length (Anonymous, 1987). Also in Virginia, TBT paints applied on large ships and aluminum craft should not exceed a daily leach rate of 0.000004 mg/cm3 (Huggett et al., 1992); similar legislation is proposed in at least 12 other states. The most stringent criteria now proposed for tin and aquatic life protection are for triorganotins. These vary from 0.000002 to 0.000008 mg/L (Cardwell and Sheldon, 1986; Huggett et al., 1992; Pinkney et al., 1990; Side, 1987; USPHS, 1992). However, even these comparatively low concentrations will not protect certain species of gastropods from TBT impact, as discussed earlier.
Molluscs 329
6.48 Titanium Up to 26.2 mg Ti/kg DW soft parts were measured in soft parts of scallops collected from an oceanic dump site rich in titanium (Table 6.22).
6.49 Tungsten The maximum tungsten concentration recorded in field collections of molluscs was 0.03 mg W/kg DW in clam soft tissues (Table 6.22).
6.50 Uranium Limited data indicate that the maximum concentration recorded in shell of the razor clam, E. siliqua, collected from the west coast of Britain was 4.7 mg U/kg DW (Table 6.22). Uranium isotopes were detected in rock jingles P. macroschisma, blue mussels M. trossulus, and horse mussels M. modiolus collected near Amchitka Island during summer 2004; Amchitka Island in the Aleutian chain was the site of nuclear tests between 1965 and 1971 (Burger et al., 2007b). Naturally occurring levels of 234U, 235U, and 238U were found in all three species, and anthropogenic 236U only in the rock jingle (Burger et al., 2007b).
6.51 Vanadium Vanadium concentrations in molluscan tissues vary substantially with season of year, with tissue specificity—shell being a prime repository—and between species (Table 6.23). For all species of molluscs collected, the highest concentration recorded was 290.0 mg V/kg DW in pteropod tests (Table 6.23). The ability to concentrate vanadium from ambient seawater by five species of bivalves from coastal waters of Greece ranged from 110 for the poorest accumulator to 940 for the best (Papadopoulu, 1973). The significance of vanadium in molluscs is imperfectly understood.
6.52 Ytterbium The single datum available for ytterbium is 0.002-0.049 mg Yb/kg DW soft parts of the common mussel, M. edulis (Karbe et al., 1977).
6.53 Zinc It is generally agreed that the highest concentrations of zinc in marine biota are found in tissues of filter-feeding molluscs, especially oysters (Eisler, 1980, 2000f). Crassostreid oysters, for example, frequently contain more than 4000.0 mg Zn/kg in soft tissues on a DW basis (Table 6.24). It is probable that zinc is not limiting to normal molluscan life processes
330 Chapter 6 Table 6.23: Vanadium Concentrations in Field Collections of Molluscs Organism
Concentration
Giant squid, Architeuthis dux; 2001-2005; hepatopancreas; Bay of Biscay vs. Mediterranean Sea
2.2 DW vs. 1.7 DW
Clam, Arctica islandica; soft parts March August February June
Reference 16
4.3-20.6 DW 1.6-4.3 DW 1.6-3.1 DW 1.3-2.9 DW
1 1 1 1
0.18-0.82 FW
2
<0.1 to 0.2 FW 0.2-0.4 FW 0.4-0.6 FW 0.6-2.0 FW
3 3 3 3
5.8-8.4 DW
4
Common mussel, Mytilus edulis Soft parts Shell
0.22 DW 1.0-1.4 DW
5 15
Mussel, Mytilus edulis aoteanus Soft parts Mantle Gill Muscle Visceral mass Foot Gonad Shell
5.0 DW 3.0 DW 5.0 DW 2.0 DW 23.0 DW 44.0 DW <2.0 DW 110.0 DW
6 6 6 6 6 6 6 6
Molluscs Soft parts Edible tissues; 18 commercial species 2 spp. 6 spp. 7 spp. 3 spp. Softshell clam, Mya arenaria; soft parts
Mussel, Mytilus galloprovincialis Soft parts; Adriatic Sea; 2001-2002; summer vs. winter Industrialized sites Reference site Soft parts; Adriatic Sea; 2001-2005; winter vs. summer
1.6-8.5 DW vs. 2.9-3.9 DW 5.1 DW vs. 4.6 DW 2.0-2.8 DW vs. 0.4-1.2 DW
a
12 12 17 (Continues)
Molluscs 331 Table 6.23: Organism Octopus, Octopus vulgaris Portugal; 1999-2002; 3 sites Digestive gland Branchial heart Portugal; 1999-2000; 3 sites Digestive gland Branchial heart Squid, Ommastrephes illicebrosa; whole
Cont’d
Concentration
Reference
3.3-4.6 DW 24.0-54.0 DW
18 18
5.0-7.2 DW 27.5-53.0 DW
19 19
4.0 AW
7
Oyster, Ostrea sinuata Soft parts Mantle Gills Muscle Visceral mass Kidney Heart Shell
3.0 DW 12.0 DW 3.0 DW <2.0 DW <2.0 DW 4.0 DW 4.0 DW 49.0 DW
6 6 6 6 6 6 6 6
Scallop, Pecten novae-zelandiae Soft parts Mantle Gills Visceral mass Kidney Foot Gonad Shell
9.0 DW 7.0 DW 3.0 DW 30.0 DW 4.0 DW 4.0 DW 32.0 DW 130.0 DW
6 6 6 6 6 6 6 6
Bivalve, Pinna nobilis Soft parts Mantle and gills Muscle Nervous system Stomach and intestine Gonads Hepatopancreas Byssus Byssus gland
28.0 AW 17.0 AW 5.4 AW 23.0 AW 53.0 AW 74.0 AW 4.1 AW 2.5 AW 6.5 AW
8 8 8 8 8 8 8 8 8
28.5 (11.4-40.7) DW
1
Scallop, Placopecten magellanicus Soft parts Muscle
a
(Continues)
332 Chapter 6 Table 6.23: Cont’d Organism
Concentration
Reference
March August February June Viscera February March June August
Max. 1.7 DW <0.1 DW Max. 0.8 DW Max. 5.4 DW
1 1 1 1
7.8-21.3 DW 21.0-74.2 DW 4.6-13.2 DW 6.9-35.1 DW
1 1 1 1
Pteropods; shell
50.0-290.0 DW
9
Common cuttlefish, Sepia officinalis Egg Eggshell Embryo Yolk Hatchlings Whole Cuttlebone Juveniles, age 1 month Whole Digestive gland Cuttlebone Immatures, age 12 months Whole Digestive gland Cuttlebone Adults, age 18 months Whole Digestive gland Cuttlebone Clam, Tapes japonica Soft parts Soft parts Clam, Trivela mactroidea; Venezuela; 2002; 14 sites; soft parts
3.4 DW <0.1 DW <0.1 DW
13 13 13
<0.1 DW <0.5 DW
13 13
<0.1 DW 1.6 DW <0.5 DW
13 13 13
0.47 DW 2.9 DW <0.5 DW
13 13 13
0.5 DW 3.3 DW <0.5 DW
13 13 13
15.0 AW 1.1 DW
10 11
2.0-13.2 DW
14
a
Values are in mg V/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Reynolds, 1979; 2, Ikebe and Tanaka, 1979; 3, Hall et al., 1978; 4, Eisler, 1977b; 5, Carlisle, 1958; 6, Brooks and Rumsby, 1965; 7, Nicholls et al., 1959; 8, Papadopoulu, 1973; 9, Pyle and Tieh, 1970; 10, Fukai and Meinke, 1959; 11, Fukai and Meinke, 1962; 12, Scancar et al., 2007; 13, Miramand et al., 2006; 14, LaBrecque et al., 2004; 15, Protasowicki et al., 2008; 16, Bustamante et al., 2008; 17, Fattorini et al., 2008; 18, Napoleao et al., 2005; 19, Seixas and Pierce, 2005.
Molluscs 333 Table 6.24: Zinc Concentrations in Field Collections of Molluscs Organism
Concentration
Reference
Abalones; soft parts
55.0 (38.0-100.0) DW
88
Gastropod, Acmaea digitalis Shell Soft parts
8.4-29.9 DW 420.0-763.0 DW
1 1
Cockle, Anadara trapezia; April 2000; soft parts; New South Wales, Australia
Max. 160.0 DW
Mussel, Anodonta cygnea; soft parts
141.0-165.0 DW
3
Mussel, Anodonta sp. Shell Soft parts
6.4 DW 120.0 DW
4 4
Gastropod, Aplysia benedicti Ctenidium Gonad Parapodia Hepatopancreas Buccal mass Intestine Gut content Shell
55.0-60.0 DW 33.0-40.0 DW 39.0 DW 61.0-74.0 DW 25.0 DW 90.0 DW 58.0 DW 15.0-28.0 DW
5 5 5 5 5 5 5 5
Giant squid, Architeuthis dux; 2001-2005; Spain; hepatopancreas Bay of Biscay Mediterranean Sea
103.0 DW 219.0 DW
Clam, Arctica islandica; soft parts
2.4-25.8 FW
6
Scallop, Argopecten gibbus; kidney concretion
14,466.0 DW
7
Scallop, Argopecten irradians; kidney concretion
16,550.0 DW
7
Cockle, Austrovenus stutchburyi; soft parts; New Zealand; 1993-1994
40.0-118.0 DW
142
40.0 DW 111.0 DW 61.0 DW
156 156 156
Hydrothermal vent mussel, Bathymodiolus azoricus; mid-Atlantic ridge 2001 840 m deep Digestive gland Gills Mantle
a
149
172 172
(Continues)
334 Chapter 6 Table 6.24: Cont’d Organism
Concentration
Reference
201.0 DW 555.0 DW 68.0 DW
156 156 156
80.0 DW 106.0 DW 46.0 DW
156 156 156
150.0 FW vs. 130.0 FW 140.0 FW vs. 60.0 FW 152.0 FW vs. 80.0 FW 2500.0 FW vs. <10.0 FW 9.4-13.0 (4.1-21.4) DW
144 144 144 144 162
106.0-1997.0 DW 28.0-145.0 DW 45.0-276.0 DW
163 163 163
Bivalves; 5 spp.; whole; Australia; lead smelter outfall 2.5-5.2 km from outfall 18.0-18.8 km from outfall
4480.0 DW; max. 20,300.0 DW 2590.0 DW
100 100
Bivalves Soft parts Kidney granules
91.0-660.0 DW 10,000.0-43,320.0 DW
107 106
9.0 (3.3-17.9) FW
139
Mussel, Brachidontes pharaonis; Mersin cost, Turkey; 2002-2003; max. concentrations Muscle Gill Hepatopancreas
105.0 DW 240.0 DW 115.0 DW
134 134 134
Whelk, Buccinum undatum Shell Soft parts
13.0 DW 620.0 DW
4 4
Whelk, Busycon canaliculatum Muscle Digestive diverticula Muscle Digestive gland
25.0 DW 2600.0 DW 15.3-29.5 FW 405.0-2650.0 FW
8 8 9 9
1700 m deep Digestive gland Gills Mantle 2300 m deep Digestive gland Gills Mantle Summer 2002; start vs. 30 days in metals-free seawater Gill Mantle Digestive gland Byssus thread Shell; 2001; 4 sites 2001; 5 sites Gills Mantle Digestive gland
Bivalves; 5 spp.; soft parts; East China Sea; August 2002
a
(Continues)
Molluscs 335 Table 6.24:
Cont’d
Organism
Concentration
Reference
Calcasieu River Estuary; Louisiana; soft parts Hooked mussel, Brachidontes exustus American oyster, Crassostrea virginica
61.0 (39.0-86.0) DW 3300.0 (1000.0-7794.0) DW
105 105
Cephalopods Soft parts Whole
81.0-150.0 DW; max. 580.0 DW 250.0 DW
88, 107 118
Cockle, Cardium edule Soft parts Mantle fluids Shell Soft parts
52.0-81.0 DW 95.0 DW 6.8 DW 130.0 DW
Mussel, Cerastoderma edule Soft parts Soft parts
63.0-208.0 DW 55.0 (46.0-66.0) DW
10 11
Chitons; soft parts
290.0-700.0 DW
88
462.0 DW 45.1 DW 152.0 DW 384.0 DW 132.0 DW
12 12 12 12 12
61.7 DW 111.0 DW 117.0 DW 40,800.0 DW 7.3-11.0 DW
12 12 12 12 4
73.0-113.0 DW 16.0 FW
13 14
81.0-115.0 DW; max. 510.0 DW 16.0-58.0 FW; 295.0-590.0 DW; 2825.0-5650.0 AW
88 15
8.7-28.0 FW; 9.1-44.1 DW; 43.0-88.0 AW
15
Scallop, Chlamys opercularis Soft parts Body fluids Mantle Gill Digestive gland Adductor muscle Striated Unstriated Gonad and foot Kidney Shell Mussel, Choromytilus meridionalis Soft parts Soft parts Clams Soft parts Soft parts Shell
a
3 3 4 4
(Continues)
336 Chapter 6 Table 6.24: Cont’d Organism
Concentration
Reference
Scallop, Comptopallium radula; Santa Marie Bay (metals-contaminated), New Caledonia; October 2004 Soft parts Digestive gland
183.0 (109.0-308.0) EW 1115.0 DW
158 158
Oyster, Crassostrea angulata; soft parts; Spain Sanlucar Sancti-Petri Barbate Rio Pedras Ayamonte
2064.0 FW 437.6 FW 366.6 FW 1101.0 FW 1027.0 FW
Sydney rock oyster, Crassostrea commercialis Soft parts Soft parts Soft parts; southeast Asia
318.0 FW 80.0-665.0 FW 800.0 (64.0-1920.0) DW
17 18 108
1420.0 DW
167
Oyster, Crassostrea corteziensis; soft parts; Gulf of California; 1999-2000
a
16 16 16 16 16
Oyster, Crassostrea cucullata Soft parts Soft parts
254.5 FW 446.0-2800.0 DW
19 20
Pacific oyster, Crassostrea gigas Soft parts Soft parts Soft parts Soft parts Soft parts Soft parts
86.0-344.0 FW 333.0-10,019.0 FW 99,220.0 DW 396.0 DW 424.0 DW 1272.0-3627.0 DW
21 17 22 23 13 135
Oyster, Crassostrea gryphoides; soft parts
323.0-550.0 DW
20
Oyster, Crassostrea madrasensis; soft parts
203.4 FW
19
Oyster, Crassostrea margaritacea; soft parts
886.0 DW
23
Mangrove oyster, Crassostrea rhizophorae Sepetiba Bay, Brazil; soft parts; near zinc smelting plant closed in 1996 1978 1980 1983 1989
2240.0 DW; max. 4150.0 DW 1533.0 DW 8073.0 DW; max. 16,130.0 DW 4950.0 DW; max. 5016.0 DW
120 121 122 123, 124 (Continues)
Molluscs 337 Table 6.24: Organism 1996 tailings spill following heavy rains 1997 1999 2001 2002 Soft parts; near Natal Brazil; summer 2001; contaminated estuary vs. reference site American oyster, Crassostrea virginica Soft parts Lower Chesapeake Bay Near Baltimore Chesapeake Bay Gulf of Mexico Galveston Bay, Texas; 1992-1993 Pensacola, Florida; 2003-2004 South Carolina United States Savannah, Georgia; 2000-2001 Soft parts Soft parts Newport River, North Carolina April 1965 Mantle Gill Labial palps Muscle Digestive gland February 1966 Shell Soft parts January 1969 Shell Soft parts North River, North Carolina, November 1966 Mantle Gill Labial palps Muscle
Cont’d a
Concentration
Reference
80,724.0 DW
125
9174.0 DW 14,849.0 (8058.0-28,233.0) DW 9770.0 DW 11,984.0 (10,963.0-17,420.0) DW 997.0-2082.0 DW; max. 4862.0 DW vs. 983.0-1491.0 DW; max. 1874.0 DW
126 125 127 128 147
310.0 FW 4000.0 FW 3975.0 (60.0-12,800.0) DW 2150.0 (485.0-10,000.0) DW 2082.0 (602.0-4819.0) DW Max. 1000.0 FW 2410.0 (280.0-6305.0) DW 1018.0-1641.0 (204.0-4000.0) DW 978.0-2428.0 DW 230.0 (24.0-820.0) FW 1428.0 (180.0-4120.0) FW
24 24 108 108 109 152 108 110 157 25 21, 26, 27
135.0 FW 182.0 FW 123.0 FW 79.0 FW 260.0 FW
28 28 28 28 28
24.7 FW 159.4 FW
28 28
245.1 FW 210.5 FW
28 28
450.6 FW 508.1 FW 501.2 FW 126.1 FW
28 28 28 28 (Continues)
338 Chapter 6 Table 6.24: Cont’d Organism Digestive gland Rectum Pericardial sac Gonad Shell Soft parts Soft parts Soft parts Soft parts North Carolina Virginia Soft parts August November Shell Soft parts; metals-contaminated area vs. reference site Soft parts Soft parts Soft parts; United States East coast Gulf coast
Concentration
Reference
491.8 FW 531.0 FW 223.9 FW 435.9 FW 1.5-8.1 DW 1200.0-5700.0 DW Max. 12,675.0 DW mean 3915.0 DW; max. 10,000.0 DW
28 28 28 28 29 29 30 31
125.0-325.0 FW 275.0-425.0 FW
32 32
5000.0 DW 2100.0 DW 2.5 DW 4100.0 DW vs. 1700.0 DW
33 33 33 33
322.0 DW 1215.0-1980.0 FW
34 35
830.0-4060.0 DW 370.0-7080.0 DW
36 36
Limpet, Crepidula fornicata Soft parts Shell Soft parts
116.0 DW 1.1 DW 940.0 DW
Clam, Donax serra; soft parts
16.0 FW
14
Clam, Ensis arcuatus; shell
1.4 DW
37
0.8 DW
37
Razor clam, Ensis siliqua Shell Shell; 23 stations; West coast of England 9 stations 12 stations 2 stations Gastropods Muscle Shell Viscera Operculum Soft parts
a
3 4 4
23.5-66.7 DW 70.1-125.0 DW 184.0-295.0 DW
129 129 129
6500.0 AW 330.0 AW 13.0 AW 6000.0 AW 84.0-763.0 DW
15 15 15 15 107 (Continues)
Molluscs 339 Table 6.24:
Cont’d
Organism
Concentration
Reference
Gastropod drills; soft parts
536.0-3470.0 DW
88
Abalone, Haliotis midea; soft parts
12.0 FW
14
Abalone, Haliotis rufescens Gill Mantle Digestive gland Foot
28.0-54.0 DW 42.0-74.0 DW 536.0-980.0 DW 38.0-46.0 DW
38 38 38 38
Abalone, Haliotis tuberculata Soft parts Foot Viscera Digestive gland Blood Muscle Gill Left kidney Right kidney
98.0-103.0 DW 28.0-33.1 DW 238.0-288.0 DW 624.0-656.0 DW 19.9 DW 38.0 DW 63.4 DW 124.0 DW 298.0 DW
39 39 39 39 39 39 39 39 39
Scallop, Hinnites multirugosus Kidney Digestive gland
37.2 FW 68.8 FW
40 40
Periwinkle, Littoraria scabra; soft parts; Tanzania; 2005 Industrial sites Reference site
750.0 DW 95.0 DW
160 160
Limpet, Littorina littoralis; soft parts
312.0 DW
3
Limpet, Littorina littorea Soft parts Soft parts Soft parts Soft parts Soft parts Soft parts Soft parts Digestive gland and gonad Shell Soft parts and operculum
38.0 DW 6.6-20.2 FW Max. 520.0 DW 28.0-274.0 DW 88.0 DW 15.5-24.3 FW 92.1-186.0 DW 111.2-133.7 DW 2.6-3.0 DW 117.0 (45.0-284.0) DW
3 41 42 43 39 44 45 45 45 11
Limpets; soft parts 18 species 7 species
112.0 (14.0-760.0) DW 196.0 (86.0-430.0) DW
88 88
a
(Continues)
340 Chapter 6 Table 6.24: Cont’d Organism
Concentration
Reference
Squid, Loligo opalescens; liver
247.0-449.0 DW
46
Baltic clam, Macoma balthica Soft parts Soft parts Soft parts; adults; San Francisco Bay Soft parts; 1996-1997; Gulf of Gdansk; age 3-4 years
804.0 (510.0-1160.0) DW 88.0-99.0 FW 200.0-600.0 DW 300.0-749.0 DW
Hardshell clam, Mercenaria mercenaria Soft parts Mantle Gill Muscle Soft parts Shell Soft parts Soft parts Soft parts Soft parts, Maryland James River York River Chesapeake Bay
a
11 47 111 151
1680.0 AW 810.0 AW 3070.0 AW 1500.0 AW 20.6 (11.5-40.2) FW 3.4 DW 94.0 DW 12.4-27.6 DW Max. 298.0 DW
48 48 48 48 21, 26 4 4 10 30
11.8-35.5 FW 7.5-14.6 FW 11.3-26.8 FW
49 49 49
Clam, Meretrix casta; soft parts
50.2 DW
20
Clam, Meretrix lamarckii; soft parts
63.0 DW
19
Mexico; Sinaloa; 2004-2005; sort parts; rainy season vs. dry season Oyster, Crassostrea corteziensis Mussel, Mytella strigata Clam, Megapitaria squalida
1048.5 DW vs. 849.2 DW 69.5 DW vs. 63.3 DW 98.3 DW vs. 94.2 DW
Mussel, Modiolus demissus; soft parts
Max. 52.0 DW
Mussel, Modiolus modiolus Shell Soft parts Mantle and gills Muscle Gonad Gut and digestive gland
6.2 DW 320.0-530.0 DW 180.0 DW 68.0 DW 140.0 DW 190.0 DW
Morocco; 2001; clams; soft parts Scrobicularia plana Cerastoderma edule
204.0 DW 80.0 DW
164 164 164 30 4 4 4 4 4 4 166 166 (Continues)
Molluscs 341 Table 6.24:
Cont’d
Organism
Concentration
Reference
Morocco; 2004-2005; soft parts Mussel, Mytilus galloprovincialis Clam, Venerupis decussatus Pacific oyster, Crassostrea gigas
292.0 (112.6-612.3) DW 103.1 (67.2-157.3) DW 481.7 (28.3-672.4) DW
159 159 159
Mussels; soft parts
109.0-267.0 DW; max. 7700.0 DW
Molluscs Soft parts West Norway coast Rio Tinto estuary, Spain Chile, Strait of Magellan; 5 spp.; 2001; 17 stations Edible tissues; commercial species 3 spp. 13 spp. 1 spp. 1 spp. 12 spp. 3 spp. 3 spp.; India; 2003
88
Max. 2800.0 DW Max. 370.0 DW 8.5-35.4 FW
57 52 150
5.0-9.0 FW 10.0-20.0 FW 100.0-200.0 FW 300.0-400.0 FW 7.0-337.0 FW 12.0-18.0 FW 10.3-16.2 FW
53 53 53 53 54 55 155
Softshell clam, Mya arenaria Soft parts Soft parts
17.0 (9.0-28.0) FW 9.5-11.2 FW; 93.0-127.0 DW
21, 26 56
Mussel, Mytilus californianus Shell Soft parts Digestive gland Soft parts
8.6-26.5 DW 164.0-310.0 DW 46.0-110.0 DW 60.0-200.0 DW
1 1 57 36
Mussel, Mytilus corscum; soft parts
160.0 DW
50
Common mussel, Mytilus edulis Shell Shell; Baltic Sea; 2005; 12 sites Kidney; Newfoundland October 1984 April 1985 Soft parts; weight 0.43 g Visceral mass Gills and palps Remainder
a
0.04 DW 2.2-10.3 DW
4 169
144.0 (50.0-427.0) DW 828.0 (94.0-3410.0) DW
113 113
34.0-100.0 DW 47.0-94.0 DW 46.0-110.0 DW
112 112 112 (Continues)
342 Chapter 6 Table 6.24: Cont’d Organism Soft parts; weight 0.22 g Visceral mass Gills and palps Remainder Soft parts Shell Soft parts Shell Soft parts Soft parts Soft parts Soft parts Soft parts Digestive gland Gonad Muscle Soft parts Soft parts Soft parts Soft parts Soft parts Soft parts Hepatopancreas San Diego harbor Offshore Soft parts Soft parts Protein fraction I Protein fraction II Protein fraction III Soft parts U.S. West coast East coast Greenland; near lead zinc flotation mill outfall vs. reference site The Netherlands; summer, 2002 Scheldt estuary, Europe; March 2000 Soft parts Shell
Concentration
Reference
28.0-112.0 DW 38.0-158.0 DW 40.0-130.0 DW 91.0 DW 0.6 DW 40.0 DW 6.9-14.2 DW 204.0-341.0 DW 253.0-779.0 DW 12.5-82.5 FW 45.8 FW 269.0 DW Max. 185.0 FW Max. 183.0 FW Max. 172.0 FW 19.3-60.1 FW 16.4-97.1 FW 29.0-41.8 FW 14.0-460.0 DW 38.0-575.0 DW 140.0-500.0 DW
112 112 112 4 37 37 1 1 43 41 58 3 59 59 59 60 61 44 62 63 64
120.0-210.0 DW 120.0-140.0 DW 132.0 (57.0-199.0) DW
65 65 11
0.03 FW 0.2 FW 0.2 FW
66 66 66
90.0-260.0 DW 67.0-189.0 DW 502.0 (340.0-813.0) FW vs. 100.0 FW
36 36 119
Max. 170.0 DW 790.0 DW
136 171
85.0-359.0 DW 4.0-12.0 DW
67 67
a
(Continues)
Molluscs 343 Table 6.24:
Cont’d
Organism
Concentration
Reference
Mussel, Mytilus edulis aoteanus Soft parts Mantle Gill Visceral mass Gonad
91.0 DW 192.0 DW 336.0 DW 525.0 DW 260.0 DW
68 68 68 68 68
301.0-702.0 DW
69
22.1 FW 26.7 FW
70 70
Mussel, Mytilus edulis planulatus Soft parts Soft parts June January Soft parts, dry weight 0.09 g 0.39 g 0.48 g 0.69 g Mussel, Mytilus galloprovincialis Protein extracts; Bulgarian Black Sea Coast; polluted vs. reference site Soft parts Soft parts Soft parts; Adriatic Sea, Italy; 2 sites Soft parts; Adriatic Sea; 2001-2002; summer vs. winter Industrialized sites Reference site Soft parts; Adriatic Sea; 2001-2005; winter vs. summer Soft parts; Aegean Sea, Turkey; 20022003 Soft parts; Izmir Bay, Turkey; 2004; near shore vs. mid-bay Soft parts; Gulf of Gemlik, Turkey; 2004 Soft parts; May 2003; NW Mediterranean Sea Near Genova, Italy Near Marseille, France Near Barcelona, Spain Soft parts; Venice lagoon, Italy; 20052006; San Giuliano vs. Sacca Sessola
142.0 DW 203.0 DW 207.0 DW 264.0 DW
a
2 2 2 2
143.0 DW vs. 112.4 DW
145
209.0 DW 29.8 FW 21.9-26.0 FW
71 72 168
235.0-249.0 DW vs. 73.0-244.0 DW 201.0 DW vs. 102.0 DW 66.2-119.0 DW vs. 23.2-105.0 DW
143 143 173
23.3 (16.1-37.1) FW
137
27.7 DW vs. 17.9 DW
170
196.0 DW
176
74.0-240.0 DW 135.0-153.0 DW 167.0-299.0 DW
132 132 132
(Continues)
344 Chapter 6 Table 6.24: Cont’d Organism April July October February Soft parts Mussel, Mytilus viridis Soft parts Soft parts Soft parts Soft parts
Concentration
Reference
260.3 DW vs. 215.5 DW 186.2 DW vs. 164.0 DW 134.9 DW vs. 216.8 DW 144.1 DW vs. 400.2 DW 124.5 (48.9-316.7) DW
153 153 153 153 133
11.0 FW 15.3-63.0 DW 14.1 FW 4.3-11.2 DW
19 20 73 74
Abalone, Notohaliotis discus; soft parts less viscera
33.0 DW
50
Gastropod, Nucella conccina; soft parts; Antarctica; 2004
64.4 DW
131
Whelk, Nucella lapillus Shell Soft parts Soft parts Beer, Dorset Transplants from Beer to Bristol Channel for 5 months Soft parts plus operculum Soft parts
0.59 DW 860.0 DW
4 4
345.0 DW 2530.0 DW
75 75
416.0 (235.0-520.0) DW 415.0 DW
11 3
Oyster drill, Ocenebra erinacea; soft parts
1451.0-2160.0 DW
Octopus, Octopus sp. Whole Whole
106.0 FW 18.5 FW
Octopus, Octopus vulgaris Portugal; 1999-2002; 3 sites Digestive gland Branchial heart Gill Muscle Portugal; 2005-2006; digestive gland; northwest region vs. south coast Whole Nuclei
a
114 76 58
1247.0-1666.0 DW 80.0-85.0 DW 67.0-77.0 DW Max. 76.0 DW
174 174 174 174
850.0 (410.0-2040.0) DW vs. 1840.0 (740.0-2870.0) DW 1070.0 (570.0-1660.0) DW vs. 3880.0 (1230.0-1660.0) DW
165 165 (Continues)
Molluscs 345 Table 6.24: Organism Mitochondria Lysosomes Microsomes Squid, Ommastrephes bartrami Liver Muscle Gonad Liver Oyster, Ostrea angasi Soft parts Soft parts Soft parts Soft parts June January European flat oyster, Ostrea edulis Soft parts Soft parts; 1991-2005; Balearic Islands; western Mediterranean Sea; Port of Mahon Soft parts Soft parts Contaminated site Reference site Cornwall, England vs. Anglesey, North Wales Gills Mantle Kidney Viscera Muscle Hemolymph Whole cell-free Oyster, Ostrea equestris; soft parts; United States East coast Gulf coast
Cont’d
Concentration
Reference
1300.0 (390.0-18,180.0) DW vs. 2600.0 (990.0-18,230.0) DW 630.0 (220.0-10,100.0) DW vs. 1960.0 (630.0-6420.0) DW 1750.0 (1080.0-2250.0) DW vs. 1900.0 (1150.0-17,060.0) DW
165 165 165
163.0 DW 54.0 DW 73.0 DW 115.0-124.0 DW
46 77 77 77
371.0-8865.0 FW 5657.0 FW 3740.0-38,700.0 DW
17 58 69
1217.0 FW 954.0 FW
70 70
660.0 DW 1458.2 (204.5-3404.8) DW
2480.0-3280.0 DW
a
23 133
79
10,560.0 (4700.0-12,640.0) DW 98.0 DW
115 115
14,746.0 FW vs. 10,027.0 FW 12,770.0 FW vs. 6,189.0 FW 6155.0 FW vs. 6050.0 FW 5817.0 FW vs. 2988.0 FW 2342.0 FW vs. 2683.0 FW
78 78 78 78 78
155.0 FW vs. 60.0 FW 30.0 FW vs. 15.0 FW
78 78
2800.0 DW 310.0-3600.0 DW
36 36 (Continues)
346 Chapter 6 Table 6.24: Cont’d Organism
Concentration
Reference
200.0 FW 580.0 FW
80 80
250.0 FW 800.0-900.0 FW 800.0-900.0 FW 800.0-900.0 FW
81 81 81 81
1072.0 FW vs. 95.0 FW 4270.0 FW vs. 171.0 FW 2178.0 FW vs. 112.0 FW 221.0 FW vs. 17.0 FW 1013.0 FW vs. 122.0 FW 953.0 FW vs. 108.0 FW
82 82 82 82 82 82
Oyster, Ostrea sinuata Soft parts Mantle Gill Muscle Visceral mass Kidney Heart
1103.0 DW 4760.0 DW 3300.0 DW 369.0-400.0 DW 1122.0 DW 1248.0 DW 2090.0 DW
68 68 68 68 68 68 68
Oysters; soft parts Metals-contaminated area Reference site
Max. 21,000.0 FW Max. 7670.0 FW
83, 83 83, 84
1960.0-7270.0 DW; max. 49,000.0 DW
88
Oyster, Ostrea gigas Soft parts; transplants from control area to metal-contaminated area for 120 days Controls Transplants Transplants to metal-contaminated area for 120 days Adductor muscle Labial palps Mantle Gills Transplants from zinc-contaminated area vs. after 116 days in “clean” water Mantle Gill Labial palps Muscle Remainder Whole
Oysters, various; soft parts Limpet, Patella candei gomesii; soft parts; 2007; Azores Near hydrothermal vent Reference site
44.4-48.4 DW 40.2-40.4 DW
Limpet, Patella sp. Soft parts Beer, Dorset, United Kingdom
91.0 DW
a
161 161
75 (Continues)
Molluscs 347 Table 6.24: Organism Transplants from Beer to Bristol Channel for 8 months Shell Soft parts Soft parts Soft parts Soft parts Soft parts Soft parts From desalinization plant outfall Reference site Gastropod, Patella piperata; Canary Islands, Spain; soft parts; March-April 2003
Cont’d
Concentration
Reference
340.0 DW
75
51.0 DW 84.0 DW Max. 580.0 DW 158.0 DW 95.0-229.0 DW 101.0 DW
4 4 42 85 3 39
255.0 DW 175.0 DW
10 10
10.4 (1.6-24.1) DW
a
138
Limpet, Patella vulgata Soft parts Soft parts Shell
165.0 (83.0-224.0) DW 127.0-238.0 DW 3.0-18.0 DW
11 67 67
Scallop, Pecten maximus Upper valve Lower valve Soft parts Muscle Gut and digestive gland Mantle and gills Gonad Soft parts Body fluid Mantle Gill Digestive gland Striated muscle Unstriated muscle Gonad and foot Kidney Edible tissues Kidney; soft parts vs. excretory granule
4.1 DW 6.1 DW 230.0 DW 70.0 DW 1100.0 DW 160.0-420.0 DW 180.0-360.0 DW 273.0 DW 30.1 DW 59.4 DW 100.0 DW 407.0 DW 69.9 DW 94.2 DW 196.0 DW 19,300.0 DW 19.1-45.5 FW 5898.0 FW vs. 140,000.0 FW
4 4 4 4 4 4 4 12 12 12 12 12 12 12 12 12 86 87
Scallop, Pecten novae-zelandiae Soft parts Muscle
283.0 DW 108.0 DW
68 68 (Continues)
348 Chapter 6 Table 6.24: Cont’d Organism
Concentration
Reference
400.0 DW 392.0 DW 2630.0 DW 210.0 DW 256.0 DW 20.8 FW 24.0 FW 27.0 FW 16.0 FW
68 68 68 68 68 54 54 54 54
Scallop, Pecten sp. Kidney Kidney granules Soft parts
32,000.0 DW 120,000.0 DW 200.0 DW
88 88 88
Pelycopods Soft parts Shell
340.0 AW 2050.0 AW
15 15
Visceral mass Intestine Kidney Foot Gonads Soft parts Stomach Gonad Adductor muscle
Green mussel, Perna viridis Soft parts; 1986-1987 Soft parts; 1986 March May Soft parts; India; January 2002; 28 sites Hong Kong; juveniles vs. adults Reference site Soft parts Byssus Shell Polluted site Soft parts Byssus Shell Bivalve, Pinna nobilis Soft parts Muscle Nervous system Gonads Hepatopancreas Byssus Byssus gland
56.0-134.0 DW
116
63.0-150.0 DW 77.0-94.0 DW 9.5-10.5 FW
117 117 148
104.0 DW vs. 108.0 DW 103.0 DW vs. 112.0 DW 0.25 DW vs. 0.39 DW
175 175 175
116.0 DW vs. 152.0 DW 314.0 DW vs. 297.0 DW 0.9 DW vs. 0.7 DW
175 175 175
4900.0 AW 3200.0 AW 3400.0 AW 4600.0 AW 6900.0 AW 3100.0 AW 840.0 AW
a
89 89 89 89 89 89 89 (Continues)
Molluscs 349 Table 6.24:
Cont’d
Organism
Concentration
Reference
Clam, Pitar morrhuana; soft parts
145.0-276.0 DW
90
Scallop, Placopecten magellanicus Soft parts Soft parts Muscle Gonad Visceral mass Soft parts
105.0 DW 9.3-24.0 FW; max. 109.0 FW 2.0-8.1 FW 4.7-75.4 FW 7.4-22.5 FW 105.0 DW
91 92 93 93 93 94
Clam, Protothaca staminea Shell Soft parts
9.2 DW 67.7 DW
Pteropods; shell
36.0 DW; max. 312.0 DW
15
Clam, Rangia cuneata Soft parts Whole
51.0 DW 6.8 DW
34 96
Manila clam, Ruditapes philippinarum Soft parts; Korea; 2002-2003 Females vs. males Postspawn vs. prespawn Jiaozhou Bay, China; sediments vs. soft parts; November 2004 Bohai Sea, China; soft parts
1 1
81.2 DW vs. 76.5 DW 105.0 DW vs. 79.1 DW 90.8 DW vs. 35.5-85.5 DW
130 130 140
10.0-20.1 DW
141
Rock oyster, Saccostrea cucullata; soft parts; Hong Kong; 1986 March May
2082.0-3275.0 DW 2210.0-22,863.0 DW
117 117
Oyster, Saccostrea glomerata; soft parts
1908.0-5786.0 DW
97
Scallops; soft parts
105.0-212.0 DW; max. 462.0 DW
88
974.0 DW
11
1470.0-2940.0 DW 9630.0 DW 316.0 DW 235.0 DW 406.0 DW 132.0 DW 280.0 DW
98 98 98 98 98 98 98
Clam, Scrobicularia plana Soft parts Gannel estuary, England Soft parts Digestive gland Mantle and siphons Foot and gonads Gills and palps Adductor muscles Kidney
a
(Continues)
350 Chapter 6 Table 6.24: Cont’d Organism Camel estuary, England Soft parts Digestive gland Mantle and siphons Foot and gonads Gills and palps Adductor muscles Kidney Transferred from Camel estuary to Gannel estuary for 352 days Digestive gland Remaining tissues Transferred from Gannel estuary to Camel estuary for 352 days Digestive gland Remaining tissues Tamar estuary; England; soft parts Squid, Sepia esculenta; trunk Common cuttlefish, Sepia officinalis Gill Mantle Blood; dialyzed vs. not dialyzed Liver; dialyzed vs. not dialyzed Gut; dialyzed vs. not dialyzed Branchial gland; dialyzed vs. not dialyzed Arterial heart; dialyzed vs. not dialyzed Ovary; dialyzed vs. not dialyzed Mantle Dorsal shield Beak Gills Liver Ink Egg Eggshell Embryo Yolk Hatchlings Whole Cuttlebone
Concentration
Reference
353.0-394.0 DW 1104.0 DW 170.0 DW 149.0 DW 388.0 DW 87.0 DW 315.0 DW
98 98 98 98 98 98 98
3030.0 DW 199.0 DW
98 98
4605.0 DW 249.0 DW 1950.0 (501.0-3990.0) DW
98 98 99
58.0 DW
50
99.0 DW 52.0 DW 22.0 FW vs. 7.0 FW 259.0 DW vs. 52.0 DW 41.0 DW. vs. 12.0 DW 124.0 DW vs. 25.0 DW
3 3 101 101 101 101
122.0 DW vs. 21.0 DW 19.0 DW vs. 4.0 DW 16.3 FW 12.6 FW 12.6 FW 24.7 FW 487.5 FW 1.4 FW
101 101 16 16 16 16 16 16
69.0 DW 68.0 DW 50.0 DW
146 146 146
100.0 DW 30.0 DW
146 146
a
(Continues)
Molluscs 351 Table 6.24: Organism Juveniles, age 1 month Whole Digestive gland Cuttlebone Immatures, age 12 months Whole Digestive gland Cuttlebone Adults, age 18 months Whole Digestive gland Cuttlebone
Cont’d
Concentration
Reference
113.0 DW 500.0 DW 75.0 DW
146 146 146
145.0 DW 770.0 DW 116.0 DW
146 146 146
156.0 DW 1400.0 DW 150.0 DW
146 146 146
Squid, Sepia sp.; whole
50.0 FW
76
Clam, Spisula solidissima; muscle
18.4 FW
9
Squid Flesh Flesh with skin Viscera Pen Whole
47.4 DW 144.0 DW 94.3 DW 263.0 DW 710.0 AW
102 102 102 102 103
110.0-210.0 FW; 120.0-210.0 DW; 120.0-220.0 AW 12.0-25.0 FW; 55.0-110.0 DW; 510.0-1100.0 AW 39.0-250.0 FW; 250.0-1500.0 DW; 1500.0-3500.0 AW 23.0-93.0 FW; 96.0-560.0 DW; 280.0-2300.0 AW
104
Gastropod, Strombus pugilis Shell Foot Soft parts Internal organs
a
104 104 104
Squid, Symplectoteuthis oualeniensis; liver
513.0 DW
46
Clam, Tapes decussatus; soft parts
16.1-25.5 FW
16
Clam, Tapes semidecussata Shell Soft parts
11.2 DW 11.2 DW
1 1
Gastropod, Thais emarginata Shell Soft parts
1.4-23.5 DW 1701.0 DW
1 1 (Continues)
352 Chapter 6 Table 6.24: Cont’d Organism
Concentration
Reference
Gastropod, Thais lapillus Soft parts Soft parts Soft parts Digestive gland and gonad Shell
Max. 3100.0 DW 916.0-1980.0 DW 492.1-2354.0 DW 558.9-760.7 DW 2.7-3.1 DW
42 43 45 45 45
Clam, Trivela mactroidea; Venezuela; 2002; 14 sites; soft parts
5.0-166.0 DW
Whelks; soft parts
198.0 (13.0-650.0) DW
a
154 88
Values are in mg Zn/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Graham, 1972; 2, Harris et al., 1979; 3, Leatherland and Burton, 1974; 4, Segar et al., 1971; 5, Patel et al., 1973; 6, Palmer and Rand, 1977; 7, Carmichael et al., 1979; 8, Greig, 1975; 9, Greig et al., 1977; 10, Romeril, 1974; 11, Bryan and Hummerstone, 1977; 12, Bryan, 1973; 13, Watling and Watling, 1976b; 14, Van As et al., 1973; 15, Lowman et al., 1970; 16, Establier, 1977; 17, Ratkowsky et al., 1974; 18, Mackay et al., 1975; 19, Sastry and Bhatt, 1965; 20, Zingde et al., 1976; 21, Pringle et al., 1968; 22, Boyden and Romeril, 1974; 23, Watling and Watling, 1976a; 24, McFarren et al., 1962; 25, Kopfler and Mayer, 1967; 26, Shuster and Pringle, 1968; 27, Shuster and Pringle, 1969; 28, Wolfe, 1970; 29, Windom and Smith, 1972; 30, Valiela et al., 1974; 31, Drifmeyer, 1974; 32, Huggett et al., 1975; 33, Frazier, 1975; 34, Sims and Presley, 1976; 35, Greig and Wenzloff, 1978; 36, Goldberg et al., 1978; 37, Bertine and Goldberg, 1972; 38, Anderlini, 1974; 39, Bryan et al., 1977; 40, Vattuone et al., 1976; 41, Topping, 1973; 42, Butterworth et al., 1972; 43, Ireland, 1973; 44, Wharfe and Van den Broek, 1977; 45, Ireland and Wooton, 1977; 46, Martin and Flegal, 1975; 47, Miettinen and Verta, 1978; 48, Eisler and Weinstein, 1967; 49, Larsen, 1979; 50, Ishii et al., 1978; 51, Stenner and Nickless, 1974b; 52, Stenner and Nickless, 1975; 53, Hall et al., 1978; 54, Nielsen and Nathan, 1975; 55, Van As et al., 1975; 56, Eisler, 1977b; 57, Alexander and Young, 1976; 58, Eustace, 1974; 59, Young and McDermott, 1975; 60, Phillips, 1976a; 61, Phillips, 1976b; 62, Phillips, 1977b; 63, Karbe et al., 1977; 64, Simpson, 1979; 65, Young et al., 1979; 66, Talbot and Magee, 1978; 67, Lande, 1977; 68, Brooks and Rumsby, 1965; 69, Bloom and Ayling, 1977; 70, Thomson, 1979; 71, Fowler and Oregioni, 1976; 72, Uysal, 1978a; 73, D’Silva and Kureishy, 1978; 74, Bhosle and Matondkar, 1978; 75, Stenner and Nickless, 1974a; 76, Matsumoto et al., 1964; 77, Hamanaka et al., 1977; 78, George et al., 1978; 79, Fukai et al., 1978; 80, Ikuta, 1968a; 81, Ikuta, 1968b; 82, Ikuta, 1968c; 83, Thrower and Eustace, 1973a; 84, Thrower and Eustace, 1973b; 85, Preston et al., 1972; 86, Topping, 1973; 87, George et al., 1980; 88, Sprague, 1986; 89, Papadopoulu, 1973; 90, Eisler et al., 1978; 91, Pesch et al., 1977; 92, Palmer and Rand, 1977; 93, Greig et al., 1978; 94, Reynolds, 1979; 95, Pyle and Tieh, 1970; 96, White et al., 1979; 97, Phillips, 1979; 98, Bryan and Hummerstone, 1978; 99, Bryan and Uysal, 1978; 100, Ward et al., 1986; 101, Decleir et al., 1978; 102, Horowitz and Presley, 1977; 103, Robertson, 1967; 104, Lowman et al., 1966; 105, Ramelow et al., 1989; 106, Sullivan et al., 1988; 107, White and Rainbow, 1985; 108,Presley et al., 1990; 109, Jiann and Presley, 1997; 110, USNAS, 1979; 111, Cain and Luoma, 1986; 112, Amiard et al., 1986; 113, Lobel, 1986; 114, Amiard-Triquet et al., 1988; 115. Bryan et al., 1987a; 116, Chan, 1988a; 117, Chu et al., 1990; 118, Young et al., 1980; 119, Loring and Asmund, 1989; 120, Lacerda, 1983; 121, Pfeiffer et al., 1985; 122, Lima et al., 1986; 123, Carvalho et al., 1991; 124, Carvalho et al., 1993; 125, Rebelo et al., 2003a; 126, Lacerda and Molisani, 2006; 127, Amaral et al., 2005; 128, Rebelo et al., 2003b; 129, Pearce and Mann, 2006; 130, Ji et al., 2006; 131, Santos et al., 2006; 132, Zorita et al., 2007; 133, Deudero et al., 2007; 134, Karayakar et al., 2007; 135, Liu and Deng, 2007; 136, Mubiana and Blust, 2006; 137, Sunlu, 2006; 138, Bergasa et al., 2007; 139, Huang et al., 2007; 140, Li et al., 2006; 141, Liang et al., 2004a; 142, Peake et al., 2006; 143, Scancar et al., 2007; 144, Kadar, 2007; 145, Gorinstein et al., 2006; 146, Miramand et al., 2006; 147, Silva et al., 2006; 148, Sasikumar et al., 2006; 149, Burt et al., 2007; 150, Espana et al., 2007; 151, Sokolowski et al., 2007; 152, Karouna-Renier et al., 2007; 153, Nesto et al., 2007; 154, LaBrecque et al, 2004; 155, Sankar et al., 2006; 156, Colaco et al., 2006; 157, Kumar et al., 2008; 158, Metian et al., 2008; 159, Maanan, 2008; 160, De Wolf and Rashid, 2008; 161, Cunha et al., 2008; 162, Cravo et al., 2008; 163, Cosson et al., 2008; 164, Frias-Espericueta et al., 2008; 165, Raimundo et al., 2008; 166, Anajjar et al., 2008; 167, Ruelas-Inzunza and Paez-Osuna, 2008; 168, Conti et al., 2008; 169, Protasowicki et al., 2008; 170, Kucuksezgin et al., 2008; 171, Wepener et al., 2008; 172, Bustamante et al., 2008; 173, Fattorini et al., 2008; 174, Napoleao et al., 2005; 175, Nicholson and Szefer, 2003; 176, Unlu et al., 2008.
Molluscs 353 in the marine environment and is accumulated in excess of the organism’s immediate needs, at least on the basis of enzymatically bound zinc (Pequegnat et al., 1969). The information in Table 6.24 supports the observations that zinc is not limiting, and in several cases accumulated far in excess of biological requirements. It has also been stated (Robertson et al, 1972) that intraspecies zinc concentrations in a wide range of flora and fauna were relatively constant, suggesting definite physiological needs. However, much of the information in Table 6.24 contradicts the findings of Robertson and his coworkers. Marked variations in zinc content were evident both within and among closely related groups such as ostreid and crassostreid oysters, and among limpets of the genus Patella. In fact, numerous factors can account for the observed variations in zinc content of marine molluscs, of which proximity to anthropogenic sources of zinc was probably one of the most important. The influence of biotic and abiotic modifiers on zinc accumulations will be discussed later. At this time it is sufficient to note from Table 6.24 that zinc concentrations were markedly influenced by season of collection, geographic locale, and zinc-specific sites of accumulation, such as kidney and digestive gland (Eisler, 2000f). Oysters and scallops are among the most efficient accumulators of zinc. Nonconcentration factors were highest in scallop kidney, with values 1.7-4.0 million times those of ambient seawater (Bryan, 1973). Concentration factors in excess of 100,000 were reported for soft parts of O. sinuata (Brooks and Rumsby, 1965) and C. virginica (Pringle et al., 1968). The lowest concentration factors reported among field collections of molluscs ranged from 1525 in surf clams, S. solidissima and 1700 in softshell clams, M. arenaria, to 2100 in hardshell clams, M. mercenaria (Pringle et al., 1968). Intermediate values were reported for many species, including oysters C. gryphoides (Bhatt et al., 1968), squid Ommastrephes spp. (Ketchum and Bowen, 1958), mussels C. meridionalis (Van As et al., 1973), and scallops Pecten novae-zelandiae (Brooks and Rumsby, 1965). Concentration factors for radiozinc-65 in Pacific oysters, C. gigas, collected from the outfall area of a nuclear-powered steam electric station generally followed changes in concentration of 65Zn in the discharge waters (Salo and Leet, 1969); concentration factors for two distinct year classes of these oysters ranged from 5600 to 12,000. Salo and Leet (1969) concluded that the maximum concentration of 65Zn that a human would derive from a protein diet of oysters raised in the canal would be well within the maximum permissible body burden established by United States regulatory agencies. However, concentration factors based on radiozinc accumulation data should be viewed with caution; the addition of stable zinc to the medium reduced radiozinc accumulation disproportionately in scallop tissues, suggesting an ability by this group to discriminate among chemical species of zinc (Bryan, 1973). Ingestion of seafood products of commerce that contain extremely high concentrations of zinc probably do not represent a major threat to public health, although available evidence is not conclusive. In one case, high concentrations of zinc and other metals in oysters from Tasmania reportedly caused nausea and vomiting in some human consumers; these oysters
354 Chapter 6 exceeded the Australian food regulation at that time of 40.0 mg Zn/kg FW by a factor of about 500 (Thrower and Eustace, 1973a,b). The current zinc standard in Turkey is 50.0 mg Zn/kg DW for seafoods, and is sometimes exceeded in mussels from contaminated areas (Unlu et al., 2008). Zinc accumulations in natural populations are influenced by many variables. Some of the more extensively documented modifiers, together with appropriate examples, follow.
6.53.1 Proximity to Anthropogenic Zinc Sources When compared to more distant sites, elevated zinc concentrations were found in tissues of mussels and oysters from the vicinity of industrial operations in Australia (Bloom and Ayling, 1977), in clams P. morrhuana near an electroplating plant outfall in Narragansett Bay, Rhode Island, United States (Eisler, 1995a; Eisler et al., 1978), in mussels M. edulis near a lead-zinc flotation mill in Greenland (Loring and Asmund, 1989), and in various species of shellfish collected near heavily populated and industrialized areas of California (Graham, 1972). Similar observations are recorded in molluscs from widely separated geographic areas (Fowler and Oregioni, 1976; Maanan, 2007; Phillips, 1977b, 1979; Ratkowsky et al., 1974; Romeril, 1974; Thrower and Eustace, 1973a,b). In the Fal estuary, England, long-term metal pollution over the past 125 years has resulted in zinc sediment burdens of 679.0-1780.0 mg/kg DW, producing benthic communities that favor zinc-tolerant organisms, such as oysters, and a general impoverishment of mussels, cockles, and gastropods (Bryan et al, 1987). It is not known if this tolerance is genetic or acquired.
6.53.2 Body Weight Increasing concentrations of zinc per unit body weight are recorded with increasing body weight in various species of clams (Boyden, 1974; Eisler et al., 1978), oysters (Downes, 1957), mussels (Boyden, 1974), and squid (Bustamante et al., 2008). However, this pattern is reversed in other species of shellfish, with higher zinc concentrations recorded in smaller organisms (Boyden, 1974, 1977; Boyden et al., 1975; Watling and Watling, 1976a). Studies with 65Zn and clams, G. tumidum, showed concentration factors in soft parts of 400-500 after 15 days; however, these values were higher for smaller clams and lower for larger clams (Hedouin et al., 2006).
6.53.3 Gender Females of C. meridionalis contained zinc concentrations in total soft parts that were twice that of males (Watling and Watling, 1976b). However, testes of M. californianus contained 60% more zinc than ovarian tissue, with no sex-related differences evident for muscle or digestive gland (Alexander and Young, 1976).
Molluscs 355 Zinc was demonstrated histochemically in cytoplasmic inclusions shown to be lysosomes in a number of cell types in the common mussel, M. edulis (Lowe and Moore, 1979). Males had more zinc in kidneys than females, the latter appearing to use oocytes as an additional means of excretion. Lysosome-vascular systems are considered important detoxification mechanisms for zinc and other metals in molluscs and other organisms (Lowe and Moore, 1979). In Pacific oysters, C. virginica, there is no evidence linking high body burdens of zinc with high concentrations in sex products. Unlike other trace metals, zinc residues in adults and eggs of C. virginica were essentially the same, although this was not the case for copper and cadmium (Greig et al., 1976).
6.53.4 Tissue Specificity Zinc tends to accumulate in molluscan digestive gland and stomach as excretory granules, and in kidney as concretions (Eisler, 1981; Sprague, 1986; Sullivan et al., 1988; Table 6.24). Kidney is the preferred storage site in mussels and scallops (Sprague, 1986), and digestive gland in oysters (Sprague, 1986), and cuttlefish (Miramand et al., 2006). In oysters, granules may contain up to 60% of the total body zinc, and this may account, in part, how shellfish exist with grossly elevated body burdens of zinc (Sprague, 1986). Different tissues are preferred as zinc storage sites in closely related species. For example, stomach and digestive gland were the major repositories for zinc in M. edulis (Pentreath, 1973); however, for M. californianus, it was digestive gland (Alexander and Young, 1976) and kidney (Young and Folsom, 1967). But in two species of scallops, highest accumulations of zinc were in kidney and digestive gland of both species (Bryan, 1973). Zinc persistence in selected organs shows considerable variability and may be significantly different from halftime persistence values seen in whole animal. For example, the half-time persistence of zinc in M. edulis kidney was estimated at 2-3 months (Lobel and Marshall, 1988) versus 4 days for whole mussel (USNAS, 1979). Gravid cuttlefish, S. officinalis were fed crabs radiolabeled with 65 Zn over a 2 week period to determine rate of maternal transfer into eggs; during embryonic development, 65Zn was progressively transferred to the embryo, and also to juveniles after hatching (Lacoue-Labarthe et al., 2008b). Concentrations of zinc in tissues of molluscs are usually far in excess of that required for normal metabolism; much of the excess zinc is bound to macromolecules or present as insoluble metal inclusions in tissues (Eisler, 2000f). In many organisms, zinc and other trace metals concentrate in membrane-limited granules (George et al., 1980). These could be considered as either a long-term store or a means of excretion or detoxification of toxic metals. Excretory granules, or concretions, in kidney of the scallop P. maximus are primarily inorganic in composition and contain calcium, manganese, zinc, and phosphorus, the total
356 Chapter 6 being equivalent to about 75% of the DW of the granule, with smaller amounts present of magnesium, copper, iron, cadmium, potassium, sulfur, and chlorine. It is postulated that the granules develop from lysomal membranes to mineralized membrane-limited vacuoles or residual bodies and eventually excreted via the urinary tract (George et al., 1980).
6.53.5 Protein Binding Zinc was associated mainly with high molecular weight proteins in M. edulis (Noel-Lambot, 1976). In C. virginica nearly all zinc was bound either to soluble high-molecular-weight proteins or to structural cell components; dialysis of soluble tissue extracts removed up to 96% of total zinc without effect on alkaline phosphatase (Wolfe, 1970). Low-molecularweight metal-binding proteins—not metallothionein—were induced in gastropods in metalscontaminated environments (Andersen et al., 1989). In rock oysters (S. cucullata) collected near an iron ore shipping terminal, some of the tissue zinc was bound to high-molecularweight (around 550,000) iron-binding protein called ferritin (Webb et al., 1985). Ferritin accounts for about 40% of the protein-bound zinc in rock oysters, and probably in other bivalves containing elevated tissue levels of zinc (Webb et al., 1985).
6.53.6 Diet The actual role of water in the accumulation of zinc by M. edulis is minor when compared to diet (Pentreath, 1973). Young (1977) agrees that the food chain is the major source of zinc in molluscan tissues. In N. lapillus, the input from food is about 100 times greater than that of seawater (Young, 1977). In L. obtusata, food accounts for about 60% of accumulated zinc with an estimated input of 1.1 mg Zn/kg tissue/day compared to the total tissue concentration of 46.7 mg Zn/kg tissue (Young, 1975).
6.53.7 Sediment Substrate In general, zinc concentrations in both sediments and molluscan tissues are elevated in the vicinity of smelters and other point sources of zinc, and both decrease with increasing distance from the source (Ward et al., 1986). Extractable concentrations of sediment bound zinc were positively correlated with zinc concentrations on deposit-feeding clams (Luoma and Bryan, 1979; Romeril, 1974). Highest zinc concentrations in soft tissues of the clam M. balthica were observed in clams collected from calcareous substrates, such as crushed clam shells; lower accumulations were noted in Macoma collected from substrates of detrital organics, manganese oxides, and iron oxides, in that order (Luoma and Jenne, 1977). In general, availability of sediment zinc to bivalve molluscs was higher at increased sediment concentrations of amorphous inorganic oxides or humic substances, and lower at increased concentrations of inorganic carbon and ammonium acetate-soluble manganese (Luoma and Bryan, 1979).
Molluscs 357
6.53.8 Inherent Species Differences The half-time persistence of zinc in molluscs is variable and reported to range from 4 days in the common mussel (M. edulis) to 650 days in the duck mussel (Anodonta nutalliana); intermediate values were 23-40 days in limpet (L. littorea), 76 days in the California mussel (M. californianus), and 300 days in the Pacific oyster (USNAS, 1979). Zinc accumulation kinetics in molluscs vary considerably between and within species (Chu et al., 1990) and are attributed to a variety of factors. Variations in zinc content of clam tissues, for example, were associated with seasonal changes in tissue weights (Cain and Luoma, 1986). Gastropods from the Mediterranean Sea near a ferronickel smelter had elevated zinc concentrations in hepatopancreas when compared to conspecifics from distant sites; however, there were no consistent seasonal variations (Nicolaidu and Nott, 1990). Fluctuations in zinc content in tissues of M. edulis related to mussel size or to season of collection were sufficient to conceal low chronic or shortterm pollution (Amiard et al., 1986). Diet—the main route of zinc accumulation in most molluscs—had no significant effect on whole-body zinc content of certain predatory marine gastropods. For example, whole-body zinc concentrations in gastropod oyster drills (Ocenebra erinacea) ranged from 1451.0 to 2169.0 mg/kg DW, and remained unchanged after feeding for 6 weeks on Pacific oysters (C. gigas) containing 1577.0 mg Zn/kg DW or mussels (M. edulis) containing 63.0 mg Zn/kg DW (Amiard-Triquet et al., 1988). Taxonomically close groups, such as crassostreid and ostreid oysters show marked differences in zinc contents. Adults of crassostreid oysters usually contain higher concentrations of zinc than ostreid adults, although tissue distributional patterns were similar in both groups (Romeril, 1971). Oysters, when compared to other groups of filter-feeding bivalves, show a greater capacity for zinc uptake. For example, in Chesapeake Bay, Maryland, oysters had 30-40 times more zinc than did clams and up to 90 times more zinc than mussels (McFarren et al., 1962).
6.53.9 Seasonality Variations in zinc content of soft tissues from individual shellfish species are correlated with seasonal—as distinct from thermal—regimes (Bryan, 1973; Fowler and Oregioni, 1976; Frias-Espericueta et al., 2008; Karayakar et al., 2007; Maanan, 2007; Patel et al., 1973; Romeril, 1974). In one case, zinc content in soft parts of mussels, M. galloprovincialis, collected near shore coincided with a period of high precipitation and runoff with a concomitant increase in suspended particle loading of coastal waters (Fowler and Oregioni, 1976). Jiann and Presley (1997) demonstrate that zinc concentrations in American oyster soft parts were highest in summer and lowest in winter and spring.
358 Chapter 6
6.53.10 Dredging Zinc content of marine molluscs correlates positively with particulate matter produced as a result of dredging operations (Rosenberg, 1977). Zinc accumulated in this manner persists for lengthy periods. In the case of oysters, O. edulis, at least 31% of the zinc accumulated during dredging operations was retained for at least 18 months (Rosenberg, 1977). It is possible that some of the high body burdens reported in Table 6.24 may have been influenced by incomplete removal of zinc-contaminated sediments as well as food and other materials. For example, contamination of biological samples by ingested sediments is reported for several species of molluscs and crustaceans. In some locations, elemental zinc concentrations in organisms reflected elemental zinc in inorganic residues from gut contents (Flegal and Martin, 1977). In another study, corrosion of galvanized zinc suspension trays was the cause of grossly elevated zinc (99,000.0 mg Zn/kg DW) in soft parts of Pacific oysters (Boyden and Romeril, 1974).
6.53.11 Depth Mussels, P. canaliculus, collected from different portions of the water column were analyzed for content of zinc, lead, iron, and cadmium (Nielsen, 1974). At one location, all metals except zinc increased in Perna with increasing depth. At another location, all metals were essentially the same from mussels collected from the surface to a depth of 9 m. Differences between stations were attributed to differences in mixing of the water column. The differences in mixing may cause variations in the type of food organisms available at the various depths, or variations in the particulate/dissolved ratio of metal levels with depth. Either or both of thee conditions could affect the biological availability of zinc and other metals at different depths (Nielsen, 1974).
6.53.12 Salinity In general, bivalve molluscs residing in comparatively saline waters contained reduced zinc concentration in soft tissues when compared to conspecifics from lower salinity waters (Duke, 1967; Huggett et al., 1973, 1975; Larsen, 1979; Luoma and Bryan, 1979; Phillips, 1977a,b; Tabata, 1969). However, within the 1.5-3.5% salinity range (15-35 ppt), salinity of the medium was not an important factor governing uptake of zinc in the common mussel, M. edulis (Phillips, 1976a); in the case of the clam, S. plana, uptake was actually higher at elevated salinities (Garcia-Luque et al., 2007).
6.53.13 Temperature Increasing water temperatures were associated with increasing concentrations of zinc in soft parts of clams (Duke, 1967; Eisler, 1977b), oysters, and scallops (Duke, 1967); however, common mussels, M. edulis, showed no trend within the 10-18 C range (Phillips, 1976a).
Molluscs 359
6.53.14 pH Duke (1967) reports that pH of the ambient medium significantly affected 65Zn accumulation from seawater by a community of oysters, clams, and scallops; in all cases, uptake was higher at elevated pH levels.
6.53.15 Interactions Zinc accumulations in molluscs are mediated by many factors, including interaction effects of zinc with salts of calcium, cobalt, iron, cadmium, copper, mercury, phosphates, various organic substances, and others. Zinc, for example, inhibited mercury accumulations in marine gastropods (Andersen et al., 1989). Radiozinc-65 was rapidly accumulated in southern quahog (Mercenaria campechiensis) over a 10-day period; accumulation in kidney was linear over time and was enhanced at elevated phosphate loadings in the medium (Miller et al., 1985). In soft parts of C. meridionalis, concentrations of copper, lead, manganese, and bismuth were all positively correlated with zinc content, but not with each other (Watling and Watling, 1976b). In oysters, O. edulis, the total amount of zinc measured was far in excess of the amount of zinc contributed by zinc-dependent enzymes, such as carbonic anhydrase, alkaline phosphatase, carboxypeptidase A, malic dehydrogenase, and alpha-D-mannoside; however, the amount of nondialyzable zinc was of the same order of magnitude (Coombs, 1972). This apparent excess of dialyzable zinc was linked to the high levels of calcium in tissues, demonstrating a competition between calcium and zinc in uptake potential (Coombs, 1972). Mussels, M. edulis, during exposure to 0.2 mg cadmium/L for 20 days, showed only a slight increase in zinc content of soft parts (George and Coombs, 1977). On the other hand, zinc at 0.5 mg/L substantially decreased cadmium uptake in M. edulis, and clams, Mulinia lateralis (Jackim et al., 1977). Also reported were interaction effects of zinc, lead, and cadmium salts on zinc accumulation in mussels (Phillips, 1976a); depressed zinc uptake in oysters by iron or cobalt (Romeril, 1971); increased zinc accumulation in mantle tissue of hardshell clams during exposure to organochlorine and organophosphorus insecticides (Eisler and Weinstein, 1967); and influence of dissolved carbonates (Tabata, 1969) and chelators (Keckes et al., 1968, 1969) on zinc uptake and retention in mussels. In the case of chelators, EDTA increased the loss rate of zinc from mussels at 50.0 mg EDTA/L, but uptake rates were depressed in the range of 0.01-5.0 mg EDTA/L (Keckes et al., 1968, 1969). To confound matters, the loss rate of zinc from some species of mussels was not constant, suggesting multicompartmental zinc metabolism, dependent, perhaps, on the solubility of various chemical species (Keckes et al., 1968; Tabata, 1969; Van Weers, 1973). Mixtures of zinc and copper, and also mercury and zinc, were more than additive in toxicity to oyster larvae (Sprague, 1986). Pre-exposure of the common mussel, M. edulis, to 0.05 mg
360 Chapter 6 Zn/L for 28 days conferred increased tolerance to 0.075 mg inorganic mercury/L (Roesijadi and Fellingham, 1987).
6.53.16 Laboratory Studies Uptake, retention, and translocation of zinc by molluscs under controlled physicochemical conditions is a subject that has received extensive documentation (D’Silva and Kureishy, 1978; Eisler, 1977a, 2000f; Keckes et al., 1968, 1969; Mehran and Tremblay, 1965; Metian et al., 2008; Mishima and Odum, 1963; Pentreath, 1973; Phillips, 1977a; Pringle et al., 1968; Romeril, 1971; Shuster and Pringle, 1968, 1969; Young and Folsom, 1967). M. edulis has been used extensively as a model for molluscan zinc kinetics. Results of selected studies follow. In the common mussel, zinc is taken up by the digestive gland, gills, and mantle and rapidly transported via hemolymph where it is stored as insoluble granules (Lobel and Marshall, 1988). There is a high degree of variability in zinc content of soft tissues of M. edulis due entirely to an unusually high degree of variability in kidney zinc of 97.0-7864.0 mg/kg DW (Lobel, 1987). This variability in kidney zinc content is attributed mainly to a low-molecular-weight zinc complex (MW 700-1300)that showed a high degree of variability and a positive correlation with kidney zinc concentration (Lobel and Marshall, 1988). However, at low ambient concentrations of 0.05 mg Zn/L, the most sensitive bioindicators of zinc exposure were gills and labial palps (Amiard-Triquet et al., 1988). Food composition had little effect on tissue distribution of radiozinc-65 in mussels, as judged by 5-day feeding studies of radiolabeled diatoms (Thalassiosira pseudonana), green alga (Dunaliella tertiolecta), glass beads, and egg albumin particles (Fisher and Teyssie, 1986). Soft part BCF values ranged between 12 and 35 times that of the medium and was probably de to a rapid desorption of radiozinc from the food particles into the acidic gut, followed by binding to specific ligands or molecules. The half-time persistence in mussel soft parts ranged from 42 to 80 days for all food items—including glass beads—and about 20 days in shell (Fisher and Teyssie, 1986; Wang et al., 1996). Zinc concentrations in mussels are proportionately related to zinc loadings in the water column and to the AE of ingested particles, which in M. edulis ranges from 32% to 41% (Wang et al., 1996). Elevated temperatures in the range 10-25 C were associated with increased uptake rates of zinc from seawater by mussels (Watkins and Simkiss, 1988). If the temperature is oscillated through this range over a 6 h period, there is a further enhancement of zinc uptake. This effect parallels decreases in zinc content of cytosol fractions and increases in granular fractions (Watkins and Simkiss, 1988). Mussels were more sensitive to zinc than were other bivalves tested. The pumping rate of mussels completely stopped for up to 7 h on exposure to 0.470.86 mg Zn/L; other bivalves tested showed only a 50% reduction in filtration rates in the range 0.75-2.0 mg Zn/L (Redpath and Davenport, 1988). M. edulis accumulates zinc under natural conditions, but sometimes does not depurate (Luten et al., 1986). This conclusion was
Molluscs 361 based on results of a study wherein mussels were transferred from a pristine environment in the Netherlands to a polluted estuary for 70 days, than back again for 77 days. At the start, zinc concentration was 106.0 mg/kg DW soft parts. By day 70, it had risen to 265.0 mg/ kg DW, at a linear daily uptake rate of 0.47 mg/kg, but mussels contained 248.0 mg/kg DW on day 147, indicating that elimination was negligible (Luten et al., 1986). In another study, zinc depressed sperm motility through respiratory inhibition at 6.6 mg/L, a concentration much higher than those normally found environmentally (Earnshaw et al., 1986). In mussel spermatozoa, zinc caused reductions of bound calcium and phosphorus in both acrosomes and mitochondria, suggesting increased permeability of organelle membranes to both elements (Earnshaw et al., 1986). Results of uptake studies of ligand-bound 65Zn by the green mussel, P. viridis, show that radiozinc uptake could not be fully explained by free zinc concentrations in the presence of different ligands, indicating that metal-ligand complexes were available for uptake (Chuang and Wang, 2006). Scallops, C. radula held for 96 h in seawater containing 65 Zn had BCFs of 149 in total soft parts; however the BCF for kidney was 549 (Metian et al., 2008). Marked interspecies variations were documented in ability to regulate zinc accumulation. At comparatively low ambient zinc concentrations of 0.1 or 0.2 mg/L, crassostreid oysters continued to accumulate zinc over a 20 week period (maximum value recorded of 3813.0 mg Zn/kg FW soft parts) with little evidence of regulation (Shuster and Pringle, 1968, 1969). But softshell clams, M. arenaria, at 0.5 mg Zn/L showed some regulatory ability at comparatively low water temperatures during exposure for 16 weeks, as evidenced by a drop in the concentration factor (Eisler, 1977b). This was not evident at higher temperatures during exposure for only 2 weeks, although accumulation was significantly more rapid (Eisler, 1977b). Mussels, M. edulis, however, appear to plateau or regulate zinc accumulations at concentrations above 0.4 mg Zn/L seawater (Phillips, 1977a). Maximum net daily accumulation rates recorded, in mg Zn/kg FW whole organism, were 7.7 for the common mussel, 19.8 for the American oyster, and 32.0 for the soft shell clam; in general, accumulation rates and total accumulations were higher at elevated water temperatures and at higher ambient zinc water concentrations (Eisler, 1980). Loss rate of zinc from mussels, M. galloprovincialis, was greater with shorter contact time in zinc-contaminated seawater, and loss rate was greater from shell than soft tissues (Keckes et al., 1969). A similar pattern was observed in L. obtusata (Mehran and Tremblay, 1965). Stomach and digestive gland of mussels had the highest accumulations of zinc, but loss rate of zinc from these tissues was also highest (Pentreath, 1973). Mussels accumulate 65Zn slowly from seawater and depurate it rapidly indicating a reduced risk of contamination of mussels following incidental release of 65Zn in coastal waters (Van Weers, 1973). Loss rate of zinc in laboratory populations of bivalves may be lower than those in natural populations (Romeril, 1971), although this has not been resolved with certainty. For a marine
362 Chapter 6 gastropod, Littorina irrorata, zinc excretion seems governed by increasing respiration rate (linked to increasing water temperature) and increasing body size (Mishima and Odum, 1963). Variability in daily zinc accumulation rates by the softshell clam, M. arenaria, is one example what may be typical for marine bivalve molluscs. During immersion in 0.5 mg Zn/L in flow-through system at elevated (16-22 C) temperatures, Mya soft parts accumulated 2.0 mg Zn/kg FW daily during the first 24 h; between 24 h and 7 days this value was 7.7; and between 7 and 14 days, 3.3. Under the same conditions, except that ambient zinc levels were maintained at 2.5 mg/L, the accumulation rate during the first 24 h was 32.0 mg Zn/kg FW soft parts daily; between 24 h and 7 days, this dropped to 11.7 mg Zn/kg daily. At lower temperatures of 0-10 C, and 0.5 mg Zn/L, Mya accumulated zinc at the rate of 0.9 mg/kg FW daily during the first 42 days; however, between days 42 and 112, Mya lost zinc at the rate of 0.24 mg/kg FW daily. Eisler (1977b) concluded that changes in accumulation rates of zinc by Mya reflected, in part, complex interaction effects between water temperature, ambient zinc concentrations, duration and season of exposure, and physiological saturation and detoxication mechanisms. Deficiency and toxicity effects of zinc in molluscs are under investigation. Zinc deficiency effects have been produced experimentally in a wide variety of marine organisms, including molluscs, at nominal seawater concentrations between 0.00065 and 0.0065 mg Zn/L; however, zinc deficiency in natural waters has not yet been credibly documented for molluscs (Eisler, 2000f). Theoretically, whole molluscs should contain at least 34.5 mg total Zn/kg DW in order to avoid zinc deficiency (White and Rainbow, 1985), but this requires verification. Zinc was most toxic to representative molluscs at elevated temperatures and low salinities (Khangarot and Ray, 1987; Sprague, 1986), at earlier developmental stages (Munzinger and Guarducci, 1988), at low dissolved oxygen (Khangarot and Ray, 1987), and with increasing exposure to high zinc concentrations (Amiard-Triquet et al., 1988). The LC50(96 h) range for zinc and representative molluscs was 0.195 mg/L for embryos of the hardshell clam, M. mercenaria, to more than 320.0 mg/L for adults of the Baltic clam, M. balthica (Eisler, 2000f). Molluscan deaths and developmental abnormalities were common at 0.05 mg Zn/L in larvae of the red abalone, H. rufescens (Hunt and Anderson, 1989), at 0.12 mg Zn/L in larvae of the bay scallop (Yantian, 1989), at 0.195 mg/L in embryos of the hardshell clam (USEPA, 1987), at 0.23 mg Zn/L in embryos of the American oyster and larvae of the Pacific oyster (USEPA, 1987), at 1.75 mg Zn/L in adults of the common mussel in 48 h (Hunt and Anderson, 1989), and at 6.1 mg/L in adult green-lipped mussels P. viridis (Chan, 1988b). Adverse sublethal effects of zinc to representative molluscs were most pronounced among embryos and larvae. Adverse effects documented at 0.01-0.02 mg Zn/L include reduced settlement of larvae of the Pacific oyster in 20 days (USEPA, 1987), and significant accumulations in 42 days in kidney and other tissues in adults of the gastropod L. littorea
Molluscs 363 (Mason, 1988). At 0.03-0.035 mg Zn/L, there was a reduction in larval settlement of the Pacific oyster in 6 days (USEPA, 1987). And at 0.05 mg Zn/L, there was a 22% reduction in growth rate in 9 days of larvae of the bay scallop, A. irradians (Yantian, 1989). Adults of the clam, D. trunculus, immersed for 24 h in seawater containing 0.1 mg Zn/L had feeding rate inhibited by 25% (Neuberger-Cywiak et al., 2007).
6.53.17 Proposed Criteria Most species of molluscs can tolerate without harm seawater concentrations up to 0.054 mg total Zn/L (Sprague, 1986), although sensitive species—such as larvae of the Pacific oyster— are harmed at 0.01-0.02 mg Zn/L (USEPA, 1987). Proposed criteria to protect marine molluscs include a mean seawater concentration of less than 0.058 mg Zn/L, never to exceed 0.17 mg/L; for acid-soluble zinc, these values are less than 0.086 and 0.095 mg Zn/L, respectively (USEPA, 1980d, 1987). However, as shown earlier, sensitive species of molluscs are adversely affected at significantly lower concentrations, suggesting that these proposed criteria be further scrutinized before implementation.
6.54 Zirconium The single datum available on zirconium and field collections of molluscs is that of Karbe et al. (1977) indicating that soft parts of the common mussel, M. edulis contained between 0.62 and 43.0 mg Zr/kg DW.
6.55 Literature Cited Aarkrog, A., 1971. Radioecological investigations of plutonium in an arctic marine environment. Health Phys. 20, 31–47. Aarkrog, A., 1977. Environmental behaviour of plutonium accidentally released at Thule, Greenland. Health Phys. 32, 271–284. Aarkrog, A., 1990. Environmental radiation and radiation releases. Int. J. Radiat. Biol. 57, 619–631. Abbe, G.R., Sanders, J.G., 1990. Pathways of silver uptake and accumulation by the American oyster (Crassostrea virginica) in Chesapeake Bay. Estuar. Coast. Shelf Sci. 31, 113–123. Abbott, O.J., 1977. The toxicity of ammonium molybdate to marine invertebrates. Mar. Pollut. Bull. 8, 204–205. Absil, M.C.P., Gerringa, L.S.A., Wolterbeek, B.T., 1993. The relation between salinity and copper complexing capacity of natural estuarine waters and the uptake of dissolved 64Cu by Macoma balthica. Chem. Spec. Bioavail. 5, 119–128. Adema, D.M.M., De Swaaf-Mooy, S.I., Bais, P., 1972. Laboratory investigations concerning the influence of copper on mussels (Mytilus edulis). TNO-Nieuws 27, 482–487. Airas, S., Duinker, A., Julshamn, K., 2004. Copper, zinc, arsenic, cadmium, mercury, and lead in blue mussels (Mytilus edulis) in the Bergen Harbor area, western Norway. Bull. Environ. Contam. Toxicol. 73, 276–284. Alexander, C.V., Young, D.R., 1976. Trace metals in southern California mussels. Mar. Pollut. Bull. 7, 7–9. Alquezar, R., Markich, S.J., Twining, J.R., 2007. Uptake and loss of dissolved 109Cd and 75Se in estuarine macroinvertebrates. Chemosphere 67, 1201–1210. Alzieu, C., Sanjuan, J., Deltreil, J.P., Borel, M., 1986. Tin contamination in Arcachon Bay: effects on oyster shell anomalies. Mar. Pollut. Bull. 17, 494–498.
364 Chapter 6 Amaral, M.C.B., Rebelo, M.F., Torres, J.P.M., Pfeiffer, W.C., 2005. Bioaccumulation and depuration of Zn and Cd in mangrove oysters (Crassostrea rhizophorae Guilding, 1828) transplanted to and from a contaminated tropical lagoon. Mar. Environ. Res. 59, 277–285. Amiard, J.C., Amiard-Triquet, C., Berthet, B., Metayer, C., 1986. Contribution to the ecotoxicological study of cadmium, lead, copper and zinc in the mussel Mytilus edulis. I. Field study. Mar. Biol. 90, 425–431. Amiard-Triquet, C., Amiard, J.C., 1976. L’orgaotropisme du 60Co chez Scrobicularia plana et Carcinus maenas en fonction du vecteur de contamination. Oikos 27, 122–126. Amiard-Triquet, C., Amiard, J.C., Berthet, B., Metayer, C., 1988. Field and experimental study of the bioaccumulation of some trace metals in a coastal food chain: seston, oyster (Crassostrea gigas), drill (Ocenebra erinacea). Water Sci. Technol. 20, 13–21. Anajjar, E.M., Chiffoleau, J.F., Bergayou, H., Moukrim, A., Burgeot, T., Cheggour, M., 2008. Monitoring of trace metal contamination in the Souss estuary (south Morocco) using the clams Cerastoderma edule and Scrobicularia plana. Bull. Environ. Contam. Toxicol. 80, 283–288. Anderlini, V., 1974. The distribution of heavy metals in the red abalone, Haliotis rufescens, on the California coast. Arch. Environ. Contam. Toxicol. 2, 253–265. Anderlini, V.C., 1992. The effect of sewage on trace metal concentrations on scope for growth in Mytilus edulis aoteanus and Perna canaliculus from Wellington Harbour, New Zealand. Sci. Total Environ. 125, 263–288. Andersen, R.A., Eriksen, K.D.H., Bakke, T., 1989. Evidence of the presence of a low molecular weight, nonmetallothionein-like metal-binding protein in the marine gastropod, Nassarius reticulatus L. Comp. Biochem. Physiol. 94B, 285–291. Andrews, H.L., Warren, S., 1969. Ion scavenging by the eastern clam and quahaug. Health Phys. 17, 807–810. Anonymous, 1987. Legislators consider plan to ban TBT paints on small craft only. Ecol. USA July 20, 1937, 124. Arai, T., Ikemoto, T., Hokura, A., Terada, Y., Kunito, T., Tanabe, S., et al., 2004. Chemical forms of mercury and cadmium accumulated in marine mammals and seabirds as determined by XAFS analysis. Environ. Sci. Technol. 38, 6468–6474. Argese, E., Bettiol, C., Ghirardini, A.V., Fasolo, M., Giurin, G., Ghetti, P.F., 1998. Comparison of in vitro submitochondrial particle and Microtox assays for determining the toxicity of organotin compounds. Environ. Toxicol. Chem. 17, 1005–1012. Argiero, L., Manfredini, S., Palmas, G., 1966. Absorption de produits de fission par les organismes marins. Health Phys. 12, 1259–1265. Avargues, M., Ancellin, J., Vilquin, A., 1968. Experimental investigation on the accumulation of radionuclides by marine organisms. In: Proceedings of the Third International Colloquium on Medical Oceanography, Fifth and Sixth Sessions, pp. 87–100. Belanger, S.E., Farris, J.L., Cherry, D.S., Cairns Jr., J., 1990. Validation of Corbicula fluminea growth reductions induced by copper in artificial streams and river systems. Can. J. Fish. Aquat. Sci. 47, 904–914. Belcheva, N.N., Zakhartsev, M., Silina, A.V., Slinko, E.N., Chelomin, V.P., 2006. Relationship between shell weight and cadmium content in whole digestive gland of the Japanese scallop Patinopecten yessoensis (Jay). Mar. Environ. Res. 61, 396–409. Bergasa, O., Ramirez, R., Collado, C., Hernandez-Brito, J.J., Gelado-Caballero, M.D., Rodriguez-Somozas, M., et al., 2007. Study of metals concentration levels in Patella piperata throughout the Canary Islands, Spain. Environ. Monit. Assess. 127, 127–133. Berland, B.R., Bonin, D.J., Kapkov, W.I., Maestrini, S.Y., Arlhac, D.P., 1976. Action toxique de quatre metaux lourds sur la croissance d’algues unicellulaires marines. C. R. Acad. Sci. Paris 282D, 633–636. Berrow, S.D., 1991. Heavy metals in sediments and shellfish from Cork Harbour, Ireland. Mar. Pollut. Bull. 22, 467–469. Berthet, B., Amiard-Triquet, C., Martoja, R., 1990. Effets chimiques et histologiques de la decontamination de l’huitre Crassostrea gigas Thurberg prealablement exposee a l’argent. Water Air Soil Pollut. 50, 355–369.
Molluscs 365 Berthet, B., Amiard, J.C., Amiard-Triquet, C., Martoja, M., Jeantet, A.Y., 1992. Bioaccumulation, toxicity and physico-chemical speciation of silver in bivalve molluscs: ecotoxicological and health consequences. Sci. Total Environ. 125, 97–122. Bertine, K.K., Goldberg, E.D., 1972. Trace elements in clams, mussels, and shrimps. Limnol. Oceanogr. 17, 877–884. Berto, D., Giani, M., Boscolo, R., Covelli, S., Giovanardi, O., Massironi, M., et al., 2007. Organotins (TBT and DBT) in water, sediments, and gastropods of the southern Venice lagoon (Italy). Mar. Pollut. Bull. 55, 425–435. Betzer, S.B., 1972. Copper metabolism, copper toxicity, and a review of the function of hemocyanin in Busycon canaliculatum L. Ph.D. thesis, University of Rhode Island, Kingston, 133 pp. Betzer, S.B., Pilson, M.E.Q., 1974. The seasonal cycle of copper concentration in Busycon canaliculatum L. Biol. Bull. 146, 165–175. Betzer, S.B., Pilson, M.E.Q., 1975. Copper uptake and excretion by Busycon canaliculatum. L. Biol. Bull. 148, 1–15. Betzer, S.B., Yevich, P.P., 1975. Copper toxicity in Busycon canaliculatum. L. Biol. Bull. 148, 16–25. Bhatt, Y.M., Sastry, V.N., Shah, S.M., Krishnamoorthy, T.M., 1968. Zinc, manganese and cobalt contents of some marine bivalves from Bombay. Proc. Natl. Inst. Sci. India B Biol. Sec. 34(B6), 283–287. Bhosle, N.B., Matondkar, S.G.P., 1978. Variation in trace metals in two populations of green mussel Mytilus viridis L. from Goa. Mahasagar Bull. Nat. Inst. Oceanogr. 11, 191–194. Bianchini, A., Playle, R.C., Wood, C.M., Walsh, P.J., 2007. Short-term silver accumulation in tissues of three marine invertebrates: shrimp Penaeus duorarum, sea hare Aplysia californica, and sea urchin Diadema antillarum. Aquat. Toxicol. 84, 182–189. Bigler, J., Crecelius, E., 1998. Methods for the analysis of arsenic speciation in seafood from Cook Inlet, Alaska. In: Society of Environmental Geochemistry and Health, 3rd International Conference on Arsenic Exposure and Health Effects, 9 pp. Bloom, M., Ayling, G.M., 1977. Heavy metals in the Derwent estuary. Environ. Geol. 1, 3–22. Blunden, S.J., Cusack, P.A., Hill, R., 1985. The Industrial Uses of Tin Chemicals. Royal Society of Chemistry, London, 337 pp. Bohn, A., 1975. Arsenic in marine organisms from West Greenland. Mar. Pollut. Bull. 6, 87–89. Bordin, G., McCourt, J., Rodriguez, A., 1994. Trace metals in the marine bivalve Macoma balthica in the Westerschelde estuary, the Netherlands. Part 2: intracellular partitioning of copper, cadmium, zinc and iron—variations of the cytoplasmic metal concentrations in natural and in vitro contaminated clams. Sci. Total Environ. 151, 113–124. Boyden, C.R., 1974. Trace element content and body size in molluscs. Nature 251, 311–314. Boyden, C.R., 1977. Effect of size upon metal content of shellfish. J. Mar. Biol. Assoc. UK 57, 675–714. Boyden, C.R., Romeril, M.G., 1974. A trace metal problem in pond oyster culture. Mar. Pollut. Bull. 5, 74–78. Boyden, C.R., Watling, H., Thornton, I., 1975. Effect of zinc on the settlement of the oyster Crassostrea gigas. Mar. Biol. 31, 227–234. Brooks, R.R., Rumsby, M.G., 1965. The biogeochemistry of trace element uptake by some New Zealand bivalves. Limnol. Oceanogr. 10, 521–527. Brooks, R.R., Rumsby, M.G., 1967. Studies on the uptake of cadmium by the oyster Ostrea sinuata (Lamarck). Aust. J. Mar. Freshw. Res. 15, 53–61. Brooks, S.J., Bolam, T., Tolhurst, L., Bassett, J., La Roche, J., Waldock, M., et al., 2007. Effects of dissolved organic carbon on the toxicity of copper to the developing embryos of the Pacific oyster (Crassostrea gigas). Environ. Toxicol. Chem. 26, 1756–1763. Brown, C.L., Luoma, S.N., 1995. Use of the euryhaline bivalve Potamocorbula amurensis as a biosentinel species to assess trace metal contamination in San Francisco Bay. Mar. Ecol. Prog. Ser. 124, 129–142. Brown, K.R., McPherson, R.G., 1992. Concentrations of copper, zinc and lead in the Sydney rock oyster, Saccostrea commercialis (Iredale and Roughley) from the Georges River, New South Wales. Sci. Total Environ. 126, 27–33.
366 Chapter 6 Bryan, G.W., 1963a. The accumulation of radioactive caesium by marine invertebrates. J. Mar. Biol. Assoc. UK 43, 519–539. Bryan, G.W., 1963b. The accumulation of 137Cs by brackish water invertebrates and its relation to the regulation of potassium and sodium. J. Mar. Biol. Assoc. UK 43, 541–565. Bryan, G.W., 1971. The effects of heavy metals (other than mercury) on marine and estuarine organisms. Proc. R. Soc. Lond. 177B, 389–410. Bryan, G.W., 1973. The occurrence and seasonal variation of trace metals in the scallops Pecten maximus (L.) and Chlamys opercularis (L.). J. Mar. Biol. Assoc. UK 53, 145–166. Bryan, G.W., Hummerstone, L.G., 1973. Brown seaweed as an indicator of heavy metals in estuaries in southwest England. J. Mar. Biol. Assoc. UK 59, 89–108. Bryan, G.W., Hummerstone, L.G., 1977. Indicators of heavy metal contamination in the Looe estuary (Cornwall) with particular regard to silver and lead. J. Mar. Biol. Assoc. UK 57, 75–92. Bryan, G.W., Hummerstone, L.G., 1978. Heavy metals in the burrowing bivalve Scrobicularia plana from contaminated and uncontaminated estuaries. J. Mar. Biol. Assoc. UK 58, 401–419. Bryan, G.W., Langston, W.J., 1992. Bioavailability, accumulation and effects of heavy metals in sediments with special reference to United Kingdom estuaries: a review. Environ. Pollut. 76, 89–131. Bryan, G.W., Uysal, H., 1978. Heavy metals in the burrowing bivalve Scrobicularia plana from the Tamar estuary in relation to environmental levels. J. Mar. Biol. Assoc. UK 58, 89–108. Bryan, G.W., Potts, G.W., Forster, G.R., 1977. Heavy metals in the gastropod mollusc Haliotis tuberculata (L.). J. Mar. Biol. Assoc. UK 57, 379–390. Bryan, G.W., Langston, W.J., Hummerstone, L.S., Burt, G.R., Ho, Y.B., 1983. An assessment of the gastropod, Littorina littorea, as an indicator of heavy-metal contamination in United Kingdom estuaries. J. Mar. Biol. Assoc. UK 63, 327–345. Bryan, G.W., Gibbs, P.E., Hummerstone, L.G., Burt, G.R., 1986. The decline of the gastropod Nucella lapillus around south-west England: evidence for the effect of tributyltin from antifouling paints. J. Mar. Biol. Assoc. UK 66, 611–640. Bryan, G.W., Gibbs, P.E., Hummerstone, L.G., Burt, G.R., 1987a. Copper, zinc, and organotin as long-term factors in governing the distribution of organisms in the Fal estuary in southwest England. Estuaries 10, 208–219. Bryan, G.W., Gibbs, P.E., Burt, G.R., Hummerstone, L.G., 1987b. The effects of tributyltin (TBT) accumulation on adult dog-whelks, Nucella lapillus: long-term field and laboratory experiments. J. Mar. Biol. Assoc. UK 67, 525–544. Bryant, V., Newbery, D.M., McLusky, D.S., Campbell, R., 1985. Effect of temperature and salinity on the toxicity of arsenic to three estuarine invertebrates (Corophium volutator, Macoma balthica, Tubifex costatus). Mar. Ecol. Prog. Ser. 24, 129–137. Burger, J., Gochfeld, M., 2006. Seasonal differences in heavy metals and metalloids in Pacific blue mussels Mytilus [edulis] trossulus from Adak Island in the Aleutian Chain, Alaska. Sci. Total Environ. 368, 937–950. Burger, J., Stern, A.H., Gochfeld, M., 2005. Mercury in commercial fish: optimizing individual choices to reduce risk. Environ. Health Perspect. 113, 266–270. Burger, J., Gochfeld, M., Jeitner, C., Burke, S., Stamm, T., Snigaroff, R., et al., 2007a. Mercury levels and potential risk from subsistence foods from the Aleutians. Sci. Total Environ. 384, 93–105. Burger, J., Gochfeld, M., Jewett, S.C., 2007b. Radionuclide concentrations in benthic invertebrates from Amchitka and Kiska Islands in the Aleutian Chain, Alaska. Environ. Monit. Assess. 128, 329–341. Burt, A., Maher, W., Roach, A., Krikowa, F., Honkoop, P., Bayne, B., 2007. The accumulation of Zn, Se, Cd, and Pb and physiological condition of Anadara trapezia transplanted to a contamination gradient in Lake Macquarie, New South Wales, Australia. Mar. Environ. Res. 64, 54–78. Burton, J.D., Leatherland, T.M., 1971. Mercury in a coastal marine environment. Nature 231, 440–442. Bustamante, P., Lahaye, V., Durnez, C., Churlaud, C., Caurant, F., 2006a. Total and organic Hg concentrations in cephalopods from the north eastern Atlantic waters: influence of geographical origin and feeding ecology. Sci. Total Environ. 368, 585–596.
Molluscs 367 Bustamante, P., Teyssie, J.L., Fowler, S.W., Warnau, M., 2006b. Assessment of the exposure pathway in the uptake and distribution of americium and cesium in cuttlefish (Sepia officinalis) at different stages of its life cycle. J. Exp. Mar. Biol. Ecol. 331, 198–207. Bustamante, P., Gonzalez, A.F., Rocha, F., Miramand, P., Guerra, A., 2008. Metal and metalloid concentrations in the giant squid Architeuthis dux from Iberian waters. Mar. Environ. Res. 66, 278–287. Butterworth, J., Lester, P., Nickless, G., 1972. Distribution of heavy metals in the Severn estuary. Mar. Pollut. Bull. 3, 72–74. Byers, J.E., 1993. Variations in the bioaccumulation of zinc, copper, and lead in Crassostrea virginica and Ilyanassa obsoleta in marinas and open water environments. J. Elisha Mitchell Sci. Soc. 109, 163–170. Cain, D.J., Luoma, S.N., 1986. Effect of seasonally changing tissue weight on trace metal concentrations in the bivalve Macoma balthica, in San Francisco Bay. Mar. Ecol. Prog. Ser. 28, 209–217. Cain, D.J., Luoma, S.N., 1990. Influence of seasonal growth, age, and environmental exposure on Cu and Ag in a bivalve indicator, Macoma balthica, in San Francisco Bay. Mar. Ecol. Prog. Ser. 60, 45–55. Cajaraville, M.P., Bebianno, M.J., Blasco, J., Porte, C., Sarasquete, C., Viarengo, A., 2000. The use of biomarker to assess the impact of pollution in coastal environments of Iberian Peninsula: a practical approach. Sci. Total Environ. 247, 295–311. Calabrese, A., Nelson, D.A., 1974. Inhibition of embryonic development of the hard clam, Mercenaria mercenaria, by heavy metals. Bull. Environ. Contam. Toxicol. 11, 92–97. Calabrese, A., Collier, R.S., Nelson, D.A., MacInnes, J.R., 1973. The toxicity of heavy metals to embryos of the American oyster Crassostrea virginica. Mar. Biol. 18, 162–166. Calabrese, A., MacInnes, J.R., Nelson, D.E., Miller, J.E., 1977a. Survival and growth of bivalve larvae under heavy-metal stress. Mar. Biol. 41, 179–184. Calabrese, A., Thurberg, F.P., Gould, E., 1977b. Effects of cadmium, mercury, and silver on marine animals. Mar. Fish. Rev. 39, 5–11. Calabrese, A., MacInnes, J.R., Nelson, D.A., Greig, R.A., Yevich, P.P., 1984. Effects of long-term exposure to silver or copper on growth, bioaccumulation and histopathology in the blue mussel Mytilus edulis. Mar. Environ. Res. 11, 253–274. Cappon, C.J., Smith, J.C., 1982. Chemical form and distribution of selenium in edible seafood. J. Anal. Toxicol. 6, 10–21. Cardwell, R.D., Sheldon, A.W., 1986. A risk assessment concerning the fate and effects of tributyltins in the aquatic environment. In: Maton, G.L. (Ed.), Proceedings Oceans 86 Conference, Washington, DC, September 23-25, 1986, vol. 4. Organotin Symposium. Available from Marine Technology Society, 2000 Florida Avenue NW, Washington, DC, pp. 1117–1129. Carlisle, D.B., 1958. Niobium in ascidians. Nature 181, 933. Carmichael, N.G., Squibb, K.S., Fowler, B.A., 1979. Metals in the molluscan kidney: a comparison of two closely related bivalve species (Argopecten), using X-ray microanalysis and atomic absorption spectroscopy. J. Fish. Res. Board Can. 36, 1149–1155. Carr, R.S., McCullough, W.L., Neff, J.M., 1982. Bioavailability of chromium from a used chrome lignosulphonate drilling mud to five species of marine invertebrates. Mar. Environ. Res. 6, 189–203. Carvalho, C.E.V., Lacerda, L.D., Gomes, M.P., 1991. Heavy metal contamination of the marine biota along the Rio de Janeiro coast, SE Brazil. Water Air Soil Pollut. 57/58, 645–653. Carvalho, C.E.V., Lacerda, L.D., Gomes, M.P., 1993. Metais pesados na biota bentica da Baia de Sepetiba e Angra dos Reis, RJ. Acta Limnol. Brasil 6, 222–229. Casterline Jr., J.L., Yip, G., 1975. The distribution and binding of cadmium in oyster, soybean, and rat liver and kidney. Arch. Environ. Contam. Toxicol. 3, 319–329. Champ, M.A., 1986. Organotin symposium: introduction and review. In: Maton, G.L. (Ed.), Proceedings Oceans 86 Conference, Washington DC, September 23-25, 1986, vol. 4. Organotin Symposium. Available from Marine Technology Society, 2000 Florida Avenue NW, Washington, DC, pp. 1093–1100. Chan, H.M., 1988a. A survey of trace metals in Perna viridis (L.) (Bivalvia: mytilacea) from the coastal waters of Hong Kong. Asian Mar. Biol. 5, 89–102.
368 Chapter 6 Chan, H.M., 1988b. Accumulation and tolerance to cadmium, copper, lead and zinc by the green mussel Perna viridis. Mar. Ecol. Prog. Ser. 48, 295–303. Chan, K.M., Yeung, K.M.L., Cheung, K.C., Wong, M.H., Qiu, J.W., 2008. Seasonal changes in imposex and tissue burden of butyltin compounds in Thais clavigera populations along the coastal area of Mirs Bay, China. Mar. Pollut. Bull. 57, 645–651. Chau, Y.K., Maguire, R.J., Wong, P.T.S., Glen, B.A., Bengert, G.A., Tkacz, R.J., 1984. Occurrence of methyltin and butyltin species in environmental samples in Ontario. Natl. Water Inst. Rep., 8401, pp. 1–25. Cheevaparanapivat, V., Menasveta, P., 1979. Total and organic mercury in marine fish of the upper Gulf of Thailand. Bull. Environ. Contam. Toxicol. 23, 291–299. Chelomin, V.P., Belcheva, N.N., 1992. The effect of heavy metals on processes of lipid peroxidation in microsomal membranes from the hepatopancreas of the bivalve mollusc Mizuhopecten yessoensis. Comp. Biochem. Physiol. 103C, 419–422. Cheung, Y.H., Wong, M.H., 1992. Trace metal contents of the Pacific oyster (Crassostrea gigas) purchased from markets in Hong Kong. Environ. Manag. 16, 753–761. Cheung, M.S., Fok, E.M.W., Ng, T.Y.T., Yen, Y.F., Wang, W.X., 2006. Subcellular cadmium distribution, accumulation, and toxicity in a predatory gastropod, Thais clavigera, fed different prey. Environ. Toxicol. Chem. 25, 174–181. Chipman, W., Thommeret, J., 1970. Manganese content and the occurrence of fallout 54Mn in some marine benthos of the Mediterranean. Bull. Inst. Oceanogr. 69(1402), 1–15. Chou, C.L., Uthe, J.F., Zook, E.G., 1978. Polarographic studies on the nature of cadmium in scallop, oyster, and lobster. J. Fish. Res. Board Can. 35, 409–413. Chow, T.J., Snyder, H.G., Snyder, C.B., 1976. Mussels (Mytilus sp.) as an indicator of lead pollution. Sci. Total Environ. 6, 55–63. Chu, K.H., Cheung, W.M., Lau, S.K., 1990. Trace metals in bivalves and sediments from Tolo Harbour, Hong Kong. Environ. Int. 16, 31–36. Chuang, C.Y., Wang, W.X., 2006. Co-transport of metal complexes by the green mussel Perna viridis. Environ. Sci. Technol. 40, 4523–4527. Claisse, D., Alzieu, C., 1993. Copper contamination as a result of antifouling paint regulations? Mar. Pollut. Bull. 26, 395–397. Clarke, G.L., 1947. Poisoning and recovery in barnacles and mussels. Biol. Bull. 92, 73–91. Coelho, J.P., Pimenta, J., Gomes, R., Barroso, C.M., Pereira, M.E., Pardal, M.A., et al., 2006a. Can Nassarius reticulatus be used as a bioindicator for Hg contamination? Results for a longitudinal study of the Portuguese coastline. Mar. Pollut. Bull. 52, 674–680. Coelho, M.R., Langston, W.J., Bebianno, M.J., 2006b. Effect of TBT on Ruditapes decussatus juveniles. Chemosphere 63, 1499–1505. Coglianse, M.P., Martin, M., 1981. Individual and interactive effects of environmental stress on the embryonic development of the Pacific oyster, Crassostrea gigas. I. The toxicity of copper and silver. Mar. Environ. Res. 5, 13–27. Colaco, A., Bustamante, P., Fouquet, Y., Sarradin, P.M., Serrao-Santos, R., 2006. Bioaccumulation of Hg, Cu, and Zn in the Azores triple junction hydrothermal vent fields food web. Chemosphere 65, 2260–2267. Coleman, N., 1980. The effect of emersion on cadmium accumulation by Mytilus edulis. Mar. Pollut. Bull. 11, 359–362. Colwell, R.R., Nelson Jr., J.D., 1975. Metabolism of mercury compounds in microorganisms. US Environ. Protect. Agen. Rep., 600/3-75–007, pp. 1–84. Colwell, R.R., Sayler, G.S., Nelson Jr., J.D., Justice, A., 1976. Microbial utilization of mercury in the aquatic environment. In: Nriagu, J.O. (Ed.), Environmental Biogeochemistry, Volume 2. Metals Transfer and Ecological Mass Balances. Ann Arbor Science Publishers, Ann Arbor, MI, pp. 437–487. Connell, D.B., Sanders, J.G., Riedel, G.F., Abbe, G.R., 1991. Pathways of silver uptake and trophic transfer in estuarine organisms. Environ. Sci. Technol. 25, 921–924. Connor, P.M., 1972. Acute toxicity of heavy metals to some marine larvae. Mar. Pollut. Bull. 3, 190–192.
Molluscs 369 Conti, M.E., Iacobucci, M., Cecchetti, G., Alimonti, A., 2008. Influence of weight on the content of trace metals in tissues of Mytilus galloprovincialis (Lamarck, 1819): a forecast model. Environ. Monit. Assess. 141, 27–34. Cooke, M., Nickless, G., Lawn, R.E., Roberts, D.J., 1979. Biological availability of sediment-bound cadmium to the edible cockle, Cerastoderma edule. Bull. Environ. Contam. Toxicol. 23, 381–386. Coombs, T.L., 1972. The distribution of zinc in the oyster Ostrea edulis and its relation to enzymic activity and to other metals. Mar. Biol. 12, 170–178. Cossa, D., Bourget, E., Piuze, J., 1979. Sexual maturation as a source of variation in the relationship between cadmium concentration and body weight of Mytilus edulis L. Mar. Pollut. Bull. 10, 174–176. Cosson, R.P., Thiebaut, E., Company, R., Castrec-Rouelle, M., Colaco, A., Martins, I., et al., 2008. Spatial variation of metal bioaccumulation in the hydrothermal vent mussel Bathymodiolus azoricus. Mar. Environ. Res. 65, 405–415. Costa, M.R.M., da-Fonseca, M.I.C., 1967. Teor de arsenico em mariscos. Rev. Portuguesa Farm. 17(1), 1–19. Craig, S., 1967. Toxic ions in bivalves. J. Am. Osteopath. Assoc. 66, 1000–1002. Cravo, A., Foster, P., Almeida, C., Bebianno, M.J., Company, R., 2008. Metal concentrations in the shell of Bathymodiolus azoricua from contrasting hydrothermal vent fields on the mid-Atlantic ridge. Mar. Environ. Res. 65, 338–348. Crecelius, E.A., 1993. The concentration of silver in mussels and oysters from NOAA National Status and Trends Mussel Watch Sites. In: Andren, A.W., Bober, T.W., Crecelius, E.A., Kramer, J.R., Luoma, S.N., Rodgers, J.H., Sodergren, A. (Eds.), Proceedings of the First International Conference on Transport, Fate, and Effects of Silver in the Environment. Univ. Wisconsin Sea Grant Inst, Madison, WI, pp. 65–66. Crowe, A.J., 1987. The chemotherapeutic properties of tin compounds. Drugs Future 12, 255–275. Crowley, M., Mitchell, P.I., O’Grady, J., Vires, J., Sanchez-Cabeza, J.A., Vidal-Quadras, A., et al., 1990. Radiocaesium and plutonium concentrations in Mytilus edulis (L.) and potential dose implications for Irish critical groups. Ocean Shoreline Manag. 13, 149–161. Culkin, F., Riley, J.P., 1958. The occurrence of gallium in marine organisms. J. Mar. Biol. Assoc. UK 37, 607–615. Cumont, G., Gilles, G., Bernard, F., Briand, M.B., Stephan, G., Ramonda, G., et al., 1975. Bilan de la contamination des poissons de mer par le mercure a l’occasion d’un controle portant sur 3 annees. Ann. Hyg. L. Fr.—Med. et Nut. 11(1), 17–25. Cunha, L., Amaral, A., Medeiros, V., Martins, G.M., Wallenstein, F.F.M.M., Couto, R.P., et al., 2008. Bioavailable metals and cellular effects in the digestive gland of marine limpets living close to shallow water hydrothermal vents. Chemosphere 71, 1356–1362. Cunningham, P.A., Tripp, M.R., 1973. Accumulation and depuration of mercury in the American oyster Crassostrea virginica. Mar. Biol. 20, 14–19. Cunningham, P.A., Tripp, M.R., 1975a. Factors affecting the accumulation and removal of mercury from tissues of the American oyster Crassostrea virginica. Mar. Biol. 31, 311–319. Cunningham, P.A., Tripp, M.R., 1975b. Accumulation, tissue distribution and elimination of 203HgCl2 and CH3 203 HgCl in the tissues of the American oyster Crassostrea virginica. Mar. Biol. 31, 324–334. Darracott, A., Watling, H., 1975. The use of molluscs to monitor cadmium levels in estuaries and coastal marine environments. Trans. R. Soc. S. Afr. 41(4), 325–338. Daskalakis, K.D., 1995. Silver in oyster soft tissue: relations to site selection and sampling size. In: Andren, A.W., Bober, T.W. (Organizers), Transport, Fate and Effects of Silver in the Environment. 3rd International Conference, Washington, DC, August 6-9, 1995. Univ. Wisconsin Sea Grant Inst, Madison, WI. Davies, M.S., 1992. Heavy metals in seawater: effects on limpet pedal mucus production. Water Res. 26, 1691–1693. Davies, I.M., McKie, J.C., Paul, J.D., 1986. Accumulation of tin and tributyltin from anti-fouling paint by cultivated scallops (Pecten maximum) and Pacific oysters (Crassostrea gigas). Aquaculture 55, 103–114.
370 Chapter 6 Davies, I.M., Bailey, S.K., Moore, D.C., 1987. Tributyltin in Scottish sea lochs, as indicated by degree of imposex in the dogwhelk, Nucella lapillus (L.). Mar. Pollut. Bull. 18, 404–407. Davies, I.M., Harding, M.J.C., Bailey, S.K., Shanks, A.M., Lange, R., 1997. Sublethal effects of tributyltin oxide on the dogwhelk Nucella lapillus. Mar. Ecol. Prog. Ser. 158, 191–204. Dean, R.B., 1972. The case against mercury. Nat. Tech. Infor. Serv. Springfield, VA, Doc. PB-213-6921–11. Decleir, W., Lemaire, J., Richard, A., 1970. Determination of copper in embryos and very young specimens of Sepia officinalis. Mar. Biol. 5, 256–258. Decleir, W., Vlaeminck, A., Geladi, P., Van Grieken, R., 1978. Determination of protein-bound copper and zinc in some organs of the cuttlefish, Sepia officinalis. L. Comp. Biochem. Physiol. 60B, 347–350. De Gieter, M., Leermakers, M., Van Ryssen, R., Noyen, J., Goeyens, L., Baeyens, W., 2002. Total and toxic arsenic levels in North Sea fish. Arch. Environ. Contam. Toxicol. 43, 406–417. Dehlinger, P., Fitzgerald, W.F., Feng, S.Y., Paskausky, D.F., Garvine, M.W., Bohlen, W.F., 1975. Determination of budgets of heavy metal wastes in Long Island Sound. Annual Rept. Parts I and II. Univ. Connecticut, Marine Sciences Inst, Groton, CT. Delhaye, W., Cornet, D., 1975. Contribution to the study of the effect of copper on Mytilus edulis during reproductive period. Comp. Biochem. Physiol. 50A, 511–513. Denton, G.R.W., Concepcion, L.P., Wood, H.R., Morrison, R.J., 2006. Trace metals in marine organisms from four harbours in Guam. Mar. Pollut. Bull. 52, 1784–1804. Deudero, S., Box, A., March, D., Valencia, J.M., Grau, A.M., Tintora, J., et al., 2007. Temporal trends of metals in benthic invertebrate species from the Balearic Islands, Western Mediterranean. Mar. Pollut. Bull. 54, 1545–1558. Devi, V.U., 1996. Bioaccumulation and metabolic effects of cadmium on marine fouling dressinid bivalve, Mutilopsis sallei (Recluz). Arch. Environ. Contam. Toxicol. 31, 47–53. De Wolf, P., 1975. Mercury content of mussels from West European coasts. Mar. Pollut. Bull. 6, 61–63. De Wolf, H., Rashid, R., 2008. Heavy metal accumulation in Littoraria scabra along polluted and pristine mangrove areas of Tanzania. Environ. Pollut. 152, 636–643. Diamond, J.M., Mackler, D.G., Collins, M., Gruber, D., 1990. Deviation of a freshwater silver criteria for the New River, Virginia, using representative species. Environ. Toxicol. Chem. 9, 1425–1434. Dick, J., Pugsley, L.I., 1950. The arsenic, lead, tin, copper, and iron content of canned clams, oysters, crabs, lobsters, and shrimps. Can. J. Res. 28F, 199–201. Dietz, R., Riget, F., Johansen, P., 1996. Lead, cadmium, mercury and selenium in Greenland marine animals. Sci. Total Environ. 186, 67–93. Di Giulio, R.T., Scanlon, P.F., 1985. Heavy metals in aquatic plants, clams, and sediments from the Chesapeake Bay U.S.A. Implications for waterfowl. Sci. Total Environ. 41, 259–274. Dillon, T.M., 1977. Mercury and the estuarine marsh clam, Rangia cuneata Gray. I. Toxicity. Arch. Environ. Contam. Toxicol. 6, 249–255. Dillon, T.M., Neff, J.M., 1978. Mercury and the estuarine marsh clam Rangia cuneata Gray. II. Uptake, tissue distribution and depuration. Mar. Environ. Res. 1, 67–77. Dimitriadis, V.K., Domouhtsidou, G.P., Raftopoulou, E., 2003. Localization of Hg and Pb in the palps, digestive gland and the gills in Mytilus galloprovincialis (L.) using autometallography and X-ray microanalysis. Environ. Pollut. 125, 345–353. D’Itri, F.M., 1972. Mercury in the aquatic ecosystem. Tech. Rep. Inst. Water Res. Michigan State Univ., Lansing, MI 23, 1–101. Dixon, D.R., Prosser, H., 1986. An investigation of the genotoxic effects of an organotin antifouling compound (bis (tributyltin) oxide) in the chromosomes of the edible mussel, Mytilus edulis. Aquat. Toxicol. 8, 185–195. Doi, R., Ui, J., 1975. The distribution of mercury in fish and its form of occurrence. In: Krenkel, P.A. (Ed.), Heavy Metals in the Aquatic Environment. Pergamon, New York, pp. 197–221. Dorneles, P.R., Lailson-Brito, J., dos Santos, R.A., da Costa, P.A.S., Malm, O., Azevedo, A.F., et al., 2007. Cephalopods and cetaceans as indicators of offshore bioavailability of cadmium off Central South Brazil Bight. Environ. Pollut. 148, 352–359.
Molluscs 371 Downes, K.M., 1957. An investigation of manganese and zinc in the oyster Crassostrea virginica (Gmelin). Ph.D. thesis, Univ. Maryland, College Park, pp. 1–54. Drifmeyer, N.E., 1974. Zn and Cu levels in the eastern oyster, Crassostrea virginica, from the lower James River. J. Wash. Acad. Sci. 64 (4), 292–294. D’Silva, C., Kureishy, T.W., 1978. Experimental studies on the accumulation of copper and zinc in the green mussel. Mar. Pollut. Bull. 9, 187–190. D’Silva, C., Quasim, S.Z., 1979. Bioaccumulation and elimination of copper in the rock oyster Crassostrea cucullata. Mar. Biol. 52, 343–346. Duchemin, M.B., Auffret, M., Wessel, N., Fortier, M., Morin, Y., Pellerin, J., et al., 2008. Multiple experimental approaches of immunotoxic effects of mercury chloride in the blue mussel, Mytilus edulis, through in vivo, in tubo and in vitro exposures. Environ. Pollut. 153, 416–423. Duke, T.W., 1967. Possible routes of zinc-65 from an experimental estuarine environment to man. J. Water Pollut. Control Fed. 39, 536–542. Earnshaw, M.J., Wilson, S., Akberali, H.B., Butler, R.D., Marriott, K.R.M., 1986. The action of heavy metals on the gametes of the marine mussel, Mytilus edulis (L.)—III. The effect of applied copper and zinc on sperm motility in relation to ultrastructural damage and intracellular metal localisation. Mar. Environ. Res. 20, 261–278. Ecological Analysts, Inc., 1981. In: The Sources, Chemistry, Fate, and Effects of Chromium in Aquatic Environments. Available from American Petroleum Institute, 2101 L Street NW, Washington, DC, 207 pp. Eganhouse, R.P., Young, D.R., 1978. In situ uptake of mercury by the intertidal mussel, Mytilus californianus. Mar. Pollut. Bull. 9, 214–217. Eisler, R., 1977a. Acute toxicities of selected heavy metals to the softshell clam, Mya arenaria. Bull. Environ. Contam. Toxicol. 17, 137–145. Eisler, R., 1977b. Toxicity evaluation of a complex metal mixture to the softshell clam, Mya arenaria. Mar. Biol. 43, 265–276. Eisler, R., 1978. Mercury contamination standards for marine environments. In: Thorp, J.H., Gibbons, J.W. (Eds.), Energy and Environmental Stress in Aquatic Systems. US Dept. Energy Sympos. Ser. 48. Available as CONF-771114 from NTIS, US Dept. Commerce, Springfield, VA, pp. 241–272. Eisler, R., 1979. Copper accumulations in coastal and marine environments. In: Nriagu, J.O. (Ed.), Copper in the Environment, Part I: Ecological Cycling. Wiley, New York, pp. 383–449. Eisler, R., 1980. Accumulation of zinc by marine biota. In: Nriagu, J.O. (Ed.), Zinc in the Environment, Part 2: Health Effects. Wiley, New York, pp. 259–351. Eisler, R., 1981. Trace Metal Concentrations in Marine Organisms. Pergamon, New York, 687 pp. Eisler, R., 1995a. Electroplating wastes in marine environments: a case history at Quonset Point, Rhode Island. In: Hoffman, D.J., Rattner, B.A., Burton Jr., G.A., Cairns Jr., A.J. (Eds.), Handbook of Ecotoxicology. Lewis Publishers, Boca Raton, FL, pp. 539–548. Eisler, R., 1995b. Ecological and toxicological aspects of the partial meltdown of the Chernobyl nuclear plant reactor. In: Hoffman, D.J., Rattner, B.A., Burton Jr., G.A., Cairns Jr., A.J. (Eds.), Handbook of Ecotoxicology. Lewis Publishers, Boca Raton, FL, pp. 549–564. Eisler, R., 2000. Mercury. In: Handbook of Chemical Risk Assessment: Health Hazards to Humans, Plants, and Animals. Vol. 1. Metals. Lewis Publishers, Boca Raton, FL, pp. 313–409. Eisler, R., 2000a. Chromium. In: Handbook of Chemical Risk Assessment: Health Hazards to Humans, Plants, and Animals. Vol. 1. Metals. Lewis Publishers, Boca Raton, FL, pp. 45–92. Eisler, R., 2000b. Copper. In: Handbook of Chemical risk Assessment: Health Hazards to Humans, Plants, and Animals. Vol. 1: Metals. Lewis Publishers, Boca Raton, FL, pp. 93–200. Eisler, R., 2000c. Lead. In: Handbook of Chemical Risk Assessment: Health Hazards to Humans, Plants, and Animals. Vol. 1: Metals. Lewis Publishers, Boca Raton, FL, pp. 201–311. Eisler, R., 2000d. Silver. In: Handbook of Chemical Risk Assessment: Health Hazards to Humans, Plants, and Animals. Vol. 1: Metals. Lewis Publishers, Boca Raton, FL, pp. 499–550. Eisler, R., 2000e. Tin. In: Handbook of Chemical Risk Assessment: Health Hazards to Humans, Plants, and Animals. Vol. 1: Metals. Lewis Publishers, Boca Raton, FL, pp. 551–603.
372 Chapter 6 Eisler, R., 2000f. Zinc. In: Handbook of Chemical Risk Assessment: Health Hazards to Humans, Plants, and Animals. Vol. 1: Metals. Lewis Publishers, Boca Raton, FL, pp. 605–714. Eisler, R., 2000g. Cadmium. In: Handbook of Chemical Risk Assessment: Health Hazards to Humans, Plants, and Animals. Vol. 1: Metals. Lewis Publishers, Boca Raton, FL, pp. 1–43. Eisler, R., 2003. The Chernobyl nuclear power plant reactor accident: ecotoxicological update. In: Hoffman, D.J., Rattner, B.A., Burton Jr., G.A., Cairns Jr., A.J. (Eds.), Handbook of Ecotoxicology, second ed. Lewis Publishers, Boca Raton, FL, pp. 703–736. Eisler, R., 2006. Mercury Hazards to Living Organisms. CRC Press, Boca Raton, FL, 312 pp. Eisler, R., Hennekey, R.J., 1977. Acute toxicities of Cd2+, Cr+6, Hg2+, Ni2+, and Zn2+ to estuarine macrofauna. Arch. Environ. Contam. Toxicol. 6, 315–323. Eisler, R., Weinstein, M.P., 1967. Changes in metal composition of the quahaug clam, Mercenaria mercenaria, after exposure to insecticides. Chesapeake Sci. 8, 253–258. Eisler, R., Zaroogian, G.E., Hennekey, R.J., 1972. Cadmium uptake by marine organisms. J. Fish. Res. Board Can. 29, 1367–1369. Eisler, R., Barry, M.M., Lapan Jr., R.L., Telek, G., Davey, E.W., Soper, A.E., 1978. Metal survey of the marine clam Pitar morrhuana collected near a Rhode Island (USA) electroplating plant. Mar. Biol. 45, 311–317. Espana, M.S.A., Rodriguez, E.M.R., Romero, C.D., 2007. Application of chemometric studies to metal concentrations in molluscs from the Strait of Magellan (Chile). Arch. Environ. Contam. Toxicol. 52, 519–524. Establier, R., 1977. Estudio de la contaminacion marine por metales pesados y sus effectos biologicos. Inf. Tech. Inst. Invest. Pesq. 47, 1–36. Ettajani, H., Amiard-Triquet, C., Amiard, J.C., 1992. Etude experimentale du transfert de deux elements traces (Ag, Cu) dans une chain trophique marine: eau—particles (sediment, natural, microalgue)—mollusques filtreurs (Crassostrea gigas Thunberg). Water Air Soil Pollut. 65, 215–236. Eustace, I.J., 1974. Zinc, cadmium, copper and manganese in species of finfish and shellfish caught in the Derwent Estuary, Tasmania. Aust. J. Mar. Freshw. Res. 25, 209–220. Evans, D.W., Laughlin Jr., R.B., 1984. Accumulation of bis(tributylin)oxide by the mud crab, Rithropanopeus harrisii. Chemosphere 13, 213–219. Evans, S.M., Dawson, M., Frid, C.L.J., Gill, M.E., Pattisina, L.A., Porter, J., 1995. Domestic waste and TBT pollution in coastal areas of Ambon Island (eastern Indonesia). Mar. Pollut. Bull. 30, 109–115. Eversole, A.G., 1978. Marking clams with rubidium. Proc. Nat. Shellfish. Assoc. 68, 78. Fagerstrom, T., Jernelov, A., 1972. Some aspects of the quantitative ecology of mercury. Water Res. 6, 1193–1202. Fagioli, F., Locatelli, C., Landi, S., 1994. Heavy metals in the Goro Bay: sea water, sediments and mussels. Ann. Chim. 84, 129–140. Fang, S.C., 1973. Uptake and biotransformation of phenylmercuric acetate by aquatic organisms. Arch. Environ. Contam. Toxicol. 1, 18–26. Fang, J., Wang, K.X., Tang, J.L., Wang, Y.M., Ren, S.J., Wu, H.Y., et al., 2004. Copper, lead, zinc, cadmium, mercury, and arsenic in marine products of commerce from Zhejiang coastal area, China, May, 1998. Bull. Environ. Contam. toxicol. 73, 583–590. Fattorini, D., Notti, A., Di Mento, R., Cicero, A.M., Gabellini, M., Russo, A., et al., 2008. Seasonal, spatial and inter-annual variations of trace metals in mussels from the Adriatic Sea: a regional gradient for arsenic and implications for monitoring the impact of off-shore activities. Chemosphere 72, 1524–1533. Ferrell, R.E., Carville, T.E., Martinez, J.D., 1973. Trace metals in oyster shells. Environ. Lett. 4(4), 311–316. Fisher, N.S., Teyssie, J.L., 1986. Influence of food composition on the biokinetics and tissue distribution of zinc and americium in mussels. Mar. Ecol. Prog. Ser. 28, 37–43. Fisher, N.S., Wang, W., 1998. Trophic transfer of silver to marine herbivores: a review of recent studies. Environ. Toxicol. Chem. 17, 562–571. Fisher, N.S., Wang, W., Reinfelder, J.R., Luoma, S.N., 1994. Bioaccumulation of silver in marine bivalves. In: Andren, A.W., Bober, T.W., Kramer, J.R., Sodergren, A., Crecelius, E.A., Luoma, S.N., Rodgers, J.H. (Organizers), Transport, Fate and Effects of Silver in the Environment. 3rd International Conference. Proceedings of the 2nd International Conference. Univ. Wisconsin Sea Grant Inst, Madison, WI, pp. 139–140.
Molluscs 373 Flegal, A.R., Martin, J.H., 1977. Contamination of biological samples by ingested sediment. Mar. Pollut. Bull. 8, 90–92. Folsom, T.R., Young, D.R., 1965. Silver-110m and cobalt-60 in oceanic and coastal organisms. Nature 206 (4986), 803–806. Fowler, S.W., Benayoun, G., 1976a. Influence of environmental factors on selenium flux in two marine invertebrates. Mar. Biol. 37, 59–68. Fowler, S.W., Benayoun, G., 1976b. Accumulation and distribution of selenium in mussel and shrimp tissues. Bull. Environ. Contam. Toxicol. 16, 339–346. Fowler, S.W., Oregioni, B., 1976. Trace metals in mussels from the N.W. Mediterranean. Mar. Pollut. Bull. 7, 26–29. Fowler, B.A., Wolfe, D.A., Hettler, W.F., 1975. Mercury and iron uptake by cytosomes in mantle epithelial cells of quahog clams (Mercenaria mercenaria) exposed to mercury. J. Fish. Res. Board Can. 32, 1767–1775. Fowler, S.W., Heyraud, M., La Rosa, J., 1978. Factors affecting methyl and inorganic mercury dynamics in mussels and shrimp. Mar. Biol. 46, 267–276. Franson, J.C., Koehl, P.S., Derksen, D.V., Ruth, T.C., Bunk, C.M., Moore, J.F., 1995. Heavy metals in seaducks and mussels from Misty Fjords National Monument in southeast Alaska. Environ. Monit. Assess. 36, 149–167. Frazier, J.M., 1975. The dynamics of metals in the American oyster, Crassostrea virginica. I. Seasonal effects. Chesapeake Sci. 16, 162–171. Frazier, J.M., 1976. The dynamics of metals in the American oyster, Crassostrea virginica. II. Environmental effects. Chesapeake Sci. 17, 188–197. Freidrich, A.R., Felice, F.P., 1976. Uptake and accumulation of the nickel ion by Mytilus edulis. Bull. Environ. Contam. Toxicol. 16, 750–755. Frias-Espericueta, M.G., Osuna-Lopez, J.I., Voltolina, D., Lopez-Lopez, G., Izaguirre-Fierro, G., Muy-Rangel, M.D., 2008. The metal content of bivalve molluscs of a coastal lagoon of NW Mexico. Bull. Environ. Contam. Toxicol. 80, 90–92. Friberg, L., Vostal, J. (Eds.), 1972. Mercury in the Environment. CRC Press, Cleveland, OH, 215 pp. Fujiki, M., 1963. Studies on the course that the causative agent of Minamata Disease was formed, especially on the accumulation of the mercury compound in the fish and shellfish of Minamata Bay. J. Kumamoto Med. Soc. 37, 494–521. Fukai, R., 1965. Analysis of trace amounts of chromium in marine organisms by the isotope dilution of Cr-51. In: Radiochemical Methods of Analysis. Int. Atom. Ener. Agen, Vienna, Austria, pp. 335–351. Fukai, R., Meinke, W.W., 1959. Some activation analyses of six trace elements in marine biological ashes. Nature 184, 815–816. Fukai, R., Meinke, W.W., 1962. Activation analyses of vanadium, arsenic, molybdenum, tungsten, rhenium, and gold in marine organisms. Limnol. Oceanogr. 7, 186–200. Fukai, R., Oregioni, B., Vas, D., 1978. Interlaboratory comparability of measurements of trace elements in marine organisms: results of intercalibration exercise on oyster homogenate. Oceanol. Acta 1, 391–396. Gabbianelli, R., Moretti, M., Carpene, E., Falcioni, G., 2006. Effect of different organotins on DNA of mollusk (Scapharca inaequivalvis) erythrocytes assessed by the comet assay. Sci. Total Environ. 367, 163–169. Gainey Jr., L.F., Kenyon, J.R., 1990. The effects of reserpine on copper induced cardiac inhibition in Mytilus edulis. Comp. Biochem. Physiol. 95C, 177–179. Galtsoff, P.S., 1942. Accumulation of manganese and the sexual cycle in Ostrea virginica. Physiol. Zool. 15, 210–215. Galtsoff, P., 1953. Accumulation of manganese, iron, copper, and zinc in the body of the American oyster, Crassostrea (Ostrea) virginica. Anatom. Rec. 117, 601–602. Garaventa, F., Faimali, M., Terlizzi, A., 2006. Imposex in pre-pollution times. Is TBT to blame? Mar. Pollut. Bull. 52, 701–702. Garaventa, F., Centanni, E., Pellizzato, F., Faimali, M., Terlizzi, A., Pavoni, B., 2007. Imposex and accumulation of organotin compounds in populations of Hexaplex trunculus (Gastropoda, Muricidae) from the Lagoon of Venice (Italy) and Istrian Coast (Croatia). Mar. Pollut. Bull. 54, 615–622.
374 Chapter 6 Garcia-Luque, E., DelValls, A.T., Forja, J.M., Gomez-Parra, A., 2007. Biological adverse effects on bivalves associated with trace metals under estuarine conditions. Environ. Monit. Assess. 131, 27–35. Gavis, J., Ferguson, J.F., 1972. The cycling of mercury through the environment. Water Res. 6, 989–1000. Geffard, A., Geffard, O., Amiard, J.C., His, E., Amiard-Triquet, C., 2007. Bioaccumulation of metals in sediment elutriates and their effects on growth, condition index, and metallothionein contents in oyster larvae. Arch. Environ. Contam. Toxicol. 53, 57–65. Genest, P.E., 1979. A study of some heavy metals. In: Mercenaria mercenaria, M.S. thesis, Southeastern Massachusetts Univ, 56 pp. George, S.G., Coombs, T.L., 1975. A comparison of trace metal and metalloenzyme profiles in different molluscs and during development of the oyster. In: Barnes, H. (Ed.), Proceedings of the Nineth European Marine Biology Symposium, pp. 433–449. George, S.G., Coombs, T.L., 1977. The effects of chelating agents on the uptake and accumulation of cadmium by Mytilus edulis. Mar. Biol. 39, 261–268. George, S.G., Pirie, B.J.S., Coombs, T.L., 1976. The kinetics of accumulation and excretion of ferric hydroxide in Mytilus edulis (L.) and its distribution in the tissues. J. Exp. Mar. Biol. Ecol. 23, 71–84. George, S.G., Pirie, B.J.S., Cheyne, A.R., Coombs, T.L., Grant, P.T., 1978. Detoxication of metals by marine bivalves: an ultrastructural study of the compartmentation of copper and zinc in the oyster Ostrea edulis. Mar. Biol. 45, 147–156. George, S.G., Pirie, B.J.S., Coombs, T.L., 1980. Isolation and elemental analysis of metal-rich granules from the kidney of the scallop, Pecten maximus (L.). J. Exp. Mar. Biol. Ecol. 42, 143–156. Ghiretti, F., Salvato, B., Carlucci, S., DePieri, R., 1972. Manganese in Pinna nobilis. Experientia 28, 232–233. Ghiretti-Magaldi, A., Giuditta, A., Ghiretti, F., 1958. Pathways of terminal respiration in marine invertebrates. I. The respiratory system in cephalopods. J. Cell. Comp. Physiol. 52, 389–429. Gibbs, P.E., Bryan, G.W., 1986. Reproductive failure in populations of the dog-whelk, Nucella lapillus, caused by imposex induced from tributyltin from antifouling paints. J. Mar. Biol. Assoc. UK 66, 767–777. Gibbs, P.E., Bryan, G.W., Pascoe, P.L., Burt, G.R., 1987. The use of the dog-whelk, Nucella lapillus, as an indicator of tributyltin (TBT) contamination. J. Mar. Biol. Assoc. UK 67, 507–523. Giordno, R., Arata, P., Ciaralli, L., Rinaldi, S., Giani, M., Cicero, A.M., et al., 1991. Heavy metals in mussels and fish from Italian coastal waters. Mar. Pollut. Bull. 22, 10–14. Glickstein, N., 1978. Acute toxicity of mercury and selenium to Crassostrea gigas and Cancer magister larvae. Mar. Biol. 49, 113–117. Glynn, D., Tyrrell, L., McHugh, B., Rowe, A., Monaghan, E., Costello, J., et al., 2003. Trace Metal and Chlorinated Hydrocarbon Concentrations in Shellfish from Irish Waters, 2001. Marine Institute, Marine Environment and Food Safety Services, Abbotstown, Dublin, pp. 1–15. Goldberg, E.D., Bowen, V.T., Farrington, J.W., Harvey, G., Martin, J.H., Parker, P.L., et al., 1978. The mussel watch. Environ. Conserv. 5, 101–125. Gomez-Ariza, J.L., Santos, M.M., Morales, E., Giraldez, I., Sanchez-Rodas, D., Vieira, N., et al., 2006. Organotin contamination in the Atlantic Ocean off the Iberian Peninsula in relation to shipping. Chemosphere 64, 1100–1108. Gonzalez, P.M., Abele, D., Puntarulo, S., 2008. Iron and radical content in Mya arenaria. Possible sources of NO generation. Aquat. Toxicol. 89, 122–128. Gorbushin, A.M., 1997. Field evidence of trematode-induced gigantism in Hydrobia spp. (Gastropoda: Prosobranchia). J. Mar. Biol. Assoc. UK 77, 785–800. Gorinstein, S., Moncheva, S., Toledo, F., Avila, P.A., Trakhtenberg, S., Gorinstein, A., et al., 2006. Relationship between seawater pollution and qualitative changes in the extracted proteins from mussels Mytilus galloprovincialis. Sci. Total Environ. 364, 252–259. Gorski, J., Nugegoda, D., 2006. Toxicity of trace metals to juvenile abalone, Haliotis rubra following short-term exposure. Bull. Environ. Contam. Toxicol. 77, 732–740. Gould, E., MacInnes, J.R., 1977. Short term effects of two silver salts on tissue respiration and enzyme activity in the cunner (Tautogolabrus adspersus). Bull. Environ. Contam. Toxicol. 18, 401–408.
Molluscs 375 Graham, D.L., 1972. Trace metal levels in intertidal mollusks of California. Veliger 14, 365–372. Greig, R.A., 1975. Comparison of atomic absorption and neutron activation analyses for determination of silver, chromium and zinc in various marine organisms. Anal. Chem. 47, 1682–1684. Greig, R.A., 1979. Trace metal uptake by three species of mollusks. Bull. Environ. Contam. Toxicol. 22, 643–647. Greig, R.A., Sennefelder, G., 1985. Metals and PCB concentrations in mussels from Long Island Sound. Bull. Environ. Contam. Toxicol. 35, 331–334. Greig, R.A., Wenzloff, D.R., 1978. Metal accumulation and depuration by the American oyster, Crassostrea virginica. Bull. Environ. Contam. Toxicol. 20, 499–504. Greig, R.A., Nelson, B.A., Nelson, D.A., 1975. Trace metal content in the American oyster. Mar. Pollut. Bull. 6, 72–73. Greig, R.A., Wenzloff, D.R., Pearce, J.B., 1976. Distribution and abundance of heavy metals in finfish, invertebrates and sediments collected at a deepwater disposal site. Mar. Pollut. Bull. 7, 185–187. Greig, R.A., Wenzloff, D.R., Adams, A., Nelson, B., Shelpuk, C., 1977. Trace metals in organisms from ocean disposal sites of the middle eastern United States. Arch. Environ. Contam. Toxicol. 6, 395–409. Greig, R.A., Wenzloff, D.R., McKenzie Jr., C.L., Merrill, A.S., Zdanowicz, V.S., 1978. Trace metals in sea scallops, Placopecten magellanicus from eastern United States. Bull. Environ. Contam. Toxicol. 19, 326–334. Guary, J.C., Frazier, A., 1977. Etude comparee des teneurs en plutonium chez divers mollusques de quelques sites littoraux fransais. Mar. Biol. 41, 263–267. Guary, J.C., Fowler, S.W., 1978. Uptake from water and tissue distribution of neptunium-237 in crabs, shrimp, and mussels. Mar. Pollut. Bull. 9, 331–334. Guerin, T., Sirot, V., Volatier, J.L., Leblanc, J.C., 2007. Organotin levels in seafood and its implications for health risk in high-seafood consumers. Sci. Total Environ. 388, 66–77. Hall, R.A., Zook, E.G., Meaburn, G.M., 1978. National Marine Fisheries Service survey of trace elements in the fishery resources. In: US Dept. Commerce NOAA Tech. Rept., NMFS SSRF-721. pp. 1–313. Hall Jr., L.W., Lenkevich, M.J., Hall, W.S., Pinkney, A.E., Bushong, S.J., 1987. Evaluation of butyltin compounds in Maryland waters of Chesapeake Bay. Mar. Pollut. Bull. 18, 78–83. Hall Jr., L.W., Bushong, S.J., Hall, W.S., Johnson, W.E., 1988. Acute and chronic effects of tributyltin on a Chesapeake Bay copepod. Environ. Toxicol. Chem. 7, 41–46. Hamanaka, T., Kato, H., Tsujita, T., 1977. Cadmium and zinc in ribbon seal, Histriophoca fasciata, in the Okhotsk Sea. Res. Inst. N. Pac. Fish. Hokkaido Univ. (Japan) Spec. Vol., 547–561. Hamasaki, T., Nagase, H., Yoshioka, Y., Sato, T., 1995. Formation, distribution, and ecotoxicity of methyl-metals of tin, mercury, and arsenic in the environment. Crit. Rev. Environ. Sci. Technol. 25, 45–91. Hamilton, E.I., Clifton, R.J., 1980. Concentration and distribution of the transuranium radionuclides 239+240Pu, 238 Pu and 241Am in Mytilus edulis, Fucus vesiculosus and surface sediment of Esk estuary. Mar. Ecol. Prog. Ser. 3, 267–277. Han, B.C., Hung, T.C., 1990. Green oysters caused by copper pollution on the Taiwan coast. Environ. Pollut. 65, 347–362. Han, B.C., Jeng, W.L., Tsai, Y.N., Jeng, M.S., 1993. Depuration of copper and zinc by green oysters and blue mussels of Taiwan. Environ. Pollut. 82, 93–97. Han, B.C., Jeng, W.L., Chen, R.Y., Fang, G.T., Hung, T.C., Tseng, R.J., 1998. Estimation of target hazard quotients and potential health risks for metals by consumption of seafood in Taiwan. Arch. Environ. Contam. Toxicol. 35, 711–720. Hanks, R.W., 1965. Effect of metallic aluminum particles on oysters and clams. Chesapeake Sci. 6, 146–149. Harino, H., Fukushima, M., Yamamoto, Y., Kuwai, S., Miyazaki, N., 1998. Organotin compounds in water, sediment, and biological samples from the port of Osaka, Japan. Arch. Environ. Contam. Toxicol. 35, 558–564. Harrington, J.M., 1991. Tributyltin residues in Lake Tahoe and San Diego Bay, California, 1988. In: State of California Dept. Fish Game, Environ. Serv. Div., Admin. Rep. 91-1, pp. 1–29. Harris, J.E., Fabris, G.J., Statham, P.J., Tawfik, F., 1979. Biogeochemistry of selected heavy metals in Western Port, Victoria, and use of invertebrates as indicators with emphasis on Mytilus edulis planulatus. Aust. J. Mar. Freshw. Res. 30, 159–178.
376 Chapter 6 Harriss, R.C., 1971. Ecological indications of mercury pollution in aquatic systems. Biol. Conserv. 3, 279. Harvey Sr., E.J., Knight Jr., L.A., 1978. Concentration of three toxic metals in oysters (Crassostrea virginica) of Biloxi and Pascagoula, Mississippi estuaries. Water Air Soil Pollut. 9, 255–261. Hayashi, A., 1960. Biogeochemical studies on Ostrea gigas. IX. Lead content. Seikagaku 32, 871–873. Hedouin, L., Metian, M., Teyssie, J.L., Fowler, S.W., Fichez, R., Warnau, M., 2006. Allometric relationships in the bioconcentration of heavy metals by the edible tropical clam Gafrarium tumidum. Sci. Total Environ. 366, 154–163. Hedouin, L., Pringault, O., Metian, M., Bustamante, P., Warnau, M., 2007. Nickel bioaccumulation in bivalves from New Caledonia lagoon: seawater and food exposure. Chemosphere 66, 1449–1457. Herdman, W.A., Boyce, R., 1899. Oysters and disease. An account of certain observations upon the normal and pathological histology and bacteriology of the oyster and other shellfish. Lancashire Sea Fish. Mem. 1, 1–60. Heyraud, M., Cherry, R.D., 1979. Polonium-210 and lead-210 in marine food chains. Mar. Biol. 52, 227–236. Hill, J.M., Helz, G.R., 1973. Copper and zinc in estuarine waters near a coal-fired electric power plant—correlation with oyster greening. Environ. Lett. 5(3), 165–174. Hiyama, Y., Shimizu, M., 1964. On the concentration factors of radioactive Cs, Sr, Cd, Zn, and Ce in marine organisms. Rec. Oceanogr. Works Jpn. 7(2), 43–47. Hoare, K., Beaumont, A.R., Davenport, J., 1995a. Variation among populations in the resistance of Mytilus edulis embryos to copper: adaptation to pollution? Mar. Ecol. Prog. Ser. 120, 155–161. Hoare, K., Davenport, J., Beaumont, A.R., 1995b. Effects of exposure and previous exposure to copper on growth of veliger larvae and survivorship of Mytilus edulis embryos. Mar. Ecol. Prog. Ser. 120, 163–168. Hobden, D.J., 1967. Iron metabolism in Mytilus edulis. I. Variation in total content and distribution. J. Mar. Biol. Assoc. UK 47, 597–606. Hobden, D.J., 1969. Iron metabolism in Mytilus edulis. II. Uptake and distribution of radioactive iron. J. Mar. Biol. Assoc. UK 49, 661–668. Hoggins, F.E., Brooks, R.R., 1973. Natural dispersion of mercury from Puhipuhi, Northland, New Zealand. N. Z. J. Mar. Freshw. Res. 7, 125–132. Holden, A.V., 1973. Mercury in fish and shellfish, a review. J. Food Technol. 8, 1–25. Horiguchi, T., Li, Z., Uno, S., Shimizu, M., Shiraishi, H., Morita, M., et al., 2003. Contamination of organotin compounds and imposex in molluscs from Vancouver, Canada. Mar. Environ. Res. 57, 75–88. Horiguchi, F., Nakata, L., Ito, N., Okawa, K., 2006. Risk assessment of TBT in the Japanese short-neck clam (Ruditapes philippinarum) of Tokyo Bay using a chemical fate model. Estuar. Coast. Shelf Sci. 70, 589–598. Horowitz, A., Presley, B.J., 1977. Trace metal concentrations and partitioning in zooplankton, neuston, and benthos from the south Texas Outer Continental Shelf. Arch. Environ. Contam. Toxicol. 5, 241–255. Horvath, G.J., Harriss, R.C., Mattraw, H.C., 1972. Land development and heavy metal distribution in the Florida Everglades. Mar. Pollut. Bull. 3, 182–184. Hu, J., Zhen, H., Wan, Y., Gao, J., An, W., An, L., et al., 2006. Trophic magnification of triphenyltin in a marine food web of Bohai Bay, North China: comparison to tributyltin. Environ. Sci. Technol. 40, 3142–3147. Huang, H., Wu, J.Y., Wu, J.H., 2007. Heavy metal monitoring using bivalved shellfish from Zhejiang coastal waters, East China Sea. Environ. Monit. Assess. 129, 315–320. Huggett, R.J., Bender, M.E., Slone, H.D., 1973. Utilizing metal concentration relationships in the eastern oyster (Crassostrea virginica) to detect heavy metal pollution. Water Res. 7, 451–460. Huggett, R.J., Cross, F.A., Bender, M.E., 1975. Distribution of copper and zinc in oysters and sediments from three coastal plain estuaries. In: Howell, F.G., Gentry, J.B., Smith, M.H. (Eds.), Mineral Cycling in Southeastern Ecosystems, US Energy Res. Dev. Admin. CONF-740513, pp. 224–228. Huggett, R.J., Unger, M.A., Seligman, P.F., Valkirs, A.O., 1992. The marine biocide tributyltin. Environ. Sci. Technol. 26, 232–237. Hung, T.C., Lin, T.T., 1976. Study on mercury in the water, sediments, and benthonic organisms along Cahi—I. Coastal area. Acta Oceanogr. Taiwan. 6, 30–38. Hung, T.C., Chuang, A., Wu, S.J., Tsai, C.C.H., 1990. Relationships among the species and forms of copper and biomass along the Erhjin Chi coastal water. Acta Oceanogr. Taiwan. 25, 65–76.
Molluscs 377 Hunt, J.W., Anderson, B.S., 1989. Sublethal effects of zinc and municipal effluents on larvae of the red abalone, Haliotis rufescens. Mar. Biol. 101, 545–552. Hussain, M., Bleiler, E.L., 1973. Mercury in Australian oysters. Mar. Pollut. Bull. 4, 44. Ichikawa, R., 1961. On the concentration factors of some important radionuclides in marine food organisms. Bull. Jpn. Soc. Sci. Fish. 27, 66–74. Ikebe, K., Tanaka, R., 1979. Determination of vanadium and nickel in marine samples by flameless and flame atomic absorption spectrophotometry. Bull. Environ. Contam. Toxicol. 21, 526–532. Ikuta, K., 1967. Studies on accumulation of heavy metals in aquatic organisms. I. On the copper content in oysters. Bull. Jpn. Soc. Sci. Fish. 33, 405–409. Ikuta, K., 1968a. Studies on accumulation of heavy metals in aquatic organisms. II. On accumulation of copper and zinc in oysters. Bull. Jpn. Soc. Sci. Fish. 34, 112–116. Ikuta, K., 1968b. Studies on accumulation of heavy metals in aquatic organisms. III. On accumulation of copper and zinc in the parts of oysters. Bull. Jpn. Soc. Sci. Fish. 34, 117–122. Ikuta, K., 1968c. Studies on accumulation of heavy metals in aquatic organisms. IV. On disappearance of abnormally accumulated copper and zinc in oysters. Bull. Jpn. Soc. Sci. Fish. 34, 482–487. Inoue, S., Abe, S.I., Oshima, Y., Kai, N., Honjo, T., 2006a. Tributyltin contamination of bivalves in coastal areas around northern Kyushu, Japan. Environ. Toxicol. 21, 244–249. Inoue, S., Oshima, Y., Usuki, H., Hamaguchi, M., Hanamura, Y., Kai, N., et al., 2006b. Effects of tributyltin maternal and/or waterborne exposure on the embryonic development of the Manila clam, Ruditapes philippinarum. Chemosphere 63, 881–888. Inoue, S., Oshima, Y., Abe, S.I., Wu, R.S.S., Kai, N., Honjo, T., 2007a. Effects of tributyltin on the energy metabolism of pen shell (Atrina pectinata japonica). Chemosphere 66, 1226–1229. Inoue, A., Oshima, Y., Usuki, H., Hamaguchi, M., Hanamura, Y., Kai, N., et al., 2007b. Effect of tributyltin on veliger larvae of the Manila clam, Ruditapes philippinarum. Chemosphere 66, 1353–1357. Ireland, M.P., 1973. Result of fluvial zinc pollution on the zinc content of littoral and sublittoral organisms in Cardigan Bay, Wales. Environ. Pollut. 4, 27–35. Ireland, M.P., Wooton, R.J., 1977. Distribution of lead, zinc, copper and manganese in the marine gastropods, Thais lapillus and Littorina littorea, around the coast of Wales. Environ. Pollut. 12, 27–41. Irukayama, K., 1967. In: The pollution of Minamata Bay and Minamata disease. In: Proceedings of the 3rd International Conference on Water Pollution Research, Munich, 1966, pp. 153–180. Irukayama, K., Kondo, T., Kai, F., Fujiki, M., 1961. Studies on the origin of the causative agent of Minamata disease. I. Organic mercury compound in the fish and shellfish from Minamata Bay. Kumamoto Med. J. 14, 158–169. Irukayama, K., Fujiki, M., Kai, F., Kondo, T., 1962a. Studies on the origin of the causative agent of Minamata disease. II. Comparison of the mercury compound in the shellfish from Minamata Bay with mercury compounds experimentally accumulated in the control shellfish. Kumamoto Med. J. 15, 1–12. Irukayama, K., Kai, F., Fujiki, F., Kondo, T., 1962b. Studies on the causative agent of Minamata disease. III. Industrial wastes containing mercury compounds from Minamata factory. Kumamoto Med. J. 15, 57–68. Ishii, T., Suzuki, H., Koyanagi, T., 1978. Determination of trace elements in marine organisms. I. Factors for variation of concentration of trace element. Bull. Jpn. Soc. Sci. Fish. 44, 155–162. Ishikawa, M., Sumiya, M., Saiki, M., 1973. Chemical behaviour of 106Ru in seawater and uptake by marine organisms. In: Radioactive Contamination of the Marine Environment. IAEA, Vienna, pp. 359–367. Ishikawa, M., Koyanagi, T., Saiki, M., 1976. Studies on the chemical behaviour of 106Ru in seawater and its uptake by marine organisms. I. Accumulation and excretion of 106Ru by clam. Bull. Jpn. Soc. Sci. Fish. 42, 287–297. Ivanina, A.V., Sokolova, I.M., 2008. Effects of cadmium exposure on expression and activity of P-glycoprotein in eastern oysters, Crassostrea virginica Gmelin. Aquat. Toxicol. 88, 19–28. Jackim, E., Morrison, G., Steele, R., 1977. Effects of environmental factors on radiocadmium uptake by four species of marine bivalves. Mar. Biol. 40, 303–308.
378 Chapter 6 Janssen, H., Scholz, N., 1979. Uptake and cellular distribution of cadmium in Mytilus edulis. Mar. Biol. 55, 133–141. Jeng, S.S., Huang, Y.W., 1973. Heavy metals contents in Taiwan’s cultured fish. Bull. Inst. Zool. Acad. Sin. 12, 79–85. Jenkins, D.W., 1980. Biological Monitoring of Toxic Trace Metals. Vol. 2. Toxic Trace Metals in Plants and Animals of the World. Part I. US Environ. Protect. Agen. Rep. 600/3-80–090, pp. 30-138; Part II. US Environ. Protect Agen. Rep. 600/3-80-091, pp. 505–618. Jernelov, A., 1969. Conversion of mercury compounds. In: Miller, M.W., Berg, G.G. (Eds.), Chemical Fallout, Current Research on Persistent Pesticides. Charles C Thomas Publishers, Springfield, IL, pp. 68–74. Jernelov, A., Hartung, R., Trost, P.B., Bisque, R.E., 1972. Environmental dynamics of mercury. In: Hartung, R., Dinman, B.D. (Eds.), Environmental Mercury Contamination. Ann Arbor Science Publishers, Ann Arbor, MI, pp. 167–201. Jernelov, A., Landner, L., Larsson, T., 1975. Swedish perspectives on mercury pollution. J. Water Control Pollut. Fed. 47, 810–822. Ji, J., Choi, H.J., Ahn, I.Y., 2006. Evaluation of Manila clam Ruditapes philippinarum as a sentinel species for metal pollution monitoring in estuarine tidal flats of Korea: effects of size, sex, and spawning on baseline accumulation. Mar. Pollut. Bull. 52, 447–453. Jiann, K.T., Presley, B.J., 1997. Variations in trace metal concentrations in American oysters (Crassostrea virginica) collected from Galveston Bay, Texas. Estuaries 20, 710–724. Jing, G., Li, Y., Zhang, R., 2007. Different effects of Pb2+ and Cu2+ on immune and antioxidant enzyme activities in the mantle of Pinctada fucata. Environ. Toxicol. Pharmacol. 24, 122–128. Johnels, A.G., Westermark, T., 1969. Mercury contamination of the environment in Sweden. In: Miller, M.W., Berg, G.G. (Eds.), Chemical Fallout, Current Research on Persistent Pesticides. Charles C Thomas Publishers, Springfield, IL, pp. 221–239. Johns, C., Luoma, S.N., 1990. Arsenic in benthic bivalves of San Francisco Bay and the Sacramento/San Joaquin River delta. Sci. Total Environ. 97/98, 673–684. Jones, M.B., 1973. Influence of salinity and temperature on the toxicity of mercury to marine and brackish water isopods (Crustacea). Estuar. Coast. Mar. Sci. 1, 425–431. Jones, A.M., Jones, Y., Stewart, W.D.P., 1972. Mercury in marine organisms of the Tay region. Nature 238, 164–165. Julshamn, K., Duinker, A., Frantzen, S., Torkildsen, L., Maage, A., 2008. Organ distribution and food safety aspects of cadmium and lead in great scallops, Pecten maximus L., and horse mussels, Modiolus modiolus L., from Norwegian waters. Bull. Environ. Contam. Toxicol. 80, 385–389. Kadar, E., 2007. Postcapture depuration of essential metals in the deep sea hydrothermal mussel Bathymodiolus azoricus. Bull. Environ. Contam. Toxicol. 78, 99–106. Kadar, E., Santos, R.S., Powell, J.L., 2006. Biological factors influencing tissue compartmentalization of trace metals in the deep-sea hydrothermal vent bivalve Bathymodiolus azoricus at geochemically distinct vent sites of the mid-Atlantic Ridge. Environ. Res. 101, 221–229. Kanatireklap, S., Tanabe, S., Sanguansin, J., Tabucanon, M.S., Hungspreugs, M., 1997. Contamination by butyltin compounds and organochlorine residues in green mussel (Perna viridis, L.) from Thailand coastal waters. Environ. Pollut. 97, 78–89. Karayakar, F., Erdem, C., Cicik, B., 2007. Seasonal variation in copper, zinc, chromium, lead and cadmium levels in hepatopancreas, gill and muscle tissues of the mussel Brachidontes pharaonis Fischer, collected along the Mersin coast, Turkey. Bull. Environ. Contam. Toxicol. 79, 350–355. Karbe, L., Schnier, C., Siewers, H.O., 1977. Trace elements in mussels (Mytilus edulis) from coastal areas of the North Sea and the Baltic. Multielement analyses using instrumental neutron activation analysis. J. Radioanal. Chem. 37, 927–943. Karouna-Renier, N.K., Snyder, R.A., Allison, J.G., Wagner, M.G., Rao, K.R., 2007. Accumulation of organic and inorganic contaminants in shellfish collected in estuarine waters near Pensacola, Florida: contamination profiles and risks to human consumers. Environ. Pollut. 145, 474–488.
Molluscs 379 Karpevich, A.F., Shurin, A.T., 1977. Manganese in the metabolic processes of mollusks of the Baltic Sea. Sov. J. Mar. Biol. 3, 437–442. Keckes, S., Miettinen, J., 1972. Mercury as a marine pollutant. In: Ruivo, M. (Ed.), Marine Pollution and Sea Life. Fishing Trading News (Books), London, pp. 276–289. Keckes, S., Pucar, Z., Marazovic, L., 1966. The influence of the physico-chemical form of 106Ru on its uptake by mussels from sea water. In: Aberg, B., Hungate, F.P. (Eds.), Radioecological Concentration Processes. Proceedings of an International Symposium, Stockholm, 1966. Pergamon Press, New York, pp. 993–994. Keckes, S., Ozretic, B., Krajnovic, M., 1968. Loss of Zn-65 in the mussel Mytilus galloprovincialis. Malacologia 7, 1–6. Keckes, S., Ozretic, B., Krajnovic, M., 1969. Metabolism of zinc-65 in mussels (Mytilus galloprovincialis Lam). Uptake of zinc-65. Rapp. Comm. Int. Mer Medit. 19, 949–952. Kerfoot, W.B., 1979. Artificial shellfish for monitoring ambient cadmium levels in seawater. In: Proceedings of the Workshop on Alternatives for Cadmium Electroplating in Metal Finishing, October 4-6, 1977. US Environ. Protect. Agen. Rep. 560/2-79-003, pp. 215–240. Keskin, Y., Baskaya, R., Ozyaral, O., Yurdun, T., Luleci, N.E., Hayran, O., 2007. Cadmium, lead, mercury and copper in fish from the Marmara Sea, Turkey. Bull. Environ. Contam. Toxicol. 78, 258–261. Ketchum, B.M., Bowen, V.T., 1958. Biological factors determining the distribution of radioisotopes on the sea. In: Proceeding of the Second Annual U.N. Conference on the Peaceful Uses of Atomic Energy, vol. 18. Waste Treat. Environ Aspect Atom. Ener., Geneva, pp. 429–433. Khangarot, B.S., Ray, P.K., 1987. Zinc sensitivity of a freshwater snail, Lymnaea luteola L., in relation to seasonal variations in temperature. Bull. Environ. Contam. Toxicol. 39, 45–49. Kim, N.S., Shim, W.J., Yim, U.H., Ha, S.Y., Park, P.S., 2008. Assessment of tributyltin contamination in a shipyard area using a mussel transplantation approach. Mar. Pollut. Bull. 57, 883–888. Kiyoura, R., 1963. Water pollution and Minamata disease. Int. J. Air Water Pollut. 7, 459–470. Klein, D.H., Goldberg, E.D., 1970. Mercury in the marine environment. Environ. Sci. Technol. 4, 765–768. Klemmer, H., Luoma, S.N., Lau, L.S., 1973. Mercury levels in marine biota. Gov. Rep. Announ. 73(10), 76. Klemmer, H.W., Unninayer, C.S., Ukubo, W.I., 1976. Mercury content of biota in coastal waters in Hawaii. Bull. Environ. Contam. Toxicol. 15, 454–457. Kljakovic-Gaspic, Z., Odzak, N., Ujevic, I., Zvonaric, T., Horvat, M., Baric, A., 2006. Biomonitoring of mercury in polluted coastal area using transplanted mussels. Sci. Total Environ. 368, 199–209. Knothe, D.W., Van Riper, G.G., 1988. Acute toxicity of sodium molybdate dehydrate (Molhibit 100) to selected saltwater organisms. Bull. Environ. Contam. Toxicol. 40, 785–790. Kobayashi, N., 1971. Fertilized sea urchin eggs as an indicatory material for marine pollution bioassay, preliminary experiments. Publ. Seto Mar. Biol. Lab. 18, 379–406. Koch, I., McPherson, K., Smith, P., Easton, L., Doe, K.G., Reimer, K.J., 2007. Arsenic bioavailability and speciation in clams and seaweed from a contaminated marine environment. Mar. Pollut. Bull. 54, 586–594. Koczy, F.F., Titze, H., 1958. Radium content of carbonate shells. J. Mar. Res. 17, 302–311. Kopfler, F.C., 1974. The accumulation of organic and inorganic mercury compounds by the eastern oyster (Crassostrea virginica). Bull. Environ. Contam. Toxicol. 11, 275–280. Kopfler, F.C., Mayer, J., 1967. Studies of trace metals in shellfish. In: Proceedings of the Gulf and South Atlantic States Shellfish Sanitation Research Conference, pp. 67–80. Krinsley, D., Bieri, R., 1959. Changes in the chemical composition of pteropod shells after deposition on the sea floor. J. Paleontol. 33, 682–684. Krishnakumar, P.K., Asokan, P.K., Pillai, V.K., 1990. Physiological and cellular responses to copper and mercury in the green mussel Perna viridis (Linnaeus). Aquat. Toxicol. 18, 163–174. Kucuksezgin, F., Kayatekin, B.M., Uluturhan, E., Oysal, N., Acikgoz, O., Gonenc, S., 2008. Preliminary investigation of sensitive biomarkers of metal pollution in mussel (Mytilus galloprovincialis) from Izmir Bay (Turkey). Environ. Monit. Assess. 141, 339–345. Kuenzler, E.J., 1969. Elimination of iodine, cobalt, iron, and zinc by marine zooplankton. In: Proceedings of the 2nd National Symposium on Radioecology. US Atom. Ener. Comm. Conf. 67053, pp. 462–473.
380 Chapter 6 Kumagi, H., Saeki, K., 1978. Contents of total mercury, alkyl mercury and methyl mercury in some coastal fish and shells. Bull. Jpn. Soc. Sci. Fish. 44, 807–811. Kumar, K.S., Sajwan, K.S., Richardson, J.P., Kannan, K., 2008. Contamination profiles of heavy metals, organochlorine pesticides, polycyclic aromatic hydrocarbons and alkylphenols in sediment and oyster collected from marsh/estuarine Savannah GA, USA. Mar. Pollut. Bull. 56, 136–149. Kurland, T., Faro, S.N., Siedler, H., 1960. Minamata disease. The outbreak of a neurologic disorder in Minamata, Japan, and its relationship to the ingestion of seafood contaminated by mercuric compounds. World Neurol. 1, 370–395. LaBrecque, J.J., Benzo, Z., Alfonso, J.A., Cordoves, P.R., Quintal, M., Gomez, C.V., et al., 2004. The concentrations of selected trace elements in clams, Trivela mactroidea along the Venezuelan coast in the state of Miranda. Mar. Pollut. Bull. 49, 664–667. Lacerda, L.D., 1983. Aplicacao da metodologia de abordagem peios parametros criticos no estudo da poluicao por metais pesados na Baia de Sepetiba, Rio de Janeiro. Ph.D. thesis, Inst. Biofisica, Univ. Fed. Rio de Janeiro, UFRJ, Rio de Janeiro, 134 pp. Lacerda, L.D., Molisani, M.M., 2006. Three decades of Cd and Zn contamination in Sepetiba Bay, SE Brazil: evidence from the mangrove oyster Crassostrea rhizophorae. Mar. Pollut. Bull. 52, 974–977. Lacoue-Labarthe, T., Warnau, M., Oberhansli, F., Teyssie, J.L., Koueta, N., Bustamante, P., 2008a. Differential bioaccumulation behaviour of Ag and Cd during the early development of the cuttlefish Sepia officinalis. Aquat. Toxicol. 86, 437–446. Lacoue-Labarthe, T., Warnau, M., Oberhansli, F., Teyssie, J.L., Jeffree, R., Bustamante, P., 2008b. First experiments on the maternal transfer of metals in the cuttlefish Sepia officinalis. Mar. Pollut. Bull. 57, 826–831. Laevastu, T., Thompson, T.G., 1956. The determination and occurrence of nickel in seawater, marine organisms, and sediments. J. Conseil 21, 125–143. Lafabrie, C., Pergent, G., KAntin, R., Pergent-Martini, C., Gonzalez, J.L., 2007. Trace metals assessment in water, sediment, mussel and seagrass species—validation of the use of Posidonia oceanica as a metal biomonitor. Chemosphere 68, 2033–2039. Lahaye, V., Bustamante, P., Dabin, W., Canney, O.V., Dhermain, F., Cesarini, C., et al., 2006. New insights from age determination on toxic element accumulation in striped and bottlenose dolphins from Atlantic and Mediterranean waters. Mar. Pollut. Bull. 52, 1219–1230. Lande, E., 1977. Heavy metal pollution in Trondheimsfjorden, Norway, and the recorded effects on the fauna and flora. Environ. Pollut. 12, 187–198. Langley, D.G., 1973. Mercury methylation in an aquatic environment. J. Water Pollut. Control Fed. 45, 44–51. Larsen, P.F., 1979. The distribution of heavy metals in the hard clam, Mercenaria mercenaria in the lower Chesapeake Bay region. Estuaries 2, 1–8. Lauenstein, G.G., Robertson, A., O’Connor, T.P., 1990. Comparison of trace metal data in mussels and oysters from a mussel watch programme of the 1970s with those from a 1980s programme. Mar. Pollut. Bull. 21, 440–447. Laughlin, R., Linden, O., 1985. Sublethal responses of the tadpoles of the European frog Rana temporaria to two tributyltin compounds. Bull. Environ. Contam. Toxicol. 28, 494–499. Laughlin, R., Nordlund, K., Linden, O., 1984. Long-term effects of tributyltin compounds on the Baltic amphipod, Gammarus oceanicus. Mar. Environ. Res. 12, 243–271. Laughlin Jr., R.B., French, W., Guard, H.E., 1986. Accumulation of bis(tributyltin) oxide by the marine mussel Mytilus edulis. Environ. Sci. Technol. 20, 884–890. Laughlin, R.B., Gustafson, J.R., Pendoley, P., 1988. Chronic embryo-larval toxicity of tributyltin (TBT) to the hard-shell clam Mercenaria mercenaria. Mar. Ecol. Prog. Ser. 50, 4829–4836. Laumond, F., Neuberger, M., Donnier, B., Fourcy, A., Bittel, R., Aubert, M., 1973. Experimental investigations, at laboratory, on the transfer of mercury in marine trophic chains. In: Sixth International Symposium on Medical Oceanography, Portoroz, Yugoslavia, September 26-30, 1973, pp. 47–53. Lawler, I.F., Aldrich, J.C., 1987. Sublethal effects of bis(tri-n-butyltin)oxide on Crassostrea gigas spat. Mar. Pollut. Bull. 18, 274–278.
Molluscs 381 Leatherland, T.M., Burton, J.D., 1974. The occurrence of some trace metals in coastal organisms with particular reference to the Solent region. J. Mar. Biol. Assoc. UK 54, 457–468. Lee, R.F., 1985. Metabolism of tributyltin oxide by crabs, oysters and fish. Mar. Environ. Res. 17, 145–148. Lee, E.H., Ryu, B.H., Yang, S.T., 1975. Suitability of shellfish for processing. Bull. Korean Fish. Soc. 8, 85–89. Lee, B.G., Lee, J.S., Luoma, S.N., 2006. Comparison of selenium bioaccumulation in the clams Corbicula fluminea and Potamocorbula amurensis: a bioenergetic modeling approach. Environ. Toxicol. Chem. 25, 1933–1940. LeGall, P., Ancellin, J., 1971. Concentration Factors for Cs 137, Ce 144, and Ru 106 in Several Species of Edible Marine Mollusks and Crustaceans. Available from NTIS, Springfield, VA, as CEA-N-1488, 17 pp. Lekhi, P., Cassis, D., Pearce, C.M., Ebell, N., Maldonado, M.T., Orians, K.J., 2008. Role of dissolved and particulate cadmium in the accumulation of cadmium in cultured oysters (Crassostrea gigas). Sci. Total Environ. 393, 309–325. Leung, K.M.Y., Kwong, R.P.Y., Ng, W.C., Horiguchi, T., Qiu, J.W., Yang, R., et al., 2006. Ecological risk assessments of endocrine disrupting organotin compounds using marine neogastropods in Hong Kong. Chemosphere 65, 922–938. Li, Y., Yu, Z., Song, X., Mu, Q., 2006. Trace metal concentrations in suspended particles, sediments and clams (Ruditapes philippinarum) from Jiaozhou Bay of China. Environ. Monit. Assess. 121, 491–501. Liang, L.N., He, B., Jiang, G.B., Chen, D.Y., Yao, Z.W., 2004a. Evaluation of mollusks as biomonitors to investigate heavy metal contaminations along the Chinese Bohai Sea. Sci. Total Environ. 324, 105–113. Liang, L.N., Hu, J.T., Chen, D.Y., Zhou, Q.F., He, B., Jiang, G.B., 2004b. Primary investigation of heavy metal contamination status in molluscs collected from Chinese coastal sites. Bull. Environ. Contam. Toxicol. 72, 937–944. Lima, N.R.W., Lacerda, L.D., Pfeiffer, W.C., Fiszman, M., 1986. Temporal and spatial variability in Zn, Cr, Cd and Fe concentrations in oyster tissues (Crassostrea brasiliana Lamarck, 1819) from Sepetiba Bay, Brazil. Environ. Technol. Lett. 7, 453–460. Limaverde, A.M., Wagener, A.L.R., Fernandez, M.A., Scofield, A.L., Coutino, R., 2007. Stramonita haemastoma as a bioindicator for organotin contamination in coastal environments. Mar. Environ. Res. 64, 384–398. Liu, W., Deng, P.Y., 2007. Accumulation of cadmium, copper, lead and zinc in the Pacific oyster, Crassostrea gigas, collected from the Pearl River estuary, southern China. Bull. Environ. Contam. Toxicol. 78, 535–538. Liu, C.W., Liang, C.P., Huang, F.M., Hsueh, Y.M., 2006. Assessing the human health risks from exposure of inorganic arsenic through oyster (Crassostrea gigas) consumption in Taiwan. Sci. Total Environ. 361, 57–66. Liu, C.W., Huang, Y.K., Hsueh, Y.M., Lin, K.H., Jang, C.S., Huang, L.P., 2008. Spatiotemporal distribution of arsineic species of oysters (Crassostrea gigas) in the coastal area of southwestern Taiwan. Environ. Monit. Assess. 138, 181–190. Lobel, P.B., 1986. Role of the kidney in determining the whole soft tissue zinc concentration of individual mussels (Mytilus edulis). Mar. Biol. 92, 355–359. Lobel, P.B., 1987. Short-term and long-term uptake of zinc by the mussel, Mytilus edulis: a study in individual variability. Arch. Environ. Contam. Toxicol. 16, 723–732. Lobel, P.B., Marshall, H.D., 1988. A unique low molecular weight zinc-binding ligand in the kidney cytosol of the mussel Mytilus edulis, and its relationship to the inherent variability of zinc accumulation in this organism. Mar. Biol. 99, 101–105. Loring, D.H., Asmund, G., 1989. Heavy metal contamination of a Greenland fjord system by mine wastes. Environ. Geol. Water Sci. 14, 61–71. Lowe, V.P.W., Horrill, A.D., 1991. Caesium concentration factors in wild herbivores and the fox (Vulpes vulpes L.). Environ. Pollut. 70, 93–107. Lowe, D.M., Moore, M.N., 1979. The cytochemical distributions of zinc (Zn II) and iron (Fe III) in the common mussel, Mytilus edulis, and their relationship with lysosomes. J. Mar. Biol. Assoc. UK 59, 851–858. Lowman, F.G., Ting, R.Y., 1973. The state of cobalt in seawater and its uptake by marine organisms and sediments. In: Radioactive Contamination of the Marine Environment. IAEC, Vienna, Austria, pp. 369–384. Lowman, F.G., Phelps, D.K., Ting, R.Y., Escalera, R.M., 1966. Progress Summary Report No.4, Marine Biology Program June 1965-June 1966. Puerto Rico Nucl. Cen. Rep.. PRNC 85, , pp. 1–57.
382 Chapter 6 Lowman, F.G., Martin, J.H., Ting, R.Y., Barnes, S.S., Swift, D.J.P., Seiglie, G.A., et al., 1970. Bioenvironmental and radiological-safety feasibility studies, Atlantic-Pacific interoceanic canal. Estuar. Mar. Ecol.I-IV. Prepared for Battelle Memorial Institute, 505 King Avenue, Columbus, OH, Contract AT (26-1)-171. Lucu, C., Jelisavcic, O., Lucic, S., Strohal, P., 1969. Interactions of 233Pa with tissues of Mytilus galloprovincialis and Carcinus mediterraneus. Mar. Biol. 2, 103–104. Lunde, G., 1970. Analysis of arsenic and selenium in marine raw materials. J. Sci. Food Agric. 21, 242–247. Luoma, S.N., Bryan, G.W., 1978. Factors controlling the availability of sediment-bound lead to the estuarine bivalve Scrobicularia plana. J. Mar. Biol. Assoc. UK 58, 793–802. Luoma, S.N., Bryan, G.W., 1979. Trace metal bioavailability: modeling chemical and biological interactions of sediment-bound zinc. In: Jenne, E.A. (Ed.), Chemical modeling in Aqueous Systems, Amer. Chem. Soc. Ser. 93, Washington, DC, 577–609. Luoma, S.N., Jenne, E.A., 1977. The availability of sediment-bound cobalt, silver, and zinc to a deposit-feeding clam. In: Drucker, H., Wildung, R.E. (Eds.), Biological Implications of Metals in the Environment. ERDA Sympos. Ser. 42. Available as CONF-750929 from NTIS, Springfield, VA, pp. 213–230. Luoma, S.N., Phillips, D.J.H., 1988. Distribution, variability, and impacts of trace elements in San Francisco Bay. Mar. Pollut. Bull. 19, 413–425. Luoma, S.N., Dagovitz, R., Axtmann, E., 1990. Temporally intensive study of trace metals in sediments and bivalves from a large river-estuarine system: Suisan Bay/Delta in San Francisco Bay. Sci. Total Environ. 97/98, 685–712. Luoma, S.N., 1994, Fate, Bioavailability and toxicity of silver in estuarine environments. In: Andren, A.W., Bober, T.W., Kramer, J.R., Sodergren, A., Crecelius, E.A., Luoma, S.N., Rodgers, J.H. (Organisers). Transport, Fate and Effects of Silver in the Environment, Proceedings of the 2nd International Conference, Univ. Wisconsin, Madison, 151-155. Luten, J.B., Bouquet, W., Burggraaf, M.M., Rus, J., 1986. Accumulation, elimination, and speciation of cadmium and zinc in mussels, Mytilus edulis, in the natural environment. Bull. Environ. Contam. Toxicol. 35, 579–586. Maanan, M., 2007. Biomonitoring of heavy metals using Mytilus galloprovincialis in Safi coastal waters, Morocco. Environ. Toxicol. 22, 525–531. Maanan, M., 2008. Heavy metal concentrations in marine molluscs from the Moroccan coastal region. Environ. Pollut. 153, 176–183. MacFarlane, G.R., Markich, S.J., Linz, K., Gifford, S., Dunstan, R.H., O’Connor, W., et al., 2006. Akoya pearl oyster shell as an archival monitor of lead exposure. Environ. Pollut. 143, 166–173. Machreki-Ajmi, M., Hamza-Chaffai, A., 2006. Accumulation of cadmium and lead in Cerastoderma glaucum originating from the Gulf of Gabes, Tunisia. Bull. Environ. Contam. Toxicol. 76, 529–537. Mackay, N.J., Williams, R.J., Kacprzac, J.L., Kazacos, M.N., Collins, A.J., Auty, E.H., 1975. Heavy metals in cultivated oysters (Crassostrea commercialis ¼ Saccostrea cucullata) from the estuaries of New South Wales. Aust. J. Mar. Freshw. Res. 26, 31–46. Maddock, B.G., Taylor, D., 1980. The acute toxicity and bioaccumulation of some lead alkyl compounds in marine animals. In: Branica, M., Konrad, Z. (Eds.), Lead in the Marine Environment. Pergamon Press, Oxford, UK, pp. 233–261. Maguire, R.J., 1991. Aquatic environmental aspects of non-pesticidal organotin compounds. Water Pollut. Res. J. Can. 26, 243–360. Maher, W.A., 1983. Selenium in marine organisms from St. Vincent’s Gulf, South Australia. Mar. Pollut. Bull. 14, 35–36. Majori, L., Petronio, F., 1973. Marine pollution by metals and their accumulation by biological indicators (accumulation factor). In: Sixth International Symposium on Medical Oceanography, Portoroz, Yugoslavia, September 26-30, 1973, pp. 55–90. Mandelli, E.F., 1975. The effects of desalinization brines on Crassostrea virginica (Gmelin). Water Res. 9, 287–295. Marks, G.W., 1938. The copper content and copper tolerance of some species of mollusks of the southern California coast. Biol. Bull. 75, 224–237.
Molluscs 383 Martin, J.L.M., 1979. Schema of lethal action of copper on mussels. Bull. Environ. Contam. Toxicol. 21, 808–814. Martin, J.H., Flegal, A.R., 1975. High copper concentrations in squid livers in association with elevated levels of silver, cadmium, and zinc. Mar. Biol. 30, 51–55. Martin, M., Stephenson, M.D., Martin, J.H., 1977. Copper toxicity experiments in relation to abalone deaths observed in a power plant’s cooling waters. Calif. Fish Game 63, 95–100. Martin, M., Stephenson, M.D., Smith, D.R., Gitierrez-Galindo, E.A., Munoz, G.F., 1988. Use of silver in mussels as a tracer of domestic wastewater discharge. Mar. Pollut. Bull. 19, 512–520. Martoja, M., Tue, V.T., Elkaim, B., 1980. Bioaccumulation du cuivre chez Littorina littorea (L.) (gasteropode prosobranche): signification physiologique et ecologique. J. Exp. Mar. Biol. Ecol. 43, 251–270. Mason, A.Z., 1988. The kinetics of zinc accumulation by the marine prosobranch gastropod Littorina littorea. Mar. Environ. Res. 24, 135–139. Mat, I., 1994. Arsenic and trace metals in commercially important bivalves, Anadara granosa and Paphia undulata. Bull. Environ. Contam. Toxicol. 52, 833–839. Mat, I., Maah, M.J., Johari, A., 1994. Trace metals in sediments and potential availability to Anadara granosa. Arch. Environ. Contam. Toxicol. 27, 54–59. Mathew, P., Menon, N.R., 1993. Heavy metal stress induced variations in O:N ratio in two tropical bivalves Perna indica (Kuriakose & Nair) and Donax incarnatus Gmelin. Indian J. Exp. Biol. 31, 694–698. Matida, Y., Kumada, H., 1969. Distribution of mercury in water, bottom mud and aquatic organisms of Minamata Bay, the River Agano and other water bodies in Japan. Bull. Freshw. Fish. Res. Lab. Tokyo 19(2), 73–79. Matida, Y., Kumada, H., Kimura, S., Saiga, Y., Nose, T., Yokote, M., et al., 1972. Toxicity of mercury compounds to aquatic organisms and accumulation of the compounds by the organisms. Bull. Freshw. Fish. Res. Lab. Tokyo 21, 197–227. Matsumoto, T., Satake, M., Yamamoto, J., Haruna, S., 1964. On the micro constituent elements in marine invertebrates. J. Oceanogr. Soc. Jpn 20(3), 15–19. Matthiessen, P., Gibbs, P.E., 1998. Critical appraisal of the evidence for tributyltin-mediated endocrine disruption in mollusks. Environ. Toxicol. Chem. 17, 37–43. Mauchline, J., Templeton, W.L., 1966. Strontium, calcium and barium in marine organisms from the Irish Sea. J. Conseil 30, 161–170. Mauri, M., Orlando, E., Nigro, M., Regoli, F., 1990. Heavy metals in the Antarctic scallop Adamussium colbecki. Mar. Ecol. Prog. Ser. 67, 27–33. McClellan-Green, P., Romano, J., Rittschof, D., 2006. Imposex induction in the mud snail, Ilyanassa obsoleta by three tin compounds. Bull. Environ. Contam. Toxicol. 76, 581–588. McFarren, E.F., Campbell, J.E., Engle, J.B., 1962. The occurrence of copper and zinc in shellfish. In: Jensen, E.D. (Ed.), Proceedings of the 1961 Shellfish Sanitation Workshop. U.S. Dept. Health, Educa. Welfare, Publ. Health Serv, pp. 229–234. Mehran, A.R., Tremblay, J.L., 1965. An aspect of zinc metabolism in Littorina obtusa L. and Fucus edentatus. Rev. Can. Biol. 24, 157–161. Messiha, N.N., Ikladious, N.E., 1986. Antifouling performance of some new organotin polymers in the Mediterranean and Red Sea. J. Control. Release 3, 235–242. Metian, M., Bustamante, P., Hedouin, L., Warnau, M., 2008. Accumulation of nine metals and one metalloid in the tropical scallop Comptopallium radula from coral reefs in New Caledonia. Environ. Pollut. 152, 542–552. Miettinen, V., Verta, M., 1978. On the heavy metals and chlorinated hydrocarbons in the Gulf of Bothnia in Finland. Finn. Mar. Res. 244, 219–226. Miettinen, J.K., Tillander, M., Risanen, K., Miettinen, V., Ohmomo, Y., 1969. Distribution and excretion rates of phenyl- and methylmercury nitrate in fish muscles, molluscs and crayfish. In: Proceedings of the Sixth Japan. Conf. Radioisotopes, Tokyo, pp. 474–478. Miettinen, J.K., Heyraud, M., Keckes, S., 1972. Mercury as a hydrospheric pollutant. II. Biological half-time of methyl mercury in four Mediterranean species: a fish, a crab, and two molluscs. In: Ruivo, M. (Ed.), Marine Pollution and Sea Life. Fishing Trading News (Books), London, pp. 295–298.
384 Chapter 6 Miller, W.L., Blake, N.J., Byrne, R.H., 1985. Uptake of Zn65 and Mn54 into body tissues and renal concretions by the southern quahog, Mercenaria campechiensis (Gmelin): effects of elevated phosphate and metal concentrations. Mar. Environ. Res. 17, 167–171. Miramand, P., Bentley, D., 1992. Concentration and distribution of heavy metals in two cephalopods, Eledone cirrhosa and Sepia officinalis, from the French coast of the English Channel. Mar. Biol. 114, 407–414. Miramand, P., Bustamante, P., Bentley, D., Koueta, N., 2006. Variation of heavy metal concentrations (Ag, Cd, Co, Cu, Fe, Pb, V, and Zn) during the life cycle of the common cuttlefish Sepia officinalis. Sci. Total Environ. 361, 132–143. Mishima, J., Odum, E., 1963. Excretion rate of 65Zn by Littorina irrorata in relation to temperature and body size. Limnol. Oceanogr. 8, 39–44. Morgan, J.D., Mitchell, D.G., Chapman, P.M., 1986. Individual and combined toxicity of manganese and molybdenum to mussel, Mytilus edulis, larvae. Bull. Environ. Contam. Toxicol. 37, 303–307. Morris, R.J., Law, R.J., Allchin, C.R., Kelly, C.A., Fileman, C.F., 1989. Metals and organochlorines in dolphins and porpoises of Cardigan Bay, West Wales. Mar. Pollut. Bull. 20, 512–523. Morse, J.W., Presley, B.J., Taylor, R.J., Benoit, G., Santschi, P., 1993. Trace metal chemistry of Galveston Bay: water, sediments, and biota. Mar. Environ. Res. 36, 1–37. Mubiana, V.K., Blust, R., 2006. Metal content of marine mussels from western Scheldt estuary and nearby protected marine bay, the Netherlands: impact of past and present contamination. Bull. Environ. Contam. Toxicol. 77, 203–210. Mubiana, V.K., Blust, R., 2007. Effects of temperature on scope for growth and accumulation of Cd, Co, Cu and Pb by the marine bivalve Mytilus edulis. Mar. Environ. Res. 63, 219–235. Munzinger, A., Guarducci, M.L., 1988. The effect of low zinc concentrations on some demographic parameters of Biomphalaria glabrata (Say), mollusca: gastropoda. Aquat. Toxicol. 12, 51–61. Nambisan, P.N.K., Lakshmanan, P.T., Salih, K.Y., 1977. On the uptake of copper (II) by Meretrix casta (Cheminitz), an indicator species of pollution. Curr. Sci. 46, 437–440. Napoleao, P., Pinheiro, T., Reis, C.S., 2005. Elemental characterization of tissues of Octopus vulgaris along the Portuguese coast. Sci. Total Environ. 345, 41–49. Navrot, J., Amiel, A.J., Kronfeld, J., 1974. Patella vulgata: a biological monitor of coastal metal pollution—a preliminary study. Environ. Pollut. 7, 303–308. Nelson, J.D., Blair, W., Brinckman, F.E., Colwell, R.R., Iverson, W.P., 1971. Biodegradation of phenylmercuric acetate by mercury-resistant bacteria. Appl. Microbiol. 26, 321–326. Nelson, D.A., Calabrese, A., Nelson, B.A., MacInnes, J.R., Wenzloff, D.R., 1976. Biological effects of heavy metals on juvenile bay scallops, Argopecten irradians, in short-term exposures. Bull. Environ. Contam. Toxicol. 16, 275–282. Nelson, D.A., Calabrese, A., MacInnes, J.R., 1977. Mercury stress on juvenile bay scallops, Argopecten irradians, under various salinity-temperature regimes. Mar. Biol. 43, 293–297. Nelson, D.A., Calabrese, A., Greig, R.A., Yevich, P.P., Chang, S., 1983. Long-term silver effects on the marine gastropod Crepidula fornicata. Mar. Ecol. Prog. Ser. 12, 155–165. Nesto, N., Romano, S., Moschino, V., Mauri, M., Da Ros, J., 2007. Bioaccumulation and biomarker responses of trace metals and micro-organic pollutants in mussels and fish from the Lagoon of Venice, Italy. Mar. Pollut. Bull. 53, 469–484. Neuberger-Cywiak, L., Achituv, Y., Garcia, E.M., 2007. Effects of sublethal Zn++and Cd++concentrations on filtration rate, absorption efficiency and scope for growth in Donax trunculus (bivalvia; donacidae). Bull. Environ. Contam. Toxicol. 79, 622–627. Ng, T.Y.T., Rainbow, P.S., Amiard-Triquet, C., Amiard, J.C., Wang, W.X., 2007. Metallothionein turnover, cytosolic distribution and the uptake of Cd by the green mussel Perna viridis. Aquat. Toxicol. 84, 153–161. Nias, D.J., McKillup, S.C., Edyvane, K.S., 1993. Imposex in Lepsiella vinosa from southern Australia. Mar. Pollut. Bull. 26, 380–384.
Molluscs 385 Nicholls, G.D., Curl Jr., H., Bowen, V.T., 1959. Spectrographic analyses of marine plankton. Limnol. Oceanogr. 4, 472–476. Nicholson, S., Szefer, P., 2003. Accumulation of metals in the soft tissues, byssus and shell of the mytilid mussel Perna viridis (Bivalvia: Mytilidae) from polluted and uncontaminated locations in Hong Kong coastal waters. Mar. Pollut. Bull. 46, 1039–1043. Nicolaidu, A., Nott, J.A., 1990. Mediterranean pollution from a ferro-nickel smelter: differential uptake by some gastropods. Mar. Pollut. Bull. 21, 137–143. Nielsen, S.A., 1974. Vertical concentration gradients of heavy metals in cultured mussels. N. Z. J. Mar. Freshw. Res. 8, 631–636. Nielsen, S.A., 1975. Cadmium in New Zealand dredge oysters: geographic distribution. Int. J. Environ. Anal. Chem. 4, 1–7. Nielsen, S.A., Nathan, A., 1975. Heavy metal levels in New Zealand molluscs. N. Z. J. Mar. Freshw. Res. 9, 467–481. Noel-Lambot, F., 1976. Distribution of cadmium, zinc and copper in the mussel, Mytilus edulis. Existence of cadmium-binding proteins similar to metallothioneins. Experientia 32, 324–325. Noel-Lambot, F., Bouquegneau, J.M., Frankenne, F., Disteche, A., 1980. Cadmium, zinc and copper accumulation in limpets (Patella vulgata) from the Bristol Channel with special reference to metallothioneins. Mar. Ecol. Prog. Ser. 2, 81–89. Norum, U., Lai, V.W.M., Cullen, W.R., 2005. Trace element distribution during the reproductive cycle of female and male spiny and Pacific scallops, with implications for biomonitoring. Mar. Pollut. Bull. 50, 175–184. Olson, K.R., Harrel, R.C., 1973. Effect of salinity on acute toxicity of mercury, copper, and chromium for Rangia cuneata (Pelycopoda, Mactridae). Contrib. Mar. Sci. 17, 9–13. Orlando, E., Mauri, M., 1978. Accumulation of manganese in Donax trunculus. L. (Bivalvia). IVes J. Etud. Pollut. 297–299. Ozretic, B., Krajinovic-Ozretic, M., Santin, J., Medjugorac, B., Kras, M., 1990. As, Cd, Pb, and Hg in benthic animals from the Kvarner-Rijeka Bay region, Yugoslavia. Mar. Pollut. Bull. 21, 595–597. Paez-Osuna, F., Osuna-Lopez, J.I., Izaguirse-Fiero, G., Zazueta-Padilla, H.M., 1994. Trace metals in mussels from the Ensenada del Pallon Lagoon, Mexico. Mar. Pollut. Bull. 28, 124–126. Palmer, J.B., Rand, G.M., 1977. Trace metal concentrations in two shellfish species of commercial importance. Bull. Environ. Contam. Toxicol. 18, 512–520. Papadopoulu, C., 1973. In: The elementary composition of marine invertebrates as a contribution to the sea pollution investigation. Proceedings of MAMBO Meeting, Castellabate, Italy, June 18-22, 1973, pp. 1–18. Papadopoulu, C., Hadzistelios, I., 1977. Radiochemical determination of europium and application of the method in marine samples. Rapp. Comm. Int. Mer Medit. 24, 89–93. Parchevskii, V.P., Polikarpov, G.G., Zabarunova, I.S., 1965. Certain regularities in the accumulation of yttrium and strontium by marine organisms. Dokl. Akad. Nauk SSSR 164, 913–916. Parsons, T.R., Bawden, C.A., Heath, W.A., 1973. Preliminary survey of mercury and other metals contained in animals from the Fraser River mudflats. J. Fish. Res. Board Can. 30, 1014–1016. Patel, B., Ganguly, A.K., 1973. Occurrence of Se 75 and Sn 113 in oysters. Health Phys. 24, 559–562. Patel, B., Valanju, P.G., Mulay, C.D., Balani, M.C., Patel, S., 1973. Radioecology of certain molluscs in Indian coastal waters. In: Radioactive Contamination of the Marine Environment. IAEA, Vienna, Austria, pp. 307–330. Patel, B., Patel, S., Balani, M.C., Pawar, S., 1978. Flux of certain radionuclides in the blood-clam Anadara granosa Linnaeus under environmental conditions. J. Exp. Mar. Biol. Ecol. 35, 177–195. Paul, J.D., Davies, I.M., 1986. Effects of copper- and tin-based anti-fouling compounds on the growth of scallops (Pecten maximus) and oysters (Crassostrea gigas). Aquaculture 54, 191–203. Pavoni, B., Centanni, E., Valcanover, S., Fasolato, M., Ceccato, S., Tagliapietra, D., 2007. Imposex levels and concentrations of organotin compounds (TBT and its metabolites) in Nassarius nitidus from the Lagoon of Venice. Mar. Pollut. Bull. 55, 505–511. Peake, B.M., Marsden, I.D., Bryan, A.M., 2006. Spatial and temporal variations in trace metal concentrations in the cockle, Austrovenus stutchburyi from Otago, New Zealand. Environ. Monit. Assess. 115, 119–144.
386 Chapter 6 Pearce, N.J.G., Mann, V.L., 2006. Trace metal variations in the shells of Ensis siliqua record pollution and environmental conditions in the sea to the west of mainland Britain. Mar. Pollut. Bull. 52, 739–755. Peden, J.D., Crothers, J.H., Waterfall, C.E., Beasley, J., 1973. Heavy metals in Somerset marine organisms. Mar. Pollut. Bull. 4, 7–10. Penrose, W.R., Black, R., Hayward, M.J., 1975. Limited arsenic dispersion in seawater, sediments, and biota near a continuous source. J. Fish. Res. Board Can. 32, 1275–1281. Pentreath, R.J., 1973. The accumulation from water of 65Zn, 54Mn, 58Co and 59Fe by the mussel, Mytilus edulis. J. Mar. Biol. Assoc. UK 53, 127–143. Pequegnat, J.E., Fowler, S.W., Small, L.F., 1969. Estimates of the zinc requirements of marine organisms. J. Fish. Res. Board Can. 26, 145–150. Pesch, G.G., Stewart, N.E., 1980. Cadmium toxicity to three species of invertebrates. Mar. Environ. Res. 3, 145–156. Pesch, G., Reynolds, B., Rogerson, P., 1977. Trace metals in scallops from within and around two ocean disposal sites. Mar. Pollut. Bull. 8, 224–228. Peshut, P.J., Morrison, R.J., Brooks, B.A., 2008. Arsenic speciation in marine fish and shellfish from American Samoa. Chemosphere 71, 484–492. Pfeiffer, W.C., Lacerda, L.D., Fiszman, M., Lima, N.R.W., 1985. Metais pesados no pescado do Baia de Sepetiba, Estado de Rio de Janeiro. Ciencia Cultura 37, 297–302. Phelps, H.L., 1979. Cadmium sorption in estuarine mud-type sediment and the accumulation of cadmium in the soft-shell clam, Mya arenaria. Estuaries 2, 40–44. Phelps, D.K., Telek, G., Lapan Jr., R.L., 1975. Assessment of heavy metal distribution within the food web. In: Pearson, E.A., Frangipane, E.D. (Eds.), Marine Pollution and Marine Waste Disposal. Pergamon Press, Elmsford, NY, pp. 341–348. Phillips, J.H., 1976a. The common mussel Mytilus edulis as an indicator of pollution by zinc, cadmium, lead and copper. I. Effects of environmental variables on uptake of metals. Mar. Biol. 38, 59–69. Phillips, J.H., 1976b. The common mussel Mytilus edulis as an indicator of pollution by zinc, cadmium, lead and copper. II. Relationship of metals in the mussels to those discharged by industry. Mar. Biol. 38, 71–80. Phillips, D.J.H., 1977a. The use of biological indicator organisms to monitor trace metal pollution in marine and estuarine environments—a review. Environ. Pollut. 13, 281–317. Phillips, D.J.H., 1977b. Effects of salinity on the net uptake of zinc by the common mussel Mytilus edulis. Mar. Biol. 41, 79–88. Phillips, D.J.H., 1977c. The common mussel Mytilus edulis as an indicator of trace metals in Scandinavian waters. I. Zinc and cadmium. Mar. Biol. 43, 283–291. Phillips, D.J.H., 1978. The common mussel Mytilus edulis as an indicator of trace metals in Scandinavian waters. II. Lead, iron, and manganese. Mar. Biol. 46, 147–156. Phillips, D.J.H., 1979. The rock oyster Saccostrea glomerata as an indicator of trace metals in Hong Kong. Mar. Biol. 53, 353–360. Phillips, D.J.H., Depledge, M.H., 1986. Chemical forms of arsenic in marine organisms, with emphasis on Hemifusus species. Water Sci. Technol. 18, 213–222. Phillips, D.J.H., Thompson, G.B., Gabuji, K.M., Ho, C.T., 1982. Trace metals of toxicological significance to man in Hong Kong seafood. Environ. Pollut. 3B, 27–45. Pilkey, O.H., Goodell, H.G., 1963. Trace elements in recent mollusk shells. Limnol. Oceanogr. 8, 137–148. Pillai, K.C., Smith, R.C., Folsom, T.R., 1964. Plutonium in the marine environment. Nature 203, 568–571. Pinkney, A.E., Matteson, L.L., Wright, D.A., 1990. Effects of tributyltin on survival, growth, morphometry, and RNA-DNA ratio of larval striped bass, Morone saxatilis. Arch. Environ. Contam. Toxicol. 19, 235–240. Podgurskaya, O.V., Kavun, V.Y., 2006. Cadmium concentration and subcellular distribution in organs of the mussel Crenomytilus grayanus from upwelling regions of Okhotsk Sea and Sea of Japan. Arch. Environ. Contam. Toxicol. 51, 567–572. Pouvreau, B., Amiard, J.C., 1974. Etude experimentale de l’accumulation de l’argent 110 m chez divers organismes marins. Comm. Ener. Atom. France. Rept. CEA-R-4571, pp. 1–19.
Molluscs 387 Presley, B.J., Taylor, R.J., Boothe, P.N., 1990. Trace metals in Gulf of Mexico oysters. Sci. Total Environ. 97/98, 551–593. Preston, E.M., 1971. The importance of ingestion in chromium-51 accumulation by Crassostrea virginica (Gmelin). J. Exp. Mar. Biol. Ecol. 6, 47–54. Preston, A., Dutton, J.W.R., Harvey, B.R., 1968. Detection, estimation, and radiological significance of silver110m in oysters in the Irish Sea and the Blackwater Estuary. Nature 218, 689–690. Preston, A., Jeffries, D.F., Dutton, J.W.R., Harvey, B.R., Steele, A.K., 1972. British Isles coastal waters: the concentrations of selected heavy metals in sea water, suspended matter and biological indicators—a pilot survey. Environ. Pollut. 3, 69–82. Price, R.J., Lee, J.S., 1972. Effects of cations on the interactions between paralytic shellfish poison and butter clam Saxidomus giganteus melanin. J. Fish. Res. Board Can. 29, 1659–1661. Pringle, B.H., Hissong, D.E., Katz, E.L., Malawka, S.T., 1968. Trace metal accumulation by estuarine mollusks. J. Sanit. Eng. Div. 94(SA3), 455–475. Protasowicki, M., Dural, M., Jaremek, J., 2008. Trace metals in the shells of blue mussels (Mytilus edulis) from the Poland coast of Baltic Sea. Environ. Monit. Assess. 141, 329–337. Pyle, T.E., Tieh, T.T., 1970. Strontium, vanadium, and zinc in the shells of pteropods. Limnol. Oceanogr. 15, 153–154. Raimundo, J., Caetano, M., Viale, C., 2004. Geographical variation and partition of metals in Octopus vulgaris along the Portuguese coast. Sci. Total Environ. 325, 71–81. Raimundo, J., Vale, C., Duarte, R., Moura, J., 2008. Sub-cellular partitioning of Zn, Cu, Cd and Pb in the digestive gland of native Octopus vulgaris exposed to different metal concentrations (Portugal). Sci. Total Environ. 390, 410–416. Ramelow, G.J., Webre, C.L., Mueller, C.S., Beck, J.N., Young, J.C., Langley, M.P., 1989. Variations of heavy metals and arsenic in fish and other organisms from the Calcasieu River and Lake, Louisiana. Arch. Environ. Contam. Toxicol. 18, 804–818. Ratkowsky, D.A., Thrower, S.J., Eustace, I.J., Olley, J., 1974. A numerical study of the concentration of some heavy metals in Tasmanian oysters. J. Fish. Res. Board Can. 31, 1165–1171. Rato, M., Sousa, A., Quinta, R., Langston, W., Barroso, C., 2006. Assessment of inshore/offshore tributyltin pollution gradients in the northwest Portugal continental shelf using Nassarius reticulatus as a bioindicator. Environ. Toxicol. Chem. 25, 3213–3220. Ratte, H.T., 1999. Bioaccumulation and toxicity of silver compounds: a review. Environ. Toxicol. Chem. 18, 89–108. Raymont, J.E.G., 1972. Some aspects of pollution in Southampton water. Proc. R. Soc. Lond. 180B (1061), 451–468. Rebelo, M.F., Amaral, M.C.R., Pfeiffer, W.C., 2003a. High Zn and Cd accumulation in the oyster Crassostrea rhizophorae and its relevance as a sentinel species. Mar. Pollut. Bull. 46, 1341–1358. Rebelo, M.F., Pfeiffer, W.C., Silva, H., Moraes, M.O., 2003b. Cloning and detection of metallothionein mRNA by PT-PCR in mangrove oysters (Crassostrea rhizophorae). Aquat. Toxicol. 64, 359–362. Redpath, K.J., Davenport, J., 1988. The effect of copper, zinc and cadmium on the pumping rate of Mytilus edulis. L. Aquat. Toxicol. 13, 217–226. Rees, H.I., Waldock, R., Matthiessen, P., Pendle, M.A., 1999. Surveys of the epibenthos of the Crouch Estuary (UK) in relation to TBT contamination. J. Mar. Biol. Assoc. UK 79, 209–223. Reimer, A.A., Reimer, R.D., 1975. Total mercury in some fish and shellfish along the Mexican coast. Bull. Environ. Contam. Toxicol. 14, 105–111. Reish, D.J., 1977. Effects of chromium on the life history of Capitella capitata (Annelida: Polychaeta). In: Vernberg, F.J., Calabrese, A., Thurberg, F.P., Vernberg, W.B. (Eds.), Physiological Responses of Marine Biota to Pollutants. Academic Press, New York, pp. 199–207. Reish, D.J., Martin, J.M., Piltz, F.M., Word, J.Q., 1976. The effect of heavy metals on laboratory population of two polychaetes with comparison to the water quality conditions and standards in southern California marine waters. Water Res. 10, 299–302.
388 Chapter 6 Renzoni, A., Bacci, E., Falciai, L., 1973. In: Mercury concentrations in the water, sediments and fauna of an area of the Tyrrhenian coast. Sixth International Symposium on Medical Oceanography, Portoroz, Yugoslavia, September 26-30, 1973, pp. 17–45. Reynolds, B.H., 1979. Trace metals monitoring at two ocean disposal sites. US Environ. Protect. Agen., Rep. EPA 600/3-79-037, pp. 1–64. Robertson, D.E., 1967. Trace elements in marine organisms. Rapp. Am. BNWL 481-2, pp. 56–59. Robertson, D.E., Rancitelli, L.A., Langford, J.C., Perkins, R.W., 1972. In: Battelle-Northwest Contribution to the IDOE Base-Line Study. Battelle Pacific Northwest Laboratory, Richland, WA, pp. 1–46. Rocca, E., 1969. Copper distribution in Octopus vulgaris Lam. hepatopancreas. Comp. Biochem. Physiol. 28, 67–82. Roesijadi, G., 1994. Behavior of metallothionein-bound metals in a natural population of an estuarine mollusc. Mar. Environ. Res. 38, 147–168. Roesijadi, G., Fellingham, G.W., 1987. Influence of Cu, Cd, and Zn preexposure on Hg toxicity in the mussel Mytilus edulis. Can. J. Fish. Aquat. Sci. 44, 680–684. Romeril, M.G., 1971. The uptake and distribution of 65Zn in oysters. Mar. Biol. 9, 347–354. Romeril, M.G., 1974. Trace metals in sediments and bivalve mollusca in Southampton water and the Solent. Rev. Int. Oceanogr. Med. 33, 31–47. Romeril, M.G., 1977. Heavy metal accumulation in the vicinity of a desalination plant. Mar. Pollut. Bull. 8, 84–87. Roosenburg, W.H., 1969. Greening and copper accumulation in the American oyster, Crassostrea virginica, in the vicinity of a steam electric generating station. Chesapeake Sci. 10, 241–252. Roper, D.S., Hickey, C.W., 1994. Behavioural responses of the marine bivalve Macoma liliana exposed to copper- and chlordane-exposed sediments. Mar. Biol. 118, 673–680. Rose, K.A., Summers, J.K., McLean, R.I., Domotor, S.L., 1988. Radiosilver (Ag-110m) concentrations in Chesapeake Bay oysters maintained near a nuclear power plant: a statistical analysis. Environ. Monit. Assess. 10, 205–218. Rosemarin, A., Notini, M., Holmgren, K., 1985. The fate of arsenic in the Baltic Sea Fucus vesiculosus ecosystem. Ambio 14, 342–345. Rosen, G., Rivera-Duarte, I., Chadwick, D.B., Ryan, A., Santore, R.C., Paquin, P.R., 2008. Critical tissue copper residues for marine bivalve (Mytilus galloprovincialis) and echinoderm (Strongylocentrotus purpuratus) embryonic development: conceptual regulatory and environmental regulations. Mar. Environ. Res. 55, 327–336. Rosenberg, R., 1977. Effects of dredging operations on estuarine benthic fauna. Mar. Pollut. Bull. 8, 102–104. Rucker, J.B., Valentine, J.W., 1961. Salinity response of trace element concentration in Crassostrea virginica. Nature 190, 1099–1100. Ruddell, C.L., Rains, D.W., 1975. The relationship between zinc, copper and the basophils of two crassostreid oysters, C. gigas and C. virginica. Comp. Biochem. Physiol. 51A, 591–595. Ruelas-Inzunza, J., Paez-Osuna, F., 2008. Trophic distribution of Cd, Pb, and Zn in a food web from Alata-Ensenada del Pabellon subtropical lagoon, SE Gulf of Mexico. Arch. Environ. Contam. Toxicol. 54, 584–596. Ruelas-Inzunza, J., Garate-Viera, Y., Paez-Osuna, F., 2007. Lead in clams and fish of dietary importance from Coatzacoalcos estuary (Gulf of Mexico), an industrialized tropical region. Bull. Environ. Contam. Toxicol. 79, 508–513. Said, T.O., Farag, R.S., Younis, A.M., Shreadah, M.A., 2006. Organotin species in fish and bivalves samples collected from the Egyptian Mediterranean Coast of Alexandria, Egypt. Bull. Environ. Contam. Toxicol. 77, 451–458. Saiz-Salinas, J.I., Ruiz, J.M., Frances-Zubillaga, G., 1996. Heavy metal levels in intertidal sediments and biota from the Bidasoa estuary. Mar. Pollut. Bull. 32, 69–71. Sajwan, K.S., Kumar, K.S., Paramasivam, S., Compton, S.S., Richardson, J.P., 2008. Elemental status in sediment and American oyster collected from Savannah marsh/estuarine ecosystem: a preliminary assessment. Arch. Environ. Contam. Toxicol. 54, 245–258.
Molluscs 389 Salo, E.W., Leet, W.L., 1969. The concentration of zinc-65 by oysters maintained in the discharge canal of a nuclear power plant. In: Proceedings of the 2nd National Symposium on Radioecology, Ann Arbor, MI, 1967, pp. 363–371. Sanders, J.G., Abbe, G.R., Riedel, G.F., 1990. Silver uptake and subsequent effects on growth and species composition in an estuarine community. Sci. Total Environ. 97/98, 761–769. Sanders, B.M., Martin, L.S., Nelson, W.G., Phelps, D.K., Welch, W., 1991a. Relationships between accumulation of a 60 kDa stress protein and a scope-for-growth in Mytilus edulis exposed to a range of copper concentrations. Mar. Environ. Res. 31, 81–97. Sanders, J.G., Riedel, G.F., Abbe, G.R., 1991b. Factors controlling the spatial and temporal variability of trace metal concentrations in Crassostrea virginica (Gmelin). In: Elliott, M., Ducrotoy, J.P. (Eds.), Estuaries and Coasts: Spatial and Temporal Comparisons. ECSA Sympos. 19 (Univ. Caen, France, 1989). Olsen & Olsen, Fredensborg, Denmark, pp. 335–339. Sanders, B.M., Martin, L.S., Howe, S.R., Nelson, W.G., Hegre, E.S., Phelps, D.K., 1994. Tissue-specific differences in accumulation of stress proteins in Mytilus edulis exposed to a range of copper concentrations. Toxicol. Appl. Pharmacol. 125, 206–213. Sankar, T.V., Zynudheen, A.A., Anandan, R., Nair, P.G.V., 2006. Distribution of organochlorine pesticides and heavy metal residues in fish and shellfish from Calicut region, Kerala, India. Chemosphere 65, 583–590. Sankaranarayanan, V.N., Pusushan, K.S., Rao, T.S.S., 1978. Concentration of some of the heavy metals in the oyster, Crassostrea madrasensis (Preston) from the Cochin Region. Indian J. Mar. Sci. 7, 130–131. Santos, I.R., Silva-Filho, E.V., Schaefer, C., Sella, S.M., Silva, C.A., Gomes, V., et al., 2006. Baseline mercury and zinc concentrations in terrestrial and coastal organisms of Admiralty Bay, Antarctica. Environ. Pollut. 140, 304–311. Sasikumar, G., Krishnakumar, P.K., Bhat, G.S., 2006. Monitoring trace metal contaminants in green mussel, Perna viridis from the coastal waters of Karnataka, southwest coast of India. Arch. Environ. Contam. Toxicol. 51, 206–214. Sastry, V.W., Bhatt, Y.M., 1965. Zinc content of some marine bivalves and barnacles from Bombay Shores. J. Indian Chem. Soc. 42, 121–122. Sautet, J., Oliver, H., Quicke, J., 1964. Contribution to the study of the biological fixation and elimination of arsenic by Mytilus edulis. Second note. Ann. Med. Leg. Criminol. Police Sci. Toxicol. 44, 466–471. Savari, A., Lockwood, A.P.M., Sheader, M., 1991. Effects of season and size (age) on heavy metal concentrations of the common cockle (Cerastoderma edule (L.)) from Southampton water. J. Molluscan Stud. 57, 45–57. Saward, D., Stirling, A., Topping, G., 1975. Experimental studies on the effects of copper on a marine food chain. Mar. Biol. 29, 351–356. Sayler, G.S., Nelson Jr., J.D., Colwell, R.R., 1975. Role of bacteria in bioaccumulation of mercury in the oyster Crassostrea virginica. Appl. Microbiol. 30, 91–96. Scancar, J., Zuliani, T., Turk, T., Milacic, R., 2007. Organotin compounds and selected metals in the marine environment of northern Adriatic Sea. Environ. Monit. Assess. 127, 271–282. Scanes, P., 1993. Trace metal uptake in cockles Anadara trapezium from Lake Macquarie, New South Wales. Mar. Ecol. Prog. Ser. 102, 135–142. Schell, W.R., Nevissi, A., 1977. Heavy metals from waste disposal in Central Puget Sound. Environ. Sci. Technol. 11, 887–893. Schintu, M., Durante, L., Maccioni, A., Meloni, P., Degetto, S., Contu, A., 2008. Measurement of environmental trace-metal levels in Mediterranean coastal areas with transplanted mussels and DGT techniques. Mar. Pollut. Bull. 57, 832–837. Schipp, R., Hevert, F., 1978. Distribution of copper and iron in some central organs of Sepia officinalis (cephalopoda). A comparative study by flameless atomic absorption and electron microscopy. Mar. Biol. 47, 391–399. Schneider, J., 1972. Lower fungi as test organisms of pollutants in sea and brackish water. The effects of heavy metal compounds and phenol on Thraustochytrium striatum. Mar. Biol. 16, 214–225.
390 Chapter 6 Schuhmacher, M., Bosque, M.A., Domingo, J.L., Corbella, J., 1990. Lead and cadmium concentrations in marine organisms from the Tarragona coastal waters, Spain. Bull. Environ. Contam. Toxicol. 44, 784–789. Schuhmacher, M., Domingo, J.L., Bosque, M.A., Corbella, J., 1992. Heavy metals in marine species from the Tarragona Coast, Spain. J. Environ. Sci. Health 27A, 1939–1948. Schuhmacher, M., Batiste, J., Bosque, M.A., Domingo, J.L., Corbella, J., 1994. Mercury concentrations in marine species from the coastal area of Tarragona Province, Spain. Dietary intake of mercury through fish and seafood consumption. Sci. Total Environ. 156–273. Schulz-Baldes, M., 1972. Toxicity and accumulation of lead in the common mussel Mytilus edulis in laboratory experiment. Mar. Biol. 16, 226–229. Schulz-Baldes, M., 1973. Die Miesmuschel, Mytilus edulis, als Indikator fuer die Bleikonzentration in Weseraestuar un in der Deutschen Bucht. Mar. Biol. 21, 98–102. Schulz-Baldes, M., 1974. Lead uptake from sea water and food, and lead loss in the common mussel, Mytilus edulis. Mar. Biol. 25, 177–193. Scott, D.M., Major, C.W., 1972. The effect of copper (II) on survival, respiration and heart rate in the common blue mussel, Mytilus edulis. Biol. Bull. 143, 679–688. Segar, D.A., Collins, J.D., Riley, J.P., 1971. The distribution of the major and some minor elements in marine animals. Part II. Molluscs. J. Mar. Biol. Assoc. UK 51, 131–136. Seixas, S., Pierce, G.J., 2005. Vanadium, rubidium, and potassium in Octopus vulgaris (Mollusca: Cephalopoda). Sci. Mar. 69, 215–222. Sen, H., Sunlu, U., 2007. Effects of cadmium (CdCl2) on development and hatching of eggs in European squid (Loligo vulgaris Lamarck, 1798) (Cephalopoda: Loliginidae). Environ. Monit. Assess. 133, 371–378. Sericano, J.L., Wade, T.L., Qian, Y., 1999. NOAA’s national status and trends project: environmental significance of the uptake and depuration of the antifouling agent tributyltin by the American oyster Crassostrea virginica. In: 218th American Chemical Society National Meeting, New Orleans, August 22-26, 1999. Book of Abstracts, Part I, AGRO 59. Shiber, J.G., Shatila, T.A., 1978. Lead, cadmium, copper, nickel and iron in limpets, mussels and snails from the coast of Ras Beirut, Lebanon. Mar. Environ. Res. 1, 125–134. Shim, W.J., Oh, J.R., Kahng, S.H., Shim, J.H., Lee, S.H., 1998. Accumulation of tributyl-and triphenyltin compounds in Pacific oyster, Crassostrea gigas, from the Chinhae Bay system, Korea. Arch. Environ. Contam. Toxicol. 35, 41–47. Shimizu, M., Kajihara, T., Hiyama, Y., 1970. Uptake of 60Co by marine animals. Rec. Oceanogr. Works Jpn. 10, 137–145. Shimizu, M., Kajihara, T., Suyama, I., Hiyama, Y., 1971. Uptake of 58Co by mussel, Mytilus edulis. J. Rad. Res. 12, 17–28. Shiomi, K., Shinigawa, A., Hirota, K., Yamanaka, H., Kikuchi, T., 1984. Identification of arsenobetaine as a major arsenic compound in the ivory shell Buccinum striatissimum. Agric. Biol. Chem. 48, 2863–2864. Shore, R., Carney, G., Stygall, T., 1975. Cadmium levels and carbohydrate metabolism in limpets. Mar. Pollut. Bull. 6, 187–189. Shuster Jr., C.N., Pringle, B.H., 1968. Effects of trace metals on estuarine molluscs. In: Proceedings of the First Mid-Atlantic Industrial Waste Conference, November 1967. Available from Dept. Civil Eng., Univ. Delaware, Newark, DE, pp. 285–304. Shuster Jr., C.N., Pringle, B.H., 1969. Trace metal accumulation by the American oyster, Crassostrea virginica. 1968 Proc. Nat. Shellfish Assoc. 59, 91–103. Side, J., 1987. Organotins—not so good relations. Mar. Pollut. Bull. 18, 205–206. Silva, C.A.R., Smith, B.D., Rainbow, P.S., 2006. Comparative biomonitors of coastal trace metal contamination in tropical South America (N. Brazil). Mar. Environ. Res. 61, 439–445. Simmonds, M., 1986. The case against tributyltin. Oryx 20, 217–220. Simpson, R.D., 1979. Uptake and loss of zinc and lead by mussels (Mytilus edulis) and relationship with body weight and reproductive cycle. Mar. Pollut. Bull. 10, 74–78. Sims Jr., R.R., Presley, B.J., 1976. Heavy metal concentrations in organisms from an actively dredged Texas bay. Bull. Environ. Contam. Toxicol. 16, 520–527.
Molluscs 391 Smith, B.S., 1981a. Male characteristics on female mud snails caused by antifouling bottom paints. J. Appl. Toxicol. 1, 22–25. Smith, B.S., 1981b. Tributyltin compounds induce male characteristics on female mud snails Nassarius obsoletus ¼ Ilyanassa obsoleta. J. Appl. Toxicol. 1, 141–144. Smith, A.J., Thain, J.E., Barry, J., 2006. Exploring the use of caged Nucella lapillus to monitor changes to TBT hotspot areas: a trial in the River Tyne estuary (UK). Mar. Environ. Res. 62, 149–163. Sokolowski, A., Wolowicz, M., Hummel, H., 2007. Metal sources to the Baltic clam Macoma balthica (mollusca: bivalvia) in the southern Baltic Sea (the Gulf of Gdansk). Mar. Environ. Res. 63, 236–256. Sorentino, C., 1979. Mercury in marine and freshwater fish of Papua, New Guinea. Aust. J. Mar. Freshw. Res. 30, 617–623. Soria-Dengg, S., Ochavillo, D., 1990. Comparative toxicities of trace metals on embryos of the giant clam, Tridacna derasa. Asian Mar. Biol. 7, 161–166. Sousa, A., Matsudaira, C., Takahashi, S., Tanabe, S., Barroso, C., 2007. Integrative assessment of organotin contamination in a southern European estuarine system (Ria de Aveiro, NW Portugal): tracking temporal trends in order to evaluate the effectiveness of the EU ban. Mar. Pollut. Bull. 54, 1645–1653. Sparling, D.W., Lowe, T.P., 1996. Environmental hazards of aluminum to plants, invertebrates, fish, and wildlife. Rev. Environ. Contam. Toxicol. 145, 1–127. Sprague, J.B., 1986. Toxicity and Tissue Concentrations of Lead, Zinc, and Cadmium for Marine Molluscs and Crustaceans. Available from International Lead Zinc Research Organization, 2525 Meridian Parkway, Research Triangle Park, NC215. Stenner, R.D., Nickless, G., 1974a. Absorption of cadmium, copper and zinc by dog whelks in the Bristol Channel. Nature 247, 198–199. Stenner, R.D., Nickless, G., 1974b. Distribution of some heavy metals in organisms in Hardangerfjord and Skjerstadfjord, Norway. Water Air Soil Pollut. 3, 279–291. Stenner, R.D., Nickless, G., 1975. Heavy metals in organisms of the Atlantic coast of S.W. Spain and Portugal. Mar. Pollut. Bull. 6, 89–92. Stephenson, J.D., Leonard, G.H., 1994. Evidence for the decline of silver and lead and the increase of copper from 1977 to 1990 in the coastal marine waters of California. Mar. Pollut. Bull. 28, 148–153. Stephenson, R.F., Taylor, D., 1975. The influence of EDTA on the mortality and burrowing activity of the clam (Venerupis decussata) exposed to sublethal concentrations of copper. Bull. Environ. Contam. Toxicol. 14, 304–308. Stewart, J., Schulz-Baldes, M., 1976. Long term lead accumulation in abalone (Haliotis spp.) fed on lead-treated brown algae (Egregia laevigata). Mar. Biol. 36, 19–24. Stromgren, T., Nielsen, M.V., 1991. Spawning frequency, growth and mortality of Mytilus edulis larvae exposed to copper and diesel oil. Aquat. Toxicol. 21, 171–180. Stronkhorst, J., 1992. Trends in pollutants in blue mussel Mytilus edulis and flounder Platichthys flesus from two Dutch estuaries, 1985-1990. Mar. Pollut. Bull. 24, 250–258. Stump, I.G., Kearney, J., D’Auria, J.M., Popham, J.D., 1979. Monitoring trace elements in the mussel, Mytilus edulis, using X-ray energy spectroscopy. Mar. Pollut. Bull. 10, 270–274. Sturesson, U., 1976. Lead enrichment in shells of Mytilus edulis. Ambio 5, 235–236. Sturesson, U., 1978. Cadmium enrichment in shells of Mytilus edulis. Ambio 7, 122–125. Sturesson, U., Reyment, R.A., 1971. Some minor chemical constituents of the shell of Macoma balthica. Oikos 22, 414–416. Sullivan, P.A., Robinson, W.E., Morse, M.P., 1988. Isolation and characterization of granules from the kidney of the bivalve Mercenaria mercenaria. Mar. Biol. 99, 359–368. Sunlu, U., 2006. Trace metal levels in mussels (Mytilus galloprovincialis L. 1758) from Turkish Aegean sea coast. Environ. Monit. Assess. 114, 273–286. Swaileh, K.M., Adelung, D., 1994. Levels of trace metals and effect of body size on metal content and concentration in Arctica islandica L. (Mollusca: Bivalvia) from Kiel Bay, western Baltic. Mar. Pollut. Bull. 28, 500–505.
392 Chapter 6 Szefer, P., Fowler, S.W., Ikuta, K., Osuna, F.P., Ali, A.A., Kim, B.S., et al., 2006. A comparative assessment of heavy metal accumulation in soft parts and byssus of mussels from subarctic, temperate, and subtropical and tropical marine environments. Environ. Pollut. 139, 70–78. Tabata, K., 1969. Studies on the toxicity of heavy metals to aquatic animals and the factors to decrease the toxicity—I. On the formation and the toxicity of precipitate of heavy metals. Bull. Tokai Fish. Res. Lab. Tokyo 58, 203–214. Takevich, T., 1972. Distribution of mercury in the environment of Minamata Bay and inland Ariake Sea. In: Hartung, B.D., Dinman, B.D. (Eds.), Environmental Mercury Contamination. Ann Arbor Science Publications, Ann Arbor, MI, pp. 79–81. Talbot, V., 1985. Heavy metal concentrations in the oysters Saccostrea cucullata and Saccostrea sp. From the Dampier Archipelago, Western Australia. Aust. J. Mar. Freshw. Res. 36, 169–175. Talbot, V., Magee, R.J., 1978. Naturally occurring heavy metal binding proteins in invertebrates. Arch. Environ. Contam. Toxicol. 7, 73–81. Talbot, V., Magee, R.J., Hussain, M., 1976a. Lead in Port Phillip Bay mussels. Mar. Pollut. Bull. 7, 234–237. Talbot, V.W., Magee, R.J., Hussain, M., 1976b. Cadmium in Port Phillip Bay mussels. Mar. Pollut. Bull. 7, 84–86. Talbot, V., Creagh, S., Schulz, R., 1985. The derivation of threshold mean concentrations of copper and zinc in seawater, to protect the edible tropical rock oyster Saccostrea cucullata, from exceeding the health (food) standards. Dept. Conserv. Environ. Perth, West. Aust. Bull. 12, 1–25. Tedesco, S., Doyle, H., Redmond, G., Sheehan, D., 2008. Gold nanoparticles and oxidative stress in Mytilus edulis. Mar. Environ. Res. 66, 131–133. Thain, J.E., Waldock, M.J., 1986. The impact of tributyl tin (TBT) antifouling paints on molluscan fisheries. Water Sci. Technol. 18, 193–202. Thebault, H., Rodriguez y Baena, A.M., Andral, B., Barisic, D., Albaladejo, J.B., Bologa, A.S., et al., 2008. 137Cs baseline levels in the Mediterranean and Black Sea: a cross-basin survey of the CIESM Mediterranean Mussel Watch programme. Mar. Pollut. Bull. 57, 801–806. Thibaud, J., 1973. Teneur en mercure dans les moules du littoral francais. Sci. Peche Bull. Inst. Peches Marit. 221, 1–6. Thompson, T.G., Chow, T.J., 1955. The strontium-calcium atom ratio in carbonate-secreting marine organisms. Deep Sea Res. 3 (Suppl.), 20–39. Thompson, J.A.J., Davis, J.C., Drew, R.E., 1976. Toxicity, uptake and survey studies of boron in the marine environment. Water Res. 10, 869–875. Thompson, J.A.J., Sheffer, M.G., Pierce, R.C., Chau, Y.K., Cooney, J.J., Cullen, W.R., et al., 1985. Organotin compounds in the aquatic environment: scientific criteria fo assessing their effects on environmental quality. Natl. Res. Coun. Can.. Publ. NRCC 22494, pp. 1–284. Thomson, J.D., 1979. Heavy metals in the native oyster (Ostrea angasi) and mussel (Mytilus edulis planulatus) from Port Davey, south-western Tasmania. Aust. J. Mar. Freshw. Res. 30, 421–424. Thornton, I., Watling, H., Darracott, A., 1975. Biochemical studies in several rivers and estuaries used for oyster rearing. Sci. Total Environ. 4, 325–345. Thorsson, M.H., Hedman, J.E., Bradshaw, C., Gunnarsson, J.S., Gilek, M., 2008. Effects of settling organic matter on the bioaccumulation of cadmium and BDE-99 by Baltic Sea invertebrates. Mar. Environ. Res. 65, 264–281. Thrower, S.J., Eustace, I.J., 1973a. Heavy metal accumulation in oysters grown in Tasmanian waters. Food Tech. Aust. 25, 546–553. Thrower, S.J., Eustace, I.J., 1973b. Heavy metals in Tasmanian oysters in 1972. Aust. Fish. 32 (Oct. 1973), 7–10. Thurberg, F.P., Calabrese, A., Dawson, M.A., 1974. Effects of silver on oxygen consumption of bivalves at various salinities. In: Vernberg, F.J., Vernberg, W.B. (Eds.), Pollution and Physiology of Marine Organisms. Academic Press, New York, pp. 67–78. Thurberg, F.P., Cable, W.D., Dawson, M.A., MacInnes, J.R., Wenzloff, D.R., 1975. Respiratory response of larval, juvenile and adult surf clams, Spisula solidissima, to silver. In: Cech Jr., J.J., Bridges, D.W., Horton, D.B. (Eds.), Respiration of Marine Organisms. TRIGOM Publications, South Portland, ME, pp. 41–52.
Molluscs 393 Topping, G., 1973. Heavy metals in shellfish from Scottish waters. Aquaculture 1, 379–384. Townsley, S.J., 1954. Studies on copper in mollusks, with particular reference to Busycon canaliculatum Linnaeus. Ph.D. thesis, Yale University, New Haven, CT, 126 pp. Tran, D., Moody, A.J., Fisher, A.S., Foulkes, M.E., Jha, A.N., 2007. Protective effects of selenium on mercuryinduced DNA damage in mussel haemocytes. Aquat. Toxicol. 84, 11–18. Truchet, M., Martoja, R., Berthet, B., 1990. Consequences histologiques de la pollution metallique d’un estuaire sur deux mollusques, Littorina littorea L. et Scrobicularia plana da costa. C. R. Acad. Sci. Ser. III 311, 261–268. Tsubaki, T., Sato, T., Kondo, K., Shirakawa, K., Kanbayashi, K., Hirota, K., et al., 1967. Outbreak of intoxication by organic mercury compound in Niigata Prefecture. An epidemiological and clinical study. Jpn. J. Med. 6, 132–133. Tugrul, S., Balkas, T.I., Goldberg, E.D., 1983. Methyltins in the marine environment. Mar. Pollut. Bull. 14, 297–303. Turgeon, D.D., O’Connor, T.P., 1991. Long Island Sound: distributions, trends, and effects of chemical contamination. Estuaries 14, 279–289. Turekian, K.K., Armstrong, R.L., 1960. Magnesium, strontium, and barium concentrations and calcite-aragonite ratios of some recent molluscan shells. J. Mar. Res. 18, 133–151. Turekian, K.K., Katz, A., Chan, L., 1973. Trace element trapping in pteropod tests. Limnol. Oceanogr. 18, 240–249. Ueda, T., Nakamura, R., Suzuki, Y., 1978. Comparison of influences of sediments and sea water on accumulation of radionuclides by marine organisms. J. Radiat. Res. 19, 93–99. Unlu, M.Y., Fowler, S.W., 1979. Factors affecting the flux of arsenic through the mussel Mytilus galloprovincialis. Mar. Biol. 51, 209–219. Unlu, M.Y., Heyraud, M., Keckes, S., 1972. Mercury as a hydrospheric pollutant. I. Accumulation and excretion of 203HgCl2 in Tapes decussata L. In: Ruivo, M. (Ed.), Marine Pollution and Sea Life. Fishing Trading News (Books), London, pp. 292–295. Unlu, S., Topcuoglu, S., Alpar, B., Kurbasoglu, C., Yilmaz, Z.Y., 2008. Heavy metal pollution in surface sediment and mussel samples in the Gulf of Gemlik. Environ. Monit. Assess. 144, 169–178. US Environmental Protection Agency (USEPA), 1977. Fed. Regist. 42(7), 2477. USEPA, 1980a. Ambient water quality criteria for chromium. USEPA, Rep. 440/5-80-035, pp. 1–105. USEPA, 1980b. Ambient water quality criteria for copper. USEPA, Rep. 440/5-80-036, pp. 1–162. USEPA, 1980c. Ambient water quality criteria for nickel. USEPA, Rep. 440/5-80-060, pp. 1–206. USEPA, 1980d. Ambient water quality criteria for zinc. USEPA, Rep. 440/5-80-079, pp. 1–158. USEPA, 1985a. Ambient water quality criteria for arsenic—1984. USEPA, Rep. 440/5-84-033, pp. 1–66. USEPA, 1985b. Ambient water quality criteria for lead—1984. USEPA, Rep. 440/5-84-027, pp. 1–81. USEPA, 1986. Initiation of a special review of certain pesticide products containing tributyltins used as antifoulants; availability of support document. Fed. Regist. 51(5), 778–779. USEPA, 1987. Ambient water quality criteria for zinc—1987. USEPA, Rep. 440/5-87-003, pp. 1–207. US National Academy of Sciences (USNAS), 1973. Water Quality Criteria, 1972. US Environ. Protect. Agen. Rep. R3-73–033, 252 pp. USNAS, 1975. Medical and Biological Effects of Environmental Pollutants. Nickel. Nat. Res. Coun., USNAS, Washington, DC, 277 pp. USNAS, 1977. Arsenic. USNAS, Washington, DC , 332 pp. USNAS, 1979. Zinc. USNAS, Natl. Res. Coun., Subcomm. Zinc., Univ. Park Press, Baltimore, MD, 471 pp. US Navy (USN), 1984. Environmental Assessment of Fleetwide Use of Organotin Antifouling Paint. US Naval Sea Systems Command, Washington, DC, 184 pp. US Public Health Service (USPHS), 1962. Drinking water standards. USPHS, Publ. 956, pp. 1–61. USPHS, 1990. Toxicological profile for silver. Agen. Toxic Subs. Dis. Reg. TP-90-24, pp. 1–145. USPHS, 1992. Toxicological profile for tin. Agen. Toxic Subs. Dis. Reg. TP-91/27, pp. 1–160. Uysal, H., 1978a. The effects of some pollutants on Mytilus galloprovincialis Lam. and Paracentrotus lividus Lam. in the Bays of Izmir and Aliaga. IVes J. Etud. Pollut. 313–317.
394 Chapter 6 Uysal, H., 1978b. Accumulation and distribution of heavy metals in some marine organisms in the bay of Izmir and on Aegean coasts. IV.esJ. Etud. Pollut. 213–217. Valiela, I., Banus, M.D., Teal, J.M., 1974. Response of salt marsh bivalves to enrichment with metal-containing sewage sludge and retention of lead, zinc and cadmium by marsh sediments. Environ. Pollut. 7, 149–157. Valkirs, A.O., Davidson, B.M., Seligman, P.F., 1987. Sublethal growth effects and mortality to marine bivalves from long-term exposure to tributyltin. Chemosphere 16, 201–220. Van As, D., Fourie, H.O., Vleggaar, C.M., 1973. Accumulation of certain trace elements in the marine organisms from the sea around the Cape of Good Hope. Radioactive Contamination of the Marine Environment. IAEA, Vienna, Austria. Van As, D., Fourie, H.O., Vleggaar, C.M., 1975. Trace element concentrations in marine organisms from the Cape West Coast. S. Afr. J. Sci. 71, 151–154. van Slooten, K.B., Tarradellas, J., 1994. Accumulation, depuration and growth effects of tributyltin in freshwater bivalve Dreissena polymorpha under field conditions. Environ. Toxicol. Chem. 13, 755–762. Van Weers, A.W., 1973. Uptake and loss of 65Zn and 60Co by the mussel Mytilus edulis L. In: Radioactive Contamination of the Marine Environment. IAEA, Vienna, Austria, pp. 401–853. Vaskovsky, V.E., Korotchenko, O.D., Kosheleva, L.R., Levin, V.S., 1972. Arsenic in the lipid extracts of marine invertebrates. Comp. Biochem. Physiol. 41B(4), 777–784. Vattuone, G.M., Griggs, K.S., McIntyre, D.R., Littlepage, J.L., Harrison, F.L., 1976. Cadmium concentrations in rock scallops in comparison with some other species. US Ener. Res. Dev. Admin., UCRL 52022, pp. 1–11. Vecchio, P.V., Alasia, A.M., Gualdi, G., 1962. Determination of arsenic in molluscs (Mytilus Linn.). Ig. Sanita Pubbl. 18, 18–30. Viarengo, A., Pertica, M., Mancinelli, G., Palermo, S., Zanicchi, G., Orunesu, M., 1981. Synthesis of Cu-binding proteins in different tissues of mussels exposed to the metal. Mar. Pollut. Bull. 12, 347–350. Viarengo, A., Canesi, L., Pertica, M., Poli, G., Moore, M.N., Orunesu, M., 1990. Heavy metal effects on lipid peroxidation in the tissues of Mytilus galloprovincialis Lam. Comp. Biochem. Physiol. 97C, 37–42. Viarengo, A., Canesi, L., Mazzucotelli, A., Ponzano, E., 1993. Cu, Zn and Cd content in different tissues of the Antarctic scallop Adamussium colbecki: role of metallothionein in heavy metal homeostasis and detoxication. Mar. Ecol. Prog. Ser. 95, 163–168. Vijayavel, K., Gopalakrishnan, S., Balasubramanian, M.P., 2007. Sublethal effects of silver and chromium in the green mussel Perna viridis with reference to alterations in oxygen uptake, filtration rate and membrane bound ATPase system as biomarkers. Chemosphere 69, 979–986. Vishwakiran, Y., Anil, A.C., Venkat, K., Sawant, S.S., 2006. Gyrineum natator: a potential indicator of imposex along the Indian coast. Chemosphere 62, 1718–1725. Vlahogianni, T., Dassenakis, M., Scoullos, M.J., Valavanidis, A., 2007. Integrated use of biomarkers (superoxide dismutase, catalase, and lipid peroxidation) in mussels Mytilus galloprovincialis for assessing heavy metals’ pollution in coastal areas from the Saronikos Gulf of Greece. Mar. Pollut. Bull. 54, 1361–1371. Vos, G., Hovens, J.P.C., 1986. Chromium, nickel, copper, zinc, arsenic, selenium, cadmium, mercury and lead in Dutch fishery products 1977-1984. Sci. Total Environ. 52, 25–40. Vosjan, J.H., Van der Hoek, G.J., 1972. A continuous culture of Desulfovibrio on a medium containing mercury and copper ions. Neth. J. Sea Res. 5, 440–444. Vucetic, T., Vernberg, W.B., Anderson, G., 1974. Long-term annual fluctuations of mercury in zooplankton of the east central Adriatic. Rev. Int. Oceanogr. Med. 33, 75–81. Waldock, M.J., Thain, J.E., 1983. Shell thickening in Crassostrea gigas: organotin antifouling or sediment induced? Mar. Pollut. Bull. 14, 411–415. Waldock, R., Rees, H.I., Matthiessen, P., Pendle, M.A., 1999. Surveys of the benthic infauna of the Crouch Estuary (UK) in relation TBT contamination. J. Mar. Biol. Assoc. UK 79, 225–232. Walsh, A.R., O’Halloran, J., 1998. Accumulation of chromium by a population of mussels (Mytilus edulis (L.)) exposed to leather tannery effluent. Environ. Toxicol. Chem. 17, 1429–1438. Walsh, G.E., McLaughlin, L.L., Lores, E.M., Louie, M.K., Deans, C.H., 1985. Effects of organotins on growth and survival of two marine diatoms, Skeletonema costatum and Thalassiosira pseudonana. Chemosphere 14, 383–389.
Molluscs 395 Wang, W.X., Fisher, N.S., Luoma, S.N., 1996. Kinetic determinations of trace element bioaccumulation in the mussel Mytilus edulis. Mar. Ecol. Prog. Ser. 140, 91–113. Ward, R.E., 1990. Metal concentrations and digestive gland lysomal stability in mussels from Halifax inlet, Canada. Mar. Pollut. Bull. 21, 237–240. Ward, T.J., Correll, R.I., Anderson, R.B., 1986. Distribution of cadmium, lead and zinc amongst the marine sediments, sea grasses and fauna, and the selection of sentinel accumulators, near a lead smelter in South Australia. Aust. J. Mar. Freshw. Res. 37, 567–585. Waska, H., Kim, S., Kim, G., Kang, M.R., Kim, G.B., 2008. Distribution patterns of chalcogens (S, Se, Te, and 210 Po) in various tissues of the squid, Todarodes pacificus. Sci. Total Environ. 392, 218–224. Watkins, B., Simkiss, K., 1988. The effect of oscillating temperatures on the metal ion metabolism of Mytilus edulis. J. Mar. Biol. Assoc. UK 68, 93–100. Watling, H.R., Watling, R.J., 1976a. Trace metals in oysters from Knysna Estuary. Mar. Pollut. Bull. 7, 45–48. Watling, H.R., Watling, R.J., 1976b. Trace metals in Choromytilus meridionalis. Mar. Pollut. Bull. 7, 91–94. Webb, J., Macey, D.J., Talbot, V., 1985. Identification of ferritin as a major high molecular weight zinc-binding protein in the tropical rock oyster, Saccostrea cucullata. Arch. Environ. Contam. Toxicol. 14, 403–407. Weis, J.S., Weis, P., 1992. Transfer of contaminants from CCA-treated lumber to aquatic biota. J. Exp. Mar. Biol. Ecol. 168, 25–34. Weis, J.S., Weis, P., 1993. Trophic transfer of contaminants form organisms living by chromated-copper-arsenate (CCA) wood to their predators. J. Exp. Mar. Biol. Ecol. 168, 25–34. Weis, J.S., Weis, P., 1994. Effects of contaminants from chromated copper arsenate-treated lumber on benthos. Arch. Environ. Contam. Toxicol. 26, 103–109. Weis, P., Weis, J.S., Couch, J., 1993a. Histopathology and bioaccumulation in oysters Crassostrea virginica living on wood preserved with chromated copper arsenate. Dis. Aquat. Org. 17, 41–46. Weis, P., Weis, J.S., Lores, E., 1993b. Uptake of metals from chromated-copper-arsenate (CCA)-treated lumber by epibiota. Mar. Pollut. Bull. 26, 428–430. Weiss, H.V., Shipman, W.H., 1957. Biological concentration by killer clams of cobalt-60 from radioactive fallout. Science 125, 695. Wepener, V., Bervoets, L., Mubiana, V., Blust, R., 2008. Metal exposure and biological responses in resident and transplanted blue mussels (Mytilus edulis) from the Scheldt estuary. Mar. Pollut. Bull. 57, 624–631. Westernhagen, H.V., Dethlefsen, V., Rosenthal, H., Furstenberg, G., Klinckmann, J., 1978. Fate and effects of cadmium in an experimental marine ecosystem. Helg. Wiss. Meer. 31, 471–484. Wharfe, J.R., Van Den Broek, W.L.F., 1977. Heavy metals in macroinvertebrates and fish from the Lower Medway Estuary, Kent. Mar. Pollut. Bull. 8, 31–34. White, S.L., Rainbow, P.S., 1985. On the metabolic requirements for copper and zinc in molluscs and crustaceans. Mar. Environ. Res. 16, 215–229. White, D.H., Stendell, R.C., Mulhern, B.M., 1979. Relations of wintering canvasbacks to environmental pollutants—Chesapeake Bay, Maryland. Wilson Bull. 91, 279–287. Whitehead, N.E., Ballestra, S., Holm, E., Huynh-Ngoc, L., 1988. Chernobyl radionuclides in shellfish. J. Environ. Radioact. 7, 107–121. Widmeyer, J.R., Bendell-Young, L.I., 2007. Influence of food quality and salinity on dietary cadmium availability in Mytilus trossulus. Aquat. Toxicol. 81, 144–151. Williams, P.M., Weiss, H.V., 1973. Mercury in the marine environment: concentration in sea water and in a pelagic food chain. J. Fish. Res. Board Can. 30, 293–295. Williams, R.J., Mackay, N.J., Collett, L.C., Kacprzak, J.L., 1976. Total mercury concentration in some fish and shellfish from NSW estuaries. Food Technol. Aust. 18, 8–10. Windom, H.L., Smith, R.G., 1972. Distribution of iron, magnesium, copper, zinc, and silver in oysters along the Georgia coast. J. Fish. Res. Board Can. 29, 450–452. Windom, H.L., Gardner, W.S., Dunstan, W.M., Paffenhofer, G.A., 1976. Cadmium and mercury transfer in a coastal marine ecosystem. In: Windom, H.L., Duce, R.A. (Eds.), Marine Pollutant Transfer. D.C. Heath, Lexington, MA, pp. 135–137.
396 Chapter 6 Wolfe, D.A., 1970. Fallout cesium-137 in clams (Rangia cuneata) from the Neuse River Estuary, North Carolina. Limnol. Oceanogr. 16, 797–805. Wolfe, D.A., Coburn Jr., C.B., 1970. Influence of salinity and temperature on the accumulation of cesium-137 by an estuarine clam under laboratory conditions. Health Phys. 18, 499–505. Wolfe, D.A., Jennings, C.D., 1973. Iron-55 and ruthenium-103 and 106 in the brackish-water clam Rangia cuneata. In: Nelson, D.J. (Ed.), Radionuclides in Ecosystems: Proceedings of the 3rd National Symposium on Radioecology, vol. 2. US Atom. Ener. Comm, pp. 783–790. Won, J.H., 1973. The concentrations of mercury, cadmium, lead and copper in fish and shellfish of Korea. Bull. Korean Fish. Soc. 6, 1–19. Wood, J.M., 1973. Metabolic cycles for toxic elements in aqueous systems. In: Sixth International Symposium, Med. Ocean., Portoroz, Yugoslavia, September 26-30, 1973, pp. 7–16. Wrench, J.J., 1978. Biochemical correlates of dissolved mercury uptake by the oyster Ostrea edulis. Mar. Biol. 47, 79–86. Yang, R., Zhou, Q., Jiang, G., 2006. Butyltin accumulation in the marine clam Mya arenaria: and evaluation of its suitability for monitoring butyltin pollution. Chemosphere 63, 1–8. Yannai, S., Sachs, K., 1978. Mercury compounds in some eastern Mediterranean fishes, invertebrates, and their habitats. Environ. Res. 16, 408–418. Yantian, L., 1989. Effect of zinc on the growth and development of larvae of the bay scallop Argopecten irradians. Chin. J. Oceanol. Limnol. 7, 318–326. Yarsan, E., Baskaya, R., Yildiz, A., Altintas, L., Yesilot, S., 2007. Copper, lead, cadmium and mercury concentrations in the mussel Elliptio. Bull. Environ. Contam. Toxicol. 79, 218–220. Young, M.L., 1975. The transfer of 65Zn and 59Fe along a Fucus serratus (L.)—Littorina obtusata (L.) food chain. J. Mar. Biol. Assoc. UK 55, 583–610. Young, M.L., 1977. The roles of food and direct uptake from water in the accumulation of zinc and iron in the tissues of the dogwhelk Nucella lapillus (L.). J. Exp. Mar. Biol. Ecol. 30, 315–325. Young, D.R., Folsom, T.R., 1967. Loss of zinc-65 from the California sea mussel. Mytilus californianus. Biol. Bull. 133, 438–447. Young, D.R., Folsom, T.R., 1973. Mussels and barnacles as indicators of the variation of 54Mn, 60Co and 65Zn in the marine environment. In: Radioactive Contamination of the Marine Environment. IAEA, Vienna, Austria, pp. 633–650. Young, D.R., Jan, T.K., 1976. Metals in scallops. In: 1976 Annual Report of Southern California Coastal Water Research Projecct, El Segundo, CA, pp. 117–121. Young, D.R., McDermott, D.J., 1975. Trace metals in harbor mussels. In: Annual Report of Southern California Coastal Water Research Project, June 30, El Segundo, CA, pp. 139–142. Young, D.R., Alexander, G.V., McDermott-Ehrlich, D., 1979. Vessel-related contamination of southern California harbours by copper and other metals. Mar. Pollut. Bull. 10, 50–56. Young, D.R., Jan, T.K., Hershelman, G.P., 1980. Cycling of zinc in the nearshore marine environment. In: Nriagu, J.O. (Ed.), Zinc in the Environment. Part 1: Ecological Cycling. Wiley, New York, pp. 297–355. Zaroogian, G.E., 1979. Studies on the depuration of cadmium and copper by the American oyster, Crassostrea virginica. Bull. Environ. Contam. Toxicol. 23, 117–122. Zaroogian, G.E., Cheer, S., 1976. Cadmium accumulation by the American oyster, Crassostrea virginica. Nature 261, 408–410. Zaroogian, G.E., Hoffman, G.L., 1982. Arsenic uptake and loss in the American oyster, Crassostrea virginica. Environ. Monit. Assess. 1, 345–358. Zaroogian, G.E., Johnson, M., 1983. Chromium uptake and loss in the bivalves Crassostrea virginica and Mytilus edulis. Mar. Ecol. Prog. Ser. 12, 167–173. Zaroogian, G.E., Morrison, G., Heltshe, J.F., 1979. Crassostrea virginica as an indicator of lead pollution. Mar. Biol. 52, 189–196. Zaroogian, G., Anderson, S., Voyer, R.A., 1992. Individual and combined cytotoxic effects of cadmium, copper, and nickel on brown cells of Mercenaria mercenaria. Ecotoxicol. Environ. Safety 24, 328–337.
Molluscs 397 Zauke, G.P., 1977. Mercury in benthic invertebrates of the Elbe estuary. Helg. Wiss. Meer. 29, 358–374. Zesenko, A.Y., Polikarpov, G.G., 1965. Coefficients of accumulation and distribution of ruthenium-106 in organs and tissues of sea molluscs. Radiobiologiya 5, 320–322. Zingde, M.D., Singbal, S.Y.S., Moraes, C.F., Reddy, C.V.G., 1976. Arsenic, copper, zinc & manganese in the marine flora & fauna of coastal & estuarine waters around Goa. Indian J. Mar. Sci. 5, 212–217. Zitko, V., Carson, W.V., 1975. Accumulation of thallium in clams and mussels. Bull. Environ. Contam. Toxicol. 14, 530–533. Zorita, I., Apraiz, I., Ortiz-Zarragoitia, M., Orbea, A., Cancio, I., Soto, M., et al., 2007. Assessment of biological effects of environmental pollution along the NW Mediterranean Sea using mussels as sentinel organisms. Environ. Pollut. 148, 236–250.
This page intentionally left blank
CHAPTER 7
Crustaceans Crustaceans are aquatic arthropods which typically respire by gills and possess two pairs of antennae, three pairs of primary mouth parts, and numerous appendages on thorax and abdomen. This is an unusually diverse and widespread group that includes marine species of major economic importance—such as lobsters, shrimps, and crabs—as well as isopods, copepods, barnacles, and euphausiids. It is probable that all marine biological communities contain significant crustacean biomass and diversity, with representative species present as predators, parasites, and grazers, or as intermediary links in the food chain. Trace metal concentrations in crustaceans are comparatively well documented; however, the process of ecdysis, including the frequency of molting, is a major confounder of trace metal residue interpretation, especially among decapods.
7.1 Aluminum Aluminum concentrations in whole crustaceans were variable and ranged—on a mg Al/kg dry weight (DW) basis—from 7.3 to 11,200.0, being highest in copepods from a Taiwanese sewage outfall (Table 7.1).
7.2 Antimony Antimony values in crustacean tissues—on a fresh weight (FW) basis—did not exceed 2.0 mg Sb/kg (Table 7.2). Antimony is taken up from uncontaminated seawater: muscle of the lobster Jasus lalandi contained 170 times more antimony than the ambient medium (Van As et al., 1973). Antimony flux in the Mediterranean Sea due to fecal pellet deposition of euphausiids is substantial and equivalent to about 9.2 mg Sb/kg fecal pellets daily (Fowler, 1977). At present, there are no known health hazards associated with antimony accumulations and cycling rates via marine vectors.
7.3 Arsenic Arsenic concentrations in tissues of marine biota—including crustaceans—show a wide range of values, being highest in lipids, liver, and muscle tissues, and varying with the age of the organisms, geographic locale, and proximity to anthropogenic activities (Eisler, 2000a; 399
400 Chapter 7 Table 7.1: Aluminum Concentrations in Field Collections of Crustaceans Organism
Concentration
Reference
Copepods Whole Whole Whole; 3 spp.; Taiwan; near sewage outfall
70.0 DW 55.0 DW 2100.0-11,200.0 DW
2 3 6
Blue crab, Callinectes sapidus; muscle; Iskenderun Bay, Turkey; August 2005
7.3 (1.2-17.6) DW
5
Crustaceans; whole; Irish Sea
(166.0-1041.0) DW
4
Euphausiids; whole
31.0 DW
2
Crab, Seserma cinerum; whole; south Chesapeake Bay, Maryland
1847.0 DW
1
Crab, Pachygrapsus sp.; whole; San Francisco Bay, California
1965.0 DW
1
a
Values are in mg Al/kg dry weight (DW). a 1, Sparling and Lowe, 1996; 2, Martin and Knauer, 1973; 3, Tijoe et al., 1977; 4, Culkin and Riley, 1958; 5, Turkmen et al., 2006; 6, Feng et al., 2006.
Table 7.3). Arsenic appears to be elevated in marine biota mainly owing to their ability to accumulate and retain arsenic from seawater or food sources, and not from localized pollution (Maher, 1985). The great majority of arsenic in marine organisms exists as watersoluble and lipid-soluble organoarsenicals that include arsenolipids, arsenosugars, arsenocholine, arsenobetaine [(CH3)AsCH2COOH], monomethylarsonate [CH3AsO(OH)2], and dimethylarsinate [(CH3)2AsO(OH)], as well as other forms (Edmonds et al., 1993). There is no convincing hypothesis to account for the existence of the various forms of organoarsenicals found in marine organisms. One suggested hypothesis is that each form involves a single anabolic/catabolic pathway concerned with the synthesis and turnover of phosphatidylcholine (Phillips and Depledge, 1986). Arsenosugars (arsenobetaine precursors) are the dominant arsenic species in brown kelp (Ecklonia radiata), giant clam (Tridacna maxima), shrimp (Pandalus borealis), and ivory shell (Buccinum striatissimum) (Francesconi et al., 1985; Matsuto et al., 1986; Phillips and Depledge, 1986; Shiomi et al., 1984a,b). For most marine species, however, there is general agreement that arsenic exists primarily as arsenobetaine, a water-soluble organoarsenical that has been identified in tissues of western rock lobster (Panulirus cygnus), American lobster (Homarus americanus), octopus (Paraoctopus sp.), sea cucumber (Stichopus japonicus), blue shark (Prionace glauca), sole (Limanda sp.), squid (Sepioteuthis australis), prawn (Penaeus latisulcatus), scallop (Pecten alba), and many other species, including teleosts, molluscs, tunicates, and crustaceans (Edmonds et al., 1993; Francesconi et al., 1985; Hanaoka and Tagawa, 1985a,b; Kaise and
Crustaceans 401 Table 7.2: Antimony Concentrations in Field Collections of Crustaceans Organism
Concentration
Reference
Copepods; whole
0.027 DW
1
Crustaceans; 16 economically important species; edible tissues 2 spp. 1 spp. 3 spp. 7 spp. 3 spp.
0.2-0.3 FW 0.7-0.8 FW 0.8-0.9 FW 0.9-1.0 FW 1.0-2.0 FW
2 2 2 2 2
Euphausiids; whole
1.9 AW
3
Lobster, Jasus lalandi; muscle
(0.12-0.14) FW
7,8
Euphausiid, Meganyctiphanes norvegicus Whole Molts Whole
<4.5 DW 0.8 DW 0.037 DW
4 4 5
Shrimp, Palaemon elegans; whole
0.016 DW
6
Amphipod, Paramoera walkeri; East Antarctica; 2003-2004; whole
(0.03-0.10) DW
10
Black tiger shrimp, Penaeus monodon; Vietnam; 2003-2005; max. values Muscle Exoskeleton Hepatopancreas
0.02 DW 0.04 DW 0.07 DW
11 11 11
Shrimps; coast of Belgium Proteinaceous molts Remainder
0.03 DW 0.15 DW
9 9
a
Values are in mg Sb/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Tijoe et al., 1977; 2, Hall et al., 1978; 3, Robertson, 1967; 4, Fowler, 1977; 5, Leatherland et al., 1973; 6, Leatherland and Burton, 1974; 7, Van As et al., 1973; 8, Van As et al., 1975; 9, Bertine and Goldberg, 1972; 10, Palmer et al., 2006; 11, Tu et al., 2008.
Fukui, 1992; Maher, 1985; Matsuto et al., 1986; Norin et al., 1985; Ozretic et al., 1990; Phillips, 1990; Shiomi et al., 1984b). The potential risks associated with consumption of seafoods containing arsenobetaine seems to be minor (Eisler, 2000a). Decapod crustaceans contained relatively high concentrations of arsenic; concentrations varied widely, but usually ranged from 1.0 to 100.0 mg kg on a DW basis (Fowler and Unlu, 1978). Edible tissues of crustaceans from coastal waters of the United States usually contained 3.0-10.0 mg As/kg FW (Table 7.3); these values were elevated when compared to
402 Chapter 7 Table 7.3: Arsenic Concentrations in Field Collections of Crustaceans Organism
Concentration
Amphipods; whole
7.9 DW
1
0.6 DW 0.36 (0.20-0.88) FW; 1.8 (1.0-4.4) DW 7.7 FW (0.5-1.8) FW
2 3 28 28
Max. 9.6 FW Max. 8.3 FW
31 31
Blue crab, Callinectes sapidus Whole Whole Whole; Florida Soft parts; Maryland Pensacola, Florida; 2003-2004 Hepatopancreas Muscle
Reference
Crab, Cancer irroratus Muscle Gills
1.9 FW (0.57-0.87) FW
Dungeness, crab, Cancer magister Soft parts Muscle
37.8 FW 4.0 FW
5 5 22
7.4 FW
22
Alaskan snow crab, Chinocetes bairdi; muscle Copepods Whole Whole Whole Whole Whole Crabs Muscle; total arsenic vs. inorganic arsenic Muscle
4 4
0.88 (0.42-1.25) FW; 4.2 (2.0-6.0) DW 1.4 FW 5.6 DW 6.0 DW 8.2 DW
3
3.7 FW vs. < 0.5 FW
9
6 1 7 8
(6.1-6.4) FW
10
Sand shrimp, Crangon crangon; Netherlands; 1977-1984; muscle
3.0 (2.0-6.8) FW
23
Crustaceans; whole; 4 species; lipid extracts
7300.0-24,400.0 FW
11
3.0-5.0 FW 5.0-10.0 FW 10.0-20.0 FW
12 12 12
Crustaceans; economically important species; edible tissues; North America 6 spp. 3 spp. 4 spp.
a
(Continues)
Crustaceans 403 Table 7.3:
Cont’d
Organism
Concentration
Reference
2 spp. 1 spp. 9 spp.
20.0-30.0 FW 40.0-50.0 FW 5.6-220.2 DW
12 12 13
Crustaceans; edible tissues; Hong Kong; 1976-1978 Crabs Lobsters Prawns and shrimps
(5.4-19.1) FW (26.7-52.8) FW (1.2-44.0) FW
24 24 24
Euphausiids; whole
1.8 FW
6
Gammarids; whole
6.6 FW
6
Mantis shrimp, Gonodactylus sp; Guam; June 1998; muscle vs. gonad
5.06 DW vs. 4.58 DW
29
Lobster, Homarus americanus Muscle Hepatopancreas Whole Whole
(3.8-7.6) DW 22.5 FW (3.8-7.5) DW (0.95-3.00) FW; (5.0-16.0) DW
28 28 14 3
Lobster; total arsenic vs. inorganic arsenic Tail Hepatopancreas
40.5 FW vs. < 0.5 FW 22.5 FW vs. 0.9 FW
Euphausiid, Meganyctiphanes norvegica Whole Whole
42.0 DW (1.9-5.5) FW
16 3
Stone crab, Menippe mercenaria; whole
(9.0-11.8) DW
28
Shrimp, Metapenaeus affinis; edible portions
13.6 DW
17
North Sea; 1997-1998; muscle Shrimp, Crangon crangon Crab, Cancer pagurus
5.2 FW Max. 40.0 FW
34 34
Shrimp, Palaemon elegans; whole
16.0 DW
18
Deep sea prawn, Pandalus borealis Whole Muscle Head and shell Muscle
(7.3-11.5) FW 80.0 DW 68.3 DW 61.6 DW
6 7 28 28
a
9 9
(Continues)
404 Chapter 7 Table 7.3: Organism Oil Egg
Cont’d
Concentration 42.0 DW; 10.1 FW (3.7-14.0) FW
Reference 28 28
Shrimp, Pandalus montagui; whole
(7.4-10.8) FW
Shrimp, Pandalus sp. Whole Soft parts
0.83 AW 0.05 DW
Lobster, Panulirus argus; muscle
3.8 FW; 14.0 DW
Reef lobster, Panulirus spp.; American Samoa; 2001-2002; soft parts Total arsenic Inorganic arsenic
(19.8-98.2) FW (<0.009-0.083) FW
32 32
8.6 FW
22
Marsh crab, Parasesarma erythodactyla; soft parts; 2002; New South Wales, Australia; metals-contaminated estuary Males Females
Max. 7.2 DW Max. 32.6 DW
30 30
Brown shrimp, Peneus aztecus Whole Muscle
0.6 DW (3.1-5.2) FW
2 28
(9.3-11.2) DW
17
18.0 DW 7.7 DW 20.0 DW
33 33 33
Alaskan king crab, Paralithodes camtschatica; muscle
Black tiger shrimp, Penaeus monodon Edible portions Vietnam; 2003-2005; juveniles; max. values Muscle Exoskeleton Hepatopancreas White shrimp, Peneus setiferus Whole Whole Muscle Mississippi Florida
1.3 (0.8-2.2) FW 3.8 (2.2-6.3) DW
a
6 19 20 3
3 3
(1.7-4.4) FW (2.8-7.7) FW
28 28
Crab, Portunus pelagicus; edible portions
(11.3-25.2) DW
17
Crab, Portunus sp.; edible portions
(5.5-6.5) FW
15 (Continues)
Crustaceans 405 Table 7.3:
Cont’d
Organism
Concentration
Reference
Crab, Pugettia producta; feces
(190.0-340.0) AW
21
Shrimp, Sergestes lucens; muscle; total arsenic vs. arsenobetaine
5.5 FW vs. 4.5 FW
25
Shrimps; whole
12.7 FW
15
Taiwan; 1995-1996; shrimps; muscle
Max. 5.1 DW
27
South Texas, Lower Laguna Madre; 1986-1987; whole Grass shrimp, Palaemonetes sp. Brown shrimp, Penaeus aztecus Blue crab, Callinectes sapidus
26.9 (9.7-55.0) DW 17.9 (8.1-50.0) DW 18.4 (2.7-50.0) DW
26 26 26
a
Values are in mg As/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Bohn and McElroy, 1976; 2, Sims and Presley, 1976; 3, Bernhard and Zattera, 1975; 4, Greig et al., 1977a; 5, LeBlanc and Jackson, 1973; 6, Kennedy, 1976; 7, Bohn, 1975; 8, Tijoe et al., 1977; 9, Reinke et al., 1975; 10, Hoover et al., 1974; 11, Vaskofsky et al., 1972; 12, Hall et al., 1978; 13, Costa and da Fonseca, 1967; 14, Penrose et al., 1975; 15, Johnson and Braman, 1975; 16, Leatherland et al., 1973; 17, Zingde et al., 1976; 18, Leatherland and Burton, 1974; 19, Fukai and Meinke, 1959; 20, Fukai and Meinke, 1962; 21, Boothe and Knauer, 1972; 22, Francesconi et al., 1985; 23, Vos and Hovens, 1986; 24, Phillips et al., 1982; 25, Shiomi et al., 1984b; 26, Custer and Mitchell, 1993; 27, Han et al., 1998; 28, Jenkins, 1980; 29, Denton et al., 2006; 30, MacFarlane et al., 2006; 31, Karouna-Renier et al., 2007; 32, Peshut et al., 2008; 33, Tu et al., 2008; 34, De Gieter et al., 2002.
finfish and molluscan tissues (Hall et al., 1978). Arsenic in crustaceans and other marine species is concentrated in lipid fractions primarily as an organoarsenic compound of negligible toxicity, and this is believed to account for the lack of adverse effects to consumers of crustaceans with relatively high arsenic body burdens. The carnivorous shrimp Lysmata seticaudata derived organoarsenicals indirectly from primary producers, which efficiently transfer these compounds along the food chain (Wrench et al., 1979). No organic arsenic could be formed by shrimp; in the case of Lysmata, arsenate taken up from seawater was converted mostly to arsenite (Wrench et al., 1979). Factors known to modify rates of arsenic accumulation and retention in L. seticaudata include water temperature and salinity, arsenic concentration in diet and ambient medium, age of shrimp, and especially the frequency of molting (Fowler and Unlu, 1978). There is only slight uptake of inorganic arsenicals by crustaceans from the medium or from food (Rosemarin et al., 1985). In a simplified estuarine food chain, there was no significant increase in arsenic content of grass shrimp, Palaemonetes pugio, exposed to arsenate-contaminated food or to elevated water concentrations of arsenate (Lindsay and Sanders, 1990). Sensitive species of crustaceans died at 0.23-0.51 mg As3+/L, with 50% mortality recorded in 96 h for juvenile copepods, Acartia clausi, Eurytemora affinis, and zoeae of dungeness crab, Cancer magister (Sanders, 1986; USEPA, 1985a). Arsenic toxicity increases with increasing
406 Chapter 7 water temperature between 5 C and 15 C to the marine amphipod Corophium volutator (Bryant et al., 1985). Studies with the mysid, Mysidopsis bahia, showed that lifetime exposure (about 28 days) to As3+ produced a no-effect level at 0.63 mg/L and an observed effect at 1.27 mg/L; short-term tests with As5+ produced an LC50, 96 h concentration of 2.3 mg/L (USEPA, 1985a). Copepods, Tigriopus japonicus, exposed for two generations to As3+ or As5+ had reduced fecundity at 0.0001 mg/L and higher, and an increase in the proportion of males and reduced survival at 0.01 mg/L and higher (Lee et al., 2008).
7.4 Barium Whole copepods contained up to 2000.0 mg Ba/kg on an ash weight (AW) basis, and whole hermit crabs, Eupagurus bernhardus, contained up to 84.0 mg Ba/kg on a FW basis (Table 7.4). Table 7.4: Barium, Beryllium, and Boron Concentrations in Field Collections of Crustaceans Element and Organism
Concentration
Reference
a
Barium Copepods Whole Whole
17.0 DW 2000.0 AW
1 2
Shrimp, Crangon sp.; whole
0.3 DW
6
Crustaceans; whole; 12 spp.
11.0-21.0 FW
3
Crab, Eupagurus bernhardus; whole
84.0 FW
3
Euphausiids; whole
24.0 DW
1
Black tiger shrimp, Penaeus monodon; juveniles; Vietnam; 2003-2005; max. values Muscle Exoskeleton Hepatopancreas
0.18 DW 76.0 DW 2.6 DW
7 7 7
3.0 AW
2
Copepod, Calanus finmarchicus; whole
760.0 AW
4
Crab, Cancer magister; whole
1.8 FW
5
Euphausiid, Euphausia krohni; whole
440.0 AW
4
Beryllium Copepods; whole Boron
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Martin and Knauer, 1973; 2, Vinogradova and Koual’skiy, 1962; 3, Mauchline and Templeton, 1966; 4, Nicholls et al., 1959; 5, Thompson et al., 1976; 6, Zumholz et al., 2006; 7, Tu et al., 2008.
Crustaceans 407
7.5 Beryllium The single datum available for beryllium is 3.0 mg Be/kg AW in whole copepods (Table 7.4).
7.6 Bismuth Maximum bismuth concentrations in tissues of juvenile tiger shrimp, Penaeus monodon, from Vietnam during 2003-2005 were (in mg Bi/kg DW) 0.02 in muscle, 0.006 in exoskeleton, and 0.06 in hepatopancreas (Tu et al., 2008). Plankton, mostly crustaceans, collected at Eniwetok Atoll in 1964 had the highest concentration of 207Bi of all biological samples analyzed (Welander, 1969).
7.7 Boron Whole copepods contained up to 760.0 mg B/kg on an AW basis and the euphausiid Euphausia krohnii had 440.0 mg B/kg AW (Table 7.4). Boron is a common ingredient in many dishwashing detergents and cleansers, and this should be considered as one source of the element into coastal waters of the United States (Eisler, 2000b).
7.8 Cadmium The highest cadmium concentrations were usually found in digestive gland, hepatopancreas, or kidney, and the lowest concentrations in edible muscle (Table 7.5). Some of these data suggest that cadmium levels in edible tissues may approach or exceed 13.0-15.0 mg Cd/kg FW, a concentration that will induce vomiting in human consumers. However, edible tissues in those instances included viscera, wherein cadmium burdens were greatest. There is no demonstrable hazard to human health associated with ingestion of edible muscle tissues of marine crustaceans (Eisler, 1981). The highest concentration of cadmium in whole crustaceans reported in a nationwide survey of 736 stations in estuaries of the United States during 2000-2001 was 0.70 mg Cd/kg FW in the shrimp, Farfantepenaeus aztecus; about 29% of all samples exceeded the putative guideline of 0.4 mg Cd/kg FW (Harvey et al., 2008). Amphipods, Paramoera walkeri, from the Australian Antarctic Territory in 1999-2000 had whole-body bioconcentration factors that ranged between 150 and 630 when seawater contained between 0.00006 and 0.0001 mg Cd/L; BCFs decreased with increasing seawater concentration (Clason et al., 2003). Amphipods showed increased sensitivity when seawater contained 0.0009-0.003 mg Cd/L (Clason et al., 2003). Cadmium concentrations in gill and hepatopancreas of a prawn, Penaeus indicus, were mostly in the insoluble fraction, wherein cadmium was associated with phosphorus, calcium, magnesium, and silicon (Nunez-Nogueira et al., 2006a). Exposure to 0.1 mg Cd/L for 10 days caused a 50-fold increase in cadmium concentration in hepatopancreas and a 60-fold increase
408 Chapter 7 Table 7.5: Cadmium Concentrations in Field Collections of Crustaceans Organism
Concentration
Reference
Amphipods; whole
7.0 DW
1
Copepod, Anomalocera patersoni; whole; males vs. females
1.4 DW vs. 1.6 DW
2
Barents Sea and environs; 1991-2000; whole Copepods; 4 spp. Euphausid, Meganyctiphanes norvegica Amphipod, Themisto abyssorum Shrimp, Pandalus borealis
1.2-6.3 DW 0.2 DW 10.5 DW 1.6 DW
Barnacles; soft parts
12.1 DW
Barnacles; summer 2001; near Natal, Brazil; soft parts Fistulobalanus citerosum Balanus amphitrite
(2.7-4.2) DW 5.1 DW
40 40
0.1 DW 1.8 (0.09-5.6) DW
4 38
Max. 4.6 FW Max. 0.08 FW
42 42
Crab, Cancer irroratus Muscle Digestive gland Gills
(0.08-1.0) FW (1.1-4.8) FW (0.7-2.7) FW
5 5 5
Crab, Cancer pagurus Edible tissues Brown meat Whole
(3.6-13.0) FW (0.03-3.4) FW 5.0 FW
6 7 8
Crab, Carcinus maenas; whole
(14.3-33.1) FW
8
Copepods Whole Whole Whole Whole; 3 spp.; Taiwan; near sewage outfall
5.0 DW 4.1 DW 0.72 DW 0.23-1.8 DW
Blue crab, Callinectes sapidus Whole Muscle; Iskenderun Bay, Turkey; August 2005 Pensacola, Florida; 2003-2004 Hepatopancreas Muscle
a
48 48 48 48 3
1 9 10 39 (Continues)
Crustaceans 409 Table 7.5:
Cont’d
Organism
Concentration
Crabs Muscle Shell
0.19 FW 0.14 FW
11 11
(0.98-2.8) FW 8.8 DW (0.01-0.40) DW
12 13 14
<0.1 FW 0.1-0.2 FW 0.2-0.4 FW
15 15 15
Crustaceans Whole Whole Soft parts Commercial species; edible tissues 3 spp. 9 spp. 4 spp.
Reference
Euphausiid, Euphausia pacifica; whole
(0.05-0.36) FW; (0.33-2.8) DW
Euphausiid, Euphausia superba; East Antarctica; whole
3.3 DW
35
Euphausiids Whole Whole
2.8 DW 0.14 FW
9 17
Greenland; 1975-1991; 6 spp.; whole
0.2-4.6 FW
33
Mantis shrimp, Gonodactylus sp.; Guam; June 1998; muscle vs. gonad
0.36 DW vs. 9.1 DW
34
Lobster, Homarus americanus Muscle Whole Muscle Exoskeleton Gill Viscera
0.03 FW 0.51 FW; 0.20 FW; 0.59 FW; 0.49 FW; 1.21 FW;
18 19 19 19 19 19
Lobster, Homarus vulgaris; muscle
(<0.03-0.09) FW
Blue shrimp, Litopenaeus stylirostris; Gulf of California; 2004-2005; muscle
0.66 (0.38-1.1) DW
36
0.41 FW; 1.7 DW 0.76 FW; 3.1 DW 0.91 FW; 2.8 DW 0.09 FW; 0.39 DW 0.42 FW; 1.3 DW 1.3 FW; 5.5 DW
7 7 7 7 7 7
Shrimp, Lysmata seticaudata Whole Exoskeleton Viscera Muscle Eyes Molts
5.3 AW 10.0 AW 4.1 AW 17.2 AW 33.8 AW
a
7
6
(Continues)
410 Chapter 7 Table 7.5:
Cont’d
Organism
Concentration
Euphausiid, Megancytiphanes norvegica Whole Molts Feces Eggs Stomach contents Whole Feces Whole
0.7 DW 2.1 DW 9.6 DW 0.3 DW 2.1 DW <4.5 DW <80.0 DW 0.25 DW
20 20 20 20 20 21 21 16
Peneid shrimp, Melicertus kerathurus; Lesinalagoon, Italy; October 2004; 3 sites Muscle Exoskeleton
0.10-0.23 DW 0.91-2.9 DW
47 47
1.1 DW
45
0.5 DW 3.1 DW
45 45
Mexico; Gulf of California; 1999-2000 Barnacle, Balanus eburneus; soft parts Shrimps; muscle Leptopenaeus stylirostris Leptopenaeus vanamei
Reference
Lobster, Nephrops norvegicus; edible tissues
(<0.03-0.1) FW
Shrimp, Palaemon elegans; whole
0.31 DW
22
Shrimp, Palaemonetes pugio; whole
3.3 (1.4-6.2) DW
23
Amphipod, Paramoera walkeri; East Antarctica; 200-2004; whole
2.3-7.0 DW
35
Shrimp, Pandalus jordani; whole
0.16 (0.06-0.30) FW; 0.49 (0.18-0.96) DW
a
6
7
Shrimp, Pandalus montagui Tail Egg Carcass Hepatopancreas Whole
0.03 DW 0.12 DW 0.34 DW 6.4 DW 0.47 DW
24 24 24 24 24
Lobster, Panulirus interruptus Muscle Hepatopancreas
(0.28-0.31) FW (5.6-29.3) FW
25 25 (Continues)
Crustaceans 411 Table 7.5:
Cont’d
Organism
Concentration
Reference
Marsh crab, Parasesarma erythodactyla; soft parts; 2002; New South Wales, Australia; metals-contaminated estuary Males Females
Max. 25.9 DW Max. 22.5 DW
41 41
Prawn, Penaeus indicus; juveniles Hepatopancreas Whole Soluble fraction Insoluble fraction Gills Whole Soluble fraction Insoluble fraction
0.8 DW 0.2 DW 0.6 DW
43 43 43
0.6 DW 0.1 DW 0.5 DW
43 43 43
Black tiger shrimp, Penaeus monodon; juveniles; Vietnam; 2003-2005; max. values Muscle Exoskeleton Hepatopancreas
0.04 DW 0.03 DW 8.4 DW
46 46 46
Shrimp, Peneus aztecus Muscle Exoskeleton Viscera Whole
0.16 DW 0.50 DW 2.6 DW <0.4 DW
26 26 26 4
Shrimp, Peneus duorarum; whole
0.3 FW
28
White shrimp, Peneus setiferus; muscle; Gulf of Mexico
6.1 DW
37
Crab, Portunus holsatus; whole
0.14 FW
29
Crab, Pugettia producta; feces
(3.1-3.2) AW
30
Shrimps Muscle Shell Muscle Exoskeleton
(<0.02-0.35) FW (0.28-0.35) FW 0.25 DW 0.49 DW
11 11 26 26
a
(Continues)
412 Chapter 7 Table 7.5:
Cont’d
Organism
Concentration
Zooplankton Surface vs. > 99 m depth Whole Baltic Sea; May 1999; cladocerans vs. copepods; whole
16.0 AW vs. 15.0 AW 2.5 (0.3-10.9) DW 2.0 DW vs. 0.7 DW
Reference
a
31 32 44
Values are in mg Cd/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Bohn and McElroy, 1976; 2, Polikarpov et al., 1979; 3, Stenner and Nickless, 1975; 4, Sims and Presley, 1976; 5, Greig et al., 1977b; 6, Topping, 1973; 7, Bernhard and Zattera, 1975; 8, Peden et al., 1973; 9, Martin and Knauer, 1973; 10, Tijoe et al., 1977; 11, Won, 1973; 12, Wright, 1976; 13, Stenner and Nickless, 1974b; 14, Stickney et al., 1975; 15, Hall et al., 1978; 16, Leatherland et al., 1973; 17, Greig and Wenzloff, 1977; 18, Chou et al., 1978; 19, Eisler et al., 1972; 20, Benayoun et al., 1975; 21, Fowler, 1977; 22, Leatherland and Burton, 1974; 23, Pesch and Stewart, 1980; 24, Ray et al., 1980; 25, Vattuone et al., 1976; 26, Horowitz and Presley, 1977; 28, Nimmo et al., 1977; 29, DeClerck et al., 1979; 30, Boothe and Knauer, 1972; 31, Martin, 1970; 32, Hardstedt-Romeo and Laumond, 1980; 33, Dietz et al., 1996; 34, Denton et al., 2006; 35, Palmer et al., 2006; 36, Frias-Espericueta et al., 2007; 37, Vazquez et al., 2001; 38, Turkmen et al., 2006; 39, Feng et al., 2006; 40, Silva et al., 2006; 41, MacFarlane et al., 2006; 42, Karouna-Renier et al., 2007; 43, Nunez-Nogueira et al., 2006a; 44, Pempkowiak et al., 2006; 45, Ruelas-Inzunza and Paez-Osuna, 2008; 46, Tu et al., 2008; 47, D’Adamo et al., 2008; 48, Zauke and Schmalenbach, 2006.
in gill; more than 80% of the cadmium was in the insoluble fraction of the Cd-exposed prawns (Nunez-Nogueira et al., 2006a). Juvenile mysids, Neomysis integer, exposed to 0.045 mg Cd/L for 7 days at different salinities were analyzed for metallothionein induction and cytosolic metal concentrations (Erk et al., 2008). Metallothionein induction occurred at all salinities and cytosolic cadmium increased 29% from the lowest salinity tested of 5 ppt to the highest salinity tested of 25 ppt; however, cytosolic copper decreased 44% within this salinity range, although there was a significant positive correlation between metallothionein and cytosolic copper concentration (Erk et al., 2008). Metal assimilation from food plays an important role in cadmium accumulation, especially in estuarine stages of the life cycle (Nunez-Nogueira et al., 2006b). Juvenile prawns, P. indicus, fed with radiolabeled 109Cd squid muscle (Loligo vulgaris) or filaments of the green alga (Cladophora sp.) for 60 min, were then transferred to clean seawater. The assimilation efficiency (AE) was calculated from the time at which no radioactivity was detected in feces, or about 6 h after ingestion of algae and 10 h after ingestion of squid muscle. The AE of 109Cd was 42% from algae at 6 h and 75% (64-83%) from squid muscle at 10 h. During the depuration period of 49 h, assimilated cadmium was lost at a constant rate from the diet. Prawns fed 109Cd-labeled algae had most of the assimilated 109Cd in hepatopancreas (71%) after 49 h depuration, 12% in exoskeleton, 5% in foregut, 4% in external organs, 3% in muscle, and 2% in gills. Prawns fed 109Cd-labeled squid muscle showed (after 134 h) 53% of the radioactivity in hepatopancreas, 12% in exoskeleton, and 8% in foregut (Nunez-Nogueira et al., 2006b). Thorsson et al. (2008) aver that settling organic matter (OM) is the major food source for heterotrophic benthic fauna. OM attached to 109Cd-labeled microalgae Tetraselmis spp. fed
Crustaceans 413 to the amphipod Monoporeia affinis for 34 days was biomagnified by a factor of 3.0 (Thorsson et al., 2008). Crustaceans are comparatively sensitive to cadmium insult. A crab, Pontoporia affinis, held in 0.0065 mg Cd/L for 265 days had a reduced F1 life span (Sundlein, 1983). An LC-50 range of 0.015-0.019 mg Cd/L was reported for two species of mysid shrimp during lifetime exposure (i.e., 23-27 days) to cadmium salts (Gentile et al., 1982). Crustaceans immersed in ambient cadmium concentrations between 0.005 and 0.019 mg/L had decreased growth, abnormal respiration, delayed molt, shortened life span, altered enzyme levels, and abnormal muscular contractions (as quoted in Eisler, 2000d). Cadmium was fatal to 50% of nauplii of copepods (E. affinis) at 0.051 mg/L and 5 ppt salinity, and 0.083-0.213 mg Cd/L at higher salinities (Hall et al., 1995). In general, resistance to cadmium is higher in marine than in fresh water organisms, and survival is usually higher at lower temperatures and higher salinities tested for any given level of cadmium in the medium (Eisler, 2000d). Studies with Leptocheirus plumulosus, an estuarine amphipod, showed that gravid females were more resistant than males or mature females to the biocidal properties of Cd2+; juveniles were more sensitive than adults; sensitivity was greatest among starved animals and immediately after molting; field-collected amphipods were more sensitive to dissolved cadmium than were laboratory strains, regardless of the season of collection (McGee et al., 1998). Acute toxicity tests of 96 h duration with adults of T. japonicus—a species proposed as a benchmark for routine ecotoxicity testing in the western Pacific Ocean region—showed no effect on survival at 10.0 mg Cd/L, 10% mortality at 13.9 mg/L, and 50% mortality at 25.2 mg Cd/L (Lee et al., 2007). Laboratory studies on cadmium accumulation in crustaceans and on the factors modifying cadmium uptake rates show that adult fiddler crabs, Uca pugilator, as one example, accumulated maximum concentrations of cadmium under conditions of comparatively high water temperatures and low salinities; concentrations were greatest in green gland, gill, hepatopancreas, and muscle, in that order (O’Hara, 1973a,b). However, Leander adspersus took up significantly more cadmium at 6 C than at 15 C (Bengtsson, 1977). Most authorities concluded that cadmium-stressed crabs and shrimps showed greatest uptake at lower salinities (Hutcheson, 1974; Vernberg and DeCoursey, 1977; Vernberg et al., 1977; Wright, 1977a,b). Cadmium was more toxic to juveniles of the euryhaline crab Chasmagnathus granulatus at 5 ppt salinity than at 25 ppt salinity, as judged by LC50 (96 h) values of 2.2 mg Cd/L at 5 ppt and 14.4 mg Cd/L at 25 ppt salinity (Beltrame et al., 2008). Viscera were acknowledged as the main site of cadmium accumulation. Cadmium-loaded shrimp contained highest residues in hepatopancreas, followed by gill, exoskeleton muscle, and serum (Nimmo et al., 1977); similar patterns were demonstrated for shrimp, Leander sp. (Hiyama and Shimizu, 1964), blue crab, Callinectes sapidus (Hutcheson, 1974), green crab, Carcinus maenas (Wright, 1977c), the euphausiid, Megancytiphanes norvegica (Benayoun et al., 1975), and the prawn, Pandalus montagui (Ray et al., 1980). The effects of cadmium on fiddler crabs depend upon stage of the life cycle, thermal history, and salinity of the
414 Chapter 7 medium; larvae were more sensitive than adults, with survival lowest at elevated temperatures and depressed salinities (Vernberg and DeCoursey, 1977). Transfer of cadmium to shrimp was less efficient via the diet than transfer directly from seawater. In order to produce equivalent whole-body cadmium residues in shrimp, about 15,000 times more cadmium must be introduced in food than could be obtained from the medium (Nimmo et al., 1977). A similar conclusion was reached for the euphausiid M. norvegica (Benayoun et al., 1975). Amphipods (Gammarus lawrencianus) labeled with 109Cd via the medium were fed to grass shrimp, P. pugio; about 50% of the radiocadmium was retained by the shrimp after 7 days (Seebaugh et al., 2006). Cadmium accumulation by brine shrimp, Artemia salina, directly from solution and from diet was investigated at seawater cadmium concentrations of 0.1, 1.0, and 10.0 mg Cd/L (Jennings and Rainbow, 1979b). At lower cadmium concentrations, diet was the major route for accumulation. At higher cadmium concentrations, cadmium-laden food items displaced cadmium-rich water from the gut with less cadmium accumulated by Artemia. It seems that food chain is the major source of cadmium to Artemia provided that lower trophic levels biomagnify cadmium to the extent that it is more available to Artemia than direct uptake from seawater (Jennings and Rainbow, 1979b). Depuration of cadmium from whole green crab, C. maenas, is reported: crabs containing 19.0 mg Cd/kg FW after immersion in cadmium-containing solutions for 37 days lost about half during a postexposure period of 11 days (Wright, 1977a). Two heavy metal-binding proteins occur naturally in the midgut glands of green crabs; these proteins of approximately 27.000 molecular weight (MW) and 11,500 MW together bound about 32% of the soluble cadmium in the midgut gland and may represent a possible defense mechanism against atypically high cadmium insults (Rainbow and Scott, 1979). Cadmium accumulation by green crabs was measured under controlled conditions (Jennings and Rainbow, 1979a; Jennings et al., 1979). When cadmium was offered via the diet, most of the cadmium accumulated was adsorbed onto the exoskeleton surface, with midgut gland containing about 10% of the total body burden. When cadmium was introduced via the diet, midgut gland contained about 17% of the total absorbed cadmium; levels in exoskeleton were dramatically lower (Jennings et al., 1979). Dependent on tissue and MW of cadmium-binding proteins, which ranged between <6000 and >50,000, differential tissue uptake was evident. In the midgut gland, for example, which had the highest concentrations of cadmium, at least four cadmium binding proteins were identified (Jennings et al., 1979). Duration of exposure and nominal cadmium concentrations in ambient seawater affected final residue values in crustaceans. In general, uptake was continuous over time, with little evidence of equilibrium or plateauing (Vernberg et al., 1977); also, lower concentration factors were evident at higher initial cadmium levels in the medium (Nimmo et al., 1977). At relatively low cadmium concentrations of 0.003-0.010 mg Cd/L, the uptake patterns were different for some species. Thus, adult lobsters, H. americanus, held for 21 days in flowing seawater solutions
Crustaceans 415 containing 0.010 mg Cd/L had up to 41% more cadmium than controls on a FW basis (Eisler et al., 1972). Not all tissues accumulated at the same rate: gills showed the largest increase of 78% and viscera the least, with no increase (Eisler et al., 1972). Shrimp, Crangon crangon, held for 8 days in media containing 0.005 mg Cd/L had a bioconcentration factor of 860 for the whole animal (Jung and Zauke, 2008). At 0.003 and 0.006 mg Cd/L, lobsters held for 30 or 60 days showed little accumulation in digestive glands, but muscle cadmium levels almost doubled when compared to controls (Thurberg et al., 1977). Grass shrimp, P. pugio, after exposure for 6 weeks in seawater solutions containing 0.06 mg Cd/L, had up to 20.4 mg Cd/kg DW whole body versus 6.2 in controls (Pesch and Stewart, 1980). At higher experimental cadmium concentrations of 0.12, 0.25, 0.5, and 1.0 mg Cd/L, wholebody residues in shrimp ranged up to 31.0, 58.2, 63.9, and 106.0 mg Cd/kg DW, respectively (Pesch and Stewart, 1980). High mortality was documented in grass shrimp at seawater concentrations of more than 0.25 mg Cd/L. Hermit crabs, Pagurus longicarpus, were even more sensitive than grass shrimp, with many deaths noted at the lowest test concentration of 0.06 mg Cd/L, commencing at week 6 of exposure and continuing until week 10, when the study was terminated (Pesch and Stewart, 1980). Cadmium uptake rates in various tissues of a cold water pandalid shrimp, P. montagui, held in seawater solutions containing 0.037 mg Cd/L, ranged from 0.002 to 0.06 mg Cd/kg dry tissue per hour (Ray et al., 1980). After 14 days, hepatopancreas had 25.6 mg Cd/kg DW; values for carcass, egg, and tail were 8.2, 4.3, and 0.8, respectively, in a similar period. During depuration for 57 days, cadmium concentrations in most tissues decreased, but continued to rise in hepatopancreas, indicating cadmium redistribution (Ray et al., 1980). Radiocadmium uptake studies with C. maenas show that most of the cadmium entering hemolymph was freely labile and quickly displaced by stable cadmium taken up subsequently (Wright and Brewer, 1979). Some hemolymph cadmium was probably translocated to hepatopancreas; however, a significant portion of whole-body cadmium was adsorbed onto gills and exoskeleton. The rapid efflux of radiocadmium from Carcinus over a period of 7 days was due mainly to cadmium loss from the outer body surface (Wright and Brewer, 1979). Radiocadmium-109 uptake during exposure of 385 h and loss during 189 h in 109Cd-free seawater was measured in semaphore crab, Heloecius cordiformis, soldier crab, Mictryris platycheles, and ghost shrimp, Trypnaea australiensis (Alquezar et al., 2007). Cadmium concentration factors over the medium during uptake were 5.7 for semaphore crab, 9.7 for soldier crab, and 68.0 for ghost shrimp; loss during immersion in 109 Cd-free media was 59% for semaphore crab, 66% for soldier crab, and 69% for ghost shrimp. Excretion followed a biphasic pattern. The biological half-time for short-lived and long-lived components ranged from 5 to 12 h, and from 1370 to 2590 h, respectively (Alquezar et al., 2007). Grass shrimp, P. pugio, were exposed for 8 months to Cd2+ concentrations of 0.0015 or 0.0025 mg/L for an entire life cycle from larva to reproductive adult, and through
416 Chapter 7 the production of second-generation larvae (Manyin and Rowe, 2008). Cadmium concentrations in whole adult shrimp, in mg Cd/kg DW, after 8 months were 0.64 in controls, 59.6 in the low-dose group, and 80.4 in the high-dose group. Adult survival was significantly reduced in the high-dose group, but had no effect on survival or stage duration of embryos, larvae, or juveniles. Brood size was reduced by 27% in the low-dose group and by 36% in the high-dose group. Both populations showed a dose-dependent decrease in population growth, up to 12% for the high-dose group. The ability of populations to withstand predation pressure is unknown, but would probably be compromised (Manyin and Rowe, 2008). The chemical form of cadmium, as well as interaction with other substances in solution, may affect the bioavailability of ionic cadmium. Nimmo et al. (1977) aver that at certain given cadmium concentrations, nitrate salts were accumulated to higher levels in whole shrimp than were sulfate, chloride, or acetate salts, in that order. Interactive toxicity among metalpolycyclic aromatic hydrocarbons mixtures are common among benthic copepods (Fleeger et al., 2007). For example, cadmium-phenanthrene mixtures were more than additive in toxicity by way of sediments or medium to the copepod Schizopera knabeni; however, cadmium-mercury-lead mixtures were less than additive in toxicity. In the copepod Amphiascoides atopus, mixtures of cadmium-phenanthrene and cadmium-fluoranthrene were more than additive in toxicity (Fleeger et al., 2007). Chelating agents, such as humates and alginates, significantly reduced cadmium accumulation in barnacles, Semibalanus balanoides, during the first 7 days of exposure, but not afterwards (Rainbow et al., 1980). Authors concluded that the amount of cadmium accumulated by barnacles is a function of the free Cd2+ ions available in solution and that uptake of cadmium does not require external binding of ionic cadmium to released metabolites prior to uptake (Rainbow et al., 1980). In studies with Aesop shrimp, P. montagui, and mixtures of cadmium and zinc (0.04 mg Cd/L plus 0.07 mg Zn/L), cadmium concentrations in Pandalus hepatopancreas doubled when compared to concentrations accumulated during exposure to cadmium alone (Ray et al., 1980). Increased amounts of zinc (0.41 mg Zn/L) resulted in a depression of hepatopancreatic cadmium, although the cadmium burden was still greater than in the case of exposure to cadmium alone; there was no significant accumulations of zinc in all studies at the concentrations studied (Ray et al., 1980). Weis (1978) reports that limb regeneration and ecdysis in three species of fiddler crabs were severely retarded by low concentrations of cadmium in the ambient medium; a similar effect was observed with methylmercury. However, mixtures of cadmium and methylmercury, or cadmium and calcium, ameliorated the severe effects of cadmium, indicating antagonism or site-specific competition of cadmium-mercury and cadmium-calcium mixtures. At present, seawater concentrations in excess of 0.0045 mg/L of total cadmium at any time should be considered potentially hazardous to marine life until additional data prove otherwise (Eisler, 2000d).
Crustaceans 417
7.9 Cerium The high concentrations of cerium in fecal pellets of the euphausiid M. norvegica (Table 7.6) indicated that diet was the most important transfer mechanism for this element in crustaceans. Cerium flux attributable to euphausiid fecal pellets in the Mediterranean Sea was small, but measurable (Fowler, 1977). Following the Chernobyl nuclear reactor accident in April 1986 (Eisler, 1995, 2003), radiocerium-141 and -144 concentrated in fecal pellets of copepods (Fowler et al., 1987). Fecal pellets, when compared to whole copepods, contained 45 times more 141Ce and 25 times more 144Ce (Fowler et al., 1987). Laboratory studies with radiocerium and the prawn, Leander sp., showed that viscera contained 200 times more cerium than seawater (Hiyama and Shimizu, 1964); for muscle and exoskeleton, these values were 25 and 2, respectively. The addition of chelating agents to the medium, such as ethylenediaminetetraacetic acid (EDTA), decreased the bioavailability of cerium, with the result that all tissue cerium values were lowered by an order of magnitude (Hiyama and Shimizu, 1964). The euphausiid, M. norvegica accumulated radiocerium from seawater by a factor of about 65; after 12 h in cerium-free seawater, about 10% of the radiocerium was lost (Antonini-Kane et al., 1972). In another study with M. norvegica, Table 7.6: Cerium and Cesium Concentrations in Field Collections of Crustaceans Element and Organism
Concentration
Reference
a
Cerium Amphipod, Paramoera walkeri; East Antarctica; 2003-2004; whole
(0.11-0.25) DW
5
<4.5 DW 200.0 DW
1 1
Lobster, Jasus lalandi; muscle
0.01 FW
2.3
Black tiger shrimp, Penaeus monodon; juveniles; Vietnam; 2003-2005; max. values Muscle Exoskeleton Hepatopancreas
0.04 DW 0.03 DW 0.09 DW
6 6 6
Shrimp, Peneus japonica; muscle
0.046 DW
4
Stomatopod, Squilla oratoria; muscle
0.028 DW
4
Euphausiid, Meganyctiphanes norvegica Whole Fecal pellets Cesium
Values are in mg element/kg fresh weight (FW), or dry weight (DW). a 1, Fowler,1977; 2, Van As et al., 1973; 3, Van As et al., 1975; 4, Ishii et al., 1978; 5, Palmer et al., 2006; 6, Tu et al., 2008.
418 Chapter 7 molting was responsible for up to 99% loss of total body burden of radiocerium at first molt, and about 45% of the remaining radiocerium at the second molt (Fowler et al., 1973). Fecal pellets did not contain measurable 144Ce activity when the euphausiids accumulated the isotope from the medium, suggesting that surface adsorption was the key accumulating process from the medium (Fowler et al., 1973).
7.10 Cesium The maximum concentration of stable cesium recorded in crustacean tissues from field collections was 0.09 mg Cs/kg DW in hepatopancreas of shrimp (Table 7.6). Cesium is taken up from seawater to various degrees in different species of crustaceans. For whole copepods, Centropages sp. and Calanus sp., the concentration factors ranged from 0.1 to 1.0 times seawater levels (Ketchum and Bowen, 1958). In muscle tissues of the lobster, J. lalandi, cesium was concentrated by a factor of 32 over ambient seawater (Van As et al., 1973). Soft tissues and exoskeleton of a prawn, Leander sp., both took up radiocesium over nominal cesium levels by a factor of 15; time to reach equilibrium was 4 days for soft tissues, and 2 days for exoskeleton (Hiyama and Shimizu, 1964). Whole isopods, Sphaeroma serratum, contained 6-9 times more cesium than the medium (Bryan, 1963). Plasma of the stomatopod, Squilla desmaresti show low potential for cesium accumulation with a concentration factor of 1.4 times seawater; for muscle and digestive gland, these values ranged from 19.4 to 22.0 (Bryan, 1963). Cesium concentrations increased with increasing weight in amphipods (Palmer et al., 2006), and this should be considered when interpreting cesium residues. Uptake of 134Cs by C. maenas was not affected by a nonradioactive diet; muscle was the main limiting factor in the attainment of equilibrium by whole crabs (Bryan, 1961). Radiocesium accumulation occurs primarily across the body surface in starved animals; however, uptake of 134Cs from the diet is rapid and complete and would probably enhance attainment of equilibrium in a natural environment. The squat lobster, Galathea squamifera, shows evidence of regulating radiocesium at blood plasma levels 1.1 times those of seawater; maximum radiocesium accumulation in Galathea was in hepatopancreas and excretory organs at levels 23-29 times that of seawater (Bryan, 1965). Cesium recycling via fecal pellets is documented in copepods after radiocesium contamination from the Chernobyl nuclear accident. Three Mediterranean Sea species contained 155 times more 134Cs in fecal pellets than did whole organism; for 137Cs, this value was 185 (Fowler et al., 1987).
7.11 Chromium Whole crustaceans from chromium-contaminated environments in Egypt contained up to 483.0 mg Cr/kg FW, and those from Taiwan and Texas 195.0-463.0 mg Cr/kg on a DW basis (Table 7.7). Chromium concentrations, however, seldom exceed 0.3 mg/kg FW in edible
Crustaceans 419 Table 7.7: Chromium Concentrations in Field Collections of Crustaceans Organism
Concentration
Copepod, Acartia clausi; whole
1.52 DW
1
Copepod, Anomalocera patersoni; whole; males vs. females
2.08 DW vs. 2.16 DW
2
Barnacle, Balanus amphitrite; soft parts
(2.1-3.9) DW
3
Blue crab, Callinectes sapidus Muscle; Iskenderun Bay, Turkey; August 2005 New Jersey; Hackensack River wetlands vs. reference site Hepatopancreas
Reference
4.5 (0.6-11.6) DW
22
5.2 (1.8-7.3) DW vs. 1.4 (0.8-1.8) DW 0.45 DW vs. 0.54 DW
17
Max. 1.1 FW Max. 0.98 FW
25 25
Crab, Cancer irroratus Muscle Digestive gland Gills
(<0.3-0.6) FW (<0.5-1.2) FW (0.8-2.5) FW
4 4 4
Copepod, Centropages spp.; whole
260.0 AW
5
Copepods Whole Whole Whole; 3 spp.; Taiwan; near sewage outfall
2.1 DW 0.23 DW 16.5-195.0 DW
6 7 23
0.1-0.2 FW 0.2-0.3 FW 0.10-0.38 FW
8 8 19
212.0-483.0 FW
18
0.4 DW 0.7 DW 0.48 DW
9 9 10
Muscle Pensacola, Florida; 2003-2004 Hepatopancreas Muscle
Crustaceans; commercial species; edible tissues 7 spp. 9 spp. 5 spp; Spain; April-May 1990; Mediterranean Sea Crustaceans; whole; 2 spp.; Egypt; chromium-contaminated Bay Crab, Eriphia verrucosa Carapace Soft parts Muscle
a
17
(Continues)
420 Chapter 7 Table 7.7:
Cont’d
Organism
Concentration
Euphausiids; whole
0.46 FW
11
Mantis shrimp, Gonodactylus sp.; Guam; June 998; muscle vs. gonad
0.57 DW vs. 0.91 DW
21
Lobster, Jasus lalandi; muscle
(0.08-0.11) FW
12, 13
Peneid shrimp, Melicertus kerathurus; Lesina lagoon, Italy; October 2004; 3 sites Muscle Exoskeleton
1.9-4.3 DW 3.1-5.0 DW
28 28
Crab, Paralithodes kamtschatica; muscle
0.09 DW
6
Shrimp, Parapenaeus longirostris Carapace Soft parts
0.05 DW 1.1 DW
9 10
Marsh crab, Parasesarma erythodactyla; soft parts; 2002; New South Wales, Australia; metals-contaminated estuary Males Females
Max. 4.5 DW Max. 3.5 DW
24 24
Shrimp, Penaeus aztecus Muscle Exoskeleton Viscera
2.1 DW 10.6 DW 4.0 DW
16 16 16
Black tiger shrimp, Penaeus monodon; juveniles; Vietnam; 2003-2005; max. values Muscle Exoskeleton Hepatopancreas
0.35 DW 0.94 DW 0.79 DW
27 27 27
Crab, Portunus holsatus; whole
0.33 FW
14
Crab, Pugettia producta; feces
(1.1-7.6) AW
15
Shrimp Muscle Exoskeleton
2.8 DW 1.7 DW
16 16
68.0 (15.0-463.0) DW 60.0 (8.0-130.0) DW 1.4 (0.5-5.7) DW
20 20 20
Texas; Laguna Madre; 1986-1987 Grass shrimp, Palaemonetes sp.; whole Brown shrimp, Penaeus aztecus; whole Blue crab, Callinectes sapidus; whole minus legs, carapace and abdomen
Reference
a
(Continues)
Crustaceans 421 Table 7.7:
Cont’d
Organism
Concentration
Crab, Ucides cordatus; adult males Gills Hepatopancreas Muscle
4.8 DW 1.7 DW 2.5 DW
29 29 29
1.5 DW vs. 16.5 DW
26
Zooplankton; Baltic Sea; May 1999; cladocerans vs. copepods; whole
Reference
a
Values are in mg Cr/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Fukai, 1965; 2, Polikarpov et al., 1979; 3, Barbaro et al., 1978; 4, Greig et al., 1977b; 5, Nicholls et al., 1959; 6, Fukai and Broquet, 1965; 7, Tijoe et al., 1977; 8, Hall et al., 1978; 9, Bernhard and Zattera, 1975; 10, Fukai, 1965; 11, Greig and Wenzloff, 1977; 12, Van As et al., 1973; 13, Van As et al., 1975; 14, DeClerck et al., 1979; 15, Boothe and Knauer, 1972; 16, Horowitz and Presley, 1977; 17, Hall and Pulliam, 1995; 18, Dahab et al., 1990; 19, Schuhmacher et al., 1992; 20, Custer and Mitchell, 1993; 21, Denton et al., 2006; 22, Turkmen et al., 2006; 23, Feng et al., 2006; 24, MacFarlane et al., 2006; 25, Karouna-Renier et al., 2007; 26, Pempkowiak et al., 2006; 27, Tu et al., 2008; 28, D’Adamo et al., 2008; 29, Correa et al., 2005.
tissues of commercial species of crustaceans from North America (Table 7.7). A value of 0.6 mg Cr/kg FW in edible muscle of the crab Cancer irroratus was from specimens collected near an ocean dump site receiving large quantities of metals; digestive gland and gills from these crabs also contained elevated chromium residues (Table 7.7). Chromium concentrations in tissues of amphipods from east Antarctica increased with increasing weight of the organism (Palmer et al., 2006). Chromium burdens in soft tissues of the marsh crab, Parasesarma erythodactyla, were significantly correlated with sediment chromium concentrations; this pattern held for both males and females (MacFarlane et al., 2006). Of the 65,000 tons of chromium compounds used annually in exploratory oil drilling, a significant portion enters the marine environment through the discharge of used drilling muds. It is estimated that more than 225 tons of drilling mud may be used in a single 3000 m well (Carr et al., 1982). One of the most frequently used muds in offshore drilling operations is a chrome lignosulfonate mud containing barium sulfonate, bentonite clay, and ferrochrome or chrome lignosulfonates (Carr et al., 1982). The bioavailability of chromium to shrimp from used chrome lignosulfonate drilling muds is most pronounced at the mud aqueous layers. At chromium concentrations of 0.248 mg/L in the mud aqueous layer, grass shrimp took up 23.7 mg Cr/kg DW whole body after 7 days (Carr et al., 1982). Concentrations of drilling mud of 1% or greater in seawater were toxic to sensitive species of crustaceans (Neff et al., 1981). Uptake of 4.0-5.0 mg/kg was reported in grass shrimp exposed to sediments containing 188.0 mg Cr/kg (Neff et al., 1978). The toxicity of chromiumcontaminated drilling muds to grass shrimp may sometimes be attributable to large residuals of petroleum hydrocarbons in the sediments (Conklin et al., 1983).
422 Chapter 7 Sediment chromium concentrations of 3200.0 mg/kg in the New Bedford (Massachusetts) Acushnet estuary and 100.0 mg/kg in New York Bight have been recorded (Doughti et al., 1983). Massive cuticular lesions suggestive of shell disease characterized up to 30% of the lobsters, crabs, and shrimp collected from New York Bight, and these lesions could also be induced in crustaceans exposed to New York Bight sediments in the laboratory. This shell disease syndrome has been induced in 41% of grass shrimp (P. pugio) during exposure to 0.5 mg Cr6+/L for 28 days (Doughti et al., 1983). It is proposed that chromium interferes with the normal function of subcuticular epithelium, particularly cuticle formation, and subsequently causes structural weaknesses or perforations to develop in the cuticle of newly molted shrimp. As a result of these chromium-induced exoskeletal deficiencies, a viaduct for pathogenic bacteria and direct chromium influx is formed, which perpetuates the development of the lesion. Adult male mangrove crabs, Ucides cordatus, exposed for 96 h to a very high sublethal concentration of approximately 100.0 mg Cr3+/L, contained grossly elevated concentrations in tissues—when compared to controls—of 17,396.4 mg Cr/kg DW in gills versus 4.8 in controls, 316.5 in hepatopancreas versus 1.7 in controls, and 47.3 in muscle versus 2.5 mg/kg DW in controls (Correa et al., 2005). Trivalent chromium reportedly precipitates on the gill surface colocalized with epiphyte bacteria (Correa et al., 2005). Barnacles (Balanus sp.) incorporated hexavalent chromium (Cr6+) in soft tissues up to 1000 times over ambient seawater concentrations, reaching equilibrium in 7 days (biological halftime for some components was 120 days); however, trivalent chromium (Cr3+), which precipitates in seawater, was quickly removed by filtering activity, was not concentrated in soft tissues, and was rapidly excreted by way of the digestive system (Van Weerelt et al., 1984). Marine crustaceans were among the most sensitive organisms tested to hexavalent chromium; for example, LC50 values for early life stages of the blue crab, C. sapidus, were 0.93 mg/L at 96 h and 0.32 mg/L at 40 days (as quoted in Eisler, 2000e). Chelators, such as EDTA, reduce the toxicity of trivalent and hexavalent chromium compounds to adult crabs, Petrolisthes laevigatus, sometimes by as much as 41-48% (Urrutia et al., 2008). In other laboratory studies, Sather (1967) observed that uptake and loss of radiochromium by the crab Podophthalmus vigil was independent of gender and eyestalk hormone influence, Most of the radiochromium in that study accumulated in gills. Gills and muscle reached equilibrium in 2-3 days, but midgut and hemolymph required 4-5 days. Iron interfered with chromium uptake and retention in Podophthalmus (Sather, 1967). In another study, Tennant and Forster (1969) demonstrated that chromium concentrated in setae, gills, and hepatopancreas of the dungeness crab C. magister, and concluded that surface adsorption and physiological processes were both instrumental in chromium accumulation. To protect human consumers of crustaceans, it is proposed that edible tissues should not exceed concentration of 12.0 mg Cr/kg FW (Sankar et al., 2006).
Crustaceans 423
7.12 Cobalt Concentrations of cobalt in field collections, in mg Co/kg, never exceeded 0.004 on a FW basis, 5.6 on a DW basis, or 44.0 on an AW basis (Table 7.8). Crustaceans concentrated cobalt from the surrounding medium, but this ability varied considerably among species. Concentration factors of 200-600 are reported for copepods (Ketchum and Bowen, 1958), 800 for euphausiids (Ketchum and Bowen, 1958), 4000 for whole spiny lobster (Ichikawa, 1961), and 140 for muscle of the lobster J. lalandi (Van As et al., 1973). Table 7.8: Cobalt Concentrations in Field Collections of Crustaceans Organism
Concentration
Reference
Copepod, Calanus finmarchicus; whole
3.0 AW
Blue crab, Callinectes sapidus; muscle; August 2006; Iskenderun Bay, Turkey
2.95 (0.65-5.6) DW
Copepod, Centropages spp; whole
4.0 AW
1
Copepods Whole Whole
15.0 AW 0.12 DW
2 3
Euphausiid, Euphausia krohni; whole
5.0 AW
1
Euphausiids; whole
0.63 AW
4
Lobster, Jasus lalandi; muscle
0.004 FW
5, 6
Shrimp, Penaeus japonica; muscle
0.05 DW
7
Black tiger shrimp, Penaeus monodon; Vietnam; juveniles; 2003-2005; max. values Muscle Exoskeleton Hepatopancreas
0.08 DW 0.38 DW 2.9 DW
13 13 13
Crab, Pugettia producta; feces
(0.6-0.9) AW
8
Shrimps; proteinaceous molts vs. muscle
0.47 DW vs. 0.46 DW
9
Stomatopod; Squilla oratoria; muscle
0.16 DW
7
Zooplankton Surface vs. > 99 m depth Baltic Sea; May 1999; cladocerans vs. copepods; whole
44.0 AW vs. 37.0 AW 0.4 DW vs. 2.4 DW
a
1 11
10 12
Values are in mg Co/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Nicholls et al., 1959; 2, Vinogradova and Koual’shiy, 1962; 3, Tijoe et al., 1977; 4, Robertson, 1967; 5, Van As et al., 1973; 6, Van As et al., 1975; 7, Ishii et al., 1978; 8, Boothe and Knauer, 1972; 9, Bertine and Goldberg, 1972; 10, Martin, 1970; 11, Turkmen et al., 2006; 12, Pempkowiak et al., 2006; 13, Tu et al., 2008.
424 Chapter 7 In laboratory studies, concentration factors for cobalt in shrimp, Leander pacificus, over a 30-day period were 5 for muscle and 18 for exoskeleton (Shimizu et al., 1970); hermit crab, Clibanarius virescens, had a whole-body concentration factor of 520 in a similar period (Shimizu et al., 1970). Elimination rates of accumulated radiocobalt were estimated at 4-6%/h for copepods and 1%/h for euphausiids (Kuenzler, 1969). Chitin from ground lobster exoskeletons can adsorb 40-60% of trace metals and metalloids—including cobalt—in 183 h from distilled water (Yoshinari and Subramanian, 1976); this technique appears to hold considerable potential, together with biomonitoring in assessing marine water quality. Transfer of cobalt—an essential element for normal growth and metabolism of crustaceans— through the food chain is documented. Crabs, C. maenas, feeding on annelid worms, Arenicola marina, containing radiocobalt show high assimilation rates with most of the radiocobalt accumulating in hepatopancreas (Amiard-Triquet and Amiard, 1974). A similar pattern was observed when radiocobalt-containing clams, Scrobicularia plana, were fed to C. maenas (Amiard-Triquet and Amiard, 1975). It was concluded that the surrounding medium was the main source of external cobalt contamination in C. maenas, that diet was the primary source of internal cobalt contamination, and that accumulation was largely in digestive glands (Amiard-Triquet and Amiard, 1976).
7.13 Copper Among the highest copper concentrations documented in field collections of marine crustaceans, in mg Cu/kg DW, were 603.0 in hepatopancreas of lobster, 1120.0 in hepatopancreas of shrimp, 1000.0-2050.0 in various tissues of deep sea shrimps, and up to 22,900.0 in pylorus of deep sea shrimps (Table 7.9). In marine ecosystems, the high copper levels encountered in heavily contaminated coastal areas sometimes approach the incipient lethal concentrations for some organisms (Neff and Anderson, 1977). Elevated copper concentrations in saline environments may result from atmospheric deposition, industrial and municipal wastes, urban runoff, rivers, shoreline erosion (Eisler, 2000f), and proximity to deep sea hydrothermal vents (Table 7.9; Kadar et al., 2006). For example, Chesapeake Bay, Maryland, receives more than 1800 kg of copper daily from these sources (Hall et al., 1988a,b). In the Elizabeth River estuary of Chesapeake Bay, anthropogenic copper and other chelatable metals are present at concentrations sufficient to adversely affect growth and survival of the copepod Acartia tonsa (Sunda et al., 1990). Blood and hepatopancreatic tissues usually contain the greatest accumulations of copper and muscle the least (Table 7.9). The presence of copper-containing respiratory pigments in crustaceans and some other invertebrate groups could account for the elevated levels found in blood. For example, copper accounted for 93% of the weight of hemocyanin in blood of the green crab C. maenas (Martin et al., 1977). Hepatopancreas is a major storage and regulatory organ for copper in crustaceans, with the result that copper residues are almost
Crustaceans 425 Table 7.9: Copper Concentrations in Field Collections of Crustaceans Organism
Concentration
Reference
Copepod, Acartia clausi; whole
55.3 (34.0-107.0) DW
1
Amphipods; whole
26.0 DW
2
Copepod, Anomalocera patersoni; whole; males vs. females
42.4 DW vs. 41.3 DW
3
Antarctic Ocean; 1985-1988; 17 spp.; whole; various crustaceans 2 spp. 3 spp. 6 spp. 4 spp. 2 spp.
5.5-7.7 DW 37.0-42.0 DW 53.0-68.0 DW 81.0-107.0 DW 123.0-149.0 DW
42 42 42 42 42
Barents Sea and environs; 1991-2000; whole Copepods; 4 spp. Euphausid, Meganyctiphanes norvegica Amphipod, Themisto abyssorum Shrimp, Pandalus borealis
6.0-9.0 DW 47.0 DW 9.0 DW 61.0 DW
59 59 59 59
Barnacles; Natal, Brazil; summer 2001; soft parts Fistulobalanus citerosum Balanus amphitrite
(26.4-62.8) DW 22.8 DW
52 52
Barnacle, Balanus amphitrite; soft parts
(44.0-109.0) DW
4
Barnacle, Balanus balanoides; soft parts; March vs. August
(0.3-0.7) DW vs. (0.1-0.2) DW
5
Barnacles; whole
Max. 600.0 DW
8
Copepod, Calanus finmarchicus; whole
1350.0 AW
6
Blue crab, Callinectes sapidus Whole Muscle; May vs. June Muscle; August 2005; Turkey Pensacola, Florida; 2003-2004 Hepatopancreas Muscle Crab, Cancer irroratus Muscle Digestive gland Gill
54.0 DW 19.0 (5.0-97.0) FW vs. 11.0 (5.0-18.0) FW 7.0 (3.9-9.4) DW
47
Max. 99.0 FW Max. 14.0 FW
54 54
(13.0-25.4) FW (48.0-161.0) FW (26.5-46.4) FW
a
32 7
9 9 9 (Continues)
426 Chapter 7 Table 7.9:
Cont’d
Organism
Concentration
Reference
Crab, Cancer pagurus Blood Muscle Stomach fluid Hepatopancreas Urine Excretory organs Gills Vas deferens Shell Ovary External eggs Muscle Muscle
76.0 FW 7.5 FW 7.1 FW 137.0 FW 0.4 FW 17.0 FW 32.0 FW 7.6 FW 0.5 FW 9.0 FW 39.0 FW (8.0-125.0) FW 14.3 (4.6-32.8) FW
10 10 10 10 10 10 10 10 10 10 10 11 12
Crab, Carcinus maenas Whole Whole Blood Muscle Stomach fluid Hepatopancreas Urine Excretory organs Gills Shell Vas deferens Hemolymph Fibrin Blood cells, lipids, carotenoids
(15.4-31.4) FW 22.0 DW 46.0 FW 5.7 FW 3.6 FW 42.0 FW 0.5 FW 16.0 FW 18.0 FW 0.6 FW 4.0 FW 44.7 FW 2.1 FW 0.4 FW
13 10 10 10 10 10 10 10 10 10 10 14 14 14
Copepod, Centropages typicus; whole
600.0 AW
Crab, Clibanarius strigimanus; whole
15.8 FW
35
Copepods Whole Whole; surface collection vs. > 99 m depth collection Whole Whole Whole Whole; 3 spp.; Taiwan; near sewage outfall
3.7 DW 115.0 (50.0-215.0) AW vs. 132.0 (50.0-620.0) AW 10.5 (9.0-22.6) DW 15,000.0 AW 7.1 DW 14.0-160.0 DW
2 15
a
6
16 17 18 51 (Continues)
Crustaceans 427 Table 7.9:
Cont’d
Organism
Concentration
Crabs; muscle vs. shell
10.9 (5.8-24.4) FW vs. 6.4 (4.1-9.2) FW
19
Crabs; hepatopancreas; Wales 1989; coastal area
58.0 FW
41
18.5 FW 32.0 DW 68.0 DW 4.0 FW 520.0 FW
13 10 10 10 10
13.0-74.0 DW Max. 94.0 DW (6.8-10.9) FW
20 21 23
1.0-3.0 FW 3.0-5.0 FW 5.0-7.0 FW 7.0-20.0 FW
22 22 22 22
800.0 DW 300.0 DW 1060.0 DW not detectable 300.0 DW 700.0 DW 22,900.0 DW
48 48 48 48 48 48 48
1000.0 DW 80.0 DW 1700.0 DW not detectable 200.0 DW 400.0 DW 26,300.0 DW
48 48 48 48 48 48 48
Shrimp, Crangon vulgaris Whole Whole Blood Muscle Hepatopancreas Crustaceans Various tissues; 12 spp. Muscle Whole Commercial species; North America; edible tissues; 16 spp. 4 spp. 4. spp. 4 spp. 4 spp. Deep sea shrimps; Rainbow hydrothermal vent site; mid-Atlantic Ridge; summer 2002; adults; 2 spp. Rimicaris exoculata Whole body Cuticle Gill Antennae Muscle Digestive gland Pylorus Microcaris fortunata Whole body Cuticle Gill Antennae Muscle Digestive gland Pylorus
Reference
a
(Continues)
428 Chapter 7 Table 7.9:
Cont’d
Organism
Concentration
Benthic crab, Dorippe granulata; Hong Kong; contaminated harbor Exoskeleton Gills Hemolymph Midgut gland Muscle
7.7 DW 123.9 DW 53.2 FW 114.9 DW 36.6 DW
36 36 36 36 36
Crab, Eupagurus bernhardus Whole Blood Leg muscle Abdominal muscle Stomach fluid Hepatopancreas Excretory organs Gills Shell Vas deferens Ovary
25.0 DW 89.0 FW 8.4 FW 5.4 FW 2.0 FW 69.0 FW 16.0 FW 31.0 FW 4.9 FW 6.9 FW 11.0 FW
10 10 10 10 10 10 10 10 10 10 10
10.1 FW 15.6 (7.5-21.3) DW
24 16
55.0 (30.0-86.0) DW 58.0 (40.0-83.0) DW
37 37
Euphausiids Whole Whole Antarctic Ocean and Atlantic Ocean; whole; 1985-1986 Euphausia superba Meganyctiphanes norvegica
Reference
Euphausiid, Euphausia krohni; whole
600.0 AW
6
Euphausiid, Euphausia superba; Antarctica; whole
103.0 DW
44
264.0 DW vs. 44.0 DW
56
150.0 DW vs. 47.0 DW 2840.0 DW vs. 125.0 DW 2850.0 DW vs. 125.0 DW
56 56 56
Hydrothermal vent field; mid-Atlantic Ridge; 2001 Shrimp, Chlorocaris chacei;1700 m deep; digestive gland vs. muscle Hydrothermal crab, Segonzacia mesatlantica; digestive gland vs. muscle 840 m deep 1700 m deep 2300 m deep
a
(Continues)
Crustaceans 429 Table 7.9:
Cont’d
Organism
Concentration
Lobster, Galathea squamifera Whole Blood Muscle Hepatopancreas Gills
29.0 DW 77.0 FW 7.2 FW 603.0 FW 26.0 FW
10 10 10 10 10
11.0 DW vs. 3195.0 DW
43
33.0 DW 82.0 FW 6.0 FW 5.0 FW 438.0 FW 1.3 FW 17.0 FW 44.0 FW 8.0 FW 15.0 FW (6.2-13.2) FW 10.3 (6.0-18.0) FW 32.0 FW 3.0 FW 26.0 FW 335.0 FW 4.0 FW 50.0 FW 10.0 FW 1.0 FW 2.0 FW 17.0 FW
10 10 10 10 10 10 10 10 10 10 11 12 38 38 38 38 38 38 38 38 38 38
25.4 DW; max. 38.3 DW
45
25.0 DW 43.0 FW 3.2 FW 1.2 FW 65.0 FW
10 10 10 10 10
Mantis shrimp, Gonodactylus sp.; Guam; June 1998; muscle vs. gonad Lobster, Homarus vulgaris Whole Blood Muscle Stomach fluid Hepatopancreas Urine Excretory organs Gills Vas deferens Ovary Muscle Muscle Blood Exoskeleton Gill Liver Muscle Ovaries Stomach fluid Testes Urine Whole Blue shrimp, Litopenaeus stylirostris; Gulf of California, Mexico; 2004-2005; muscle Crab, Maia squinado Whole Blood Muscle Stomach fluid Hepatopancreas
Reference
a
(Continues)
430 Chapter 7 Table 7.9: Organism Urine Excretory organs Gills Shell Vas deferens Ovary
Cont’d
Concentration
Reference
0.2 FW 5.0 FW 25.0 FW 1.4 FW 3.0 FW 11.0 FW
10 10 10 10 10 10
Euphausiid, Meganyctiphanes norvegica Whole Fecal pellets
48.0 DW 226.0 FW
25 25
Peneid shrimp, Melicertus kerathurus; Lesina lagoon, Italy; October 2004; 3 sites Muscle Exoskeleton
6.6-26.0 DW 39.2-57.9 DW
58 58
Shrimp, Metapenaeus affinis; muscle
28.9 DW
26
Lobster, Nephrops norvegicus; muscle
(2.1-11.3) FW
11
Beach hopper (amphipod), Orchestia gammarellus; whole; North Sea; 19891990; reference site vs. contaminated site
Usually < 70.0 DW vs. > 145.0 DW; max. 340.0 DW
39
Amphipod, Orchestoidea corniculata; whole
(10.0-125.0) DW
27
Shrimp, Palaemon serratus Whole Blood Muscle Hepatopancreas Gills External eggs
30.0 DW 97.0 FW 3.5 FW 185.0 FW 55.0 FW 50.0 FW
10 10 10 10 10 10
Shrimp, Palaemon squilla; whole
31.0 DW
10
Shrimp, Palaemonetes varians Whole Blood Muscle Hepatopancreas
32.0 DW 180.0 FW 7.9 FW 137.0 FW
10 10 10 10
Lobster, Palinurus vulgaris Blood Muscle
103.0 FW (9.0-11.0) FW
10 10
a
(Continues)
Crustaceans 431 Table 7.9: Organism Stomach fluid Hepatopancreas Urine Excretory organs Gills Shell Ovary External eggs
Cont’d
Concentration
Reference
10.0 FW 163.0 FW 6.0 FW 20.0 FW 57.0 FW 3.0 FW 17.0 FW 5.0 FW
10 10 10 10 10 10 10 10
Amphipod, Paramoera walkeri; East Antarctica; 2003-2004; whole
(7.2-42.0) DW
44
Shrimp, Pandalus jordani; muscle
(1.1-8.2) FW; (6.7-40.0) DW
12
Marsh crab, Parasesarma erythodactyla; soft parts; 2002; New South Wales, Australia; metals-contaminated estuary Males Females
Max. 86.8 DW Max. 239.0 DW
53 53
Brown Shrimp, Penaeus aztecus Whole Muscle Exoskeleton Viscera
34.0 DW 24.2 (18.0-29.0) DW 32.4 DW 173.0 (65.0-260.0) DW
32, 33, 33, 33,
Shrimp, Penaeus japonica; muscle
14.0 DW
28
(21.5-48.3) DW
26
42.0 DW 1120.0 DW 28.2 DW
57 57 57
White shrimp, Peneus setiferus; muscle; Gulf of Mexico
17.3 DW
46
Shrimp; Penaeus spp.; whole
47.0 DW
29
Isopod, Porcellana platycheles; whole
27.0 DW
10
Crab, Portunus depurator Whole Blood Muscle
18.0 DW 87.0 FW 7.1 FW
10 10 10
Black tiger shrimp, Penaeus monodon Muscle Vietnam; 2003-2005; juveniles; max. values Exoskeleton Hepatopancreas Muscle
a
38 38 38 38
(Continues)
432 Chapter 7 Table 7.9: Organism Stomach fluid Hepatopancreas Urine Excretory organs Gills Shell Vas deferens
Cont’d
Concentration
Reference
8.1 FW 103.0 FW 0.2 FW 11.0 FW 35.0 FW 1.1 FW 14.0 FW
10 10 10 10 10 10 10
Crab, Portunus holsatus; whole
12.2 FW
30
Crab, Portunus pelagicus; muscle
(29.0-94.4) DW
26
Crab, Portunus puber Whole Blood Muscle Stomach fluid Hepatopancreas Urine Excretory organs Gills Shell Vas deferens Ovary
21.0 DW 113.0 FW 8.4 FW 36.0 FW 134.0 FW 0.9 FW 28.0 FW 36.0 FW 9.5 FW 17.0 FW 18.0 FW
10 10 10 10 10 10 10 10 10 10 10
Crab, Pugettia producta; whole
(15.0-60.0) AW
31
Shrimp Muscle Muscle; 2 spp.; Taiwan; 1995-1996 Exoskeleton Muscle Shell
31.1 DW Max. 27.5 DW 16.3 DW (2.4-4.5) FW (4.9-10.7) FW
33 40 33 19 19
Amphipod, Themisto spp.; whole; Antarctic Ocean and Atlantic Ocean; 1985-1986
28.0-31.0 (13.0-79.0) DW
37
Crab, Xantho incisus; whole
20.0 DW
10
Zooplankton; mostly copepods; NW Mediterranean Sea; whole
32.6 (5.9-121.1) DW
34
639.7 DW 152.7 DW
50 50
Fiddler crab, Uca pugnax; New Jersey Intermolt; contaminated site Soft tissue Carapace
a
(Continues)
Crustaceans 433 Table 7.9: Organism Intermolt; reference site Soft tissue Carapace Immediate postmolt; contaminated site Soft tissue Exoskeleton Immediate postmolt; reference site Soft tissue Exoskeleton Zooplankton; Baltic Sea; May 1999; cladocerans vs. copepods; whole
Cont’d
Concentration
Reference
518.9 DW 136.6 DW
50 50
306.5 DW 75.3 DW
50 50
194.4 DW 16.7 DW
50 50
2.0 DW vs. 25.1 DW
55
a
Values are in mg Cu/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Zafiropoulos and Grimanis, 1977; 2, Bohn and McElroy, 1976; 3, Polikarpov et al., 1979; 4, Barbaro et al., 1978; 5, Ireland, 1974; 6, Nicholls et al., 1959; 7, Boon, 1973; 8, Stenner and Nickless, 1975; 9, Greig et al., 1977b; 10, Bryan, 1968; 11, Topping, 1973; 12, Bernhard and Zattera, 1975; 13, Wharfe and Van Den Broek, 1977; 14, Martin et al., 1977; 15, Martin, 1970; 16, Martin and knauer, 1973; 17, Vinogradova and Koual’skiy, 1962; 18, Tijoe et al., 1977; 19, Won, 1973; 20, Stickney et al., 1975; 21, Stenner and Nickless, 1974a; 22, Hall et al., 1978; 23, Wright, 1976; 24, Greig and Wenzloff, 1977; 25, Fowler, 1977; 26, Zingde et al., 1976; 27, Bender, 1975; 28, Ishii et al., 1978; 29, Knauer, 1970; 30, DeClerck et al., 1979; 31, Boothe and Knauer, 1972; 32, Sims and Presley, 1976; 33, Horowitz and Presley, 1977; 34, Hardstedt-Romeo and Laumond, 1980; 35, Eustace, 1974; 36, Depledge et al., 1993; 37, Rainbow, 1989; 38, Jenkins, 1980; 39, Moore et al., 1991; 40, Han et al., 1998; 41, Morris et al., 1989; 42, Petri and Zauke, 1993; 43, Denton et al., 2006; 44, Palmer et al., 2006; 45, Frias-Espericueta et al., 2007; 46, Vazquez et al., 2001; 47, Turkmen et al., 2006; 48, Kadar et al., 2006; 50, Bergey and Weis, 2007; 51, Feng et al., 2006; 52, Silva et al., 2006; 53, MacFarlane et al., 2006; 54, Karouna-Renier et al., 2007; 55, Pempkowiak et al., 2006; 56, Colaco et al., 2006; 57, Tu et al., 2008; 58, D’Adamo et al., 2008; 59, Zauke and Schmalenbach, 2006.
always highest at that site. However, sites of copper accumulation, storage, and action vary widely among crustaceans. In C. maenas as one case, heavy metal-binding proteins in midgut gland protect midgut against high environmental levels of copper; the two proteins, of about 27,000 and 11,500 MW are associated with 0.9% and 34.4%, respectively, of the total midgut gland copper content (Rainbow and Scott, 1979). Biological and abiotic variables need to be considered in the interpretation of copper concentrations in crustaceans, including developmental stage, prior exposure to copper, chemical form of copper, temperature and salinity of the medium, chelators, season of collection, tissue specificity, pH, and many others. Selected examples follow for various crustacean groups. Molting is a feasible mechanism of copper depuration in the fiddler crab, Uca pugnax (Bergey and Weis, 2007). Average percent of total body copper burden eliminated during molting from a relatively clean site was 3% versus 12% from a metal-contaminated site. Prior to molting, crabs shifted copper from the carapace into soft tissues (Bergey and Weis, 2007;
434 Chapter 7 Table 7.9). Soft tissues of male, but not female, marsh crabs, P. erythodactyla, from a metalcontaminated estuary in Australia in 2002 reflected sediment copper concentrations; at higher salinities, copper content increased in males (MacFarlane et al., 2006). In the amphipod, Orchestia gammarellus, copper concentrations vary seasonally due to variable copper loadings, are higher in organisms from contaminated sites, and higher in females with juveniles in the brood pouch than females without juveniles (Moore et al., 1991). Marine amphipods readily accumulate dissolved copper from seawater in a dosedependent manner (Weeks and Rainbow, 1991). But some species of talitrid amphipods are unable to meet their copper requirements from seawater alone and depend on dietary sources of copper (Weeks and Rainbow, 1993). The tolerance of talitrid amphipods to high concentrations of ambient copper is attributable, in part, to the formation of intracellular copper granules within the cells of the ventral caeca (Weeks, 1992). The existence of copperrich granules is common to all invertebrate phyla; these granules are usually found in the digestive gland or its evolutionary equivalent, and their formation is related to high concentrations of copper in the immediate environment (Weeks, 1992). Gender-related differences in uptake, retention, and accumulation of copper and other metals are reported in crustaceans (Burger et al., 2007a; Rabitsch, 1995; Zodle and Whitman, 2003), but results are variable. Adult amphipods, Peramphithoe parmerong, were less likely to select coppercontaminated habitat or diet (Roberts et al., 2006). In a 30-day study, juvenile amphipods fed copper-contaminated macroalgae had 75% mortality, although no effect was observed on growth of survivors (Roberts et al., 2006). Among barnacles, certain developmental stages were extremely sensitive to Cu2+, resulting in impaired settling and growth (Pyefinch and Mott, 1948); it is probable that copper accumulation rates were higher in these stages. Barnacles, S. balanoides, held in seawater containing 0.02-0.09 mg Cu/L for 100 days show dose-dependent increases in copper loadings in body and egg masses (Powell and White, 1990). In barnacles, Balanus amphitrite nireus, the respiratory surface in the thorax is a primary copper absorption site with excretion usually through hindgut epithelia (Bernard and Lane, 1961, 1963). Inorganic granules found in parenchyma cells surrounding the midgut of Balanus balanoides contained 1200.0 mg Cu/kg, and this could account for the high copper burdens found in that species (Walker et al., 1975a,b; Walker, 1977). Nauplii of the barnacle Balanus amphitrite albicostatus, when compared to oyster eggs, sea urchin eggs, and adult rotifers, were 5-10 times more resistant to biocidal properties of copper sulfate during a 24-h period; for barnacle nauplii, the highest concentration tested without significant adverse effect was 1.0 mg Cu/L (Kobayashi, 1979). Interaction effects with other metals are documented and need to be considered in residue interpretation. For example, barnacles tend to accumulate cadmium—a potentially toxic metal—in the presence of copper (Powell and White, 1990). Barnacles attacked by flatworm predators can be treated successfully with copper. For example, barnacles, Balanus variegatus, infested with free-living flatworms, Stylochus pygmaeus,
Crustaceans 435 treated with 0.025 mg Cu/L for 10 days resulted in reduced egg deposition and hatching success of flatworms by 80%, although barnacle feeding rate was inhibited during copper treatment (Lee and Johnston, 2007). Whole-body copper accumulation in the euryhaline copepod A. tonsa is dependent on salinity, decreasing as salinity increased (Pinho et al., 2007). In the salinity range 5-30 ppt, copper-exposed copepods had higher whole-body sodium concentrations at higher salinities and lower sodium concentrations at lower salinities. Physiological effects induced by waterborne copper exposure to A. tonsa acclimatized to salinities of 15-30 ppt are due to a combined effect of food restriction and copper exposure and not due to differences in wholebody copper burden (Pinho et al., 2007). Based on 96-h toxicity tests, copepods, T. japonicus, were more sensitive to copper in summer than in winter, and more sensitive to copper acetate than to copper chloride or copper sulfate (Bao et al., 2008). Adverse effects of copper on survival of copepods are reduced or eliminated by the presence of clay minerals, diatoms, ascorbic acid, sewage effluents, water extracts of humic acid, and certain soil types (Lewis et al., 1972). Chelators, such as EDTA, and more alkaline pH increase the survival and larval developmental rates of copepods challenged with copper through increased complexation of cupric ions (Sunda et al., 1990). Copper uptake by brine shrimp, Artemia franciscana, increases with decreasing pH and decreasing carbonate complexation (Blust et al., 1991). Copper is toxic to the copepod, A. tonsa, when fed a copper-contaminated phytoplankton diet (Bielmyer et al., 2006). In that study, diatoms, Thalassiosira pseudonana, were held in seawater containing 0.0012 mg Cu/L for 7 days, reaching a copper concentration of 22.3 mg Cu/kg DW diatom; this, in turn, was fed to Acartia for 7 days, producing a 20% reduction in copepod reproduction. Authors note that the current water quality criterion for marine life protection is 0.003 mg Cu/L, far in excess of the 0.0012 mg Cu/L used in this study to produce a toxic diet (Bielmyer et al., 2006). Copper is increasingly toxic to the copepod E. affinis with increasing salinity in the range 5-25 ppt, and increasingly less toxic with increasing dissolved organic carbon in the range 2.0-8.0 mg/L (Hall et al., 2008). Acute toxicity bioassays of 96-h duration with adults of T. japonicus copepods—a species recommended for routine ecotoxicity testing in the western Pacific Ocean region—showed that all survived 1.0 mg Cu/L, 10% died at 2.2 mg/L, and 30% died at 3.9 mg Cu/L (Lee et al., 2007). Soldier crabs, Mictyris longicarpus, take up copper mainly from sediments rather than the water column (Weimin et al., 1994). The fine particles of sediment trapped as food contain bioavailable fractions of copper and other metals, and these significantly correlate with metal concentrations in crab tissues. However, copper accumulated from sediments by soldier crabs occurs only at an artificially high level (1900.0 mg Cu/kg DW sediment), which also had toxic effects. Soldier crabs seem unable to regulate copper within the body (Weimin et al., 1994); however, many marine decapod crustaceans reportedly regulate tissue copper concentrations within the range of 25.0-35.0 mg kg DW tissue (Neff and Anderson, 1977). Transfer of copper from wood treated with chromated copper arsenate is documented
436 Chapter 7 in fiddler crabs, Uca spp. (Weis and Weis, 1992). In the crab Carcinus mediterraneus, tissue copper concentrations are lower in winter than in summer and correlate positively with total protein and hemolymph copper contents (Devescovi and Lucu, 1995). Elevated copper burdens in crab hemolymph probably reflect the incorporation of copper atoms in the structure of hemocyanin, the major hemolymph protein (Depledge et al., 1993). Starved shore crabs show a reduction in carapace copper content; starvation in combination with copper exposure (0.5 mg Cu/L) results in an increase in carapace copper and a decrease in carapace calcium (Scott-Fordsmand and Depledge, 1993). In C. maenas, ionic copper displaces ionic magnesium in gills, leading to inhibition of phosphoryl transfer (Hansen et al., 1992b). The question of physiological adaptation to copper is unresolved. In one case, progeny of brine shrimp, A. salina, showed high tolerance to 1.0 mg Cu/L, when compared to controls, after exposure for two or three generations to 0.025-0.1 mg Cu/L; however, this tolerance diminished in successive generations (Saliba and Ahsanullah, 1973). At any given copper concentration, growth inhibition of A. salina previously acclimatized to 0.100, 0.050, or 0.025 mg Cu/L was least in cupric sulfate, and increased progressively in chloride, acetate, and carbonate salts (Saliba and Krzyz, 1976). But in survival tests with unacclimatized Artemia adults and larvae, cupric chloride was least toxic, followed progressively by sulfate, chloride, and acetate salts (Saliba and Krzyz, 1976). Temperature of the medium affects the biocidal properties of copper salts, and presumably copper accumulation rates. In one study the shrimp, Pandalus danae, was more sensitive to copper at 20 C than at 10 C (Gibson et al., 1976), and lobsters, H. americanus, stressed by copper survived longer at 5 C than at 13 C (McLeese, 1974). The season of collection was linked to copper burdens in crab muscle (Boon, 1973) and whole copepods (HardstedtRomeo and Laumond, 1980); these differences were not wholly explainable on the basis of water temperature. Decreasing salinity of the medium was associated with decreasing survival of isopods at tested copper concentrations (Jones, 1975), and this appears to corroborate trends reported by others for different groups of marine biota. Copper absorption was coincident with the presence of other substances, especially calcium in barnacles (Bernard and Lane, 1961), mercury in copepods (Barnes and Stanbury, 1948; Reeve et al., 1977), and chelating agents in copepods (Lewis et al., 1972, 1973). In isopods, copper seems to move freely in an easily dissociable state between storage cells and other cells of the hepatopancreas (Wieser, 1967). Granular chitin from lobster shells absorbed 40-60% of copper in seawater in 183 h, with accumulation independent of initial copper concentration in the range 1.0-16.0 mg Cu/L (Yoshinari and Subramanian, 1976). This last observation may have application in environmental programs to control or monitor metals wastes in saline waters. No documented report of fatal copper deficiency is available for any species of aquatic organism, and no correlation is evident in aquatic biota for the presumed nutritional copper requirements and its sensitivity to dissolved copper (Neff and Anderson, 1977). However,
Crustaceans 437 extremely low copper concentrations in whole bodies of 2 of 17 species of crustaceans (5.5 and 6.7 mg/kg DW) from the Antarctic Ocean support the hypothesis that certain Antarctic crustaceans may show copper deficiency or reduced metal requirements (Petri and Zauke, 1993). Amphipods collected in 2003-2004 from Antarctica show increasing concentrations of whole-body copper with increasing age (Palmer et al., 2006), suggesting a need for copper in reproduction. Amphipods, P. walkeri, from the Australian Antarctic Territory in 1999-2000 had whole-body bioconcentration factors of 1700-3800 when the seawater medium contained 0.0001-0.0002 mg Cu/L; however, BCFs decreased with increasing seawater concentration (Clason et al., 2003). Paramoera showed increased sensitivity when seawater concentrations were between 0.002 and 0.003 mg Cu/L (Clason et al., 2003). Copper is lethal to sensitive crustaceans in the range of 0.01-0.16 mg/L. Some deaths were reported in amphipods, Allorchestes compressa, during immersion in 0.01 mg Cu/L for 4 weeks (Ahsanullah and Williams, 1991), in T. japonicus copepods at 0.01 mg/L for one generation (Lee et al., 2008), in Melita spp. amphipods at 0.04 mg/L in 96 h (King et al., 2006a,b), in copepods Acartia spp., in 96 h at 0.031-0.052 mg Cu/L (USEPA, 1980b), and in a marine cladoceran, Moina monogolica in 48 h at 0.099-0.112 mg Cu/L (Wang et al., 2007a). Norway lobsters, Nephrops norvegicus, all died in 14 days when held in seawater containing 0.1 mg Cu/L (Canli and Furness, 1993). Half the larvae of a peneid shrimp, Metapeneus ensis, held in 0.16 mg Cu/L for 48 h died (Wong et al., 1993). Among amphipods, juveniles were more sensitive to copper than were adults, and epibenthic amphipods were more sensitive than infaunal tube-dwelling amphipods (King et al., 2006a,b). Tissue hypoxia through gill destruction is probably the major cause of copper-induced death in crustaceans (Nonnotte et al., 1993). The horseshoe crab, Limulus polyphemus, is relatively resistant to copper, although populations from New Jersey and Delaware show differential embryo sensitivity: LC-50 (72 h) values for embryos were 2.0 mg Cu/L for the New Jersey population versus 171.0 mg/L for the Delaware population (Botton et al., 1998). Other species were remarkably resistant, with significant mortality at more than 2.0 mg Cu/L for C. maenas, and more than 10.0 mg Cu/L for others (Scott-Fordsmand and Depledge, 1993). Sublethal effects include adverse effects on growth of a copepod, Tisbe furcata, at 0.057 mg Cu/L (Bechmann, 1994); increased copper uptake and lowered egg production in the amphipod C. volutator at 0.1 mg Cu/L, with effects exacerbated at low dissolved oxygen (Ericksson and Weeks, 1994); and reduced growth and high uptake in amphipods surviving 0.01 mg Cu/L for 4 weeks (Ahsanullah and Williams, 1991). Other sublethal effects of copper intoxication include abnormal variation in enzyme activities. In A. salina, for example, amylase activity was disrupted within 24 h and trypsin activity within 72 h by 2.0 mg Cu/L (Alayse-Danet et al., 1979). At high sublethal concentrations of waterborne copper for several days, shore crabs experienced extensive damage to the gill epithelium (Nonnotte et al., 1993), and altered enzyme and ATPase activity (Hansen et al., 1992a,b). Chinese mitten crabs, Eriocheir sinensis, exposed to graded concentrations of Cu2+ for 10
438 Chapter 7 days showed gill and hepatopancreas histopathology and metallothionein induction (Yang et al., 2007, 2008). No damage effects were evident at 0.01 mg Cu/L; however, metallothionein induction was maximal at 0.1 mg Cu/L and histopathology evident at 0.1-5.0 mg Cu/L. The current Chinese National Water Quality Standard for Fisheries is 0.01 mg Cu/L, but this is routinely exceeded in many regions to at least 0.07 mg Cu/L from copper sulfate, used extensively as an algicide in culture of the Chinese mitten crab and other crustaceans (Yang et al., 2007). The maximum acceptable toxicant concentration (MATC) for the cladoceran Moina mongolica, wherein the lower value indicates no measurable effect (here the test period is 21 days), and the higher value has some observable effect (here reduced brood size) is in the range 0.0051-0.0089 mg Cu/L (Wang et al., 2007a). Dietary toxicity of copper is also reported for M. mongolica fed green alga, Chlorella pyrenoidosa, containing various concentrations of copper for 21 days (Wang et al., 2007b). Adverse effects were documented when Moina ate algae exposed to 0.044 mg Cu/L and higher for 96 h; effects included reduction in brood size and net reproductive rate (Wang et al., 2007b). The formation of copper granules as a cellular response to copper detoxification along with normal storage of copper during the molt cycle is a proposed strategy to cope with copper insult by crustaceans (Correia et al., 2002). In one case, amphipods, Gammarus lacustris, that were subjected to sublethal concentrations of copper via seawater or copper-spiked sediments, accumulated copper as Cu-S granules stored in the hepatopancreas. The abundance of the granules increased with increasing whole-body copper content. The presence of sulfur within the granule represents an organic detoxification mechanism for copper (Correia et al., 2002). In another case, T. japonicus copepods were exposed for 7 days to high sublethal concentrations of copper (Barka, 2007). Copper localized in digestive epithelium cells and cuticular integument. Copper-containing granules were found in copperexposed copepods and in controls within lysosomes, intracellular calcospherites, and extracellular granules. Similar results were reported for T. japonicus and other metals tested, suggesting a generalized model for crustaceans coping with metal stress (Barka, 2007). Proposed copper criteria to protect most marine resources include less than 0.004-0.005 mg Cu/L and less than 5.0-15.0 mg Cu/kg DW sediments; for human health protection, this value is less than 30.0 mg Cu/kg DW in seafood (Eisler, 2000f).
7.14 Dysprosium Whole amphipods from east Antarctica in 2003-2004 contained a maximum of 0.014 mg Dy/kg DW (Palmer et al., 2006).
7.15 Erbium Whole amphipods, P. walkeri, from east Antarctica contained a maximum of 0.007 mg Er/kg DW (Palmer et al., 2006).
Crustaceans 439
7.16 Europium In 1977, whole euphausiids contained less than 4.5 mg Eu/kg DW, the detection limit at that time (Table 7.10). In 2004, however, whole amphipods contained up to 0.005 mg Eu/kg DW, the improved detection limit (Palmer et al., 2006).
7.17 Gadolinium Whole amphipods, P. walkeri, from east Antarctica in 2003-2004 contained 0.007-0.016 mg Gd/kg DW (Palmer et al., 2006).
7.18 Gallium Maximum gallium concentrations in field collections—based on limited data—were 40.0 mg Ga/kg on an AW basis and 0.36 mg Ga/kg on a DW basis (Table 7.10). Table 7.10: Europium, Gallium, Germanium, and Gold Concentrations in Field Collections of Crustaceans Element/Organism
Concentration
Reference
a
Europium Amphipod, Paramoera walkeri; East Antarctica; 2003-2004; whole
Max. 0.005 DW
7
Euphausiid, Meganyctiphanes norvegica; whole
<4.5 DW
1
Copepods; whole
40.0 AW
2
Crustaceans; whole
(0.03-0.36) DW
3
Barnacle, Lepas sp.; whole
0.006 FW
4
Crab, Portunus sp.; whole
(0.00-0.01) FW
4
Shrimp; whole
(0.002-0.025) FW
4
0.0046 AW 0.00028 DW
5 6
Gallium
Germanium
Gold Shrimp, Pandalus sp. Whole Soft parts
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Fowler, 1977; 2, Vinogradova and Koual’skiy, 1962; 3, Culkin and Riley, 1958; 4, Johnson and Braman, 1975; 5, Fukai and Meinke, 1959; 6, Fukai and Meinke, 1962; 7, Palmer et al., 2006.
440 Chapter 7
7.19 Germanium Germanium concentrations in field collections—on a FW basis—ranged from nondetectable to 0.025 mg Ge/kg (Table 7.10).
7.20 Gold Data on gold concentrations in field collections of crustaceans are scarce and concentrations— based on a single species—were 0.0046 mg Au/kg AW and 0.00028 mg Au/kg on a DW basis (Table 7.10). A laboratory study was conducted with radiogold and blue crab, C. sapidus. Crabs given an oral dose of radiogold were measured for radioactivity 4 days post exposure; almost all of the retained radiogold was in digestive gland and gut (Duke et al., 1966).
7.21 Holmium A single datum is available indicating that whole amphipods, P. walkeri, from east Antarctica in 2003-2004 contained less than 0.005 mg Ho/kg DW, the detection limit at that time (Palmer et al., 2006).
7.22 Iron It is clear that iron concentrations vary widely between and among species with different tissues, depth of collection, and geographic locale (Table 7.11). Maximum iron concentrations, in mg Fe/kg DW, are documented for whole copepods collected near a Taiwan sewage outfall (7255.0), whole crustaceans from Antarctica (1080.0), all tissues from deep sea shrimps (920.0-179,720.0), and euphausiid fecal pellets (24,000.0) (Table 7.11). The ability of various crustacean groups to accumulate iron from the medium, as judged by bioconcentration factors, ranged from 250,000 for whole copepods (Ketchum and Bowen, 1958) to 4000 for whole noncopepod crustaceans (Ichikawa, 1961), to 1800 for lobster muscle (Van As et al., 1973). During intermolt stages, blue crabs, C. sapidus, accumulated greatest iron concentrations in gill tissue: up to 500.0 mg Fe/kg gill on a FW basis. A concentration ratio of only 30 was reported for the euphausiid, M. norvegica, with about a third of the accumulated iron lost on transfer to iron-free water for 12 h (Antonini-Kane et al., 1972); however, the uptake portion of that study was of relatively short duration. High levels of iron occur in barnacles, B. balanoides, from Menai Straits, United Kingdom (Walker et al., 1975a,b). This species contains inorganic granules or concretions in parenchyma cells surrounding the midgut; concentrations of iron in these granules are estimated at 1100.0 mg/kg FW, and this might account for the elevated iron levels sometimes
Crustaceans 441 Table 7.11: Iron Concentrations in Field Collections of Crustaceans Organism
Concentration
Copepod, Acartia clausi; whole
5200.0 FW
1
Amphipods; whole
87.0 DW
2
Barnacles; Natal, Brazil; summer 2001; soft parts Fistulobalanus citerosum Balanus amphitrite
(371.0-527.0) DW 466.0 DW
24 24
Blue crab, Callinectes sapidus Whole Muscle; August 2005; Turkey
143.0 FW 14.3 (2.1-45.3) DW
4 21
Crab, Cancer irroratus; gills
500.0 FW
5
78.0 DW 197.0 DW 59.0 DW 40,000.0 AW 2900.0 AW vs. 4200.0 AW
2 6 7 8 9
Copepods Whole Whole Whole Whole Whole; surface vs. > 99 m collection depth Whole; 3 spp.; Taiwan; near sewage outfall
Reference
256.0-7255.0 DW
23
Crustaceans; whole
(146.0-1045.0) DW
10
Crustaceans; whole; 4 spp.; 2004; Antarctica
72.0-1108.0 DW
20
35,600.0 DW 3200.0 DW 90,460.0 DW 920.0 DW 610.0 DW 6640.0 DW 138,990.0 DW
22 22 22 22 22 22 22
6600.0 DW 6960.0 DW 122,970.0 DW 12,360.0 DW
22 22 22 22
Deep sea shrimps; 2 spp.; adults; Rainbow hydrothermal vent site; mid-Atlantic Ridge; summer 2002 Rimicaris exoculata Whole body Cuticle Gill Antennae Muscle Digestive gland Pylorus Microcaris fortunata Whole body Cuticle Gill Antennae
a
(Continues)
442 Chapter 7 Table 7.11: Cont’d Organism
Concentration
Reference
940.0 DW 3010.0 DW 179,720.0 DW
22 22 22
15.3 DW
19
Euphausiids Whole Whole
92.0 DW 100.0 FW
6 1
Lobster, Jasus lalandi Muscle Muscle
17.0 FW 2.9 FW
11 12
Lobster Muscle Carapace Head
34.0 AW 100.0 AW 130.0 AW
13 13 13
Euphausiid, Meganyctiphanes norvegica Whole Fecal pellets Molts Eggs
64.0 DW 24,000.0 DW 232.0 DW 330.0 DW
14 14 14 14
Amphipod, Orchestoidea corniculata; whole
(100.0-225.0) DW
15
Amphipod, Paramoera walkeri; East Antarctica; 2003-2004; whole
(98.0-164.0) DW
19
Muscle Digestive gland Pylorus Euphausiid, Euphausia superba; East Antarctica; 2003-2004; whole
Shrimp, Penaeus aztecus Muscle Exoskeleton Viscera
14.2 DW 45.1 DW 338.0 DW
3 3 3
Shrimp, Penaeus japonica; muscle
76.0 DW
16
Shrimp, Penaeus sp. Whole Whole
76.0 FW 50.0 DW
4 17
Crab, Pugettia producta; feces
(750.0-1650.0) AW
18
Shrimps Muscle Exoskeleton
40.2 DW 235.0 DW
a
3 3 (Continues)
Crustaceans 443 Table 7.11: Organism Muscle Carapace Whole Stomatopod, Squilla oratoria; muscle
Cont’d
Concentration
Reference
920.0 AW 8300.0 AW 640.0 AW
13 13 13
29.0 DW
16
a
Values are in mg Fe/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Fujita et al., 1969; 2, Bohn and McElroy, 1976; 3, Horowitz and Presley, 1977; 4, Wolfe et al., 1973; 5, Martin, 1973; 6, Martin and Knauer, 1973; 7, Tijoe et al., 1977; 8, Vinogradova and Koual’skiy, 1962; 9, Martin, 1970; 10, Culkin and Riley, 1958; 11, Van As et al., 1975; 12, Van As et al., 1973; 13, Lowman et al., 1970; 14, Fowler, 1977; 15, Bender, 1975; 16, Ishii et al., 1978; 17, Knauer, 1970; 18, Boothe and Knauer, 1972; 19, Palmer et al., 2006; 20, Santos et al., 2006; 21, Turkmen et al., 2006; 22, Kadar et al., 2006; 23, Feng et al., 2006; 24, Silva et al., 2006.
observed in Balanus spp. (Walker et al., 1975a,b). Iron was associated with soluble proteins in the hepatopancreas and hemolymph of Cancer pagurus. In hepatopancreas, iron was generally associated with high molecular weight proteins of about 450,000, which might be crustacean ferritin, an iron-storing protein (Guary and Negrel, 1980). In hemolymph, a common carrier protein for iron and plutonium of MW near 250,000 was demonstrated (Guary and Negrel, 1980). Iron content of fecal pellets from the crab Pugettia producta fed with brown alga Macrocystis pyrifera was up to 14 times higher than algal iron content, suggesting that fecal material is significant in iron cycling in the marine environment (Boothe and Knauer, 1972). Fecal deposition of euphausiids, M. norvegica, contributed substantially to iron fluxes in the Mediterranean Sea: a daily rate of 910.0 mg Fe/kg DW pellets was estimated for that species (Fowler, 1977). A similar pattern was observed, though not as pronounced, for arsenic, cobalt, manganese, lead, and zinc (Boothe and Knauer, 1972). Frequency of molting is also a factor in iron transfer through marine ecosystems owing to the observations that some species contained more than 28% of total organism iron in molts (Fowler, 1977; Horowitz and Presley, 1977; Lowman et al., 1970).
7.23 Lanthanum Whole amphipods, P. walkeri, from east Antarctica had 0.10-0.17 mg La/kg DW (Palmer et al., 2006).
7.24 Lead Most of the lead in crustaceans is localized in the exoskeleton, with comparatively low residues in other tissues (Table 7.12).
444 Chapter 7 Table 7.12: Lead Concentrations in Field Collections of Crustaceans Organism
Concentration
Reference
Copepod, Anomalocera patersoni; whole; males vs. females
6.0 DW vs. 3.5 DW
1
Barnacle, Balanus amphitrite; soft parts
(7.1-11.7) DW
2
Copepod, Calanus finmarchicus; whole
575.0 AW
3
Blue crab, Callinectes sapidus Pensacola, Florida; 2003-2004; hepatopancreas vs. muscle Whole Muscle; August 2005; Iskenderun Bay, Turkey
Max. 0.36 FW vs. max. 0.39 FW <0.2 DW 3.5 (0.43-6.9) DW
31 6 27
Crab, Cancer irroratus Muscle Digestive gland Gills
(<0.5-3.4) FW (<0.6-1.3) FW (0.9-2.9) FW
4 4 4
Crab, Cancer pagurus; whole
<0.8 FW
5
Copepod, Centropages spp.; whole
1300.0 AW
3
Copepods Whole Whole Whole; 3 spp.; Taiwan; near sewage outfall
150.0 AW 3.3 DW 2.6-56.2 DW
Crabs Muscle Shell Crustaceans Whole Whole; 12 spp. 16 commercial species; North America; edible tissues 5 spp. 9 spp. 2 spp.
0.50 FW 0.66 FW
a
7 8 28
9 9
Max. 31.0 DW 0.03-0.94 DW
10 11
0.4-0.6 FW 0.6-0.7 FW 0.7-0.9 FW
12 12 12
Euphausiid, Euphausia krohni; whole
20.0 AW
3
Euphausiid, Euphausia superba; Antarctica; 2003-2004; whole
0.01 DW
24 (Continues)
Crustaceans 445 Table 7.12:
Cont’d
Organism
Concentration
Euphausiids; whole
2.1 DW
Greenland; 1978-1993; 6 spp. Exoskeleton Muscle
0.08-0.18 FW 0.01-0.05 FW
Lobster, Homarus vulgaris; muscle
<0.4 FW
Blue shrimp, Litopenaeus stylirostris; muscle; Gulf of California, Mexico; 2004-2005
5.3 (3.2-9.6) DW
25
Lobster; digestive gland; total lead vs. tetraalkyllead
0.20 FW vs. 0.16 FW
13
Euphausiid, Meganyctiphanes norvegica; molts
22.0 DW
14
0.47-0.68 DW 1.8-5.7 DW
35 35
2.1 DW
38
0.9 DW 0.5 DW
38 38
Peneid shrimp, Melicertus kerathurus; Lesina lagoon, Italy; October 2004; 3 sites Muscle Exoskeleton Mexico; Gulf of California; 1999-2000 Barnacle, Balanus eburneus; soft parts Shrimps; muscle Litopenaeus stylirostris Litopenaeus vanamei
Reference 8 20 20 5
Lobster, Nephrops norvegicus; muscle
(<0.2-0.5) FW
Grass shrimp, Palaemonetes pugio; whole; Virginia Natural marsh area Spoil disposal area
0.2 DW 11.0 DW
22 22
(0.4-1.7) DW
24
Shrimp, Pandalus montagui; soft parts Sewage dump site Reference site
31.0 DW 24.0 DW
23 23
Marsh crab, Parasesarma erythodactyla; soft parts; 2002; New South Wales, Australia; metals-contaminated estuary Males Females
Max. 132.0 DW Max. 193.0 DW
30 30
Amphipod, Paramoera walkeri; East Antarctica; 2003-2004; whole
a
5
(Continues)
446 Chapter 7 Table 7.12: Cont’d Organism
Concentration
Shrimp, Penaeus aztecus Muscle Exoskeleton Viscera Whole
1.1 DW 17.1 DW 2.8 DW 20.2 DW
15 15 15 6
Black tiger shrimp, Penaeus monodon; Vietnam; 2003-2005; juveniles; max. values Muscle Exoskeleton Hepatopancreas
0.02 DW 0.33 DW 0.34 DW
34 34 34
White shrimp, Peneus setiferus; muscle; Gulf of Mexico
7.7 DW
26
Crab, Portunus holsatus; whole
1.3 FW
16
Crab, Pugettia producta; feces
(27.0-40.0) AW
17
Shrimps Muscle Exoskeleton Muscle Shell
1.6 DW 15.4 DW (0.24-1.2) FW (0.44-1.2) FW
15 15 9 9
Max. 1.6 FW
21
41.4 DW 41.2 DW
28 28
20.4 DW 27.0 DW
28 28
18.3 DW 129.8 DW
28 28
11.5 DW 33.1 DW
28 28
3.7 (2.0-7.0) FW 13.4 (3.0-26.0) DW
18 18
Spain; Tarragona coast; commercial species; edible parts Fiddler crab, Uca pugnax; New Jersey Intermolt; contaminated site Soft tissue Carapace Intermolt; reference site Soft tissue Carapace Immediate postmolt; contaminated site Soft tissue Exoskeleton Immediate postmolt; reference site Soft tissue Exoskeleton Shrimp, Xiphopenaeus krogeri Whole Whole
Reference
a
(Continues)
Crustaceans 447 Table 7.12:
Cont’d
Organism
Concentration
Zooplankton Surface vs. > 99 m collection Baltic Sea; May 1999; cladocerans vs. copepods; whole
117.0 AW vs. 183.0 AW 1.0 DW vs. 13.3 DW
Reference
a
190 32
Values are in mg Pb/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Polikarpov et al., 1979; 2, Barbaro et al., 1978; 3, Nicholls et al., 1959; 4, Greig et al., 1977b; 5, Topping, 1973; 6, Sims and Presley, 1976; 7, Vinogradova and Koual’skiy, 1962; 8, Martin and Knauer, 1973; 9, Won, 1973; 10, Stenner and Nickless, 1974a,b; 11, Stickney et al., 1975; 12, Hall et al., 1978; 13, Sirota and Uthe, 1977; 14, Fowler, 1977; 15, Horowitz and Presley, 1977; 16, DeClerck et al., 1979; 17, Boothe and Knauer, 1972; 18, Bernhard and Zattera, 1975; 19, Martin, 1970; 20, Dietz et al., 1996; 21, Schuhmacher et al., 1990; 22, Drifmeyer and Odum, 1975; 23, Mackay et al., 1972; 24, Palmer et al., 2006; 25, Frias-Espericueta et al., 2007; 26, Vazquez et al., 2001; 27, Turkmen et al., 2006; 28, Bergey and Weis, 2007; 29, Feng et al., 2006; 30, MacFarlane et al., 2006; 31, KarounaRenier et al., 2007; 32, Pempkowiak et al., 2006; 33, Ruelas-Inzunza znd Paez-Osuna, 2008; 34, Tu et al., 2008; 35, D’Adamo et al., 2008.
Lead tissue burdens in the red fingered marsh crab, P. erythodactyla, collected in 2002 from an Australian estuary contaminated with lead and other metals, reflected lead sediment levels; this pattern held for both males and females (MacFarlane et al., 2006; Table 7.12). Glutathione peroxidase activity was elevated in crabs with elevated metal burdens, and, in females only, an increase in lipid peroxidation products (MacFarlane et al., 2006). Amphipods, Elasmopus laevis, held on sediments containing 58.0-424.0 mg Pb/kg DW as lead acetate for 60 days and two generations had reduced fecundity and increased body lead burdens proportional to lead sediment concentrations (Ringenary et al., 2007). Amphipods held on sediments containing 118.0 mg Pb/kg DW and higher had reduced population size when compared to control sediments containing 30.0 mg Pb/kg DW. On the basis of this study, authors propose a sediment lead concentration guideline of less than 118.0 mg Pb/kg DW (Ringenary et al., 2007). Amphipods, P. walkeri, from the Australian Antarctic Territory in 1999-2000 had wholebody bioconcentration factors of 1600-7000 when seawater contained 0.00001-0.0001 mg Pb/L; BCFs decreased at higher seawater concentrations (Clason et al., 2003). Paramoera showed increased sensitivity when seawater concentrations ranged from 0.00012 to 0.00025 mg Pb/L (Clason et al., 2003). Molting is an important pathway for lead depuration in the fiddler crab, U. pugnax (Bergey and Weis, 2007). Average percent of total body lead eliminated by Uca during molting from a relatively clean site was 56%, and for a metal-contaminated site it was 76%. Prior to molting, crabs shifted lead from soft tissues to exoskeleton in contaminated areas, and the reverse for the relatively clean site (Table 7.12; Bergey and Weis, 2007). In the euphausiid,
448 Chapter 7 M. norvegica, molts represent most of the lead body burden and are probably more significant than fecal pellets in lead cycling processes (Fowler, 1977). The influence of deposited lead on surface sand meiofauna communities is not known with certainty, although harpacticoid copepods were among the most sensitive groups in that niche when subjected to lead contamination (Roberts and Maguire, 1976). Radiolead-210 concentrations in whole crustaceans were approximately 100 times higher than seawater; the highest 210Pb concentration factors were found in shrimp, Sergestes spp., ranging from a low of 10 in muscle up to 1,000,000 in hepatopancreas (Heyraud and Cherry, 1979). Whole shrimp, C. crangon, held in seawater containing 0.018 mg Pb/L for 8 days had a bioconcentration factor of 750 (Jung and Zauke, 2008). Many factors influence lead accumulation rates in crustaceans. For example, lead concentrations in barnacles, B. balanoides, vary according to the time of the year when samples were taken, site of collection, reproductive state of the barnacles, tidal flows, and fluvial lead concentrations (Ireland, 1974). Significant differences were evident in lead content of male and female copepods, Anomalocera patersoni, from the Mediterranean Sea (Polikarpov et al., 1979). These differences were demonstrated for other metals examined, including chromium, copper, and cadmium. Data on lead accumulations by crustaceans under controlled conditions show that U. pugilator fiddler crabs contain 2.04 mg Pb/kg whole fresh organism after exposure for 14 days in 0.1 mg Pb/L (Weis, 1978). In another study, zinc-lead mixtures prolong hatching times of Rithropanopeus harrisii megalops (Benijts-Claus and Benijts, 1975); zinc may have influenced lead uptake rates in that study. Decreasing salinity and increasing temperature were associated with elevated body burdens in lead-stressed marine isopods (Jones, 1975). Lethal properties of lead compounds to crustaceans are dependent on the formulation. For the shrimp, C. crangon, LC50 (96 h) values—in mg Pb/L—are 375.0 for inorganic ionic lead, 8.8 for trimethyllead, 5.8 for triethyllead, 0.110 for tetramethyllead, and 0.02 for tetraethyllead (Maddock and Taylor, 1980). American lobsters, H. americanus, held for 30 days in 0.05 mg inorganic Pb/L all survived, but show reduced Delta aminolevulinic acid dehydratase activity, biochemical alterations in antennal gland, and bioconcentration factors of 2760 for antennal gland and 58 for gill (Gould and Greig, 1983; USEPA, 1985b).
7.25 Lithium Planktonic copepods from the Black Sea reportedly contain 400.0 mg Li/kg whole organism on an AW basis (Vinogradova and Koual’skiy, 1962).
7.26 Lutetium Amphipods collected in east Antarctica in 2003-2004 had <0.006 mg Lu/kg DW whole organism or below the current detection limit (Palmer et al., 2006).
Crustaceans 449
7.27 Manganese In general, manganese concentrations in field collections of crustaceans were highest in calcified tissues and lowest in muscle (Table 7.13). In the dungeness crab, C. magister, manganese concentrations were highest in setae and calcareous exoskeleton, presumably because of surface-adsorbed MnO2 (Tennant and Forster, 1969). Manganese values in barnacle shells range from 80.0 to 3800.0 mg/kg on a DW basis; these values were directly related to the concentration of manganese in the ambient seawater, which in turn was directly related to salinity (Gordon et al., 1970). About 98% of the manganese in the body of lobsters, Homarus vulgaris, is in the calcified exoskeleton (Bryan and Ward, 1965). Manganese is lost from lobster blood during starvation and is absorbed so slowly from seawater that most manganese is absorbed from the diet. Primary losses of manganese from Mn-loaded lobsters occur via urinary excretion (20-40%), across the body surface (40-80%), and via the feces (up to 20%). It is possible that some absorption and release of manganese by exoskeleton occurs and this may assist in maintaining blood and tissue manganese concentrations (Bryan and Ward, 1965). Manganese
Table 7.13: Manganese Concentrations in Field Collections of Crustaceans Organism
Concentration
Copepod, Acartia clausi; whole
188.0 FW
Barnacles; summer 2001; Natal, Brazil; soft parts Fistulobalanus citerosum Balanus amphitrite
(9.4-28.1) DW 9.6 DW
19 19
Blue crab, Callinectes sapidus whole Muscle; August 2005; Turkey
25.0 FW 4.8 (0.1-15.4) DW
2 17
Crab, Cancer irroratus Muscle New York Bight New York Bight dumpsite Long Island Sound Delaware dumpsite Chincoteague inlet, Virginia Digestive gland Gills Long Island Sound Chincoteague inlet
Reference
a
1
1.1 FW 0.8 FW 28.7 FW 1.4 FW 0.8 FW (<0.6-3.0) FW
3 3 3 3 3 3
22.1 FW 5.7 FW
3 3 (Continues)
450 Chapter 7 Table 7.13: Cont’d Organism
Concentration
Reference
Copepods Whole Whole Whole; 3 spp.; Taiwan; near sewage outfall
500.0 AW 4.4 DW 5.5-80.8 DW
4 5 18
Shrimp, Crangon sp.; whole
1.2 DW
20
Crustaceans; North America; 16 commercial species; edible tissues 3 spp. 7 spp. 3 spp. 3 spp.
0.1-0.3 FW 0.3-0.5 FW 0.5-0.7 FW 0.7-2.0 FW
Euphausiid, Euphausia superba; Antarctica; whole Euphausiids Whole Whole Lobster, Homarus vulgaris Blood Muscle Hepatopancreas Gills Exoskeleton Gastric mill teeth Stomach fluid Hindgut and rectum Excretory organs Ovary Stomach contents Carapace Semi-transparent layer of shell Shell with inner surface removed Complete calcified shell Shell with outer surface removed
a
6 6 6 6
3.2 DW
16
3.6 DW 2.0 FW
5 1
(0.5-2.4) FW (0.3-0.8) FW (3.2-4.8) FW (8.6-23.3) FW (218.0-252.0) FW 150.0 FW (0.2-2.8) FW (1.0-10.5) FW (3.9-4.6) FW 1.6 FW 77.0 FW
7 7 7 7 7 7 7 7 7 7 7
0.0 FW (245.0-267.0) FW (223.0-241.0) FW (189.0-218.0) FW
7 7 7 7
Lobster, Jasus lalandi; muscle
0.22-0.27 FW
89
Lobster Muscle Carapace Head
11.0 AW 21.0 AW 26.0 AW
10 10 10 (Continues)
Crustaceans 451 Table 7.13:
Cont’d
Organism
Concentration
Reference
Euphausiid, Meganyctiphanes norvegica; fecal pellets
243.0 DW
11
Shrimp, Penaeus aztecus Muscle Exoskeleton Viscera
1.5 DW 17.8 DW 14.2 DW
12 12 12
Peneid shrimp, Melicertus kerathurus; Lesina lagoon, Italy; October 2004; 3 sites Muscle Exoskeleton
1.0-5.0 DW 12.3-13.8 DW
22 22
Shrimp, Penaeus monodon Muscle Vietnam; 2003-2005; max. values Muscle Exoskeleton Hepatopancreas
(14.9-21.3) DW
13
2.3 DW 94.5 DW 20.0 DW
21 21 21
Shrimp, Penaeus japonica; muscle
1.0 DW
14
Shrimp, Penaeus spp. Whole Whole
6.1 DW 2.4 FW
15 2
Shrimp Muscle Exoskeleton Muscle Carapace Whole
8.0 DW 89.8 DW 24.0 AW 100.0 AW 90.0 AW
12 12 10 10 10
Stomatopod, Squilla oratoria; muscle
1.9 DW
14
Crab, Ucides cordatus; adult males Gill Hepatopancreas Muscle
5.4 DW 10.1 DW 1.2 DW
23 23 23
a
Values are in mg Mn/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Fujita et al., 1969; 2, Wolfe et al., 1973; 3, Greig et al., 1977b; 4, Vinogradova and Koual’skiy, 1962; 5, Martin and Knauer, 1973; 6, Hall et al., 1978; 7, Bryan and Ward, 1965; 8, Van As et al., 1973; 9, Van As et al., 1975; 10, Lowman et al., 1966; 11, Fowler, 1977; 12, Horowitz and Presley, 1977; 13, Zingde et al., 1976; 14, Ishii et al., 1978; 15, Knauer, 1970; 16, Palmer et al., 2006; 17, Turkmen et al., 2006; 18, Feng et al., 2006; 19, Silva et al., 2006; 20, Zumholz et al., 2006; 21, Tu et al., 2008; 22, D’Adamo et al., 2008; 23, Correa et al., 2005.
452 Chapter 7 is a naturally abundant metal in marine sediments where it occurs mainly as manganese dioxide (MnO2); however, during hypoxic conditions it is converted into the bioavailable Mn2+ (up to 15.0 mg Mn/L) and, when accumulated, can adversely affect immune competent cells of the lobster, N. norvegicus (Oweson et al., 2006). Adult male crabs, U. cordatus, subjected to a high sublethal concentration of 50.0 mg Mn2+/L for 96 h had grossly elevated manganese burdens in gills (317.3 mg/kg DW versus 5.4 in controls), hepatopancreas (101.6 versus 10.1 in controls), and muscle (7.7 versus 1.2) (Correa et al., 2005).
7.28 Mercury Most tissue mercury concentrations in field collections of crustaceans worldwide were below the United States Food and Drug Administration action guideline of 0.5 mg Hg/kg FW, except for samples collected in Minamata Bay, Japan, and other areas heavily impacted by mercury-containing anthropogenic wastes (Eisler, 1981, 2006; Schuhmacher et al., 1994; Srinivasin and Mahajan, 1989; Table 7.14). Organomercury concentrations in the green crab, C. maenas comprised 70-95% of the total mercury burdens in muscle and hepatopancreas (Pereira et al., 2006). Green crabs continue to accumulate mercury throughout their life, although rates differ depending on degree of environmental contamination (Coelho et al., 2008). For example, under conditions of low mercury contamination, where diet is the major pathway, mercury tends to accumulate in muscle and hepatopancreas with 80-90% of the muscle mercury as organomercury. Under these conditions, mercury concentrations in tissues increase with increasing age. Under conditions of high mercury contamination where seawater is the major uptake pathway, mercury preferentially accumulates in gills; organomercury content is usually less than 40% of the total mercury burden, and organism age was not a significant factor (Coelho et al., 2008). Methylmercury concentrations in hepatopancreas of Chinese mitten crabs, E. sinensis, declined with increasing crab size, possibly through molting, suggesting a mechanism for mercury excretion (Hui et al., 2005), with important implications for crab predators that select larger crabs. Uptake rates of total mercury in field collections of C. maenas were about the same regardless of size: larger crabs took up 0.011-0.015 mg/kg body weight weekly versus 0.008-0.015 mg/kg BW weekly for smaller crabs. However, weekly excretion rates were different, with larger crabs excreting up to 0.034 mg/kg BW and smaller crabs up to 0.024 mg/kg BW (Pereira et al., 2006). Differences in reported mercury concentrations can significantly affect mercury intake estimates of seafood by human consumers of seafoods in the United States (Sunderland, 2007). National exposure estimates are most influenced by reported methylmercury concentrations in imported shrimp (0.04 mg/kg FW) and in Atlantic Ocean crabs (0.026 mg/kg FW; Sunderland, 2007).
Crustaceans 453 Table 7.14: Mercury Concentrations in Field Collections of Crustaceans Organism Aleutian Islands, Alaska; 2004-2005; edible portions Golden king crab, Lithodes aquispina Red king crab, Paralithodes camtschaticus
Concentration
0.043 FW; max. 0.070 FW 0.10 FW; max 0.21 FW
Reference
50 50
Amphipod, Asellus aquaticus; whole
(0.22-0.56) FW
1
Barnacle, Balanus amphitrite; soft parts
(0.06-1.35) DW
2
Barnacle, Balanus spp.; soft parts
(0.09-0.22) FW
3
0.26 (0.02-1.54) FW 1.3 (0.1-7.7) DW 0.45
4 4 5
Blue crab, Callinectes sapidus Whole Whole Muscle; Southeast United States Pensacola, Florida; 2003-2004 Hepatopancreas Muscle Crab, Cancer irroratus Muscle Digestive gland Gills Shore crab, Carcinus maenas; Portugal; 1999-2000; high mercury site (max. 5.4 mg Hg/kg DW sediment) vs. low mercury site (max. 0.23 mg Hg/kg DW sediment) Larger crabs Muscle Hepatopancreas Smaller crabs Muscle Hepatopancreas
Max. 1.1 FW Max. 0.24 FW (0.15-0.19) FW (0.07-1.9) FW 0.03 FW
a
51 51 6 6 6
(0.03-0.63) FW vs. max. 0.1 FW (0.02-0.34) FW vs. max < 0.1 FW
47
0.45 FW vs max. 0.2 FW Max. 0.3 FW vs. max. 0.1 FW
47 47
47
Copepods Whole Whole
0.11 DW 0.27 DW
7 8
Amphipod, Corophium volutator; whole
(0.04-0.13) FW
1
Crabs Muscle Shell
(0.09-0.53) FW (0.06-0.23) FW
9 9 (Continues)
454 Chapter 7 Table 7.14: Cont’d Organism
Concentration
Reference
Shrimp, Crangon crangon Muscle Whole Whole
0.19 FW (0.2-1.7) DW (0.03-0.12) FW
10 4 1
0.078 FW 41.0-100.0 DW
11 12
<0.1 FW 0.1-0.2 FW 0.2-0.3 FW 0.006-0.72 FW
13 13 13 44
0.06-1.57 DW 0.00-0.10 FW Max. 0.33 DW 0.034-0.037 DW
14 15 41 48
0.07 DW 0.03 DW 0.2 DW 0.9 DW 0.01 DW 0.4 DW 2.8 DW
49 49 49 49 49 49 49
0.05 DW 0.07 DW 0.5 DW 0.6 DW 0.02 DW 0.09 DW 2.2 DW
49 49 49 49 49 49 49
Crustaceans Edible portions Japan, 4 spp. Japan, Minamata Bay; 2 spp.; 1960s North America; 16 spp. 6 spp. 9 spp. 1 spp. Spain; Catalonia; November 1992 to February 1993; 4 spp. Whole 12 spp. 5 spp. 6 spp.; Greenland; 1983-1991 4 spp.; Antarctica; 2004 Deep sea shrimps; 2 spp.; Rainbow hydrothermal vent site; mid-Atlantic Ridge; adults; summer 2003 Rimicaris exoculata Whole body Cuticle Gill Antennae Muscle Digestive gland Pylorus Microcaris fortunata Whole body Cuticle Gill Antennae Muscle Digestive gland Pylorus
a
(Continues)
Crustaceans 455 Table 7.14: Organism Chinese mitten crab, Eriocheir sinensis; San Francisco Bay, California; JulyAugust 2002; total mercury vs. methylmercury Hepatopancreas
Cont’d
Concentration
Reference
0.25 (0.04-1.03) DW vs. 0.036 (0.006-0.069) DW 0.15 (0.04-0.69) DW vs. 0.04 (0.007-0.095) DW
40
Crab, Eupagurus bernhardus; whole
0.67 FW
16
Euphausiid, Euphausia pacifica Whole Whole
(0.008-0.058) FW (0.25-0.52) DW
Euphausiids Whole Whole
0.08 DW <0.09 FW
Amphipod, Gammarus sp.: whole
(0.01-0.15) FW
Lobster, Homarus americanus Muscle Liver
0.31 FW 0.60 FW
18 18
Lobster, Homarus vulgaris; muscle
(0.21-0.54) FW
19
1.4 DW vs. 0.06 DW
52
1.4 DW vs. 0.7 DW 0.4 DW vs. 0.3 DW 0.2 DW vs. 0.2 DW
52 52 52
1.3 DW vs. 0.5 DW 0.7 DW vs. 0.08 DW no data vs. 1.0 DW
52 52 52
Barnacle, Lepas sp.; whole
0.08 FW
20
Euphausiid, Meganyctiphanes norvegica; whole
0.26 DW
21
Mysidaceans; whole
(0.06-0.09) FW
22
Other tissues
Hydrothermal vent field; mid-Atlantic Ridge; 2001 Shrimp, Chlorocaris chacei; 1700 m deep; digestive gland vs. muscle Hydrothermal crab, Segonzacia mesatlantica digestive gland vs. muscle 840 m deep 1700 m deep 2300 m deep Shrimp, Mirocaris fortunata; digestive gland vs. muscle 840 m deep 1700 m deep 2300 m deep
a
40
4 4 7 17 1
(Continues)
456 Chapter 7 Table 7.14: Cont’d Organism
Concentration
Reference
Spiny lobster, Nephrops norvegicus Muscle Edible portions; Tyrrhenian Sea; 1981
(0.10-0.22) FW 2.9 FW
23 42
Crab, Pachygrapsus marmoratus; whole
(0.50-4.5) FW
16
Shrimp, Palaemon debilis; whole
(0.015-0.30) FW
24
Shrimp, Palaemon elegans; whole
0.98 DW
25
Shrimp, Pandalus jordani; muscle
(0.06-0.18) FW
Shrimp, Penaeus aztecus; muscle; Tampico, Mexico
0.06 (0.01-0.67) FW
26
Shrimp, Penaeus californiensis; muscle
0.12 (0.02-0.46) FW
26
Shrimp, Penaeus kerathurus Muscle Muscle
(0.09-0.26) FW (0.01-0.04) FW
27 28
Black tiger shrimp, Penaeus monodon; Vietnam; 2003-2005; juveniles; max. values Muscle Exoskeleton Hepatopancreas
0.07 DW <0.05 DW 0.09 DW
53 53 53
Shrimp, Penaeus orientalis; muscle
Max. 0.04 FW
29
Shrimp, Penaeus setiferus; muscle; Mexico Vera Cruz Ciudad del Carmen
0.04 (0.02-0.06) FW 0.03 (0.01-0.16) FW
26 26
Shrimp, Penaeus sp.; muscle; total mercury vs. organic mercury
0.011 (0.002-0.016) FW vs. 0.006 (0.001-0.010) FW
30
Shrimp, Penaeus stylirostris; muscle; Mexico Vera Cruz Ciudad del Carmen
0.09 (0.01-0.20) FW 0.05 (0.01-0.15) FW
26 26
Crab, Portunus holsatus; whole
0.10 FW
31
Crab, Portunus sp.; whole
(<0.01-0.03) FW
20
Prawns Soft parts Muscle
<0.03 FW 0.02 FW
32 33
a
3
(Continues)
Crustaceans 457 Table 7.14:
Cont’d
Organism
Concentration
Reference
Puerto Rico; estuaries; 1988 Blue crab, Callinectes sapidus; all tissues Shrimps, Palaemonetes sp.; all tissues
Not detectable Not detectable
43 43
(0.03-0.09) FW 0.24 (0.08-0.88) FW (0.04-0.18) FW (0.005-0.012) FW <0.02 DW
20 34 32 35 26
(0.08-0.17) FW 0.22 DW 0.01 (0.002-0.02) FW
9 5 46
1.3 DW 0.01-0.015 (0.004-0.028) FW
36 39
2.2-2.4 (0.7-5.4) DW (0.02-0.05) FW 1.3 DW
45 9 36
0.12 FW
27
Shrimp Whole Gulf of Mexico Persian Gulf North Sea Persian Gulf Texas Muscle Korea Southeastern United States; 4 spp. New Jersey supermarkets; July-October 2003 Belgium China; Zhejiang coastal area; May 1998; 3 spp. Taiwan; 1995-1996; 2 spp. Shell Molts Stomatopod, Squilla mantis; muscle Crab, Thalamita crenata Muscle; chela vs. body Viscera Gills Crab, Uca sp.; whole
(0.020-0.058) (0.027-0.061) (0.021-0.044) (0.033-0.119) 0.04 DW
FW vs. FW FW FW
a
37 37 37 38
Values are in mg Hg/kg fresh weight (FW) or dry weight (DW). a 1, Zauke, 1977; 2, Barbaro et al., 1978; 3, Yannai and Sachs, 1978; 4, Bernhard and Zattera, 1975; 5, Gardner et al., 1975; 6, Greig et al., 1977a,b, Martin and Knauer, 1973; 8, Tijoe et al., 1977; 9, Won, 1973; 10, DeClerck et al., 1974; 11, Kumagai and Saeki, 1978; 12, Matida and Kumada, 1969; 13, Hall et al., 1978; 14, Stickney et al., 1975; 15, Ramos et al., 1979; 16, Renzoni et al., 1973; 17, Greig and Wenzloff, 1977; 18, Greig et al., 1975; 19, Holden and Topping, 1972; 20, Johnson and Braman, 1975; 21, Leatherland et al., 1973; 22, Nuorteva and Hasanen, 1975; 23, Cumont et al., 1975; 24, Luoma, 1977; 25, Leatherland and Burton, 1974; 26, Reimer and Reimer, 1975, Establier, 1977; 28, Tuncel et al., 1980; 29, Doi and Ui, 1975; 30, Cheevaparanapivat and Menasveta, 1979; 31, DeClerck et al., 1979; 32, Anonymous, 1978; 33, Sorentino, 1979; 34; Parveneh, 1977; 35, Eftekhari, 1975; 36, Bertine and Goldberg, 1972; 37, Luoma, 1976; 38, Windom et al., 1976; 39, Fang et al., 2004; 40, Hui et al., 2005; 41, Dietz et al., 1996; 42, Schreiber, 1983; 43, Burger et al., 1992; 44, Schuhmacher et al., 1994; 45, Han et al., 1998; 46, Burger et al., 2005; 47, Pereira et al., 2006; 48, Santos et al., 2006; 49, Kadar et al., 2006; 50, Burger et al., 2007b; 51, Karouna-Renier et al., 2007; 52, Colaco et al., 2006; 53, Tu et al., 2008.
458 Chapter 7 Laboratory studies demonstrate that many biological and abiotic variables modify mercury accumulation, retention, and effects among crustaceans. Biological modifiers include tissue specificity, diet, feeding niche, gender, life stage, and health of the organism. Abiotic modifiers include the temperature and salinity of the medium, duration of exposure to mercury, chemical form of mercury, and presence of other compounds. Selected studies illustrating these points follow. American lobsters, H. americanus, held in seawater containing up to 0.006 mg Hg/L for 30 days, show significant accumulations of total mercury in various tissues: 15.2 mg Hg/kg FW digestive gland, up from 0.12 at the start; 85.3 in gills, up from 0.14; and 1.0 mg Hg/kg FW muscle, up from 0.23 (Thurberg et al., 1977). With increasing exposure of 60 days, all tissues contained increasing burdens of mercury: gill, for example, contained 119.5 mg Hg/kg FW (Thurberg et al., 1977). Altered enzyme activity levels were documented in the green crab, C. maenas, at sublethal levels of 0.09 mg Hg2+/L (Elumalai et al., 2007). Effects of high sublethal concentrations of mercury (0.18 mg/L) on fiddler crabs, U. pugilator, is modified by life stage, gender, and thermosaline regime. Adults were significantly more resistant than larvae, adult males more sensitive than females, and resistance lowest at low temperatures and low salinities (Vernberg and DeCoursey, 1977). Exposure for 3 h in 0.18 mg Hg/L, as HgCl2, show that gill tissues of fiddler crabs are the major site of mercury concentration; lesser amounts accumulate in hepatopancreas and green gland. Crabs are more susceptible to biocidal properties of mercury at low temperatures (5 C) than at elevated (33 C) temperatures. The inability to transfer mercury from gill to hepatopancreas at low temperatures is a factor in the higher toxicity of mercury to fiddler crabs at low temperatures (Vernberg and O’Hara, 1972; Vernberg and Vernberg, 1972). Corner and Rigler (1958) found that larvae of a barnacle, Elminius modestus, accumulate up to 920.0 mg Hg/kg DW during exposure for 3 h in 0.2 mg Hg/L as mercuric chloride. Higher accumulations (700.0 mg Hg/kg)were observed with amylmercuric chloride (n-C5H11HgCl) during exposure for 3 h in only 0.01 mg Hg/L solutions. Similar trends were observed for brine shrimp, A. salina (Corner and Rigler, 1958). Studies with adult prawns, Leander serratus, held in toxic solutions of mercury (50.0 mg Hg/L) as HgCl2; prawns dying during 3 h exposure to 1.0 mg Hg/L as n-C5H11HgCl contained 320.0-460.0 mg Hg/kg DW in antennary gland (Corner and Rigler, 1958). Corner (1959) reports that crabs, Maia squinado, held in seawater containing inorganic mercuric chloride show major accumulations in gills and other sites. Eventually, the mercury concentrations in blood surpass that of the external medium, the concentration in antennary gland above that in blood, and the crabs excrete small, but increasing, amounts of mercury in the urine. Most (95%) of the mercury in blood is attached to protein, with mercury concentrations in blood remaining constant for several weeks following mercury exposure. When Maia was poisoned with n-methylmercuric chloride, mercury again
Crustaceans 459 concentrates in gills and various internal organs; however, mercury burdens in blood were low and no mercury was found in urine (Corner, 1959). Mercury content among crustaceans feeding in contact with sediment is highest among carnivores and lowest in herbivores; a similar pattern exists for crustaceans feeding above the sediment/water interface (Klemmer et al., 1976). Although crustaceans biomagnify mercury in tissues via the diet, some studies found that mercury accumulations from solution are more rapid and more pronounced than food sources (Luoma, 1976, 1977). In an algae to copepod link, however, copepods show no impairment of egg laying or egg development, and no retention of mercury in tissues, eggs, or feces (Parrish and Carr, 1976); in that study, the algae Croomonas salina, had 1400.0 mg Hg/kg DW. Fowler et al. (1978) report that 45% of all mercury in the shrimp L. seticaudata localizes in viscera, 39% in muscle, 15% in exoskeleton, and 1.8% in molts. It is probable that most of the mercury was in methylated form as has been demonstrated for tissues of blue crabs (Gardner et al., 1975), fiddler crabs (Windom et al., 1976), and other decapods (Eganhouse and Young, 1978). It is generally agreed that organomercury compounds are accumulated by crustaceans more rapidly and to a higher level than inorganic mercury compounds (D’Agostino and Finney, 1974; Fowler et al., 1978). Some evidence exists that iodide salts of mercury have greater uptake potential than chloride salts in copepods and brine shrimp (Boney et al., 1959). Larvae of dungeness crab, C. magister, were extremely sensitive to mercury with 50% dead within 48 h at 0.0066 mg/L (Glickstein, 1978). High levels of selenium (>5.0 mg Se/L) increased mercury toxicity but moderate levels of 0.010-1.0 mg Se/L decreased mercury toxicity (Glickstein, 1978) and accumulations (Fowler and Benayoun, 1976a,b,c). Larvae and newly molted crustaceans were more sensitive to mercury effects than were adults of the same species (Shealy and Sandifer, 1975; Vernberg et al., 1974; Wilson and Connor, 1971); also, male adult fiddler crabs were more sensitive than females (Vernberg et al., 1974). Starved larvae of grass shrimp, Palaemonetes vulgaris were more sensitive to mercury insult than were fed larvae (Shealy and Sandifer, 1975). Biocidal properties of mercury salts, and presumably uptake rates, were more pronounced for crab Petrolisthes armatus at lower salinities within the range 7-35 ppt (Roesijadi et al., 1974). A similar pattern was recorded for the fiddler crab U. pugilator (Vernberg et al., 1974). However, salinities as low as 6 ppt did not affect uptake patterns in the shrimp Palaemon debilis (Luoma, 1977). Negligible uptake or effects were demonstrated in U. pugilator during exposure for 2 weeks in seawater containing 0.1 mg Hg/L (Weis, 1978). Similarly, pre-exposure of shrimp, Penaeus setiferus, for 57 days to 0.001 mg Hg/L had no effect on measured parameters during subsequent mercury stress experiments with that species (Green et al., 1976).
460 Chapter 7
7.29 Molybdenum Highest molybdenum values recorded in field collections of crustaceans were 0.4 mg/kg on a FW basis, 2.6 on a DW basis, and 50.0 mg/kg on an AW basis (Table 7.15). Molybdenum is relatively nontoxic to the crabs E. bernhardus and C. maenas at alkaline pH typical of seawater, but death and presumably accumulation occur at pH values near 5.0 (Abbott, 1977). The concentration of molybdenum fatal to 50% of the euphausiid, Euphausia pacifica, in 8 days is 560.0 mg/L (Anderson and Mackas, 1986); to 50% of the amphipod A. compressa in 96 h it is 247.0 mg/L (Ahsanullah, 1982); to 50% of the copepod, Calanus marshallae, in 19 days it is 560.0 mg/L (Anderson and Mackas, 1986); and to 50% in 96 h of pink shrimp, Penaeus duorarum it is 1909.0 mg/L and to mysid shrimp, M. bahia it is 1205.0 mg/L (Knothe and Van Riper, 1988).
Table 7.15: Molybdenum Concentrations in Field Collections of Crustaceans Organism
Concentration
Reference
Copepod, Calanus finmarchicus; whole
12.0 AW
1
Copepod, Centropages spp.; whole
10.0 AW
1
Copepods Whole Whole
50.0 AW 1.3 DW
2 3
Crustaceans; North America; 16 commercial species; edible tissues 11 spp. 3 spp. 2 spp.
0.1-0.2 FW 0.2-0.3 FW 0.3-0.4 FW
4 4 4
Euphausiid, Euphausia krohni; whole
17.0 AW
1
Tiger shrimp, Penaeus monodon; Vietnam; 2003-2005; juveniles; max. values Muscle Exoskeleton Hepatopancreas
0.05 DW 0.09 DW 2.6 DW
6 6 6
Zooplankton; Baltic Sea
2.0 DW
5
a
Values are in mg Mo/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, 1, Nicholls et al., 1959; 2, Vinogradova and Koual’skiy, 1962; 3, Tijoe et al., 1977; 4, Hall et al., 1978; 5, Prange and Kremling, 1985; 6, Tu et al., 2008.
Crustaceans 461
7.30 Neodymium Whole amphipods collected from East Antarctica in 2003-2004 contained a maximum of 0.11 mg Nd/kg DW (Palmer et al., 2006).
7.31 Neptunium The uptake of 237Np was followed in tissues of a crab, C. pagurus, and shrimp, L. seticaudata, for 48 days. Accumulation was observed in all tissues measured with 92-98% of the organism’s total 237Np content associated with exoskeleton; most of the remainder was in hepatopancreas and gut (Guary and Fowler, 1978). This artificial element will assume increasing environmental importance with further expansion of the nuclear fuel reprocessing industry.
7.32 Nickel Large variations in nickel content of field collections of crustaceans were evident between species, tissues, depths of collection, and other variables (Table 7.16). Maximum nickel concentrations in crustacean tissues were 27.0 mg/kg FW in whole spiny lobster, Panulirus argus, 92.0 mg/kg DW in soft parts of sand shrimp, Crangon allmani, from a waste dump site, and 150.0 mg/kg AW in zooplankton collected at depths greater than 99 m (Table 7.16). Most investigators showed that nickel concentrations were lowest in muscle and highest in exoskeleton. Molts of the euphausiid M. norvegica, for example, contained 78% of the total nickel body burden of that species (Fowler, 1977). Yoshinari and Subramanian (1976) demonstrated that granular chitin from lobster shell has high nickel-absorbing capability from distilled water; as was true for other metals tested, absorption decreased with increasing salinity. Mysid shrimp were comparatively sensitive to ionic nickel, with 50% mortality documented in 96 h at 0.15 mg Ni/L for Mysidopsis formosa and 0.51-0.64 mg Ni/L for M. bahia (USEPA, 1980c). Nickel is toxic to the copepod, A. tonsa, when fed a nickel-contaminated algal diet (Bielmyer et al., 2006). In that study, diatoms T. pseudonana, were held in seawater containing 0.0024 mg Ni/L for 7 days, reaching a concentration of 15.3 mg Ni/kg DW diatom; this, in turn, was fed to Acartia for 7 days, producing a measurable reduction in copepod reproduction. Authors note that the proposed water quality criterion for marine life protection is 0.008 mg Ni/L, which is far in excess of the 0.0024 mg Ni/L used in this study to produce a toxic diet (Bielmyer et al., 2006). To protect human consumers of crustaceans, it is proposed that edible seafood tissues contain less than 70.0 mg Ni/kg FW (Sankar et al., 2006).
462 Chapter 7 Table 7.16: Nickel Concentrations in Field Collections of Crustaceans Organism
Concentration
Amphipods; Whole; Antarctica
2.2 DW
12
Barnacles; summer 2001; soft parts; Natal, Brazil Fistulobalanus citerosum Balanus amphitrite
(3.7-12.0) DW 9.1 DW
18 18
Copepod, Calanus finmarchicus; whole
165.0 AW
Blue crab, Callinectes sapidus Muscle; August 2005; Turkey Pensacola, Florida; 2003-2004 Hepatopancreas Muscle
Reference
1
2.8 (0.3-15.4) DW
17
Max. 0.56 FW Max. 0.29 FW
19 19
Green crab, Carcinus maenas; all tissues
(6.2-12.3) FW
13
Copepod, Centropages spp.; whole
55.0 AW
1
Copepods Whole Whole
2.0 DW 1.5 DW
2 3
Sand shrimp, Crangon allmani; Scotland; soft parts; reference site vs. waste dump site
15.0 DW vs. 92.0 DW
13
Crustaceans Whole Edible tissues; 16 commercial species; North America 4 spp. 8 spp. 4 spp.
(6.5-9.8) FW
4
0.2-0.3 FW 0.3-0.4 FW 0.4-0.9 FW
5 5 5
Euphausiid, Euphausia krohni; whole
6.0 AW
1
Euphausiid, Euphausia superba; Antarctica; whole
4.4 DW
16
Euphausiids; whole
3.8 DW
2
American lobster, Homarus americanus Serum
0.012 (0.008-0.020) FW
Euphausiid, Meganyctiphanes norvegica; molts
6.7 DW
a
14, 15 6 (Continues)
Crustaceans 463 Table 7.16:
Cont’d
Organism
Concentration
Aesop shrimp, Pandalus montagui; soft parts; Scotland; reference site vs. waste dump site
25.0 DW vs. 70.0 DW
13
1.3 (1.0-2.0) FW; 4.5 DW vs. 4.6 (1.4-5.0) FW; 36.0 (22.0-60.0) DW (1.3-27.0 FW); (4.5-50.0) DW
13
Caribbean spiny lobster, Panulirus argus Soft parts; Puerto Rico, Anasco Bay vs. West coast Whole
Reference
a
7
Brown shrimp, Penaeus aztecus; Texas Muscle Exoskeleton Viscera
1.4 DW; max. 1.9 DW 6.2 DW; max. 17.9 DW 5.7 DW; max. 5.8 DW
8 8 8
Shrimp; 2 spp.; Texas; outer continental shelf Muscle Exoskeleton Whole
1.6 DW 5.8 DW 1.4-1.6 DW
8 8 8
Stomatopod, Squilla oratoria; muscle
1.2 DW
9
Barnacle, Tetraclota sp.; whole
0.43 FW
10
Shrimp, Xiphopenaeus kroyeri; whole
5.1 (2.0-7.0) FW
Zooplankton Surface vs. > 99 m depth collections Baltic Sea; May 1999; cladocerans vs. copepods; whole
100.0 AW vs. 150.0 AW 2.6 DW vs. 10.7 DW
7 11 20
Values are in mg Ni/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Nicholls et al., 1959; 2, Martin and Knauer, 1973; 3, Tijoe et al., 1977; 4, Wright, 1976; 5, Hall et al., 1978; 6, Fowler, 1977; 7, Bernhard and Zattera, 1975; 8, Horowitz and Presley, 1977; 9, Ishii et al., 1978; 10, Ikebe and Tanaka, 1979; 11, Martin, 1970; 12, Szefer et al., 1993; 13, Jenkins, 1980; 14, USEPA, 1980b; 15, Mushak, 1980; 16, Palmer et al., 2006; 17, Turkmen et al., 2006; 18, Silva et al., 2006; 19, Karouna-Renier et al., 2007; 20, Pempkowiak et al., 2006.
7.33 Niobium Whole shrimp, Crangon sp., contained 0.00086 mg Nb/kg DW (Zumholz et al., 2006).
7.34 Plutonium Crabs, C. pagurus collected near the La Haque, France, nuclear fuel reprocessing plant were examined for plutonium isotope activity. Gills contained the highest concentration of radioactivity, followed by hepatopancreas, gut, exoskeleton, gonad, and hemolymph, in
464 Chapter 7 that order (Guary et al., 1976). In hepatopancreas and hemolymph, plutonium was associated with low MW fractions of soluble proteins (Guary and Negrel, 1980). The significance of these results in terms of human health or effects on marine food chains is unclear. Accidental contamination of crustaceans with plutonium resulted when a military aircraft carrying nuclear weapons crashed near Greenland. Benthic crustaceans in the crash area contained up to 1000 times more plutonium radioactivity than background; however, pelagic zooplankton did not contain significant accumulations (Aarkrog, 1971, 1990).
7.35 Polonium Zooplankton, mainly calanoid and cyclopoid copepods, from a Caribbean Sea location accumulated 210Po from ambient seawater by a factor of 970 (Kharkar et al., 1976). Polonium-210 concentrations in whole Mediterranean Sea crustaceans were up to 10,000 higher than ambient seawater 210Po concentrations (Heyraud and Cherry, 1979). Concentration factors were highest in Sergestes spp., especially in hepatopancreas which contained up to 90% of all 210Po (Heyraud and Cherry, 1979). Laboratory feeding studies with euphausiids, M. norvegica, on food low in 210Po resulted in an approximate biological half-life of only 6.5 days in hepatopancreas (Heyraud and Cherry, 1979).
7.36 Praseodymium Whole amphipods, P. walkeri, collected in East Antarctica in 2003-2004 had 0.013-0.027 mg Pr/kg DW (Palmer et al., 2006).
7.37 Protactinium Lucu et al (1969) in uptake studies of 20-day duration with C. mediterraneus and 233Pa showed that gills had the greatest ability to accumulate this isotope (1500 times over medium). For reproductive system and muscle, these values ranged between 5 and 20; no uptake was observed in hemolymph (Lucu et al., 1969).
7.38 Radium The ability of mixed zooplankton cultures, mainly copepods, to accumulate seawater is about five times over ambient levels (Kharkar et al., 1976).
226
Ra from
7.39 Rhenium Pandalus sp. from the coast of Japan have low body burdens of rhenium, estimated at <0.005 mg/kg on an AW basis (Fukai, 1965) and <0.0003 mg/kg on a DW basis (Fukai and Meinke, 1962).
Crustaceans 465
7.40 Rubidium Edible tissues of shrimp, Penaeus japonica, and stomatopod, Squilla oratoria contained 4.1 and 3.2 mg Rb/kg DW, respectively (Ishii et al., 1978). Rubidium concentrations in juvenile black tiger shrimp, P. monodon, from Vietnam in 2003-2005 were as high as 12.2 mg Rb/kg DW in muscle, 4.8 in exoskeleton, and 8.4 in hepatopancreas (Tu et al., 2008). In a controlled study, crabs, Panopeus herbstii, were fed clams preloaded with rubidium; rubidium accumulated in the hepatopancreas but most was lost—mainly via fecal excretion—4 to 7 days post feeding (Eversole, 1978).
7.41 Ruthenium Accumulation of 106Ru by the euphausiid, M. norvegica, was influenced by the concentration in solution and the chemical form of the radioisotope, ruthenium chloride fractions being accumulated at a faster rate than nitrosyl-nitrate complexes (Keckes et al., 1972). Molting was the primary loss route for accumulated 106Ru, with first molts accounting for up to 80% of the loss. When euphausiids accumulated 106Ru from the diet, initial loss was rapid due to fecal excretion. Molts from these individuals did not contain 106Ru, thus loss from euphausiids obtaining the isotope through feeding is mainly due to fecal pellet deposition and other excretion or exchange processes (Keckes et al., 1972). Similar findings were reported for this species (Antonini-Kane et al., 1972) and other species of crustaceans (Ancellin et al., 1967). Radioruthenium recycling via crustacean feces is an important pathway. On May 6, 1986— about 2 weeks after the Chernobyl nuclear power reactor accident (Eisler, 1995, 2003) — fecal pellets of copepods contained 57 and 82 times more 103Ru and 106Ru, respectively, than did whole organism (Fowler et al., 1987).
7.42 Samarium Whole amphipods, P. walkeri, from East Antarctica in 2003-2004 contained 0.009-0.017 mg Sm/kg DW (Palmer et al., 2006).
7.43 Scandium The single datum available for scandium in field collections of crustaceans is 0.016 mg Sc/kg AW whole euphausiid (Table 7.17). Fowler (1977) reports that scandium levels in M. norvegica were below analytical detection limits of 4.5 mg/kg DW for whole organisms, and below 80.0 mg/kg DW for fecal pellets; scandium flux was <0.8 mg/kg/day due to fecal deposition.
466 Chapter 7 Table 7.17: Scandium, Selenium, and Silver Concentrations in Field Collections of Crustaceans Element and Organism
Concentration
Reference
a
Scandium Euphausiids; whole
0.016 AW
1
Selenium Blue crab, Callinectes sapidus Pensacola, Florida; 2003-2004; hepatopancreas vs. muscle
Max. 2.0 FW vs. max 1.0 FW
Copepods; whole
3.4 DW
Crustaceans; digestive system; 3 spp.
3.0-3.5 DW
11
0.2-0.4 FW 0.4-0.7 FW 0.7-2.0 FW
3 3 3
Crustaceans; 16 commercial species; North America; edible tissues 5 spp. 6 spp. 5 spp. 2 spp. Total selenium Selenate Selenite plus selenide
21 2
0.21 FW 0.05 FW 0.16 FW
12 12 12
Greenland; 1975-1991; 6 spp.; whole
0.2-3.2 FW
13
Euphausiid, Meganyctiphanes norvegica Viscera Eyes Muscle Exoskeleton
11.7 DW 7.8 DW 1.8 DW 0.84 DW
Marsh crab, Parasesarma erythodactyla; soft parts; 2002; New South Wales, Australia; metals-contaminated estuary Males Females
Max. 12.4 DW Max. 20.2 DW
20 20
Black tiger shrimp, Penaeus monodon; Vietnam; 2003-2005; max. values Muscle Exoskeleton Hepatopancreas
1.5 DW 0.63 DW 7.9 DW
22 22 22
Shrimps Muscle Molts
6.1 DW 5.0 DW
5 5
4 4 4 4
(Continues)
Crustaceans 467 Table 7.17:
Cont’d
Element and Organism
Concentration
Reference
Texas; Lower Laguna Madre; shoalgrass community; 1986-1987; whole Grass shrimp, Palaemonetes sp. Brown shrimp, Penaeus aztecus
1.2 (0.7-1.8) DW 1.8 (0.6-3.2) DW
14 14
Amphipods; whole; Antarctica; February-March 1989
1.2 (0.7-1.4) DW
17
Arabian Sea; shrimps; edible tissues; 2 spp.
0.40-0.76 FW
15
Barnacle, Elminius modestus; pyrophosphate granules
10.5 (9.7-11.3) DW
18
Calcasieu River estuary, Louisiana Blue crab, Callinectes sapidus; muscle Shrimps; 2 spp.; muscle
0.1 DW 0.04 DW
16 16
Crab, Cancer irroratus Muscle Digestive gland Muscle Digestive gland
(0.24-0.79) FW (2.1-3.4) FW 0.21 DW 6.3 DW
6 6 7 7
Copepods; whole
30.0 AW
8
Crustaceans; 16 commercial species; North America; edible tissues 8 spp. 5 spp. 3 spp.
<0.1 FW 0.1-0.2 FW 0.3-0.5 FW
3 3 3
Euphausiids; whole
0.15 FW
9
Mantis shrimp, Gonodactylus sp.; Guam; June 1988; muscle vs. gonad
0.27 DW vs. 1.4 DW
19
Lobster, Homarus americanus; muscle
(0.37-0.54) DW
10
Black tiger shrimp, Penaeus monodon; Vietnam; 2003-2005; juveniles; max. values Muscle Exoskeleton Hepatopancreas
0.02 DW 0.02 DW 8.4 DW
22 22 22
a
Silver
(Continues)
468 Chapter 7 Table 7.17: Cont’d Element and Organism
Concentration
Shrimps Muscle Molts
0.24 DW 1.1 DW
Reference
a
5 5
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Robertson, 1967; 2, Tijoe et al., 1977; 3, Hall et al., 1978; 4, Fowler and Benayoun, 1976a; 5, Bertine and Goldberg, 1972; 6, Greig et al., 1977a; 7, Greig et al., 1977b; 8, Vinogradova and Koual’skiy, 1962; 9, Greig and Wenzloff, 1977; 10, Greig, 1975; 11, Maher, 1983; 12, Cappon and Smith, 1982; 13, Dietz et al., 1996; 14, Custer and Mitchell, 1993; 15, Tariq et al., 1993; 16, Ramelow et al., 1989; 17, Szefer et al., 1993; 18, Pullen and Rainbow, 1991; 19, Denton et al., 2006; 20, MacFarlane et al., 2006; 21, Karouna-Renier et al., 2007; 22, Tu et al., 2008.
7.44 Selenium The highest selenium concentrations recorded in crustacean tissues from field collections were 3.2 mg Se/kg FW and 20.2 mg Se/kg DW (Table 7.17). Selenium levels in soft tissues of the marsh crab, P. erythodactyla, increased with increasing concentrations of selenium in the ambient sediments, and increased with decreasing salinities; this pattern held for both males and females (MacFarlane et al., 2006). Selenium accumulates in internal tissues of M. norvegica, with about 67% of all selenium in the viscera (Fowler and Benayoun, 1976a). With shrimp, L. seticaudata, highest concentrations were in exoskeleton when selenium was administered via the medium and in viscera and exoskeleton when administered via the diet (Fowler and Benayoun, 1976c). About half the artificially accumulated selenium in Lysmata was eliminated in 58-60 days (Fowler and Benayoun, 1976b). Marine crabs exposed to seawater concentration of 0.25 mg Se/L accumulated selenium over water concentration level by a factor of 25 for carapace, and 3.8 for gill; accumulations in muscle and hepatopancreas were negligible (Bjerragaard, 1982). Cadmium in solution enhanced selenium uptake (Bjerragaard, 1982). Uptake of radioselenium-75 by semaphore crab, H. cordiformis, soldier crab, M. platycheles, and ghost shrimp, T. australiensis during immersion for 385 h, and loss in 75Se-free seawater over the next 189 h was determined (Alquezar et al., 2007). Uptake factors (loss) were 39 (28%) for semaphore crab, 17 (42%) for soldier crab, and 54 (91%) for ghost shrimp. Excretion followed a biphasic pattern with short-lived and long-lived components. The biological half-time for short-lived components (long-lived) components were 23 h (161 h) for semaphore crab, 22 h (330 h) for soldier crab, and 16 h (1500 h) for ghost shrimp (Alquezar et al., 2007). LC50 (96 h) values—in mg Se/L—for copepods, Acartia spp., ranged from 0.8-1.74; for blue crab, C. sapidus, it was 4.6; for mysid shrimp, M. bahia, adults and juveniles, it was 1.5 and 0.6, respectively; and for brown shrimp, Penaeus aztecus, it was 1.2 (USEPA, 1980a;
Crustaceans 469 Ward et al., 1981). Results of a 28-day chronic exposure life cycle test with M. bahia, showed a NOAEL (no observed adverse effect level) of 0.027 mg Se/L and an LOAEL (lowest observed adverse effect level) of 0.143 mg Se/L (USEPA, 1980a). The concentration of total acid-soluble selenium currently recommended for marine life protection is less than 0.071 mg/L (Eisler, 2000c; USEPA, 1987a).
7.45 Silicon The copepod A. tonsa can extract sufficient silicon necessary to form siliceous teeth from media so low in silicon that diatom growth was negligible (Miller et al., 1980). This suggests that low concentrations of silicates are not important limiting factors for A. tonsa or other species of pelagic copepods, unlike many species of marine alga.
7.46 Silver Highest values recorded for silver in field collections of crustaceans were 3.4 mg Ag/kg FW in crab digestive gland, 11.3 mg/kg DW in barnacle pyrophosphate granules, and 30.0 mg Ag/kg AW in whole copepods (Table 7.17). Among arthropods, pyrophosphate granules isolated from barnacles can bind and effectively detoxify silver and other metals under natural conditions (Pullen and Rainbow, 1991). Hepatopancreas of the pink shrimp, Penaeus duorarum readily accumulates ionic silver from the medium (Bianchini et al., 2007). In one study, pink shrimp that were exposed to 0.001 or 0.01 mg Ag/L for 48 h had silver burdens in hepatopancreas, in mg Ag/kg FW, of 123.7 in the low-dose group and 265.1 in the high-dose group; other tissues (hemolymph, gill muscle, eyestalk) were always <1.5 mg Ag/kg FW (Bianchini et al., 2007). Large variations were observed in ability of whole decapod crustaceans to accumulate 110 Ag from seawater, with concentration factors ranging between 70 and 4000 (Pouvreau and Amiard, 1974). The reasons for this variability are unknown, but is generally agreed that hepatopancreas or digestive gland are the major repositories of silver in decapods (Beasley and Held, 1971; Greig, 1975; Greig et al., 1977a,b). Silver is accumulated both from the medium and from the diet by grass shrimp, P. pugio (Connell et al., 1991). Silver accumulations from the medium is documented by P. pugio immersed in 0.002, 0.005, or 0.010 mg Ag/L for 2 weeks: 0.36 mg Ag/kg DW whole shrimp in controls, 0.5 in the 0.002 mg/L group, 3.7 in the 0.005 mg/L group, and 4.5 mg/kg DW whole shrimp in the 0.010 mg/L group (Connell et al., 1991). Silver accumulations from the diet is reported for grass shrimp fed Artemia nauplii containing 0.72 mg Ag/kg DW or bryozoans (Victorella sp.) containing 38.0 or 180.0 mg Ag/kg DW, or control bryozoans (11.5 mg Ag/kg DW). Silver concentrations (mg/kg DW whole body) in shrimp on Artemia diet were 0.19 versus 0.09 in silver-free Artemia diet; 0.26-0.62 in the high-silver bryozoan diet and 0.36 in the control
470 Chapter 7 bryozoan diet (Connell et al., 1991). Authors concluded that grass shrimp rapidly incorporate silver dissolved in brackish water in proportion to its concentration, but not from planktonic or detrital food sources containing elevated silver burdens (Connell et al., 1991). Ionic silver is lethal to copepods, A. tonsa, at 0.036 mg/L (USEPA, 1980d), to amphipods, Ampelisca abdita at 0.03 mg/L (Berry et al., 1999), and to mysid shrimp, M. bahia, at 0.25 mg/L (USEPA, 1980d). Sediment chemistry affects silver toxicity to A. abdita exposed for 10 days on silver-loaded sediments (Berry et al., 1999). In general, sediments with an excess of acid volatile sulfide (AVS) relative to simultaneously extracted metal (SEM) were toxic to marine amphipods. Sediments with an excess of SEM relative to AVS, and no measurable AVS, were generally toxic. Sediments with measurable AVS were not toxic (Berry et al., 1999). In acute toxicity studies with the euryhaline A. tonsa, silver was about six times more toxic to starved copepods than fed animals, and more sensitive with decreasing salinity in the range 5-30 ppt (Pedroso et al., 2007a). Na+, K+, ATPase molecules seem to be a key site of acute silver toxicity in A. tonsa (Pedroso et al., 2007b). The mysid, Americamysis bahia, held in seawater for 28 days at 10, 20, or 30 ppt and dissolved organic carbon up to 6.0 mg/L were more sensitive to silver at 10 ppt (0.0039 mg dissolved Ag/L for reduced survival) than at 30 ppt salinity (0.060 mg/L); dissolved organic carbon had no effect on silver toxicity (Ward et al., 2006). Silver is also toxic to the copepod, A. tonsa, when fed a silver-contaminated algal diet (Bielmyer et al., 2006). In that study, diatoms (T. pseudonana) were held in seawater containing 0.00064 mg Ag/L (as traced by radiosilver-110 m) for 7 days, reaching a silver burden of 5.4 mg Ag/kg DW diatom; this, in turn, was fed to Acartia for 7 days, causing a significant reduction in copepod fertility. Authors note that the proposed silver criterion for marine life protection is 0.003 mg Ag/L, and is in excess of 0.00064 mg Ag/L used in this study to produce a toxic diet (Bielmyer et al., 2006).
7.47 Strontium All crustacean tissues and organs contain significant concentrations of strontium, especially exoskeleton (Table 7.18). Strontium concentrations tend to decrease with increasing size in the amphipod, P. walkeri (Palmer et al., 2006), and this may confound the interpretation of strontium residues in this and other species. The ability of whole crustaceans to accumulate strontium from seawater is low, ranging from 0.3 to 1.0 times the concentration in seawater (Ichikawa, 1961; Ketchum and Bowen, 1958). Some organs show greater strontium accumulation potential than others. Leander sp., for example, shows strontium concentration factors of 0.2 in muscle, 1.3 in viscera, and 15.0 in exoskeleton (Hiyama and Shimizu, 1964). Molts of M. norvegica account for 23% of the strontium body burden in that species and molts
Crustaceans 471 Table 7.18: Strontium Concentrations in Field Collections of Crustaceans Organism
Concentration
Copepods Whole Whole
125.0 DW 1500.0 AW
1 2
Shrimp, Crangon sp.; whole
42.1 DW
9
Crustaceans Whole Exoskeleton; 15 spp.
(0.97-17.0) FW 2210.0-6970.0 DW
3 4
Euphausiid, Euphausia pacifica; whole
(440.0-1000.0) AW
5
Euphausiids; whole
163.0 DW
1
Lobster Muscle Carapace Head
59.0 AW 4000.0 AW 6800.0 AW
6 6 6
Euphausiid, Meganyctiphanes norvegica Molts Whole
350.0 DW 117.0 DW
7 7
Mysidacean, Neomysis japonica; whole
360.0 AW
5
Black tiger shrimp, Penaeus monodon; juveniles; Vietnam; 2003-2005; max. values Muscle Exoskeleton Hepatopancreas
9.3 DW 2060.0 DW 81.7 DW
10 10 10
Shrimp Muscle Carapace Whole
510.0 AW 600.0 AW 1500.0 AW
6 6 6
890.0 AW vs. 1140.0 AW
8
Zooplankton; surface vs. > 99 m depth collections
Reference
a
Values are in mg Sr/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Martin and Knauer, 1973; 2, Vinogradova and Koual’skiy, 1962; 3, Mauchline and Templeton, 1966; 4, Gibbs and Bryan, 1972; 5, Fukai et al., 1962; 6, Lowman et al., 1970; 7, Fowler, 1977; 8, Martin, 1970; 9, Zumholz et al., 2006; 10, Tu et al., 2008.
contribute significantly (3.2 mg Sr/kg euphausiid molt per day) to strontium cycling in the Mediterranean Sea (Fowler, 1977). Strontium can also accumulate in viscera of the crabs C. maenas (Martin, 1972) and Birgus latro (Chakravarti and Eisler, 1961). In Birgus, the fat content of liver accounted for an average of 47% of the wet weight, but less than 0.5% of the total strontium content; variability in fat content of crustacean liver should be
472 Chapter 7 considered in evaluating mineral composition of this organ, preferably by expressing results on a fat-free basis (Chakravarti and Eisler, 1961).
7.48 Terbium Amphipods from East Antarctica contained <0.006 mg Tb/kg DW, or below the current detection limit (Palmer et al., 2006).
7.49 Thallium Maximum thallium concentrations in tissues of juvenile tiger shrimp, P. monodon, from Vietnam in 2003-2005, in mg Tl/kg DW, were 0.005 in muscle, 0.01 in exoskeleton, and 0.005 in hepatopancreas (Tu et al., 2008).
7.50 Thorium A concentration factor of 20 from seawater is reported for comprised mainly of copepods (Kharkar et al., 1976).
228
Th and zooplankton samples
7.51 Thulium Whole amphipods collected from East Antarctica in 2003-2004 had <0.005 mg Tm/kg DW, or below the current detection limit (Palmer et al., 2006).
7.52 Tin Edible tissues of crustaceans from North American waters contained a maximum of 2.0 mg total Sn/kg fresh tissue (Table 7.19). Total organotin concentrations in edible tissues of six species of crustaceans sold commercially in France in 2005 contained a maximum of 0.014 mg total organotins/kg FW, mostly tributyltins (Guerin et al., 2007; Table 7.19). However, triphenyltin concentrations in muscle of crustaceans from Bohai Bay, China in 2002 were higher than tributyltin concentrations, suggesting trophic magnification of triphenyltins through the algae-mollusc-crustacean food chain (Table 7.19; Hu et al., 2006). In aquatic systems, triorganotins were the most toxic group of organotins tested, followed in decreasing order of toxicity by diorganotins, tetraorganotins, and monoorganotins (Argese et al., 1998). Within each series, butyltin and phenyltin compounds seemed most toxic (Argese et al., 1998). The toxicity of triorganotin compounds is attributed, in part, to their ability to bind to proteins and to inhibit oxidative phosphorylation (Blunden and Chapman, 1986; Davies and Smith, 1982; Duncan, 1980; Smith, 1978; WHO, 1980). The derangement of triorganotin-induced energy-coupled processes, which occur at the membrane level, appears
Crustaceans 473 Table 7.19: Tin, Titanium, and Tungsten Concentrations in Field Collections of Crustaceans Element and Organism
Concentration
Reference
a
Tin Bohai Bay, North China; 2002; soft tissues Crab, Portunus trituberculatus Monobutyltins Dibutyltins Tributyltins Triphenyltins Burrowing shrimp, Upogebia sp. Monobutyltins Dibutyltins Tributyltins Triphenyltins
0.003 FW 0.005 FW 0.005 FW 0.017 FW
11 11 11 11
0.015 FW 0.005 FW 0.003 FW 0.017 FW
11 11 11 11
Copepod, Calanus finmarchicus; whole
<1.0 AW
1
Blue crab, Callinectes sapidus Pensacola, Florida; 2003-2004; hepatopancreas vs. muscle
Max. 0.75 FW vs. max. 0.55 FW
Copepod, Centropages spp.; whole
50.0 AW
1
Copepods; whole
70.0 AW
2
Crustaceans; 16 commercial species; North America; edible tissues 5 spp. 8 spp. 3 spp.
0.6-0.7 FW 0.7-0.9 FW 0.9-2.0 FW
3 3 3
0.0016-0.0087 FW
9
0.0140 FW 0.0115 FW 0.0022 FW 0.0003 FW
9 9 9 9
American lobster, Homarus americanus; muscle
0.6 FW
6
Amphipod, Paramoera walkeri; East Antarctica; 2003-2004; whole
(0.05-0.12) DW
8
France; January-April 2005; edible portions; sold commercially; organotins Total organotins; 5 spp. Crab, unidentified Total organotins Butyltins Phenyltins Octyltins
10
(Continues)
474 Chapter 7 Table 7.19: Cont’d Element and Organism
Concentration
Black tiger shrimp, Penaeus monodon; Vietnam; 2003-2005; juveniles; max. values Muscle Exoskeleton Hepatopancreas
0.17 DW 0.18 DW 0.28 DW
Zooplankton; Osaka Bay, Japan; 1990; whole; tributyltins
Reference
a
12 12 12
(0.3-4.2) FW
7
Copepod, Calanus finmarchicus; whole
10.0 AW
1
Copepod, Centropages spp.; whole
3.0 AW
1
Copepods; whole
700.0 AW
2
Euphausiid, Euphausia krohni; whole
9.0 AW
1
<0.005 AW; < 0.0003 DW
4, 5
Titanium
Tungsten Shrimp, Pandalus spp; soft parts
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Nicholls et al., 1959; 2, Vinogradova and Koual’skiy, 1962; 3, Hall et al., 1978; 4, Fukai and Meinke, 1959; 5, Fukai and Meinke, 1962; 6, Jenkins, 1980; 7, Harino et al., 1998; 8, Palmer et al., 2006; 9, Guerin et al., 2007; 10, Karouna-Renier et al., 2007; 11, Hu et al., 2006; 12, Tu et al., 2008.
to be the most probable mode of action in aquatic organisms (Argese et al., 1998). Triorganotins also interfere with phagocytosis and other pathways where sulfhydryl groups play a pivotal role (Elferink et al., 1986) and inhibit uptake of gamma-aminobutyric acid and Na+-K+-ATPase in brain (Costa, 1985). Impairment of phagocytosis and related activities of polymorphonuclear eukaryotes may enhance susceptibility for infection (Elferink et al., 1986). Adverse effects of TBT compounds to sensitive species of crustaceans tested are documented at 0.0000011-0.001 mg/L. Exposure of juvenile amphipods, Caprella danilevskii, for 49 days to tributyltin concentrations near or below ambient levels in seawater adversely affected adult reproduction; the total number of juveniles per female decreased from 39.5 in controls to 24.5 in those held in 0.0000011 mg TBT/L, and 17.5 in 0.0000107 mg TBT/L (Aono and Takeuchi, 2008). Female copepods, Pseudodiaptomus marinus, exposed to 0.000006 mg TBT/L for 72 h show a significant delay in egg sac production; at 0.00002 mg/L, fecundity was increased and frequency of males increased (Huang et al., 2006). Other effects include reduced survival in 96 h of Pseudodiaptomus at 0.00057 mg/L (Huang et al., 2006); death in 7 days of the copepod E. affinis at 0.0001 mg/L (Hall et al., 1988a,b); reduced survival in
Crustaceans 475 5 weeks of the Baltic amphipod Gammarus oceanicus at 0.0003 mg/L (Laughlin et al., 1984); 50% immobilization in 6 days of the copepod A. tonsa at 0.0004 mg/L (U’ren, 1983); a decrease in the proportion of females of T. japonicus copepods after long-term exposure to 0.0001 mg/L (Lee et al., 2008); abnormal limb regeneration of the fiddler crab U. pugilator at 0.0005 mg/L (Weis and Kim, 1988; Weis et al., 1987); and death in 96 h of juvenile mysidaceans Metamysidopsis elongatus at 0.0005-0.001 mg/L (Hall and Pinkney, 1985). Acute toxicity bioassays of 96-h duration with adult T. japonicus copepods, a species recommended for routine ecotoxicity testing in the western Pacific Ocean region, showed that all survived 0.02 mg tributyltin/L, 10% died at 0.03, and 50% died at 0.05 mg TBT/L (Lee et al., 2007). Several factors are known to affect sensitivity, and accumulations of TBT and other organotins in crustaceans. For example, early developmental stages of mysid shrimps were more sensitive to organotins than later developmental stages (Thompson et al., 1985). Mortality of zoeae of fiddler crab, U. pugilator, to trimethyltins was greatest at comparatively elevated temperatures and reduced salinities (Thompson et al., 1985). Survival of grass shrimp, P. pugio, was decreased by several orders of magnitude when exposed simultaneously to organotins through contaminated water and contaminated sediments (Clark et al., 1987). Uptake of organotins from the medium by crustaceans was variable and greatest at low ambient tin concentrations (<0.001 mg/L), lengthy exposures, and high organism lipid content (Champ, 1986; Laughlin et al., 1986; Thain and Waldock, 1986; Thompson et al., 1985); however, diet remains the major pathway of tin uptake in crustaceans (Evans and Laughlin, 1984; Hall and Pinkney, 1985; Laughlin et al., 1986). Structure-activity relations seem to have high predictive capacity in hazard assessment, and those for organotins are particularly promising (Vighi and Calamari, 1985). For example, studies on the biocidal properties of structurally distinct diorganotins (R2SnX2) and triorganotins (R3SnX) to zoeae of the mud crab, R. harrisii, show, within a homologous series, that diorganotins are less toxic than the corresponding triorganotins, and the toxicity of organotins to crab zoeae are a function of the hydrophobic characteristics conferred by the number and structure of the organic ligands (Laughlin et al., 1985). For example, at least 50% mortality occurs in diorganotins (triorganotins), in mg Sn/L, at 10.8 dimethyltin (0.067 trimethyltin), at 2.4 diethyltin (0.053), at 2.2 dipropyltin (0.03), at 0.78 dibutyltin (0.011), at 0.27 diphenyltin (0.007), and at 0.082 dicyclohexyltin (0.0023) (Laughlin et al., 1985). Abiotic and biological degradation of organotins generally occurs through sequential dealkylation and dearylation (Blunden et al., 1985; Chau et al., 1984; Eisler, 2000g; Smith, 1981; WHO, 1980; Zuckerman et al., 1978). Organotin compounds undergo successive cleavage of tin-carbon bonds to ultimately produce inorganic tin as follows: R4Sn (via k4) to R3SnX (k3) to R2SnX2 (k2) to RSnX3 (k1) to SnX4. The reaction rate, k, usually proceeds as k4 > k3 > k2 = k1. The breaking of a Sn-C bond can occur via ultraviolet radiation, biological cleavage, gamma irradiation, and thermal cleavage (Blunden and Chapman, 1982, 1986; Blunden et al., 1985; Thompson et al., 1985; WHO, 1980). In general, UV and biological
476 Chapter 7 cleavage are the most important processes. The main abiotic factors that limit organotin persistence include elevated temperatures, increased sunlight, and aerobic conditions (Eisler, 2000g). The biological effects of the tetraorganotin compounds, R4Sn, seem to be caused entirely by the R3SnX derivative that is produced by their rapid in vivo dealkylation (Blunden and Chapman, 1986; Davies and Smith, 1982; Duncan, 1980). Marine sediment concentrations less than 0.l61 mg TBT/kg are considered safe to mysid shrimp, although proposed sediment criteria range from <0.001 to <0.007 mg/kg (Cardwell and Sheldon, 1986). For seawater, proposed TBT concentrations considered safe to aquatic life range from less than 0.000002 mg/L (Huggett et al., 1992) to the less stringent <0.00001 to <0.000002 in the United States (Harrington, 1991; Pinkney et al., 1990) and <0.00002 mg/L in the United Kingdom (Side, 1987). The banning of TBT-containing antifouling paints in the United Kingdom in 1987 was accompanied by increases in abundance and diversity of benthic fauna, especially amphipod crustaceans in River Crouch Estuary (Rees et al., 1999; Waldock et al., 1999).
7.53 Titanium The maximum titanium value recorded in field collections of crustaceans was 700.0 mg Ti/kg AW from Black Sea copepods (Table 7.19).
7.54 Tungsten The single datum available for tungsten indicated that this element was below analytical detection limits in a pandalid shrimp (Table 7.19).
7.55 Uranium Whole shrimp, Crangon sp., had 0.00076 mg U/kg DW (Zumholz et al., 2006). Uranium-238 in zooplankton samples consisting mainly of copepods was only 0.17 times 238U levels in ambient seawater (Kharkar et al., 1976).
7.56 Vanadium Vanadium concentrations in any crustacean tissue did not exceed 0.5 mg V/kg FW, 3.3 mg V/kg DW, or 70.0 mg V/kg AW (Table 7.20). The significance of vanadium in crustaceans in not known with certainty.
7.57 Ytterbium A maximum of <0.007 mg Yb/kg DW, or below the current detection limit, was found in amphipods from east Antarctica (Palmer et al., 2006).
Crustaceans 477 Table 7.20: Vanadium Concentrations in Field Collections of Crustaceans Organism
Concentration
Reference
Copepod, Calanus finmarchicus; whole
21.0 AW
1
Copepod, Centropages spp.; whole
16.0 AW
1
Copepods Whole Whole
70.0 AW 3.3 DW
2 3
Crustaceans; 16 commercial species; North America; edible tissues 3 spp. 5 spp. 8 spp.
0.1-0.3 FW 0.3-0.4 FW 0.4-0.5 FW
4 4 4
Euphausiid, Euphausia krohni; whole
45.0 AW
1
Shrimp, Pandalus sp. Whole Soft parts
1.1 AW 0.07 AW
5 6
Tiger shrimp, Penaeus monodon; Vietnam; 2003-2005; juveniles; max. values Muscle Exoskeleton Hepatopancreas
0.063 DW 0.80 DW 0.80 DW
8 8 8
Barnacle, Tetraclita sp.; whole
0.36 FW
7
a
Values are in mg V/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Nicholls et al., 1959; 2, Vinogradova and Koual’skiy, 1962; 3, Tijoe et al., 1977; 4, Hall et al., 1978; 5, Fukai and Meinke, 1959; 6, Fukai and Meinke, 1962; 7, Ikebe and Tanaka, 1979; 8, Tu et al., 2008.
7.58 Yttrium Whole shrimp, Crangon sp., contained 0.0033 mg Y/kg DW (Zumholz et al., 2006).
7.59 Zinc There is general agreement that zinc is present in all tissues of all crustaceans examined; concentrations are elevated in organisms near anthropogenic point sources of zinc contamination; concentrations are normally grossly elevated in some species of barnacles; zinc-specific sites of accumulation in crustaceans include the hepatopancreas; interspecies variations in zinc content are considerable, even among closely related species; intraspecies differences in zinc content are modified by a host of biologic and abiotic variables; and many species regulate zinc within a threshold range of concentrations (as quoted in Eisler, 2000h).
478 Chapter 7 In the case of deep sea shrimps collected from hydrothermal vent sites, extremely high concentrations of zinc (>100,000.0 mg/kg DW) were measured in gut or adsorbed onto tissues (Kadar et al., 2006; Table 7.21). Concentrations of total zinc in organs and tissues of representative species of marine, estuarine, and oceanic crustaceans from numerous geographic locations are listed (Table 7.21). According to Pequegnat et al. (1969), zinc is not limiting to normal life processes in the marine environment and is accumulated in excess of the organism’s immediate needs, at least on the basis of enzymatically bound zinc. The information in Table 7.21 tends to support the observations that zinc is not limiting, and in several cases probably accumulated far in excess of biological requirements. Zinc concentrations in crustacean tissues are usually less than 75.0 mg/kg FW or <100.0 mg/ kg DW; exceptions include hepatopancreas, molts, eggs, fecal pellets, barnacles, and proximity to hydrothermal vents (Table 7.21). In crustaceans, zinc is slightly elevated in hepatopancreas, but most tissues are only 2-3 times higher than muscle (Sprague, 1986). The high concentration recorded in crustacean muscle of 57.0 mg Zn/kg FW in king crab, Paralithodes camtschaticus (USNAS, 1989), was associated with two metal-binding proteins of MW 11,500 and 27,000 (Eisler, 1981). In crustacean tissues, zinc levels were usually highest in summer, at low salinities, and in young animals (Eisler, 1981), although young amphipods had higher zinc residues than older stages (Rainbow, 1989). Seasonal accumulations of whole-body zinc in the shrimp Palaemon elegans during spring and summer and loss in winter seem to reflect water zinc concentration in the range 0.000-0.009 mg/L (Alliot and Frenet-Piron, 1990). Zinc is present in crustacean serum at concentrations of more than 1000 times higher than ambient seawater; in serum, it serves mainly as a cofactor of carbonic anhydrase, the principal enzyme involved in calcification. Serum zinc concentrations in crustaceans seem to be independent of season, water temperature, or salinity (Sprague, 1986). In the prawn, P. indicus, most of the zinc in hepatopancreas and gill is in the insoluble fraction (Table 7.21) and is presumably bound by phosphorous, calcium, magnesium, and silicon (Nunez-Nogueira et al., 2006a). Exposure to 0.1 mg Zn/L for 10 days resulted in negligible uptake or change in soluble/insoluble ratios of gill and hepatopancreas (NunezNogueira et al., 2006a). In another study, Nunez-Nogueira et al. (2006b) demonstrated the importance of diet in zinc assimilation; they fed juvenile P. indicus radiolabeled 65Zn squid muscle (L. vulgaris) or filaments of a green alga (Cladophora sp.) for 60 min then transferred to clean seawater. The AE was calculated from the point at which no radioactivity was detected in feces or about 6 h after ingestion of algae and 10 h after ingestion of squid muscle. The AE of zinc ranged between 50% and 69% from algae and between 60% and 70% from squid muscle. Prawns fed algae and dissected after 49 h depuration had 53% of the 65Zn in hepatopancreas, 24% in exoskeleton, and 13% in muscle. Prawns fed squid muscle and dissected 134 h after initial feeding had 29% of the 65Zn in abdominal muscle and 21% in hepatopancreas (Nunez-Nogueira et al., 2006b).
Crustaceans 479 Table 7.21: Zinc Concentrations in Field Collections of Crustaceans Organism
Concentration
Copepod, Acartia clausi; whole
1270.0 DW
1
Amphipods; whole
43.0 DW
2
Amphipods; whole; western Britain; coastal waters; 4 spp.
104.0-506.0 DW
47
Barnacle, Balanus amphitrite; soft parts
Max. 1937.0 DW
49
Barnacle, Balanus amphitrite communis; soft parts
71.5 FW
Barents Sea and environs; 1991-2000; whole Copepods; 4 spp. Euphausid, Meganyctiphanes norvegica Amphipod, Themisto abyssorum Shrimp, Pandalus borealis
108.0-509.0 DW 73.0 DW 110.0 DW 79.0 DW
Barnacle, Balanus balanoides; soft parts
(4500.0-23,100.0) DW
Barnacles; summer 2001; soft parts; Natal, Brazil Fistulobalanus citerosum Balanus amphitrite
(1624.0-1719.0) DW 1185.0 DW
Barnacles Soft parts Whole, 3 spp. Soft parts, 3 spp. Gut and parenchyma, 3 spp.
Max. 3300.0 DW 138.0-3438.0 FW 110.0-2980.0 FW Max. 2220.0 FW
Calcasieu River Estuary, Louisiana Blue crab, Callinectes sapidus; muscle Brown shrimp, Penaeus aztecus; whole White shrimp, Penaeus setiferus; whole Blue crab, Callinectes sapidus Whole Whole Muscle; August 2005; Iskenderun Bay, Turkey Pensacola, Florida; 2003-2004 Hepatopancreas Muscle
Reference
a
4
76 76 76 76 5
67 67 6 7, 8 7, 8 7, 8
112.0 (106.0-213.0) DW (46.0-61.0) DW
50 50
(44.0-62.0) DW
50
14.0 DW 17.0 FW 9.1 (3.6-18.3) DW
9 11 63
Max. 48.0 FW Max. 54.0 FW
69 69 (Continues)
480 Chapter 7 Table 7.21: Cont’d Organism
Concentration
Reference
Crab, Cancer irroratus Digestive diverticula Muscle Digestive gland
(35.0-43.0) DW (32.1-64.6) FW (18.1-31.5) FW
12 13, 14 13, 14
Crab, Cancer pagurus Whole Muscle Stomach fluid Hepatopancreas Urine Excretory organ Gill Shell Vas deferens External eggs Blood Whole Claw muscle Abdominal muscle Gills
27.0 FW 64.0 FW 15.0 FW 45.0 FW 0.6 FW 29.0 FW 42.0 FW 3.0 FW 16.0 FW 94.0 FW 49.0 FW (21.3-34.5) (51.0-61.0) (29.2-66.0) (10.0-30.0)
FW FW FW FW
3 3 3 3 3 3 3 3 3 3 3 15 15 15 15
Crab, Carcinus maenas Whole Hepatopancreas Leg muscle Whole Blood Muscle Stomach fluid Hepatopancreas Urine Excretory organ Gill Shell Vas deferens Whole Hemolymph
24.5 FW 56.0 FW 44.0 FW 22.0 FW 36.0 FW 44.0 FW 18.0 FW 56.0 FW 0.4 FW 19.0 FW 26.0 FW 3.0 FW 23.0 FW (25.1-38.8) FW 32.2 FW
16 16 16 3 3 3 3 3 3 3 3 3 3 17 18
Copepods Whole Whole Whole
60.0 DW (62.0-170.0) DW 4000.0 AW
2 11 20
a
(Continues)
Crustaceans 481 Table 7.21: Organism Whole Whole; 3 spp.; Taiwan; near sewage outfall Crabs Muscle Carapace
Cont’d
Concentration
Reference
(160.0-165.0) DW 132.0-3891.0 DW
21 66
(24.0-51.0) FW; (120.0-250.0) DW; (750.0-1900.0) AW (7.0-46.0) FW; (15.0-120.0) DW; (23.0-110.0) AW
22 22
Shrimp, Crangon sp.; whole
2.8 DW
71
Shrimp, Crangon vulgaris Whole Blood Muscle Hepatopancreas Whole
34.0 FW 23.0 FW 14.0 FW 78.0 FW 26.4 FW
3 3 3 3 17
(23.7-28.9) FW 55.0-290.0 DW Max. 275.0 DW 50.2-84.1 DW
23 24 25 60
10.0-20.0 FW 20.0-40.0 FW 40.0-60.0 FW
26 26 26
(35.0-57.0) DW (44.0-96.0) DW (24.0-44.0) DW
51 51 51
(73.0-109.0) DW (690.0-27,837.0) DW 1050.0-5144.0 DW; max. 113,000.0 DW (60.0-170.0) DW 164.0-177.0 DW; max. 1300.0 DW 68.00-102.0 DW; max. 340.0 DW (53.0-83.0) DW 94.0 DW 14.0-69.0 DW; max. 150.0 DW
52 52 53
Crustaceans Whole Soft parts, 12 spp. Whole Whole; 4 spp.; Antarctica; 2004 Edible tissues, 16 spp. 8 spp. 5 spp. 3 spp. Northeast Atlantic Ocean; July 1985; whole Decapods Euphausiids Mysids Soft parts Amphipods Barnacles Barnacles Copepods Copepods Crabs Euphausiids Isopods Shrimps
a
52 53 53 52 52 53 (Continues)
482 Chapter 7 Table 7.21: Cont’d Organism Near marine outfall of lead smelter; South Australia; 5 spp.; whole 2.5-5.2 km from outfall 18-18.8 km from outfall Deep sea shrimps; Rainbow hydrothermal vent site; mid-Atlantic Ridge; adults; summer 2002 Rimicaris exoculata; adults Whole body Cuticle Gill Antennae Muscle Digestive gland Pylorus Microcaris fortunata; adults Whole body Cuticle Gill Antennae Muscle Digestive gland Pylorus
Concentration
Reference
148.0 DW; max. 767.0 DW 68.0 DW
54 54
1800.0 DW 500.0 DW 2900.0 DW 200.0 DW 300.0 DW 800.0 DW 25,900.0 DW
64 64 64 64 64 64 64
2500.0 DW 300.0 DW 4300.0 DW 900.0 DW 200.0 DW 600.0 DW 40,900.0 DW
64 64 64 64 64 64 64
Crab, Eupagurus bernhardus Whole Blood Leg muscle Abdominal muscle Stomach fluid Hepatopancreas Excretory organ Gill Vas deferens Ovary
28.0 FW 11.6 FW 36.0 FW 24.0 FW 26.0 FW 69.0 FW 23.0 FW 69.0 FW 27.0 FW 46.0 FW
Euphausiid, Euphausia pacifica Whole Whole
13.0 FW (50.0-110.0) DW
27 28
Euphausiid, Euphausia superba Whole Whole; Antarctica
68.0 (42.0-75.0) DW 41.3 DW
48 59
a
3 3 3 3 3 3 3 3 3 3
(Continues)
Crustaceans 483 Table 7.21:
Cont’d
Organism
Concentration
Reference
Euphausiids Whole Whole Whole
(53.0-83.0) DW 430.0 AW 17.1 FW
Lobster, Galathea squamifera Whole Blood Muscle Stomach fluid Hepatopancreas Gill Shell
18.0 FW 2.5 FW 10.0 FW 47.0 FW 49.0 FW 27.0 FW 9.0 FW
American lobster, Homarus americanus Gills Green gland Hepatopancreas Pincer muscle Tail muscle
(102.0-126.0) DW (114.0-148.0) DW (70.0-135.0) DW (100.0-127.0) DW 80.0 DW
55 55 55 55 55
Lobster, Homarus vulgaris Muscle Slow-contracting Fast contracting Whole Whole Blood Leg muscle Abdominal muscle Stomach fluid Hepatopancreas Urine Excretory organ Gill Shell Vas deferens Ovary Whole Leg muscle Blood Urine Excretory organs Abdominal muscle
(93.0-105.0) DW (13.0-20.0) DW (13.8-16.7) FW 23.0 FW 7.4 FW 60.0 FW 15.0 FW 0.7 FW 34.0 FW 2.2 FW 20.0 FW 15.0 FW 5.0 FW 13.0 FW 50.0 FW 22.0 FW 64.0 FW (4.7-11.8) FW (0.1-6.1) FW (17.3-21.9) FW (14.3-17.7) FW
31 31 15 3 3 3 3 3 3, 16 3 3 3 3 3 3 16 16 32 32 32 32
a
19 29 30 3 3 3 3 3 3 3
(Continues)
484 Chapter 7 Table 7.21: Cont’d Organism Hepatopancreas Stomach fluid Gill Shell Vas deferens Ovary
Concentration
Reference
(23.3-59.5) FW (0.5-1.3) FW (12.8-19.9) FW (0.9-8.9) FW 13.3 FW 50.2 FW
32 32 32 32 32 32
Hydrothermal vent field; mid-Atlantic Ridge; 2001 Shrimp, Chlorocaris chacei; 2001; 1700 m deep; digestive gland vs. muscle Hydrothermal crab, Segonzacia mesatlantica; digestive gland vs. muscle 840 m deep 1700 m deep 2300 m deep
2330.0 DW vs. 50.0 DW
72
439.0 DW vs. 111.0 DW 133.0 DW vs. 268.0 DW 108.0 DW vs. 271.0 DW
72 72 72
Lobster, Jasus lalandi; muscle
17.0 FW
33, 34
Lobster Carapace Head Muscle
88.0 AW 140.0 AW 600.0 AW
22 22 22
57.8 DW; max. 80.4 DW
61
Blue shrimp, Litopenaeus stylirostris; Gulf of California, Mexico; 2004-2005; muscle Crab, Maia squinado Whole Blood Muscle Stomach fluid Hepatopancreas Urine Excretory organ Gill Shell Vas deferens Ovary
21.0 FW 2.4 FW 63.0 FW 31.0 FW 71.0 FW 0.3 FW 15.0 FW 10.0 FW 5.0 FW 16.0 FW 45.0 FW
Euphausiid, Meganyctiphanes norvegica Whole Whole
104.0 DW 62.0 DW
a
3 3 3 3 3 3 3 3 3 3 3 35 36 (Continues)
Crustaceans 485 Table 7.21: Organism Molts Eggs Fecal pellets Whole Firth of Clyde Northeast Atlantic Ocean
Cont’d
Concentration
Reference
146.0 DW 318.0 DW 950.0 DW
36 36 36
43.0 (27.0-62.0) DW 102.0 (40.0-281.0) DW
48 48
Peneid shrimp, Melicertus kerathurus; Lesina lagoon, Italy; October 2004; 3 sites Muscle Exoskeleton
41.8-60.4 DW 46.3-59.3 DW
75 75
Shrimp, Metapenaeus affinis; muscle
58.3 DW
37
1210.0 DW
73
61.0 DW 53.0 DW
73 73
Lobster, Nephrops norvegicus; muscle
8.5-12.2 FW
15
Amphipod, Orchestoidea corniculata; whole
150.0-300.0 DW
38
Crab, Paguristes sericeus; whole
(29.0-37.0) FW; (92.0-120.0) DW; (230.0-360.0) AW
39
Mexico; Gulf of California; 1999-2000 Barnacle, Balanus eburneus; soft parts Shrimps; muscle Litopenaeus stylirostris Litopenaeus vanamei
Shrimp, Palaemon serratus Whole Blood Muscle Hepatopancreas Gill External eggs
21.0 FW 38.0 FW 10.0 FW 64.0 FW 35.0 FW 24.0 FW
3 3 3 3 3 3
Shrimp, Palaemon squilla; whole
30.0 FW
3
58.0 FW 55.0 FW
56 56
18.0 FW 30.0 FW
56 56
Grass shrimp, Palaemonetes pugio From sediments containing 627 mg Zn/kg DW Exoskeleton Muscle From sediments containing 8 mg Zn/kg DW Exoskeleton Muscle
a
(Continues)
486 Chapter 7 Table 7.21: Cont’d Organism
Concentration
Shrimp, Palaemonetes varians Whole Blood Muscle Hepatopancreas
20.0 FW 87.0 FW 14.0 FW 65.0 FW
3 3 3 3
Lobster, Palinurus vulgaris Blood Leg muscle Abdominal muscle Stomach fluid Hepatopancreas Urine Excretory organ Gill Shell Ovary External eggs
3.1 FW 66.0 FW 20.0 FW 48.0 FW 97.0 FW 0.6 FW 20.0 FW 20.0 FW 16.0 FW 82.0 FW 107.0 FW
3 3 3 3 3 3 3 3 3 3 3
Amphipod, Paramoera walkeri; East Antarctica; 2003-2004; whole
Reference
(48.0-82.0) DW
59
Shrimp, Pandalus jordani Whole Muscle
58.0 FW 11.0 FW
27 27
Prawn, Pandalus montagui Tail Whole Carcass Egg Hepatopancreas Cuticle Eye Gill Hepatopancreas Muscle Whole
44.0 DW 70.0 DW 78.0 DW 100.0 DW 118.0 DW 57.0 DW 70.0 DW 106.0 DW 30.0 DW 57.0 DW 58.0 DW
40 40 40 40 40 57 57 57 57 57 57
Lobster, Panulirus argus; muscle
32.8 FW; 97.0 DW
22
a
Marsh crab, Parasesarma erythodactyla; soft parts; 2002; New South Wales, Australia; metals-contaminated estuary (Continues)
Crustaceans 487 Table 7.21: Organism Males Females
Cont’d
Concentration
Reference
Max. 403.0 DW Max. 292.0 DW
68 68
14.0 DW 47.7 DW 28.3 DW 105.0 DW
9 10 10 10
Shrimp, Penaeus brasiliensis; adults; whole
(47.0-75.0) FW; (181.0-290.0) DW
58
Shrimp, Penaeus japonica; muscle
63.0 DW
41
Shrimp, Penaeus monodon; muscle
(21.5-70.0) DW
37
White shrimp, Peneus setiferus; muscle; Gulf of Mexico
107.0 DW
62
62.0 DW 9.6 FW
42 11
150.3 DW 25.1 DW 125.2 DW
70 70 70
78.4 DW 35.0 DW 43.4 DW
70 70 70
Tiger shrimp, Penaeus monodon; Vietnam; 2003-2005; juveniles; max. values Muscle Exoskeleton Hepatopancreas
51.0 DW 25.8 DW 165.0 DW
74 74 74
Crab, Porcellana platycheles; whole
54.0 FW
3
Crab, Portunus depurator Whole Blood Muscle Stomach fluid Hepatopancreas Urine
21.0 FW 1.8 FW 15.0 FW 13.0 FW 24.0 FW 0.3 FW
3 3 3 3 3 3
Shrimp, Penaeus aztecus Whole Muscle Exoskeleton Viscera
Shrimp, Penaeus spp. Whole Whole Prawn, Penaeus indicus; juveniles Hepatopancreas Whole Soluble fraction Insoluble fraction Gills Whole Soluble fraction Insoluble fraction
a
(Continues)
488 Chapter 7 Table 7.21: Cont’d Organism Excretory organ Gill Shell
Concentration
Reference
8.0 FW 25.0 FW 3.0 FW
3 3 3
Crab, Portunus holsatus; whole
34.1 FW
43
Crab, Portunus pelagicus; muscle
(73.7-80.2) DW
37
Crab, Portunus puber Whole Blood Muscle Stomach fluid Hepatopancreas Urine Excretory organ Gill Shell Vas deferens Ovary
27.0 FW 7.0 FW 28.0 FW 15.0 FW 42.0 FW 0.2 FW 10.0 FW 23.0 FW 13.0 FW 20.0 FW 87.0 FW
Crab, Pugettia producta; fecal pellets
(39.0-119.0) AW
44
56.3 DW 10.3 DW (12.0-36.0) FW; (44.0-130.0) DW; (610.0-1100.0) AW (4.0-39.0) FW; (17.0-110.0) DW; (190.0-710.0) AW 790.0 AW 76.0 DW
10 10 22
Stomatopod, Squilla oratoria; muscle
110.0 DW
41
Amphipods, Themisto spp.; whole
76.0 (72.0-81.0) DW
48
165.8 DW 46.6 DW
65 65
149.8 DW 46.6 DW
65 65
Shrimp Muscle Exoskeleton Muscle Carapace Whole Molts
Fiddler crab, Uca pugnax; New Jersey Intermolt; contaminated site Soft tissue Carapace Intermolt; reference site Soft tissue Carapace Immediate postmolt; contaminated site
a
3 3 3 3 3 3 3 3 3 3 3
22 22 45
(Continues)
Crustaceans 489 Table 7.21: Organism Soft tissue Exoskeleton Immediate postmolt; reference site Soft tissue Exoskeleton
Cont’d
Concentration
Reference
133.3 DW 79.6 DW
65 65
108.8 DW 25.6 DW
65 65
Crab, Xantho incisus; whole
26.0 FW
Zooplankton; mostly copepods; whole; N.W. Mediterranean Sea
268.0 (52.0-742.0) DW
a
3 46
Values are in mg Zn/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Zafiropoulos and Grimanis, 1977; 2, Bohn and McElroy, 1976; 3, Bryan, 1968; 4, Sastry and Bhatt, 1965; 5, Ireland, 1973; 6, Stenner and Nickless, 1975; 7, Walker et al., 1975a; 8, Walker et al., 1975b; 9, Sims and Presley, 1976; 10, Horowitz and Presley, 1977; 11, Wolfe et al., 1973; 12, Greig, 1975; 13, Greig et al., 1977a; 14, Greig et al., 1977b; 15, Topping, 1973; 16, Bryan, 1966; 17, Wharfe and Van Den Broek, 1977; 18, Martin et al., 1977; 19, Martin and Knauer, 1973; 20, Vinogradova and Koual’skiy, 1962; 21, Tijoe et al., 1977; 22, Lowman et al., 1970; 23, Wright, 1976; 24, Stickney et al., 1975; 25, Stenner and Nickless, 1974b; 26, Hall et al., 1978; 27, Cutshall et al., 1977; 28, Robertson et al., 1972; 29, Robertson, 1967; 30, Greig and Wenzloff, 1977; 31, Bryan, 1967; 32, Bryan, 1964; 33, Van As et al., 1973; 34, Van As et al., 1975; 35, Leatherland et al., 1973; 36, Fowler, 1977; 37, Zingde et al., 1976; 38, Bender, 1975; 39, Lowman et al., 1966; 40, Ray et al., 1980; 41, Ishii et al., 1978; 42, Knauer, 1970; 43, DeClerck et al., 1979; 44, Boothe and Knauer, 1972; 45, Bertine and Goldberg, 1972; 46, Hardstedt-Romeo and Laumond, 1980; 47, Weeks and Moore, 1991; 48, Rainbow, 1989; 49, Anil and Wagh, 1988; 50, Ramelow et al., 1989; 51, Ridout et al., 1989; 52, White and Rainbow, 1985; 53, Sprague, 1986; 54, Ward et al., 1986; 55, Waiwood et al., 1987; 56, Khan et al., 1989; 57, Nugegoda and Rainbow, 1988b; 58, Shrestha and Morales, 1987; 59, Palmer et al., 2006; 60, Santos et al., 2006; 61, Frias-Espericueta et al., 2007; 62, Vazquez et al., 2001; 63, Turkmen et al., 2006; 64, Kadar et al., 2006; 65, Bergey and Weis, 2007; 66, Feng et al., 2006; 67, Silva et al., 2006; 68, MacFarlane et al., 2006; 69, Karouna-Renier et al., 2007; 70, Nunez-Nogueira et al., 2006a; 71, Zumholz et al., 2006; 72, Colaco et al., 2006; 73, Ruelas-Inzunza and Paez-Osuna, 2008; 74, Tu et al., 2008; 75, D’Adamo et al., 2008; 76, Zauke and Schmalenbach, 2006.
Zinc is toxic to the copepod A. tonsa when fed a zinc-contaminated algal diet (Bielmyer et al., 2006). In that study, diatoms (T. pseudonana) were held in seawater containing 0.0003 mg Zn/L for 7 days, reaching a zinc concentration of 0.55 mg Zn/kg DW diatom; diatoms, in turn, were fed to Acartia for 7 days, adversely affecting copepod reproduction. Authors note that the current proposed zinc criterion for marine life protection is 0.086 mg Zn/L, which exceeds the 0.0003 mg Zn/L used in this study to produce a toxic diet (Bielmyer et al., 2006). Crustaceans can accumulate zinc from both the medium and the diet (USEPA, 1987b). In uncontaminated waters, diet is the major source of zinc. Absorption from the stomach is efficient and occurs, in part, via the hepatopancreas. When a large pulse of zinc reaches the blood from the stomach, some is excreted, but much is resorbed and stored in hepatopancreas in a relatively nonlabile form. Ultimately, stored zinc is also excreted, although removal via the gut is unimportant (Bryan et al., 1986). Zinc absorption occurs initially at the gill surface, followed by transport on a saturable carrier in the cell wall, and is most efficient at low dissolved ambient zinc concentrations. Urinary excretion is an
490 Chapter 7 important body removal pathway, especially at high dissolved ambient concentrations when it can account for 70-80% of total zinc excretion (Bryan et al., 1986). Excess zinc in crustaceans is usually sequestered by metal-binding proteins and subsequently transported to storage or detoxification sites; soluble proteins and amino acids may contain 20-70% zinc (Sprague, 1986). Half-time persistence of zinc in the prawn, P. elegans, is about 17 days (Nugegoda and Rainbow, 1988b) and between 30 and 270 days for five other crustacean species (USNAS, 1989). Differences in half-time persistence are linked to differences in excretion rates of ionic zinc and complexed zinc. In general, ionic zinc is turned over faster than internally adsorbed zinc; molting accounts for 22-50% loss of the total zinc body burden in crabs (Bergey and Weis, 2007; Eisler, 1981). Crustaceans can regulate body concentrations of zinc against fluctuations in intake, although the ways in which regulation is achieved vary among species (Bryan et al., 1986). Regulation of whole-body zinc to a constant level is reported for many crustaceans, including intertidal prawns (Palaemon spp.), sublittoral prawns (P. montagui), green crab (C. maenas), lobster (Homarus gammarus), isopods (Asellus communis), and others (Bryan et al., 1986; Devineau and Amiard-Triquet, 1985; Johnson and Jones, 1989; Lewis and McIntosh, 1986; Nugegoda and Rainbow, 1988b; Rainbow and White, 1989). The body zinc concentration at which zinc is regulated in crustaceans usually increases with temperature, salinity, molting frequency, bioavailability of the uncomplexed free metal ions, and chelators in the medium (Nugegoda and Rainbow, 1987, 1988a, 1989a,b). Lobsters (H. gammarus) are able to equilibrate over a 30-day period with seawater containing between 0.002 and 0.505 mg Zn/L. In response to a 100-fold increase in seawater concentrations (0.005-0.5 mg/L), zinc levels in whole body, blood, hepatopancreas, excretory organs, and gills approximately doubled, but changed little in muscle. Shell zinc concentration increased about 12 times, largely through adsorption (Bryan et al., 1986). Regulation of zinc in lobster blood is achieved by balancing uptake through the gills against urinary excretion and loss over the body surface, including the gills (Bryan et al., 1986). The sublittoral prawn, P. montagui, can regulate total body zinc concentration to a constant level (75.0 mg/kg DW) and dissolved zinc concentrations up to 0.022 mg/L, beyond which there is net accumulation of body zinc. This threshold of zinc regulation breakdown is lower than that in P. elegans (0.093 mg/L) and Palaemonetes varians (0.190 mg Zn/L) under the same physicochemical conditions (Nugegoda and Rainbow, 1987, 1988a,b, 1989a,b,c; Rainbow and White, 1989). The authors conclude that regulation of body zinc concentration is most efficient in decapods adapted to the fluctuating environments of littoral habitats, possibly as a result of changes in permeability of uptake surfaces in combination with improved zinc excretion systems. Metallothioneins are actively involved in zinc regulation during normal growth processes in the blue crab, C. sapidus, as judged by a decrease in zinc content in hemolymph and digestive gland during molting (Engel, 1987). Unlike decapod crustaceans, marine amphipods are unable to regulate body zinc concentrations; amphipod body burdens of zinc
Crustaceans 491 may reflect sediment total zinc levels and suggest that certain groups may be suitable bioindicators (Rainbow et al., 1989). Molting had no effect on body zinc concentration in four species of adult marine amphipods (Weeks and Moore, 1991), and this forces a reexamination of the role of cast exuviae in zinc transport. In marsh crabs, P. erythodactyla, soft tissues reflected zinc concentrations in the ambient sediments; this pattern held for both males and females (MacFarlane et al., 2006). At higher salinities, males—but not females—showed significant increases in soft tissue zinc levels. In general, crabs with elevated zinc burdens had increased glutathione peroxidase activity; a similar case is made for lead and copper (MacFarlane et al., 2006). Bioconcentration factors for whole amphipods, P. walkeri, from the Australian Antarctic Territory in 1999-2000 ranged from 670 to 2800 when seawater contained 0.0004-0.0009 mg Zn/L; BCFs decreased as seawater zinc concentrations increased (Clason et al., 2003). Increased sensitivity to zinc occurred when seawater concentrations were in the range 0.009-0.026 mg Zn/L (Clason et al., 2003). Bioconcentration factors for zinc and representative crustaceans range widely from 85 to 1500,000 (Eisler, 1980). Numerous factors account for variations in zinc content between and among crustaceans, of which industrial contamination is one of the most important (Bloom and Ayling, 1977; Eisler, 2000h). In the case of barnacles, Balanus sp., the high (>3300.0 mg/kg DW soft parts) zinc levels recorded were attributed to inorganic granules that contained up to 38% zinc and which accumulated in tissues surrounding the midgut (Eisler, 1980, 1981). The granules consist of phosphorus, zinc, potassium, sulfur, and chlorine, in that order (Thomas and Ritz, 1986). These insoluble, membrane-limited, form in response to high zinc levels in the ambient seawater within 12 days of exposure, and concentrate in specialized cells around the gut, the stratum perintestinale (Sprague, 1986; Thomas and Ritz, 1986; Walker et al., 1975a,b). Zinc granules in barnacles represent a detoxification mechanism for surplus zinc (Thomas and Ritz, 1986). Older barnacles have greater whole-body zinc accumulations than younger stages, and accumulations change seasonally (Anil and Wagh, 1988). Zinc detoxification mechanisms of the stored zinc in the barnacle E. modestus includes production of metabolically inert zinc phosphate granules (Rainbow and White, 1989); however, E. modestus transplanted from an area of high-ambient zinc (0.101 mg/L) to a lowambient zinc (0.004 mg/L) environment lost zinc slowly (0.3% body burden daily) over an 11-week period. Whole-body zinc burden declined from 1554.0 to 125.0 mg/kg DW or about 4.1 mg/kg DW daily (Thomas and Ritz, 1986). In the crab, C. maenas, two heavy metal-binding proteins of about 27,000 and 11,500 MW, respectively, were isolated from the midgut gland (Rainbow and Scott, 1979). About 1.6% of the total soluble zinc in midgut gland was associated with the higher weight protein, and 6.3% with the lower MW protein. Both metal-binding proteins also bound to measurable amounts of copper and cadmium, but not lead (Rainbow and Scott, 1979).
492 Chapter 7 Acquired zinc tolerance is reported in amphipods from zinc-contaminated sewage wastes and in fiddler crabs (Uca spp.) from a metals-contaminated area. Uca from zinc-contaminated areas were more resistant to zinc than were conspecifics from pristine areas, as judged by increased survival and lower tissue zinc burdens (Devi, 1987; Devi and Rao, 1989a,b). Zinc-tolerant populations of the amphipod Gammarus duebeni had 50% mortality in 14 days at 1.0 mg Zn/L and 10 ppt salinity and 33% dead in 14 days at 1.0 mg/L and 30 ppt salinity versus nonresistant populations showing reduced survival at more than 0.1 mg Zn/L in 7 days, and 100% mortality in 7 days at 10 ppt salinity and 84% dead in 7 days at 1.0 mg/l and 30 ppt salinity (Johnson and Jones, 1989). Chemical species of zinc need to be considered in risk assessment. In seawater at pH 8.1, the dominant species of soluble zinc are zinc hydroxide (62.0%), free ion (17.0%), monochloride ion (6.4%), and zinc carbonate (5.8%) (USEPA, 1987b). In estuaries, the relative abundance of zinc species changes with increasing salinity. At low salinities, ZnSO4 and ZnCl+ predominate; at higher salinities, the highly toxic zinc aquo ion [(Zn(H2O)6)2+] predominates (Spear, 1981). But as salinity decreases, the concentration of free zinc ion increases and the concentration of zinc-chloro complexes decreases, resulting in increased bioavailability of the free metal ion and increased bioconcentration by resident organisms (Nugegoda and Rainbow, 1989b). The biocidal properties of zinc, and presumably accumulation rates, were more pronounced for crustacean adults than for other groups of adult invertebrates tested (Eisler, 1981; Eisler and Hennekey, 1977). In general, toxicity was greatest to larvae (Ahsanullah and Arnott, 1978; Brown and Ahsanullah, 1971; Eisler, 1980; Kobayashi, 1979) at elevated temperatures (McLusky and Hagerman, 1987; Spear, 1981; Sprague, 1986) during extended exposures (USEPA, 1980e, 1987a), under conditions of starvation (USNAS, 1989; Verriopoulos and Moraitu-Apostolopoulu, 1989), at salinity extremes above and below the isosmotic point (McLusky and Hagerman, 1987), in summer (Eisler, 1980), in proximity to anthropogenic discharges (Eisler, 2000h), and at low-sediment particulate loadings (Memmert, 1987). Zinc was fatal to sensitive crustaceans under the following conditions: at 0.01 mg/L to the copepod, Tisbe holothuriae in the fourth generation of exposure (Verriopoulos and Hardouvelis, 1988); at 0.07 mg/L to T. holothuriae in a single generation (Verriopoulos and Hardouvelis, 1988); at 0.001-0.09 mg/L to hermit crab in a dose-dependent manner (delayed mortality) (Ajmalkhan et al., 1986); at <0.10 mg/L to embryos of the horseshoe crab, L. polyphemus (an arachnoid, not a true crustacean) (Botton et al., 1998); at 0.10 mg/L to larvae of the hermit crab, Clibanarius olivaceous (Ajmalkhan et al., 1986); at 0.130.38 mg Zn/L to larvae of the American lobster, H. americanus (Spear, 1981; USEPA, 1987a); at 0.2 mg/L to adults of a hermit crab, P. longicarpus (Eisler and Hennekey, 1977); and at 0.294 mg/L to a copepod, A. tonsa (USEPA, 1987a). Among amphipods, juveniles were more sensitive to zinc than were adults, and epibenthic species were more sensitive than infaunal tube-dwelling species (King et al., 2006). At 5 ppt salinity, zinc was more toxic
Crustaceans 493 to juveniles of the euryhaline crab C. granulatus, as judged by LC50 (96 h) values (7.1 mg Zn/L) than at 25 ppt salinity (11.4 mg/L) (Beltrame et al., 2008). Acute toxicity bioassays of 96-h duration with adults of T. japonicus copepods—a relatively resistant species that is proposed for routine use in ecotoxicity testing in the western Pacific—showed that all survived 2.5 mg Zn/L, 10% died at 4.7 mg/L, and 50% died at 7.8 mg Zn/L (Lee et al., 2007). Adverse sublethal effects of zinc insult to crustaceans include gill histopathology (Patel and Kaliwal, 1989); increased tissue total proteins, decreased glycogen, and decreased acid phosphatase activity in the crab Portunus pelagicus (Hilmy et al., 1988); retardation of limb regeneration of fiddler crab, U. pugilator (Weis, 1980); altered enzyme activity in the green crab, C. maenas (Elumalai et al., 2007); and elevated tissue residues in American lobster, H. americanus (Waiwood et al., 1987). For example, tissue zinc concentrations in H. americanus exposed for 4 days to 25.0 mg Zn/L were especially high in gill (2570.0 mg Zn/kg DW versus 126.0 at start), hepatopancreas (734.0 versus 135.0), and green gland (1032.0 versus 148.0) (Waiwood et al., 1987). After 7 days in uncontaminated seawater, tissue zinc residues remained elevated in gill (675.0 mg Zn/kg DW), hepatopancreas (603.0), green gland (286.0), and other tissues (Waiwood et al., 1987). Zinc concentrations in crustacean soft tissues usually range between 50.0 and 208.0 mg/kg DW, and exceed soft tissue zinc enzymatic requirements by factors of 1.4-6.0 (Depledge, 1989). Metabolic derangement is also associated with zinc insult. Thus, amylase and trypsin activities were disrupted in A. salina during immersion in sublethal concentrations of zinc. Trypsin activity was disturbed within 24 h by 5.0 mg Zn/L; amylase activity was significantly different from controls after 72 h in 5.0 mg Zn/L (Alayse-Danet et al., 1979). However, at very low sublethal zinc concentrations P. montagui, a coldwater shrimp, showed no significant accumulations during exposure to 0.065 mg Zn/L solutions for 14 days (Ray et al., 1980), although zinc concentrations increased in eggs and hepatopancreas during the first 6 days of depuration (Ray et al., 1980). Seasonal fluctuations in zinc body burdens of copepods, barnacles, and decapod crustaceans are documented. Summer maxima in Acartia were associated with termination of active vertical transport (Pearcy and Osterberg, 1967; Zafiropoulos and Grimanis, 1977), and proximity to anthropogenic discharges (Pearcy and Osterberg, 1967). In barnacles, B. balanoides, and some decapods, seasonal variations in zinc content were correlated with river flow rates, tidal flow, and primary productivity (Bender, 1975; Ireland, 1974; Tennant and Forster, 1969). Among euphausiids, there were no seasonal variations in zinc content from collections made at 550 m; however, some variation was evident among conspecifics at 150-500 m depth (Pearcy and Osterberg, 1967). Zinc content of euphausiids and pelagic shrimp was inversely correlated with body weight. Depending on species, zinc concentrations of smaller individuals were 1.2-4.1 times greater than larger conspecifics (Fowler, 1974). A similar pattern was observed in Orchestoidea sp.
494 Chapter 7 (Bender, 1975). Other factors known to impact uptake, retention, and translocation of zinc by crustaceans include water temperature (Cross et al., 1969; Fowler et al., 1971; Jones, 1975; McKenney and Neff, 1979), salinity (Jones, 1975; McKenney and Neff, 1979), sediment composition, diet, and general health of the organism (Cross et al., 1969). Zinc interacts with salts of cadmium, copper, zinc, nickel, and chromium, but results were not always predictable. Waterborne solutions of zinc-cadmium mixtures were usually additive in toxicity to copepods (Verriopoulos and Dimas, 1988) and amphipods (Ahsanullah et al., 1988). Zinc counteracted adverse effects of cadmium on limb regeneration and growth of the fiddler crab U. pugilator (Weis, 1980). Zinc concentrations in larvae of shrimp Palaemon serratus, within its threshold regulation range of 0.075-0.525 mg Zn/L, were not affected by the addition of 0.1 mg Cd/L (Devineau and Amiard Triquet, 1985). Zinc-copper mixtures are more than additive in toxicity to marine copepods (Sunda et al., 1990; Verriopoulos and Dimas, 1988); however, zinc-copper mixtures were less than additive in toxicity to the marine amphipod A. compressa (Ahsanullah et al., 1988). Zinc added to seawater depressed copper accumulations in barnacles E. modestus; however, simultaneous exposure to copper and zinc resulted in enhanced uptake of both metals (Elliott et al., 1985). Antifouling paints containing mixtures of zinc pyrithione and copper (as a replacement for tributyltin) were more than additive in toxicity to amphipods, Elasmopus rapax, during 96-h tests, and this should be considered when developing zinc water quality criteria (Bao et al., 2008). Lead-zinc mixtures were more than additive in toxicity to copepods (Verriopoulos and Dimas, 1988) and significantly delayed larval development of mud crab, Rithropanopeus harrissii (USEPA, 1987a). Nickel-zinc mixtures were additive in toxicity to marine copepods (Verriopoulos and Dimas, 1988). Chromium-zinc mixtures were more than additive in toxicity to T. holothuriae, a marine copepod. Zinc in combination with chromium was more toxic to copepods than were mixtures of zinc with copper, lead, nickel, or cadmium (Verriopoulos and Dimas, 1988). Zinc exchange with the environment is reportedly slow. Zinc pools within adult aquatic organisms exchange only slowly, if at all, with zinc atoms in the organism’s food or surrounding water (Renfro et al., 1975), although not all investigators agree. For example, among euphausiids, there is a major loss of 65Zn due to isotopic exchange with seawater, with 96% of the radiozinc body burden eliminated over a period of 5 months (Fowler et al., 1971). In any event, diet is considered more important than the medium as a pathway for zinc accumulation among decapod crustaceans (Bender, 1975; Renfro et al., 1975). Among shrimp, P. serratus, different zinc excretion rates occur depending on the size of the animal. In general, ionic zinc is excreted first and then zinc complexes (Small et al., 1974). There is also the possibility that ionic particulate zinc and dissolved organic compounds may be excreted separately with subsequent combination in water to yield zinc complexes (Small et al., 1974). Surface-adsorbed zinc is turned over faster than internally adsorbed zinc in the dungeness crab, C. magister (Tennant and Forster, 1969). Zooplankters, including
Crustaceans 495 copepods and euphausiids, all eliminate accumulated zinc—presumably surface-adsorbed zinc—at rates of 1-5%/h (Kuenzler, 1969). In the well-studied euphausiid, M. norvegica, about half the whole-body zinc content is shed through molting when accumulated through the medium, but only 33% when accumulated by grazing on brine shrimp, A. salina (Fowler et al., 1971, 1972); molts constitute an important vehicle of zinc transfer into marine ecosystems (Fowler, 1977; Fowler et al., 1972). Finally, the participatory turnover time (i.e., the time required to cycle an element in a system through a given material in that system) for ionic zinc in the Ligurian Sea by adult euphausiids is lengthy. This interval is estimated at 498-1234 years depending upon available food and considering food chain as the only route of zinc accumulation (Small and Fowler, 1973). Fecal pellet deposition represented over 90% of zinc flux in this model (Fowler, 1977; Small et al., 1973). In general, molting results in a 33-50% loss of total zinc in marine crustaceans; molts, together with fecal pellets, constitute an important vehicle of zinc transfer in marine ecosystems (Eisler, 1981). For marine life protection, the United States Environmental Protection Agency recommends that total recoverable zinc in seawater should average less than 0.058 mg/L and never exceed 0.17 mg/L; for acid-soluble zinc, these values are less than 0.086 and 0.095 mg/L, respectively (USEPA, 1980e, 1987a). Most crustaceans can tolerate up to 0.23 mg Zn/L without adverse effects (Sprague, 1986); however, as shown earlier, adverse effects occur at 0.01 mg Zn/L (Verriopoulos and Hardouvelis, 1988). Zinc is important in pH regulation of sperm of the horseshoe crab; zinc reduction to <0.0065 mg/L in semen adversely affected sperm pH and motility (Clapper et al., 1985a,b). To protect against zinc deficiency, whole crustaceans should contain at least 34.5 mg Zn/kg DW (White and Rainbow, 1985) and the medium should contain at least 0.0065 mg Zn/L (Clapper et al., 1985a,b). Zinc deficiency in natural aquatic ecosystems, however, has not yet been credibly documented.
7.60 Zirconium Planktonic copepods from the Black Sea reportedly contain 70.0 mg Zr/kg AW (Vinogradova and Koual’skiy, 1962). Whole shrimp, Crangon sp., had 0.0096 mg Zr/kg DW (Zumholz et al., 2006).
7.61 Literature Cited Aarkrog, A., 1971. Radioecological investigations of plutonium in an arctic marine environment. Health Phys. 20, 31–47. Aarkrog, A., 1990. Environmental radiation and radiation releases. Int. J. Radiat. Biol. 57, 619–631. Abbott, O.J., 1977. The toxicity of ammonium molybdate to marine invertebrates. Mar. Pollut. Bull. 8, 204–205. Ahsanullah, M., 1982. Acute toxicity of chromium, mercury, molybdenum and nickel to the amphipod Allorchestes compressa. Aust. J. Mar. Freshw. Res. 33, 465–474. Ahsanullah, M., Arnott, G.H., 1978. Acute toxicity of copper, cadmium, and zinc to larvae of the crab Paragrapsus quadridentatus (H. Milne Edwards), and implications for water quality criteria. Aust. J. Mar. Freshw. Res. 29, 1–8.
496 Chapter 7 Ahsanullah, M., Williams, A.R., 1991. Sublethal effects and bioaccumulation of cadmium, chromium, copper and zinc in the marine amphipod Allorchestes compressa. Mar. Biol. 108, 59–65. Ahsanullah, M., Mobley, M.C., Rankin, P., 1988. Individual and combined effects of zinc, cadmium and copper on the marine amphipod Allorchestes compressa. Aust. J. Mar. Freshw. Res. 39, 33–37. Ajmalkhan, S., Rajendran, K., Natarajan, R., 1986. Effect of zinc on zoeal development of the estuarine hermit crab Clibanarius olivaceus (Henderson). Proc. Indian Acad. Sci. 95, 515–524. Alayse-Danet, A.M., Charlou, J.L., Jezequel, M., Samain, J.F., 1979. Modele de detection rapide des effets subletaux des pollutants: Modification faux d’amylase et de trypsine d’Artemia salina contaminees par le cuivre ou le zinc. Mar. Biol. 51, 41–46. Alliot, A., Frenet-Piron, M., 1990. Relationship between metals in sea-water and metal accumulation in shrimps. Mar. Pollut. Bull. 21, 30–33. Alquezar, R., Markich, S.J., Twining, J.R., 2007. Uptake and loss of dissolved 109Cd and 75Se in estuarine macroinvertebrates. Chemosphere 67, 1201–1210. Amiard-Triquet, C., Amiard, J.C., 1974. Contamination de chaines trophiques par le cobalt 60. Rev. Int. Oceanogr. Med. 33, 49–59. Amiard-Triquet, C., Amiard, J.D., 1975. Etude experimentale du transfert du cobalt 60 dans une chaine trophique marine benthique. Helg. Wiss. Meeres. 27, 283–297. Amiard-Triquet, C., Amiard, J.C., 1976. L’organotropisme du 60Co chez Scrobicularia plana et Carcinus maenas en fonction du vecteur de contamination. Oikos 27, 122–126. Ancellin, J., Bovard, P., Vilquin, A., 1967. New studies on experimental contamination of marine species by ruthenium-106. In: Actes du Congres Int. sur la Radioprotection du Milieu Soc. Franc. de Radioprot, Toulouse, France, January 14-16, 1967, pp. 213–234. Anderson, E.P., Mackas, D.L., 1986. Lethal and sublethal effects of a molybdenum mine tailing on marine zooplankton: Mortality, respiration, feeding and swimming behavior in Calanus marshallae, Metridia pacifica and Euphausia pacifica. Mar. Environ. Res. 19, 131–155. Anil, A.C., Wagh, A.B., 1988. Accumulation of copper and zinc by Balanus amphitrite in a tropical estuary. Mar. Pollut. Bull. 19, 177–180. Anonymous, 1978. Selected pollution profiles: North Atlantic, North Sea, Baltic Sea, and Mediterranean Sea. Ambio 7, 75–78. Antonini-Kane, J., Fowler, S.W., Heyraud, M., Keckes, S., Small, L.F., Beglia, A., 1972. Accumulation and loss of radionuclides by Meganyctiphanes norvegica M. Sars. Rapp. Comm. Int. Mer Medit. 21, 289–290. Aono, A., Takeuchi, I., 2008. Effects of tributyltin at concentrations below ambient levels in seawater on Caprella danilevskii (crustacea: amphipoda: caprellidae). Mar. Pollut. Bull. 57, 515–523. Argese, E., Bettiol, C., Ghirardini, A.V., Fasolo, M., Giurin, G., Ghetti, P.F., 1998. Comparison of in vitro submitochondrial particle and Microtox assays for determining the toxicity of organotin compounds. Environ. Toxicol. Chem. 17, 1005–1012. Bao, V.W.W., Leung, K.M.Y., Kwok, K.W.H., Zhang, A.Q., Lui, G.C.S., 2008. Synergistic toxic effects of zinc pyrithione and copper to three marine species: Implications on setting appropriate water quality criteria. Mar. Pollut. Bull. 57, 616–623. Barbaro, A., Francescon, A., Polo, B., Bilio, M., 1978. Balanus amphitrite (Cirripedia: Thoracica): A potential indicator of fluoride, copper, lead, chromium, and mercury in North Atlantic lagoons. Mar. Biol. 46, 247–257. Barka, S., 2007. Insoluble detoxification of trace metals in a marine copepod Tigriopus brevicornis (Muller) exposed to copper, zinc, nickel, cadmium, silver and mercury. Ecotoxicology 16, 491–502. Barnes, H., Stanbury, F.A., 1948. The toxic action of copper and mercury salts both separately and when mixed on the harpacticoid copepod, Nitroca spinipes (Boeck). J. Exp. Biol. 25, 270–275. Beasley, T.M., Held, E.E., 1971. Silver-108m in biota and sediments at Bikini and Eniwetok Atolls. Nature 230 (5294), 450–451. Bechmann, R.K., 1994. Use of life tables and LC50 tests to evaluate chronic and acute toxicity effects of copper on the marine amphipod Tisbe furcata (Baird). Environ. Toxicol. Chem. 13, 1509–1517.
Crustaceans 497 Beltrame, M.O., De Marco, S.G., Marcovecchio, J.E., 2008. Cadmium and zinc in Mar Chiquita coastal lagoon (Argentina): Salinity effects on lethal toxicity in juveniles of the burrowing crab Chasmagnathus granulatus. Arch. Environ. Contam. Toxicol. 55, 78–85. Benayoun, G., Fowler, S.W., Oregioni, B., 1975. Flux of cadmium through euphausiids. Mar. Biol. 27, 205–212. Bender, J.A., 1975. Trace metal levels in beach dipterans and amphipods. Bull. Environ. Contam. Toxicol. 14, 187–192. Bengtsson, B.E., 1977. Accumulation of cadmium in some aquatic animals from the Baltic Sea. Ambio Spec. Rep. 5, 69–73. Benijts-Claus, C., Benijts, F., 1975. The effect of low lead and zinc concentrations on the larval development of the mudcrab, Rithropanopeus harrisii Gould. In: Koeman, J.H., Strik, J.J.T.W.A. (Eds.), Sublethal Effects of Toxic Chemicals on Aquatic Animals. Elsevier, Amsterdam, pp. 43–52. Bergey, L.L., Weis, J.S., 2007. Molting as a mechanism of depuration of metals in the fiddler crab, Uca pugnax. Mar. Environ. Res. 64, 556–562. Bernard, F.J., Lane, C.E., 1961. Absorption and excretion of copper ion during settlement and metamorphosis of the barnacle, Balanus amphitrite nireus. Biol. Bull. 121, 438–448. Bernard, F.J., Lane, C.E., 1963. Effects of copper ion in oxygen uptake to planktonic cyprids of the barnacle, Balanus amphitrite nireus. Proc. Soc. Exp. Biol. Med. 113, 418–420. Bernhard, M., Zattera, A., 1975. Major pollutants in the marine environment. In: Pearson, E.A., Frangipane, E.D. (Eds.), Marine Pollution and Marine Waste Disposal. Pergamon, Elmsford, NY, pp. 195–300. Berry, W.J., Cantwell, M.G., Edwards, P.A., Serbst, J.R., Hansen, D.J., 1999. Predicting toxicity of sediments spiked with silver. Environ. Toxicol. Chem. 18, 40–48. Bertine, K.K., Goldberg, E.D., 1972. Trace elements in clams, mussels, and shrimp. Limnol. Oceanol. 17, 877–884. Bianchini, A., Playle, R.C., Wood, C.M., Walsh, P.J., 2007. Short-term silver accumulation in tissues of three marine invertebrates: Shrimp Penaeus duorarum, sea hare Aplysia californica, and sea urchin Diadema antillarum. Aquat. Toxicol. 84, 182–189. Bielmyer, G.K., Grosell, M., Brix, K.V., 2006. Toxicity of silver, zinc, copper, and nickel to the copepod Acartia tonsa exposed via a phytoplankton diet. Environ. Sci. Technol. 40, 2063–2068. Bjerragaard, P., 1982. Accumulation of cadmium and selenium and their mutual interaction in the shore crab Carcinus maenus (L.). Aquat. Toxicol. 2, 113–125. Bloom, H., Ayling, G.M., 1977. Heavy metals in the Derwent Estuary. Environ. Geol. 2, 3–22. Blunden, S.J., Chapman, A.H., 1982. The environmental degradation of organotin compounds: A review. Environ. Technol. Lett. 3, 267–272. Blunden, S.J., Chapman, A.H., 1986. Organotin compounds in the environment. In: Craig, P.J. (Ed.), Organometallic Compounds in the Environment. Longman Group, London, pp. 111–159. Blunden, S.J., Cusack, P.A., Hill, R., 1985. The Industrial Uses of Tin Chemicals. Royal Society of Chemistry, London, 337 pp. Blust, R., Fontaine, A., Decleir, W., 1991. Effect of hydrogen ion and inorganic complexing on the uptake of copper by the brine shrimp Artemia franciscana. Mar. Ecol. Prog. Ser. 76, 273–282. Bohn, A., 1975. Arsenic in marine organisms from West Greenland. Mar. Pollut. Bull. 6, 87–89. Bohn, A., McElroy, R.O., 1976. Trace metals (As, Cd, Cu, Fe, and Zn) in Arctic cod, Boreogadus saida, and selected zooplankton from Strathcona Sound, Northern Baffin Island. J. Fish. Res. Board Can. 33, 2836–2840. Boney, A.D., Corner, E.D.S., Sparrow, B.W.P., 1959. The effects of various poisons on the growth and viability of sporelings of the red alga Plumaria elegans (Bonnem.). Biochem. Pharmacol. 2, 37–49. Boon, D.D., 1973. Iron, zinc, magnesium, and copper concentrations in body meat of the blue crab, Callinectes sapidus. Chesapeake Sci. 14, 143–144. Boothe, P.N., Knauer, G.A., 1972. The possible importance of fecal material in the biological amplification of trace and heavy metals. Limnol. Oceanol. 17, 270–274. Botton, M.L., Johnson, K., Helleby, L., 1998. Effects of copper and zinc on embryos and larvae of the horseshoe crab, Limulus polyphemus. Arch. Environ. Contam. Toxicol. 35, 25–32.
498 Chapter 7 Brown, B., Ahsanullah, M., 1971. Effects of heavy metals on mortality and growth. Mar. Pollut. Bull. 2, 182–187. Bryan, G.W., 1961. The accumulation of radioactive caesium in crabs. J. Mar. Biol. Assoc. UK 41, 551–575. Bryan, G.W., 1963. The accumulation of 137Cs by brackish water invertebrates and its relation to the regulation of potassium and sodium. J. Mar. Biol. Assoc. UK 43, 541–565. Bryan, G.W., 1964. Zinc regulation in the lobster Homarus americanus. I. Tissue zinc and copper concentrations. J. Mar. Biol. Assoc. UK 44, 549–563. Bryan, G.W., 1965. Ionic regulation in the squat lobster Galathea squamifera, with special reference to the relationship between potassium metabolism and the accumulation of radioactive caesium. J. Mar. Biol. Assoc. UK 45, 97–113. Bryan, G.W., 1966. The metabolism of Zn and 65Zn in crabs, lobsters and freshwater crayfish. In: Radioecological Concentration Processes. Pergamon, Elmsford, NY, pp. 1005–1016. Bryan, G.W., 1967. Zinc concentrations of fast and slow contracting muscles in the lobster. Nature 213, 1043–1044. Bryan, G.W., 1968. Concentrations of zinc and copper in the tissues of decapod crustaceans. J. Mar. Biol. Assoc. UK 48, 303–321. Bryan, G.W., Ward, E., 1965. The absorption and loss of radioactive and non-radioactive manganese by the lobster, Homarus vulgaris. J. Mar. Biol. Assoc. UK 45, 65–95. Bryan, G.W., Hummerstone, L.W., Ward, E., 1986. Zinc regulation in the lobster Homarus gammarus: Importance of different pathways and excretion. J. Mar. Biol. Assoc. UK. 66, 175–199. Bryant, V., Newbery, D.M., McLuskey, D.S., Campbell, R., 1985. Effect of temperature and salinity on the toxicity of arsenic to three estuarine invertebrates (Corophium volutator, Macoma balthica, Tubifex costatus). Mar. Ecol. Prog. Ser. 24, 129–137. Burger, J., Cooper, K., Saliva, J., Gochfeld, D., Lipsky, D., Gochfeld, M., 1992. Mercury bioaccumulation in organisms from three Puerto Rican estuaries. Environ. Monit. Assess. 22, 181–197. Burger, J., Stern, A.H., Gochfeld, M., 2005. Mercury in commercial fish: Optimizing individual choices to reduce risk. Environ. Health Perspect. 113, 266–270. Burger, J., Fossi, C., McClellan-Green, P., Orlando, E.F., 2007a. Methodologies, bioindicators, and biomarkers for assessing gender-related differences in wildlife exposed to environmental chemicals. Environ. Res. 104, 135–152. Burger, J., Gochfeld, M., Jeitner, C., Burke, S., Stamm, T., Snigaroff, R., et al., 2007b. Mercury levels and potential risk from subsistence foods from the Aleutians. Sci. Total Environ. 384, 93–105. Canli, M., Furness, R.W., 1993. Toxicity of heavy metals dissolved in sea water and influences of sex and size on metal accumulation and tissue distribution in the Norway lobster Nephrops norvegicus. Mar. Environ. Res. 36, 217–236. Cappon, C.J., Smith, J.C., 1982. Chemical form and distribution of selenium in edible seafood. J. Anal. Toxicol. 6, 10–21. Cardwell, R.D., Sheldon, A.W., 1986. A risk assessment concerning the fate and effects of tributyltins in the aquatic environment. In: Maton, G.L. (Ed.), Proceedings Oceans 86 Conference, Washington, DC, September 23-25, 1986, vol. 4, Organotin Symposium. Available from Marine Technology Society, 2000 Florida Avenue, New York, Washington, DC, pp. 1117–1129. Carr, R.S., McCullough, W.L., Neff, J.M., 1982. Bioavailability of chromium from a used chrome lignosulphonate drilling mud to five species of marine invertebrates. Mar. Environ. Res. 6, 189–203. Chakravarti, D., Eisler, R., 1961. Strontium-90 and gross beta activity in the fat and nonfat fractions of the liver of the coconut crab (Birgus latro) collected at Rongelap Atoll during March 1958. Pacific Sci. 15, 155–159. Champ, M.A., 1986. Organotin symposium: Introduction and review. In: Maton, G.L. (Ed.), Proceedings Oceans 86 Conference, Washingon, DC, September 23-25, 1986, vol. 4, Organotin Symposium. Available from Marine Technology Society, 2000 Florida Avenue, New York, Washington, DC, pp. 1093–1100. Chau, Y.K., Maguire, R.J., Wong, P.T.S., Glen, B.A., Bengert, G.A., Tkacz, R.J., 1984. Occurrence of methyltin and butyltin species in environmental samples in Ontario. Natl. Water Res. Inst., Rep. 8401. Available from Department of Environment, Canada Centre for Inland Waters, Burlington, Ontario, Canada L7R 4A6, pp. 1–25.
Crustaceans 499 Cheevaparanapivat, V., Menasveta, P., 1979. Total and organic mercury in marine fish of the upper Gulf of Thailand. Bull. Environ. Contam. Toxicol. 23, 291–299. Chou, C.L., Uthe, J.F., Zook, E.G., 1978. Polarographic studies on the nature of cadmium in scallop, oyster, and lobster. J. Fish. Res. Board Can. 35, 409–413. Clapper, D.L., Davis, J.A., Lamothe, P.J., Patton, C., Epel, D., 1985a. Involvement of zinc in the regulation of ph, motility, and acrosome reactions in sea urchin sperm. J. Cell Biol. 100, 1817–1824. Clapper, D.L., Lamothe, P.J., Davis, J.A., Epel, D., 1985b. Sperm motility in the horseshoe crab. V: Zinc removal mediates chelator initiation of motility. J. Exp. Zool. 236, 83–91. Clark, J.R., Patrick Jr., J.M., Moore, J.C., Lores, E.M., 1987. Waterborne and sediment-source toxicities of six organic chemicals to grass shrimp (Palaemonetes pugio) and amphioxus (Branchiostoma caribaeum). Arch. Environ. Contam. Toxicol. 16, 401–407. Clason, B., Duquesne, S., Liess, M., Schulz, R., Zauke, G.P., 2003. Bioaccumulation of trace metals in the Antarctic amphipod Paramoera walkeri (Stebbing 1906): Comparison of two-compartment and hyperbolic toxicokinetic models. Aquat. Toxicol. 65, 117–140. Coelho, J.P., Reis, A.T., Ventura, S., Pereira, M.E., Duarte, A.C., Pardal, M.A., 2008. Pattern and pathways for mercury lifespan bioaccumulation in Carcinus maenas. Mar. Pollut. Bull. 56, 1104–1110. Colaco, A., Bustamante, P., Fouquet, Y., Sarradin, P.M., Serrao-Santos, R., 2006. Bioaccumulation of Hg, Cu, and Zn in the Azores triple junction hydrothermal vent fields food web. Chemosphere 65, 2260–2267. Conklin, P.J., Drysdale, D., Doughti, D.G., Rao, K.R., Kakareka, J.P., Gilbert, T.R., et al., 1983. Comparative toxicity of drilling muds: Role of chromium and petroleum hydrocarbons. Mar. Environ. Res. 10, 105–125. Connell, D.B., Sanders, J.G., Riedel, G.F., Abbe, G.R., 1991. Pathways of silver uptake and trophic transfer in estuarine organisms. Environ. Sci. Technol. 25, 921–924. Corner, E.D.S., 1959. The poisoning of Maia squinado (Herbst) by certain compounds of mercury. Biochem. Pharmacol. 2, 121–132. Corner, E.D.S., Rigler, F.H., 1958. The modes of action of toxic agents. III. Mercuric chloride and n-amylmercuric chloride on crustaceans. J. Mar. Biol. Assoc. UK 37, 85–96. Correa, J.D., da Silva, M.R., da Silva, A.C.B., de Lima, S.M.A., Malm, O., Allodi, S., 2005. Tissue distribution, subcellular localization and endocrine disruption patterns induced by Cr and Mn in the crab Ucides cordatus. Aquat. Toxicol. 73, 139–154. Correia, A.D., Costa, M.H., Ryan, K.P., Nott, J.A., 2002. Studies on biomarkers of copper exposure and toxicity in the marine amphipod Gammarus locusta (Crustacea): I. Copper-containing granules within the midgut gland. J. Mar. Biol. Assoc. UK 82, 827–834. Costa, L.G., 1985. Inhibition of gamma: [3H] aminobutyric acid uptake by organotin compounds in vitro. Toxicol. Appl. Pharmacol. 79, 471–479. Costa, M.R.M., da Fonseca, M.I.C., 1967. Tero de arsenico en mariscos. Rev. Port. Farm. 17 (1), 1–19. Cross, F.A., Dean, J.M., Osterberg, C.L., 1969. The effect of temperature, sediment, and feeding on the behavior of four radionuclides in a marine benthic amphipod. In: Proceedings of the Second National Symposium on Radioecology. U.S. Atomic Energy Commission, Conf. 67053, pp. 450–461. Culkin, F., Riley, J.P., 1958. The occurrence of gallium in marine organisms. J. Mar. Biol. Assoc. UK 37, 607–615. Cumont, G., Gilles, G., Bernard, F., Briand, M.B., Stephan, G., Ramonda, G., et al., 1975. Bilan de la contamination des poissons de mer par le mercure a l’occasion d’un controle portant sur 3 annees. Ann. Hyg. L. Fr. Med. et Nut. 11 (1), 17–25. Custer, T.W., Mitchell, C.A., 1993. Trace elements and organochlorines in the shoalgrass community of the lower Laguna Madre, Texas. Environ. Monit. Assess. 25, 235–246. Cutshall, N.H., Naidu, J.R., Pearcy, W.G., 1977. Zinc and cadmium in the Pacific hake, Merluccius productus off the western U.S. coast. Mar. Biol. 44, 195–202. D’Adamo, R., Di Stasio, M., Fabbrocini, A., Petitto, F., Roselli, L., Volpe, M.G., 2008. Migratory crustaceans as biomonitors of metal pollution in their nursery areas. The Lesina lagoon (SE Italy) as a case study. Environ. Monit. Assess. 143, 15–24.
500 Chapter 7 D’Agostino, A., Finney, C., 1974. The effect of copper and cadmium on the development of Tigriopus japonicus. In: Vernberg, F.J., Vernberg, W.B. (Eds.), Pollution and Physiology of Marine Organisms. Academic Press, New York, pp. 445–463. Dahab, O.A., Khalil, A.N., Halim, Y., 1990. Chromium fluxes through Mex Bay inshore waters. Mar. Pollut. Bull. 21, 68–73. Davies, A.G., Smith, P.J., 1982. Tin. In: Wilkinson, G. (Ed.), Comprehensive Organometallic Chemistry. Pergamon, New York, pp. 519–627. DeClerck, R., Vanderstappen, R., Vyncke, W., 1974. Mercury content of fish and shrimps caught off the Belgian coast. Ocean Manage. 2, 117–126. DeClerck, R., Vanderstappen, R., Vyncke, W., Van Hoeyweghen, P., 1979. La teneur en metaux lourds dans les organismes marins provenant de la capture accessoire de la peche coteiere belge. Rev. de l’Agric. 3 (32), 793–801. De Gieter, M., Leermakers, M., Van Ryssen, R., Noyen, J., Goeyens, L., Baeyens, W., 2002. Total and toxic arsenic levels in North Sea fish. Arch. Environ. Contam. Toxicol. 43, 406–417. Denton, G.R.W., Concepcion, L.C., Wood, H.R., Morrison, R.J., 2006. Trace metals in marine organisms from four harbours in Guam. Mar. Pollut. Bull. 52, 1784–1804. Depledge, M.H., 1989. Re-evaluation of metabolic requirements for copper and zinc in decapod crustaceans. Mar. Environ. Res. 27, 115–126. Depledge, M.H., Forbes, T.L., Forkes, V.E., 1993. Evaluation of cadmium, copper, zinc, and iron concentrations and tissue distributions in the benthic crab, Dorippe granulata (De Haan, 1841) from Tolo Harbour, Hong Kong. Environ. Pollut. 81, 15–19. Devescovi, M., Lucu, C., 1995. Seasonal changes of the copper level in shore crabs Carcinus mediterraneus. Mar. Ecol. Prog. Ser. 120, 169–174. Devi, V.U., 1987. Heavy metal toxicity to fiddler crabs, Uca annulipes Latreille and Uca triangularis (Milne Edwards): Tolerance to copper, mercury, cadmium, and zinc. Bull. Environ. Contam. Toxicol. 39, 1010–1027. Devi, V.U., Rao, Y.P., 1989a. Heavy metal toxicity to fiddler crabs, Uca annulipes Latreille and Uca triangularis (Milne Edwards): Respiration on exposure to copper, mercury, cadmium, and zinc. Bull. Environ. Contam. Toxicol. 43, 165–172. Devi, V.U., Rao, Y.P., 1989b. Zinc accumulation in fiddler crabs Uca annulipes Latreille and Uca triangularis (Milne Edwards). Ecotoxicol. Environ. Safety 18, 129–140. Devineau, J., Amiard Triquet, C., 1985. Patterns of bioaccumulation of an essential trace element (zinc) and a pollutant metal (cadmium) in larvae of the prawn Palaemon serratus. Mar. Biol. 86, 139–143. Dietz, R., Riget, F., Johansen, P., 1996. Lead, cadmium, mercury and selenium in Greenland marine animals. Sci. Total Environ. 186, 67–93. Doi, R., Ui, J., 1975. The distribution of mercury in fish and its form of occurrence. In: Krenkel, P.A. (Ed.), Heavy Metals in the Aquatic Environment. Pergamon Press, New York, pp. 197–221. Doughti, D.G., Conklin, P.J., Rao, K.R., 1983. Cuticular lesions induced in grass shrimp exposed to hexavalent chromium. J. Invert. Pathol. 42, 249–258. Drifmeyer, J.E., Odum, W.E., 1975. Lead, zinc and manganese in dredge-spoil pond ecosystems. Environ. Conserv. 2, 39–43. Duke, T.W., Baptist, J.P., Hoss, D.E., 1966. Bioaccumulation of radioactive gold used as a sediment tracer in the estuarine environment. US Fish Wildl. Serv. Fish. Bull. 65, 427–436. Duncan, J., 1980. The toxicology of molluscicides. The organotins. Pharmacol. Ther. 10, 407–429. Edmonds, J.S., Francesconi, K.A., Stick, R.V., 1993. Arsenic compounds from marine organisms. Nat. Prod. Rep. 10, 421–428. Eftekhari, M., 1975. Teneur en mercure de quelques crevettes du Golfe Persique. Science Peche. Bull. Inst. Peches Marit. 250, 9–10. Eganhouse, R.P., Young, D.R., 1978. Total and organic mercury in benthic organisms near a major submarine wastewater outfall system. Bull. Environ. Contam. Toxicol. 19, 758–766.
Crustaceans 501 Eisler, R., 1980. Accumulation of zinc by marine biota. In: Nriagu, J.O. (Ed.), Zinc in the Environment. Part II. Health Effects. John Wiley, New York, pp. 259–351. Eisler, R., 1981. Trace Metal Concentrations in Marine Organisms. Pergamon, Elmsford, New York, 687 pp. Eisler, R., 1995. Ecological and toxicological aspects of the partial meltdown of the Chernobyl nuclear plant reactor. In: Hoffman, D.J., Rattner, B.A., Burton Jr., G.A., Cairns Jr., A.J. (Eds.), Handbook of Ecotoxicology. Lewis Publishers, Boca Raton, FL, pp. 549–564. Eisler, R., 2000a. Arsenic. In: Handbook of Chemical Risk Assessment, vol. 3. Lewis Publishers, Boca Raton, FL, pp. 1501–1566. Eisler, R., 2000b. Boron. In: Handbook of Chemical Risk Assessment, vol. 3. Lewis Publishers, Boca Raton, FL, pp. 1567–1612. Eisler, R., 2000c. Selenium. In: Handbook of Chemical Risk Assessment, vol. 3. Lewis Publishers, Boca Raton, FL, pp. 1649–1705. Eisler, R., 2000d. Cadmium. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 1–44. Eisler, R., 2000e. Chromium. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 45–92. Eisler, R., 2000f. Copper. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 93–200. Eisler, R., 2000g. Tin. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 551–603. Eisler, R., 2000h. Zinc. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 605–714. Eisler, R., 2003. The Chernobyl nuclear power plant reactor accident: Ecotoxicological update. In: Hoffman, D.J., Rattner, B.A., Burton Jr., G.A., Cairns Jr., J. (Eds.), Handbook of Ecotoxicology, second ed. Lewis Publishers, Boca Raton, FL, pp. 703–736. Eisler, R., 2006. Mercury Hazards to Living Organisms. CRC Press, Boca, Raton, FL, 312 pp. Eisler, R., Hennekey, R.J., 1977. Acute toxicities of Cd2+, Cr+6, Hg2+, Ni2+, and Zn2+ to estuarine macrofauna. Arch. Environ. Contam. Toxicol. 6, 315–323. Eisler, R., Zaroogian, G., Hennekey, R.J., 1972. Cadmium uptake by marine organisms. J. Fish. Res. Board Can. 29, 1367–1369. Elferink, J.G.R., Deierkauf, M., Steveninck, J.V., 1986. Toxicity of organotin compounds for polymorphonuclear leukocytes. The effect on phagocytosis and exocytosis. Biochem. Pharmacol. 35, 3727–3732. Elliott, N.G., Ritz, D.A., Swain, R., 1985. Interaction between copper and zinc accumulation in the barnacle Elminius modestus Darwin. Mar. Environ. Res. 17, 13–17. Elumalai, M., Antunes, C., Guilhermino, L., 2007. Enzymatic biomarkers in the crab Carcinus maenas from the Minho River estuary (NW Portugal) exposed to zinc and mercury. Chemosphere 66, 1249–1255. Engel, D.W., 1987. Metal regulation, and molting in the blue crab, Callinectes sapidus: Copper, zinc, and metallothionein. Biol. Bull. 172, 69–82. Ericksson, S.P., Weeks, J.M., 1994. Effects of copper and hypoxia on two populations of the benthic amphipod, Corophium volutator (Pallas). Aquat. Toxicol. 29, 73–81. Erk, M., Muyssen, B.T.A., Ghekiere, A., Janssen, C.R., 2008. Metallothioneins and cytosolic metals in Neomysis integer exposed to cadmium at different salinities. Mar. Environ. Res. 65, 437–444. Establier, R., 1977. Estudio de la contaminacion marine por metals pesados y sus effectos biologicos. Inf. Tec. Inst. Invest. Pesq. 47, 1–36. Eustace, I.J., 1974. Zinc, cadmium, copper, and manganese in species of finfish and shellfish caught in the Derwent Estuary, Tasmania. Aust. J. Mar. Freshw. Res. 25, 209–220. Evans, D.W., Laughlin, R.B. Jr. 1984. Accumulation of bis(tributyltin) oxide by the mud crab. Rithropanopeus harrisii. Chemosphere 13, 213–219. Eversole, A.G., 1978. Marking clams with rubidium. Proc. Nat. Shellfish. Assoc. 68, 78.
502 Chapter 7 Fang, J., Wang, K.X., Tang, J.L., Wang, Y.M., Ren, S.J., Wu, H.Y., et al., 2004. Copper, lead, zinc, cadmium, mercury, and arsenic in marine products of commerce from Zhejiang coastal area, China, May, 1998. Bull. Environ. Contam. Toxicol. 73, 583–590. Feng, T.H., Hwang, J.S., Hsiao, S.H., Chen, H.Y., 2006. Trace metals in seawater and copepods in the ocean outfall area of the northern Taiwan coast. Mar. Environ. Res. 61, 224–243. Fleeger, J.W., Gust, K.A., Marlborough, S.J., Tita, G., 2007. Mixtures of metals and polynuclear aromatic hydrocarbons elicit complex nonadditive toxicological interactions in meiobenthic copepods. Environ. Toxicol. Chem. 26, 1677–1685. Fowler, 1974. The effect of organism size on the content of certain trace metals in marine zooplankton. Rapp. Comm. Int. Mer Medit. 22 (9), 145–146. Fowler, S.W., 1977. Trace elements in zooplankton particulate products. Nature 269, 51–53. Fowler, S.W., Benayoun, G., 1976a. Selenium kinetics in marine zooplankton. Mar. Sci. Comm. 2, 43–67. Fowler, S.W., Benayoun, G., 1976b. Influence of environmental factors on selenium flux in two marine invertebrates. Mar. Biol. 37, 59–68. Fowler, S.W., Benayoun, G., 1976c. Accumulation and distribution of selenium in mussel and shrimp tissues. Bull. Environ. Contam. Toxicol. 16, 339–346. Fowler, S.W., Unlu, M.Y., 1978. Factors affecting bioaccumulation and elimination of arsenic in the shrimp Lysmata seticaudata. Chemosphere 9, 711–720. Fowler, S.W., Small, L.F., Dean, J.M., 1971. Experimental studies on elimination of zinc-65, cesium-137, and cerium-144 by euphausiids. Mar. Biol. 8, 224–231. Fowler, S.W., Small, L.F., La Rosa, J., 1972. The role of euphausiid molts in the transport of radionuclides in the sea. Rapp. Comm. Int. Mer Medit. 21 (6), 291–292. Fowler, S.W., Heyraud, M., Small, L.F., Benayoun, G., 1973. Flux of 141Ce through euphausiid crustacean. Mar. Biol. 21, 317–325. Fowler, S.W., Heyraud, M., La Rosa, J., 1978. Factors affecting methyl and inorganic mercury dynamics in mussels and shrimp. Mar. Biol. 46, 267–276. Fowler, S.W., Buat-Menard, P., Yokoyama, Y., Ballestra, S., Holm, E., Van Nguyen, H., 1987. Rapid removal of Chernobyl fallout from Mediterranean surface waters by biological activity. Nature 329, 56–58. Francesconi, K.A., Micks, P., Stockton, R.A., Irgolic, K.J., 1985. Quantitative determination of arsenobetaine, the major water-soluble arsenical in three species of crab, using high pressure liquid chromatography and an inductively coupled argon plasma emission spectrometer as the arsenic-specific detector. Chemosphere 14, 1443–1453. Frias-Espericueta, M.G., Izaguirre-Fierro, G., Valenzuela-Quinonez, F., Osuna-Lopez, J.L., Voltolina, D., LopezLopez, G., et al., 2007. Metal content of California blue shrimp Litopenaeus stylirostris (Stimpson). Bull. Environ. Contam. Toxicol. 79, 214–217. Fujita, T., Yamamoto, T., Yamazi, I., Shigematsu, T., 1969. The contents of ash, iron and manganese in marine plankton. J. Chem. Soc. Jpn. 90, 680–686. Fukai, R., 1965. Analysis of trace amounts of chromium in marine organisms by the isotope dilution of Cr-51. In: Radiochemical Methods of Analysis. IAEA, Vienna, Austria, pp. 335–351. Fukai, R., Broquet, D., 1965. Distribution of chromium in marine organisms. Bull. Inst. Oceanol. 65 (1336), 1–19. Fukai, R., Meinke, W.W., 1959. Some activation analyses of six trace elements in marine biological ashes. Nature 184, 815–816. Fukai, R., Meinke, W.W., 1962. Activation analyses of vanadium, arsenic, molybdenum, tungsten, rhenium, and gold in marine organisms. Limnol. Oceanol. 7, 186–200. Fukai, R., Suzuki, H., Watankae, K., 1962. Strontium-90 in marine organisms during the period 1957-1961. Bull. Inst. Oceanogr. Monaco 1251, 1–16. Gardner, W.S., Windom, H.L., Stephens, J.A., Taylor, F.A., Stickney, R.R., 1975. Concentrations of total mercury in fish and other coastal organisms: Implications to mercury cycling. In: Howell, F.G., Gentry, J.B., Smith, M.H. (Eds.), Mineral Cycling in Southeastern Ecosystem, pp. 268–278. U.S. Ener. Res. Dev. Admin. CONF-740513.
Crustaceans 503 Gentile, S.M., Gentile, J.H., Walker, J., Heltshe, J.F., 1982. Chronic effects of cadmium on two species of mysid shrimp: Mysidopsis bahia and Mysidopsis bigelowi. Hydrobiologia 93, 195–204. Gibbs, P.E., Bryan, G.W., 1972. A study of strontium, magnesium, and calcium in the environment and exoskeleton of decapod crustaceans with special reference to Uca burgersi on Barbuda, West Indies. J. Exp. Mar. Biol. Ecol. 9, 97–110. Gibson, C.I., Thatcher, T.O., Apts, C.W., 1976. Some effects of temperature, chlorine, and copper on the survival and growth of the coon stripe shrimp. In: Esch, G.W., McFarlane, R.W. (Eds.), Thermal Ecology II, pp. 88–92 U.S. Ener. Res. Dev. Admin. CONF-750425. Glickstein, N., 1978. Acute toxicity of mercury and selenium to Crassostrea gigas embryos and Cancer magister larvae. Mar. Biol. 49, 113–117. Gordon, C.M., Carr, R.A., Larson, R.E., 1970. The influence of environmental factors on the sodium and manganese content of barnacle shells. Limnol. Oceanol. 15, 461–466. Gould, E., Greig, R.A., 1983. Short-term low-salinity response in lead-exposed lobsters, Homarus americanus (Milne Edwards). J. Exp. Mar. Biol. Ecol. 69, 283–295. Green Jr., F.A., Anderson, J.W., Petrocelli, S.R., Presley, B.J., Sims, R., 1976. Effect of mercury on the survival, respiration, and growth of postlarval white shrimp, Penaeus setiferus. Mar. Biol. 37, 75–81. Greig, R.A., 1975. Comparison of atomic absorption and neutron activation analyses for determination of silver, chromium, and zinc in various marine organisms. Anal. Chem. 47, 1682–1684. Greig, R., Wenzloff, D., 1977. Final report on heavy metals in small pelagic finfish, euphausiid crustaceans, and apex predators, including sharks, as well as on heavy metals and hydrocarbons (C15+) in sediments collected at stations in and near Deepwater Dumpsite 106, Vol. III, Contaminant inputs and chemical characteristics. In: Baseline Report of the Environmental Conditions in Deepwater Dumpsite 106. U.S. Department of Commerce, NOAA, pp. 547–564. Greig, R.A., Wenzloff, D., Shelpuk, C., 1975. Mercury concentrations in fish, North Atlantic offshore waters— 1971. Pestic. Monit. J. 9, 15–20. Greig, R.A., Adams, A., Wenzloff, D.R., 1977a. Trace metal content of plankton and zooplankton collected from the New York Bight and Long Island Sound. Bull. Environ. Contam. Toxicol. 18, 3–8. Greig, R.A., Wenzloff, D.R., Adams, A., Nelson, B., Shelpuk, C., 1977b. Trace metals in organisms from ocean disposal sites of the middle eastern United States. Arch. Environ. Contam. Toxicol. 6, 395–409. Guary, J.C., Fowler, S.W., 1978. Uptake from water and tissue distribution of neptunium-237 in crabs, shrimp, and mussels. Mar. Pollut. Bull. 9, 331–334. Guary, J.C., Negrel, R., 1980. Plutonium and iron association with metal-binding proteins in the crab Cancer pagurus (L.). J. Exp. Mar. Biol. Ecol. 42, 87–98. Guary, J.C., Masson, M., Fraizier, A., 1976. Etude preliminaire, in situ, de la distribution du plutonium dans differents tissues et organes de Cancer pagurus (crustacea: decapoda) et de Pleuronectes platessa (pisces: pleuronectidae). Mar. Biol. 36, 13–17. Guerin, T., Sirot, V., Volatier, J.L., Leblanc, J.C., 2007. Organotin levels in seafood and its implications for health risk in high-seafood consumers. Sci. Total Environ. 388, 66–77. Hall Jr., L.W., Pinkney, A.E., 1985. Acute and sublethal effects of organotin compounds on aquatic biota: An interpretive literature evaluation. CRC Crit. Rev. Toxicol. 14, 159–209. Hall, W.S., Pulliam, G.W., 1995. An assessment of metals in an estuarine wetlands ecosystem. Arch. Environ. Contam. Toxicol. 29, 164–173. Hall, R.A., Zook, E.G., Meaburn, G.M., 1978. National Marine Fisheries Service survey of trace elements in the fishery resource. U.S. Dept. Commerce NOAA Tech. Rept., NMFS SSRF-721, pp. 1–313. Hall Jr., L.W., Bushong, S.J., Hall, W.S., Johnson, W.E., 1988a. Acute and chronic effects of tributyltin to a Chesapeake Bay copepod. Environ. Toxicol. Chem. 7, 41–46. Hall, W.S., Bushong, S.J., Hall Jr., L.W., Lenkevich, M.S., Pinkney, A.E., 1988b. Monitoring dissolved copper concentrations in Chesapeake Bay, U.S.A. Environ. Monit. Assess. 11, 33–42. Hall Jr., L.W., Zeigenfuss, M.C., Anderson, R.D., Lewis, B.L., 1995. The effect of salinity on the acute toxicity of total and free cadmium to a Chesapeake Bay copepod and fish. Mar. Pollut. Bull. 30, 376–384.
504 Chapter 7 Hall Jr., L.W., Anderson, R.D., Lewis, B.L., Arnold, W.R., 2008. The influence of salinity and dissolved organic carbon on the toxicity of copper to the estuarine copepod, Eurytemora affinis. Arch. Environ. Contam. Toxicol. 54, 44–56. Han, B.C., Jeng, W.L., Chen, R.Y., Fang, G.T., Hung, T.C., Tseng, R.J., 1998. Estimation of target hazard quotients and potential health risks for metals by consumption of seafood in Taiwan. Arch. Environ. Contam. Toxicol. 35, 711–720. Hanaoka, K., Tagawa, S., 1985a. Isolation and identification of arsenobetaine as a major water soluble arsenic compound from muscle of blue pointer Isurus oxyrhincus and whitetip shark Carcharhinus longimanus. Bull. Jpn. Soc. Sci. Fish. 51, 681–685. Hanaoka, K., Tagawa, S., 1985b. Identification of arsenobetaine in muscle of roundnose flounder Eopsetta grigorjewi. Bull. Jpn. Soc. Sci. Fish. 51, 1203. Hansen, J.I., Mustafa, T., Depledge, M., 1992a. Mechanisms of copper toxicity in the shore crab, Carcinus maenas. I. Effects on Na, K, ATPase activity, haemolymph electrolyte concentrations and tissue water contents. Mar. Biol. 114, 253–257. Hansen, J.I., Mustafa, T., Depledge, M., 1992b. Mechanisms of copper toxicity in the shore crab, Carcinus maenas. II. Effects on key metabolic enzymes, metabolites and energy charge potential. Mar. Biol. 114, 259–264. Hardstedt-Romeo, M., Laumond, F., 1980. Zinc, copper and cadmium in zooplankton from the N.W. Mediterranean. Mar. Pollut. Bull. 11, 133–138. Harino, H., Fukushima, M., Yamamoto, Y., Kawai, S., Miyazaki, N., 1998. Organotin compounds in water, sediment, and biological samples from the Port of Osaka, Japan. Arch. Environ. Contam. Toxicol. 35, 558–564. Harrington, J.M., 1991. Tributyltin residues in Lake Tahoe and San Diego Bay, California, 1988, State of California Dept. Fish Game. Environ. Serv. Div. Admin. Rep. 91-1, pp. 1–29. Harvey, J., Harwell, L., Summers, J.K., 2008. Contaminant concentrations in whole-body fish and shellfish from US estuaries. Environ. Monit. Assess. 137, 403–412. Heyraud, M., Cherry, R.D., 1979. Polonium-210 and lead-210 in marine food chains. Mar. Biol. 52, 227–236. Hilmy, A.M., El-Hamid, N.F.A., Ghazaly, K.S., 1988. Biochemical and physiological changes in the tissues and serum of both sexes in Portunus pelagicus (L.) following acute exposures to zinc and copper. Folia Morphol. 36, 79–94. Hiyama, Y., Shimizu, M., 1964. On the concentration factors of radioactive Cs, Sr, Cd, Zn and Ce in marine organisms. Rec. Oceanogr. Works Jpn. 7 (2), 43–77. Holden, A.V., Topping, G., 1972. XIV: Occurrence of specific pollutants in fish in the Forth and Tay estuaries. Proc. R. Soc. Edin. 71B, 189–194. Hoover, W.L., Melton, J.R., Howard, P.A., Bassett Jr., J.W., 1974. Atomic absorption spectrometric determination of arsenic. JAOAC 57, 18–21. Horowitz, A., Presley, B.J., 1977. Trace metal concentrations and partitioning in zooplankton, neuston, and benthos from the south Texas Outer Continental Shelf. Arch. Environ. Contam. Toxicol. 5, 241–255. Hu, J., Zhen, H., Wan, Y., Gao, J., An, W., An, L., et al., 2006. Trophic magnification of triphenyltin in a marine food web of Bohai Bay, North China: Comparison to tributyltin. Environ. Sci. Technol. 40, 3142–3147. Huang, Y., Zhu, L., Liu, G., 2006. The effects of bis(tributyltin) oxide on the development, reproduction and sex ratio of calanoid copepod Pseudodiaptomus marinus. Estuar. Coast. Shelf Sci. 69, 147–152. Huggett, R.J., Unger, M.A., Seligman, P.F., Valkirs, A.O., 1992. The marine biocide tributyltin. Environ. Sci. Technol. 26, 232–237. Hui, C.A., Rudnick, D., Williams, E., 2005. Mercury burdens in Chinese mitten crabs (Eriocheir sinensis) in three tributaries of southern San Francisco Bay, California, USA. Environ. Pollut. 133, 481–487. Hutcheson, M.S., 1974. The effect of temperature and salinity on cadmium uptake by the blue crab, Callinectes sapidus. Chesapeake Sci. 15, 237–241. Ichikawa, R., 1961. On the concentration factors of some important radionuclides in marine food organisms. Bull. Jpn. Soc. Sci. Fish. 27, 66–74.
Crustaceans 505 Ikebe, K., Tanaka, R., 1979. Determination of vanadium and nickel in marine samples by flameless and flame atomic absorption spectrophotometry. Bull. Environ. Contam. Toxicol. 21, 526–532. Ireland, M.P., 1973. Result of fluvial zinc pollution on the zinc content of littoral and sublittoral organisms in Cardigan Bay, Wales. Environ. Pollut. 4, 27–35. Ireland, M.P., 1974. Variations in the zinc, copper, manganese, and lead content of Balanus balanoides in Cardigan Bay, Wales. Environ. Pollut. 7, 65–75. Ishii, T., Suzuki, H., Koyanagi, T., 1978. Determination of trace elements in marine organisms: I. Factors for variation of concentration of trace element. Bull. Jpn. Soc. Sci. Fish. 44, 155–162. Jenkins, D.W., 1980. Biological monitoring of toxic trace metals. Vol. 2. Toxic trace metals in plants and animals of the world. Part III. U.S. Environ. Protect. Agen. Rep. 600/3-80-092, pp. 1130–1148. Jennings, J.R., Rainbow, P.S., 1979a. Studies on the uptake of cadmium by the crab Carcinus maenas in the laboratory. I. Accumulation from seawater and a food source. Mar. Biol. 50, 131–139. Jennings, J.R., Rainbow, P.S., 1979b. Accumulation of cadmium by Artemia salina. Mar. Biol. 51, 47–53. Jennings, J.R., Rainbow, P.S., Scott, A.G., 1979. Studies on the uptake of cadmium by the crab Carcinus maenas in the laboratory. II. Preliminary investigation of cadmium-binding proteins. Mar. Biol. 50, 141–149. Johnson, D.L., Braman, R.S., 1975. The speciation of arsenic and the content of germanium and mercury in members of the pelagic Sargassum community. Deep Sea Res. 22, 503–507. Johnson, I., Jones, M.B., 1989. Effects of zinc/salinity combinations on zinc regulation in Gammarus duebeni from the estuary and the sewage treatment works at Looe, Cornwall. J. Mar. Biol. Assoc. UK 69, 249–260. Jones, M.B., 1975. Effects of copper on survival and osmoregulation in marine and brackish water isopods (Crustacea). In: Proceedings of Ninth European Marine Biology Symposium, pp. 419–431. Jung, K., Zauke, G.P., 2008. Bioaccumulation of trace metals in the brown shrimp Crangon crangon (Linnaeus, 1758) from the German Wadden Sea. Aquat. Toxicol. 88, 243–249. Kadar, E., Costa, V., Santos, R.S., 2006. Distribution of micro-essential (Fe, Cu, Zn) and toxic (Hg) metals in tissue of two nutritionally distinct hydrothermal shrimps. Sci. Total Environ. 358, 143–150. Kaise, T., Fukui, S., 1992. The chemical form and acute toxicity of arsenic compounds in marine organisms. Appl. Organomet. Chem. 6, 155–160. Karouna-Renier, N.K., Snyder, R.A., Allison, J.G., Wagner, M.G., Rao, K.R., 2007. Accumulation of organic and inorganic contaminants in shellfish collected in estuarine waters near Pensacola, Florida: Contamination profiles and risks to human consumers. Environ. Pollut. 145, 474–488. Keckes, S., Fowler, S.W., Small, L.F., 1972. Flux of different forms of 106Ru through a marine zooplankter. Mar. Biol. 13, 94–99. Kennedy, V.S., 1976. Arsenic concentrations in some coexisting marine organisms from Newfoundland and Labrador. J. Fish. Res. Board Can. 33, 1388–1393. Ketchum, B.M., Bowen, V.T., 1958. Biological factors determining the distribution of radioisotopes in the sea. In: Proceedings of the Second Annual United Nations International Congress on the Peaceful Uses of Atomic Energy: Vol. 18, Waste Treatment and Environmental Aspects of Atomic Energy. IAEA, Geneva, pp. 429–433. Khan, A.T., Weis, J.S., D’Andrea, L., 1989. Bioaccumulation of four heavy metals in two populations of grass shrimp, Palaemonetes pugio. Bull. Environ. Contam. Toxicol. 42, 339–343. Kharkar, D.P., Thomson, J., Turekian, K.K., Forster, W.O., 1976. Uranium and thorium decay series nuclides in plankton from the Caribbean. Limnol. Oceanol. 21, 294–299. King, C.K., Gale, S.A., Hyne, R.V., Stauber, J.L., Simpson, S.L., Hickey, C.W., 2006a. Sensitivities of Australian and New Zealand amphipods to copper and zinc in waters and metal-spiked sediments. Chemosphere 63, 1466–1476. King, C.K., Gale, S.A., Stauber, J.L., 2006b. Acute toxicity and bioaccumulation of aqueous and sediment-bound metals in the estuarine amphipod Melita plumulosa. Environ. Toxicol. 21, 489–504. Klemmer, H.W., Unninayer, C.S., Ukubo, W.I., 1976. Mercury content of biota in coastal waters in Hawaii. Bull. Environ. Contam. Toxicol. 15, 454–457. Knauer, G.A., 1970. The determination of magnesium, manganese, iron, copper, and zinc in marine shrimp. Analyst 93, 476–480.
506 Chapter 7 Knothe, D.W., Van Riper, G.G., 1988. Acute toxicity of sodium molybdate dihydrate (Molhibit 100) to selected saltwater organisms. Bull. Environ. Contam. Toxicol. 40, 785–790. Kobayashi, N., 1979. Barnacle larvae and rotifers as indicatory materials for marine pollution bioassay, preliminary experiments. Sci. Eng. Rev. Doshisha Univ. 19, 61–67. Kuenzler, E.J., 1969. Elimination and transport of cobalt by marine zooplankton. In: Proceedings of the 2nd National Symposium on Radioecology. U.S. Atom. Ener. Comm., Conf. 670503, pp. 483–492. Kumagai, H., Saeki, K., 1978. Contents of total mercury, alkyl mercury and methylmercury in some coastal fish and shells. Bull. Jpn. Soc. Sci. Fish. 44, 807–811. Laughlin, R., Nordlund, K., Linden, O., 1984. Long-term effects of tributyltin compounds on the Baltic amphipod, Gammarus oceanicus. Mar. Environ. Res. 12, 243–271. Laughlin Jr., R.B., Johannesen, R.B., French, W., Guard, H., Brinckman, F.E., 1985. Structure-activity relationships for organotin compounds. Environ. Toxicol. Chem. 4, 343–351. Laughlin Jr., R.B., French, W., Guard, H.E., 1986. Accumulation of bis(tributyltin)oxide by the marine mussel Mytilus edulis. Environ. Sci. Technol. 20, 884–890. Leatherland, T.M., Burton, J.D., 1974. The occurrence of some trace metals in coastal organisms with particular reference to the Solent region. J. Mar. Biol. Assoc. UK 54, 457–468. Leatherland, T.M., Burton, J.D., Culkin, F., McCartney, M.J., Morris, R.J., 1973. Concentrations of some trace metals in pelagic organisms and of mercury in Northeast Atlantic Ocean water. Deep Sea Res. 20, 679–685. LeBlanc, P.J., Jackson, A.L., 1973. Arsenic in marine fish and invertebrates. Mar. Pollut. Bull. 4, 88–90. Lee, K.M., Johnston, E.L., 2007. Low levels of copper reduce the reproductive success of a mobile invertebrate predator. Mar. Environ. Res. 64, 336–346. Lee, K.W., Raisuddin, S., Hwang, D.S., Park, H.G., Lee, J.S., 2007. Acute toxicities of trace metals and common xenobiotics to the marine copepod Tigriopus japonicus: Evaluation of its use as a benchmark species for routine ecotoxicity tests in western Pacific coastal regions. Environ. Toxicol. 22, 532–538. Lee, K.W., Raisuddin, S., Hwang, D.S., Park, H.G., Dahms, H.U., Ahn, I.Y., et al., 2008. Two-generation toxicity study on the copepod model species Tigriopus japonicus. Chemosphere 72, 1359–1365. Lewis, T.E., McIntosh, A.W., 1986. Uptake of sediment-bound lead and zinc by the freshwater isopod Asellus communis at three different pH levels. Arch. Environ. Contam. Toxicol. 15, 495–504. Lewis, A.G., Whitfield, P.H., Ramnarine, A., 1972. Some particulate and soluble agents affecting the relationship between metal toxicity and organism survival in the calanoid copepod Euchaeta japonica. Mar. Biol. 17, 215–221. Lewis, A.G., Whitfield, P., Ramnarine, A., 1973. The reduction of copper toxicity in a marine copepod by sediment extract. Limnol. Oceanol. 18, 324–326. Lindsay, D.M., Sanders, J.G., 1990. Arsenic uptake and transfer in a simplified estuarine food chain. Environ. Toxicol. Chem. 9, 391–395. Lowman, F.G., Phelps, D.K., Ting, R.Y., Escalera, R.M., 1966. Progress Summary Report No. 4, Marine Biology Program June 1965-June 1966. Puerto Rico Nucl. Cen Rep. PRNC, 85, pp. 1–57 + Appendices A-F. Lowman, F.G., Martin, J.H., Ting, R.Y., Barnes, S.S., Swift, D.J.P., Seiglei, G.A., et al., 1970. Bioenvironmental and Radiological-Safety Feasibility Studies, Atlantic-Pacific Interoceanic Canal, vol. I-IV, Contract AT (26-1)-171. Battelle Memorial Institute, Columbus, OH. Lucu, C., Jelisavcic, O., Lucic, S., Strohal, P., 1969. Interactions of 233Pa with tissues of Mytilus galloprovincialis and Carcinus mediterraneus. Mar. Biol. 2, 103–104. Luoma, S.N., 1976. The uptake and interorgan distribution of mercury in a carnivorous crab. Bull. Environ. Contam. Toxicol. 16, 719–723. Luoma, S.N., 1977. The dynamics of biologically available mercury in a small estuary. Estuar. Coast. Mar. Sci. 5, 643–652. MacFarlane, G.R., Schreider, M., McLennan, B., 2006. Biomarkers of heavy metal contamination in the red fingered marsh crab, Parasesarma erythodactyla. Arch. Environ. Contam. Toxicol. 51, 584–593. Mackay, D.W., Halcrow, W., Thornton, I., 1972. Sludge dumping in the Firth of Clyde. Mar. Pollut. Bull. 3, 7–10.
Crustaceans 507 Maddock, B.G., Taylor, D., 1980. The acute toxicity and bioaccumulation of some lead alkyl compounds in marine animals. In: Branica, M., Konrad, Z. (Eds.), Lead in the Marine Environment. Pergamon, Oxford, UK, pp. 233–261. Maher, W.A., 1983. Selenium in marine organisms from St. Vincent’s Gulf, South Australia. Mar. Pollut. Bull. 14, 35–36. Maher, W.A., 1985. The presence of arsenobetaine in marine animals. Biochem. Physiol. 80C, 199–201. Manyin, T., Rowe, C.L., 2008. Modeling effects of cadmium on population growth of Palaemonetes pugio: Results of a full life cycle exposure. Aquat. Toxicol. 88, 111–120. Martin, J.H., 1970. The possible transport of trace metals via molted copepod exoskeletons. Limnol. Oceanol. 15, 756–761. Martin, J.L.M., 1972. Study of the uptake, concentration, and metabolism of strontium 85 by the decapod crustacean Carcinus maenas. Mar. Biol. 12, 154–158. Martin, J.L.M., 1973. Iron metabolism in Cancer irroratus (crustacea: decapoda) during the intermoult cycle, with special reference to iron in the gills. Comp. Biochem. Physiol. 46A, 123–129. Martin, J.H., Knauer, G.A., 1973. The elemental composition of plankton. Geochim. Cosmochim. Acta 37, 1639–1653. Martin, J.L.M., Van Wormhoudt, A., Ceccaldi, H.H., 1977. Zinc-hemocyanin binding to the hemolymph of Carcinus maenas (Crustacea: Decapoda). Comp. Biochem. Physiol. 58A, 193–195. Matida, Y., Kumada, H., 1969. Distribution of mercury in water, bottom mud and aquatic organisms of Minamata Bay, the River Agano and other water bodies in Japan. Bull. Freshw. Fish. Res. Lab. Tokyo 19 (2), 73–93. Matsuto, S., Stockton, R.A., Irgolic, K.J., 1986. Arsenobetaine in the red crab, Chionoecetes opilio. Sci. Total Environ. 48, 133–140. Mauchline, J., Templeton, W.L., 1966. Strontium, calcium, and barium in marine organisms from the Irish Sea. J. Cons. Perm. Int. Explor. Mer 30, 161–170. McGee, B.L., Wright, D.A., Fisher, D.J., 1998. Biotic factors modifying acute toxicity of aqueous cadmium to estuarine amphipod Leptocheirus plumulosus. Arch. Environ. Contam. Toxicol. 34, 34–40. McKenney Jr., C.L., Neff, J.M., 1979. Individual effects and interactions of salinity, temperature, and zinc on larval development of the grass shrimp Palaemonetes pugio. I. Survival and developmental duration through metamorphosis. Mar. Biol. 52, 177–188. McLeese, D.W., 1974. Toxicity of copper at two temperatures and three salinities to the American lobster (Homarus americanus). J. Fish. Res. Board Can. 31, 1949–1952. McLusky, D.S., Hagerman, L., 1987. The toxicity of chromium, nickel and zinc: Effects of salinity and temperature, and the osmoregulatory consequences in the mysid Praunus flexuosus. Aquat. Toxicol. 10, 225–238. Memmert, U., 1987. Bioaccumulation of zinc in two freshwater organisms (Daphnia magna, crustacea and Brachydanio rerio, pisces). Water Res. 21, 99–106. Miller, C.D., Nelson, D.M., Guillard, R.R.L., Woodward, B.L., 1980. Effects of media with low silicic acid concentrations on tooth formation in Acartia tonsa Dana (Copepoda, Calanoida). Biol. Bull. 159, 349–363. Moore, P.G., Rainbow, P.S., Hayes, E., 1991. The beach hopper Orchestia gammarellus (Crustacea: Amphipoda) as a biomonitor for copper and zinc: North Sea trials. Sci. Total Environ. 106, 221–238. Morris, R.J., Law, R.J., Allchin, C.R., Kelly, C.A., Fileman, C.F., 1989. Metals and organochlorines in dolphins and porpoises of Cardigan Bay, West Wales. Mar. Pollut. Bull. 20, 512–523. Mushak, P., 1980. Metabolism and systemic toxicity of nickel. In: Nriagu, J.O. (Ed.), Nickel in the Environment. John Wiley, New York, pp. 499–523. Neff, J.M., Anderson, J.W., 1977. The effects of copper (II) on molting and growth of juvenile lesser blue crabs Callinectes similis. In: Giam, C.S. (Ed.), Pollutant Effects on Marine Organisms. D.C. Heath, Lexington, MA, pp. 155–165. Neff, J.M., Foster, R.S., Slowey, J.F., 1978. Availability of sediment-absorbed heavy metals o benthos with particular emphasis on deposit-feeding infauna. Tech. Rep. D-78-42. U.S. Army Waterways Exp. Sta., Vicksburg, MS, 286 pp.
508 Chapter 7 Neff, J.M., Carr, R.S., McCullough, W.L., 1981. Acute toxicity of a used chrome lignosulfonate drilling mud to several species of marine invertebrates. Mar. Environ. Res. 4, 251–266. Nicholls, G.D., Curl Jr., H., Bowen, V.T., 1959. Spectrographic analyses of marine plankton. Limnol. Oceanol. 4, 472–476. Nimmo, D.R., Lightner, D.V., Bahner, L.H., 1977. Effects of cadmium on the shrimps, Penaeus duorarum, Palaemonetes pugio, and Palaemonetes vulgaris. In: Vernberg, F.J., Calabrese, A., Thurberg, F.P., Vernberg, W.B. (Eds.), Physiological Responses of Marine Biota to Pollutants. Academic Press, New York, pp. 131–183. Nonnotte, L., Boitel, F., Truchot, J.P., 1993. Waterborne copper causes gill damage and hemolymph hypoxia in the shore crab Carcinus maenas. Can. J. Zool. 71, 1569–1576. Norin, H., Vahter, M., Christakopoulos, A., Sandstrom, M., 1985. Concentration of inorganic and total arsenic in fish from industrially polluted water. Chemosphere 14, 1125–1134. Nugegoda, D., Rainbow, P.S., 1987. The effect of temperature on zinc regulation by the decapod crustacean Palaemon elegans Rathke. Ophelia 27, 17–30. Nugegoda, D., Rainbow, P.S., 1988a. Effect of a chelating agent (EDTA) on zinc uptake and regulation by Palaemon elegans (crustacea: decapoda). J. Mar. Biol. Assoc. UK 68, 25–40. Nugegoda, D., Rainbow, P.S., 1988b. Zinc uptake and regulation by the sublittoral prawn Pandalus montagui (crustacea: decapoda). Estuar. Coast. Shelf Sci. 26, 619–632. Nugegoda, D., Rainbow, P.S., 1989a. Effects of salinity changes on zinc uptake and regulation by the decapod crustaceans Palaemon elegans and Palaemonetes varians. Mar. Ecol. Prog. Ser. 51, 57–75. Nugegoda, D., Rainbow, P.S., 1989b. Salinity, osmolality, and zinc uptake in Palaemon elegans (crustacea: decapoda). Mar. Ecol. Prog. Ser. 55, 149–157. Nugegoda, D., Rainbow, P.S., 1989c. Zinc uptake and regulation breakdown in the decapod crustacean Palaemon elegans Rathke. Ophelia 30, 199–212. Nunez-Nogueira, G., Mouneyrac, C., Amiard, J.C., Rainbow, P.S., 2006a. Subcellular distribution of zinc and cadmium in the hepatopancreas and gills of the decapod crustacean Penaeus indicus. Mar. Biol. 150, 197–211. Nunez-Nogueira, G., Rainbow, P.S., Smith, B.D., 2006b. Assimilation efficiency of zinc and cadmium in the decapod crustacean Penaeus indicus. J. Exp. Mar. Biol. Ecol. 332, 75–83. Nuorteva, P., Hasanen, E., 1975. Bioaccumulation of mercury in Myoxocephalus quadricornis (L.) (Teleostei, Cottidae) in an unpolluted area of the Baltic. Ann. Zool. Fennici 12, 247–254. O’Hara, J., 1973a. The influence of temperature and salinity on the toxicity of cadmium to the fiddler crab, Uca pugilator. US Dept. Comm. Fish. Bull. 71 (1), 149–153. O’Hara, J., 1973b. Cadmium uptake by fiddler crabs exposed to temperature and salinity stress. J. Fish. Res. Board Can. 30, 846–848. Oweson, C., Baden, S., Henroth, B., 2006. Manganese induced apoptosis in haematopoietic cells of the lobster, Nephrops norvegicus. Aquat. Toxicol. 77, 322–328. Ozretic, B., Krajinovic-Ozretic, N., Santin, J., Medjugorac, B., Kras, M., 1990. As, Cd, Pd, and Hg in benthic animals from the Kvarner-Rijeka Bay region, Yugoslavia. Mar. Pollut. Bull. 21, 595–597. Palmer, A.S., Snape, I., Stark, J.S., Johnstone, G.J., Townsend, A.T., 2006. Baseline metal concentrations in Paramoera walkeri from East Antarctica. Mar. Pollut. Bull. 52, 1441–1449. Parrish, K.M., Carr, R.A., 1976. Transport of mercury through a laboratory two-level marine food chain. Mar. Pollut. Bull. 7, 90–91. Parveneh, V., 1977. A survey of the mercury content of the Persian Gulf shrimp. Bull. Environ. Contam. Toxicol. 18, 778–782. Patel, H.S., Kaliwal, M.B., 1989. Histopathological effects of zinc on the gills of prawn Macrobrachium hendersodyanum. Zeit. Ange. Zool. 76, 505–509. Pearcy, W.G., Osterberg, C.L., 1967. Depth, diel, seasonal, and geographic variations in zinc-65 of midwater animals off Oregon. Int. J. Oceanol. Limnol. 1, 103–116. Peden, J.D., Crothers, J.H., Waterfall, C.W., Beasley, J., 1973. Heavy metals in Somerset marine organisms. Mar. Pollut. Bull. 4, 7–10.
Crustaceans 509 Pedroso, M.S., Bersano, J.G.F., Bianchini, A., 2007a. Acute silver toxicity in the euryhaline copepod Acartia tonsa: Influence of salinity and food. Environ. Toxicol. Chem. 26, 2158–2165. Pedroso, M.S., Pinho, C.L.L., Rodrigues, S.C., Bianchini, A., 2007b. Mechanism of acute silver toxicity in the euryhaline copepod Acartia tonsa. Aquat. Toxicol. 82, 173–180. Pempkowiak, J., Walkusz-Miotk, J., Beldowski, J., Walkusz, W., 2006. Heavy metals in zooplankton from the southern Baltic. Chemosphere 62, 1697–1708. Penrose, W.R., Black, R., Hayward, M.J., 1975. Limited arsenic dispersion in seawater, sediments, and biota near a continuous source. J. Fish. Res. Board Can. 32, 1275–1281. Pequegnat, J.E., Fowler, S.W., Small, L.F., 1969. Estimates of the zinc requirements of marine organisms. J. Fish. Res. Board Can. 26, 145–150. Pereira, E., Abreu, S.N., Coelho, J.P., Lopes, C.B., Pardal, M.A., Vale, C., et al., 2006. Seasonal fluctuations of tissue mercury contents in the European shore crab Carcinus maenas from low and high contamination areas (Ria de Aveiro, Portugal). Mar. Pollut. Bull. 52, 1450–1457. Pesch, G.G., Stewart, N.E., 1980. Cadmium toxicity to three species of invertebrates. Mar. Environ. Res. 3, 145–146. Peshut, P.J., Morrison, R.J., Brooks, B.A., 2008. Arsenic speciation in marine fish and shellfish from American Samoa. Chemosphere 71, 484–492. Petri, G., Zauke, G.P., 1993. Trace metals in crustaceans in the Antarctic Ocean. Ambio 22, 529–536. Phillips, D.J.H., 1990. Arsenic in aquatic organisms: A review, emphasizing chemical speciation. Aquat. Toxicol. 16, 151–186. Phillips, D.J.H., Depledge, M.H., 1986. Chemical forms of arsenic in marine organisms, with emphasis on Hemifusus species. Water Sci. Technol. 18, 213–222. Phillips, D.J.H., Thompson, G.B., Gabuji, K.M., Ho, C.T., 1982. Trace metals of toxicological significance to man in Hong Kong seafood. Environ. Pollut. 3B, 27–45. Pinho, G.L.L., Pedroso, M.S., Rodrigues, S.C., d Souza, S.S., Bianchini, A., 2007. Physiological effects of copper in the euryhaline copepod Acartia tonsa: Waterborne versus waterborne plus dietborne exposure. Aquat. Toxicol. 84, 62–70. Pinkney, A.E., Matteson, L.L., Wright, D.A., 1990. Effects of tributyltin on survival, growth, morphometry, and RNA-DNA ratio of larval striped bass, Morone saxatilis. Arch. Environ. Contam. Toxicol. 19, 235–240. Polikarpov, G.G., Oregioni, B., Parchevskaya, D.S., Benayoun, G., 1979. Body burden of chromium, copper, cadmium and lead in the neustonic copepod Anomalocera patersoni (Pontellidae) collected from the Mediterranean Sea. Mar. Biol. 53, 79–82. Pouvreau, B., Amiard, J.C., 1974. Etude experimentale de l’accumulation de l’argent 110 a chez divers organismes marins. Comm. Ener. Atom. France, Rept. CEA-R-4571, pp. 1–19. Powell, M.L., White, K.N., 1990. Heavy metal accumulation by barnacles and its implications for their use as biological monitors. Mar. Environ. Res. 30, 91–118. Prange, A., Kremling, K., 1985. Distribution of dissolved molybdenum, uranium and vanadium in Baltic Sea waters. Mar. Chem. 16, 259–274. Pullen, J.S.H., Rainbow, P.S., 1991. The composition of pyrophosphate heavy metal detoxification granules in barnacles. J. Exp. Mar. Biol. Ecol. 150, 249–266. Pyefinch, K.A., Mott, J.C., 1948. The sensitivity of barnacles and their larvae to copper and mercury. J. Exp. Biol. 25, 296–298. Rabitsch, W.B., 1995. Metal accumulation in arthropods near a lead/zinc mine in Arnoldstein, Austria. Environ. Pollut. 90, 221–227. Rainbow, P.S., 1989. Copper, cadmium and zinc concentrations in oceanic amphipod and euphausiid crustaceans, as a source of heavy metals to pelagic seabirds. Mar. Biol. 103, 513–518. Rainbow, P.S., Scott, A.G., 1979. Two heavy metal-binding proteins in the midgut gland of the crab Carcinus maenas. Mar. Biol. 55, 143–150. Rainbow, P.S., White, S.L., 1989. Comparative strategies of heavy metal accumulation by crustaceans: Zinc, copper and cadmium in a decapod, an amphipod and a barnacle. Hydrobiologia 174, 245–262.
510 Chapter 7 Rainbow, P.S., Scott, A.G., Wiggins, E.A., Jackson, R.W., 1980. Effects of chelating agents on the accumulation of cadmium by the barnacle Semibalanus balanoides, and complexation of soluble Cd, Zn and Cu. Mar. Ecol. Prog. Ser. 2, 143–152. Rainbow, P.S., Moore, P.G., Watson, D., 1989. Talitrid amphipods (crustacea) as biomonitors for copper and zinc. Estuar. Coast. Shelf Sci. 28, 567–582. Ramelow, G.J., Webre, C.L., Mueller, C.S., Beck, J.N., Young, J.C., Langley, M.P., 1989. Variations of heavy metals and arsenic in fish and other organisms from the Calcasieu River and Lake, Louisiana. Arch. Environ. Contam. Toxicol. 18, 804–818. Ramos, A., de Campos, M., Olszyna-Marzys, A.E., 1979. Mercury contamination of fish in Guatemala. Bull. Environ. Contam. Toxicol. 22, 488–491. Ray, S., McLeese, D.W., Waiwood, B.A., Pezzack, D., 1980. The disposition of cadmium and zinc in Pandalus montagui. Arch. Environ. Contam. Toxicol. 9, 675–681. Rees, H.L., Waldock, R., Matthiessen, P., Pendle, M.A., 1999. Surveys of the epibenthos of the Crouch Estuary (UK) in relation to TBT contamination. J. Mar. Biol. Assoc. UK 79, 209–223. Reeve, M.R., Walter, M.A., Darcy, K., Ikeda, T., 1977. Evaluation of potential indicators of sub-lethal toxic stress on marine zooplankton (feeding, fecundity, respiration, and excretion): Controlled ecosystem pollution experiment. Bull. Mar. Sci. 27, 105–113. Reimer, A.A., Reimer, R.D., 1975. Total mercury in some fish and shellfish along the Mexican coast. Bull. Environ. Contam. Toxicol. 14, 105–111. Reinke, J., Uthe, J.F., Freeman, H.C., Johnston, J.R., 1975. The determination of arsenite and arsenate ions in fish and shellfish by selective extraction and polarography. Environ. Lett. 8, 371–380. Renfro, W.C., Fowler, S.W., Heyraud, M., LaRosa, J., 1975. Relative importance of food and water in long-termzinc-65 accumulation by marine biota. J. Fish. Res. Board Can. 31, 1339–1345. Renzoni, A., Bacci, E., Falciai, L., 1973. Mercury concentration in the water, sediments, and fauna of an area of the Tyrrhenian Coast. In: Sixth International Symposium Medic. Ocean., Portoroz, Yugoslavia, 26-30 September 1973, pp. 17–45. Ridout, P.S., Rainbow, P.S., Roe, H.S.J., Jones, H.R., 1989. Concentrations of V, Cr, Mn, Fe, Ni, Co, Cu, Zn, As and Cd in mesopelagic crustaceans from the north east Atlantic Ocean. Mar. Biol. 100, 465–471. Ringenary, M.J., Molof, A.H., Tancredi, J.T., Schreibman, M.P., Kostarelos, K., 2007. Long-term sediment bioassay of lead toxicity in two generations of the marine amphipod Elasmopus laevis, S.I. Smith, 1873. Environ. Toxicol. Chem. 26, 1700–1710. Roberts, D., Maguire, C., 1976. Interactions of lead with sediment and meiofauna. Mar. Pollut. Bull. 7, 211–213. Roberts, D.A., Poore, A.G.B., Johnston, E.L., 2006. Ecological consequences of copper contamination in macroalgae: Effects on epifauna and associated herbivores. Environ. Toxicol. Chem. 25, 2470–2479. Robertson, D.E., 1967. Trace elements in marine organisms. Rapp. Amer., BNWL 481-2, pp. 56–59. Robertson, D.E., Rancitelli, L.A., Langford, J.C., Perkins, R.W., 1972. Battelle-Northwest contribution to the IDOE base-line study. Battelle Pac. Northwest Lab., Richland, Washington, 1–46. Roesijadi, G., Petrocelli, S.E., Anderson, J.W., Presley, B.J., Sims, R., 1974. Survival and chloride ion regulation of the porcelain crab Petrolisthes armatus exposed to mercury. Mar. Biol. 17, 213–217. Rosemarin, A., Notini, N., Holmgren, K., 1985. The fate of arsenic in the Baltic Sea Fucus vesiculosus ecosystem. Ambio 14, 342–345. Ruelas-Inzunza, J., Paez-Osuna, F., 2008. Trophic distribution of Cd, Pb, and Zn in a food web from AltataEnsenada del Pebellon subtropical lagoon, SE Gulf of California. Arch. Environ. Contam. Toxicol. 54, 584–596. Saliba, L.J., Ahsanullah, M., 1973. Acclimation and tolerance of Artemia salina and Ophryotrocha labronica to copper sulphate. Mar. Biol. 12, 297–302. Saliba, L.J., Krzyz, R.M., 1976. Acclimation and tolerance of Artemia salina to copper salts. Mar. Biol. 38, 231–238. Sanders, J.G., 1986. Direct and indirect effects of arsenic on the survival and fecundity of estuarine zooplankton. Can. J. Fish. Aquat. Sci. 43, 694–699.
Crustaceans 511 Sankar, T.V., Zynudheen, A.A., Anandan, R., Nair, P.G.V. 2006. Distribution of organochlorine pesticides and heavy metal residues in fish and shellfish from Calicut region, Kerala, India. Chemosphere 65, 583–590. Santos, I.R., Silva-Filho, E.V., Schaefer, C., Sella, S.M., Silva, C.A., Gomes, V., et al., 2006. Baseline mercury and zinc concentrations in terrestrial and coastal organisms of Admiralty Bay, Antarctica. Environ. Pollut. 140, 304–311. Sastry, V.W., Bhatt, Y.M., 1965. Zinc content of some marine bivalves and barnacles from Bombay shores. J. Indian Chem. Soc. 42, 121–122. Sather, B.T., 1967. Chromium absorption and metabolism by the crab, Podophthalmus vigil. In: Proceedings of the International Symposium on Radioecological Concentration Processes, Stockholm, 1966, pp. 943–976. Schreiber, W., 1983. Mercury content of fishery products: Data from the last decade. J. Am. Med. Assoc. 289, 1667–1674. Schuhmacher, M., Bosque, M.A., Domingo, J.L., Corbella, J., 1990. Lead and cadmium concentrations in marine organisms from the Tarragona coastal waters, Spain. Bull. Environ. Contam. Toxicol. 44, 784–789. Schuhmacher, M., Domingo, J.L., Bosque, M.A., Corbella, J., 1992. Heavy metals in marine species from the Tarragona Coast, Spain. J. Environ. Sci. Health 27A, 1939–1948. Schuhmacher, M., Batiste, J., Bosque, M.A., Domingo, J.L., Corbella, J., 1994. Mercury concentrations in marine species from the coastal area of Tarragona Province, Spain. Dietary intake of mercury through fish and seafood consumption. Sci. Total Environ. 156, 269–273. Scott-Fordsmand, J.J., Depledge, M.H., 1993. The influence of starvation and copper exposure on the composition of the dorsal carapace and distribution of trace metals in the shore crab Carcinus maenas (L.). Comp. Biochem. Physiol. 106C, 537–543. Seebaugh, D.R., Estephan, A., Wallace, W.G., 2006. Relationship between dietary cadmium absorption by grass shrimp (Palaemonetes pugio) and trophically available cadmium in amphipod (Gammarus lawrencianus) prey. Bull. Environ. Contam. Toxicol. 76, 16–23. Shealy, M.H., Sandifer, P.A., 1975. Effects of mercury on survival and development of the larval grass shrimp, Palaemonetes vulgaris. Mar. Biol. 33, 7–16. Shimizu, M., Kajihara, T., Hiyama, Y., 1970. Uptake of 60Co by marine animals. Rec. Oceanogr. Works Jpn. 10, 137–145. Shiomi, K., Shinagawa, A., Hirota, K., Yamanaka, H., Kikuchi, T., 1984a. Identification of arsenobetaine as a major arsenic compound in the ivory shell Buccinum striatissimum. Agric. Biol. Chem. 48, 2863–2864. Shiomi, K., Shinigawa, A., Igarashi, T., Yamanaka, H., Kikuchi, T., 1984b. Evidence for the presence of arsenobetaine as a major arsenic compound in the shrimp Sergestes lucens. Experientia 40, 1247–1248. Shrestha, K.P., Morales, E., 1987. Seasonal variations of iron, copper and zinc in Penaeus brasiliensis from two areas of the Caribbean Sea. Sci. Total Environ. 65, 175–180. Side, J., 1987. Organotins: Not so good relations. Mar. Pollut. Bull. 18, 205–206. Silva, C.A.R., Smith, B.D., Rainbow, P.S., 2006. Comparative biomonitors of coastal trace metal contamination in tropical South America (N. Brazil). Mar. Environ. Res. 61, 439–455. Sims Jr., R.R., Presley, B.J., 1976. Heavy metal concentrations in organisms from an actively dredged Texas bay. Bull. Environ. Contam. Toxicol. 16, 520–527. Sirota, G.R., Uthe, J.P., 1977. Determination of tetraalkyl lead compounds in biological materials. Anal. Chem. 49, 823–825. Small, L.F., Fowler, S.W., 1973. Turnover and vertical transport of zinc by the euphausiid Meganyctiphanes norvegica in the Ligurian Sea. Mar. Biol. 18, 284–290. Small, L.F., Fowler, S.W., Keckes, S., 1973. Flux of zinc through a macroplanktonic crustacean. In: Radioactive Contamination of the Marine Environment. IAEA, Vienna, Austria, pp. 437–452. Small, L.F., Keckes, S., Fowler, S.W., 1974. Excretion of different forms of zinc by the prawn, Palaemon serratus (Pennant). Limnol. Oceanol. 18, 789–793. Smith, P.J., 1978. Structure/Activity Relationships for Di- and Triorganotin Compounds. I.T.R.I Rep. 569. Available from International Tin Research Institute, Greenford, Middlesex, UK, 16 pp.
512 Chapter 7 Smith, B.S., 1981. Tributyltin compounds induce male characteristics on female mud snails Nassarius obsoletus = Ilyanassa obsolete. J. Appl. Toxicol. 1, 141–144. Sorentino, C., 1979. Mercury in marine and freshwater fish of Papua, New Guinea. Aust. J. Mar. Freshw. Res. 30, 617–623. Sparling, D.W., Lowe, T.P., 1996. Environmental hazards of aluminum to plants, invertebrates, fish, and wildlife. Rev. Environ. Contam. Toxicol. 145, 1–127. Spear, P.A., 1981. Zinc in the aquatic environment: Chemistry, distribution, and toxicology. Natl. Res. Coun. Canada, Publ. NRCC 17589, 145 pp. Sprague, J.G., 1986. Toxicity and Tissue Concentrations of Lead, Zinc, and Cadmium for Marine Molluscs and Crustaceans. Available from International Lead Zinc Research Organization, 2525 Meridian Parkway, Research Triangle Park, North Carolina 27709-2036, 215 pp. Srinivasin, M., Mahajan, B.A., 1989. Mercury pollution in an estuarine region and its effects on a coastal population. Int. J. Environ. Stud. 35, 63–69. Stenner, R.D., Nickless, G., 1974a. Absorption of cadmium, copper, and zinc by dog whelks in the Bristol Channel. Nature 247, 198–199. Stenner, R.D., Nickless, G., 1974b. Distribution of some heavy metals in organisms in Hardangerfjord and Skjerstadfjord, Norway. Water Air Soil Pollut. 3, 279–291. Stenner, R.D., Nickless, G., 1975. Heavy metals in organisms of the Atlantic coast of S.W. Spain and Portugal. Mar. Pollut. Bull. 6, 89–92. Stickney, R.R., Windom, H.L., White, D.B., Taylor, E.F., 1975. Heavy-metal concentrations in selected Georgia estuarine organisms with comparative food-habit data. In: Howell, F.G., Gentry, J.B., Smith, M.H. (Eds.), Mineral Cycling in South-Eastern Ecosystems. U.S. ERDA. Available as CONF 740513 from NTIS, Springfield, Virginia, pp. 257–267. Sunda, W.G., Tester, P.A., Huntsman, S.A., 1990. Toxicity of trace metals to Acartia tonsa in the Elizabeth River and southern Chesapeake Bay. Estuar. Coast. Shelf Sci. 30, 207–221. Sunderland, E.M., 2007. Mercury exposure from domestic and imported estuarine and marine fish in the U.S. seafood market. Environ. Health Perspect. 115, 235–242. Sundlein, B., 1983. Effects of cadmium on Pontoporeia affinis (Crustacea: Amphipoda) in laboratory soft bottom microcosms. Mar. Biol. 74, 203–212. Szefer, P., Pempkowiak, J., Skwarzec, B., Bojanowski, F., Holm, E., 1993. Concentration of selected metals in penguins and other representative fauna of the Antarctica. Sci. Total Environ. 138, 281–288. Tariq, J., Jaffar, M., Ashraf, M., Moazzam, M., 1993. Heavy metal concentrations in fish, shrimp, seaweed, sediment, and water from the Arabian Sea, Pakistan. Mar. Pollut. Bull. 26, 644–647. Tennant, D.A., Forster, W.D., 1969. Seasonal variation and distribution of 65-Zn, 54-Mn, and 51-Cr in tissues of the crab Cancer magister Dana. Health Phys. 18, 649–659. Thain, J.E., Waldock, M.J., 1986. The impact of tributyl tin (TBT) antifouling paints on molluscan fisheries. Water Sci. Technol. 18, 193–202. Thomas, P.G., Ritz, D.A., 1986. Growth of zinc granules in the barnacle Elminius modestus. Mar. Biol. 90, 255–260. Thompson, J.A.J., Davis, J.C., Drew, R.E., 1976. Toxicity, uptake, and survey studies of boron in the marine environment. Water Res. 10, 869–875. Thompson, J.A.J., Sheffer, M.G., Pierce, R.C., Chau, Y.K., Cooney, J.J., Cullen, W.R., et al., 1985. Organotin compounds in the aquatic environment: Scientific criteria for assessing their effects on environmental quality. Natl. Res. Coun. Canada, Publ. NRCC 22494. Available from Publications, NRCC/NRC, Ottawa, Canada, K1A OR6, 284 pp. Thorsson, M.H., Hedman, J.E., Bradshaw, C., Gunnarsson, J.S., Gilek, M., 2008. Effects of settling organic matter on the bioaccumulation of cadmium and BDE-99 by Baltic Sea invertebrates. Mar. Environ. Res. 65, 264–281. Thurberg, F.P., Calabrese, A., Gould, E., Greig, R.A., Dawson, M.A., Tucker, R.K., 1977. Response of the lobster Homarus americanus, to sublethal levels of cadmium and mercury. In: Vernberg, F.J., Calabrese, A.,
Crustaceans 513 Thurberg, W.B., Vernberg, W.B. (Eds.), Physiological Responses of Marine Biota to Pollutants. Academic Press, New York, pp. 185–197. Tijoe, P.S., de Goeij, J.J.M., de Bruin, M., 1977. Determination of trace elements in dried sea plant homogenate (SP-M-1) and in dried copepod homogenate (MA-A-1) by means of neutron activation analysis. Interuniv. Reactor Inst. (Delft, Netherlands), Rept. 133-77-05, pp. 1–14. Topping, G., 1973. Heavy metals in shellfish from Scottish waters. Aquaculture 1, 379–384. Tu, N.P.C., Ha, N.N., Ikemoto, T., Tuyen, B.C., Tanabe, S., Takeuchi, I., 2008. Regional variations in trace element concentrations in tissues of black tiger shrimp Penaeus monodon (decapod: penaeidae) from South Vietnam. Mar. Pollut. Bull. 57, 858–866. Tuncel, G., Ramelow, G., Balkas, T.I., 1980. Mercury in water, organisms and sediments from a section of the Mediterranean coast. Mar. Pollut. Bull. 11, 18–22. Turkmen, A., Turkmen, M., Tepe, Y., Mazlum, Y., Oymael, S., 2006. Metal concentrations in blue crab (Callinectes sapidus) and mullet (Mugil cephalus) in Iskenderun Bay, northern east Mediterranean, Turkey. Bull. Environ. Contam. Toxicol. 77, 186–193. U.S. Environmental Protection Agency (USEPA), 1980a. Ambient water quality criteria for selenium. USEPA Rep., 440/5-80-070, pp. 1–123. USEPA, 1980b. Ambient water quality criteria for copper. USEPA Rep., 440/5-80-036, pp. 1–162. USEPA, 1980c. Ambient water quality criteria for nickel. USEPA Rep., 440/5-80-060, pp. 1–206. USEPA, 1980d. Ambient water quality criteria for silver. USEPA Rep., 440/5-80-071, pp. 1–212. USEPA, 1980e. Ambient water quality criteria for zinc. USEPA Rep., 440/5-80-079, pp. 1–158. USEPA, 1985a. Ambient water quality criteria for arsenic—1984. USEPA Rep., 440/5-84-033, pp. 1–66. USEPA, 1985b. Ambient water quality criteria for lead—1984. USEPA Rep., 440/5-84-027, pp. 1–81. USEPA, 1987a. Ambient water quality criteria for selenium—1987. USEPA Rep., 440/5-87-006, pp. 1–121. USEPA, 1987b. Ambient water quality criteria for zinc—1987. USEPA Rep., 440/5-87-003, pp. 1–207. U.S. National Academy of Sciences (USNAS), 1989. Zinc. USNAS, Natl. Res. Coun., Subcomm. Zinc, Univ. Park Press, Baltimore, MD, 471 pp. U’ren, S.C., 1983. Acute toxicity of bis(tributyltin)oxide to a marine copepod. Mar. Pollut. Bull. 14, 303–306. Urrutia, C., Rudolph, A., Lermanda, M.P., Ahumada, R., 2008. Assessment of EDTA in chromium (III-VI) toxicity on marine intertidal crab (Petrolisthes laevigatus). Bull. Environ. Contam. Toxicol. 80, 1–3. Van As, D., Fourie, H.O., Vleggaar, C.M., 1973. Accumulation of certain trace elements in the marine organisms from the sea around the Cape of Good Hope. In: Radioactive Contamination of the Marine Environment. IAEA, Vienna, Austria, pp. 615–624. Van As, D., Fourie, H.O., Vleggaar, C.M., 1975. Trace element concentrations in marine organisms from the Cape West Coast. South Afr. J. Sci. 71, 151–154. Van Weerelt, M., Preifer, W.C., Fiszman, M., 1984. Uptake and release of 51Cr (VI) and 51Cr (III) by barnacles (Balanus sp.). Mar. Environ. Res. 11, 201–211. Vaskofsky, V.E., Korotchenko, O.D., Kosheleva, L.P., Levin, V.S., 1972. Arsenic in the lipid extracts of marine invertebrates. Comp. Biochem. Physiol. 41B (4), 777–784. Vattuone, G.M., Griggs, K.S., McIntyre, D.R., Littlepage, J.L., Harrison, F.L., 1976. Cadmium concentrations in rock scallops in comparison with some other species. U.S. Ener. Res. Dev. Admin, UCRL 52022, pp. 1–11. Vazquez, F.G., Sharma, V.K., Mendoza, Q.A., Hernandez, R., 2001. Metals in fish and shrimp of the Campeche Sound, Gulf of Mexico. Bull. Environ. Contam. Toxicol. 67, 756–762. Vernberg, W.B., DeCoursey, P.J., 1977. Effect of sublethal metal pollutants on the fiddler crab Uca pugilator. U.S. Environ. Protect. Agen., Rept 600/3-77-024, pp. 1–59. Vernberg, W.B., O’Hara, J., 1972. Temperature-salinity stress and mercury uptake in the fiddler crab, Uca pugilator. J. Fish. Res. Board Can. 29, 1491–1494. Vernberg, W.B., Vernberg, F.J., 1972. The synergistic effects of temperature, salinity, and mercury on survival and metabolism of the adult fiddler crab, Uca pugilator. US Dept. Comm. Fish. Bull. 70 (2), 415–420.
514 Chapter 7 Vernberg, W.B., DeCoursey, P.J., O’Hara, J., 1974. Multiple environmental factor effects on physiology and behavior of the fiddler crab, Uca pugilator. In: Vernberg, F.J., Vernberg, W.B. (Eds.), Pollution and Physiology of Marine Organisms. Academic Press, New York, pp. 381–425. Vernberg, W.B., DeCoursey, P.J., Kelly, M., Johns, D.M., 1977. Effects of sublethal concentrations of cadmium on adult Palaemonetes pugio under static and flow-through conditions. Bull. Environ. Contam. Toxicol. 17, 16–24. Verriopoulos, G., Dimas, S., 1988. Combined toxicity of copper, cadmium, zinc, lead, nickel, and chrome in the copepod Tisbe holothuriae. Bull. Environ. Contam. Toxicol. 41, 378–384. Verriopoulos, G., Hardouvelis, D., 1988. Effects of sublethal concentrations of zinc on survival and fertility in four successive generations of Tisbe. Mar. Pollut. Bull. 19, 162–166. Verriopoulos, G., Moraitu-Apostolopoulou, M., 1989. Toxicity of zinc to the marine copepod Tisbe holothuriae; the importance of the food factor. Arch. Hydrobiol. 114, 457–463. Vighi, M., Calamari, D., 1985. QSARs for organotin compounds on Daphnia magna. Chemosphere 14, 1925–1932. Vinogradova, Z.A., Koual’skiy, V.V., 1962. Elemental composition of the Black Sea plankton. Doklady Acad. Sci. USSR Earth Sci. Sec. 147, 217–219. Vos, G., Hovens, J.P.C., 1986. Chromium, nickel, copper, zinc, arsenic, selenium, cadmium, mercury and lead in Dutch fishery products 1977-1984. Sci. Total Environ. 52, 25–40. Waiwood, B.A., Zitko, V., Haya, K., Burridge, L.E., McLeese, D.W., 1987. Uptake and excretion of zinc in several tissues of the lobster (Homarus americanus). Environ. Toxicol. Chem. 6, 27–32. Waldock, R., Rees, H.L., Matthiessen, P., Pendle, M.A., 1999. Surveys of the benthic infauna of the Crouch Estuary (UK) in relation to TBT contamination. J. Mar. Biol. Assoc. UK 79, 225–232. Walker, G., 1977. “Copper” granules in the barnacle Balanus balanoides. Mar. Biol. 39, 343–349. Walker, G., Rainbow, P.S., Foster, P., Crisp, D.J., 1975a. Barnacles: Possible indicators of zinc pollution? Mar. Biol. 30, 57–65. Walker, G., Rainbow, P.S., Foster, P., Holland, D.L., 1975b. Zinc phosphate granules in tissues surrounding the midgut of the barnacle Balanus balanoides. Mar. Biol. 33, 161–166. Wang, Z., Kong, H., Wu, D., 2007a. Acute and chronic copper toxicity to a saltwater cladoceran Moina monogolica Daday. Arch. Environ. Contam. Toxicol. 53, 50–56. Wang, Z.S., Kong, H.N., Wu, D.Y., 2007b. Reproductive toxicity of dietary copper to a saltwater cladoceran, Moina monogolica Daday. Environ. Toxicol. Chem. 36, 126–131. Ward, G.S., Hollister, T.A., Heitmuller, P.T., Parrish, P.R., 1981. Acute and chronic toxicity of selenium to estuarine organisms. Northeast Gulf Sci. 4, 73–78. Ward, T.J., Correll, R.L., Anderson, R.B., 1986. Distribution of cadmium, lead and zinc amongst the marine sediments, sea grasses and fauna, and the selection of sentinel accumulators, near a lead smelter in South Australia. Aust. J. Mar. Freshw. Res. 37, 567–585. Ward, T.J., Boeri, R.L., Hogstrand, C., Kramer, J.R., Lussier, S.M., Stubblefield, W.A., et al., 2006. Influence of salinity and organic carbon on the chronic toxicity of silver to mysids (Americamysis bahia) and silversides (Menidia beryllina). Environ. Toxicol. Chem. 25, 1809–1816. Weeks, J.M., 1992. Copper-rich granules in the ventral caeca of talitrid amphipods (crustacea: amphipoda: talitridae). Ophelia 36, 119–133. Weeks, J.M., Moore, P.G., 1991. The effect of synchronous moulting on body copper and zinc concentrations in four species of talitrid amphipods (crustacea). J. Mar. Biol. Assoc. UK 71, 481–488. Weeks, J.M., Rainbow, P.S., 1991. The uptake and accumulation of zinc and copper from solution by two species of talitrid amphipods (Crustacea). J. Mar. Biol. Assoc. UK 71, 811–826. Weeks, J.M., Rainbow, P.S., 1993. The relative importance of food and seawater as sources of copper and zinc to talitrid amphipods (crustacea; amphipoda; talitridae). J. Appl. Ecol. 30, 722–735. Weimin, Y., Batley, G.E., Ahsanullah, M., 1994. Metal bioavailability to the soldier crab Mictyris longicarpus. Sci. Total Environ. 141, 27–44.
Crustaceans 515 Weis, J.S., 1978. Interactions of methylmercury, cadmium and salinity on regeneration in the fiddler crabs Uca pugilator, U. Pugnax, and U. Minax. Mar. Biol. 49, 119–124. Weis, J., 1980. Effect of zinc on regeneration in the fiddler crab Uca pugilator and its interactions with methylmercury and cadmium. Mar. Environ. Res. 3, 249–255. Weis, J.S., Kim, K., 1988. Tributyltin is a teratogen in producing deformities in limbs of the fiddler crab, Uca pugilator. Arch. Environ. Contam. Toxicol. 17, 583–587. Weis, J.S., Weis, P., 1992. Transfer of contaminants from CCA-treated lumber to aquatic biota. J. Exp. Mar. Biol. Ecol. 161, 189–199. Weis, J.S., Gottlieb, J., Kwiatkowski, J., 1987. Tributyltin retards regeneration and produces deformities of limbs in the fiddler crab, Uca pugilator. Arch. Environ. Contam. Toxicol. 16, 321–326. Welander, A.D., 1969. Distribution of radionuclides in the environment of Eniwetok and Bikini Atolls, August 1964. In: Nelson, D.J., Evans, F.C. (Eds.), Symposium on Radioecology. Proceedings of the Second National Symposium. Available as CONF-370503 from NTIS, Springfield, Virginia, pp. 346–354. Wharfe, J.R., Van Den Broek, W.L.F., 1977. Heavy metals in macroinvertebrates and fish from the lower Medway Estuary, Kent. Mar. Pollut. Bull. 8, 31–34. White, S.L., Rainbow, P.S., 1985. On the metabolic requirements for copper and zinc in molluscs and crustaceans. Mar. Environ. Res. 16, 215–229. Wieser, W., 1967. Conquering terra firma: The copper problem from the isopod’s point of view. Helg. wiss. Meeres. 15, 282–293. Wilson, K.W., Connor, P.M., 1971. The use of a continuous-flow apparatus in the study of longer-term toxicity of heavy metals. Int. Coun. Explor. Sea C.M., 1971/E8, pp. 343–347. Windom, H., Gardner, W., Stephens, J., Taylor, F., 1976. The role of methylmercury production in the transfer of mercury in a salt marsh ecosystem. Estuar. Coast. Mar. Sci. 4, 579–583. Wolfe, D.A., Cross, F.A., Jennings, C.D., 1973. The flux of Mn, Fe, and Zn in an estuarine ecosystem. In: Radioactive Contamination of the Marine Environment. IAEA, Vienna, Austria, pp. 159–175. Won, J.H., 1973. The concentrations of mercury, cadmium, lead, and copper in fish and shellfish of Korea. Bull. Korean Fish. Soc. 6, 1–19. Wong, C.K., Chu, K.H., Tang, K.W., Tam, T.W., Wong, J.L., 1993. Effects of chromium, copper and nickel on survival and feeding behavior of Metapenaeus ensis larvae and postlarvae (Decapoda: Penaeidae). Mar. Environ. Res. 36, 63–78. World Health Organization (WHO), 1980. Tin and organotin compounds: A preliminary review. Environ. Health Crit. 15, 1–109. Wrench, J., Fowler, S.W., Unlu, M.Y., 1979. Arsenic metabolism in a marine food chain. Mar. Pollut. Bull. 10, 18–20. Wright, D.A., 1976. Heavy metals in animals from the north east coast. Mar. Pollut. Bull. 7, 36–38. Wright, D.A., 1977a. The uptake of cadmium into the haemolymph of the shore crab Carcinus maenas: The relationship with copper and other divalent cations. J. Exp. Biol. 67, 147–161. Wright, D.A., 1977b. The effect of salinity on cadmium uptake by the tissues of the shore crab Carcinus maenas. J. Exp. Biol. 67, 136–146. Wright, D.A., 1977c. The effect of calcium on cadmium uptake by the shore crab Carcinus maenas. J. Exp. Biol. 67, 163–173. Wright, D.A., Brewer, C.C., 1979. Cadmium turnover in the shore crab Carcinus maenas. Mar. Biol. 50, 151–156. Yang, Z.B., Zhao, Y.L., Li, N., Yang, J., 2007. Effect of waterborne copper on the microstructures of gill and hepatopancreas in Eriocheir sinensis and its induction of metallothionein synthesis. Arch. Environ. Contam. Toxicol. 52, 222–228. Yang, Z.B., Zhao, Y.L., Li, N., Yang, J., 2008. Effect of waterborne copper on the microstructures and ultrastructure of the X-organ sinus gland complex in Eriocheir sinensis. Bull. Environ. Contam. Toxicol. 80, 68–73. Yannai, S., Sachs, K., 1978. Mercury compounds in some eastern Mediterranean fishes, invertebrates, and their habitats. Environ. Res. 16, 408–418.
516 Chapter 7 Yoshinari, T., Subramanian, V., 1976. Adsorption of metals by chitin. In: Nriagu, J.O. (Ed.), Environmental Biogeochemistry: Vol. 2. Metals Transfer and Ecological Mass Balances. Ann Arbor Science Publishers, Ann Arbor, MI, pp. 542–555. Zafiropoulos, D., Grimanis, A.P., 1977. Trace elements in Acartia clausi from Elefsis Bay of the upper Saronikos Gulf, Greece. Mar. Pollut. Bull. 8, 79–81. Zauke, G.P., 1977. Mercury in benthic invertebrates of the Elbe estuary. Helgol. Wiss. Meers. 19, 358–374. Zauke, G.P., Schmalenbach, I., 2006. Heavy metals in zooplankton and decapod crustaceans from the Barents Sea. Sci. Total Environ. 359, 283–294. Zingde, M.D., Singbal, S.Y.S., Moraes, C.F., Reddy, C.V.G., 1976. Arsenic, copper, zinc, and manganese in the marine flora and fauna of coastal and estuarine waters around Goa. Indian J. Mar. Sci. 5, 212–217. Zodle, B., Whitman, K.J., 2003. Effects of sampling, preparation and defecation on metal concentrations in selected invertebrates at urban sites. Chemosphere 52, 1095–1103. Zuckerman, J.J., Reisdorf, R.P., Ellis III, H.V., Wilkinson, R.R., 1978. Organotins in biology and the environment. In: Brinckman, F.E., Bellama, J.M. (Eds.), Organometals and Organometalloids, Occurrence and Fate in the Environment. Amer. Chem. Soc. Sympos. Series 82. American Chemical Society, Washington, DC, pp. 388–424. Zumholz, K., Hansteen, T.H., Klugel, A., Piatkowski, U., 2006. Food effects on statolith composition of the common cuttlefish (Sepia officinalis). Mar. Biol. 150, 237–244.
CHAPTER 8
Insects Sea-skaters of the genus Halobates are the only known insects found in the open ocean and the only marine invertebrates which live exclusively at the air-water interface. Other marine insects, including flies, occupy inshore niches. Attempts have been made to relate environmental contamination with concentrations of cadmium and other trace metals in marine insects; however, data are insufficient to warrant firm conclusions. Variables known to influence metal concentrations in marine insects include life stage and gender (Table 8.1).
8.1 Cadmium Mean cadmium concentrations in whole Halobates spp. ranged from 6.0 to 152.0 mg Cd/kg DW (dry weight), although maxima as high as 309.0 mg Cd/kg DW are recorded (Table 8.1). Halobates can accumulate cadmium from diet as well as from the medium; however, diet was less important as a route than the medium, in this case the surface microlayers (Cheng et al., 1979). Since these insects normally feed on fluidized soft tissues of prey zooplankton, it was probable that the high concentrations of cadmium and other metals in zooplankton exoskeletons were not biologically available. Halobates, in turn, are preyed upon by at least two species of Pacific seabirds (Bull et al., 1977), but transfer rates are unknown. Laboratory studies with Halobates robustus and radiocadmium demonstrate cadmium accumulation in tissues, but levels were below those in the ambient medium (Schulz-Baldes and Cheng, 1979). It was concluded that cadmium was incorporated into body tissues, not merely adsorbed onto surfaces. Uptake, as well as depuration, followed a biphasic pattern, with the biological half-life of cadmium ranging from 0.6 h to 19.7 days for uptake into the first compartment, and depuration in the second compartment, respectively (Schulz-Baldes and Cheng, 1979), suggesting that the chemical form or site of bound cadmium had changed.
8.2 Chromium Mean chromium concentrations in H. robustus ranged from 1.0 to 3.0 mg Cr/kg DW, being highest in females, lowest in males, and intermediate in nymphs (Table 8.1).
517
518 Chapter 8 Table 8.1: Trace Element Concentrations in Field Collections of Marine Insects Element and Organism
Value
Reference
a
Cadmium Halobates micans; whole
22.7 (0.0-309.0) DW
1
Halobates robustus; whole Males Females Nymphs
6.0 DW 8.0 DW 7.0 DW
2 2 2
Halobates sericeus; whole
40.0 DW
3
Halobates sobrinus; whole
152.0 DW
3
Marine flies; whole; 2 spp.
40.0-150.0 DW
4
Rheumobates aestuarius; whole
>5.0 DW
3
1.0 DW 3.0 DW 2.0 DW
2 2 2
Halobates robustus; whole Males Females Nymphs
129.4 DW 162.3 DW 134.6 DW
2 2 2
Halobates sericeus; whole
45.0 DW
3
Halobates sobrinus; whole
50.0 DW
3
Marine flies; whole; 2 spp.
10.0-125.0 DW
4
Rheumobates aestuarius; whole
64.0 DW
3
Halobates sericeus; whole
178.0 DW
3
Halobates sobrinus; whole
289.0 DW
3
Marine flies; whole; 2 spp.
100.0-225.0 DW
4
Rheumobates aestuarius; whole
204.0 DW
3
Chromium Halobates robustus; whole Males Females Nymphs Copper
Iron
(Continues)
Insects 519 Table 8.1: Element and Organism
Cont’d
Value
Reference
a
Lead Halobates robustus; whole Males Females Nymphs
<1.0 DW <1.0 DW <1.0 DW
2 2
Halobates sericeus; whole
7.0 DW
3
Halobates sobrinus; whole
10.0 DW
3
Rheumobates aestuarius; whole
>2.0 DW
3
<10.0 DW
4
Halobates sericeus; whole
7.0 DW
3
Halobates sobrinus; whole
18.0 DW
3
Rheumobates aestuarius; whole
6.0 DW
3
Halobates robustus; whole Males Females Nymphs
115.4 DW 145.7 DW 109.8 DW
2 2 2
Halobates sericeus; whole
176.0 DW
3
Halobates sobrinus; whole
176.0 DW
3
Marine flies; whole; 2 spp.
150.0 to >300.0 DW
4
Rheumobates aestuarius; whole
197.0 DW
3
Manganese Marine flies; whole; 2 spp. Nickel
Zinc
Values are in mg element/kg dry weight (DW). a 1, Bull et al., 1977; 2, Cheng et al., 1979; 3, Cheng et al., 1976; 4, Bender, 1975.
8.3 Copper The highest mean copper concentration on record for marine insects is 162.3 mg Cu/kg DW whole female H. robustus (Table 8.1).
520 Chapter 8
8.4 Iron Mean iron concentrations in whole marine insects ranged from 100.0 to 289.0 mg Fe/kg DW (Table 8.1).
8.5 Lead The highest lead concentration recorded is 10.0 mg Pb/kg DW in whole Halobates sobrinus (Table 8.1).
8.6 Manganese A single datum is available for manganese, being less than 10.0 mg Mn/kg DW whole fly (Table 8.1).
8.7 Nickel Mean nickel concentrations in three species of marine insects ranged from 6.0 to 18.0 mg Ni/kg DW whole organism (Table 8.1).
8.8 Zinc Mean zinc concentrations in a variety of marine insects ranged from a low of 109.8 mg Zn/kg DW in whole H. robustus nymphs to >300.0 mg Zn/kg DW in whole marine flies (Table 8.1).
8.9 Literature Cited Bender, J.A., 1975. Trace metal levels in beach dipterans and amphipods. Bull. Environ. Contam. Toxicol. 14, 187–192. Bull, K.E., Murton, R.K., Osborn, D., Ward, P., Cheng, L., 1977. High levels of cadmium in Atlantic seabirds and sea-skaters. Nature 269, 507–509. Cheng, L., Alexander, G.V., Franco, P.J., 1976. Cadmium and other heavy metals in seaskaters (Gerridae: Halobates, Rheumobates). Water Air Soil Pollut. 6, 33–38. Cheng, L.P., Franco, P.J., Schulz-Baldes, M., 1979. Heavy metals in the sea-skater Halobates robustus from the Galapagos Islands: Concentrations in nature and uptake experiments with special reference to cadmium. Mar. Biol. 54, 201–206. Schulz-Baldes, M., Cheng, L., 1979. Uptake and loss of radioactive cadmium by the sea-skater Halobates robustus (Heteroptera: Gerridae). Mar. Biol. 52, 253–258.
CHAPTER 9
Chaetognaths The phylum Chaetognatha is a small group of pelagic, mostly oceanic, invertebrates consisting of about 50 species. The most studied genus is Sagitta with about 30 species. Chaetognaths seldom exceed 3 cm in length and each contains a distinct head, trunk, and tail region. Typically, the head contains a pair of eyes and two pairs of sickle-shaped setae, the body a pair of lateral fins, and the tail a lateral caudal fin. These hermaphroditic carnivores frequently occur in large schools and are preyed upon by pelagic fishes; in turn, they readily devour fish fry, some as large as themselves. Most of what is known about trace metal composition of chaetognaths is based upon analysis of collections from three different geographic locales: the mid-Pacific Ocean (Nicholls et al., 1959); the Black Sea (Vinogradova and Koual’skiy, 1962); and Strathcona Sound, Baffin Island, near the Arctic Circle (Bohn and McElroy, 1976). A strict comparison between locales was not possible for several reasons. First, the observations of Vinogradova and Koual’skiy (1962) represent maximum values recorded, whereas those of Nicholls et al. (1959) and Bohn and McElroy (1976) are means. Second, different species were collected from different areas with no species in common; it is probable that closely related species of chaetognaths differ substantially in their ability to accumulate trace metals, as is the case for other phyla. Finally, different analytical techniques were used including atomic absorption spectrophotometry and emission spectrographic analysis, as well as different sample preparation techniques. Until these and other sample preparation techniques and methodologies are cross-validated by interlaboratory comparisons, there will always be some doubt regarding the accuracy and precision of elemental data in chaetognaths and other groups.
9.1 Arsenic Chaetognaths collected near the Arctic circle contain 7.5-7.7 mg As/kg DW (Table 9.1).
9.2 Barium The single datum available shows that Sagitta sp. from the Black Sea contain up to 1500.0 mg Ba/kg AW (Table 9.1).
521
522 Chapter 9 Table 9.1: Trace Element Concentrations in Field Collections of Chaetognaths Element and Organism
Concentration
Reference
a
Arsenic Chaetognaths
7.5-7.7 DW
1
1500.0 AW
2
130.0 AW
3
Chaetognaths
1.2-1.3 DW
1
Eukronia hamata Barents Sea Greenland Sea
0.8 DW 1.1 DW
4 5
Sagitta elegans
<1.0 AW
3
Sagitta sp.
80.0 AW
2
110.0 AW
3
Chaetognaths
(5.6-6.3) DW
1
Eukronia hamata Barents Sea Greenland Sea
4.0 DW 3.0 DW
4 5
Sagitta elegans
1100.0 AW
3
Sagitta sp.
30,000.0 AW
2
10.0 AW
2
Chaetognaths
(32.0-33.0) DW
1
Sagitta sp.
100,000.0 AW
2
Barium Sagitta sp. Boron Sagitta elegans Cadmium
Chromium
Cobalt Sagitta elegans Copper
Gallium Sagitta sp. Iron
(Continues)
Chaetognaths 523 Table 9.1: Element and Organism
Concentration
Cont’d Reference
a
Lead Eukronia hamata; Greenland Sea
<0.3 DW
5
Sagitta elegans
300.0 AW
3
Sagitta sp.
1500.0 AW
2
500.0 AW
2
3.0 AW
3
Sagitta elegans
480.0 AW
3
Sagitta sp.
300.0 AW
2
60.0 AW
2
1500.0 AW
2
Sagitta elegans
20.0 AW
3
Sagitta sp.
400.0 AW
2
Sagitta elegans
3.0 AW
3
Sagitta sp.
500.0 AW
2
Sagitta elegans
13.0 AW
3
Sagitta sp.
20.0 AW
2
Chaetognaths; Arctic Circle
76.0-90.0 DW
1
Eukronia hamata Barents Sea Greenland Sea
124.0 DW 69.0 DW
4 5
Lithium Sagitta sp. Molybdenum Sagitta elegans Nickel
Silver Sagitta sp. Strontium Sagitta sp. Tin
Titanium
Vanadium
Zinc
(Continues)
524 Chapter 9 Table 9.1:
Cont’d
Element and Organism
Concentration
Reference
Sagitta sp.
20,000.0 AW
2
70.0 AW
2
a
Zirconium Sagitta sp.
Values are in mg element/kg whole organism dry weight (DW), or ash weight (AW). a 1, Bohn and McElroy, 1976; 2, Vinogradova and Koual’skiy, 1962; 3, Nicholls et al., 1959; 4, Zauke and Schmalenbach, 2006; 5, Ritterhoff and Zauke, 1997.
9.3 Boron The single datum available shows that Sagitta elegans from the mid-Pacific Ocean contain 130.0 mg B/kg AW (Table 9.1).
9.4 Cadmium Chaetognaths from the Arctic Circle contain 1.2-1.3 mg Cd/kg DW; concentrations in chaetognaths from the Barents Sea are 0.8 mg Cd/kg DW, and for those from the Greenland Sea it is 1.1 mg Cd/kg DW (Table 9.1).
9.5 Chromium Sagitta spp. contain up to 80.0 mg Cr/kg AW (Table 9.1).
9.6 Cobalt S. elegans from the mid-Pacific Ocean contain 110.0 mg Co/kg AW (Table 9.1). Ketchum and Bowen (1958) report that Sagitta sp. can concentrate cobalt isotopes from seawater by a factor of 1000. Sagitta enflata eliminates radiocobalt at the rate of 11%/h (Kuenzler, 1969).
9.7 Copper The highest copper concentrations recorded in field collections of chaetognaths were 6.3 mg Cu/kg on a DW (dry weight) basis, and 30,000.0 mg Cu/kg on an AW (ash weight) basis (Table 9.1).
9.8 Gallium Sagitta sp. from the Black Sea contain up to 10.0 mg Ga/kg AW (Table 9.1).
Chaetognaths 525
9.9 Iron Chaetognaths near the Arctic Circle contain 32.0-33.0 mg Fe/kg DW, and Sagitta sp. from the Black Sea contain up to 100,000.0 mg Fe/kg AW (Table 9.1). Iron isotopes in seawater are accumulated by Sagitta sp. by a factor approaching 5000 (Ketchum and Bowen, 1958). Much of the radioiron eliminated by S. enflata was particulate, with significant amounts nonexchangeable, that is, not biologically available (Kuenzler, 1969).
9.10 Lead Chaetognaths from the mid-Pacific Ocean contain 300.0 mg Pb/kg AW and those from the Black Sea contain up to 1500.0 mg Pb/kg AW (Table 9.1).
9.11 Lithium Chaetognaths from the Black Sea contain up to 500.0 mg Li/kg AW (Table 9.1).
9.12 Molybdenum The single datum available indicates that S. elegans from the mid-Pacific Ocean contain an average of 3.0 mg Mo/kg AW (Table 9.1).
9.13 Nickel Sagitta spp. from two locales contain 300.0 to 480.0 mg Ni/kg AW (Table 9.1).
9.14 Silver Sagitta sp. from the Black Sea contain up to 60.0 mg Ag/kg AW (Table 9.1).
9.15 Strontium Sagitta sp. from the Black Sea contain up to 1500.0 mg Sr/kg AW whole organism (Table 9.1). Sagitta sp. can accumulate strontium isotopes from seawater by a factor of 70 (Ketchum and Bowen, 1958).
9.16 Tin The maximum mean tin concentration recorded in field collections of chaetognaths is 400.0 mg Sn/kg AW (Table 9.1).
526 Chapter 9
9.17 Titanium Sagitta spp. from two locales contained 3.0-500.0 mg Ti/kg AW (Table 9.1). The role of titanium in crustacean metabolism is unknown.
9.18 Vanadium Sagitta spp. from two locales contained between 13.0 and 20.0 mg V/kg AW (Table 9.1).
9.19 Zinc Chaetognaths collected near the Arctic Circle contain an average of 76.0-90.0 mg Zn/kg dry weight; Sagitta sp. from the Black Sea had a maximum of 20,000.0 mg Zn/kg AW, and Eukronia hamata contained 69.0-124.0 mg Zn/kg DW (Table 9.1). Radiozinc is eliminated from S. enflata at a rate of 3%/h (Kuenzler, 1969).
9.20 Zirconium Sagitta sp. from the Black Sea contain up to 70.0 mg Zr/kg AW (Table 9.1).
9.21 Literature Cited Bohn, A., McElroy, R.O., 1976. Trace metals (As, Cd, Cu, Fe, and Zn) in Arctic cod, Boreogadus saida, and selected zooplankton from Strathcona Sound, Northern Baffin Island. J. Fish. Res. Board Can. 33, 2836–2840. Ketchum, B.M., Bowen, V.T., 1958. Biological factors determining the distribution of radioisotopes in the sea. In: Proceedings of the Second Annual United Nations Conference on Peaceful Uses of Atomic Energy, Vol. 18, Geneva, pp. 429–433. Kuenzler, E.J., 1969. Elimination and transport of cobalt by marine zooplankton. In: Proceedings of the 2nd National Symposium on Radioecology. U.S. Atom. Ener. Comm. Conf. 670503, pp. 483–492. Nicholls, G.D., Curl Jr., H., Bowen, V.T., 1959. Spectrographic analyses of marine plankton. Limnol. Oceanol. 4, 472–476. Ritterhoff, J., Zauke, G.P., 1997. Trace metals in field samples of zooplankton from the Fram Strait and the Greenland Sea. Sci. Total Environ. 199, 255–270. Vinogradova, Z.A., Koual’skiy, V.V., 1962. Elemental composition of the Black Sea plankton. Doklady Acad. Sci. USSR Earth Sci. Sec. 147, 217–219. Zauke, G.P., Schmalenbach, I., 2006. Heavy metals in zooplankton and decapod crustaceans from the Barents Sea. Sci. Total Environ. 359, 283–294.
CHAPTER 10
Annelids This phylum of segmented worms includes earthworms and leeches as well as a large number of free-living or tube-building species belonging to the class Polychaeta. The name Polychaeta refers to the numerous tufts of setae at the sides of the body. Class Polychaeta is the largest in this phylum with more than 10,000 species recorded, and widely distributed in marine habitats—although some species are found in brackish and fresh water and in moist earth. Polychaetes are most common in coastal zones of all oceans in depths up to 600 m, but some have been recorded from the abyss. Several groups of polychaetes are dominant in tropical ecosystems, others in frigid waters, and many others with limited geographic ranges. Some are entirely pelagic, but others are pelagic only through larval stages. Some are mainly sand dwelling and others rock borers, some commensal and a few parasitic. Polychaetes are used extensively by several investigators as indicators of metal-contaminated sediments and as experimental animals to assess the comparative toxicity and physiological effects of metals and metalloids.
10.1 Aluminum The polychaete Branchipolynoe seepensis, a commensal parasite on gills of a hydrothermal vent mussel, Bathymodiolus azoricus, contained 11.9 mg Al/kg DW (dry weight) whole animal (Kadar et al., 2006). Eggs of Hydroides elegans were subjected to various concentrations of aluminum from fertilization through the 24 h trocophore stage. Arrested development was evident at 1.1 mg Al/L for the 2 h blastula, and at 0.21 mg Al/L for trocophore larvae (Gopalakrishnan et al., 2007).
10.2 Americium Beasley and Fowler (1976) report that americium concentrations in whole sandworms, Nereis diversicolor, reflect sediment americium concentrations; Nereis contain about 0.5% of the americium burden of the surrounding sediments.
527
528 Chapter 10
10.3 Antimony Limited data indicate that whole-body concentrations in field populations of polychaetes do not exceed 0.03 mg Sb/kg DW (Table 10.1).
10.4 Arsenic Arsenic appears to concentrate in lipids, reaching 46,000.0 mg As/kg extract on a fresh weight (FW) basis (Table 10.1). The Mediterranean fan worm, Sabella spallanzanii, normally contains about 1400.0 mg As/ kg DW in branchial crowns and about 30.0 mg As/kg DW in body portions, including high levels (84%) of dimethylarsinic acid (DMA), a relatively toxic compound with a possible antipredatory role (Notti et al., 2007). Sabella exposed under laboratory conditions to arsenate (0.02 mg As/L), DMA (0.06 mg As/L), trimethylarsine (TMA; 0.06 mg As/L), Table 10.1: Antimony, Arsenic, Barium, and Cadmium Concentrations in Field Collections of Annelids Element and Organism
Concentration
Reference
a
Antimony Sandworm, Nereis diversicolor; whole
0.03 DW
1
Polychaete, Chaetopterus variopedatus; lipid extract
46,000.0 FW
2
Sandworm, Nereis diversicolor; whole
5.2 DW
1
0.16 FW
3
13.6 DW
7
Polychaete, Nephtys hombergi; whole March October
9.0 FW 89.0 FW
4 4
Sandworm, Nereis diversicolor; whole
0.53 (0.08-3.6) FW
5, 6
Arsenic
Barium Annelids Cadmium Polychaete, Branchipolynoe seepensis; from gill of deep-sea-hydrothermal vent mussel; 2002; whole
Values are in mg element/kg fresh weight (FW) or dry weight (DW). a 1, Leatherland and Burton, 1974; 2, Vaskovsky et al., 1972; 3, Mauchline and Templeton, 1966; 5, Rosenberg, 1977; 5, Bryan and Hummerstone, 1973b; 6, Bryan and Hummerstone, 1977; 7, Kadar et al., 2006.
Annelids 529 or arsenobetaine (0.06 mg As/L) for 20 days showed the highest increases in branchial crowns treated with arsenate, lower increases with DMA and TMA, and no increase of arsenobetaine. Accumulated arsenic, except for arsenobetaine, could be chemically transformed to DMA, accounting for the elevated DMA levels typical of this species (Notti et al., 2007). Water-soluble arsenic compounds in the polychaete Arenicola marina from Odense Fjord, Denmark differ significantly from most other marine animals in that arsenobetaine was present only as a minor (6%) constituent (Geiszinger et al., 2002). Water-soluble inorganic forms included arsenite (58%) and arsenate (16%). Other arsenic compounds were dimethylarsinate (4%), two arsenosugars (at 1% and 3%, respectively), tetramethylarsonium ion (1.5%), arsenocholine (<1%), trimethylarsoniopropionate (<1%), and an unknown anionic arsenical (ca. 10%). Polychaetes subjected to 0.01-1.0 mg As/L, as arsenate, in the laboratory took up arsenic in a dose-dependent nonlinear manner. There were no deaths during the 12 day exposure, and the highest whole-body concentration of 270.0 mg As/kg DW was recorded at 1.0 mg As/L. Most of the accumulated arsenic was biotransformed to arsenite and dimethylarsinate, with the rest being accumulated as unchanged arsenate. Other arsenic compounds found in A. marina did not increase as a result of arsenate exposure (Geiszinger et al., 2002).
10.5 Barium Barium concentrations in whole annelids average 0.16 mg Ba/kg FW (Table 10.1).
10.6 Cadmium The abnormally high concentration of 89.0 mg Cd/kg FW whole Nephtys hombergi (Table 10.1) is attributed to contamination from sediments as a result of dredging operations (Rosenberg, 1977). Cadmium resistance has been documented in marine annelids (Wallace et al., 1998). Oligochaetes (Limnodrilus hoffmeisteri) from Foundry Cove, New York—a severely cadmium-contaminated site—were more tolerant of cadmium than conspecifics from a reference site, surviving twice as long in a 7 day acute toxicity study (1.0 mg Cd/L) and with bioconcentration factors of 2020 versus 577 for the controls (radiocadmium-109). The cadmium-resistant worms produced metal-rich granules and metallothioneins for cadmium storage and detoxification, whereas nonresistant worms only produced metallothioneins. Grass shrimp (Palaemonetes pugio) fed with cadmium-resistant worms absorbed 21% of the ingested cadmium versus 75% for shrimp fed with nonresistant worms (Wallace et al., 1998). Settling organic matter is a major food source for heterotrophic benthic fauna (Thorsson et al., 2008). In one study, the polychaete Marenzellaria spp. fed with 109Cd-labeled green microalgae, Tetraselmis spp. for 34 days had a whole-body concentration factor of 12 over
530 Chapter 10 the diet (Thorsson et al., 2008). Uptake and retention of radiocadmium by a polychaete, Eunice sp., was studied (Alquezar et al., 2007). In that study Eunice was held for 385 h in seawater spiked with 109Cd followed by 189 h in 109Cd-free media. During uptake, radiocadmium was concentrated by a factor of 41 over seawater; during depuration 62% was lost. A biphasic depuration pattern was evident: the biological half-life of the short-lived component was 11 h, and for the long-lived component it was 5950 h (Alquezar et al., 2007). Cadmium interacts with zinc (Goto and Wallace, 2007). Polychaetes, Capitella capitata were coexposed to 0.05 mg Cd/L plus 0.086 mg Zn/L with 109Cd and 65Zn radiotracers for 1 week, followed by depuration for 1 week. Uptake and loss of cadmium and zinc were similar, with worms depurating most of the cadmium (75%) and zinc (64%). Cadmium and zinc behaved similarly at the subcellular level; worms partitioned most of the cadmium (65%) and zinc (55%) to the heat stable proteins and organelles fraction. The heat denaturable proteins and metal-rich granules contained less than 6% of both metals. Authors conclude that cadmium-zinc interactions reduce partitioning of cadmium and zinc to heat stable proteins, indicating that metallothioneins and other metal-binding proteins are key to these interactions (Goto and Wallace, 2007). Cadmium also interacts with petroleum hydrocarbons (Sun and Zhou, 2007). A polychaete, Hediste japonica, exposed to 0.5 mg Cd/L or to 0.5 mg Cd/L plus 0.1 mg petroleum hydrocarbons/L for 3 days had BCF values of 25 for cadmium alone and 81 for the mixture, indicating significant interaction. Net accumulation rates, in mg Cd/kg body weight daily, were 4.3 for cadmium alone and 8.5 for the mixture (Sun and Zhou, 2007). Three laboratory studies with Nereis spp. and cadmium are of interest. Ueda et al. (1976) found that Nereis japonica, when compared to controls, contained six times more cadmium when subjected to cadmium-contaminated sediments for 8 days, and up to 200 times more cadmium from cadmium-containing seawater in a similar period; they concluded that the main cadmium uptake route for this species is via the medium. N. japonica excreted the accumulated cadmium in multicompartmental phases: the major short-lived component had a computed biological half-life of 4 days. In a second study, Nereis virens of 1-2 g in weight, immersed in seawater containing 0.03 mg Cd/L for 14 days, accumulated cadmium at the rate of 0.01 mg Cd/kg DW whole animal per hour, with a final concentration of 7.5 mg Cd/kg DW whole worm (Ray et al., 1980). At a seawater concentration of 9.2 mg Cd/L, these values were 2.127 mg Cd/kg DW/h and a final whole-body content of 755.5 mg Cd/kg DW. Intermediate values were obtained with seawater cadmium concentrations of 0.09, 0.90, 1.90, and 4.4 mg/L. When the study was repeated with larger worms of 5-7 g wet weight, similar— but slightly lower—values were obtained in each case (Ray et al., 1980). Further studies indicated that cadmium uptake by N. virens is primarily from the aqueous phase rather than from cadmium-laden sediments (Ray et al., 1980). In the third study, Bryan and Hummerstone (1973b) demonstrated that survival and cadmium accumulation rates over a 17 day period for N. diversicolor was related to the organism’s previous history of exposure to cadmium. Nereids from a low-cadmium sediment environment of 0.22 mg Cd/kg DW
Annelids 531 had shorter survival times, higher daily absorption rates, and higher whole-body concentrations at any given cadmium concentration in the medium than did nereids from a high-cadmium sediment environment of 3.1 mg Cd/kg DW. At 1.0 mg Cd/L, for example, N. diversicolor from the low-cadmium sediment environment had a daily absorption rate of 6.0 mg Cd/kg on a DW basis and a final concentration of 208.0 mg Cd/kg whole-body DW after 17 days; at 10.0 mg Cd/L, these values were 55.0 and 1860.0, respectively. Nereids from the high-cadmium sediment environment, when held in 1.0 mg Cd/L, had a daily absorption rate of only 4.0 mg Cd/kg whole-body DW and a final whole-body content of 140.0 mg Cd/kg DW; at 10.0 mg Cd/L, these values were 18.0 and 629.0, respectively. This pattern held at all cadmium concentrations tested, namely, 1.0, 2.5, 10.0, 25.0, and 100.0 mg Cd/L. Bryan and Hummerstone (1973b) suggest that long-time contamination from mining operations produced the elevated levels of cadmium in sediments, and that the polychaete populations from this area could withstand metals-induced stress to a higher degree than polychaete populations from less-contaminated areas. It is not known if differences between the two populations of nereids are genetic or the result of physiological adaptation. Bryan and Hummerstone (1973b) state that cadmium is not regulated by worms, and the resultant body concentrations appear to reflect sediment cadmium burdens. A study with glycerid polychaetes showed that bloodworms, Glycera dibranchiata, accumulate cadmium through the body surface and the intestine (Rice and Chien, 1979). Cadmium absorbed through the gut bound rapidly to coelomic proteins, including hemoglobin. Ionic cadmium injected into the coelom at 7.0 mg Cd/L increased proline incorporation rates into hemoglobin by a factor of 15 in 72 h (Rice and Chien, 1979), and this may adversely affect survival over time. Sandrini et al. (2006) exposed the polychaete Laeonereis acuta to 0.1 mg Cd/L for up to 24 h. After 12 h, the mean whole-body cadmium content was 1.0 mg Cd/kg DW; after 24 h, it was about 2.3 mg Cd/kg DW. Cadmium was stored mainly in the cytosolic fractions. Cadmium generates oxidative stress in Laeonereis as indicated by altered enzyme activity (Sandrini et al., 2006). Polychaetes, Perinereis aibuhitensis, exposed to 0.05 mg Cd/L for 1 week contained 0.35 mg Cd/kg FW versus 0.04 mg Cd/kg FW for controls (Ng et al., 2008). However, cadmium exposure did not affect overall cadmium uptake rates, efflux rates, and metallothionein concentrations. During exposure, cadmium concentrations increased in the cytosolic fraction of Perinereis; it also increased during depuration, suggesting that the insoluble fraction of cadmium was lost at a faster rate than cytosolic cadmium (Ng et al., 2008). Embryos and sperm of the polychaete H. elegans were the two most sensitive stages to cadmium insult with toxic effects apparent to sperm at 0.09 mg Cd/L (20 min exposure) and 0.18 mg Cd/L to embryos (2 h exposure); by contrast, the LC-50 (96 h) value for adults was 0.23 mg Cd/L (Gopalakrishnan et al., 2008). To protect annelids and other marine benthos against acute cadmium intoxication, a maximum water concentration of 0.023 mg Cd/L is recommended; however, to protect against chronic cadmium poisoning, a water concentration
532 Chapter 10 of <0.00025 mg Cd/L is recommended (Hall et al., 1998). Eisler (2000) states that seawater concentrations in excess of 0.0045 mg Cd/L should be considered potentially hazardous to marine life until additional data prove otherwise.
10.7 Cesium The principal isotope of radiocesium found in the muscle of juvenile flounders, Pleuronectes platessa, was 137Cs; the major source of cesium to Pleuronectes was diet, especially the N. hombergi fraction of the diet, despite its relatively low 137Cs content (Pentreath and Jefferies, 1971). Some evidence exists demonstrating that various species of polychaetes accumulate 137Cs from the surrounding geophysical environment. Ueda et al. (1977) report a concentration factor of 6 after 11 days by N. japonica for 137Cs; Bryan (1963) found that N. diversicolor also had a sixfold accumulation factor and that Perinereis sp. had a whole-body concentration factor of 7.5, with individual Perinereis tissues showing concentration factors of 11.2 for pharynx, 12.2 for body wall, and 13.2 for gut.
10.8 Chromium The highest concentration of chromium in field collections of annelids is 38.0 mg Cr/kg DW whole organism from urban coastal areas considered grossly contaminated by metals wastes (Table 10.2; Phelps et al., 1975). Chipman (1967) conducted laboratory studies on uptake and excretion of Cr3+ and Cr6+ by Hermione hystrix. It was determined that trivalent chromium was not readily accumulated by Hermione when present in seawater owing to the formation of particles and adsorption to the surface; moreover, little accumulation of Cr3+ was evident on contact with contaminated sediments. In the case of Cr6+ in the medium, however, Cr6+ was readily accumulated by Hermione; the process was slow and only small amounts (0.01-0.03 mg Cr6+/kg FW whole organism) was taken up from media containing 0.003-0.01 mg Cr6+/L over a period of 19 days. Higher body burdens of 0.49-1.1 mg Cr/kg fresh body weight were reported at 0.10.5 mg Cr6+/L, but some deaths were noted at these concentrations. Chromium accumulation by Hermione is a passive process and directly related to Cr6+ concentration of the medium. At least two rates of biological loss are involved, one of 8 days, another of 123 days. Chipman (1967) concluded that the greater part of chromium accumulated by Hermione from a long exposure would be bound in a body component having a slow turnover rate with an estimated biological half-life of 123 days. Uptake of Cr6+ from seawater is recorded for Neanthes arenaceodentata. Whole Neanthes contained 30.0 mg Cr/kg DW after exposure for 150 days in 0.03 mg Cr/L (Mearns and Young, 1977) and 0.5-1.6 mg Cr/kg FW following immersion for 440 days (Oshida et al., 1976); both of these observations are similar to those of Chipman (1967) after correction for wet/DWs.
Annelids 533 Table 10.2: Chromium, Cobalt, and Copper Concentrations in Field Collections of Annelids Element and Organism
Concentration
Reference
a
Chromium Polychaetes; 3 spp.; whole
8.1-14.7 DW; 16.9-20.0 FW
1, 3
Sandworm, Nereis diversicolor; whole
0.55 (<0.1-2.4) DW
2
Polychaetes; whole
23.8-38.0 DW
4
Cobalt Polychaete, Branchipolynoe seepensis; from gill of deep-sea mussel; 2002; whole
0.7 DW
Sandworm, Nereis diversicolor; whole
4.7 (1.6-7.9) DW
12
2
Copper Polychaete, Branchipolynoe seepensis; mid-Atlantic Ridge; hydrothermal vent field; whole; 2001 1700 m deep 2300 m deep
29.0 DW 45.0 DW
Bloodworm, Glycera gigantea Jaws Whole
14,340.0-16,320.0 DW 43.0-60.0 DW
13 13 5 5
Polychaetes; lugworm; whole; Wales, coastal areas; 1989
3.9 FW
11
Polychaete, Lycastis ouanaryensis; whole; India; 1984-1985; contaminated site vs. reference site
32.0-95.0 DW vs. 4.0-27.0 DW
10
Polychaete, Neanthes arenaceodentata; whole; held for 85 days on various sediment types No sediments Sand Sand-mud mixture Mud
31.6 DW 25.1 DW 23.3 DW 18.7 DW
6 6 6 6
Sandworm, Nereis diversicolor Jaws Basal section jaws Distal section jaws Whole Whole
10.0 DW 2.0 DW 15.0 DW 44.0 (22.0-78.0) DW 1.6-5.1 FW
7 7 7 2 8 (Continues)
534 Chapter 10 Table 10.2: Cont’d Element and Organism Whole Parapodia Body wall Gut Segment
Concentration 28.0-1142.0 DW 779.0-902.0 DW 48.0-543.0 DW 1678.0-1980.0 DW 494.0-638.0 DW
Reference
a
9 9 9 9 9
Values are in mg element/kg fresh weight (FW) or dry weight (DW). a 1, Bernhard and Zattera, 1975; 2, Bryan and Hummerstone, 1977; 3, Fukai and Broquet, 1965; 4, Phelps et al., 1975; 5, Gibbs and Bryan, 1980; 6, Pesch, 1979; 7, Bryan and Gibbs, 1979; 8, Wharfe and Van Den Broek, 1977; 9, Bryan and Hummerstone, 1971; 10, Athalye and Gokhole, 1991; 11, Morris et al., 1989; 12, Kadar et al., 2006; 13, Colaco et al., 2006.
Concentrations as low as 0.0125 mg Cr6+/L can decrease brood size in N. arenaceodentata (Mearns et al., 1976; Oshida et al., 1976), although chromium body burdens in experimental subjects were the same as in controls. Uptake of Cr6+ by Neanthes was related to dose at low ambient chromium concentrations. Worms subjected to 0.0026, 0.0045, 0.0098, and 0.0166 mg Cr/L for 309 days contained 0.5, 0.7, 2.2, and 2.5 mg Cr/kg whole fresh organism, respectively (Oshida and Word, 1982). There was no direct relation between tissue concentration and brood size, suggesting that chromium in Neanthes attaches to proteins in the body wall, gut, and parapodial regions (Oshida and Word, 1982). N. arenaceodentata is the most sensitive marine organism yet tested to hexavalent chromium and for which data are available. In worms exposed to sublethal concentrations, feeding was disrupted after 14 days at 0.079 mg/L (USEPA, 1980a), reproduction ceased after 440 days (three generations) at 0.1 mg/L (Oshida and Word, 1982; Oshida et al., 1981), and abnormalities in larval development increased after 5 months in 0.025 mg/L (Reish, 1977). However, exposure for 293 days (two generations) in 50.4 mg trivalent chromium/L caused no adverse effects on survival, maturation time required for spawning, or brood size (Oshida et al., 1981). The polychaete C. capitata was more resistant to hexavalent chromium than Neanthes; a decrease in brood size was noted only after exposure for 5 months to 0.05 and 0.1 mg Cr6+/L (USEPA, 1980a).
10.9 Cobalt Limited data indicate that the highest concentration of cobalt recorded in field collections of annelids is 7.9 mg Co/kg DW in sandworms, N. diversicolor (Table 10.2). Cobalt uptake and excretion by N. japonica is reported by Ueda et al. (1977). They found that whole Nereis contain six times more cobalt than the medium after exposure for 11 days. Half the accumulated cobalt was excreted in 37 days after transfer to cobalt-free media; this period was slightly longer in unfed worms. Triquet (1973) reports that cobalt accumulation in
Annelids 535 lugworm, A. marina is mainly via the medium and not from cobalt-contaminated sediments; blood and digestive tract contained the highest cobalt concentrations.
10.10 Copper The highest concentration of copper measured in whole marine polychaetes was 1142.0 mg Cu/kg DW in organisms collected from coastal areas contaminated by metals wastes (Table 10.2). Copper tends to concentrate in the jaws of some polychaetes, and this needs to be considered when assessing risk on the basis of whole organism. In fact, copper is the principal metal in jaws of Glycera gigantas, a glycerid polychaete, accounting for about 1.5% of the DW and up to 67% of the total body burden of copper (Gibbs and Bryan, 1980). The copper is concentrated in the distal tip of the jaw where it accounts for up to 13% of the copper body content; high copper levels were measured in jaws of other species of glycerid polychaetes, and this seems characteristic of that group (Gibbs and Bryan, 1980). Copper accumulations in marine polychaetes are influenced mainly by the copper content and nature of the surrounding substrate. In one case, body content of copper in N. diversicolor directly reflected sediment copper concentrations (Bryan, 1974; Bryan and Hummerstone, 1971). However, in Capitella and Paraprionspio, highest concentrations of copper (and also samarium, scandium, and iron) were found in annelids collected from organic silt substrates, with consistently lower values from conspecifics collected from gravelly sand or clayey silts (Phelps et al., 1969). Pesch and Morgan (1978) clearly demonstrate the influence of presence or absence of sediment on whole-body burden of copper in N. arenaceodentata; at any given copper concentration in the medium, whole-body burden was significantly lower when sand was the substrate versus no substrate except glass. In follow-up studies, Pesch (1979) showed that sediment type influences the survival and accumulation of copper in N. arenaceodentata immersed in seawater containing 0.01 mg Cu/L for 85 days. In general, Neanthes survival was highest in mud, mud-sand mixtures, sand, and no sediment, in that order. Whole-body copper burdens after death, in mg Cu/kg DW were 270.0 without sediment, 994.0 in sand, 1047.0 in the mixture, and 1464.0 in mud. It was concluded that high organic content and small grain size were the two most important sediment parameters positively influencing survival of copper-stressed polychaetes (Pesch, 1979). Polychaetes, and other invertebrates, reared or found in high-copper environments may tolerate additional copper stress more readily than conspecifics from low-copper environments. In one case, polychaetes from metal-polluted estuaries had elevated body burdens of copper and were more resistant to copper lethality than were polychaetes from low-copper environments and with low body burdens of copper (Bryan, 1974). In another case, Ophryotrocha labronica had greater tolerance to 1.0 mg Cu/L solutions after exposure to two to three generations in 0.025 to 0.1 mg Cu/L than did controls; however, this tolerance diminished in successive generations (Saliba and Ahsanullah, 1973).
536 Chapter 10 Naturally occurring chelators can reduce copper toxicity to marine annelids. For example, fulvic acid—a major component in dissolved organic matter—complexes with copper, effectively reducing copper toxicity to larvae of the polychaete H. elegans (Qiu et al., 2007). Copper alone causes 50% abnormal development in 48 h at 0.056 mg Cu/L; however, the addition of 20.0 mg fulvic acid/L resulted in an increase to 0.137 mg Cu/L in the same period (Qiu et al., 2007). Polychaetes, H. japonica, exposed to 0.1 mg Cu/L for 6 days or to 0.1 mg Cu/L plus 0.1 mg petroleum hydrocarbons/L had BCF values of 83 for copper alone and 133 for the mixture, indicating significant interaction. Net accumulation rates, in mg Cu/kg body weight daily, were 2.1 for copper alone and 4.4 for the mixture (Sun and Zhou, 2007). Copper was the most toxic metal tested to trocophore larvae of H. elegans. Arrested development occurred at 0.122 mg Cu/L, with order of toxicity being copper > aluminum > lead > nickel > zinc (Gopalakrishnan et al., 2007). Laboratory and field studies with nereid polychaetes suggest that body wall and gut are the most useful indicators of environmental copper as these tissues show the greatest concentration potential (Bryan and Hummerstone, 1971; Raymont and Shields, 1963). Age of the organism and salinity of the medium are additional variables for consideration in the interpretation of copper residues. Juveniles of N. arenaceodentata are more sensitive than adults to copper insult and show greater accumulations during 28 day tests (Reish et al., 1976). Salinity affects sensitivity of N. diversicolor to copper stress, with adverse effects most pronounced at comparatively high and low salinities (Jones et al., 1976). The synergistic effect of increased copper toxicity under conditions of extreme salinities is more important as a lethal factor than sediment copper levels or amount of copper accumulated in Nereis tissues (Jones et al., 1976). Larvae of the sandworm (N. diversicolor) are more resistant to copper with increasing organism age and with increasing temperature and salinity of the medium (Ozoh and Jones, 1990). In adult sandworms, whole-body loadings of copper usually increase with increasing temperature in the range of 12-22 C and with decreasing salinity in the 7-31 ppt salinity range (Ozoh, 1992a,b); copper-temperature-salinity interactions are significant and complex in this species (Ozoh, 1994). Adult lugworms (A. marina) living in sediments containing 182.0-204.0 mg Cu/kg DW sediment had inhibited digestive processes; it was concluded that the digestive system of lugworms, and perhaps other deposit feeders, are vulnerable to copper-contaminated sediments (Chen and Mayer, 1998). Polychaetes, Hediste diversicolor, exposed to increasing concentrations of copper showed behaviors indicative of metal stress, including inconsistent burrowing, eversion of the proboscis, and abnormal crawling. Behavioral endpoints at 10 ppt salinity and copper concentrations as low as 0.2 mg Cu/L were considered predictors of survival in acute toxicity bioassays (Burlinson and Lawrence, 2007). However, in formulation of marine water quality criteria for metals, behavioral responses should be accompanied by tissue concentrations of the stressor (Eisler, 1979). Antifouling paints containing mixtures of zinc pyrithione and copper (tributyltin replacement) were more than additive in toxicity to larval
Annelids 537 polychaetes, H. elegans, in 96 h survival tests; this should be considered in developing copper and zinc water quality criteria (Bao et al., 2008).
10.11 Iron High variability was evident in concentrations of iron from polychaetes at different collection locales (Table 10.3). Highest values (>22,000.0 mg Fe/kg DW whole organism) were recorded in select deposit feeders, that is, those polychaetes which feed primarily at the sediment-water interface (Phelps, 1967).
10.12 Lead Limited data indicate that lead content in whole N. diversicolor ranges from 2.1 to 261.0 mg Pb/kg DW whole organism (Table 10.3). Studies with the polychaete H. elegans show that the two most sensitive stages to lead insult are sperm at 0.38 mg Pb/L (20-min exposure) and egg at 0.69 mg Pb/L (20 min exposure); by contrast, the LC50 (96 h) value for adults is 0.95 mg Pb/L (Gopalakrishnan et al., 2008).
10.13 Manganese Manganese concentrations in field collections of annelids were variable (Table 10.3). Manganese burdens in N. diversicolor are influenced by salinity of the medium, with concentrations greatest in worms collected from low salinity regimes (Bryan and Hummerstone, 1973a), and this, in part, may account for some of the variability. Laboratory studies with N. diversicolor show high accumulations of manganese in whole worms after exposure for 2 weeks (Bryan and Hummerstone, 1973a). At 1.0 mg Mn/L, body burdens were 27.0 mg Mn/kg DW versus 4.0 for controls; at 5.0 mg Mn/L, this value was 81.0. On transfer to manganese-free media for 7 days, whole Nereis body burdens were 2.0 mg Mn/kg DW (controls), 9.0 (1.0 mg Mn/L), and 20.0 (5.0 mg Mn/L), respectively (Bryan and Hummerstone, 1973a); authors suggest that manganese occurs in Nereis in two distinct pools, one exchanging slowly, the other more rapidly.
10.14 Mercury The highest mercury values recorded in field collections of annelids were 0.15 mg Hg/kg FW and 0.6 mg Hg/kg DW (Table 10.4). Periodic dredging to enlarge existing ship channels and for other purposes was associated with increasing body concentrations of mercury in annelids. For example, N. hombergi from a recently dredged area contained up to 0.15 mg Hg/kg FW, or three times more mercury than conspecifics collected from a control area
538 Chapter 10 Table 10.3: Iron, Lead, and Manganese in Field Collections of Annelids Element and Organism
Concentration
Reference
a
Iron Polychaete, Aglophamus sp.; whole
390.0-1500.0 FW
1
Polychaete, Armandia maculata; whole
30,600.0 DW
2
Polychaete, Capitella sp.; whole
22,100.0 DW
2
Bloodworm, Glycera gigantea; jaws
34.0-122.0 DW
3
Sandworm, Nereis diversicolor Whole Jaws, whole Jaws, basal section Jaws, distal section
362.0 (260.0-462.0) DW 586.0 DW 95.0 DW 1089.0 DW
5 4 4 4
Polychaete, Paraprionspio sp.; whole
24,600.0 DW
2
Polychaetes; 6 spp., whole
500.0-4000.0 (300.0-5300.0) DW
6
45.0 (2.1-261.0) DW
5
Polychaete, Branchipolynoe seepensis; parasite on gill of deep-sea mussel; 2002; whole
10.8 DW
9
Bloodworm, Glycera gigantea; jaws
Max. 5.0 DW
3
Polychaete, Hermione hystrix Whole Body Cuticle Bristles
1510.0 AW 1970.0 AW 3980.0 AW 1360.0 AW
7 7 7 7
Sandworm, Nereis diversicolor Whole Jaws, whole Jaws, basal section Jaws, distal section
5.0-12.5 DW 806.0 DW 380.0 DW 1079.0 DW
5, 8 4 4 4
Polychaetes, 6 spp.; whole
<10.0-58.0 (<10.0-110.0) DW
6
Polychaete, Spirographis spallanzini Body Tube
102.0 AW 337.0 AW
7 7
Lead Sandworm, Nereis diversicolor; whole Manganese
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Phelps et al., 1969; 2, Phelps, 1967; 3, Gibbs and Bryan, 1980; 4, Bryan and Gibbs, 1979; 5, Bryan and Hummerstone, 1977; 6, Cross et al., 1970; 7, Chipman and Thommeret, 1970; 8, Bryan and Hummerstone, 1973a; 9, Kadar et al., 2006.
Annelids 539 Table 10.4: Mercury and Nickel Concentrations in Field Collections of Annelids Element and Organism
Concentration
Reference
a
Mercury Lugworm, Arenicola marina; whole
0.01-0.07 FW
1
0.6 DW
7
0.4 DW 0.2 DW
8 8
Polychaete, Nephtys hombergi; whole
0.01 DW; 0.15 FW
1, 4
Sandworm, Nereis diversicolor Whole Whole
0.03-0.08 FW 0.35 DW
1 2
Polychaete, Nereis succinea; whole
0.008-0.13 FW
3
Sandworm, Nereis diversicolor; whole Britain; coastal waters Bidasoa estuary; French-Spanish border; April 1993
2.2-5.2 DW 5.4 (3.2-8.5) DW
4 5
Polychaetes; 3 spp.; whole; California
3.8-18.7 DW
6
Polychaete, Branchipolynoe seepensis; whole From gill of deep-sea mussel; 2002 Mid-Atlantic Ridge; hydrothermal vent field; 2001 1700 m deep 2300 m deep
Nickel
Values are in mg Hg/kg fresh weight (FW) or dry weight (DW). a 1, Zauke, 1977; 2, Leatherland and Burton, 1974; 3, Luoma, 1977; Rosenberg, 1977; 4, Bryan and Hummerstone, 1977; 5, Saiz-Salinas et al., 1996; 6, Jenkins, 1980; 7, Kadar et al., 2006; 8, Colaco et al., 2006.
(Table 10.4; Rosenberg, 1977); about 55% of the accumulated mercury was excreted over the next 18 months when the area was free from dredging (Rosenberg, 1977). Luoma (1977) reports that whole Nereis succinea accumulated up to 1.8 mg Hg/kg FW when fed terrigenous sediment; this accumulation exceeded mercury concentrations in solution by a factor of 350. The increased suspended solids in seawater, to which most of the mercury compounds readily sorbed, was the probable source of increased mercury in N. succinea. Luoma (1977) also noted that mercury uptake by N. succinea was markedly reduced at salinities of 16 ppt and lower. The presence of sediments in assay containers strongly affects mercury accumulation and elimination by adult Eurythoe complanata, a polychaete annelid (Vazquez-Nunez et al., 2007). Inorganic mercury was strongly accumulated during exposure for 8 days to 0.0015-0.011 mg Hg2+/L, but was much lower in the presence of sediments. Mercury elimination of 25-36% occurred during an 8 day depuration period, but only in the presence of sediments (Vazquez-Nunez et al., 2007).
540 Chapter 10 In laboratory studies, methylmercury was rapidly accumulated by whole G. dibranchiata; elimination was rapid, with 30% loss in 8 h following immersion for 8 days in 0.01 mg methylmercury/L (Medeiros et al., 1980). The addition of cysteine to the depuration media accelerated loss, with only 14% of the methylmercury remaining after 8 h (Medeiros et al., 1980). Absorption of glycine from ambient seawater across the body surface by the oligochaete Enchytraeus albidus and the polychaete N. diversicolor was significantly reduced in the presence of 0.1-0.15 mg Hg/L (Siebers and Ehlers, 1979). Mercury was more effective in preventing glycine absorption than were the following: copper, silver, and cadmium at 0.25-2.0 mg/L; aluminum, chromium, iron, lead, molybdenum, vanadium, and zinc up to 10.0 mg/L; and nickel, manganese, cobalt, and selenium up to 150.0 mg/L (Siebers and Ehlers, 1979). Early life stages of the polychaete H. elegans were most sensitive to inorganic mercury. Toxicity was evident to sperm at 0.032 mg Hg/L (20-min exposure) and to embryos at 0.054 mg Hg/L (2 h exposure); by contrast, the LC-50 (96 h) value for adults was 0.1 mg Hg/L (Gopalakrishnan et al., 2008). In general, mercury was most toxic to early life stages of H. elegans, followed by cadmium, lead, nickel, and zinc, in that order (Gopalakrishnan et al., 2008).
10.15 Nickel Sandworms, N. diversicolor, from British coastal waters contained between 2.2 and 5.2 mg Ni/kg DW whole organism (Table 10.4); sandworms from the Bidasoa estuary along the French-Spanish border contained up to 8.5 mg Ni/kg DW whole organism (Table 10.4). Concentrations up to 18.7 mg Ni/kg DW were recorded in whole polychaetes collected from the California coast (Table 10.4). Polychaete annelids were comparatively resistant to nickel. No deaths occurred in 168 h among sandworm adults immersed in seawater containing 10.0 mg Ni/L (Eisler and Hennekey, 1977), and LC50(96 h) values for three species of polychaetes ranged from 17.0 to 49.0 mg Ni/L (USEPA, 1980b). However, early life stages of marine polychaetes were more sensitive to nickel insult than were adults. Toxicity was evident to sperm of H. elegans at 0.73 mg Ni/L after 20 min exposure, and to eggs at 1.18 mg Ni/L after 20 min exposure (Gopalakrishnan et al., 2008).
10.16 Plutonium Accidental contamination of the marine environment near Greenland from the crash of a United States military aircraft transporting plutonium-containing materials raised median background levels of plutonium by three orders of magnitude (Aarkrog, 1971). From 1968 to 1970, the 239+240Pu concentrations in benthic organisms, including annelids and molluscs, decreased by an order of magnitude; since 1970, the decline is less evident (Aarkrog, 1977).
Annelids 541 Laboratory studies with N. diversicolor show that whole-body content of plutonium is about 0.5% of the plutonium content of the surrounding sediment, and that no preferential uptake of 238Pu over 239+240Pu is evident (Beasley and Fowler, 1976).
10.17 Ruthenium Over a period of 11 days, N. japonica concentrated 106Ru from seawater by a factor of about 6; the time for 50% excretion was 35 days in fed worms and was slightly longer in starved worms (Ueda et al., 1977). Uptake factor for 106Ru by a gobiid fish fed with N. japonica was only 0.002; thus, transfer of 106Ru from worm to fish was relatively small in comparison with accumulation from the surrounding seawater (Kimura and Ichikawa, 1969).
10.18 Samarium The highest concentration of samarium recorded in field collections of whole annelids is 3.6 mg Sm/kg DW (Table 10.5). Samarium concentrations in polychaetes seem to reflect the levels in surrounding sediments (Phelps, 1967). Table 10.5: Samarium, Scandium, Silver, and Strontium in Field Collections of Annelids Element and Organism
Concentration
Reference
a
Samarium Polychaete, Aglophamus sp.; whole
0.14 FW
1
Polychaetes; benthic; whole
0.04-3.6 DW
2
0.7-3.0 DW 0.3-6.9 DW 2.9-26.4 DW
2 2 2
Sandworm, Nereis diversicolor; whole
5.2 (0.7-30.0) DW
3
Polychaete, Marphysa sanguinea; whole; San Francisco Bay; 1982
Max. 5.5 DW
5
2.1 FW
4
Scandium Polychaetes; whole; 9 spp. 3 spp. 3 spp. 3 spp. Silver
Strontium Annelids; whole
Values are in mg element/kg fresh weight (FW) or dry weight (DW). a 1, Phelps et al., 1969; 2, Phelps, 1967; 3, Bryan and Hummerstone, 1977; 4, Mauchline and Templeton, 1966; 5, Luoma and Phillips, 1988.
542 Chapter 10
10.19 Scandium The highest scandium concentration recorded in whole marine annelids is 26.4 mg Sc/kg DW (Table 10.5), although this requires verification; concentrations seem to reflect scandium concentrations in the surrounding sediments (Phelps, 1967). Scandium is concentrated by a few species more markedly than by ecological groups; however, there is a tendency for reduced accumulations as the organisms move up the food chain from deposit feeders (Phelps, 1967).
10.20 Selenium Uptake and retention of radioselenium was determined in a polychaete, Eunice sp. (Alquezar et al., 2007). Eunice was held for 385 h in seawater spiked with 75Se followed by 189 h in 75 Se-free media. During uptake, whole Eunice concentrated radioselenium from the medium by a factor of 45; about 71% was lost over the next 189 h. During depuration, the short-lived component had a biological half-time of 34 h; for the long lived component, it was 555 h (Alquezar et al., 2007).
10.21 Silver The maximum silver concentration recorded in annelids of 30.0 mg Ag/kg DW was in whole N. diversicolor (Table 10.5) from a metals-contaminated estuary (Bryan and Hummerstone, 1977). Uptake and retention of silver by adults of Sabella pavonia held in seawater containing 0.05 mg Ag/L for 8 weeks, then transferred to silver-free media for an additional 8 weeks is reported (Koechlin and Grasset, 1988). During immersion, the maximum whole-body silver burden was 22.1 mg/kg DW versus 0.8 in controls; main sites of accumulation were the connective tissues of nephridia and gut. There was no detectable histopathology. A constant elimination of silver in urine occurs simultaneously with silver accumulation. During depuration, new connective tissues were formed and silver concentrations were reduced by 88%. Ionic or free silver interferes with calcium metabolism of marine polychaetes contaminated with silver, that is, the calcium content of nephridial cells was reduced although silver was not detected in the calcium vesicles. Silver binds with protein sulfhydryl groups, and this process protects the annelid against silver intoxication (Koechlin and Grasset, 1988).
10.22 Strontium Whole marine annelids contain an average of 2.1 mg Sr/kg FW (Table 10.5).
Annelids 543
10.23 Tin No deaths were documented in larvae of the lugworm, Arenicola cristata, in 168 h at 0.002 mg tributyltin (TBT)/L (Walsh et al., 1986); however, all larvae died at 0.004 mg TBT/ L in 96 h (Maguire et al., 1984). At sublethal TBT concentrations, teratogenic effects were observed in lugworm larvae (Walsh et al., 1986). Laboratory studies with H. elegans show that eggs were the most sensitive stage tested in 48 h assays: LC-50 was 0.00018 mg TBT/L (Lau et al., 2007). Results of 17 day exposure from egg to juvenile demonstrate that TBT concentrations >0.00001 mg/L adversely affect survival and growth of Hydroides. In longer exposures of 44 days, only juveniles exposed to <0.0001 mg TBT/L reached maturity; and in 60 day fecundity tests, egg production, fertilization success, and egg development were all reduced at >0.0001 mg TBT/L (Lau et al., 2007). Annelids accumulate organotins from sediments. For example, sediments spiked with 0.98 mg Sn (as TBT)/kg DW resulted in concentrations of 4.41 mg/kg DW whole body in oligochaete annelids after 22 weeks, up from 0.38 at the start (Maguire and Tkacz, 1985). Annelids in sediments containing less than 0.61 mg TBT/kg DW had normal growth and survival (Cardwell and Sheldon, 1986). However, survival decreased when annelids were exposed simultaneously to organotins through both water and sediments (Clark et al., 1987).
10.24 Zinc Whole-body concentrations of zinc in annelids from different collections range from 22.0 to 1554.0 mg Zn/kg on a DW basis (Table 10.6). It is noteworthy that jaws of nereid polychaetes analyzed contained 2880.0-34,950.0 mg Zn/kg DW, and this accounted for up to 40% of the total body zinc burden (Bryan and Gibbs, 1979). In N. diversicolor, zinc content was not related to zinc content of surrounding sediments; a high zinc content seems to be a structural characteristic of nereid jaws (Bryan and Gibbs, 1979). Among the polychaetes, the composition of the feeding community based on feeding types is an important factor in the partitioning of stable zinc; the less dependent an organism is on the sediment as a source of food, the lower its concentration of zinc (Phelps, 1967). Polychaetes that feed mainly from the sediment-water interface (selective deposit feeders), concentrate iron to the apparent exclusion of zinc, and polychaetes that feed mainly below the sediment water interface (nonselective deposit feeders, omnivores, carnivores) preferentially concentrate zinc over iron (Phelps, 1967). N. diversicolor, as one example, could remove up to 4% of the 65Zn in the upper 2 cm of a hypothetical radioactive estuary (Renfro, 1973). Qualitative and quantitative structure of the benthic faunal community has a direct effect on zinc distribution: a shift in preponderance from polychaete annelids to bivalve molluscs could result in a decrease in the amount of zinc incorporated into the biological community (Phelps, 1967).
544 Chapter 10 Table 10.6: Zinc Concentrations in Field Collections of Annelids Organism
Concentration
Reference
Polychaete, Branchipolynoe seepensis; whole; mid-Atlantic Ridge; hydrothermal vent field; 2001 1700 m deep 2300 m deep
219.0 DW 304.0 DW
Sandworm, Nereis diversicolor Whole Whole Jaws Jaws, basal section Jaws, distal section Head Parapodia Trunk
130.0-315.0 DW 22.0-37.0 FW 14,000.0 DW 1790.0 DW 34,950.0 DW 843.0-995.0 DW 216.0-413.0 DW 158.0-218.0 DW
4, 5 6 7 7 7 9 9 9
Polychaetes; 9 spp.; jaws
4971.0-24,050.0 DW
7
Polychaetes; whole; 5 spp.
78.0-165.0 DW
1
Polychaetes; whole Lugworm, Arenicola marina Polynoid spp. Ceratonereis sp. Protoaricia sp.
1.8 FW 55.0-59.0 DW 123.0 DW 370.0-1554.0 DW
8 2 2 2
Bloodworm, Glycera gigantea Jaws Whole
2880.0-3300.0 DW 2210.0-4070.0 DW
3 3
a
10 10
Values are in mg Zn/kg fresh weight (FW) or dry weight (DW). a 1, Cross et al., 1970.; 2, Phelps, 1967; 3, Gibbs and Bryan, 1980; 4, Bryan and Hummerstone, 1973b; 5, Bryan and Hummerstone, 1977; 6, Wharfe and Van Den Broek, 1977; 7, Bryan and Gibbs, 1979. 8, Morris et al., 1989; 9, Fernandez and Jones, 1989; 10, Colaco et al., 2006.
In the sandworm, N. diversicolor, zinc is localized in the gut wall, epidermis, nephridia, and blood vessels; most of the body zinc is present in wandering amoebocyte cells of excretory organs (Fernandez and Jones, 1989). Zinc in Nereis may be present as insoluble granules in membrane-bound vesicles. Excretion is via exocytosis with the aid of amoebocytes (Fernandez and Jones, 1989). Unlike the insoluble zinc phosphate granules of molluscs and crustacean, zinc granules in Nereis were very soluble and retained only by sulfide precipitation (Pirie et al., 1985). Zinc uptake in N. diversicolor increased with increasing sediment zinc concentrations, at lower salinities (Eisler, 1980), and at elevated temperatures (Fernandez and Jones, 1987, 1989). Zinc had no measurable effect on burrowing behavior of
Annelids 545 Nereis, even at acutely lethal concentrations (Fernandez and Jones, 1987). Sandworms from zinc-contaminated sediments were more resistant to waterborne zinc insult by 10-100 times than those form clean sediments (USEPA, 1987). Tolerance to zinc in sandworms may be a result of acclimatization or genetic adaptation. In either event, the degree of metal tolerance decreases rapidly as the level of zinc contamination declines, suggesting that some zinc-tolerant sandworms may be competitively inferior to normal individuals in clean environments (Grant et al., 1989). Body zinc burdens of nereid worms tend to reflect zinc burdens in the surrounding sediments (Bryan, 1974). Physiological adaptation of N. diversicolor to zinc-impacted sediments is proposed by Bryan and Hummerstone (1973b), owing, in part, to decreased body surface permeability (Bryan, 1974). Under laboratory conditions Bryan and Hummerstone (1973b) found that Nereis from high-zinc sediments, when compared to those collected from low-zinc sediments, accumulated less zinc per unit body weight daily and had higher survival; this pattern appeared to hold over a range of salinities. It is emphasized that the rate of net absorption, in mg Zn/kg DW daily, in whole N. diversicolor was 2230.0—the highest reported value for any group of invertebrates (Bryan and Hummerstone, 1973b). That study was conducted for 35 days in seawater solutions containing 250.0 mg Zn/L with Nereis collected from sediments of low zinc content. Rate of net absorption decreased with increasing zinc concentration until it was 55.0 mg Zn/kg DW daily in 10.0 mg Zn/L (Bryan and Hummerstone, 1973b). Sometimes, however, trace metal content of polychaetes did not differ markedly when collected from sediments that contained substantially different quantities of iron, manganese, or zinc. The order of enrichment in six species of polychaetes over sediments is zinc > iron > manganese. This order of enrichment agrees with the hypothesis that enrichment of divalent metal ions by the marine biosphere follows the order of stability of metal-ligand complexes (Cross et al., 1970). There was no difference in body burden of zinc and other metals analyzed in polychaetes from two stations which had markedly different concentrations of trace metals in the sediments, suggesting that these organisms may be able to regulate trace metal content or that much of the metal associated with the sediment is in an unacceptable chemical form for biological uptake (Cross et al., 1970). In another study, zinc levels in benthic communities—mainly annelids—show no relation to proximity of the land mass or to changes in substrate, although there is a trend for higher zinc values to occur in organisms found in the offshore silts and clays (Phelps et al., 1969). Time to reach equilibrium with the sediment is another variable; for example, the polychaete Hermione hystrix required 60 days to approach a steady state with zinc in the sediments (Renfro, 1973). In many species of marine biota, zinc is bound to metallothioneins; however, not all zinc-binding proteins are metallothioneins (Andersen et al., 1989; Eriksen et al., 1990). Low-molecular-weight metal-binding proteins—not metallothioneins—were induced in polychaete annelids in metals-contaminated environments (Andersen et al., 1989). In less contaminated environments, zinc was mainly associated with high-molecular-weight proteins in four
546 Chapter 10 species of sediment-feeding polychaetes, suggesting that metallothionein-like proteins may not be satisfactory for monitoring purposes and that other cytosolic components should be studied (Eriksen et al., 1990). Unlike other major groups of marine benthic organisms, polychaete annelids, as judged by N. arenaceodentata, have a limited capacity to regulate zinc (Mason et al., 1988). Uptake in Neanthes occurs from the free ionic pool of zinc, whereas EDTA and EDTA-zinc complexes are largely excluded. Zinc accumulates linearly over time (350 h), and the rate decreases with increasing temperature in the range 4-21 C. Mason et al. (1988) conclude that uptake and accumulation of zinc is passive in Neanthes and does not require metabolic energy. Zinc transfer across the plasma membrane is by way of diffusion. Within the cell, zinc binds to a variety of excising ligands which maintain an inwardly directed diffusion gradient, preventing zinc efflux. Accumulation rate is determined by the number and binding characteristics of the available ligands and their accessibility to zinc. After 50 h of exposure, worms selectively accumulated zinc over cadmium from the medium by a process requiring metabolic energy, and this is attributed to a change in the turnover rate and the size and nature of the zinc-binding ligands (Mason et al., 1988). Life stage of the organism, possible discrimination against various chemical species of zinc, normal interspecies differences, and dredging practices should also be considered when interpreting zinc residues in annelids. In regard to life stage, juveniles of Neanthes and Capitella were more sensitive to zinc effects than were adults (Reish et al., 1976); a similar case is made for H. elegans (Gopalakrishnan et al., 2008). H. hystrix is apparently capable of distinguishing radiozinc species from stable zinc species: the biological half-life of 65Zn in Hermione is 52-197 days but only 14-17 days for stable zinc (Renfro, 1973). Variability in zinc content of closely related species of polychaetes is considerable; for six species, the zinc content differed by an eightfold factor (Cross et al., 1970). The influence of dredging on zinc concentrations in N. hombergi is considerable (Rosenberg, 1977). Nephtys from a recently dredged area contained elevated levels of zinc when compared to conspecifics from a reference area; however, 95% to 98% was excreted during the next 18 months while the area was free from dredging. Abnormal larval development of the polychaete C. capitata was documented during exposure for ten days to 0.05-0.1 mg Zn/L (USEPA, 1987). Zinc was lethal to adult C. capitata at 1.25 mg Zn/L in 28 days (USEPA, 1987), to adult N. arenaceodentata at 0.9 mg/L in 28 days (Spear, 1981), and to adults of N. diversicolor at 2.6 mg/L in seven days (Eisler and Hennekey, 1977). Adults of N. diversicolor held in 10.0 mg Zn/L for 96 h at 6 C contained zinc burdens (in mg/kg DW) of 1031.0 in head versus 843.0 in controls, 366.0 versus 158.0 in trunk, and 455.0 versus 275.0 in parapodia; uptake was higher at 12 C and 20 C (Fernandez and Jones, 1989). Surviving adults of N. diversicolor subjected to zinc concentrations of 10.0 mg/L for 34 days had whole-body burdens of 2500.0 mg/kg DW versus 180.0 in controls (as quoted in Eisler, 1980).
Annelids 547
10.25 Zirconium Uptake studies with radiozirconium-95 and N. japonica indicate a concentration factor of 4 over the medium, a biological half-life (time for 50% excretion) of 32 days for accumulated 95Zr in fed worms, and a slightly longer half-life for starved worms (Ueda et al., 1977).
10.26 Literature Cited Aarkrog, A., 1971. Radioecological investigations of plutonium in an Arctic marine environment. Health Phys. 20, 31–47. Aarkrog, A., 1977. Environmental behaviour of plutonium accidentally released at Thule, Greenland. Health Phys. 32, 271–284. Alquezar, R., Markich, S.J., Twining, J.R., 2007. Uptake and loss of dissolved 109Cd and 75Se in estuarine macroinvertebrates. Chemosphere 67, 1201–1210. Andersen, R.A., Eriksen, K.D.H., Bakke, T., 1989. Evidence of presence of a low molecular weight, non-metallothionein-like metal-binding protein in the marine gastropod Nassarius reticulatus L. Comp. Biochem. Physiol. 94B, 285–291. Athalye, R.P., Gokhole, K.S., 1991. Heavy metals in the polychaete Lycastis ouanaryensis from Thane Creek, India. Mar. Pollut. Bull. 22, 233–236. Bao, V.W.W., Leung, K.M.Y., Kwok, K.W.H., Zhang, A.Q., Lui, G.C.S., 2008. Synergistic toxic effects of zinc pyrithione and copper to three marine species: Implications on setting appropriate water quality criteria. Mar. Pollut. Bull. 57, 616–623. Beasley, T.M., Fowler, S.W., 1976. Plutonium and americium: Uptake from contaminated sediments by the polychaete Nereis diversicolor. Mar. Biol. 38, 95–100. Bernhard, M., Zattera, A., 1975. Major pollutants in the marine environment. In: Pearson, E.A., Frangipane, E.D. (Eds.), Marine Pollution and Marine Waste Disposal. Pergamon, New York, pp. 195–300. Bryan, G.W., 1963. The accumulation of radioactive caesium by marine invertebrates. J. Mar. Biol. Assoc. UK 43, 519–539. Bryan, G.W., 1974. Adaptation of an estuarine polychaete to sediments containing high concentrations of heavy metals. In: Vernberg, F.J., Vernberg, W.B. (Eds.), Pollution and Physiology of Marine Organisms. Academic Press, New York, pp. 123–135. Bryan, G.W., Gibbs, P.E., 1979. Zinc—a major inorganic component of nereid polychaete jaws. J. Mar. Biol. Assoc. UK 59, 969–973. Bryan, G.W., Hummerstone, L.G., 1971. Adaptation of the polychaete Nereis diversicolor to estuarine sediments containing high concentrations of heavy metals. I. General observations and adaptation to copper. J. Mar. Biol. Assoc. UK 51, 845–863. Bryan, G.W., Hummerstone, L.G., 1973a. Adaptation of the polychaete Nereis diversicolor to manganese in estuarine sediments. J. Mar. Biol. Assoc. UK 53, 859–872. Bryan, G.W., Hummerstone, L.G., 1973b. Adaptation of the polychaete Nereis diversicolor to estuarine sediments containing high concentrations of zinc and cadmium. J. Mar. Biol. Assoc. UK 53, 839–857. Bryan, G.W., Hummerstone, L.G., 1977. Indicators of heavy metal contamination in the Looe estuary (Cornwall) with particular regard to silver and lead. J. Mar. Biol. Assoc. UK 57, 75–92. Burlinson, F.C., Lawrence, A.J., 2007. Development and validation of a behavioural assay to measure the tolerance of Hediste diversicolor to copper. Environ. Pollut. 145, 274–278. Cardwell, R.D., Sheldon, A.W., 1986. A risk assessment concerning the fate and effects of tributyltins in the aquatic environment. In: Maton, G.L. (Ed.), Proceedings Oceans 86 Conference, Washington, DC, 23-25 September 1986, vol. 4. Organotin symposium. Available from Marine Technology Society, 2000 Florida Ave, New York, Washington, DC, pp. 1117–1129.
548 Chapter 10 Chen, Z., Mayer, L.M., 1998. Digestive processes of the lugworm (Arenicola marina) inhibited by Cu from contaminated sediments. Environ. Toxicol. Chem. 17, 433–438. Chipman, W.A., 1967. Some aspects of the accumulation of chromium-51 by marine organisms. In: Proceedings of an International Symposium on Radioecological Concentration Processes, Stockholm, 1966, pp. 931–994. Chipman, W., Thommeret, J., 1970. Manganese content and the occurrence of fallout 54Mn in some marine benthos of the Mediterranean. Bull. Inst. Oceanogr. 69(1402), 1–15. Clark, J.R., Patrick Jr., J.M., Moore, J.C., Lores, E.M., 1987. Waterborne and sediment-source toxicities of six organic chemicals to grass shrimp (Palaemonetes piugio) and amphioxus (Branchiostoma caribaeum). Arch. Environ. Contam. Toxicol. 16, 401–407. Colaco, A., Bustamante, P., Fouquet, Y., Sarradin, P.M., Serraos-Santos, R., 2006. Bioaccumulation of Hg, Cu, and Zn in the Azores triple junction hydrothermal vent fields food web. Chemosphere 65, 2260–2267. Cross, F.A., Duke, T.W., Willis, J.N., 1970. Biogeochemistry of trace elements in a coastal plain estuary: Distribution of manganese, iron, and zinc in sediments, water and polychaetous worms. Chesapeake Sci. 11, 221–234. Eisler, R., 1979. Behavioural responses of marine poikilotherms to pollutants. Phil. Trans. R. Soc. Lond. 286B, 507–521. Eisler, R., 1980. Accumulation of zinc by marine biota. In: Nriagu, J.O. (Ed.), Zinc in the Environment. Part II. Health Effects. John Wiley, New York, pp. 259–351. Eisler, R., 2000. Cadmium. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 1–43. Eisler, R., Hennekey, R.J., 1977. Acute toxicities of Cd2+, Cr+6, Hg2+, Ni2+ and Zn2+ to estuarine macrofauna. Arch. Environ. Contam. Toxicol. 6, 315–323. Eriksen, K.D.H., Andersen, T., Stenersen, J., Andersen, R.A., 1990. Cytosolic binding of Cd, Cu, Zn, Zn and Ni in four polychaete species. Comp. Biochem. Physiol. 95C, 111–115. Fernandez, T.V., Jones, N.V., 1987. Some studies on the effect of zinc on Nereis diversicolor (polychaete-annelida). Trop. Ecol. 28, 9–21. Fernandez, T.V., Jones, N.V., 1989. The distribution of zinc in the body of Nereis diversicolor. Trop. Ecol. 30, 285–293. Fukai, R., Broquet, D., 1965. Distribution of chromium in marine organisms. Bull. Inst. Oceanogr. 65(1336), 1–19. Geiszinger, A.E., Goessler, W., Francesconi, K.A., 2002. The marine polychaete Arenicola marina: Its unusual arsenic compound pattern and its uptake of arsenate from seawater. Mar. Environ. Res. 53, 37–50. Gibbs, P.E., Bryan, G.W., 1980. Copper—The major metal component of glycerid polychaete jaws. J. Mar. Biol. Assoc. UK 60, 205–214. Gopalakrishnan, S., Thilagam, H., Raja, P.V., 2007. Toxicity of heavy metals on embryogenesis and larvae of the marine sedentary polychaete Hydroides elegans. Arch. Environ. Contam. Toxicol. 52, 171–178. Gopalakrishnan, S., Thilagam, H., Raja, P.V., 2008. Comparison of heavy metal toxicity in life stages (spermotoxicity, egg toxicity, and larval toxicity) of Hydroides elegans. Chemosphere 71, 515–528. Goto, D., Wallace, W.G., 2007. Interaction of Cd and Zn during uptake and loss in the polychaete Capitella capitata: Whole body and subcellular perspectives. J. Exp. Mar. Biol. Ecol. 352, 65–77. Grant, A., Hately, J.G., Jones, N.V., 1989. Mapping the ecological impact of heavy metals on the estuarine polychaete Nereis diversicolor using inherited metal tolerance. Mar. Pollut. Bull. 20, 235–238. Hall Jr., L.W., Scott, M.C., Killen, W.D., 1998. Ecological risk assessment of copper and cadmium in surface waters of Chesapeake Bay watershed. Environ. Toxicol. Chem. 17, 1172–1189. Jenkins, D.W., 1980. Biological monitoring of trace metals. Volume 2. Toxic trace metals in plants and animals of the world. Part III. 1–290 U.S. Environ. Protect. Agent. Rep. 600/3-80-092, pp. 1-290. Jones, L.H., Jones, N.V., Radlett, A.J., 1976. Some effects of salinity on the toxicity of copper to the polychaete Nereis diversicolor. Estuar. Coast. Mar. Sci. 4, 107–111.
Annelids 549 Kadar, E., Santos, R.S., Powell, J.J., 2006. Biological factors influencing tissue compartmentalization of trace metals in the deep-sea hydrothermal vent bivalve. Bathymodiolus azoricus at geochemically distinct vent sites of the mid-Atlantic Ridge. Environ. Res. 101, 221–229. Kimura, K., Ichikawa, R., 1969. Accumulation and retention of ingested ruthenium-106 by genuine goby. Bull. Jpn. Soc. Sci. Fish. 35, 435–440. Koechlin, N., Grasset, M., 1988. Silver contamination in the marine polychaete annelid Sabella pavonina S.: A cytological and analytical study. Mar. Environ. Res. 26, 249–263. Lau, K.C., Chan, K.M., Leung, K.M.Y., Luan, T.G., Yang, M.S., Qiu, J.W., 2007. Acute and chronic toxicities of tributyltin to various life stages of the marine polychaete Hydroides elegans. Chemosphere 69, 135–144. Leatherland, T.M., Burton, J.D., 1974. The occurrence of some trace metals in coastal organisms with particular reference to the Solent Region. J. Mar. Biol. Assoc. UK 54, 457–468. Luoma, S.N., 1977. Physiological characteristics of mercury uptake by two estuarine species. Mar. Biol. 41, 269–273. Luoma, S.N., Phillips, D.J.H., 1988. Distribution, variability, and impacts of trace elements in San Francisco Bay. Mar. Pollut. Bull. 19, 413–425. Maguire, R.J., Tkacz, R.J., 1985. Degradation of the tri-n-butyltin species in water and sediment from Toronto Harbor. J. Agric. Food Chem. 33, 947–953. Maguire, R.J., Wong, P.T.S., Rhamey, J.S., 1984. Accumulation and metabolism of tri-n-butyltin cation by a green alga, Ankistrodesmus falcatus. Can. J. Fish. Aquat. Sci. 41, 537–540. Mason, A.Z., Jenkins, K.D., Sullivan, P.A., 1988. Mechanisms of trace metal accumulation in the polychaete Neanthes arenaceodentata. J. Mar. Biol. Assoc. UK 68, 61–80. Mauchline, J., Templeton, W.L., 1966. Strontium, calcium, and barium in marine organisms from the Irish Sea. J. Cons. Int. Explor. Mer. 30, 161–170. Mearns, A.J., Young, D.R., 1977. Chromium in the southern California marine environment. In: Giam, C.S. (Ed.), Pollutant Effects on Marine Organisms. D.C. Heath, Lexington, MA, pp. 125–142. Mearns, A.J., Oshida, P.S., Sherwood, M.J., Young, D.R., Reish, D.J., 1976. Chromium effects on coastal organisms. J. Water Pollut. Control Fed. 48, 1929–1939. Medeiros, D.M., Caldwell, L.L., Preston, R.L., 1980. A possible physiological uptake mechanism of methylmercury by the marine bloodworm (Glycera dibranchiata). Bull. Environ. Contam. Toxicol. 24, 97–101. Morris, R.J., Law, R.J., Allchin, C.R., Kelly, C.A., Fileman, C.F., 1989. Metals and organochlorines in dolphins and porpoises of Cardigan Bay, West Wales. Mar. Pollut. Bull. 20, 512–523. Ng, T.Y.T., Rainbow, P.S., Amiard-Triquet, C., Amiard, J.C., Wang, W.X., 2008. Decoupling of cadmium biokinetics and metallothionein turnover in a marine polychaete after metal exposure. Aquat. Toxicol. 89, 47–54. Notti, A., Fattorini, D., Razzetti, E.M., Regoli, F., 2007. Bioaccumulation and biotransformation of arsenic in the Mediterranean polychaete Sabella spallanzanii: Experimental observations. Environ. Toxicol. Chem. 26, 1186–1191. Oshida, P.S., Word, L.S., 1982. Bioaccumulation of chromium and its effects on reproduction in Neanthes arenaceodentata (Polychaeta). Mar. Environ. Res. 7, 167–174. Oshida, P.S., Mearns, A.J., Reish, D.J., Word, L.S., 1976. The effects of hexavalent and trivalent chromium on Neanthes arenaceodentata (Polychaeta: Annelida). SCCWRP (1500 E. Imperial Highway, El Segundo, California) TM 225, 1–58. Oshida, P.S., Word, L.S., Mearns, A.J., 1981. Effects of hexavalent and trivalent chromium on the reproduction of Neanthes arenaceodentata (Polychaeta). Mar. Environ. Res. 5, 41–49. Ozoh, P.T.E., 1992a. The effects of salinity, temperature and sediment on the toxicity of copper to juvenile Hediste (Nereis) diversicolor (O.F. Muller). Environ. Monit. Assess. 21, 1–10. Ozoh, P.T.E., 1992b. The effect of temperature and salinity on copper body-burden and copper toxicity to Hediste (Nereis) diversicolor. Environ. Monit. Assess. 21, 11–17. Ozoh, P.T.E., 1994. The effect of salinity, temperature and time on the accumulation and depuration of copper in ragworm, Hediste (Nereis) diversicolor (O.F. Muller). Environ. Monit. Assess. 29, 155–164.
550 Chapter 10 Ozoh, P.T.E., Jones, N.V., 1990. The effects of salinity and temperature on the toxicity of copper to 1-day and 7day-old larvae of Hediste (Nereis) diversicolor (O.F. Muller). Ecotoxicol. Environ. Safety 19, 24–32. Pentreath, R.J., Jefferies, D.F., 1971. The uptake of radionuclides by I-group plaice (Pleuronectes platessa) off the Cumberland Coast, Irish Sea. J. Mar. Biol. Assoc. UK 51, 963–976. Pesch, C.E., Morgan, D., 1978. Influence of sediment in copper toxicity tests with the polychaete Neanthes arenaceodentata. Water Res. 12, 747–751. Pesch, C.E., 1979. Influence of three sediment types on copper toxicity to the polychaete Neanthes arenaceodentata. Mar. Biol. 52, 237–245. Phelps, D.K., 1967. Partitioning of the stable elements Fe, Zn, Sc, and Sm within the benthic community, Anasco Bay, Puerto Rico. In: Proceedings of an International Symposium on Radioecological Concentration Processes, Stockholm, 1966, pp. 721–734. Phelps, D.K., Santiago, R.J., Luciano, D., Irizarry, N., 1969. Trace element composition of inshore and offshore benthic populations. In: Proceedings of the 2nd National Symposium on Radioecology. USAEC Conf. 67053, pp. 509–526. Phelps, D.K., Telek, G., Lapan Jr., R.L., 1975. Assessment of heavy metal distribution within the food web. In: Pearson, E.A., Frangipane, E.D. (Eds.), Marine Pollution and Marine Waste Disposal. Pergamon, Elmsford, NY, pp. 341–348. Pirie, B., Fayi, L., George, S., 1985. Ultrastructural localisation of copper and zinc in the polychaete, Nereis diversicolor, from a highly contaminated estuary. Mar. Environ. Res. 17, 197–198. Qiu, J.W., Tang, X., Zheng, C., Li, Y., Huang, H., 2007. Copper complexation by fulvic acid affects copper toxicity to the larvae of the polychaete Hydroides elegans. Mar. Environ. Res. 64, 563–573. Ray, S., McLeese, D., Pezzack, D., 1980. Accumulation of cadmium by Nereis virens. Arch. Environ. Contam. Toxicol. 9, 1–8. Raymont, J.E.G., Shields, J., 1963. Toxicity of copper and chromium in the marine environment. Int. J. Air Water Pollut. 7, 435–443. Reish, D.J., 1977. Effects of chromium on the life history of Capitella capitata (Annelida: Polychaeta). In: Vernberg, F.J., Calabrese, A., Thurberg, F.P., Vernberg, W.B. (Eds.), Physiological Responses of Marine Biota to Pollutants. Academic Press, New York, pp. 199–207. Reish, D.J., Martin, J.M., Piltz, F.M., Word, J.Q., 1976. The effect of heavy metals on laboratory populations of two polychaetes with comparisons to other water quality conditions and standards in southern California marine waters. Water Res. 10, 299–302. Renfro, W.C., 1973. Transfer of 65Zn from sediments by marine polychaete worms. Mar. Biol. 21, 305–316. Rice, M.A., Chien, P.K., 1979. Uptake, binding and clearance of divalent cadmium in Glycera dibranchiata (Annelida: Polychaeta). Mar. Biol. 53, 33–39. Rosenberg, R., 1977. Effects of dredging operations on estuarine benthic macrofauna. Mar. Pollut. Bull. 8, 102–104. Saiz-Salinas, J.I., Ruiz, J.M., Frances-Zubillaga, G., 1996. Heavy metal levels in intertidal sediments and biota from the Bidasoa estuary. Mar. Pollut. Bull. 32, 69–71. Saliba, L.J., Ahsanullah, M., 1973. Acclimation and tolerance of Artemia salina and Ophryotrocha labronica to copper sulphate. Mar. Biol. 23, 297–302. Sandrini, J.Z., Regoli, F., Fattorini, D., Notti, A., Inacio, A.F., Linde-Arias, A.R., et al., 2006. Short-term responses to cadmium exposure in the estuarine polychaete Laeonereis acuta (polychaeta, nereididae): Subcellular distribution and oxidative stress generation. Environ. Toxicol. Chem. 25, 1337–1344. Siebers, D., Ehlers, U., 1979. Heavy metal action on trans-integumentary absorption of glycine in two annelid species. Mar. Biol. 50, 175–179. Spear, P.A., 1981. Zinc in the aquatic environment: Chemistry, distribution, and toxicology. Natl. Res. Coun. Can. Publ. NRCC 17589. pp. 1–145. Sun, F.H., Zhou, Q.X., 2007. Metal accumulation in the polychaete Hediste japonica with emphasis on interaction between heavy metals and petroleum hydrocarbons. Environ. Pollut. 149, 92–98.
Annelids 551 Thorsson, M.H., Hedman, J.E., Bradshaw, C., Gunnarsson, J.S., Gilek, M., 2008. Effects of settling organic matter on the bioaccumulation of cadmium and BDE-99 by Baltic Sea benthic invertebrates. Mar. Environ. Res. 65, 264–281. Triquet, C., 1973. Study of the contamination of Arenicola marina L. by cobalt-60. Comptes Rend. Acad. Sci. 276 (Ser. D, No. 4), 645–648. Ueda, T., Nakamura, R., Suzuki, Y., 1976. Comparison of 115mcd accumulation from sediments and sea water by polychaete worms. Bull. Jpn. Soc. Sci. Fish. 42, 299–306. Ueda, T., Nakamura, R., Suzuki, Y., 1977. Comparison of influences of sediments and sea water on accumulation of radionuclides by worms. J. Radiat. Res. 18, 84–92. U.S. Environmental Protection Agency (USEPA), 1980a. Ambient water quality criteria for chromium. USEPA Rep. 440/5-80-035. USEPA, 1980b. Ambient water quality criteria for nickel. USEPA Rep. 440/5-80-060. pp. 1–206. USEPA, 1987. Ambient water quality criteria for zinc-1987. USEPA Rep. 440/5-87-003. pp. 1–207. Vaskovsky, V.E., Korotchenko, O.D., Kosheleva, L.P., Levin, V.S., 1972. Arsenic in the lipid extracts of marine invertebrates. Comp. Biochem. Physiol. 41B (4), 777–784. Vazquez-Nunez, R.V., Mendez, N., Green-Ritz, C., 2007. Bioaccumulation and elimination of Hg in the fireworm Eurythoe complanata (annelida: polychaeta) from, Mazatlan, Mexico. Arch. Environ. Contam. Toxicol. 52, 541–548. Wallace, W.G., Lopez, G.R., Levinton, J.S., 1998. Cadmium resistance in an oligochaete and its effect on cadmium trophic transfer to an omnivorous shrimp. Mar. Ecol. Prog. Ser. 172, 225–237. Walsh, G.E., Louie, M.K., McLaughlin, L., Lores, E.M., 1986. Lugworm (Arenicola cristata) larvae in toxicity tests: Survival and development when exposed to organotins. Environ. Toxicol. Chem. 5, 749–754. Wharfe, J.R., Van Den Broek, W.L.F., 1977. Heavy metals in macroinvertebrates and fish from the lower Medway Estuary, Kent. Mar. Pollut. Bull. 8, 31–34. Zauke, G.P., 1977. Mercury in benthic invertebrates of the Elbe estuary. Helgol. Wiss. Meeres. 29, 358–374.
This page intentionally left blank
CHAPTER 11
Echinoderms This widely distributed group includes sea urchins, sea cucumbers, starfishes, brittle stars, sand dollars, and sea lilies. These metazoan coelomates have a unique water vascular system, and all show a division of most of the body structures into five sectors commonly produced as arms or rays. Although some species tolerate a change in salinity better than others, only a few species can tolerate brackish waters. Within the sea, however, echinoderms occur anywhere between the littoral zone to depths of 6000 m or more, with the greatest number and variety between 1000 and 2000 m. Echinoderms are cosmopolitan and range from cold seas, where they are the most abundant, to the tropics where numerous colorful varieties abound. All are comparatively sluggish and can remain immobile for extended periods. Almost all are bottom dwellers, although a few highly modified species are free floating. Echinoderms are prime movers of sediments and detritus in the sea and are probably quite important in the cycling of trace metals.
11.1 Aluminum Maximum concentrations of aluminum in echinoderm field collections of 2100.0 mg Al/kg dry weight (DW) in intestine and 1000.0 mg Al/kg DW in gonad are recorded (Table 11.1). The significance of these elevated levels is imperfectly understood, but in the case of intestine this may reflect environmental sediment levels (Riley and Segar, 1970).
11.2 Antimony Antimony concentrations in whole echinoderms usually ranged between 0.01 and 0.07 mg Sb/kg DW, although one sea urchin, Arbacia lixula, inexplicably contained 5.5 mg Sb/kg DW whole animal (Table 11.2).
11.3 Arsenic It is clear from Table 11.3 that arsenic accumulates in lipids of echinoderms and that gonadal tissues of sea urchins may be useful in assessing anthropogenic arsenic contamination. Vaskovsky et al. (1972) found that arsenic content of 553
554 Chapter 11 Table 11.1: Aluminum Concentrations in Field Collections of Echinoderms Organism
Concentration
Reference
Starfish, Asterias rubens Whole Oral skin Aboral skin Pyloric ceca Gonad
<100.0 DW 230.0 DW <95.0 DW <100.0 DW <100.0 DW
1 1 1 1 1
Echinoderms; body and shell
159.0-183.0 DW
2
Echinoid, Echinus esculentus Oral shell Aboral shell Aristotle’s lantern Spines Intestines Gonad
120.0 DW 140.0 DW 160.0 DW 130.0 DW 2100.0 DW 95.0 DW
1 1 1 1 1 1
Starfish, Henricia sanguinolenta; whole
90.0 DW
1
Sea cucumber, Holothuria sp.; whole
73.0 FW
3
Starfish, Solaster papposus; whole
240.0-500.0 DW
1
Sea urchin, Spatangus purpureus Test and spines Gonad
160.0 DW 1000.0 DW
1 1
a
Values are in mg Al/kg fresh weight (FW) or dry weight (DW). a 1, Riley and Segar, 1970; 2, Culkin and Riley, 1958; 3, Matsumoto et al., 1964.
Table 11.2: Antimony Concentrations in Field Collections of Echinoderms Organism
Concentration
Sea urchin, Arbacia lixula; whole
5.5 DW
1
Starfish, Asterias rubens; whole
0.01 DW
2
Starfish, Echinaster sepositus; whole
0.02 DW
1
Sea cucumber, Holothuria tubulosa; whole
0.05 DW
1
Starfish, Marthasterias glacialis; whole
0.02-0.03 DW
1, 2
Brittle star, Ophioderma longicauda; whole
0.01 DW
1
Sea urchin, Paracentrotus lividus; whole
0.07 DW
1
Echinoid, Sphaerechinus granularis; whole
0.13 DW
1
Values are in mg Sb/kg dry weight. a 1, Papadopoulu et al., 1976; 2, Leatherland and Burton, 1974.
Reference
a
Echinoderms 555 Table 11.3: Arsenic Concentrations in Field Collections of Echinoderms Organism
Concentration
Reference
Starfish, Asterias amurensis; lipid extract, soft tissues
51,200.0 FW
1
Starfish, Asterias rubens; whole
10.0 DW
2
Sea cucumber, Cucumaria fraudatrix; lipid extract, soft tissues
10,200.0 FW
1
Starfish, Distolasterias nippon; lipid extract, soft tissues
41,800.0 (23,500.0-59,200.0) FW
1
Echinoid, Echinocardium cardatum; lipid extract, soft tissues
7900.0 FW
1
Guam; 1998-1999; 4 locations; sea cucumbers; dorsal body wall vs. hemal system; maximum concentration Bohadschia argus Holothuria atra
17.7 DW vs. 42.9 DW 23.2 DW vs. 28.3 DW
6 6
Starfish, Marthasterias glacialis; whole
5.8 DW
2
Sea urchin, Paracentrotus lividus; whole; 1991-2005; western Mediterranean Sea; Balearic Islands; Port of Mahon
1.6 (0.7-4.1) DW
7
Starfish, Patira pectinifera; lipid extract, soft tissues
17,400.0 FW
1
Starfish, Pisaster ochraceus; whole
1.3 DW
3
Sea cucumber, Stichopus japonicus; lipid extract, soft tissues
1400.0 FW
1
6.0 DW 5.6 DW 3.8 DW 1.9 DW 2.7-4.5 DW 6.8-16.0 DW
4 4 4 4 5 5
13,000.0-16,700.0 FW
1
Sea urchin, Strongylocentrotus droebachiensis Gonads; distance in meters from arsenic mining wastes outfall 0 35 157 189 Whole Gonads Sea urchin, Strongylocentrotus spp.; lipid extract, soft tissues
a
Values are in mg As/kg fresh weight (FW) or dry weight (DW). a 1, Vaskovsky et al., 1972; 2, Leatherland and Burton, 1974; 3, Gorgy et al., 1948; 4, Penrose et al., 1975; 5, Bohn, 1979; 6, Denton et al., 2006; 7, Deudero et al., 2007.
556 Chapter 11 echinoderms collected from different localities varied substantially. For example, arsenic content in lipids of sea stars, Distolasterias nippon, ranged from 23,500.0 to 59,200.0 mg As/kg fresh weight (FW), and concluded that reasons for this are essentially unknown. In addition, Vaskovsky and his colleagues report that lipids of echinoderms of the same species, but occupying different habitats, had different arsenic contents. Laboratory studies of 7 week duration on uptake and retention of arsenic by the sea urchin Strongylocentrotus droebachiensis fed arsenic-loaded algae, Fucus vesiculosus, showed that each animal, on average, consumed 0.203 mg arsenic, excreted 0.036 mg, and converted most of the arsenic in tissues to an organic form (Penrose et al., 1977). Other studies by Penrose et al. (1977) with 74As confirmed that more than half the inorganic arsenic was converted to an organic form in as little as 72 h, with up to 40% conversion in 15 min. Embryos of the sea urchin Anthocidaris crassispina developed normally in media containing 2.1 mg pentavalent As/L, but 4.2 mg/L was fatal (Kobayashi, 1971). Subsequent studies showed that seawater solutions containing 3.0 mg As/L were associated with retarded development and abnormal pluteus formation (Kobayashi, 1977).
11.4 Barium Mauchline and Templeton (1966) report that echinoderms from the Irish Sea contain between 0.2 and 1.3 mg Ba/kg FW whole organism.
11.5 Boron Embryos of a sea urchin, A. crassispina, are relatively resistant to boron as boric acid (H3BO3). Normal development occurs at 37.0 mg B/L; however, 75.0 mg B/L is fatal (Kobayashi, 1971). No data wee available on boron concentrations in field collections of echinoderms.
11.6 Cadmium Most cadmium values recorded in echinoderm tissues were less than 1.0 mg Cd/kg DW (Table 11.4). However, some species, such as the starfish Asterias rubens, frequently exceed this value, and some tissues including intestine and pyloric ceca have comparatively elevated cadmium burdens (Table 11.4). This latter observation tends to confirm the findings of Hiyama and Shimisu (1964), who demonstrate that digestive tract of the sea urchin Strongylocentrotus sp. had the highest cadmium residues of all tissues examined.
Echinoderms 557 Table 11.4: Cadmium Concentrations in Field Collections of Echinoderms Organism
Concentration
Starfish, Asterias rubens Whole Oral skin Aboral skin Pyloric ceca Gonad Whole Whole
3.7 1.7 3.6 8.7 1.5 1.6 0.2
Reference
DW DW DW DW DW DW DW
1 1 1 1 1 2 3
Starfish, Coscinasterias calamaria; whole
0.6 FW
4
Echinoderms; whole
Max. 18.0 DW
5
Echinoid, Echinus esculentus Oral shell Aboral shell Aristotle’s lantern Spines Intestines Gonad
0.7 0.3 0.2 0.7 8.9 0.7
DW DW DW DW DW DW
1 1 1 1 1 1
3.5 DW
1
0.11 DW vs. 0.39 DW 0.07 DW vs. 0.25 DW
9 9
Sea urchin, Molpadia intermedia; muscle
1.7 DW
6
Sea urchin, Paracentrotus lividus; whole; 1991-2005; Balearic Islands; Port of Mahon; western Mediterranean Sea
0.67 (0.14-1.6) DW
Starfish, Patirella regularis; whole
0.7 FW
4
Starfish, Solaster papposus; whole
4.5-5.3 DW
1
Echinoid, Spatangus purpureus Test and spines Gonad
0.1 DW 1.1 DW
1 1
Starfish, Henricia sanguinolenta; whole Guam; 1998-1999; sea cucumbers; 4 stations; dorsal body wall vs. hemal system; max. concentrations Bohadschia argus Holothuria atra
a
10
(Continues)
558 Chapter 11 Table 11.4: Cont’d a
Organism
Concentration
Sea urchin, Strongylocentrotus droebachiensis Whole Gonads
0.6-1.8 DW 0.9-1.5 DW
7 7
0.57 FW
8
Sea urchin, Strongylocentrotus transicanus; gonad
Reference
Values are in mg Cd/kg fresh weight (FW) or dry weight (DW). a 1, Riley and Segar, 1970; 2, Leatherland and Burton, 1974; 3, De Clerck et al., 1979; 4, Eustace, 1974; 5, Stenner and Nickless, 1974; 6, Thompson and Paton, 1978; 7, Bohn, 1979; 8, Vattuone et al., 1976; 9, Denton et al., 2006; 10, Deudero et al., 2007.
Laboratory studies show that seawater containing 0.35-1.41 mg Cd/L resulted in developmental abnormalities in embryos of the sea urchins A. crassispina and Hemicentrotus sp., including decreased rates of fertilization, decreased cell division during gastrulation, and increased rate of polyspermy (Kobayashi and Fujinaga, 1976). Both species developed normally in 0.18 mg Cd/L, which is substantially in excess of cadmium concentrations normally encountered in coastal waters. Death of adult starfish, A. rubens, is recorded at 0.70 mg Cd/L in starfish during exposure for 7 days (Eisler and Hennekey, 1977), and of A. crassispina embryos at 1.6 mg Cd/L within 48 h (Kobayashi, 1971).
11.7 Cerium Laboratory studies with radiocerium and the sea urchin Strongylocentrotus pulcherrimus demonstrate that cerium was concentrated in digestive tract by factors in excess of 250-fold over the ambient medium; for gonad and test, these values were 3 and 15, respectively (Hiyama and Shimisu, 1964). Addition of the chelating agent EDTA to the medium was associated with lower radiocerium values in these tissues by an order of magnitude in most cases (Hiyama and Shimisu, 1964). The fate and effects of chelated cerium is not known with certainty.
11.8 Cesium Concentrations of stable cesium in five species of representative coastal echinoderms from Greece ranged between 0.003 and 0.050 mg Cs/kg DW whole organism (Papadopoulu et al., 1976). A sixth species, the echinoid Sphaerechinus granularis, contained 0.13 mg
Echinoderms 559 Cs/kg DW whole animal (Papadopoulu et al., 1976). Radiocesium-137 levels were below the minimum detection limit in the green sea urchin, Strongylocentrotus polyacanthus, collected from the Aleutian Islands in summer 2004: the site of nuclear tests between 1965 and 1971 (Burger et al., 2007b). Accumulation of radiocesium under controlled conditions was investigated for a sea urchin, S. pulcherrimus (Hiyama and Shimisu, 1964), and an echinoid Psammechinus miliaris (Bryan, 1963). The sea urchin accumulated radiocesium from the medium in digestive tract by a factor of 9.3 in 2 days; values for gonad and test were lower: 2 for gonad and 0.4 for test. The echinoid also demonstrated radiocesium uptake over the medium in gut (28.1), followed by gonad (17.7), muscle (9.1), shell plus tube feet (4.0), teeth (1.9), and no uptake in coelomic fluid (1.0) (Bryan, 1963).
11.9 Chromium Chromium concentrations in echinoderm tissues were usually less than 1.0 mg Cr/kg DW, with the exception of samples from Puerto Rico (Table 11.5). The elevated levels (24.2-43.2 mg Cr/kg FW whole organism) seen in Echinometra and Ophiothrix from Puerto Rico were not reflected in Holothuria from the same vicinity (Table 11.5), and the former values should be interpreted with caution pending verification. Echinoderms from the United Kingdom and environs were comparatively low in chromium, with values of less than 0.46 mg Cr/kg DW whole organism recorded for Asterias, Echinus, Solaster, Porania, and Spatangus (Riley and Segar, 1970). In laboratory tests, embryos of the sea urchin, Anthocidaris sp., developed normally in seawater containing 3.2-4.2 mg Cr/L, but failed to develop at 8.4-10.0 mg Cr/L (Kobayashi, 1971; Okubo and Okubo, 1962). Larvae of Hemicentrotus sp. were more sensitive, showing abnormal development or death within 24 h at concentrations less than 1.0 mg Cr/L (Okubo and Okubo, 1962). Hexavalent chromium at 6.0 mg/L was associated with abnormal development of A. crassispina embryos (Kobayashi, 1977). Results of 7-day tests with adult starfish, A. rubens, and hexavalent chromium show that all survived at 5.0 mg/L, 50% died at 8.0 mg/L, and all died at 20.0 mg/L (Eisler and Hennekey, 1977).
11.10 Cobalt Whole sea cucumbers, Stichopus tremulus, accumulated cobalt up to 240 times over ambient seawater concentrations (Ichikawa, 1961); however, cobalt body residues were low, and probably reflected the low environmental levels. In fact, cobalt concentrations in most field collections of echinoderms were near or below analytical detection limits for cobalt, with the
560 Chapter 11 Table 11.5: Chromium Concentrations in Field Collections of Echinoderms Organism
Concentration
Reference
Sea urchin, Arbacia lixula; whole
13.0 DW
1
Starfish, Asterias rubens; whole
0.46 FW
2
Echinoid, Echinaster sepositus; whole
0.83 DW
1
Echinoderms; whole
0.03-1.2 DW
3
Sea urchin, Echinometra lacunter; whole
43.2 FW
4
Guam; 1998-1999; 4 stations; sea cucumbers; max. concentrations; dorsal body wall vs. hemal system Bohadschia argus Holothuria atra
0.43 DW vs. 31.9 DW 0.25 DW vs. 8.6 DW
8 8
Starfish, Henricia sanguinolenta; whole
0.46 DW
5
Sea cucumber, Holothuria forksalii; muscle
0.28 DW
6
Sea cucumber, Holothuria tubulosa; whole
0.8 DW
1
Starfish, Marthasterias glacialis; whole
1.6 DW
1
Sea urchin, Molpadia intermedia; muscle
2.2 DW
7
Brittle star, Ophioderma longicauda; whole
0.46 DW
1
Brittle star, Ophiothrix suensoni; whole
24.2 FW
4
Brittle star, Ophiura texturata; whole
0.8 DW
4
Sea urchin, Paracentrotus lividus Whole Whole
4.8 DW 1.6 (0.4-3.2) DW
1 9
Echinoid, Sphaerechinus granularis; whole
6.4 DW
1
Sea cucumber, Stichopus regalis; whole less gut
1.1 DW
4
a
Values are in mg Cr/kg fresh weight (FW) or dry weight (DW). a 1, Papadopoulu et al., 1976; 2, De Clerck et al., 1979; 3, Fukai and Broquet, 1965; 4, Bernhard and Zattera, 1975; 5, Riley and Segar, 1970; 6, Fukai, 1965; 7, Thompson and Paton, 1978; 8, Denton et al., 2006; 9, Deudero et al., 2007.
possible exceptions of gonad and pyloric ceca tissues (Table 11.6). Radiocobalt-60 levels were not detectable in sea urchins collected from the Aleutian Islands during 2004 near sites used in nuclear tests from 1965 to 1971 (Burger et al., 2007b). In the laboratory, it was shown that embryos of a sea urchin A. crassispina developed normally in seawater solutions containing 17.0 mg Co/L as cobalt acetate; however, 170.0 mg Co/L was fatal (Kobayashi, 1971).
Echinoderms 561 Table 11.6: Cobalt Concentrations in Field Collections of Echinoderms Organism
Concentration
Reference
Starfish, Asterias rubens Whole Oral skin Aboral skin Pyloric ceca Gonad
<0.3 DW <0.3 DW <0.3 DW 2.1 DW 0.6 DW
1 1 1 1 1
Echinoderms; whole 3 spp. 7 spp.
<0.2-1.0 DW 0.09-0.66 DW
1 2
Echinoid, Echinus esculentus Gonad Other tissues
0.4 DW <0.3 DW
1 1
Echinoid, Spatangus purpureus Test and spines Gonad
<0.2 DW 0.5 DW
1 1
a
Values are in mg Co/kg dry weight (DW). a 1, Riley and Segar, 1970; 2, Papadopoulu et al., 1976.
11.11 Copper Maximum copper concentrations measured in echinoderm body parts, in mg/kg, were 31.4 in whole starfish on a FW basis, 90.0 DW in body and shell, and 324.0 ash weight (AW) in sea urchin sperm (Table 11.7). Copper concentrations in echinoderms, when compared to other marine invertebrate groups examined (except coelenterates) were low, suggesting sensitivity to this metal (Eisler, 1979). Laboratory studies with eggs of sea urchins, Hemicentrotus pulcherrimus and A. crassispina, showed that development was normal at 0.04-0.08 mg Cu/L, but higher levels of 0.08-0.16 mg/L inhibited development (Kobayashi and Fujinaga, 1976). Sensitivity of sea urchin sperm and eggs to copper was investigated by Kobayashi (1980); sperm activity was inhibited at low sublethal copper concentrations, and fertilization and gastrulation stages were more sensitive to copper than were first cleavage, blastulation, and pluteus stages. Abnormal development was observed at concentrations as low as 0.06 mg Cu/L (Kobayashi, 1977). Copper was more toxic to sperm of the sea urchin, Paracentrotus lividus (EC50 of 0.018 mg Cu/L) than embryos (0.046 mg Cu/L); however, mixtures of copper, triazines, and dimethylureas interact significantly on spermotoxicity and embryotoxicity (Manzo et al., 2008). Mixtures of copper and zinc or copper and cadmium produced more than additive
562 Chapter 11 Table 11.7: Copper Concentrations in Field Collections of Echinoderms Organism
Concentration
Reference
Starfish, Asterias rubens Whole Whole Oral skin Aboral skin Pyloric ceca Gonad
18.8 FW 4.3 DW 2.5 DW 2.0 DW 16.0 DW 4.1 DW
1 2 2 2 2 2
Starfish, Coscinasterias calamaria; whole
10.4 FW
3
Echinoderms Body and shell Whole
20.0-90.0 DW Max. 18.0 DW
4 3, 5
Echinoid, Echinus esculentus Oral shell Aboral shell Aristotle’s lantern Spines Intestines Gonad
1.8 DW 0.9 DW 0.4 DW 1.6 DW 5.9 DW 16.0 DW
2 2 2 2 2 2
Starfish, Henricia sanguinolenta; whole
8.2 DW
2
Sea cucumber, Holothuria sp.; whole
1.9 FW
6
Sand dollar, Mellita lata; whole
6.0-8.2 FW; 10.0-14.0 DW; 11.0-15.0 AW
7
Sand dollar, Mellita sexiesperforata; whole
5.0-20.0 FW; 9.4-38.0 DW; 10.0-40.0 AW
7
Sea urchin, Molpadia intermedia; muscle
26.0 DW
8
Sea urchin, Paracentrotus lividus; whole; 1991-2005; Balearic Islands, Port of Mahon; western Mediterranean Sea
4.9 (1.6-7.5) DW
12
Asteroid, Pisaster brevispinus; California Gonad Hepatic caecum Stomach
2.0-10.0 DW 18.0-36.0 DW 5.0-40.0 DW
11 11 11
Starfish, Patiriella regularis; whole
31.4 FW
3
Sea urchin, Pseudocentrotus depressus Spermatozoa homogenate Spermatozoa head
17.0-19.0 AW 0.0 AW
9 9
a
(Continues)
Echinoderms 563 Table 11.7: Organism Spermatozoa mid-piece Spermatozoa tail
Cont’d
Concentration
Reference
257.0-324.0 AW 0.0 AW
9 9
Starfish, Solaster papposus; whole
6.1-11.0 DW
2
Echinoid, Spatangus purpureus Test and spines Gonad
1.2 DW 8.7 DW
2 2
Sea urchin, Strongylocentrotus droebachiensis Whole Gonad
2.3-4.0 DW 3.3-9.0 DW
a
10 10
Values are in mg Cu/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, De Clerck et al., 1979; 2, Riley and Segar, 1970; 3, Eustace, 1974; 4, Culkin and Riley, 1958; 5, Stenner and Nickless, 1974; 6, Matsumoto et al., 1964; 7, Lowman et al., 1966; 8, Thompson and Paton, 1978; 9, Morisawa and Mohri, 1972; 10, Bohn, 1979; 11, Jenkins, 1980; 12, Deudero et al., 2007.
effects in suppressing embryonic development of sea urchins than could be predicted on the basis of individual metals; however, copper-nickel mixtures acted additively (Kobayashi and Fujinaga, 1976). In another study with sea urchins, adults of the comparatively sensitive Strongylocentrotus nudus were held in seawater containing 0.025 mg Cu/L for 30 days and the resultant embryos reared in uncontaminated seawater for 30 days (Durkina and Evtushenko, 1991). Food consumption of adults decreased after day 16; there was accelerated development of pluteal stages; and all developmental stages had increased activities of acid phosphatase (Durkina and Evtushenko, 1991). Recent studies (Rosen et al., 2008) with eggs and larvae of the purple sea urchin, Strongylocentrotus purpuratus, related whole body residues to effects. For example, controls exposed for up to 96 h to 0.0025 mg Cu/L contained up to 3.7 mg Cu/kg DW; higher concentrations up to 0.0091 mg Cu/L produced whole body residues up to 23.8 mg Cu/kg DW but with no observable adverse effects. Adverse effects on normal larval development were associated with 0.014-0.021 mg Cu/L and whole body residues of 108.0-192.0 mg Cu/kg DW (Rosen et al., 2008).
11.12 Europium Radioeuropium-152 levels in sea urchins from the Aleutian Islands in summer 2004 were below detection limits; collection locales were near the site of three nuclear tests conducted between 1965 and 1971 (Burger et al., 2007b).
564 Chapter 11
11.13 Gallium Culkin and Riley (1958) report values of 0.02-0.35 mg Ga/kg DW in body and shell of echinoderms from the Irish Sea and environs.
11.14 Iron Echinoderms accumulate radioiron to relatively high levels over ambient seawater: concentration factors were 1000 in intestine of the sea cucumber Stichopus japonicus, 78,000 in whole Stichopus, and 10,000 in ovary of the sea urchin A. crassispina (Ichikawa, 1961). Concentrations of stable iron in echinoderms are quite variable (Table 11.8). It is possible that the grossly elevated iron burdens reported in intestine and whole body of some organisms may reflect anthropogenic contamination of sediments. Iron, as was true of copper, is comparatively abundant in the mid-piece section of spermatozoa from the sea urchin Pseudocentrotus depressus when compared to other portions of the spermatozoan (Table 11.8), but the significance of this observation is not clear. Embryonic development of larval sea urchins proceeds normally at 3.2 mg Fe/L; however, developmental abnormalities occur at 10.0 mg Fe/L and higher (Okubo and Okubo, 1962).
Table 11.8: Iron Concentrations in Field Collections of Echinoderms Organism
Concentration
Sea urchin, Arbacia lixula; whole
620.0 DW
1
Starfish, Asterias rubens Whole Oral skin Aboral skin Pyloric ceca Gonad
37.0 18.0 21.0 87.0 19.0
2 2 2 2 2
Echinoid, Echinaster sepositus; whole
170.0 DW
1
Echinoid, Echinus esculentus Oral shell Aboral shell Aristotle’s lantern Spines Intestines Gonad
6.9 DW 2.5 DW 1.6 DW 16.0 DW 22,000.0 DW 15.0 DW
2 2 2 2 2 2
Echinoderms; body and shell
149.0-1700.0 DW
3
DW DW DW DW DW
Reference
a
(Continues)
Echinoderms 565 Table 11.8:
Cont’d
Organism
Concentration
Reference
Sea urchin, Echinometra lucunter; skeleton
35.0-38.0 DW
4
Starfish, Henricia sanguinolenta; whole
1800.0 DW
2
Sea cucumber, Holothuria sp.; whole
50.0 FW
5
Sea cucumber, Holothuria tubulosa; whole
74.0 DW
1
Starfish, Marthasterias glacialis; whole
110.0 DW
1
Brittle star, Ophioderma longicauda; whole
130.0 DW
1
Sea urchin, Paracentrotus lividus; whole
600.0 DW
1
Sea urchin, Pseudocentrotus depressus; spermatozoa Homogenate Head Mid-piece Tail
194.0-219.0 AW 201.0-222.0 AW 1171.0-1465.0 AW 88.0-140.0 AW
6 6 6 6
Starfish, Solaster papposus; whole
170.0-200.0 DW
2
Echinoid, Spatangus purpureus Test and spines Gonad
53.8 DW 19.2 DW
2 2
Echinoid, Sphaerechinus granularis; whole
1100.0 DW
1
Sea urchin, Strongylocentrotus droebachiensis; collected various distances from Zn/Pb mine 1 km; whole 15 km; whole vs. gonads
1310.0 DW 495.0 DW vs. 217.0 DW
7 7
Sea urchin, Tripneustes esculentus; skeleton
53.0-81.0 DW
4
a
Values are in mg Fe/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Papadopoulu et al., 1976; 2, Riley and Segar, 1970; 3, Culkin and Riley, 1958; 4, Stevenson and Ufret, 1966; 5, Matsumoto et al., 1964; 6, Morisawa and Mohri, 1972; 7, Bohn, 1979.
11.15 Lead The elevated concentrations of lead in echinoderms from the western Norway coast (up to 460.0 mg Pb/kg DW; Stenner and Nickless, 1974) and Japan (14.4 mg/kg FW; Matsumoto et al., 1964) were probably associated with human activities. In contrast, echinoderms from the United Kingdom showed much lower lead burdens (Table 11.9).
566 Chapter 11 Table 11.9: Lead Concentrations in Field Collections of Echinoderms Organism
Concentration
Starfish, Asterias rubens Whole Oral skin Aboral skin Pyloric ceca Gonad Whole
2.3 1.1 1.1 4.0 0.5 1.6
DW DW DW DW DW FW
Reference 1 1 1 1 1 5
Echinoderms; whole; West Norway coast
Max. 460.0 DW
2
Starfish, Henricia sanguinolenta; whole
<0.5 DW
1
Sea cucumber, Holothuria sp.; whole
14.4 FW
3
Sea urchin, Molpadia intermedia; muscle
1.4 DW
4
20.0 DW 42.0 DW 3.0 (0.8-6.7) DW
6 6 7
5.2-6.8 DW
1
Sea urchin, Paracentrotus lividus Italy; soft parts Reference site Polluted site Western Mediterranean Sea; whole; 1991-2005 Starfish, Solaster papposus; whole
a
Values are in mg Pb/kg fresh weight (FW) or dry weight (DW). a 1, Riley and Segar, 1970; 2, Stenner and Nickless, 1974; 3, Matsumoto et al., 1964; 4, Thompson and Paton, 1978; 5, De Clerck et al., 1979; 6, Sheppard and Bellamy, 1974; 7, Deudero et al., 2007.
Kobayashi (1971) reports that embryos of a sea urchin, A. crassispina, develop normally in seawater containing 1.1 mg Pb/L as lead acetate, but do not develop at 2.2 mg Pb/L.
11.16 Manganese Most values were less than 57.0 mg Mn/kg on a DW basis (Table 11.10). Where interspecies comparisons were possible, elevated levels were recorded in gonad, aboral skin, and Aristotle’s lantern (Table 11.10). A sea cucumber, Stichopus regalis, took up radiomanganese from seawater by a factor of about 200-fold (Ichikawa, 1961), suggesting a need for this metal by Stichopus. On the other hand, high burdens of manganese inhibited motility of sperm of the sea urchin Arbacia punctulata; sperm motility was restored with the addition of
Echinoderms 567 Table 11.10: Manganese Concentrations in Field Collections of Echinoderms Organism
Concentration
Reference
Starfish, Asterias rubens Whole Oral skin Aboral skin Pyloric ceca Gonad
6.5 DW 8.2 DW 11.0 DW 2.3 DW 3.7 DW
1 1 1 1 1
Starfish, Coscinasterias calamaria; whole
6.9 FW
2
Sea urchin, Echinometra lucunter; skeleton
20.0-21.0 DW
3
Echinoid, Echinus esculentus Oral shell Aboral shell Aristotle’s lantern Spines Intestines Gonad
56.0 DW 57.0 DW 88.0 DW 4.5 DW 11.0 DW 0.5 DW
1 1 1 1 1 1
Starfish, Henricia sanguinolenta; whole
34.0 DW
1
Sea cucumber, Holothuria tubulosa; whole
8.9 AW
4
Starfish, Patiriella regularis; whole
51.7 FW
2
Starfish, Solaster papposus; whole
31.0-43.0 DW
1
Echinoid, Spatangus purpureus Test and spines Gonad
27.0 DW 82.0 DW
1 1
Sea urchin, Tripneustes esculentus; skeleton
13.0-14.0 DW
3
a
Values are in mg Mn/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Riley and Segar, 1970; 2, Eustace, 1974; 3, Stevenson and Ufret, 1966; 4, Chipman and Thommeret, 1970.
EDTA, a chelating agent (Young and Nelson, 1974). Comparatively high concentrations of manganese, that is 6.6-10.0 mg/L, do not interfere with embryonic development of sea urchins, Anthocidaris spp.; however, higher concentrations of 13.2-32.0 mg Mn/L adversely affect growth and survival (Kobayashi, 1971; Okubo and Okubo, 1962). Manganese occurs naturally in marine sediments as manganese dioxide (MnO2); however, during hypoxic conditions it is converted to the bioavailable Mn2+and can be accumulated by starfish, A. rubens (Oweson et al., 2008). Starfish exposed to 5.5 mg Mn/L in the laboratory for up to 25 days showed cytotoxicity and adverse effects on immune mechanisms that suppress defense against pathogens (Oweson et al., 2008).
568 Chapter 11
11.17 Mercury Mercury concentrations in echinoderms from nonpolluted areas never exceed 0.40 mg Hg/kg on a FW basis or 0.92 mg Hg/kg on a DW basis (Eisler, 1981; Table 11.11). Mercury contamination from a chloralkali plant in Cuba was reflected in elevated soil mercury concentrations and its terrestrial vegetation, and in sediments and gonads of benthic fauna from these sediments (Table 11.11). Mercury contamination is measurable for at least 5 km from the chloralkali pant (Gonzalez, 1991). Asteroids from a mercury-contaminated site in
Table 11.11: Mercury Concentrations in Field Collections of Echinoderms Organism
Concentration
Reference
Starfish, Asterias rubens Whole Whole
0.22 DW 0.12 FW
1 2
Asteroids; 4 spp.; Golfo Triste, Venezuela; 1981; mercury-contaminated in 1980 Stomach contents Exoskeleton Gonads
0.17-2.2 FW; 0.53-7.3 DW 0.59-2.0 FW; 2.2-7.3 DW 0.88-1.6 FW; 3.8-8.7 DW
8 8 8
Echinoderms; whole
0.28-0.40 FW
3
Sea urchin, Lytechinus variegatus; gonads; Cuba; 1985-1987; near chloralkali plant Near discharge Transition area Reference site
0.38 DW 0.29 DW 0.07 DW
5 5 5
Starfish, Marthasterias glacialis; whole
0.92 FW
1
Sea urchin, Paracentrotus lividus; whole; western Mediterranean Sea; Balearic Islands; Port of Mahon
0.14 (0.03-0.38) DW
6
Sea urchin, Strongylocentrotus fragilis; gonads; total mercury vs. organic mercury
0.020-0.034 FW vs. 0.003 FW
4
Green sea urchin, Strongylocentrotus polyacanthus; edible portions; Aleutian Islands; 2004
0.005 FW; max. 0.016 FW
7
a
Values are in mg Hg/kg fresh weight (FW) or dry weight (DW). a 1, Leatherland and Burton, 1974; 2, De Clerck et al., 1979; 3, Williams and Weiss, 1973; 4, Eganhouse and Young, 1978; 5, Gonzalez, 1991; 6, Deudero et al., 2007; 7, Burger et al., 2007a; 8, Iglesias and Penchaszadeh, 1983.
Echinoderms 569 Venezuela had comparatively high concentrations in stomach when compared to exoskeleton, and elevated concentrations in tissues of inshore specimens when compared to offshore conspecifics (Iglesias and Penchaszadeh, 1983). Sea urchin development is arrested at concentrations exceeding 0.010-0.023 mg inorganic Hg/L (Kobayashi, 1971; Okubo and Okubo, 1962), with a high proportion of abnormal plutei at 0.03 mg Hg/L (Kobayashi, 1977). Effects were more pronounced at similar concentrations of organic mercury salts (Kobayashi, 1971). Mercury inhibits the motility of spermatozoa of a sea urchin, A. punctulata (Young and Nelson, 1974). This effect was reversed by EDTA. EDTA alone can block motility by complexing essential seawater cations, but may also deplete intracellular regulatory cations, which otherwise may exist in a state of dynamic equilibrium with seawater (Young and Nelson, 1974).
11.18 Molybdenum The starfish, A. rubens, is relatively resistant to molybdenum salts. Concentrations from 127.0 to 254.0 mg Mo/L were necessary to kill 50% in 24 h, with mortality higher at the lower end of the pH range tested of 5.8-8.2 (Abbott, 1977).
11.19 Nickel Echinoderms collected from Puerto Rico, including Echinometra and Tripneustes, contained up to 10 times more nickel than did asteroids and echinoids from Britain (Table 11.12). It is not known if these differences are real, or to differences in sample collection, digestion, and analysis procedures. Laboratory studies with Japanese sea urchins suggest that ambient seawater concentrations up to 0.18 mg Ni/L do not affect embryonic development; however, 0.37-1.47 mg Ni/L inhibited development in as little as 15 h (Kobayashi and Fujinaga, 1976). Research on other species demonstrate that concentrations as low as 0.058 mg Ni/L adversely affects development of embryos of the sea urchin, Lytechinus pictus (Timourian and Watchmaker, 1972; USEPA, 1980a), that 0.059 mg Ni/L inhibits motility of sperm of the purple sea urchin Strongylocentrotus purpurea (Timourian and Watchmaker, 1977), and that death of adults of the starfish, Asterias forbesi, and the sea urchin A. punctulata occur at comparatively elevated concentrations of 13.0-17.0 mg Ni/L (Eisler and Hennekey, 1977; USEPA, 1980a).
11.20 Plutonium Echinoderms from Bylot Sound, Greenland, had elevated levels of radioplutonium following accidental release of that element from military nuclear missiles when a bomber crashed at that site (Aarkrog, 1971). Half-time retention of 239 þ 240Pu in brittle stars is estimated at 50 years (Aarkrog, 1990).
570 Chapter 11 Table 11.12: Nickel Concentrations in Field Collections of Echinoderms Organism
Concentration
Starfish, Asterias rubens Whole Oral skin Aboral skin Pyloric ceca Gonad
1.5 0.8 0.7 4.1 2.4
Rock boring sea urchin, Echinometra lucunter Skeleton Puerto Rico; skeleton vs. whole
49.0-59.0 DW 51.0 (42.0-78.0) DW vs. 37.0 DW
2 3
Echinoid, Echinus esculentus Spines Gonad Other tissues
1.6 DW 7.7 DW <0.2 DW
1 1 1
30.0 DW
4
40.0 DW
4
Starfish, Henricia sanguinolenta; whole
3.7 DW
1
Sea urchin, Paracentrotus lividus; whole; 1991-2005; western Mediterranean Sea; Balearic Islands; Port of Mahon
1.7 (0.8-2.7) DW
5
Starfish, Solaster papposus; whole
2.3-4.0 DW
1
Echinoid, Spatangus purpureus Test and spines Gonad
<0.2 DW 1.4 DW
1 1
Sea urchin, Tripneustes esculentus Skeleton Ovary Testes
35.0 (18.0-54.0) DW 1.4 FW 22.0 FW
2, 3 3 3
Florida; near sewage outfall; exposure for 120 days Sea urchin, Lytechinus variegatus; whole Sea cucumber, Holothuria mexicana; whole
DW DW DW DW DW
Reference
a
1 1 1 1 1
Values are in mg Ni/kg fresh weight (FW) or dry weight (DW). a 1, Riley and Segar, 1970; 2, Stevenson and Ufret, 1966; Jenkins, 1980; 4, Montgomery et al., 1978; 5, Deudero et al., 2007.
Echinoderms 571
11.21 Rubidium Representative species of adult echinoderms from the Aegean Sea contained between 0.9 and 4.7 mg Rb/kg DW whole organism (Table 11.13).
11.22 Scandium Adults of six species of echinoderms found in the Aegean Sea contained 0.005-0.051 mg Sc/kg DW whole organism (Papadopoulu et al., 1976). A seventh species, S. granularis, contained 0.171 mg Sc/kg DW whole adult (Papadopoulu et al., 1976), and this may be related to the comparatively high concentrations of iron, chromium, and other metals found in that same sample.
11.23 Selenium Concentrations of selenium in whole adults of seven species from coastal waters of Greece ranged from 0.8 to 4.4 mg Se/kg DW (Table 11.14).
11.24 Silver Silver concentrations in almost all species of echinoderms examined were either low, nondetectable, or near the limits of analytical detection (Table 11.15). The comparatively high value of 0.6 mg Ag/kg DW in whole Henricia is indicative of the high body burdens of other metals reported in this species (Riley and Segar, 1970). Silver concentrations of 7.3 mg Ag/kg DW in whole Marthasterias and 4.9 mg/kg DW in hemal system of Holothuria atra (Table 11.15) requires confirmation. Table 11.13: Rubidium Concentrations in Field Collections of Echinoderms Organism
Concentration
Sea urchin, Arbacia lixula; whole
2.6 DW
1
Echinoid, Echinaster sepositus; whole
0.9 DW
1
Sea cucumber, Holothuria tubulosa; whole
2.0 DW
1
Starfish, Marthasterias glacialis; whole
2.1 DW
1
Brittle star, Ophioderma longicauda; whole
1.8 DW
1
Sea urchin, Paracentrotus lividus; whole
4.7 DW
1
Echinoid, Sphaerechinus granularis; whole
3.5 DW
1
Values are in mg Rb/kg dry weight (DW). a 1, Papadopoulu et al., 1976.
Reference
a
572 Chapter 11 Table 11.14: Selenium Concentrations in Field Collections of Echinoderms Organism
Concentration
Reference
Sea urchin, Arbacia lixula; whole
2.4 DW
1
Echinoid, Echinaster sepositus; whole
4.4 DW
1
Sea cucumber, Holothuria tubulosa; whole
3.4 DW
1
Starfish, Marthasterias glacialis; whole
3.0 DW
1
Brittle star, Ophioderma longicauda; whole
1.9 DW
1
Sea urchin, Paracentrotus lividus; whole
1.1 DW
1
Echinoid, Sphaerechinus granularis; whole
0.8 DW
1
a
Values are in mg Se/kg dry weight (DW). a 1, Papadopoulu et al., 1976.
Table 11.15: Silver Concentrations in Field Collections of Echinoderms Organism
Concentration
Reference
Sea urchin, Arbacia lixula; whole
0.30 DW
1
Starfish, Asterias rubens All tissues
Not detectable
2
Echinoid, Echinaster sepositus; whole
0.25 DW
1
Echinoid, Echinus esculentus Oral shell Aboral shell Aristotle’s lantern Spines Intestine Gonad
0.09 DW <0.05 DW 0.53 DW <0.03 DW <0.8 DW <0.03 DW
2 2 2 2 2 2
Guam; 1998-1999; 4 stations; sea cucumbers; max. concentrations; dorsal body wall vs. hemal system Bohadschia argus Holothuria atra
<0.14 DW vs.<0.14 DW 0.24 DW vs. 4.9 DW
4 4
Starfish, Henricia sanguinolenta; whole
0.6 DW
2
Sea cucumber, Holothuria tubulosa; whole
0.05 DW
1
Starfish, Luidia clathrata; Tampa Bay, Florida vs. Gulf of Mexico; 1982 Body wall Pyloric ceca
0.26-0.84 DW vs. 0.67 DW 0.4-1.1 DW vs. 0.17 DW
3 3
a
(Continues)
Echinoderms 573 Table 11.15:
Cont’d
Organism
Concentration
Starfish, Marthasterias glacialis; whole
7.3 DW
1
Brittle star, Ophioderma longicauda; whole
0.07 DW
1
0.32 DW 1.7 (0.2-6.8) DW
1 5
0.32 DW
1
Sea urchin, Paracentrotus lividus Whole Whole; 1991-2005; western Mediterranean Sea; Balearic Islands; Port of Mahon Echinoid, Sphaerechinus granularis; whole
Reference
a
Values are in mg Ag/kg dry weight (DW). a 1, Papadopoulu et al., 1976; 2, Riley and Segar, 1970; 3, Lawrence et al., 1993; 4, Denton et al., 2006; 5, Deudero et al., 2007.
Silver accumulates in eggs of the sea urchin Diadema antillarum (Bianchini et al., 2007). In that study, sea urchins were exposed to 0.001 or 0.01 mg Ag/L for 48 h. Silver burdens were highest in eggs (20.0-30.0 mg Ag/kg FW), tube feet (5.0 mg/kg FW in the highdose group), and less than 2.0 mg Ag/kg FW in other tissues, including muscle and hemolymph. The effects of these concentrations on reproduction are unknown (Bianchini et al., 2007). Ionic silver at 0.0005 mg/L reportedly inhibits embryo development of the sea urchin, A. lixula, after 52 h (USEPA, 1980b). In 30-day tests, all adults survived 0.019 mg/L of dissolved silver (about 0.000029 ionic Ag/L); only 75% survived 0.033 mg/L of dissolved silver (about 0.000049 mg ionic Ag/L; Ward et al., 2006). Sea urchin sperm (0.000014 mg/L) and embryos (0.000028 mg/L) were more sensitive to ionic silver in 1 h and 48 h tests, respectively, than were adults in 30-day tests (Ward et al., 2006).
11.25 Strontium Strontium was especially abundant in shell and other hard tissues of echinoderms, and comparatively low in soft tissues (Table 11.16). In this respect, it probably follows calcium levels with which it is closely and positively associated. Variability in strontium accumulations among echinoderm species may be associated with variability between species in ability to accumulate strontium from seawater; interspecies echinoderm strontium concentration factors from seawater range from 0.4 to 2.0 (Ichikawa, 1961; Hiyama and Shimisu, 1964). Strontium is the most abundant trace element in disk and arm tissue of brittle stars, Ophiothrix spiculata, collected from San Diego Bay, California, in summer 2001 (Deheyn and Latz, 2006). In order of decreasing concentration in disc, strontium was followed by iron, aluminum, zinc, tin, nickel, lead, manganese, arsenic, selenium, titanium, copper, silver, chromium, and cadmium; for arm, this order was strontium, iron, zinc, aluminum, tin,
574 Chapter 11 Table 11.16: Strontium and Tin Concentrations in Field Collections of Echinoderms Element and Organism
Concentration
Reference
a
Strontium Starfish, Asterias rubens Whole Oral skin Aboral skin Pyloric ceca Gonad
390.0 DW 600.0 DW 520.0 DW <17.0 DW 18.0 DW
1 1 1 1 1
Echinoderms Whole, 4 spp. Body and shell
700.0-2500.0 AW 2.3-8.8 FW
2 3
Echinoid, Echinus esculentus Oral shell Aboral shell Aristotle’s lantern Spines Intestines Gonad
930.0 DW 820.0 DW 920.0 DW 760.0 DW 150.0 DW 20.0 DW
1 1 1 1 1 1
Starfish, Henricia sanguinolenta; whole
200.0 DW
1
Starfish, Solaster papposus; whole
260.0-490.0 DW
1
Echinoid, Spatangus purpureus Test and spines Gonad
1100.0 DW <19.0 DW
1 1
0.0053 0.0047 0.0003 0.0003
4 4 4 3
Tin Sea urchin; edible portions; France; 2005; organotins Total organotins Butyltins Phenyltins Octyltins
FW FW FW FW
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Riley and Segar, 1970; 2, Fukai et al., 1962; 3, Mauchline and Templeton, 1966; 4, Guerin et al., 2007.
manganese, lead, arsenic, copper, nickel, silver, titanium, selenium, cadmium, and chromium (Deheyn and Latz, 2006). Radiostrontium-90 levels were below detection limits in green sea urchins, S. polyacanthus, collected in summer 2004 from the Aleutian Islands near the sites of nuclear tests conducted between 1965 and 1971 (Burger et al., 2007b).
Echinoderms 575
11.26 Technetium No detectable levels of radiotechnetium-99 were found in sea urchins collected during June-July 2004 in the Aleutian Islands from the vicinity of nuclear tests conducted in 1965-1971 (Burger et al., 2007b).
11.27 Tin Edible portions of sea urchins sold for human consumption in France in 2005 had low organotin content (0.0053 mg/kg FW), of which 89% was butyltins (Table 11.16); tributyltins comprised 62% of all organotins (Guerin et al., 2007). Suppression of regeneration in echinoderms by organotins is due mainly to the neurotoxicological action of organotins, and secondarily due to direct action on tissue at the breakage point (Walsh et al., 1986). Arm regeneration in a brittle star, Ophioderma brevispina, was inhibited at 0.001 mg Sn (as tributyltin)/L (Walsh et al., 1986). Tributyltin chloride, at 0.007 mg Sn/L, resulted in 50% immobilization of sperm of the sea urchin, A. crassispina (Shim et al., 2006). Tributyltin chloride was the most toxic of all organotins tested to sea urchin sperm, followed by triphenyltin chloride, dibutyltin chloride, monophenyltin chloride, trimethyltin chloride, diphenyltin chloride, monobutyltin chloride, and dimethyltin dichloride, in that order; the same general order of toxicity was observed for egg development (Shim et al., 2006).
11.28 Zinc Zinc concentrations greater than 100.0 mg/kg DW in various tissues were not unusual (Table 11.17), supporting a conclusion that zinc was not limiting among echinoderms and probably accumulated in excess of the organism’s immediate needs. Despite the comparatively high accumulations of zinc in echinoderms, several investigators have demonstrated that relatively low seawater concentrations of <0.0065 mg Zn/L were associated with developmental abnormalities and other adverse effects, including reduced semen production in sea urchins and starfish and reduced sperm pH and motility (Clapper et al., 1985a,b). At 0.023 mg Zn/L for 5 days, embryos of the purple sea urchin, S. purpuratus, experienced 50% inhibition of development (USEPA, 1987); similar results were observed at 0.097-0.107 mg/L in only 96 h (Phillips et al., 1998). At 0.028 mg Zn/L for 60 min, sperm of the sand dollar, Dendraster excentricus, had a 50% reduction in fertilization success (USEPA, 1987). This may be a case of nutritional zinc deficiency, which has been induced experimentally in echinoderms (Eisler, 2000). Concentrations of zinc, in mg/L, which inhibited echinoderm embryogenesis were 0.065-0.65 in P. miliaris (Cleland, 1953); 0.06-0.41 in A. crassispina (Okubo and Okubo, 1962; Kobayashi, 1977; Kobayashi and
576 Chapter 11 Table 11.17: Zinc Concentrations in Field Collections of Echinoderms Organism
Concentration
Starfish, Asterias rubens Whole Oral skin Aboral skin Pyloric ceca Gonad Whole Whole
190.0 DW 110.0 DW 110.0 DW 160.0 DW 360.0 DW 220.0 DW 56.6 FW
1 1 1 1 1 2 3
Starfish, Coscinasterias calamaria; whole
40.6 FW
4
Echinoderms Whole Whole, 7 spp. Various species; whole
40.6 FW 16.0-120.0 DW Usually 100.0 DW or lower; frequently >100.0 DW; max. 245.0 FW, 1500.0 DW
Reference
a
5 6 12
Echinoid, Echinus esculentus Oral shell Aboral shell Aristotle’s lantern Spines Intestines Gonad
110.0 DW 12.0 DW 22.0 DW 28.0 DW 550.0 DW 110.0 DW
1 1 1 1 1 1
Starfish, Henricia sanguinolenta; whole
240.0 DW
1
Sea cucumber, Holothuria sp.; whole
8.7 FW
7
Sand dollar, Mellita lata; whole
31.0-130.0 FW; 54.0-220.0 DW; 57.0-240.0 AW
8
Sand dollar, Mellita sexiesperforata; whole
24.0-56.0 FW; 43.0-83.0 DW; 46.0-88.0 AW
8
Sea urchin, Molpadia intermedia; whole
171.0 DW
9
Sea urchin, Paracentrotus lividus; whole; 1991-2005; western Mediterranean Sea; Balearic Islands; Port of Mahon
40.3 (5.7-74.5) DW
Starfish, Patiriella regularis; whole
245.0 FW
Sea urchin, Pseudocentrotus depressus; spermatozoa Homogenate Head
66.0-79.0 AW 34.0-41.0 AW
13
4
10 10 (Continues)
Echinoderms 577 Table 11.17: Organism Mid-piece Tail Microtubules
Cont’d
Concentration
Reference
281.0-337.0 AW 172.0-186.0 AW 118.0-142.0 AW
10 10 10
Starfish, Solaster papposus; whole
120.0-130.0 DW
1
Echinoid, Spatangus purpureus Test and spines Gonad
35.0 DW 170.0 DW
1 1
Sea urchin, Strongylocentrotus droebachiensis Whole; 1 km from zinc ore tailings vs. 15 km Gonads; 15 km from zinc ore tailings
57.0 DW vs. 34.0 DW
11
153.0 DW
11
a
Values are in mg Zn/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Riley and Segar, 1970; 2, Leatherland and Burton, 1974; 3, De Clerck et al., 1979; 4, Eustace, 1974; 5, Stenner and Nickless, 1974; 6, Papadopoulu et al., 1976; 7, Matsumoto et al., 1964; 8, Lowman et al., 1966; 9, Thompson and Paton, 1978; 10, Morisawa and Mohri, 1972; 11, Bohn, 1979; 12, Young et al., 1980; 13, Deudero et al., 2007.
Fujinaga, 1976; Nakamura et al., 1989); and 0.2 for Henricia pulcherrimus (Kobayashi and Fujinaga, 1976). Zinc inhibits the formation of the fertilization membrane in sea urchin eggs by interfering with cortical granule-derived proteases and proteins (Nakamura et al., 1989). At 0.24 mg/L, female adults of the starfish, A. rubens, showed increased steroid metabolism in pyloric ceca after 21 days (Voogt et al., 1987). Adults of the starfish, A. rubens, survived exposure to 1.0 mg Zn/L for 168 h; however, 50% died at 2.3 mg/L in 168 h (Eisler and Hennekey, 1977). Bioconcentration factors for stable zinc and echinoderms were comparatively low, and usually ranged between 15 and 500 (Eisler, 1980). Sea cucumbers, S. tremulus, took up radiozinc-65 from solution by a factor of 1400 (Ichikawa, 1961), suggesting that the ambient medium is an important route of zinc intake. However, concentration factors based on 65Zn accumulation data should be viewed with reservation as the addition of stable zinc substantially reduced radiozinc burdens in echinoderm viscera, sometimes by an order of magnitude (Hiyama and Shimisu, 1964). Diet and water depth influence zinc accumulations in echinoderms. Carey (1970) stated that certain detrital feeders contain more zinc than carnivores, and that species which feed near the surface contain more zinc per unit weight than sediment feeders. Further, Carey (1970) found lower zinc concentrations in echinoderms collected offshore in deeper waters when compared to conspecifics collected inshore. To protect important species of marine animals, the United States Environmental Protection Agency (USEPA) proposed that total recoverable zinc in seawater should average less
578 Chapter 11 than 0.058 mg/L and never exceed 0.17 mg/L; for acid-soluble zinc, these values are <0.086 and 0.095 mg/L (USEPA, 1987). As shown earlier, adverse effects of zinc to echinoderms are documented at 0.023-0.028 mg Zn/L, suggesting re-examination of these proposed criteria.
11.29 Literature Cited Aarkrog, A., 1971. Radiological investigations of plutonium in an Arctic marine environment. Health Phys. 20, 31–47. Aarkrog, A., 1990. Environmental radiation and radiation releases. Int. J. Radiat. Biol. 57, 619–631. Abbott, O.J., 1977. The toxicity of ammonium molybdate to marine invertebrates. Mar. Pollut. Bull. 8, 204–205. Bernhard, M., Zattera, A., 1975. Major pollutants in the marine environment. In: Pearson, E.A., Frangipane, R. (Eds.), Marine Pollution and Marine Waste Disposal. Pergamon, Elmsford, NY, pp. 195–300. Bianchini, A., Playle, R.C., Wood, C.M., Walsh, P.J., 2007. Short-term silver accumulation in tissues of three marine invertebrates: shrimp Penaeus duorarum, sea hare Aplysia californica, and sea urchin Diadema antillarum. Aquat. Toxicol. 84, 182–189. Bohn, A., 1979. Trace metals in fucoid algae and purple sea urchins near a high Arctic lead/zinc ore deposit. Mar. Pollut. Bull. 10, 325–327. Bryan, G.W., 1963. The accumulation of radioactive caesium by marine invertebrates. J. Mar. Biol. Assoc UK 43, 519–539. Burger, J., Gochfeld, M., Jeitner, C., Burke, S., Stamm, T., Snigaroff, R., et al., 2007a. Mercury levels and potential risk from subsistence foods from the Aleutians. Sci. Total Environ. 384, 93–105. Burger, J., Gochfeld, M., Jewett, S.C., 2007b. Radionuclide concentrations in benthic invertebrates from Amchitka and Kiska Islands in the Aleutian Chain, Alaska. Environ. Monit. Assess. 128, 329–341. Carey Jr., A.G., 1970. Zn65 in benthic invertebrates off the Oregon coast. Available from as RLO-1750-55, NTIS, Springfield, VA, as RLO-1750-55, 27 pp. Chipman, W., Thommeret, J., 1979. Manganese content and the occurrence of fallout 54Mn in some marine benthos of the Mediterranean. Bull. Inst. Ocean. 69(1402), 1–15. Clapper, D.L., Davis, J.A., Lamothe, P.J., Patton, C., Epel, D., 1985a. Involvement of zinc in the regulation of pH, motility, and acrosome reactions in sea urchin sperm. J. Cell Biol. 100, 1817–1824. Clapper, D.L., Lamothe, P.L., Davis, J.A., Epel, D., 1985b. Sperm motility in the horseshoe crab. V: zinc removal mediates chelator initiation of motility. J. Exp. Zool. 236, 83–91. Cleland, K.W., 1953. Heavy metals, fertilization and cleavage in the eggs of Psammechinus miliaris. Exp. Cell Res. 4, 246–248. Culkin, F., Riley, J.P., 1958. The occurrence of gallium in marine organisms. J. Mar. Biol. Assoc. UK 37, 607–615. De Clerck, R., Vanderstappen, R., Vyncke, W., Van Hoeyweghen, P., 1979. La teneur en metaux lourds dans les organismes marins provenant de la capture accessoire de la peche coterie belge. Rev. de l’Agric. 3 (32), 793–801. Deheyn, D.D., Latz, M.I., 2006. Bioavailability of metals along a contamination gradient in San Diego Bay (California, USA). Chemosphere 63, 818–834. Denton, G.R.W., Concepcion, L.R., Wood, H.R., Morrison, R.J., 2006. Trace metals in marine organisms from four harbours in Guam. Mar. Pollut. Bull. 52, 1784–1804. Deudero, S., Box, A., March, D., Valencia, J.M., Grau, A.M., Tintora, J., et al., 2007. Temporal trends in benthic invertebrate species from the Balearic Islands, Western Mediterranean. Mar. Pollut. Bull. 54, 1545–1558. Durkina, V.B., Evtushenko, Z.S., 1991. Changes in activity of certain enzymes in sea urchin embryos and larvae after exposure of adult organisms to heavy metals. Mar. Ecol. Prog. Ser. 72, 111–115. Eganhouse, R.P., Young, D.R., 1978. Total and organic mercury in benthic organisms near a major submarine wastewater outfall system. Bull. Environ. Contam. Toxicol. 19, 758–766. Eisler, R., 1979. Copper accumulations in coastal and marine biota. In: Nriagu, J.O. (Ed.), Copper in the Environment, Part 1: Ecological Cycling. John Wiley, New York, pp. 383–449.
Echinoderms 579 Eisler, R., 1980. Accumulation of zinc by marine biota. In: Nriagu, J.O. (Ed.), Zinc in the Environment. Part II: Health Effects. John Wiley, New York, pp. 259–351. Eisler, R., 1981. Trace Metal Concentrations in Marine Organisms. Pergamon, Elmsford, NY, 687 pp. Eisler, R., 2000. Zinc. In: Handbook of Chemical Risk Assessment. Volume 1. Metals. Lewis Publishers, Boca Raton, FL, pp. 605–714. Eisler, R., Hennekey, R.J., 1977. Acute toxicities of Cd2+, Cr+6, Hg2+, Ni2+, and Zn2+to estuarine macrofauna. Arch. Environ. Contam. Toxicol. 6, 315–323. Eustace, I.J., 1974. Zinc, cadmium, copper and manganese in species of finfish and shellfish caught in the Derwent Estuary, Tasmania. Aust. J. Mar. Freshw. Res. 25, 209–220. Fukai, R., 1965. Analysis of trace amounts of chromium in marine organisms by the isotope dilution of Cr-51. In: Radiochemical Methods of Analysis. IAEA, Vienna, pp. 335–351. Fukai, R., Broquet, D., 1965. Distribution of chromium in marine organisms. Bull. Inst. Oceanogr. 65 (1336), 1–19. Fukai, R., Suzuki, H., Watanake, K., 1962. Strontium-90 in marine organisms during the period 1957-1961. Bull. Inst. Oceanogr. Monaco 1251, 1–16. Gonzalez, H., 1991. Mercury pollution caused by a chloralkali plant. Water Air Soil Pollut. 56, 219–233. Gorgy, S., Rakestraw, N.W., Fox, D.L., 1948. Arsenic in the sea. J. Mar. Res. 7, 22–32. Guerin, T., Sirot, V., Volatier, J.L., Leblanc, J.C., 2007. Organotin levels in seafood and its implications for health risk in high-seafood consumers. Sci. Total Environ. 388, 66–77. Hiyama, Y., Shimisu, M., 1964. On the concentration factors of radioactive Cs, Sr, Cd, Zn, and Ce in marine organisms. Rec. Oceanogr. Works Jpn. 7 (2), 43–77. Ichikawa, R., 1961. On the concentration factors of some important radionuclides in marine food organisms. Bull. Jpn. Soc. Sci. Fish. 27, 66–74. Iglesias, N., Penchaszadeh, P.E., 1983. Mercury in sea stars from Golfo Triste, Venezuela. Mar. Pollut. Bull. 14, 396–398. Jenkins, D.W., 1980. Biological monitoring of toxic trace metals. Volume 2, Toxic trace metals in plants and animals of the world. Part II. U.S. Environ. Prot. Agen. Rep. 600/3-80-091, 505–618 pp. Kobayashi, N., 1971. Fertilized sea urchin eggs as an indicatory material for marine pollution bioassay, preliminary experiments. Publ. Seto Mar. Biol. Lab. 18, 379–406. Kobayashi, N., 1977. Preliminary experiments with sea urchin pluteus and metamorphosis in marine pollution bioassay. Publ. Seto Mar. Biol. Lab. 24, 9–21. Kobayashi, N., 1980. Comparative sensitivity of various developmental stages of sea urchins to some chemicals. Mar. Biol. 58, 163–171. Kobayashi, N., Fujinaga, K., 1976. Synergism of inhibiting actions of heavy metals upon the fertilization and development of sea urchin eggs. Sci. Eng. Rev. Doshisha Univ. 17, 54–69. Lawrence, J.M., Mahon, W.D., Avery, W., Lares, M., 1993. Concentrations of metals in Luidia clathrata and Luidia senegalensis (Echinodermata: Asteroidea) in Tampa Bay and the nearshore Gulf of Mexico, Florida. Comp. Biochem. Physiol. 105C, 203–206. Leatherland, T.M., Burton, J.D., 1974. The occurrence of some trace metals in coastal organisms with particular reference to the Solent Region. J. Mar. Biol. Assoc. UK 54, 457–468. Lowman, F.G., Phelps, D.K., Ting, R.Y., Escalera, R.M., 1966. Progress Summary Report No. 4, Marine Biology Program June 1965-June 1966. Puerto Rico Nucl. Cen. Rep., PRNC 85, pp. 1–57. Manzo, S., Buono, S., Cremisini, C., 2008. Predictability of copper, irgarol, and diuron combined effects on sea urchin Paracentrotus lividus. Arch. Environ. Contam. Toxicol. 54, 57–68. Matsumoto, T., Satake, M., Yamamoto, J., Haruna, S., 1964. On the micro constituent elements in marine invertebrates. J. Oceanogr. Soc. Jpn. 20 (3), 15–19. Mauchline, J., Templeton, W.L., 1966. Strontium, calcium and barium in marine organisms from the Irish Sea. J. Cons. Perm. Int. Explor. Mer 30, 161–170. Montgomery Jr., M., Price, M., Thurston, J., de Castro, G.L., Cruz, L.L., Zimmerman, D.D., 1978. Biological availability of pollutants to marine organisms. US Environ. Prot. Agen. Rep. 600/3-78-035, pp. 1–134.
580 Chapter 11 Morisawa, M., Mohri, H., 1972. Heavy metals and spermatozoan motility. I. Distribution of iron, zinc, and copper in sea urchin spermatozoa. Contrib. Tamano Mar. Lab. 187, 1–6. Nakamura, S., Ohmi, C., Kojima, M.K., 1989. Effect of zinc ion on formation of the fertilization membrane in sea urchin eggs. Zool. Sci. (Jpn.) 6, 329–333. Okubo, K., Okubo, T., 1962. Study on the bioassay method for the evaluation of water pollution—II. Use of the fertilized eggs of sea urchins and bivalves. Bull. Tokai Reg. Fish. Res. Lab. 32, 131–140. Oweson, C., Skold, H., Pinsino, A., Matranga, V., Hernroth, B., 2008. Manganese effects on haematopoietic cells and circulating coelomocytes of Asterias rubens (Linnaeus). Aquat. Toxicol. 89, 75–81. Papadopoulu, C., Kanias, G.D., Kassinati, E.M., 1976. Stable elements of radioecological importance in certain echinoderm species. Mar. Pollut. Bull. 7, 143–144. Penrose, W.R., Black, R., Hayward, M.J., 1975. Limited arsenic dispersion in seawater, sediments, and biota near a continuous source. J. Fish. Res. Board Can. 32, 1275–1281. Penrose, W.R., Conacher, H.B.S., Black, R., Meranger, J.C., Miles, W., Cunningham, H.M., et al., 1977. Implications of inorganic/organic interconversion on fluxes of arsenic in marine food webs. Environ. Health Perspect. 19, 53–59. Phillips, B.M., Anderson, B.S., Hunt, J.W., 1998. Spatial and temporal variation in results of purple urchin (Strongylocentrotus purpuratus) toxicity tests with zinc. Environ. Toxicol. Chem. 17, 453–459. Riley, J.P., Segar, D.A., 1970. The distribution of the major and some minor elements in marine animals. I. Echinoderms and coelenterates. J. Mar. Biol. Assoc. UK 50, 721–730. Rosen, G., Rivera-Duarte, I., Chadwick, B.C., Ryan, A., Santore, R.C., Paquin, P.R., 2008. Critical tissue copper residues for marine bivalve (Mytilus galloprovincialis) and echinoderm (Strongylocentrotus purpuratus) embryonic development: conceptual, regulatory and environmental implications. Mar. Environ. Res. 66, 327–336. Sheppard, C.R.C., Bellamy, D.J., 1974. Pollution of the Mediterranean around Naples. Mar. Pollut. Bull. 5, 42–44. Shim, W.J., Hong, S.H., Agafonova, I.G., Aminin, D.L., 2006. Comparative toxicities of organotin compounds on fertilization and development of sea urchin (Anthocidaris crassispina). Bull. Environ. Contam. Toxicol. 77, 755–763. Stenner, R.D., Nickless, G., 1974. Distribution of some heavy metals in organisms in Hardangerfjord and Skjerstadfjord, Norway. Water Air Soil Pollut. 3, 279–291. Stevenson, R.A., Ufret, S.L., 1966. Iron, manganese and nickel in skeletons and food of the sea urchins Tripneustes esculentus and Echinometra lucunter. Limnol. Oceanogr. 11, 11–17. Thompson, J.A.J., Paton, D.W., 1978. Heavy metals in benthic organisms from Point Grey dumpsite—Vancouver, B.C. A preliminary report. Inst. Ocean Sci. Sidney B.C., Canada, PMCR 78-11, pp. 1–18. Timourian, H., Watchmaker, G., 1972. Nickel uptake by sea urchin embryos and their subsequent development. J. Exp. Zool. 182, 379–387. Timourian, H., Watchmaker, G., 1977. Assay of sperm motility to study the effects of metal ions. In: Drucker, H., Wildung, R.E. (Eds.), Biological Implications of Metals in the Environment. Proceedings of the Fifteenth Annual Hanford Life Sciences Symposium. Richland, WA, September 29-October 1, 1975, Ener. Res. Develop. Admin. Sympos., Ser 42, CONF-750929, pp. 523–536. U.S. Environmental Protection Agency (USEPA), 1980a. Ambient water quality criteria for nickel USEPA Rep., 440/5-80-060, pp. 1–206. USEPA, 1980b. Ambient water quality criteria for silver. USEPA Rep., 440/5-80-071, pp. 1–212. USEPA, 1987. Ambient water quality criteria for zinc—1987. USEPA Rep., 440/5-87-003, pp. 1–207. Vaskovsky, V.E., Korotchenko, O.D., Kosheleva, L.P., Levin, V.S., 1972. Arsenic in the lipid extracts of marine invertebrates. Comp. Biochem. Physiol. 41B (4), 777–784. Vattuone, G.M., Griggs, K.S., McIntyre, D.R., Littlepage, J.L., Harrison, F.L., 1976. Cadmium concentrations in rock scallops in comparison with some other species. U.S. Ener. Res. Dev. Admin. UCRL 52020, pp. 1–11. Voogt, P.A., Besten, P.J.D., Kusters, G.C.M., Messing, M.W.J., 1987. Effects of cadmium and zinc on steroid metabolism and steroid level in the sea star Asterias rubens L. Comp. Biochem. Physiol. 86C, 83–89.
Echinoderms 581 Walsh, G.E., McLaughlin, L.L., Louie, M.K., Deans, C.H., Lores, E.M., 1986. Inhibition of arm regeneration by Ophioderma brevispina (Echinodermata, Ophiuroidea) by tributyltin oxide and triphenyltin oxide. Ecotoxicol. Environ. Safety 12, 95–100. Ward, T.J., Kramer, J.R., Boeri, R.L., Gorsuch, J.W., 2006. Chronic toxicity of silver to the sea urchin (Arbacia punctulata). Environ. Toxicol. Chem. 25, 1568–1573. Williams, P.M., Weiss, H.V., 1973. Mercury in the marine environment: concentration in sea water and in pelagic food chain. J. Fish. Res. Board Can. 30, 293–295. Young, L.G., Nelson, L., 1974. The effects of heavy metal ions on the motility of sea urchin spermatozoa. Biol. Bull. 147, 236–246. Young, D.E., Jan, T.K., Hershelman, G.P., 1980. Cycling of zinc in the nearshore marine environment. In: Nriagu, J.O. (Ed.), Zinc in the Environment. Part I: Ecological Cycling. John Wiley, New York, pp. 297–335.
This page intentionally left blank
CHAPTER 12
Tunicates Tunicates are common, cosmopolitan, frequently seen but seldom noticed, marine organisms related to vertebrates. Tunicates possess distinctive gills and a unique dorsal tubular spinal cord found in no other invertebrate animals. In general, mature tunicates are permanently attached forms with no capacity for locomotion, using an enlarged and elaborate gill system to filter large volumes of seawater to procure its planktonic diet. A tunic is secreted by the skin which helps anchor the organism to a solid structure and give rigidity to its outer form, allowing the fragile inner organism to feed undisturbed. Some tunicates are solitary creatures growing to the size of an orange, and some are colonial. Tunicates are universally distributed throughout the seas of the world from the intertidal zone to the deep abyss. Some groups have given up a fixed existence for a drifting floating life. The more primitive group, the ascidians or sea squirts, are associated with the sea bottom and may be found along or near the shore of all seas, growing on seaweeds, on or under rocks, in submerged sand flats, on coral reefs, ship bottoms, wharf piles, and attached to lobsters and sea snails. They are common from the polar regions to the tropics. Some species are cosmopolitan, others so limited in range as to be known only from isolated locations. Alone among animals it secretes its coat of tunicin, a substance similar to that of cellulose in plants. Its blood is unique. Although tunicate blood has no respiratory pigment and contains no more oxygen than a similar amount of seawater, it is frequently rich in both sulfuric acid and vanadium.
12.1 Antimony Whole body concentrations of antimony in field collections of tunicates ranged from 0.02 to 0.26 mg Sb/kg DW (dry weight) (Table 12.1).
12.2 Arsenic Arsenic concentrations in tunicate tissues did not exceed 6.5 mg As/kg on a fresh weight (FW) basis or 34.0 on a DW basis, except for lipids (Table 12.1). Arsenic concentrations in tunicate lipids reached a spectacular 23,700.0 mg/kg FW (Table 12.1), and this corroborates the findings of other investigators who have analyzed arsenic in lipid extracts of marine organisms other than tunicates. 583
584 Chapter 12 Table 12.1: Antimony, Arsenic, Barium, Boron, and Cadmium Concentrations in Field Collections of Tunicates Element and Organism
Concentration
Reference
a
Antimony Botryllus schlosseri; whole
0.26 DW
1
Ciona intestinalis Whole Tunic Whole less tunic
0.16 DW; 0.007 FW 0.15 DW 0.40 DW
2 2 2
Cynthia claudicans; soft parts
0.17 DW; 0.032 FW
3
Microcosmus sulcatus; whole
0.1 DW
2
Pyrosoma sp.; whole
0.02 DW
4
Styella clava; whole
0.15 DW
1
Botryllus schlosseri; whole
6.6 DW
1
Cynthia claudicans; soft parts
6.5 FW; 34.0 DW
3
Guam; 1998-1999; 4 locales; whole Ascidia sp. Rhopalaea sp.
2.7-3.9 DW 2.3-3.6 DW
9 9
Halocynthia aurantium; lipid extract, soft tissues
23,700.0 FW
5
Pyrosoma sp.; whole
1.5 DW
4
Styella clava; whole
4.8 DW
1
Cynthia claudicans; soft parts
0.5 FW
3
Tunicates, whole
0.07-0.1 FW
6
50.0 AW
7
Ascidacea sp.; whole
0.2 FW
8
Botryllus schlosseri; whole
2.7 DW
1
Arsenic
Barium
Boron Salpa fusiformis; whole Cadmium
(Continues)
Tunicates 585 Table 12.1:
Cont’d
Element and Organism
Concentration
Reference
Guam; 1998-1999; 4 locations; whole Ascidia sp. Rhopalaea sp.
0.08-0.36 DW 0.13-0.44 DW
9 9
Pyrosoma sp.; whole
0.44 DW
4
a
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Leatherland and Burton, 1974; 2, Papadopoulu and Kanias, 1977; 3, Papadopoulu et al., 1972; 4, Leatherland et al., 1973; 5, Vaskovsky et al., 1972; 6, Mauchline and Templeton, 1966; 7, Nicholls et al., 1959; 8, Eustace, 1974; 9, Denton et al., 2006.
12.3 Barium Barium levels in tunicates do not exceed 0.1 mg Ba/kg FW whole organism or 0.5 mg Ba/kg FW soft parts (Table 12.1).
12.4 Boron A single datum indicates that whole salp contains 50.0 mg B/kg on an ash weight (AW) basis (Table 12.1).
12.5 Cadmium Cadmium burdens in whole tunicates range from 0.08 to 2.7 mg Cd/kg DW (Table 12.1).
12.6 Cesium Concentrations of stable cesium in whole tunicates did not exceed 0.071 mg/kg DW or 0.008 mg/kg FW (Table 12.2). Results of studies by Bryan (1963) with Ciona intestinalis and 137Cs show that cesium was always absorbed more slowly than potassium. At equilibrium, however, concentration factors for cesium usually exceeded those of potassium. Ciona accumulated cesium over environmental levels by factors of 1.01 for blood, 1.11 for test, 4.6 for gut, and 6.5 for pharynx plus body wall muscles (Bryan, 1963).
586 Chapter 12 Table 12.2: Cesium, Chromium, and Cobalt Concentrations in Field Collections of Tunicates Element and Organism
Concentration
Reference
a
Cesium Ciona intestinalis; Greece Whole Tunic
0.071 DW; 0.003 FW 0.021 DW
1 1
Microcosmus sulcatus; whole; Greece
0.047 DW; 0.008 FW
1
Ciona intestinalis; Greece Whole Tunic Whole less tunic
5.5 DW; 0.24 FW 1.9 DW; 0.075 FW 6.1 DW; 0.25 FW
1 1 1
Guam; 1998-1999; 4 locations; whole Ascidia sp. Rhopalaea sp.
1.0-5.1 DW 1.8-9.7 DW
3 3
Microcosmus sulcatus; whole; Greece
6.6 DW; 1.1 FW
1
Podoclavella moluccensis; blood Plasma, whole Plasma fractions 9-12 EtOH/HCl extract Cell residue
0.35 DW 940.0 DW 58.0 DW 22.0 DW
2 2 2 2
Ciona intestinalis; Greece Whole Tunic
0.52 DW; 0.022 FW 0.44 DW; 0.017 FW
1 1
Microcosmus sulcatus; whole; Greece
1.9 DW
1
Chromium
Cobalt
Values are in mg element/kg fresh weight (FW), or dry weight. a 1, Papadopoulu and Kanias, 1977; 2, Hawkins et al., 1980; 3, Denton et al., 2006.
12.7 Chromium Stable chromium in whole tunicates from Greece did not exceed 6.6 mg/kg DW, with tunic containing disproportionately low burdens (Table 12.2). Elevated accumulations of 940.0 mg Cr/kg DW is recorded in selected plasma fractions of Podoclavella moluccensis (Hawkins et al., 1980; Table 12.2). Eggs of the ascidian, Pyura momus, reportedly accumulated radiochromium-51 from the medium (Townsley et al., 1962), but the extent of accumulation or its significance is unknown.
Tunicates 587
12.8 Cobalt The highest concentration of stable cobalt in tunicate tissues is 1.9 mg/kg DW (Table 12.2). Tunicates are important in cobalt cycling. Kuenzler (1969) reports that diurnally migrating zooplankton, including salps, are significant agents in cobalt cycling from the sea surface and in its transport through the thermocline. Elimination rates of accumulated cobalt by Salpa cylindrica ranged from 8% to 19%/h; some of the eliminated cobalt was particulate, but most was positively charged (Kuenzler, 1969). Pyrosoma verticillatum, one of the luminous species of tunicates, has a comparatively low cobalt elimination rate of 2-3%/h (Kuenzler, 1969). Styella plicata accumulated radiocobalt-60 from seawater over a 30-day period by factors of 850 in viscera, and 400 in test (Shimizu et al., 1970). A concentration factor of 60 for cobalt was reported in whole Salpa sp. (Ketchum and Bowen, 1958).
12.9 Copper The highest copper concentrations reported in field collections of tunicates were 8.3 mg/kg in whole Ascidacea on a FW basis, 130.0 mg/kg DW in blood of Podoclavella, and 500.0 mg/kg AW in whole Salpa (Table 12.3).
Table 12.3: Copper, Iron, and Lead Concentrations in Field Collections of Tunicates Element and Organism
Concentration
Reference
a
Copper Ascidacea sp.; whole
8.3 FW
1
Podoclavella moluccensis; blood Plasma; whole Plasma fractions 9-12 EtOH extract EtOH/HCl extract Cell residue
0.66 DW 130.0 DW 0.0 DW 18.0 DW 16.0 DW
2 2 2 2 2
Sea squirt, Ciona intestinalis California; tunic vs. viscera Sweden; whole
55.0 DW vs. 73.0 DW 13.0 DW
8 8
Guam; 1998-1999; 4 locales; whole Ascidia sp. Rhopalaea sp.
3.1-5.6 DW 6.4-9.9 DW
10 10
Pyura microcosmus; soft parts
7.3-7.8 DW
3 (Continues)
588 Chapter 12 Table 12.3: Cont’d Element and Organism
Concentration
Reference
Salpa fusiformis; whole
500.0 AW
4
Various species; Wales; 1989; whole; coastal area
2.6 FW
9
Ascidia ceratodes; whole
1900.0 DW
5
Sea squirt, Ciona intestinalis Blood Whole Tunic Whole less tunic
50.0 AW 880.0 DW; 39.0 FW 610.0 DW; 24.0 FW 3000.0 DW; 120.0 FW
5 6 6 6
Clavelina huntsmani; whole
900.0 DW
5
Cynthia claudicans; soft parts
330.0 FW; 1740.0 DW
7
Distaplia occidentalis; whole
500.0-2200.0 DW
5
Eudistoma molle; whole
400.0 DW
5
Eudistoma ritteri; whole
2400.0-2600.0 DW
5
Microcosmus sulcatus; whole
840.0 DW; 140.0 FW
6
Molgula manhattensis; whole less tunic Intestines cleared Intestines not cleared
900.0-1700.0 DW 16,400.0-26,600.0 DW
5 5
Perophora annectens; whole
940.0 DW
5
Podoclavella moluccensis; blood Plasma, whole Plasma fractions 9-12 EtOH/HCl extract Cell residue
1.3 DW 4530.0 DW 624.0 DW 964.0 DW
2 2 2 2
Synoieum sp.; whole
600.0 DW
5
Cynthia claudicans; soft parts
3.4 FW; 18.0 DW
7
Salpa fusiformis; whole
3.0 AW
4
a
Iron
Lead
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Eustace, 1974; 2, Hawkins et al., 1980; 3, Papadopoulu et al., 1967; 4, Nicholls et al., 1959; 5, Swinehart et al., 1974; 6, Papadopoulu and Kanias, 1977; 7, Papadopoulu et al., 1972; 8, Jenkins, 1980; 9, Morris et al., 1989; 10, Denton et al., 2006.
Tunicates 589
12.10 Iron Elevated iron concentrations up to 2600.0 mg/kg DW are recorded in whole tunicates (Table 12.3). The high iron levels may have been associated with iron-containing sediments in the intestines. For example, Molgula with intestines cleared had significantly lower total iron than did freshly collected specimens (Swinehart et al., 1974). Age of the tunicate and tissue specificity should also be considered when interpreting the significance of iron concentrations. Experiments with C. intestinalis and radioiron-59 show that accumulation was maximal after 2-3 days, especially in the tunic; young Ciona accumulated greater 59Fe concentrations than did adults (Battani et al., 1968).
12.11 Lead The highest lead concentration recorded in tunicates is 18.0 mg Pb/kg DW soft parts (Table 12.3).
12.12 Manganese Manganese concentrations up to 80,000.0 mg/kg on an AW basis and 112.6 mg/kg on a FW basis are recorded in tunicate tissues; moreover, manganese concentrations are similar in viscera and body wall (Table 12.4), suggesting uniform distribution.
12.13 Mercury Mercury concentrations in tunicates were relatively low, with the exception of the specimen collected from Minamata Bay, Japan (Table 12.4). Minamata Bay—a site of notorious mercury pollution—is discussed elsewhere in this volume.
12.14 Nickel Whole tunicates had nickel maxima of 0.13 mg/kg FW and 60.0 mg/kg AW (Table 12.4).
12.15 Niobium Niobium concentrations in tunicates were either negligible, that is, <0.001 mg Nb/kg DW, or considerable, ranging up to 56.0 mg Nb/kg DW (Table 12.4). Carlisle (1958) shows a direct inverse correlation with niobium and vanadium; high vanadium levels being associated with low niobium concentrations and the reverse. If, as has been suggested, the vanadium present in petroleum deposits is derived from ascidian tunicates, it also seems likely that tunicates are the source of the niobium present on petroleum deposits.
590 Chapter 12 Table 12.4: Manganese, Mercury, Nickel, and Niobium Concentrations in Field Collections of Tunicates Element and Organism
Concentration
Reference
a
Manganese Ascidacea sp.; whole
112.6 FW
1
Cynthia claudicans; soft parts
44.0 FW
2
Halocynthia papillosa; whole
80,000.0 AW
3
Phallusia mammilata Viscera Body wall
24.0 AW 23.1 AW
3 3
Podoclavella moluccensis; blood plasma Whole Fractions 9-12 Cell residue
0.45 DW 45.0 DW 7.0 DW
4 4 4
Botryllus schlosseri; whole
0.57 DW
5
Ciona intestinalis; whole
0.03-0.12 FW
6
Cynthia claudicans; soft parts
0.049 FW; 0.26 DW
5
Styella plicata; whole; Minamata Bay, Japan
35.0 DW
7
Halocynthia roretzi; whole
0.13 FW
8
Salpa fusiformis; whole
60.0 AW
9
Molgula manhattensis Whole Test Flesh without test
26.5 DW 1.9 DW 56.0 DW
10 10 10
Phallusia mammillata; whole
<0.001 DW
10
Mercury
Nickel
Niobium
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Eustace, 1974; 2, Papadopoulu et al., 1972; 3, Chipman and Thommeret, 1970; 4, Hawkins et al., 1980; 5, Leatherland and Burton, 1974; 6, Yannai and Sachs, 1978; 7, Matida and Kumada, 1969; 8, Ikebe and Tanaka, 1979; 9, Nicholls et al., 1959; 10, Carlisle, 1958.
Tunicates 591
12.16 Rubidium Mean rubidium concentrations in tissues from two species of tunicates from the Aegean Sea ranged from 2.6 to 7.0 mg/kg DW (Table 12.5). Table 12.5: Rubidium, Scandium, Selenium, and Silver Concentrations in Field Collections of Tunicates Element and Organism
Concentration
Reference
Rubidium Ciona intestinalis Whole Tunic Whole less tunic
2.6 DW; 0.11 FW 3.7 DW; 0.14 FW 7.0 DW; 0.29 FW
1 1 1
Microcosmus sulcatus; whole
2.6 DW; 0.43 FW
1
Ciona intestinalis Whole Tunic Whole less tunic
0.15 DW; 0.0065 FW 0.0410 DW; 0.0046 FW 0.520 DW; 0.021 FW
1 1 1
Microcosmus sulcatus; whole
0.078 DW; 0.012 FW
1
Ciona intestinalis Whole Tunic Whole less tunic
1.2 DW; 0.051 FW 1.0 DW; 0.04 FW 2.7 DW; 0.11 FW
1 1 1
Microcosmus sulcatus; whole
5.1 DW; 2.8 DW
1
Ciona intestinalis Whole Tunic Whole less tunic
0.021 DW; 0.0009 FW 0.011 DW; 0.0004 FW 0.067 DW; 0.0027 FW
1 1 1
Cynthia claudicans; soft parts
0.9 FW; 4.8 DW
2
Guam; 1998-1999; 4 locales; whole Ascidia sp. Rhopalaea sp.
0.13-0.33 DW <0.27-0.27 DW
3 3
Microcosmus sulcatus; whole
0.031 DW; 0.005 FW
1
Scandium
Selenium
Silver
Values are in mg element/kg fresh weight (FW) or dry weight (DW). a 1, Papadopoulu and Kanias, 1977; 2, Papadopoulu et al., 1972; 3, Denton et al., 2006.
a
592 Chapter 12
12.17 Ruthenium Of all tunicates studied, Dendroda grassularia was the most active concentrator of radioruthenium-106 (Ancellin et al., 1967). The chemical form of ruthenium is important: insoluble ruthenium compounds were accumulated about 10 times greater than dissolved ruthenium compounds (Ancellin and Bovard, 1971).
12.18 Scandium Concentrations of scandium in two species of whole tunicates from the same collection area were 0.078 and 0.15 mg Sc/kg DW and 0.0065 and 0.012 mg Sc/kg on a FW basis (Table 12.5).
12.19 Selenium Average selenium concentrations in two species of tunicates from the same collection area were 1.2 and 5.1 mg Se/kg on a DW basis and 0.051 and 2.8 mg Se/kg on a FW basis (Table 12.5), suggesting significant interspecies differences in selenium burdens.
12.20 Silver The maximum silver concentration recorded in whole tunicates was 0.33 mg Ag/kg on a DW basis; for soft parts, it was 4.8 mg Ag/kg DW (Table 12.5).
12.21 Strontium Strontium is present in tunicates at concentrations up to 7.3 mg Sr/kg FW (Table 12.6). Table 12.6: Strontium, Tin, and Titanium Concentrations in Field Collections of Tunicates Element and Organism
Concentration
Reference
Strontium Cynthia claudicans; soft parts
7.2 FW
1
Tunicates; whole
3.7-7.3 FW
2
8.0 AW
3
1.0 AW
3
Tin Salpa fusiformis; whole Titanium Salpa fusiformis; whole
Values are in mg element/kg fresh weigh (FW) or dry weight (DW). a 1, Papadopoulu et al., 1972; 2, Mauchline and Templeton, 1966; 3, Nicholls et al., 1959.
a
Tunicates 593
12.22 Tin Tin is present at 8.0 mg Sn/kg AW in whole salps (Table 12.6).
12.23 Titanium A single datum indicates that whole salps contain 1.0 mg Ti/kg on an AW basis (Table 12.6).
12.24 Vanadium Vanadium is accumulated by many groups of marine organisms, but concentrations in some species of ascidian tunicates are spectacular (Table 12.7). Table 12.7: Vanadium Concentrations in Field Collections of Tunicates Organism
Concentration
Reference
Ascidia ceratodes Whole Blood Outer fluid
1300.0 DW 6200.0 AW 8000.0 AW
1 1 1
Ascidia nigra Whole blood Centrifuged blood cells
51.0 FW 14,600.0 FW
2 3
Amaroucium sp.; whole
<10.0 AW
1
Ciona intestinalis Whole Ovary Incurrent siphon Anterior gut Posterior gut Stomach Blood Whole Blood
100.0 DW 76.0 DW 109.0 DW 911.0 DW 178.0 DW 248.0 DW 1.2-1.8 DW 400.0-7000.0 AW 160.0 AW
4 4 4 4 4 4 5 6 1
Clavelina huntsmani; whole
30.0 DW
1
Cynthia claudicans; soft parts
0.03 FW
7
Cystodes lobatus; whole
50.0 DW
1
Distaplia occidentalis; whole
600.0-1200.0 DW
1
Eudistoma diaphanes; whole
25.0 DW
1
a
(Continues)
594 Chapter 12 Table 12.7: Cont’d Organism
Concentration
Reference
Eudistoma molle Whole Zooids Test
1000.0 DW 560.0-1200.0 DW; 5000.0-6000.0 AW 1000.0 AW
1 1 1
Eudistoma psammion Whole Zooids
80.0-130.0 DW 610.0-614.0 DW
1 1
Eudistoma ritteri; whole Large colony Small colony
320.0 AW 270.0 AW
1 1
Euherdmania sp.; whole
475.0 DW
4
Halocynthia roretzi; whole
0.12 FW
8
Molgula manhattensis Test Flesh without test Whole Whole
16.0 DW 101.0 DW 54.0 DW <20.0 AW
9 9 9 1
Perophora annectens; whole
700.0-9000.0 DW
1
Phallusia mammillata Whole Eggs
1260.0 DW 170.0 DW
9 3
Phlebobranchia; whole; 12 species
206.0-4123.0 DW
3
Podoclavella moluccensis; blood Whole plasma Plasma fractions 9-12 EtOH extract EtOH/HCl extract Cell residue
4.1 DW 96.0 DW 0.0 DW 480.0 DW 681.0 DW
10 10 10 10 10
Polyclinum planum; whole
<10.0 AW
1
Polyclitoridae; whole
0.0 FW
3
Pyura microcosmus; soft tissues
0.95-1.04 DW
Rhopalaea abdominalis; whole
1800.0 DW
Salpa fusiformis; whole
7.0 AW
12
Salpa spp.; whole
0.0 FW
3
a
11 1
(Continues)
Tunicates 595 Table 12.7:
Cont’d
Organism
Concentration
Reference
Styella spp.; whole
0.0 DW
4
Styelidae; whole
0.0 FW
3
Synocidae
0.0 FW
3
a
Values are in mg V/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Swinehart et al., 1974; 2, Kustin et al., 1976; 3, Ciereszko et al., 1963; 4, Goldberg et al., 1951; 5, Rummel et al., 1967; 6. Elroi and Komarovsky, 1961; 7, Papadopoulu et al., 1972; 8, Ikebe and Tanaka, 1979; 9, Carlisle, 1958; 10, Hawkins et al., 1980; 11, Papadopoulu et al., 1967; 12, Nicholls et al., 1959.
It is clear that not all groups of tunicates readily take up vanadium. For example, members of the family Ascidiidae and Perophoridae from the order Phlebobranchia and several species in the order Aplausobranchia have comparatively large vanadium burdens, while other groups contain little or none. It is generally agreed that vanadium accumulates in tunicate blood cells, or vanadocytes, and forms a steady-state concentration in membranes of the branchial net and gastrointestinal tract (Kustin et al., 1975, 1976; Rummel et al., 1967). However, there are at least five morphologically distinct types of vanodocytes in tunicates, and the distribution and valence of vanadium in these cells is uncertain (Kustin et al., 1976). Thus, tunicates may accumulate vanadium from seawater as V+ (Kustin et al., 1976), and through transformation show up as V4+ in order Aplausobranchia or V3+ in the order Phlebobranchia (Swinehart et al., 1974). Studies by Hawkins et al. (1980) with Pyura stolonifera, in which iron is the major plasma metal, and Ascidia ceratodes, in which vanadium is the major plasma metal, indicates differential uptake and binding of radioiron and radiovanadium. In the case of Pyura, iron uptake is independent of iron concentration, and vanadium is not strongly bound to plasma components. With Ascidia, iron uptake is inhibited at lower iron concentrations but vanadium is strongly bound and retained by plasma components. The interaction of niobium with vanadium has been documented earlier by Carlisle (1958). In addition, vanadium uptake by tunicates is allegedly inhibited by high phosphate levels in seawater (Goldberg et al., 1951). These last two observations assume increasing significance in coastal waters impacted by wastes from the fossil fuel industry and phosphate loadings of household cleansers.
12.25 Zinc Highest zinc concentrations reported in various ascidian tissues were 720.0 mg/kg on a DW basis and 64.0 mg/kg on a FW basis (Table 12.8). It is probable that tunicates reflect environmental levels of zinc, and this could account for some of the variability observed.
596 Chapter 12 Table 12.8: Zinc Concentrations in Field Collections of Tunicates Organism
Concentration
Reference
Ascidacea sp.; whole
64.0 FW
1
Botryllus schlosseri Whole Whole
179.0-251.0 DW 135.0 DW
2 3
Ciona intestinalis Whole Tunic
100.0 DW 110.0 DW
4 4
Microcosmus sulcatus; whole
180.0 DW
4
Podoclavella moluccensis; blood Whole plasma Plasma fractions 9-12 Cell residue
4.3 DW 370.0 DW 49.0 DW
5 5 5
Polycarpa pediculata; whole; near lead smelter outfall, Australia; 2.5-5.2 km from outfall vs. 18-18.8 km
153.0 DW; max. 345.0 DW vs. 98.0 DW
9
Pyrosoma sp.; whole
105.0 DW
6
Pyura microcosmus; soft parts
684.0-720.0 DW
7
Tunicates; whole
200.0 DW; max. 370.0 DW; max. 64.0 FW
8
a
Values are in mg Zn/kg fresh weight (FW) or dry weight (DW). a 1, Eustace, 1974; 2, Ireland, 1973; 3, Leatherland and Burton, 1974; 4, Papadopoulu and Kanias, 1977; 5, Hawkins et al., 1980; 6, Leatherland et al., 1973; 7, Papadopoulu et al., 1967; 8, Young et al., 1980; 9, Ward et al., 1986.
For example, Salpa spp. showed decreasing concentrations of radiozinc with increasing distance from the mouth of the Columbia River (United States), suggesting that the river is the major source of 65Zn (Osterberg, 1962). Accumulated radiozinc is eliminated at the rate of about 1%/h by P. verticillatum; for radiocobalt and radioiron, elimination rates were 2-3%/h, suggesting a need for zinc by this species (Kuenzler, 1969).
12.26 Literature Cited Ancellin, J., Bovard, P., 1971. Observations concernant les contaminations experimentales et les contaminations “in situ” d’especes marines par le ruthenium 106. Rev. Int. Oceanogr. Med. 21, 85–92. Ancellin, J., Bovard, P., Vilquin, A., 1967. New studies on experimental contamination of marine species by ruthenium-106. In: Actes du Congress Int. sur le radioprotection du mileu Soc. Franc. de radioprot, Toulouse, France, January 14-16, 1967, pp. 213–234. Battani, M., Chambost, M.D., Leandri, M., 1968. Study of the contamination by iodine-131 and iron-59 of Ciona intestinalis Linn. In: Proc. Third Inter. Coll. Medical Ocean., Fifth and Sixth Sess., pp. 71–86.
Tunicates 597 Bryan, G.W., 1963. The accumulation of radioactive caesium by marine invertebrates. J. Mar. Biol. Assoc. UK 43, 519–539. Carlisle, D.B., 1958. Niobium in ascidians. Nature 181, 933. Chipman, W., Thommeret, J., 1970. Manganese content and the occurrence of 54Mn in some marine benthos of the Mediterranean. Bull. Inst. Oceanogr. 69(1402), 1–15. Ciereszko, L.S., Ciereszko, E.M., Harris, E.R., Lane, C.A., 1963. Vanadium content of some tunicates. Comp. Biochem. Physiol. 8, 137–140. Denton, G.R.W., Concepcion, L.P., Wood, H.R., Morrison, R.J., 2006. Trace metals in marine organisms from four harbours in Guam. Mar. Pollut. Bull. 52, 1784–1804. Elroi, D., Komarovsky, B., 1961. On the possible use of the fouling ascidian Ciona intestinalis as a source of vanadium, cellulose and other products. Proc. Gen. Fish. Counc. Medit. 6, 261–267. Eustace, I.J., 1974. Zinc, cadmium, copper and manganese in species of finfish and shellfish caught in the Derwent Estuary, Tasmania. Aust. J. Mar. Freshw. Res. 25, 209–220. Goldberg, E.D., McBlair, W., Taylor, K.M., 1951. The uptake of vanadium by tunicates. Biol. Bull. 101, 84–94. Hawkins, C.J., Merefield, P.M., Parry, D.L., Biggs, W.R., Swinehart, J.H., 1980. Comparative study of the blood plasma of the ascidians Pyura stolonifera and Ascidia ceratodes. Biol. Bull. 159, 656–668. Ikebe, K., Tanaka, R., 1979. Determination of vanadium and nickel in marine samples by flameless and flame atomic absorption spectrophotometry. Bull. Environ. Contam. Toxicol. 21, 526–532. Ireland, M.P., 1973. Result of fluvial zinc pollution on the zinc content of littoral and sublittoral organisms in Cardigan Bay, Wales. Environ. Pollut. 4, 27–35. Jenkins, D.W., 1980. Biological monitoring of toxic trace metals. Volume 2. Toxic trace metals in plants and animals of the world. Part II. U.S. Environ. Protect. Agen, Rep. 600/3-80-091, pp. 505–618. Ketchum, B.M., Bowen, V.T., 1958. Biological factors determining the distribution of radioisotopes in the sea. In: Proceedings of the Second Annual United Nations Conference on Peaceful Uses of Atomic Energy, Geneva, vol. 18, pp. 429–433. Kuenzler, E.J., 1969. Elimination of iodine, cobalt, iron, and zinc by marine zooplankton. In: Proceedings of the Second National Symposium on Radioecology, USAEC Conf. 670503, pp. 462–473. Kustin, K., Ladd, K.V., McLeod, G.C., 1975. Site and rate of vanadium assimilation in the tunicate Ciona intestinalis. J. Gen. Physiol. 615, 315–328. Kustin, K., Levine, D.S., McLeod, G.S., Curby, W.A., 1976. The blood of Ascidia nigra: blood cell frequency distribution, morphology, and the distribution and valence of vanadium in living blood cells. Biol. Bull. 150, 426–441. Leatherland, T.M., Burton, J.D., Culkin, F., McCartney, M.J., Morris, R.J., 1973. Concentrations of some trace metals in pelagic organisms and of mercury in Northeast Atlantic Ocean water. Deep Sea Res. 20, 679–685. Leatherland, T.M., Burton, J.D., 1974. The occurrence of some trace metals in coastal organisms with particular reference to the Solent region. J. Mar. Biol. Assoc. UK 54, 457–468. Matida, Y., Kumada, H., 1969. Distribution of mercury in water, bottom mud and aquatic organisms of Minamata Bay, the River Agano and other water bodies in Japan. Bull. Freshw. Fish. Res. Lab. Tokyo 19(2), 73–93. Mauchline, J., Templeton, W.L., 1966. Strontium, calcium and barium in marine organisms from the Irish Sea. Cons. Perm. Int. Explor. Mer. 30, 161–170. Morris, R.J., Law, R.J., Allchin, C.R., Kelly, C.A., Fileman, C.F., 1989. Metals and organochlorines in dolphins and porpoises of Cardigan Bay, West Wales. Mar. Pollut. Bull. 20, 512–523. Nicholls, H.D., Curl Jr., H., Bowen, V.T., 1959. Spectrographic analyses of marine plankton. Limnol. Oceanogr. 4, 472–476. Osterberg, C., 1962. Zinc-65 content of salps and euphausids. Limnol. Oceanogr. 7, 478–479. Papadopoulu, C., Kanias, G.D., 1977. Tunicate species as marine pollution indicators. Mar. Pollut. Bull. 8, 229–231. Papadopoulu, C.P., Cazianis, C.T., Grimanis, A.P., 1967. Neutron activation analysis of vanadium, copper, zinc, bromine and iodine in Pyura microcosmus. In: Proceedings of a Symposium. Nuclear Activation Techniques in the Life Sciences. IAEA, Vienna, pp. 365–377.
598 Chapter 12 Papadopoulu, C., Hadzistelios, I., Grimanis, A.P., 1972. Trace element uptake by Cynthia claudicans (Savigny). Greek Limnol. Oceanogr. 11, 651–653. Rummel, W., Beilig, H.J., Forth, W., Pfleger, K., Rudiger, W., Seifen, E., 1967. Absorption and accumulation of vanadium by tunicates. Protides Biol. Fluids Proc. Colloq. Bruges. 14, 205–210. Shimizu, M., Kajihara, T., Hiyama, Y., 1970. Uptake of 60Co by marine animals. Rec. Oceanogr. Works Jpn. 10, 137–145. Swinehart, J.H., Biggs, W.R., Halko, D.J., Schroeder, N.C., 1974. The vanadium and selected metal contents of some ascidians. Biol. Bull. 146, 302–312. Townsley, S.J., Reid, D.F., Ego, W.T., 1962. Theaccumulation of radioactive isotopes by tropical marine organisms. Annual Rep. 1960-61. USAEC, TID 14420, pp. 1–36. Vaskovsky, V.E., Korotchenko, O.D., Kosheleva, L.P., Levin, V.S., 1972. Arsenic in the lipid extracts of marine invertebrates. Comp. Biochem. Physiol. 41B(4), 777–784. Yannai, S., Sachs, K., 1978. Mercury compounds in some eastern Mediterranean fishes, invertebrates, and their habitats. Environ. Res. 16, 408–418. Young, D.R., Jan, T.K., Hershelman, G.P., 1980. Cycling of zinc in the nearshore marine environment. In: Nriagu, J.O. (Ed.), Zinc in the Environment. Part I: Ecological Cycling. John Wiley, New York, pp. 297–335. Ward, T.J., Correll, R.L., Anderson, R.B., 1986. Distribution of cadmium, lead and zinc amongst the marine sediments, sea grasses and fauna, and the selection of sentinel accumulators, near a lead smelter in South Australia. Aust. J. Mar. Freshw. Res. 37, 567–585.
CHAPTER 13
Concluding Remarks 13.1 General Much of the variability in elemental content of marine plants and invertebrates—as documented herein—is now attributed to tissue analyzed, age and gender of the organism, proximity to anthropogenic and natural point sources, to variations in seawater pH, temperature, and salinity, and to interactions with other chemicals in the environment, especially organic chemicals introduced as a result of human activities. Diet, sediment composition, inherent species differences, and metabolism of different chemical forms of metals and metalloids also influence elemental content. Additional studies are recommended on interaction effects of contaminant mixtures on metal contents of representative marine flora and fauna and on their modes of action. Basic research on most trace metals is now lacking or deficient in a number of areas including essentiality, metabolism, uptake, and retention mechanisms; frequency of carcinogenicity, mutagenicity, teratogenicity, and histopathology; acclimatization mechanisms; and effects of long-term exposure to low sublethal levels under changing thermosaline regimes typical of areas now subjected to global warming effects. Also needed is a vastly improved technology for prevention or removal of comparatively toxic metals originating from anthropogenic sources into the marine biosphere, and repeated monitoring over time using selected indicator species native to the region for assessment of progress. Since the publication of Trace Metal Concentrations in Marine Organisms (Eisler, 1981), there has been a steady output in the trace metal and metalloid technical literature on marine plants and animals from scientists in western Europe, North America, Australia, New Zealand, and Japan, with emphasis on polar fauna, uptake mechanisms, and metabolism. At the same time there has been a disproportionate increase in the technical literature on trace metal concentrations in marine flora and fauna from China, India, Mexico, South America, Africa, and numerous other regions. The reasons for this are unclear, but it is probable that nations that have benefited from the recent redistribution of global wealth now have the resources to train and equip marine scientists with the dual
599
600 Chapter 13 goals of protecting the dwindling marine resources, and the health of human consumers of seafood products of commerce. Environmental awareness seems high in these formerly impoverished regions and their political leaders have provided the long-range funding and the expensive equipment necessary for establishment of metal and metalloid standards based on concentrations in tissues, sediments, diet, and seawater. Throughout this volume, and the companion volume on vertebrates (Eisler, 2009), proposed criteria for resource protection and human consumers of seafood are abundant and based mainly on recommendations of national and international regulatory organizations. These criteria are almost always based on maximum permissible concentrations in seawater, tissues, sediments, chemical species (most notably, arsenic, chromium, mercury, and tin), and food chain transfer. Criteria, unlike legislatively administered standards, are virtually unenforceable. Legislatively administered standards exist in isolated geographic regions; however, enforcement of these standards are lax, except for the most egregious violations. Chemical risk assessment needs to be based—at a minimum—on sound science, public support, and meaningful and enforceable penalties for violators.
13.2 Breadth of Coverage Breadth of coverage—as indicated by citations of metals and metalloids for each of the marine groups examined, namely, algae and macrophytes, annelids, chaetognaths, coelenterates, crustaceans, echinoderms, insects, molluscs, protists, sponges, and tunicates—was most extensive for cadmium, copper, iron, nickel, and zinc and least extensive for dysprosium, erbium, gadolinium, hafnium, holmium, lutetium, neodymium, praseodymium, tantalum, tellurium, and thulium (Table 13.1). Additional research is merited on the less extensively studied metals and metalloids, with emphasis on acquisition of baseline data. Similar data for marine vertebrates, namely, elasmobranchs, fishes, reptiles, birds, and mammals, was most extensive for arsenic, cadmium, chromium, copper, iron, lead, manganese, mercury, selenium, silver, strontium, and zinc, and least extensive for bismuth, europium, germanium, lanthanum, neptunium, niobium, palladium, platinum, radium, rhenium, scandium, technetium, tellurium, thorium, yttrium, and zirconium (Eisler, 2009).
13.3 Depth of Coverage Of the approximately1980 references cited (Table 13.2), molluscs—especially the bivalves, viz., clams, oysters, mussels, and scallops—continue to be the dominant group researched (38.2% of the total references) by virtue of their economic importance, their comparatively
Concluding Remarks 601 Table 13.1: Trace Metals and Marine Biota: Breadth of Coverage Trace Element Cadmium, copper, iron, nickel, zinc
a
a Breadth of Coverage (%)
100
Arsenic, barium, chromium, cobalt, lead, manganese, strontium
91
Mercury, silver, tin
82
Aluminum, antimony, cesium, gallium
73
Boron, selenium, titanium, ruthenium
64
Molybdenum, plutonium, rubidium, scandium, vanadium
55
Zirconium, lithium
46
Bismuth, cerium, europium, radium, silicon, uranium
37
Americium, gold, niobium, rhenium, samarium, technetium, thorium, tungsten,
28
Beryllium, germanium, lanthanum, neptunium, polonium, protactinium, terbium, thallium, ytterbium, yttrium
19
Dysprosium, erbium, gadolinium, hafnium, holmium, lutetium, neodymium, praseodymium, tantalum, tellurium, thulium
10
A rating of 100% means that the eleven major groups covered herein (algae and macrophytes, annelids, chaetognaths, coelenterates, crustaceans, echinoderms, insects, molluscs, protists, sponges, and tunicates) are listed in the technical literature. Ratings of 91%, 82%, 73%, 64%, 55%, 46%, 37%, 28%, 19%, and 10% represent ten, nine, eight, seven, six, five, four, three, two, and one major taxonomic groups, respectively.
sessile existence, and their ability to reflect trace metals in their immediate biosphere. The crustacean literature is also abundant (23.0% of total references) and reflects their economic importance, although trace metal interpretation is confounded by molting frequency. Algae and other plants that form the basis of most marine food chains assume an increasingly important role in the trace metal literature with 19.9% of the total references (Table 13.2). Collectively, algae and macrophytes, molluscs, and crustaceans account for about 81.1% of the total research effort. Comparatively neglected are the annelids (4.8% of all references), protists (4.7%), echinoderms (3.6%), coelenterates (2.0%), tunicates (1.7%), sponges (1.4%), chaetognaths (0.4%), and insects (0.3%); acquisition of additional baseline data on these groups is strongly recommended. Similar data for marine vertebrates, based on 1376 references, showed that 45.9% of all references were devoted to fishes, as expected, due to their commercial importance (Eisler, 2009). Marine birds accounted for 24.8%, mammals 20.5%, elasmobranchs 5.0%, and reptiles 3.8% (Eisler, 2009). It is clear that acquisition of baseline data on elasmobranches and marine reptiles should be given a high priority.
602 Chapter 13 Table 13.2: Trace Metals and Marine Biota: Depth of Coverage Taxonomic Group Algae and macrophytes Annelids
Approximate Number of References (Percent of Total) 395 (19.9) 96 (4.8)
Chaetognaths
7 (0.4)
Coelenterates
40 (2.0)
Crustaceans
455 (23.0)
Echinoderms
71 (3.6)
Insects
5 (0.3)
Molluscs
755 (38.2)
Protists
94 (4.7)
Sponges
28 (1.4)
Tunicates
34 (1.7)
Total
1980 (100.0)
13.4 Literature Cited Eisler, R., 1981. Trace Metal Concentrations in Marine Organisms. Pergamon, Elmsford, NY, 687 pp. Eisler, R., 2009. Compendium of Trace Metals and Marine Biota. Volume 2: Vertebrates. Elsevier, Amsterdam.
Index A Acetaldehyde, 267 Acid phosphatase, 493, 563 Acid volatile sulfide, 470 Acushnet estuary, 422 Adak Island, 153, 162, 181, 243, 260, 275, 297 Admiralty Bay, 38, 52, 72 Adriatic Sea, 9, 10, 153–4, 156, 163, 181–2, 189, 205, 210, 231, 244, 261, 267, 275, 287, 297, 320, 330, 343 AE, 169–70, 310, 360, 412, 478 Aegean Sea, 148, 163, 176, 206, 224–5, 244, 343, 571, 591 Alabama, 198 ALAD, 448 Alanine, 126 Alaska, 151, 153, 162, 181, 243, 260, 275, 281, 297, 402, 404, 453 Aleutian Islands, 52, 270, 312, 453, 559–60, 563, 568, 574–5 Alexandria, 24, 316, 318 Alginates, 416 Alginic acid, 23, 71 Algulose, 23, 28, 71 Alkaline phosphatase, 356, 359 Aluminum, 1, 2, 7–8, 69, 99–100, 115–6, 123–4, 144–7, 269, 328, 399–400, 527, 536, 540, 553–4, 573, 601 Amchitka Island, 147, 176, 192, 224, 292, 312, 329 American Samoa, 151, 404 Americium, 1, 2, 8, 147–8, 293, 527, 601 Ammonium chloride, 108
Amylase, 437, 493 Anaheim Bay, 242 Anasco Bay, 463 Anglesey, 345 Antarctica, 38, 52, 72, 231, 276, 344, 401, 409–10, 417, 421, 428, 431, 437–45, 448, 450, 454, 461, 462, 464–5, 467, 472–3, 476, 481–2, 486 Antarctic Ocean, 425, 428, 432, 437 Antarctic region, 9–10 Antimony, 1, 2, 8–9, 35, 115–6, 123–4, 148–9, 399, 401, 528, 553–4, 583–4, 601 Antimony trioxide, 8 Arabian Sea, 64, 126, 128, 130, 131–3, 135, 140, 467 Arcachon Bay, 197, 219, 317, 328 Arctic Circle, 521, 523–6 Arctic Ocean, 59, 425, 428, 432, 437 Argentina, 10, 15, 17, 24, 27, 29, 38, 43, 49, 55, 57, 63, 71, 73 Arsenate, 9, 12–14, 33, 99, 150, 152, 199, 218, 405, 435, 528–9 Arsenic, 1, 2, 9–14, 35, 99–101, 115–8, 123–4, 150–5, 269, 316, 325, 399–406, 443, 521, 522, 528–9, 553–6, 573–4, 583–5, 600–1 Arsenite, 9, 12–14, 150, 152, 405, 529 Arsenobetaine, 13, 99, 150–2, 400–1, 405, 529 Arsenocholine, 13, 400, 529 Arsenolipids, 13, 400 Arsenosugars, 9, 12–13, 400, 529
603
Ascorbic acid, 435 Assimilation efficiency, 169–70, 310, 360, 412, 478 Athens, 150 Atlantic Ocean, 52, 57, 60, 72, 99, 198, 237, 239, 271, 273, 290, 428, 432, 452, 481, 485 Atlantic Provinces, 27, 29, 49 ATP, 104 Australia, 18–19, 24, 29, 30, 38–9, 43, 45, 49, 50, 58, 71, 73, 75–7, 158, 162, 171, 173, 213, 219, 237–8, 242, 296, 306, 320, 333–4, 354, 404, 407, 411, 420, 431, 434, 437, 445, 447, 466, 482, 486, 491, 596, 599 Australian Antarctic Territory, 407, 437, 447, 491 Aveiro, 108, 322 AVS, 470 Ayamonte, 196, 336 Azores, 164, 175, 189, 209, 232, 246, 262, 277, 294, 297, 314, 346
B Baffin Island, 521 Baja California, 19, 32, 77, 203, 303 Balearic Islands, 154, 164, 181, 183, 205, 208, 275, 288, 555, 557, 562, 568, 570, 573, 576 Baltic Sea, 17, 30, 44, 49, 57, 74, 146, 162, 180, 194, 203, 230, 242, 255, 260, 266, 275, 286, 341, 412, 421, 423, 433, 447, 460, 463
604 Index Baltimore, 337 Barbate, 196, 336 Barbuda, 67 Barcelona, 163, 181, 205, 244, 276, 343 Barents Sea, 408, 425, 479, 522, 523, 524, 526 Barium, 1, 2, 14, 28, 71, 100–1, 116, 118, 124–5, 155–7, 406, 421, 521–4, 528–9, 556, 584–5, 601 Barium sulfonate, 421 Bay of Biscay, 151, 158, 178, 187, 193, 227, 238, 271, 300, 330, 333 Beer, 171, 344, 346–7 Belgium, 303, 401, 457 Bentonite, 172, 421 Benzo(a)anthracene, 119 Benzo(a)pyrene, 119 Benzo(b)fluoranthene, 119 Benzo(e)pyrene, 119 Benzo(j)fluoranthene, 119 Benzo(k)fluoranthene, 119 Bergen Harbor, 280 Bermuda, 132 Beryllium, 1, 2, 14–15, 406–7, 601 Bidaron estuary, 290 Bidasoa estuary, 539, 540 Bioconcentration factors (BCFs), 46, 48, 65, 67, 77–9, 147–8, 167, 174, 177, 192, 223, 266, 282, 293, 298, 306, 315, 326, 360–1, 407, 437, 447, 491, 530, 536 Biomagnification, 26, 33, 60, 68, 108, 282 Bismuth, 1, 2, 15, 125, 156–7, 359, 407, 600–1 Black Sea, 36, 57, 64, 66, 70–1, 79, 176, 205, 343, 448, 476, 495, 521, 524–6 Block Island Sound, 194 Bodega Bay, 206, 303 Bohai Bay, 68, 317, 472–3 Bohai Sea, 184, 212, 248, 271, 319, 349 Boric acid, 556
Boron, 1, 2, 15–16, 125, 156–7, 406–7, 522, 524, 556, 584–5, 601 Boston Harbor, 106, 109 Brazil, 19, 31, 40, 50, 58, 75, 158–60, 199, 228, 257, 284, 336–7, 408, 425, 441, 449, 462, 479 Bristol Channel, 168, 171, 210, 344, 347 British Columbia, 55, 271, 320 Brunswick, 53 Bryozoans, 469, 470 Butyltins, 325, 327, 472 Bylot Sound, 293, 569
C Cadmium, 1, 2, 16–21, 78, 101, 109, 118, 126–7, 157–74, 308, 311, 358–9, 407–16, 434, 448, 468, 491, 517, 522, 524, 528–32, 540, 546, 556–8, 574, 585, 601 Calcasieu River Estuary, 140, 335, 467, 479 Calcium, 1, 2, 21, 61, 66–7, 108, 118–9, 125, 134, 167, 172, 222, 293, 312, 327, 355, 359, 361, 407, 416, 436, 478, 542, 573 Calcium carbonate, 61, 172 California, 8, 18, 19, 30–2, 39, 41, 44–6, 50–1, 69, 75, 77, 159, 161, 180, 186, 201, 206, 239, 268, 302–3, 308, 354, 357, 400, 409–10, 429, 445, 455, 484–5, 539–40, 562, 573, 587 Camel estuary, 166, 184, 191, 213, 234–5, 248, 264, 290, 306, 350 Canada, 27, 29, 49, 55, 57, 72, 204, 271, 321, 327 Canary Islands, 164, 246 Carbon, 2, 13, 15, 37, 105, 109, 170, 222, 356, 435, 470, 475 Carbonates, 251, 359, 435 Carbonic anhydrase, 359, 478 Carbonyl, 37
Carboxylic, 60 Carboxypeptidase, 359 Carcinogenicity, 599 Caribbean Sea, 464 Catalonia, 116–7, 278, 454 Cellulose, 583 Cerium, 1, 2, 22, 119, 175, 417–8, 558, 601 Cesium, 1, 2, 22–3, 102, 127, 175–7, 417–8, 532, 558–9, 585–6, 601 Charlotte Harbor, 12 Chelators, 26, 34, 217, 359, 422, 433, 435, 490, 536 Chernobyl, 176, 295, 417–8, 465 Chertsey, 148, 270 Chesapeake Bay, 8, 44, 52, 65, 105, 108, 145, 194, 198, 218, 239, 258, 301, 308, 316, 337, 340, 357, 424 Chile, 9, 16, 29, 44, 52, 58, 64, 67, 71, 75, 161, 202, 230, 259, 286, 297, 341 China, 29, 31, 43, 45, 68, 73, 76, 132, 151, 158–9, 166, 171, 184, 195, 197, 212, 238–9, 248, 264, 271, 279, 317, 319, 334, 349, 457, 472–3, 599 Chincoteague inlet, 449 Chinese National Water Quality Standard for Fisheries, 438 Chitin, 434, 436, 461 Chlorine, 2, 356, 491 Chlorophyll, 8, 14, 37, 41, 79 Chromated copper arsenate, 33, 199, 218, 435 Chrome lignosulfonate, 421 Chromium, 1, 2, 23–6, 102, 127–8, 177–86, 291, 308, 418–24, 517–9, 524, 532–4, 559–60, 571, 586 Citrate, 34, 225, 237 Ciudad del Carmen, 456 Coatzacoalcos estuary, 240 Cobalt, 1, 2, 26–8, 42, 78, 102, 119, 127–8, 186–92, 423–4, 524, 534–5, 559–61, 587, 601 Cobalt acetate, 560 Cobo Bay, 200
Index Columbia, 72 Columbia River, 596 Connecticut, 301, 303 Cook Inlet, 151 Copper, 1, 2, 28–36, 102–3, 119, 127–9, 192–224, 279, 424–38, 519, 524, 535–7, 561–3, 587–8 Copper acetate, 435 Copper chloride, 435 Copper sulfate, 434–5, 438 Copper sulfide, 222 Corio Bay, 162 Cornwall, 208, 345 Corpus Christi Harbor, 101 Corsica, 19, 25, 27, 45, 53, 58 Croatia, 275, 318 Cuba, 568 Cupric ion, 34, 435 Cysteine, 540 Cytochrome P450, 326
East China Sea, 151, 195, 238, 271 East Indies, 49, 72 East Japan Sea, 293, 298, 315 EDTA, 26, 47, 72, 217, 359, 417, 422, 435, 546, 558, 567, 569 Egypt, 24, 316, 318, 418–9 Eikhamrane, 17, 43, 52, 73 Elizabeth River estuary, 424 England, 24, 29, 52, 57–8, 66, 130, 157, 160, 184, 190–1, 197, 204, 208, 213, 234, 240, 242–3, 248, 258, 260, 264, 283, 285, 290, 323, 325, 338, 349–50, 354 English Channel, 200, 214, 301 Eniwetok Atoll, 407 Erbium, 1, 3, 438, 600–1 Europium, 3, 224–5, 439, 563, 600–1
D
F
DDT, 78 Deficiency, 56, 78, 103, 107, 362, 436–7, 495, 575 Delaware, 13, 249–50, 437, 449 Denmark, 32, 529 Dibutyltin, 68, 108, 317–21, 473, 475, 575 Dimethylarsenosoribosyl, 12 Dimethylarsinate, 12, 529 Dimethylarsinic acid, 99, 151, 152, 528 Dimethyltin, 68, 108, 319, 322, 475, 575 Dimethylureas, 561 Dinitrophenol, 61 Diphenyltin, 318–20, 322, 475, 575 Dissolved organic matter, 536 DNA, 63, 295, 298, 325 Dorset, 18, 171, 344, 346 Douro River estuary, 16 Dulas Bay, 17–18, 38–9, 43, 44, 49, 57–8, 73, 74 Dysprosium, 2, 438, 601
Fal estuary, 354 Faroe Islands, 271 Fermain Bay, 200 Ferric hydroxide, 61, 226 Ferric oxide, 41, 103 Ferritin, 356, 443 Ferrochrome, 421 Ferromanganese, 104 Firth of Clyde, 485 Firth of Tay, 52–3 Flak, 17, 43, 52, 73 Flatworms, 434–5 Florida, 12, 54, 57, 152, 160, 179, 198–9, 239, 243, 272, 284, 296, 318, 337, 402, 404, 408, 419, 444, 453, 466, 473, 570, 572 Florida Everglades, 54 Fluoranthrene, 416 Former Soviet Union, 57 Foundry Cove, 529 France, 19, 25, 27, 45, 51, 53, 58, 181, 197, 205, 219, 244, 276, 290, 299, 316–8, 328, 463, 472 Fucoidan, 28, 71 Fulvic acid, 536
E East Antarctica, 417, 439, 442, 461, 464–5, 472–3, 486
605
G Gadolinium, 1, 3, 439, 600–1 Gallium, 1, 3, 36, 100, 103, 117, 119, 129–30, 224–5, 439, 522, 524, 564, 601 Galveston Bay, 239, 337 Gannel estuary, 166, 184, 190–1, 213, 234–5, 248, 264, 290, 306, 349–50 Genova, 163, 181, 205, 244, 276, 343 Georges Bank, 194 Georges River, 213 Georgia, 53, 54, 145, 152, 156, 157, 160, 179, 198, 228, 239, 258, 272, 281, 284, 299, 301, 337 Germanium, 1, 3, 36–7, 439, 440, 600–1 Germany, 243 Glucose–6-phosphate dehydrogenase, 16 Glutamate, 126 Glutathione, 21, 170, 295, 447, 491 Glutathione peroxidase, 170, 295, 447, 491 Glycine, 540 Glycogen, 174, 311, 493 Glycoprotein, 173 Glycyl-L-histidine, 107 Goa, 27, 29, 38, 43, 49, 57, 72 Gold, 1, 3, 36–7, 224–5, 439, 440, 601 Golfo Triste, 568 Greece, 150, 155, 163, 181, 192, 206, 231, 244, 280, 287, 312, 329, 558, 571, 586 Greenland, 58, 74, 160, 240, 243, 251, 272, 293, 342, 354, 409, 445, 454, 464, 466, 540, 569 Greenland Sea, 522–4 Guam, 11, 18, 24, 64, 116–7, 120, 124, 126, 128, 130, 136, 154, 163, 182, 207, 276, 304, 403, 409, 420, 429, 467, 555, 557, 560, 572, 584–7, 591 Gulf coast, 198, 208, 239, 245, 258, 301, 338, 345
606 Index Gulf of California, 18–19, 30–2, 39, 41, 44–6, 50, 75, 77, 159, 239, 336, 410, 445, 485 Gulf of Gabes, 159 Gulf of Gdansk, 17, 30, 44, 49, 57, 74, 201, 255, 340 Gulf of Gemlik, 163, 182, 189, 205, 231, 244, 261, 287, 343 Gulf of Mannar, 118, 120 Gulf of Mexico, 37, 79, 240, 308, 318, 324, 337, 411, 431, 446, 457, 487, 572
H Hackensack River, 24, 419 Hafnium, 1, 3, 225–6, 600–1 Hainan Island, 132 Halifax, 204 Harbour Island, 27, 57, 58, 75 Hardangerfjord, 17, 43, 52, 73 Hawaii, 99, 127, 129, 137, 139 Hemocyanin, 195, 222, 424, 436 Hemoglobin, 531 Hemolymph, 171–2, 207–8, 221, 232, 309, 345, 360, 415, 422, 426, 428, 436, 443, 463–4, 469, 480, 490, 573 Hexavalent chromium, 23, 26, 102, 185, 186, 422, 534, 559 Histidine, 107 Holmium, 1, 3, 440, 600–1 Hong Kong, 29, 43, 73, 101, 109, 132, 153, 165, 183, 197, 211, 213, 219, 234, 247, 263, 289, 322, 327, 348–9, 428 Huangshi Sea, 271 Humic acid, 172, 222, 435 Hydrogen peroxide, 107 Hydroxycarboxylic, 60 4-Hydroxy–3-nitrobenzene arsonic acid, 99 Hyperion sewer outfall, 268
72, 75, 78, 112, 118, 120, 165, 180, 183, 202, 211, 233, 247, 259, 263, 278, 289, 326, 341, 348, 533, 599 Indonesia, 132, 326 Ireland, 17, 24, 27, 77, 140, 181, 303, 448, 489, 493, 596 Irish Sea, 18, 27, 29, 36, 38, 44, 49, 58, 64, 66, 74, 99, 195, 400, 556, 564 Iron, 1, 3, 26, 34, 38–42, 100, 103, 117, 119, 131, 226–37, 440–3, 518, 520, 525, 537, 538, 564–5, 588–9 Iron oxide, 172, 192, 299, 356 Iskenderun Bay, 400, 408, 419, 423, 444 Israel, 17, 29, 57, 288, 305 Italy, 19, 31, 40, 45, 53, 163, 181, 205, 206, 231, 244, 273, 276, 321, 343, 410, 420, 445, 451, 566 Izmir Bay, 162, 182, 205, 231, 244, 261, 275, 343
J Jamaica, 63, 66 James River, 340 Japan, 15, 19, 22, 24–6, 32, 36, 40, 42, 53, 55, 59, 61, 63, 74, 131–2, 134, 204, 208, 267, 273, 297, 319, 328, 452, 589, 599 Japan Sea, 293, 297, 298, 315 Jiaozhou Bay, 166, 171, 184, 212, 248, 264, 349
K Korea, 19, 25, 27, 32, 40, 51, 52, 166, 183, 190, 212, 241, 248, 264, 290, 315, 318, 321, 349, 457 Kyushu, 267, 319, 328
I
L
Iberian Peninsula, 326 Iceland, 27, 29, 49, 72 Imposex, 325–7 India, 18–9, 25–7, 29–31, 38–9, 43–4, 46, 49, 52, 57, 66, 68,
La Haque, 463 Lagoon of Venice, 326 Laguna Madre, 11, 24, 63, 405, 420 Lanthanum, 1, 3, 237, 443, 600–1
Laverbread, 60 Lead, 1, 3, 35, 42–8, 103–4, 117, 120, 131–2, 144, 170–1, 174, 218–9, 237–54, 269, 316, 325, 334, 342, 354, 358–9, 443–8, 491, 494, 520, 523, 525, 537–8, 540, 565–6, 573–4, 588–9, 600–1 Lead acetate, 447, 566 Lebanon, 285 Lesina lagoon, 420, 430, 445, 451, 485 Leucine, 103 Lisbon, 319 Lithium, 1, 3, 48, 125, 132–3, 255, 448, 523, 525, 601 LOAEL (lower observed adverse effect level), 469 Lofoten, 17, 52 Long Island, 196, 204, 283, 290, 449 Long Island Sound, 196, 204, 449 Looe estuary, 162, 184, 191, 204, 213, 234, 242, 260, 264, 290, 302–3 Los Angeles, 268 Louisiana, 301, 335, 467, 479 Lutetium, 1, 3, 448, 600–1
M Magnesium, 1, 3, 21, 60, 67, 102, 107, 108, 222, 356, 407, 436, 478 Maine, 320 Malaysia, 52, 193, 209, 322 Malic dehydrogenase, 359 Manchester, 199 Manganese, 1, 3, 42, 48–51, 69, 99, 100, 103–4, 120, 133, 144, 170–2, 192, 218, 255–66, 291, 355, 359, 443, 449–52, 519–20, 537–8, 540, 545, 566–7, 573–4, 589–90, 600–1 Manganese dioxide, 452, 567 Manganese oxide, 172, 192, 356 Mannoside, 359 Marmara Sea, 160, 162, 200, 205, 272, 275 Marseille, 51, 53, 163, 181, 205, 244, 276, 343
Index Maryland, 8, 52, 145, 198, 218, 301, 308, 316, 340, 357, 400, 402, 424 Massachusetts, 106, 109, 249, 250, 422 Maximum acceptable toxicant concentration (MATC), 438 Mediterranean Sea, 11, 17, 19, 25, 26, 27, 29, 30, 40, 45, 57, 58, 61, 66, 78, 118–20, 151, 154, 158, 163–4, 169, 176, 178, 180–1, 183, 187, 189, 193, 205, 208, 227, 238, 244, 245, 261, 273, 275–7, 287–8, 300, 321, 330, 333, 343, 345, 357, 399, 417–9, 432, 443, 448, 464, 471, 489, 555, 557, 562, 566, 568, 570, 573, 576 Melanin, 147 Menai Straits, 17–18, 38–9, 43–4, 49, 57–8, 73, 74, 440 Mercurials, 54–5, 106, 280 Mercuric chloride, 106, 269, 279, 458 Mercuric reductase, 106 Mercury, 4, 51–5, 101, 104–107, 117, 120, 133–4, 266–80, 295, 452–9, 537–40, 568–9, 589–90, 601 Mersin coast, 158, 169, 178, 238 Metallothioneins, 168, 170–1, 174, 223, 311, 356, 412, 438, 490, 529–31, 545–6 Methane, 99, 105–6 Methylarsonic acid, 12 Methylcobalamin, 105 Methylmercury, 104–6, 275, 279–80, 416, 452, 455, 540 Mex Bay, 24 Mexico, 18–9, 30–2, 36–7, 39, 41, 44–6, 50–1, 59, 75, 77, 79, 161, 169, 202–3, 219, 240–1, 272, 303, 308, 318, 324, 337, 340, 410–1, 429, 431, 445–6, 456–7, 484–5, 487, 572, 599 Mid-Atlantic ridge, 145, 158, 187, 194, 227, 256, 270, 300, 313,
333, 427–8, 441, 454–5, 482, 484, 533, 539, 544 Minamata Bay, 52–3, 105–6, 134, 267, 273, 452, 454, 589 Mission Point, 327 Mississippi, 239, 272, 404 Molting, 399, 405, 413, 418, 433, 443, 447, 452, 465, 490, 495, 601 Molybdate, 55, 56 Molybdenum, 1, 4, 55–6, 134–5, 280–2, 460, 495, 523, 525, 540, 569, 601 Monaco, 24 Monobutyltin, 68, 108, 317–22, 324–5, 473, 575 Monomethylarsonate, 400 Monomethylarsonic acid, 99, 152 Monophenyltin, 319, 320, 322, 575 Monterey Bay, 50, 69, 75 Morocco, 161–2, 169, 180, 203, 242, 259, 274, 286, 340–1 Mutagenicity, 599
N Narragansett Bay, 23, 24, 206, 303, 354 Natal, 19, 31, 40, 50, 58, 75, 160, 199, 337, 408, 425, 441, 449, 462, 479 Neodymium, 4, 461, 600–1 Neptunium, 4, 282, 461, 600–1 Netherlands, 162, 201, 242, 260, 286, 342, 361, 402 New Bedford, 422 New Caledonia, 151, 159, 179, 188, 196, 228, 257, 284, 300, 336 New England, 130, 258, 283 New Jersey, 24, 31, 43, 46, 276, 419, 432, 437, 446, 457, 488 New South Wales, 158, 171, 238, 296, 333, 404, 411, 420, 431, 445, 466, 486 New York, 196, 204, 283, 290, 529 New York Bight, 194, 422, 449 New Zealand, 178, 194, 204, 242, 256, 283, 304, 305, 333, 599
607
Newfoundland, 341 Newport River, 198, 337 Newport River estuary, 73 Nickel, 1, 4, 35, 56–60, 101, 109, 117, 120, 134–5, 144, 218, 255, 269, 282–9, 461–3, 494, 519–20, 523, 525, 536, 539, 540, 569–70, 573–4, 589–90, 600–1 Nickel-cadmium battery plant, 56 Nickel chloride, 107 Niobium, 1, 4, 292, 463, 589, 595, 600–1 Nitrates, 15–6 Nitrogen, 4, 23, 56, 61 NOAEL (no observed adverse effect level), 469 Nobeoka Bay, 208 North America, 148, 150, 153, 177, 241, 316, 402, 421, 427, 444, 450, 454, 460, 462, 466–7, 472–3, 477, 599 North Carolina, 73, 77, 198–9, 201, 337–8 North River, 337 North Sea, 154, 303, 403, 430, 457 North Wales, 345 Norway, 17, 18, 24, 27, 29, 31–2, 38–40, 43, 44, 46, 51–2, 55, 57–8, 63, 72–4, 76, 161, 165, 202, 204, 241, 243, 246, 275, 280, 286, 288, 303, 341, 437, 565–6 Nova Scotia, 10, 57–8, 153
O Octyltins, 318, 322, 326, 473, 574 Odense Fjord, 529 Ogasawara Island, 131 Okhotsk Sea, 160 Oregon, 11, 19, 25, 32, 41, 59, 77, 99 Organoarsenicals, 11–4, 99, 150, 400, 405 Organoethylleads, 47 Organoiron, 41 Organolead, 47, 103 Organomercurial lyase, 106
608 Index Organomercury, 54, 268–9, 271, 276, 279–80, 452, 459 Organomethylleads, 47 Organoselenium, 62 Organotins, 68, 69, 108–9, 316–8, 323–8, 472–3, 475–6, 543, 574–5 Orkney, 12 Osaka Bay, 319, 474 Otago, 194 Outer continental shelf, 59, 291, 463
P Pacific Ocean, 42, 61, 99, 130, 413, 435, 475, 521, 524, 525 PAH (polycyclic aromatic hydrocarbon), 104, 119 Pakistan, 64 Palk Bay, 55 Panama, 72 Paralytic shellfish poisoning (PSP), 147 Pensacola, 152, 160, 179, 198, 239, 272, 284, 296, 318, 337, 402, 408, 419, 425, 444, 453, 462, 466, 473, 479 Persian Gulf, 457 Perth, 320 Petroleum hydrocarbons, 421, 530, 536 Phenanthrene, 416 Phenyltins, 318, 472–3, 574 Phosphate, 9, 12, 16, 42, 103, 107, 359, 491, 544, 595 Phosphatidylcholine, 400 Phosphorus, 4, 9, 355, 361, 407, 491 Photosynthesis, 15, 21, 26, 37, 42, 47, 54, 60, 69, 78, 79 Phytochelatins, 21, 35 Plutonium, 1, 4, 8, 60–1, 120, 292–3, 443, 463–4, 540–1, 569, 601 Polonium, 1, 4, 293, 464, 601 Polychlorinated biphenyls (PCBs), 144 Polycyclic aromatic hydrocarbon, 104
Polysaccharides, 21, 61 Port of Mahon, 154, 163–4, 181, 183, 205, 208, 244–5, 275, 277, 288, 345, 555, 557, 565, 568, 570, 573, 576 Port Phillip Bay, 162, 237, 242 Portland, 18 Portugal, 16, 20, 32–3, 47, 52, 108, 154, 163, 204, 207, 232, 245, 261, 276, 281, 287, 294, 297, 319, 322, 331, 344, 453 Potassium, 1, 4, 67, 102, 108, 356, 491, 585 Praseodymium, 1, 4, 464, 600–1 Proline, 531 Protactinium, 1, 4, 293, 464, 601 Proteases, 577 Puerto Rico, 23, 24, 50–1, 57, 76, 119, 457, 463, 559, 569–70 Puget Sound, 46, 53, 58, 242 Purdy, 198
Q Queensland, 24, 38, 71
R Radium, 1, 4, 61, 134, 195, 221, 293, 464, 600–1 Rappahannock River estuary, 198 Raritan Bay, 31, 43, 44, 46 Ras Beirut, 285 Red tide, 79 Rhenium, 1, 4, 61, 294, 464, 600–1 Rhode Island, 23–4, 99, 198, 206, 303, 354 Rio de Aveiro, 322 Rio Pedras, 336 Rio Tinto estuary, 17, 29, 43, 72, 202, 341 River Calligan, 181 River Crouch, 321, 328, 476 River Tyne, 320–1 Ross Sea, 193 Rotifers, 434 Rubidium, 1, 4, 16, 61–2, 134, 294, 465, 571, 591, 601 Ruthenium, 1, 4, 61, 119–20, 134, 175, 295, 465, 541, 592, 601
S Saanach Inlet, 55 Sacca Sessola, 163, 181, 206, 231, 244, 261, 343 St. Croix, 132 Samarium, 1, 4, 295, 465, 535, 541, 601 Samoa, 127–8, 136, 139, 151, 404 San Antonio Bay, 239 Sancti-Petri, 196, 336 San Diego, 204, 243, 268, 342 San Diego Bay, 303, 320, 573 San Diego Harbor, 204, 243, 320, 342 San Francisco Bay, 8, 145, 219, 301–3, 306, 340, 400, 455, 541 San Giuliano, 163, 181, 206, 231, 244, 261, 343 Sanlucar, 196, 336 Santa Marie Bay, 151, 159, 179, 284, 300, 336 Sardinia, 163, 205, 244, 287 Sargasso Sea, 99 Saronikos Gulf of Greece, 181, 206, 244 Savannah, 145, 152, 156–7, 160, 179, 198, 228, 239, 258, 272, 281, 284, 299, 337 Scandium, 1, 5, 127, 135–6, 295–6, 465, 535, 541–2, 571, 591–2, 600–1 Scheldt estuary, 146, 153, 162, 181, 189, 230, 242, 260, 286, 303, 342 Scotland, 12, 31, 52–3, 57–8, 195, 242, 462–3 Sea of Japan, 24, 27, 29, 38, 49, 57, 70–1, 160 Seal Harbour, 10, 153 Selenite, 62, 295–6, 298, 466 Selenium, 1, 5, 35, 62–3, 117, 120, 268–9, 295–9, 459, 466, 468–9, 540, 542, 571–2, 574, 591–2, 600–1 Sellafield, 67 Sepetiba Bay, 159, 336 Severn estuary, 18, 44, 74
Index Shenzhen, 29, 43, 73 Silica, 37 Silicates, 15, 37, 63, 469 Silicic acid, 37, 63 Silicon, 1, 5, 62–3, 135–6, 299, 407, 469, 478, 601 Silver, 1, 5, 64–5, 107–8, 121, 135, 172, 218, 269, 299–312, 325, 466–7, 469–70, 523, 525, 540–2, 571–4, 591–2, 600–1 Silver sulfide, 310–1 Sinaloa, 161, 202, 219, 241, 340 Sodium metavanadate, 70 Solent region, 52 Sorfjorden, 17, 18, 43–4, 46, 73, 74, 76 South Africa, 27, 40, 51, 76, 157, 197, 261, 284 South Australia, 482 South Wales, 158, 171, 238, 296, 333, 404, 411, 420, 431, 445, 466, 486 Southampton, 148, 236, 270 Soviet Union, 24, 57 Spain, 11, 17, 29, 32, 40, 43, 52, 72, 77, 116–8, 120, 163, 164, 180–1, 196, 202, 204–5, 209, 243–4, 246, 249, 256, 276, 278, 283, 290, 296, 300, 333, 336, 341, 343, 347, 419, 446, 454 Spitsbergen, 59 Strait of Magellan, 9, 64, 161, 202, 230, 286, 297, 341 Strathcona Sound, 521 Strontium, 1, 5, 8, 14, 21, 40, 42, 50, 66–7, 69–70, 72, 101, 108, 121, 125, 137–9, 155, 312–3, 470–2, 523, 525, 541–2, 573–4, 592, 600–1 Succinate, 324 Sulfate, 34, 56, 105, 107, 108, 416, 434–6, 438 Sulfide, 222, 310–1, 470, 544 Sulfur, 5, 99, 356, 438, 491 Sulfuric acid, 583 Superoxide dismutase, 170 Svalbard, 59
Sweden, 61, 117, 120, 130, 201, 255, 587 Sydney, 18, 24, 30, 39, 45, 50, 58, 75, 159, 213, 336
T Tagus estuary, 20, 33, 47 Tahiti, 127–9, 136, 137, 139 Taiwan, 150–2, 155, 197, 219, 399–400, 405, 408, 418–9, 426, 432, 440–1, 444, 450, 457, 481 Tamar estuary, 18, 39, 44, 49, 58, 64, 74, 184, 191, 213, 234, 248, 264, 290, 350 Tamil Nadu, 30, 39, 44, 49, 52, 67–8, 74 Tampa Bay, 572 Tampico, 456 Tantalum, 1, 5, 312, 600–1 Tanzania, 145, 160, 179, 201, 229, 240, 258, 339 Tarragona coast, 249, 446 Tasmania, 162, 197, 260, 353 TBT, 35, 67–9, 108–9, 219, 316, 320–8, 474–6, 543 Technetium, 1, 5, 67, 312, 575, 600–1 Tellurium, 1, 5, 315, 600–1 Teratogenicity, 599 Terbium, 1, 5, 315, 472, 601 Terra Nova Bay, 52 Tetrachloroaurate, 37 Tetraethyllead, 42, 104, 252, 254, 448 Tetramethylarsonium, 529 Tetramethyllead, 42, 104, 254, 448 Tetramethyltins, 68 Tetravalent tin, 108 Texas, 11, 24, 27, 32, 45, 50–1, 55, 57–9, 63, 75, 101, 198, 239, 272, 291, 337, 405, 418, 420, 457, 463, 467 Texas Continental Shelf, 50, 51, 75 Thailand, 272, 322 Thallium, 1, 5, 315–6, 472, 601 Thiol, 37
609
Thorium, 1, 5, 61, 137–8, 316, 317, 472, 600–1 Thulium, 1, 5, 472, 600–1 Tin, 1, 5, 67–9, 108–9, 137, 138, 219, 316–28, 472–6, 523, 525, 543, 573–5, 592–3, 600–1 Titanium, 1, 5, 8, 14, 40, 42, 50, 66, 69, 70, 101, 109, 127, 137, 317, 322, 329, 473–4, 476, 523, 526, 573–4, 592, 593, 601 Tokyo Bay, 319 Triazines, 561 Tributyltin, 35, 68, 108, 137, 219, 317–22, 325, 472–5, 494, 536, 543, 575 Triethyllead, 47, 254, 448 Trimethylarsine, 528 Trimethylarsoniopropionate, 529 Trimethyllead, 47, 254, 448 Trimethyltins, 68–9, 319, 322, 475 Tripentyltins, 69 Triphenyltins, 68–9, 317–8, 320, 322, 327, 472–3 Tripropyltins, 69, 109 Trivalent chromium, 23, 186, 422, 532, 534 Trivalent gold, 37 Trondheimsfjord, 17, 38, 52, 57, 73 Trypsin, 437, 493 Tungsten, 1, 5, 69, 317, 323, 329, 473–4, 476, 601 Tunicin, 583 Tunisia, 25, 30, 76, 78, 159, 238 Turkey, 158, 160, 162–3, 169, 178, 182, 189, 195, 200, 205–6, 231, 238, 240, 244, 261, 272, 275, 287, 334, 343, 354, 400, 408, 419, 423, 425, 441, 444, 449, 462, 479 Tuscany, 53 Tyrrhenian Sea, 456
U United Kingdom, 17–8, 24–5, 27, 29, 32, 38–9, 43–4, 49, 51, 55, 57–60, 62, 64, 68, 70–1, 73–4, 148, 162, 166, 168, 171, 179, 200, 208, 210, 270, 284–6,
610 Index 288, 303, 317, 320–1, 328, 346, 440, 476, 559, 565 United States, 23, 31, 43–5, 53–5, 73, 77, 79, 162, 197–8, 204, 206, 208, 239, 242, 245, 249, 258, 260, 276, 284–5, 288, 301, 303, 320, 323, 328, 337–8, 342, 345, 353–4, 401, 407, 452–3, 457, 476, 495, 540, 577, 596 United States Environmental Protection Agency, 79, 495, 577 United States Food and Drug Administration, 452 United States Navy, 323, 328 Unleaded gasoline, 131–2 Uranium, 1, 6, 61, 69–70, 139, 293, 317, 323, 329, 476, 601
V Vanadium, 1, 6, 70–1, 118, 121, 125, 139–40, 172, 329–30, 476–7, 523, 526, 540, 589, 593–5, 601
Vanadocytes, 595 Vancouver, 327 Venezuela, 130, 167, 185, 216, 250, 291, 332, 352, 568–9 Venice lagoon, 25, 32, 58, 76, 163, 181, 206, 231, 244, 261, 318, 321, 343 Vera Cruz, 456 Victoria, 327 Vietnam, 401, 404, 406–7, 411, 417, 420, 423, 431, 446, 451, 456, 460, 465–7, 471–2, 474, 477, 487 Virginia, 196, 198, 328, 338, 445, 449 Vistula Lagoon, 17, 30, 44, 49, 57, 74
W Wakayama Prefecture, 15 Wales, 67, 74, 130, 203, 345, 427, 533, 588 Washington, 46, 53, 58, 198–9, 242 West Indies, 67
Western Port Bay, 162 Windscale, 60–1 World Health Organization, 237
Y Yangtze River estuary, 31, 45, 76 Yingluo Bay, 31, 45, 76 York River, 340 Ytterbium, 1, 6, 329, 476, 601 Yttrium, 1, 6, 71–2, 477, 600–1 Yugoslavia, 153
Z Zhejiang, 271, 457 Zinc, 1, 21, 34, 35, 42, 72–9, 109, 121, 140, 170–1, 218, 252, 269, 308, 329–63, 477–95, 520, 526, 540, 543–6, 573, 575–8, 595–6, 600 Zinc aquo ion, 492 Zinc hydroxide, 492 Zinc phosphate, 491, 544 Zinc pyrithione, 35, 494, 536 Zirconium, 1, 6, 79, 119, 363, 495, 524, 526, 600–1
Elsevier The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, UK Radarweg 29, PO Box 211, 1000 AE Amsterdam, The Netherlands First edition 2010 Copyright
#
2010 Elsevier BV. All rights reserved
No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means electronic, mechanical, photocopying, recording or otherwise without the prior written permission of the publisher Permissions may be sought directly from Elsevier’s Science & Technology Rights Department in Oxford, UK: phone (þ44) (0) 1865 843830; fax (þ44) (0) 1865 853333; email:
[email protected]. Alternatively you can submit your request online by visiting the Elsevier web site at http://elsevier.com/locate/permissions, and selecting Obtaining permission to use Elsevier material Notice No responsibility is assumed by the publisher for any injury and/or damage to persons, or property as a matter of products liability, negligence or otherwise, or from any use, or operation of any methods, products, instructions or ideas contained in the material, herein. British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress ISBN (Set): 978-0-444-53439-2 ISBN (Vol 2): 978-0-444-53437-8 For information on all Elsevier publications visit our website at books.elsevier.com Printed and bound in Great Britain 10 11 12 10 9 8 7 6 5 4 3
2 1
This volume is dedicated to the memory of my mentors: Yohay Bin-Nun Lauren R. Donaldson Clarence P. Idyll Morton I. Grossman Frank G. Lowman James E. Lynch Lionel A. Walford
Acknowledgments Early work on this project was conducted at research libraries of the United States Environmental Protection Agency, the United States Department of the Interior, and the National Library of Medicine. During the past several years, all work was conducted at the National Agricultural Library (NAL) of the United States Department of Agriculture, located in Beltsville, Maryland. I thank the librarians and staff of the NAL for their assistance in procuring needed research materials.
xvii
About the Author Ronald Eisler received the B.A. degree from New York University, and the M.S. and Ph.D. degrees from the University of Washington. As a federal research scientist, he served with the United States Department of the Interior in the Territory of Alaska (Egegik), New Jersey (Highlands), Maryland (Laurel), and Washington, DC; the United States Environmental Protection Agency in Rhode Island (Narragansett); and the United States Army Medical Service Corps in Colorado (Denver). In addition to federal service, he was a research assistant at the University of Miami Marine Laboratory (Coral Gables, Florida), a radiochemist at the Laboratory of Radiation Ecology at the University of Washington (Seattle), an aquatic biologist at the New York State Department of Environmental Conservation (Raybrook), and the senior science advisor to the American Fisheries Society (Bethesda, Maryland). Dr. Eisler participated in research and monitoring studies in the Pacific Northwest, the Territory of Alaska, Colorado, the Marshall and Marianas Islands, all along the eastern seaboard of the United States Atlantic coast, the Adirondacks region of New York, the Gulf of Aqaba in the Red Sea, and the Gulf of Mexico. Since 1955 he has authored more than 150 technical articles—including several books and 16 book chapters— mainly on contaminant hazards to plants, animals, and human health, with emphasis on trace metals. He has held a number of adjunct professor appointments and taught for extended periods at the Graduate School of Oceanography of the University of Rhode Island, and the Department of Biology of American University in Washington, DC. He also served as Visiting Professor and Resident Director of Hebrew University’s Marine Biology Laboratory in Eilat, Israel. In retirement, he actively consults and writes on chemical risk assessment. Eisler resides in Potomac, Maryland, with his wife, Jeannette, a teacher of French and Spanish.
xxi
List of Tables – Vol. 2 Table 1.1: Symbol, Atomic Number, and Atomic Weight of the Known Elements Table 2.1: Arsenic Concentrations in Field Collections of Elasmobranchs Table 2.2: Cadmium and Chromium Concentrations in Field Collections of Elasmobranchs Table 2.3: Copper Concentrations in Field Collections of Elasmobranchs Table 2.4: Iron and Lead Concentrations in Field Collections of Elasmobranchs Table 2.5: Manganese Concentrations in Field Collections of Elasmobranchs Table 2.6: Mercury Concentrations in Field Collections of Elasmobranchs Table 2.7: Nickel, Selenium, Silver, and Tin Concentrations in Field Collections of Elasmobranchs Table 2.8: Zinc Concentrations in Field Collections of Elasmobranchs Table 3.1: Antimony Concentrations in Field Collections of Fishes Table 3.2: Arsenic Concentrations in Field Collections of Fishes Table 3.3: Cadmium Concentrations in Field Collections of Fishes Table 3.4: Cesium Concentrations in Field Collections of Fishes Table 3.5: Chromium Concentrations in Field Collections of Fishes Table 3.6: Cobalt Concentrations in Field Collections of Fishes Table 3.7: Copper Concentrations in Field Collections of Fishes Table 3.8: Iron Concentrations in Field Collections of Fishes Table 3.9: Lead Concentrations in Field Collections of Fishes Table 3.10: Manganese Concentrations in Field Collections of Fishes Table 3.11: Mercury Concentrations in Field Collections of Fishes Table 3.12: Molybdenum Concentrations in Field Collections of Fishes Table 3.13: Nickel Concentrations in Field Collections of Fishes Table 3.14: Rhenium, Rubidium, Ruthenium, and Scandium Concentrations in Field Collections of Fishes
xix
xx List of Tables – Vol. 2 Table 3.15: Selenium Concentrations in Field Collections of Fishes Table 3.16: Silver Concentrations in Field Collections of Fishes Table 3.17: Strontium Concentrations in Field Collections of Fishes Table 3.18: Tellurium, Thallium, Tin, Titanium, and Tungsten Concentrations in Field Collections of Fishes Table 3.19: Vanadium Concentrations in Field Collections of Fishes Table 3.20: Zinc Concentrations in Field Collections of Fishes Table 4.1: Cadmium Concentrations in Field Collections of Reptiles Table 4.2: Aluminum, Arsenic, and Barium Concentrations in Field Collections of Reptiles Table 4.3: Chromium and Cobalt Concentrations in Field Collections of Reptiles Table 4.4: Copper Concentrations in Field Collections of Reptiles Table 4.5: Iron, Lead, and Manganese in Field Collections of Reptiles Table 4.6: Mercury Concentrations in Field Collections of Reptiles Table 4.7: Nickel and Selenium Concentrations in Field Collections of Reptiles Table 4.8: Zinc Concentrations in Field Collections of Reptiles Table 5.1: Aluminum, Arsenic, and Boron Concentrations in Field Collections of Birds Table 5.2: Cadmium Concentrations in Field Collections of Birds Table 5.3: Chromium and Cobalt Concentrations in Field Collections of Birds Table 5.4: Copper Concentrations in Field Collections of Birds Table 5.5: Iron Concentrations in Field Collections of Birds Table 5.6: Lead Concentrations in Field Collections of Birds Table 5.7: Lithium and Manganese Concentrations in Field Collections of Birds Table 5.8: Mercury Concentrations in Field Collections of Birds Table 5.9: Molybdenum, Nickel, and Rubidium Concentrations in Field Collections of Birds Table 5.10: Selenium Concentrations in Field Collections of Birds Table 5.11: Silver, Strontium, and Tin Concentrations in Field Collections of Birds Table 5.12: Zinc Concentrations in Field Collections of Birds Table 6.1: Aluminum, Antimony, Arsenic, and Boron Concentrations in Field Collections of Mammals Table 6.2: Cadmium Concentrations in Field Collections of Mammals Table 6.3: Chromium, Cobalt, and Copper Concentrations in Field Collections of Mammals Table 6.4: Iron Concentrations in Field Collections of Mammals
List of Tables – Vol. 2 xxi Table 6.5: Lead Concentrations in Field Collections of Mammals Table 6.6: Manganese Concentrations in Field Collections of Mammals Table 6.7: Mercury Concentrations in Field Collections of Mammals Table 6.8: Molybdenum, Nickel, and Rubidium Concentrations in Field Collections of Mammals Table 6.9: Selenium Concentrations in Field Collections of Mammals Table 6.10: Silver, Strontium, Tin, and Vanadium Concentrations in Field Collections of Mammals Table 6.11: Zinc Concentrations in Field Collections of Mammals Table 7.1: Trace Metals and Marine Vertebrates: Breadth of Coverage Table 7.2: Trace Metals and Marine Vertebrates: Depth of Coverage
Books by Ronald Eisler 2010. Compendium of Trace Metals and Marine Biota. Volume 1: Plants and Invertebrates, Elsevier, Amsterdam, 638 pp. 2007. Eisler’s Encyclopedia of Environmentally Hazardous Priority Chemicals, Elsevier, Amsterdam, 950 pp. 2006. Mercury Hazards to Living Organisms, CRC Press, Boca Raton, Florida, 312 pp. 2004. Biogeochemical, Health, and Ecotoxicological Perspectives on Gold and Gold Mining, CRC Press, Boca Raton, Florida, 356 pp. 2000. Handbook of Chemical Risk Assessment: Health Hazards to Humans, Plants, and Animals. Vol. 1, Metals; Vol. 2, Organics; Vol.3, Metalloids, Radiation, Cumulative Index to Chemicals and Species, Lewis Publishers, Boca Raton, Florida, 1903 pp. 1981. Trace Metal Concentrations in Marine Organisms, Pergamon Press, Elmsford, New York, 687 pp.
xv
CHAPTER 1
Introduction The first major attempt to systematically summarize all that was known about trace metal and metalloid content of marine biota was Vinogradov’s classic The Elementary Chemical Composition of Marine Organisms (Vinogradov, 1953) and the last was Trace Metal Concentrations in Marine Organisms (Eisler, 1981). At that time, I recommended major revision in about 25 years owing to a growing technical literature and to a greater availability of atomic absorption spectroscopy and newer analytical techniques that accurately measure trace metal concentrations in tissues of marine plants and animals at biologically significant levels. This volume on vertebrates—and the companion volume on marine plants and invertebrates (Eisler, 2009)—has two main objectives. The first is to summarize the available world literature on trace metal and metalloid concentrations in tissues of representative field populations of marine, estuarine, and oceanic elasmobranchs; fishes, reptiles, birds, and mammals; and their significance to organisms’ health and their consumers. The database in this subject area alone has more than doubled in the past 25 years. Information on the following elements are presented: aluminum, americium, antimony, arsenic, barium, beryllium, bismuth, boron, cadmium, cerium, cesium, chromium, cobalt, copper, europium, gallium, germanium, gold, indium, iron, lanthanum, lead, lithium, manganese, mercury, molybdenum, neptunium, nickel, niobium, palladium, platinum, plutonium, polonium, radium, rhenium, rubidium, ruthenium, scandium, selenium, silver, strontium, technetium, tellurium, thallium, thorium, tin, titanium, tungsten, uranium, vanadium, yttrium, zinc, and zirconium (Table 1.1). Information on sodium, potassium, calcium, and magnesium were especially abundant, but these were excluded as their concentrations in marine vertebrates were almost always in excess of the 100.0 mg/kg dry weight limit that I set arbitrarily as a trace concentration. The second objective is to synthesize existing information on biological, chemical, and physical factors known to modify uptake, retention, and translocation of each element by selected groups of marine vertebrates under field and laboratory conditions. Recognition of the importance of these modifiers and their accompanying interactions is essential to the understanding of metal kinetics in marine systems and to the interpretation of baseline residue data in marine vertebrates. It is emphasized that major changes are now being
1
2 Chapter 1 Table 1.1: Symbol, Atomic Number, and Atomic Weight of the Known Elements Element
Symbol
Atomic Number
Atomic Weight
Actinium
Ac
89
(227)a
Aluminum
Al
13
26.98
Americium
Am
95
(243)a
Antimony
Sb
51
121.76
Argon
Ar
18
39.95
Arsenic
As
33
74.92
Astatine
At
85
(210)a
Barium
Ba
56
137.33
Berkelium
Bk
97
(247)a
Beryllium
Be
4
Bismuth
Bi
83
208.98
Bohrium
Bh
197
(264)a
Boron
B
5
10.81
Bromine
Br
35
79.90
Cadmium
Cd
48
112.41
Calcium
Ca
20
40.01
Californium
Cf
98
(251)a
Carbon
C
6
12.01
Cerium
Ce
58
140.12
Cesium
Cs
55
132.90
Chlorine
Cl
17
35.45
Chromium
Cr
24
52.00
Cobalt
Co
27
58.93
Copper
Cu
29
63.54
Curium
Cm
96
(247)a
Dubnium
Db
105
(262)a
Dysprosium
Dy
66
162.50
Einsteinium
Es
99
(252)a
9.01
(Continues)
Introduction 3 Table 1.1: Element
Symbol
Cont’d Atomic Number
Atomic Weight
Erbium
Er
68
167.26
Europium
Eu
63
151.96
Fermium
Fm
100
(257)a
Fluorine
F
9
19.00
Francium
Fr
87
(223)a
Gadolinium
Gd
64
157.25
Gallium
Ga
31
69.72
Germanium
Ge
32
72.61
Gold
Au
79
196.97
Hafnium
Hf
72
178.49
Hassium
Hs
108
(269)a
Helium
He
2
Holmium
Ho
67
Hydrogen
H
1
Indium
In
49
114.82
Iodine
I
53
126.90
Iridium
Ir
77
192.22
Iron
Fe
26
55.85
Krypton
Kr
36
83.80
Lanthanum
La
57
138.91
Lawrencium
Lr
103
(262)a
Lead
Pb
82
207.20
Lithium
Li
3
Lutetium
Lu
71
174.97
Magnesium
Mg
12
24.31
Manganese
Mn
25
54.94
Meitnerium
Mt
109
(268)a
Mendelevium
Md
101
(258)a
4.00 164.93 1.01
6.94
(Continues)
4 Chapter 1 Table 1.1:
Cont’d
Element
Symbol
Atomic Number
Atomic Weight
Mercury
Hg
80
200.59
Molybdenum
Mo
42
95.94
Neodymium
Nd
60
144.24
Neon
Ne
10
20.18
Neptunium
Np
93
(237)a
Nickel
Ni
28
58.69
Niobium
Nb
41
92.91
Nitrogen
N
7
14.01
Nobelium
No
102
(259)a
Osmium
Os
76
190.23
Oxygen
O
8
16.00
Palladium
Pd
46
106.42
Phosphorus
P
15
30.97
Platinum
Pt
78
195.08
Plutonium
Pu
94
(244)a
Polonium
Po
84
(210)a
Potassium
K
19
39.10
Praseodymium
Pr
59
140.91
Promethium
Pm
61
(145)a
Protactinium
Pa
91
231.04
Radium
Ra
88
(226)a
Radon
Rn
86
(222)a
Rhenium
Re
75
186.21
Rhodium
Rh
45
102.91
Rubidium
Rb
37
85.47
Ruthenium
Ru
44
101.07
Rutherfordium
Rf
104
(261)a
Samarium
Sm
62
150.36 (Continues)
Introduction 5 Table 1.1: Element
Symbol
Cont’d Atomic Number
Atomic Weight
Scandium
Sc
21
44.96
Seaborgium
Sg
106
(266)a
Selenium
Se
34
78.96
Silicon
Si
14
28.09
Silver
Ag
47
107.87
Sodium
Na
11
23.00
Strontium
Sr
38
87.62
Sulfur
S
16
32.07
Tantalum
Ta
73
180.95
Technetium
Tc
43
(98)a
Tellurium
Te
52
127.60
Terbium
Tb
65
158.92
Thallium
Tl
81
204.38
Thorium
Th
90
232.04
Thulium
Tm
69
168.93
Tin
Sn
50
118.71
Titanium
Ti
22
47.88
Tungsten
W
74
183.84
Ununbium
Unb
112
(277)a
Ununennium
Uue
119
–b
Ununhexium
Uuh
116
–b
Ununnilium
Uun
110
(269)a
Ununoctiium
Uuo
118
–b
Ununpentium
Uup
115
–b
Ununquadium
Uuq
114
–b
Ununseptium
Uus
117
–b
Ununtriium
Uut
113
–b
Unununium
Unn
111
(272)a (Continues)
6 Chapter 1 Table 1.1: Element
Symbol
Cont’d Atomic Number
Atomic Weight
Uranium
U
92
238.03
Vanadium
V
23
50.94
Xenon
Xe
54
131.29
Ytterbium
Yb
70
173.04
Yttrium
Y
39
88.91
Zinc
Zn
30
65.39
Zirconium
Zr
40
91.22
a
Most stable or best known isotope. Yet to be reported.
b
recorded in global climate extremes and in the amounts of metals, metalloids, and other contaminants discharged into the biosphere as a result of human activities; these changes, and others, may ultimately render obsolete certain terms—now used liberally in this volume— such as “controls,” “reference site,” and “environmentally pristine area.” In many cases, the relations between concentrations of these elements in tissues have little relation to concentrations of the same element in the animal’s immediate geophysical environment, including sediments, sediment interstitial waters, diet, and water column. The reasons for this are explored, and their role examined in formulation of proposed criteria to protect natural resources and their consumers. The organization of this book is similar to that of my earlier work on this subject (Eisler, 1981): chapters are arranged in evolutionary order from most primitive to most advanced; within each chapter, metals are arranged in alphabetical order; and, finally, all concentrations are listed in milligrams per kilogram (mg/kg ¼ parts per million) on a fresh weight (FW), dry weight (DW), or ash weight (AW) basis. In all tables, concentrations shown in parentheses represent the range of values documented; others, the arithmetic means.
1.1 Literature Cited Eisler, R., 1981. Trace Metal Concentrations in Marine Organisms. Pergamon, Elmsford, New York, 687 pp. Eisler, R., 2009. Compendium of Trace Metals and Marine Biota. Volume 1: Plants and Invertebrates. Elsevier, Amsterdam. Vinogradov, A.P., 1953. The elementary chemical composition of marine organisms. Sears Foundation for Marine Research, Memoir 2. Yale University, New Haven, Connecticut, 647 pp.
CHAPTER 2
Elasmobranchs The elasmobranchs comprise a group of fish-like vertebrates that includes the sharks and rays. They are often ranked as a subclass of the Teleostei, but differ so fundamentally from the bony fishes that it is best to recognize them as a distinct class. Typical elasmobranchs contain an internal cartilaginous skeleton, cartilaginous jaws, skin with denticles structurally similar to teeth, and with a series of 5-7 gill openings laterally in sharks and ventrally in rays and skates. This is an extremely primitive and successful group, with fossil remains of living species known from the Cretaceous and Jurassic eras. Geographically, elasmobranchs are mostly restricted to tropical and subtropical seas; however, many species regularly inhabit temperate waters, possibly as strays, and some, mostly bottom dwellers, are cosmopolitan in distribution. There is a growing literature on trace metal composition of elasmobranchs.
2.1 Americium Encased embryos of the spotted dogfish, Scyliorhinus canicula, were exposed for 15 days to 241 Am and then transferred to unlabeled seawater for 21 days (Jeffree et al., 2006). During uptake, more than 98% of the 241Am was associated with the egg case and less than 1% with the embryo; very small percentages were found in both yolk and jelly. After 21 days in unlabeled seawater, about half the 241Am remained, with egg case containing nearly 99% and most of the rest in kidney. Uptake rate of 241Am was low when compared to radioisotopes of zinc, manganese, cobalt, and cadmium, in that order. Net influx through the egg case during 96 h exposure for 241Am was equivalent to a concentration factor over seawater of >1000 in the outer layer and about 100 in the inner layer. Juveniles took up about 30 times more 241Am than did encased embryos under similar conditions (Jeffree et al., 2006).
2.2 Arsenic Mean arsenic content in 10 species of Mediterranean Sea sharks was highest in muscle of ghost shark, Chimaera monstrosa (52.4 mg/kg fresh weight, FW) and in liver of the longnose spurdog, Squalus blainvillei (14.2 mg/kg FW; Table 2.1). Interspecies concentration 7
8 Chapter 2 Table 2.1: Arsenic Concentrations in Field Collections of Elasmobranchs Organism
Concentration
Whitetip shark, Carcharhinus longimanus Muscle
3.1 FW
5
Spottail shark, Carcharhinus sorrah Muscle Gills Liver Bone Eye
6.3-10.8 DW 15.2 DW 23.2 DW 10.0 DW 1.6 DW
1 1 1 1 1
Silky shark, Carcharhinus falciformis Muscle Liver Spleen
<1.0 DW 20.0 DW 3.3 DW
2 2 2
Sandbar shark, Carcharhinus milberti Liver
11.2 DW
2
Dusky shark, Carcharhinus obscurus Muscle Liver Brain Pups, whole
6.0 DW 10.0 DW 10.0 DW 2.2-2.8 DW
2 2 2 2
Tope, Galeorhinus australis Muscle
5.0-23.0 FW
3
Six gill shark, Hexanchus griseus Muscle
2.4-5.9 FW
4
Blue pointer, Isurus oxyrhincu Muscle
9.5 FW
5
Gummy shark, Mustelus antarcticus Muscle
7.0-30.0 FW
3
6.2-35.0 FW Max. 10.0 FW
9 9
21.3-64.0 FW Max. 61.0 FW
9 9
North Sea; 1997-1998 Thornback ray, Raja clavata Muscle Liver Lesser spotted dogfish, Scyliorhinus canicula Muscle Liver
Reference
a
(Continues)
Elasmobranchs Table 2.1:
Cont’d
Organism
Concentration
Clearnose skate, Raja eglanteria Muscle Liver Yolk sac
19.0 DW 6.0 DW 22.0 DW
2 2 2
Ray, Raja sp. Muscle
16.2 FW
4
Atlantic guitarfish, Rhinobatus lentiginous Muscle Liver Stomach Yolk sac
11.0 DW 16.0 DW 15.0 DW 1.6 DW
2 2 2 2
Cownose ray, Rhinoptera bonasus Muscle Liver Brain Stomach Spiral valve Spleen Uterus
4.7 DW 17.0 DW 5.4 DW 3.7 DW 2.2 DW 3.8 DW 4.9 DW
2 2 2 2 2 2 2
7.8 (5.1-10.6) FW vs. 10.1 (8.9-17.7) FW 7.1 (2.4-11.5) FW vs. 3.4 (2.1-4.8) FW 5.6 (2.6-11.7) FW vs. 2.1 (1.0-4.9) FW 13.1 (6.8-28.2) FW vs. 9.6 (4.9-21.0) FW 13.6 (9.2-20.6) FW vs. 4.1 (2.5-6.4) FW 14.6 (10.5-22.2) FW vs. 9.6 (5.0-13.4) FW 18.9 FW, max. 25.0 FW vs. 9.2 FW, max. 14.2 FW 12.7 (4.9-20.0) FW vs. 14.2 (6.2-26.5) FW
7
Sharks; 10 species; Mediterranean Sea; muscle versus liver Blackmouth dogfish, Galeus melastomus Length 35-55 cm; weight 42-440 g; Italy Length 19-50 cm; weight 33-319 g; Albania Length 13-52 cm; weight 6-395 G; Italy Length 19-63 cm; weight 16-547 g; Greece Small spotted shark, Scyliorhinus canicula Kitefin shark, Dalatia licha Gulper shark, Centrophorus granulosus Longnose spurdog, Squalus blainvillei
9
Reference
a
7 7 7 7 7 7 7 (Continues)
10 Chapter 2 Table 2.1: Organism Velvet belly, Etmopterus spinax Smooth hound, Mustelus mustelus Blue shark, Prionace glauca Sharpnose sevengill, Heptranchias perlo Ghost shark, Chimaera monstrosa
Cont’d
Concentration 19.1 (17.7-20.8) FW vs. 10.6 (8.2-13.4) FW 15.4 (6.5-31.3) FW vs. 11.9 (8.0-15.3) FW 7.2 (3.3-11.2) FW vs. 6.0 (3.0-11.0) FW 10.9 (7.2-13.3) FW vs. 6.2 (4.2-7.4) FW 52.4 (20.7-79.3) FW vs. 8.6 (1.1-25.2) FW
Reference 7 7 7 7 7
Scalloped hammerhead, Sphyrna lewini Muscle Liver Stomach Intestine
2.2 DW 6.0 DW 1.8 DW 1.9 DW
2 2 2 2
Bonnethead, Sphyrna tiburo Muscle Liver Stomach Spleen Ovary
14.0 DW 17.0 DW 8.9 DW 17.0 DW 17.0 DW
2 2 2 2 2
Common hammerhead, Sphyrna zygaena; Ionian Sea; July 2001; males Muscle Liver
18.0 (15.6-20.2) FW 44.2 (42.0-46.4) FW
8 8
10.0 DW 5.6 FW 5.7 DW <1.0 DW 9.8 DW 9.1 DW 2.6 DW
2 4 2 2 2 2 2
<0.03 DW <0.03 DW 15.6-16.0 DW 0.02-0.04 DW
6 6 6 6
Spiny dogfish, Squalus acanthias Muscle Liver Stomach Spleen Yolk sac Embryo Muscle Arsenate Arsenite Arsenobetaine Arsenocholine
a
(Continues)
Elasmobranchs 11 Table 2.1: Organism Dimethylarsinic acid Methylarsonic acid Tetramethylarsonium Trimethylarsine oxide Unknown
Cont’d
Concentration
Reference
0.28-0.49 DW <0.03 DW 0.23-0.38 DW <0.03 DW 0.16-0.32 DW
6 6 6 6 6
a
Values are in mg As/kg fresh weight (FW) or dry weight (DW). a 1, Zingde et al., 1976; 2, Windom et al., 1973; 3, Glover, 1979; 4, LeBlanc and Jackson, 1973; 5, Hanaoka and Tagawa, 1985; 6, Goessler et al., 1998; 7, Storelli and Marcotrigiano, 2004; 8, Storelli et al., 2003; 9, De Gieter et al., 2002.
differences of arsenic in liver and muscle of Mediterranean Sea sharks ranged widely (Table 2.1) and is attributed to inherent species differences, diet, environmental arsenic in the biosphere, tissue, depth of collection, and body size (Storelli and Marcotrigiano, 2004; Storelli et al., 2003). Arsenic (and other metals and metalloids measured) in tissues of the hammerhead shark, Sphyrna zygaena, was similar to uptake patterns of polychlorinated biphenyls, suggesting significant interactions (Storelli et al., 2003). In general, tissues with high lipid content, such as liver and yolk, contain elevated arsenic concentrations; however, high arsenic concentrations were also measured in muscle of the gummy shark, Mustelus antarcticus (30.0 mg/kg FW) and muscle of a ray, Raja sp. (16.2 mg/kg FW; Table 2.1). The major form of arsenic in shark tissues is arsenobetaine (Goessler et al., 1998; Hanaoka and Tagawa, 1985; Hanaoka et al., 1993), a relatively harmless arsenic compound (Eisler, 2000). Degradation of arsenobetaine in muscle and liver of the star spotted shark (Mustelus manazo) to comparatively toxic inorganic arsenic species occurs in a natural environment and suggests that arsenobetaine bioconverted from inorganic arsenic in seawater is degraded to the original inorganic arsenic; about 13% of the arsenobetaine in shark muscle and 4% in liver was degraded to inorganic arsenic within 40 days (Hanaoka et al., 1993).
2.3 Cadmium Cadmium concentrations in elasmobranchs were usually low, seldom exceeding 0.3 mg Cd/kg FW tissue, although liver cadmium in male hammerhead sharks ranged from 18.4 to 21.0 mg Cd/kg FW (Storelli et al., 2003; Table 2.2). Cadmium burdens in various tissues and organs of nine species of sharks and rays from the North Atlantic Ocean coast were, with some exceptions, always less than 0.5 mg Cd/kg DW (dry weight) tissue (Windom et al., 1973). Comparatively, high cadmium concentrations of 5.0 and 2.6 mg/kg DW were recorded in liver and kidney, respectively, of silky shark, Carcharhinus falciformes; 2.1 in muscle of dusky shark, Carcharhinus obscurus; and 3.7 in stomach of spiny dogfish, Squalus acanthias (Windom et al., 1973). The hepatic cadmium burden in thorny skate, Raja radiata, collected in 1993 from the Gulf of St. Lawrence was three times higher than in conspecifics
12 Chapter 2 Table 2.2: Cadmium and Chromium Concentrations in Field Collections of Elasmobranchs Element and Organism
Concentration
Reference
a
Cadmium Bamboo shark, Chiloscyllium plagiosum; Hong Kong; 2003-2004 Muscle Spleen Liver
0.01 (<0.001-0.17) FW 0.01 (<0.001-0.05) FW 0.24 (0.04-1.1) FW
6 6 6
Medians <0.05 FW; max. 0.3 FW
1
Tope, Galeorhinus australis Muscle
<0.01-0.06 FW
2
Gummy shark, Mustelus antarcticus Muscle
<0.01-0.05 FW
2
Smooth dogfish, Mustelus canis Liver Muscle
<0.2 FW <0.1 FW
3 3
Thornback ray, Raja clavata Blood Heart Spleen Liver Kidney Gut Gill filaments Skin Muscle Cartilage
0.010 FW <0.010 FW 0.007 FW 0.030 FW 0.016 FW 0.025 FW 0.018 FW 0.018 FW <0.005 FW 0.005 FW
4 4 4 4 4 4 4 4 4 4
Sharks; 3 species; Bahia Blanca estuary, Argentina; 1985-1986 Muscle Liver
0.14-0.18 (0.0-12.0) FW 5.6-8.4 (1.5-13.6) FW
7 7
Sharks; 4 spp. Muscle Liver
<0.012 FW 0.28-7.2 FW
3 3
Sharks; Hong Kong and environs Spleen; 9 spp. Liver; 20 spp. Muscle; 31 spp.
<0.02-0.09 FW <0.02-19.8 FW 0.003-0.79 FW
6 6 6
Elasmobranchs; 7 spp. Muscle
(Continues)
Elasmobranchs 13 Table 2.2:
Cont’d
Element and Organism
Concentration
Reference
Common hammerhead, Sphyrna zygaena; Ionian Sea; July 2001; males Muscle Liver
Max. 0.03 FW 19.7 (18.4-21.0) FW
8 8
Spiny dogfish, Squalus acanthias Muscle Liver
0.11 FW; 0.40 DW 0.03 FW; 0.10 DW
5 5
Bamboo shark, Chiloscyllium plagiosum; Hong Kong; 2003-2004 Muscle Spleen Liver
0.21 (0.09-0.97) FW 0.24 (0.001-0.96) FW 0.12 (0.05-0.44) FW
6 6 6
Sharks; Hong Kong and environs Spleen; 9 spp. Muscle; 31 spp. Liver; 20 spp.
0.24 FW 0.14-0.50 FW 0.12-0.53 FW
6 6 6
Common hammerhead, Sphyrna zygaena; Ionian Sea; July 2001; males Muscle Liver
0.18 (0.14-0.20) FW 0.53 (0.51-0.56) FW
8 8
a
Chromium
Values are in mg metal/kg fresh weight (FW) or dry weight (DW). a 1, Eustace, 1974; 2, Glover, 1979; 3, Greig and Wenzloff, 1977a,b; 4, Pentreath, 1977a; 5, Bernhard and Zattera, 1975; 6, Cornish et al., 2007; 7, Marcovecchio et al., 1991; 8, Storelli et al., 2003.
from the St. Lawrence estuary 600 km inland, and is reportedly related to the higher cadmium concentrations in Gulf sediments that were reflected in cadmium content of prey (Rouleau et al., 2006). Cadmium uptake by the thornback ray, Raja clavata, was studied under laboratory conditions by Pentreath (1977a). He found that R. clavata retained cadmium from food, with highest accumulations in liver; cadmium was also taken up from seawater, but this was not as important a route as diet. Encased embryos of the spotted dogfish were held for 15 days in seawater containing 109Cd, then transferred to cadmium-free seawater for 21 days (Jeffree et al., 2006). Concentration factors from seawater during uptake were about 0.4 for embryo, 1.2 for yolk, 1.3 for jelly, and 957.0 for case. At the end of the 21-day depuration period,
14 Chapter 2 these values were 0.1 for embryo, 0.02 for yolk, 0.02 for jelly, and 99.8 for case; the absolute amount of 109Cd declined by a factor near 2 (Jeffree et al., 2006).
2.4 Cerium Radiocerium-144 activity levels in R. clavata from a 144Ce-contaminated area were highest in stomach tissues, suggesting that diet is the major route for cerium accumulation in this species (Mauchline and Taylor, 1964).
2.5 Cesium Radiocesium-137 is soluble and tends to remain in seawater (Mauchline and Taylor, 1964); the highest 137Cs levels measured in the thornback ray, R. clavata, collected near a nuclear fuel reprocessing facility were in stomach contents, with lower and similar levels in all other tissues measured. Jefferies and Hewett (1971) aver that the biological half-times of 134Cs in various tissues of R. clavata ranged from a low of 89 days in kidney to 219 days in cartilage. Intermediate half-times of 105-142 days were measured in gut, gills, and liver; 154-189 days for muscle, skin, and blood; and 180 days for whole animal. After 720 days, tissues with the highest 134Cs accumulations relative to the medium were gut (5.8), kidney (5.7), and muscle (5.7). Lowest accumulation relative to the medium was in blood (0.6). In general, there was increasing accumulation with increasing length of exposure (Jefferies and Hewett, 1971). Encased embryos of spotted dogfish, S. canicula, were exposed for 15 days to 134Cs then transferred to unlabeled seawater for 21 days (Jeffree et al., 2006). At day 15, 10% of the total 134Cs activity was associated with the embryo, 20% with the jelly, >69% with the case, and a small percentage with the yolk. This is in sharp contrast to results of studies with 65 Zn, 54Mn, 57Co, 109Cd, and 241Am wherein >98% of the radioactivity was associated with the case (Jeffree et al., 2006). Embryo to water concentration factor ranged from 0.14 for 134Cs to 7.4 for 65Zn, and this may account for the high embryo uptake of 134Cs. After 21 days in unlabeled seawater, the egg case contained 87.5% of the total radioactivity, the embryo 10%, and the jelly 3% (Jeffree et al., 2006). Net influx of 134Cs through the egg case of spotted dogfish during 96 h was about 3 in the external layer—versus 241Am and 60Co with concentration factors of >1000—and about 1.5 in the interior layers versus about 100 for 241 Am and 60Co (Jeffree et al., 2007).
2.6 Chromium Smooth dogfish, Mustelus canis, from the New York Bight and Long Island Sound had chromium burdens below analytical detection limits. In muscle, this value was less than 0.3 mg Cr/kg FW; in liver, it was less than 0.8 mg/kg FW (Greig and Wenzloff, 1977a,b).
Elasmobranchs 15 Sharks collected in the vicinity of Hong Kong, China, usually contained 0.1-0.5 mg Cr/kg FW in muscle, liver, and spleen, with maximum concentrations of about 1.0 mg Cr/kg FW (Table 2.2; Cornish et al., 2007). Tissue concentrations of chromium in the bamboo shark tend to decrease with increasing body weight (Cornish et al., 2007).
2.7 Cobalt Encased embryos of spotted dogfish, S. canicula, were held in seawater containing 57Co for 15 days then transferred to cobalt-free media for 21 days (Jeffree et al., 2006). At day 15, 99.4% of the total radioactivity was in egg case and about 0.3% in embryo. At day 21 postexposure, total radioactivity had declined about 21%, at which time mean concentration factors were about 3.0 for embryo, 0.2 for yolk, 1031.6 for case, and 7.1 for jelly; more than 99% of the total 57Co radioactivity was in the case (Jeffree et al., 2006). Net influx of 60Co through the egg case, as was true for 241Am, was >1000 in the outer layer and about 100 in the inner layer (Jeffree et al., 2007).
2.8 Copper The highest copper concentrations recorded in elasmobranch tissues were 56.3 mg Cu/kg FW in spleen of the bamboo shark collected near Hong Kong in 2003-2004, 12.1 mg/kg FW in skin of sharks from British waters, 44.0 mg Cu/kg DW in liver of the clearnose skate, and 230.0 mg Cu/kg AW (ash weight) in liver of the oceanic whitetip shark (Table 2.3). Among rays, liver always contained the highest copper concentrations of all tissues examined (Table 2.3). Among sharks collected in British waters, copper concentrations in all tissues are highest from inshore demersal species and lowest from offshore pelagic species, with males having higher copper concentrations in liver than females (Vas, 1991). Copper burdens in tissues of marine vertebrates, including elasmobranchs were consistently lower than copper tissue burdens from all invertebrate groups examined (Eisler, 1979), suggesting discrimination against copper among the highest marine trophic levels. Moreover, tissue copper concentrations in elasmobranchs tend to decrease with increasing body weight (Cornish et al., 2007). Spiny dogfish, S. acanthias can survive immersion in 0.5, 1.0, or 1.5 mg Cu/L for 96 h; however, all concentrations induced acidosis, and lactate accumulation (De Boeck et al., 2007). At all exposures, plasma Na+ and Cl concentrations increased, urea excretion increased, and plasma urea dropped. At high copper levels, gill Na+/K+-ATPase activities were reduced by 45% (1.0 mg/L) and 62% (1.5 mg/L). Copper accumulations significantly increased in gill (3.2 mg Cu/kg DW in controls vs. 21.6 in 0.5, 41.0 in 1.0, and 142.4 in 1.5 mg Cu/L), plasma (8.6 mg/kg DW in controls vs. 13.3-20.0 mg/kg DW in experimentals), and kidney (5.7 DW in controls vs. 8.5, 26.4, and 82.7 mg Cu/kg DW in experimentals). Authors conclude that copper exerts a toxic effect on Na+/K+-ATPase activities in sharks similar to those of teleosts, but there is an additional toxic action on elasmobranch urea retention (De Boeck et al., 2007).
16 Chapter 2 Table 2.3: Copper Concentrations in Field Collections of Elasmobranchs Organism Silky shark, Carcharhinus falciformes Muscle
Concentration
Reference
0.3-0.6 FW; 1.0-10.0 DW; 19.0–25.0 AW 2.1 DW 4.9 DW 5.7 DW 8.4 DW <1.0 DW 6.3 DW 4.6 DW
2 2 2 2 2 2 2
Oceanic whitetip shark, Carcharhinus longimanus Skin Muscle Stomach Liver Vertebrae
8.6 FW; 21.0 DW; 100.0 AW 0.5 FW; 2.4 DW; 43.0 AW 0.04 FW; 2.1 DW; 24.0 AW 1.3 FW; 2.2 DW; 230.0 AW 3.5 FW; 11.0 DW; 37.0 AW
1 1 1 1 1
Sandbar shark, Carcharhinus milberti Liver
2.7 DW
2
Dusky shark, Carcharhinus obscurus Muscle Liver Brain Pup, whole
1.5 DW 1.3 DW 8.4 DW 1.6-2.4 DW
2 2 2 2
0.15 (0.07-0.47) FW 9.1 (0.49-56.3) FW 1.1 (0.08-12.1) FW Medians: <0.2-0.7 FW; max. 4.3 FW
8 8 8 4
Tope, Galeorhinus australis Muscle
0.2-0.6 FW
5
Gummy shark, Mustelus antarcticus Muscle
0.2-0.4 FW
5
Smooth dogfish, Mustelus canis Liver Muscle
0.6-1.5 FW 0.7-1.0 FW
6 6
Muscle Liver Kidney Brain Gonads Gills Spleen
Bamboo shark, Chiloscyllium plagiosum; Hong Kong; 2003-2004 Muscle Spleen Liver Elasmobranchs; 7 spp; muscle
a
1
(Continues)
Elasmobranchs 17 Table 2.3:
Cont’d
Organism
Concentration
Reference
Clearnose skate, Raja eglanteria Muscle Liver Yolk-sac
3.2 DW 44.0 DW 4.4 DW
2 2 2
Atlantic guitarfish, Rhinobatis lentiginous Muscle Liver Stomach Yolk-sac
2.2 DW 6.6 DW 6.2 DW 2.7 DW
2 2 2 2
Cownose ray, Rhinoptera bonasus Muscle Liver Brain Spiral valve Spleen Uterus Stomach
2.3 DW 13.0 DW 10.0 DW 5.2 DW 3.6 DW 3.4 DW 7.0 DW
2 2 2 2 2 2 2
Sharks; 10 spp.; coastal and Atlantic Ocean; Britain; 1984-1988 Gill Gonad Heart Jaws Kidney Liver Muscle Pancreas Skin Spleen Vertebra
0.05-2.2 FW 0.1-4.9 FW 0.03 FW 1.7-3.3 FW 0.02-4.0 FW 0.2-7.8 FW 0.2-2.4 FW 0.7 FW 0.6-12.1 FW 0.03-2.5 FW 0.5-5.9 FW
7 7 7 7 7 7 7 7 7 7 7
Sharks; 4 spp.; near ocean dumpsite Muscle Liver
<1.5 FW 1.3-9.0 FW
6 6
Sharks; Honk Kong and environs Muscle; 31 spp. Liver; 20 spp. Spleen; 9 spp.
0.07-1.9 FW <0.02-7.8 FW <0.02-9.1 FW
8 8 8
a
(Continues)
18 Chapter 2 Table 2.3:
Cont’d
Organism
Concentration
Reference
Scalloped hammerhead, Sphyrna lewini Muscle Liver Stomach Intestine
2.0 DW 6.2 DW 10.0 DW 5.7 DW
2 2 2 2
Bonnethead, Sphyrna tiburo Muscle Liver Stomach Spleen Ovary
3.0 DW 3.6 DW 4.8 DW 2.4 DW 2.4 DW
2 2 2 2 2
Common hammerhead, Sphyrna zygaena; Ionian Sea; July 2001; males Muscle Liver
1.5 (1.0-1.8) FW 6.1 (5.0-7.3) FW
9 9
Spiny dogfish, Squalus acanthias Muscle Liver Stomach Spleen Yolk-sac Embryo
2.3 DW 4.5 DW 4.8 DW 16.0 DW 0.9 DW 3.0 DW
2 2 2 2 2 2
a
Values are in mg Cu/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Lowman et al., 1966; 2, Windom et al., 1973; 3, Zingde et al., 1976; 4, Eustace, 1974; 5, Glover, 1979; 6, Greig and Wenzloff, 1977a,b; 7, Vas, 1991; 8, Cornish et al., 2007; 9, Storelli et al., 2003.
2.9 Iron Blood and highly vascularized tissues in the thornback ray, R. clavata contained the highest concentrations of total iron, with a maximum recorded value of 109.8 mg Fe/kg FW in spleen (Table 2.4). After 20 days immersion in radioactive iron-59 solutions, whole thornback rays contained 20 times more 59Fe than ambient seawater, with most iron probably in hematopoietic tissues. The significance of decreasing iron concentrations in sandbar shark vertebrae with increasing age of the organism is not clear (Table 13.4), but might be associated positively with calcium and zinc, and negatively with magnesium (Eisler, 1967).
Elasmobranchs 19 Table 2.4: Iron and Lead Concentrations in Field Collections of Elasmobranchs Element and Organism
Concentration
Reference
Iron Sandbar shark, Carcharhinus milberti; vertebrae Small sharks, 64 cm total length Medium sharks, 130 cm total length Large sharks, 209 cm total length
920.0 AW 230.0 AW
1 1
60.0 AW
1
105.4 FW 29.2 FW 109.8 FW 62.8 FW 33.5 FW 9.2 FW 13.6 FW 24.5 FW 9.2 FW 2.6 FW 5.4 FW 34.1 FW 9.4 FW 10.1 FW
2 2 2 2 2 2 2 2 2 2 2 2 2 2
Bamboo shark, Chiloscyllium plagiosum; Hong Kong; 2003-2004 Muscle Spleen Liver
<0.001 FW <0.001 FW <0.001 FW
3 3 3
Sharks; Hong Kong and environs Muscle; 31 spp. Liver; 20 spp. Spleen; 9 spp.
<0.03-1.9 FW <0.02-3.8 FW <0.001-0.2 FW
3 3 3
Common hammerhead, Sphyrna zygaena; Ionian Sea; July 2001; males Muscle Liver
Max. 0.04 FW 0.17 (0.14-0.19) FW
4 4
Thornback ray, Raja clavata Blood Heart Spleen Liver Kidney Gonad Gut Gill filaments Skin Muscle Cartilage Rectal gland Whole body Brain and nerve cord Lead
Values are in mg metal/kg fresh weight (FW) or ash weight (AW). a 1, Eisler, 1967; 2, Pentreath, 1973; 3, Cornish et al., 2007; 4, Storelli et al., 2003.
a
20 Chapter 2
2.10 Lead Smooth dogfish, M. canis from Long Island Sound and the New York Bight always contained less than 0.8 mg Pb/kg FW in liver and muscle (Greig and Wenzloff, 1977a,b). Mean concentrations in tissues of sharks from the Hong Kong vicinity range up to 3.8 mg Pb/kg FW in liver, 1.9 in muscle, and 0.2 mg Pb/kg FW in spleen (Table 2.4; Cornish et al., 2007).
2.11 Manganese Except for cartilage and skin, which contain 9.1 and 2.7 mg Mn/kg FW, respectively, most elasmobranch tissues contain less than 1.0 mg Mn/kg FW (Table 2.5). Intermediate values were recorded in liver, kidney, gill filaments, and rectal gland (Table 2.5). Tissue manganese concentrations tend to decrease with increasing body weight (Cornish et al., 2007). Encased embryos of spotted dogfish were exposed for 15 days to 54Mn; then transferred to unlabeled seawater for 21 days (Jeffree et al., 2006). At day 15, 98.5% of the total radioactivity was in egg case, 0.54% in embryo, 0.06% in jelly, and 0.05% in yolk. After 21 days of depuration, total 54Mn radioactivity had declined 56%; of the total, 97.2% was in the case and 0.18% in the embryo (Jeffree et al., 2006).
2.12 Mercury Total mercury concentrations in tissues and organs of nine species of North Atlantic Ocean sharks and rays were usually less than 2.0 mg Hg/kg tissue on a DW basis; however, comparatively elevated burdens were measured in muscle (5.3 mg/kg DW) and gonads of Carcharhinus falciformis, in muscle (4.2 mg/kg DW) of C. obscurus (Windom et al., 1973), and in liver (39.5 mg/kg FW) and muscle (21.1 mg/kg FW) of the common hammerhead, S. zygaena (Storelli et al., 2002, 2003; Table 2.6). Total mercury and organomercury concentrations in muscle of blue shark, Prionace glauca, are positively correlated with shark length (Branco et al., 2007). Mercury concentrations in muscle of five species of sharks from coastal waters of Brazil increased with increasing shark length; most of the mercury (63-95%) was methylmercury (de Pinho et al., 2002). Forrester et al. (1972) report that sex, length, and collection area influenced mercury levels in muscle of the spiny dogfish, S. acanthias. For any given body length above 65 cm, the mercury content was higher in males than in females, and higher in samples taken in the Fraser River estuary than other areas of the Strait of Georgia, British Columbia. Methylmercury levels in shark muscle were significantly higher in males than in females (de Pinho et al., 2002).
Elasmobranchs 21 Table 2.5: Manganese Concentrations in Field Collections of Elasmobranchs Organism
Concentration
Reference
Spottail shark, Carcharhinus sorrah Muscle
6.6-10.6 DW
1
Bamboo shark, Chiloscyllium plagiosum; Hong Kong; 2003-2004 Muscle Spleen Liver
0.09 (0.03-0.39) FW 1.1 (0.31-3.8) FW 0.21 (0.05-0.83) FW
6 6 6
Elasmobranchs; 7 spp. Muscle
<0.5-1.6 FW
2
Tope, Galeorhinus australis Muscle
0.3-0.6 FW
3
Gummy shark, Mustelus antarcticus Muscle Liver
0.4 FW 0.4 FW
4 4
Thornback ray, Raja clavata Blood Heart Spleen Liver Kidney Gonad Gut Gill filaments Skin Muscle Cartilage Rectal gland Brain and nerve cord Whole body
0.16 FW 0.27 FW 0.32 FW 1.4 FW 1.9 FW 0.37 FW 0.82 FW 1.4 FW 2.7 FW 0.29 FW 9.1 FW 1.1 FW 0.41 FW 2.4 FW
5 5 5 5 5 5 5 5 5 5 5 5 5 5
Sharks; 4 species Muscle
<0.5 FW
4
Sharks; Hong Kong and environs Spleen; 9 spp. Liver; 20 spp. Muscle; 31 spp.
<0.02-2.05 FW <0.02-2.06 FW <0.02-2.07 FW
6 6 6
a
Values are in mg Mn/kg fresh weight (FW) or dry weight (DW). a 1, Zingde et al., 1976; 2, Eustace, 1974; 3, Glover, 1979; 4, Greig and Wenzloff, 1977a,b; 5, Pentreath, 1973; 6, Cornish et al., 2007.
22 Chapter 2 Table 2.6: Mercury Concentrations in Field Collections of Elasmobranchs Organism
Concentration
Carcharhinus; spp.; muscle; northern Gulf of Mexico; summer 2002-2003; total mercury
1.61 (0.46-4.08) FW
Reference 26
Elasmobranchs; muscle 4 spp. 8 spp.
0.06-0.48 FW 1.5-4.0 DW
2 3
Shark, Eulamia ellioti Testes Liver Muscle
<0.01 FW 0.01 FW 0.19 FW
4 4 4
Shark, Galeus canis; muscle
0.51 (0.09-1.91) FW
5
Blackmouth dogfish, Galeus melastomus; liver; 1999; Mediterranean Sea Total mercury Methylmercury
0.60 (0.04-4.09) FW 0.28 (0.02-1.89) FW
19 19
Tope, Galeorhinus australis Muscle Muscle Muscle
0.38 FW 2.0 DW 0.6-2.2 FW
6 7 8
0.65 (0.04-3.94) FW
5
Gummy shark, Mustelus antarcticus Muscle Muscle
0.50 FW 0.3-1.2 FW
6 8
Smooth dogfish, Mustelus canis Muscle Liver
0.53 (0.15-1.47) FW 2.0 FW
5 1
Gatuso shark, Mustelus schmitti; Argentina; Bahia Blanca estuary; 1982-2003; muscle vs. liver 1982-1988 1989-2000 2001-2003
0.89 FW vs. 0.88 FW 0.33 FW vs. 0.31 FW 0.09 FW vs. 0.07 FW
25 25 25
Porbeagle, Lamna cornubica; muscle
a
(Continues)
Elasmobranchs 23 Table 2.6: Organism North Sea and environs; 1997-1999; muscle; total mercury vs. methylmercury Thornback ray, Raja clavata Lesser spotted dogfish, Scyliorhinus canicula
Cont’d
Concentration
0.021 FW vs. 0.019 FW 0.61 FW vs. 0.60 FW
Reference
28 28
Blue shark, Prionace glauca Muscle Azores area vs. Equator area; September 2004-February 2005 Total mercury Muscle Liver Organic mercury Muscle Liver
0.22-1.3 FW vs. 0.68-2.5 FW 0.03-0.96 FW vs. 0.15-2.2 FW
18 18
0.18-1.2 FW vs. 0.65-1.95 FW 0.01-0.80 FW vs. 0.08-0.83 FW
18 18
Thornback ray, Raja clavata Blood Gut Gill filaments Muscle Blood plasma
0.22 FW 0.16 FW 0.13 FW 0.05 FW 0.001 FW
0.55-0.74 FW
a
1
9 9 9 9 9
Starry ray, Raja radiata; Greenland; Barents Sea; summers 1991-1992; muscle
0.2-0.4 DW
15
Rays; muscle
0.39 (0.04-1.4) FW
Milk shark, Rhizoprionodon acutus; muscle; Gulf of Oman; May-June 2004 Total mercury Methylmercury
0.03-0.76 FW 0.02-0.41 FW
27 27
Lesser spotted dogfish, Scyliorhinus caniculus; muscle; Irish Sea; August 1995 North and NW areas Northeast sites Southeast sites Southwest sites
0.15-2.1 FW 0.3-2.2 FW 0.2-5.6 FW 0.1-2.8 FW
16 16 16 16
5
(Continues)
24 Chapter 2 Table 2.6:
Cont’d
Organism
Concentration
Sharks; Australia; 1980; muscle; 7 spp. Carcharhinus spp. Sphyrna spp.
Max. 4.3 FW Max. 4.9 FW
17 17
1.77 FW
22
1.9 FW 2.22 FW; max. 4.1 FW
22 22
0.41 FW
22
0.36 FW
22
0.36-0.58 (0.03-3.4) FW 0.8-2.3 (0.0-2.9) FW
23 23
(1.0-8.8) FW
20
(0.5-8.4) FW
20
(1.8-4.6) FW
20
9.7 (8.8-10.5) FW vs. 9.1 (7.9-10.0) FW 4.4 (3.6-6.0) FW vs. 3.8 (3.2-5.0) FW 0.6 (0.2-1.1) FW vs. 0.6 (0.2-1.0) FW
21
2.7 (0.7-5.0) FW vs. 2.1 (0.5-3.7) FW 1.0 (0.2-2.1) FW vs. 1.0 (0.2-2.0) FW
21
Sharks; 5 spp.; offshore waters; Brazil; muscle Piscivores Night shark, Carcharhinus signatus Dogfish, Squalus megalops Dogfish, Squalus mitsukurii Invertebrate feeders Smooth dogfish, Mustelus canis Florida smoothhound, Mustelus norrisi Sharks; 3 species; Bahia Blanca estuary, Argentina; 1985-1986 Muscle Liver Sharks; muscle; Mediterranean Sea, Israel Blackmouth dogfish, Galeus melastomus Gulper shark, Centrophorus granulosus Velvet belly, Etmopterus spinax Sharks; Mediterranean Sea, Italy; 1999; muscle; total mercury vs. methylmercury Gulper shark, Centrophorus granulosus Kitefin shark, Dalatia licha Velvet belly, Etmopterus spinax Blackmouth dogfish, Galeus melastomus Adriatic Sea, Italy Adriatic Sea, Albania
Reference
a
21 21
21 (Continues)
Elasmobranchs 25 Table 2.6: Organism Ionian Sea Aegean Sea Sharpnose sevengill, Heptranchus perlo Smoothhound, Mustelus mustelus Small spotted shark, Scyliorhinus canicula Common hammerhead, Sphyrna zygaena Longnose spurdog, Squalus blainvillei Winghead shark, Sphyrna blochi Ovary Liver Muscle Common hammerhead, Sphyrna zygaena; Ionian Sea; July 2001; males Total mercury Muscle Liver Methylmercury Muscle Liver Spiny dogfish, Squalus acanthias Muscle Muscle Muscle Females Males Belly flaps Females Males Ovarian embryos, whole Age group zero+ Age group 1+
Cont’d
Concentration
Reference
0.8 (0.2-2.8) FW vs. 0.7 (0.2-2.2) FW 2.1 (0.9-5.5) FW vs. 1.6 (0.6-4.3) FW 1.3 (1.1-1.4) FW vs. 1.2 (1.0-1.4) FW 0.31 (0.23-0.34) FW vs. 0.2 (0.18-0.28) FW 1.5 (0.8-2.6) FW vs. 1.2 (0.7-2.0) FW 18.3 FW vs. 16.1 FW
21
4.5 (3.9-7.4) FW vs. 4.1 (3.2-7.2) FW
21
<0.1 FW 0.12 FW 0.21 FW
a
21 21 21 21 21
4 4 4
12.1 (8.6-21.1) FW 35.9 (32.3-39.5) FW
24 24
14.0 (7.5-19.6) FW 23.8 (19.1-23.8) FW
24 24
0.20-1.14 FW 0.25 (0.07-0.64) FW
10 5
0.92 (0.09-2.58) FW 0.96 (0.21-1.61) FW
11 11
0.85 (0.14-2.24) FW 0.93 (0.49-1.24) FW
11 11
0.015 FW 0.029 FW
12 12 (Continues)
26 Chapter 2 Table 2.6: Organism Adults; muscle Males; body length 72 cm 95 cm Females; body length 77 cm 120 cm Muscle Gills Spleen Kidney Gonad Pancreas Muscle; from body length ranges 48-65 cm 66-75 cm 76-85 cm 86-99 cm Adult females Muscle Gills Kidney Spleen Pups taken from adult females Muscle Liver Gills Kidney Spleen Yolk Dogfish, Squalus sp.; muscle California dogfish, Squalus suckleyi Maternal females Muscle Uteral membrane Graafian follicles; 1 cm diameter vs. 3 cm diameter
Cont’d
Concentration
Reference
0.5 FW 1.7 FW
12 12
0.5 FW 2.0 FW 0.1-1.5 FW 0.02-0.62 FW 0.01-0.60 FW 0.02-1.3 FW Max. 0.08 FW 0.09-0.12 FW
12 12 13 13 13 13 13 13
0.23 FW 0.35 FW 0.42 FW 0.60 FW
13 13 13 13
0.4-1.1 FW 0.10-0.62 FW 0.10-1.32 FW 0.03-0.60 FW
13 13 13 13
<0.05 FW <0.05 FW <0.05 FW <0.05 FW <0.05 FW <0.05 FW
13 13 13 13 13 13
0.76 FW
0.66 FW 0.08 FW 0.047 FW vs. 0.034 FW
a
6
14 14 14 (Continues)
Elasmobranchs 27 Table 2.6: Organism Fetus; 7.5 cm Whole Yolk-sac Fetus; 10 cm Whole Yolk-sac Pup, whole
Concentration
Cont’d Reference
0.046 FW 0.024 FW
14 14
0.021 FW 0.009 FW 0.037 FW
14 14 14
a
Values are in mg Hg/kg fresh weight (FW) or dry weight (DW). a 1, Greig and Wenzloff, 1977a,b; 2, Menasveta and Siriyong, 1977; 3, Gardner et al., 1975; 4, Kureishy et al., 1979; 5, Cumont et al., 1975; 6, Bloom and Ayling, 1977; 7, Ratkowsky et al., 1975; 8, Glover, 1979; 9, Pentreath, 1976; 10, Childs and Gaffke, 1973; 11, Hall et al., 1977; 12, Forrester et al., 1972; 13, Greig et al., 1977; 14, Childs et al., 1973; 15, Joiris et al., 1997; 16, Leah et al., 1991; 17, Lyle, 1984; 18, Branco et al., 2007; 19, Storelli and Marcotrigiano, 2002; 20, Hornung et al., 1993; 21, Storelli et al., 2002; 22, de Pinho et al., 2002; 23, Marcovecchio et al., 1991; 24, Storelli et al., 2003; 25, De Marco et al., 2006; 26, Cai et al., 2007; 27, Al-Reasi et al., 2007; 28, Baeyens et al., 2003.
High uptake of mercury from seawater by the thornback ray, R. clavata, is documented by Pentreath (1976). Uptake was greater with methylmercury salts than inorganic divalent mercury salts, and retention was longer with organomercury compounds. Mercury levels in fetuses of the California dogfish, Squalus suckleyi, were significantly lower than maternal levels (Childs et al., 1973). Fetuses of the S. suckleyi do not reflect the comparatively high concentrations of mercury found in maternal musculature. On an AW basis, mercury in muscle of the maternal female was 21 times greater than in any follicle or fetal stage and 42 times greater than the uterine wall, suggesting that mercury is uniquely absent from the fetal environment and may even be selectively excluded. Childs et al. (1973) speculate that since follicles are primarily lipid in composition, and since mercury is normally bound to a sulfhydryl ligand, then mercury would probably not accumulate in the follicles to any great extent. In Brazil, the mercury criterion for shark muscle and other seafood products of commerce for human consumers is 0.5 mg total mercury/kg FW (de Pinho et al., 2002).
2.13 Nickel Nickel concentrations in tissues of sharks from coastal and oceanic waters of Britain ranged from <0.02 to 10.8 mg/kg FW (Table 2.7); concentrations were highest in fish-eating, mid-water species such as the blue shark (P. glauca) and tope shark (Galeorhinus galeus) (Vas, 1991). Nickel interacts with cadmium in smooth muscle of the ventral aorta of the spiny dogfish, S. acanthias. Muscle contracted significantly on exposure to cadmium or 6.0-11.0 mg Ni/L, but not other divalent cations (Evans and Walton, 1990). Cadmium-induced vasoconstriction of shark muscle (but not nickel) was inhibited by atropine (WHO, 1991).
28 Chapter 2 Table 2.7: Nickel, Selenium, Silver, and Tin Concentrations in Field Collections of Elasmobranchs Element and Organism
Concentration
Reference
a
Nickel Whitetip shark, Carcharhinus longimanus Liver Skin Vertebrae
0.05 FW; 0.1 DW 1.9 FW; 7.3 DW 1.6 FW; 4.9 DW
1 1 1
<0.001 FW
4
Smooth dogfish, Mustelus canis; New York Bight and Long Island Sound Liver Muscle
<0.3 FW <0.3 FW
3 3
Sharks; Hong Kong and environs Muscle; 31 spp. Liver; 20 spp. Spleen; 9 spp.
<0.01-2.8 FW <0.001-3.2 FW <0.001-1.3 FW
4 4 4
Sharks; 10 spp.; coastal and Atlantic Ocean waters; Britain; 1984-1988; inshore species vs. Offshore species Gills Gonads Heart Jaws Kidneys Liver Muscle Pancreas Skin Spleen Vertebrae
0.3-1.8 FW vs. 1.7-1.9 FW <0.02-8.3 FW vs. 1.7 FW No data vs. 2.8 FW 5.7 FW vs. 0.3 FW 0.07-1.2 FW vs. 1.6 FW <0.02-0.8 FW vs. 1.4-2.6 FW <0.02-1.8 FW vs. 1.4-2.6 FW 0.9 FW vs. no data <0.02-3.4 FW 1.0-2.0 FW <0.02-0.8 FW vs. 1.3 FW 0.5-2.4 FW vs. 0.2-10.8 FW
2 2 2 2 2 2 2 2 2 2 2
0.92 (0.20-2.13) FW
6
Bamboo shark, Chiloscyllium plagiosum; Hong Kong; 2003-2004; all tissues
Selenium Blackmouth dogfish, Galeus melastomus; liver; 1999; Mediterranean Sea
(Continues)
Elasmobranchs 29 Table 2.7:
Cont’d a
Element and Organism
Concentration
Reference
Blue shark, Prionace glauca; Azores area vs. Equator area; 2005 Muscle Liver
0.08-0.30 FW vs. 0.23-0.46 FW 0.47-3.0 FW vs. 0.82-3.0 FW
6 6
Common hammerhead, Sphyrna zygaena; Ionian Sea; July 2001; males Muscle Liver
3.2 (2.9-3.6) FW 8.1 (6.5-9.4) FW
7 7
Bamboo shark, Chiloscyllium plagiosum; Hong Kong; 2003-2004 Muscle Spleen Liver
<0.001 FW 0.01 (<0.001-0.067) FW 0.25 (0.09-0.77) FW
4 4 4
Smooth dogfish, Mustelus canis; New York Bight Liver Muscle
Max. 0.3 FW <0.1 FW
3 3
Sharks; Hong Kong and environs Muscle; 31 spp. Spleen; 9 spp. Liver; 20 spp.
<0.001 FW 0.01 FW <0.25 FW
4 4 4
0.0063 FW 0.0045 FW 0.0015 FW 0.0004 FW
5 5 5 5
0.0026 FW 0.0018 FW 0.0006 FW 0.0003 FW
5 5 5 5
Silver
Tin France; January-April 2005; edible portions; sold commercially; organotins Catshark, unidentified Total organotins Butyltins Phenyltins Octyltins Ray, unidentified Total organotins Butyltins Phenyltins Octyltins
Values are in mg Ni/kg fresh weight (FW) or dry weight (DW). a 1, Jenkins, 1980; 2, Vas, 1991; 3, Greig and Wenzloff, 1977a,b; 4, Cornish et al., 2007; 5, Guerin et al., 2007; 6, Storelli and Marcotrigiano, 2002; 7, Storelli et al., 2003.
30 Chapter 2
2.14 Plutonium Pentreath (1978) reported that thornback rays, R. clavata, absorbed 237Pu across the gut wall with subsequent accumulation in liver. Unlike teleosts, rays can take up significant amounts of 237Pu when administered through the medium, through the diet, or by injection; moreover, elimination rates were comparatively slow. There is no ready explanation to account for differences between rays and bony fishes, although a similar phenomenon has been observed by the same author (Pentreath, 1977b) for absorption of silver-110 m.
2.15 Ruthenium Ruthenium-106 comprises more than half the radioactive effluent discharged into the Irish Sea by the Windscale Works of the United Kingdom Atomic Energy Authority (Mauchline and Taylor, 1964). Thornback rays, R. clavata, collected from the vicinity of this outfall contained measurable accumulations of 196Ru, with most located in liver, stomach, and especially stomach contents. Mauchline and Taylor (1964) indicated that 106Ru—and also 144Ce and 95Zr/95Nb—were relatively insoluble in seawater, tend to form complexes in the water, and coprecipitate or adsorb onto free organic and inorganic substances.
2.16 Selenium Selenium in muscle from two species of sharks ranged from 0.2 to 0.8 mg Se/kg FW in tope, Galeorhinus australis, and from 0.2 to 0.5 mg Se/kg FW in gummy shark, M. antarcticus (Glover, 1979). Liver of blue shark, P. glauca, contained up to 3.0 mg Se/kg FW (Table 2.7). Maximum concentrations of selenium in muscle (3.6 mg Se/kg FW) and liver (9.4 mg/kg FW) were measured in male hammerheads, S. zygaena, captured in the Ionian Sea during July 2001 (Storelli et al., 2003; Table 2.7). The Se:Hg molar ratio in liver of blackmouth dogfish, Galeus melastomus, approaches 1.0 provided that total mercury concentration in liver exceeds 1.0 mg/kg FW (Storelli and Marcotrigiano, 2002).
2.17 Silver The highest silver concentration recorded in elasmobranch tissues is 0.77 mg Ag/kg FW in liver of the bamboo shark, Chiloscyllium plagiosum from Hong Kong in 2003-2004 (Table 2.7). Silver concentrations in muscle and liver of smooth dogfish, M. canis, collected from the New York Bight and environs were low: less than 0.1 mg Ag/kg FW in muscle and up to 0.3 mg Ag/kg FW in liver (Greig and Wenzloff, 1977a,b). Thornback rays, R. clavata, held in seawater solutions containing 0.04 mg Ag/L for 2 months accumulate silver in all tissues and at a higher rate than plaice, Pleuronectes platessa
Elasmobranchs 31 similarly exposed. Final tissue burdens in rays, in mg Ag/kg FW were 0.008 in blood, 0.015 in blood plasma, 0.24 in heart, 0.07 in spleen, 1.47 in liver, 0.05 in kidney, 0.56 in gut, 0.18 in gill filament, 0.05 in skin, 0.03 in muscle, and 0.025 in cartilage. Silver, when administered through the diet in the form of Nereis worms labeled with 110mAg was not retained to any great extent; only 4.2% of the original dose remained after 96 h (Pentreath, 1977b). Silver is comparatively toxic to adult spiny dogfish, S. acanthias; all died within 72 h during exposure to 0.2 mg Ag/L (De Boeck et al., 2001).
2.18 Strontium Strontium-90 accounts for about 5% of the radioactive effluent from the Windscale nuclear fuel reprocessing facility in the UK (Mauchline and Taylor, 1964). Thornback rays, R. clavata, from the Windscale vicinity had 90Sr concentrations in the order of liver > skin > cartilage > stomach contents. Data on the relative concentrations of radioactivity in skin, muscle, and cartilage suggest that the physical state of radionuclides introduced as effluent complexes, including 90Sr, may change after several hours or days in the natural environment, thus changing their potentiality as contaminants (Mauchline and Taylor, 1964).
2.19 Tin Muscle of spiny dogfish, S. acanthias, contained 2.0 mg total Sn/kg DW (Jenkins, 1980). Total organotins in edible tissues of sharks and rays sold commercially in France in 2005 contained 0.0026-0.0063 mg/kg FW; butyltins, especially tributyltin, accounted for the majority of the organotins (Table 2.7; Guerin et al., 2007).
2.20 Zinc Zinc concentrations in field collections of elasmobranchs (Table 2.8) seldom exceeded 10.0 mg Zn/kg on a FW basis or 50.0 mg Zn/kg on a DW basis, although concentrations in muscle could reach 38.5 mg Zn/kg FW and in liver 97.5 mg/kg FW (Marcovecchio et al., 1991). Zinc concentrations in shark tissues tend to decrease with increasing body weight (Cornish et al., 2007). In general, elasmobranch zinc burdens were consistently lower than those recorded for marine invertebrates and plants, and roughly similar in value of zinc levels recorded for the highest marine trophic groups, such as teleosts and mammals (Eisler, 1980). The apparent discrimination against zinc by marine vertebrates, including elasmobranchs, when compared to more primitive forms, has not yet been satisfactorily resolved.
32 Chapter 2 Table 2.8: Zinc Concentrations in Field Collections of Elasmobranchs Organism Silky shark, Carcharhinus falciformes Muscle Liver Kidney Brain Gonad Gill Spleen Muscle Oceanic whitetip shark, Carcharhinus longimanus Muscle Stomach Skin Liver Vertebrae
Concentration
Reference
10.0 DW 19.0 DW 25.0 DW 10.0 DW 10.0 DW 24.0 DW 28.0 DW 4.3-61.0 FW; 16.0-170.0 DW; 300.0-580.0 AW
2 2 2 2 2 2 2 3
3.4 FW; 16.0 DW; 90.0 AW 11.0 FW; 80.0 DW; 1200.0 AW 32.0 FW; 81.0 DW; 380.0 AW 2.7 FW; 4.9 DW; 500.0 AW 11.0 FW; 35.0 DW; 120.0 AW
3 3 3 3 3
Sandbar shark, Carcharhinus milberti Liver Vertebrae; from sharks of different total length 64 cm 130 cm 209 cm
9.0 DW
2
130.0 AW 80.0 AW 50.0 AW
4 4 4
Dusky shark, Carcharhinus obscurus Muscle Liver Brain Pup, whole
19.0 DW 16.0 DW 27.0 DW 12.0-14.0 DW
2 2 2 2
17.6-18.0 DW
5
Spottail shark, Carcharhinus sorrah; muscle Bamboo shark, Chiloscyllium plagiosum; Hong Kong; 2003-2004 Muscle Spleen Liver
7.4 (3.9-20.8) FW 9.9 (0.8-42.0) FW 8.7 (0.6-44.8) FW
Elasmobranchs; 7 species; muscle
4.6-5.0 FW; Max. 9.6 FW
a
12 12 12 9 (Continues)
Elasmobranchs 33 Table 2.8:
Cont’d a
Organism
Concentration
Reference
Tope, Galeorhinus australis; muscle
3.3-4.2 FW
Shortfin mako, Isurus oxyrinchus; vertebrae
36.0 (5.0-127.0) DW
Gummy shark, Mustelus antarcticus; muscle
3.2-4.8 FW
6
Smooth dogfish, Mustelus canis Muscle Liver
3.7-4.7 FW 3.2-3.6 FW
1 1
Blue shark, Prionace glauca Muscle Vertebrae
3.6-3.9 FW 95.0 (32.0-210.0) DW
Thornback ray, Raja clavata Whole Blood Heart Spleen Liver Kidney Gonad Gut Gill filament Skin Muscle Cartilage Rectal gland Brain and nerve cord
9.6 FW 4.7 FW 9.4 FW 15.9 FW 17.1 FW 11.3 FW 10.9 FW 14.8 FW 11.1 FW 12.3 FW 4.8 FW 19.3 FW 8.5 FW 10.1 FW
7 7 7 7 7 7 7 7 7 7 7 7 7 7
Clearnose skate, Raja eglanteria Muscle Liver Yolk-sac
20.0 DW 44.0 DW 31.0 DW
2 2 2
Longnose skate, Raja rhina; whole
7.1 FW
8
Atlantic guitarfish, Rhinobatis lentiginous Muscle Liver Stomach Yolk-sac
11.0 DW 29.0 DW 38.0 DW 19.0 DW
2 2 2 2
6 10
1 10
(Continues)
34 Chapter 2 Table 2.8: Organism
Concentration
Cownose ray, Rhinoptera bonasus Muscle Liver Brain Stomach Spiral valve Spleen Uterus
8.0 DW 9.0 DW 36.0 DW 34.0 DW 29.0 DW 32.0 DW 30.0 DW
Lesser spotted dogfish, Scyliorhinus canicula; liver
Cont’d Reference
a
2 2 2 2 2 2 2
8.7 FW
11
Sharks; Hong Kong and environs Liver; 20 spp. Spleen; 9 spp. Muscle
<0.05-26.7 FW 1.1-9.9 FW <0.05-16.9 FW
12 12 12
Sharks; 3 species; Bahia Blanca estuary, Argentina; 1985-1986 Muscle Liver
16.0-26.4 (0.5-38.5) FW 33.0-84.1 (13.0-97.5) FW
13 13
Scalloped hammerhead, Sphyrna lewini Muscle Liver Stomach
15.0 DW 16.0 DW 40.0 DW
2 2 2
Bonnethead, Sphyrna tiburo Muscle Liver Stomach Spleen Ovary
8.0 DW 13.0 DW 28.0 DW 25.0 DW 36.0 DW
2 2 2 2 2
Common hammerhead, Sphyrna zygaena; Ionian Sea; July 2001; males Muscle Liver
7.0 (6.8-7.1) FW 26.7 (25.0-28.7) FW
Spiny dogfish, Squalus acanthias Muscle Liver Stomach Spleen
3.0 FW; 12.0 DW 15.0 DW 70.0 DW 30.0 DW
14 14 2 2 2 2 (Continues)
Elasmobranchs 35 Table 2.8: Organism Yolk-sac Embryo Monkfish, Squatina squatina; liver
Concentration 16.0 DW 37.0 DW 8.0 FW
Cont’d a
Reference 2 2 11
Values are in mg Zn/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Greig and Wenzloff, 1977a,b; 2, Windom et al., 1973; 3, Lowman et al., 1966; 4, Eisler, 1967; 5, Zingde et al., 1976; 6, Glover, 1979; 7, Pentreath, 1973; 8, Vanderploeg, 1979; 9, Eustace, 1974; 10, Vas et al., 1990; 11, Morris et al., 1989; 12, Cornish et al., 2007; 13, Marcovecchio et al., 1991; 14, Storelli et al., 2003.
Dogfish, Scyliorhinus sp. exposed to 15.0 mg Zn/L for 25 days had no significant accumulations in kidney and muscle, but had elevated levels (as judged by bioconcentration factors = mg Zn per kg FW tissue/mg Zn per L of medium) in gill filament (1.6), spleen (1.7), pancreas (2.7), and liver (5.2) (Crespo et al., 1979; Flos et al., 1979). Encased embryos of the spotted dogfish, S. canicula, were exposed for 15 days to 65Zn then transferred to unlabeled seawater for 21 days (Jeffree et al., 2006). After uptake, 99.43% was taken up by the case and 0.42% by the embryo. After depuration, total radioactivity declined 28%, but case contributed 99.7% of total and the embryo 0.23% (Jeffree et al., 2006).
2.21 Literature Cited Al-Reasi, H.A., Ababneh, F.A., Lean, D.R., 2007. Evaluating mercury biomagnification from a tropical marine environment using stable isotopes (d 13C and d 15N). Environ. Toxicol. Chem. 26, 1572–1581. Baeyens, W., Leermakers, M., Papina, T., Saprykin, A., Brion, N., Noyen, J., et al., 2003. Bioconcentration and biomagnification of mercury and methylmercury in North Sea and Scheldt estuary fish. Arch. Environ. Contam. Toxicol. 45, 498–508. Bernhard, M., Zattera, A., 1975. Major pollutants in the marine environment. In: Pearson, E.A., Frangipane, E.D. (Eds.), Marine Pollution and Marine Waste Disposal. Pergamon, Elmsford, NY, pp. 195–300. Bloom, H., Ayling, G.M., 1977. Heavy metals in the Derwent Estuary. Environ. Geol. 2, 3–22. Branco, V., Vale, C., Canario, J., dos Santos, M.N., 2007. Mercury and selenium in blue shark (Prionace glauca, L. 1758) and swordfish (Xiphias gladius, L. 1758) from two areas of the Atlantic Ocean. Environ. Pollut. 150, 373–380. Cai, Y., Rooker, J.R., Gill, G.A., Turner, J.P., 2007. Bioaccumulation of mercury in pelagic fishes from the northern Gulf of Mexico. Canad. J. Fish. Aquat. Sci. 64, 458–469. Childs, E.A., Gaffke, J.N., 1973. Mercury content in Oregon ground fish. U.S. Dept. Comm. Fish Bull. 71, 713–717. Childs, E.A., Gaffke, J.N., Crawford, D.L., 1973. Exposure of dogfish shark feti to mercury. Bull. Environ. Contam. Toxicol. 9, 276–280. Cornish, A.S., Ng, W.C., Ho, C.C.M., Wong, H.L., Lam, J.C.W., Lam, P.K.S., et al., 2007. Trace metals and organochlorines in the bamboo shark Chiloscyllium plagiosum from the southern waters of Hong Kong, China. Sci. Total Environ. 376, 335–345. Crespo, S., Flos, R., Balasch, J., Alonso, G., 1979. Zinc in the gills of dogfish (Scyliorhinus canicula L.) related to experimental aquatic zinc pollution. Comp. Biochem. Physiol. 63C, 261–266.
36 Chapter 2 Cumont, G., Gilles, G., Bernard, F., Briand, M.B., Stephan, G., Ramonda, G., et al., 1975. Bilan de la contamination des poissons de mer par le mercure a l’occasion d’un controle portant sur 3 annees. Ann. Hyg. L. Fr. Med. Nut. 11(1), 17–25. De Boeck, G., Grosell, M., Wood, C.M., 2001. Sensitivity of spiny dogfish (Squalus acanthias) to waterborne silver exposure. Aquat. Toxicol. 54, 261–275. De Boeck, G., Hattink, J., Franklin, N.M., Bucking, C.P., Wood, S., Walsh, P.J., et al., 2007. Copper toxicity in the spiny dogfish (Squalus acanthias): urea loss contributes to the osmoregulatory disturbance. Aquat. Toxicol. 84, 133–141. De Gieter, M., Leermakers, M., Van Ryssen, M., Noyen, J., Goeyens, I., Baeyens, W., 2002. Total and toxic arsenic levels in North Sea fish. Arch. Environ. Contam. Toxicol. 43, 406–417. De Marco, S.G., Botte, S.E., Marcovecchio, J.E., 2006. Mercury distribution in abiotic and biological compartments within several estuarine systems from Argentina: 1980–2005 period. Chemosphere 65, 213–223. de Pinho, A.P., Guimaraes, J.R.D., Martins, A.S., Costa, P.A.S., Olavo, G., Valentin, J., 2002. Total mercury in muscle tissue of five shark species from Brazilian offshore waters: effects of feeding habit, sex, and length. Environ. Res. 89A, 250–258. Eisler, R., 1967. Variations in mineral content of sandbar shark vertebrae (Carcharhinus milberti). Nat. Canad. 94, 321–326. Eisler, R., 1979. Copper accumulations in coastal and marine biota. In: Nriagu, J.O. (Ed.), Copper in the Environment. Part 1: Ecological Cycling. Wiley, New York, pp. 383–449. Eisler, R., 1980. Accumulation of zinc by marine biota. In: Nriagu, J.O. (Ed.), Zinc in the Environment. Part 2: Health Effects. Wiley, New York, pp. 259–351. Eisler, R., 2000. Arsenic. In: Handbook of Chemical Risk Assessment, Vol. 3. Lewis Publishers, Boca Raton, FL, pp. 1501–1566. Eustace, I.J., 1974. Zinc, cadmium, copper and manganese in species of finfish and shellfish caught in the Derwent Estuary, Tasmania. Austral. J. Mar. Freshw. Res. 25, 209–220. Evans, D.H., Walton, J.S., 1990. Muscarinic receptors are not involved in the nickel-induced constriction of vascular smooth muscle of the dogfish shark (Squalus acanthias) ventral aorta. Bull. Mount Desert Island Biol. Lab. 29, 122–123. Flos, R., Caritat, A., Balasch, J., 1979. Zinc content in organs of dogfish (Scyliorhinus canicula L.) Subject to sublethal aquatic zinc pollution. Comp. Biochem. Physiol. 64C, 77–81. Forrester, C.R., Ketchen, K.S., Wong, C.C., 1972. Mercury content of spiny dogfish (Squalus acanthias) in the Strait of Georgia, British Columbia. J. Fish. Res. Bd. Canada 29, 1487–1490. Gardner, W.S., Windom, H.L., Stephens, J.A., Taylor, F.E., Stickney, R.R., 1975. Concentrations of total mercury in fish and other coastal organisms: implications to mercury cycling. In: Howell, F.G., Gentry, J.B., Smith, M.H. (Eds.), Mineral Cycling in Southeastern Ecosystems. U.S. Energy Res. Dev. Admin. Available as CONF-740513 from NTIS. U.S. Department of Commerce, Springfield, VA, pp. 268–278. Glover, J.W., 1979. Concentrations of arsenic, selenium and ten heavy metals in school shark, Galeorhinus australis (Macleay), and gummy shark, Mustelus antarcticus Gunther, from south-eastern Australian waters. Austral. J. Mar. Freshw. Res. 30, 505–510. Goessler, W., Kuehnelt, D., Schlagenhaufen, C., Slejklovec, Z., Irgolic, K.J., 1998. Arsenobetaine and other arsenic compounds in the National Research Council of Canada certified reference materials DORM 1 and DORM 2. J. Anal. Atom. Spectrom. 13, 183–187. Greig, R.A., Wenzloff, D.R., 1977b. Final report on heavy metals in small pelagic finfish, euphausiid crustaceans and apex predators, including sharks, as well as on heavy metals and hydrocarbons (C15+) in sediments collected at stations in and near deepwater dumpsite 106. In: Contaminant Inputs and Chemical Characteristics. Baseline Report of the Environmental Conditions on Deepwater Dumpsite 106, Vol. III. U.S. Department of Commerce, NOAA, Rockville, MD, pp. 547–564. Greig, R.A., Wenzloff, D.R., 1977a. Trace metals in finfish from the New York Bight and Long Island Sound. Mar. Pollut. Bull. 8, 198–200.
Elasmobranchs 37 Greig, R.A., Wenzloff, D., Shelpuk, C., Adams, A., 1977. Mercury concentrations in three species of fish from North Atlantic offshore waters. Arch. Environ. Contam. Toxicol. 5, 315–323. Guerin, T., Sirot, V., Volatier, J.L., Leblanc, J.C., 2007. Organotin levels in seafood and its implications for health risk in high-seafood consumers. Sci. Total Environ. 388, 66–77. Hall, A.S., Teeny, F.M., Gauglitz Jr., E.J., 1977. Mercury in fish and shellfish of the northeast Pacific. III. Spiny dogfish, Squalus acanthias. U.S. Dept. Comm. Fish Bull. 75, 642–645. Hanaoka, K., Tagawa, S., 1985. Isolation and identification of arsenobetaine as a major water soluble arsenic compound from muscle of blue pointer Isurus oxyrhincus and whitetip shark Carcharhinus longimanus. Bull. Jpn. Soc. Sci. Fish. 51, 681–685. Hanaoka, K., Kogure, T., Miura, Y., Tagawa, S., Kaise, T., 1993. Post-mortem formation of inorganic arsenic from arsenobetaine in a shark under natural conditions. Chemosphere 27, 2163–2167. Hornung, H., Krom, M.D., Cohen, Y., Bernhard, N., 1993. Trace metal content in deep water sharks from eastern Mediterranean Sea. Mar. Biol. 115, 331–338. Jefferies, D.F., Hewett, C.J., 1971. The accumulation and excretion of radioactive caesium by the plaice (Pleuronectes platessa) and the thornback ray (Raja clavata). J. Mar. Biol. Assoc. UK 51, 411–422. Jeffree, R.A., Warnau, M., Oberhansli, F., Teyssie, J.L., 2006. Bioaccumulation of heavy metals and radionuclides from seawater by encased embryos of the spotted dogfish, Scyliorhinus canicula. Mar. Pollut. Bull. 52, 1278–1286. Jeffre-e, R.A., Oberhansli, F., Teyssie, J.L., 2007. Accumulation and transport behaviour of 241americium, 60 cobalt and 134cesium by eggs of the spotted dogfish, Scyliorhinus canicula. Mar. Pollut. Bull. 54, 912–920. Jenkins, D.W., 1980. Biological Monitoring of Toxic Trace Metals. Volume 2. Toxic Trace Metals in Plants and Animals of the World, Part III. U.S. Environmental Protection Agency Report, 600/3–80–092, pp. 1–290. Joiris, C.R., Ali, I.B., Holsbeek, L., Kanuya-Kinoti, M., Tekele-Michael, Y., 1997. Total and organic mercury in Greenland and Barents Seas demersal fish. Bull. Environ. Contam. Toxicol. 58, 101–107. Kureishy, T.W., George, M.D., Sengapta, R., 1979. Total mercury content in some marine fish from the Indian Ocean. Mar. Pollut. Bull. 10, 357–360. Leah, R., Evans, S., Johnson, M., 1991. Mercury in muscle tissue of lesser-spotted dogfish (Scyliorhinus caniculus L.) From the north-east Irish Sea. Sci. Total Environ. 108, 215–224. LeBlanc, P.J., Jackson, A.L., 1973. Arsenic in marine fish and invertebrates. Mar. Pollut. Bull. 4, 88–90. Lowman, F.G., Phelps, D.K., Ting, R.Y., Escalera, R.M., 1966. Progress Summary Report No. 4, Marine Biology Program June 1965-June 1066. Puerto Rico Nuclear Center Report, PRNC 85, pp. 1–57. Lyle, J.M., 1984. Mercury concentrations in four carcharhinid and three hammerhead sharks from coastal waters of the Northern Territory. Austral. J. Mar. Freshw. Res. 35, 441–451. Marcovecchio, J.E., Moreno, V.J., Perez, A., 1991. Metal accumulation in tissues of sharks from the Bahia Blanca estuary, Argentina. Mar. Environ. Res. 31, 263–274. Mauchline, J., Taylor, A.M., 1964. The accumulation of radionuclides by the thornback ray, Raja clavata L., in the Irish Sea. Limnol. Oceanogr. 9, 303–309. Menasveta, P., Siriyong, R., 1977. Mercury content of several predacious fish in the Andaman Sea. Mar. Pollut. Bull. 8, 200–204. Morris, R.J., Law, R.J., Allchin, C.R., Kelly, C.A., Fileman, C.F., 1989. Metals and organochlorines in dolphins and porpoises of Cardigan Bay, West Wales. Mar. Pollut. Bull. 20, 512–523. Pentreath, R.J., 1973. The accumulation from seawater of 65Zn, 54Mn, 58Co and 59Fe by the thornback ray, Raja clavata L. J. Exp. Mar. Biol. Ecol. 12, 327–334. Pentreath, R.J., 1976. The accumulation of mercury by the thornback ray, Raja clavata L. J. Exp. Mar. Biol. Ecol. 25, 131–140. Pentreath, R.J., 1977a. The accumulation of cadmium by the plaice, Pleuronectes platessa L., and the thornback ray, Raja clavata L. J. Exp. Mar. Biol. Ecol. 30, 223–232. Pentreath, R.J., 1977b. The accumulation of 110mag by the plaice, Pleuronectes platessa L. and the thornback ray, Raja clavata L. J. Exp. Mar. Biol. Ecol. 29, 315–325. Pentreath, R.J., 1978. 237Pu experiments with the thornback ray, Raja clavata. Mar. Biol. 48, 337–342.
38 Chapter 2 Ratkowsky, D.A., Dix, T.G., Wilson, K.C., 1975. Mercury in fish in the Derwent estuary, Tasmania and its relation to the position of the fish in the food chain. Aust. J. Mar. Freshw. Res. 26, 223–231. Rouleau, C., Gobeil, C., Tjalve, H., 2006. Cadmium accumulation in coastal demersal fish. Mar. Ecol. Prog. Ser. 311, 13143. Storelli, M.M., Marcotrigiano, G.O., 2002. Mercury speciation and relationship between mercury and selenium in liver of Galeus melastomus from the Mediterranean Sea. Bull. Environ. Contam. Toxicol. 69, 516–522. Storelli, M.M., Marcotrigiano, G.O., 2004. Interspecific variation in total arsenic body concentrations in elasmobranch fish from the Mediterranean Sea. Mar. Pollut. Bull. 48, 1145–1167. Storelli, M.M., Giacominelli-Stuffler, R., Marcotrigiano, G., 2002. Mercury accumulation and speciation in muscle tissue of different species of sharks from Mediterranean Sea, Italy. Bull. Environ. Contam. Toxicol. 68, 201–210. Storelli, M.M., Ceci, E., Storelli, A., Marcotrigiano, G.O., 2003. Polychlorinated biphenyl, heavy metal, and methylmercury residues in hammerhead sharks: contaminant status and assessment. Mar. Pollut. Bull. 46, 1035–1048. Vanderploeg, H.A., 1979. Dynamics of zinc-65 specific activity and total zinc in benthic fishes on the outer continental shelf off central Oregon. Mar. Biol. 52, 259–272. Vas, P., 1991. Trace metal levels in sharks from British and Atlantic waters. Mar. Pollut. Bull. 22, 67–72. Vas, P., Stevens, J.D., Bonwick, G.A., Tizini, O.A., 1990. Cd, Mn, and Zn concentrations in vertebrae of blue shark and shortfin mako in Australian coastal waters. Mar. Pollut. Bull. 21, 203–206. Windom, H., Stickney, R., Smith, R., White, D., Taylor, F., 1973. Arsenic, cadmium, copper, mercury, and zinc in some species of North Atlantic finfish. J. Fish. Res. Bd. Canada 30, 275–279. World Health Organization (WHO), 1991. Nickel. Environ. Health Crit. 108, 1–383. Zingde, M.D., Singbal, S.Y.S., Moraes, C.F., Reddy, C.V.G., 1976. Arsenic, copper, zinc & manganese in the marine flora & fauna of coastal & estuarine waters around Goa. Indian J. Mar. Sci. 5, 212–217.
CHAPTER 3
Fishes This group consists of cold-blooded aquatic vertebrates, typically with gills, fins, and scales. Fishes are the most numerous of the vertebrates, with current estimates ranging between 15,000 and 17,000 living species, although some estimates range up to 40,000 living species. By contrast, bird species number about 8600, mammals 4500, reptiles 6000, and amphibians (all nonmarine) 2500. Thus, fishes now account for about 42% of all living species of terrestrial and aquatic vertebrates. In the marine environment, fishes constitute the vast majority of all species of vertebrates recorded. The enormous variation in size, shape, and specialized structures among fishes enable individual species to survive in almost every marine ecological niche known, regardless of temperature, salinity, or depth. Although the economically important marine groups are few in number—including the tunas, cods, herrings, salmonids, flounders, and their relatives—it is probable that more than 1000 additional species are regularly taken by sport and commercial fishermen for human consumption. Fishes have been studied extensively for trace metal concentrations, although much remains to be discovered.
3.1 Aluminum Muscle from striped mullet, Mugil cephalus, collected on August 2005 in Iskenderun Bay, Turkey, contained 1.3 mg Al/kg DW (range 0.04-3.5) (Turkmen et al., 2006). The significance of this observation is unknown because field data are scarce for aluminum and marine teleosts. In the rudd, Scardinus erythrophthalmus, the major site of aluminum accumulation is kidney, followed by decreasing concentrations in scales, gills, spleen, liver, swimbladder, and muscle, in that order (Vorob’yev and Zaystev, 1975). Otoliths of blackfin tuna, Thunnus atlanticus, from the Gulf of Mexico in 2002, contained 0.32 mg Al/kg DW (Arslan and Secor, 2008). Increased concentrations of gill-reactive aluminum occur in estuarine waters after flooding events (Tien et al., 2006). In laboratory tests, aluminum associated with organic colloids was mobilized by low molecular mass cationic aluminum species upon contact with seawater and deposited almost immediately on gills of Atlantic salmon, Salmo salar. Aluminum concentration in gills was up to 10 times higher than input river water, but decreased within 39
40 Chapter 3 30 min as high runoff subsided. However, aluminum accumulation in estuarine fish gills is predicted to be significantly higher during severe flooding events, with adverse effects on survival anticipated (Tien et al., 2006). In acute toxicity bioassays, concentrations of 400.0 mg þ Al3 /L killed all larval and juvenile striped bass, Morone saxatilis, in 7 days at pH 7.2; however, no deaths were observed at 150.0-200.0 mg/L (Buckler et al., 1987; Hall et al., 1985).
3.2 Americium Isotopes of americium—and other transuranics, including curium, berkelium, and californium—are taken up from seawater by teleosts by a factor of less than 50; concentration factors for macroalgae are higher by several orders of magnitude (Morse and Choppin, 1991).
3.3 Antimony Mean antimony concentrations in most finfish liver and muscle tissues collected from coastal waters of the United States, Alaska, and Hawaii fell within the range 0.5-0.9 mg Sb/kg fresh weight (Table 3.1); most species of whole finfishes analyzed contained between 1.0 and 2.0 mg Sb/kg fresh weight (Hall et al., 1978). However, antimony burdens were substantially lower in muscle and whole fish from specimens collected outside U.S. territorial waters (Table 3.1), suggesting reexamination of the U.S. data.
3.4 Arsenic Arsenic concentrations in whole finfish, liver, and muscle varied widely, with most samples falling between 2.0 and 5.0 mg As/kg fresh weight, although some values >30.0 mg As/kg FW were recorded (Table 3.2). Fish with elevated arsenic concentrations in tissues came from sites where arsenic concentrations in invertebrates were high, suggesting that dietary input is important for arsenic uptake; however, elevated arsenic concentrations in seawater also affect intake (Meador et al., 2004). Arsenic burdens were usually higher in liver than in muscle, and highest in lipids. The elevated concentrations of arsenic recorded in some tissues, including muscle, were sometimes attributable to mining or waste disposal activities (Bohn and Fallis, 1978; Bohn and McElroy, 1976; Denton et al., 2006; Greig et al., 1977; Grimanis et al., 1978). Most investigators agree that inorganic trivalent (arsenite) forms of arsenic are the most hazardous to human health, and organic pentavalent (arsenate) the least. It is probable that most of the arsenic in edible fish tissues is in the least hazardous form of arsenobetaine (Eisler, 2000a); however, some evidence exists showing rapid postmortem reduction of arsenate to arsenite in fish tissues (Reinke et al., 1975), indicating a need for additional research in this subject area. Most investigators agree that arsenic concentrations in terrestrial organisms are comparatively low, seldom exceeding 1.0 mg As/kg dry weight tissue, and that corresponding
Fishes 41 Table 3.1: Antimony Concentrations in Field Collections of Fishes Organism
Concentration
Reference
European eel, Anguilla anguilla; muscle
0.015 DW
1
<0.1 FW 0.1-0.2 FW 0.3-0.4 FW 0.4-0.5 FW 0.5-0.6 FW 0.6-0.7 FW 0.7-0.8 FW 0.8-0.9 FW 0.9-1.0 FW 1.0-2.0 FW
2-4 2 2 2 2 2 2 2 2 2
<0.1-0.3 FW 0.3-0.5 FW 0.5-0.7 FW 0.7-0.9 FW 0.9-2.0 FW
2 2 2 2 2
Fish Muscle 17 spp. 1 sp. 2 spp. 2 spp. 18 spp. 51 sp. 33 spp. 28 spp. 9 spp. 10 spp. Liver 6 spp. 13 spp. 29 spp. 17 spp. 17 spp. Whole fish 10 spp. 14 spp. Fishmeal Press cake N liquor Meal
<0.1-0.4 FW 1.0-2.0 FW
2, 5 2
0.061 DW <0.01 DW 0.20 DW
6 6 6
Gadoid, Gadus callarias; muscle
0.011 DW
1
Goby, Gobius niger Muscle Liver
<0.02 DW 0.03 DW
7 7
European bass, Morone labrax; muscle
0.010 DW
1
Striped bass, Morone saxatilis Muscle Liver
<0.01 DW <0.01 DW
8 8
Bronze bream, Pachymetopon grande; muscle
0.019 FW
3
European flounder, Platichthys flesus; muscle
0.006 DW
1
a
(Continues)
42 Chapter 3 Table 3.1:
Cont’d
Organism
Concentration
Reference
Sparid, Sargus annularis Muscle Liver
0.03-0.04 DW <0.02 DW
7 7
0.006 DW
1
0.003 DW 0.017 DW 0.007 DW 1.6 AW
9 9 9 10
No data vs. <0.01 FW
11
Atlantic mackerel, Scomber scombrus; muscle Mackerel, Scombresox sp. Muscle Heart Liver Whole Southern bluefin tuna, Thunnus maccoyii; Australia; April 2004; muscle; wild vs. farmed
a
Values are in mg Sb/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Leatherland and Burton, 1974; 2, Hall et al., 1978; 3, Van As et al., 1973; 4, Van As et al., 1975; 5, Strohal et al., 1975; 6, Lunde, 1968a; 7, Grimanis et al., 1978; 8, Heit, 1979; 9, Leatherland et al., 1973; 10, Robertson, 1967; 11, Padula et al., 2008.
concentrations for marine biota range from several mg/kg to more than 100.0 mg As/kg dry weight tissue (Lunde, 1977). Unlike terrestrial organisms, marine biota can convert inorganic arsenic compounds to organoarsenic compounds. In aquatic organisms, the arsenic is present as both lipid-soluble and water-soluble compounds. Water-soluble organoarsenic compounds are very stable to chemical and metabolic breakdown (Lunde, 1977). Arsenic concentrations in edible fish tissues are generally lower than those reported for edible portions of algae, crustaceans, and bivalve molluscs (Eisler, 1981; Lunde, 1977), but sometimes are sufficiently elevated to pose a risk to human consumers (Burger et al., 2007a). Arsenic tolerance was measured in mummichogs, Fundulus heteroclitus, preexposed to sublethal concentrations of sodium arsenite (8.0 mg As/L) for 96 h or naive to elevated arsenic, then subjected to 12.0-22.5 mg As/L (Shaw et al., 2007). Dose-dependent tolerance to arsenic was acquired in 96 h in preexposed mummichogs. These fish were more resistant to a lethal arsenite level when compared to naive mummichogs; also, onset of mortality was delayed. Increased tolerance was associated with lower concentrations of arsenic in all monitored tissues, possibly due to an increase in liver of the multidrug resistance associated gene protein (MRP)-2-gene, which is responsible for transporting arsenic conjugated to glutathione out of cells (Shaw et al., 2007). Arsenobetaine is the dominant arsenic species in fish tissues; however, uptake and retention differs between species and tissues, and this may account, in part, for the differences in
Fishes 43 Table 3.2: Arsenic Concentrations in Field Collections of Fishes Organism
Concentration
Surf bream, Acanthopagrus australis; muscle
1.1 (0.1-2.4) FW
Alaska, Adak Island; June 2004 Flathead sole, Hippoglossoides elassodon Kidney Liver Muscle Great sculpin, Myoxocephalus polyacanthocephalus Kidney Liver Muscle American Samoa; 2001-2002 Lined surgeonfish, Acanthurus lineatus; muscle Total arsenic Inorganic arsenic Brassy trevally, Caranx papuensis; total arsenic vs. inorganic arsenic Muscle Whole Torpedo scad, Megalopsis cordyla; total arsenic vs. inorganic arsenic Muscle Whole Squirrelfish, Sargocentrum spp.; total arsenic vs. inorganic arsenic Muscle Whole
Reference
a
1
32.4 FW 18.9 FW 19.5 FW
48 48 48
0.53 FW 2.4 FW 1.3 FW
48 48 48
0.33-0.56 FW Max. 0.02 FW
52 52
0.39-0.68 FW vs. <0.009 FW 0.28-0.93 FW vs. <0.009 FW
52 52
1.9-2.5 FW vs. <0.009 FW 1.1-1.5 FW vs. <0.009 FW
52 52
Usually 6.1-18.7 FW vs. 0.009-0.03 FW Usually 4.2-11.9 FW vs. 0.009-0.48 FW
52 52
Bay anchovy, Anchoa mitchelli; whole
0.52 FW; 2.1 DW
2
European eel, Anguilla anguilla; muscle
1.7 DW
3
Blue hake, Antimora rostrata; ocean dumpsite off New York; muscle
0.4 (0.3-0.5) FW
4
Australian salmon, Arripes trutta; muscle
0.4 (0.3-0.5) FW
1
Bodega Bay, California; 6 sites; 1992-1993; white croaker, Genyonemus lineatus and English sole, Pleuronectes vetulus Liver Muscle
5.7-40.5 DW 3.5-45.6 DW
50 50 (Continues)
44 Chapter 3 Table 3.2: Organism Gill Stomach
Cont’d
Concentration 1.4-3.3 DW 2.8-45.4 DW
Reference 50 50
Arctic cod, Boreogadus saida Muscle Liver
46.0 DW 4.4 DW
5 5
Black sea bass, Centropristes striata; muscle
1.6 FW; 6.4 DW
6
Squirefish, Chrysophrys auratus; muscle
2.2 (0.4-4.4) FW
1
0.5 (0.2-3.1) 2.0 (0.8-3.0) 3.0 (1.5-3.8) 1.1 (0.2-2.6) 0.2 FW 1.5 FW 3.1-14.3 FW 5.0-21.0 DW
2 2 2 2 2 2 7 8
Baltic herring, Clupea harengus Muscle Southern Baltic Sea England Norway SW Baltic Sea Sweden Caspian Sea Oil N-liquor Whole Inorganic Organic Atlantic cod, Gadus morhua Fillet Gutted fish less tongue Tongue Roe (juvenile) Roe (mature) Milt Head minus gills Gills Skin Vertebrae Intestines Intestines less stomach Stomach, empty Stomach contents Gall bladder Oil
3.2 DW 3.4 DW 3.2 FW 1.2-6.2 FW 2.6 FW 0.9 FW 0.8 FW 5.4 FW 2.6 FW 1.4 FW 0.4 FW 2.9 FW 1.1 FW 5.5 FW 1.4 FW 1.1 FW 3.9 FW 0.7-26.0 FW
a
FW FW FW FW
9 9 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 7 (Continues)
Fishes 45 Table 3.2: Organism Muscle Newfoundland Southern Baltic Sea Norway England, Sweden Liver; N-liquor
Cont’d
Concentration
0.8 FW 0.62 (0.26-1.05) FW 2.69 (0.95-11.0) FW 2.1 (0.4-3.3) FW 37.0 FW
Reference
11 2 2 2 12
Spotted seatrout, Cynoscion nebulosus; muscle
0.6 FW; 2.5 DW
Roundnose flounder, Eopsetta grigorjewi; muscle
20.1 FW
35
Graysby, Epinephelus cruentatus; muscle
1.8 FW
13
Nassau grouper, Epinephelus striatus; muscle
9.1 FW
13
Green chromidae, Etropus suratensis; muscle
8.6-11.2 DW
14
2.6 (0.3-8.4) FW
10
0.7-2.0 FW 2.0-4.0 FW 4.0-6.0 FW 6.0-10.0 FW 10.0-30.0 FW 30.0-50.0 FW 7.0-512.0 DW
15 15 15 15 15 15 16
0.6-2.0 FW 2.0-4.0 FW 4.0-6.0 FW 6.0-8.0 FW 8.0-10.0 FW 10.0-20.0 FW 20.0-30.0 FW <1.0-22.5 DW
15 15 15 15 15 15 15 6
1.4-10.0 FW <0.5 FW 0.3-0.4 DW 17.0-307.0 DW (2.8-10.9) FW
17 17 14 16 38
Fish Byproducts Liver 10 spp. 25 spp. 23 spp. 13 spp. 8 spp. 2 spp. 3 spp. Muscle 9 spp. 82 spp. 25 spp. 16 spp. 13 spp. 12 spp. 2 spp. 22 spp. 4 spp. Total Inorganic 6 spp. 3 spp. 4 spp.; Netherlands; 1977-1984
a
2
(Continues)
46 Chapter 3 Table 3.2: Organism North Sea; 1997-1998 10 spp. 11 spp. 3 spp. 6 spp. 8 spp.; Taiwan; 1995-1996 10 spp.; October 2004; Pearl River Delta, China Oil; 10 spp. Whole 14 spp. 2 spp. 1 sp.
Cont’d
Concentration
0.0-5.0 FW 6.0-20.0 FW 21.0-76.1 FW (0.18-0.30) DW Max. 5.3 DW 0.65-8.1 FW
Reference
a
31 31 31 39 40 53
0.5-15.5 FW
7
1.0-5.0 FW 5.0-8.0 FW 20.0-30.0 FW
15 15 15
Finfish; near metal smelter; water concentrations 2.3-2.9 mg As/L; total arsenic vs. inorganic arsenic Muscle; 6 spp. Liver; 4 spp.
(0.2-2.6) FW vs. (0.02-0.1) FW (0.4-1.8) FW vs. (0.02-0.07) FW
36 36
Finfish; reference site; water concentration <2.0 mg As/L; total arsenic vs. inorganic arsenic Muscle; 5 spp. Liver; 4 spp.
(0.1-1.2) FW vs. (0.02-0.15) FW (0.2-1.5) FW vs. (0.02-0.05) FW
36 36
Fishmeal Presscake N-liquor Meal
4.5 DW 15.2 DW 19.1 DW
18, 34 18, 34 18, 34
Goby, Gobius niger; Aegean Sea Muscle; polluted area vs. reference site Liver; polluted area
142.0 DW vs. 18.0 DW 8.4-17.0 DW
19 19
Guam; 1998-1999; 4 stations; max. Concentrations Muscle Liver
77.6 DW 13.0 DW
45 45
Greenling, Hexagrammos sp,; muscle
0.8 FW
20
Flathead sole, Hippoglossoides elassodon; Gulf of Alaska; 4 sites; 1992-1993 Liver Muscle Stomach
26.8-290.0 DW 20.7-52.3 DW 8.7-40.4 DW
50 50 50 (Continues)
Fishes 47 Table 3.2:
Cont’d
Organism
Concentration
American plaice, Hippoglossoides platessoides; muscle
4.4 FW
11
<3.0-10.0 DW 5.4-312.0 FW
21 21
1.6-5.4 FW 1.8-9.8 FW
21 21
Spotted ratfish, Hydrolagus colliei; muscle
10.3 FW
20
Irish Sea; sludge deposit site vs. reference site; muscle; total arsenic (<1% inorganic) Whiting, Merlangius merlangius Plaice, Pleuronectes platessa
6.2 FW vs. <4.0 FW 20.5 FW vs. <7.5 FW
41 41
Pinfish, Lagodon rhomboides; whole; Lower Laguna Madre, Texas; 1986-1987
9.4 (1.7-20.0) DW
37
Capelin, Mallotus villosus; N-liquor
3.0-8.0 DW
Atlantic halibut, Hippoglossus hippoglossus; fishmeal Whole Aqueous phase Lipid phase Hexane extract Hexane/isopropanol extract
Reference
8
Mediterranean Sea; summer 2003 Swordfish, Xiphias gladius Muscle Liver Bluefin tuna, Thunnus thynnus Muscle Liver
3.7 (1.7-7.4) FW 6.2 (2.6-14.8) FW
49 49
2.6 (1.6-5.0) FW 7.1 (2.1-11.2) FW
49 49
European bass, Morone labrax; muscle
7.1 DW
Striped bass, Morone saxatilis Muscle Muscle Liver
0.45 FW; 1.8 DW 0.25 FW 0.7 FW
2 22 22
0.8 (0.1-3.8) FW Max. 1.3 FW
1 42
2.38 DW vs. 4.18 DW 9.4 DW vs. 5.4 DW 6.5 DW vs. 11.8 DW no data vs. 12.9 DW
47 47 47 47
Striped mullet, Mugil cephalus Muscle Viscera Taiwan; 2002; wild fish vs. cultured mullet; total arsenic Muscle Stomach Ovary Testes
a
3
(Continues)
48 Chapter 3 Table 3.2:
Cont’d
Organism
Concentration
Mullet, Mugil parsia; muscle
8.3-12.6 DW
14
Scamp, Mycteroperca phenax; muscle
1.36 FW
13
Tiger grouper, Mycteroperca tigris; muscle
1.66 FW
13
Shorthorn sculpin, Myoxocephalus scorpius Muscle Liver
40.0 DW 81.0 DW
23 23
Norway; Glomma estuary; MarchDecember 1988; muscle Atlantic cod, Gadus morhua European flounder, Platichthys flesus
4.1 FW 5.2 FW
43 43
Pandora, Pagellus erythrinus; Aegean Sea Polluted environment vs. reference site Bone Liver Skin Muscle Fins Eyes Eggs Gills Brain Liver Intestine Spleen Muscle Skin Bone Whole
10.0 DW 67.0 DW 16.0 DW 39.0 DW 6.6 DW 14.0 DW 18.0 DW 7.6 DW 8.3 DW 30.0 DW 27.0 DW 16.0 DW 15.0 DW 8.1 DW 3.2 DW 14.0 DW
Papua New Guinea; 5 spp.; 1999-2002; tropical deepwater fishes Muscle Liver
8.1 FW 13.1 FW
46 46
English sole, Parophrys vetulus; muscle
11.5 FW
20
European flounder, Platichthys flesus; muscle
8.7 DW
3
Gurnard, Platycephalus fuscus; muscle
0.2 (0.1-0.4) FW
1
Plaice, Pleuronectes platessa; muscle Sweden
0.5 FW
2
vs. vs. vs. vs.
4.1 DW 29.0 DW 8.1 DW 18.0 DW
Reference
a
24 24 24 24 25 25 25 25 25 25 25 25 25 25 25 25
(Continues)
Fishes 49 Table 3.2: Organism Japan Baltic Sea England; offshore vs. coastal Norway
Cont’d
Concentration 1.25 FW 1.23 (0.84-1.8) FW 3.75 (1.8-5.7) FW vs. 1.7 FW 5.6 FW
Reference
a
2 2 2 2
English sole, Pleuronectes vetulus; muscle
1.1 (0.6-11.5) FW
44
Mackerel, Pneumatophorus japonicus (Scomber colias); muscle
0.015 DW; 0.34 AW
26, 27
Pollock, Pollachius virens; whole; inorganic
0.7 DW
28, 29
Bluefish, Pomatomus saltatrix; muscle
0.4 (0.1-0.6) FW
Sand sole, Psettichthys melanostichus; muscle
11.5 FW
20
Greenland halibut, Rheinhardtius hippoglossoides; muscle
0.8 FW
11
Arctic char, Salvelinus alpinus Muscle Liver
0.5 DW 0.7 DW
23 23
Sardine; canned; Caspian Sea
0.9-1.2 FW
30
Fringe scale sardinella, Sardinella fimbriata; muscle
2.3-7.6 DW
14
Sparid, Sargus annularis Muscle Liver
2.5-9.1 DW 18.0-29.0 DW
19 19
Kob, Agrosomus hololepidotus; muscle
0.3 (0.1-0.4) FW
1
Atlantic mackerel, Scomber scombrus N-liquor Muscle
3.1 DW 2.2 DW
8 3
Spanish mackerel, Scomberomerus maculatus Muscle Liver
0.45 FW; 1.8 DW 2.7 DW
2 2
Mackerel, Scombresox saurus Muscle Heart Liver
5.4 DW 6.6 DW 8.4 DW
Windowpane, Scopthalmus aquosus; muscle
1.4-2.7 DW
1
31 31 31 4 (Continues)
50 Chapter 3 Table 3.2:
Cont’d
Organism
Concentration
Ocean perch, Sebastes marinus Muscle Muscle
0.8 FW 2.6 FW
11 20
Amberjack, Seriola grandis; muscle
0.3 FW
1
Yellowfin tuna, Thunnus albacares; muscle
0.5 (0.4-0.7) FW
1
Southern bluefin tuna, Thunnus maccoyii; Australia; April 2004; muscle; wild vs. farmed
0.57 (0.46-0.72) FW vs. 0.71 (0.16-1.8) FW
51
<3.0-7.0 DW 6.7-23.0 FW 1.2-2.5 FW vs. 5.6-19.0 FW
21, 32 21, 32 21, 32
Mediterranean scad, Trachurus mediterraneus Muscle Liver
3.9-9.2 DW 14.1 DW
33 33
Tunafish; canned; Persian Gulf
0.6-1.0 FW
30
Bluefin tuna, Thunnus thynnus; fishmeal Whole Aqueous phase Lipid phase; hexane extract vs. hexane/ isopropanol extract
Reference
a
Values are in mg As/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Bebbington et al., 1977; 2, Bernhard and Zattera, 1975; 3, Leatherland and Burton, 1974; 4, Greig et al., 1977; 5, Bohn and McElroy, 1976; 6, Windom et al., 1973; 7, Lunde, 1967; 8, Lunde, 1969; 9, Lunde, 1973a; 10, Julshamn et al., 1978a; 11, Kennedy, 1976; 12, Lunde, 1970; 13, Taylor and Bright, 1973; 14, Zingde et al., 1978; 15, Hall et al., 1978; 16, Bohn, 1975; 17, Reinke et al., 1975; 18. Lunde, 1968b; 19, Grimanis et al., 1978; 20, LeBlanc and Jackson, 1973; 21, Lunde, 1973d; 22, Heit, 1979; 23, Bohn and Fallis, 1978; 24, Papadopoulu et al., 1973; 25, Papadopoulu et al., 1972; 26, Fukai and Meinke, 1959; 27, Fukai and Meinke, 1962; 28, Lunde, 1973b; 29, Lunde, 1973c; 30, Karapetian and Shahmoradi, 1978; 31, De Gieter et al., 2002; 32, Leatherland et al., 1973; 33, Papadopoulu et al., 1978b; 34, Lunde, 1968b; 35, Hanaoka and Tagawa, 1985; 36, Norin et al., 1985; 37, Custer and Mitchell, 1993; 38, Vos and Hovens, 1986; 39, Ramelow et al., 1989; 40, Han et al., 1998; 41, Leah et al., 1992a; 42, Hallacher et al., 1985; 43, Staveland et al., 1993; 44, Jenkins, 1980c; 45, Denton et al., 2006; 46, Brewer et al., 2007; 47, Liu et al., 2006a; 48, Burger et al., 2007a; 49, Storelli et al., 2005; 50, Meador et al., 2004; 51, Padula et al., 2008; 52, Peshut et al., 2008; 53, Cheung et al., 2008.
arsenic levels observed among marine teleosts (Amlund et al., 2006). In one study, Atlantic salmon (Salmo slar) and Atlantic cod (Gadus morhua) were fed diets containing 25.0 mg As/kg ration, as arsenobetaine, for 3 months followed by a 3-month depuration period. Total arsenic concentrations in salmon muscle, liver, and kidney increased significantly; in cod, however, only muscle arsenic burden increased. Half-time persistence of arsenobetaine in muscle of cod was 77 days and for salmon 37 days, resulting in absorption efficiency about twofold higher in cod than in salmon (Amlund et al., 2006). Mortality of 50% in 96 h of sensitive marine teleosts was associated with 12.7-28.5 mg As3+/L; survivors had skin discoloration, respiratory problems, and increased liver
Fishes 51 metallothionein levels (Jessen-Eller and Crivello, 1998; Taylor et al., 1985; USEPA, 1985a,b). Oral administration of sodium arsenate (As5+) to estuary catfish (Cnidoglanis macrocephalus) and school whiting (Sillago bassensis) resulted in tissue accumulations of trimethylarsine oxide. Arsenobetaine levels, which occur naturally in these teleosts, were not affected by As5+dosing. The toxicity of trimethylarsine oxide is unknown, but the ease with which it can be reduced to the highly toxic trimethylarsine is cause for concern (Edmonds and Francesconi, 1987). Proposed arsenic criteria to protect marine fishes and other saltwater biota include muscle residues less than 40.0 mg total arsenic/kg fresh weight (NRCC, 1978), and seawater concentrations less than 0.036 mg As3+/L (4-day average, not to be exceeded more than once every 3 years) and less than 0.069 mg As3+/L (not to be exceeded more than once every 3 years; USEPA, 1985a,b). The proposed arsenic criterion in seafood for human health protection is 0.5 mg inorganic As/kg FW (Cheung et al., 2008).
3.5 Barium Marine cage-reared Atlantic salmon, S. salar, in Scotland during 2000 were fed diets containing 7.0 mg Ba/kg DW; feces contained 8.5 mg Ba/kg DW (Dean et al., 2007), suggesting little accumulation in tissues. Whole Baltic herring, Clupea harengus, contained 0.059 mg Ba/kg dry weight (Zumholz et al., 2006). Barium concentrations in otoliths of snapper, Pagrus auratus, from the vicinity of Port Phillip Bay, Australia, were positively correlated with ambient seawater concentrations of 0.006-0.011 mg Ba/L (Hamer et al., 2006). Otoliths from snappers collected in Port Phillip Bay had 17.5 (6.4-54.0) mg Ba/kg DW; those from coastal waters had <1.0-6.4 mg Ba/kg DW; and those of oceanic Pagrus had 3.2 (1.0-9.9) mg Ba/kg DW (Hamer et al., 2006). However, barium concentrations in otoliths of juvenile flatfishes collected from the central California coast during 1999-2000 were usually higher in offshore locations versus estuaries; a similar pattern is reported for manganese (Brown, 2006). Results of studies with radiobarium-137 to measure the relative contribution of seawater and diet to barium deposited in otoliths of juvenile mummichogs, F. heteroclitus, demonstrated that seawater is the dominant factor controlling accumulation (Walther and Thorrold, 2006).
3.6 Beryllium Muscle and liver of striped bass, M. saxatilis, had less than 0.001 mg Be/kg fresh weight (Heit, 1979). In laboratory studies, whole mummichogs, F. heteroclitus, did not reach equilibrium in 96 h during immersion in seawater solutions containing various concentrations of stable beryllium salts; the maximum concentration factor reached was 0.85 (Eisler, 1974). Whole body concentrations among survivors, in mg Be/kg fresh weight, were <0.4 in controls;
52 Chapter 3 3.7 for those held in 5.0 mg Be/L; 5.8 in the 25.0 mg Be/L group; and 43.0 in the 50.0 mg Be/L group. Some deaths were observed within 96 h at 25.0 mg Be/L and higher (Eisler, 1974).
3.7 Bismuth Otoliths from blackfin tuna, T. atlanticus, collected in the Gulf of Mexico in 2002 contained an average of 0.026 mg Bi/kg DW (Arslan and Secor, 2008).
3.8 Boron Boron concentrations in whole anchovetta, Cetengraulis mysticetus, ranged from 3.3 to 3.6 mg/kg on an ash weight basis (Jenkins, 1980). For yellowfin tuna, Thunnus albacares, boron concentrations were highest in muscle (39.0 mg B/kg ash weight) and whole tuna (9.0 mg/kg AW), and ranged from 1.5 to 5.6 mg/kg ash weight in heart (1.5), gill (1.8), spleen (3.3), and eyeball (5.6; Jenkins, 1980). Boron concentrations in gill, liver, kidney, and muscle of sockeye salmon, Oncorhynchus nerka, ranged from 0.5 to 0.7 mg B/kg fresh weight; for bone, this value was 1.5 (Thompson et al., 1976). The LC50 (96 h) value for dab, Limanda limanda, was 74.0 mg B/L (Taylor et al., 1985); for fry of coho salmon, Oncorhynchus kisutch, this value was 600.0 mg B/L in brackish water (Hamilton and Buhl, 1990). For seawater-adapted coho salmon underyearlings, the LC50 (16 days) value was 12.0 mg B/L (Thompson et al., 1976). After exposure for 3 weeks in seawater solutions containing 10.0 mg B/L—a high sublethal concentration—sockeye salmon bone contained 10.5 mg B/kg fresh weight; for other tissues examined, these values ranged from 3.8 in muscle to 7.3 in kidney (Thompson et al., 1976).
3.9 Cadmium Fish muscle usually contained less than 0.1 mg Cd/kg fresh weight; however, liver concentrations were higher and ranged up to 24.7 mg Cd/kg fresh weight (Table 3.3). Whole finfishes examined generally contained 0.1-0.3 mg Cd/kg fresh weight (Table 3.3), as did molluscs and crustaceans (Hall et al., 1978). Hepatic cadmium burdens in three species of demersal fishes from the Gulf of St. Lawrence was up to five times higher than conspecifics from the St. Lawrence estuary 600 km inland, and may be related to higher cadmium concentrations in Gulf sediments that is reflected in cadmium content of prey (Rouleau et al., 2006). Intraspecies variations among teleosts in cadmium burdens (Table 3.3) may be related to the age, size, or sex of the fish. For mummichog, F. heteroclitus, an estuarine cyprinodontiform fish, there was an inverse relation between length and whole body cadmium content for both males and females (Chernoff and Dooley, 1979). But Pacific hake, Merluccius productus,
Fishes 53 Table 3.3: Cadmium Concentrations in Field Collections of Fishes Organism Alaska. Adak Island; June 2004 Flathead sole, Hippoglossoides elassodon Kidney Liver Muscle Great sculpin, Myoxocephalus polyacanthocephalus Kidney Liver Muscle
Concentration
Reference
0.23 FW 4.95 FW 0.004 FW
55 55 55
0.06 FW 1.26 FW 0.004 FW
55 55 55
European eel, Anguilla anguilla; muscle
0.03 DW
1
Halfbridled goby, Arenigobius frenatus; Australia; industrialized site vs. reference estuary Gonad Muscle
0.16 DW vs. 0.004 DW 0.07 DW vs. <0.007 DW
Arctic cod, Boreogadus saida; muscle
0.68 DW
2
Jolthead porgy, Calamus bajonado Muscle Gill GI tract Vertebrae Scales
0.09 FW; 0.38 DW 0.09 FW; 0.79 DW 0.59 FW; 2.6 DW 0.76 FW; 1.3 DW 1.9 FW; 2.7 DW
3 3 3 3 3
Canned fish; Saudi Arabia; purchased locally Sardine Salmon Tuna
0.18 (0.01-0.69) FW 0.16 (0.02-0.38) FW 0.22 (0.07-0.64) FW
a
63 63
51 51 51
Fivebeard rockling, Ciliata mustela; whole minus viscera
2.1-4.2 DW
4
Baltic herring, Clupea harengus; muscle
0.03-0.12 FW
5
Little tunny, Euthynnus alletteratus Muscle Liver
0.2 DW 2.6 DW
6 6
Fish Byproducts Gills; 7 spp. Gonad; 7 spp.
0.033 (0.005-0.180) FW 0.1-0.5 FW 0.1-0.2 FW
7 8 8 (Continues)
54 Chapter 3 Table 3.3: Organism Heart; 7 spp. Kidney; 8 spp. Liver 24 spp. 18 spp. 18 spp. 14 spp. 7 spp. 1 sp. 8 spp. Muscle 149 spp. 10 spp. 10 spp. 7 spp. 11 spp. 8 spp. 40 spp. 11 spp. 25 spp. 6 spp. 4 spp. 4 spp. 8 spp. 6 spp., Malaysia 12 spp., Australia 8 spp., Gulf of Bothnia 7 spp., coast of Belgium 17 spp.; Turkey; Marmara Sea; 2005 1 species; India; 2003 10 spp.; Mumbai, India; 2004-2005 10 spp.; China; October 2004 Skin; 8 spp. Spleen; 7 spp. Vertebrae 7 spp. 40 spp. Viscera 40 spp. 3 spp.
Cont’d
Concentration
Reference
0.1-0.3 FW 0.1-5.4 FW
8 8
<0.1-0.4 FW 0.4-0.8 FW 0.8-2.0 FW 2.0-7.0 FW 7.0-20.0 FW 20.0-30.0 FW 0.4-24.7 FW
9 9 9 9 9 9 8
<0.1 FW 0.1-0.2 FW <0.05-0.3 FW 0.06-0.16 FW 0.02-0.22 DW 0.002-0.016 FW 0.09 (<0.02-0.52) FW 0.1-0.7 DW <0.1-1.6 DW 0.01-0.09 FW 0.018-0.024 FW 0.1-1.8 DW 0.08-0.15 DW 0.03-0.05 DW 0.04-0.08 FW 0.003-0.042 FW <0.01-0.07 FW 0.012-0.054 FW
9 9 10 11 12 8 13 14 6 16 17 18 19 20 21 22 23 49
0.1 FW 0.02 FW; max. 0.05 FW
58
<0.01-0.09 FW 0.15-0.42 DW 0.3-2.4 FW
61 19 8
0.2-0.9 FW 0.07 (<0.02-0.44) FW
8 13
0.19 (0.02-1.31) FW 0.56-2.58 DW
13 19
a
(Continues)
Fishes 55 Table 3.3: Organism
Cont’d
Concentration
Reference
<0.1-0.2 FW 0.2-0.4 FW 3.0-8.5 DW <0.1-0.5 DW
9 9 24 18
Mummichog, Fundulus heteroclitus Whole Viscera Gills Muscle
5.6 AW; 0.33 FW 6.0 FW 5.0 FW 2.0 FW
25 26 26 26
Pacific cod, Gadus macrocephalus Muscle Liver
0.14 DW 0.17 DW
27 27
Max. 0.05 DW 0.02 DW 0.01-0.07 DW 0.09 DW 0.004-0.028 FW 0.11-2.2 FW
28 29 29 29 30 30
0.12 FW 0.18 FW 0.05 FW 0.002 FW 0.08 FW 0.001-0.008 FW 0.18 FW 0.01 FW 0.02 FW 0.03 FW
31 31 31 7 7 7 7 7 7 7
<0.3 DW <0.3-0.91 DW
32 32
Max. 0.05 FW vs. 0.03-2.1 FW
46
0.24 FW 0.11 FW 0.03 FW
33 33 33
Whole 15 spp. 2 spp. 5 spp. 5 spp.
Atlantic cod, Gadus morhua Roe Muscle Gonad Liver Muscle Liver Muscle Inshore North Sea Distant waters Muscle Tongue Gonads Gills Skin Vertebrae Intestines Goby, Gobius niger Muscle Liver Greenland; 1975-1991; 10 spp.; muscle vs. liver Sapo, Halobatrachus didactylus Intestine Blood Muscle
a
(Continues)
56 Chapter 3 Table 3.3: Organism Indian Ocean; 2004; Mozambique Channel vs. Reunion Island Common dolphinfish, Coryphaena hippurus Liver Muscle Kidney Skipjack, Katsuwonus pelamis Liver Muscle Kidney Yellowfin tuna, Thunnus albacares Liver Muscle Kidney Swordfish, Xiphias gladius Liver Muscle Kidney Yellowtail flounder, Limanda ferruginea Muscle Liver Dab, Limanda limanda Vertebrae Fins Gills Liver Muscle Otoliths Skin Skin plus muscle Striped seasnail, Liparis liparis Whole Whole minus guts Black marlin, Makaira indica Muscle Liver Mediterranean Sea; summer 2003 Swordfish, Xiphias gladius Muscle Liver
Cont’d
Concentration
Reference
5.6 FW vs. 5.5 FW 2.0 FW vs. 0.03 FW 0.4 FW vs. 1.4 FW
56 56 56
no data vs 50.9 FW no data vs. 0.18 FW no data vs. 19.4 FW
56 56 56
39.5 FW vs. 40.4 FW 0.06 FW vs. 0.06 FW 1.0 FW FW vs. 6.3 FW
56 56 56
46.9 FW vs. 46.3 FW 0.25 FW vs. 0.19 FW 7.4 FW vs. 5.2 FW
56 56 56
<0.1-0.1 FW <0.1-0.5 FW
34 34
0.05 DW 0.16 DW 0.22 DW 0.43 DW 0.07 DW 0.19 DW 0.20 DW Max. 0.2 FW
35 35 35 35 35 35 35 36
16.8 DW 2.4-10.4 DW
24 4
0.09 (0.05-0.40) FW 9.2 (0.2-83.0) FW
37 37
0.005 (0.002-0.01) FW 0.16 (0.10-0.29) FW
57 57
a
(Continues)
Fishes 57 Table 3.3: Organism Bluefin tuna, Thunnus thynnus Muscle Liver Pacific hake, Merluccius productus Muscle Whole Mexico; Gulf of California; 1999-2000; muscle Striped mullet, Mugil cephalus Colorado snapper, Lutjanus colorado Orangemouth corvina, Cynoscion xanthulus Dover sole, Microstomus pacificus Muscle Liver
Cont’d
Concentration
Reference
0.02 (0.01-0.04) FW 1.5 (0.06-2.72) FW
57 57
0.012-0.030 FW 0.086-0.12 FW
38 38
0.3 DW 0.2 DW 0.9 DW
64 64 64
3.0 DW 0.19-0.58 DW
39 40
European bass, Morone labrax; muscle Striped bass, Morone saxatilis Muscle Liver
0.03 DW
1
0.03 FW 0.30 FW
41 41
Striped mullet, Mugil cephalus Muscle Muscle
0.04 (0.02-0.08) FW 0.33 (0.01-1.84) DW
16 50
Shorthorn sculpin, Myoxocephalus scorpius Muscle Liver
1.4 DW 4.1 DW
42 42
Papua New Guinea; 5 spp.; tropical deepwater fish; 1999-2002 Muscle Liver
<0.04 FW 11.9 FW
47 47
0.03 DW
1
1.1 DW 1.4 DW 1.6 DW 1.7 DW
24 24 24 24
4.0 DW
24
European flounder, Platichthys flesus Muscle Whole, UK Barnstaple Bay Age 2+ years Age 3+ Age 4+ Age 5+ Oldbury-on-Severn Age 2+
a
(Continues)
58 Chapter 3 Table 3.3: Organism Age 3+ Age 4+ Age 5+
Cont’d
Concentration
Reference
4.5 DW 5.1 DW 5.2 DW
24 24 24
Plaice, Pleuronectes platessa Blood Heart Spleen Liver Kidney Gut Gill filaments Skin Muscle Bone Gut contents Muscle Vertebrae Muscle Fins Gills Liver Otoliths Skin
<0.005 FW 0.005 FW 0.030 FW 0.230 FW 0.046 FW 0.048 FW 0.020 FW 0.068 FW 0.010 FW <0.100 FW 0.030 FW <0.003 FW 0.05-0.35 DW 0.02-0.20 DW 0.03-0.5 DW 0.09-0.48 DW 0.03-0.40 DW 0.06 DW 0.01-1.0 DW
43 43 43 43 43 43 43 43 43 43 43 5 35 35 35 35 35 35 35
Bluefish, Pomatomus saltatrix; muscle
0.04 (0.02-0.08) FW
16
Winter flounder, Pleuronectes americanus Muscle Liver
<0.1 FW <0.1-0.29 FW
34 34
Atlantic salmon, Salmo salar; marine cage farmed; Scotland; 2000 Muscle Bone Gill Gut Adipose Liver Kidney Spleen Diet vs. feces
0.26 DW 0.07 DW 0.003 DW 0.002 DW 0.002 DW 0.004 DW 0.001 DW <0.001 DW 0.21 DW vs. 0.68 DW
54 54 54 54 54 54 54 54 54
a
(Continues)
Fishes 59 Table 3.3:
Cont’d
Organism
Concentration
Windowpane, Scopthalmus aquosus Muscle Liver
<0.1 FW <0.1-0.1 FW
44 44
King mackerel, Scomberomorus cavalla Muscle Muscle Liver
0.3 DW 0.2 DW 4.2 DW
6 48 48
(0.10-1.37) DW
62
(0.02-0.34) DW
62
0.05 DW 0.10 DW 0.62 DW
45 45 45
Spain; 2 spp.; October 2003; liver Four-spotted megrim, Lepidorhombus boscii; 70-120 m depth Pouting, Trisopterus luscus; 200-500 m depth Mackerel, Scombresox saurus Muscle Heart Liver Turkey; Camlik Lagoon, Mediterranean Sea; 2000-2001; winter vs. autumn European bass, Dicentrarchus labrax Gill Liver Gonad Muscle Striped mullet, Mugil cephalus Gill Liver Gonad Muscle Gilthead bream, Sparus auratus Gill Liver Gonad Muscle Turkey; northeast Mediterranean Sea coast; 2003; winter vs. summer Striped mullet, Mugil cephalus Liver Gill Muscle
Reference
0.44 DW 1.49 DW 0.43 DW 0.11 DW
vs. vs. vs. vs.
0.50 DW 0.98 DW 0.45 DW 0.09 DW
52 52 52 52
0.50 DW 1.64 DW 0.41 DW 0.10 DW
vs. vs. vs. vs.
0.54 DW 0.94 DW 0.40 DW 0.06 DW
52 52 52 52
0.43 DW vs. 0.50 DW 0.93 DW vs. 0.58 DW 0.38 vs. 0.39 DW 0.13 DW vs. 0.12 DW
52 52 52 52
5.9 DW vs. 8.1 DW 3.2 DW vs. 4.9 DW 1.2 DW vs. 2.2 DW
53 53 53
a
(Continues)
60 Chapter 3 Table 3.3: Organism Striped goatfish, Mullus barbatus Liver Gill Muscle
Cont’d
Concentration
Reference
14.5 DW vs. 10.9 DW 7.9 DW vs. 5.3 DW 3.1 DW vs. 1.9 DW
53 53 53
Yellowfin tuna, Thunnus albacares; muscle
0.04 (0.02-0.08) FW
16
Blackfin tuna, Thunnus atlanticus; otoliths; Gulf of Mexico; 2002
0.0025 DW
66
Southern bluefin tuna, Thunnus maccoyii; Australia; April 2004; muscle; wild vs. farmed
<0.91 FW vs. <0.01 FW
60
Tuna; canned
0.04 FW
15
0.02-0.06 FW vs. 0.04 FW 0.06-0.24 FW vs. 0.10 FW
65 65
0.02 FW vs. 0.02-0.03 FW 0.23 FW vs. 0.07-0.69 FW
65 65
<0.1 FW <0.1 FW
34 34
Turkey; 2005; Black Sea vs. Aegean Sea European anchovy, Engraulis encrasicolus Muscle Liver Picarel, Spicara smaris Muscle Liver Hake, Urophycis spp. Liver Muscle
a
Values are in mg Cd/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Leatherland and Burton, 1974; 2, Bohn and McElroy, 1976; 3, Lowman et al., 1966; 4, Badsha and Sainsbury, 1978; 5, Topping, 1973; 6, Windom et al., 1973; 7, Julshamn et al., 1978b; 8, Brooks and Rumsey, 1974; 9, Hall et al., 1978; 10, Eustace, 1974; 11, Holden and Topping, 1972; 12, Stickney et al., 1975; 13, Won, 1973; 14, Roth and Hornung, 1977; 15, Stein and McClallan, 1980; 16, Bebbington et al., 1977; 17, Taylor and Bright, 1973; 18, Sims and Presley, 1976; 19, Horowitz and Presley, 1977; 20, Babji et al., 1979; 21, Plaskett and Potter, 1979; 22, Miettinen and Verta, 1978; 23, DeClerck et al., 1979; 24, Hardisty et al., 1974; 25, Eisler et al., 1972; 26, Chernoff and Dooley, 1979; 27, Hamanaka et al., 1977; 28, Julshamn and Braekkan, 1978; 29, Julshamn and Braekkan, 1975; 30, Havre et al., 1973; 31, Portmann, 1972; 32, Grimanis et al., 1978; 33, Gutierrez et al., 1978; 34, Greig and Wenzloff, 1977a; 35, Westernhagen et al., 1980; 36, Newell et al., 1979; 37, Mackay et al., 1975; 38, Cutshall et al., 1977a,b; 39, McDermott et al., 1976; 40, Young, 1974; 41, Heit, 1979; 42, Bohn and Fallis, 1978; 43, Pentreath, 1977a; 44, Greig et al., 1977; 45, Leatherland et al., 1973; 46, Dietz et al., 1996; 47, Brewer et al., 2007; 48, Ploetz et al., 2007; 49, Keskin et al., 2007; 50, Turkmen et al., 2006; 51, Ashraf et al., 2006; 52, Dural et al., 2006; 53, Cogun et al., 2006; 54, Dean et al., 2007; 55, Burger et al., 2007a; 56, Kojadinovic et al., 2007; 57, Storelli et al., 2005; 58, Sankar et al., 2006; 59, Mishra et al., 2007; 60, Padula et al., 2008; 61, Cheung et al., 2008; 62, Fernandes et al., 2008a; 63, Roach et al., 2008; 64, Ruelas-Inzunza and Paez-Osuna, 2008; 65, Turkmen et al., 2008; 66, Arslan and Secor, 2008.
Fishes 61 showed increasing cadmium concentrations in whole body with increasing weight (Cutshall et al., 1977b). Cadmium tends to accumulate in liver of plaice, Pleuronectes platessa (Pentreath, 1977a; Westernhagen et al., 1978) with residues positively linked to the age of the fish but not its weight. For king mackerel, Scomberomorus cavalla, cadmium concentrations in liver increased with increasing fork length (Ploetz et al., 2007). Gender-related differences in cadmium uptake are reported for Atlantic croakers and kelp bass, with males accumulating more cadmium (Burger et al., 2007b). Cadmium as an estrogenic factor is proposed as a contributory cause of elevated vitellogenin (VTG) levels in males of the Antarctic benthic fish, Trematomus bernacchii (Canapa et al., 2007). Mean hepatic cadmium concentrations in male Trematomus in November 2001January 2002 ranged from 9.2 to 21.3 mg Cd/kg DW, or about 10-20 times higher than similar temperate species. Synthesis of VTG in male fish is a widely recognized effect for estrogenic pollutants in temperate organisms. The endocrine properties of cadmium, naturally elevated in Terra Nova Bay, Ross Sea, and increasing during algal blooms would explain, in part, the presence of VTG in males and the seasonal changes of gene induction (Canapa et al., 2007). Uptake, retention, and sublethal effects of cadmium on F. heteroclitus and other teleosts have been investigated under controlled conditions. Concentrations as low as 0.01 mg Cd/L in the medium were potentially harmful to mummichogs and other marine teleosts (Eisler, 1971); whole mummichogs contained up to 45% more cadmium than controls after immersion for 21 days in flowing seawater solutions containing 0.01 mg Cd/L (Eisler et al., 1972); mummichogs with whole body burdens in excess of 86.0 mg Cd/kg body ash will probably die within 5 weeks (Eisler, 1971); concentrations of cadmium not ordinarily lethal to mummichogs exert a negative effect on survival of fish intoxicated by salts of copper, zinc, or a copper-zinc mixture (Eisler and Gardner, 1973); residues of zinc and cadmium in survivors held in mixtures of these salts did not conform to expected uptake patterns based on single metals (Eisler and Gardner, 1973); rate of whole body accumulation of cadmium decreased with increasing concentrations of cadmium in the medium (Eisler, 1974); viscera were the major repository of cadmium during uptake, especially GI tract and liver (Eisler, 1974); and loss of accumulated cadmium over a period of 180 days was about 90% with gall bladder and especially liver most influential in the excretion process, regardless of the level of stable cadmium present in the medium during uptake (Eisler, 1974). Cadmium residue data in mummichogs—and probably other fish species already dead on collection—are of limited worth owing to marked accumulation after death. For example, dead mummichogs held in 40.0 mg Cd/L for 24 h accumulated 53 times as much cadmium as did living mummichogs; this increased to 89 times after immersion for 48 h (Eisler, 1971). Juveniles of the euryhaline black sea bream, Acanthopagrus schlegeli, held in seawater containing low sublethal concentrations of cadmium for up to 7 days had 43-58% of the total cadmium body burden localized in the intestines, especially the anterior intestine (Zhang and Wang, 2007b).
62 Chapter 3 After depuration for 7 days, the intestines contained over 90% of the cadmium body burden, suggesting that little waterborne cadmium entered the rest of the body via intestine and that cadmium may exert its toxic effects mainly on the GI system (Zhang and Wang, 2007b). Cadmium uptake increased as salinity decreased in the range 0-35 ppt, with gill the most sensitive accumulator at lower salinities (Zhang and Wang, 2007a). Liver catalase activity is a useful indicator of cadmium poisoning in mummichogs. Exposure to cadmium concentrations greater than 1.0 mg/L, both in vitro and in vivo, significantly depress liver catalase activity; moreover, preexposure to 1.0 mg Cd/L for 96 h prevents additional catalase inhibition during subsequent exposure for 192 h to 25.0 mg Cd/L (Pruell and Engelhardt, 1980). Cadmium thioneine in Fundulus liver was correlated with adaptive responses in liver catalase activity and appeared to be a better indicator of cadmium toxicity than liver catalase or liver cadmium residues (Pruell and Engelhardt, 1980). In another series of studies, juvenile flatfishes, L. limanda and P. platessa were immersed in seawater containing nominal concentrations of 0.005 or 0.05 mg Cd/L for up to 96 days. At both cadmium concentrations, there was significant accumulation in liver and gills after 96 days when compared to controls. At 0.005 mg Cd/L, all tissues analyzed (vertebrae, fins, gills, liver, muscle, otoliths, and skin) except for otoliths showed significant uptake. However, at 0.05 mg Cd/L, both species had reduced survival, and plaice developed fin erosion (Westernhagen et al., 1980). Many studies have been conducted on cadmium accumulation by eggs and larvae of marine teleosts under laboratory conditions. In general, older developmental stages took up less cadmium than younger stages, with uptake inhibited at comparatively low temperatures and high salinities (Middaugh and Dean, 1977; Voyer et al., 1977; Westernhagen and Dethlefsen, 1975; Westernhagen et al., 1974, 1975). Westernhagen et al. (1974) reared eggs of Baltic herring, C. harengus, in seawater solutions of various salinities, each containing 5.0 mg Cd/L. At the highest rearing salinity of 32 ppt, individual eggs contained 0.000013 mg Cd/egg. Progressively, higher burdens were associated with decreasing salinity, with highest values recorded at the lowest rearing salinity of 5 ppt: 0.000038-0.000057 mg Cd/egg. Uptake of cadmium by herring eggs is rapid. Concentrations of 18.0 mg/kg whole egg, on a fresh weight basis, are reported in solutions containing 5.0 mg Cd/L; the primary site of cadmium uptake was the egg capsule surface, reaching 85.0 mg/kg in the chorion (Rosenthal and Sperling, 1974). Eggs and larvae of Baltic herring and flounder, Platichthys stellatus, had different accumulation rates when compared to those of a needlefish, Belone belone (Dethlefsen et al., 1975). Larvae of herring and flounder reared in 0.05 mg Cd/L, contained 7.0 and 23.0 mg Cd/kg larvae dry weight, respectively at hatch; for needlefish, this value was 0.018 mg/kg. Larval uptake rate for herring larvae immersed in 0.4 mg Cd/L was up to 60.0 mg Cd/kg dry wight daily versus 7.2 for flounder, and negligible accumulations in Belone larvae (Dethlefsen et al., 1975).
Fishes 63 Benzo(a)pyrene (BaP)—a polycyclic aromatic hydrocarbon—did not influence accumulation of cadmium in the Antarctic fish, T. bernacchii; however, cadmium caused significant changes in tissue levels of BaP (Benedetti et al., 2007). In this study, Trematomus were exposed to a mixture of 10.0 mg BaP/kg FW plus 2.0 mg Cd/kg BW, administered by intraperitoneal injection. Cadmium completely suppressed BaP activity; a similar pattern was recorded for copper (2.0 mg Cu/kg BW), but no effects were documented for other metals tested: nickel (2.0 mg Ni/kg BW), lead (2.0 mg Pb/kg BW), or mercury (0.2 mg Hg/kg BW) (Benedetti et al., 2007). Metallothionein-cadmium interactions are important. Metallothioneins are low molecular weight proteins with high cysteine and metal content. Although metallothioneins are usually present in low concentrations in the organs of nonstressed animals, exposure to heavy metals dramatically increases their concentration. Seawater-adapted European eels, Anguilla anguilla, subjected to cadmium salts for long periods accumulated cadmium in liver and gills in the form of bound metallothioneins (Noel-Lambot et al., 1978). In the case of acute cadmium intoxication, only liver accumulated cadmium as cadmium-thioneins. Metallothioneins are present in the liver on noncadmium-exposed eels, but in lower amounts than chronically intoxicated eels; these metallothioneins are mainly in the form of zinc and copper derivatives. In the gills, metallothionein levels were below detection limits (NoelLambot et al., 1978). In an earlier study with seawater-adapted European eels, Noel-Lambot and Bouquegneau (1977) demonstrated that eels immersed in 0.1-0.13 mg Cd/L for 32 days contained 13.0-116.0 mg Cd/kg fresh weight in various organs and tissues, and that muscle accounted for 66% of all cadmium burdens and skin 13%. Continued immersion for up to 60 days showed marked translocation and detoxification: cadmium residues at 60 days in various organs and tissues ranged from 0.6 to 16.0 mg Cd/kg fresh weight with muscle containing 27% of the total body burden, digestive tract 25%, and kidney 20%. Hepatic cadmium concentrations in European eels and metallothionein concentrations increased with increasing weight and age of the eel and tended to be higher in winter (Bird et al., 2008). Liver metallothionein levels in sea bass, Dicentrarchus labrax, increased following intraperitoneal injection of 0.05-0.25 mg Cd/kg BW, being saturated beyond 0.1 mg Cd/kg BW; maximum induction was obtained at 0.1 mg Cd/kg BW, being 5.3 times higher than controls (Jebali et al., 2008). Diet is considered an important pathway for cadmium accumulation in marine fishes. Juvenile rockfish, Sebastes schlegeli, all survived diets containing 0.0, 0.5, 5.0, 25.0, or 125.0 mg Cd/kg ration for 60 days (Kim et al., 2006). Growth was inhibited in the 25.0 and 125.0 mg/kg diet groups. Cadmium accumulation in gill, intestine, kidney, liver, and muscle increased with increasing dosage and was significantly elevated above control levels in gill (<0.5 mg Cd/kg DW) at 25.0 mg Cd/kg diet (3.3 mg Cd/kg DW) and 125.0 mg Cd/kg ration (8.6 mg Cd/kg DW). After 30 days on a Cd-free diet, gill cadmium concentrations were
64 Chapter 3 2.0 mg Cd/kg DW in the 25.0 mg Cd/kg diet group and 6.0 in the 125.0 mg Cd/kg diet. Fish fed with 125.0 mg Cd/kg diet for 60 days had 180.0 mg Cd/kg DW in intestine, 90.0 in kidney, 105.0 in liver, 8.6 in gill, and 0.7 mg Cd/kg DW muscle; during depuration, there was no decrease in kidney or muscle, and intestine decreased to 80.0 mg Cd/kg DW (Kim et al., 2006). Porgies, Pagrus major, fed diets containing 0.0, 37.0, 150.0, or 375.0 mg Cd/kg dry weight for 113 days had significant cadmium accumulations in tissues (Itazawa and Koyama, 1978). Fish given the 375.0 mg Cd/kg diet contained, in mg Cd/kg dry weight, 64.0 in digestive tract, 146.0 in hepatopancreas, and 164.0 in liver; there were no detectable concentrations in muscle or gill. Although cadmium interferes with calcium metabolism in freshwater teleosts, this effect was not observed in porgies, suggesting that the relatively high calcium level in marine waters may counteract cadmium effects (Itazawa and Koyama, 1978). Plaice, P. platessa accumulated cadmium from seawater and also from diet; in both instances cadmium residues were highest in liver (Pentreath, 1977a). Cadmium was most toxic to larvae of the sheepshead minnow, Cyprinodon variegatus. At reduced salinities and reduced temperatures; the free ion (Cd2+) accounted for 20% of total cadmium at 5 ppt, 8% at 15 ppt, and 4.5% at 25 ppt salinity (Hall et al., 1995). The exact mechanism of acute cadmium poisoning is unknown, but is dependent, in part, on exposure period, concentration of cadmium in the medium, and temperature and salinity of the medium. It seems that under conditions of high cadmium concentration and short exposure, the gill is the main site of damage and accumulation. But under conditions of prolonged exposure and comparatively low cadmium concentrations, the intestines, kidneys, and possibly other tissues were measurably affected (Eisler, 1971). Other studies indicate that the ability of adult marine teleosts to accumulate and retain cadmium from the medium is dependent, in part, on exposure period, ambient cadmium concentration, tissue uptake potential, and postexposure recovery period (Bengtsson, 1977; Eisler, 1974; Greig et al., 1974; Gutierrez et al., 1978; Hiyama and Shimizu, 1964; MacInnes et al., 1977; Middaugh et al., 1975). Unfortunately, most of these studies were conducted using extremely high levels of cadmium not likely to be encountered by feral teleosts. Although cadmium concentrations in edible muscle of marine teleosts do not exceed the human emetic threshold of 13.0-15.0 mg/kg fresh weight, the significance of lower concentrations in these tissues and their implications for human health are imperfectly understood. European eels, A. anguilla, at the glass eel stage were exposed to 0, 0.02, or 0.01 mg Cd/L for 14 days under conditions of adequate oxygen (normoxia) or hypoxia in brackish water for 14 days (Pierron et al., 2007b). Cadmium mimics the effect of hypoxia on gills of glass eels, although hypoxia induces a stronger decrease in antioxidant enzymes expression than does cadmium. Coexposure to cadmium and hypoxia could lead to severe impairment of gill function in European eels and this, in part, may account for the 10-fold decline in eel population since the 1980s (Pierron et al., 2007b). Adult European eels exposed to
Fishes 65 0.005 mg Cd/L for 30 days had reduced growth rate and a lower efficiency of lipid storage when compared to controls (Pierron et al., 2007a). Impairment was attributed to a cadmium-induced increase in fat consumption which, in turn, could affect reproduction during migration (Pierron et al., 2007a). Preexposure to cadmium—but not zinc—affects kinetics of metal uptake (Zhang and Wang, 2006). In the case of juvenile black sea bream, A. schlegeli, the exposure for 24 h to cadmium concentrations up to 0.3 mg/L increased the cadmium accumulation linearly with increasing exposure time after the initial cadmium surface binding; viscera were the most important site of cadmium uptake followed by gills. These same fish were then subjected to waterborne (0.114 mg Cd/L) or dietary cadmium (615.0 mg Cd/kg) for 1 week. Following preexposure, cadmium body burdens were enhanced up to 8-fold (waterborne) and 49-fold (dietary), suggesting that previous exposure history is important in assessing the significance of cadmium burdens in fish (Zhang and Wang, 2006). Flight behavior of sea bass, D. labrax, was affected during exposure to 0.0005 mg Cd/L for 4-h daily over an 8-day period (Faucher et al., 2008). These fish had damage to lateral line system neuromasts together with decreased escape behavior. After 15 days of 4-h exposure, neuromasts presented progressively less damage, cadmium accumulations in gills and scales decreased, and fish escape behavior had recovered (Faucher et al., 2008). To protect human consumers of fish muscle, the European Union recommends less than 0.1 mg Cd/kg FW muscle (Kojadinovic et al., 2007); the same level of protection is recommended in Turkey (Keskin et al., 2007), and China (Cheung et al., 2008). To protect fish and other aquatic life in UK estuaries and coastal waters, a maximum seawater concentration of 0.005 mg Cd/L is recommended (Canli and Stagg, 1996). To protect 90% of the teleost species in Chesapeake Bay against acute cadmium intoxication, the cadmium concentration should not exceed 0.163 mg/L; for freshwater portions of Chesapeake Bay and freshwater teleosts, this value is less than 0.0009 mg Cd/L (Hall et al., 1998). Eisler (2000c) states that seawater containing more than 0.0045 mg Cd/L is considered potentially hazardous to marine life pending acquisition of additional data.
3.10 Cerium Marine teleosts took up radiocerium from seawater by whole body concentration factors that ranged from 1 to 5 (Ancellin and Vilquin, 1966, 1968). Uptake factors for individual tissues of Chasmichthys gulosus, for example, varied substantially: >70 in gill to 0.3 in muscle; intermediate values occurred in digestive tract (>20), head and fins (>15), viscera (>4), and vertebrae (>4) (Hiyama and Shimizu, 1964). The addition of chelating agents to the medium, such as EDTA, reduced cerium uptake significantly (Hiyama and Shimizu, 1964).
66 Chapter 3
3.11 Cesium Cesium in fish tissues, except scales, ranged from 0.006 to 0.045 mg/kg on a fresh weight basis; scales contained up to 0.53 mg Cs/kg on a dry weight basis (Table 3.4). Cesium is accumulated over ambient seawater concentrations by whole fish (Ancellin and Vilquin, 1968; Ichikawa, 1961) and selected tissues (Hiyama and Shimizu, 1964; Van As et al., 1973). Cesium in diets of cultured Atlantic salmon, S. salar, contained 0.2 mg Cs/kg DW and feces contained only 0.01 mg Cs/kg DW (Dean et al., 2007), suggesting some uptake from diet. Most 137Cs detected in marine biota has been attributed to global fallout from atmospheric nuclear tests between 1954 and 1980, and to the Chernobyl accident in 1986 (Eisler, 2000i, 2003). Radiocesium concentrations in muscle of Atlantic cod, G. morhua, and European flounder, Pleuronectes flesus, in the southern Baltic Sea increased as a result of contamination from the Chernobyl nuclear reactor incident by factors ranging from 2 to 5 (Grzybowska, 1989). Radiocesium-137 levels in two species of whole teleosts from the Gulf of Finland increased as a result of the April 1986 Chernobyl nuclear reactor accident; levels increased by a factor of 41 in 1986 post-Chernobyl to 86 in 1987, to 83 in 1990 (Kryshev, 1995). Elevated concentrations of 137Cs in walleye pollock, Theragra chalcogramma, from Japan in 2000 could not, however, be reconciled with 137Cs in the Japanese biogeochemical environment or with a nuclear reactor accident in the Sea of Japan involving a submarine (Morita et al., 2007). Pollack—which migrate extensively through
Table 3.4: Cesium Concentrations in Field Collections of Fishes Organism
Concentration
Fish Muscle 17 spp. 8 spp. 10 spp. Scales; 7 spp.
0.006-0.044 FW 0.06-0.16 DW 0.011-0.045 FW 0.008-0.530 DW
1 2 3 4
0.0009-0.0081 DW
5
0.060 FW 0.027 FW 0.037 FW
6 6 6
Chub mackerel, Scomber japonicus; otoliths Albacore, Thunnus alalunga Blood Liver Muscle
Reference
a
Values are in mg Cs/kg fresh weight (FW) or dry weight (DW). a 1, Van As et al., 1975; 2, Ishii et al., 1978; 3, Van As et al., 1973; 4, Papadopoulu and Kassimati, 1977; 5, Papadopoulu et al., 1980; 6, Hansen et al., 1978.
Fishes 67 137
Cs-contaminated coastal waters of Russia and Korea in the Sea of Japan—were presumably contaminated in these waters and not in Japanese costal waters (Morita et al., 2007). Similar observations and conclusions were reached with Masu salmon, Oncorhynchus masu, that also migrate extensively in the Sea of Japan (Sazykina, 1998; Yoshida et al., 1994). Postlarval summer flounder, Paralichthys dentatus, took up 9 to 11 times the amount of 137Cs in seawater over a period of 91 days (Baptist and Price, 1962). Adults of Atlantic croakers, Micropogon undulatus, showed a similar pattern with major accumulations in heart, liver, and spleen (Baptist and Price, 1962). Cesium uptake from diet is reportedly greater than from seawater (Hewett and Jefferies, 1978; Pentreath and Jefferies, 1971). For example, 137Cs accumulated in muscle of plaice, P. platessa, with concentrations directly related to the cesium content of the annelid (Nephtys sp.) in their diet (Pentreath and Jefferies, 1971). Uptake of 134Cs is dependent on the weight of the organism. For plaice and eel, over 1000-fold ranges of weight, the uptake varied according to weight0.78 (Morgan, 1964). Mugil chelo and Blennius pholis contaminated by 137Cs have two distinct elimination phases: one fast and the other slow (Frazier and Vilquin, 1971). The fast stage ranged from 20 to 30 days; the slow stage was 154 days for Mugil and 203 days for Blennius. Biological half-times of 134 Cs in various tissues of the plaice ranged from 10 days in liver to 120 days in muscle (Jefferies and Hewett, 1971). The long biological half-time of cesium in edible muscle of fish increases slowly with fish size. Commercial sizes of plaice, viz., greater than 150 g, are not expected to reach equilibrium with water cesium concentrations in the vicinity of radioactive waste outfalls because seawater cesium concentrations decrease with increasing distance from the outfall and the pattern of fish migration will not permit equilibration (Jefferies and Hewett, 1971).
3.12 Chromium Chromium concentrations in tissues of most species of finfishes ranged from 0.1 to 0.4 mg Cr/kg fresh weight; for whole fishes, the majority of these values were in the range 0.2-0.6 mg Cr/kg fresh weight (Table 14.5). However, grossly elevated chromium burdens of 151.0 mg/kg fresh weight and 1386.0 mg/kg dry weight were recorded in whole fish from chromium-contaminated coastal bays in Egypt and Texas (Table 3.5). Chromium seems to concentrate in the scales of some species from Greece, with burdens up to 97.0 mg Cr/kg dry weight recorded (Table 3.5). There is general agreement that chromium does not biomagnify in freshwater, marine, or terrestrial food chains involving invertebrates, fishes, birds, and mammals; instead, there is decreasing concentrations with increasing trophic level (Holdaway, 1988; Outridge and Scheuhammer, 1993; USPHS, 1993a). Chromium concentrations vary significantly among different species of fish from the same geographic area. For example, muscle of a porgy, Pachymetopon grande, contains 1430 times more chromium per unit
68 Chapter 3 Table 3.5: Chromium Concentrations in Field Collections of Fishes Organism Alaska, Adak Island; June 2004 Flathead sole, Hippoglossoides elassodon Liver Kidney Muscle Great sculpin, Myoxocephalus polyacanthocephalus Liver Kidney Muscle
Concentration
Reference
0.28 FW 0.11 FW 0.09 FW
28 28 28
0.17 FW 0.24 FW 0.09 FW
28 28 28
Sparid, Boops boops; muscle
0.22 DW
1
Canned fish; Saudi Arabia; purchased locally Sardine Salmon Tuna
0.31 (0.02-0.89) FW 0.4 (0.1-0.7) FW 0.18 (0.07-0.33) FW
27 27 27
<0.1-0.6 FW 5.5-7.5 DW
2 18
<0.1-0.3 FW <0.1-0.8 FW <0.1-0.3 FW
2 2 2
<0.1-0.3 FW <0.1 FW 0.1-0.2 FW 0.2-0.4 FW 0.4-2.0 FW
2 3 3 3 3
Fish Gills; 7 spp. Gills; various species; Arabian Gulf; 1992; oil spill in 1991 Gonad; 7 spp. Heart; 7 spp. Kidney; 8 spp. Liver 8 spp. 7 spp. 44 spp. 27 spp. 4 spp. Muscle 8 spp. 7 spp. 7 spp.; Israel; Mediterranean Sea 6 spp.; India; 2003 8 spp.; Spain; April-May 1990; Mediterranean Sea 10 spp.; China; October 2004 10 spp. 11 spp. 15 spp.; Morocco; Mediterranean Sea
2.0-7.3 DW 0.22-0.45 FW 0.07-0.8 (0.06-3.7) DW 0.1-1.0 FW 0.01-0.47 FW
4 5 19 30 22
0.04-0.18 FW <0.1-1.9 FW 0.6-4.9 DW (<0.01-1.8) FW
32 6 7 20
a
(Continues)
Fishes 69 Table 3.5: Organism 8 spp. 12 spp. 4 spp. 90 spp. 56 spp. 9 spp. 13 spp. Otoliths; 8 spp. Scales; 6 spp. Skin; 8 spp. Spleen; 7 spp. Viscera 4 spp. 4 spp. Whole 4 spp.; Egypt; chromiumcontaminated Bay 5 spp. 9 spp. 3 spp.
Cont’d
Concentration
Reference
0.01-0.03 FW 0.05-0.18 FW; 0.22-0.80 DW <0.1 FW 0.1-0.2 FW 0.2-0.3 FW 0.3-0.5 FW <0.1-3.0 FW 2.5-6.9 DW 0.6-97.0 DW 3.1-8.1 DW <0.1-4.8 FW
2 8 3 3 3 3 9 10 10 4 2
1.8-4.5 DW 0.03-0.5 DW
4 11
64.0-151.0 FW
21
<0.1-0.3 FW 0.3-0.5 FW 0.5-0.8 FW
3 3 3
Killifish, Fundulus sp.; whole; New Jersey; Hackensack River wetlands vs. reference site; August-November 1991
3.4 (0.9-8.4) DW vs. 1.7 (1.1-2.4) DW
24
Pinfish, Lagodon rhomboides; whole; Texas; Laguna Madre; 1986-1987
40.0 (3.0-1386.0) DW
23
Yellowtail flounder, Limanda ferruginea Muscle Liver
Max 0.1 FW Max 0.2 FW
12 12
Dab, Limanda limanda; skin plus muscle
0.2 FW
13
Mullet, Liza saliens; contaminated lagoon; Portugal; 2003-2004 Muscle Liver
<0.037 DW <0.037 DW
31 31
<0.2 DW
14
5.0 FW 5.0-6.0 FW
15 15
Dover sole, Microstomus pacificus; muscle Striped bass, Morone saxatilis Muscle Liver
a
(Continues)
70 Chapter 3 Table 3.5:
Cont’d
Organism
Concentration
Reference
Mullet, Mugil spp.; Mediterranean Sea; June-July 2003 Muscle Liver Gills Skin
0.15-0.16 FW 0.64-0.90 FW 0.32-0.35 FW 0.20-0.23 FW
25 25 25 25
Striped mullet, Mugil cephalus; muscle; August 2005; Turkey
1.1 (0.13-4.3) DW
26
Summer flounder, Paralichthys dentatus; muscle
0.22-0.68 DW
16
<0.5 FW Max. 0.5 FW
12 12
Winter flounder, Pleuronectes americanus Muscle Liver European pilchard, Sardina pilchardus; muscle
0.14 DW
Windowpane, Scopthalmus aquosus Muscle Liver
<0.3-0.6 FW <0.7 FW
Jack, Seriola sp.; muscle
2.8 FW
Spain; October 2003; liver Four-spotted megrim, Lepidorhombus boscii; depth 70-120 m Pouting, Trisopterus luscus; depth 200-500 m Shallow-water sole, Synaptura marginata; muscle Turkey; 2005; Black Sea vs. Aegean Sea European anchovy, Engraulis encrasicolus Muscle Liver Picarel, Spicara smaris Muscle Liver Red hake, Urophycis chuss Muscle Liver
1
17 17 6
(1.0-2.9) DW
33
(0.4-3.6) DW
33
4.1 FW
a
6
0.09-0.17 FW vs. 0.36 FW 0.28-0.51 FW vs. 0.64 FW
34 34
0.09 FW vs. 0.16-0.51 FW 0.33 FW vs. 0.6-3.0 FW
34 34
<0.6 FW <0.6 FW
12 12 (Continues)
Fishes 71 Table 3.5: Organism White hake, Urophycis tenuis Liver Muscle Liver Grass goby, Zosterisessor ophiocephalus; muscle; Venice lagoon; 2005-2006; San Giuliano vs. Sacca Sessola April July October February
Cont’d
Concentration <0.2 FW <0.2 FW 0.2-0.6 DW
0.3 DW 1.2 DW 0.3 DW 0.2 DW
vs. vs. vs. vs.
Reference
a
12 12 16
0.2 DW 0.002 DW 0.3 DW 0.6 DW
29 29 29 29
Values are in mg Cr/kg fresh weight (FW) or dry weight (DW). a 1, Fukai, 1965; 2, Brooks and Rumsey, 1974; 3, Hall et al., 1978; 4, Horowitz and Presley, 1977; 5, DeClerck et al., 1979; 6, Van As et al., 1973; 7, Roth and Hornung, 1977; 8, Plaskett and Potter, 1979; 9, Van As et al., 1975; 10, Papadopoulu and Kassimati, 1977; 11, Fukai and Broquet, 1965; 12, Greig and Wenzloff, 1977a; 13, Newell et al., 1979; 14, McDermott et al., 1976; 15, Heit, 1979; 16, Greig, 1975; 17, Greig et al., 1977;18, Al-Yakoob et al., 1994; 19, Hornung and Ramelow, 1987; 20, El Hraiki et al., 1992; 21, Dahab et al., 1990; 22, Schuhmacher et al., 1992; 23, Custer and Mitchell, 1993; 24, Hall and Pulliam, 1995; 25, Storelli et al., 2006; 26, Turkmen et al., 2006; 27, Ashraf et al., 2006; 28, Burger et al., 2007a; 29, Nesto et al., 2007; 30, Sankar et al., 2006; 31, Fernandes et al., 2008b; 32, Cheung et al., 2008; 33, Fernandes et al., 2008a; 34, Turkmen et al., 2008.
weight than does muscle of a goosefish, Lophius piscatorius, from the same collection (Van As et al., 1973). The reasons for this disparity are unclear. Elwood et al. (1980) aver that chromium is an element with a determinant concentration in fish, and that accumulation is independent of environmental concentration; this concept requires validation. Noteworthy is their observation that chromium concentrations were lower in muscle and carcass of older freshwater teleosts—an observation consistent with the findings of Eisler (1984), who noted that liver chromium decreased with increasing age of marine teleosts. Uptake of chromium under laboratory conditions is documented for the speckled sanddab, Citharichthys stigmaeus (Mearns and Young, 1977) and the Atlantic croaker, M. undulatus (Baptist et al., 1970). Sanddabs held in seawater solutions containing 3.0-5.0 mg Cr/L contained up to 100.0 mg Cr/kg intestine on a dry weight basis; for liver and muscle, these values were 10.0 and 3.0, respectively. Sanddabs can accumulate significant concentrations of chromium in various tissues during chronic exposure to ambient seawater concentrations as low as 0.016 mg Cr/L (Mearns and Young, 1977). Baptist et al. (1970) studied the retention of 51Cr in croakers after a single intraperitoneal injection. They concluded that 51Cr retention was expressed as two exponential rate functions: 70 days for the long-lived component, and 20 days for the short-lived component.
72 Chapter 3 Trivalent chromium, as chromic oxide, in the diet has been used as an indigestible marker to measure nutrient digestibility in American lobsters and freshwater-reared Arctic char, Salvelinus alpinus (Ringo, 1993). The addition of 1% trivalent chromium to the diet of seawater-reared char results in altered intestinal microflora and increased lipids in the feces (Ringo, 1993), and suggests that use of Cr3+for this purpose be discontinued. Trivalent chromium is relatively innocuous to the gray mullet, Chelon labrosus (Walsh et al., 1994). Mullet held for 60 days in aquaria with sediments containing 46.0 mg Cr3+/dry weight and fed diets containing 4.4-13.8 mg Cr3+/kg dry weight ration had normal growth, survival, macroscopic physiology, and behavior; however, when compared to controls (6.4 mg Cr/kg sediments, 0.3-0.9 mg/kg DW ration), liver concentrations were elevated: 34.0 mg/kg dry weight versus 2.0 (Walsh et al., 1994). Larvae of mummichog, F. heteroclitus, exposed to concentrations as high as 24.0 mg Cr/L, as hexavalent chromium, for 30 days had reduced larval growth and altered gene expression. The no-observable-effect-concentration was 1.5 mg Cr6+/L and the lowest observable effect concentration was 3.0 mg/L (Roling et al., 2006). Body burdens of Cr6+-exposed fish show a dose-dependent increase that was inversely correlated with body weight. Larvae exposed to Cr6+differentially expressed 16 genes in a dose-dependent manner; many of these genes are involved in energy metabolism or growth. Adult mummichogs exposed to Cr6+for 7 days at 0.0, 1.5, or 3.0 mg Cr/L had altered gene expression of 10 genes in liver, most of which are involved in energy metabolism (Roling et al., 2006). Proposed hexavalent chromium criteria for marine life protection is 0.018 mg/L as a 24-h average, not to exceed 1.26 mg/L at any time (USEPA, 1980g); there is an insufficient database for trivalent chromium, but presumably it would be less stringent than hexavalent chromium (USEPA, 1980g). The State of California has proposed the following chromium criteria for protection of marine teleosts and other marine biota: <0.002 mg/L of total chromium, 6 month median; <0.008 mg/L of total chromium, daily maximum; and <0.02 total chromium, instantaneous mix (Ecological Analysts, 1981). For waste discharges into California waters, effluents should contain <0.005 mg total chromium/L for at least 50% of measurements, and <0.01 mg/L for less than 10% of measurements (Reish, 1977). To protect human health in China, seafood products should contain <2.0 mg Cr/kg FW (Cheung et al., 2008).
3.13 Cobalt Cobalt is essential for the normal growth of freshwater teleosts although its role has not been as clearly defined in marine fishes. Maximum cobalt concentrations reported in edible tissues of marine teleosts were 0.36 mg Co/kg on a fresh weight basis, and 4.7 on a dry weight basis; concentrations in scales and spleen were somewhat higher (Table 3.6).
Fishes 73 Table 3.6: Cobalt Concentrations in Field Collections of Fishes Organism
Concentration
Sandlance, Ammodytes tobianus; whole
0.07-008 DW
1
0.13 (0.003-0.074) FW
2
0.002-0.012 FW 0.007-0.022 DW 0.002-0.033 FW 0.07 FW; max. 0.17 FW 0.24-0.36 FW; 0.801.45 DW 0.02-1.3 DW 0.05-5.60 DW 0.14-0.56 AW
3 4 5 16 6
Fish Byproducts Muscle 10 spp. 8 spp. 15 spp. 10 spp.; Mumbai, India; 2004-2005 12 spp. Otoliths; 8 spp. Scales; 11 spp. Whole; 4 spp.
Reference
7 7 8
Fishmeal; 4 spp. Presscake N-liquor Meal
0.17 DW 0.28 DW 0.82 DW
Atlantic cod, Gadus morhua Roe Muscle Tongue Gonads Gills Skin Vertebrae Intestines
0.002-0.030 DW <0.005 FW 0.003 FW 0.002-0.008 FW 0.005 FW 0.004 FW 0.005 FW 0.24 FW
10 2 2 2 2 2 2 2
Goby, Gobius niger Muscle Liver
0.02 DW 0.05 DW
11 11
1.3 (0.02-4.7) DW
14
6.4 DW 1.8 DW 6.4 DW 5.0 DW 9.2 DW 4.8 DW 8.1 DW
12 12
Striped mullet, Mugil cephalus; muscle; August 2005; Turkey Pandora, Pagellus erythrinus Fins Eyes Eggs Gills Brain Liver Intestine
a
9 9 9
12 12 12 (Continues)
74 Chapter 3 Table 3.6: Organism Spleen Muscle Skin Bone Whole
Cont’d
Concentration 26.0 DW 4.1 DW 4.8 DW 0.2 DW 5.2 DW
Reference 12 12 12 12
Pollock, Pollachius virens; whole
0.02-0.04 DW
Atlantic salmon, Salmo salar; marine reared; diet vs. feces
0.17 DW vs. 0.36 DW
15
Sparid, Sargus annularis Muscle Liver
0.03-0.04 DW 0.25-0.42 DW
11 11
Mackerel, Scomber sp.; otoliths; Aegean Sea Cyclades Islands Dodecanese area Petalion Gulf
0.012 (0.001-0.024) DW 0.008 (0.005-0.010) DW 0.110 (0.004-0.220) DW
13 13 13
0.0032 DW
18
0.06-0.08 FW vs. 0.05 FW 0.11-0.53 FW vs. 0.10 FW
17 17
0.04 FW vs. 0.01-0.04 FW 0.08 FW vs. 0.07-0.23 FW
17 17
Blackfin tuna, Thunnus atlanticus; otoliths; Gulf of Mexico; 2002 Turkey; 2005; Black Sea vs. Aegean Sea European anchovy, Engraulis encrasicolus Muscle Liver Picarel, Spicara smaris Muscle Liver
a
1
Values are in mg Co/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Julshamn and Braekkan, 1973; 2, Julshamn et al., 1978b; 3, Van As et al., 1973; 4, Ishii et al., 1978; 5, Van As et al., 1975; 6, Plaskett and Potter, 1979; 7, Papadopoulu and Kassimati, 1977; 8, Robertson, 1967; 9, Lunde, 1968b; 10, Julshamn and Braekkan, 1978; 11, Grimanis et al., 1978; 12, Papadopoulu et al., 1972; 13, Papadopoulu et al., 1980; 14, Turkmen et al., 2006; 15, Dean et al., 2007; 16, Mishra et al., 2007; 17, Turkmen et al., 2008; 18, Arslan and Secor, 2008.
Laboratory studies with isotopes of radiocobalt indicate that marine teleosts accumulate and retain cobalt when administered via the medium (Ichikawa, 1961), the diet (Amiard-Triquet and Amiard, 1974), or by injection (Baptist et al., 1970). In one study, P. platessa fed annelid worms, Arenicola marina, contaminated with radiocobalt, showed low assimilation rates with almost all radioactivity confined to liver and kidney tissues (Amiard-Triquet and Amiard, 1974). In the Atlantic croaker, M. undulatus, the half-time persistence of 60Co
Fishes 75 following a single intraperitoneal injection was about 31 days, and, unlike many other elements, appeared to be a single rate function (Baptist et al., 1970).
3.14 Copper Copper concentrations among marine vertebrates, including teleosts, are among the lowest recorded for this metal among all groups of marine biota. The reasons for this are unknown, but suggest a discrimination against copper by the highest trophic levels (Eisler, 1978, 1984). However, elevated tissue burdens are not uncommon in teleosts collected from areas receiving copper-containing wastes (Denton et al., 2006; Table 3.7). Sites of copper accumulation, storage, and action vary among marine teleosts. Hall et al. (1978) report that there is a significant difference in mean copper levels between muscle and liver of North American finfish. They found that muscle contained from 0.1 to 2.0 mg Cu/kg fresh weight, with most values between 0.2 and 0.5 mg Cu/kg; liver contained between 1.0 and 110.0 mg Cu/kg fresh weight, with no apparent mode. Similar observations were recorded by other investigators (Table 3.7). In rudd, S. erythrophthalmus, liver was the most active site of copper deposition, followed by scales, spleen, kidney, gill, swim bladder, and muscle, in that order (Vorob’yev and Zaystev, 1975). Viscera of mummichog, F. heteroclitus, which accounts for only 4% of the total fish ash weight, contained a disproportionate 41% of total body copper on an ash weight basis; the head contained about 42% of the total body copper, and the remainder of the fish 17% (Eisler and LaRoche, 1972). In Atlantic cod, G. morhua, the copper burdens in roe show significant increases during the reproductive cycle (Julshamn and Braekkan, 1978). Copper binding proteins were isolated from plasma of winter flounder, Pleuronectes americanus; a single fraction of molecular weight 170,000 was isolated from plasma of both males and females (Fletcher and Fletcher, 1980; Fletcher and King, 1978b). Elevated metallothionein levels in the anterior intestine of red mullet, Mullus barbatus, from coastal marine areas of the Eastern Adriatic Sea are useful biomarkers of copper exposure; however, this relation did not hold for zinc, iron, manganese, and cadmium (Marijic and Raspor, 2007). Metallothionein levels in liver of sea bass, D. labrax increased linearly in response to increasing doses of copper ion (0.05-0.25 mg Cu/kg BW) injected intraperitoneally; after 48 h, maximum induction was obtained at 0.25 mg Cu/kg BW with an eightfold increase over controls (Jebali et al., 2008). Copper in liver of European eels, A. anguilla, was positively correlated with metallothionein loadings; metallothionein (and copper) increased with increasing age and length of eels, and was highest in winter (Bird et al., 2008). Other factors known to modify copper accumulations in marine fishes include the gender and age of the fish (Table 3.7), the season of the year, temperature, and salinity of the medium, and the presence of other elements. Copper concentrations in tissues of marine
76 Chapter 3 Table 3.7: Copper Concentrations in Field Collections of Fishes Organism
Concentration
Wahoo, Acanthocybium sp.; muscle
0.9-14.0 FW; 3.3-42.0 DW; 49.0-130.0 AW
1
Surf bream, Acanthopagrus australis; muscle
0.5 (0.1-2.0) FW
2
110.0 AW 0.6-2.9 FW; 2.7-12.0 DW; 24.0-110.0 AW
3 1
10.0 DW
4
European eel, Anguilla anguilla Muscle Liver
0.5-0.6 FW 14.9-25.1 FW
5 5
American eel, Anguilla rostrata; muscle
0.8 DW
4
Halfbridled goby, Arenigobius frenatus; Australia; industrialized site vs. reference estuary Gonad Muscle
6.1 DW vs. 3.5 DW 1.5 DW vs. 0.51 DW
Kob, Argyrosomus notolepidotus; muscle
0.64 (0.1-2.4) FW
2
Australian salmon, Arripes trutta Muscle Liver; male vs. female
0.87 (0.2-1.7) FW 15.0 FW vs. 45.0 FW
2 6
Bigeye anchovy, Anchoa lamprotaenia Whole Muscle Bay anchovy, Anchoa mitchelli; whole minus head
Reference
a
69 69
Gafftopsail catfish, Bagre marinus; muscle
0.7 DW
Silver perch, Bairdiella chrysoura; muscle
3.5 DW
4
Arctic cod, Boreogadus saida Muscle Liver
4.0 DW 4.0 DW
7 7
Jolthead porgy, Calamus bajonado Muscle GI tract Gills Scales Eyes Vertebrae
0.4 FW; 1.5 DW; 17.0 AW 2.4 FW; 10.0 DW; 76.0 AW 1.2 FW; 3.5 DW; 13.0 AW 4.9 FW; 6.9 DW; 13.0 AW 52.0 AW 8.3 FW; 14.0 DW; 26.0 AW
1 1 1 1 1 1 (Continues)
Fishes 77 Table 3.7:
Cont’d
Organism
Concentration
Reference
Canned fish; Saudi Arabia; purchased locally Sardine Salmon Tuna
2.3 (0.6-4.3) FW 1.7 (0.6-3.1) FW 1.0 (0.1-1.9) FW
Horse-eye jack, Caranx latus; muscle
1.9 FW; 7.8 DW; 34.0 AW
1
Black sea bass, Centropristes striata; muscle
<0.3 DW
4
Myctophid, Ceratoscopelus warmingii; muscle
2.2 DW
4
Anchovy, Cetengraulis edentulus; muscle
1.6 FW; 6.4 DW; 27.0 AW
1
Blackfin icefish, Chaenocephalus aceratus; Antarctica; 1989 Liver Muscle
4.5 FW 1.5 DW
Squirefish, Chrysophrys auratus; muscle
0.59 (0.2-1.5) FW
2
Baltic herring, Clupea harengus Muscle Muscle
4.4 DW 0.48 FW
8 9
Eel, Conger sp.; muscle
8.7 DW
4
Spotted seatrout, Cynoscion nebulosus Muscle Whole; South Carolina; 1990-1993
9.5 DW 0.03-2.9 (0.0-19.0) FW
59 59 59
46 46
5 47
Mackerel scad, Decapterus macarellus; muscle
1.4 FW; 5.5 DW; 34.0 AW
1
Round scad, Decapterus punctatus; muscle
2.0 DW
4
Myctophid, Diaphus mollis; muscle
7.0 DW
4
Adriatic anchovy, Engraulis encrasicolus Liver Muscle Whole
3.9 FW 0.7 FW 1.1 FW
48 48 48
20.0-24.0 AW
12
Northern anchovy, Engraulis mordax; whole
a
(Continues)
78 Chapter 3 Table 3.7:
Cont’d
Organism
Concentration
Coney, Epinephelus fulvus; muscle
1.1-1.6 FW; 3.7-5.7 DW; 24.0-33.0 AW
1
Little tunny, Euthynnus alletteratus; muscle
1.6 DW
4
Skipjack tuna, Euthynnus pelamis Whole Muscle Fish Byproducts Gills; 8 spp. Gonad; 8 spp. Heart; 8 spp. Kidney; 8 spp. Liver 7 spp. 17 spp. 16 spp. 11 spp. 7 spp. 18 spp. 3 spp. 3 spp. 8 spp. Wales; 1989; coastal area; 4 spp. Muscle Belgium; coast; 7 spp. Australia; 12 spp. India; 6 spp.; 2003 Gulf of Bothnia, Finland; 8 spp. Taiwan; 1995-1996; 8 spp. China; 10 spp.; October 2004 Turkey; Marmara Sea; 17 spp.; 2005 13 spp. 2 spp. 2 spp. Various locations worldwide 5 spp. 63 spp. 13 spp.
Reference
30.0 AW 3.2 FW; 14.0 DW; 130.0 AW
12 1
1.10 (0.34-4.60) FW 0.6-1.8 FW 0.5-3.0 FW 0.7-6.5 FW 0.8-6.7 FW
11 13 13 13 13
1.0-2.0 FW 2.0-4.0 FW 4.0-6.0 FW 6.0-8.0 FW 8.0-10.0 FW 10.0-30.0 FW 30.0-50.0 FW 50.0-110.0 FW 1.4-22.1 FW 1.6-4.4 FW
14 14 14 14 14 14 14 14 13 50
0.44-1.18 FW 0.17-0.60 FW 1.5-2.8 FW 0.12-1.1 FW Max. 6.8 DW 0.14-0.29 FW
15 16
<1.0 FW 1.0-3.0 FW 3.1-9.5 FW
56 56 56
0.5-4.6 FW 1.3 (0.1-14.1) FW 0.1-0.2 FW
18 19 14
a
17 49 67
(Continues)
Fishes 79 Table 3.7: Organism
Cont’d
Concentration
Reference
0.2-0.3 FW 0.3-0.4 FW 0.4-0.5 FW 0.5-0.7 FW 0.7-0.9 FW 0.9-2.0 FW 0.7-8.3 DW 0.3-1.6 FW 0.9-5.2 DW 0.5-2.1 FW 0.2-0.3 FW 2.6-32.5 DW 0.51-1.56 DW 0.9-3.4 DW 1.3-2.3 DW
14 14 14 14 14 14 20 21 22 23 24 25 26 27 28
0.5 (0.2-1.1) FW 0.6-2.3 FW 1.1-2.5 DW 1.0-30.0 FW
19 13 27 13
5.6 (0.4-87.9) FW 4.4-11.2 DW
19 27
0.4-0.5 FW 0.5-0.7 FW 0.7-0.9 FW 0.9-2.0 FW 2.6-4.3 DW
14 14 14 14 28
Fishmeal; 4 spp. Presscake N-liquor Meal
11.2 DW 17.2 DW 4.1 DW
29 29 29
Mummichog, Fundulus heteroclitus Whole, body length in mm 46 61 76 88 106 118
59.0 AW 49.0 AW 46.0 AW 45.0 AW 49.0 AW 49.0 AW
30 30 30 30 30 30
54 spp. 35 spp. 22 spp. 14 spp. 14 spp. 7 spp. 10 spp. 7 spp. 11 spp. 23 spp. 3 spp. 9 spp. 7 spp. 8 spp. 4 spp. Skeleton 63 spp. 8 spp. Skin; 7 spp. Spleen; 8 spp. Viscera 63 spp. 3 spp. Whole 4 spp. 3 spp. 5 spp. 5 spp. 5 spp.
a
(Continues)
80 Chapter 3 Table 3.7: Organism Viscera Gills Muscle
Cont’d
Concentration
Reference
27.0 FW 17.0 FW 4.0 FW
31 31 31
0.52-2.30 DW 0.6 DW 5.8 DW 0.8-1.3 DW
32 33 33 33
0.4 FW 0.6 FW 1.0 FW 0.3 FW 0.7 FW 1.3 FW 0.6 FW 1.6 FW 0.6 FW 0.6 FW 0.4 FW 2.5 FW 2.4 FW 2.7 FW 2.4 FW
10 10 10 11 11 11 11 11 11 11 11 11 11 11 11
(4.0-19.0) DW (8.0-18.0) DW (1.0-3.0) DW
48 48 48
0.9-1.3 DW 6.1-8.1 DW
34 34
Guam; 10 spp.; muscle; 1998-1999; Apra Harbor vs. 3 less contaminated sites
1.6 (0.5-7.7) DW vs. <1.0 DW
54
Longspine squirrelfish, Holocentrus rufus; muscle
2.6-2.8 FW; 7.5-8.5 DW; 24.0-29.0 AW
Atlantic cod, Gadus morhua Roe Muscle Liver Gonad Muscle Inshore Coastal Offshore Muscle Tongue Roe (juvenile) Roe (mature) Milt Gills Skin Vertebrae Intestines Intestines less stomach Stomach contents Gall bladder Norway Gill Liver Muscle Goby, Gobius niger Muscle Liver
a
1
Indian Ocean; 2004; Mozambique Channel vs. Reunion Island (Continues)
Fishes 81 Table 3.7: Organism Common dolphinfish, Coryphaena hippurus Liver Muscle Kidney Skipjack, Katsuwonus pelamis Liver Muscle Kidney Yellowfin tuna, Thunnus albacares Liver Muscle Kidney Swordfish, Xiphias gladius Liver Muscle Kidney
Cont’d
Concentration
Reference
10.7 FW vs. 17.8 FW 0.14 FW vs. 0.22 FW 0.37 FW vs. 1.4 FW
62 62 62
no data vs. 31.2 FW no data vs. 0.29 FW no data vs. 2.4 FW
62 62 62
34.6 FW vs. 77.0 FW 0.24 FW vs. 0.52 FW 0.7 FW vs. 2.9 FW
62 62 62
15.7 FW vs. 17.9 FW 0.15 FW vs. 0.20 FW 1.1 FW vs. 0.5 FW
62 62 62
Myctophid, Lampanyctus pusillus; muscle
2.7-23.0 DW
4
Spot, Leiostomus xanthurus; muscle
8.4 DW
4
Yellowtail flounder, Limanda ferruginea Muscle Liver
0.3-1.2 FW 1.8-5.3 FW
35 35
1.4 FW 4.3-10.4 FW vs. 5.5-16.0 FW
36 51
Mullet, Liza saliens; Northwest Portugal; 2003-2004 Muscle Liver
<2.6 DW 262.1 (51.0-547.0) DW
66 66
Tilefish, Lophalatilus chamaeleonticeps; liver; males vs. females
210.0 (80.0-320.0) AW vs. 340.0 (140.0-590.0) AW
37
Black marlin, Makaira indica Muscle Liver
0.4 (0.3-1.2) FW 4.6 (0.5-22.0) FW
38 38
Dab, Limanda limanda Skin plus muscle Liver; German Bight; March 1990; males vs. females
a
(Continues)
82 Chapter 3 Table 3.7: Organism Blue marlin, Makaira nigricans Muscle Muscle; Japan
Cont’d
Concentration
0.3-2.6 FW; 1.5-10.0 DW; 15.0-130.0 AW 0.4 (0.1-0.7) FW
Reference
1 48
European whiting, Merlangius merlangus Muscle Liver Gut wall
0.6-0.7 FW 2.4 FW 1.4 FW
5 5 5
Dover sole, Microstomus pacificus; muscle
0.5-0.6 DW
39
Striped bass, Morone saxatilis Muscle Liver Muscle
0.35 FW 2.1-2.2 FW 2.5 DW
40 40 4
Striped mullet, Mugil cephalus Muscle Muscle Muscle
1.9 DW 0.86 (0.2-0.8) FW 1.5 (0.06-4.6) DW
4 2 58
Mullet, Mugil spp.; Mediterranean Sea; June-July 2003 Muscle Skin Gills Liver
0.84-0.93 FW 0.92-1.14 FW 2.17-2.43 FW 154.6-177.8 FW
57 57 57 57
17.6-48.1 DW
52
4.1 DW 7.6 DW
41 41
Myctophid, Notoscopelus caudispinous; muscle
3.2 DW
4
Hump rock cod, Notothenia gibberifrons; Antarctica; 1989; muscle
0.85 DW
46
Snake eel, Ophichthus sp.; muscle
1.5-2.7 DW
Red mullet (Mullidae), Mullus barbatus; Gills; France Shorthorn sculpin, Myoxocephalus scorpius Muscle Liver
a
4 (Continues)
Fishes 83 Table 3.7: Organism Atlantic thread herring, Opisthonema oglinum Muscle Whole
Cont’d
Concentration
0.8-2.7 FW; 1.3-10.0 DW; 16.0-53.0 AW 28.0 AW
Kelp bass, Paralabrax clathratus; California; Los Angeles site near effluent discharge of steam utility plants vs. Catalina Island (reference site) Eyeball Gonad Heart Liver Muscle
8.0 DW 6.0 DW 1.5 DW 5.0 DW 5.0 DW
Summer flounder, Paralichthys lethostigma Muscle Whole; South Carolina; 1990-1993
3.0 DW 1.1-1.9 (0.0-22.2) FW
European flounder, Platichthys flesus Muscle Liver Gut wall Ovary Seawater-adapted (0.003 mg Cu/L vs. freshwater-adapted (0.005 mg Cu/L) Gill Kidney Liver Muscle Gurnard, Platycephalus fuscus; muscle Winter flounder, Pleuronectes americanus Muscle Liver Texas; muscle vs. skin Plaice, Pleuronectes platessa Muscle Inshore Coastal Offshore
vs. vs. vs. vs. vs.
4.0 DW 5.0 DW 12.0 DW 6.0 DW 2.0 DW
0.3-1.3 FW 12.9-18.3 FW 2.7 FW 2.4 FW
2.7 DW vs. 6.5 DW 4.1 DW vs. 14.3 DW 15.6 DW vs. 157.8 DW 2.7 DW vs. 1.8 DW 0.47 (0.1-1.3) FW
Reference
a
1 3
48 48 48 48 48 4 47 5 5 5 5
53 53 53 53 2
0.5-1.1 FW 2.7-13.8 FW 1.0 (0.6-1.5) DW vs. 1.7 (1.2-2.1) DW
35 35 48
0.8 FW 0.8 FW 1.5 FW
10 10 10 (Continues)
84 Chapter 3 Table 3.7: Organism Muscle Muscle Liver Gut wall Blood cells Blood serum Heart Spleen Liver Kidney Gut Stomach Gill filaments Skin Muscle Bone Barbu, Polydactylus virginicus; muscle Bluefish, Pomatomus saltatrix Muscle White muscle Liver; males vs. females
Cont’d
Concentration 1.3-6.7 DW 0.8-1.1 FW 3.3 FW 2.4 FW 0.27 FW 0.57 FW 3.0 FW 3.0 FW 1.7 FW 0.67 FW 1.1 FW 0.8 FW 0.6 FW 0.6 FW 0.22 FW 1.6 FW 1.0 FW; 4.6 DW; 30.0 AW
Reference
a
42 5 5 5 43 43 43 43 43 43 43 43 43 43 43 43 1
0.67 (0.2-1.4) FW 0.4-0.6 FW 360.0 (160.0-820.0) AW vs. 680.0 (150.0-1600.0) AW
2 44 37
Sand seatrout, Cynoscion arenarius Air bladder Digestive tract Liver Muscle Skin
1.0 DW 8.9 DW 22.6 DW 1.7 DW 2.5 DW
27 27 27 27 27
Atlantic salmon, Salmo salar; marine cage farmed; Scotland; 2000 Muscle Bone Gill Gut Fat Liver Kidney Spleen Gonad Diet vs. feces
0.77 DW 9.85 DW 0.30 DW 0.08 DW 0.09 DW 4.8 DW 0.007 DW 0.02 DW 0.15 DW 8.9 DW vs. 12.9 DW
61 61 61 61 61 61 61 61 61 61 (Continues)
Fishes 85 Table 3.7:
Cont’d
Organism
Concentration
Reference
Sparid, Sargus annularis Muscle Liver
1.0-1.7 DW 22.0-35.0 DW
34 34
Red drum, Sciaenops ocellatus; whole; South Carolina; 1990-1993
0.4-9.2 (0.0-52.9) FW
47
Spanish mackerel, Scomberomorus maculatus; muscle
2.3 DW
4
0.4-8.1 FW; 1.5-12.1 DW; 22.0-57.0 AW 2.0 DW 52.0 DW
1 55 55
Windowpane, Scopthalmus aquosus Muscle Liver
0.7-1.4 FW 10.5 FW
45 45
Jack, Seriola grandis; muscle
0.59 (0.2-1.7) FW
Painted comber, Serranus cabrilla; Gills; France
5.3-27.2 DW
52
(9.8-27.7) DW
68
(2.3-8.0) DW
68
King mackerel, Scomberomerus cavalla Muscle Muscle Liver
Spain; October 2003; liver Four-spotted megrim, Lepidorhombus boscii; depth 70-120 m Pouting, Trisopterus luscus; depth 200-500 m Bandtail puffer, Sphoeroides spengleri; muscle
1.6 FW; 7.1 DW; 38.0 AW
European barracuda, Sphyraena sphyraena; muscle
4.8-23.5 DW
Sprat, Sprattus sprattus Whole Muscle
a
2
1 20
1.1 (0.5-2.0) FW 5.6 DW
5 8
Blackcheek tonguefish, Symphurus plagiusa; muscle
0.5 FW; 2.3 DW; 14.0 AW
1
Tautog, Tautoga onitis; liver; males vs. females
830.0 (430.0-1350.0) AW vs. 490.0 (280.0-3700.0) AW
Yellowfin tuna, Thunnus albacares; muscle
0.4 (0.2-0.7) FW
37 2 (Continues)
86 Chapter 3 Table 3.7:
Cont’d
Organism
Concentration
Blackfin tuna, Thunnus atlanticus; otoliths; Gulf of Mexico; 2002
0.66 DW
71
Southern bluefin tuna, Thunnus maccoyii; Australia; April 2004; muscle; wild vs. farmed
0.3 (0.3-0.4) FW vs. 0.3 (0.2-0.5) FW
65
Bluefin tuna, Thunnus thynnus; Spain Heart Intestine Kidney Liver Ovary Spleen
4.2 FW; 18.1 DW 1.4 FW; 5.8 DW 8.6 FW; 27.8 DW 74.0 FW; 245.0 DW (1.4-2.3) FW; (5.4-11.0) DW 1.2 FW; 4.4 DW
48 48 48 48 48 48
Atlantic cutlassfish, Trichiurus lepturus; muscle
0.9-2.4 FW; 4.1-11.0 DW; 34.0-93.0 AW
Turkey; northeast Mediterranean Sea coast; winter vs. summer; 2003 Striped mullet, Mugil cephalus Liver Gill Muscle Striped goatfish, Mullus barbatus Liver Gill Muscle
Reference
1
83.3 DW vs. 98.6 DW 11.2 DW vs. 15.2 DW 8.3 DW vs. 12.9 DW
60 60 60
125.4 DW vs. 175.2 DW 13.6 DW vs. 19.8 DW 10.9 DW vs. 17.5 DW
60 60 60
0.9-8.6 FW vs. 0.2 FW 1.1-30.7 FW vs. 3.6 FW
70 70
0.8 FW vs. 0.6-1.4 FW 1.9 FW vs. 12.5-21.7 FW
70 70
Red hake, Urophycis chuss Muscle Liver
0.5-0.7 FW 2.6-6.0 FW
35 35
Swordfish, Xiphias gladius; muscle
(0.3-1.4) FW
48
Turkey; 2005; Black Sea vs. Aegean Sea European anchovy, Engraulis encrasicolus Muscle Liver Picarel, Spicara smaris Muscle Liver
a
(Continues)
Fishes 87 Table 3.7:
Cont’d
Organism
Concentration
Grass goby, Zosterisessor ophiocephalus; muscle; 2005-2006; Venice Lagoon; San Giuliano vs. Sacca Sessola April July October February
1.3 DW 0.9 DW 0.7 DW 2.0 DW
vs. vs. vs. vs.
0.8 DW 0.9 DW 0.7 DW 1.4 DW
Reference
a
62 62 62 62
Values are in mg Cu/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Lowman et al., 1966; 2, Bebbington et al., 1977; 3, Ting and Devega, 1969; 4, Windom et al., 1973; 5, Wharfe and Van Den Broek, 1977; 6, Beck, 1956; 7, Bohn and McElroy, 1976; 8, Andersen et al., 1973; 9, Vanderstappen et al., 1978; 10, Portmann, 1972; 11, Julshamn et al., 1978b; 12, Goldberg, 1962; 13, Brooks and Rumsey, 1974; 14, Hall et al., 1978; 15, DeClerck et al., 1979; 16, Plaskett and Potter, 1979; 17, Miettinen and Verta, 1978; 18, Wright, 1976; 19, Won, 1973; 20, Roth and Hornung, 1977; 21, Holden and Topping, 1972; 22, Stickney et al., 1975; 23, Eustace, 1974; 24, Taylor and Bright, 1973; 25, Zingde et al., 1976; 26, Ishii et al., 1978; 27, Horowitz and Presley, 1977; 28, Sims and Presley, 1976; 29, Lunde, 1968b; 30, Eisler and LaRoche, 1972; 31, Chernoff and Dooley, 1979; 32, Julshamn and Braekkan, 1978; 33, Julshamn and Braekkan, 1975; 34, Grimanis et al., 1978; 35, Greig and Wenzloff, 1977a; 36, Newell et al., 1979; 37, Mears and Eisler, 1977; 38, Mackay et al., 1975; 39, McDermott et al., 1976; 40, Heit, 1979; 41, Bohn and Fallis, 1978; 42, Vink, 1972; 43, Harvey, 1978; 44, Cross et al., 1973; 45, Greig et al., 1977; 46, Szefer et al., 1993; 47, Mathews, 1994; 48, Jenkins, 1980a; 49, Han et al., 1998; 50, Morris et al., 1989; 51, Hylland et al., 1992; 52, Romeo et al., 1994; 53, Stagg and Shuttleworth, 1982; 54, Denton et al., 2006; 55, Ploetz et al., 2007; 56, Keskin et al., 2007; 57, Storelli et al., 2006; 58, Turkmen et al., 2006; 59, Ashraf et al., 2006; 60, Cogun et al., 2006; 61, Dean et al., 2007; 62, Kojadinovic et al., 2007; 63, Nesto et al., 2007; 64, Sankar et al., 2006; 65, Padula et al., 2008; 66, Fernandes et al., 2008b; 67, Cheung et al., 2008; 68, Fernandes et al., 2008a; 69, Roach et al., 2008; 70, Turkmen et al., 2008; 71, Arslan and Secor, 2008.
fishes tend to decrease with increasing age of the organism (Law et al., 1992; Watanabe et al., 1998). Regardless of species or tissue, copper concentrations in marine teleosts decrease with increasing age of the organism (Eisler, 1984). Smaller mummichogs contain higher concentrations of copper in whole males and females than did larger mummichogs; however, females have more copper than males (Chernoff and Dooley, 1979). Among several species of New Zealand teleosts, body length was negatively correlated with copper content of muscle (Brooks and Rumsey, 1974). Seasonally, coregonids from the Bay of Bothnia contained highest copper concentrations in liver during winter and lowest in summer and autumn (Hyvarinen and Valtonen, 1973). It is not known with certainty to what extent seasonal changes in tissue copper burdens are related to water temperature, reproductive cycle, changes in diet, and presumably other variables. In one study, copper accumulations in whole mummichogs held in seawater at 5 or 20 C were essentially the same, suggesting internal regulation (Eisler and LaRoche, 1972); a similar pattern held for mummichogs at salinities between 9 and 27 ppt (Eisler and LaRoche, 1972). Decreases in tissue copper content are also associated with spawning migrations of salmonids when entering freshwater from the sea and with reproductive cycles of Atlantic cod and other gadoids (Eisler, 1984).
88 Chapter 3 For example, copper in blood plasma of spawning sockeye salmon, O. nerka, dropped from 1.4 to 0.5 mg/L during upstream migration to less saline waters (Fletcher et al., 1975); there was, however, little change in copper content of gonad or liver during passage from salt to freshwater (Fletcher and King, 1978a). Freshwater-adapted hybrid striped bass (Morone chrysops X M. saxatilis) were comparatively sensitive to copper at sublethal (0.06 mg Cu/L; high tissue accumulations) and lethal concentrations (0.094 mg Cu/L = LC-50, 96 h). However, at 15 ppt salinity, no deaths occurred at 10.0 mg Cu/L in 96 h with no significant accumulations in liver or intestine (Bielmyer et al., 2006). A food chain transfer study with phytoplankters, clams, and plaice, P. platessa, at nominal copper concentrations in the medium of 0.01 mg Cu/L and higher, resulted in reduced fish growth; there was no copper accumulation in plaice muscle, even at ambient concentrations of 0.10 mg Cu/L (Saward et al., 1975). However, at 0.01, 0.03, and 0.10 mg Cu/L, viscera showed significant accumulations after 100 days, namely 71.0 mg Cu/kg dry weight at 0.01 mg Cu/L versus 30.0 in controls; 147.0 mg/kg at 0.03 mg Cu/L; and 567.0 mg/kg at 0.10 mg Cu/L (Saward et al., 1975). Copper uptake is dose related in the European flounder, Platichthys flesus (Stagg and Shuttleworth, 1982); flounders exposed for 42 days to seawater containing 0.17 mg Cu/L (vs. controls exposed to 0.003 mg Cu/L) had increased concentrations—in mg Cu/kg DW tissue—in gill (7.7 vs. 2.7), kidney (13.1 vs. 4.1), liver (640.2 vs. 15.6), and muscle (7.7 vs. 2.7). Adverse effects of copper to various species of teleosts are documented. For topsmelt, Atherinops affinis, sperm exposed to 0.109 mg Cu/L for 15 min resulted in a 50 percent reduction in egg fertilization (Anderson et al., 1991); 0.137 mg Cu/L was fatal to 50 percent of larvae in 48 h (McNulty et al., 1994); and 0.146 mg Cu/L to developing embryos for 48 h resulted in 50 percent abnormal development (Anderson et al., 1991). It is emphasized that the biocidal properties of copper to developing embryos of various marine teleosts, and probably other growth stages, is dependent on the free cupric ion activity and not necessarily on the concentration of dissolved copper (Engel and Sunda, 1979). For juvenile flounders, Paralichthys spp., exposure to 0.0064 mg Cu/L interferes with calcium metabolism and 0.448 mg Cu/L is fatal in 14 days (Dodoo et al., 1992). For red drum, Sciaenops ocellatus, 0.52 mg Cu/L killed 50 percent of juveniles at 25 C and 8 ppt salinity; copper toxicity to this species is greater at elevated temperatures and reduced salinities (Peppard et al., 1991). For Florida pompano, Trachinotus carolinus, copper was most toxic at lower salinities in the 10-30 ppt test range (Birdsong and Avault, 1971). For fingerlings of the striped bass, M. saxatilis, tested at 3 salinities, copper was most toxic in freshwater (LC50, 96 h = 0.05-0.10 mg Cu/L; USEPA, 1980c), less toxic at 5 ppt salinity (2.6 mg/L; Reardon and Harrell, 1990), and least toxic at 15 ppt salinity (7.8-8.0 mg Cu/L; Reardon and Harrell, 1990). Early juvenile stages of silver
Fishes 89 salmon, O. kisutch, were more sensitive to copper toxicity than later juvenile stages, and this was related to physiological changes preparatory to seaward migration (Lorz and McPherson, 1977). Copper accumulations and toxicity in mummichogs were difficult to predict under laboratory conditions when individuals were stressed by a mixture of cadmium, copper, and zinc salts, owing to significant interactions (Eisler and Gardner, 1973). Copper is positively correlated with zinc in gills of two species of fishes from the Mediterranean Sea (Romeo et al., 1994). Mixtures of copper and zinc salts are more-than-additive in toxicity to marine teleosts and other aquatic groups, producing more deaths than expected on the basis of individual components (Birge and Black, 1979; Eisler, 1993; Eisler and Gardner, 1973; Fernandez and Jones, 1990; Hodson et al., 1979). As was true for cadmium and zinc, whole body aggregates of copper from dead mummichogs were of limited worth owing to probable accumulation of this metal from the medium after death (Eisler and Gardner, 1973). In New Zealand, copper concentrations in fish muscle were positively linked to manganese and iron contents (Brooks and Rumsey, 1974), suggesting a continued research need on biological effects of metal interactions. Proposed copper criteria to protect marine teleosts include less than 0.004 mg total recoverable Cu/L, not to exceed 0.023 mg/L at any time (USEPA, 1980c); and less than 0.005 mg Cu/L at any time (Fagioli et al., 1994). To protect 90% of the species tested in Chesapeake Bay, Maryland, Hall et al. (1998) propose less than 0.0064 mg Cu/L for chronic exposures, and less than 0.016 mg Cu/L for acute exposures. However, concentrations greater than 0.05 mg Cu/L routinely occur in portions of the Chesapeake Bay (Hall et al., 1998). To protect human consumers of fish flesh in Turkey, the maximum allowable concentration at present is 20.0 mg Cu/kg FW (Keskin et al., 2007); however, this needs verification. In China, seafood products should contain less than 50.0 mg Cu/kg FW (Cheung et al., 2008).
3.15 Gallium Heit (1979) found nondetectable (<0.005 mg/kg fresh weight) concentrations of gallium in muscle and liver of striped bass, M. saxatilis. Arslan and Secor (2008), using improved instrumentation, found 0.0014 mg Ga/kg DW in otoliths from blackfin tuna, T. atlanticus, captured in the Gulf of Mexico during 2002.
3.16 Germanium Germanium burdens in filefish from a Sargassum community in the Gulf of Mexico did not exceed 0.002 mg Ge/kg fresh weight for any tissue examined (Johnson and Braman, 1975); this value was probably at or near the sensitivity of the analytical procedure.
90 Chapter 3
3.17 Gold Muscle from mackerel, Pneumatophorus japonicus, reportedly contained 0.00012 mg Au/kg on a dry weight basis (Fukai and Meinke, 1962) and 0.0026 mg/kg on an ash weight basis (Fukai and Meinke, 1959). When an aqueous solution of radioactive gold was placed directly in the gut of oyster toadfish, Opsanus tau, or spot, Leiostomus xanthurus, there was negligible transfer of the isotope to various body tissues (Duke et al., 1966a,b). Toadfish fed radiogold in an aqueous solution retained more of the isotope than did toadfish fed the same amount of radiogold sorbed onto clay particles (Duke et al., 1966a,b).
3.18 Indium Half-time retention of 114mIn by Atlantic croaker, M. undulatus, following a single intraperitoneal injection was expressed as two exponential rate functions: 224 days for the long-lived component and 40 days for the short-lived component (Baptist et al., 1970).
3.19 Iron Greatest concentrations of iron in field collections of marine fishes occurred in scales, in hematopoietic organs, and in highly vascularized tissues (Table 3.8). For example, iron is significantly more abundant in dark muscle of tunas than light muscle because dark muscle is more heavily vascularized and contains more iron-bearing respiratory pigments (Held, 1971). Iron is an essential trace metal for normal fish metabolism. In the case of artificially reared red sea bream, also known as squirefish, diets that contain less than 150.0 mg Fe/kg were associated with abnormal blood patterns (Sakamoto and Yone, 1978). Iron localizes in viscera. Viscera of the mummichog, F. heteroclitus, contributed 4% of the ash weight of the organism, but contained 43% of the total iron in whole fish, as well as 29% of the zinc, 39% of the strontium, and 41% of the copper (Eisler and LaRoche, 1972). The order of iron accumulation in the rudd, S. erythrophthalmus is kidneys > gill > spleen > liver > scales > swim bladder > muscle; in all tissues except swim bladder iron concentrations were significantly higher in males (Vorob’yev and Zaystev, 1975). In the sand sea trout the order of iron accumulation in tissues examined was liver >> digestive tract >> skin > air bladder > muscle (Horowitz and Presley, 1977). Excretion of accumulated iron seems to follow a biphasic pattern. Half-time retention of 59Fe in Atlantic croaker, M. undulatus, following intraperitoneal injection was 215 days for the long-lived component and 37 days for the short-lived component (Baptist et al., 1970). Radioiron-55 is selectively accumulated over stable iron by marine biota, including teleosts (Weimer et al., 1978). Differences in the chemical and physical forms of radioactive and stable isotopes results in greater bioavailability of 55Fe, and suggests that natural levels of stable iron in saline environments may not effectively dilute radioiron (Weimer et al., 1978).
Fishes 91 Table 3.8: Iron Concentrations in Field Collections of Fishes Organism
Concentration
Arctic cod, Boreogadus saida; liver
40.0 DW
Canned fish; Saudi Arabia; purchased locally Sardine Salmon Tuna
6.8 (2.4-12.3) FW 6.3 (2.8-9.8(FW 2.9 (1.1-5.3) FW
Atlantic cod, Gadus morhua Muscle Gutted fish less tongue Tongue Roe (juvenile) Roe (mature) Milt Gills Skin Vertebrae Intestines Stomach contents Gall bladder
2.1 FW 20.0 FW 4.0 FW 17.0 FW 9.0 FW 4.0 FW 25.0 FW 13.0 FW 16.0 FW 19.0 FW 23.0 FW 36.0 FW
2 2 2 2 2 2 2 2 2 2 2 2
24.0 (5.6-71.4) FW 18.0-148.0 FW 15.0-98.0 FW 146.0-430.0 FW 62.0-650.0 FW 110.0-1092.0 FW
2 3 3 3 3 3
3.5-22.0 FW 3.2-22.0 FW 1.6-6.8 FW 2.2-9.2 FW 6.1-23.0 DW 7.7-31.9 DW 130.0 AW 200.0 AW 2700.0 AW vs. 3100.0 AW
4 5 6 3 7 8 9 9 9
Fish Byproducts Gills; 7 spp. Gonads; 7 spp. Heart; 7 spp. Kidney; 8 spp. Liver; 8 spp. Muscle 12 spp. 17 spp. 12 spp. 8 spp. 8 spp. 8 spp. Plankton feeders Bottom feeders Pelagic feeders; white muscle vs. dark muscle Otoliths; 7 spp. Scales; 9 spp.
14.0-120.0 DW 30.0-320.0 DW
Reference
a
1
23 23 23
10 10 (Continues)
92 Chapter 3 Table 3.8: Organism Skin Plankton feeders Bottom feeders Pelagic feeders 8 spp. Spleen; 7 spp. Vertebrae 8 spp. Plankton feeders Bottom feeders Pelagic feeders Viscera Plankton feeders Bottom feeders Pelagic feeders 3 spp. Whole 2 spp.; Antarctica; 2004 11 spp. Plankton feeders Bottom feeders
Cont’d
Concentration
97.0 AW 11,000.0 AW 5100.0 AW 19.4-487.0 DW 57.0-7535.0 FW
Reference
8.0-59.0 FW 180.0 AW 1200.0 AW 5000.0 AW
9 9 9 8 3 3 3 9 9 9
75.0 AW 39,000.0 AW 3000.0 AW 381.0-467.0 DW
9 9 9 8
24.0-78.0 DW 14.0-200.0 FW 300.0 AW 10,000.0 AW
21 11 9 9
1040.0 AW 23.0 DW 4.4 DW 106.0 DW
9 12 12 12 12
Atlantic cod, Gadus morhua Roe Muscle Gonad Liver
5.3-25.9 DW 2.6 DW 5.8-8.9 DW 12.0 DW
13 14 14 14
Goby, Gobius niger Muscle Liver
15.0-25.0 DW 240.0 DW
15 15
Indian Ocean; 2004; Mozambique Channel vs. Reunion Island Common dolphinfish, Coryphaena hippurus Liver Muscle
90.7 FW vs. 61.8 FW 2.2 FW vs. 5.8 FW
27 27
Fishmeal Plankton feeders 4 spp. Presscake N-liquor Meal
a
(Continues)
Fishes 93 Table 3.8: Organism Kidney Skipjack, Katsuwonus pelamis Liver Muscle Kidney Yellowfin tuna, Thunnus albacares Liver Muscle Kidney Swordfish, Xiphias gladius Liver Muscle Kidney
Cont’d
Concentration
Reference
1598.0 FW vs. 93.3 FW
27
no data vs. 432.0 FW no data vs. 20.1 FW no data vs. 361.0 FW
27 27 27
210.0 FW vs. 221.0 FW 9.8 FW vs. 13.3 FW 693.0 vs. 280.0 FW
27 27 27
178.0 FW vs. 153.0 FW 5.3 FW vs. 5.9 FW 79.2 FW vs. 110.0 FW
27 27 27
Dab, Limanda limanda; skin plus muscle
13.0 FW
16
Striped mullet, Mugil cephalus; muscle; August 2005; Turkey
13.6 (4.3-38.2) DW
22
Goatfish, Mulloidichthys sp.; liver
370.0-1150.0 FW
16
Pandora, Pagellus erythrinus Fins Eyes Eggs Gills Brain Liver Intestine Spleen Muscle Skin Bone Whole
13.0 DW 12.0 DW 15.0 DW 12.0 DW 38.0 DW 62.0 DW 33.0 DW 180.0 DW 3.4 DW 9.2 DW 13.0 DW 5.0 DW
18 18 18 18 18 18 18 18 18 18 18 18
Bluefish, Pomatomus saltatrix; muscle
4.5-5.0 FW
19
Atlantic salmon, Salmo salar; marine farmed; diet vs. feces
420.3 DW vs. 1174.2 DW
26
23.0-37.0 DW 320.0-440.0 DW
15 15
Sparid, Sargus annularis Muscle Liver
a
Mackerel, Scomber japonicus colias; otoliths (Continues)
94 Chapter 3 Table 3.8: Organism Cyclades Islands area; Aegean Sea Age one year Age 2 years Age 3 years Age 4 years Age 5 years Age 6 years Dodecanese area; Aegean Sea Age 2 years Age 3 years Age 4 years Age 5 years Age 6 years Petalion Gulf area Age one year Age 4 years Age 5 years Age 6 years Spain; October 2003; liver Four-spotted megrim, Lepidorhombus boscii; depth 70-120 m Pouting, Trisopterus luscus; depth 200-500 m Northern puffer, Sphoeroides maculatus Liver Gill arch Gill filaments Muscle Ovary Testes Blood serum Turkey; Camlik lagoon, Mediterranean Sea; 2000-2001; winter vs. autumn European bass, Dicentrarchus labrax Gill Liver Gonad Muscle Striped mullet, Mugil cephalus Gill
Cont’d
Concentration
Reference
9.1 DW 7.0 DW 12.0 DW 3.7 DW 7.0 DW 1.0 DW
20 20 20 20 20 20
1.2 DW 2.5 DW 18.0 DW 8.4 DW 5.4 DW
20 20 20 20 20
6.5 DW 5.0 DW 1.6 DW 3.2 DW
20 20 20 20
(101.0-220.0) DW
29
(66.0-118.0) DW
29
44,000.0 AW 900.0 AW 2900.0 AW 1100.0 AW 1900.0 AW 5500.0 AW 7.8 FW
21 21 21 21 21 21 21
115.1 DW vs. 144.9 DW 141.7 DW vs. 51.4 DW 12.4 DW vs. 83.0 DW 7.2 DW vs. 3.9 DW
24 24 24 24
128.8 DW vs. 124.7 DW
24
a
(Continues)
Fishes 95 Table 3.8: Organism Liver Gonad Muscle Gilthead bream, Sparus auratus Gill Liver Gonad Muscle Turkey; NE Mediterranean Sea coast; winter vs. summer; 2003 Striped mullet, Mugil cephalus Liver Gill Muscle Striped goatfish, Mullus barbatus Liver Gill Muscle Turkey; 2005; Black Sea vs. Aegean Sea European anchovy, Engraulis encrasicolus Muscle Liver Picarel, Spicara smaris Muscle Liver Grass goby, Zosterisessor ophiocephalus; Venice lagoon, Italy; 2005-2006; muscle; San Giuliano vs. Sacca Sessola April July October February
Cont’d
Concentration
Reference
131.0 DW vs. 96.1 DW 16.7 DW vs. 94.4 DW 6.1 DW vs. 8.8 DW
24 24 24
116.3 DW vs. 114.4 DW 224.3 DW vs. 143.7 DW 18.3 DW vs. 19.5 DW 9.1 DW vs. 6.4 DW
24 24 24 24
224.3 DW vs. 284.5 DW 128.2 DW vs. 167.4 DW 29.7 DW vs. 41.2 DW
25 25 25
298.6 DW vs. 395.2 DW 150.1 DW vs. 192.5 DW 40.4 DW vs. 56.7 DW
25 25 25
35.7-44.4 FW vs. 20.1 FW 78.0-188.0 FW vs. 75.9 FW
30 30
32.2 FW vs. 14.3-169.0 FW 75.7 FW vs. 51.2-316.0 FW
30 30
4.9 DW vs. 3.4 DW 16.4 DW vs. 24.9 DW 6.9 DW vs. 6.9 DW 6.8 DW vs. 9.9 DW
28 28 28 28
a
Values are in mg Fe/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Bohn and McElroy, 1976; 2, Julshamn et al., 1978b; 3, Brooks and Rumsey, 1974; 4, Van As et al., 1973; 5, Van As et al., 1975; 6, Plaskett and Potter, 1979; 7, Ishii et al., 1978; 8, Horowitz and Presley, 1977; 9, Lowman et al., 1970; 10, Papadopoulu and Kassimati, 1977; 11, Wolfe et al., 1973; 12, Lunde, 1968a; 13, Julshamn and Braekkan, 1978; 14, Julshamn and Braekkan, 1975; 15, Grimanis et al., 1978; 16, Newell et al., 1979; 17, Beasley et al., 1972; 18, Papadopoulu et al., 1972; 19, Cross et al., 1973; 20, Papadopoulu et al., 1980; 21, Santos et al., 2006; 22, Turkmen et al., 2006; 23, Ashraf et al., 2006; 24, Dural et al., 2006; 25, Cogun et al., 2006; 26, Dean et al., 2007; 27, Kojadinovic et al., 2007; 28, Nesto et al., 2007; 29, Fernandes et al., 2008a; 30, Turkmen et al., 2008.
96 Chapter 3
3.20 Lead Elevated lead concentrations in marine teleosts and other aquatic organisms are reported in proximity to mining activities, areas where lead arsenate pesticides are used, metal finishing facilities, organolead industries, and areas of lead aerosol fallout (Gnassia-Barelli and Romeo, 1993; Eisler, 2000d). Geographical variations in lead concentrations among California tidepool fishes reflect contamination of the intertidal zone by atmospheric lead pollution (Alley et al., 1974). For example, the inner city of the Los Angeles metropolitan area contains almost 35 times more atmospheric lead than remote mountainous areas of California and almost 9 times more atmospheric lead than rural areas (Alley et al., 1974). Lead concentrations in spotted wolffish, Anarhichas minor, near a lead mine and an ore concentration plant in West Greenland increased significantly since mining started; major sites of accumulation were liver and kidney, with smaller wolffish containing more lead than larger ones per unit weight (Bollingberg and Johansen, 1979). Fish meal contained up to 5.3 mg Pb/kg FW; about 90% of the total was tetraalkyllead (Table 3.9). Maximum values recorded for other tissues, in mg Pb/kg FW, were 9.7 in spleen, 4.8 in vertebrae, and 6.3 in viscera (Table 3.9). Mean lead concentrations, in mg Pb/kg fresh weight, in most fish species collected from U.S. coastal waters ranged from 0.3 to 0.7 in muscle and 0.2 to 0.6 in liver; no pattern was observed for mean lead burdens in whole fish although these tended to show higher concentrations than muscle and liver, possibly due to lead accumulations in hard tissues, such as bone (Hall et al., 1978). Similar observations were recorded by other investigators at various collection areas (Table 3.9). Comparatively, high concentrations of radiolead-210 are reported in lantern fishes (Nriagu, 1978), but the significance of this observation is not clear. The ability of tunas to accumulate lead from seawater is reported; concentration factors for whole tunas were about 100, being highest in liver and lowest in muscle (Heyraud and Cherry, 1979). The effects of canning on lead content of tuna muscle have been underestimated for decades, according to Settle and Patterson (1980). This was allegedly due to analytical errors which resulted in reduced lead concentrations in canned tuna by factors up to 10,000 times. The magnitude of this pollution effect partially accounts for the difference between the lead concentration in diets of present-day Americans, estimated at 0.2 mg/kg fresh weight, and those of prehistoric peoples, estimated to be less than 0.002 mg/kg fresh weight. It also explains, in part, why mean lead concentrations in bone of Americans have increased up to 500 times when compared to humans living in a lead-unpolluted environment 1800 years ago (Settle and Patterson, 1980). However, the link between lead content in canned tuna and adverse impacts on human health remain unproven at this time. Inhibition of blood delta amino-levulinic acid dehydratase (ALAD) activity—a key enzyme in hemoglobin production—after exposure to lead is documented in many species
Fishes 97 Table 3.9: Lead Concentrations in Field Collections of Fishes Organism
Concentration
Surf bream, Acanthopagrus australis; muscle
0.66 (0.3-1.7) FW
Alaska, Adak Island; June 2004 Flathead sole, Hippoglossoides elassodon Kidney Liver Muscle Great sculpin, Myoxocephalus polyacanthocephalus Kidney Liver Muscle Spotted wolffish, Anarhichas minor Muscle Kidney Liver Stomach Bone Heart Mucous Skin European eel, Anguilla anguilla Germany; 1991 Bile Intestine Liver Adult parasites; whole; Paratenuisentis sp. (acanthocephalan) vs. Anguillicola sp. (nematode) England; 1983-1987 Liver Muscle
Reference 1
1.24 FW 0.12 FW 0.05 FW
49 49 49
0.05 FW 0.03 FW 0.01 FW
49 49 49
0.02-0.12 FW 0.05-1.04 FW 0.04-1.77 FW 9.3 FW 1.3 FW 1.4 FW 0.5 FW 0.3 FW
a
2 2 2 2 2 2 2 2
0.03 FW 0.09 FW 0.18 (0.12-0.28) FW 3.7 (2.1-5.6) FW vs. 0.02 FW
38 38 38 38
0.6 (0.04-3.8) FW 0.06 FW; max. 0.8 FW
39 39
Halfbridled goby, Arenigobius frenatus; Australia; industrialized site vs. reference estuary Gonad Muscle
0.06 DW vs. 0.04 DW 0.71 DW vs. 0.03 DW
59 59
Kob, Argyrosomus hololepidotus; muscle
0.54 (0.1-1.6) FW
1
Australian salmon, Arripis trutta; muscle
0.67 (0.3-1.3) FW
1 (Continues)
98 Chapter 3 Table 3.9:
Cont’d
Organism
Concentration
Canned fish; Saudi Arabia; purchased locally Sardine Salmon Tuna
0.84 (0.13-2.0) FW 0.31 (0.03-1.2) FW 0.23 (0.03-0.51) FW
Squirefish, Chrysophrys auratus; muscle
0.65 (0.2-1.5) FW
1
Fivebeard rockling, Ciliata mustela; whole minus viscera
8.1-24.5 DW
3
Wooly sculpin, Clinocottus analis; muscle; California Los Angeles area San Simeon area Catalina Island area
4.9 FW 2.7 FW 0.6 FW
4 4 4
Baltic herring, Clupea harengus Muscle Muscle
7.0 DW 0.31 FW
5 6
Twoband bream, Diplodus vulgaris; muscle
0.3 DW
7
Graysby, Epinephelus cruentatus; muscle
0.09 FW
8
Nassau grouper, Epinephelus striatus; muscle
0.09 FW
8
Grouper, Epinephelus sp.; muscle
0.04-0.3 DW
7
0.20 (0.02-1.54) FW
9
Fish Byproducts Gills Gulf of Mexico; 14 spp.; 2005-2006 7 spp. Gonads; 7 spp. Heart; 7 spp. Kidney 8 spp. 4 spp.; Indian Ocean; 2004 Liver 5 spp. 20 spp. 33 spp. 13 spp. 6 spp. 5 spp.
Reference
a
46 46 46
<0.001-2.9 DW 0.2-4.0 FW 0.3-2.6 FW 0.3-0.7 FW
50 10 10 10
0.3-2.4 FW 0.01-0.15 FW
10 51
<0.1-0.2 FW 0.2-0.4 FW 0.4-0.6 FW 0.6-0.8 FW 0.8-1.0 FW 1.0-3.0 FW
11 11 11 11 11 11 (Continues)
Fishes 99 Table 3.9: Organism 8 spp. Gulf of Mexico; 14 spp.; 2005-2006 Indian Ocean; 4 spp.; 2004 Meal Total lead Tetralkyllead Muscle 4 spp.; Indian Ocean; 2004 10 spp.; Mumbai, India; 2004-2005 10 spp.; China; October 2004 5 spp. 92 spp. 51 spp. 7 spp. 4 spp. 8 spp. 63 spp. 4 spp. 8 spp. 11 spp. 7 spp. Gulf of Mexico; 14 spp.; 2005-2006 West Norway coast Spain; Rio Tinto Estuary Spain; Tarragona coast; commercial species Malaysia; 6 spp. Australia; 12 spp. Finland; Gulf of Bothnia; 8 spp. Belgium; coast; 7 spp. Turkey; Marmara Sea; 17 spp.; 2005 10 spp. 7 spp. Skin; 8 spp. Spleen; 7 spp. Vertebrae 7 spp. 63 spp. Viscera 63 spp. 3 spp.
Cont’d
Concentration
Reference
0.3-3.0 FW <0.001-2.1 DW 0.02-0.22 FW
10 50 51
5.34 FW 4.79 FW
24 24
<0.04 FW 0.08 FW; max. 0.26 FW 0.05-0.24 FW 0.1-0.3 FW 0.3-0.5 FW 0.5-0.7 FW 0.7-1.0 FW 1.0-3.0 FW 0.16-0.87 FW 1.09 (0.06-3.40) FW <0.2-1 DW 0.3-1.1 DW 0.01-0.16 DW <0.5-1.0 FW <0.001-4.9 DW Max. 14.0 DW Max. 7.0 DW Max. 1.1 FW
51 54 57 11 11 11 11 11 10 12 13 14 15 16 50 17 18 41
0.21-0.32 FW 0.35-0.57 FW 0.03-0.25 FW 0.28-0.45 FW
19 20 21 22
<0.1 FW 0.1-0.3 FW 3.3-8.0 DW 0.4-9.7 FW
43 43 14 10
0.3-4.1 FW 0.95 (0.12-4.84) FW
10 12
1.58 (0.12-6.26) FW 2.6-5.5 DW
12 14
a
(Continues)
100 Chapter 3 Table 3.9: Organism
Cont’d
Concentration
Reference
0.1-0.4 FW 0.5-0.8 FW 0.8-1.0 FW 1.0-3.0 FW 17.6-25.8 DW <0.3-2.3 DW Max. 0.15 FW
11 11 11 11 23 13 40
Max. 0.64 DW 0.09 DW 0.03-0.06 DW 0.43 DW 0.06-0.25 FW 0.17-3.3 FW <0.50 FW 0.04 FW 0.15 FW 0.05-0.08 FW 0.11 FW 0.08 FW 0.03 FW 0.03 FW
25 25 25 25 26 26 27 9 9 9 9 9 9 9
0.39 FW vs.0.52 FW 0.037 FW vs. 0.125 FW
24 24
Muscle
<0.2-0.8 FW
28
Liver
<0.2-1.2 FW
28
Dab, Limanda limanda; skin plus muscle
0.3-0.9 FW
29
Striped seasnail, Liparis liparis; whole minus viscera
12.4-31.8 DW
Whole 2 spp. 3 spp. 2 spp. 10 spp. 6 spp. 6 spp. 4 spp; Greenland; 1978-1993 Atlantic cod, Gadus morhua Roe Muscle Gonad Liver Muscle Liver Muscle Muscle Tongue Gonads Gills Skin Vertebrae Intestines Liver homogenate; frozen vs. fresh Total lead Tetraalkyllead
a
Yellowtail flounder, Limanda ferruginea
Mullet, Liza saliens; Portugal; 2003-2004 Muscle Liver Mackerel; muscle; total lead vs. tetraalkyllead
3
<0.019 DW <0.019 DW
56 56
0.14 FW vs. 0.054 FW
24 (Continues)
Fishes 101 Table 3.9:
Cont’d
Organism
Concentration
Black marlin, Makaira indica Muscle Liver
0.6 (0.1-0.9) FW 0.7 (0.4-1.1) FW
30 30
0.05 (0.04-0.08) FW 0.09 (0.06-0.11) FW
53 53
0.10 (0.07-0.18) FW 0.21 (0.11-0.39) FW
53 53
Mediterranean Sea; summer 2003 Swordfish, Xiphias gladius Muscle Liver Bluefin tuna, Thunnus thynnus Muscle Liver European hake, Merluccius merluccius; muscle Mexico; Gulf of California; 1999-2000; muscle Striped mullet, Mugil cephalus Colorado snapper, Lutjanus colorado Orangemouth corvina, Cynoscion xanthulus
2.6-4.8 DW
Reference
a
7
1.0 DW 1.3 DW 2.6 DW
60 60 60
Dover sole, Microstomus pacificus; muscle
<1.1-1.3 DW
31
Striped bass, Morone saxatilis Muscle Liver
0.5 FW 0.8-1.0 FW
22 22
Mullet, Mugil spp.; Mediterranean Sea; June-July 2003 Muscle Liver Gills Skin
0.04-0.05 FW 0.28-0.30 FW 2.33-2.49 FW 0.10-0.18 FW
44 44 44 44
Striped mullet, Mugil cephalus Muscle Muscle
0.71 (0.2-4.1) FW 1.68 (0.09-4.3) DW
1 45
Striped goatfish, Mullus barbatus; muscle
0.4-3.4 DW
7
Scamp, Mycteroperca phenax; muscle
0.29 FW
8
Tiger grouper, Mycteroperca tigris; muscle
0.06 FW
8
Shorthorn sculpin, Myoxocephalus scorpius; liver
0.3 DW
33 (Continues)
102 Chapter 3 Table 3.9:
Cont’d
Organism
Concentration
Pandora, Pagellus erythrinus Gills Brain Spleen Other tissues
5.1 DW 24.0 DW 29.0 DW <3.0 DW
European flounder, Platichthys flesus; whole; Barnstaple Bay vs. Oldbury-on-Severn Age 2+ Age 3+ Age 4+ Age 5+
14.1 DW 16.0 DW 18.0 DW 19.1 DW
Gurnard, Platycephalus fuscus; muscle
0.56 (0.1-1.5) FW
Plaice, Pleuronectes platessa; muscle; inshore vs. offshore
0.54 FW vs. <0.50 FW
Bluefish, Pomatomus saltatrix; muscle
0.65 (0.3-1.4) FW
Atlantic salmon, Salmo salar; marinereared; diet vs. feces
0.72 DW vs. 3.6 DW
Sardine, Sardinella aurita; muscle
0.3-0.7 DW
7
Lizardfish, Saurida undosquamis; muscle
0.3-3.2 DW
7
King mackerel, Scomberomorus cavalla; Gulf of Mexico Muscle Liver
1.8 DW 1.0 DW
42 42
Windowpane, Scopthalmus aquosus Muscle Liver
<0.5-1.0 FW <0.5-1.7 FW
35 35
Amberjack, Seriola grandis; muscle
0.54 (0.2-0.8) FW
1
(0.002-0.011) DW
58
(0.002-0.050) DW
58
Spain; October 2003; liver Four-spotted megrim, Lepidorhombus boscii; depth 80-120 m Pouting, Trisopterus luscus; 200-500 m depth
Reference
a
34 34 34 34
vs. vs. vs. vs.
20.5 DW 24.0 DW 26.2 DW 28.2 DW
23 23 23 23 1 27 1 48
Marbled spinefoot, Siganus rivulatus; muscle
0.3 DW
7
Common sole, Solea solea; muscle
0.3 DW
7 (Continues)
Fishes 103 Table 3.9:
Cont’d
Organism
Concentration
European barracuda, Sphyraena sphyraena; muscle
1.8-5.2 DW
7
Sprat, Sprattus sprattus; muscle
8.2 DW
5
Albacore, Thunnus alalunga Pectoral fin Epidermis Scales Dermis Gill filaments Muscle Muscle; canned in oil Cannery A Cannery B
Reference
0.45 FW 1.4-1.7 FW 0.06 FW 0.01 FW 0.014 FW 0.0002 FW
36 36 36 36 36 36
0.10 FW 0.93 FW
36 36
0.45 (0.1-0.8) FW 1.6 (0.1-2.0) FW; 4.7 (4.0-5.0) DW
1 37
Blackfin tuna, Thunnus atlanticus; otoliths; Gulf of Mexico 2002
0.029 DW
62
Southern bluefin tuna, Thunnus maccoyii; Australia; April 2004; muscle; wild vs. farmed
<0.01 FW vs. <0.01 FW
55
11.2 DW vs. 16.8 DW 18.7 DW vs. 26.7 DW 5.8 DW vs. 7.8 DW
47 47 47
16.8 DW vs. 23.6 DW 21.8 DW vs. 32.5 DW 6.1 DW vs. 9.4 DW
47 47 47
0.1-0.9 FW vs. 0.4 FW 0.5-3.4 FW vs 0.4 FW
61 61
0.15 FW vs. 0.4 FW 1.0 FW vs. 0.3-2.5 FW
61 61
Yellowfin tuna, Thunnus albacares Muscle Muscle
Turkey; NE Mediterranean Sea coast; winter vs. summer; 2003 Striped mullet, Mugil cephalus Liver Gill Muscle Striped goatfish, Mullus barbatus Liver Gill Muscle Turkey; 2006; Black Sea vs. Aegean Sea European anchovy, Engraulis encrasicolus Muscle Liver Picarel, Spicara smaris Muscle Liver
a
(Continues)
104 Chapter 3 Table 3.9:
Cont’d
Organism
Concentration
Goatfish, Upeneus sp.; muscle
0.3-5.3 DW
7
White hake, Urophycis tenuis Muscle Liver
<0.3-0.8 FW 1.1 FW
28 28
Grass goby, Zosterisessor ophiocephalus; 2005-2006; Venice lagoon, Italy; muscle; San Giuliano vs. Sacca Sessola April July October February
0.76 DW 0.04 DW 0.03 DW 0.13 DW
vs. vs. vs. vs.
0.76 DW 0.12 DW 0.03 DW 0.08 DW
Reference
a
52 52 52 52
Values are in mg Pb/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Bebbington et al., 1977; 2, Bollingberg and Johansen, 1979; 3, Badsha and Sainsbury, 1978; 4, Alley et al., 1974; 5, Andersen et al., 1973; 6, Vanderstappen et al., 1978; 7, Roth and Hornung, 1977; 8, Taylor and Bright, 1973; 9, Julshamn et al., 1978b; 10, Brooks and Rumsey, 1974; 11, Hall et al., 1978; 12, Won, 1973; 13, Sims and Presley, 1976; 14, Horowitz and Presley, 1977; 15, Stickney et al., 1975; 16, Holden and Topping, 1972; 17, Stenner and Nickless, 1974; 18, Stenner and Nickless, 1975; 19, Babji et al., 1979; 20, Plaskett and Potter, 1979; 21, Miettinen and Verta, 1978; 22, DeClerck et al., 1979; 23, Hardisty et al., 1974; 24, Sirota and Uthe, 1977; 25, Julshamn and Braekkan, 1978; 26, Havre et al., 1972; 27, Portmann, 1972; 28, Greig and Wenzloff, 1977b; 29, Newell et al., 1979; 30, Mackay et al., 1975; 31, McDermott et al., 1976; 32, Heit, 1979; 33, Bohn and Fallis, 1978; 34, Papadopoulu et al., 1972; 35, Greig et al., 1977; 36, Chow et al., 1974; 37, Lowman et al., 1966; 38, Sures et al., 1994; 39, Barak and Mason, 1990; 40, Dietz et al., 1996; 41; Schuhmacher et al., 1990; 42, Ploetz et al., 2007; 43, Keskin et al., 2007; 44, Storelli et al., 2006; 45, Turkmen et al., 2006; 46, Ashraf et al., 2006; 47, Cogun et al., 2006; 48, Dean et al., 2007; 49, Burger et al., 2007a; 50, Ruelas-Inzunza et al., 2007; 51, Kojadinovic et al., 2007; 52, Nesto et al., 2007; 53, Storelli et al., 2005; 54, Mishra et al., 2007; 55, Padula et al., 2008; 56, Fernandes et al., 2008b; 57, Cheung et al., 2008; 58, Fernandes et al., 2008a; 59, Roach et al., 2008; 60, Ruelas-Inzunza and Paez-Osuna, 2008; 61, Turkmen et al., 2008; 62, Arslan and Secor, 2008.
of marine teleosts (Eisler, 2000d). Mullet, Mugil auratus, held in 0.5 mg Pb/L for 82 days had up to 40% inhibition in ALAD activity (Krajnovic-Ozretic and Ozretic, 1980). Mixtures of lead with salts of cadmium, copper, or mercury produced additional inhibition. Zinc, however, proved effective in restoring ALAD activity of the lead-exposed mullets. Distinct tissue-specific accumulation rates for lead were found in the longjaw mudsucker, Gillichthys mirabilis: spleen, gill, fin, and intestine accumulated the greatest amount of lead, and liver and muscle the least (Somero et al., 1977a). The rate of lead accumulation in Gillichthys was highest at relatively high temperatures and low salinities. Rapid loss of lead from tissues of lead-exposed fish was observed only for gills, fins, and intestine. These tissues all had an outer or inner covering of mucous. Somero et al. (1977b) suggest that lead turnover in these mucous-covered tissues is a result of lead complexing with mucous and subsequent loss of this complex when the mucous layer is sloughed. In spleen and bone, lead levels continued to rise in fish returned to lead-free seawater from lead-spiked media. Juveniles of Atlantic croaker, Micropogonias undulatus, fed lead chloride
Fishes 105 in the diet equivalent to 12.0 mg Pb/kg body weight daily for 6 weeks had significant increases in the glutathione contents of liver and intestine that plateaued after 2 weeks and significant increases in brain and kidney glutathione after 6 weeks (Thomas and Juedes, 1992). Maximum tissue residues, in mg Pb/kg fresh weight, after 6 weeks were 50.0 in intestine, 20.0 in kidney, 2.0 in liver, and <1.0 in brain (Thomas and Juedes, 1992). Genderrelated differences in uptake, retention, and accumulation of lead are documented for Atlantic croakers, with males having higher accumulations (Burger et al., 2007b). The presence of tetraalkyllead compounds in fish tissues was demonstrated by Sirota and Uthe (1977). Marchetti (1978) showed that tetraethyllead is 1.5-4.5 times more toxic to marine teleosts than tetramethyllead compounds, and this is reflected in the comparatively rapid uptake of tetraethyllead compounds. Sirota and Uthe (1977) aver that the Canadian permissible concentration of 10.0 mg total Pb/kg fresh weight in fishery products should be reexamined for three reasons: organolead compounds are more toxic than ionic forms; methylation of ionic lead in vivo or in stored tissue is possible; and liver enzyme systems exist that can convert tetraethyllead to the more toxic triethyl species. Different chemical forms of lead vary significantly in lethality to plaice, P. platessa (Maddock and Taylor, 1980). Concentrations fatal to 50% of palice adults in 96 h were 0.05 mg/L for tetramethyllead (bioconcentration factor (BCF) of 60), 0.23 mg/L for tetraethyllead (BCF of 130), 1.7 mg/L for triethyllead (BCF of 2), 24.6 mg/L for trimethyllead (BCF of 1), 75.0 mg/L for diethyllead, 180.0 mg/L for inorganic ionic lead, and 300.0 mg/L for dimethyllead (Maddock and Taylor, 1980). Proposed lead criteria to protect marine life in California, in mg total Pb/L, are 0.002 for a 6-month median, <0.008 for a daily maximum, and <0.02 for an instantaneous maximum (USPHS, 1993b). Proposed nationwide total lead criteria for seawater (USEPA, 1985a; USPHS, 1993b) include 0.0056 mg/L (4-day average, not to be exceeded more than once every 3 years) and 0.140 mg/L (1-h average, not to be exceeded more than once every 3 years). To protect human consumers of fish muscle in Turkey, the maximum allowable concentration is 1.0 mg Pb/kg FW; for China, it is 0.5 mg Pb/kg FW (Cheung et al., 2008); and for the European Union, it is 0.2 mg Pb/kg FW (Keskin et al., 2007; Storelli et al., 2006), or 0.4 mg Pb/kg FW (Kojadinovic et al., 2007).
3.21 Lithium Blood of albacore tuna collected in the northern Pacific Ocean about 1500 km off California reportedly contained 231.5 mg Li/kg fresh weight (Hansen et al., 1978). Lithium concentrations in otoliths from juvenile English sole, Pleuronectes vetulus, and speckled sanddab, C. stigmaeus, collected along the central California coast during 1999-2000 were significantly higher in offshore sites than estuaries; the reverse was true for strontium (Brown, 2006).
106 Chapter 3
3.22 Manganese Manganese concentrations seldom exceed 0.5 mg Mn/kg fresh weight in muscle, 2.0 in liver, or 9.0 in whole fish, although concentrations up to 37.0 mg Mn/kg FW are recorded (Table 3.10). Manganese concentrations in tissues increase with increasing size of the fish (Burger et al., 2007a). Hard tissues, such as vertebrae, whole fish, and skin with scales had consistently higher accumulations than soft tissues (Table 3.10). Petkevich (1967) generalized that bony tissues of plankton-feeding fish concentrated trace metals to a greater extent than benthos-feeders; this was especially pronounced for manganese, and also nickel, chromium, vanadium, titanium, tin, lead, and strontium. Seasonal changes in manganese content of tuna liver is reported; burdens were significantly lower in summer, and higher in samples collected offshore than nearshore samples (Pearcy and Osterberg, 1968). Table 3.10: Manganese Concentrations in Field Collections of Fishes Organism Alaska, Adak Island; June 2004 Flathead sole, Hippoglossoides elassodon Kidney Liver Muscle Great sculpin, Myoxocephalus polyacanthocephalus Kidney Liver Muscle Baltic herring, Clupea harengus; whole Fish Byproducts Gills; 7 spp. Gonads; 7 spp. Heart; 7 spp. Kidney 8 spp. 4 spp.; Indian Ocean; 2004 Liver 4 spp. 21 spp. 24 spp. 33 spp. 8 spp. 4 spp.; Indian Ocean; 2004
Concentration
Reference
0.34 FW 0.89 FW 0.36 FW
24 24 24
0.41FW 0.98 FW 0.47 FW
24 24 24
0.45 DW
27
1.3 (0.14-8.5) FW 0.6-11.0 FW 0.2-3.3 FW 0.1-0.8 FW
a
1 2 2 2
0.2-1.4 FW 0.18-0.65 FW
2 25
0.2-0.5 FW 0.5-0.7 FW 0.7-0.9 FW 0.9-2.0 FW 0.9-6.7 FW 1.0-1.9 FW
3 3 3 3 2 25 (Continues)
Fishes 107 Table 3.10: Organism Muscle 17 spp. 102 spp. 24 spp. 9 spp. 3 spp. 4 spp. 12 spp. 10 spp. 8 spp. 16 spp. 8 spp. 8 spp. 23 spp. 8 spp. 6 spp.; India; 2003 10 spp.; Mumbai, India; 2004-2005 4 spp.; Indian Ocean; 2004 Pelagic feeders; white muscle vs. dark muscle Bottom feeders Skin Pelagic feeders Plankton feeders Bottom feeders 8 spp. Spleen; 7 spp. Vertebrae 8 spp. Pelagic feeders Plankton feeders Bottom feeders Viscera 4 spp. 3 spp. Pelagic feeders Bottom feeders Whole 2 spp. 3 spp. 9 spp. 2 spp.
Cont’d
Concentration
Reference
<0.1 FW 0.1-0.2 FW 0.2-0.3 FW 0.3-0.5 FW 0.5-0.7 FW 0.7-2.0 FW 0.18-0.44 FW 0.07-0.58 FW 3.7-26.3 DW 0.14-0.91 FW 0.18-1.15 FW 0.31-0.79 DW <0.5-1.3 FW 0.4-2.5 DW 0.4-3.1 FW 1.7 FW; max. 4.8 FW 0.05-0.08 FW 28.0 AW vs. 12.0 AW
3 3 3 3 3 3 4 5 6 7 2 8 9 10 28 29 25 11
16.0 AW
11
72.0 AW 36.0 AW 69.0 AW 5.1-25.6 DW 0.1-3.5 FW
11 11 11 10 2
1.0-27.4 FW 45.0 AW 73.0 AW 170.0 AW
2 11 11 11
140.0 AW 6.4-17.1 DW 22.0 AW 470.0 AW
12 10 11 11
0.2-0.5 FW 0.5-0.7 FW 0.7-2.0 FW 2.0-6.0 FW
a
3 3 3 3 (Continues)
108 Chapter 3 Table 3.10: Cont’d Organism 1 sp. 11 spp. Bottom feeders
Concentration
Reference
9.5 FW 0.0-8.8 FW 170.0 AW
3 13 11
Mummichog, Fundulus heteroclitus Viscera Gills Muscle
37.0 FW 20.0 FW 9.0 FW
14 14 14
Atlantic cod, Gadus morhua Muscle Gonad Liver Roe Muscle Tongue Gonads Gills Skin Vertebrae Intestines Stomach contents Gall bladder
0.2 DW 0.4-0.8 DW 1.1 DW 0.13-1.10 DW 0.12 FW 0.53 FW 0.40-0.82 FW 1.2 FW 1.0 FW 1.2 FW 0.61 FW 1.5 FW 2.3 FW
15 15 15 16 1 1 1 1 1 1 1 1 1
Yellowtail flounder, Limanda ferruginea Muscle Liver
0.1-1.8 FW 0.1-2.5 FW
17 17
Dab, Limanda limanda; skin plus muscle
0.4-0.6 FW
18
Striped mullet, Mugil cephalus; muscle; August 2005; Turkey
2.1 (0.48-6.01) DW
22
Pandora, Pagellus erythrinus Fins Eyes Eggs Brain Spleen Skin Whole
25.0 DW 1.6 DW 4.2 DW 11.0 DW 59.0 DW 7.2 DW 15.0 DW
19 19 19 19 19 19 19
Winter flounder, Pleuronectes americanus Liver Muscle
<0.1-2.5 FW 0.25-0.35 FW
17 17
Bluefish, Pomatomus saltatrix; muscle
0.20-0.28 FW
20
a
(Continues)
Fishes 109 Table 3.10:
Cont’d
Organism
Concentration
Atlantic salmon, Salmo salar; marine farmed; diet vs. feces
46.7 DW vs. 102.7 DW
Sardine, Sardinops ocellata; muscle
1.1 FW
Windowpane, Scopthalmus aquosus Muscle Liver
0.18-0.40 FW 1.7-2.5 FW
21 21
Blackfin tuna, Thunnus atlanticus; otoliths
0.54 DW
31
0.7-2.8 FW vs, 0.6 FW 1.1-9.7 FW vs. 1.2 FW
30 30
0.4 FW vs. 0.2-0.7 FW 0.7 FW vs. 1.8-4.5 FW
30 30
0.3-0.4 FW 0.6-1.2 FW
17 17
13.6 DW vs. 14.4 DW 1.8 DW vs. 4.4 DW 1.5 DW vs. 1.4 DW 3.9 DW vs. 3.5 DW
26 26 26 26
Turkey; 2005; Black Sea vs. Aegean Sea European anchovy, Engraulis encrasicolus Muscle Liver Picarel, Spicara smaris Muscle Liver Red hake, Urophycis chuss Muscle Liver Grass goby, Zosterisessor ophiocephalus; muscle; 2005-2006; Venice lagoon, Italy; San Giuliano vs. Sacca Sessola April July October February
Reference
a
23 5
Values are in mg Mn/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Julshamn et al., 1978a,b; 2, Brooks and Rumsey, 1974; 3, Hall et al., 1978; 4, Plaskett and Potter, 1979; 5, Van As et al., 1973; 6, Zingde et al., 1976; 7, Van As et al., 1975; 8, Ishii et al., 1978; 9, Eustace, 1974; 10, Horowitz and Presley, 1977; 11, Lowman et al., 1970; 12, Goldberg, 1962; 13, Wolfe et al., 1973; 14, Chernoff and Dooley, 1979; 15, Julshamn and Braekkan, 1975; 16, Julshamn and Braekkan, 1978; 17, Greig and Wenzloff, 1977a; 18, Newell et al., 1979; 19, Papadopoulu et al., 1972; 20, Cross et al., 1973; 21, Greig et al., 1977; 22, Turkmen et al., 2006; 23, Dean et al., 2007; 24, Burger et al., 2007a; 25, Kojadinovic et al., 2007; 26, Nesto et al., 2007; 27, Zumholz et al., 2006; 28, Sankar et al., 2006; 29, Mishra et al., 2007; 30, Turkmen et al., 2008; 31, Arslan and Secor, 2008.
Julshamn and Braekkan (1978) suggest that manganese is essential to normal development of embryos of the Atlantic cod, G. morhua, because manganese concentrations increased significantly during development. A similar case is made for larvae of plaice, P. platessa (Pentreath, 1976c). However, larger mummichogs, F. heteroclitus, had lower manganese concentrations than did smaller whole fish, with no differences attributable to gender (Chernoff and Dooley, 1979).
110 Chapter 3 Diet seems to be the major route of manganese accumulation in teleosts. Direct accumulation from water plays only a minor role relative to food in the metabolism of manganese by plaice (Jefferies and Hewett, 1971; Pentreath, 1973). Adult plaice fed 54 Mn-labeled nereid worms exchanged half the accumulated isotope with seawater in 35 days (Pentreath, 1976c).
3.23 Mercury Data on mercury accumulations in marine fishes are especially abundant and only a few of the more representative observations are shown in Table 3.11. Geographic areas of concern where mercury concentrations in marine fish muscle exceed existing regulations for human consumers include Italy, Spain, Taiwan, Florida, and Oregon (Table 3.11). In general, concentrations of mercury in feral populations of marine vertebrates—including elasmobranchs, fishes, birds, and mammals—are clearly related to the age of the organism. Regardless of species or tissue, all data for mercury and marine vertebrates show increasing concentrations with increasing age of the organism (Eisler, 1984). Factors that may account, in part, for this trend include differential uptake at various life stages, reproductive cycle, diet, general health, bioavailability of different chemical species, mercury interactions with other metals, metallothioneins, critical body parts, and anthropogenic influences (Eisler, 1984). Mercury is one of the most toxic metals known to marine teleosts. Concentrations of inorganic mercury lethal to 50 percent of sensitive species of teleosts (haddock, spot, tidewater silverside, mummichog, etc.) in 96 h range from 0.036 to 0.098 mg/L (Eisler and Hennekey, 1977; Mayer, 1987; U.S. Environmental Protection Agency, 1980a). At lower sublethal methylmercury concentrations, effects include reduced insemination success of eggs (Khan and Weis, 1993), altered blood chemistry (Dawson, 1982), decreased respiration (Armstrong, 1979), high accumulations (Choi and Cech, 1998), and impaired ability to avoid predators or to locate, capture, and consume prey (Weis and Weis, 1995a,b). Mercurytolerant strains of F. heteroclitus are reported, but reasons to account for adaptation to both methylmercury and inorganic mercury remain unclear (Weis, 1984). Long-term dietary exposure of teleosts to methylmercury is associated with impaired coordination, diminished appetite, inhibited swimming activity, starvation, and sometimes death (as quoted in Eisler, 2006). One of the earliest and most extensively documented cases of mercury poisoning occurred in the 1950s at Minamata Bay, in southwestern Kyushu, Japan, especially among fishermen and their families (as quoted in Eisler, 2006). Deaths and congenital birth defects in humans were attributed to long-term ingestion of marine fish and shellfish highly contaminated with methylmercury compounds. An abnormal mercury content of greater than 30.0 mg/kg fresh weight was measured in edible tissues of fish from the Bay (Table 14.11). The source of the mercury was in waste discharged from an acetaldehyde plant that used inorganic mercury as
Fishes 111 Table 3.11: Mercury Concentrations in Field Collections of Fishes Organism
Concentration
Surf bream, Acanthopagrus australis Muscle Muscle
0.23 (0.03-0.81) FW 0.03-0.67 FW
White sturgeon, Acipenser transmontanus; Columbia River estuary; 2000-2001 Liver Gonad Muscle (cheek)
0.08 FW 0.02 FW 0.17 FW
135 135 135
0.15 FW 0.24 FW 0.28 FW
138 138 138
0.11 FW 0.29 FW 0.32 FW
138 138 138
0.042-0.092 FW; max. 0.247 FW 0.099 FW; max. 0.493 FW
131 131
0.114 FW; max. 0.552 FW 0.130 FW; max. 0.535 FW 0.158 FW; max. 0.928 FW 0.167 FW; max. 0.506 FW 0.173 FW; max. 0.868 FW 0.277 FW; max. 0.517 FW 0.281 FW; max. 0.944 FW 0.336 FW max. 1.096 FW
131 131 131 131 131 131 131 131
Alaska, Adak Island; June 2004 Flathead sole, Hippoglossoides elassodon Kidney Liver Muscle Great sculpin, Myoxocephalus polyacanthocephalus Kidney Liver Muscle Aleutian Islands, Alaska; 2003-2005; edible portions 6 spp. Rock greenling, Hexagrammos lagocephalus Dolly varden, Salvelinus malma Red Irish lord, Hemilepidotus hemilepidotus Pacific halibut, Hippoglossus stenolepis Black rockfish, Sebastes melanops Pacific cod, Gadus macrocephalus Flathead sole, Hippoglossoides elassodon Yellow Irish lord, Hemilepidotus jordani Great sculpin, Myoxocephalus polyacanthocephalus European eel, Anguilla anguilla; muscle Sanlucar, Spain; total body length <20 cm 20-30 cm 30-40 cm 40-50 cm 50-60 cm 60-70 cm
0.12 FW 0.19 FW 0.25 FW 0.33 FW 0.32 FW 0.36 FW
Reference
a
1 2
3 3 3 3 3 3 (Continues)
112 Chapter 3 Table 3.11: Cont’d Organism Cadiz, Spain; total body length 20-30 cm 30-40 cm 40-50 cm 50-60 cm 60-70 cm Muscle Bay of Biscay, France; 2005 Methylmercury Inorganic mercury Total mercury East Anglia, UK; River estuary; total mercury Grunt, Anisotremus interruptus Muscle Liver Sablefish, Anoplopoma fimbria Muscle Decapitated, eviscerated Bering Sea SE Alaska Washington State Oregon California Northern Central Southern Antarctica; Terra Nova Bay; 1989-1991; 4 spp. Muscle Liver Kidney Gills Gonads Blue hake, Antimora rostrata; NW Atlantic Ocean; collected from depth or 2500 m; muscle; museum samples; 1880 vs. 1970
Concentration
0.11 FW 0.16 FW 0.23 FW 0.24 FW 0.36 FW 0.23 DW 0.27 (0.12-0.45) FW 0.04 (0.003-0.13) FW 0.31 (0.16-0.48) FW 0.26 FW
Reference
a
3 3 3 3 3 4 117 117 117 118
0.12 FW 0.26 FW
5 5
0.06-0.18 FW
7
0.04 FW 0.28 FW 0.40 FW 0.40 FW
6 6 6 6
0.26 FW 0.47 FW 0.60 FW
6 6 6
0.3-0.8 (0.01-1.8) DW 0.2-0.5 (0.1-0.8) DW 0.3-1.0 (0.1-2.6) DW 0.06-0.4 (0.01-1.0) DW 0.2-0.3 (0.01-0.4) DW
63 63 63 63 63
0.51 FW vs. 0.34 FW
81
(Continues)
Fishes 113 Table 3.11:
Cont’d
Organism
Concentration
Reference
Halfbridled goby, Arenigobius frenatus; Australia; industrialized site vs. reference estuary Gonad Muscle
<0.007 DW vs. <0.007 DW 0.028 DW vs. 0.048 DW
155 155
Argentina; Bahia Blanca estuary; 1982-2003; 3 spp.; muscle vs. liver 1982-1988 1989-2000 2001-2003
0.22-0.39 FW vs. 0.19-0.32 FW 0.20-0.24 FW vs. 0.09-0.28 FW 0.12 FW vs. 0.07 FW
145 145 145
Hardhead catfish, Arius felis; muscle
1.8 DW
9
Australian salmon, Arripis trutta; muscle
0.28 (0.14-0.62) FW
1
Arrowtooth flounder, Atheresthes stomias; muscle
0.01-0.33 FW
7
Frigate tuna, Auxis thazard thazard; Ghana, Gulf of Guinea; April 2004; 0.6-2.0 kg body weight Muscle Liver Duodenum Heart Intestine Gonads Stomach Gills
0.108 (0.044-0.201) FW 0.107 FW 0.086 FW 0.073 FW 0.050 FW 0.044 FW 0.044 FW 0.031 FW
127 127 127 127 127 127 127 127
Azores; 8 spp.; 1997; from 5-1200 m depth Muscle; total mercury vs. methylmercury 4 spp. 4 spp. Diet; total mercury
0.59-0.92 DW vs. 0.52-0.79 DW 1.23-3.70 DW vs. 1.01-2.96 DW 0.08-0.32 DW
121 121 121
Baltic Sea coast; 1993-2002 Baltic herring, Clupea harengus Muscle vs. liver Ovary vs. testes Lumpfish, Cyclopterus sp. Muscle vs. liver Ovary vs. testes
0.10 FW vs. 0.12 FW 0.03 FW vs. 0.03 FW
83 83
0.02 FW vs. 0.03 FW 0.01 FW vs. 0.01 FW
83 83
a
(Continues)
114 Chapter 3 Table 3.11: Cont’d Organism European smelt, Osmerus eperlanus Muscle vs. liver Ovary vs. testes Four-horned sculpin, Myoxocephalus quadricornis Muscle vs. liver Ovary vs. testes European flounder, Platichthys flesus Muscle vs. liver Ovary vs. testes Eelpout, Zoarces viviparus Muscle vs. liver Ovary vs. testes
Concentration
Reference
0.12 FW vs. 0.05 FW 0.07 FW vs. 0.03 FW
83 83
0.23 FW vs. 0.11 FW 0.06 FW vs. 0.05 FW
83 83
0.08 FW vs. 0.04 FW 0.03 FW vs. 0.03 FW
83 83
0.11 FW vs. 0.09 FW 0.03 FW vs. 0.06 FW
83 83
Glacier lanternfish, Benthosema glaciale; whole; North Atlantic Ocean; 1930s-1990s; museum specimens; max. concentrations 1930s 1940s 1950s 1960s 1970s 1980s 1990s
0.23 DW 0.48 DW 0.21 DW 0.25 DW 0.18 DW 0.21 DW 0.20 DW
134 134 134 134 134 134 134
Sparid, Boops salpa; mercury-contaminated area Muscle Liver Kidney
0.11 FW 3.81 FW 4.00 FW
10 10 10
0.27-0.50 DW
11
Cusk, Brosme brosme Muscle Liver Gills Kidneys
0.09-0.54 FW 0.02-0.62 FW 0.02-0.14 FW 0.02-0.33 FW
12 12 12 12
Snook, Centropomus sp.; muscle
0.02-0.61 FW
5
Atlantic menhaden, Brevoortia tyrannus; muscle and organs
a
(Continues)
Fishes 115 Table 3.11: Organism Squirefish, Chrysophrys auratus Muscle Muscle; Australia; Sydney vs. Nowra; 1976 Total mercury
Cont’d
Concentration
0.33 (0.06-1.94) FW
Reference
1
0.32 (0.08-1.7) FW vs. 0.11 (0.01-0.78) FW 0.3 (0.25-0.32) FW vs. 0.1 (0.06-0.11) FW
84
0.13 FW 0.30 FW 0.24 FW 0.35 FW 0.40 FW 1.00 FW
13 13 13 13 13 13
Baltic herring, Clupea harengus Muscle Muscle
0.04-0.30 FW 0.04 FW
14 15
Sardine, Clupea sardina; canned Italy Spain
0.22 FW 0.17 FW
16 16
Pacific saury, Cololabis saira Muscle Liver
0.09-0.21 FW 0.08-0.13 FW
20 20
Wrasse, Coris julis; from mercurycontaminated area Muscle Liver Kidney
2.77 FW 16.12 FW 12.23 FW
10 10 10
0.17-0.31 FW
21
Methylmercury Muscle; as function of total fish length <30 cm 30-34.5 cm 35-39.5 cm 40-44.5 cm 45-49.5 cm >50 cm
Dolphin (fish), Coryphaena hippurus; muscle Mojarra, Diapterus sp. Muscle Liver Seabass, Dicentrarchus labrax Rio de Aveiro, Portugal; 1997-1998; muscle Mercury-contaminated coastal lagoon; Portugal; 1988
0.06 FW 0.07 FW 0.2-1.3 FW
a
84
5 5 116
(Continues)
116 Chapter 3 Table 3.11: Cont’d Organism Muscle Liver Gills Stomach contents Blacktail, Diplodus sargus; muscle Mercury-contaminated area vs. reference site Haifa Bay, Israel vs. reference site; 1990
Concentration 1.1 FW 2.0 FW 0.71 FW 0.43 FW
Reference 136 136 136 136
0.3-1.7 FW vs. 0.04-0.64 FW
85
0.6 FW vs. 0.15 FW
86
1.90 FW 17.00 FW 29.80 FW
10 10 10
0.42 FW 0.073 FW vs. 0.052 FW
16 8
England; near River Tyne; 1992 Muscle; 5 spp. Stomach contents; 3 spp.
0.03-0.14 (0.006-0.43) FW 0.01-0.04 FW; max. 0.11 FW
87 87
Petrale sole, Eopsetta jordani; muscle
0.05-0.32 FW
7
Graysby, Epinephelus cruentatus; muscle
0.41-0.60 FW
22
Nassau grouper, Epinephelus striatus; muscle
0.15-0.81 FW
22
Skipjack tuna, Euthynnus pelamis Canned Muscle Muscle Liver Spleen Stomach Pyloric caeca
0.27 FW 0.11-0.64 FW 0.20 FW 0.18 FW 0.21 FW 0.11 FW 0.13 FW
16 59 20 20 20 20 20
Fish Brain, 13 spp. Total mercury Inorganic mercury
0.66 FW 0.015 FW
23 23
Twoband bream, Diplodus vulgaris; mercury-contaminated area Muscle Liver Kidney Anchovy, Engraulis sp. Canned Canned, Turkey; total mercury vs. methylmercury
a
(Continues)
Fishes 117 Table 3.11: Organism Brain, 1 sp.; total mercury vs. inorganic mercury Byproducts Dried fish; total mercury vs. methylmercury Gastric content, 13 spp.; total mercury vs. inorganic mercury Gonads, 13 spp. Kidneys, 13 spp.; total mercury vs. inorganic mercury Liver 31 pp. 17 spp. 6 spp. 5 spp. 1 sp. 3 spp. 4 spp. 8 spp. 4 spp. 2 spp. 1 sp. 13 spp. 41 spp. 13 spp. Muscle Alaska; 24 spp; 1971-2004 17 spp. 3 spp. 3 spp. 1 spp. Bangladesh; 3 spp.; 1993-1994; total mercury vs. methylmercury China; 10 spp.; October 2004 Florida (USA); southern estuaries; 1995; 7 spp.; total mercury vs. methylmercury Gulf of Oman; May-June 2004; 12 spp.; total mercury vs. methylmercury Mumbai, India; 2004-2005 Total mercury
Cont’d
Concentration
Reference
7.36 FW vs. not detected
23
0.05 (0.01-0.19) FW 0.17-7.39 DW vs. 0.07-6.37 DW
24 25
0.72 FW vs. 0.03 FW
23
not detected 0.72 FW vs. 0.25 FW
26 23
<0.1 FW 0.1-0.2 FW 0.2-0.3 FW 0.3-0.4 FW 0.4-0.5 FW 0.5-0.7 FW 0.7-0.9 FW 0.9-2.0 FW 2.0-4.0 FW 5.0-8.0 FW 10.0-20.0 FW 0.86 FW <0.05-0.42 FW Max. 0.2 FW
27 27 27 27 27 27 27 27 27 27 27 23 28 26
0.01-0.10 FW 0.11-0.20 FW 0.21-0.30 FW 0.32 FW 0.03-0.12 (0.01-0.37) FW vs. 0.01-0.10 (0.001-0.34) FW 0.06-0.51 FW 1.4 (0.1-10.1) DW; 0.31 (0.03-2.2) FW vs. 1.05 (0.06-4.5) DW; 0.23 (0.01-1.0) FW 0.003-0.31 FW vs. 0.0001-0.22 FW
130 130 130 130 144
0.015 FW; 95th percentile 0.019 FW
150
a
153 95
149
(Continues)
118 Chapter 3 Table 3.11: Cont’d Organism Methylmercury New Jersey; Newark Bay North Sea; 1997-1999; 12 spp. Total mercury Methylmercury Oregon; Willamette Basin; 20022003 Piscivores Omnivores Malaysia; 6 spp. New Guinea; 6 spp. Belgium; coast; 5 spp. Persian Gulf; 5 spp. Gulf of Thailand; total mercury vs. organomercury Gulf of Bothnia, Finland Ghana; Gulf of Guinea; 20 spp.; November 2003-February 2004 India; 4 spp.; 2003 Indian Ocean; 13 spp. Scotland; Firth of Clyde; 1991-1992; 5 spp. Turkey; coast, 7 spp. France; coast, 18 spp. Korea; 40 spp. Australia; 6 spp. Turkey; Marmara Sea; 17 spp.; 2005 7 spp. 8 spp. 2 spp. Various locations, worldwide 5 spp. 45 spp. 49 spp. 18 spp. 15 spp. 1 sp. 8 spp. 3 spp. 4 spp. 3 spp.
Concentration
Reference
0.013 FW; 95th percentile 0.022 FW 0.1-1.4 DW
150
0.045-0.172 FW 0.043-0.160 FW
156 156
1.63 FW 0.38 FW 0.08-0.10 FW 0.02-0.19 FW 0.07-0.18 FW 0.04-0.56 FW 0.063 (0.010-0.650) FW vs. 0.035 (0.004-0.280) FW 0.01-1.2 FW Means 0.009-0.160 FW; maxima 0.01-0.19 FW 0.3-0.5 FW 0.074-0.160 FW 0.01-0.07 (0.01-0.25) FW 0.002-0.130 FW 0.08-0.37 FW 0.17 (0.02-0.58) FW 0.03-0.75 FW
a
97
99 99 29 30 31 32 33 34 92 146 26 93 35 36 38 40
<0.05 FW 0.24-0.43 FW 0.51-0.55 FW
124 124 124
0.06-0.34 DW <0.1 FW 0.1-0.2 FW 0.2-0.3 FW 0.3-0.4 FW 0.4-0.5 FW 0.5-0.6 FW 0.6-0.7 FW 0.7-0.8 FW 0.8-0.9 FW
122 27 27 27 27 27 27 27 27 27 (Continues)
Fishes 119 Table 3.11: Organism 8 spp. 4 spp. 1 sp. 5 spp. 30 spp. 22 spp. 16 spp. 8 spp. 7 spp. 12 spp. 7 spp. 13 spp. 20 spp. 41 spp. 11 spp. 4 spp. Protein concentrate; 7 spp. Skeleton; Korea Viscera Korea Japan, Minamata Bay; 3 spp. Whole 13 spp. 13 spp. 3 spp. 1 sp. 3 spp. 3 spp. 6 spp. 2 spp.; Antarctica; 2004
Cont’d
Concentration
Reference
1.0-2.0 FW 2.0-3.0 FW 4.0-5.0 FW <0.3 FW 0.069 FW 0.1-4.5 DW 0.02-0.65 FW 0.02-0.65 FW 0.22-0.73 FW 0.05-0.34 FW 0.09-1.0 FW 0.20 FW 0.1-1.0 DW <0.05-0.35 FW 0.10-2.74 DW 0.10-0.25 FW 0.34-0.90 DW 0.14 (0.04-0.27) FW
27 27 27 41 42 43 44 45 46 3 47 23 9 28 48 49 50 38
0.16 (0.07-0.31) FW 18.0-23.0 DW
38 37
Max. 0.06 FW <0.1 FW 0.1-0.2 FW 0.2-0.3 FW 0.07-0.22 FW 0.32-0.71 FW 0.00-0.61 FW 0.0160-0.0163 DW
a
26 27 27 27 47 16 51 120
Fishmeal Presscake N-liquor Meal
0.41 DW <0.01 DW 0.40 DW
52 52 52
Mummichog, Fundulus heteroclitus; muscle
0.001-0.009 FW
53
Gadoid, Gadus callarias; muscle
0.24 DW
Atlantic cod, Gadus morhua Muscle North Sea and Baltic Sea North Atlantic Ocean
0.02-0.88 FW 0.02-0.32 FW
4
17 17 (Continues)
120 Chapter 3 Table 3.11: Cont’d Organism Inshore waters North Sea Offshore waters Liver Roe Liver oil Cleithrum bones; recent vs. 100-year old museum specimen Ghana; Gulf of Guinea; May 2004; muscle; tunas; total mercury vs. methylmercury Yellowfin tuna, Thunnus albacares Frigate, Auxis thazard thazard
Concentration 0.26 FW 0.10 FW 0.09 FW 0.01-0.09 FW 0.02-0.04 DW 0.12-0.15 FW 0.064 DW vs. 0.056 DW
0.06 (0.04-0.09) FW vs. 0.06 FW 0.11 (0.05-0.20) FW vs. 0.11 (0.05-0.19) FW
Reference 19 19 19 17 54 55 56
123 123
Chub, Girella tricuspidata; muscle
0.02-0.12 FW
57
Rex sole, Glyptocephalus zachirus; muscle
0.05-0.24 FW
7
Goby, Gobius niger Muscle Liver
0.08-0.33 DW 0.38-0.72 DW
58 58
Greenland; 1983-1991; 10 spp. Liver Muscle
<0.01-0.6 FW 0.01-0.3 FW
95 95
(0.07-0.19) DW 0.13-0.9 (0.06-1.8) DW
96 96
(0.24-1.1) DW
96
0.3 (0.2-0.5) DW 0.25-1.2 DW; max. 2.5 DW
96 96
Greenland; Barents Sea; summers 1991-1992; muscle; demersal species Atlantic cod, Gadus morhua Longrough dab, Hippoglossoides platessoides Atlantic halibut, Hippoglossus hippoglossus Plaice, Pleuronectes platessa Greenland halibut, Reinhardtius hippoglossoides Gulf of Mexico; summer 2002-2003; muscle; total mercury; 9 spp. Blackfin tuna, Thunnus atlanticus Blue marlin, Makaira nigricans Cobia, Rachycentron canadum Dolphinfish, Coryphaena hippurus Greater amberjack, Seriola dumerili King mackerel, Scomberomerus cavalla
0.63 (0.0-1.4) FW 10.5 (4.95-18.72) FW 0.89 (0.2-2.4) FW 0.07 (0.01-0.49) FW 0.6 (0.24-1.1) FW 0.96 (0.37-1.46) FW
a
147 147 147 147 147 147 (Continues)
Fishes 121 Table 3.11: Organism Little tunny, Euthynnus alletteratus Wahoo, Acanthocybium solandri Yellowfin tuna, Thunnus albacares Sardine, Harengus sp.; Turkey; canned; total mercury vs. methylmercury
Cont’d
Concentration 1.08 (0.24-2.52) FW 0.78 (0.01-3.31) FW 0.18 (0.07-0.87) FW 0.063 FW vs. 0.045 FW
Rosefish, Helicolenus dactylopterus Muscle Liver Gills Kidney
0.07-0.12 FW Max. 0.41 FW Max. 0.05 FW 0.06-0.17 FW
Pacific halibut, Hippoglossus stenolepsis; muscle Bering Sea Gulf of Alaska Southeast Alaska British Columbia Washington-Oregon
0.15 FW 0.20 FW 0.26 FW 0.32 FW 0.45 FW
Indian Ocean; Mozambique Channel vs. Reunion Island; muscle Swordfish, Xiphias gladius Yellowfin tuna, Thunnus albacares Skipjack, Katsuwonus pelamis Common dolphinfish, Coryphaena hippurus Wahoo, Acanthocybium solandri Indian Ocean; 2004; Mozambique Channel vs. Reunion Island Common dolphinfish Liver Muscle Kidney Skipjack Liver Muscle Kidney Yellowfin tuna Liver Muscle Kidney
Reference
a
147 147 147 8
12 12 12 12
6 6 6 6 6
1.61 DW vs. 3.97 DW; 0.38 FW vs. 1.24 FW 0.51 DW vs. 0.70 DW; 0.13 FW vs. 0.21 FW no data vs. 0.67 DW; 0.13 FW 0.98 DW vs. 0.20 DW; 0.17 FW vs. 0.01 FW no data vs. 0.13 DW; 0.10 FW
129
0.16 FW vs. 0.06 FW 0.17 FW vs. 0.01 FW 0.11 FW vs. 0.04 FW
139 139 139
no data vs. 0.17 FW no data vs. 0.19 FW no data vs. 0.20 FW
139 139 139
0.19 FW vs. 1.05 FW 0.13 FW vs. 0.30 FW 0.45 FW vs. 0.39 FW
139 139 139
129 129 129 129
(Continues)
122 Chapter 3 Table 3.11: Cont’d Organism Swordfish Liver Muscle Kidney
Concentration
Reference
1.5 FW vs. 2.6 FW 0.38 FW vs. 1.2 FW 0.7 FW vs. 0.95 FW
139 139 139
Japan; Minamata Bay; muscle 1950s; 13 spp. 1960 1961 1963 1965 1968 1969 1966-1972 1974
Max. 309.1 DW 10.0-30.0 FW 23.0 DW 3.5 DW 11.5 DW 0.3 FW Max. 50.0 DW <0.6 DW Max. 0.6 DW
37, 39 110 111 111 111 111 112 111 113
Wrasse, Labrus sp.; mercury-contaminated area Muscle Liver Kidney
1.89 FW 7.31 FW 8.14 FW
10 10 10
Yellowtail flounder, Limanda ferruginea Muscle Liver
0.06-0.13 FW 0.08-0.17 FW
60 60
Dab, Limanda limanda; skin plus muscle
0.06-0.07 FW
61
Mackerel; canned; New Jersey grocery; 1998-2003
0.03 FW
a
141
Black marlin, Makaira indica Muscle Liver Muscle
7.3 (0.5-16.5) FW 10.4 (0.3-63.0) FW 5.7 FW
62 62 30
Marlin, Makaira sp.; muscle
4.8 (0.35-14.0) FW
21
Blue marlin, Makaira nigricans Liver Total mercury Organomercury Total mercury Methylmercury Inorganic mercury
6.3 FW 0.2 FW 13.4 FW 0.2 FW 11.0 FW
64 64 65 65 65 (Continues)
Fishes 123 Table 3.11: Organism Muscle Total mercury Organomercury Total mercury Methylmercury Inorganic mercury Central nervous system tissue; total mercury vs. organomercury Gonad Total mercury Organomercury Total mercury Methylmercury Spleen Total mercury Methylmercury Inorganic mercury Gill Total mercury Methylmercury Stomach Total mercury Methylmercury Blood Total mercury Methylmercury Marine mammal food items; whole; Atlantic Ocean vs. Mediterranean Sea Adriatic anchovy, Engraulis encrasicolus European hake, Merluccius merluccius Blue whiting, Micromesistias poutassau European pilchard, Sardina pilchardus Mediterranean Sea; summer 2003 Swordfish, Xiphias gladius Muscle Liver Bluefin tuna, Thunnus thynnus Muscle Liver
Cont’d
Concentration
Reference
2.0 FW 0.4 FW 4.3 FW 0.4 FW 2.3 FW 0.5 FW vs. 0.09 FW
64 65 65 65 65 64
0.3 FW 0.07 FW 0.7 FW 0.2 FW
64 64 65 65
8.5 FW 0.2 FW 7.3 FW
65 65 65
0.3 FW 0.1 FW
65 65
1.1 FW 0.1 FW
65 65
0.3 FW 0.1 FW
65 65
0.028 (0.026-0.032) FW vs. 0.050 (0.043-0.061) FW 0.033 FW vs. 0.045 FW 0.016 FW vs. 0.021 FW 0.023 (0.019-0.034) FW vs. 0.095 (0.067-0.127) FW
a
115 115 115 115
0.07 (0.02-0.15) FW 0.19 (0.10-0.37) FW
140 140
0.20 (0.13-0.35) FW 0.39 (0.27-0.60) FW
140 140 (Continues)
124 Chapter 3 Table 3.11: Cont’d Organism
Concentration
Tarpon, Megalops atlantica; Puerto Rico estuaries; 1988; muscle
0.09-0.24 FW
European hake, Merluccius merluccius; muscle; 47 cm total length hake vs. <31 cm total length
0.88 FW vs. 0.10-0.26 FW
Pacific hake, Merluccius productus; muscle
0.06-0.18 FW
7
0.01-0.29 FW
7
Dover sole, Microstomus pacificus Muscle California Palos Verdes area Muscle Liver Kidney Gill Catalina Island area Muscle Liver Kidney Gill Bight area; liver European bass, Morone labrax; muscle Striped bass, Morone saxatilis Muscle Liver Muscle; fish weight <3.2 kg 3.2-5.7 kg >5.7 kg Muscle; Chesapeake Bay, Maryland; 2002-2004 Total mercury Fish <5.0 kg FW Fish 5.0-17.5 kg Methylmercury Fish <5.0 kg FW Fish 5.0-17.5 kg Otoliths; Chesapeake Bay; 2003 Total mercury Methylmercury
Reference 100 44
0.052 DW 0.099 DW 0.041 DW 0.024 DW
66 66 66 66
0.157 DW 0.141 DW 0.030 DW 0.019 DW 0.11-0.19 DW
66 66 66 66 67
1.8 DW
a
4
0.35 FW 0.52-0.55 FW
68 68
<0.5 FW 0.5 FW >0.5 FW
69 69 69
<0.25 FW >0.25-0.8 FW
132 132
<0.15 FW Max. 0.5 FW
132 132
0.1-0.55 FW Usually <0.3 FW
132 132 (Continues)
Fishes 125 Table 3.11: Organism Muscle; total mercury; coast Atlantic Ocean Gulf of Mexico Pacific Ocean Lisa, Mugil brasiliensis; Argentina La Plata river estuary; 1990s; muscle vs. liver Mar Chiquita Lagoon; muscle; 19821990 vs. 1994-2000 Striped mullet, Mugil cephalus Muscle Muscle Liver Mercury-contaminated area Muscle Liver Kidney
Cont’d
Concentration
Reference
0.15 FW; max. 0.84 FW 0.21 FW; max. 0.4 FW 0.46 FW; max. 0.9 FW
133 133 133
0.4 (0.3-0.5) FW vs. 0.53 (0.25-0.79) FW 0.33 (0.1-0.43) FW vs. 0.29 (0.07-0.37) FW
145
0.03 FW 0.03-0.07 FW 0.01-0.09 FW 0.39 FW 5.36 FW 4.71 FW
a
145
1 5 5 10 10 10
White mullet, Mugil curema; whole
0.04 (0.01-0.10) FW
5
Mullet, Mugil liza; Argentina Muscle Liver
0.40 FW 0.53 FW
125 125
Mullet, Mugil spp.; Mediterranean Sea; June-July 2003 Muscle Liver Gills Skin
0.04-0.05 FW 0.11-0.14 FW 0.04-0.05 FW 0.05-0.05 FW
126 126 126 126
Goatfish, Mullus surmuletus; mercurycontaminated area Muscle Liver Kidney
1.65 FW 2.42 FW 2.09 FW
10 10 10
Scamp, Mycteroperca phenax; muscle
0.13-0.50 FW
22
Tiger grouper, Mycteroperca tigris; muscle
0.17-0.38 FW
22
Fourhorn sculpin, Myoxocephalus quadricornis; muscle
<0.47 FW
70 (Continues)
126 Chapter 3 Table 3.11: Cont’d Organism
Concentration
Reference
Shorthorn sculpin, Myoxocephalus scorpius; liver; Greenland Northwest Greenland 1987 1995 2002 2004 Central West Greenland; total length <27 cm vs. >27 cm 1994 1999 2000 2001 2002 2003 2004
0.054 FW 0.056 FW 0.093 FW 0.065 FW
114 114 114 114
0.029 FW vs. 0.026 FW 0.010 FW vs. 0.017 FW 0.011 FW vs. 0.015 FW 0.022 FW vs. 0.061 FW 0.015 FW vs. 0.016 FW no data vs. 0.044 FW no data vs. 0.016 FW
114 114 114 114 114 114 114
Holocentrid, Myripristis arayomus; muscle
0.10-0.43 FW
21
0.1 (0.006-0.03) FW 0.05 (0.002-0.14) FW 0.25 (0.2-0.3) FW 0.3 (0.009-0.76) FW; 32% >0.3 FW; 2% >0.5 FW 0.08 (0.02-0.2) FW 0.6 (0.08-2.5) FW; 62% >0.3 FW; 42% >0.5 FW; 20% >0.75 FW 0.03 (0.006-0.1) FW
98 98 98 98
New Jersey, USA; 57 supermarkets/fish stalls; July-October 2003; fillets Croakers (Sciaenidae) Flounders; several species Atlantic cod, Gadus morhua Bluefish, Pomatomus saltatrix Porgies (Sparidae) Tuna, mainly yellowfin tuna, Thunnus albacares Whiting, Merlangius merlangius
a
98 98
98
Lingcod, Ophiodon elongatus; muscle
0.06-0.73 FW
7
Oyster toadfish, Opsanus tau; muscle
2.9 DW
9
Pandora, Pagellus erythrinus Bone Liver Skin Muscle
0.22 DW 1.3-1.4 DW 0.23 DW 0.9-1.1 DW
73 73 73 73
Tuna, Parathunnus spp. Muscle Canned
0.03-0.23 FW 0.65 FW
72 16 (Continues)
Fishes 127 Table 3.11:
Cont’d
Organism
Concentration
Reference
English sole, Parophrys vetulus; muscle
0.06-0.21 FW
7
Sea lamprey, Petromyzon marinus; Massachusetts; 2003-2004; whole Eggs Ammocoetes Adults
0.084 FW 0.492 FW 0.083-0.942 FW
European flounder, Platichthys flesus Muscle Muscle Muscle; Irish Sea Northern areas Central areas Southern areas
0.15 FW 0.52 FW 0.03-0.13 (0.008-0.39) DW 0.16-0.48 (0.06-1.2) DW 0.16-0.40 (0.04-2.0) DW
a
148 148 148 4 32 101 101 101
Starry flounder, Platichthys stellatus; muscle
0.08-0.50 FW
7
Sand flathead, Platycephalus fuscus; muscle; Derwent estuary, Tasmania vs. other Tasmanian locations
0.44-1.06 FW vs. 0.05-0.36 FW
Gurnard, Platycephalus fuscus; muscle
0.13 (0.07-0.22) FW
Winter flounder, Pleuronectes americanus Muscle Liver
0.06-0.09 FW <0.03-0.17 FW
60 60
0.25 FW 0.08 FW 0.05 FW
19 19 19
74
1
Plaice, Pleuronectes platessa; muscle Coastal North Sea Distant waters Liverpool Bay; United Kingdom; sludge disposal ground Early 1970s (2.7 tons of mercury yearly) 1991 (0.16 tons of mercury yearly)
0.5 FW
102
0.2 FW
102
Pollock, Pollachius virens; muscle
0.06-0.50 FW
18
Bluefish, Pomatomus saltatrix; muscle Fish weight <2.4 kg Fish weight 2.4-5.6 kg Fish weight >5.6 kg Total mercury
<0.5 FW 0.5 FW >0.5 FW 0.21 (0.05-0.42) FW
69 69 69 1 (Continues)
128 Chapter 3 Table 3.11: Cont’d Organism Methylmercury Inorganic mercury
Concentration
Reference
0.20 (0.05-0.39) FW 0.012 (0.00-<0.03) FW
1 1
Sand sole, Psettichthys melanostichus; muscle
0.03-0.16 FW
7
Greenland halibut, Reinhardtius hippoglossoides; Barents Sea; January 2006; muscle; fish weight 0.8-3.0 kg vs. 3.0-7.1 kg
0.10 (0.02-0.42) FW vs. 0.39 (0.06-1.1) FW
128
0.042 FW 0.07 FW 0.08 FW 0.02 FW 0.05 FW
119 119 119 119 119
0.016 FW 0.033 FW 0.033 FW 0.024 FW 0.008 FW
119 119 119 119 119
0.024 FW 0.044 FW 0.044 FW 0.035 FW 0.005 FW
119 119 119 119 119
0.017 FW 0.04 FW 0.048 FW 0.028 FW 0.008 FW
119 119 119 119 119
Atlantic salmon; Salmo salar; saltwater rearing Age 10 months; weight 0.1 kg; transferred to marine aquaculture Facility Muscle Liver Kidney Gill Diet Age 15 months; weight 0.7 kg Muscle Liver Kidney Gill Diet Age 21 months; weight 1.6 kg Muscle Liver Kidney Gill Diet Age 27 months; weight 3.56 kg (marketable) Muscle Liver Kidney Gill Diet Spanish sardine, Sardinella aurita; edible portions
0.01-0.12 FW
a
44 (Continues)
Fishes 129 Table 3.11:
Cont’d
Organism
Concentration
Clupeid, Sardinops melanosticta Muscle Liver
Max. 0.12 FW 0.07-0.12 FW
20 20
Sparid, Sargus annularis Muscle Liver
0.24-1.90 DW 0.66-1.10 DW
58 58
Lizardfish, Saurida undosquamis; muscle
0.12-0.51 FW
44
Croaker, Sciaena antarctica; muscle
0.24 (0.06-0.82) FW
Red drum, Sciaenops ocellatus; Florida; muscle All fish Legal-sized fish (<689 mm total length or <565 mm standard length)
0.02-3.6 FW 0.17-0.30 (0.02-2.7) FW
Reference
a
1
103 103
Chub mackerel, Scomber japonicus Muscle Liver Spleen
0.06-0.15 FW 0.08-0.29 FW 0.13-0.16 FW
20 20 20
Atlantic mackerel, Scomber scombrus Muscle Canned
0.09 DW 0.26 FW
4 16
Windowpane, Scopthalmus aquosus Muscle Liver
0.12-0.27 FW 0.13-0.30 FW
12 12
Scorpionfish, Scorpaena porcus; mercurycontaminated area Muscle Liver Kidney
2.61 FW 4.26 FW 4.89 FW
10 10 10
Scotland; 1982-1987; sludge disposal site vs. reference site; muscle Atlantic cod, Gadus morhua European flounder, Platichthys flesus Plaice, Pleuronectes stellatus Whiting, Merlangius merlangius
0.04-0.2 FW vs. 0.05-0.07 FW 0.09-0.55 FW vs. 0.1-0.13 FW 0.006-0.2 FW vs. 0.03-0.1 FW 0.03-0.1 FW vs. 0.06-0.08 FW
Rockfish, Sebastes inermis Muscle Liver Spleen
0.02-0.03 FW 0.04-0.05 FW 0.01-0.27 FW
104 104 104 104 20 20 20 (Continues)
130 Chapter 3 Table 3.11: Cont’d Organism
Concentration
Reference
0.06-0.53 FW
7
Rockfish, Sebastes spp. Muscle Muscle; British Columbia; 2004-2005 Near salmon aquaculture facilities Reference sites
0.45 FW <0.2 FW
Amberjack, Seriola grandis; muscle
0.18 (0.06-0.70) FW
Jack, Seriola quinqueradiata Spleen Muscle Liver Stomach Pyloric caeca
0.14 FW 0.18 FW 0.16 FW 0.04 FW 0.18 FW
20 20 20 20 20
Sea bass, Serranus scriba; mercurycontaminated area Muscle Liver Kidney
4.64 FW 11.60 FW 7.99 FW
10 10 10
151 151 1
Bass, Serranus sp.; Italy; coast; summer 1986-1987; muscle
0.09-0.63 FW
105
Pescadinha, Sillago sihama; muscle
0.02-0.15 FW
20
Spain; October 2003; liver Four-spotted megrim, Lepidorhombus boscii; depth 70-120 m Pouting, Trisopterus luscus; depth 200-500 m
a
(0.011-0.422) DW
154
(0.001-0.034) DW
154
Barracuda, Sphyraena spp.; muscle
0.61-0.67 FW
30
Guaguanche, Sphyraena guachancho; whole
0.02-0.31 FW
5
White marlin, Tetrapturus albidus; muscle
1.34 FW
Texas; coastal bays; reference sites; muscle vs. liver Spotted seatrout, Cynoscion nebulosus Southern flounder, Paralichthys lethostigma Red drum, Sciaenops ocellatus
0.07-0.44 FW vs. <0.12-0.84 FW <0.05-0.2 FW vs. 0.1-0.2 FW
106 106
<0.004-0.59 FW vs. 0.07-0.63 FW
106
Tunas; 1981; 5 spp.; muscle
1.0-6.3 FW
107
73
(Continues)
Fishes 131 Table 3.11: Organism Tunas; 1985-1986; Indian Ocean; blood; total mercury vs. methylmercury Yellowfin tuna; Thunnus albacares Big-eye tuna, Thunnus obesus Albacore, Thunnus alalunga; muscle Yellowfin tuna, Thunnus albacares White muscle Red muscle Muscle Muscle; Taiwan; 1995-1996 Muscle Total mercury Methylmercury Inorganic mercury Methylmercury Dark muscle Dorsal muscle Liver Abdominal muscle Spleen Kidney Muscle Muscle Heart Liver Spleen Kidney Brain Gonad GI tract Blood Bile Skin Southern bluefin tuna, Thunnus maccoyii; Australia; April 2004; muscle; wild vs. farmed
Cont’d
Concentration
0.08 (0.003-0.27) FW vs. 0.01 (0.00-0.03) FW 0.8 (0.5-1.3) FW vs. 0.5 (0.2-0.7) FW
Reference
108 108
0.13-0.27 FW
73
1.8 DW 2.1 DW 0.03-0.23 FW 9.8 (8.8-10.4) DW
71 71 72 91
0.38 (0.11-0.66) FW 0.37 (0.11-0.63) FW 0.017 FW 0.21 FW 0.19 FW 0.11 FW 0.20 FW 0.03 FW 0.07 FW 0.07-1.32 FW 0.16-0.24 FW 0.05-0.14 FW 0.07-0.18 FW 0.10-2.92 FW 0.05-0.53 FW 0.05-0.09 FW 0.04-0.08 FW 0.04-0.16 FW 0.03-0.08 FW 0.02-0.05 FW 0.02-0.10 FW 0.34 (0.28-0.42) FW vs. 0.31 (0.18-0.45) FW
a
1 1 1 78 78 78 78 78 78 77 75 75 75 75 75 75 75 75 75 75 75 152
(Continues)
132 Chapter 3 Table 3.11: Cont’d Organism
Concentration
Bigeye tuna, Thunnus obesus; muscle
0.23-0.75 FW
73
Tuna, Thunnus spp. Muscle Canned; Turkey; total mercury vs. methylmercury
0.74-2.34 FW 0.73 FW vs. 0.56 FW
79 8
0.07-0.11 FW
21
0.03-0.07 FW 0.04-0.08 FW 0.06-0.10 FW
20 20 20
Carangid, Trachurops crumenophthalmus; muscle Carangid, Trachurus japonicus Muscle Liver Spleen
Reference
Horse mackerel, Trachurus trachurus Turkey; canned; total mercury vs. methylmercury Muscle
0.73 FW
31
Atlantic cutlassfish, Trichiurus lepturus Muscle Liver
0.09 FW 0.04-0.22 FW
20 20
Tuna; canned; New Jersey supermarket Total mercury; 1998-2003 1998 vs. 1999 2000 vs. 2001 2002 vs. 2003 All cans Methylmercury; 2003 Chunk light Chunk white Solid white All white Oil Drained Undrained Tunas Muscle, 3 spp. Liver, 2 spp. Muscle 4, spp. Canned
0.063 FW vs 0.047 FW
8
0.32 FW vs. 0.31 FW 0.21 FW vs. 0.52 FW 0.33 FW vs. 0.48 FW 0.33 FW; max. 1.0 FW
141 141 141 141
0.04 FW 0.45 FW 0.33 FW 0.36 FW 0.23 FW 0.43 FW 0.46 FW
141 141 151 141 141 141 141
0.15-0.71 FW 0.08-0.27 FW 0.02-0.22 FW 0.32-2.87 FW
a
77 77 30 80 (Continues)
Fishes 133 Table 3.11: Organism Muscle; Mediterranean Sea Muscle; recent vs. 100-year-old museum samples
Cont’d
Concentration 2.5-3.5 FW 0.44-1.53 DW vs. 0.53-1.51 DW
Reference 17 76
Tunisia; Mediterranean Sea; summer 1994 Sardine, Sardinella aurita Muscle Liver Gonads Pilchard, Sardina pilchardus Muscle Liver
0.19-0.32 DW 0.5 DW 0.34 DW
142 142 142
0.26-0.41 (0.19-0.75) DW 0.93 DW
142 142
Goatfish, Upeneus molluccensis; muscle
0.23-0.56 FW
44
Red hake, Urophycis chuss Muscle Liver
<0.03-0.05 FW <0.03-0.05 FW
60 60
White hake, Urophycis tenuis Muscle Liver
0.10-0.12 FW 0.13 FW
60 60
Swordfish, Xiphias gladius Azores; November 1987; muscle; males vs. females <125 cm length >125 cm length Southwest Atlantic Ocean; 1999; muscle; weight 10 kg to 412 kg All Weight <100 kg Weight >100 kg Muscle; museum specimen circa 1909 vs. 1960s Muscle Muscle Muscle Azores area vs. Equator area; September 2004-February 2005 Total mercury Muscle Liver
0.4 FW vs. 0.25 FW 1.9 FW, max. 4.9 FW vs. 1.1 FW
109 109
0.62 (0.04-2.21) FW; 14% >1.0 FW 0.53 FW 0.94 FW 1.36 DW vs. 0.94-5.1 DW
143
0.05-4.90 FW 0.99-2.01 FW 0.99-4.24 FW
0.03-2.4 FW vs. 0.90-2.2 FW 0.05-8.5 FW vs. 1.1-9.8 FW
a
143 143 76 59 3 82
137 137 (Continues)
134 Chapter 3 Table 3.11: Cont’d Organism Organic mercury Muscle Liver
Concentration
0.03-2.4 FW vs. 0.90-2.1 FW 0.05-3.0 FW vs. 0.86-6.7 FW
Reference
a
137 137
Values are in mg Hg/kg fresh weight (FW) or dry weight (DW). a 1, Bebbington et al., 1977; 2, Williams et al., 1976; 3, Establier, 1977; 4, Leatherland and Burton, 1974; 5, Reimer and Reimer, 1975; 6, Hall et al., 1976a; 7, Childs and Gaffke, 1973; 8, Sanli et al., 1977; 9, Gardner et al., 1975; 10, Renzoni et al., 1973; 11, Cocoros et al., 1973; 12, Greig et al., 1977; 13, Robertson et al., 1975; 14, Linko and Terho, 1977; 15, Vanderstappen et al., 1978; 16, Cugurra and Maura, 1976; 17, Anonymous, 1978; 18, Havre et al., 1972; 10, Portmann, 1972; 20, Doi and Ui, 1975; 21, Rivers et al., 1972; 22, Taylor and Bright, 1973; 23, Suzuki et al., 1973; 24, Julshamn et al., 1978b; 25, Ui and Kitamuri, 1971; 26, Kureishy et al., 1979; 27, Hall et al., 1978; 28, Greig et al., 1977; 29, Babji et al., 1979; 30, Sorentino, 1979; 31, DeClerck et al., 1979; 32, Parvaneh, 1979; 33, Cheevparanapivat and Menasveta, 1979; 34, Miettinen and Verta, 1978; 35, Tuncel et al., 1980; 36, Cumont et al., 1975; 37, Matida and Kumada, 1969; 38, Won, 1973; 39, Fujiki, 1963; 40, Chvojka and Williams, 1980; 41, Ociepa and Protasowicki, 1976; 42, Kumagai and Saeki, 1978; 43, Windom et al., 1973; 44, Yannai and Sachs, 1978; 45, Ramelow and Hornung, 1978; 46, Bloom and Ayling, 1977; 47, Kari and Kauranen, 1978; 48, Stickney et al., 1975; 49, DeClerck et al., 1974; 50, Beasley, 1971; 51, Ramos et al., 1979; 52, Lunde, 1968a; 53, Chernoff and Dooley, 1979; 54, Julshamn and Braekkan, 1978; 55, van de Ven, 1978; 56, Scott, 1977; 57, Williams et al., 1976; 58, Grimanis et al., 1978; 59, Peterson et al., 1973; 60, Greig and Wenzloff, 1977a; 61, Newell et al., 1979; 62, Mackay et al., 1975; 63, Bargagli et al., 1998; 64, Schultz et al., 1976; 65, Schultz and Crear, 1976; 66, Eganhouse and Young, 1978; 67, Young, 1974; 68, Heit, 1979; 69, Alexander et al., 1973; 70, Nuorteva and Hasanen, 1975; 71, Thibaud, 1971; 72, Menasveta and Siriyong, 1977; 73, Papadopoulu et al., 1973; 74, Dix et al., 1975; 75, Hamada et al., 1977; 76, Miller et al., 1972; 77, Greig and Krzynowek, 1979; 78, Ueda and Takeda, 1977; 79, Arima and Umemoto, 1976; 80, Ganther et al., 1972; 81, Barber et al., 1984; 82, Freeman et al., 1978; 83, Voigt, 2004; 84, Chvojka et al., 1990; 85, Hornung et al., 1984; 86, Krom et al., 1990; 87, Dixon and Jones, 1994; 88, Fang et al., 2004; 89, Sohn and Jung, 1993; 90, Schuhmacher et al., 1994; 91, Han et al., 1998; 92, Voegborlo et al., 2004; 93, Mathieson and McLusky, 1995; 94, Kannan et al., 1998; 95, Dietz et al., 1996; 96, Joiris et al., 1997; 97, Gillis et al., 1993; 98, Burger et al., 2005; 99, Hope and Rubin, 2005; 100, Burger et al., 1992; 101, Leah et al., 1992b; 102, Leah et al., 1993; 103, Adams and Onorato, 2005; 104, Clark and Topping, 1989; 105, Giordano et al., 1991; 106, Sager, 2004; 107, Schreiber, 1983; 108, Kai et al., 1988; 109, Monteiro and Lopes, 1990; 110, Silver et al., 1994; 111, Fujiki, 1980; 112, Davies, 1991; 113, Nishimura and Kumagai, 1983; 114, Riget et al., 2007; 115, Lahaye et al., 2006; 116, Ramalhosa et al., 2006; 117, Arleny et al., 2007; 118, Edwards et al., 1999; 119, Chou, 2007; 120, Santos et al., 2006; 121, Magalhaes et al., 2007; 122, Monteiro et al., 1996; 123, Voegborlo et al., 2006; 124, Keskin et al., 2007; 125, Marcovecchio, 2004; 126, Storelli et al., 2006; 127, Voegborlo et al., 2007; 128, Julshamn et al., 2006; 129, Kojadinovic et al., 2006; 130, Jewett and Duffy, 2007; 131, Burger et al., 2007; 132, Mason et al., 2006; 133, Cunningham et al., 2003; 134, Martins et al., 2006; 135, Webb et al., 2006; 136, Abreu et al., 2000; 137, Branco et al., 2007; 138, Burger et al., 2007a; 139, Kojadinovic et al., 2007; 140, Storelli et al., 2005; 141, Burger and Gochfeld, 2004; 142, Joiris et al., 1999; 143, Mendez et al., 2001; 144, Joiris et al., 2000; 145, De Marco et al., 2006; 146, Sankar et al., 2006; 147, Cai et al., 2007; 148, Drevnick et al., 2006; 149, Al-Reasi et al., 2007; 150, Mishra et al., 2007; 151, Debruyn et al., 2006; 152, Padula et al., 2008; 153, Cheung et al., 2008; 154, Fernandes et al., 2008b; 155, Roach et al., 2008; 156, Baeyens et al., 2003.
a catalyst between 1932 and 1968. Minamata Bay received at least 260 tons of mercury, and perhaps as much as 600 tons. A severe neurological disorder was recognized in late 1953 and had reached epidemic proportions by 1956. At that time, the mercury level in sediments near the plant outfall was about 2010.0 mg/kg fresh weight; this decreased sharply with increasing distance from the plant, and sediments in the Bay contained between 0.4 and 3.4 mg Hg/kg FW. concentrations of mercury in fish, shellfish, and other organisms consumed by the Japanese decreased with increasing distance from the point of effluence and appeared to reflect sediment mercury levels. After intensive remediation involving dredging of contaminated
Fishes 135 sediments and bacterial degradation with mercury-resistant strains, fishing resumed in the Bay in the 1990s (as quoted in Eisler, 2006). Several observations are made regarding mercury burdens in field collections of teleosts. First, mercury tends to concentrate in muscle of finfish, with older fish containing more mercury per unit weight than young fish (Abreu et al., 2000; Alexander et al., 1973; Barber and Whaling, 1983; Barber et al., 1972; Branco et al., 2007; Cheevparanapivat and Menasveta, 1979; Chvojka and Williams, 1980; Cross et al., 1973; Cumont et al., 1972; Cutshall et al., 1978; DeClerck et al., 1974; Evans et al., 1972; Forrester et al., 1972; Giblin and Massaro, 1973; Greichus et al., 1973; Hall et al., 1976a,b; Hannerz, 1968; Johnels and Westermark, 1969; Johnels et al., 1967; Kojadinovic et al., 2006; Magalhaes et al., 2007; Mason et al., 2006; Matsunaga, 1978; Nuorteva and Hasanen, 1971; Peterson et al., 1973; Svansson, 1975; Taylor and Bright, 1973; Trudel and Rasmussen, 2006; Voegborlo et al., 2006). This is particularly well documented in marlins of the genus Makaira wherein mercury in muscle may exceed 15.0 mg/kg FW (Barber and Whaling, 1983); squirefish, Chrysophrys auratus (Robertson et al., 1975), European eel, A. anguilla (Establier, 1977), European hake, Merluccius merluccius (Yannai and Sachs, 1978), striped bass, M. saxatilis (Alexander et al., 1973), bluefish, Pomatomus saltatrix (Alexander et al., 1973), and others (Table 3.11). Similar data are available for liver in shorthorn sculpin, Myoxocephalus scorpius, from Greenland (Riget et al., 2007), and sardines from Tunisia (Joiris et al., 1999). Second, most of the mercury in fish muscle was in the organic form, primarily methylmercury (Bebbington et al., 1977; Bloom, 1992; Cheevparanapivat and Menasveta, 1979; Chvojka and Williams, 1980; Eganhouse and Young, 1978; Fukai et al., 1972; Gardner et al., 1975; Hamada et al., 1977; Hammerschmidt et al., 1999; Joiris et al., 1999; Kamps et al., 1972; Mason et al., 2006; Peterson et al., 1973; Rissanen et al., 1972; Rivers et al., 1972; Suzuki et al., 1973; Tamura et al., 1975; Ui and Kitamuri, 1971; Westoo, 1966, 1969, 1973; Zitko et al., 1971). Methylmercury as the dominant mercury species in fish muscle is attributed to the ability of fish to assimilate inorganic mercury less efficiently than methylmercury from the ambient medium and from their diet, and eliminate inorganic mercury more rapidly than methylmercury (Huckabee et al., 1979; Ribeiro et al., 1999; Trudel and Rasmussen, 1997). Maximum concentrations of total mercury in fish muscle usually do not exceed 2.0 mg Hg/kg fresh weight; however, forms of mercury with very low toxicity can be transformed into forms of very high toxicity—namely, methylmercury— through biological and other processes. Third, levels of mercury in muscle from adult tunas, billfishes, and other carnivores were higher than those in young fishes with a shorter food chain; this indicates associations among predatory behavior, longevity, and mercury accumulation (Eisler, 1981, 2006; Forrester et al., 1972; Hall et al., 1976a,b; Jerneloev, 1972; Klemmer et al., 1976; Matsunaga, 1978; Ociepa and Protasowicki, 1976; Peakall and Lovett, 1972; Peterson et al., 1973; Ratkowsky
136 Chapter 3 et al., 1975; Rivers et al., 1972; Ui, 1972; Yannai and Sachs, 1978). Oceanic tunas and swordfish caught in the 1970s had mercury levels similar to those of museum conspecifics caught nearly 100 years earlier (Miller et al., 1972). It is speculated that mercury levels in fishes were much higher 13,000-20,000 years ago during the last period of glaciation when ocean mercury concentrations were four to five times higher than today (Vandal et al., 1993). Fourth, total mercury was uniformly distributed in muscle of finfish, demonstrating that a small sample of muscle tissue taken from any region is representative of the whole mercury tissue when used for mercury analysis (Freeman and Horne, 1973a,b; Hall et al., 1976a,b). Finally, elevated levels of mercury in wide-ranging oceanic fish were not solely the consequence of anthropogenic activities but also resulted from natural concentrations (Greig et al., 1976; Miller et al., 1972; Schultz et al., 1976; Scott, 1977; Yannai and Sachs, 1978). This last point is not consistent with the rationale underlying U.S. seafood guidelines regulating mercury levels in food and formulated in the 1970s. According to Peterson et al. (1973), when the U.S. Food and Drug Administration introduced safety guidelines—which eventually were instrumental in the temporary removal of all swordfish and substantial quantities of canned tuna from market—it acted essentially under the assumption that the fish product was “adulterated” by an “added substance.” It is noteworthy that muscle from two species of recreationally important fish (spotted seatrout, Cynoscion nebulosus; red drum, S. ocellatus) collected from coastal bays in Texas considered “minimally impacted” by mercury exceeded the current recommended value in the United States of 0.3 mg total Hg/kg fresh weight muscle (Sager, 2004). Recent studies by Peterson et al. (2007) demonstrate that wet tissue homogenates of fish can be held frozen for at least 4 years without affecting analytical results for mercury. This finding extends the 28-day (at 20 C) holding time recommended for total mercury analysis by the United States Environmental Protection Agency (USEPA, 1995), and the 180-day, 20 C holding time recommended for all metals, including mercury (California Department of Fish Game, 1990; Crawford and Luoma, 1993). Of 159 species of finfish from coastal waters of Alaska, Hawaii, and the conterminous United States, most muscle samples had mean mercury concentrations less than 0.3 mg/kg fresh weight (Hall et al., 1978). However, 31 species contained mean mercury concentrations above 0.5 mg Hg/kg fresh weight, a designated “action level” of the U.S. Food and Drug Administration. Based on landings, less than 2% of the U.S. catch intended for consumption may be in excess of the action level (Hall et al., 1978). Whole Pacific staghorn sculpin, Leptocottus armatus, contained 0.96 mg Hg/kg FW, the highest concentration reported in whole fish collected from 736 stations in U.S. estuaries during 2000-2001 (Harvey et al., 2008). Inshore marine biota contained higher mercury concentrations than conspecifics collected offshore (Dehlinger et al., 1973; Jones et al., 1972; Westoo, 1969). In Sweden, marine fish
Fishes 137 caught near shore had comparatively high methylmercury burdens, with many values in the range 5.0-10.0 mg Hg/kg fresh weight (Ackefors et al., 1970; Westoo, 1969); concentrations above 1.0 mg Hg/kg in Swedish fish were usually associated with industrial discharges of mercury compounds (Westoo, 1969). In Mediterranean Sea fishes, the mercury body burden was about twice that of conspecifics of the same size from the Atlantic Ocean (Baldi et al., 1978; Renzoni et al., 1978). It is possible that the higher mercury body burdens were due to the higher natural geochemical mercury levels in the Mediterranean Sea. Mercury concentrations in fish muscle from fishing grounds of Germany seldom exceeded 0.1 mg total Hg/kg fresh weight (Jacobs, 1977). Of the total mercury in German fish, methylmercury constituted 70-98%, a value that is in general agreement with reports from Japan, Sweden, and other reports on the subject (Jacobs, 1977). The efficiency of mercury transfer through natural marine food chains among lower trophic levels was comparatively low; higher trophic levels, however, including fishes, fish-eating birds, and mammals show marked mercury amplification (Cocoros et al., 1973; Huckabee and Blaylock, 1972; Jerneloev and Lann, 1971; Skei et al., 1976; Stickney et al., 1975). The variability of concentrations is partly explainable in terms of collection locale: some field collections were taken from areas where human activities have raised the mercury content in the aquatic environment above natural levels, thus producing a significant increase in the mercury content of native fauna (Debruyn et al., 2006; Hearnden, 1970; Johnels et al., 1967; Kazantzis, 1971; Kleinert and Degurse, 1972; Magalhaes et al., 2007; Renzoni et al., 1973; Wobeser et al., 1970; Zitko et al., 1971). In frigate tuna, Auxis thazard thazard, Voegborlo et al. (2007) aver that mercury uptake is mainly through the diet as judged by mercury tissue burdens in the order muscle > liver > duodenum > heart > intestine > gonads > stomach > gills. Not all investigators agreed that diet was the most important concentration mechanism for marine teleosts. Fujiki et al. (1977), for example, report that mercury in suspended solids and bottom sediments were not transferred in significant amounts to Chrysophrys major, that accumulation via the food chain was very low, and that dissolved methylmercury in seawater was the critical agent for methylmercury accumulation. Gardner (1978) states that there is a positive correlation between mercury content of bottomfish tissues in various United Kingdom fishing grounds and average mercury concentration in water samples from the same locales. A similar case is made for Japanese waters (Matsunaga, 1976). Gardner (1978) also showed that ionic mercury predominated in water, and that mercury in fish tissues contained more than 80% methylmercury; Gardner contends that dissolved mercury is removed rapidly from seawater by particulate matter and subsequently to sediments where methylation occurs. Gardner (1978) concludes that causes of variations in mercury concentrations in fish tissues are attributed to the following: availability of food and its mercury content; the chemical form and concentration of dissolved mercury; the fish species and trophic level; and growth rate, gender, and length of the fish. To this list must be added changes associated with latitude, where mercury levels in selected species were opposite to that reported for other fish species over the same geographic
138 Chapter 3 area (Cutshall et al., 1978; Hall et al., 1976a), seasonal changes (Staveland et al., 1993) wherein mercury concentrations in muscle of marine flatfish were higher in the spring than in the autumn, and gender (as quoted in Eisler, 2006) wherein adult females often contain higher concentrations of mercury than males, possibly because they consume more food than males in order to support the energy requirements of egg production. Elevated levels of mercury in muscle of demersal rockfishes, Sebastes spp., near salmon aquaculture farms in coastal British Columbia is attributable to a combination of higher mercury levels in prey near farms, to high rockfish trophic position, and to the comparatively long life span (>40 years) of rockfish (Debruyn et al., 2006). Based on museum specimens of whole lanternfish, Benthosema glaciale, over an 80-year period, mercury contamination was highest during the World War II years (1939-1945) followed by a general decrease (Table 3.11; Martins et al., 2006). Laboratory studies on the uptake, retention, and translocation of mercury by marine teleosts is the subject of a growing literature. Captive Atlantic cod, G. morhua, were fed diets containing 0.05 mg Hg(as methylmercury)/kg FW ration for 3 months (Amlund et al., 2007). The final mercury concentration in muscle was 0.38 mg Hg/kg FW, with methylmercury accounting for 90-95% of the mercury burden. Elimination was slow, with a calculated halftime persistence of 377 days. The transfer of methylmercury from diet to Atlantic cod was 38%. In muscle, more than 99% of the methylmercury was found in the protein fraction, suggesting that Atlantic cod readily accumulates dietary methylmercury and efficiently stores it in muscle peptides and proteins. Similar results are documented for cultured Atlantic salmon, S. salar (Amlund et al., 2007). Rapid accumulation of mercury, especially organomercury compounds, is well documented (Amlund et al., 2007; Bligh, 1972; Fang, 1973; Hannerz, 1968; Hasselrot, 1968; Hibaya and Oguri, 1961; Johnels et al., 1967; Kramer and Neidhart, 1975; MacLeod and Pessah, 1973; Middaugh and Rose, 1974; Olson et al., 1973; Pentreath, 1976a,b; Rucker and Amend, 1969). Uptake of mercury from seawater by eggs and larvae of plaice demonstrated that eggs bioconcentrated environmental mercury levels by a factor of 465 in 12 days; for larvae this was 2000 in 8 days (Pentreath, 1976a). Whole adult plaice had BCFs of 600 in 64 days, with most of the mercury in muscle (Pentreath, 1976a). Adults of mullet, M. auratus, held in seawater solutions containing 0.1 mg Hg/L, as HgCl2, for 57 days contained 2.2 mg Hg/kg fresh weight muscle versus 0.11 in controls (Establier et al., 1978). Higher accumulations were observed with methylmercury: exposure of Mugil for 45 days in 0.008 mg Hg/L, as methylmercury chloride, produced 2.6 mg Hg/kg fresh weight muscle (Establier et al., 1978). Uptake of mercury and its compounds from seawater is modified by many factors. These include the chemical form of mercury administered (Hannerz, 1968; Kramer and Neidhart, 1975; Pentreath, 1976a,b; Renfro et al., 1974); the mode of administration (Jarvenpaa et al., 1970; Schmidt-Nielsen et al., 1977); the presence of complexing or chelating agents in the
Fishes 139 medium (Kramer and Neidhart, 1975); the initial mercury concentration (Calabrese et al., 1975; Hannerz, 1968; Koeller and Wallace, 1977; Kramer and Neidhart, 1975; Weis and Weis, 1978); tissue specificity (Calabrese et al., 1975; Hannerz, 1968; Pentreath, 1976a,b; Schmidt-Nielsen et al., 1977); salinity of the medium (Renfro et al., 1974); and exposure time (Calabrese et al., 1975; Koeller and Wallace, 1977). In one study, accumulation of methylmercury by freshwater- and seawater-adapted Japanese eels, Anguilla japonica, held in 0.010 mg Hg/L as methylmercury chloride for 72 h was significantly greater in marineadapted eels than freshwater-adapted eels for liver (2.8 mg/kg FW vs. 2.0 mg/kg FW), spleen (3.4 vs.2.4), kidney (1.6 vs. 1.4), pancreas (1.0 vs. 0.5), bile (0.4 vs. 0.06), and blood (4.1 mg/kg FW vs. 1.9 mg/kg FW; Yamaguchi et al., 2004). In freshwater-adapted eels, but not marine-adapted eels, methylmercury induced stimulation of GSH in both liver and kidney and this may interfere with mercury uptake in that group (Yamaguchi et al., 2004). Skeletal muscle of fish is a methylmercury reservoir (Giblin and Massaro, 1973; Johnels et al., 1967; MacLeod and Pessah, 1973; Middaugh and Rose, 1974; Pentreath, 1976b; Weisbart, 1973). Maximum concentration factors of radiomercury were reached in skeletal muscle, brain, and lens after 34, 56, and >90 days, respectively; maximum values were reached in most other tissues and organs in about 7 days (Giblin and Massaro, 1973). One pathway by which anadromous fishes accumulate mercury from the medium is through the gills; up to 90% of the mercury taken up on gills is bound to erythrocytes within 40 min (Olson et al., 1973). Metallothionein induction in liver of sea bass, D. labrax, was induced by intraperitoneal injections of inorganic mercury in the range 0.05-0.25 mg Hg/kg body weight. After 48 h, metallothionein levels increased linearly with increasing dose; maximum induction was obtained at 0.25 mg Hg/kg BW, being 5.1 times higher than controls (Jebali et al., 2008). In the food chain, algae to detritus to worm to fish (prey) to fish (predator), mercury had a long biological half time, more than 1000 days in predatory fish versus 55 days in prey fish (Huckabee and Blaylock, 1972). The transfer efficiency of inorganic mercury from prey fish to predator fish was about 40%, but from worm to prey fish, it was only 12%; worms assimilated 60% of the inorganic mercury contained in the algae-detritus. Huckabee and Blaylock concluded that food chain uptake can account for a significant percentage of the mercury body burden in fishes. Methylmercury accumulation was studied in the food chain of diatom, Skeletonema costatum, to copepod, Acartia clausi, to the red sea bream, C. major (Fujiki et al., 1978). Diatoms reared for 24 h in seawater containing 0.005 mg Hg/L, as methylmercury, contained 3.45 mg Hg/kg. Copepods fed on these diatoms for 4 days contained 3.14 mg Hg/kg. Bream fed copepods for 10 days had 3.10 mg Hg/kg. Additional studies indicated that the most effective pathway for methylmercury accumulation by the red sea bream is not via the food chain but rather from seawater directly through the gills (Fujiki et al., 1978). No progressive mercury concentration was observed in a clam to eel
140 Chapter 3 transfer (Tsuraga, 1963). When dogfish meal containing up to 2.3 mg total Hg/kg, of which 1.9 mg/kg was methylmercury, replaced low mercury fish rations used in salmon culture, salmon muscle contained >0.5 mg Hg/kg within 8 months; however, when dogfish meal comprised less than half the diet, mercury levels were <0.5 mg/kg (Spinelli and Mahnken, 1976). Similar results were observed in sablefish fed dogfish meal (Kennedy and Smith, 1972). The retention time of mercury in marine teleosts depends on several factors. Weisbart (1973) found that gill, heart, and swimbladder tissues of fish lost mercury at rates faster than the whole organism but that some tissues—including brain, muscle, liver, and kidney—showed no significant decrease over time. Half-time persistence of 203Hg in most marine species were comparatively lengthy, ranging up to 267 days in Serranus scriba (Miettinen et al., 1969, 1972). Miettinen and coworkers found that phylogenetically related species follow a similar pattern of methylmercury excretion, with half-time persistence directly dependent on water temperature and with mode of entry, being longer after intramuscular injection than oral administration. A study by Amend (1970) of juvenile sockeye salmon indicated that fish treated repeatedly with mercurials during their freshwater hatchery phase accumulated and retained high levels of mercury for several months, but after 4 years at sea the returning salmon contained normal levels of mercury in all tissues examined. Fish heavily contaminated by methylmercury, both naturally and through laboratory-administered feeding studies eliminated the accumulated mercury to safe levels of human consumption in 37 weeks when maintained in mercury-free media and fed a mercury-free diet; shorter depuration periods were unsuccessful (Kikuchi et al., 1978). Thus, mercury-contaminated Serranus cabrilla eliminated mercury from whole body when held in clean seawater for 10 day; however, only gill and digestive tract showed reduced levels with essentially no change in mercury content of liver, kidney, or edible muscle (Radoux and Bouquegneau, 1979). In Florida, baseline data collected in 1995 from southern estuaries showed acceptable mercury concentrations in sediments and water, and unacceptable levels of total mercury (up to 2.2 mg/kg FW) and methylmercury (up to 1.0 mg/kg FW) in teleost muscle (Kannan et al., 1998). In the Florida recreational fishery for red drum, S. ocellatus, the current maximum size limit of less than 565 mm standard length or less than 689 mm total length is an effective filter that limits consumption of large fish containing elevated mercury concentrations (Adams and Onorato, 2005). About 94% of all adult red drum from waters adjacent to Tampa Bay, Florida, contain mercury levels greater than 0.5 mg/kg FW muscle—the Florida Department of Health threshold value—and 64% contained more than 1.5 mg Hg/kg FW muscle, which is the Florida “no consumption” level. All fish from this area containing more than 1.5 mg Hg/kg FW muscle were longer than the 689 mm total length (Adams and Onorato, 2005). Burger et al. (2005), on analyzing edible marine products of commerce sold in New Jersey supermarkets during 2003 for mercury content, concluded that four fish species that were
Fishes 141 available in more than half the supermarkets or fish markets sampled contained significantly different concentrations of mercury: tuna (max. 2.5 mg total Hg/kg FW muscle), bluefish (max. 0.76), snapper (max. 0.3), and flounder (max. 0.14). Consumers selecting only for price could choose from whiting, porgy, croaker, and bluefish, all with average mercury concentrations less than 0.3 mg/kg FW muscle. Since flounders were comparatively available, modest in cost, and with very low mercury levels, authors suggest that state agencies should publicize this and similar information to their citizens, enabling them to make informed decisions about risks from fish consumption (Burger et al., 2005, 2007c). Moreover, marine fish culture facilities in Germany should restrict fish diets to less than 0.5 mg total Hg/kg FW (Weinreich et al., 1994). The findings of elevated blood mercury levels, increased chromosome breakage, and easy passage of mercury through placental membranes in humans who regularly eat fish containing 1.0-17.0 mg Hg/kg fresh weight (Kazantzis, 1971; Keckes and Miettinen, 1972) suggests to some health authorities that the former accepted level of 0.5 mg Hg/kg fresh weight fish tissue (Keskin et al., 2007)—now 0.3 mg Hg/kg fresh weight in the United States (Cai et al., 2007; Eisler, 2006) and China (Cheung et al., 2008)—did not have an appreciable level of safety for pregnant women (Establier, 1975a,b; Peakall and Lovett, 1972; Skerfring et al., 1970). Differences in reported mercury concentrations can significantly affect mercury intake estimates of seafood by U.S. human consumers (Sunderland, 2007). National exposure estimates are most influenced by reported methylmercury concentrations in imported tuna (0.37-0.48 mg/kg FW), imported sword fish (1.03 mg/kg FW), and Pacific pollack (0.06 mg/kg FW) (Sunderland, 2007). In Sweden, the accepted limit in fish is 1.0 mg/kg fresh weight; human risk in consumption of mercury-contaminated fish within this guideline is considered negligible in that country (Berglund and Berlin, 1969); however, some Scandinavian scientists recommend that fish consumption should be limited to one meal weekly (Lofroth, 1970). Consumers of fish originating from the southwestern Indian Ocean should limit consumption to one fish meal daily if they consume tuna, wahoo, or common dolphinfish, or one fish meal weekly if they eat swordfish (Kojadinovic et al., 2006). The State of Alaska guideline for seafood products is <1.0 mg methylmercury/kg fresh weight (Jewett and Duffy, 2007). The European Union recommends less than 1.0 mg total mercury/kg FW seafood products destined for human consumption (Kojadinovic et al., 2007). For high seafood consumers in Taiwan, the proposed acceptable ingestion rates of fish muscle during 2003-2004 were <50 g daily for children and <91 g daily for women of childbearing age (Chien et al., 2007).
3.24 Molybdenum Maximum concentrations of molybdenum in all tissues and byproducts of marine teleosts examined did not exceed 2.0 mg Mo/kg fresh weight; concentrations in edible muscle seldom exceeded 0.5 mg Mo/kg fresh weight (Table 3.12).
142 Chapter 3 Table 3.12: Molybdenum Concentrations in Field Collections of Fishes Organism Fish Liver 4 spp. 12 spp. 27 spp. 16 spp. 14 spp. 6 spp. 3 spp. 2 spp. Muscle 21 spp. 48 spp. 61 spp. 18 spp. 7 spp. 4 spp. Whole 2 spp. 7 spp. 8 spp. 8 spp. Fishmeal, 4 spp. Presscake N-liquor Meal Atlantic salmon, Salmo salar; marine farmed; diet vs. feces
Concentration
Reference
<0.1 FW 0.1-0.2 FW 0.2-0.3 FW 0.3-0.4 FW 0.4-0.5 FW 0.5-0.6 FW 0.6-2.0 FW 0.4-1.0 DW
1 1 1 1 1 1 1 3
<0.1 FW 0.1-0.2 FW 0.2-0.3 FW 0.3-0.4 FW 0.4-0.5 FW 0.5-0.6 FW
1 1 1 1 1 1
<0.1 FW 0.1-0.3 FW 0.3-0.6 FW 0.012-0.15 FW
1 1 1 4
0.26 DW <0.05 DW 0.16 DW
2 2 2
0.80 DW vs. 0.92 DW
5
a
Values are in mg Mo/kg fresh weight (FW) or dry weight (DW). a 1, Hall et al., 1978; 2, Lunde, 1968b; 3, Papadopoulu et al., 1981; 4, Rao, 1984; 5, Dean et al., 2007.
In general, molybdenum was more toxic to teleosts in freshwater than in seawater, and more toxic to younger fish than to older fish (Eisler, 2000b). The LC50 (96 h) value for molybdenum and sheepshead minnow, C. variegatus, was 3057.0 mg/L (Knothe and Van Riper, 1988).
3.25 Neptunium The maximum concentration factor for radioneptunium isotopes from seawater by whole marine teleosts is 10 (vs. 5000 for algae) (Morse and Choppin, 1991).
Fishes 143
3.26 Nickel Edible tissues of most marine teleosts seldom had more than 0.3 mg Ni/kg fresh weight, although values greater than 5.0 mg Ni/kg fresh weight and greater than 10.0 mg/kg dry weight are sometimes reported (Table 3.13). Nickel concentrations in fish tissues are frequently elevated in the vicinity of nickel smelters and refineries, nickel-cadmium battery plants, sewage outfalls, and coal ash disposal basins (Eisler, 2000e). In general, internal organs had slightly higher nickel concentrations than muscle, but the significance of this finding is unclear. For example, blue hake collected from the vicinity of a major marine disposal site had the highest concentration (0.82 mg Ni/kg fresh weight) of nickel in liver of the seven species of teleosts examined (Greig et al., 1976). Nickel burdens in liver of tautog (Tautoga onitis) from New Jersey significantly decrease with increasing body length in both males and females; however, this trend was not observed in bluefish (P. saltatrix) or tilefish (Lopholatilus chamaeleonticeps; Mears and Eisler, 1977). Effects of ionic nickel on survival of representative marine teleosts are variable. Concentrations fatal to 50% in 96 h—in mg Ni/L—include 8.0 for adults of the Atlantic silverside (Menidia menidia; WHO, 1991), 13.0 for adults of the American eel (Anguilla rostrata; USEPA, 1980d), 38.0 for larvae of the tidewater silverside (Menidia peninsulae; WHO, 1991), 70.0 for adults of the spot (L. xanthurus; WHO, 1991), and 150.0 for adults of the mummichog (F. heteroclitus; Eisler and Hennekey, 1977). To protect the comparatively resistant marine teleosts as well as sensitive marine invertebrates against nickel, various seawater criteria have been proposed, including less than 0.0071 mg total recoverable nickel/ L (24-h average), and less than 0.14 mg Ni/L at any time (USEPA, 1980d).
3.27 Niobium Whole Baltic herring, C. harengus, contained nondetectable (<0.00002 mg/kg DW) concentrations of niobium (Zumholz et al., 2006). Excretion of radioniobium by Atlantic croakers, M. undulatus, following intraperitoneal injection appeared to follow a biphasic pattern. Half-time of the longer lived component was 465 days; for the short-lived component, this was 33 days (Baptist et al., 1970).
3.28 Palladium Following the introduction of automobile catalysts in the mid-1980s, there was an increasing emission of palladium and other platinum group metals. Road dust containing 0.0213 mg Pd/kg was added to freshwater (10 kg road dust in 100 L) containing juvenile European eels, A. anguilla (Sures et al., 2001). After 4 weeks, livers contained 0.00018 (0.00014-0.00025) mg Pd/kg FW; kidney concentrations were below detection limits of 0.0001 mg Pd/kg FW.
144 Chapter 3 Table 3.13: Nickel Concentrations in Field Collections of Fishes Organism
Concentration
Canned fish; Saudi Arabia; purchased locally Sardine Salmon Tuna
1.33 (0.79-2.13) FW 0.84 (0.12-1.70) FW 0.41 (0.13-0.81) FW
20 20 20
Blackfin icefish, Chaenocephalus aceratus; Antarctica; muscle vs. liver
0.2 DW vs. 0.3 (0.2-0.5) DW
14
Lumpfish, Cyclopterus lumpus; United Kingdom; all tissues
3.2-5.2 FW
15
2.0 FW; 5.0 DW 0.5 FW; 2.2 DW
15 15
Skipjack tuna, Euthynnus pelamis; muscle Peru Puerto Rico Fish Gills, 7 spp. Gonad, 7 spp. Heart, 7 spp. Kidney, 8 spp. Liver 22 spp. 32 spp. 14 spp. 9 spp. 5 spp. 8 spp. Muscle 12 spp. 11 spp. 2 spp. 36 spp. 111 spp. 6 spp. 2 spp. 2 spp. 8 spp. 7 spp. 8 spp. 10 spp; Bay of Bengal, India 10 spp.; Mumbai, India; 2004-2005 10 spp.; China; October 2004
Reference
0.1-1.0 FW 0.1-0.4 FW 0.1-0.4 FW 0.1-0.8 FW
1 1 1 1
0.1-0.2 FW 0.2-0.3 FW 0.3-0.5 FW 0.5-0.7 FW 0.8-3.0 FW 0.1-0.4 FW
2 2 2 2 2 1
0.11-0.39 FW; 0.43-1.55 DW 0.1-10.8 DW <0.1 FW 0.1-0.2 FW 0.2-0.3 FW 0.3-0.5 FW 0.6-0.8 FW 0.9-3.0 FW 0.02-0.07 FW 0.31-0.55 DW 0.6-4.0 DW 0.7-6.1 DW 0.68 FW; 95th percentile 1.6 FW <0.05-0.70 FW
a
3 4 2 2 2 2 2 2 1 5 6 16 21 22 (Continues)
Fishes 145 Table 3.13: Organism 9 spp. New Zealand 8 spp.; United Kingdom Texas; outer continental shelf Skin, 8 spp. Spleen, 7 spp. Vertebrae, 8 spp. Viscera 4 spp. 3 spp. Whole 10 spp. 8 spp. 5 spp. 4 spp. 10 spp.; Israel; Mediterranean Sea coast; 1974
Cont’d
Concentration
Reference
0.02-0.07 DW 2.1-3.5 DW 0.6-4.9 DW 1.9-4.9 DW 0.1-2.0 FW 0.2-2.0 FW
15 15 6 6 1 1
240.0 AW 2.5-4.2 DW
7 6
Max. 0.14 FW 0.2-0.4 FW 0.4-0.6 FW 0.6-1.0 FW 0.1-10.8 DW
8 2 2 2 4
Atlantic cod, Gadus morhua; all tissues
1.6-4.6 FW
15
Dab, Limanda limanda; skin plus muscle
0.4-1.1 FW
9
Atlantic croaker, Micropogonias undulatus; Texas; muscle vs. skin
2.7 DW vs. 3.8 DW
15
Dover sole, Microstomus pacificus; California; muscle vs. Liver
0.2 (0.1-0.3) FW vs. 1.4-2.6 FW
15
Striped bass, Morone saxatilis Muscle Liver
1.0 FW 2.0 FW
10 10
Mullet, Mugil spp.; Mediterranean Sea; June-July 2003 Muscle Skin Gills Liver
1.1-1.2 FW 1.4-1.6 FW 4.5-4.7 FW 3.0-3.8 FW
18 18 18 18
Striped mullet, Mugil cephalus; muscle; 2005; Turkey
1.2 (0.05-3.5) DW
19
Blue hake, Nematonurus armatus; liver
0.8 FW
13
Hump rock cod, Notothenia gibberfrons; muscle; Antarctica
0.2 DW
14
a
(Continues)
146 Chapter 3 Table 3.13: Cont’d Organism
Concentration
Pandora, Pagellus erythrinus Fins Eyes Eggs Gills Brain Liver Intestine Spleen Muscle Skin Bone Whole
8.6 DW 7.3 DW 8.4 DW 9.7 DW 10.0 DW 5.8 DW 8.1 DW 16.1 DW 5.6 DW 4.2 DW 1.0 DW 8.4 DW
11 11 11 11 11 11 11 11 11 11 11 11
Kelp bass, Paralabrax clathratus; California Gonad Liver Muscle Skin
1.5-2.2 DW 3.9-7.6 DW 5.0-6.4 DW 9.0-10.2 DW
15 15 15 15
<0.3-0.5 FW <0.3-0.5 FW vs. <0.3-1.0 FW 3.3 (0.6-7.4) DW vs. 4.4 (2.9-7.4) DW
12 15 15
0.2-1.1 FW vs. <0.2-0.4 FW
15
Winter flounder, Pleuronectes americanus Muscle New York Bight; muscle vs. skin Texas; muscle vs. skin Yellowtail flounder, Pleuronectes ferruginea; New York Bight; liver vs. muscle
Reference
South Carolina; gamefish; 1990-1993; whole; max. Values Spotted seatrout, Cynoscion nebulosus Southern flounder, Paralichthys lethostigma Red drum, Sciaenops ocellatus
12.6 FW 8.2 FW
17 17
2.9 FW
17
Scup, Stenotomus chrysops; Texas Muscle Skin Viscera
1.0 (0.5-2.0) DW 4.9 (2.8-7.4) DW 3.5 DW
15 15 15
0.023 DW
24
Blackfin tuna, Thunnus atlanticus; otoliths; Gulf of Mexico; 2002
a
(Continues)
Fishes 147 Table 3.13: Organism Turkey; 2005; Black Sea vs. Aegean Sea European anchovy, Engraulis encrasicolus Muscle Liver Picarel, Spicara smaris Muscle Liver Red hake, Urophycis chuss Muscle Liver White hake, Urophycis tenuis; muscle
Cont’d
Concentration
Reference
0.6-1.5 FW vs. 1.5 FW 1.2-5.1 FW vs. 4.4 FW
23 23
0.25 FW vs. 0.7-1.3 FW 5.7 FW vs. 10.2-11.6 FW
23 23
0.3-0.5 FW <0.2-1.7 FW <0.1 FW
12 12 12
a
Values are in mg Ni/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Brooks and Rumsey, 1974; 2, Hall et al., 1978; 3, Plaskett and Potter, 1979; 4, Roth and Hornung, 1977; 5, Ishii et al., 1978; 6, Horowitz and Presley, 1977; 7, Goldberg, 1962; 8, Ikebe and Tanaka, 1979; 9, Newell et al., 1979; 10, Heit, 1979; 11, Papadopoulu et al., 1972; 12, Greig and Wenzloff, 1977a; 13, Greig et al., 1976; 14, Szefer et al., 1993; 15, Jenkins, 1980a; 16, Sharif et al., 1993; 17, Mathews, 1994; 18, Storelli et al., 2006; 19, Turkmen et al., 2006; 20, Ashraf et al., 2006; 21, Mishra et al., 2007; 22, Cheung et al., 2008; 23, Turkmen et al., 2008; 24, Arslan and Secor, 2008.
More research is recommended on the platinum group metals (platinum, palladium, and rhodium) on seawater phases of species that migrate between salinity gradients (Sures et al., 2001).
3.29 Plutonium In teleosts, bone and liver are the major repositories for plutonium; muscle, however, contains relatively low concentrations (Noshkin, 1972). The maximum concentration factor of radioplutonium isotopes from seawater by whole fishes is estimated at 10 (vs. 2000 for macroalgae) (Morse and Choppin, 1991). Accidental contamination of the marine environment near Greenland by nuclear missiles jettisoned from an aircraft produced plutonium levels 10-20 times over fallout background levels in bottom fish populations (Aarkrog, 1971, 1977). Pillai et al. (1964) state that teleosts have the lowest uptake potential for plutonium of all marine groups examined and that the maximum plutonium value in muscle of bonito, Sarda lineolata, was only three times the background levels. The concentrations of a number of alpha emitters, including plutonium-238,-239, and -240, americium-241, and curium 242, 243-244 were determined in organs and tissues of P. platessa from the vicinity of an English nuclear fuel reprocessing plant. Over a period of several years, the highest concentrations of all nuclides were in kidney and the lowest in
148 Chapter 3 muscle. In all organs analyzed, americium was greater than those of plutonium in terms of its concentration and the rates of discharge for these nuclides (Pentreath and Lovett, 1976, 1978). P. platessa collected from the vicinity of a French nuclear fuel reprocessing plant had the highest concentrations of plutonium isotopes in gut, followed by whole fish, gonad, and bone in that order (Guary et al., 1976). Laboratory studies with P. platessa and 237Pu showed little uptake in tissues after exposure for 2 months in labeled seawater. Oral retention from a variety of labeled foods was also very poor, and apart from the gut, no incorporation of this isotope could be demonstrated in any tissue examined of this flatfish (Pentreath, 1978). When 237Pu was injected, growing Pleuronectes incorporated a relatively large fraction of the isotope into skeletal material at the expense of liver; in any event, very little of the injected 237Pu accumulated in muscle (Pentreath, 1978).
3.30 Polonium The concentration factor for 210Po from seawater to whole tuna is about 1000, with highest concentration factors in liver and lowest in muscle (Heyraud and Cherry, 1979). Attempts to relate accumulations of naturally occurring radiopolonium-210 in carnivorous teleosts with 210 Po in their diets were inconclusive. In one study, 210Po activities in nine food organisms (all teleosts) of tunas were highest in viscera from a surface living fish, Cololabis saira; however, the average concentration in the nine food organisms was the same as whole body 210 Po values observed in albacore tuna (Hoffman et al., 1974). In another study, an unusually high concentration of 210Po was found in liver of sablefish; zooplankton from the same collection areas also had elevated 210Po concentrations (Schell et al., 1973).
3.31 Radium Naturally occurring radioisotopes of radium tend to accumulate in bone, with lowest concentrations recorded in soft tissues (Pentreath, 1977c).
3.32 Rhenium Rhenium was not present in measurable quantities in mackerel muscle (Table 3.14).
3.33 Rubidium Rubidium concentrations never exceeded 1.4 mg Rb/kg muscle on a fresh weight basis or 4.0 on a dry weight basis (Table 3.14). There was no marked trend towards tissue specificity; in some cases, the highest rubidium values were in liver, in others it was muscle or bone (Table 3.14).
Fishes 149 Table 3.14: Rhenium, Rubidium, Ruthenium, and Scandium Concentrations in Field Collections of Fishes Element and Organism
Concentration
Reference
<0.008 AW <0.0004 DW
1 2
Fish; muscle 6 spp. 7 spp.
0.75-1.40 FW 2.6-4.0 DW
3 4
Goby, Gobius niger Muscle Liver
2.6 DW 0.52-0.76 DW
5 5
Coelacanth, Latimeria chalumnae Muscle Liver Kidney
0.18 FW 0.52 FW 0.31 FW
3 3 3
Plaice, Pleuronectes platessa Muscle Liver Bone
0.86 FW 0.53 FW 0.98 FW
3 3 3
Porgy, Sargus annularis Muscle Liver
1.9-2.9 DW 1.7-2.8 DW
5 5
0.23 DW
6
0.024-0.320 DW 0.19 DW
6 6
0.443 FW
7
0.06-0.16 AW
8
a
Rhenium Chub mackerel, Scomber japonicus Muscle Muscle Rubidium
Chub mackerel, Scomber japonicus; muscle Horse mackerel, Trachurus trachurus Muscle Liver Ruthenium Albacore, Thunnus alalunga; blood Scandium Whole fish, 4 spp.
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Fukai and Meinke, 1959; 2, Fukai and Meinke, 1962; 3, Pentreath, 1977c; 4, Ishii et al., 1978; 5, Grimanis et al., 1978; 6, Papadopoulu et al., 1978b; 7, Hansen et al., 1978; 8, Robertson, 1967.
150 Chapter 3
3.34 Ruthenium Uptake of radioruthenium-106 by fish is reported. On a whole fish basis, ruthenium was approximately in equilibrium with ambient seawater during immersion for 200-250 h (Ancellin and Vilquin, 1966, 1968; Ancellin et al., 1967). Gut, gill, and skin tended to concentrate 106Ru (Jones, 1960). The single available datum for stable ruthenium was 0.44 mg/kg in fresh tuna blood (Table 3.14).
3.35 Scandium Scandium concentrations were extremely low in whole teleosts, with a maximum recorded value of 0.16 mg Sc/kg ash weight (Table 3.14).
3.36 Selenium Except for tunas, marlins, billfishes, and liver tissues, all selenium values in fish tissues were generally less than 8.0 mg/kg fresh weight (Table 3.15). For muscle, the mean concentration in the majority of species ranged from 0.4 to 0.9 mg Se/k fresh weight. Livers, however, showed a greatly extended range of 0.6-30.0 mg Se/kg fresh weight, with most values in the 1.0-3.0 mg/kg range. In five species of tunas, the highest levels of selenium recorded were in liver, spleen, and kidney at 10.0-15.0 mg Se/kg fresh weight tissues; lower concentrations of 0.5-1.3 mg Se/kg fresh weight were in muscle (Tamura et al., 1975). Selenium concentrations exceeded those of mercury in all tuna tissues. The lowest Se:Hg molar ratio was about 6 in muscle; this ratio in other organs examined exceeded 100 (Tamura et al., 1975). In black marlin, Makaira indica, there is a significant positive correlation between selenium and mercury concentrations, and both of these elements are positively related to the length of the fish (Mackay et al., 1975). Freeman et al. (1978) observed that the concentration of selenium in swordfish muscle exceeded mercury in all fish having mercury content up to 2.0 mg Hg/kg fresh weight muscle. Studies have shown that selenium lowers the toxic effects of organomercury compounds and Freeman and his colleagues suggest that the use of swordfish should be reviewed, presumably towards liberalizing the then current U.S. Food and Drug Administration concentration of 0.5 mg/kg mercury fresh weight in comestibles. However, at present, mercury concentrations in U.S. seafood products are restricted to less than 0.3 mg total mercury/kg fresh weight (Eisler, 2006). Selenium toxicity to marine teleosts ranged from 0.97 to 17.35 mg/L. The most sensitive species was the sheepshead minnow, C. variegatus, subjected to lifetime selenium exposure with 0.97 mg Se/L being the lowest concentration tested that had a measurable adverse effect (USEPA, 1987b). Fourspine stickleback, Apeltes quadracus, was the most
Fishes 151 Table 3.15: Selenium Concentrations in Field Collections of Fishes Organism Alaska, Adak Island; June 2004 Flathead sole, Hippoglossoides elassodon Kidney Liver Muscle Great sculpin, Myoxocephalus polyacanthocephalus Kidney Liver Muscle Halfbridled goby, Arenigobius frenatus; Australia; industrialized site vs. reference estuary Gonad Muscle Squirefish, Chrysophrys auratus; Australia; 1976; muscle Fish Byproducts Digestive system: 4 spp. Liver 6 spp. 35 spp. 25 spp. 6 spp. 6 spp. 1 spp. Muscle 4 spp. 31 spp. 56 spp. 36 spp 32 spp. 7 spp. 8 spp. Otoliths, 7 spp. Scales, 10 spp. Whole 5 spp. 8 spp. 4 spp. 3 spp.
Concentration
Reference
5.21 FW 2.60 FW 0.40 FW
26 26 26
1.86 FW 2.08 FW 0.61 FW
26 26 26
5.6 DW vs. 4.5 DW 3.6 DW vs. 2.4 DW
29 29
Max. 0.85 FW
22
0.53 (0.21-1.20) FW 1.0-2.4 DW
1 21
0.6-0.9 FW 0.9-2.0 FW 2.0-5.0 FW 5.0-9.0 FW 9.0-20.0 FW 20.0-30.0 FW
2 2 2 2 2 2
0.1-0.3 FW 0.3-0.5 FW 0.5-0.7 FW 0.7-0.9 FW 0.9-2.0 FW 0.1-0.8 FW 0.21-0.50 FW 0.02-0.06 DW 0.17-3.4 DW
2 2 2 2 2 3 4 5 5
0.3-0.6 FW 0.6-0.9 FW 1.0-2.0 FW 0.37-0.50 FW
2 2 2 4
a
(Continues)
152 Chapter 3 Table 3.15: Cont’d Organism
Concentration
Fishmeal, 4 spp. Presscake N-liquor Meal
2.7 DW 15.1 DW 5.3 DW
6 6 6
Fishmeal, 3 spp.
1.05-3.98 DW
7
Atlantic cod, Gadus morhua Skin Liver oil Muscle Tongue Gonads Gills Skin Vertebrae Intestines Stomach contents Gall bladder Liver
8.4 FW 0.13-0.15 FW 0.22 FW 0.25 FW 0.24-0.76 FW 1.0 FW 0.29 FW 0.58 FW 1.2 FW 1.4 FW 0.76 FW 3.67 DW
8 9 1 1 1 1 1 1 1 1 1 10
Goby, Gobius niger Muscle Liver
0.75-1.40 DW 1.6-2.6 DW
11 11
0.3-0.9 FW vs. <0.2-0.7 FW
24
1.4-2.4 DW 1.1-3.4 FW <0.04 FW vs. 0.07-0.20 FW
12 12 13
3.7 FW vs. 4.0 FW 0.33 FW vs. 0.78 FW 6.1 FW vs. 4.8 FW
27 27 27
no data vs. 24.4 FW
27
Greenland; 1975-1991; 5 spp.; liver vs. muscle Atlantic halibut, Hippoglossus hippoglossus Whole fish Meal Aqueous phase Lipid phase; hexane extract vs. hexane/isopropyl extract Indian Ocean; 4 spp.; 2004; Mozambique Channel vs. Reunion Island Common dolphinfish, Coryphaena hippurus Liver Muscle Kidney Skipjack, Katsuwonus pelamis Liver
Reference
a
(Continues)
Fishes 153 Table 3.15: Organism Muscle Kidney Yellowfin tuna, Thunnus albacares Liver Muscle Kidney Swordfish, Xiphias gladius Liver Muscle Kidney
Cont’d
Concentration
Reference
no data vs. 4.5 FW no data vs.14.0 FW
27 27
26.0 FW. vs. 26.8 FW 1.2 FW. vs. 1.6 FW 32.1 FW vs. 32.7 FW
27 27 27
15.3 FW vs. 21.3 FW 0.6 FW vs. 1.2 FW 11.5 FW vs. 23.2 FW
27 27 27
1.4 (0.8-2.2) DW
25
Black marlin, Makaira indica Muscle Liver
2.2 (0.4-4.3) FW 5.4 (1.4-13.5) FW
14 14
Striped bass, Morone saxatilis Muscle Liver
0.3 FW 0.60-0.66 FW
15 15
Bluefish, Pomatomus saltatrix; muscle
0.4 (0.1-0.6) FW
Porgy, Sargus annularis Muscle Liver
0.9-1.4 DW 2.6-6.6 DW
11 11
Chub mackerel, Scomber japonicus; otoliths
0.07-0.28 DW
16
Ocean perch, Sebastes marinus; muscle; N-liquor
4.5 FW
8
Albacore, Thunnus alalunga; muscle
3.3 FW
18
Yellowfin tuna, Thunnus albacares; muscle
0.5 (0.4-0.7) FW
Southern bluefin tuna, Thunnus maccoyii; Australia; April 2004; muscle; wild vs. farmed
1.3 (1.1-1.6) FW vs. 0.93 (0.62-1.1) FW
28
Bluefin tuna, Thunnus thynnus Whole meal Aqueous phase Lipid phase; hexane extract vs. hexane/isopropanol extract
2.6-33.0 DW 1.5-70.0 FW 0.1-7.6 FW vs.0.3-13.9 FW
19 19 19
Tuna, canned
1.9-2.9 DW
20, 23
Pinfish, Lagodon rhomboides; Texas; 1986-1987; whole
a
3
3
(Continues)
154 Chapter 3 Table 3.15: Cont’d Organism Swordfish, Xiphias gladius Muscle Azores area vs. Equator area; 2005 Muscle Liver
Concentration
Reference
0.29-1.27 FW
17
0.18-1.2 FW vs. 0.36-0.73 FW 2.3-9.7 FW vs. 2.5-15.0 FW
23 23
a
Values are in mg Se/kg fresh weight (FW) or dry weight (DW). a 1, Julshamn et al., 1978b; 2, Hall et al., 1978; 3, Bebbington et al., 1977; 4, Kari and Kauranen, 1978; 5, Papadopoulu and Kassimati, 1977; 6, Lunde, 1968b; 7, Kifer and Payne, 1968; 8, Lunde, 1970; 9, van de Ven, 1978; 10, Egaas and Julshamn, 1978; 11, Grimanis et al., 1978; 12, Lunde, 1973c; 13, Lunde, 1973b; 14, Mackay et al., 1975; 15, Heit, 1979; 16, Papadopoulu et al., 1980; 17, Freeman et al., 1978; 18, Orvini et al., 1974; 19, Lunde, 1973d; 20, Ganther et al., 1972; 21, Maher, 1983; 22, Chvojka et al., 1990; 23,Branco et al., 2007; 24, Dietz et al., 1996; 25; Custer and Mitchell, 1993; 26, Burger et al., 2007a; 27, Kojadinovic et al., 2007; 28, Padula et al., 2008; 29, Roach et al., 2008.
resistant with an LC50 (96 h) value of 17.35 mg/L (USEPA, 1980a); intermediate in resistance were pinfish (Ward et al., 1981a,b), larvae of haddock (Melanogrammus aeglifinus and summer flounder (P. dentatus) (USEPA, 1980a), and striped bass, M. saxatilis—with selenite being six times more toxic to striped bass than selenate (USEPA, 1987a,b).
3.37 Silver Silver concentrations in fish tissues seldom exceeded 0.2 mg/kg DW muscle, 0.5 mg/kg FW liver, and 0.2 mg/kg DW whole fish (Table 3.16). Livers of Atlantic cod, G. morhua, contain significantly more silver than muscle or ovaries (Table 3.16); a similar pattern is evident in other species of marine teleosts analyzed (Garnier et al., 1990; Hellou et al., 1992; Szefer et al., 1993). Biomagnification of silver through the food chain in offshore populations of teleosts is rare, even among specimens collected from dumpsites impacted by substantial quantities of trace metals, including silver. For example, of seven fish species captured from the New York Bight ocean disposal site and examined for silver content, muscle of the blue hake, Antimora rostrata, contained the highest concentrations of all species examined at 0.15 mg Ag/kg fresh weight (Greig et al., 1976). Similarly, the elevated silver content in winter flounder, P. americanus of 0.8 mg/kg fresh weight (Table 14.16) was from a specimen collected from the same general area (Greig and Wenzloff, 1977b). Laboratory studies with radiosilver show that whole fish take up 110mAg from seawater by factors up to 40 over a period of 98 days (Pouvreau and Amiard, 1974). Exposure of plaice, P. platessa, to 0.04 mg Ag/L for 2 months resulted in elevated silver concentrations in gut contents of 0.49 mg Ag/kg fresh weight; however, all other tissues examined—including
Fishes 155 Table 3.16: Silver Concentrations in Field Collections of Fishes Organism
Concentration
Blue hake, Antimora rostrata; muscle
0.15 FW
1
<0.1 FW 0.1-0.3 FW 0.3-0.6 FW
2 2 2
Fish Liver 66 spp. 12 spp. 4 spp. Muscle 158 spp. 1 sp. 3 spp.; Arabian Sea; 1987-1988 7 spp.; Louisiana Scales, 7 spp. Whole 10 spp. 7 spp. 3 spp. 1 sp.
<0.1 FW 0.1-0.2 FW 0.29-0.53 FW 0.1 DW 0.001-0.300 DW <0.1 FW 0.1-0.2 FW <1.0 AW 4.4 AW
Reference
a
2 2 12 13 3 2 2 4 4
Halfbridled goby, Arenigobius frenatus; Australia; industrialized site vs. reference estuary Gonad Muscle
0.11 DW vs. <0.007 DW 0.032 DW vs. <0.001 DW
17 17
Blackfin icefish, Chaenocephalus aceratus; Antarctica; February-March 1989 Liver Muscle
0.05 DW 0.01 (0.008-0.012) DW
11 11
Atlantic cod, Gadus morhua; Newfoundland; November 1990-March 1991; females; maximum concentrations Liver Muscle Ovaries
1.49 DW; 0.44 FW 0.3 DW; 0.02 FW 0.32 DW; 0.04 FW
14 14 14
Guam; 10 spp.; 1998-1999; 4 stations; max. concentrations Muscle Liver
0.28 DW 5.1 DW
15 15 (Continues)
156 Chapter 3 Table 3.16: Cont’d Organism
Concentration
Dover sole, Microstomus pacificus; muscle; near wastewater outfall vs. reference site
0.2 DW vs. 0.1 FW
5
0.003 FW 0.080 FW
6 6
Striped bass, Morone saxatilis Muscle Liver Hump rock cod, Notothenia gibberfrons; Antarctica; FebruaryMarch 1989; muscle
Reference
0.014 (0.012-0.016) DW
11
Papua New Guinea; 5 spp.; tropical deepwater fishes; 1999-2002 Muscle Liver
0.01 FW 0.07 FW
16 16
Winter flounder, Pleuronectes americanus Liver Muscle
<0.1-0.8 FW <0.1 FW
7 7
0.008-0.330 DW
8
Windowpane, Scopthalmus aquosus Muscle Liver
<0.1 FW <0.1-0.5 FW
9 9
Red hake, Urophycis chuss Liver Muscle
<0.1-0.5 FW <0.1 FW
7 7
White hake, Urophycis tenuis Muscle Liver
<0.1 FW 0.18-0.32 DW
7 10
Chub mackerel, Scomber japonicus; otoliths
a
Values are in mg Ag/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Greig et al., 1976; 2, Hall et al., 1978; 3, Papadopoulu and Kassimati, 1977; 4, Robertson, 1967; 5, McDermott et al., 1976; 6, Heit, 1979; 7, Greig and Wenzloff, 1977a; 8, Papadopoulu et al., 1980; 9, Greig et al., 1977; 10, Greig, 1975; 11, Szefer et al., 1993; 12, Tariq et al., 1993; 13, Ramelow et al., 1989; 14, Hellou et al., 1992; 15, Denton et al., 2006; 16, Brewer et al., 2007; 17, Roach et al., 2008.
blood cells, blood plasma, heart, spleen, kidney, gut, gill filament, skin, bone, and muscle— contained at least an order of magnitude less silver than gut contents (Pentreath, 1977b). Plaice fed nereid worms labeled with 110mAg retained about 4.2% of the ingested dose after 3 days (Pentreath, 1977b), and suggests that the high concentration factors reported by Pouvreau and Amiard (1974) may have been due to loosely bound adsorbed silver.
Fishes 157 Silver ion (Ag+) was the most toxic chemical species tested to fishes. The general order of toxicity was Ag+ > silver chloride >> silver sulfide > silver thiosulphate. In all cases, toxicity reflected the free silver ion content of tested compounds (Eisler, 2000f). Ionic silver caused respiratory depression in cunners, Tautogolabrus adspersus (Gould and MacInnes, 1977). Silver interferes with sodium and chloride regulation in gills. In seawater, unlike freshwater, plasma Na+and Cl concentrations rise rather than fall, and death may result from the elevated Na+and Cl concentrations combined with dehydration (Hogstrand and Wood, 1998). Osmoregulatory failure occurs in marine teleosts exposed to high concentrations of Ag+, the intestine being the main toxic site of action (Wood et al., 1999). In tidepool sculpins, Oligocottus maculatus, ionic silver was more toxic at lower salinities, longer exposure durations, and increasing medium ammonia concentrations; however, there was no correlation between whole body silver content and survival at 25 ppt salinity, and no uptake at 32 ppt salinity (Shaw et al., 1998). Ionic silver was lethal to the comparatively sensitive larvae of the summer flounder, P. dentatus, at 0.0047 mg/L (USEPA, 1980e), to mottled sculpin, Cottus bairdi, at 0.0053 mg/L (USEPA, 1980e), to winter flounder, P. americanus, at 0.092 mg/L (USEPA, 1980e), to the Atlantic silverside, M. menidia, at 0.11 mg/L (USEPA, 1980e), to the tidepool sculpin at 0.12 mg/L (Shaw et al., 1998), and to juvenile sheepshead minnow, C. variegatus, at 1.4 mg/L (USEPA, 1980e). Inland silversides, Menidia beryllina, were subjected to various silver concentrations for 28 days at salinities of 10, 20, or 30 ppt, and up to 6 mg/L of dissolved organic carbon (Ward et al., 2006). Silver was less toxic at higher salinities, with LC-20 concentrations of 0.038 mg dissolved Ag/L at 10 ppt and 0.17 mg/L at 30 ppt; organic carbon had no significant effect on toxicity. Chronic toxicity values for silver in seawater, based on growth inhibition, were not affected when silver was also added to the food (Ward et al., 2006). The proposed silver criterion for marine life protection is less than 0.032 mg total Ag/L and less than 0.027 mg dissolved Ag/L (Ward et al., 2006).
3.38 Strontium Strontium concentrates in bony or calcareous tissues, especially in bottom-dwelling species and in older fish (Table 3.17). Otoliths of masou salmon, Oncorhynchus masou, from coastal environments had significantly higher strontium concentrations than did freshwater conspecifics; the Sr/Ca ratio in sea-run salmon was 3900-5000 versus 2500-2700 in freshwater residents (Ohji et al., 2007b). Otoliths from Japanese eels, A. japonica, with highest Sr/Ca ratios are indicative of the longest oceanic residence times (Ohji et al., 2007a; Tzeng et al., 2002). The Sr/Ca ratio in Japanese eel otoliths is positively correlated with ambient salinity, negatively correlated with increasing fish growth rate, and unaffected by diet (Lin et al., 2007). Otoliths from juvenile flatfishes collected from estuaries along the
158 Chapter 3 Table 3.17: Strontium Concentrations in Field Collections of Fishes Organism
Concentration
Baltic herring, Clupea harengus; whole
3.1 DW
7
420.0 AW vs. 630.0 AW 0.01-0.06 FW 200.0 AW vs. 100.0 AW
1 3 1
150.0 AW vs. 1900.0 AW 130.0 AW vs. 300.0 AW
1 1
130.0 AW vs. 300.0 AW
1
Mummichog, Fundulus heteroclitus; whole; different lengths 46 mm 61 mm 77 mm 88 mm 106 mm 119 mm
210.0 AW 248.0 AW 244.0 AW 255.0 AW 313.0 AW 331.0 AW
4 4 4 4 4 4
Pandora, Pagellus erythrinus Fins Eyes Eggs Gills Brain Liver Intestine Spleen Muscle Skin Bone Whole
11.0 DW 2.4 DW 7.2 DW 7.5 DW 11.0 DW 5.3 DW 6.9 DW 34.0 DW 8.0 DW 10.0 DW 32.0 DW 8.4 DW
5 5 5 5 5 5 5 5 5 5 5 5
<200.0 FW vs. >300.0 FW
6
1100.0-1600.0 AW 150.0-350.0 AW
2 2
Fish Bone; pelagic species vs. bottom fish Bone, 6 spp. Muscle; pelagic species; white muscle vs. dark muscle Skin; pelagic species vs. bottom fish Viscera; pelagic species vs. bottom fish Whole; plankton feeders vs. bottom fish
Brown trout, Salmo trutta; scales; freshwater race vs. seawater race Tunas, 4 spp. Bone Muscle
Reference
a
Values are in mg Sr/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Lowman et al., 1970; 2, Fukai et al., 1962; 3, Mauchline and Templeton, 1966; 4, Eisler and LaRoche, 1972; 5, Papadopoulu et al., 1978b; 6, Bagenal et al., 1973; 7, Zumholz et al., 2006.
Fishes 159 California coast in 1999-2000 had higher strontium concentrations than did conspecifics from offshore sites; the reverse was observed for lithium (Brown, 2006). Laboratory studies with radiostrontium isotopes confirm that strontium has an affinity for calcareous tissues (Amiard, 1975; Hiyama and Shimizu, 1964; Martin and Goldberg, 1962). In studies with plaice, P. platessa, strontium uptake during the first 12 days was mainly by soft tissues; later, strontium accumulated in hard tissues (Amiard, 1975). Strontium accumulation rates in plaice were lower at colder temperatures and higher salinities, and with increasing sediment load in the experimental aquaria; however, concentrations of calcium had little influence on strontium accumulation rates within the limits tested (Amiard, 1975). Pacific mackerel, Pneumatophorus diego, excreted 95% of the radiostrontium ingested via the diet within 24 h; the remaining 5% concentrated in the calcareous portions of the fish (Martin and Goldberg, 1962). Results of studies with radiostrontim-86 to measure the relative contributions of seawater and diet to strontium deposited in otoliths of juvenile mummichogs, F. heteroclitus, demonstrated that water chemistry is the dominant route (Walther and Thorrold, 2006).
3.39 Tellurium Concentrations of tellurium in muscle and liver of striped bass, M. saxatilis, were near analytical detection limits of 0.10-0.14 mg Te/kg fresh weight (Table 3.18).
3.40 Thallium Thallium concentrations in fish tissues were near or below detection limits of 0.10-0.14 mg Tl/kg fresh weight (Table 3.18).
3.41 Tin Total tin concentrations in most species of marine products of commerce from U.S. coastal waters ranged from 0.4 to 0.8 mg Sn/kg fresh weight in muscle and 0.3-0.7 mg Sn/kg fresh weight in liver; tin concentrations were usually higher in whole finfish—and higher in larger fish when compared to smaller conspecifics (Said et al., 2006)—with most species containing 0.8-2.0 mg total Sn/kg fresh weight (Table 3.18). Total maximum organotin concentrations in edible portions of fish sold for human consumption in France between January and April 2005 were 0.0139 mg/kg fresh weight for canned fish, 0.0063 for smoked fish, and 0.0232 mg/kg fresh weight for fresh and frozen fish; in all cases, butyltins— especially the highly toxic tributyltins (TBTs)—accounted for most of the organotin burden (Table 3.18; Guerin et al., 2007). However, triphenyltin concentrations in muscle from six species of commercial teleosts collected from Bohai Bay, China, in 2002 were always higher than TBT concentrations, suggesting trophic magnification of triphenyltins through the algae-invertebrate (mollusc, crustacean)-fish food chain (Hu et al., 2006).
160 Chapter 3 Table 3.18: Tellurium, Thallium, Tin, Titanium, and Tungsten Concentrations in Field Collections of Fishes Element and Organism
Concentration
Reference
a
Tellurium Striped bass, Morone saxatilis Muscle Liver
0.10 FW 0.14 FW
1 1
0.10 FW 0.14 FW
1 1
Thallium Striped bass, Morone saxatilis Muscle Liver Tin Japanese eel, Anguilla japonica; liver; 2003-2004; Tokushima region, Japan; total butyltins vs. total phenyltins Sea-run Estuarine Freshwater
0.73 FW vs. 0.22 FW 0.30 FW vs. 0.12 FW 0.13 FW vs. 0.09 FW
17 17 17
Bohai Bay, North China; 2002; muscle; 6 spp.; tributyltins vs. triphenyltins
0.001-0.007 FW vs. 0.007-0.035 FW
18
Pacific herring, Clupea harengus pallasi; whole; Vancouver, Canada; 1984 Inorganic tin Butyltin Dibutyltin Tributyltin
0.04 FW 0.06 FW 0.05 FW 0.24 FW
Sparid, Diplodus sargus; whole; Alexandria, Egypt; 2004; body weight 91 g vs. 201 g Dibutyltins Tributyltins Diphenyltins Total tin
0.010 DW vs. 0.016 DW 0.044 DW vs. 0.052 DW 0.010 DW vs. 0.043 DW 0.13 DW vs. 0.24 DW
Fish Liver 1 sp. 26 spp. 25 spp. 20 spp. 10 spp.
<0.1 FW 0.2-0.4 FW 0.4-0.6 FW 0.6-0.8 FW 0.8-2.0 FW
7 7 7 7
11 11 11 11
2 2 2 2 2 (Continues)
Fishes 161 Table 3.18: Element and Organism Muscle 2 spp. 6 spp. 35 spp. 75 spp. 23 spp. 11 spp. 4 spp. 3 spp. 10 spp.; Mumbai, India; 2004-2005; tributyltin Whole 2 spp. 12 spp. 3 spp. France; January-April 2005; commercial seafood products; organotins Fresh and frozen fish; edible portions Total organotins; 25 spp. Swordfish, unidentified Total organotins Butyltins Phenyltins Octyltins Halibut, unidentified Total organotins Butyltins Phenyltins Octyltins Seabass, unidentified Total organotins Butyltins Phenyltins Octyltins Canned fish; 6 spp.; total organotins Smoked fish; 4 spp.; total organotins Atlantic cod, Gadus morhua; total tin; muscle
Cont’d
Concentration
0.2-0.3 FW 0.3-0.4 FW 0.4-0.5 FW 0.5-0.6 FW 0.6-0.7 FW 0.7-0.8 FW 0.8-0.9 FW 1.0-2.0 FW 0.024 FW; 95th percentile 0.028 FW
Reference
2 2 2 2 2 2 2 2 19
0.3-0.6 FW 0.8-2.0 FW 2.0-9.0 FW
2 2 2
<0.009 FW
12
0.019 FW 0.017 FW 0.002 FW 0.0003 FW
12 12 12 12
0.023 FW 0.019 FW 0.001 FW 0.001 FW
12 12 12 12
0.011 FW 0.007 FW 0.004 FW 0.0005 FW 0.004-0.014 FW 0.001-0.006 FW
12 12 12 12 12 12
(0.6-3.7) FW
a
8 (Continues)
162 Chapter 3 Table 3.18: Cont’d Element and Organism
Concentration
Atlantic halibut, Hippoglossus hippoglossus, muscle; total tin
1.2 FW
8
0.30 FW 0.33 FW
1 1
Striped bass, Morone saxatilis Muscle Liver Striped mullet, Mugil cephalus, Mediterranean Sea; Morocco; inshore vs. open sea Liver Total butyltins Total phenyltins Muscle Total butyltins Total phenyltins Masou salmon, Oncorhynchus masou; sea-run; tributyltin, expressed as Sn4+ Liver Muscle Gill Ovary
Reference
0.004-0.018 FW vs. <0.0001 FW 0.0003-0.003 FW vs. <0.0006 FW
14
0.0005-0.006 FW vs. <0.0002 FW 0.00005-0.0004 FW vs. <0.0002 FW
14
0.012 FW 0.007 FW 0.006 FW 0.003 FW
16 16 16 16
14
14
Starry flounder, Platichthys stellatus; British Columbia; muscle; 1992-1993
0.04-0.06 DW
9
Winter flounder, Pleuronectes americanus; muscle; total tin
3.2 FW
8
Cobia, Rachycentron canadum; Taiwan; cultured; 2003-2004; butyltins Body weight 3.4 kg Skin Total Monobutyltins Butyltins Tributyltins Liver Total Monobutyltins Dibutyltins
a
0.877 FW 0.122 FW 0.227 FW 0.228 FW
13 13 13 13
0.984 FW 0.223 FW 0.761 FW
13 13 13 (Continues)
Fishes 163 Table 3.18: Element and Organism Tributyltins Dorsal muscle Total Monobutyltins Dibutyltins Tributyltins Dark muscle Total Monobutyltins Dibutyltins Tributyltins Body weight 4.8 kg Skin Total Monobutyltins Tributyltins Dorsal muscle Total Monobutyltins Tributyltins Dark muscle Total Monobutyltins Dibutyltins Tributyltins Atlantic salmon, Salmo salar; (farmed) Muscle Gonad Gill Kidney Liver Taiwan; 2001-2004; 31 spp. Tributyltins Muscle Viscera Whole Triphenyltins Muscle Viscera Whole
Cont’d
Concentration
Reference
not detected
13
0.688 FW 0.109 FW 0.242 FW 0.338 FW
13 13 13 13
0.656 FW 0.072 FW 0.315 FW 0.269 FW
13 13 13 13
0.710 FW 0.124 FW 0.506 FW
13 13 13
0.472 FW 0.135 FW 0.337 FW
13 13 13
0.803 FW 0.180 FW 0.209 FW 0.414 FW
13 13
0.07 FW 0.15 FW 0.03 FW 0.06 FW 0.04 FW
10 10 10 10 10
0.267 (0.004-3.39) FW 0.371 (<0.01-1.82) FW 0.470 (<0.01-1.41) FW
15 15 15
Max. 3.77 FW <0.5 FW (<0.5-4.86) FW
15 15 15
a
13
(Continues)
164 Chapter 3 Table 3.18: Cont’d Element and Organism Tributyltins vs. triphenyltins; muscle Reef species Demersal species Pelagic species Total Southern bluefin tuna, Thunnus maccoyii; muscle; Australia; April 2004; wild vs. farmed
Concentration
0.566 FW 0.226 FW 0.134 FW 0.309 FW
vs. vs. vs. vs.
0.338 FW 0.229 FW 0.600 FW 0.389 FW
No data vs. <0.02 FW
Reference
a
15 15 15 15 20
Titanium Dab, Limanda limanda; skin plus muscle
2.3-3.1 FW
3
Fishmeal, 4 spp. Presscake N-liquor Meal
<0.005 DW <0.005 DW 0.030 DW
4 4 4
Mackerel, Pneumatophorus sp. Muscle Muscle
<0.014 AW <0.006 DW
5 6
Tungsten
Values are in mg element/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Heit, 1979; 2, Hall et al., 1978; 3, Newell et al., 1979; 4, Lunde, 1968b; 5, Fukai and Meinke, 1959; 6, Fukai and Meinke, 1962; 7, Maguire et al., 1986; 8, Jenkins, 1980b; 9, Stewart and Thompson, 1994; 10, Davies and McKie, 1987; 11, Said et al., 2006; 12, Guerin et al., 2007; 13, Liu et al., 2006b; 14, Hassani et al., 2006; 15, Lee et al., 2006; 16, Ohji et al., 2007b; 17, Ohji et al., 2007a; 18, Hu et al., 2006; 19, Mishra et al., 2007; 20, Padula et al., 2008.
Striped mullet, M. cephalus, from inshore locales of the Mediterranean Sea contained up to 0.018 mg total butyltins/kg FW liver and up to 0.006 mg total butyltins/kg FW muscle; total triphenyltins ranged up to 0.003 mg/kg FW liver and 0.0004 mg/kg FW muscle (Hassani et al., 2006; Table 3.18). Concentrations from offshore locations were significantly lower. In all samples, TBT was the dominant butyltin compound and triphenyltin was the dominant phenyltin (Hassani et al., 2006). TBT concentrations were highest in muscle of fish collected from Taiwanese harbors in 2001-2004 (up to 3.38 mg TBT/kg FW), being higher than maximum concentrations reported in fish muscle from Germany (0.202 mg TBT/kg FW; Shawky and Emons, 1998), Australia (0.013; Kannan et al., 1995), Sri Lanka (1.7; Guruge and Tanabe, 2001), Korea (0.01; Shim et al., 2002), and Japan (0.18 mg TBT/kg FW muscle; Takahashi et al., 1998). In masou salmon, O. masou, organotin concentrations differed significantly among tissues, migratory habitats, and chemical species (Ohji et al., 2007b). TBT concentrations were highest in sea-run salmon, with values of 0.012 mg/kg FW in liver, 0.007 in muscle, 0.006 in
Fishes 165 gill, and 0.003 mg/kg FW in ovary. Triphenyltin concentrations in sea-run salmon were significantly lower than TBT concentrations in all tissues. Among freshwater resident salmon, both TBT and TPT concentrations were significantly lower than sea-run conspecifics (Ohji et al., 2007b). In the Japanese eel, A. japonica, concentrations of total butyltins and total phenyltins in livers of mature eels were significantly higher than those in immature eels and higher in sea-run eels than freshwater conspecifics; the risk of organotin contamination increases with increasing length of sea residence (Ohji et al., 2007a). Antifouling paints containing TBT compounds are used widely on netting panels of sea cages at fish and shellfish aquaculture units to minimize the obstruction of water exchange through the cages (Davies et al., 1987). Atlantic salmon, S. salar, held for 3 months during summer in cages with TBT-treated net panels contained 0.75-1.5 mg TBT/kg fresh weight muscle versus 0.28 mg/kg at the start (Davies and McKie, 1987). Based on laboratory studies, it is probable that Atlantic salmon were exposed to about 0.001 mg TBT/L during the interval (Davies and McKie, 1987). Chinook salmon, Oncorhynchus tshawytscha, reared in sea pens treated with TBT paints contained <0.013 mg TBT/kg muscle FW when introduced into the pens (Short and Thrower, 1986). TBT concentrations in chinook muscle were 0.3 mg/kg after 3 months, 0.8 at 13 months, and 0.9 mg TBT/kg FW muscle at 19 months. Cooking did not destroy or remove organotins from salmon muscle (Short and Thrower, 1986). Pink salmon, Oncorhynchus gorbuscha, and chum salmon, Oncorhynchus keta, fry cultured in TBT-treated marine net pens for 20-68 days prior to ocean release contained mean concentrations of 1.5 mg Sn/kg FW whole fry (chum) and 2.7 mg/kg FW (pinks) versus <0.1 in controls; however, growth and survival were normal and returning adults 1-3 years later had no detectable TBT (Thrower and Short, 1991). TBT at environmentally realistic levels can inhibit ovarian development in fish (Zhang et al., 2007). Female Cuvier (Sebastiscus marmoratus held in seawater containing 0.000001, 0.00001, or 0.0001 mg TBT/L for 50 days had elevated testosterone levels (all groups), and a reduction in ovarian vitellogenic follicles (0.00001 mg/L group). At the highest dose level of 0.0001 mg TBT/L, follicles were at the earliest stage of development (Zhang et al., 2007). TBT oxide is also involved in the suppression of fish spermatogenesis (Mochida et al., 2007). Mummichogs, F. heteroclitus, exposed to 0.008 mg TBT/L for 2 weeks showed severe histological damage to the testis, including reduction in spermatids and spermatozoa, and malformation of somatic cells around the seminal duct (Mochida et al., 2007). Tributyltin oxide (TBTO) causes sex reversal in fish; specifically, masculinization of Japanese flounders, Paralichthys olivaceus, exposed to TBTO via the diet (Shimasaki et al., 2003). In that study, genetically female Japanese flounders were fed diets containing TBTO at concentrations of 0.1 or 1.0 mg TBTO/kg diet from age 35-100 days after hatching, which includes the sex differentiation period. The ratio of sex-reversed males was 2.2% in the control group, 25.7% in the 0.1 mg TBTO/kg group, and 31.1% in the 1.0 mg TBTO/kg group. This may be the first
166 Chapter 3 case of TBT-induced sex reversal in vertebrates (Shimasaki et al., 2003). Other studies with Japanese flounders show altered lysozyme activity in kidney and plasma after exposure to 0.001-0.002 mg TBT/L for 14-28 days; after exposure, blood contained 0.017 mg TBT/L FW in controls, 1.98 mg/kg FW in the 0.001 mg/L group, and 4.45 mg/kg FW in the 0.002 mg/L group (Nakayama et al., 2007). Organotins are persistent in sediments and biota. Fish, shellfish, and sediment samples from southwestern British Columbia in 1992-1993 contained TBT and its metabolites dibutyltin and monobutyltin, strongly suggesting that TBT is a widespread contaminant in this geographic area and a continuing cause for concern despite restrictions on the use of organotin-based marine antifouling paints imposed in 1989 (Stewart and Thompson, 1994). Organotin content is fish tissues is variable, ranging from a maximum of 18% of the total body tin burden in goatfish, Upeneus moluccensis (Tugrul et al., 1983) but only 5% in M. barbatus, another species of goatfish (Salihoglu et al., 1987). TBTs are highly toxic to fish and other aquatic organisms, readily accumulate in fish and molluscs from contaminated localities, and are present in harbors and marinas where their release from antifouling paints applied to small boats and recreational craft is the putative source (Eisler, 2000g; Laughlin et al., 1986; USEPA, 1986; Walsh et al., 1985). LC50 (96 h) values for TBT are reported for larvae of the sole, Solea solea, at 0.002 mg/L (Hall and Pinkney, 1985), for speckled sanddab, C. stigmaeus, at 0.02 mg/L (Hall and Pinkney, 1985), and for the mummichog, F. heteroclitus, at 0.024 mg/L (Champ, 1986). Avoidance behavior was documented for the mummichog at 0.0009 mg TBT/L (Hall and Pinkney, 1985) and juvenile Atlantic menhaden, Brevoortia tyrannus, at 0.015 mg TBT/L (Hall and Pinkney, 1985). American plaice, Hippoglossoides platessoides, given a single oral dose of 113Sn-TBT showed 113Sn distribution over the entire body, especially liver and gallbladder, with steady state achieved in 5-10 days; average retention efficiency of TBT over a 6-week period was 44%, with half-time persistence of 15-77 days (Rouleau et al., 1998). Red sea bream, P. major, fed TBT or triphenyltin compounds in the diet at 0.008-1.0 mg Sn/kg ration for 8 weeks, and simultaneously challenged with seawater containing 0.000067-0.000083 mg/L of triorganotin compounds took up 25% of their whole body tin burden from the diet, regardless of tin concentration or chemical species in the ration. TBT assimilation in red sea bream was 10% and retention 24%; for triphenyltin, assimilation was 13% and retention 60% (Yamada et al., 1994). Sheepshead minnows, C. variegatus, held for 167 days in seawater containing 0.0000180.001 mg TBT/L had maximum BCFs of 1600 in muscle, 3900 in viscera, and 52,000 in liver; no adverse effects on growth or reproduction were noted (Ward et al., 1981a,b). Sheepshead minnows were unable to reach equilibrium in a medium containing 0.0016 mg TBT/L after 58 days of exposure with maximum BCF values of 2600 in whole fish, 1810 in muscle, 4500 in viscera, and 2120 in head; however, whole body loss was 52% after depuration for 7 days in
Fishes 167 clean seawater, and 74% in 28 days (Ward et al., 1981a,b). The LC50 (21 days) value for TBT and sheepshead minnow was 0.000096 mg/L (Thompson et al., 1985). However, sheepshead minnows rapidly metabolize TBT into lower alkyl moieties of reduced toxicity; thus, even though significant uptake from the medium occurred, the chronic toxicity of TBTs to this species was the same as its acute toxicity (Ward et al., 1981a,b). Organotin accumulation by way of the diet is low and occurs mainly via hydrophobic mechanisms; elimination is also low and follows metal-like kinetics pathways (Veltman et al., 2006). Biomagnification of organotins from annelid to fish, and fish to fish, is low. In the case of lugworm, A. marina, to various species of fish (sand lance, Ammodytes sp.; gray gurnard, Eutrigla gurnardus; plaice, P. platessa; herring, Clupea spp.; black goby, Gobius niger), mean biomagnification factors are 0.8 for TBTs and 3.4 for triphenyltins. In a fish to fish food chain (whiting, Merlangius merlangus and plaice on sand lance and herring), mean biomagnification is 0.2 for TBTs and 0.4 for triphenyltins (Veltman et al., 2006). Exposure to TBT may alter both cytochrome P450-dependent metabolism, and induction response to other environmental pollutants (Fent and Stegeman, 1993). Studies with scup, Stenotomus chrysops, show that an intraperitoneal injection of 3.3, 8.1, or 16.3 mg TBT/kg body weight results in a dose-dependent decrease in liver microsome ethoxyresorufin O-deethylase activity, cytochrome P450 degradation to P420, and an increase in liver tin concentrations from 8.0 to 202.0 mg Sn/kg FW (Fent and Stegeman, 1993). TBT compounds also modify calcium flux across the plasma membrane in a dose-dependent manner in oyster toadfish, O. tau (Rice and Weeks, 1990). At 0.05 mg/L, TBT facilitated an inward flux of calcium. At 0.5 mg/L, calcium mobilization was inhibited, resulting in impaired macrophage function (Rice and Weeks, 1990). Interaction of TBT with benzo[a]pyrene (BaP) is documented (Ribeiro et al., 2007). Arctic charr, S. alpinus, given intraperitoneal injections of 0.3 mg TBT/kg body weight daily for 54 days inhibited the metabolism of coadministered BaP (3.0 mg/kg BW); BaP, in turn, stimulated the metabolism and excretion of TBT. These fish had a higher frequency of lesions among BaP-exposed fish when compared with charr exposed to TBT alone or combined with BaP, and suggests that TBT can antagonize BaP toxicity in charr exposed to both compounds. In contrast, BaP does not seem to provide protection against TBT toxicity (Ribeiro et al., 2007). The most stringent criteria proposed for triorganotins and marine life protection range from 0.000002 to 0.000017 mg/L medium (Eisler, 2000g; Hall et al., 1987; Side, 1987), and <0.001-<0.007 mg/kg sediment (Cardwell and Sheldon, 1986).
3.42 Titanium The single datum available shows that flounder muscle contains up to 3.1 mg Ti/kg fresh weight (Table 3.18); however, this needs verification.
168 Chapter 3
3.43 Tungsten The highest tungsten value recorded from available limited data is 0.03 mg W/kg dry weight in fish meal from Norway; all other determinations of tungsten in fish tissues were below analytical detection limits of the procedures used (Table 3.18).
3.44 Uranium Whole Baltic herring, C. harengus contained 0.00086 mg U/kg DW (Zumholz et al., 2006). Atlantic salmon, S. salar, cultured in marine rearing areas, were fed diets containing 0.05 mg U/kg DW; feces contained 0.14 mg U/kg DW (Dean et al., 2007), suggesting little accumulation.
3.45 Vanadium Maximum vanadium values recorded in economically important North American finfish tissues, in mg V/kg fresh weight, are 6.0 in liver, 2.0 in edible muscle, and 3.0 in whole fish (Table 3.19). Vanadium concentrations were below the detection limit in muscle of the mackerel, P. japonicus, collected from the coast of Japan (Fukai and Meinke, 1962). Gilthead bream, Sparus aurata, were injected intravenously with approximately 0.5 mg/kg body weight of V5+or V10+, labeled with 51V (Soares et al., 2006). In bream cardiac muscle, the vanadium distribution is dependent on the administration of decameric vanadate (V 10+), with vanadium being mainly distributed in plasma prior to transfer into the mitochondrial fraction. After 1-h postinjection, blood contained 295.0 mg V5+/kg DW plasma, and 383.0 mg V10+/kg DW plasma; after 12 h, vanadium in plasma decreased about 50% for both vanadium isomers (Soares et al., 2006).
3.46 Yttrium Whole Baltic herring, C. harengus, contained 0.00014 mg Y/kg DW (Zumholz et al., 2006). Only about 2% of an ingested dose of 91Y remained in Tilapia mossambica 2 days postexposure. This was much lower than the amount of strontium retained by Tilapia in similar studies. About 40% of the yttrium concentrated in viscera, 30% in muscle, 20% in skeleton, and 5% in gills; these findings were in marked contrast with those obtained with strontium in similar studies wherein strontium concentrated heavily in calcareous tissues (Boroughs et al., 1956a,b).
Fishes 169 Table 3.19: Vanadium Concentrations in Field Collections of Fishes Organism Fish Liver 18 spp. 22 spp. 16 spp. 5 spp. 6 spp. 12 spp. 3 spp. Muscle 17 spp. 68 spp. 64 spp. 7 spp. 3 spp. Whole 10 spp. 4 spp. 7 spp. 6 spp.
Concentration
Reference
<0.1 FW 0.1-0.3 FW 0.3-0.5 FW 0.5-0.7 FW 0.7-0.9 FW 0.9-2.0 FW 2.0-6.0 FW
1 1 1 1 1 1 1
<0.1 FW 0.1-0.3 FW 0.3-0.5 FW 0.5-0.7 FW 0.7-2.0 FW
1 1 1 1 1
Max. 0.112 FW <0.1-0.4 FW 0.4-0.7 FW 0.7-3.0 FW
2 1 1 1
Striped bass, Morone saxatilis Muscle Liver
0.03 FW 0.04 FW
3 3
Chub mackerel, Scomber japonicus Muscle Liver
0.014 DW 0.024 DW
4 4
Blackfin tuna, Thunnus atlanticus; otoliths
0.00095 DW
5
Mediterranean scad, Trachurus mediterraneus; muscle
0.071-0.150 DW
4
a
Values are in mg V/kg fresh weight (FW) or dry weight (DW). a 1, Hall et al., 1978; 2, Ikebe and Tanaka, 1979; 3, Heit, 1979; 4, Papadopoulu et al., 1978b; 5, Arslan and Secor, 2008.
3.47 Zinc Zinc is ubiquitous in the tissues of plants and animals (Rosser and George, 1986) and is essential for normal growth, reproduction, and wound healing (Stahl et al., 1989). More than 200 different enzymes require zinc for maximum catalytic activity (Eisler, 2000h; Thompson et al., 1989). Early interest in the environmental behavior of zinc was stimulated by the observation of Japanese scientists that 65Zn from fallout was concentrated strongly in tunas.
170 Chapter 3 Subsequently, the nuclide was reported in large amounts in many species of marine organisms when compared to ambient seawater. Stable zinc concentrations in benthic fishes collected from the outer Continental Shelf off Oregon, USA, were uniformly low, with little variation between species (Vanderploeg, 1979). However, radiozinc content varied widely in these same species and was attributed to differences in specific activity of prey organisms (Vanderploeg, 1979). Concentrations of stable zinc in representative species of finfish are listed in Table 3.20. In general, marine vertebrates—including elasmobranchs and fishes—have low zinc burdens in tissues (usually 6.0-400.0 mg Zn/kg dry weight) when compared to marine plants and invertebrates (Eisler, 1980, 1981, 1984, 2000h). Among teleosts, the zinc-specific sites of accumulation were viscera, gonad, and brain (Eisler, 1993, 2000h); muscle usually contained the lowest zinc concentrations (Table 3.20). Accumulations of stable zinc in edible portions of finfish present no known threat to human consumers at present (Eisler, 2000h). There is general agreement that zinc residues were higher in dead fish than in live or moribund fish, higher in smaller fish, higher in liver and viscera, and higher with decreasing water cadmium concentrations (Eisler, 1980). Zinc concentrations are usually higher in fish tissues near zinc-contaminated sites; tissue burdens are not proportionate to the organism’s immediate surroundings; zinc concentrations vary with age, gender, season, tissue, and other variables; and many species contain zinc loadings far in excess of immediate needs, suggesting active zinc regulation (Eisler, 2000h). The half-time persistence (Tb 1/2) of zinc in whole marine fishes ranged from 35 to 75 days in mummichog, F. heteroclitus, to 295-313 days in plaice, P. platessa; Tb1/2 in mummichog was shortest at 30 C, longest at 10 C, and intermediate at 20 C (USNAS, 1979). Most investigators agree that both diet and medium are zinc sources to marine teleosts; however, the relative importance of each varies. In some cases, dietary zinc was not well assimilated in flatfish. For example, turbot (Scophthalmus maximus) fed diets containing 100.0 (control) or 1000.0 mg Zn/kg DW ration for 200 days were not different in renal and hepatic metallothionein levels, or in zinc concentrations in liver, kidney, muscle, skin, or bone; a similar case is made for other flatfish species examined (Overnell et al., 1988). Turbot injected intraperitoneally with 2.0 mg Zn/kg body weight had an 18-fold increase in liver metallothionein content and a threefold increase in liver zinc concentration, confirming the ability of this species to synthesize metallothionein rapidly to a high concentration (Overnell et al., 1988). Zinc loadings in liver of European eels, A. anguilla, were positively correlated with metallothionein contents; zinc and metallothionein concentrations tended to increase with increasing length, weight, or age of the eel, and were highest in winter (Bird et al., 2008). Diet is thought to be the major zinc source in fishes when seawater contained less than 0.015 mg Zn/L; at higher ambient concentrations of 0.6 mg Zn/L, waterborne zinc contributed up to 50% of the total body zinc burden (Spry et al., 1988). Uptake from seawater was comparatively minor relative to diet in the metabolism of zinc by plaice, P. platessa
Fishes 171 Table 3.20: Zinc Concentrations in Field Collections of Fishes Organism
Concentration
Scombroid, Acanthocybium petus; muscle
0.11-8.0 FW; 0.39-36.0 DW; 390.0-5200.0 AW
1
Bay anchovy, Anchoa mitchelli; whole less head
397.0 DW
2
European eel, Anguilla anguilla Muscle Liver
23.8-27.2 FW 51.9-71.9 FW
3 3
American eel, Anguilla rostrata; muscle
25.0 DW
2
Sablefish, Anoplopoma fimbria; muscle
4.0 FW
4
Silverfish, Argyrozona argyrozona; muscle
2.9 FW
5
Halfbridled goby, Arenigobius frenatus; Australia; industrialized site vs. reference estuary Gonad Muscle
162.4 DW vs. 82.2 DW 33.4 DW vs. 28.8 DW
Australian salmon, Arripis trutta Muscle Liver Kidney Heart Gonad Spleen Gill Vertebrae Muscle
9.0-46.0 FW 21.0-42.0 FW 19.0-140.0 FW 10.0-24.0 FW 11.0-120.0 FW 10.0-54.0 FW 14.0-24.0 FW 15.0-22.0 FW 5.3 (3.1-14.7) FW
6 6 6 6 6 6 6 6 7
9.8 FW
8
Arrowtooth flounder, Atheresthes stomias; whole Australia; lead smelter marine outfall; whole fish; samples collected 2.5-5.2 km from source vs. 18.0-18.8 km Carnivores; 8 spp. Omnivores; 3 spp. Herbivore (six-lined trumpeter, Siphamia cephalotes) Gafftopsail catfish, Bagre marinus; muscle
163.0 DW; max 440.0 DW vs. 78.0 DW 222.0 DW; max. 619.0 DW vs. 105.0 DW 310.0 DW; max. 480.0 DW vs. 97.0 DW 12.0 DW
Reference
a
89 89
65 65 65 2 (Continues)
172 Chapter 3 Table 3.20: Cont’d Organism
Concentration
Silver perch, Bairdiella chrysoura; muscle
30.0 DW
2
Arctic cod, Boreogadus saida Muscle Liver
34.0 DW 19.0 DW
9 9
Jolthead porgy, Calamus bajonado GI tract Vertebrae Muscle Eyes Scales Gills
23.0 FW; 100.0 DW; 730.0 AW 130.0 FW; 230.0 DW; 420.0 AW 8.7 FW; 36.0 DW; 400.0 AW 54.0 FW; 280.0 DW; 2200.0 AW 166.0 FW; 230.0 DW; 430.0 AW 35.0 FW; 110.0 DW; 390.0 AW
1 1 1 1 1 1
Canned fish; Saudi Arabia; purchased locally Sardine Salmon Tuna
16.1 (8.9-23.9) FW 12.6 (5.3-19.8) FW 10.4 (3.8-17.7) FW
Horse-eye jack, Caranx latus; muscle
29.0 FW; 36.0 DW; 190.0 AW
1
Jack, Caranx lutescens Muscle Liver Kidney Heart Gonad Spleen Gill Vertebrae
1.0-35.0 FW 6.0-90.0 FW 40.0-350.0 FW 15.0-30.0 FW 21.0-256.0 FW 48.0-624.0 FW 16.0-29.0 FW 8.0-24.0 FW
6 6 6 6 6 6 6 6
Black sea bass, Centropristes striata: muscle
7.0 DW
2
Anchovy, Cetengraulis edentulus; muscle
6.7-20.0 FW; 98.0-370.0 DW; 290.0-340.0 AW
1
0.9-7.0 FW 90.0-1200.0 FW 12.0-20.0 FW 16.0-19.0 FW 52.0-100.0 FW 25.0-84.0 FW 12.0-24.0 FW 9.0-12.0 FW
6 6 6 6 6 6 6 6
Tarakihi, Cheilodactylus macropterus Muscle Liver Kidney Heart Gonad Spleen Gill Vertebrae
Reference
a
76 76 76
(Continues)
Fishes 173 Table 3.20:
Cont’d
Organism
Concentration
Reference
Squirefish, Chrysophrys auratus Muscle Liver Kidney Heart Gonad Spleen Gill Vertebrae Muscle
2.0-10.0 FW 16.0-146.0 FW 18.0-137.0 FW 6.0-112.0 FW 8.0-124.0 FW 36.0-62.0 FW 18.0-26.0 FW 10.0-34.0 FW 5.3 (1.3-10.8) FW
Fivebeard rockling, Ciliata mustela Whole Eviscerated
180.2 DW 56.6-98.1 DW
10 11
Baltic herring, Clupea harengus Whole Muscle Liver Whole
119.0 DW 6.6 FW 23.0 FW 6.4 DW
12 13 66 82
Conger eel, Conger sp.; muscle
41.0 DW
2
Spotted seatrout, Cynoscion nebulosus; muscle
21.0 DW
2
a
6 6 6 6 6 6 6 6 7
Drum, Cynoscion reticulatus Muscle Viscera Skin and scales Bone
238.0-600.0 AW 940.0-2400.0 AW 600.0-1750.0 AW 310.0-420.0 AW
Mackerel scad, Decapterus macarellus; muscle
27.0-58.0 FW; 100.0-220.0 DW; 680.0-1500.0 AW
1
Round scad, Decapterus punctatus; muscle
18.0 DW
2
Perch, Diplectrum euryplectrum Muscle Viscera Skin and scales Bone
350.0-420.0 AW 940.0 AW 260.0-490.0 AW 218.0-350.0 AW
14 14 14 14
Northern anchovy, Engraulis mordax; whole
400.0 AW
15
Coney, Epinephelus fulvus; muscle
28.0-100.0 FW; 98.0-370.0 DW; 410.0-630.0 AW
14 14 14 14
1 (Continues)
174 Chapter 3 Table 3.20: Cont’d Organism
Concentration
Nassau grouper, Epinephelus striatus; muscle
4.0 FW
16
Little tunny, Euthynnus alletteratus; muscle
8.0 DW
2
Skipjack tuna, Euthynnus pelamis Whole White muscle vs. dark muscle Viscera Skin and scales Bone Muscle Fish Bone Pelagic fish Bottom fish Byproducts Liver 4 spp. 35 spp. 21 spp. 9 spp. 5 spp. 3 spp. 3 spp. 2 spp. Muscle 7 spp. 82 spp. 48 spp. 14 spp. 2 spp. 6 spp. 11 spp. 9 spp. 8 spp. 4 spp. 9 spp. 17 spp. 11 spp.
Reference
490.0 AW 43.0-390.0 AW vs. 191.0-880.0 AW 1150.0-8400.0 AW 520.0-3300.0 AW 340.0-650.0 AW 17.0 FW; 57.0 DW; 970.0 AW
15 14
21.0-65.0 FW; 62.0-150.0 DW; 140.0-420.0 AW 12.0-150.0 FW; 36.0-380.0 DW; 100.0-900.0 AW 16.0 (7.1-47.2) FW
17
18
4.0-10.0 FW 10.0-30.0 FW 30.0-50.0 FW 50.0-70.0 FW 70.0-100.0 FW 100.0-200.0 FW 200.0-300.0 FW 300.0-700.0 FW
19 19 19 19 19 19 19 19
2.0-3.0 FW 3.0-5.0 FW 5.0-7.0 FW 7.0-9.0 FW 9.0-10.0 FW 10.0-20.0 FW 0.5-81.6 DW 0.5-21.8 FW 16.0-39.0 DW 19.0-37.0 DW 7.5-76.5 DW 3.2-11.0 FW 21.0-51.0 DW
19 19 19 19 19 19 20 7 21 22 23 24 25
a
14 14 14 1
17
(Continues)
Fishes 175 Table 3.20: Organism 7 spp. 23 spp. 6 spp. 12 spp. 8 spp. 7 spp. 6 spp. 10 spp.; China; October 2004 8 spp. 10 spp.; Mumbai, India; 2004-2005 Bottom fish Pelagic fish White muscle Dark muscle Otoliths, 8 spp. Scales, 10 spp. Skin 8 spp. Bottom fish Pelagic fish Viscera Pelagic fish Bottom fish 4 spp. 4 spp. Whole 11 spp. 3 spp. 10 spp. 5 spp. 5 spp. 2 spp.; Antarctica; 2004 Fishmeal Presscake
Cont’d
Concentration 1.7-14.7 FW Means 5.0-13.5 FW; max. 146.7 FW 2.3-6.5 FW 4.0-15.1 FW 3.5-19.0 FW 5.3-21.4 FW 6.0-8.3 FW 3.4-7.5 FW 16.0-31.8 FW 8.4 FW; 95th percentile 16.2 FW 3.0-93.0 FW; 13.0-420.0 DW; 190.0-7600.0 AW 3.0-15.0 FW; 65.0 DW max.; 210.0-880.0 AW 6.0-60.0 FW; 65.0 DW max; 120.0-1200.0 AW 0.4-38.0 DW 28.0-340.0 DW
Reference
a
26 27 28 29 30 31 83 87 32 84 1
1 1 33 33
42.4-106.0 DW 13.0-16.0 FW; 42.0-380.0 DW; 130.0-1600.0 AW 7.0-120.0 FW; 110.0-320.0 DW; 860.0-9600.0 AW
32 17
210.0 FW; 830.0 DW; 10,000.0 AW 1700.0 AW 98.4-143.0 DW 1040.0 AW
17
12.0-38.0 FW 2.0-7.0 FW 10.0-20.0 FW 20.0-30.0 FW 6.3-117.0 DW 64.6-99.1 DW
34 4, 19 19 19 22 71
86.0 DW
35
17
17 32 15
(Continues)
176 Chapter 3 Table 3.20: Cont’d Organism N-liquor Meal Industrial meal Laboratory produced meal Lipid phase 5 spp. mixture
Concentration
Reference
67.0 FW 180.0 DW 38.0-639.0 DW Max. 62.0 DW 1.1-54.0 FW 74.0-142.0 DW
35 35 36 36 36 37
Mummichog, Fundulus heteroclitus Whole fish, various total length 46 mm 61 mm 77 mm 88 mm 106 mm 119 mm Viscera Gills Muscle
1180.0 AW 1010.0 AW 945.0 AW 867.0 AW 867.0 AW 788.0 AW 75.0 FW 81.0 FW 47.0 FW
38 38 38 38 38 38 39 39 39
Pacific cod, Gadus macrocephalus Muscle Gonad Liver
6.5 DW 79.0 DW 18.0 DW
40 40 40
4.1 DW 44.9 DW 7.9 DW 16.7 DW 29.0-119.0 DW
41 41 41 41 41
4.3 FW 5.2 FW 4.7 FW 3.1 FW 9.0 FW 132.0 FW vs. 45.0 FW 5.0 FW 16.6 FW 10.0 FW 12.1 FW 29.0 FW 15.4 FW 29.8 FW
42 42 42 18 18 18 18 18 18 18 18 18 18
Atlantic cod, Gadus morhua Muscle Ovary Testes Liver Roe Muscle Inshore North Sea Offshore Muscle Tongue Roe; juvenile vs. mature Milt Gills Skin Vertebrae Intestines Stomach contents Gall bladder
a
(Continues)
Fishes 177 Table 3.20:
Cont’d
Organism
Concentration
Rex sole, Glyptocephalus zachirus; whole
8.5 FW
Goby, Gobius minutus; whole
75.6 DW
10
Goby, Gobius niger Muscle Liver
48.0-58.0 DW 15.0-22.0 DW
43 43
38.8 FW vs. 39.6 FW 8.0 FW vs. 16.4 FW 33.5 FW vs. 40.9 FW
80 80 80
no data vs. 69.3 FW no data vs. 35.9 FW no data vs. 34.8 FW
80 80 80
125.0 FW vs. 166.0 FW 15.8 FW vs. 42.1 FW
80 80
61.3 FW vs. 65.5 FW 9.9 FW vs. 22.9 FW 40.3 FW vs. 41.6 FW
80 80 80
Indian Ocean; 2004; Mozambique Channel vs. Reunion Island Common dolphinfish, Coryphaena hippurus Liver Muscle Kidney Skipjack, Katsuwonus pelamis Liver Muscle Kidney Yellowfin tuna, Thunnus albacares Liver Muscle Swordfish, Xiphias gladius Liver Muscle Kidney
Reference
a
8
Longspine squirrelfish, Holocentrus rufus; muscle
13.0-74.0 FW; 33.0-150.0 DW; 130.0-480.0 AW
1
Croaker, Johnius hololepidotus; muscle
3.5 FW
5
Spot, Leiostomus xanthurus; muscle
20.0 DW
2
Yellowtail flounder, Limanda ferruginea Muscle Muscle
4.2-4.4 DW 4.2 FW
44 45
Dab, Limanda limanda; skin plus muscle
5.8-7.0 FW
46
Striped seasnail, Liparis liparis Whole Eviscerated
86.5 DW 80.2-195.2 DW
10 11
Mullet, Liza saliens; Portugal; 2003-2004 Muscle Liver
26.7 DW 88.6 (26.0-190.0) DW
86 86 (Continues)
178 Chapter 3 Table 3.20: Cont’d Organism
Concentration
Haarder, Liza ramada; whole
120.0 DW
Goosefish, Lophius piscatorius; muscle
3.7 FW
Tilefish, Lopholatilus chamaeleonticeps; liver
1800.0 AW
47
115.0 DW 25.0 DW 29.0 DW 35.0 (16.0-61.0) DW 22.0 (17.0-31.0) DW (22.0-239.0) DW 31.0 (15.0-95.0) DW
67 67 67 67 67 67 67
36.0 DW 24.0 DW
67 67
8.6 (5.8-14.6) FW 47.5 (4.0-375.0) FW
49 48
Louisiana; CalcasieuRiver Estuary; muscle Gulf menhaden, Brevoortia patronus Gizzard shad, Dorosoma cepedianum Threadfin shad, Dorosoma petenense Blue catfish, Ictalurus furcatus Spot, Leiostomus xanthurus Spotted gar, Lepisosteus oculatus Atlantic croaker, Micropogonias undulatus White mullet, Mugil curema Southern flounder, Paralichthys lethostigma Black marlin, Makaira indica Muscle Liver Blue marlin, Makaira nigricans; muscle
4.1-70.0 FW; 72.0-210.0 DW; 260.0-2100.0 AW
Reference 10 5
1
European whiting, Merlangius merlangus Whole Whole Muscle Liver Gut wall
124.8 DW 72.5-102.4 DW 9.1-9.2 FW 28.3 FW 23.1 FW
Cape hake, Merluccius capensis; muscle
3.9 FW
5
Pacific hake, Merluccius productus Muscle Whole
4.0 FW 12.0 FW
4 4
18.4 DW 21.0 DW 21.0 DW
90 90 90
Mexico; Gulf of California; 1999-2000; muscle Striped mullet, Mugil cephalus Colorado snapper, Lutjanus colorado Orangemouth corvina, Cynoscion xanthulus
a
10 11 3 3 3
(Continues)
Fishes 179 Table 3.20: Organism Dover sole, Microstomus pacificus Muscle; wastewater site vs. reference site Muscle Whole
Cont’d
Concentration
Reference
39.4 DW vs. 38.0 DW
50
15.0-26.0 DW 8.1 FW
51 8
European bass, Morone labrax; muscle
15.0 DW
49
Striped bass, Morone saxatilis Muscle Muscle Liver
12.0 DW 3.8 FW 35.0-36.0 FW
2 52 52
Striped mullet, Mugil cephalus Muscle Muscle Muscle
17.0 DW 4.3 (0.5-13.9) FW 5.45 (1.28-12.3) DW
2 7 75
White mullet, Mugil curema Muscle Viscera Skin and scales Bone
98.0-560.0 AW 1430.0 AW 210.0-750.0 AW 98.0-290.0 AW
14 14 14 14
Mullet, Mugil liza; Argentina Muscle Liver
48.8 FW 52.0 FW
73 73
Mullet, Mugil spp.; Mediterranean Sea; June-July 2003 Muscle Skin Gills Liver
6.5-6.0 FW 60.6-72.7 FW 33.1-37.0 FW 49.2-54.9 FW
74 74 74 74
Scamp, Mycteroperca phenax; muscle
3.2 FW
16
Tiger grouper, Mycteroperca tigris; muscle
3.7 FW
16
Myctophids Whole Whole Whole less head; 8 spp.
210.0 AW 10.0 FW 15.0-81.0 DW
53 4 2
Shorthorn sculpin, Myoxocephalus scorpius Muscle Liver
43.0 DW 100.0 DW
54 54
a
(Continues)
180 Chapter 3 Table 3.20: Cont’d Organism Catfish, Mystus gulio: whole; juveniles; India From contaminated estuary (0.10.12 mg Zn/L; 120.0-145.0 mg Zn/kg DW sediment) Reference site (0.01 mg Zn/L; 30.0 mg Zn/kg DW sediment)
Concentration
Reference
160.0-180.0 DW
68
15.0 DW
68
Blue hake, Nematonurus armatus; liver
50.0 FW
55
Chum salmon, Oncorhynchus keta; adults during spawning migration; females vs. males Gonad Liver
50.0 FW vs. 15.0 FW 45.0 FW vs. 50.0 FW
56 56
Snake eel, Ophichthus spp.; muscle
21.0-26.0 DW
Deepbody thread herring, Opisthonema libertate Muscle Viscera Skin and scales Bone
770.0 AW 2550.0 AW 590.0 AW 400.0 AW
14 14 14 14
55.0-377.0 AW 378.0-2454.0 AW 227.0-987.0 AW 43.0-252.0 AW 21.0-110.0 FW; 82.0-300.0 DW; 400.0-5700.0 AW
14 14 14 14 1
Atlantic thread herring, Opisthonema oglinum Muscle Viscera Skin and scales Bone Muscle Bronze bream, Pachymetopon grande; muscle Pandora, Pagellus erythrinus Fins Eyes Eggs Gills Brain Liver Intestine Spleen
2.5 FW
3.7 DW 7.8 DW 31.0 DW 2.7 DW 1.8 DW 6.6 DW 4.4 DW 6.3 DW
a
2
5
57 57 57 57 57 57 57 57 (Continues)
Fishes 181 Table 3.20: Organism Muscle Skin Bone Whole fish Summer flounder, Paralichthys lethostigma; muscle European flounder, Platichthys flesus Whole Barnstaple Bay, United Kingdom Age 2+ years Age 3+ Age 4+ Age 5+ Oldbury-on-Severn, United Kingdom Age 2+ Age 3+ Age 4+ Age 5+ Muscle Liver Gut wall Ovary Winter flounder, Pleuronectes americanus Muscle Liver Plaice, Pleuronectes platessa Muscle Liver Gut wall Whole, age group 0+ Muscle Inshore vs. offshore North Sea Barbu, Polydactylus virginicus; muscle Hapuka, Polyprion oxygeneios Muscle Liver
Cont’d
Concentration
Reference
1.1 DW 2.8 DW 9.5 DW 2.0 DW
57 57 57 57
39.0 DW
2
224.5 DW 209.4 DW 200.2 DW 195.2 DW
10 10 10 10
125.2 DW 128.0 DW 128.6 DW 140.0 DW 1.2-18.2 FW 53.8-68.9 FW 36.2 FW 146.8 FW
10 10 10 10 3 3 3 3
5.2-6.0 FW 15.0-45.0 FW
45 45
10.0-11.9 FW 38.9 FW 27.5 FW 99.6-121.6 DW
3 3 3 58
5.4 DW vs. 6.6 DW 5.7 DW
42 42
9.3-15.0 FW; 39.0-63.9 DW; 280.0-410.0 AW
1
2.1-12.0 FW 33.0-90.0 FW
6 6
a
(Continues)
182 Chapter 3 Table 3.20: Cont’d Organism Kidney Heart Gonad Spleen Gill Vertebrae Bluefish, Pomatomus saltatrix White muscle Liver; males vs. females Muscle
Concentration 15.0-29.0 FW 8.0-17.0 FW 11.0-200.0 FW 6.0-26.0 FW 24.0-38.0 FW 40.0-104.0 FW
Reference
a
6 6 6 6 6 6
4.5-5.0 FW 1700.0 AW vs. 3700.0 AW 9.6 (2.5-18.0) FW
59 47 7
66.0 DW 154.0 (81.0-227.0) DW 291.0 (287.0-792.0) DW 29.0 (11.0-43.0) DW
70 70 70 70
32.0 DW
70
33.0 (19.0-51.0) DW
70
33.0 (13.0-112.0) DW 95.0 (43.0-146.0) DW 146.0 (72.0-259.0) DW 152.0 (141.0-164.0) DW 48.0 (25.0-70.0) DW
70 70 70 70 70
17.0 DW 62.0 DW
70 70
Red Sea; 1980-1982 Triggerfish, Balistoides viridescens Muscle Liver Ovaries Surgeonfish, Ctenochaetus strigosus; muscle Halfbeak, Hemiramphus marginatus; muscle Labrids; 3 spp.; muscle Lethrinids, Lethrinus spp. Muscle Liver Ovaries Testes Snapper, Lutianus fulviflamma; muscle Parrotfish, Scarys gyttatus Liver Muscle Serranids; 4 spp. Muscle Liver Rabbitfish, Siganus oramin Muscle Liver Sparids; 2 spp.; muscle Goatfish, Upeneus tragula; muscle
51.0 (8.0-112.0) DW 130.0 (78.0-183.0) DW
70 70
55.0 (18.0-195.0) DW 179.0 (68.0-611.0) DW 56.0 (34.0-76.0) DW 51.0 (37.0-68.0) DW
70 70 70 70
Atlantic salmon, Salmo salar; marine cage farmed; Scotland; 2000 Muscle Bone
4.4 DW 39.9 DW
79 79 (Continues)
Fishes 183 Table 3.20: Organism Gill Gut Fat Liver Kidney Spleen Gonad Diet vs. feces
Cont’d
Concentration
Reference
159.7 DW 26.1 DW 0.5 DW 0.8 DW 0.2 DW 0.5 DW 1.3 DW 196.4 DW vs. 364.5 DW
79 79 79 79 79 79 79 79
Arctic char, Salvelinus alpinus Muscle Liver
23.0 DW 130.0 DW
54 54
Sardine, Sardinops ocellata; muscle
19.0 FW
Porgy, Sargus annularis; reference site vs. metals-contaminated area Muscle Liver
71.0 DW vs. 37.0-70.0 DW 83.0 DW vs. 52.0-111.0 DW
Chub mackerel, Scomber japonicus Muscle Otoliths; Aegean Sea Dodecanese area Age 2 years Age 3 years Age 4 years Age 5 years Age 6 tears Cyclades Islands Age 1 year Age 2 years Age 3 years Age 4 years Age 5 years Age 6 years Atlantic mackerel, scomber scombrus; liver King mackerel, Scomberomerus cavalla Muscle Muscle Liver
9.0 FW
5
43 43 5
35.0 DW 33.0 DW 27.0 DW 12.0 DW 7.4 DW
60 60 60 60 60
43.0 DW 67.0 DW 20.0 DW 21.0 DW 21.0 DW 20.0 DW
60 60 60 60 60 60
31.0 FW
66
5.0-94.0 FW; 26.0-260.0 DW; 260.0-3000.0 AW 20.0 DW 420.0 DW
a
1 72 72 (Continues)
184 Chapter 3 Table 3.20: Cont’d Organism Otoliths Age <1 year Age 2 years Age 10 years
Concentration
16.0 DW; max. 50.0 DW 11.0 DW 8.0 DW
Reference
69 69 69
Spanish mackerel, Scomberomerus maculatus; muscle
15.0 DW
2
Saury, Scombersox saurus; whole
410.0 AW
53
Windowpane, Scopthalmus aquosus Muscle Muscle Liver
23.0-28.0 DW 4.6-6.3 FW 34.1-41.9 FW
44 61 61
Amberjack, Seriola grandis Muscle Liver Kidney Vertebrae Muscle
2.8-56.0 FW 15.0-37.0 FW 75.0-390.0 FW 15.0-22.0 FW 5.2 (1.4-20.8) FW
6 6 6 6 7
Jack, Seriola pappei; muscle
5.5 FW
5
Northern puffer, Sphoeroides maculatus Gill Liver Liver Gill arch Gill filament Muscle Ovary Testes Serum
4400.0 AW 37,500.0 AW 9700.0 AW 1700.0 AW 15,300.0 AW 600.0 AW 5700.0 AW 2400.0 AW 219.0 AW
Bandtail puffer, Sphoeroides spengleri; muscle Sprat, Sprattus sprattus Whole Whole
30.0 FW; 130.0 DW; 700.0 AW
133.0 DW 38.5 FW
a
62 62 63 63 63 63 63 63 63 1
12 3
Drum, Stellifer stellifer; muscle
9.7-10.0 FW; 37.0-40.0 DW; 200.0-210.0 AW
1
Sole, Synaptura marginata; muscle
5.5 FW
5 (Continues)
Fishes 185 Table 3.20:
Cont’d
Organism
Concentration
Tautog, Tautoga onitis; liver; males vs. females
1500.0 AW vs. 1300.0 AW
Eulachon, Thaleichthys pacificus; whole
10.5 FW
Yellowfin tuna, Thunnus albacares Muscle; white vs. dark
Reference 47 8
40.0-140.0 AW vs. 450.0-785.0 AW 219.0-3020.0 AW 650.0-3800.0 AW 290.0-550.0 AW 4.8 (1.8-24.0) FW
14
Blackfin tuna, Thunnus atlanticus; otoliths; Gulf of Mexico; 2002
4.49 DW
25
Southern bluefin tuna, Thunnus maccoyii; muscle; April 2004; Australia; wild vs. farmed
5.0 (4.9-5.2) FW vs. 5.0 (4.0-8.0) FW
85
European horse mackerel, Trachurus trachurus; muscle
3.0 FW
5
Atlantic cutlassfish, Trichiurus lepturus; muscle
5.7-47.0 FW; 26.0-220.0 DW; 230.0-1800.0 AW
1
Gurnard, Trigla kumu Muscle Liver Kidney Heart Gonad Spleen Gill Vertebrae
2.5-16.2 FW 12.0-102.0 FW 8.0-26.0 FW 8.0-25.0 FW 80.0-162.0 FW 26.0-36.0 FW 7.0-13.0 FW 12.0-24.0 FW
6 6 6 6 6 6 6 6
Gurnard, Trigla capensis; muscle
3.4 FW
5
Poor-cod, Trisopterus minutus; whole
158.1 DW
10
Turkey; Camlik Lagoon, Mediterranean Sea; 2000-2001; winter vs. autumn European bass, Dicentrarchus labrax Gill Liver Gonad Muscle
144.1 DW vs. 142.6 DW 48.9 DW vs. 26.3 DW 77.2 DW vs. 144.8 DW 113.1 DW vs. 71.4 DW
77 77 77 77
Viscera Skin and scales Bone Muscle
a
14 14 14 7
(Continues)
186 Chapter 3 Table 3.20: Cont’d Organism Striped mullet, Mugil cephalus Gill Liver Gonad Muscle Gilthead bream, Sparus auratus Gill Liver Gonad Muscle Turkey; NE Mediterranean Sea coast; winter vs. summer; 2003 Striped mullet, Mugil cephalus Liver Gill Muscle Striped goatfish, Mullus barbatus Liver Gill Muscle Turkey; 2005; Black Sea vs. Aegean Sea European anchovy, Engraulis encrasicolus Muscle Liver Picarel, Spicara smaris Muscle Liver Red hake, Urophycis chuss Liver Muscle White hake, Urophycis tenuis Muscle Muscle Kinglip, Xiphiurus capensis; muscle
Concentration
Reference
126.4 DW vs. 113.2 DW 96.4 DW vs. 70.3 DW 89.7 DW vs. 54.3 DW 42.2 DW vs. 101.1 DW
77 77 77 77
115.0 DW vs. 139.3 DW 61.4 DW vs. 60.3 DW 68.2 DW vs. 86.4 DW 33.4 DW vs. 67.8 DW
77 77 77 77
69.8 DW vs. 86.5 DW 54.5 DW vs. 62.4 DW 22.4 DW vs. 29.7 DW
78 78 78
101.4 DW vs. 130.2 DW 65.4 DW vs. 76.4 DW 26.7 DW vs. 34.5 DW
78 78 78
10.6-45.6 FW vs. 12.9 FW 14.1-145.0 FW vs. 21.0 FW
91 91
12.2 FW vs. 7.1-10.8 FW 18.5 FW vs. 17.9-45.8 FW
91 91
28.0-41.0 FW 3.3 FW
45 45
2.9 FW 2.9-3.8 FW
45 44
6.9 FW
a
5 (Continues)
Fishes 187 Table 3.20:
Cont’d
Organism
Concentration
Grass goby, Zosterisessor ophiocephalus; muscle; 2005-2006; Venice lagoon, Italy; San Giuliano vs. Sacca Sessola April October February
2.1 DW vs. 2.4 DW 21.6 DW vs. 24.8 DW 37.6 DW vs. 38.2 DW
Reference
a
81 81 81
Values are in mg Zn/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Lowman et al., 1966; 2, Windom et al., 1973; 3, Wharfe and Van den Broek, 1977; 4, Cutshall et al., 1977b; 5, Van As et al., 1973; 6, Brooks and Rumsey, 1974; 7, Bebbington et al., 1977; 8, Vanderploeg, 1979; 9, Bohn and McElroy, 1976; 10, Hardisty et al., 1974; 11, Badsha and Sainsbury, 1978; 12, Andersen et al., 1973; 13, Vanderstappen et al., 1978; 14, Ting, 1971; 15, Goldberg, 1962; 16, Taylor and Bright, 1973; 17, Lowman et al., 1970; 18, Julshamn et al., 1978b; 19, Hall et al., 1978; 20, Roth and Hornung, 1977; 21, Ishii et al., 1978; 22, Sims and Presley, 1976; 23, Zingde et al., 1976; 24, Van As et al., 1975; 25, Arslan and Secor, 2008; 26, Holden and Topping, 1972; 27, Eustace, 1974; 28, Babji et al., 1979; 29, Plaskett and Potter, 1979; 30, Miettinen and Verta, 1978; 31, DeClerck et al., 1979; 32, Horowitz and Presley, 1977; 33, Papadopoulu and Kassimati, 1977; 34, Wolfe et al., 1973; 35, Lunde, 1968b; 36, Lunde, 1973c; 37, Jangard et al., 1974; 38, Eisler and LaRoche, 1972; 39, Chernoff and Dooley, 1979; 40, Hamanaka et al., 1977; 41, Julshamn and Braekkan, 1975; 42, Portmann, 1972; 43, Grimanis et al., 1978; 44, Greig, 1975; 45, Greig and Wenzloff, 1977a; 46, Newell et al., 1979; 47, Mears and Eisler, 1977; 48, Mackay et al., 1975; 49, Leatherland and Burton, 1974; 50, McDermott et al., 1976; 51, Sherwood and Mearns, 1977; 52, Heit, 1979; 53, Robertson, 1967; 54, Bohn and Fallis, 1978; 55, Greig et al., 1976; 56, Fletcher and King, 1978a; 57, Papadopoulu et al., 1972; 58, Milner, 1979; 59, Cross et al., 1973; 60, Papadopoulu et al., 1978a; 61, Greig et al., 1977; 62, Eisler and Edmunds, 1966; 63, Eisler, 1967a; 64, Orvini et al., 1974; 65, Ward et al., 1986; 66, Morris et al., 1989; 67, Ramelow et al., 1989; 68, Joseph, 1989; 69, Grady et al., 1989; 70, Hanna, 1989; 71, Santos et al., 2006; 72, Ploetz et al., 2007; 73, Marcovecchio, 2004; 74, Storelli et al., 2006; 75, Turkmen et al., 2006; 76, Ashraf et al., 2006; 77, Dural et al., 2006; 78, Cogun et al., 2006; 79, Dean et al., 2007; 80, Kojadinovic et al., 2007; 81, Nesto et al., 2007; 82, Zumholz et al., 2006; 83, Sankar et al., 2006; 84, Mishra et al., 2007; 85, Padula et al., 2008; 86, Fernandes et al., 2008b; 87, Cheung et al., 2008; 88, Fernandes et al., 2008a; 89, Roach et al., 2008; 90, Ruelas-Inzunza and Paez-Osuna, 2008; 91, Turkmen et al., 2008.
(Pentreath, 1973, 1976c), and other species (Renfro et al., 1975). However, no relation between diet and whole fish zinc concentrations was observed by Hardisty et al. (1974). Ting (1971) found no significant differences in zinc content of muscle, skin, viscera, or bone of seven species of fishes representing herbivorous, benthic, and pelagic carnivorous feeding habitats. Uptake from seawater by adult mummichogs F. heteroclitus was inversely related to zinc concentrations in the medium (USEPA, 1987a). Zinc accumulates in scales of mummichogs during exposure to 10.0 mg Zn/L, significantly elevating the zinc:calcium ratio; Zn:Ca ratios remained elevated for a least 4 months after transfer to low zinc media, and this phenomenon has been proposed for environmental monitoring of prior zinc exposure (Sauer and Watabe, 1989a). Scale osteoblasts of zinc-exposed mummichogs show an increase in the number of lysosome-like structures contained by cytoplasm, and suggests that osteoblast lysosomes are involved in zinc accumulation in fish scales via enzymatic degradation of metallothioneins or other metal-binding proteins (Sauer and Watabe, 1989b). Different life stages of plaice, P. platessa, accumulated zinc from the medium at different rates ranging from negligible for embryos to 0.0072 mg/kg daily for whole larvae,
188 Chapter 3 to 0.0392 mg/kg daily in bone for 8-month-old fish (Pentreath, 1976c). Plaice given intraperitoneal injections of zinc salts resulted in elevated hepatic metallothionein-like species by a factor of 15; metallothionein levels remained elevated for the next 4 weeks (Overnell et al., 1987a). A reduction in serum zinc during egg formation in plaice may represent a transfer of zinc to eggs (Overnell et al., 1987b). Dead mummichogs, F. heteroclitus, accumulate zinc at a substantially higher rate than living mummichogs, suggesting that zinc residue data from teleosts dead on collection are of limited worth (Eisler, 1967b, 1980; Eisler and Gardner, 1973). The range of BCF values for zinc and representative fishes (mg Zn/kg FW tissue/mg Zn/L medium) ranged from 1900 to 6900 (Eisler, 1980). Maximum net daily accumulation rates from seawater for various whole marine organisms, in mg Zn/kg FW whole organism, were 1.3 for the alga Ascophyllum nodosum, 7.7 for the common mussel Mytilus edulis, 19.8 for the American oyster Crassostrea virginica, 32.0 for the cyprinodontiform teleost F. heteroclitus, 32.0 for softshell clam Mya arenaria, and 223.0 for sandworm Nereis virens; in general, accumulation rates were higher at elevated water temperatures and at high ambient zinc water concentrations (Eisler, 1980). Age and gender in some—but not all—species of fish are important governors of zinc content. For example, smaller Pacific hake, M. productus, reflected zinc contamination in whole body and in muscle tissues earlier than did larger hake (Cutshall et al., 1977a), with increasing zinc per unit weight muscle observed with increasing body length (Cutshall et al., 1977b). However, the closely related European whiting M. merlangus, from the 0 + age groups contained zinc burdens that were negatively correlated with length and weight, with upper threshold limits reached quickly when fish entered zinc-contaminated waters (Badsha and Sainsbury, 1978). Otoliths from mackerel, Scomber japonicus colias, contained decreasing concentrations of zinc with increasing age; this trend was consistent in two populations collected from the Aegean Sea, although otolith zinc content was measurably different between populations (Papadopoulu et al., 1978a). In bluefish, P. saltatrix, body length had little relation to muscle zinc content (Cross et al., 1973). Zinc concentrations in young of the year plaice was inversely related to body weight; further, over the next 2 years of life zinc concentrations, with some seasonal variations, continued to decrease in whole plaice (Milner, 1979). In whole mummichogs, there was an inverse relation between body length and zinc concentrations in both males and females, although females contained more zinc than males (Chernoff and Dooley, 1979). Others have shown that gender or sexual condition of mummichogs did not affect whole body zinc concentrations (Eisler and LaRoche, 1972). In female tilefish, L. chamaeleonticeps, liver zinc residues were not significantly different from that of males, but females, unlike males, contained increasing zinc in liver with increasing age (Mears and Eisler, 1977). In sexually mature chum salmon, O. keta, females contained about three times more zinc in gonad per unit weight than did males during a spawning migrations, suggesting that zinc is essential to normal embryonic
Fishes 189 development of salmonids (Fletcher and King, 1978a). Liver zinc contents of sexually mature salmon were the same in both sexes (Fletcher and King, 1978a). Zinc-binding proteins were isolated from plasma of winter flounder, P. americanus (Fletcher and Fletcher, 1978, 1980; Fletcher and King, 1978b). In both males and females, more than 95% of the plasma zinc was associated with zinc-binding proteins with a molecular weight of 76,000. In males, the remaining 5% was bound to protein(s) of MW 186,000; in females, this fraction was associated with two zinc-binding proteins of MW 186,000 and about 360,000. It is hypothesized that the female specific zinc-binding protein of 360,000 was VTG (Fletcher and Fletcher, 1980). Liver and viscera are major storage sites of zinc. Viscera of mummichogs, which accounted for 4% of the whole fish ash weight contained 29% of whole fish zinc; heads which accounted for 45% of whole fish ash contained only 33% of total fish zinc; the remainder contained 38% of total body zinc but accounted for 51% of whole fish ash weight (Eisler and LaRoche, 1972). Liver cells of puffers, Tetraodon hispidus, accumulated zinc against a sevenfold concentration gradient via a passive mechanism not directly coupled to metabolic energy (Saltman and Boroughs, 1960). Of seven species of marine fishes collected from a deepwater disposal site in the New York Bight, liver of blue hake contained the highest level (50.0 mg/kg fresh weight) of all tissues and species examined (Greig et al., 1976). Zinc uptake from seawater by fishes was markedly affected by other chemicals in solution. Various organochlorine and organophosphorus pesticides influenced zinc content of gill, liver, and serum in the northern puffer, Sphoeroides maculatus (Eisler, 1967a; Eisler and Edmunds, 1966). Zinc and copper acted more than additively in toxicity to mummichogs; however, zinc residues in whole fish were unaffected by the presence of copper (Eisler and Gardner, 1973). Zinc content of seawater can modify uptake of lead and other metals by teleosts. For example, lead and cadmium are taken up 10 times more rapidly at elevated ambient zinc concentrations (Havre et al., 1972). In mummichogs, zinc and cadmium act additively in biocidal properties, but zinc residues in whole fish decreased significantly with increasing ambient cadmium concentrations, suggesting competition between zinc and cadmium for the same physiologically active sites (Eisler and Gardner, 1973). Other factors reported to influence zinc uptake by marine fishes include respiration rate (Edwards, 1967; Zaba and Harris, 1978), temperature of the medium (Eisler and LaRoche, 1972; Negilski, 1976; Saltman and Boroughs, 1960; Shulman et al., 1961), duration of exposure (Edwards, 1967; Eisler and Gardner, 1973), salinity of the medium (Eisler and LaRoche 1972; Shulman et al., 1961), distance from point source (Cutshall et al., 1977a), sediment lithology (Sherwood and Mearns, 1977), metabolic transformations of zinc into various chemical species with different retention times (Baptist et al., 1970), and migratory patterns. Regarding the latter, for example, plasma zinc levels in sockeye salmon, O. nerka, dropped from 0.23 to 0.05 mg/L during upstream migration from estuary to lake (Fletcher et al., 1975). In estuaries and other marine environments, the relative abundance of zinc species changes with
190 Chapter 3 increasing salinity. At low salinities, ZnSO4 and ZnCl+predominate; at higher salinities the octahedral aquo ion [(Zn(H2O)6)2+] predominates (Spear, 1981). As salinity decreases, the concentration of free zinc ion increases and the concentration of zinc-chloro complexes decreases, resulting in increased bioavailability of the free metal ion and increased uptake by resident organisms (Nugegoda and Rainbow, 1989). Preexposure of black sea bream, A. schlegeli, to cadmium markedly affects cadmium uptake kinetics—but this is not the case with zinc (Zhang and Wang, 2006). Zinc accumulations in juvenile Acanthopagrus held in up to 3.0 mg Zn/L for up to 24 h had increasing zinc accumulations with increasing exposure time after the initial zinc surface binding; viscera were the most important site followed by gills. In this respect, observations for both cadmium and gill were similar. After preexposure, bream were subjected to waterborne (0.088 mg Zn/L) or dietary (411.0 mg Zn/kg FW) for 1 week. Unlike cadmium, there was little change in body burdens of zinc or redistribution among tissues from either exposure route, suggesting that sea breams can regulate zinc accumulation (Zhang and Wang, 2006). Zinc uptake increased as salinity decreased, with gill the most sensitive accumulator at lower salinities (Zhang and Wang, 2007a). EDTA significantly reduced intestinal zinc uptake in juvenile sea bream by 11%, while cysteine enhanced uptake by 59% (Zhang and Wang, 2007b). Nutritional zinc deficiency is rare in aquatic organisms (Spear, 1981), although reports are available of experimentally induced zinc deficiency in teleosts (Eisler, 2000h). The balance between excess and insufficient zinc is important. Zinc deficiency occurs in many species of plants, invertebrates, and vertebrates with severe adverse effects on all stages of growth, development, reproduction, and survival. Zinc deficiency effects are documented in fishes at less than 0.0065 mg Zn/L and at less than 15.0 mg Zn/kg FW diet (Eisler, 2000h). Zinc concentrations in Atlantic salmon milt ranged from 0.5 to 5.5 mg Zn/kg FW and was linearly proportional to spermatozoan abundance (Poston and Ketola, 1989). Toxic and sublethal effects of zinc are documented. Zinc has its primary effect on zincdependent enzymes that regulate the biosynthesis and catabolic rate of RNA and DNA (Gipouloux et al., 1986; Sternlieb, 1988). The main target organ in fish is gill epithelium (Eisler, 2000h). High (>35.0 mg/kg FW) zinc concentrations in eggs of Atlantic salmon (S. salar) are sometimes associated with increasing mortality, although low (14.0 mg/kg FW) concentrations seem to have no adverse effect on survival (Craik and Harvey, 1988). Zinc concentrations fatal to 50% in 96 h [(LC50(96h)] ranged from 0.191 mg/L for larvae of the cabezon, Scorpaenichthys marmoratus, to 38.0 mg/L for juvenile spot, L. xanthurus (USEPA, 1987a), to >43.0 mg/L for adult mummichogs, F. heteroclitus (Eisler, 1967b). All adult mummichogs survived exposure for 8 days to 43.0 mg Zn/L with no significant increase in tissue zinc concentrations (Eisler, 1967b). LC50 values for mummichogs were 52.0-66.0 mg Zn/L in 8 days (Ahsanullah et al., 1988; Eisler and Hennekey, 1977) and 71.0-153.0 mg/L in 48 h (Burton and Fisher, 1990). In general, zinc was more toxic to embryos and juveniles than to adults or to starved animals, at
Fishes 191 elevated temperatures, in the presence of cadmium or mercury, in the absence of chelating agents, at reduced salinities, under conditions of marked oscillations in ambient zinc concentrations, and at low dissolved oxygen concentrations (Eisler, 2000h; Paulauskis and Winner, 1988; Spear, 1981; USEPA, 1987a). Mixtures of copper and zinc were markedly more toxic than expected to marine fishes (Eisler, 1984; Eisler and Gardner, 1973). LC50 (96 h) values for most marine fishes was greater than 1.0 mg Zn/L (USEPA, 1980f). Sublethal effects on growth, reproduction, and metabolism are documented for sensitive species at nominal water concentrations as low as 0.05 mg Zn/L. At 0.05 mg Zn/L, embryos and larvae of the Atlantic herring, Clupea harengus harengus, showed a significant increase in frequency of jaw and branchial abnormalities (USEPA, 1980f, 1987a). Baltic herring, C. harengus, are more resistant than Atlantic herring. Larvae of the Baltic herring from eggs exposed through hatching to 0.5, 2.0, 6.0, or 12.0 mg Zn/L had histopathology of epidermis and kidney at 6.0 mg/L and higher, and no measurable effects at 2.0 mg/L and lower (Somasundaram, 1985; Somasundaram et al., 1985). Adults of mummichogs exposed to high sublethal zinc concentrations of 10.0 mg/L for 94 days had zinc burdens in scales of 229.0 mg/kg DW at start, 746.0 mg/kg DW at day 45, and 1608.0 mg/kg DW at day 94 (Sauer and Watabe, 1989a). Transfer to zinc-free media after 45 days (746.0 mg Zn/kg DW scales) for 21-49 days resulted in concentrations of 422.0-498.0 mg Zn/kg DW scales (Sauer and Watabe, 1989a).
3.48 Zirconium Whole Baltic herring, C. harengus, contained 0.00086 mg Zr/kg DW (Zumholz et al., 2006).
3.49 Literature Cited Aarkrog, A., 1971. Radioecological investigations of plutonium in an Arctic marine environment. Health Phys. 20, 31–47. Aarkrog, A., 1977. Environmental behaviour of plutonium accidentally released at Thule, Greenland. Health Phys. 32, 271–284. Abreu, S.N., Pereira, E., Vale, C., Duarte, A.C., 2000. Accumulation of mercury in sea bass from a contaminated lagoon (Ria de Aveiro, Portugal). Mar. Pollut. Bull. 40, 293–297. Ackefors, H., Lofroth, G., Rosen, C.G., 1970. A survey of the mercury pollution problem in Sweden with special reference to fish. Oceanogr. Mar. Biol. Ann. Rev. 8, 203–224. Adams, D.H., Onorato, G.V., 2005. Mercury concentrations in red drum, Sciaenops ocellatus, from estuarine and offshore waters of Florida. Mar. Pollut. Bull. 50, 291–300. Ahsanullah, M., Mobley, M.C., Rankin, P., 1988. Individual and combined effects of zinc, cadmium and copper on the marine amphipod, Allorchestes compressa. Aust. J. Mar. Freshw. Res. 39, 33–37. Alexander, J.E., Foehrenbach, J., Fisher, S., Sullivan, D., 1973. Mercury in striped bass and bluefish. N. Y. Fish Game J. 20, 147–151. Alley, W.P., Brown, H.r., Kawasaki, L.W., 1974. Lead concentrations in the wooly sculpin, Clinocottus analis, collected from tidepools of California. Calif. Fish Game 60, 50–51. Al-Reasi, H.A., Ababneh, F.A., Lean, D.R., 2007. Evaluating mercury biomagnification in fish from a tropical marine environment using stable isotopes (d 13C and d 15N). Environ. Toxicol. Chem. 26, 1572–1581.
192 Chapter 3 Al-Yakoob, S., Bou-Olayan, A.H., Bahloul, M.H., 1994. Trace metals in gills of fish from the Arabian Gulf. Bull. Environ. Contam. Toxicol. 53, 718–725. Amend, D.F., 1970. Retention of mercury by salmon. Prog. Fish-Cult. 32, 192–194. Amiard, J.C., 1975. Interpretation d’une etude experimentale du metabolisme du radiostrontium chez la plie (Pleuronectes platessa) a l’aide des analyses factorielles. Rev. Int. Ocean. Med. 39/40, 177–212. Amiard-Triquet, C., Amiard, J.C., 1974. Contamination de chaines trophiques marine par le cobalt 60. Rev. Int. Ocean. Med. 33, 49–59. Amlund, H., Francesconi, K.A., Bethune, C., Lundebye, A.K., Bentssen, M.H.G., 2006. Accumulation and elimination of dietary arsenobetaine in two species of fish: Atlantic salmon (Salmo salar L.) And Atlantic cod (Gadus morhua L.). Environ. Toxicol. Chem. 25, 1787–1794. Amlund, H., Lundebye, A.K., Bentssen, M.H.G., 2007. Accumulation and elimination of methylmercury in Atlantic cod (Gadus morhua L.) following dietary exposure. Aquat. Toxicol. 83, 323–330. Ancellin, J., Vilquin, A., 1966. Contaminations experimentales d’especes marines par le cerium-144, le ruthenium-106, et le zirconium-95. In: Disposal of Radioactive Wastes into Seas, Ocean and Surface Water. IAEA, Vienna, pp. 583–604. Ancellin, J., Vilquin, A., 1968. Nouvelles etudes de contaminations experimentales d’especes marines par le cesium 137, le ruthenium 106 et le cerium 144. Radioprotection 3, 185–213. Ancellin, J., Bovard, P., Vilquin, A., 1967. New studies on experimental contamination of marine species by ruthenium-106. In: Actes du Cong. Int. Radioprotect. Milieu, Soc. Franc. Radioprotect., Toulouse, France, 14–16 January 1967, pp. 213–234. Andersen, A.T., Dommasnes, A., Hesthagen, I.H., 1973. Some heavy metals in sprat (Sprattus sprattus) and herring (Clupea harengus) from the inner Oslofjord. Aquaculture 2, 17–22. Anderson, B.H., Middaugh, D.P., Hunt, J.W., Turpen, S.L., 1991. Copper toxicity to sperm, embryos and larvae of topsmelt. Atherinops affinis with notes on induced spawning. Mar. Environ. Res. 31, 17–35. Anonymous, 1978. Selected pollution profiles: North Atlantic, North Sea, Baltic Sea, and Mediterranean Sea. Ambio 7, 75–78. Arima, S., Umemoto, S., 1976. Mercury in aquatic organisms—II. Mercury distribution in muscles of tunas and swordfish. Bull. Jpn. Soc. Sci. Fish 42, 931–937. Arleny, I., Tabouret, H., Rodriguez-Gonzalez, P., Bareille, G., Donard, O.F.X., Amouroux, D., 2007. Methylmercury bioconcentration in muscle tissue of the European eel (Anguilla anguilla) from the Adour estuary (Bay of Biscay, France). Mar. Pollut. Bull. 54, 1031–1036. Armstrong, F.A.J., 1979. Effects of mercury compounds on fish. In: Nriagu, J.O. (Ed.), The Biogeochemistry of Mercury in the Environment. Elsevier/North Holland Biomedical Press, New York, pp. 657–670. Arslan, Z., Secor, D.H., 2008. High resolution micromill sampling for analysis of fish otoliths by ICP-MS: Effects of sampling and specimen preparation on trace element fingerprints. Mar. Environ. Res. 66, 364–371. Ashraf, W., Seddigi, Z., Abulkibash, A., Khalid, M., 2006. Levels of selected metals in canned fish consumed in Kingdom of Saudi Arabia. Environ. Monit. Assess. 117, 271–279. Babji, A.S., Embong, M.S., Woon, W.W., 1979. Heavy metal contents in coastal water fishes of West Malaysia. Bull. Environ. Contamin. Toxicol. 23, 830–836. Baeyens, W., Leermakers, M., Papina, T., Saprykin, A., Brion, N., Noyen, J., De Gieter, M., Elskens, M. 2003. Bioconcentration and biomagnification of mercury and methylmercury in North Sea and Scheldt estuary fish. Arch. Environ. Contam. Toxicol. 45, 498–508. Badsha, K.S., Sainsbury, M., 1978. Some aspects of the biology and heavy metal accumulation of the fish Liparis liparis in the Severn Estuary. Estuar. Coast. Mar. Sci. 7, 381–391. Bagenal, T.B., Mackereth, F.J.H., Heron, J., 1973. The distinction between brown trout and sea trout by the strontium content of their scales. J. Fish Biol. 5, 555–557. Baldi, F., Renzoni, A., Bernhard, M., 1978. Mercury concentrations in pelagic fishes (anchovy, mackerel and sardine) from the Italian coast and the Strait of Gibralter. J. Etud. Pollut. IV, 251–254. Baptist, J.P., Price, T.J., 1962. Accumulation and retention of cesium-137 by marine fishes. U.S. Fish. Bull. 206, 177–187.
Fishes 193 Baptist, J.P., Hoss, D.E., Lewis, C.W., 1970. Retention of chromium-51, iron-59, cobalt-60, zinc-65, strontium-85, niobium-95, indium-114m, and iodine-131 by the Atlantic croaker (Micropogon undulatus). Health Phys. 18, 141–148. Barak, N.A.E., Mason, C.F., 1990. Mercury, cadmium, and lead in eels and roach: the effects of size, season and locality on metal concentrations in flesh and liver. Sci. Total Environ. 92, 249–256. Barber, R.T., Whaling, P.J., 1983. Mercury in marlin and sailfish. Mar. Pollut. Bull. 14, 395–396. Barber, R.T., Vijayakumar, A., Cross, F.A., 1972. Mercury concentrations in recent and ninety-year old benthopelagic fish. Science 178, 636–639. Barber, R.T., Whaling, P.J., Cohen, D.M., 1984. Mercury in recent and century-old deep-sea fish. Environ. Sci. Technol. 18, 552–555. Bargagli, R., Monaci, F., Sanchez-Hernandez, J.C., Cateni, D., 1998. Biomagnification of mercury in an Antarctic marine coastal food web. Mar. Ecol. Prog. Ser. 169, 65–76. Beasley, T.M., 1971. Mercury in selected fish protein concentrates. Environ. Sci. Technol. 5, 634–635. Beasley, T.M., Held, E.E., Conrad, R.M., 1972. Iron-55 in Rongelap people, fish and soils. Health Phys. 22, 245–250. Bebbington, G.N., Mackay, N.J., Chvojka, R., Williams, R.J., Dunn, A., Auty, E.H., 1977. Heavy metals, selenium and arsenic in nine species of Australian commercial fish. Aust. J. Mar. Freshw. Res. 28, 277–286. Beck, A.B., 1956. The copper content of the liver and blood of some vertebrates. Aust. J. Zool. 4, 1–18. Benedetti, M., Martuccio, G., Fattorini, D., Canapa, A., Barucca, M., Nigro, N., et al., 2007. Oxidative and modulatory effects of trace metals on metabolism of polycyclic aromatic hydrocarbons in the Antarctic fish, Trematomus bernacchii. Aquat. Toxicol. 85, 165–175. Bengtsson, B.E., 1977. Accumulation of cadmium in some aquatic animals from the Baltic Sea. Ambio 5, 69–73 (Special Report). Berglund, F., Berlin, M., 1969. Human risk evaluation for various population in Sweden due to methylmercury in fish. In: Miller, M.W., Berg, G.G. (Eds.), Chemical Fallout, Current Research on Persistent Pesticides, Chas. C. Thomas, Springfield, IL, pp. 423–432. Bernhard, M., Zattera, A., 1975. In: Pearson, E.A., Frangipane, E.D. (Eds.), Marine Pollution and Marine Waste Disposal. Pergamon, Elmsford, NY, pp. 195–300. Bielmyer, G.K., Tomasso, J., Klaine, S.J., 2006. Physiological responses of hybrid striped bass to aqueous copper in freshwater and saltwater. Arch. Environ. Contam. Toxicol. 50, 531–538. Bird, D.J., Rotchell, J.M., Hesp, S.A., Newton, L.C., Hall, N.G., Potter, I.C., 2008. To what extent are hepatic concentrations of heavy metals in Anguilla anguilla at a site in a contaminated estuary related to body size and age and reflected in the metallothionein concentrations? Environ. Pollut. 151, 641–651. Birdsong, C.L., Avault Jr., J.W., 1971. Toxicity of certain chemicals to juvenile pompano. Prog. Fish-Cult. 33, 76–80. Birge, W.J., Black, J.A., 1979. Effects of copper on embryonic and juvenile stages of aquatic animals. In: Nriagu, J.O. (Ed.), Copper in the Environment. Part 2. Health Effects. Wiley, New York, pp. 373–399. Bligh, E.G., 1972. Mercury in Canadian fish. J. Inst. Can. Sci. Tech. Alim. 5(1), A6–A14. Bloom, N.S., 1992. On the chemical form of mercury in edible fish and marine invertebrate tissue. Can. J. Fish. Aquat. Sci. 49, 1010–1017. Bloom, H., Ayling, G.M., 1977. Heavy metals in the Derwent Estuary. Environ. Geol. 2, 3–22. Bohn, A., 1975. Arsenic in marine organisms from West Greenland. Mar. Pollut. Bull. 6, 87–89. Bohn, A., Fallis, B.W., 1978. Metal concentrations (As, Cd, Cu, Pb and Zn) in shorthorn sculpins, Myoxocephalus scorpius (Linnaeus), and Arctic char, Salvelinus alpinus (Linnaeus), from the vicinity of Strathcona Sound, Northwest Territories. Water Res. 12, 659–663. Bohn, A., McElroy, R.A., 1976. Trace metals (As, Cd, Cu, Fe, and Zn) in Arctic cod, Boreogadus saida, and selected zooplankton from Strathcona Sound, Northern Baffin Island. J. Fish. Res. Bd. Can. 33, 2836–2840. Bollingberg, H.J., Johansen, P., 1979. Lead in spotted wolffish, Anarhichas minor, near a zinc-lead mine in Greenland. J. Fish. Res. Bd. Can. 36, 1023–1028.
194 Chapter 3 Boroughs, H., Townsley, S.J., Hiatt, R.W., 1956a. The metabolism of radionuclides by marine organisms. I. The uptake, accumulation, and loss of strontium-89 by fishes. Biol. Bull. 111, 336–351. Boroughs, H., Townsley, S.J., Hiatt, R.W., 1956b. The metabolism of radionuclides by marine organisms. II. The uptake, accumulation, and loss of yttrium-91 by marine fish, and the importance of short lived radionuclides in the sea. Biol. Bull. 111, 352–357. Branco, V., Vale, C., Canario, J., dos Santos, M.N., 2007. Mercury and selenium in blue shark (Prionace glauca, L. 1758) and swordfish (Xiphias gladius, L. 1758) from two areas of the Atlantic Ocean. Environ. Pollut. 150, 373–380. Brewer, D.T., Milton, D.A., Fry, G.C., Dennis, D.M., Heales, D.S., Venables, W.N., 2007. Impacts of gold mine waste disposal on deepwater fish in a pristine tropical marine ecosystem. Mar. Pollut. Bull. 54, 309–321. Brooks, R.R., Rumsey, D., 1974. Heavy metals in some New Zealand commercial sea fishes. N. Z. J. Mar. Freshw. Res. 8, 15–166. Brown, J.A., 2006. Classification of juvenile flatfishes to estuarine and coastal habitats based on the elemental composition of otoliths. Estuar. Coast. Shelf Sci. 66, 594–611. Buckler, D.R., Mehrle, P.M., Cleveland, L., Dwyer, F.J., 1987. Influence of pH on the toxicity of aluminum and other inorganic contaminants to east coast striped bass. Water Air Soil Pollut. 35, 97–106. Burger, J., Gochfeld, M., 2004. Mercury in canned tuna: white versus light and temporal variation. Environ. Res. 96, 239–249. Burger, J., Cooper, K., Saliva, J., Gochfeld, D., Lipsky, D., Gochfeld, M., 1992. Mercury bioaccumulation in organisms from three Puerto Rican estuaries. Environ. Monit. Assess. 22, 181–197. Burger, J., Stern, A.H., Gochfeld, M., 2005. Mercury in commercial fish: optimizing individual choices to reduce risk. Environ. Health Perspect. 113, 266–270. Burger, J., Gochfeld, M., Jeitner, C., Burke, S., Stamm, T., 2007a. Metal levels in flathead sole (Hippoglossoides elassodon) and great sculpin (Myoxocephalus polyacanthocephalus) from Adak Island, Alaska: Potential risk to predators and fisherman. Environ. Res. 103, 62–69. Burger, J., Fossi, C., McClellan-Green, P., Orlando, E.F., 2007b. Methodologies, bioindicators, and biomarkers for assessing gender-related differences in wildlife exposed to environmental chemicals. Environ. Res. 104, 135–152. Burger, J., Gochfeld, M., Jeitner, C., Burke, S., Stamm, T., Snigaroff, R., et al., 2007c. Mercury levels and potential risk from subsistence foods from the Aleutians. Sci. Total Environ. 384, 93–105. Burton, D.J., Fisher, D.J., 1990. Acute toxicity of cadmium, copper, zinc, ammonia, 3,30 -dichlorbenzidine, 2,6dichloro-4-nitroanaline, methylene chloride, and 2,4,6-trichlorophenol to juvenile grass shrimp and killifish. Bull. Environ. Contam. Toxicol. 44, 776–783. Cai, Y., Rooker, J.R., Gill, G.A., Turner, J.P., 2007. Bioaccumulation of mercury in pelagic fishes from the northern Gulf of Mexico. Can. J. Fish. Aquat. Sci. 64, 458–469. Calabrese, A., Thurberg, F.P., Dawson, M.A., Wenzloff, D.R., 1975. Sublethal physiological stress induced by cadmium and mercury in winter flounder, Pseudopleuronectes americanus. In: Koeman, J.H., Strik, J.J.T.W.A. (Eds.), Sublethal Effects of Toxic Chemicals on Aquatic Animals. Elsevier, Amsterdam, pp. 15–21. California Department Fish Game, 1990. Laboratory Quality Assurance Program Plan. Environ. Serv. Div., Calif. Dept. Fish Game, Sacramento, CA. Canapa, A., Barucca, M., Gorbi, S., Benedetti, M., Zucchi, S., Biscotti, M.A., et al., 2007. Vitellogenin gene expression in males of the Antarctic fish Trematomus bernacchii from Tera Nova Bay (Ross Sea): A role for environmental cadmium. Chemosphere 66, 1270–1277. Canli, M., Stagg, R.M., 1996. The effects of in vivo exposure to cadmium, copper and zinc on the activities of gill atpases in the Norway lobster, Nephrops norvegicus. Arch. Environ. Contam. Toxicol. 31, 494–501. Cardwell, R.D., Sheldon, A.W., 1986. A risk assessment concerning the fate and effects of tributyltins in the aquatic environment. In: Maton, G.L. (Ed.), Proceedings Oceans 86 Conference, Washington, DC, September 23-25, 1986, vol. 4 Organotin Symposium. Available from Marine Technology Society, 2000 Florida Ave. NW, Washington, DC, pp. 1117–1129.
Fishes 195 Champ, M.A., 1986. Organotin symposium: introduction and review. In: Maton, G.L. (Ed.), Proceedings Oceans 86 Conference, Washington, DC, September 23-25, 1986. Available from Marine Technology Society, 2000 Florida Ave. NW, Washington, DC, pp. 1093–1100. Cheevparanapivat, V., Menasveta, P., 1979. Total and organic mercury in marine fish of the upper Gulf of Thailand. Bull. Environ. Contam. Toxicol. 23, 291–299. Chernoff, B., Dooley, J.K., 1979. Heavy metals in relation to the biology of the mummichog, Fundulus heteroclitus. J. Fish Biol. 14, 309–328. Cheung, K.C., Leung, H.M., Wong, M.H., 2008. Metal concentrations of common freshwater and marine fish from the Pearl River delta, South China. Arch. Environ. Contam. Toxicol. 54, 705–715. Chien, L.C., Yeh, C.Y., Jiang, C.B., Hsu, C.S., Han, B.C., 2007. Estimation of acceptable mercury intake from fish in Taiwan. Chemosphere 67, 29–35. Childs, E.A., Gaffke, J.N., 1973. Mercury content in Oregon ground fish. U.S. Dept. Comm. Fish. Bull. 71, 713–717. Choi, M.H., Cech Jr., J.J., 1998. Unexpectedly high mercury level in pelleted commercial fish feed. Environ. Toxicol. Chem. 17, 1979–1981. Chou, C.L., 2007. A time series of mercury accumulation and improvement of dietary feed in net caged Atlantic salmon (Salmo salar). Mar. Pollut. Bull. 54, 720–725. Chow, T.J., Patterson, C.C., Settle, D., 1974. Occurrence of lead in tuna. Nature 251, 159–161. Chvojka, R., Williams, R.J., 1980. Mercury levels in six species of Australian commercial fish. Aust. J. Mar. Freshw. Res. 31, 469–474. Chvojka, R., Williams, R.J., Fredrickson, S., 1990. Methyl mercury, total mercury, and selenium in snapper from two areas of the new South Wales coast. Aust. Mar. Pollut. Bull. 21, 570–573. Clark, G., Topping, G., 1989. Mercury concentrations in fish from contaminated areas in Scottish waters. J. Mar. Biol. Assoc. U.K. 69, 437–445. Cocoros, G., Cahn, P.H., Siler, W., 1973. Mercury concentrations in fish, plankton, and water from three western Atlantic estuaries. J. Fish Biol. 5, 641–647. Cogun, H.Y., Yuzereroglu, T.A., Firat, O., Gok, G., Kargin, F., 2006. Metal concentrations in fish species from the northeast Mediterranean Sea. Environ. Monit. Assess. 121, 431–438. Craik, J.C.A., Harvey, S.M., 1988. A preliminary account of metal levels in eggs of farmed and wild Atlantic salmon and their relation to egg viability. Aquaculture 73, 309–321. Crawford, J.K., Luoma, S.N., 1993. Guidelines for Studies of Contaminants in Biological Tissues for the National Water Quality Assessment Program. U.S. Geological Survey Open File Report. USGS, Lemoyne, PA, pp. 92–494. Cross, F.A., Hardy, L.H., Jones, N.Y., Barber, R.T., 1973. Relation between total body weight and concentrations of manganese, iron, copper, zinc and mercury in white muscle of bluefish (Pomatomus saltatrix) and bathyldemersal fish (Antimora rostrata). J. Fish. Res. Bd. Can. 30, 1287–1291. Cugurra, F., Maura, G., 1976. Mercury content in several species of marine fish. Bull. Environ. Contam. Toxicol. 15, 568–573. Cumont, G., Viallex, G., Lelievre, H., Bobenreith, P., 1972. Mercury contamination of fish of the sea. Rev. Int. Ocean. Med. 28, 95–127. Cumont, G., Gilles, G., Bernard, F., Briand, M.B., Stephan, G., Ramonda, G., et al., 1975. Bilan de la contamination des poissons de mer par le mercure a l’occasion d’un controle portant sur 3 annees. Ann. Hyg. L. Fr.-Med. et Nut. 11(1), 17–25. Cunningham, P., Cooter, W., Sullivan, E., 2003. Mercury in marine life database. Prepared by RTI International for U.S. Environmental Protection Agency, April 2003. Custer, T.W., Mitchell, C.A., 1993. Trace elements and organochlorines in the shoalgrass community of the lower Laguna Madre, Texas. Environ. Monit. Assess. 25, 235–246. Cutshall, N.H., Naidu, J.R., Pearcy, W.G., 1977a. Zinc-65 specific activities in the migratory Pacific hake, Merluccius productus. Mar. Biol. 40, 75–80.
196 Chapter 3 Cutshall, N.H., Naidu, J.R., Pearcy, W.G., 1977b. Zinc and cadmium in the Pacific hake Merluccius productus off the western U.S. coast. Mar. Biol. 44, 195–202. Cutshall, N.H., Naidu, J.R., Pearcy, W.G., 1978. Mercury concentrations in the Pacific hake Merluccius productus (Ayres), as a function of length and latitude. Science 200, 1489–1491. Dahab, O.A., Khalil, A.N., Halim, Y., 1990. Chromium fluxes through Mex Bay inshore waters. Mar. Pollut. Bull. 21, 68–73. Davies, F.C.W., 1991. Minamata disease: a 1989 update on the mercury poisoning epidemic in Japan. Environ. Geochem. Health 13, 35–38. Davies, I.M., McKie, J.C., 1987. Accumulation of total tin and tributyltin in muscle tissue of farmed Atlantic salmon. Mar. Pollut. Bull. 18, 405–407. Davies, I.M., Bailey, S.K., Moore, D.C., 1987. Tributyltin in Scottish sea lochs, as indicated by degree of imposex in the dog whelk, Nucella lapillus (L.). Mar. Pollut. Bull. 18, 404–407. Dawson, M.A., 1982. Effects of long-term mercury exposure on hematology of striped bass, Morone saxatilis. U.S. Natl. Mar. Fish. Serv. Fish. Bull. 80, 389–392. Dean, R.J., Shimmield, T.M., Black, K.D., 2007. Copper, zinc and cadmium in marine cage fish farm sediments: an extensive survey. Environ. Pollut. 145, 84–95. Debruyn, A.M.H., Trudel, M., Eyding, N., Harding, J., McNally, H., Mountain, R., et al., 2006. Ecosystemic effects of salmon farming increase mercury contamination in wild fish. Environ. Sci. Technol. 40, 3489–3493. DeClerck, R., Vanderstappen, R., Vyncke, W., 1974. Mercury content of fish and shrimps caught off the Belgian coast. Ocean Manage. 2, 117–126. DeClerck, R., Vanderstappen, R., Vyncke, W., Van Hoeyweghen, P., 1979. La teneur en metaux lourds dans les organisms marins provenant de la capture accessoire de la peche coteire belge. Rev. de l’Agric. 3(32), 793–801. De Gieter, M., Leermakers, M., Van Ryssen, M., Noyen, J., Goeyens, I., Baeyens, W., 2002. Total and toxic arsenic levels in North Sea fish. Arch. Environ. Contam. Toxicol. 43, 406–417. Dehlinger, P., Fitzgerald, W.F., Feng, S.Y., Paskausky, D.F., Garvine, R.W., Bohlen, W.F., 1973. Determination of budgets of heavy metal wastes in Long Island Sound. Annual Report. Pts. I and II. University of Connecticut, Marine Sciences Institute, Groton, CT. De Marco, S.G., Botte, S.E., Marcovecchio, J.E., 2006. Mercury distribution in abiotic and biological compartments within several estuarine systems from Argentina: 1980–2005 period. Chemosphere 65, 213–223. Denton, G.R.W., Concepcion, L.P., Wood, H.R., Morrison, R.J., 2006. Trace metals in marine organisms from four harbours in Guam. Mar. Pollut. Bull. 52, 1784–1804. Dethlefsen, V., Westernhagen, H.V., Rosenthal, H., 1975. Cadmium uptake by marine fish larvae. Helg. wiss. Meeres. 27, 396–407. Dietz, R., Riget, F., Johansen, P., 1996. Lead, cadmium, mercury and selenium in Greenland marine animals. Sci. Total Environ. 186, 67–93. Dix, T.G., Martin, A., Ayling, G.M., Wilson, K.C., Ratkowsky, D.A., 1975. Sand flathead (Platycephalus bassensis), an indicator species for mercury pollution in Tasmanian waters. Mar. Pollut. Bull. 6, 142–144. Dixon, R., Jones, B., 1994. Mercury concentrations in stomach contents and muscle of five fish species from the north east coast of England. Mar. Pollut. Bull. 28, 741–745. Dodoo, D.K., Engel, D.W., Sunda, W.G., 1992. Effect of cupric ion activity on calcium accumulation in juvenile flounder (Paralichthys spp.). Mar. Environ. Res. 33, 101–109. Doi, R., Ui, J., 1975. The distribution of mercury in fish and its form of occurrence. In: Krenkel, P.A. (Ed.), Heavy Metals in the Aquatic Environment. Pergamon, Elmsford, NY, pp. 197–221. Drevnick, P.E., Horgan, M.J., Oris, J.T., Kynard, B.E., 2006. Ontogenetic dynamics of mercury accumulation in Northwest Atlantic sea lamprey (Petromyzon marinus). Can. J. Fish. Aquat. Sci. 63, 1058–1066. Duke, T.W., Baptist, J.P., Hoss, D.E., 1966a. Bioaccumulation of radioactive gold used as a sediment tracer in the estuarine environment. U.S. Fish. Bull. 65, 427–436. Duke, T.W., Willis, J.N., Price, T.J., 1966b. Cycling of trace elements in the estuarine environment. I. Movement and distribution of zinc-65 and stable zinc in experimental ponds. Chesapeake Sci. 7, 1–10.
Fishes 197 Dural, M., Goksu, M.Z.L., Ozak, A.K., Derici, B., 2006. Bioaccumulation of some heavy metals in different tissues of Dicentrarchus labrax L, 1758, Sparus aurata L. 1758 and Mugil cephalus L, 1758 from the Camlik lagoon of the eastern coast of Mediterranean (Turkey). Environ. Monit. Assess. 118, 65–74. Ecological Analysts, Inc., 1981. The Sources, Chemistry, Fate, and Effects of Chromium in Aquatic Environments. Available from American Petroleum Institute, Washington, DC, p. 207. Edmonds, J.S., Francesconi, K.A., 1987. Trimethylarsine oxide in estuary catfish (Cnidoglanis. macrocephalus) and school whiting (Sillago bassensis) after oral administration of sodium arsenate; and as a natural component of estuary catfish. Sci. Total Environ. 64, 317–323. Edwards, R.R.C., 1967. Estimation of the respiratory rate of young plaice (Pleuronectes platessa L.) in natural conditions using zinc-65. Nature 216, 1335–1337. Edwards, S.C., MacLeod, C.L., Lester, J.N., 1999. Mercury contamination of the eel (Anguilla anguilla) and roach (Rutilus rutilus) in East Anglia, UK. Environ. Monit. Assess. 55, 371–387. Egaas, E., Julshamn, K., 1978. A method for the determination of selenium and mercury in fish products using the same digestion procedure. Atom. Absorp. Newsl. 17(6), 135–138. Eganhouse, R.P., Young, D.R., 1978. Total and organic mercury in benthic organisms near a major submarine wastewater outfall system. Bull. Environ. Contam. Toxicol. 19, 758–766. Eisler, R., 1967a. Tissue changes in puffers exposed to methoxychlor and methyl parathion. US Bur. Sport Fish. Wildl. Tech. Paper 17, 1–15. Eisler, R., 1967b. Acute toxicity of zinc to the killifish, Fundulus heteroclitus. Chesapeake Sci. 8, 262–264. Eisler, R., 1971. Cadmium poisoning in Fundulus heteroclitus (Pisces: Cyprinodontidae) and other marine organisms. J. Fish. Res. Bd. Can. 28, 1225–1234. Eisler, R., 1974. Radiocadmium exchange with seawater by. Fundulus heteroclitus (L.) (Pisces: Cyprinodontidae). J. Fish Biol. 6, 601–612. Eisler, R., 1978. Mercury contamination standards for marine environments. In: Thorp, J.H., Gibbons, J.W. (Eds.), Energy and Environmental Stress in Aquatic Systems. U.S. Dept. Energy Sympos. Ser. 48. Available as CONF-771114 from NTIS. U.S. Department Of Commerce, Springfield, VA, pp. 241–272. Eisler, R., 1980. Accumulation of zinc by marine biota. In: Nriagu, J.O. (Ed.), Zinc in the Environment. Part II. Health Effects. Wiley, New York, pp. 259–351. Eisler, R., 1981. Trace Metal Concentrations in Marine Organisms. Pergamon, Elmsford, NY, p. 687. Eisler, R., 1984. Trace metal changes associated with age of marine vertebrates. Biol. Trace Elem. Res. 6, 165–180. Eisler, R., 1993. Zinc hazards to fish, wildlife, and invertebrates: a synoptic review. U.S. Fish Wildl. Serv. Biol. Rep. 10, 106. Eisler, R., 2000a. Arsenic. In: Handbook of Chemical Risk Assessment, vol. 3. Lewis Publishers, Boca Raton, FL, pp. 1501–1566. Eisler, R., 2000b. Molybdenum. In: Handbook of Chemical Risk Assessment, vol. 3. Lewis Publishers, Boca Raton, FL, pp. 1613–1647. Eisler, R., 2000c. Cadmium. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 1–43. Eisler, R., 2000d. Lead. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 201–311. Eisler, R., 2000e. Nickel. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 411–497. Eisler, R., 2000f. Silver. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 499–550. Eisler, R., 2000g. Tin. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 551–603. Eisler, R., 2000h. Zinc. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 605–714.
198 Chapter 3 Eisler, R., 2000i. Radiation. In: Handbook of Chemical Risk Assessment, vol. 3. Lewis Publishers, Boca Raton, FL, pp. 1701–1828. Eisler, R., 2003. The Chernobyl nuclear power plant reactor accident: ecotoxicological update. In: Hoffman, D.J., Rattner, B.A., Burton Jr., C.A., Cairns Jr., J. (Eds.), Handbook of Ecotoxicology. second ed. Lewis Publishers, Boca Raton, FL, pp. 703–736. Eisler, R., 2006. Mercury Hazards to Living Organisms. CRC Press, Taylor and Francis Group, Boca Raton, FL, p. 312. Eisler, R., Edmunds, P.H., 1966. Effects of endrin on blood and tissue chemistry of a marine fish. Trans. Am. Fish. Soc. 95, 153–159. Eisler, R., Gardner, G.R., 1973. Acute toxicology to an estuarine teleost of mixtures of cadmium, copper, and zinc salts. J. Fish Biol. 5, 131–142. Eisler, R., Hennekey, R.J., 1977. Acute toxicities of Cd2+, Cr6+, Hg2+, Ni2+, and Zn2+ to estuarine macrofauna. Arch. Environ. Contam. Toxicol. 6, 315–323. Eisler, R., LaRoche, G., 1972. Elemental composition of the estuarine teleost, Fundulus heteroclitus (L.). J. Exp. Mar. Biol. Ecol. 9, 29–42. Eisler, R., Zaroogian, G.E., Hennekey, R.J., 1972. Cadmium uptake by marine organisms. J. Fish. Res. Bd. Can. 29, 1367–1369. El Hraiki, A., Kessabi, M., Sabhi, Y., Benard, P., Buhler, D.R., 1992. Contamination par le cadmium, le chrome, le mercure et le plomb des produits de la peche Marocaine preleves en Mer Mediterranee. Rev. Med. Vet. 143, 49–56. Elwood, J.W., Beauchamp, J.J., Allen, C.P., 1980. Chromium levels in fish from a lake chronically contaminated with chromates from cooling towers. Int. J. Environ. Stud. 14, 289–298. Engel, D.W., Sunda, W.G., 1979. Toxicity of cupric ion to eggs of the spot. Leiostomus xanthurus and the Atlantic silverside Menidia menidia. Mar. Biol. 50, 121–126. Establier, R., 1975a. Contenido en mercurio de las anguillas (Anguilla anguilla) de la desembocadura del rio Guadalquiver y esteros de las salinas de la zona de Cadiz. Invest. Pesq. 39(1), 249–255. Establier, R., 1975b. Concentracion de mercurio en los cabellos de la poblacion de Cadiz y pescadores de altura. Invest. Pesq. 39(2), 509–516. Establier, R., 1977. Estudio de la contaminacion marina por metales pesados y sus effectos biologicos. Inf. Tecn. Inst. Invest. Pesq. 47, 1–36. Establier, R., Gutierrez, M., Arias, A., 1978. Accumulation and histopathological effects of organic and inorganic mercury to the lisa (Mugil auratus) Risso. Invest. Pesq. 42, 65–80. Eustace, I.J., 1974. Zinc, cadmium, copper, and manganese in species of finfish and shellfish caught in the Derwent Estuary, Tasmania. Aust. J. Mar. Freshw. Res. 25, 209–220. Evans III, E.C., Peeling, T.J., Murchison, A.E., Stephen-Hassard, Q.D., 1972. A proximate biological survey of Pearl Harbor, Oahu. Rep. NUC TP 290. Available from NTIS, Springfield, VA, as AD-744 233, pp. 1–65. Fagioli, F., Locatelli, C., Landi, S., 1994. Heavy metals in the Goro Bay: sea water, sediments and mussels. Ann. Chim. 84, 129–140. Fang, S.C., 1973. Uptake and biotransformation of phenylmercuric acetate by aquatic organisms. Arch. Environ. Contam. Toxicol. 1, 18–26. Fang, J., Wang, K.X., Tang, J.L., Wang, Y.M., Ren, S.J., Wu, H.Y., et al., 2004. Copper, lead, zinc, cadmium, mercury, and arsenic in marine products of commerce from Zhejiang coastal area, China. Bull. Environ. Contam. Toxicol. 73, 583–590. Faucher, K., Fichet, D., Miramand, P., Lagardere, J.P., 2008. Impact of chronic cadmium exposure at environmental dose on escape behaviour in sea bass (Dicentrarchus labrax L.; teleostei, moronidae). Environ. Pollut. 151, 148–157. Fent, K., Stegeman, J.J., 1993. Effects of tributyltin in vivo on hepatic cytochrome P-450 forms in marine fish. Aquat. Toxicol. 24, 219–240. Fernandes, D., Bebianno, M.J., Porte, C., 2008a. Hepatic levels of metal and metallothioneins in two commercial fish species of the northern Iberian shelf. Sci. Total Environ. 391, 159–167.
Fishes 199 Fernandes, C., Fontainhas-Fernandes, A., Cabral, D., Salgado, M.A., 2008b. Heavy metals in water, sediment and tissues of Liza saliens from Esmoriz-Paramos lagoon, Portugal. Environ. Monit. Assess. 136, 267–275. Fernandez, T.V., Jones, N.V., 1990. Studies on the toxicity of zinc and copper applied singly and jointly to Nereis diversicolor at different salinities and temperatures. Trop. Ecol. 31, 47–55. Fletcher, P.E., Fletcher, G.L., 1978. The binding of zinc to the plasma of winter flounder (Pseudopleuronectes americanus): affinity and specificity. Can. J. Zool. 56, 114–120. Fletcher, P.E., Fletcher, G.L., 1980. Zinc- and copper-binding proteins in the plasma of winter flounder (Pseudopleuronectes americanus). Can. J. Zool. 58, 609–613. Fletcher, G.L., King, M.J., 1978a. Copper, zinc, calcium, magnesium, and phosphate in the gonads and livers of sockeye salmon (Oncorhynchus nerka) during spawning migration. Comp. Biochem. Physiol. 60A, 127–130. Fletcher, G.L., King, M.J., 1978b. Seasonal dynamics of Cu2+, Zn2+, Ca2+, and Mg2+ in gonads and liver of winter flounder (Pseudopleuronectes americanus): evidence for summer storage of Zn2+ for winter gonad development in females. Can. J. Zool. 56, 284–290. Fletcher, G.L., Watts, E.G., King, M.J., 1975. Copper, zinc, and total protein levels in the plasma of sockeye salmon (Oncorhynchus nerka) during their spawning migration. J. Fish. Res. Bd. Can. 31, 78–82. Forrester, C.R., Ketchen, K.S., Wong, C.C., 1972. Mercury content of spiny dogfish (Squalus acanthias) in the Strait of Georgia, British Columbia. J. Fish. Res. Bd. Can. 29, 1487–1490. Frazier, A., Vilquin, A., 1971. An experimental study of 137Cs elimination in the mullet, Mugil chelo and the blenny Blennius pholis. Mar. Biol. 10, 154–156. Freeman, H.C., Horne, D.A., 1973a. The total mercury and methylmercury content of the American eel (Anguilla rostrata). J. Fish. Res. Bd. Can. 30, 454–456. Freeman, H.C., Horne, D.A., 1973b. Sampling the edible muscle of the swordfish (Xiphias gladius) for total mercury analysis. J. Fish. Res. Bd. Can. 30, 1251–1252. Freeman, H.C., Shum, G., Uthe, J.F., 1978. The selenium content in swordfish (Xiphias gladius) in relation to total mercury content. J. Environ. Sci. Health A13(3), 235–240. Fujiki, M., 1963. Studies on the course that the causative agent of Minamata Disease was formed, especially on the accumulation of the mercury compound in the fish and shellfish of Minamata Bay. J. Kumamoto Med. Soc. 37, 494–521. Fujiki, M., 1980. The pollution of Minamata Bay by mercury and Minamata disease. In: Baker, R.A. (Ed.), Contaminants and Sediments, vol. 2. Ann Arbor Sci. Publ., Ann Arbor, MI, pp. 493–500. Fujiki, M., Hirota, R., Yamaguchi, S., 1977. The mechanism of methylmercury accumulation in fish. In: Management of Bottom Sediments Containing Toxic Substances. Proc. 2nd U.S.-Japan Experts’ Meeting, Tokyo, Japan, October 1976, pp. 89–95 U.S. Environ. Prot. Agen. Rep. 600/3-77-083. Fujiki, M., Fujiki, M., Yamaguchi, S., Hirota, R., Tajima, S., Shimojo, N., et al., 1978. Accumulation of methyl mercury in red sea bream (Chrysophrys major) via the food chain. In: Peterson, S.A., Randolph, K.K. (Eds.), Management of Bottom Sediments Containing Toxic Substances, Proc. 3rd U.S.-Japan Experts’ Meeting, Easton, Maryland, November 197787–94 U.S. Environ. Prot. Agen. Rep. 600/3-78-084. Fukai, R., 1965. Analysis of trace amounts of chromium in marine organisms by the isotope dilution of Cr-51. In: Radiochemical Methods of Analysis. IAEA, Vienna, pp. 335–351. Fukai, R., Broquet, D., 1965. Distribution of chromium in marine organisms. Bull. Inst. Oceanogr. 65(1136), 1–19. Fukai, R., Meinke, W.W., 1959. Some activation analyses of six trace elements in marine biological ashes. Nature 184, 815–816. Fukai, R., Meinke, W.W., 1962. Activation analyses of vanadium, arsenic, molybdenum, tungsten, rhenium, and gold in marine organisms. Limnol. Oceanogr. 7, 186–200. Fukai, R., Suzuki, H., Watanake, K., 1962. Strontium-90 in marine organisms during the period 1957–1961. Bull. Inst. Oceanogr. Monaco 1251, 1–16.
200 Chapter 3 Fukai, S., Tanaka, K., Kanno, S., Ukita, T., 1972. Improvements in the determination method of methyl mercury in fish tissues and the ratio of methyl mercury to total mercury in fish tissues. In: Advances in Water Pollution Research. Sixth International Conference, Jerusalem, Israel, June 8–23, 1972, pp. 819–827. Ganther, H.E., Goudie, C., Sunde, M.L., Kopecky, M.J., Wagner, P., Oh, S.H., et al., 1972. Selenium: relation to decreased toxicity of methylmercury added to diets containing tuna. Science 175, 1122–1124. Gardner, D., 1978. Mercury in fish and waters of the Irish Sea and other United Kingdom fishing grounds. Nature 272, 49–51. Gardner, W.S., Windom, H.L., Stephens, J.A., Taylor, F.E., Stickney, R.R., 1975. Concentrations of total mercury in fish and other coastal organisms: Implications to mercury cycling. In: Howell, F.G., Gentry, J.B., Smith, M.H. (Eds.), Mineral Cycling in Southeastern Ecosystems. U.S. Energy Res. Admin. Available as CONF-740513 from NTIS, U.S. Dept. Commerce, Springfield, VA, pp. 268–278. Garnier, J., Baudin, J.P., Folquiet, L., 1990. Accumulation from water and depuration of 110mAg by a freshwater fish, Salmo trutta L. Water Res. 24, 1407–1414. Giblin, F.J., Massaro, E.J., 1973. Pharmacodynamics of methylmercury in rainbow trout (Salmo gairdneri): tissue uptake, distribution, and excretion. Toxicol. Appl. Pharmacol. 24, 81–91. Gillis, C.A., Bonnevie, N.A., Wenning, R.J., 1993. Mercury contamination in the Newark Bay estuary. Ecotoxicol. Environ. Saf. 25, 214–226. Giordano, R., Arata, P., Ciaralli, L., Rinaldi, S., Giani, M., Cicero, A.M., et al., 1991. Heavy metals in mussels and fish from Italian coastal waters. Mar. Pollut. Bull. 22, 10–14. Gipouloux, J.D., Girard, C., Gipouloux, S., 1986. Number of somatic and germ cells during early stages of gonadal development in frog larvae treated with zinc sulfate. Roux’s Arch. Dev. Biol. 195, 193–196. Gnassia-Barelli, M., Romeo, M., 1993. Some aspects of lead ecotoxicology in the marine environment. Aquat. Toxicol. 26, 163–170. Goldberg, E.D., 1962. Elemental composition of some pelagic fishes. Limnol. Oceanogr. 7 (Suppl.), 72–75. Gould, E., MacInnes, J.R., 1977. Short term effects of two silver salts on tissue respiration and enzyme activity in the cunner (Tautogolabrus adspersus). Bull. Environ. Contam. Toxicol. 18, 401–408. Grady, J.R., Johnson, A.G., Sanders, M., 1989. Heavy metal content in otoliths of king mackerel (Scomberomerus cavalla) in relation to body length and age. Contrib. Mar. Sci. 31, 17–23. Greichus, Y.A., Greichus, A., Emerick, R.J., 1973. Insecticides, polychlorinated biphenyls, and mercury in wild cormorants, pelicans, their eggs, food, and environment. Bull. Environ. Contam. Toxicol. 9, 321–328. Greig, R.A., 1975. Comparison of atomic absorption and neutron activation analyses for determination of silver, chromium, and zinc in various marine organisms. Anal. Chem. 47, 1682–1684. Greig, R.A., Krzynowek, J., 1979. Mercury concentrations in three species of tunas collected from various oceanic waters. Bull. Environ. Contam. Toxicol. 22, 120–127. Greig, R.A., Wenzloff, D.E., 1977a. Trace metals in finfish from the New York Bight and Long Island Sound. Mar. Pollut. Bull. 8, 198–200. Greig, R.A., Wenzloff, D.E., 1977b. Final report of heavy metals in small pelagic finfish, euphausiid crustaceans and apex predators, including sharks, as well as on heavy metals and hydrocarbons (C15+) in sediments collected at stations in and near deepwater dumpsite 196. In: Contaminant Inputs and Chemical Characteristics, vol. III. Baseline Report of the Environmental Conditions on Deepwater Dumpsite 106. U.S. Department of Commerce, NOAA, Rockville, MD, pp. 547–564. Greig, R.A., Adams, A.E., Nelson, B.A., 1974. Physiological response of the cunner, Tautogolabrus adspersus, to cadmium. II. Uptake of cadmium by organs and tissues. U.S. Dep. Commerce NOAA Tech. Rep. NMFSSSRF-681, pp. 5–9. Greig, R.A., Wenzloff, D.R., Pearce, J.B., 1976. Distribution and abundance of heavy metals in finfish, invertebrates, and sediments collected at a deepwater disposal site. Mar. Pollut. Bull. 7, 185–187. Greig, R.A., Wenzloff, D.R., Adams, A., Nelson, B., Shelpuk, C., 1977. Trace metals in organisms from ocean disposal sites of the middle eastern United States. Arch. Environ. Contam. Toxicol. 6, 395–409.
Fishes 201 Grimanis, A.P., Zafiropoulos, D., Vassilaki-Grimani, M., 1978. Trace elements in the flesh and liver of two fish species from polluted and unpolluted areas of the Aegean Sea. Environ. Sci. Technol. 12, 723–726. Grzybowska, D., 1989. Concentration of 137Cs and 90Sr in marine fish from the southern Baltic Sea. Acta Hydrobiol. 31, 139–147. Guary, J.C., Masson, M., Fraizier, A., 1976. Etude preliminaire, in situ, de la distribution du plutonium dans differents tissues et organes de Cancer pagurus (crustacea: decapoda) et de Pleuronectes platessa (pisces: pleuronectidae). Mar. Biol. 36, 13–17. Guerin, T., Sirot, V., Volatier, J.L., Leblanc, J.C., 2007. Organotin levels in seafood and its implications for health risk in high-seafood consumers. Sci. Total Environ. 388, 66–77. Guruge, K.S., Tanabe, S., 2001. Contamination by persistent organochlorines and butyltin compounds in the west coast of Sri Lanka. Mar. Pollut. Bull. 42, 179–186. Gutierrez, M., Establier, R., Arias, A., 1978. Uptake and histopathological effects of cadmium and mercury to the sapo (Halobatrachus didactylus). Invest. Pesq. 42, 141–154. Hall Jr., L.W., Pinkney, A.E., 1985. Acute and sublethal effects of organotin compounds on aquatic biota: an interpretive literature evaluation. CRC Crit. Rev. Toxicol. 14, 159–209. Hall, W.S., Pulliam, G.W., 1995. An assessment of metals in an estuarine wetlands ecosystem. Arch. Environ. Contam. Toxicol. 39, 164–173. Hall, A.S., Teeny, F.M., Gauglitz Jr., E.J., 1976a. Mercury in fish and shellfish of the northeast Pacific. II. Sablefish, Anoplopoma fimbria. U.S. Dept. Commerce Fish. Bull. 74, 791–799. Hall, A.S., Teeny, F.M., Lewis, L.G., Hardman, W.H., Gauglitz Jr., E.J., 1976b. Mercury in fish and shellfish of the northeast Pacific. I. Pacific halibut, Hippoglossis stenolepis. U.S. Dept. Commerce Fish. Bull. 74, 783–789. Hall, R.A., Zook, E.G., Meaburn, G.M., 1978. National Marine Fisheries Service survey of trace elements in the fishery resource. U.S. Dept. Commerce NOAA Tech. Rep., NMFS SSRF-721, pp. 1–313. Hall Jr., L.W., Pinkney, A.E., Horseman, L.O., Finger, S.E., 1985. Mortality of striped bass larvae in relation to contaminants and water quality in a Chesapeake Bay tributary. Trans. Am. Fish. Soc. 114, 861–868. Hall Jr., L.W., Lenkevich, M.J., Hall, W.S., Pinkney, A.E., Bushong, S.J., 1987. Evaluation of butyltin compounds in Maryland waters of Chesapeake Bay. Mar. Pollut. Bull. 18, 78–83. Hall Jr., L.W., Zeigenfuss, M.C., Anderson, R.D., Lewis, B.L., 1995. The effect of salinity on the acute toxicity of total and free cadmium to a Chesapeake Bay copepod and fish. Mar. Pollut. Bull. 30, 376–384. Hall Jr., L.W., Scott, M.C., Killen, W.D., 1998. Ecological risk assessment of copper and cadmium in surface waters of Chesapeake Bay watershed. Environ. Toxicol. Chem. 17, 1172–1189. Hallacher, L.E., Kho, E.B., Bernard, N.D., Orcutt, A.M., Dudley Jr., W.C., Hammond, T.M., 1985. Distribution of arsenic in the sediments and biota of Hilo Bay, Hawaii. Pacific Sci. 39, 266–273. Hamada, M., Inamasu, Y., Ueda, T., 1977. On mercury and selenium in tuna fish tissues—III. Mercury distribution in yellowfin tuna. Shimonoski Univ. Fish. 25, 213–220. Hamanaka, T., Kato, H., Tsujita, T., 1977. Cadmium and zinc in ribbon seal, Histriophoca fasciata, in the Okhotsk Sea. Res. Inst. N. Pac. Fish. Hokkadio Univ. Spec. Vol. 547–561. Hamer, P.A., Jenkins, G.P., Coutin, P., 2006. Barium variations in Pagrus auratus (Sparidae) otoliths: a potential indicator of migration between an embayment and ocean waters in south-eastern Australia. Estuar. Coast. Shelf Sci. 68, 686–702. Hamilton, S.J., Buhl, K.J., 1990. Acute toxicity of boron, molybdenum, and selenium to fry of chinook salmon and coho salmon. Arch. Environ. Contam. Toxicol. 19, 366–373. Hammerschmidt, C.R., Wiener, J.G., Frazier, B.E., Rada, R.G., 1999. Methylmercury content of eggs in yellow perch related to maternal exposure in four Wisconsin lakes. Environ. Sci. Technol. 33, 999–1003. Han, B.C., Jeng, W.L., Chen, R.Y., Fang, G.T., Hung, T.C., Tseng, R.J., 1998. Estimation of target hazard quotients and potential health risks for metals by consumption of seafood in Taiwan. Arch. Environ. Contam. Toxicol. 35, 711–720. Hanaoka, K., Tagawa, S., 1985. Identification of arsenobetaine in muscle of roundnose flounder, Eopsetta grigorjewi. Bull. Jpn. Soc. Sci. Fish. 51, 1203.
202 Chapter 3 Hanna, R.G.M., 1989. Levels of heavy metals in some Red Sea fish before hot brine pools mining. Mar. Pollut. Bull. 20, 631–635. Hannerz, L., 1968. Experimental investigations on the accumulation of mercury in water organisms. Rep. Inst. Freshw. Res. Drottingholm 48, 120–176. Hansen, N., Folsom, T.R., Weitz Jr., W.E., 1978. Determination of alkali metals in blood from North Pacific albacore. Comp. Biochem. Physiol. 60A, 491–495. Hardisty, M.W., Kartar, S., Sainsbury, M., 1974. Dietary habits and heavy metal concentrations in fish from the Severn Estuary and Bristol Channel. Mar. Pollut. Bull. 5, 61–63. Harvey, B.R., 1978. Spark source mass spectrometric procedure employing stable isotopes to study the uptake of copper by fish from seawater and food. Anal. Chem. 50, 1866–1870. Harvey, J., Harwell, L., Summers, J.K., 2008. Contaminant concentrations in whole-body fish and shellfish from US estuaries. Environ. Monit. Assess. 137, 403–412. Hassani, L.H., Frenich, A.G., Benajiba, M.H., Rodriguez, M.J.G., Vidal, J.L.M., Debdoubi, A., 2006. Assessment of butyltin and phenyltin pollution in the sea mullet, Mugil cephalus, along the Moroccan and Spanish coasts (Mediterranean Sea). Arch. Environ. Contam. Toxicol. 51, 608–614. Hasselrot, T.B., 1968. Report on current field investigations concerning the mercury content in fish, bottom sediment, and water. Rep. Inst. Freshw. Res. Drottingholm 48, 102–111. Havre, G.N., Underdal, B., Christiansen, C., 1972. The content of lead and some other heavy elements in different fish species from a fjord in western Norway. In: Proceedings of an International Symposium on Environmental Health Aspects of Lead, Amsterdam, October 2–6, 1972, pp. 99–111. Havre, G.N., Underdal, B., Christiansen, C., 1973. Cadmium concentrations in some fish species from a coastal area in southern Norway. Oikos 24, 155–157. Hearnden, E.H., 1970. Mercury pollution. Fish. Can. 22(10), 3–6. Heit, M., 1979. Variability in the concentrations of seventeen trace elements in the muscle and liver of a single striped bass, Morone saxatilis. Bull. Environ. Contam. Toxicol. 23, 1–5. Held, E.E., 1971. Fallout radionuclides in Pacific Ocean tuna.Available from NTIS, Springfield, VA, as Rep. NVO-269-13, pp. 1–16. Hellou, J., Warren, W.G., Payne, J.F., Belkhode, S., Lobel, P., 1992. Heavy metals and other elements in three tissues of cod, Gadus morhua from the northwest Atlantic. Mar. Pollut. Bull. 24, 452–458. Hewett, C.J., Jefferies, D.F., 1978. The accumulation of radioactive caesium from food by the plaice (Pleuronectes platessa) and the brown trout (Salmo trutta). J. Fish Biol. 13, 143–153. Heyraud, M., Cherry, R.D., 1979. Polonium-210 and lead-210 in marine food chains. Mar. Biol. 52, 227–236. Hibaya, T., Oguri, M., 1961. Gill absorption and tissue distribution of some radionuclides (Cr-51, Hg-203, Zn-65, and Ag-110m, 110) in fish. Bull. Jpn. Soc. Sci. Fish. 27, 996–1000. Hiyama, Y., Shimizu, M., 1964. On the concentration factors of radioactive Cs, Sr, Cd, Zn, and Ce in marine organisms. Rec. Ocean. Wks. Jpn. 7(2), 43–77. Hodson, P.V., Borgmann, U., Shear, H., 1979. Toxicity of copper to aquatic biota. In: Nriagu, J.O. (Ed.), Copper in the Environment. Part 2: Health Effects. Wiley, New York, pp. 307–372. Hoffman, F.L., Hodge, V.F., Folsom, T.R., 1974. Polonium radioactivity in certain mid-water fish of the eastern temporal Pacific. Health Phys. 26, 65–70. Hogstrand, C., Wood, C.M., 1998. Toward a better understanding of the bioavailability, physiology, and toxicity of silver in fish: implications for water quality criteria. Environ. Toxicol. Chem. 17, 547–561. Holdaway, D.A., 1988. The toxicity of chromium to fish. In: Nriagu, J.O., Nieboer, E. (Eds.), Chromium in the Natural and Human Environments. Wiley, New York, pp. 369–397. Holden, A.V., Topping, G., 1972. XIV-Occurrence of specific pollutants in fish in the Forth and Tay Estuaries. Proc. R. Soc. Edin. B 71, 189–194. Hope, B.K., Rubin, J.R., 2005. Mercury levels and relationships in water, sediment, and fish tissue in the Willamette Basin, Oregon. Arch. Environ. Contam. Toxicol. 48, 367–380. Hornung, H., Ramelow, G.J., 1987. Distribution of Cd, Cr, Cu, and Zn in eastern Mediterranean fishes. Mar. Pollut. Bull. 18, 45–49.
Fishes 203 Hornung, H., Krumgalz, B.S., Cohen, Y., 1984. Mercury pollution in sediments, benthic organisms and inshore fishes of Haifa Bay, Israel. Mar. Environ. Res. 12, 191–208. Horowitz, A., Presley, B.J., 1977. Trace metal concentrations and partitioning in zooplankton, neuston, and benthos from the south Texas Outer Continental Shelf. Arch. Environ. Contam. Toxicol. 5, 241–255. Hu, J., Zhen, H., Wan, Y., Gao, J., An, W., An, L., et al., 2006. Trophic magnification of triphenyltin in a marine food web of Bohai Bay, North China: comparison to tributyltin. Environ. Sci. Technol. 40, 3142–3147. Huckabee, J.W., Blaylock, B.G., 1972. Transfer of mercury and cadmium from terrestrial to aquatic ecosystems. In: Dhar, S.K. (Ed.), Metal Ions in Biological Systems. Plenum, New York, pp. 125–160. Huckabee, J.W., Elwood, J.W., Hildebrand, S.G., 1979. Accumulation of mercury in freshwater biota. In: Nriagu, J.O. (Ed.), The Biogeochemistry of Mercury in the Environment. Elsevier/North Holland Biomedical Press, New York, pp. 277–302. Hylland, K., Haux, C., Hogstrand, C., 1992. Hepatic metallothionein and heavy metals in dab. Limanda limanda from the German Bight. Mar. Ecol. Prog. Ser. 91, 89–96. Hyvarinen, H., Valtonen, T., 1973. Seasonal changes in the liver mineral content of Coregonus nasus (Pallas), C. sensu Svardson, in the Bay of Bothnia. Comp. Biochem. Physiol. 45B, 875–881. Ichikawa, R., 1961. On the concentration factors of some important radionuclides in marine food organisms. Bull. Jpn. Soc. Sci. Fish. 27, 66–74. Ikebe, K., Tanaka, R., 1979. Determination of vanadium and nickel in marine samples by flameless and flame atomic absorption spectrophotometry. Bull. Environ. Contam. Toxicol. 21, 526–532. Ishii, T., Suzuki, H., Koyanagi, T., 1978. Determination of trace elements in marine organisms—I. Factors for variation of concentration of trace element. Bull. Jpn. Soc. Sci. Fish. 44, 155–162. Itazawa, Y., Koyama, J., 1978. Effects of oral administration of cadmium on fish–III. Comparison of the effects on the porgy and the carp. Bull. Jpn. Soc. Sci. Fish. 44, 891–895. Jacobs, G., 1977. Gesamt–und organisch gebundener Quecksilbergehalt in Fischen Deutschen Fangerunden (Total and organically bound mercury content in fishes from German fishing grounds). Z. Lebensm. Unters-Forsch. 164, 71–76. Jangard, P.M., Regier, L.W., Glaggett, F.G., March, B.E., Biely, J., 1974. Nutrient composition of experimentally produced meals from whole argentine, capelin, and lance, and from flounder and redfish filleting scrap. J. Fish. Res. Bd. Can. 31, 141–146. Jarvenpaa, T., Tillander, M., Miettinen, J.K., 1970. Methylmercury: half-time of elimination in flounder, pike, and eel. Suomen Kemist. B 43, 439–442. Jebali, J., Banni, M., Gerbej, H., Boussetta, H., Lopez-Barea, J., Alhama, J., 2008. Metallothionein induction by Cu, Cd and Hg in Dicentrarchus labrax liver: assessment by RP-HPLC fluorescence detection and spectrophotometry. Mar. Environ. Res. 65, 358–363. Jefferies, D.F., Hewett, C.J., 1971. The accumulation and excretion of radioactive caesium by the plaice (Pleuronectes platessa) and the thornback ray (Raia clavata). J. Mar. Biol. Assoc. UK 51, 411–422. Jenkins, D.W., 1980a. Biological Monitoring of Toxic Trace Metals. Volume 2. Toxic Trace Metals in Plants and Animals of the World. Part II. U.S. Environ. Protect. Agen. Rep. 600/3-80-091, pp. 505–618. Jenkins, D.W., 1980b. Biological Monitoring of Toxic Trace Metals. Volume 2. Toxic Trace Metals in Plants and Animals of the World. Part III. U.S. Environ. Protect. Agen. Rep. 600/3-80-092, pp. 1130–1148. Jenkins, D.W., 1980c. In: Biological Monitoring of Toxic Trace Metals. Volume 2. Toxic Trace Metals in Plants and Animals of the World. Part I. U.S. Environ. Protect. Agen. Rep. 600/3-80-090, pp. 30–138. Jerneloev, A., 1972. Mercury—a case study of marine pollution. In: The Changing Chemistry of the Oceans. Proc. 20th Nobel Sympos., Goteberg, Sweden, August 16–20, 1971. Wiley, New York, pp. 161–169. Jerneloev, A., Lann, H., 1971. Mercury accumulations in food chains. Oikos 22, 403–406. Jessen-Eller, K., Crivello, J.F., 1998. Changes in metallothionein mRNA and protein after sublethal exposure to arsenite and cadmium chloride in juvenile winter flounder. Environ. Toxicol. Chem. 17, 891–896. Jewett, S.C., Duffy, L.K., 2007. Mercury in fishes of Alaska, with emphasis on subsistence species. Sci. Total Environ. 387, 3–27.
204 Chapter 3 Johnels, A.G., Westermark, T., 1969. Mercury contamination of the environment in Sweden. In: Miller, M.W., Berg, G.G. (Eds.), Chemical Fallout, Current Research on Persistent Pesticides. Chas. C Thomas, Springfield, IL, pp. 221–239. Johnels, A.G., Westermark, T., Berg, W., Persson, P.I., Sjostrand, B., 1967. Pike (Esox lucius L.) and some other aquatic organisms in Sweden as indicators of mercury contamination of the environment. Oikos 18, 323–333. Johnson, D.L., Braman, R.S., 1975. The speciation of arsenic and the content of germanium and mercury in members of the pelagic Sargassum community. Deep Sea Res. 22, 503–507. Joiris, C.R., Ali, I.B., Holsbeek, L., Kanuya-Kinoti, M., Tekele-Michael, Y., 1997. Total and organic mercury in Greenland and Barents Seas demersal fish. Bull. Environ. Contam. Toxicol. 58, 101–107. Joiris, C.R., Holsbeek, L., Moatemri, N.L., 1999. Total and methylmercury in sardines. Sardinella aurita and Sardina pilchardus from Tunisia. Mar. Pollut. Bull. 38, 188–192. Joiris, C.R., Das, H.K., Holsbeek, L., 2000. Mercury accumulation and speciation in marine fish from Bangladesh. Mar. Pollut. Bull. 40, 454–457. Jones, R.F., 1960. The accumulation of nitrosyl ruthenium by fine particles and marine organisms. Limnol. Oceanogr. 5, 312–325. Jones, A.M., Jones, Y., Stewart, W.D.P., 1972. Mercury in marine organisms of the Tay region. Nature 238, 164–165. Joseph, K.O., 1989. Heavy metal contamination of fish of the estuarine environment in Madras region. Proc. Natl. Acad. Sci. India 59B, 45–50. Julshamn, K., Braekkan, O.R., 1973. The determination of cobalt in fish tissue by atomic absorption spectrophotometry. Atom. Absorp. News 12(6), 139–141. Julshamn, K., Braekkan, O.R., 1975. Determination of trace elements in fish tissues by the standard dilution method. Atom. Absorp. News 14(3), 49–52. Julshamn, K., Braekkan, O.R., 1978. The relation between the concentration of some main elements and the stages of maturation of ovaries in cod (Gadus morrhua). Fisk. Dir. Skr. Ser. Ernoering 1, 1–15. Julshamn, K., Haugsnes, J., Eriksen, J., 1978a. Major and minor element (mineral) levels in products and offal from the fishing industry. Fisk. Dir. Skr. Ser. Ernoering 1, 137–144. Julshamn, K., Haugsnes, J., Utne, F., 1978b. The contents of 14 major and minor elements (minerals) in Norwegian fish species and fish byproducts determined by atomic absorption spectrophotometry. Fisk. Dir. Skr. Ser. Ernoering 1, 117–135. Julshamn, K., Grosvik, G.E., Nedreaas, K., Maage, A., 2006. Mercury concentrations in fillets of Greenland halibut (Reinhardtius hippoglossoides) caught in the Barents Sea in January 2006. Sci. Total Environ. 372, 345–349. Kai, N., Ueda, T., Takeda, Y., Kataoka, A., 1988. The levels of mercury and selenium in blood of tunas. Nippon Suisan Gakkai Shi 54, 1981–1985. Kamps, L.R., Carr, R., Miller, H., 1972. Total mercury-monomethylmercury content of several species of fish. Bull. Environ. Contam. Toxicol. 8, 273–279. Kannan, K., Tanabe, S., Iwata, H., Tatsukawa, R., 1995. Butyltins in muscle and liver of fish collected from certain Asian and Oceanian countries. Environ. Pollut. 90, 279–290. Kannan, K., Smith Jr., R.G., Lee, R.R., Windom, H.L., Heitmuller, P.T., Macauley, J.M., et al., 1998. Distribution of total mercury and methyl mercury in water, sediment, and fish from south Florida estuaries. Arch. Environ. Contam. Toxicol. 34, 109–118. Karapetian, J.V., Shahmoradi, A.M., 1978. Arsenic concentration in canned tuna fish and sardine. Bull. Environ. Contam. Toxicol. 20, 602–605. Kari, T., Kauranen, P., 1978. Mercury and selenium contents of seals from fresh and brackish water in Finland. Bull. Environ. Contam. Toxicol. 19, 273–280. Kazantzis, G., 1971. The poison chain for mercury in the environment. Int. J. Environ. Stud. 1, 301–306. Keckes, S., Miettinen, J.J., 1972. Mercury as a marine pollutant. In: Ruivo, M. (Ed.), Marine Pollution and Sea Life. Fishing Trading News (Books), London, pp. 276–289.
Fishes 205 Kennedy, V.S., 1976. Arsenic concentrations in some coexisting marine organisms from Newfoundland and Labrador. J. Fish. Res. Bd. Can. 33, 1388–1393. Kennedy, W.A., Smith, M.S., 1972. Sablefish culture—progress in 1971. Fish Res. Bd. Can. Tech. Rep. 309, 1–15. Keskin, Y., Baskaya, R., Ozyaral, O., Yurdun, T., Luleci, N.E., Hayran, O., 2007. Cadmium, lead, mercury and copper in fish from the Marmara Sea, Turkey. Bull. Environ. Contam. Toxicol. 78, 258–261. Khan, A.T., Weis, J.S., 1993. Differential effects of organic and inorganic mercury on the micropyle of the eggs of Fundulus heteroclitus. Environ. Biol. Fishes 37, 323–327. Kifer, R.R., Payne, W.L., 1968. Selenium content of fish meal. Feedstuffs 40, 32. Kikuchi, T., Honda, H., Ishikawa, M., Yamanaka, H., Amano, K., 1978. Excretion of mercury from fish. Bull. Jpn. Soc. Sci. Fish. 44, 217–222. Kim, S.G., Eom, K.H., Kim, S.S., Jin, H.G., Kang, J.C., 2006. Kinetics of Cd accumulation and elimination in tissues of juvenile rockfish (Sebastes schlegeli) exposed to dietary Cd. Mar. Environ. Res. 62, 327–340. Kleinert, S.J., Degurse, P.E., 1972. Mercury levels in Wisconsin fish and wildlife. Wisconsin Dept. Nat. Res. Tech. Bull. 52, 1–22. Klemmer, H.W., Unninayer, C.S., Ikubo, W.I., 1976. Mercury content of biota in coastal waters in Hawaii. Bull. Environ. Contam. Toxicol. 15, 454–457. Knothe, D.W., Van Riper, G.G., 1988. Acute toxicity of sodium molybdate dehydrate (Molhibit 100) to selected saltwater organisms. Bull. Environ. Contam. Toxicol. 40, 785–790. Koeller, P.A., Wallace, G.T., 1977. Controlled ecosystem pollution experiment: Effect of mercury on enclosed water columns. V. Growth of juvenile chum salmon (Oncorhynchus keta). Mar. Sci. Commun. 3, 395–406. Kojadinovic, J., Potier, M., Le Corre, M., Cosson, R.P., Bustamante, P., 2006. Mercury content in commercial pelagic fish and its risk assessment in the western Indian Ocean. Sci. Total Environ. 366, 688–700. Kojadinovic, J., Potier, M., Le Corre, M., Cosson, R.P., Bustamante, P., 2007. Bioaccumulation of trace elements in pelagic fish from the western Indian Ocean. Environ. Pollut. 146, 548–566. Krajnovic-Ozretic, M., Ozretic, B., 1980. The ALA-D activity test in lead-exposed grey mullet Mugil auratus. Mar. Ecol. Prog. Ser. 3, 187–191. Kramer, H.J., Neidhart, B., 1975. The behavior of mercury in the system water-fish. Bull. Environ. Contam. Toxicol. 14, 699–701. Krom, M.D., Hornung, H., Cohen, Y., 1990. Determination of the environmental capacity of Haifa Bay with respect to input of mercury. Mar. Pollut. Bull. 21, 349–354. Kryshev, I., 1995. Radioactive contamination of aquatic ecosystems following the Chernobyl accident. J. Environ. Radioact. 27, 207–219. Kumagai, H., Saeki, K., 1978. Contents of total mercury, alkyl mercury, and methyl mercury in some coastal fish and shells. Bull. Jpn. Soc. Sci. Fish. 44, 807–811. Kureishy, T.W., George, M.D., Sengapta, R., 1979. Total mercury content in some marine fish from the Indian Ocean. Mar. Pollut. Bull. 10, 357–360. Lahaye, V., Bustamante, P., Dabin, W., Canney, O.V., Dhermain, F., Cesarini, C., et al., 2006. New insights from age determination on toxic element accumulation in striped and bottlenose dolphins from Atlantic and Mediterranean waters. Mar. Pollut. Bull. 52, 1219–1230. Laughlin Jr., R.B., French, W., Guard, H.E., 1986. Accumulation of bis(tributyltin) oxide by the marine mussel Mytilus edulis. Environ. Sci. Technol. 20, 884–890. Law, R.J., Jones, B.R., Baker, J.R., Kennedy, S., Milne, R., Morris, R.J., 1992. Trace metals in the livers of marine mammals from the Welsh coast and the Irish Sea. Mar. Pollut. Bull. 24, 296–304. Leah, R.T., Evans, S.J., Johnson, M.S., 1992a. Arsenic in plaice (Pleuronectes platessa) and whiting (Merlangius merlangus) from the North East Irish Sea. Mar. Pollut. Bull. 24, 544–549. Leah, R.T., Evans, S.J., Johnson, M.S., 1992b. Mercury in flounder (Platichthys flesus L.) from estuaries and coastal waters of the north-east Irish Sea. Environ. Pollut. 75, 317–322. Leah, R.T., Collings, S.E., Johnson, M.S., Evans, S.J., 1993. Mercury in plaice (Pleuronectes platessa) from the sludge disposal ground of Liverpool Bay. Mar. Pollut. Bull. 26, 436–439.
206 Chapter 3 Leatherland, T.M., Burton, J.D., 1974. The occurrence of some trace metals in coastal organisms with particular reference to the Solent region. J. Mar. Biol. Assoc. UK 54, 457–468. Leatherland, T.M., Burton, J.D., Culkin, F., McCartney, M.J., Morris, R.J., 1973. Concentrations of some trace metals in pelagic organisms and of mercury in Northeast Atlantic Ocean water. Deep Sea Res. 20, 679–685. LeBlanc, P.J., Jackson, A.L., 1973. Arsenic in marine fish and invertebrates. Mar. Pollut. Bull. 4, 88–90. Lee, C.C., Hsieh, C.Y., Tien, C.J., 2006. Factors influencing organotin distribution in different environmental compartments and their potential health risk. Chemosphere 65, 547–559. Lin, S.H., Chang, C.W., Iizuka, H., Tzeng, W.N., 2007. Salinities, not diets, affect strontium/calcium ratios in otoliths of Anguilla japonica. J. Exp. Mar. Biol. Ecol. 341, 254–263. Linko, R.R., Terho, K., 1977. Occurrence of methyl mercury in pike and Baltic herring from the Turku archipelago. Environ. Pollut. 14, 227–235. Liu, C.W., Lin, K.H., Jang, C.S., 2006a. Tissue accumulation of arsenic compounds in aquacultural and wild mullet (Mugil cephalus). Bull. Environ. Contam. Toxicol. 77, 36–42. Liu, S.M., Hsia, M.P., Huang, C.M., 2006b. Accumulation of butyltin compounds in cobia. Rachycentron canadum raised in offshore aquaculture sites. Sci. Total Environ. 355, 167–175. Lofroth, G., 1970. Methylmercury, a review of health hazards and side effects associated with the emission of mercury compounds into natural systems. Nat. Sci Res. Coun. Ecol. Res. Commun. Stockholm, Sweden Bull. 4, 1–56. Lorz, H.W., McPherson, B.P., 1977. Effects of copper and zinc on smoltification of coho salmon. U.S. Environ. Protect. Agen. Rep., 600/3-77-032, pp. 1–68. Lowman, F.G., Phelps, D.K., Ting, R.Y., Escalera, R.M., 1966. Progress summary report no. 4, marine biology program June 1965–June 1966. Puerto Rico Nucl. Cen. Rep., PRNC 85, pp. 1–57. Lowman, F.G., Martin, J.H., Ting, R.Y., Barnes, S.S., Swift, D.J.P., Seiglie, G.A., et al., 1970. Bioenvironmental and radiological-safety feasibility studies, Atlantic-Pacific interoceanic canal. Estuar. Mar. Ecol. I-IV. Prepared for Battelle Memorial Institute, Columbus, Ohio as Contract AT (26-1)-171. Lunde, G., 1967. Activation analysis of bromine, iodine, and arsenic in oils from fishes, whales, phyto- and zooplankton of marine and limnetic biotopes. Int. Revue Ges. Hydrobiol. 52, 265–279. Lunde, G., 1968a. Activation analysis of trace elements in fishmeal. J. Sci. Food Agric. 19, 432–434. Lunde, G., 1968b. Analysis of arsenic in marine oils by neutron activation. Evidence of arseno organic compounds. J. Am. Oil Chem. Soc. 45, 331–332. Lunde, G., 1969. Water soluble arseno-organic compounds in marine fishes. Nature 224, 186–187. Lunde, G., 1970. Analysis of arsenic and selenium in marine raw materials. J. Sci. Food Agric. 21, 242–247. Lunde, G., 1973a. Separation and analysis of organic-bound and inorganic arsenic in marine organisms. J. Sci. Food Agric. 24, 1021–1027. Lunde, G., 1973b. The analysis of organically bound elements (As, Se, Br) and phosphorus in raw, refined, bleached, and hydrogenated marine oils produced from fish of different quality. J. Am. Oil Chem. 50, 26–28. Lunde, G., 1973c. Trace metal contents of fishmeal and of the lipid phase extracted from fish meal. J. Sci. Food Agric. 24, 413–419. Lunde, G., 1973d. Analysis of trace elements, phosphorus and sulphur in the lipid and non-lipid phase of halibut (Hippoglossus hippoglossus) and tunny (Thunnus thynnus). J. Sci. Food Agric. 24, 1029–1038. Lunde, G., 1977. Occurrence and transformation of arsenic in the marine environment. Environ. Health Perspect. 19, 47–52. MacInnes, J.R., Thurberg, F.P., Greig, R.A., Gould, E., 1977. Long-term cadmium stress in the cunner Tautogolabrus adspersus. US Fish. Bull. 75, 199–203. Mackay, N.J., Kazacos, M.N., Williams, R.J., Ledow, M.L., 1975. Selenium and heavy metals in black marlin. Mar. Pollut. Bull. 6, 57–60. MacLeod, J.C., Pessah, E., 1973. Temperature effects on mercury accumulation, toxicity, and metabolic rate in rainbow trout, Salmo gairdneri. J. Fish. Res. Bd. Can. 30, 485–492.
Fishes 207 Maddock, B.G., Taylor, D., 1980. The acute toxicity and bioaccumulation of some lead alkyl compounds in marine animals. In: Branica, M., Konrad, Z. (Eds.), Lead in the Marine Environment. Pergamon, Oxford, UK, pp. 233–261. Magalhaes, M.C., Costa, V., Menezes, G.M., Pinho, M.R., Santos, R.S., Monteiro, L.R., 2007. Intra- and interspecific variability in total and methylmercury bioaccumulation by eight marine fish species from the Azores. Mar. Pollut. Bull. 54, 1654–1662. Maguire, R.J., Tkacz, R.J., Chau, Y.K., Bengert, G.A., Wong, P.T.S., 1986. Occurrence of organotin compounds in water and sediment in Canada. Chemosphere 15, 253–274. Maher, W.A., 1983. Selenium in marine organisms from St. Vincent’s Gulf, South Australia. Mar. Pollut. Bull. 14, 35–36. Marchetti, R., 1978. Acute toxicity of alkyl leads to some marine organisms. Mar. Pollut. Bull. 9, 206–207. Marcovecchio, J.E., 2004. The use of Micropogonias furnieri and Mugil liza as bioindicators of heavy metals pollution in the La Plata river estuary, Argentina. Sci. Total Environ. 323, 219–226. Marijic, V.F., Raspor, B., 2007. Metallothionein in intestine of red mullet, Mullus barbatus as a biomarker of copper exposure in the coastal marine areas. Mar. Pollut. Bull. 54, 935–940. Martin, D., Goldberg, E.D., 1962. Uptake and assimilation of radio-strontium by Pacific mackerel. Limnol. Oceanogr. 7 (Suppl.), 76–82. Martins, I., Costa, V., Porteiro, F.M., Santos, R.S., 2006. Temporal and spatial changes in mercury concentrations in the North Atlantic as indicated by museum specimens of glacier lanternfish Benthosema glaciale (pisces: myctophidae). Environ. Toxicol. 21, 528–532. Mason, R.P., Heyes, D., Sveinsdottir, A., 2006. Methylmercury concentrations in fish from tidal waters of the Chesapeake Bay. Arch. Environ. Contam. Toxicol. 51, 425–437. Mathews, T.D., 1994. Contaminants in recreationally important estuarine finfish from South Carolina. Bull. Environ. Contam. Toxicol. 53, 412–419. Mathieson, S., McLusky, D.S., 1995. Inter-species variation of mercury in skeletal muscle of five fish species from inshore waters of the Firth of Clyde, Scotland. Mar. Pollut. Bull. 30, 283–286. Matida, Y., Kumada, H., 1969. Distribution of mercury in water, bottom mud, and aquatic organisms of Minamata Bay, the River Agano, and other water bodies in Japan. Bull. Freshw. Fish. Res. Lab. Tokyo 19(2), 73–93. Matsunaga, K., 1976. Estimation of variation of mercury concentration in the oceans during the last several decades. J. Ocean. Soc. Jpn. 32, 48–50. Matsunaga, K., 1978. Concentration of mercury in marine animals. Bull. Fac. Fish. Hokkaido Univ. 29(1), 70–74. Mauchline, J., Templeton, W.L., 1966. Strontium, calcium, and barium in marine organisms from the Irish Sea. J. Cons. Perm. Int. Explor. Mer. 30, 161–170. Mayer Jr., F.L., 1987. Acute toxicity of chemicals to estuarine organisms. U.S. Environ. Protect Agen. Rep., EPA/ 600/8-87/017, pp. 1–274. McDermott, D.J., Alexander, G.V., Young, D.R., Mearns, A.J., 1976. Metal contamination of flatfish around a large submarine outfall. J. Water Pollut. Control Fed. 48, 1913–1918. McNulty, H.R., Anderson, B.S., Hunt, J.W., Turpen, S.L., Singer, M.M., 1994. Age-specific toxicity of copper to larval topsmelt Atherinops affinis. Environ. Toxicol. Chem. 13, 487–492. Meador, J.P., Ernest, D.W., Kagley, A., 2004. Bioaccumulation of arsenic in marine fish and invertebrates from Alaska and California. Arch. Environ. Contam. Toxicol. 47, 223–233. Mearns, A.J., Young, D.R., 1977. Chromium in the southern California marine environment. In: Giam, C.S. (Ed.), Pollutant Effects on Marine Organisms. D.C. Heath, Lexington, MA, pp. 125–142. Mears, H.C., Eisler, R., 1977. Trace metals in liver from bluefish, tautog, and tilefish in relation to body length. Chesapeake Sci. 18, 315–318. Menasveta, P., Siriyong, R., 1977. Mercury content of several predacious fish in the Andaman Sea. Mar. Pollut. Bull. 8, 200–204. Mendez, E., Giudice, H., Pereira, A., Inocente, G., Medina, D., 2001. Total mercury content—fish weight relationship in swordfish (Xiphias gladius) caught in the southwest Atlantic Ocean. J. Food Compost. Anal. 14, 453–460.
208 Chapter 3 Middaugh, D.P., Dean, J.M., 1977. Comparative sensitivity of eggs, larvae, and adults of the estuarine teleosts, Fundulus heteroclitus and Menidia menidia to cadmium. Bull. Environ. Contam. Toxicol. 17, 645–652. Middaugh, D.P., Rose, C.L., 1974. Retention of two mercurials by striped mullet Mugil cephalus. Water Res. 8, 173–177. Middaugh, D.P., Davis, W.R., Yoakum, R.L., 1975. The response of larval fish, Leiostomus xanthurus, to environmental stress following sublethal cadmium exposure. Contrib. Mar. Sci. 19, 13–19. Miettinen, V., Verta, M., 1978. On the heavy metals and chlorinated hydrocarbons in the Gulf of Bothnia in Finland. Finn. Mar. Res. 244, 219–226. Miettinen, J.K., Tillander, M., Rissanen, K., Miettinen, V., Ohmono, Y., 1969. Distribution and excretion rate of phenyl- and methylmercury nitrate in fish muscles, molluscs, and crayfish. In: Proceedings of the 9th Japanese Conference on Radioisotopes, Tokyo, pp. 474–478. Miettinen, J.K., Heyraud, M., Keckes, S., 1972. Mercury as a hydrospheric pollutant. II. Biological half-time of methylmercury in four Mediterranean species: a fish, a crab, and two molluscs. In: Ruivo, M. (Ed.), Marine Pollution and Sea Life. Fishing Trading News (Books), London, pp. 295–298. Miller, G.E., Grant, P.M., Kishore, R., Steinkruger, F.J., Rowland, F.S., Guinn, V.P., 1972. Mercury concentrations in museum specimens of tuna and swordfish. Science 175, 1121–1122. Milner, N.J., 1979. Zinc concentrations in juvenile flatfish. J. Mar. Biol. Assoc. UK 59, 761–775. Mishra, S., Bhalke, S., Saradhi, I.V., Suseela, B., Tripathi, R.M., Pandit, G.G., et al., 2007. Trace metals and organometals in selected marine species and preliminary risk assessment to human beings in Thane Creek area, Mumbai. Chemosphere 69, 972–978. Mochida, K., Ito, F., Kono, K., Onduka, T., Kakuno, A., Fujii, K., 2007. Molecular and histological evaluation of tributyltin toxicity on spermatogenesis in a marine fish (Fundulus heteroclitus). Aquat. Toxicol. 83, 73–83. Monteiro, L.R., Lopes, H.D., 1990. Mercury content of swordfish, Xiphias gladius, in relation to length, weight, age, and sex. Mar. Pollut. Bull. 21, 293–296. Monteiro, L.R., Costa, V., Furness, R.W., Santos, R.S., 1996. Mercury concentrations in prey fish indicate enhanced bioaccumulation in mesopelagic environments. Mar. Ecol. Prog. Ser. 141, 21–25. Morgan, F., 1964. The uptake of radioactivity by fish and shellfish. I. Cesium-134 by whole animals. J. Mar. Biol. Assoc. UK 44, 259–271. Morita, T., Fujimoto, K., Minamisako, Y., Yoshida, K., 2007. Detection of high concentrations of 137Cs in walleye pollock collected in the Sea of Japan. Mar. Pollut. Bull. 54, 1293–1300. Morris, R.J., Law, R.J., Allchin, C.R., Kelly, C.A., Fileman, C.F., 1989. Metals and organochlorines in dolphins and porpoises of Cardigan Bay, West Wales. Mar. Pollut. Bull. 20, 512–523. Morse, J.W., Choppin, G.R., 1991. The chemistry of transuranic elements in natural waters. Rev. Aquat. Sci. 4, 1–22. Nakayama, A., Kurokawa, Y., Harino, H., Kawahara, E., Miyadai, T., Seikai, T., et al., 2007. Effects of tributyltin on the immune system of Japanese flounder (Paralichthys olivaceus). Aquat. Toxicol. 83, 126–133. National Research Council of Canada (NRCC), 1978. Effects of Arsenic in the Canadian Environment. NRCC Publ. 15391, pp. 349. Negilski, D.S., 1976. Acute toxicity of zinc, cadmium, and chromium to the marine fishes, yellow-eye mullet (Aldrichetta forsteri C.& V.) And small-mouthed hardyhead (Atherinasoma microstoma Whitley). Aust. J. Mar. Freshw. Res. 27, 137–149. Nesto, N., Romano, S., Moschino, V., Mauri, M., Da Ros, L., 2007. Bioaccumulation and biomarker responses of trace metals and micro-organic pollutants in mussels and fish from the Lagoon of Venice, Italy. Mar. Pollut. Bull. 55, 469–484. Newell, P.F., Appleton, T.C., Brown, B.E., Carnwarth, J.W., 1979. Elemental distribution in relation to skin necroses of marine flatfishes from the English Channel. Mar. Biol. 51, 93–99. Nishimura, H., Kumagai, M., 1983. Mercury pollution of fishes in Minamata Bay and surrounding water analysis of pathway of mercury. Water Air Soil Pollut. 20, 401–411. Noel-Lambot, F., Bouquegneau, J.M., 1977. Comparative study of toxicity, uptake, and distribution of cadmium and mercury in the sea water adapted eel Anguilla anguilla. Bull. Environ. Contam. Toxicol. 18, 418–424.
Fishes 209 Noel-Lambot, F., Gierday, C., Disteche, A., 1978. Distribution of Cd, Zn, and Cu in liver and gills of the eel Anguilla anguilla with special reference to metallothioneins. Comp. Biochem. Physiol. 61C, 177–187. Norin, H., Vahter, M., Christakopoulos, A., Sandstrom, M., 1985. Concentration of inorganic and total arsenic in fish from industrially polluted water. Chemosphere 14, 1125–1134. Noshkin, V.E., 1972. Ecological aspects of plutonium dissemination in aquatic environments. Health Phys. 22, 537–549. Nriagu, J.O. (Ed.), 1978. The Biogeochemistry of Lead in the Environment. Part B. Biological Effects. Elsevier/ North Holland Biomedical Press, Amsterdam, p. 397. Nugegoda, D., Rainbow, P.S., 1989. Salinity, osmolality, and zinc uptake in Palaemon elegans (crustacea; decapoda). Mar. Ecol. Prog. Ser. 55, 149–157. Nuorteva, P., Hasanen, E., 1971. Observations on the mercury content of Myoxocephalus quadricornis (L.) (Teleostei, cottidae) in Finland. Ann. Zool. Fenn. 8, 331–335. Ociepa, A., Protasowicki, M., 1976. A relationship between total mercury content and a kind of food in some chosen Pacific fish species. Mar. Fish. Fd. Tech. 60, 83–87. Ohji, M., Harino, H., Arai, T., 2007a. Differences in organotin accumulation among ecological migratory types of the Japanese eel Anguilla japonica. Estuar. Coast. Shelf Sci. 69, 270–290. Ohji, M., Arai, T., Miyazaki, N., 2007b. Comparison of organotin accumulation in the masu salmon Oncorhynchus masou accompanying migratory histories. Estuar. Coast. Shelf Sci. 72, 721–731. Olson, K.R., Bergman, H.L., Fromm, P.O., 1973. Mercury uptake and ion distribution in gills of rainbow trout (Salmo gairdneri): tissue scans with an electron microprobe. J. Fish. Res. Bd. Can. 30, 1575–1578. Orvini, E., Gills, T.E., LaFleur, P.D., 1974. Method for determination of selenium, arsenic, zinc, cadmium, and mercury in environmental matrices by neutron activation analysis. Anal. Chem. 46, 1294–1297. Outridge, P.M., Scheuhammer, A.M., 1993. Bioaccumulation and toxicology of chromium: implications for wildlife. Rev. Environ. Contam. Toxicol. 130, 31–77. Overnell, J., McIntosh, R., Fletcher, T.C., 1987a. The enhanced induction of metallothionein by zinc, its half-life in the marine fish Pleuronectes platessa, and the influence of stress factors on metallothionein levels. Experientia 43, 178–181. Overnell, J., McIntosh, R., Fletcher, T.C., 1987b. The levels of liver metallothionein and zinc in plaice, Pleuronectes platessa L., during the breeding season, and the effect of oestradiol injection. J. Fish Biol. 30, 539–546. Overnell, J., Fletcher, T.C., McIntosh, R., 1988. The apparent lack of effect of supplementary dietary zinc on zinc metabolism and metallothionein concentrations in the turbot, Scopthalmus maximus (Linnaeus). J. Fish Biol. 33, 563–570. Padula, D.J., Daughtry, B.J., Nowak, B.F., 2008. Dioxins, PCBs, metals, metalloids, pesticides and antimicrobial residues in wild and farmed Australian southern bluefin tuna (Thunnus maccoyii). Chemosphere 72, 32–44. Papadopoulu, C., Kassimati, E.M., 1977. Stable elements in skeletal formations of fish species from Greek waters. Thal. Jugosl. 13, 187–192. Papadopoulu, C., Hadzistelios, I., Grimanis, A.P., 1972. Schedule of elements distribution in the main organs of fish Pagellus erythrinus. Hellenic Ocean. Limnol. 11, 9. Papadopoulu, C., Grimanis, A.P., Hadzistelios, I., 1973. Mercury and arsenic in a fish collected in polluted and non-polluted sea waters. Thal. Jugosl. 9, 211–218. Papadopoulu, C., Kanias, G.D., Kassimati, E.M., 1978a. Zinc content in otoliths of mackerel from the Aegean. Mar. Pollut. Bull. 9, 106–108. Papadopoulu, C., Zafiropoulos, D., Hadjistelios, I., Vasselaki-Grimani, M., Yannopoulos, C., 1978b. Trace elements in pelagic organisms and a pelagic food chain of the Aegean Sea. J. Etud. Pollut. IV, 231–232. Papadopoulu, C., Kanias, G.D., Kassimati, E.M., 1980. Trace element content in fish otoliths in relation to age and size. Mar. Pollut. Bull. 11, 68–72. Papadopoulu, C., Hadjistelios, I., Ziaka, M., Zafiropoulos, D., 1981. Stable molybdenum in plankton and pelagic fish from the Aegean Sea. Rapp. P.-V. Reun. Comm. Int. Explor. Sci. Mer Mediterr. 27, 135–138. Parvaneh, V., 1979. An investigation on the mercury contamination of Persian Gulf fish. Bull. Environ. Contam. Toxicol. 23, 357–359.
210 Chapter 3 Paulauskis, J.D., Winner, R.W., 1988. Effects of water hardness and humic aid on zinc toxicity to Daphnia magna Straus. Aquat. Toxicol. 12, 273–290. Peakall, D.B., Lovett, R.J., 1972. Mercury: its occurrence and effects in the ecosystem. BioScience 22(1), 20–25. Pearcy, W.G., Osterberg, C.L., 1968. Zinc-65 and manganese-54 in albacore Thunnus alalunga from the west coast of North America. Limnol. Oceanogr. 13, 490–498. Pentreath, R.J., 1973. The accumulation and retention of 65Zn and 54Mn by the plaice, Pleuronectes platessa L. J. Exp. Mar. Biol. Ecol. 12, 1–18. Pentreath, R.J., 1976a. The accumulation of mercury from food by the plaice, Pleuronectes platessa L. J. Exp. Mar. Biol. Ecol. 25, 51–65. Pentreath, R.J., 1976b. The accumulation of organic mercury from seawater by the plaice, Pleuronectes platessa L. J. Exp. Mar. Biol. Ecol. 24, 121–132. Pentreath, R.J., 1976c. Some further studies on the accumulation and retention of Zn-65 and Mn-54 by the plaice, Pleuronectes platessa L. J. Exp. Mar. Biol. Ecol. 21, 179–189. Pentreath, R.J., 1977a. The accumulation of cadmium by the plaice, Pleuronectes platessa L., and the thornback ray, Raja clavata L. J. Exp. Mar. Biol. Ecol. 30, 223–232. Pentreath, R.J., 1977b. The accumulation of 110mAg by the plaice, Pleuronectes platessa L. and the thornback ray, Raja clavata L. J. Exp. Mar. Biol. Ecol. 29, 315–325. Pentreath, R.J., 1977c. Radionuclides in marine fishes. Oceanogr. Mar. Biol. Ann. Rev. 15, 365–460. Pentreath, R.J., 1978. 237Pu experiments with the plaice Pleuronectes platessa. Mar. Biol. 48, 327–335. Pentreath, R.J., Jefferies, D.J., 1971. The uptake of radionuclides by I-group plaice (Pleuronectes platessa) off the Cumberland Coast, Irish Sea. J. Mar. Biol. Assoc. UK 51, 963–976. Pentreath, R.J., Lovett, M.B., 1976. Occurrence of plutonium and americium in plaice from the north-eastern Irish Sea. Nature 262, 814–816. Pentreath, R.J., Lovett, M.B., 1978. Transuranic nuclides in plaice (Pleuronectes platessa) from the north-eastern Irish Sea. Mar. Biol. 48, 19–26. Peppard, E.M., Walters, W.R., Avault Jr., J.W., Perry Jr., W.G., 1991. Toxicity of chelated copper to juvenile red drum Sciaenops ocellatus. J. World Aquacult. Soc. 22, 101–108. Peshut, P.J., Morrison, R.J., Brooks, B.A., 2008. Arsenic speciation in marine fish and shellfish from American Samoa. Chemosphere 71, 484–492. Peterson, C.L., Klawe, W.L., Sharp, G.D., 1973. Mercury in tunas: a review. US Dept. Commer. Fish. Bull. 71, 603–613. Peterson, S.A., Peck, D.V., Sickle, J.V., Hughes, R.M., 2007. Mercury concentrations in frozen whole-fish homogenates is insensitive to holding time. Arch. Environ. Contam. Toxicol. 53, 411–417. Petkevich, T.A., 1967. Elemental composition of bony tissues of plankton-feeding and benthos-feeding fish from the Northwest part of the Black Sea. Dop. Akad. Nauk Ukr. RSR Ser. B 29(2), 142–146. Pierron, F., Baudrimont, M., Bossy, A., Bourdineaud, J.P., Brethes, D., Elie, P., et al., 2007a. Impairment of lipid storage by cadmium in the European eel (Anguilla anguilla). Aquat. Toxicol. 81, 304–311. Pierron, F., Baudrimont, M., Gonzalez, P., Bourdineaud, J.P., Elie, P., Massabuau, J.C., 2007b. Common pattern of gene expression in response to hypoxia or cadmium in the gills of the European glass eel (Anguilla anguilla). Environ. Sci. Technol. 41, 3005–3011. Pillai, K.C., Smith, R.C., Folsom, T.R., 1964. Plutonium in the marine environment. Nature 203 (4945), 568–571. Plaskett, D., Potter, I.C., 1979. Heavy metal concentrations in the muscle tissue of 12 species of teleost from Cockburn Sound, western Australia. Aust. J. Mar. Freshw. Res. 30, 607–616. Ploetz, D.M., Fitts, B.E., Rice, T.M., 2007. Differential accumulation of heavy metals in muscle and liver of a marine fish (king mackerel, Scomberomorus cavalla Cuvier) from the northern Gulf of Mexico, USA. Bull. Environ. Contam. Toxicol. 78, 134–137. Portmann, J.E., 1972. The levels of certain metals in fish from coastal waters around England and Wales. Aquaculture 1, 91–96. Poston, H.A., Ketola, H.G., 1989. Chemical composition of maturing and spawning Atlantic salmon from different locations. Prog. Fish-Cult. 51, 133–139.
Fishes 211 Pouvreau, B., Amiard, J.C., 1974. Etude experimentale de l’accumulation de l’argent 110 m chez divers organismes marins. Comm. Ener. Atom. France, Rept. CEA-R-4571, pp. 1–19. Pruell, D., Engelhardt, F.R., 1980. Liver cadmium uptake, catalase inhibition and cadmium thionein production in the killifish (Fundulus heteroclitus) induced by experimental cadmium exposure. Mar. Environ. Res. 3, 101–111. Radoux, D., Bouquegneau, J.M., 1979. Uptake of mercuric chloride form sea water by Serranus cabrilla. Bull. Environ. Contam. Toxicol. 22, 771–778. Ramalhosa, E., Pato, P., Monterrosa, P., Pereira, E., Vale, C., Duarte, A.C., 2006. Accumulation versus remobilization of sediments of a contaminated lagoon. Mar. Pollut. Bull. 52, 353–356. Ramelow, G., Hornung, H., 1978. An investigation into possible mercury losses during lyophilization of marine biological samples. Atom. Absorp. News 17(3), 59–60. Ramelow, G.J., Webre, C.L., Mueller, C.S., Beck, J.N., Young, J.C., Langley, M.P., 1989. Variations of heavy metals and arsenic in fish and other organisms from the Calcasieu River and Lake, Louisiana. Arch. Environ. Contam. Toxicol. 18, 804–818. Ramos, A., deCampos, M., Olszyana-Marzys, A.E., 1979. Mercury contamination of fish in Guatemala. Bull. Environ. Contam. Toxicol. 22, 488–493. Rao, T.A., 1984. Iron, copper, and molybdenum in the different body parts of some clupeoids. Indian J. Fish. 31, 357–360. Ratkowsky, D.A., Dix, T.G., Wilson, K.C., 1975. Mercury in fish in the Derwent Estuary, Tasmania, and its relation to the position of the fish in the food chain. Aust. J. Mar. Freshw. Res. 26, 223–231. Reardon, L.S., Harrell, R.M., 1990. Acute toxicity of formalin and copper sulfate to striped bass fingerlings held in various salinities. Aquaculture 87, 255–270. Reimer, A.A., Reimer, R.D., 1975. Total mercury in some fish and shellfish along the Mexican coast. Bull. Environ. Contam. Toxicol. 14, 105–111. Reinke, J., Uthe, J.F., Freeman, H.C., Johnston, J.E., 1975. The determination of arsenite and arsenate ions in fish and shellfish by selective extraction and polarography. Environ. Lett. 8, 371–380. Reish, D.J., 1977. Effects of chromium on the life history of Capitella capitata (Annelida: Polychaeta). In: Vernberg, F.J., Calabrese, A., Thurberg, F.P., Vernberg, W.B. (Eds.), Physiological Responses of Marine Biota to Pollutants. Academic Press, New York, pp. 199–207. Renfro, J.L., Schmidt-Neilson, B., Miller, D., Benos, D., Allen, J., 1974. Methylmercury and inorganic mercury: uptake, distribution, and effect on osmoregulatory mechanisms in fishes. In: Vernberg, F.J., Vernberg, W.J. (Eds.), Pollution and Physiology of Marine Organisms. Academic Press, New York, pp. 101–122. Renfro, W.C., Fowler, S.W., Heyraud, M., LaRosa, J., 1975. Relative importance of food and water in long-term zinc-65 accumulation by marine biota. J. Fish. Res. Bd. Can. 32, 1339–1345. Renzoni, A., Bacci, E., Falciai, L., 1973. Mercury concentration in the water, sediments, and fauna of an area of the Tyrrhenian Coast. In: 6th International Symposium on Medical Oceanography, Portoroz, Yugoslavia, September 26–30, 1973, pp. 17–45. Renzoni, A., Bernhard, M., Sara, R., Stoeppler, M., 1978. Comparison between the Hg body burden of Thynnus thunnus from the Mediterranean and the Atlantic. J. Etud. Pollut. IV, 255–260. Ribeiro, C.A., Rouleau, C., Pelletier, E., Audet, C., Tjalve, H., 1999. Distribution kinetics of dietary methylmercury in the Arctic charr (Salvelinus alpinus). Environ. Sci. Technol. 33, 902–907. Ribeiro, C.A.O., Padros, J., Domingos, F.X.V., Akaishi, F.M., Pelletier, E., 2007. Histopathological evidence of antagonistic effects of tributyltin on benzo[a]pyrene toxicity in the Arctic charr (Salvelinus alpinus). Sci. Total Environ. 372, 549–553. Rice, C.D., Weeks, B.A., 1990. The influence of in vivo exposure to tributyltin on reactive oxygen formation in oyster toadfish macrophages. Arch. Environ. Contam. Toxicol. 19, 854–857. Riget, F., Dietz, R., Born, E.W., Sonne, C., Hobson, K.A., 2007. Temporal trends of mercury in marine biota of west and northwest Greenland. Mar. Pollut. Bull. 54, 72–80. Ringo, E., 1993. The effect of chromic oxide (Cr2O3) on faecal lipid and intestinal microflora of seawater-reared Arctic charr, Salvelinus alpinus (L.). Aquacult. Fish. Manage. 24, 341–344.
212 Chapter 3 Rissanen, K., Erkama, J., Miettinen, J.K., 1972. Experiments on microbiological methylation of mercury (2+) ion by the mud and sludge under aerobic and anaerobic conditions. In: Ruivo, M. (Ed.), Marine Pollution and Sea Life. Fishing Trading News (Books), London, pp. 289–292. Rivers, J.B., Pearson, J.E., Schultz, C.D., 1972. Total and organic mercury in marine fish. Bull. Environ. Contam. Toxicol. 8, 257–266. Roach, A.C., Maher, W., Krikowa, F., 2008. Assessment of metals in fish from Lake Macquarie, New South Wales, Australia. Arch. Environ. Contam. Toxicol. 54, 292–308. Robertson, D.E., 1967. Trace elements in marine organisms. Rapp. Am. BNWL 481–482, 56–59. Robertson, T., Waugh, G.D., Mol, J.C.M., 1975. Mercury levels in New Zealand snapper, Chrysophrys auratus. N. Z. J. Mar. Freshw. Res. 9, 265–272. Roling, J.A., Bain, L.J., Gardea-Torresdey, J., Brader, J., Baldwin, W.S., 2006. Hexavalent chromium reduces larval growth and alters gene expression in mummichog (Fundulus heteroclitus). Environ. Toxicol. Chem. 25, 2725–2733. Romeo, M.A., Mathieu, A., Gnassia-Barelli, M., Romana, A., Lafaurie, M., 1994. Heavy metal content and biotransformation enzymes in two fish species from the NW Mediterranean. Mar. Ecol. Prog. Ser. 107, 15–22. Rosenthal, H., Sperling, K.R., 1974. Effects of cadmium on development and survival of herring eggs. In: Blaxter, J.H.S. (Ed.), The Early Life History of Fish. Springer-Verlag, Berlin, pp. 383–396. Rosser, B.W.C., George, J.C., 1986. Molt-induced muscle atrophy decreases the zinc content of the pectoralis of the giant Canada goose (Branta canadensis maxima). Experientia 42, 549–550. Roth, I., Hornung, H., 1977. Heavy metal concentrations in water, sediments, and fish from Mediterranean coastal area, Israel, Environ. Sci. Technol. 11, 265–269. Rouleau, C., Gobeil, C., Tjalve, H., 1998. Pharmacokinetics and distribution of dietary tributyltin compared to those of methylmercury in the American plaice Hippoglossoides platessoides. Mar. Ecol. Prog. Ser. 171, 275–284. Rouleau, C., Gobeil, C., Tjalve, H., 2006. Cadmium accumulation in coastal demersal fish. Mar. Ecol. Prog. Ser. 311, 131–143. Rucker, R.R., Amend, D.F., 1969. Absorption and retention of organic mercurials by rainbow trout and chinook and sockeye salmon. Prog. Fish-Cult. 31, 197–201. Ruelas-Inzunza, J., Paez-Osuna, F., 2008. Trophic distribution of Cd, Pb, and Zn in a food web from AltataEnsenada del Pebellon subtropical lagoon, SE Gulf of California. Arch. Environ. Contam. Toxicol. 54, 584–596. Ruelas-Inzunza, J., Garate-Viera, Y., Paez-Osuna, F., 2007. Lead in clams and fish of dietary importance from Coatzacoalcos estuary (Gulf of Mexico), an industrialized tropical region. Bull. Environ. Contam. Toxicol. 79, 508–513. Sager, D.R., 2004. Mercury in tissues of selected estuarine fishes from minimally impacted bays of coastal Texas. Bull. Environ. Contam. Toxicol. 72, 149–156. Said, T.O., Farag, R.S., Younis, A.M., Shreadah, M.A., 2006. Organotin species in fish and bivalves samples collected from the Egyptian Mediterranean coast of Alexandria, Egypt. Bull. Environ. Contam. Toxicol. 77, 451–458. Sakamoto, S., Yone, Y., 1978. Requirement of red sea bream for dietary iron-II. Bull. Jpn. Soc. Sci. Fish. 44, 223–225. Salihoglu, I., Saydam, C., Yemenicioglu, S., 1987. Two toxicants, mercury and tin in the Gulf of Iskenderun. Chemosphere 16, 445–453. Saltman, B., Boroughs, H., 1960. The accumulation of zinc by fish liver slices. Arch. Biochem. Biophys. 86, 169–174. Sankar, T.V., Zynudheen, A.A., Anandan, R., Nair, P.G.V., 2006. Distribution of organochlorine pesticides and heavy metal residues in fish and shellfish from Calicut region, Kerala, India. Chemosphere 65, 583–590. Sanli, Y., Fouassin, A., Noirfalise, A., 1977. Mercury total et methylmercure dans ces conserves de poissons provenant de Turquie. Arch. Belges Med. Soc. Hyg. Med. Trav. Med. Legale March (3), 161–167. Santos, I.R., Silva-Filho, E.V., Schaefer, C., Sella, S.M., Silva, C.A., Gomes, V., et al., 2006. Baseline mercury and zinc concentrations in terrestrial and coastal organisms of Admiralty Bay, Antarctica. Environ. Pollut. 140, 304–311.
Fishes 213 Sauer, G.R., Watabe, N., 1989a. Temporal and metal-specific patterns in the accumulation of heavy metals by the scales of Fundulus heteroclitus. Aquat. Toxicol. 14, 233–248. Sauer, G.R., Watabe, N., 1989b. Ultrastructural and histochemical aspects of zinc accumulation by fish scales. Tissue Cell 21, 935–943. Saward, D., Stirling, A., Topping, G., 1975. Experimental studies on the effects of copper on a marine food chain. Mar. Biol. 29, 351–356. Sazykina, T.G., 1998. Long-distance radionuclide transfer in the Arctic seas related to fish migrations. Radiat. Prot. Dosimetry 75, 219–222. Schell, W.R., Jokela, T., Eagle, R., 1973. Natural 210Pb and 210Po in a marine environment. In: Radioactive Contamination of the Marine Environment. IAEA, Vienna, pp. 701–724. Schmidt-Nielsen, B., Sheline, J., Miller, D.S., Deldonno, M., 1977. Effect of methylmercury upon osmoregulation, cellular volume, and ion regulation in winter flounder, Pseudopleuronectes americanus. In: Vernberg, F.J., Calabrese, A., Thurberg, F.P., Vernberg, W.B. (Eds.), Physiological Responses of Marine Biota to Pollutants. Academic Press, New York, pp. 105–117. Schreiber, W., 1983. Mercury content of fishery products: data from the last decade. Sci. Total Environ. 31, 283–300. Schuhmacher, M., Bosque, M.A., Domingo, J.L., Corbella, J., 1990. Lead and cadmium concentrations in marine organism from the Tarragona coastal water, Spain. Bull. Environ. Contam. Toxicol. 44, 784–789. Schuhmacher, M., Domingo, J.L., Bosque, M.A., Corbella, J., 1992. Heavy metals in marine species from the Tarragona Coast, Spain. J. Environ. Health 27A, 1939–1948. Schultz, C.D., Crear, D., 1976. The distribution of total and organic mercury in seven tissues of the Pacific blue marlin, Makaira nigricans. Pacific Sci. 30, 101–107. Schultz, C.D., Crear, D., Pearson, J.E., Rivers, J.B., Hylin, J.W., 1976. Total and organic mercury in Pacific blue marlin. Bull. Environ. Contam. Toxicol. 15, 230–234. Schuhmacher, M., Batiste, J., Bosque, M.A., Domingo, J.L., Corbella, J., 1994. Mercury concentrations in marine species from the coastal area of Tarragona Province, Spain. Dietary intake of mercury through fish and seafood consumption. Sci. Total Environ. 156, 269–273. Scott, J.S., 1977. Back-calculated fish lengths and Hg and Zn levels from recent and 100-year-old cleithrum bones from Atlantic cod (Gadus morrhua). J. Fish. Res. Bd. Can. 34, 147–150. Settle, D.M., Patterson, C.C., 1980. Lead in albacore: Guide to lead pollution in Americans. Science 207(4436), 1167–1176. Sharif, A.K.M., Mustafa, A.I., Amin, M.N., Safiullah, S., 1993. Trace element concentrations in tropical marine fish from the Bay of Bengal. Sci. Total Environ. 138, 223–234. Shaw, J.R., Wood, C.M., Birge, W.J., Hogstrand, C., 1998. Toxicity of silver to the marine teleost (Oligocottus maculosus): effects of salinity and ammonia. Environ. Toxicol. Chem. 17, 594–600. Shaw, J.R., Jackson, B., Gabor, K., Stanton, S., Hamilton, J.W., Stanton, B.A., 2007. The influence of exposure history on arsenic accumulation and toxicity in the killifish, Fundulus heteroclitus. Environ. Toxicol. Chem. 26, 2704–2709. Shawky, S., Emons, H., 1998. Distribution pattern of organotin compounds at different trophic levels of aquatic ecosystems. Chemosphere 36, 523–535. Sherwood, M.J., Mearns, A.J., 1977. Environmental significance of fin erosion in southern California demersal fishes. Ann. N. Y. Acad. Sci. 298, 177–189. Shim, W.J., Jeon, J.K., Oh, J.R., Kim, N.S., Lee, S.H., 2002. Accumulation of tributyltin in the blood of fish: its application for monitoring in the marine environment. Environ. Toxicol. Chem. 21, 1451–1455. Shimasaki, Y., Kitano, T., Oshima, Y., Inoue, S., Imada, N., Honjo, T., 2003. Tributyltin causes masculinization in fish. Environ. Toxicol. Chem. 22, 141–144. Short, J.W., Thrower, F.P., 1986. Accumulation of tributyltins in muscle tissue of chinook salmon reared in sea pens treated with tri-n-butyltin. Mar. Pollut. Bull. 17, 542–545. Shulman, J., Brisbin, I.L., Knox, W., 1961. Effect of temperature, salinity, and food intake on the excretion of Zn65 in small marine fish. Biol. Bull. 121, 378.
214 Chapter 3 Side, J., 1987. Organotins—not so good relations. Mar. Pollut. Bull. 18, 205–206. Silver, S., Endo, G., Nakamura, K., 1994. Mercury in the environment and the laboratory. J. Jpn. Soc. Water Environ. 17, 235–243. Sims Jr., R.R., Presley, B.J., 1976. Heavy metal concentrations in organisms from an actively dredged Texas bay. Bull. Environ. Contam. Toxicol. 16, 520–527. Sirota, G.R., Uthe, J.F., 1977. Determination of tetraalkyl lead compounds in biological materials. Anal. Chem. 49, 823–825. Skei, J.M., Saunders, M., Price, N.B., 1976. Mercury in plankton from a polluted Norwegian fjord. Mar. Pollut. Bull. 7, 34–35. Skerfring, S., Hanson, K., Lindstem, J., 1970. Chromosome breakage in humans exposed to methylmercury through fish consumption. Arch. Environ. Health 21, 133–139. Soares, S.S., Martins, H., Aureliano, M., 2006. Vanadium distribution following decavanadate administration. Arch. Environ. Contam. Toxicol. 50, 60–64. Sohn, D.H., Jung, W.T., 1993. Mercury pollution in Korea. In: Proceedings of the International Symposium on Epidemiological Studies on Environmental Pollution and Health Effects of Methylmercury, Kumamoto, Japan, October 2, 1992. Published by National Institute for Minamata Disease, Kumamoto, Japan, pp. 37–43. Somasundaram, B., 1985. Effects of zinc on epidermal ultrastructure in the larva of Clupea harengus. Mar. Biol. 85, 199–207. Somasundaram, B., King, P.E., Shackley, S.E., 1985. The effect of zinc on the ultrastructure of the posterior gut and pronephric ducts of the larva of Clupea harengus L. Comp. Biochem. Physiol. 81C, 29–37. Somero, G.N., Chow, T.J., Yancey, P.H., Snyder, C.B., 1977a. Lead accumulation rates in tissues of the estuarine teleost fish, Gillichthys mirabilis: Salinity and temperature effects. Arch. Environ. Contam. Toxicol. 6, 337–348. Somero, G.N., Yancey, P.H., Chow, T.J., Snyder, C.B., 1977b. Lead effects on tissue and whole organism respiration of the estuarine teleost fish, Gillichthys mirabilis. Arch. Environ. Contam. Toxicol. 6, 349–354. Sorentino, C., 1979. Mercury in marine and freshwater fish of Papua, New Guinea. Aust. J. Mar. Freshw. Res. 30, 617–623. Spear, P.A., 1981. Zinc in the aquatic environment: chemistry, distribution, and toxicology. Nat. Res. Coun. Canada Publ., NRCC 17589, pp. 1–145. Spinelli, J., Mahnken, C. 1976. Effects of diets containing dogfish (Squalus acanthias) meal on the mercury content and growth of pen-reared coho salmon (Oncorhynchus kisutch), J. Fish. Res. Bd. Canada 33, 1771–1778. Spry, D.J., Hodson, P.V., Wood, C.M., 1988. Relative contributions of dietary and waterborne zinc in the rainbow trout, Salmo gairdneri. Can. J. Fish. Aquat. Sci. 45, 32–41. Stagg, R.M., Shuttleworth, T.J., 1982. The accumulation of copper in Platichthys flesus L. and its effects on plasma electrolyte concentrations. J. Fish Biol. 20, 491–500. Stahl, J.L., Cook, M.E., Sunde, M.L., Greger, J.L., 1989. Enhanced humoral immunity in progeny chicks fed practical diets supplemented with zinc. Appl. Agric. Res. 4, 86–89. Staveland, G., Marthinsen, I., Norheim, G., Julshamn, K., 1993. Levels of environmental pollutants in flounder (Platichthys flesus L.) and cod (Gadus morhua L.) caught in the waterway of Glomma, Norway. II. Mercury and arsenic. Arch. Environ. Contam. Toxicol. 24, 187–193. Stein, V.B., McClallan, B.E., 1980. Enhancement of atomic absorption sensitivity for cadmium, manganese, nickel, and silver and determination of submicrogram quantities of cadmium in nickel in environmental samples. Environ. Sci. Technol. 14, 872–877. Stenner, R.D., Nickless, G., 1974. Distribution of some heavy metals in organisms in Hardangerfjord and Skjerstadfjord, Norway. Water Air Soil Pollut. 3, 279–291. Stenner, R.D., Nickless, G., 1975. Heavy metals in organisms of the Atlantic coast of S.W. Spain and Portugal. Mar. Pollut. Bull. 6, 89–92. Sternlieb, I., 1988. Copper and zinc. In: Arias, I.M., Jakoby, W.B., Popper, H., Schachter, D., Shafritz, D.A. (Eds.), The Liver: Biology and Pathobiology. second ed. Raven Press, New York, pp. 525–533.
Fishes 215 Stewart, C., Thompson, J.A.J., 1994. Extensive butyltin contamination in southwestern British Columbia, Canada. Mar. Pollut. Bull. 28, 601–606. Stickney, R.R., Windom, H.L., White, D.B., Taylor, F.W., 1975. Heavy-metal concentrations in selected Georgia estuarine organisms with comparative food-habit data. In: Howell, F.G., Gentry, J.B., Smith, M.H. (Eds.), Mineral Cycling in South-Eastern Ecosystems. U.S. Ener. Res. Dev. Admin. Avail as CONF-740513 from NTIS, U.S. Dept. Commun., Springfield, VI, pp. 257–267. Storelli, M.M., Giacominelli-Stuffler, R., Storelli, A., Marcotrigiano, G.O., 2005. Accumulation of mercury, cadmium, lead and arsenic in swordfish and bluefin tuna from the Mediterranean Sea: a comparative study. Mar. Pollut. Bull. 50, 1004–1007. Storelli, M.M., Barone, G., Storelli, A., Marcotrigiano, G.O., 2006. Trace metals in tissues of mugilids (Mugil auratus, Mugil capito, and Mugil labrosus) from the Mediterranean Sea. Bull. Environ. Contam. Toxicol. 77, 43–50. Strohal, P., Huljev, D., Lulic, S., Picer, M., 1975. Antimony in the coastal marine environment, North Adriatic. Estuar. Coast. Mar. Sci. 3, 119–123. Sunderland, E.M., 2007. Mercury exposure from domestic and imported estuarine and marine fish in the U.S. seafood market. Environ. Health Perspect. 115, 235–242. Sures, B., Taraschewski, H., Jackwerth, E., 1994. Lead content of Paratenuisentis ambiguus (Acanthocephala), Anguillicola crassus (Nematodes) and their host Anguilla anguilla. Dis. Aquat. Org. 19, 105–107. Sures, B., Zimmermann, S., Messerschmidt, J., Van Bohlen, A., Alt, F., 2001. First report of automobile catalyst emitted palladium by European eels (Anguilla anguilla) following experimental exposure to road dust. Environ. Pollut. 113, 341–345. Suzuki, T., Miyama, T., Toyama, C., 1973. The chemical form and bodily distribution of mercury in marine fish. Bull. Environ. Contam. Toxicol. 10, 347–355. Svansson, A., 1975. Physical and chemical oceanography of the Skagerrak and the Kattegat. I. Open sea conditions. Fish. Bd. Sweden, Inst. Mar. Res. Goteborg, Rept. 1, pp. 1–88. Szefer, P., Pempkowiak, J., Skwarzec, B., Bojanowski, R., Holm, E., 1993. Concentration of selected metals in penguins and other representative fauna of the Antarctica. Sci. Total Environ. 138, 281–288. Takahashi, S., Lee, J.S., Tanabe, S., Kubodera, T., 1998. Contamination and specific accumulation of organochlorine and butyltin compounds in deep-sea organisms collected from Suruga Bay, Japan. Sci. Total Environ. 214, 49–64. Tamura, Y., Maki, T., Yamada, H., Shinamurea, Y., Ochiai, S., Nishigaki, S., et al., 1975. Studies on the behavior of accumulation of trace elements in fishes. III. Accumulation of selenium and mercury in various tissues of tunas. Tokyo Toritsu Eisei Kenkyusho Nempo 26, 200–204. (Translation avail. as Dept. Sec. State Canada, Fish, Mar. Serv. No. 3994, 1977, 11 pp.). Tariq, J., Jafar, M., Ashraf, M., Moazzam, M., 1993. Heavy metal concentrations in fish, shrimp, seaweed, sediment, and water from the Arabian Sea, Pakistan. Mar. Pollut. Bull. 26, 644–647. Taylor, D.D., Bright, T.J., 1973. The distribution of heavy metals in reef-dwelling groupers in the Gulf of Mexico and Bahama Islands. Dept. Ocean, Texas A&M Univ, College Station, Texas, Rept TAMU-SG-73-208, pp. 1–249. Taylor, D., Maddock, B.G., Mance, G., 1985. The acute toxicity of nine ‘grey list’ metals (arsenic, boron, chromium, copper, lead, nickel, tin, vanadium and zinc) to two marine fish species: Dab (Limanda limanda) and grey mullet (Chelon labrosus). Aquat. Toxicol. 7, 135–144. Thibaud, Y., 1971. Teneur en mercure dans quelqes poissons de consommation courante. Sci. Peche. Bull. Inst. Peches Marit. 209, 1–10. Thomas, P., Juedes, M.J., 1992. Influence of lead on the glutathione status of Atlantic croaker tissues. Aquat. Toxicol. 23, 11–30. Thompson, J.A.J., Davis, J.C., Drew, R.E., 1976. Toxicity, uptake, and survey studies of boron in the marine environment. Water Res. 10, 869–875. Thompson, J.A.J., Sheffer, M.G., Pierce, R.C., Chau, Y.K., Cooney, J.J., Cullen, W.R., et al., 1985. Organotin compounds in the aquatic environment: Scientific criteria for assessing their effects on environmental quality.
216 Chapter 3 NRCC/CNRC, Ottawa, Canada, p. 284 Natl. Res. Coun. Canada, Publ. NRCC 22494 KIA OR6 Avail. from publications. Thompson, E.D., McDermott, J.A., Zerkel, T.B., Skare, J.A., Evans, B.L.B., Cody, D.B., 1989. Genotoxicity of zinc in 4 short-term mutagenicity assays. Mutat. Res. 223, 267–272. Thrower, F.P., Short, J.W., 1991. Accumulation and persistence of tri-n-butyltin in pink and chum salmon fry cultivated in marine net-pens. Aquaculture 96, 223–239. Tien, H.C., Standkring, W.J.F., Salbu, B., 2006. Mobilization of river transported colloidal aluminium upon mixing with seawater and subsequent deposition in fish gills. Sci. Total Environ. 32, 149–164. Ting, R.Y., 1971. Distribution of Zn, Fe, Mn, and Sr in marine fishes of different feeding habitats. In: Vol. 2 of Radionuclides in Ecosystems, Proceedings of the Third National Symposium on Radioecology, pp. 709–720. Ting, R.Y., Devega, R., 1969. The nature of the distribution of trace elements in longnose anchovy (Anchoa lamprotaenia Hildebrand), Atlantic thread herring (Opisthonema oglinum Lasueur), and alga (Udontea flabellum Lamoroux). In: Proceedings of the 2nd National Symposium on Radioecology, U.S. Atom. Ener. Comm. Conf. 670503, pp. 527–534. Topping, G., 1973. Heavy metals in shellfish from Scottish waters. Aquaculture 1, 379–384. Trudel, M., Rasmussen, J.B., 1997. Modeling the elimination of mercury by fish. Environ. Sci. Technol. 31, 1716–1722. Trudel, M., Rasmussen, J.B., 2006. Bioenergetics and mercury dynamics in fish: a modelling perspective. Can. J. Fish. Aquat. Sci. 63, 1890–1902. Tsuraga, H. 1963. Tissue distribution of mercury orally given to fish. Bull. Japan. Soc. Sci. Fish. 29(5), 403–406 (In Japanese, English summary). Tugrul, S., Balkas, T.I., Goldberg, E.D. 1983. Methyltins in the marine environment. Mar. Pollut. Bull. 14, 297–303. Tuncel, G., Ramelow, G., Balkas, T.I., 1980. Mercury in water, organisms and sediments from a section of the Mediterranean coast. Mar. Pollut. Bull. 11, 18–22. Turkmen, A., Turkmen, M., Tepe, Y., Mazlum, Y., Oymael, S., 2006. Metal concentrations in blue crab (Callinectes sapidus) and mullet (Mugil cephalus) in Iskenderun Bay, northern east Mediterranean, Turkey. Bull. Environ. Contam. Toxicol. 77, 186–193. Turkmen, A., Tepe, Y., Turkmen, M., 2008. Metal levels in tissues of European anchovy, Engraulis encrasicolus L., 1758, and picarel, Spicara smaris L., 1758, from Black, Marmara and Aegean Seas. Bull. Environ. Contam. Toxicol. 80, 521–525. Tzeng, W.N., Shiao, J.C., Tizuka, Y., 2002. Use of otolith Sr:Ca ratios to study the riverine migratory behaviors of Japanese eel Anguilla japonica. Mar. Ecol. Prog. Ser. 245, 213–221. Ueda, T., Takeda, M., 1977. On mercury and selenium contained in tuna fish tissues—IV. Methyl mercury levels in muscles and liver of yellowfin tuna. Bull. Jpn. Soc. Sci. Fish. 43, 1115–1123. Ui, J., 1972. A few coastal pollution problems in Japan. In: The Changing Chemistry of the Oceans. Proceedings of the 20th Nobel Symposium. Stockholm. Wiley, New York, pp. 171–177. Ui, J., Kitamuri, S., 1971. Mercury in the Adriatic. Mar. Pollut. Bull. 2, 56–58. U.S. Environmental Protection Agency (USEPA), 1980a. Ambient Water Quality Criteria for Selenium. USEPA Rep. 440/5-80-070, pp. 1–123. U.S. Environmental Protection Agency (USEPA), 1980b. Ambient Water Quality Criteria for Chromium. USEPA Rep. 440/5-80-035, pp. 1–105. U.S. Environmental Protection Agency (USEPA), 1980c. Ambient Water Quality Criteria for Copper. USEPA Rep. 440/5-80-036, pp. 1–162. U.S. Environmental Protection Agency (USEPA), 1980d. Ambient Water Quality Criteria for Nickel. USEPA Rep. 440/5-80-060, pp. 1–206. U.S. Environmental Protection Agency (USEPA), 1980e. Ambient Water Quality Criteria for Silver. USEPA Rep.440/5-80-071, pp. 1–212. U.S. Environmental Protection Agency (USEPA), 1980f. Ambient Water Quality Criteria for Zinc. USEPA Rep. 440/5-80-079, pp. 1–158.
Fishes 217 U.S. Environmental Protection Agency (USEPA), 1980g. Ambient Water Quality Criteria for Mercury. USEPA Rep. 440/5-80-058. Avail. from, NTIS, Springfield, VA. U.S. Environmental Protection Agency (USEPA), 1985a. Ambient Water Quality Criteria for Lead-1984. USEPA Rep. 440/5-84-027, pp. 1–81. U.S. Environmental Protection Agency (USEPA), 1985b. Ambient Water Quality Criteria for Arsenic-1984. USEPA Rep. 440/5-84-033, pp. 1–66. U.S. Environmental Protection Agency (USEPA), 1986. Initiation of a special review of certain pesticide products containing tributyltins used as antifoulants; availability of support document. Fed. Regist. 51(5), 778–779. U.S. Environmental Protection Agency (USEPA), 1987a. Ambient Water Quality Criteria for Zinc-1987. USEPA Rep. 440/5-87-002, pp. 1–207. U.S. Environmental Protection Agency (USEPA), 1987b. Ambient Water Quality Criteria for Selenium-1987. USEPA Rep. 440/5-87-006, pp. 1–121. U.S. Environmental Protection Agency (USEPA), 1995. QA/QC Guidance for Sampling and Analysis of Sediments, Water, and Tissues for Dredged Material Evaluations—Chemical Evaluations. EPA/823/B/95/001. USEPA, Washington, DC. U.S. National Academy of Sciences (USNAS), 1979. Zinc. USNAS, Natl. Res. Coun. Subcomm. Zinc. Univ. Park Press, Baltimore, MD, p. 471. U.S. Public Health Service (USPHS), 1993a. Toxicological profile for lead. Update. Agen. Toxic Subst. Dis. Regist., Tp-92/12, pp. 1–318. U.S. Public Health Service (USPHS), 1993b. Toxicological profile for chromium. Agen. Toxic Subst. Dis. Regist., TP-92/08, pp. 1–238. Van As, D., Fourie, H.O., Vleggaar, C.M., 1973. Accumulation of certain trace elements in the marine organisms from the sea around the Cape of Good Hope. In: Radioactive Contamination of the Marine Environment. IAEA, Vienna, pp. 615–624. Van As, D., Fourie, H.O., Vleggaar, C.M., 1975. Trace element concentrations in marine organisms from the Cape West Coast. South Afr. J. Sci. 71, 151–154. Vandal, G.M., Fitzgerald, W.F., Boutron, C.F., Candelone, J.P., 1993. Variations of mercury deposition to Antarctica over the past 34,000 years. Nature 362, 621–623. Vanderploeg, H.A., 1979. Dynamics of zinc-65 specific activity and total zinc in benthic fishes on the outer continental shelf off central Oregon. Mar. Biol. 52, 259–272. Vanderstappen, R., DeClerck, R., Vyncke, W., Moermans, R., 1978. Les teneurs en mercure, zinc, cuivre, plomb et cadmium dans le hareng. Rev. de l’Agric. 2 (31), 331–336. van de Ven, W.S.M., 1978. Mercury and selenium in cod-liver oil. Clin. Toxicol. 12, 579–581. Veltman, K., Huijbregts, M.A.J., van den Heuvel-Greve, M.J., Vethaak, A.D., Hendriks, A.J., 2006. Organotin accumulation in an estuarine food chain: Comparing field measurements with model estimations. Mar. Environ. Res. 61, 511–530. Vink, G.J., 1972. Koper in vis (copper in fish). TNO Nieuws 27, 493–496. Voegborlo, R.B., Baah, D.A., Kwaansa-Ansah, E.E., Adimado, A.A., Ephraim, J.H., 2004. Mercury concentrations in fish species from the Gulf of Guinea, Ghana. Bull. Environ. Contam. Toxicol. 73, 1057–1064. Voegborlo, R.B., Matsuyama, A., Akagi, H., Adimado, A.A., Ephraim, J.H., 2006. Total mercury and methylmercury accumulation in the muscle tissue of frigate (Auxis thazard thazard) and yellow fin (Thunnus albacares) tuna from the Gulf of Guinea, Ghana. Bull. Environ. Contam. Toxicol. 76, 840–847. Voegborlo, R.B., Adimado, A.A., Ephraim, J.H., 2007. Total mercury distribution in different tissues of frigate tuna (Auxis thazard thazard) from the Atlantic coastal waters of Ghana, Gulf of Guinea. Environ. Monit. Assess. 132, 503–508. Voigt, H.R., 2004. Concentrations of mercury (Hg) and cadmium (Cd), and the condition of some Baltic fishes. Environ. Fenn. 21, 1–22. Vorob’yev, V.I., Zaystev, V.F., 1975. Dynamics of some trace elements in organs and tissues of the rudd. Hydrobiol. J. 11 (2), 57–60.
218 Chapter 3 Vos, G., Hovens, J.P.C., 1986. Chromium, nickel, copper, zinc, arsenic, selenium, cadmium, mercury and lead in Dutch fishery products 1977–1984. Sci. Total Environ. 52, 25–40. Voyer, R.A., Wentworth Jr., C.E., Barry, E.P., Hennekey, R.J., 1977. Viability of embryos of the winter flounder, Pseudopleuronectes americanus exposed to combinations of cadmium and salinity at selected temperatures. Mar. Biol. 44, 117–124. Walsh, G.E., McLaughlin, L.L., Lores, E.M., Louie, M.K., Deans, C.H., 1985. Effects of organotins on growth and survival of two marine diatoms, Skeletonema costatum and Thalassiosira pseudonana. Chemosphere 14, 383–392. Walsh, A.R., O’Halloran, J., Gower, A.M., 1994. Some effects of elevated levels of chromium (III) in sediments to the mullet Chelon labrosus (L.). Ecotoxicol. Environ. Saf. 27, 168–176. Walther, B.D., Thorrold, S.R., 2006. Water, not food, contributes the majority of strontium and barium deposited in the otoliths of a marine fish. Mar. Ecol. Prog. Ser. 311, 125–136. Ward, G.S., Cramm, G.C., Parrish, P.R., Trachman, H., Slesinger, A., 1981a. Bioaccumulation and chronic toxicity of bis(tributyltin)oxide (TBTO): tests with a salt water fish. In: Branson, D.R., Dickson, K.L. (Eds.), Aquatic Toxicology and Hazard Assessment: Fourth Conference. ASTM Spec. Tech. Publ. 737. American Society for Testing and Materials, Philadelphia, PA, pp. 183–200. Ward, G.S., Hollister, T.A., Heitmuller, P.T., Parrish, P.R., 1981b. Acute and chronic toxicity of selenium to estuarine organisms. Northeast Gulf Sci. 4, 73–78. Ward, T.J., Correll, R.L., Anderson, R.B., 1986. Distribution of cadmium, lead and zinc amongst the marine sediments, sea grasses and fauna, and the selection of sentinel accumulators, near a lead smelter in South Australia. Aust. J. Mar. Freshw. Res. 37, 567–585. Ward, T.J., Boeri, R.L., Hogstrand, C., Kramer, J.R., Lussier, S.M., Stubblefield, W.A., et al., 2006. Influence of salinity and organic carbon on the chronic toxicity of silver to mysids (Americamysis bahia) and silversides (Menidia beryllina). Environ. Toxicol. Chem. 25, 1809–1816. Watanabe, I., Tanabe, S., Amano, M., Miyazaki, N., Petrov, E.A., Tatsukawa, R., 1998. Age-dependent accumulation of heavy metals in Baikal seal (Phoca sibirica) from the Lake Baikal. Arch. Environ. Contam. Toxicol. 35, 518–526. Webb, M.A.H., Feist, G.W., Fitzpatrick, M.S., Foster, E.P., Schreck, C.B., Plumlee, M., et al., 2006. Mercury concentrations in gonad, liver, and muscle of white sturgeon Acipenser transmontanus in the Lower Columbia River. Arch. Environ. Contam. Toxicol. 50, 443–451. Weimer, W.C., Langford, J.C., Jenkins, C.E., 1978. Comparative biogeochemical behaviors of iron-55 and stable iron in the marine environment. Battelle Mem. Inst., Richland, Washington Rept PNL-2880, pp. 1–28. Weinreich, O., Koch, V., Knippel, J., 1994. Futtermittelrechtliche Vorshriften. Buchedition Agrimedia, Hamburg, Germany. Weis, P., 1984. Metallothionein and mercury tolerance in the killifish, Fundulus heteroclitus. Mar. Environ. Res. 14, 153–166. Weis, P., Weis, J.S., 1978. Methylmercury inhibition of fin regeneration in fishes and its interaction with salinity and cadmium. Estuar. Coast. Mar. Sci. 6, 327–334. Weis, J.S., Weis, P., 1995a. Effects of embryonic exposure to methylmercury on larval prey-capture ability in the mummichog, Fundulus heteroclitus. Environ. Toxicol. Chem. 14, 153–156. Weis, J.S., Weis, P., 1995b. Swimming performance and predator avoidance by mummichog (Fundulus heteroclitus) larvae after embryonic or larval exposure to methylmercury. Can. J. Fish. Aquat. Sci. 52, 2168–2173. Weisbart, M., 1973. The distribution and tissue retention of mercury-203 in the goldfish (Carassius auratus). Can. J. Zool. 51, 143–150. Westernhagen, H.V., Dethlefsen, V., 1975. Combined effects of cadmium and salinity on development and survival of flounder eggs. J. Mar. Biol. Assoc. UK 55, 945–957. Westernhagen, H.V., Rosenthal, H., Sperling, K.R., 1974. Combined effects of cadmium and salinity on development and survival of herring eggs. Helg. Wiss. Meeres. 26, 416–433. Westernhagen, H.V., Dethlefsen, V., Rosenthal, H., 1975. Combined effects of cadmium and salinity on development and survival of garpike eggs. Helg. Wiss. Meeres. 27, 268–282.
Fishes 219 Westernhagen, H.V., Dethlefsen, V., Rosenthal, H., Furstenberg, G., Klinckmann, J., 1978. Fate and effects of cadmium in an experimental marine ecosystem. Helg. Wiss. Meeres. 31, 471–484. Westernhagen, H.V., Dethlefsen, V., Rosenthal, H., 1980. Correlation between cadmium concentration in the water and tissue residue levels in dab, Limanda limanda L., and plaice, Pleuronectes platessa L. J. Mar. Biol. Assoc. UK 60, 45048. Westoo, G., 1966. Determination of methylmercury compounds in foodstuffs. I. Methylmercury compounds in fish, identification, and determination. Acta Chem. Scand. 20, 2131–2137. Westoo, G., 1969. Methylmercury compounds in animal foods. In: Miller, M.W., Berg, G.G. (Eds.), Chemical Fallout-Current Research on Persistent Pesticides. Charles C Thomas, Springfield, IL, pp. 75–90. Westoo, G., 1973. Methylmercury as percentage of total mercury in flesh and viscera of salmon and sea trout of various ages. Science 181, 567–568. Wharfe, J.R., Van Den Broek, W.L.F., 1977. Heavy metals in macroinvertebrates and fish from the Lower Medway Estuary, Kent. Mar. Pollut. Bull. 8, 31–34. Williams, R.J., Mackay, N.J., Collett, L.C., Kacprzak, J.L., 1976. Total mercury concentration in some fish and shellfish from NSW estuaries. Food Technol. Aust. 28, 8–10. Windom, H., Stickney, R., Smith, R., White, D., Taylor, F., 1973. Arsenic, cadmium, copper, mercury and zinc in some species of North Atlantic finfish. J. Fish. Res. Bd. Can. 30, 275–279. Wobeser, G., Nielsen, N.O., Dunlop, R.H., Atton, F.M., 1970. Mercury concentrations in tissues of fish form the Saskatchewan River. J. Fish. Res. Bd. Can. 27, 830–834. Wolfe, D.A., Cross, F.A., Jennings, C.D., 1973. The flux of Mn, Fe, and Zn in an estuarine ecosystem. In: Radioactive Contamination of the Marine Environment. IAEC, Vienna, pp. 159–175. Won, J.H., 1973. The concentration of mercury, cadmium, lead, and copper in fish and shellfish of Korea. Bull. Korean Fish. Soc. 6, 1–19. Wood, C.M., Playle, R.C., Hogstrand, C., 1999. Physiology and modeling of mechanisms of silver uptake and toxicity in fish. Environ. Toxicol. Chem. 18, 71–83. World Health Organization (WHO), 1991. Nickel. Environ. Health Crit. 108, 1–383. Wright, D.A., 1976. Heavy metals in animals from the north east coast. Mar. Pollut. Bull. 7, 36–38. Yamada, H., Tateishi, M., Takayanagi, K., 1994. Bioaccumulation of organotin compounds in the red sea bream (Pagrus major) by two uptake pathways: dietary uptake and direct uptake from water. Environ. Toxicol. Chem. 13, 1415–1422. Yamaguchi, M., Yasutake, A., Nagano, M., Yasuda, Y., 2004. Accumulation and distribution of methylmercury in freshwater- and seawater-adapted eels. Bull. Environ. Contam. Toxicol. 73, 257–263. Yannai, S., Sachs, K., 1978. Mercury compounds in some eastern Mediterranean fishes, invertebrates, and their habitats. Environ. Res. 16, 408–418. Yoshida, K., Minamisako, Y., Hirai, M., Katagiri, H., Yamada, N., 1994. Annual Reports of Environmental Radioactivity for 1992. Ministry of Agriculture, Forestry, and Fisheries, Tokyo, pp. 4.11–4.13. Young, D.R., 1974. Cadmium and mercury in the southern California Bight. Summary of findings, 1971–1973. Southern Calif. Coastal Water Res. Proj. (SCCWRP), 16 pp. Zaba, B.N., Harris, E.J., 1978. Accumulation and effects of trace metal ions in fish liver mitochondria. Comp. Biochem. Physiol. 61C, 89–93. Zhang, L., Wang, W.X., 2006. Alteration of dissolved cadmium and zinc uptake kinetics by metal pre-exposure in the black sea bream (Acanthopagrus schlegeli). Environ. Toxicol. Chem. 25, 1312–1321. Zhang, L., Wang, W.X., 2007a. Waterborne cadmium and zinc uptake in a euryhaline teleost Acanthopagrus schlegeli acclimated to different salinities. Aquat. Toxicol. 84, 173–181. Zhang, L., Wang, W.X., 2007b. Gastrointestinal uptake of cadmium and zinc by a marine teleost Acanthopagrus schlegeli. Aquat. Toxicol. 85, 143–153. Zhang, J., Zuo, Z., Chen, Y., Zhao, Y., Hu, S., Wang, C., 2007. Effect of tributyltin on the development of ovary in female Cuvier (Sebastiscus marmoratus). Aquat. Toxicol. 83, 174–179. Zingde, M.D., Singbal, S.Y.S., Moraes, C.F., Reddy, C.V.G., 1976. Arsenic, copper, zinc, and manganese in marine flora and fauna of coastal and estuarine waters around Goa. Indian J. Mar. Sci. 5, 212–217.
220 Chapter 3 Zitko, V., Finlayson, B.J., Wildish, D.J., Anderson, J.M., Kohler, A.C., 1971. Methylmercury in freshwater and marine fishes in New Brunswick, in the Bay of Fundy, and on the Nova Scotia Banks. J. Fish. Res. Bd. Can. 28, 1285–1291. Zumholz, K., Hansteen, T.H., Klugel, A., Piatkowski, U., 2006. Food effects on statolith composition of the common cuttlefish (Sepia officinalis). Mar. Biol. 150, 237–244.
CHAPTER 4
Reptiles Turtles, crocodiles, iguanas, and sea snakes are the most common reptiles encountered in marine waters. No kills of reptile field populations due to metal intoxication has ever been reported (Linder and Grillitsch, 2000). Except for tissue-metal levels in free-ranging reptiles, studies on the ecotoxicology of metals are rare. In addition to analytical deficiencies, information is lacking on the age, size, weight, and sexual condition of samples, all of which are important in assessing the significance of metals in long-lived species of reptiles (Linder and Grillitsch, 2000). And no studies are available that directly address metal toxicokinetics in marine reptiles impacted by changing abiotic variables such as water temperature, salinity, or pH (Linder and Grillitsch, 2000). In general, aluminum, chromium, and copper burdens are consistently higher in eggshells of marine reptiles when compared to egg contents; however, cadmium, iron, mercury, manganese, and zinc are higher in egg contents (Linder and Grillitsch, 2000). The presence of several metals (cadmium, copper, iron, mercury, manganese, zinc) in oviductal eggs of the loggerhead turtle, Caretta caretta clearly indicate maternal transfer of these metals to the eggs (Sakai et al., 1995), and also suggests that egg deposition is a significant elimination route of metals in marine turtles (Linder and Grillitsch, 2000; Stoneburner et al., 1980). A comparison of metal concentrations among eggs, fresh hatchlings, and sand samples from nests of olive Ridley turtles, Lepidochelys olivacea, shows that concentrations of the nine metals analyzed were higher in hatchlings than freshly deposited eggs by factors ranging from 2 for cadmium to 6 for lead (Sahoo et al., 1996). All metals were detected in sand samples at concentrations equal to or higher than concentrations found in eggs or hatchlings (Sahoo et al., 1996). Eggshells of the American crocodile, Crocodylus acutus, had higher concentrations of aluminum, cadmium, chromium, copper, molybdenum, nickel, lead, and strontium than did the albumen-yolk mass; cobalt was equally distributed between the two compartments but mercury was higher in albumen-yolk (Stoneburner and Kushlan, 1984). The disease known as green turtle fibropapillomatosis or GTFP is considered a threat to the survival of the green turtle, Chelonia mydas (Herbst and Klein, 1995). Anthropogenic contaminants, including metals, were suggested as a possible cause of GTFP (Herbst, 1994). However, results of analyses of trace metals (beryllium, lead, mercury, barium, cadmium, copper, iron, manganese, selenium, zinc) in tissues of green turtles afflicted with GTFP were
221
222 Chapter 4 inconclusive (Aguirre et al., 1994). In the absence of credible baseline data for metals in marine reptiles, authors concluded that metal levels were at or below concentrations considered normal for other animal groups, and that metals played a negligible role in the etiology of GTFP in the green turtles analyzed (Aguirre et al., 1994).
4.1 Aluminum There is considerable variability in aluminum content among marine reptiles. For example, loggerhead turtles, C. caretta, had maximum tissue concentrations, in mg Al/kg FW, of 7.6 in kidney, 8.4 in muscle, 31.1 in liver, and 234.1 in bone (Table 4.1). At the other extreme, aluminum concentrations in shell, yolk, and albumen of green turtle, C. mydas, eggs collected in Hong Kong during summer 2001 were all below the detection limit of 0.15 mg Al/kg FW (Lam et al., 2006). Muscle of estuarine crocodiles contained up to 132.0 mg Al/kg DW; however, osteoderms had less than 0.05 mg Al/kg DW (Table 4.2; Jeffree et al., 2001). Table 4.1: Aluminum, Arsenic, and Barium Concentrations in Field Collections of Reptiles Element and Organism
Concentration
Reference
a
Aluminum Loggerhead turtle, Caretta caretta; found stranded; Canary Islands, Spain; 1998-2001; juveniles and subadults Bone Liver Muscle Kidney
30.5 (0.03-234.1) FW 2.2 (0.12-31.1) FW 1.5 (0.06-8.3) FW 0.72 (0.03-7.6) FW
8 8 8 8
Green turtle, Chelonia mydas; eggs
<0.15 FW
5
Estuarine crocodile, Crocodylus porosus; northern Australia; 1993-1997 Muscle Osteoderms
89.9 (26.0-132.0) DW <0.05 DW
7 7
0.9 (<0.6-6.4) FW <0.6-6.8 FW
1 1
Arsenic Loggerhead turtle, Caretta caretta Hawaii Liver Kidney
(Continues)
Reptiles Table 4.1: Element and Organism Egg Shell Whole Canary Islands, Spain; found stranded; 1998-2001; juveniles and subadults Bone Liver Muscle Kidney Adriatic Sea Liver Kidney Muscle Italy; South Adriatic Sea; beached; 1998 Liver Total Organic Inorganic Muscle Total Organic Inorganic Green turtle, Chelonia mydas Hong Kong, 2001; eggs Yolk Albumen Shell Okinawa, Japan; 2000-2005; total arsenic Muscle Kidney Liver Yaeyama Islands; Japan Muscle Kidney Liver
223
Cont’d
Concentration
Reference
<0.6 FW <0.6 FW
1 1
12.5 (9.9-150.4) FW 17.1 (0.01-131.9) FW 7.4 (1.6-67.2) FW 13.8 (1.1-122.1) FW
8 8 8 8
21.7 FW 24.9 FW 68.9 FW
9 9 9
6.7 (2.7-13.1) FW 6.3 (2.2-12.7) FW 0.6 (0.3-1.2) FW
10 10 10
15.4 (2.6-32.4) FW 15.2 (2.4-31.1) FW 0.18 (0.08-0.32) FW
10 10 10
2.5 (1.4-5.0) FW 0.17 FW 0.22 FW
a
5 5 5
16.6 (11.2-165.0) DW 16.5 (4.4-44.3) DW 5.3 (0.9-9.7) DW
12 12 12
24.1 (2.6-74.9) DW 5.7 (0.2-10.0) DW 1.8 (0.4-5.3) DW
13 13 13 (Continues)
224 Chapter 4 Table 4.1: Element and Organism American crocodile, Crocodylus acutus Egg, Florida Bay, Florida Egg, whole Caudal scute; Costa Rica; 2003 Leatherback turtle, Dermochelys coriacea; United Kingdom coastal waters; found stranded Liver Muscle Blubber Ishigaki Island, Japan; adults; November 2000 and January 2005 Green turtle, Chelonia mydas Total arsenic Intestine Kidney Liver Lung Muscle Spleen Stomach Arsenobetaine Intestine Kidney Liver Lung Muscle Spleen Stomach Trimethylarsine oxide; all tissues Arsenocholine Intestine Kidney Liver Lung Muscle
Cont’d
Concentration
Reference
0.07 (0.06-0.08) FW 0.2 FW Not detectable
3 4 6
0.58 DW 0.21 DW 1.28 DW
2 2 2
6.1 DW 17.0 DW 4.9 DW 7.9 DW 69.0 DW 7.6 DW 6.1 DW
11 11 11 11 11 11 11
5.2 DW 11.7 DW 2.1 DW 6.7 DW 58.4 DW 7.0 DW 2.4 DW <0.3 DW
11 11 11 11 11 11 11 11
0.14 DW 0.4 DW 0.08 DW <0.04 DW <0.04 DW
11 11 11 11 11
a
(Continues)
Reptiles Table 4.1: Element and Organism Spleen Stomach Tetramethylarsonium ion Intestine Kidney Liver Lung Muscle Spleen Stomach Dimethylarsinic acid Intestine Kidney Liver Lung Muscle Spleen Stomach Monomethylarsonic acid; all tissues As5+; all tissues As3+ Intestine Kidney Liver Lung Muscle Spleen Stomach Hawksbill turtle, Eretmochelys imbricata Arsenobetaine Eyeball Heart Kidney Liver Lung Muscle Spleen Stomach Arsenocholine Eyeball Heart
Concentration
225
Cont’d Reference
<0.04 DW 0.15 DW
11
0.18 DW <0.03 DW 0.09 DW 0.3 DW 0.3 DW 0.4 DW >0.03 DW
11 11 11 11 11 11 11
0.41 DW 0.06 DW 0.2 DW 0.3 DW 0.1 DW <0.01 DW <0.01 DW <0.03 DW
11 11 11 11 11 11 11 11
<0.02 DW
11
0.14 DW 0.18 DW 0.08 DW 0.07 DW 0.02 DW 0.03 DW 0.21 DW
11 11 11 11 11 11 11
12.3 DW 9.4 DW 29.1 DW 13.2 DW 18.0 DW 139.0 DW 7.7 DW 8.9 DW
11 11 11 11 11 11 11 11
<0.04 DW <0.04 DW
11 11
a
(Continues)
226 Chapter 4 Table 4.1: Element and Organism Kidney Liver Lung Muscle Spleen Stomach Tetramethylarsonium ion Liver Other tissues Trimethylarsine oxide Eyeball Heart Kidney Liver Lung Muscle Spleen Stomach Dimethylarsinic acid Eyeball Heart Kidney Liver Lung Muscle Spleen Stomach Monomethylarsonic acid; all tissues As3+ Eyeball Heart Kidney Liver Lung Muscle Spleen Stomach As5+; all tissues Total arsenic Eyeball
Concentration
Cont’d Reference
1.3 DW 0.4 DW <0.04 DW <0.04 DW <0.04 DW 0.09 DW
11 11 11 11 11 11
0.14 DW <0.03 DW
11 11
9.8 DW 2.6 DW 0.8 DW 1.3 DW 6.9 DW 2.6 DW 6.6 DW 1.2 DW
11 11 11 11 11 11 11 11
0.5 DW 0.6 DW 0.8 DW 0.2 DW 0.5 DW 0.2 DW 0.4 DW 0.7 DW <0.03 DW
11 11 11 11 11 11 11 11 11
0.12 DW 0.15 DW 0.16 DW 0.08 DW 0.14 DW 0.07 DW 2.8 DW 0.3 DW <0.02 DW
11 11 11 11 11 11 11 11 11
48.0 DW
11
a
(Continues)
Reptiles Table 4.1: Element and Organism Heart Kidney Liver Lung Muscle Spleen Stomach
227
Cont’d
Concentration 28.0 DW 45.0 DW 25.0 DW 33.0 DW 210.0 DW 24.0 DW 22.0 DW
Reference
a
11 11 11 11 11 11 11
Barium Green turtle, Chelonia mydas; eggs; Hong Kong; summer 2001 Yolk Albumen Eggshell
8.7 (4.0-21.0) FW 0.5 (0.08-1.6) FW 3.5 (1.4-8.2) FW
5 5 5
Estuarine crocodile, Crocodylus porosus; northern Australia; 1993-1997 Muscle Osteoderms
0.55 (0.27-0.92) DW 24.3 (1.0-143.0) DW
7 7
Values are in mg As/kg fresh weight (FW) or dry weight (DW). a 1, Aguirre et al., 1994; 2, Davenport and Wrench, 1990; 3, Ogden et al., 1974; 4, Hall, 1980; 5, Lam et al., 2006; 6, Rainwater et al., 2007; 7, Jeffree et al., 2001; 8, Torrent et al., 2004; 9, Storelli et al., 1998b; 10, Storelli and Marcotrigiano, 2000; 11, Agusa et al., 2008b; 12, Agusa et al., 2008a; 13, Saeki et al., 2000.
4.2 Antimony Antimony concentrations in eggs of the green turtle, C. mydas, collected in Hong Kong in 2001 were—in mg Sb/kg FW—0.003 in yolk, 0.0005 in albumen, and 0.0027 in eggshell (Lam et al., 2006).
4.3 Arsenic Unusually high arsenic concentrations, that is, >10.0 mg As/kg FW, were measured in some marine turtle samples (Table 4.2), whereas tissue arsenic levels found in nonmarine reptiles were significantly lower or within the range reported normal for terrestrial birds and mammals (Linder and Grillitsch, 2000). In loggerhead turtles, C. caretta, found stranded along the Italian south Adriatic Sea coast in 1998, total arsenic in muscle and inorganic arsenic in liver both increased with increasing turtle weight (Storelli and Marcotrigiano, 2000).
228 Chapter 4 For reasons that are not clear, tissues of both green (C. mydas) and hawksbill (Eretmochelys imbricata) turtles contain high concentrations of arsenic and unique patterns of accumulation relative to higher marine vertebrates (Table 4.2; Agusa et al., 2008b). Total arsenic concentration in tissues of green turtles from Okinawa, Japan in 2000-2005 ranged from 0.9 to 165.0 mg As/kg DW (Table 4.2; Agusa et al., 2008a). Arsenobetaine was the major arsenic compound in all green turtle tissues, comprising more than 97% of the total arsenic in muscle; other arsenic compounds detected were dimethylarsinic acid, trimethylarsine oxide, and arsenite. Larger green turtles had lower arsenic burdens in tissues and this may be related to changing diet at different growth stages (Agusa et al., 2008a). Additional research seems merited on the significance of arsenic speciation in marine reptiles.
4.4 Barium Barium was detected at or near detection limits in all samples analyzed of the Atlantic green turtle, C. mydas (Aguirre et al., 1994). However, green turtle eggs collected in Hong Kong in summer 2001 had up to 21.0 mg Ba/kg FW yolk, 1.6 mg Ba/kg FW albumen, and up to 8.2 mg Ba/kg FW eggshell (Table 4.2). Barium concentration in crocodile muscle was higher in older animals (Jeffree et al., 2001).
4.5 Beryllium Beryllium concentrations in green turtle tissues were always below detection limits (Aguirre et al., 1994).
4.6 Cadmium The highest concentrations of cadmium reported were in kidney tissues of loggerhead turtles from Japan (up to 56.5 mg Cd/kg FW) and kidney tissues of green turtles from Baja California (up to 653.0 mg Cd/kg DW) and Hawaii (up to 70.2 mg Cd/kg FW; Table 4.2); cadmium concentrations in all other tissues analyzed were significantly lower (Table 4.2). In general, exceptionally high kidney cadmium concentrations are reported in green turtles from around the world, including China (Lam et al., 2004), Japan (Sakai et al., 2000b), Europe (Caurant et al., 1999), Australia (Gordon et al., 1998), the Arabian Sea (Bicho et al., 2006), and Magdalena Bay on the Pacific coast of the Baja California peninsula (Gardner et al., 2006).
Reptiles
229
Table 4.2: Cadmium Concentrations in Field Collections of Reptiles Organism Loggerhead turtle, Caretta caretta U.S. Atlantic Ocean coast nesting beaches; egg Yolk Albumen France Liver Kidney Muscle Hawaii; liver Italy; Adriatic Sea Liver Muscle Adriatic Sea Liver Kidney Muscle Japan, Kochi Prefecture Liver Kidney Muscle Egg Shell Yolk Albumen Whole Canary Islands, Spain; 1998-2001; found stranded; juveniles and subadults Bone Liver Muscle Kidney Green turtle, Chelonia mydas Hawaii Liver Kidney Egg Shell Whole
Concentration
0.03-0.19 FW 0.56 FW
Reference
1 2
2.6 FW 13.3 FW 0.08 FW 0.96 FW
12 12 12 3
2.8 FW 0.4 FW
11 11
7.6 FW 24.2 FW 0.6 FW
16 16 16
9.3 (5.7-14.6) FW 39.4 (8.1-56.5) FW 0.06 (0.04-0.12) FW
4 4 4
<0.01 FW 0.026 (0.02-0.035) FW <0.01 FW 0.013 (0.008-0.015) FW
4 4 4 4
1.4 2.5 1.1 5.9
a
(0.1-22.8) FW (0.04-22.0) FW (0.1-12.5) FW (0.01-61.1) FW
15 15 15 15
9.3 (0.4-26.0) FW 26.0 (4.7-70.2) FW
3 3
0.2 FW <0.07 FW
3 3 (Continues)
230 Chapter 4 Table 4.2: Organism
Cont’d
Concentration
Reference
Hong Kong; summer 2001 Yolk Albumen Eggshell Baja California; 2002-2003; drowned in commercial fishing nets Kidney Liver Okinawa, Japan Liver Kidney Muscle
110.0 (65.1-653.0) DW 16.9 DW; max. 72.6 DW
14 14
5.6 FW 38.5 FW 0.05 FW
17 17 17
American crocodile, Crocodylus acutus Egg Caudal scute
0.05 FW 0.34 FW
5 13
Not detectable Not detectable 0.016 FW
a
9 9 9
Leatherback turtle, Dermochelys coriacea United Kingdom coastal waters; found stranded Liver Muscle Blubber Mexico; Pacific Ocean coast; eggshell French Guiana; 2006; females Blood Eggs
0.22 DW 0.06 DW <0.01 DW 0.9 DW
6 6 6 7
0.08 FW 0.02 FW
5 5
Olive Ridley turtle; Lepidochelys olivacea India; egg Shell Albumen-yolk Whole
1.3 DW <1.0 DW 2.0 DW
8 8 8 (Continues)
Reptiles Table 4.2: Organism NW coast of Mexico; 2005; found stranded Muscle Liver Kidney Heart
Concentration
2.5 DW; 0.5 FW 13.1 DW; 3.3 FW 15.8 DW; 5.3 FW 11.0 DW
231
Cont’d Reference
a
10 10 10 10
Values are in mg Cd/kg fresh weight (FW) or dry weight (DW). a 1, Hillestad et al., 1974; 2, Stoneburner et al., 1980; 3, Aguirre et al., 1994; 4, Sakai et al., 1995; 5, Guirlet et al., 2008; 6, Davenport and Wrench, 1990; 7, Vazquez et al., 1997; 8, Sahoo et al., 1996; 9, Lam et al., 2006; 10, Frias-Espericueta et al., 2006; 11, Franzelletti et al., 2004; 12, Caurant et al., 1999; 13, Rainwater et al., 2007; 14, Talavera-Saenz et al., 2007; 15, Torrent et al., 2004; 16, Storelli et al., 1998b; 17, Sakai et al., 2000a.
4.7 Cesium Cesium concentrations in eggs of the green turtle collected in Hong Kong during summer 2001 were—in mg Cs/kg FW—0.0007 in yolk, 0.0005 in albumen, and 0.003 in eggshell (Lam et al., 2006).
4.8 Chromium Based on limited data, chromium concentrations seemed highest in egg contents or shells of turtles and crocodiles (Table 4.3).
4.9 Cobalt Cobalt concentrations in green turtle eggs from Hong Kong collected during summer 2001 were (mg/kg FW) 0.03 in yolk, 0.009 in albumen, and 3.3 (0.8-5.8) in shell (Table 4.2). Cobalt concentrations in crocodile osteoderms reached a maximum of 0.48 mg Co/kg DW (Jeffree et al., 2001; Table 4.3).
4.10 Copper Liver was usually the major repository of copper in marine reptiles. Maximum copper concentrations of 23.0-189.0 mg Cu/kg FW were measured in livers of some turtles and crocodiles (Table 4.4).
232 Chapter 4 Table 4.3: Chromium and Cobalt Concentrations in Field Collections of Reptiles Organism
Concentration
Reference
1.04-1.71 FW
1
<0.2 FW
2
0.25-0.5 FW
3
Max. 0.5 FW Max. 0.4 FW
2 2
0.4 FW <0.2 FW
2 2
0.94 (0.37-1.7) FW 0.054 FW
5 5
American crocodile, Crocodylus acutus; Florida Bay; egg Shell Albumen and yolk
20.5 DW 2.6 DW
4 4
Estuarine crocodile, Crocodylus porosus; Australia; 1993-1997 Muscle Osteoderms
0.41 (0.12-1.0) DW 0.22 (0.07-0.39) DW
6 6
Green turtle, Chelonia mydas; eggs Yolk Albumen Eggshell
0.03 FW 0.009 FW 3.3 (0.8-5.8) FW
5 5 5
Estuarine crocodile, Crocodylus porosus; northern Australia; 1993-1997 Muscle Osteoderms
<0.01 DW 0.34 (0.22-0.48) DW
6 6
a
Chromium Loggerhead turtle, Caretta caretta U.S. Atlantic Ocean coast nesting beaches; egg yolk Hawaii; liver Green turtle, Chelonia mydas Papua New Guinea; muscle Hawaii Liver Kidney Egg Shell Whole Hong Kong; summer 2001 Yolk Albumen
Cobalt
Values are in mg Cr/kg fresh weight (FW) or dry weight (DW). a 1, Stoneburner et al., 1980; 2, Aguirre et al., 1994; 3, Yoshinaga et al., 1992; 4, Stoneburner and Kushlan, 1984; 5, Lam et al., 2006; 6, Jeffree et al., 2001.
Reptiles
233
Table 4.4: Copper Concentrations in Field Collections of Reptiles Organism Loggerhead turtle, Caretta caretta U.S. Atlantic Ocean coast nesting areas; eggs Yolk Albumen Yolk Whole France Liver Kidney Muscle Hawaii; liver Italy; Adriatic Sea Liver Muscle Japan, Kochi Prefecture Liver Kidney Muscle Egg Shell Yolk Albumen Whole Blood plasma Canary Islands, Spain; 19982001; found stranded; juveniles and subadults Bone Liver Muscle Kidney Green turtle, Chelonia mydas Papua New Guinea; muscle Hawaii Liver Kidney Eggshell
Concentration
2.1 FW 6.0 FW 5.5-6.6 FW 6.0 FW
Reference
a
1 1 2 3
8.2 FW 2.2 FW 0.73 FW 2.8 FW
17 17 17 4
7.4 FW 1.5 FW
16 16
17.9 (6.5-33.9) FW 1.3 (1.0-1.6) FW 0.8 (0.5-1.3) FW
5 5 5
5.6 (4.3-6.2) FW 1.6 (1.5-1.7) FW 0.13 (0.03-0.24) FW 1.0 (0.8-1.3) FW 0.68 FW
5 5 5 5 6
3.8 (0.1-24.5) FW 15.0 (0.01-66.6) FW 2.9 (0.01-27.3) FW 4.6 (0.1-49.1) FW
20 20 20 20
0.73 FW
7
94.6 (1.3-189.0) FW 3.6 (1.1-10.5) FW 14.3 FW
4 4 4 (Continues)
234 Chapter 4 Table 4.4: Organism Hong Kong; summer 2001 Yolk Albumen Eggshell Okinawa, Japan Liver Kidney Muscle
Cont’d
Concentration
Reference
0.34 (0.17-0.77) FW 0.063 FW 1.3 (0.24-4.2) FW
14 14 14
50.2 FW 2.2 FW 0.4 FW
21 21 21
American crocodile, Crocodylus acutus Egg; Florida Contents Shell Albumen-yolk Whole Caudal scute; Costa Rica
3.7 (0.9-15.0) FW 17.2 DW 5.6 FW 15.0 FW 0.12 FW
8 9 9 3 18
Estuarine crocodile, Crocodylus porosus; northern Australia; 1993-1997 Muscle Osteoderms
1.1 (0.34-2.0) DW 4.7 (2.2-13.1) DW
19 19
Crocodiles, Crocodylus spp. Australia; liver Papua New Guinea; muscle
17.7 (11.0-23.0) DW 0.17 FW
10 7
0.15 DW 0.26 DW 0.06 DW 8.9 DW
12 12 12 13
1.34 FW 0.63 FW
22 22
Leatherback turtle, Dermochelys coriacea United Kingdom coastal waters; found stranded Liver Muscle Blubber Mexico; Pacific Ocean coast; eggshell French Guiana; 2006; females Blood Eggs
a
(Continues)
Reptiles Table 4.4: Organism Olive Ridley turtle, Lepidochelys olivacea Ecuador; humerus NW coast of Mexico; 2005; found stranded Muscle Liver Kidney Heart
Concentration
235
Cont’d Reference
7.2-11.0 AW
11
15.5 DW; 3.1 FW 33.0 DW; 8.8 FW 22.0 DW; 6.4 FW 44.9 DW
15 15 15 15
a
Values are in mg Cu/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Hillestad et al., 1974; 2, Stoneburner et al., 1980; 3, Hall, 1980; 4, Aguirre et al., 1994; 5, Sakai et al., 1995; 6, Musquera et al., 1976; 7, Yoshinaga et al., 1992; 8, Ogden et al., 1974; 9, Stoneburner and Kushlan, 1984; 10, Beck, 1956; 11, Witkowski and Frazier, 1982; 12, Davenport and Wrench, 1990; 13, Vazquez et al., 1997; 14, Lam et al., 2006; 15, Frias-Espericueta et al., 2006; 16, Franzelletti et al., 2004; 17, Caurant et al., 1999; 18, Rainwater et al., 2007; 19, Jeffree et al., 2001; 20, Torrent et al., 2004; 21, Sakai et al., 2000a; 22, Guirlet et al., 2008.
4.11 Iron Iron was found at or near detection limits in all samples analyzed of the green turtle, C. mydas (Aguirre et al., 1994). This differs significantly from the findings of Talavera-Saenz et al. (2007) who measured up to 547.0 mg Fe/kg DW in kidney and up to 671.0 mg Fe/kg DW in liver of green turtles from Baja California in 2002-2003 found drowned in commercial fishing nets (Table 4.5). Also, green turtle eggs collected in Hong Kong during summer 2001 had, in mg Fe/kg FW, 45.0 (29.0-66.0) in yolk, 3.9 (0.46-9.4) in albumen, and 2.3 (0.15-5.7) in eggshell (Lam et al., 2006). Muscle from estuarine crocodiles in northern Australia contained up to 303.0 mg Fe/kg DW; however, osteoderms from this species contained less than 21.2 mg Fe/kg DW (Table 4.5).
4.12 Lead Highest lead concentrations recorded in marine reptiles were 11.6-16.4 mg Pb/kg DW in eggshells, and 19.0-44.0 mg Pb/kg DW in osteoderms of the estuarine crocodile, Crocodylus porosus from Kakadu National Park in northern Australia (Table 4.5). The significance of elevated lead levels in crocodile osteoderms is unknown, but in avian bone, these levels would be indicative of clinical lead poisoning (Twining et al., 1999). The putative source of
236 Chapter 4 Table 4.5: Iron, Lead, and Manganese in Field Collections of Reptiles Element and Organism
Concentration
Reference
a
Iron Loggerhead turtle, Caretta caretta; found stranded; Canary Islands, Spain; 1998-2001; juveniles and subadults Bone Liver Muscle Kidney Green turtle, Chelonia mydas Baja California, Mexico; 2002-2003; found drowned Kidney Liver Okinawa, Japan Liver Kidney Muscle Estuarine crocodile, Crocodylus porosus; northern Australia; 1993-1997 Muscle Osteoderms
9.5 (0.06-189.5) FW 342.7 (0.4-2,180.4) FW 8.6 (0.2-98.4) FW 37.8 (0.3-273.1) FW
17 17 17 17
93.2 DW; max. 547.0 DW 350.0 DW; max. 671.0 DW
14 14
461.0 FW 22.8 FW 5.3 FW
19 19 19
88.7 (13.0-303.0) DW 6.5 (1.3-21.2) DW
15 15
Lead Loggerhead turtle, Caretta caretta U.S. Atlantic Ocean coast nesting beaches; egg Yolk Albumen Yolk Whole Japan; Kochi Prefecture; all samples Canary Islands, Spain; 19982001; found stranded; juveniles and subadults Bone Liver Muscle Kidney
2.9 FW 12.0 FW 1.1-2.2 FW 12.0 FW not detectable
2.4 2.9 2.3 2.4
(0.08-19.9) FW (0.03-33.1) FW (0.2-21.1) FW (0.02-17.3) FW
1 1 2 3 4
17 17 17 17 (Continues)
Reptiles Table 4.5: Element and Organism Adriatic Sea Liver Kidney Muscle Green turtle, Chelonia mydas Papua New Guinea; muscle Hong Kong; summer 2001 Yolk Albumen Eggshell Baja California, Mexico; 2002-2003; found drowned in fishing nets Kidney Liver Okinawa, Japan Liver Kidney Muscle American crocodile, Crocodylus acutus Egg; Florida Bay, Everglades National Park Contents Shell Albumen-yolk Whole Caudal scute; Costa Rica Estuarine crocodile, Crocodylus porosus; northern Australia; 1993-1997 Muscle Osteoderms Osteoderms; Kakadu National Park
237
Cont’d
Concentration
1.2 FW 0.7 FW 0.5 FW 0.03-0.06 FW
Reference
a
18 18 18 5
0.049 (0.025-0.140) FW 0.005 FW 0.110 (0.029-0.280) FW
11 11 11
0.05 DW; max. 1.7 DW Max. 0.07 DW
14 14
<0.03 FW 0.18 FW <0.03 FW
19 19 19
0.34 (0.2-0.5) FW 16.4 DW 3.4 DW 0.5 FW 0.49 FW
6 7 7 3 13
0.31 (0.12-0.45) DW 3.0 (1.2-9.4) DW 19.0-44.0 DW
15 15 16
Leatherback turtle, Dermochelys coriacea (Continues)
238 Chapter 4 Table 4.5: Element and Organism United Kingdom coastal waters; found stranded Liver Muscle Blubber Mexico; Pacific coast; eggshell; 1992-1993 French Guiana; 2006; females Blood Eggs
Cont’d
Concentration
0.12 DW 0.31 DW 0.04 DW 11.6 DW; max. 17.8 DW
Reference
8 8 8 9
0.18 FW 0.04 FW
20 20
39.0-110.0 AW
10
8.9 DW; 1.8 FW 13.3 DW; 3.3 FW 13.4 DW; 4.5 FW 10.1 DW
12 12 12 12
Green turtle, Chelonia mydas; 2002-2003; Baja California, Mexico; found dead Kidney Liver
1.5 DW; max. 7.7 DW 0.2 DW; max. 5.3 DW
14 14
Estuarine crocodile, Crocodylus porosus; Australia; 1993-1997 Muscle Osteoderms
0.71 (0.35-1.3) DW 2.6 (0.19-13.4) DW
15 15
Olive Ridley turtle, Lepidochelys olivacea Ecuador; humerus NW coast of Mexico; summer 2005; found stranded Muscle Liver Kidney Heart
a
Manganese
Values are in mg metal/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Hillestad et al., 1974; 2, Stoneburner et al., 1980; 3, Hall, 1980; 4, Sakai et al., 1995; 5, Yoshinaga et al., 1992; 6, Ogden et al., 1974; 7, Stoneburner and Kushlan, 1984; 8, Davenport and Wrench, 1990; 9, Vazquez et al., 1997; 10, Witkowski and Frazier, 1982; 11, Lam et al., 2006; 12, Frias-Espericueta et al., 2006; 13, Rainwater et al., 2007; 14, Talavera-Saenz et al., 2007; 15, Jeffree et al., 2001; 16, Twining et al., 1999; 17, Torrent et al., 2004; 18, Storelli et al., 1998b; 19, Sakai et al., 2000a; 20, Guirlet et al., 2008.
lead in crocodile osteoderms is from ingestion of wildlife killed or crippled by lead ammunition, including hunter-wounded waterfowl, pigs, and flying foxes. The absorption of ingested lead by the crocodilian digestive system is rapid, owing to an acidic and muscular stomach with a long retentive capacity (Twining et al., 1999).
Reptiles
239
Lead concentrations increased in blood of female leatherback turtles, Dermochelys coriacea, during nesting suggesting lead mobilization from bone associated with calcium requirement for egg formation and eggshell secretion (Guirlet et al., 2008).
4.13 Manganese Manganese was found at or near detection limits in all samples analyzed of Atlantic green turtles, C. mydas, from Hawaii (Aguirre et al., 1994). Manganese concentrations in green turtle eggs collected in Hong Kong during summer 2001 had measurable concentrations, in mg Mn/kg FW, of 0.27 in yolk, 0.047 in albumen, and 0.27 in eggshell (Lam et al., 2006). However, green turtles from Baja California had up to 7.7 mg Mn/kg DW in kidney and 5.3 in liver (Table 4.5). In the loggerhead turtle, C. caretta, manganese was present in oviductal eggs (Sakai et al., 1995). Crocodile osteoderms had 3.6 times more manganese than muscle: 2.6 mg Mn/kg DW versus 0.71 (Table 4.5); the reverse was observed for iron (Jeffree et al., 2001).
4.14 Mercury Total mercury concentrations in marine reptiles seldom exceeded 0.5 mg Hg/kg DW, although concentrations up to 0.8 mg Hg/kg DW are recorded in liver and 1.39 mg Hg/kg DW in yolk (Table 4.6). Total mercury in livers of female loggerhead turtles, C. caretta, increased with increasing age of the turtle; the methylmercury percent in liver decreased with increasing total mercury concentration (Storelli et al., 1998a). Table 4.6: Mercury Concentrations in Field Collections of Reptiles Organism Baja California Sur; reference collection; maximum concentrations Green turtle, Chelonia mydas Fat Liver Muscle Kidney Loggerhead turtle, Caretta caretta Fat Liver Muscle Kidney
Concentration
Reference
0.011 DW 0.168 DW 0.059 DW 0.310 DW
9 9 9 9
0.028 DW 0.183 DW 0.041 DW 0.135 DW
9 9 9 9
a
(Continues)
240 Chapter 4 Table 4.6: Organism Olive ridley turtle, Lepidochelys olivacea Fat Liver Muscle Kidney Loggerhead turtle, Caretta caretta South Adriatic Sea; found beached; February-April 1991 and June-September 1995; females; total mercury vs. methylmercury Liver Muscle U.S. Atlantic Ocean coast nesting beaches; egg Yolk Albumen Yolk Whole Canary Islands, Spain; found stranded; 1998-2001; juveniles and subadults Liver Kidney Adriatic Sea Liver Kidney Muscle Liver Mexico Italy Japan Cyprus Southeast United States Kidney Mexico Italy
Cont’d
Concentration
0.156 DW 0.795 DW 0.144 DW 0.372 DW
0.7 (0.37-1.1) FW vs. 0.28 (0.24-0.33) FW 0.21 (0.07-0.43) FW vs. 0.23 (0.0-0.41) FW
0.02-0.09 FW 0.01-0.03 FW 0.41-1.39 DW 0.09 FW
Reference
a
9 9 9 9
19 19
1 1 2 3
0.04 (0.001-0.47) FW 0.04 (0.01-0.33) FW
16 16
1.7 FW 0.7 FW 0.7 FW
17 17 17
(0.12-0.18) DW (0.13-1.3) DW (0.25-8.1) DW (0.82-7.5) DW (0.35-1.3) DW
9 10 4 11 12
(0.07-0.11) DW (0.06-0.31) DW
9 10 (Continues)
Reptiles Table 4.6: Organism Japan Cyprus Southeast United States Muscle Mexico Italy Japan Cyprus Southeast USA Fat Mexico Italy Japan Egg; Japan, Kochi Prefecture Shell Yolk Albumen Whole Blood; South Carolina and Georgia; May-July 2003 Green turtle, Chelonia mydas Okinawa, Japan Liver Kidney Muscle Muscle; Papua New Guinea Total mercury Organic mercury Inorganic mercury Liver Mexico Japan Cyprus Kidney Mexico Japan Cyprus
241
Cont’d
Concentration
Reference
(0.04-0.44) DW (0.13-0.8) DW (0.13-0.44) DW
4 11 12
(0.02-0.04) DW (0.03-0.66) DW (0.05-0.19) DW (<0.01-1.8) DW (0.05-0.50) DW
9 10 4 11 12
(0.0002-0.028) DW Max. 0.09 DW Median 0.04 DW
9 10 13
0.004 FW 0.012 (0.008-0.016) DW 0.0005 FW 0.005 (0.0038-0.0074) FW 0.029 (0.006-0.077) FW
4 4 4 4 21
0.28 FW 0.13 FW 0.02 FW
18 18 18
0.038 FW 0.023 FW 0.015 FW
5 5 5
(0.026-0.153) DW (0.077-0.301) DW (0.27-1.37) DW
9 13 11
(0.003-0.31) DW (0.042-0.048) DW <0.001 DW
9 13 11
a
(Continues)
242 Chapter 4 Table 4.6: Organism Muscle Mexico Japan Cyprus Fat Mexico Japan Egg; Hong Kong; summer 2001 Yolk Albumen Eggshell
Cont’d
Concentration
Reference
(0.003-0.059) DW (0.002-0.007) DW Max. 0.37 DW
9 13 11
Max. 0.011 DW (0.0024-0.0028) DW
9 13
0.0015 FW 0.00009 FW 0.0006 FW
14 14 14
American crocodile, Crocodylus acutus Egg Contents Shell Albumen-yolk Whole Caudal scute; Costa Rica
0.09 (0.07-0.14) FW 0.21 DW 0.66 DW; 0.13 FW 0.71 FW 0.093 FW
6 7 7 3 15
Crocodile, Crocodylus porusus; Papua New Guinea; muscle Total mercury Organic mercury Inorganic mercury
0.13 FW 0.11 FW 0.02 FW
5 5 5
Leatherback turtle, Dermochelys coriacea United Kingdom coastal waters; found stranded Liver Muscle Blubber French Guiana; 2006; females Blood Eggs
0.39 DW 0.12 DW 0.11 DW
8 8 8
0.01 FW 0.01 FW
22 22
Diamondback terrapin, Malaclemys terrapin; 2004 South Carolina; 4 sites Blood
0.043 FW
20
a
(Continues)
Reptiles Table 4.6: Organism Scutes Total mercury Methylmercury Diet (gastropod soft parts) Brunswick, Georgia; superfund site Blood Scutes Total mercury Methylmercury Diet (gastropod soft parts)
243
Cont’d
Concentration
Reference
0.339 FW 0.307 FW 0.01-0.08 (0.006-0.192) FW
20 20 20
0.746 FW
20
3.36 FW 3.02 FW 0.18 (0.08-0.415) FW
20 20 20
a
Values are in mg Hg/kg fresh weight (FW) or dry weight (DW). a 1, Hillestad et al., 1974; 2, Stoneburner et al., 1980; 3, Hall, 1980; 4, Sakai et al., 1995; 5, Yoshinaga et al., 1992; 6, Ogden et al., 1974; 7, Stoneburner and Kushlan, 1984; 8, Davenport and Wrench, 1990; 9, Kampalath et al., 2006; 10, Storelli et al., 2005; 11, Godley et al., 1999; 12, Day et al., 2005; 13, Sakai et al., 2000b; 14, Lam et al., 2006; 15, Rainwater et al., 2007; 16, Torrent et al., 2004; 17, Storelli et al., 1998b; 18, Sakai et al., 2000a; 19, Storelli et al., 1998a; 20, Blanvillain et al., 2007; 21, Day et al., 2007; 22, Guirlet et al., 2008.
Mercury concentrations in three species of sea turtles from Baja California were highest in liver, followed by kidney, muscle, and fat, in that order (Kampalath et al., 2006). Concentrations were highest in the olive ridley turtle, L. olivacea; intermediate in loggerhead, C. caretta; and lowest in the green turtle, C. mydas. Differences are attributed to diets: green turtles are herbivores, loggerheads are carnivores, and ridley turtles are opportunistic feeders (Kampalath et al., 2006). Methylmercury concentrations in turtle tissues ranged from 0.0015 to 0.027 mg/kg DW tissue, and accounted for a maximum of 23% of the total mercury burden in green turtles (kidney), 65% in loggerheads (fat), and 100% in ridleys (muscle, fat, and kidney) (Kampalath et al., 2006). Blood mercury concentrations of loggerheads from South Carolina and Georgia were positively correlated with hematocrit and creatine phosphokinase activity and negatively correlated with lymphocyte cell counts and aspartate animotransferase; the correlation with hematocrit reflects the higher affinity of mercury for erythrocytes than plasma (Day et al., 2007).
4.15 Molybdenum Eggs of the green turtle, C. mydas, collected in Hong Kong during summer 2001, contained unusually high concentrations of molybdenum. In mg Mo/kg FW, yolk contained 9.7 (4.7-19.0), albumen 5.2 (2.4-8.6), and eggshell 38.0 (14.0-57.0) (Lam et al., 2006). This requires verification.
244 Chapter 4
4.16 Nickel In general, maximum nickel concentrations were recorded in loggerhead turtles from the Canary Islands: burdens up to 11.6 mg Ni/kg FW were measured in bone, 13.1 in muscle, 13.8 in liver, and 48.1 mg Ni/kg FW in kidney (Table 4.7). Green turtles from Baja California had up to 25.1 mg Ni/kg DW kidney versus 0.61 mg/kg DW in conspecifics from Okinawa; a similar patter exists for liver (Table 4.7). Nickel concentrations in green turtle eggs collected in Hong Kong during summer 2001 were, in mg Ni/kg FW, 0.19 in yolk, 0.017 in albumen, and 12.0 (2.6-21.0) in shell (Lam et al., 2006). In estuarine crocodiles, nickel was about eight times more abundant in osteoderms than in muscle (Jeffree et al., 2001).
4.17 Rubidium Rubidium concentrations in green turtle eggs collected in Hong Kong during 2001 had maximum concentrations, in mg Rb/kg FW, of 1.3 in yolk, 0.8 in albumen, and 0.84 in eggshell (Lam et al., 2006).
Table 4.7: Nickel and Selenium Concentrations in Field Collections of Reptiles Element and Organism
Concentration
Reference
a
Nickel Loggerhead turtle, Caretta caretta; Canary Islands, Spain; found stranded; 1998-2001; juveniles and subadults Bone Liver Muscle Kidney Green turtle, Chelonia mydas Baja California; 2002-2003; found drowned in fish nets Kidney Liver Okinawa, Japan Liver Kidney Muscle
1.0 2.9 1.7 5.8
(0.02-11.6) (0.01-13.8) (0.03-13.1) (0.04-48.1)
FW FW FW FW
6 6 6 6
3.2 (1.2-25.1) DW max. 30.1 DW
5 5
0.06 FW 0.61 FW <0.03 FW
7 7 7 (Continues)
Reptiles Table 4.7:
245
Cont’d
Element and Organism
Concentration
Reference
Estuarine crocodile, Crocodylus porosus; Australia; 1993-1997 Muscle Osteoderms
0.51 (0.14-0.85) DW 4.2 (1.1-7.2) DW
5 5
3.4 FW
1
4.9 (4.0-6.1) FW 2.3 (1.2-3.2) FW
8 8
a
Selenium Loggerhead turtle, Caretta caretta Hawaii; liver South Adriatic Sea; found beached; February-April 1991 and June-September 1995; females Liver Muscle Green turtle, Chelonia mydas Hawaii Liver Kidney Hong Kong; summer 2001 Yolk Albumen Eggshell
0.79 (0.14-2.53) FW 0.46 (0.16-1.58) FW
1 1
3.5 (1.3-7.6) FW 0.27 (0.08-0.73) FW 2.5 (0.45-11.0) FW
4 4 4
Estuarine crocodile, Crocodylus porosus; Australia; 1993-1997 Muscle Osteoderms
0.99 (0.44-2.0) DW <0.01 DW
5 5
0.87 (0.48-1.21) DW
2
10.0 FW 1.4 FW
9 9
1.41 DW 3.61 DW <0.05 DW
3 3 3
Crocodile, Crocodylus sp.; egg; contents Leatherback turtle, Dermochelys coriacea French Guiana; 2006; females Blood Eggs United Kingdom coastal waters; found stranded Liver Muscle Blubber
Values are in mg element/kg fresh weight (FW) or dry weight (DW). a 1, Aguirre et al., 1994; 2, Phelps et al., 1986; 3, Davenport and Wrench, 1990; 4, Lam et al., 2006; 5, Jeffree et al., 2001; 6, Torrent et al., 2004; 7, Sakai et al., 2000a; 8, Storelli et al., 1998a; 9, Guirlet et al., 2008.
246 Chapter 4
4.18 Selenium Concentrations are usually less than 2.0 mg Se/kg FW, although some samples of liver (6.1), muscle (3.6), yolk (7.6), and eggshell (11.0) are higher (Table 4.7). In general, selenium concentrations in marine reptiles were significantly higher in liver than in muscle (Storelli et al., 1998a). Selenium concentrations in crocodile muscle increased with increasing age (Jeffree et al., 2001).
4.19 Silver Eggs of the green turtle collected in summer 2001 from Hong Kong had 0.027 mg Ag/kg FW in yolk, 0.001 mg Ag/kg FW in albumen, and 0.034 mg Ag/kg FW in eggshell (Lam et al., 2006).
4.20 Strontium Strontium concentrations in eggs of C. mydas collected in Hong Kong during summer 2001 had 0.77 mg Sr/kg FW yolk, 9.4 (1.1-22.0) mg Sr/kg FW albumen, and 0.015 mg Sr/kg FW in eggshell (Lam et al., 2006). Estuarine crocodiles, C. porosus, collected from northern Australia between 1993 and 1997, contained <0.05 mg Sr/kg DW muscle and 318.0 (121.0-983.0) DW osteoderms (Jeffree et al., 2001).
4.21 Thallium Eggs of green turtles collected in Hong Kong during summer 2001 contained 0.91 mg Tl/kg FW in eggshell, 0.12 mg Tl/kg in yolk, and 0.04 mg Tl/kg FW albumen (Lam et al., 2006).
4.22 Titanium Estuarine crocodiles, C. porosus, collected between 1993 and 1997 from northern Australia contained 6.2 (1.8-10.2) mg Ti/kg DW in muscle and <0.01 mg Ti/kg DW in osteoderms; titanium burdens in muscle decreased with increasing age (Jeffree et al., 2001).
4.23 Uranium Crocodiles, C. porosus, had <0.01 mg U/kg DW in muscle, and 0.034 (0.018-0.075) mg U/kg DW in osteoderms (Jeffree et al., 2001).
4.24 Vanadium Vanadium concentrations in green turtle eggs from Hong Kong in summer 2001 were 0.22 mg V/kg FW yolk, 0.11 mg V/kg FW in albumen, and 0.08 mg V/kg FW in eggshell (Lam et al., 2006).
Reptiles
247
4.25 Zinc Maximum zinc concentrations measured in tissues of various marine reptiles, in mg Zn/kg FW were 6.3 in eggshell, 11.1 in blood, 26.0 in egg albumen, 32.4 in muscle, 38.5 in kidney, 80.5 in egg yolk, 91.4 in liver, and 216.3 in bone (Table 4.8). Zinc seemed abundant in all tissues measured, and may have accumulated in excess of the organism’s immediate needs, as was true for many other groups of marine organisms (Eisler, 2000). Zinc concentrations in crocodile muscle were higher in older animals (Jeffree et al., 2001). A captive Cuban crocodile, Crocodylus rhombifer, was diagnosed with zinc poisoning owing to ingestion of zinc-containing coins. The blood serum level of 45.3 mg Zn/L in this crocodile dropped to 30.7 mg/L with EDTA treatment after 18 days, and to 4.88 mg Zn/L at day 39 of treatment; feeding resumed at day 24 of treatment (Cook et al., 1989).
Table 4.8: Zinc Concentrations in Field Collections of Reptiles Organism Loggerhead turtle, Caretta caretta U.S. Atlantic Ocean coast nesting beaches; egg Yolk Albumen Yolk Whole Hawaii; liver Japan; Kochi Prefecture Liver Kidney Muscle Egg Shell Yolk Albumen Whole Canary Islands, Spain; found stranded; 1998-2001; juveniles and subadults Bone Liver Muscle Kidney
Concentration
Reference
32.2 FW 26.0 FW 73.5-80.5 FW 32.0 FW 15.1 FW
1 1 2 3 4
27.9 (23.2-35.1) FW 25.8 (19.2-30.4) FW 24.2 (19.5-31.0) FW
5 5 5
2.2 (1.7-2.9) FW 34.4 (30.5-38.0) FW 0.59 (0.06-1.5) FW 14.7 (13.2-16.5) FW
5 5 5 5
51.3 (0.5-216.3) FW 13.5 (0.1-91.4) FW 6.7 (0.05-32.4) FW 9.1 (0.07-38.5) FW
16 16 16 16
a
(Continues)
248 Chapter 4 Table 4.8: Organism Green turtle, Chelonia mydas Papua New Guinea; muscle Hawaii Liver Kidney Egg Shell Contents Hong Kong; summer 2001 Yolk Albumen Eggshell Baja California; 2002-2003; found drowned Kidney Liver Okinawa, Japan Liver Kidney Muscle
Cont’d
Concentration
Reference
15.7-20.4 FW
6
31.9 (18.1-45.8) FW 22.3 (12.5-38.1) FW
4 4
6.3 FW 12.1 FW
4 4
45.0 (25.0-68.0) FW 0.3 (0.038-0.75) FW 1.2 (0.3-2.6) FW
12 12 12
189.0 (102.0-281.0) DW 90.9 (102.0-281.0) DW
14 14
30.3 FW 29.6 FW 8.8 FW
17 17 17
American crocodile, Crocodylus acutus Egg contents; Florida Bay Caudal scute; Costa Rica
8.8 (7.2-11.0) FW 4.1 FW
2,7 13
Estuarine crocodile, Crocodylus porosus; northern Australia; 1993-1997 Muscle Osteoderms
81.4 (45.0-192.0) DW 5.2 (1.7-9.6) DW
15 15
Crocodile, Crocodylus spp. Egg contents Muscle
33.8 (22.5-47.5) DW 5.8 FW
8 6
Leatherback turtle, Dermochelys coriacea United Kingdom coastal waters; found stranded Liver Muscle Blubber
2.6 DW 1.9 DW 0.08 DW
9 9 9
a
2,7
(Continues)
Reptiles Table 4.8: Organism Mexico; Pacific Ocean coast; eggshell French Guiana; 2006; females Blood Eggs Olive Ridley turtle, Lepidochelys olivacea; Ecuador; humerus
Concentration
249
Cont’d Reference
11.9 DW
10
11.1 FW 14.2 FW
18 18
575.0-955.0 AW
11
a
Values are in mg Zn/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Hillestad et al., 1974; 2, Stoneburner et al., 1980; 3, Hall, 1980; 4, Aguirre et al., 1994; 5, Sakai et al., 1995; 6, Yoshinaga et al., 1992; 7, Ogden et al., 1974; 8, Phelps et al., 1986; 9, Davenport and Wrench, 1990; 10, Vazquez et al., 1997; 11, Witkowski and Frazier, 1982; 12, Lam et al., 2006; 13, Rainwater et al., 2007; 14, Talavera-Saenz et al., 2007; 15, Jeffree et al., 2001; 16, Torrent et al., 2004; 17, Sakai et al., 2000a; 18, Guirlet et al., 2008.
4.26 Literature Cited Aguirre, A.A., Balazs, G.H., Zimmerman, B., Galey, F.D., 1994. Organic contaminants and trace metals in the tissues of green turtles (Chelonia mydas) afflicted with fibriopapillomas in the Hawaiian Islands. Mar. Pollut. Bull. 28, 109–114. Agusa, T., Takagi, K., Kubota, R., Anan, Y., Iwata, H., Tanabe, S., 2008b. Specific accumulation of arsenic compounds in green turtles (Chelonia mydas) and hawksbill turtles (Eretmochelys imbricata) from Ishigaki Island, Japan. Environ. Pollut. 153, 127–136. Agusa, T., Takagi, K., Iwata, H., Tanabe, S., 2008a. Arsenic species and their accumulation features in green turtles (Chelonia mydas). Mar. Pollut. Bull. 57, 762–789. Beck, A.B., 1956. The copper content of the liver and blood of some vertebrates. Aust. J. Zool. 4, 1–18. Bicho, R., Joaquim, N., Mendonca, V., Al Kiyumi, A., Mahmoud, I.Y., Al Kindi, A., 2006. Levels of heavy metals and antioxidant enzymes in green turtle (Chelonia mydas) in the Arabian Sea, Sultanate of Oman. In: 26th Annual Symposium on Sea Turtle Biology and Conservation. Athens, Greece. International Sea Turtle Society. Blanvillain, G., Schwenter, J.A., Day, R.D., Point, D., Christopher, S.T., Roumillat, W.A., et al., 2007. Diamondback terrapins, Malaclemys terrapin, as a sentinel species for monitoring mercury pollution of estuarine systems in South Carolina and Georgia, USA. Environ. Toxicol. Chem. 26, 1441–1450. Caurant, F., Bustamante, P., Bordes, M., Miramand, P., 1999. Bioaccumulation of cadmium, copper and zinc in some tissues of three species of marine turtles stranded along the French Atlantic coast. Mar. Pollut. Bull. 38, 1085–1091. Cook, R.A., Behler, J., Brazaitis, P., 1989. Elevated heavy metal concentrations in captive crocodilians—2 cases. In: Conference Proceedings, American Association of Zoo Veterinarians, Media, Pennsylvania, October 1989, 151 pp. Davenport, J., Wrench, J., 1990. Metal levels in a leatherback turtle. Mar. Pollut. Bull. 21, 40–41. Day, R.D., Christopher, S.J., Becker, P.R., Whitaker, D.W., 2005. Monitoring mercury in the loggerhead sea turtle, Caretta caretta. Environ. Sci. Technol. 39, 437–446. Day, R.D., Segars, A.L., Arendt, M.D., Lee, A.M., Peden-Adams, M.M., 2007. Relationship of blood mercury levels to health parameters in the loggerhead sea turtle (Caretta caretta). Environ. Health Perspect. 115, 1421–1428.
250 Chapter 4 Eisler, R., 2000. Zinc. In: Handbook of Chemical Risk Assessment. Health Hazards to Humans, Plants, and Animals. Vol. 1, Metals. Lewis Publishers, Boca Raton, FL, pp. 605–714. Franzelletti, S., Locatelli, C., Gerosa, G., Vallini, C., Fabbri, E., 2004. Heavy metals in tissues of loggerhead turtles from the northwestern Adriatic Sea. Comp. Biochem. Physiol. 138, 187–194. Frias-Espericueta, M.G., Osuna-Lopez, J.I., Ruiz-Telles, A., Quintero-Alvarez, J.M., Lopez-Lopez, G., IzaguirreFierro, G., et al., 2006. Heavy metals in the tissues of the sea turtle Lepidochelys olivacea from a nesting site of the northwest coast of Mexico. Bull. Environ. Contam. Toxicol. 77, 179–185. Gardner, S.C., Fitzgerald, S.L., Acosta-Vargas, B., Mendez-Rodriguez, L., 2006. Heavy metal accumulation in four species of sea turtles from the Baja California Peninsula, Mexico. Biometals 19, 91–99. Godley, B.J., Thompson, D.R., Furness, R.W., 1999. Do heavy metal concentrations pose a threat to marine turtles from the Mediterranean Sea? Mar. Pollut. Bull. 38, 497–502. Gordon, A.N., Pople, A.R., Ng, J., 1998. Trace metal concentrations in livers and kidneys of sea turtles from south-eastern Queensland, Australia. Austral. J. Mar. Freshw. Res. 49, 409–414. Guirlet, E., Das, K., Girondot, M., 2008. Maternal transfer of trace elements in leatherback turtles (Dermochelys coriacea) of French Guiana. Aquat. Toxicol. 88, 267–276. Hall, R.J., 1980. Effects of environmental contaminants on reptiles: a review. U.S. Fish Wildl. Serv. Spec. Sci. Rept.—Wildl. 288, 1–12. Herbst, L.H., 1994. Fibropapillomatosis of marine turtles. Annu. Rev. Fish Dis. 4, 389–425. Herbst, L.H., Klein, P.A., 1995. Green turtle fibropapillomatosis: challenges to assessing the role of environmental cofactors. Environ. Health Perspect. 103 (Suppl. 4), 27–30. Hillestad, H.O., Reimold, R.J., Stickney, R.R., Windom, H.L., Jenkins, J.H., 1974. Pesticides, heavy metals, and radionuclide uptake in loggerhead sea turtles from South Carolina and Georgia. Herpetol. Rev. 5, 75. Jeffree, R.A., Markich, S.J., Twining, J.R., 2001. Element concentrations in the flesh and osteoderms of estuarine crocodiles (Crocodylus porosus) from the Alligator Rivers region, northern Australia: biotic and geographic effects. Arch. Environ. Contam. Toxicol. 40, 236–245. Kampalath, R., Gardner, S.C., Mendez-Rodriguez, L., Jay, J.A., 2006. Total and methylmercury in three species of sea turtles of Baja California Sur. Mar. Pollut. Bull. 52, 1816–1823. Lam, J.C.W., Tanabe, S., Chan, S.K.F., Yuen, E.K.W., Lam, M.H.W., Lam, P.K.S., 2004. Trace element residues in tissues of green turtles (Chelonia mydas) from South China waters. Mar. Pollut. Bull. 48, 164–192. Lam, J.C.W., Tanabe, S., Chan, S.K.F., Lam, M.H.W., Martin, M., Lam, P.K.S., 2006. Levels of trace elements in green turtle eggs collected from Hong Kong: evidence of risks due to selenium and nickel. Environ. Pollut. 144, 790–801. Linder, G., Grillitsch, B., 2000. Ecotoxicology of metals. In: Sparling, D.W., Linder, G., Bishop, C.A. (Eds.), Ecotoxicology of Amphibians and Reptiles. SETAC Press, Pensacola, FL, pp. 325–459. Musquera, S., Massegu, J., Planas, J., 1976. Blood proteins in turtles (Testudo hermanni, Emys orbicularis, and Caretta caretta). Comp. Biochem. Physiol. 55A, 225–230. Ogden, J.C., Robertson Jr., W.B., Davis, G.E., Schmidt, T.W., 1974. South Florida Ecological Study. Pesticides, Polychlorinated Biphenyls, and Heavy Metals in Upper Food Chain Levels, Everglades National Park and Vicinity. Final Report. Available from Division of Natural Science and Research Management Studies. Everglades National Park, Homestead, FL. Phelps, R.J., Focardi, S., Fossi, C., Leonzio, C., Renzoni, A., 1986. Chlorinated hydrocarbons and heavy metals in crocodile eggs from Zimbabwe. Trans. Zimbabwe Sci. Assn. 63, 8–15. Rainwater, T.R., Wu, T.H., Finger, A.G., Canas, J.E., Yu, L., Reynolds, K.D., et al., 2007. Metals and organochlorine pesticides in caudal scutes of crocodiles from Belize and Costa Rica. Sci. Total Environ. 373, 146–156. Saeki, K., Sakakibura, H., Sakai, H., Kunito, T., Tanabe, S., 2000. Arsenic accumulation in three species of sea turtles. Biometals 13, 241–250. Sahoo, G., Sahoo, R.K., Mohanty-Hejmadi, P. 1996. Distribution of heavy metals in the eggs and hatchings of olive ridley sea turtle Lepidochelys olivacea from Gahirmatha Orissa. Indian J. Mar. Sci. 25, 371–372.
Reptiles
251
Sakai, H., Ichihashi, H., Suganuma, H., Tatsukawa, R., 1995. Heavy metal monitoring in sea turtles using eggs. Mar. Pollut. Bull. 30, 347–353. Sakai, H., Saeki, K., Ichihashi, H., Suganuma, H., Tanabe, S., Tatsukawa, R., 2000b. Species-specific distribution of heavy metals in tissues and organs of loggerhead turtle (Caretta caretta) and green turtle (Chelonia mydas) from Japanese coastal waters. Mar. Pollut. Bull. 40, 701–709. Sakai, H., Saeki, K., Ichihashi, H., Kamezaki, N., Tanabe, S., Tatsukawa, R., 2000a. Growth-related changes in heavy metal accumulation in green turtle (Chelonia mydas) from Yaeyama Islands, Okinawa, Japan. Arch. Environ. Contam. Toxicol. f39, 378–385. Stoneburner, D.L., Kushlan, J.A., 1984. Heavy metal burdens in American crocodile eggs from Florida Bay, Florida, USA. J. Herpetol. 18, 192–193. Stoneburner, D.L., Nicora, M.N., Blood, E.R., 1980. Heavy metals in loggerhead sea turtle eggs (Caretta caretta): evidence to support the hypothesis that demes exist in the western Atlantic population. J. Herpetol. 14, 171–176. Storelli, M.M., Marcotrigiano, G.O., 2000. Total organic and inorganic arsenic in marine turtles (Caretta caretta) beached along the Italian coast (South Adriatic Sea). Bull. Environ. Contam. Toxicol. 65, 732–739. Storelli, M.M., Ceci, E., Marcotrigiano, G.O., 1998b. Distribution of heavy metals residues in some tissues of Caretta caretta (Linnaeus) specimens beached along the Adriatic Sea (Italy). Bull. Environ. Contam. Toxicol. 60, 546–552. Storelli, M.M., Ceci, E., Marcotrigiano, G.O., 1998a. Comparison of total mercury, methylmercury, and selenium in muscle tissues and in the liver of Stenella coeruleoalba (Meyen) and Caretta caretta (Linnaeus). Bull. Environ. Contam. Toxicol. 61, 541–547. Storelli, M.M., Storelli, A., D’Addabbo, R., Marano, C., Bruno, R., Marcotrigiano, G.O., 2005. Trace elements in loggerhead turtles (Caretta caretta) from the eastern Mediterranean Sea: overview and evaluation. Environ. Pollut. 135, 163–170. Talavera-Saenz, A., Gardner, S.C., Rodriquez, R.R., Vargas, B.A., 2007. Metal profiles used as environmental markers of green turtle (Chelonia mydas) foraging resources. Sci. Total Environ. 373, 94–102. Torrent, A., Gonzalez-Diaz, O.M., Monagas, P., Oros, J., 2004. Tissue distribution of metals in loggerhead turtles (Caretta caretta) stranded in Canary Islands, Spain. Mar. Pollut. Bull. 49, 854–874. Twining, J.R., Markich, S.K., Prince, K.E., Jeffree, R., 1999. Osteoderms of estuarine crocodiles record their enhanced Pb exposure in Kakadu National Park. Environ. Sci. Technol. 33, 4396–4400. Vazquez, G.F., Reyes, M.C., Fernandez, G., Aguayo, J.E.C., Sharma, V.K., 1997. Contamination in marine turtle (Dermochelys coriacea) eggshells of Playon de Mexiquillo, Michoacan, Mexico. Bull. Environ. Contam. Toxicol. 58, 326–333. Witkowski, S.A., Frazier, J.G., 1982. Heavy metals in sea turtles. Mar. Pollut. Bull. 13, 254–255. Yoshinaga, J., Suzuki, T., Hongo, T., Minagawa, M., Ohtsuka, R., Kawabe, T., et al., 1992. Mercury concentration correlates with the nitrogen stable isotope ratio in the animal food of Papuans. Ecotoxicol. Environ. Safety 24, 37–45.
CHAPTER 5
Birds During the past several decades, there has been a significant increase in the world literature on trace metal concentrations in marine birds despite a major sampling problem. It seems that many species of marine birds are now considered threatened or endangered by various nations thereby severely limiting chemical analyses to nondestructive techniques using feathers, blood, and addled eggs.
5.1 Aluminum Highest concentrations of aluminum in birds were usually in feathers, with a maximum value of 866.0 mg Al/kg DW in feathers of nestling ospreys, Pandion haliaetus (Table 5.1). Birds are most likely exposed to aluminum through their diets (Sparling and Lowe, 1996). Most aluminum is excreted via the feces and only a fraction is retained; in aluminum-sensitive species, aluminum binds with phosphorus causing rickets-like signs (Sparling and Lowe, 1996). Diets containing >1000.0 mg Al/kg dry weight diet are reportedly toxic in birds and mammals, with effects exacerbated by low dietary calcium and phosphorus (Scheuhammer, 1991).
5.2 Americium Breast muscle and bone of four species of seabirds collected in the Aleutian Islands in summer 2004 had no measurable levels of 241Am, including samples from Amchitka Island, the site of underground nuclear tests between 1965 and 1971 (Burger and Gochfeld, 2007).
5.3 Antimony Antimony concentrations in muscle of Arctic region seabirds collected in 1998-1999 ranged from 0.001 to 0.002 mg Sb/kg FW; for liver, concentrations ranged from 0.002 to 0.010 mg Sb/kg FW (Borga et al., 2006).
253
254 Chapter 5 Table 5.1: Aluminum, Arsenic, and Boron Concentrations in Field Collections of Birds Element and Organism
Concentration
Reference
a
Aluminum Antarctica; molting feathers; 2002-2003 Gentoo penguin, Pygoscelis papua Chinstrap penguin, Pygoscelis antarctica
40.0 DW vs. 46.0 DW 26.0 DW vs. 26.0 DW
12 12
2.7 (0.24-13.4) DW
15
Black-crowned night-heron, Nycticorax nycticorax; 1998-1999; nestlings; feathers Baltimore Harbor, Maryland Holland Island, Maryland Pea Patch Island, Delaware
9.2 (6.8-12.3) DW 42.3 (28.4-63.0) DW 78.9 (37.9-164.3) DW
21 21 21
Osprey, Pandion haliaetus; nestlings; Chesapeake Bay, Maryland, 2000-2001 vs. Delaware Bay, Delaware, 2002; max. values Blood Feathers
<2.0 DW vs. 6.5 DW 866.0 DW vs. 382.0 DW
18 18
Clapper rail, Rallus longirostris; eggshell; Georgia; 2000 Metals-contaminated marsh Reference site
79.0 (18.0-186.0) DW 88.0 (39.0-207.0) DW
22 22
0.32 DW
19
0.29-0.34 DW vs. 0.16 DW
19
Blue-winged teal, Anas discors; liver; 1998-1999; southern Texas
0.20 (0.006-0.22) FW
16
Black duck, Anas rubripes; egg
0.18 FW
Antarctica; molting feathers; 2002 vs. 2003 Gentoo penguin, Pygoscelis papua Chinstrap penguin, Pygoscelis antarctica
0.9 DW vs. (0.6-4.0) DW 0.45 DW vs. (0.06-2.4) DW
Gray heron, Ardea cinerea; Kanto area; Japan; liver
Arsenic Alaska; Prince William Sound; 2004; breast feathers Black oystercatcher, Haematopus bachmani Black-legged kittiwake, Rissa tridactyla; oiled vs. non-oiled
1
12 12 (Continues)
Birds Table 5.1:
255
Cont’d
Element and Organism
Concentration
Reference
Arctic region seabirds; Barents Sea; May 1999; muscle Dovekie, Alle alle Thick-billed murre, Uria lomvia Black guillemot, Cepphus grylle
0.70 FW 2.4 FW 2.9 FW
17 17 17
Arctic region seabirds; Baffin Bay, Canada; May-June 1998; muscle vs. liver Dovekie Black-legged kittiwake, Rissa tridactyla Thick-billed murre Black guillemot Northern fulmar, Fulmaris glacialis Thayer’s gull, Larus thayeri
0.47 FW vs. 1.5 FW 3.0 FW vs. 8.8 FW 2.5 FW vs. 10.4 FW 1.6 FW vs. 6.6 FW 2.7 FW vs. 6.9 FW 5.4 FW vs. 19.6 FW
17 17 17 17 17 17
Gray heron, Ardea cinerea; Kanto area; Japan Liver Kidney Muscle Lung Brain
0.51 DW; max. 0.97 DW 0.74 DW; max. 3.5 DW 0.28 DW; max. 0.71 DW 0.8 DW; max. 10.0 DW 0.19 DW; max. 0.85 DW
15 15 15 15 15
Canada; Vancouver Island, British Columbia; near copper mine; 1976 vs. 1981-1982 Western grebe, Aechmophorus occidentalis; liver Glaucous-winged gull, Larus glaucescens; liver Marbled murrelet, Synthiboramphus antiguis Liver Diet, all stations Pigeon guillemot, Cepphus columba; feather; Alaska; summer 2004 Prince William Sound Amchitka Kiska
0.41 DW 0.12 DW 0.20 DW
13 13 13
Little egret, Egretta garzetta; Pearl River Delta, China; industrialized area; May 2000 Egg contents Chick feather
0.24 (0.02-0.83) DW 0.11 (0.02-4.52) DW
11 11
1.1 FW vs. 0.08 FW
7
1.6 FW vs. 0.1 FW
7
3.2 FW vs. 0.8 FW 0.03 FW vs. 0.15 FW
7 7
a
(Continues)
256 Chapter 5 Table 5.1:
Cont’d
Element and Organism
Concentration
Little penguin, Eudyptula minor; southern Victoria, Australia; 2005; found dead (killed by foxes) Muscle Liver
1.2 FW, max. 4.49 FW 1.2 FW, max. 3.5 FW
Gulls; 3 spp.; oils
0.6-13.2 FW
6
Max. 16.7 FW
4
Osprey, Pandion haliaetus Liver Nestlings; Chesapeake Bay, Maryland 2000-2001 vs. Delaware Bay, Delaware, 2002; max. values Blood Feathers
1.7 DW vs. 4.0 DW 1.7 DW vs. 3.1 DW
Reference
10 10
18 18
White-faced ibis, Plegadis chihi; egg
0.03 FW
Clapper rail, Rallus longirostris; eggshell; Georgia; 2000 Metals-contaminated marsh Reference site
0.21 (0.03-0.42) DW 0.21 (0.11-0.43) DW
22 22
0.18-0.46 (0.073-1.35) DW
14
Seabirds; Spain; 2002-2003; 3 species of alcids; liver; found dead or dying after oil spill
a
5
Shorebirds 7 spp.; Corpus Christi, Texas; liver 5 spp.; New Zealand estuaries; feathers vs. liver
0.05-1.5 FW
2
0.01-0.99 FW vs. 0.01-2.55 FW
3
Common eider, Somateria mollissima; Aleutian Islands, Alaska; summer 2007; females Feathers Eggs
0.16 DW 0.77 DW
Spain; Ebro Delta bird sanctuary; liver; January-April 1989; found dead 7 spp. 5 spp. 2 spp.
<0.2 FW 0.2-0.5 FW 1.0-1.2 FW
20 20
8 8 8 (Continues)
Birds Table 5.1: Element and Organism
257
Cont’d
Concentration
Reference
a
Boron Willet, Catoptrophorus semipalmatus; 1994; San Diego Bay, California; sediments vs. stomach contents Naval Air Station Tijuana Slough National Wildlife Refuge
<10.0 DW vs. 39.0 DW 21.0 DW vs. 6.5 DW
Osprey, Pandion haliaetus; nestlings; Chesapeake Bay, Maryland, 2000-2001 vs. Delaware Bay, Delaware, 2002; max. values Blood Feathers
2.6 DW vs. 0.8 DW 7.4 DW vs. 7.2 DW
9 9
18 18
Values are in mg element/kg fresh weight (FW) or dry weight (DW). a 1, Haseltine et al., 1980; 2, White et al., 1980; 3, Turner et al., 1978; 4, Wiemeyer et al., 1980; 5, King et al., 1980; 6, Lunde, 1977; 7, Vermeer and Thompson, 1992; 8, Guitart et al., 1994b; 9, Hui and Beyer, 1998; 10, Choong et al., 2007; 11, Zhang et al., 2006; 12, Metcheva et al., 2006; 13, Burger et al., 2007; 14, Perez-Lopez et al., 2006; 15, Horai et al., 2007; 16, Fedynich et al., 2007; 17, Borga et al., 2006; 18, Rattner et al., 2008; 19, Burger et al., 2008; 20, Burger et al., 2008a; 21, Custer et al., 2008; 22, Rodriguez-Navarro et al., 2002.
5.4 Arsenic A high concentration of 13.2 mg As/kg fresh weight was determined in gull oils (Table 5.1), and tends to corroborate the findings of others who demonstrated that arsenic concentrates in oily fractions of marine plants, invertebrates, and higher organisms. An abnormal concentration of 16.7 mg As/kg fresh weight was recorded in liver of an osprey, P. haliaetus, from Maryland, USA. When collected, this bird was alive in a weak condition, with serious histopathology including absence of subcutaneous fat, serous fluid in the pericardial sac, and lung and kidney disorders. It died shortly after collection. Arsenic concentrations in liver from other ospreys collected in the same area and environs usually contained less than 1.5 mg As/kg fresh weight (Wiemeyer et al., 1980). The acute oral LD50 value for mallards, Anas platyrhyncos, and sodium arsenite is 323.0 mg As3þ/kg body weight (Hudson et al., 1984; NRCC, 1978; USNAS, 1977). Lethality from acute inorganic arsenic poisoning is due to the destruction of blood vessels lining the gut, resulting in decreased blood pressure and subsequent shock (Nystrom, 1984). Studies with dietary sodium arsenate and mallards showed dose-
258 Chapter 5 dependent adverse effects on growth, egg laying, and eggshell thinning (Camardese et al., 1990; Hoffman et al., 1992a; Pendleton et al., 1995; Stanley et al., 1994). In mallard ducklings, arsenic concentrations in liver ranged from 0.2 mg As/kg DW in controls to 33.0 in the group fed a diet containing 400.0 mg As5þ/kg (Stanley et al., 1994). Diets containing as little as 30.0 mg As5þ/kg fed to ducklings for 10 weeks produced elevated hepatic glutathione and ATP concentrations, and decreased overall weight gain and rate of growth in females (Camardese et al., 1990). A diet of 300.0 mg As5þ/kg altered duckling brain biochemistry and nesting behavior; decreased energy levels and altered behavior can further decrease duckling survival in a natural environment (Camardese et al., 1990). Day-old ducklings fed diets containing 200.0 mg As5þ/kg for 4 weeks had only minor growth reduction when dietary protein was adequate (22%), but when protein was only 7%, growth and survival were reduced and frequency of liver histopathology increased (Hoffman et al., 1992a). Adult male mallards fed diets containing 300.0 mg As5þ/kg reached equilibrium in 10-30 days; on transfer to an uncontaminated diet, liver lost 50% of its arsenic content in 1-3 days (Pendleton et al., 1995).
5.5 Barium Livers of the gray heron, Ardea cinerea, from a Japanese estuary had a mean content of 0.36 mg Ba/kg DW, and a maximum of 5.4 mg Ba/kg DW (Horai et al., 2007). Nestlings of the osprey, P. haliaetus, from Chesapeake Bay, Maryland and Delaware Bay, Delaware collected in 2000-2002, had maximum concentrations of 0.23 mg Ba/kg DW blood and 31.2 mg Ba/kg DW in feathers (Rattner et al., 2008). Feathers of nestling black-crowned night-herons, Nycticorax nycticorax, collected in 1998-1999 from sites in Maryland and Delaware had a maximum of 2.5 mg Ba/kg DW (Custer et al., 2008).
5.6 Beryllium Nestlings of the osprey, P. haliaetus collected from Chesapeake Bay, Maryland, and Delaware Bay, Delaware, during 2000-2002 had less than 0.01 mg Be/kg DW in blood and a maximum of 0.12 mg Be/kg DW in feathers (Rattner et al., 2008).
5.7 Bismuth A maximum value of 0.05 mg Bi/kg dry weight liver was measured in the gray heron, A. cinerea (Horai et al., 2007).
Birds
259
5.8 Boron Aside from data on boron concentrations in diet of willets, Catoptrophus semipalmatus, from San Diego Bay (3.9-6.5 mg B/kg dry weight; Table 5.1), and on blood and feather burdens in nestling ospreys (Rattner et al., 2008; Table 5.1), no other information was found on boron concentrations in field collections of birds. Studies with mallards, Anas platyrhynchos, show that dietary boron concentrations well below environmental levels in certain locales represent a toxicological hazard (Hoffman et al., 1990; Smith and Anders, 1989). Thus, 300.0-400.0 mg B/kg ration on a fresh weight basis adversely affects mallard growth, behavior, and brain biochemistry and is often associated with elevated tissue boron levels; maximum boron concentrations, in mg B/kg dry weight were 24.0 in adult liver, 36.0 in duckling liver, 24.0 in adult brain, and 44.0 in duckling brain (Smith and Anders, 1989). Diets containing 100.0 mg B/kg fresh weight result in reduced growth of female mallard ducklings (Hoffman et al., 1990) and diets containing as little as 30.0 mg B/kg fresh weight fed to mallard adults adversely affected the growth rate of subsequent ducklings (Smith and Anders, 1989).
5.9 Cadmium Highest concentrations of cadmium in tissues of marine birds were in kidney tissue of oceanic birds (Table 5.2). In general, kidney contained the highest concentrations of cadmium in all avian species, followed by liver, muscle, brain, and egg, although the order of the last two may be reversed. Effects of elevated kidney cadmium burdens (Table 5.2) on the health, survival, and breeding capacity of adult male scoters, Melanitta perspicillata, may account, in part, for long-term unexplained declines in breeding bird numbers on the Pacific Ocean coast of Canada (Harris et al., 2007). Scoters from the Queen Charlotte Islands in Canada, for example, had cadmium renal burdens as high as 390.2 mg/kg DW; this concentration is potentially associated with kidney damage (Barjaktarovic et al., 2002). Kidney cadmium concentrations in scoters were usually higher in males than females, and significantly correlated with zinc and metallothionein content (Barjaktarovic et al., 2002). Pigeon guillemots from locations in Prince William Sound, Alaska, impacted by massive oil spills had higher levels of cadmium in feathers than did guillemots from unoiled places in Prince William Sound; and all guillemots from Prince William Sound had significantly higher levels of cadmium in feathers than did conspecifics from Amchitka and Kiska in the Aleutians (Burger et al., 2007). Hepatic cadmium is negatively correlated with lipid reserves in migratory lesser scaup, Aythya affinis, collected in southern Louisiana (Anteau et al., 2007). Lipid reserves of migratory female scaup decline 47% on average during spring migration
260 Chapter 5 Table 5.2: Cadmium Concentrations in Field Collections of Birds Organism Alaska; Prince William Sound; 2004; breast feathers Black oystercatcher, Haematopus bachmani Black-legged kittiwake, Rissa tridactyla; oiled vs. nonoiled Aleutian Islands; summer 2004; egg contents Common eider, Somateria mollissima Glaucous-winged gull, Larus glaucescens Blue-winged teal, Anas discors; liver; 1998-1999; southern Texas Razor-billed auk, Alca torda; St. Kilda, Scotland; males vs. females Liver Kidney Antarctica; molting feathers; 2002 vs. 2003 Gentoo penguin, Pygoscelis papua Chinstrap penguin, Pygoscelis antarctica Arctic region seabirds; Barents Sea; May 1999; muscle Dovekie, Alle alle Thick-billed murre, Uria lomvia Black guillemot, Cepphus grille Arctic region seabirds; Baffin Bay, Canada; May-June 1998; muscle vs. liver Dovekie Black-legged kittiwake, Rissa tridactyla Thick-billed murre Black guillemot Northern fulmar, Fulmaris glacialis
Concentration
Reference
0.09 DW
42
0.91 DW vs. 0.03 DW
42
0.076 DW
19
0.143 DW
19
0.97 (0.008-8.1) FW
28
1.4-2.4 DW vs. 1.8 DW 14.6-18.2 DW vs. 16.0 DW
a
2 2
0.21 DW vs. (0.15-0.43) DW 0.3 DW vs. (0.15-0.2) DW
22 22
0.15 FW 0.28 FW 0.04 FW
37 37 37
0.41 FW vs. 5.8 FW 0.46 FW vs. 8.6 FW
37 37
0.55 FW vs. 13.8 FW 0.42 FW vs. 6.8 FW 1.2 FW vs. 21.8 FW
37 37 37 (Continues)
Birds Table 5.2: Organism Thayer’s gull, Larus thayeri Gray heron, Ardea cinerea; Kanto area; Japan Liver Kidney Muscle Lung Brain Lesser scaup, Aythya affinis; 2004-2005; males; kidney Canvasback, Aythya valisineria Liver Kidney Dunlin, Calidris alpina; 1979-1982; Bristol Channel; England; kidneys; 5 sites Adult males Adult females Juveniles Dunlin diet; annelid worms vs. clams Canadian Arctic; June 1997 Common eider, Somateria mollissima; females Kidney Liver King eider, Somateria spectabilis; males vs. females Kidney Liver Canada; Pacific Northwest; 1989-1994; adults; various sites White-winged scoter, Melanitta fusca; males vs. females Kidney Liver
261
Cont’d
Concentration
Reference
0.08 FW vs. 1.8 FW
37
0.19 DW; max. 0.6 DW 0.62 DW; max. 3.2 DW 0.003 DW 0.03 DW 0.001 DW
25 25 25 25 25
9.2 (0.78-93.6) DW
40
0.59 FW 2.3 FW
a
3 3
Usually <1.3 DW; max 13.0-16.0 DW Usually <1.3 DW; max. 4.0-61.0 DW Usually <0.8 DW; max. 2.0-11.0 DW 2.4-24.5 DW vs. 1.8-4.5 DW
11
68.1 (47.1-113.5) DW 10.5 (6.5-17.8) DW
33 33
173.7 (146.8-232.5) DW vs. 154.5 (116.2-213.3) DW 33.5 (26.7-38.0) DW vs. 27.1 (15.7-41.1) DW
33
27.0-52.0 FW vs. 12.6-75.1 FW 13.0 FW vs. 10.4 FW
32 32
11 11 11
33
(Continues)
262 Chapter 5 Table 5.2: Organism Surf scoter, Melanitta perspicillata Kidney Liver; males vs. females
Cont’d
Concentration
Reference
13.8-178.7 FW 5.5-77.7 FW vs. 6.0-22.4 FW
32 32
Pigeon guillemot, Cepphus columba; feather; Alaska; summer 2004 Prince William Sound Amchitka Kiska
0.10 DW 0.03 DW 0.028 DW
23 23 23
Black-footed albatross, Diomedea nigripes Liver Kidney
124.0 DW 262.0 DW
47 47
Diving ducks; Baltic Sea; found drowned; bone (tarsometatarsus) vs. cartilage (trachea); 2000-2004 Scaup, Aythya marila Pochard, Aythya ferina
0.12 DW vs. 0.16 DW 0.19 DW vs. 0.19 DW
26 26
2.5 3.4 0.3 0.4
31 31 31 31
Diving ducks; coastal California; December 1986-March 1987; kidney Canvasback, Aythya valisineria Adult males Adult females Juvenile males Juvenile females Greater scaup, Aythya marila Adult males Adult females Lesser scaup, Aythya affinis Adult males Juvenile males
(0.4-5.8) DW (2.4-4.7) DW (0.06-1.2) DW (0.2-0.7) DW
9.8 (4.6-21.0) DW 11.6 (9.7-14.0) DW
31 31
7.1 (3.7-18.0) DW 3.2 (2.4-4.4) DW
31 31
0.01 DW
20
Little penguin, Eudyptula minor; Victoria, Australia; 2005; found dead Muscle Liver
0.53 FW; max. 4.04 FW 1.7 FW; max. 6.0 FW
17 17
Atlantic puffin, Fratercula arctica; St. Kilda, Scotland; males vs. females Liver Kidney
18.9-29.4 DW vs. 14.1 DW 109.0-125.0 DW vs. 75.1 DW
Little egret, Egretta garzetta; China; May 2000; egg contents
a
2 2 (Continues)
Birds Table 5.2: Organism Southern fulmar, Fulmaris glacialoides; St. Kilda, Scotland; males vs. females Liver Kidney Bufflehead, Glaucionetta albeola; NW Atlantic Ocean; muscle
Cont’d
Concentration
Reference
7.7-9.1 DW vs. 49.4-50.1 DW 32.8-46.7 DW vs. 184.0-240.0 DW
2 2
0.11 FW; 0.3-0.4 DW
6
Greenland; 1975-1991; seabirds; 10 spp. Muscle Liver Kidney
<0.02-0.7 FW 0.15-12.6 FW 0.3-60.5 FW
Storm petrel, Hydrobates pelagicus; St. Kilda, Scotland; males vs. females Liver Kidney
9.2-20.8 DW vs. 26.5 DW 30.2-52.9 DW vs. 36.7 DW
2 2
Herring gull, Larus argentatus; egg
0.03-0.06 FW
7
0.048 FW 0.031 FW 0.023 FW 0.496 FW 0.045 FW 0.048 FW
8 8 8 8 8 8
0.096 FW 0.683 FW 0.053 FW 0.093 FW 0.691 FW <0.001 FW
8 8 8 8 8 8
0.473 FW 0.442 FW 0.144 FW 5.014 FW 0.579 FW 0.109 FW
8 8 8 8 8 8
Laughing gull, Larus atricilla; maximum values Downy young Brain Bone Heart Kidney Liver Muscle Prefledglings Brain Bone Heart Kidney Liver Muscle Adults Brain Bone Heart Kidney Liver Muscle
263
a
12 12 12
(Continues)
264 Chapter 5 Table 5.2: Organism Stomach contents Fish, 5 spp. Insects
Cont’d
Concentration
Reference
0.553 FW 0.154 FW
8 8
Lesser black-backed gull, Larus fuscus Muscle Liver Kidney
1.0 DW 4.0 DW 10.0 DW
9 9 9
Common black-headed gull, Larus ridibundus; Mediterranean Sea coast of Italy Liver Muscle Kidney Brain
0.2-2.6 FW 0.3-1.9 FW 0.4-2.1 FW 1.4 FW
Hooded merganser, Lophodytes cucullatus; NW Atlantic Ocean; muscle Surf scoter, Melanitta perspicillata British Columbia, Canada; south coast; 4 sites; 1998-2001; kidney Immature females Adult females Immature males Adult males Red-breasted merganser, Mergus serrator; NW Atlantic Ocean; muscle Mexico; Gulf of California; 1999-2000; muscle Brown pelican, Pelecanus occidentalis Cormorant, Phalacrocorax brasilianus Leach’s petrel, Oceanodroma leucorhoa; St. Kilda, Scotland; males vs. females Liver Kidney
<0.03-0.09 FW; <0.1-0.3 DW
13.2 (6.6-28.1) DW 18.1 (11.0-84.0) DW 4.8 (1.2-7.8) DW 37.9 (19.5-172.0) DW <0.02-0.05 FW;<0.1-0.2 DW
10 10 10 10 6
21, 21, 21, 21,
29 29 29 29
6
0.7 DW
41
1.2 DW
41
20.6-57.0 DW vs. 21.5 DW 68.5-80.0 DW vs. 128.0 DW
a
2 2 (Continues)
Birds Table 5.2:
Cont’d
Organism
Concentration
Black-crowned night-heron, Nycticorax nycticorax; 1998-1999; nestlings; feathers Baltimore Harbor, Maryland Holland Island, Maryland Pea Patch Island, Delaware
0.016 (0.008-0.03) DW 0.012 (0.007-0.019) DW 0.029 (0.011-0.08) DW
46 46 46
Osprey, Pandion haliaetus; nestlings; Chesapeake Bay, Maryland 2000-2001 vs. Delaware Bay, Delaware 2002; max. values Blood Feathers
<0.008 DW vs. <0.008 DW 0.28 DW vs. 0.07 DW
38 38
Manx shearwater, Puffinus; St. Kilda; males vs. females Liver Kidney
14.6-26.0 DW vs. 39.9 DW 67.0-133.0 DW vs. 231.0 DW
2 2
Adelie penguin, Pygoscelis adeliae; liver
90.0 DW
1
Kittiwake, Rissa tridactyla, North Sea; 1992-1994; age 1 day vs. age 21-40 days Feather Kidney Liver
0.02 DW vs. 0.03 DW 0.02 DW vs. 0.12 DW 0.01 DW vs. 0.03 DW
15 15 15
Seabirds; Canadian Arctic; breeding season, 1991-1993; 5 spp. Liver Kidney
8.5-39.4 DW 67.1-256.0 (32.5-432.0) DW
43 43
6.3 DW vs. 66.8 DW 27.8 DW vs. 13.8 DW 0.12 DW vs. 9.3 DW
27 27 27
3.3 DW vs. 53.0 DW 12.6 DW vs. 147.0 DW 0.07 DW vs. 4.6 DW
27 27 27
Seabirds; 3 spp.; Reunion Island, western Indian Ocean; 2002-2004; juveniles vs. adults Barau’s petrel, Pterodroma baraui Liver Kidney Muscle Audubon’s shearwater, Puffinus lherminieri bailloni Liver Kidney Muscle
265
Reference
a
(Continues)
266 Chapter 5 Table 5.2: Organism White-tailed tropicbird, Phaethon lepturus Liver Kidney Muscle
Cont’d
Concentration
Reference
4.5 DW vs. 47.0 DW 19.5 DW vs. 117.0 DW 0.4 DW vs. 3.7 DW
27 27 27
Seabirds; liver
Usually 5.0-35.0 DW
13
Seabirds; liver; Spain; 2002-2003; found dead or dying after oil spill
0.05-1.5 DW; max. 4.8 DW
24
8.0-71.0 DW
14
<2.0 DW 2.0-10.0 DW
14 14
23.0-39.0 DW
14
180.0 DW
14
(0.002-0.076) FW (0.0003-0.031) FW
44 44
Seabirds Liver; 11 spp. 3 spp; max. values Brain, fat, bone, feather Stomach, muscle, skin, eyeball, Esophagus, trachea Intestine, liver, pancreas, spleen, gallbladder, gonad Kidney Sea ducks; Canada; breeding females; 2001-2003; blood King eider, Somateria spectabilis White-winged scoter, Melanitta fusca Shorebirds 5 spp.; New Zealand estuaries; liver vs. kidney 5 spp.; New York Bight; 1989; eggs vs. fledgling feather 7 spp.; Corpus Christi, Texas; kidney 5 spp.; Yeongjong Island, Korea; autumn migration; 1994-1995 Liver Kidney Muscle Bone Feathers Common eider, Somateria mollissima Muscle Liver Kidney Egg
0.080-1.48 FW vs. 0.05-14.75 FW
4
Max. 0.02 DW vs. 0.03-0.57 DW
16
0.33-22.7 FW
0.18-0.66 (0.07-1.84) FW 0.78-3.7 (0.26-5.95) FW 0.05-0.30 (0.01-1.50) FW 0.34-1.37 (0.16-2.32) FW 0.38-1.1 (0.17-1.7) FW 2.0 DW 13.0 DW 25.0 DW 1.0 DW
a
5
18 18 18 18 39 9 9 9 9 (Continues)
Birds Table 5.2: Organism Aleutian Islands, Alaska; summer 2007; females Feathers Eggs Northern common eider, Somateria mollissima borealis; eastern Canadian Arctic; kidney 1998-1999 Females; 1998 vs. 1999 Males; 1999 Females; 1997-2000; prenesting vs. nesting
267
Cont’d
Concentration
Reference
0.03 DW 0.001 DW
45 45
162.6 (97.7-281.3) DW vs. 81.2 (31.3-275.0) DW 134.0 (64.6-309.0) DW 74.0 (61.0-90.0) DW vs. 164.0 (146.0-184.0) DW
34
a
34 35
Red-footed booby, Sula sula; Dongdao Island; South China Sea; March-April 2003 Feces Wing bone Eggshell Feather
6.3 (5.2-7.3) DW 0.2 DW 0.1 DW 0.3 DW
36 36 36 36
Guillemot, Uria aalge; Belgium; winters; 1993-1998; normal vs. severely emaciated Liver Kidney Muscle
1.9 DW vs. 2.8 DW 7.1 DW vs. 10.1 DW <0.01 DW vs. 0.01 DW
30 30 30
Values are in mg Cd/kg fresh weight (FW) or dry weight (DW). a 1, Robertson et al., 1972; 2, Bull et al., 1977; 3, White et al., 1979; 4, Turner et al., 1978; 5, White et al., 1980; 6, Bernhard and Zattera, 1975; 7, Peden et al., 1973; 8, Hulse et al., 1980; 9, Lande, 1977; 10, Vannucchi et al., 1978; 11, Ferns and Anderson, 1994; 12,Dietz et al., 1996; 13, Furness, 1996; 14, Kim et al., 1998; 15, Wenzel et al., 1996; 16, Burger and Gochfeld, 1993; 17, Choong et al., 2007; 18, Kim et al., 2007; 19, Burger and Gochfeld, 2007; 20, Zhang et al., 2006; 21, Harris et al., 2007; 22, Metcheva et al., 2006; 23, Burger et al., 2007; 24, PerezLopez et al., 2006; 25, Horai et al., 2007; 26, Kalisinska et al., 2007; 27, Kojadinovic et al., 2007a; 28, Fedynich et al., 2007; 29, Elliott et al., 2007; 30, Debacker et al., 2000; 31, Takekawa et al., 2002; 32, Barjaktarovic et al., 2002; 33, Wayland et al., 2001; 34, Wayland et al., 2002; 35, Wayland et al., 2005; 36, Liu et al., 2006; 37, Borga et al., 2006; 38, Rattner et al., 2008; 39, Kim and Koo, 2008b; 40, Pollock and Machin, 2008; 41, RuelasInzunza and Paez-Osuna, 2008; 42, Burger et al., 2008; 43, Braune and Scheuhammer, 2008; 44, Wayland et al., 2008; 45, Burger et al., 2008a; 46, Custer et al., 2008; 47, Arai et al., 2004.
268 Chapter 5 despite the relatively low hepatic cadmium concentrations of 0.61-1.05 mg/kg DW. If levels of hepatic cadmium were to increase in scaup, cadmium could potentially cause larger decreases in lipid reserves, especially if females are nutritionally stressed (Anteau et al., 2007). Marine and terrestrial animals, including ducks, are known to be abundant in wildlife communities associated with marine sewer outfalls (Brown et al., 1977). These animals sometimes contain elevated burdens of cadmium as well as zinc and copper, but are apparently protected from deleterious effects of high metal body burdens by metallothioneins. Concentrations of the metal-binding proteinaceous metallothioneins and heavy metal burdens depend mainly on the degree of contamination and secondarily on the species of animal and its position in the food web. Ducks contained the highest levels of metallothioneins of all groups examined (Brown et al., 1977). Zinc selectively competes with cadmium on high and low molecular weight metallothioneins in duck kidney and liver (Brown and Chatel, 1978). Once the high molecular weight protein pool is saturated, excess zinc is stored on metallothionein with serious implications to health of waterfowl simultaneously stressed with zinc and cadmium (Brown and Chatel, 1978). Most of the cadmium in seabirds concentrates in the soluble fractions of liver and kidney, as was true for selenium; however, insoluble fractions preferentially accumulated iron, manganese, and zinc; a metallothioneinmediated cadmium detoxification occurs in kidney and liver (Kojadinovic et al., 2007b). Metallothionein concentrations in livers from five species of seabirds from the Canadian Arctic region collected in 1991-1993 were positively correlated with cadmium and also zinc for all species; however, there was no correlation with copper in any species (Braune and Scheuhammer, 2008). Cadmium liver burdens in migratory blue-winged teal, Anas discors, were highest in spring and lowest in autumn; the reverse was true for copper (Fedynich et al., 2007). Body condition and reproductive stage need to be considered when interpreting the significance of cadmium and other metals in tissues of eiders (Wayland et al., 2005). For example, renal cadmium burdens were significantly lower in prenesting birds when compared to nesting birds and are affected by normal changes in body and organ mass that occur during the reproductive period (Wayland et al., 2005). Cadmium concentrations in liver of eiders from the Canadian Arctic region were significantly correlated with cadmium concentrations in kidney; in liver, cadmium was positively correlated with levels of zinc, copper, and mercury (Wayland et al., 2001). Capture-induced stress, measured as the rise in corticosterone concentrations following capture was positively related to renal cadmium in 1998 when incubating eiders were sampled, but not in 1999 when prenesting eiders were sampled (Wayland et al., 2002). Feces of the red-footed booby, Sula sula, is an important vector of trace metal flux in the case of cadmium and other metals, including zinc, copper, and mercury (Liu et al., 2006).
Birds
269
Adult mallards, A. platyrhynchos, fed diets containing up to 200.0 mg Cd/kg for 90 days all survived, with no loss in body weight. After 90 days, liver contained 109.6 mg Cd/kg fresh weight and kidney 134.2 mg Cd/kg fresh weight (White and Finley, 1978). Eggs from laying hens had low cadmium burdens; however, egg production was suppressed in the group fed 200.0 mg/kg diet (White and Finley, 1978). Mallard ducklings fed only 20.0 mg Cd/kg diet for 12 weeks contained 43.0 mg Cd/kg liver (Cain et al., 1983).
5.10 Cesium Livers of the gray heron, A. cinerea, from a Japanese estuary contained between 0.05 and 1.8 mg Cs/kg dry weight (Horai et al., 2007). Following the Chernobyl nuclear reactor accident in April 1986 (Eisler, 1995, 2003), 137 Cs and 134Cs levels in eggs and eggshells of the black-headed gull, Larus ridibundus ridibundus, increased by factors of at least 4 (Lowe and Horrill, 1991). Oystercatchers, Haematopus ostralegus, collected near a nuclear facility, when compared to conspecifics from a reference site, had 28 times more 137Cs in muscle and 28 times more 137Cs in liver (Lowe, 1991). No radiocesium-137 was found in muscle and bone of four species of seabirds from the Aleutian Islands in summer 2004, including Amchitka, the site of underground nuclear tests from 1965 to 1971 (Burger and Gochfeld, 2007).
5.11 Chromium The maximum chromium concentrations in field collections of avian tissues examined were 4.3 mg/kg dry weight in liver, 26.3 mg/kg dry weight in feathers, and 0.91 mg/kg fresh weight in egg contents (Table 5.3). Investigators agree that chromium does not biomagnify in marine food chains involving birds or mammals (Eisler, 2000b; Outridge and Scheuhammer, 1993b). Waterfowl from areas contaminated by mining wastes and subsequently consumed diets rich in chromium had elevated chromium concentrations in tissues, especially in gonads, gallbladder, and pancreas (Van Eeden and Schoonbee, 1992). Young American black ducks (Anas rubripes) absorbed anionic chromium species more readily than cationic forms from the intestines, a strong indication that ionic chromium state should be considered when planning avian dietary toxicity studies (Eastin et al., 1980). In another study with black ducks, adults were fed diets containing 0.0, 20.0, or 100.0 mg/kg anionic Cr3þ and ducklings from these pairs were fed the same diets for 7 days; tests of avoidance responses of the ducklings to a fright stimulus showed that the chromium had no significant effect on their behavior (Heinz and Haseltine, 1981).
270 Chapter 5 Table 5.3: Chromium and Cobalt Concentrations in Field Collections of Birds Element and Organism
Concentration
a
Reference
Chromium Alaska; Prince William Sound; 2004; breast feathers Black oystercatcher, Haematopus bachmani Black-legged kittiwake, Rissa tridactyla; oiled vs. nonoiled
2.03 DW
17
2.0-2.1 DW vs. 0.95 DW
17
Black duck, Anas rubripes; egg
0.64 FW
1
Arctic region seabirds; Barents Sea; May 1999; muscle Dovekie, Alle alle Black guillemot, Cepphus grylle
0.05 FW 0.06 FW
15 15
Arctic region seabirds; Baffin Bay, Canada; May-June 1998; muscle vs. liver Dovekie Black-legged kittiwake, Rissa tridactyla Thick-billed murre, Uria lomvia Black guillemot Northern fulmar, Fulmaris glacialis
0.15 FW vs. 0.08 FW 0.07 FW vs. 0.06 FW 1.1 FW vs. 0.19 FW 0.06 FW vs. 0.07 FW 0.07 FW vs. 0.06 FW
15 15 15 15 15
Gray heron, Ardea cinerea; Kanto area; Japan Liver Kidney Muscle Lung Brain
0.39 DW 0.30 DW 0.24 DW 0.39 DW; max. 1.4 DW 0.27 DW
14 14 14 14 14
Canvasback, Aythya valisineria; liver
0.2 FW
Pigeon guillemot, Cepphus columba; feather; Alaska; summer 2004 Prince William Sound Amchitka Kiska
1.33 DW 0.80 DW 2.69 DW
12 12 12
Little egret, Egretta garzetta; Pearl River Delta, China; industrialized area; May 2000 Egg contents Chick feather
0.10 (0.03-0.15) DW 0.55 (0.15-11.1) DW
10 10
2
(Continues)
Birds Table 5.3:
Cont’d
Element and Organism
Concentration
Little penguin, Eudyptula minor; Victoria, Australia; 2005; found dead Muscle Liver
0.42 FW; max. 3.77 FW 0.13 FW; max. 0.82 FW
9 9
Herring gull, Larus argentatus; egg contents; Long Island, New York 1989 vs. 1991 1992 vs. 1993 1994
0.22 DW vs. 0.35 DW 0.34 DW vs. 0.91 DW 0.23 DW
6 6 6
<1.0 DW
3
Lesser black-backed gull, Larus fuscus; all tissues Black-crowned night-heron, Nycticorax nycticorax; 1998-1999; nestlings; feathers Baltimore Harbor, Maryland Holland Island, Maryland Pea Patch Island, Delaware Osprey, Pandion haliaetus Liver Nestlings; Chesapeake Bay, Maryland, 2000-2001 vs. Delaware Bay, Delaware, 2002; max. values Blood Feathers Seabirds; Spain; liver; 2002-2003; dead or moribund after oil spill Seabirds; Atlantic Ocean; Canada; 1988; breeding season; liver Herring gull, Larus argentatus Atlantic puffin, Fratercula arctica Leach’s storm petrel, Oceanodroma leucorhoa Double-crested cormorant, Phalacrocorax auritus Shorebirds; Delaware Bay; Delaware and New Jersey; breast feathers Sanderling, Calidris alba; 1991-1992 Red breast, Calidris canutus; 1991-1992 Semipalmated sandpiper; Calidris pusilus; 1991 vs. 1992
271
3.3 (2.4-4.5) DW 3.2 (1.6-6.1) DW 2.5 (1.3-4.8) DW 0.004-0.20 FW
Reference
a
19 19 19 4 4
1.4 DW vs. 1.3 DW 6.7 DW vs. 4.3 DW
16 16
0.01-0.1 (0.001-0.44) DW
13
1.0-1.2 DW 1.5-4.3 DW 1.6-3.5 DW
7 7 7
0.9-3.6 DW
7
16.5 DW 24.1 DW 26.3 DW vs. 14.5 DW
5 5 5 (Continues)
272 Chapter 5 Table 5.3:
Cont’d a
Element and Organism
Concentration
Shorebirds; New Guinea; 5 spp.; feathers
7.8-20.8 DW
8
<1.0 DW
3
1.8 DW 0.41 DW
18 18
Common eider, Somateria mollissima All tissues Aleutian Islands, Alaska; summer 2007; females Feathers Eggs Roseate tern, Sterna dougalli; Long Island, New York; 1992; eggshell vs. egg contents
1.6 DW vs. 2.7 DW
Reference
9
Cobalt Antarctica; molting feathers; 2002 vs. 2003 Chinstrap penguin, Pygoscelis antarctica Gentoo penguin, Pygoscelis papua
0.17 DW vs. 0.19 DW 0.25 DW vs. 0.25 DW
11 11
Arctic region seabirds; Barents Sea; May 1999; muscle Dovekie, Alle alle Thick-billed murre, Uria lomvia Black guillemot, Cepphus grylle
0.021 FW 0.013 FW 0.016 FW
15 15 15
Arctic region seabirds; Baffin Bay, Canadian Arctic; May-June 1998; muscle vs. liver Dovekie Black-legged kittiwake, Rissa tridactyla Thick-billed murre Black guillemot Northern fulmar, Fulmaris glacialis Thayer’s gull, Larus thayeri
0.021 FW vs. 0.07 FW 0.014 FW vs. 0.034 FW 0.023 FW vs. 0.044 FW 0.02 FW vs. 0.03 FW 0.01 FW vs. 0.028 FW 0.015 FW vs. 0.052 FW
15 15 15 15 15 15
Gray heron, Ardea cinerea; Japan; liver
0.08 (0.04-0.20) DW
14
Values are in mg element/kg fresh weight (FW) or dry weight (DW). a 1, Haseltine et al., 1980; 2, White et al., 1979; 3, Lande, 1977; 4, Wiemeyer et al., 1980; 5, Burger et al., 1993b; 6, Burger and Gochfeld, 1995; 7, Elliott et al., 1992; 8, Burger et al., 1993a; 9, Choong et al., 2007; 10, Zhang et al., 2006; 11, Metcheva et al., 2006; 12, Burger et al., 2007; 13, Perez-Lopez et al., 2006; 14, Horai et al., 2007; 15, Borga et al., 2006; 16, Rattner et al., 2008; 17, Burger et al., 2008; 18, Burger et al., 2008a; 19, Custer et al., 2008.
Birds
273
5.12 Cobalt Cobalt concentrations in avian tissues never exceeded 0.25 mg Co/kg DW or 0.052 mg/kg FW (Table 5.3). Whole shorebirds from Eniwetok Atoll in 1964, when compared to whole seabirds from the same collection area at the same time had 14 times more 60Co (Welander, 1969), and probably reflects dietary loadings of this isotope. No 60Co was found in bone or breast muscle of four species of seabirds from the Aleutian Islands in summer 2004 regardless of species or location, including Amchitka, the site of underground nuclear tests between 1965 and 1971 (Burger and Gochfeld, 2007).
5.13 Copper In general, marine birds retain a very small portion of copper and other metals ingested (Bryan and Langston, 1992). Wastes from human activities contribute significantly to avian tissue burdens of copper, but damage effects, if any, are unknown. One exception is the case of mute swans (Cygnus olor) collected from estuaries in Britain. These swans had more than 2000.0 mg Cu/kg DW in their blackened livers; blackening was attributed to ingestion of flakes of copper-based antifouling paints (Bryan and Langston, 1992). Copper concentrations in stomach contents of willets (C. semipalmatus) from San Diego Bay tend to reflect sediment copper concentrations (Hui and Beyer, 1998). However, there is no evidence of copper biomagnification in the sediment-pondweed food chain of the red-knobbed coot, Fulica cristata (Van Eeden and Schoonbee, 1992). Other elevated concentrations of copper reported include 367.0 mg/kg dry weight in liver of the common eider, Somateria mollissima, and 446.3 mg/kg fresh weight in liver of juvenile shearwaters, Puffinus spp. (Table 5.4). Copper burdens up to 4970.0 mg/kg DW in livers of gray herons, A. cinerea, from an industrialized area of Japan is probably through ingestion of copper-contaminated sediments (Horai et al., 2007). The comparatively high copper residues in immature ospreys, P. haliaetus, from Maryland (Table 5.4) are difficult to interpret. Immature ospreys from other areas were collected in autumn while those from Maryland were collected in mid-summer, suggesting that the period near fledging is associated with high copper need and subsequent uptake by this species. Copper concentrations in tissues of coastal seabirds tend to decrease with increasing age (Eisler, 1984). In New Zealand, younger marine birds have higher concentrations of copper in livers than adults (Lock et al., 1992), but juveniles and adults of common murres, Uria aalge, from Scotland have similar concentrations of copper in kidney, liver, and muscle (Stewart et al., 1994). Copper and zinc concentrations are positively correlated in kidneys and liver of common murres (Stewart et al., 1994), and this may account for low copper burdens in juveniles. Migratory blue-winged teal, A. discors, has highest copper burdens in liver during autumn and lowest in the spring (Fedynich et al., 2007).
274 Chapter 5 Table 5.4: Copper Concentrations in Field Collections of Birds Organism
Concentration
Reference
Western grebe, Aechmophorus occidentalis; Puget Sound, Washington; 1985-1986 Liver Diet (fish muscle)
12.7-17.6 DW 0.3-0.5 FW
10 10
Blue-winged teal, Anas discors; liver; 1998-1999; southern Texas
49.2 (8.1-227.3) FW
26
Black duck, Anas rubripes; Atlantic flyway; egg
1.7 FW
Antarctica; February-March 1989 Blue-eyed cormorant, Phalacrocorax atriceps; muscle Southern giant petrel, Macronectes giganteous; muscle Adelie penguin, Pygoscelis adeliae Liver Muscle Chinstrap penguin, Pygoscelis antarctica Feces Liver Muscle Gentoo penguin, Pygoscelis papua Liver Muscle
a
1
10.0 DW
11
7.2 DW
11
11.9 (11.0-12.6) DW 7.9 (6.5-8.5) DW
11 11
37.6 (35.1-49.0) DW 12.6 (12.0-13.0) DW 9.7 (9.5-10.1) DW
11 11 11
26.5 (24.0-27.6) DW 8.2 (7.7-8.9) DW
11 11
Antarctica; molting feathers; 2002 vs. 2003 Gentoo penguin Chinstrap penguin
17.0 DW vs. 16.0 DW 19.0 DW vs. 18.0 DW
21 21
Arctic region seabirds; Barents Sea; May 1999; muscle Dovekie, Alle alle Thick-billed murre, Uria lomvia Black guillemot, Cepphus grylle
7.5 FW 5.6 FW 7.3 FW
33 33 33
Arctic region seabirds; Baffin Bay; May-June 1998; muscle vs. liver Dovekie Black-legged kittiwake, Rissa tridactyla Thick-billed murre Black guillemot
6.9 FW 5.7 FW 5.2 FW 6.9 FW
vs. vs. vs. vs.
8.2 FW 6.0 FW 7.1 FW 8.1 FW
33 33 33 33 (Continues)
Birds Table 5.4: Organism Northern fulmar, Fulmaris glacialis Thayer’s gull, Larus thayeri
Cont’d
Concentration
Reference
5.3 FW vs. 6.2 FW 5.3 FW vs. 7.3 FW
33 33
Gray heron, Ardea cinerea; Kanto area, Japan Liver Kidney Muscle Lung Brain
791.0 DW; max. 4970.0 DW 46.1 DW; max. 217.0 DW 49.3 DW; max. 95.9 DW 18.2 DW; max. 79.3 DW 34.2 DW; max. 41.7 DW
23 23 23 23 23
Greater scaup, Aythya marila; liver
17.2-19.6 FW
2
Canvasback, Aythya valisineria; liver
59.0 FW
3
Canada; Pacific Northwest; 1989-1994; adults; various sites White-winged scoter, Melanitta fusca; males vs. females Kidney Liver Surf scoter, Melanitta perspicillata Kidney Liver; males vs. females Canadian Arctic; June 1997; liver Common eider, Somateria mollissima; females King eider, Somateria spectabilis; males vs. females Willet, Catoptrophorus semipalmatus; San Diego Bay; 1994; sediment vs. stomach contents Naval Air Station Tijuana Slough National Wildlife Refuge Diving ducks; Baltic Sea; bone vs. cartilage; 2000-2004 Scaup, Aythya marila Pochard, Aythya ferina
275
31.3-36.0 FW vs. 37.7-48.4 FW 93.0 FW vs. 47.8 FW
30 30
20.6-33.9 FW 61.8-66.4 FW vs. 31.6-84.1 FW
30 30
109.3 (12.5-805.4) DW
33
224.5 (86.9-580.0) DW vs. 86.7 (56.6-152.9) DW
33
3.0 DW vs. 17.0 DW 12.0 DW vs. 34.0 DW
12 12
0.23 (0.07-0.53) DW vs. 2.1 (0.4-8.9) DW 0.29 (0.1-0.6) DW vs. 4.0 (1.2-8.7) DW
24
a
24 (Continues)
276 Chapter 5 Table 5.4: Organism Diving ducks; coastal California; December 1986-March 1987; liver; early winter Canvasback, Aythya valisineria Adult males Adult females Juvenile males Juvenile females Greater scaup, Aythya marila Adult males Adult females Lesser scaup, Aythya affinis Adult males Juvenile males
Cont’d
Concentration
Reference
189.0 (67.4-765.0) DW 254.9 (171.0-380.0) DW 120.9 (9.0-833.0) DW 33.1 (9.6-114.0) DW
29 29 29 29
95.9 (94.5-97.5) DW 80.3 (71.7-90.0) DW
29 29
48.6 (37.1-105.0) DW 63.1 (48.9-81.6) DW
29 29
Little penguin, Eudyptula minor; Victoria, Australia; 2005; found dead Muscle Liver
2.8 FW; max. 3.5 FW 5.9 FW; max. 10.7 FW
20 20
Korea; 2001; chicks; black-crowned night heron Nycticorax nycticorax vs. gray heron, Ardea cinerea Liver Kidney Muscle Bone Feather
55.5 FW vs. 33.9 FW 10.9 FW vs. 10.8 FW 14.2 FW vs. 5.9 FW 4.7 FW vs. 2.0 FW 9.9 FW vs. 30.2 FW
36 36 36 36 36
Herring gull, Larus argentatus; egg
0.65-0.69 FW
Lesser black-backed gull, Larus fuscus Muscle Liver Kidney Egg
14.0 DW 17.0 DW 14.0 DW 1.0 FW
6 6 6 13
Surf scoter, Melanitta perspicillata Liver Liver; San Francisco Bay; 1985; January vs. March Liver; British Columbia; 1998-2001
10.4-10.9 FW 37.8 (29.3-47.0) DW vs. 50.1 (41.3-58.3) DW 35.5-59.7 (16.6-94.9) DW
2 14 27
Black-crowned night-heron, Nycticorax nycticorax; 1998-1999; nestlings; feathers Baltimore Harbor, Maryland
6.1 (4.6-8.0) DW
38
a
5
(Continues)
Birds Table 5.4: Organism Holland Island, Maryland Pea Patch Island, Delaware Osprey, Pandion haliaetus Kidney Liver; immatures and nestlings vs. adults Maryland Other East coast areas Nestlings; Chesapeake Bay 2000-2001 vs. Delaware Bay 2002; max. values Blood Feathers
Cont’d
Concentration 7.9 (6.7-9.3) DW 6.6 (5.6-7.8) DW
Reference
a
38 38
3.3-6.9 FW
7
141.0 FW vs. 3.0 FW 4.0 FW vs. 4.2 FW
7 7
2.0 DW vs. 2.1 DW 19.2 DW vs. 9.8 DW
34 34
Brown pelican, Pelecanus occidentalis Liver Egg
4.3-9.0 FW (0.7-1.3) FW
8 13
Clapper rail, Rallus longirostris; eggshell; Georgia; 2000 Metals-contaminated marsh Reference site
1.7 (0.8-3.3) DW 1.4 (0.3-2.6) DW
39 39
Seabirds; Canadian Arctic; 1991-1993; 5 spp.; kidney
16.0-27.0 (13.4-33.2) DW
37
Seabirds; 3 spp.; Spain; 2002-2003; liver
0.99-1.54 (0.26-4.1) DW
22
Seabirds; 19 spp.; North Pacific Ocean; 1982-1987 Kidney Liver Muscle
4.7 FW 5.9 FW; max. 7.7 FW 5.1 FW
15 15 15
Means 14.0-64.0 DW
16
<1.0 DW 1.0-5.0 DW
16 16
7.0-10.0 DW
16
11.0-15.0 DW
16
Seabirds; 14 spp. Liver; 11 spp. 3 spp. Bone, fat Lung, pancreas, spleen, gonads, uropygial gland, skin, eyeball Brain, heart, stomach, intestine, muscle Liver, gall bladder, kidney
277
Seabirds; New Zealand; 1975-1983 Albatrosses; 8 spp.; adults vs. juveniles (Continues)
278 Chapter 5 Table 5.4: Organism Feather Liver Gulls, Larus spp.; adults vs. juveniles Feather Liver Penguins; 3 spp.; liver; adults vs. juveniles Petrels; 19 spp.; adults vs. juveniles Feather Liver Shearwaters; 3 spp. of Puffinus; liver; adults vs. juveniles Shorebirds; Chile; November 1981-March 1982; near abandoned copper mine; liver vs. stomach contents Sanderling, Calidris alba Oystercatcher, Haematopus ostralegus Kelp gull, Larus dominicanus Gray gull, Larus modestus Franklin’s gull, Larus pipixcan Umbrel, Numenius phaeopus Shorebirds; 5 spp.; New Zealand estuaries; liver
Cont’d
Concentration
Reference
44.0 FW vs. 18.4-32.3 FW 5.0-8.6 FW vs. 12.2-225.3 FW
17 17
13.1-20.0 FW vs. 25.3-60.5 FW 5.0-6.6 FW vs. 23.8-35.0 FW 4.3-13.2 FW vs. 8.5-18.5 FW
17 17 17
14.0-40.0 FW vs. 20.0-79.0 FW 4.0-45.0 FW vs. 8.0-75.0 FW 6.4-7.2 FW vs. 4.6-446.3 FW
17 17 17
(9.2-11.5) FW vs. No data 8.0 (6.8-8.6) FW vs. (24.4-27.2) FW (3.8-6.3) FW vs. (0.8-3.4) FW 6.2 (4.0-7.4) FW vs. (30.0-46.7) FW (4.7-7.5) FW vs. No data (3.9-17.8) FW vs. (6.1-86.4) FW
18 18
2.8-28.9 FW
Shorebirds; 5 spp.; Korea; 1994-1995 Feathers Liver
4.1-10.4 (0.4-13.5) FW 3.5-8.6 (2.2-15.9) FW
Common eider, Somateria mollissima Muscle Liver Kidney Egg
13.0 DW 367.0 DW 43.0 DW 4.0 DW
Seabirds; 3 spp.; Reunion Island, western Indian Ocean; 2002-2004; juveniles vs. adults Barau’s petrel, Pterodroma baraui Liver Kidney
29.3 DW vs. 20.2 DW 11.7 DW vs. 19.5 DW
a
18 18 18 18 4
35 35 6 6 6 6
25 25 (Continues)
Birds Table 5.4: Organism Muscle Audubon’s shearwater, Puffinus lherminieri bailloni Liver Kidney Muscle White-tailed tropicbird, Phaethon lepturus Liver Kidney Muscle Northern gannet, Sula bassanus; liver; dead or dying birds Red-footed booby, Sula sula; South China Sea; 2003 Feces Wing bone Eggshell Feather Redshank, Tringa totanus; liver; feeding on sandworms (Nereis diversicolor) containing 500.0-1000.0 mg/kg Cu/kg DW Guillemot, Uria aalge; winters; Belgium; 1993-1998; normal vs. severely emaciated Liver Kidney Muscle
279
Cont’d
Concentration
Reference
143.0 DW vs. 27.2 DW
25
11.1 DW vs. 16.5 DW 8.6 DW vs. 15.4 DW 12.7 DW vs. 21.0 DW
25 25 25
31.5 DW vs. 29.3 DW 17.0 DW vs. 24.2 DW 18.3 DW vs. 28.1 DW
25 25 25
9.0-47.0 DW
a
9
21.1 (16.5-25.4) DW 3.0 DW 3.0 DW 4.0 DW
32 32 32 32
30.0 DW
19
48.9 DW vs. 69.4 DW 21.7 DW vs. 45.8 DW 19.5 DW vs. 19.8 DW
28 28 28
Values are in mg Cu/kg fresh weight (FW) or dry weight (DW). a 1, Haseltine et al., 1980; 2, Vermeer and Peakall, 1979; 3, White et al., 1979; 4, Turner et al., 1978; 5, Peden et al., 1973; 6, Lande, 1977; 7, Wiemeyer et al., 1980; 8, Blus et al., 1977; 9, Parslow et al., 1973; 10, Henny et al., 1990; 11, Szefer et al., 1993; 12, Hui and Beyer, 1998; 13, Jenkins, 1980; 14, Ohlendorf et al., 1991; 15,Honda et al., 1990; 16, Kim et al., 1998; 17, Lock et al., 1992; 18, Vermeer and Castilla, 1991; 19, Bryan and Langston, 1992; 20, Choong et al., 2007; 21, Metcheva et al., 2006; 22, Perez-Lopez et al., 2006; 23, Horai et al., 2007; 24, Kalisinska et al., 2007; 25, Kojadinovic et al., 2007a; 26, Fedynich et al., 2007; 27, Elliott et al., 2007; 28, Debacker et al., 2000; 29, Takekawa et al., 2002; 30, Barjaktarovic et al., 2002; 31, Wayland et al., 2001; 32, Liu et al., 2006; 33, Borga et al., 2006; 34, Rattner et al., 2008; 35, Kim and Koo, 2008b; 36, Kim and Koo, 2008a; 37, Braune and Scheuhammer, 2008; 38, Custer et al., 2008; 39, Rodriguez-Navarro et al., 2002.
280 Chapter 5 Emaciation linked to starvation in overwintering guillemots, U. aalge, was associated with increased concentrations of trace metals—including copper—in liver and kidney (Table 5.4). These excesses could represent an additional stress to birds already facing stressful conditions. Study of metal speciation in relation to body condition should provide more information on the potential toxicity of these elevated body burdens (Debacker et al., 2000). Laboratory studies with adult mallards, A. platyrhynchos, given a choice of drinking water containing zero (distilled water), 30.0, 60.0, or 100.0 mg Cu/L, consumed significantly more water containing 100.0 mg Cu/L than distilled water with no preference evident at lower concentrations (Rowe and Prince, 1983). This finding merits verification.
5.14 Europium Breast muscle and bone from four species of seabirds collected in the Aleutian Islands during summer 2004 had no measurable levels of 152Eu regardless of species or location— including Amchitka Island, the site of underground nuclear tests between 1965 and 1971 (Burger and Gochfeld, 2007).
5.15 Gallium Liver from gray heron, A. cinerea, collected in Japan had up to 0.21 mg Ga/kg dry weight (Horai et al., 2007). Gallium concentrations in muscle of six species of Arctic region seabirds analyzed in 1998-1999 did not exceed 0.024 mg Ga/kg FW; for liver, it was 0.017 mg Ga/kg FW (Borga et al., 2006).
5.16 Indium A maximum concentration of 0.06 mg In/kg dry weight liver was measured in gray heron, A. cinerea, from a contaminated Japanese estuary (Horai et al., 2007).
5.17 Iron Iron concentrations in excess of 2000.0 mg Fe/kg dry weight were measured in livers of gray heron, A. cinerea, Barau’s petrel, Pterodroma baraui, white-tailed tropicbird, Phaethon lepturus, common eider, S. mollissima, and guillemot, U. aalge and in blood of nestling ospreys, P. haliaetus (Table 5.5). Concentrations of iron in various tissues of Somateria and Larus ranged from 128.0 to 2904.0 mg Fe/kg dry weight, with highest values in liver, kidney, muscle, and egg, in that order (Table 5.5). On a fresh weight basis, maximum iron concentrations in muscle and liver of the little penguin, Eudyptula minor, were 300.0 and 1300.0 mg/kg, respectively (Table 5.5).
Birds
281
Table 5.5: Iron Concentrations in Field Collections of Birds a
Organism
Concentration
Admiralty Bay, Antarctica; January 2004 Adelie penguin, Pygoscelis adeliae Egg Feather Kelp gull, Larus dominicanus; feather
Not detectable 87.0-434.0 DW 291.0 DW
2 2 2
56.0 DW vs. 46.0 DW
4
53.0 DW vs. 42.0 DW
4
1190.0 (539.0-2170.0) DW
5
22.5 (10.9-46.0) DW vs. 76.5 (19.1-208.1) DW 28.3 (9.4-70.6) DW vs. 126.8 (52.6-292.0) DW
6
Little penguin, Eudyptula minor; 2005; Victoria, Australia; found dead Muscle Liver
170.0 FW; max. 300.0 FW 554.0 FW; max. 1300.0 FW
3 3
Korea; 2001; chicks; black-crowned night heron, Nycticorax nycticorax vs. gray heron, Ardea cinerea Liver Kidney Muscle Bone Feather
251.0 FW vs. 250.0 FW 70.0 FW vs. 55.7 FW 55.8 FW vs. 56.9 FW 32.3 FW vs. 28.1 FW 45.8 FW vs. 155.0 FW
Lesser black-backed gull, Larus fuscus Muscle Liver Kidney
229.0 DW 1367.0 DW 476.0 DW
Black-crowned night-heron, Nycticorax nycticorax; 1998-1999; nestlings; feathers Baltimore Harbor, Maryland Holland Island, Maryland Pea Patch Island, Delaware
36.4 (23.5-56.5) DW 63.3 (48.4-82.8) DW 154.4 (93.1-255.9) DW
Antarctica; molting feathers; 2002 vs. 2003 Gentoo penguin, Pygoscelis papua Chinstrap penguin, Pygoscelis antarctica Gray heron, Ardea cinerea; Kanto area; Japan; liver Diving ducks; Baltic Sea; 2000-2004; bone (tarsometatarsus vs. tracheal cartilage) Scaup, Aythya marila Pochard, Aythya ferina
Reference
6
10 10 10 10 10 1 1 1
11 11 11 (Continues)
282 Chapter 5 Table 5.5:
Cont’d
Organism
Concentration
Osprey, Pandion haliaetus; nestlings; Chesapeake Bay, Maryland vs. Delaware Bay, Delaware; 2000-2002; max. values Blood Feathers
2170.0 DW vs. 2290.0 DW 703.0 DW vs. 372.0 DW
Clapper rail, Rallus longirostris; eggshell; Georgia; 2002 Metals-contaminated marsh Reference site
147.0 (77.0-286.0) DW 159.0 (89.0-330.0) DW
Seabirds; 3 spp.; Reunion Island, western Indian Ocean; 2002-2004; juveniles vs. adults Barau’s petrel, Pterodroma baraui Liver Kidney Muscle Audubon’s shearwater, Puffinus lherminieri bailloni Liver Kidney Muscle White-tailed tropicbird, Phaethon lepturus Liver Kidney Muscle Common eider, Somateria mollissima Muscle Liver Egg
262.0 DW 2904.0 DW 128.0 DW
Guillemot, Uria aalge; Belgium; winters; 1993-1998; normal vs. severely emaciated Liver Kidney Muscle
2580.0 DW vs. 4411.0 DW 744.0 DW vs. 670.0 DW 689.0 DW vs. 11,063.0 DW
Reference
a
9 9
12 12
1240.0 DW vs. 2620.0 DW 327.0 DW vs. 526.0 DW 201.0 DW vs. 440.0 DW
7 7 7
1350.0 DW vs. 1540.0 DW 538.0 DW vs. 499.0 DW 206.0 DW vs. 365.0 DW
7 7 7
4050.0 DW vs. 2320.0 DW 524.0 DW vs. 539.0 DW 337.0 DW vs. 367.0 DW
7 7 7 1 1 1
8 8 8
Values are in mg Fe/kg fresh weight (FW) or dry weight (DW). a 1, Lande, 1977; 2, Santos et al., 2006; 3, Choong et al., 2007; 4, Metcheva et al., 2006; 5, Horai et al., 2007; 6, Kalisinska et al., 2007; 7, Kojadinovic et al., 2007a; 8, Debacker et al., 2000; 9, Rattner et al., 2008; 10, Kim and Koo, 2008a; 11, Custer et al., 2008; 12, Rodriguez-Navarro et al., 2002.
Birds
283
5.18 Lanthanum Lanthanum concentrations in liver of Arctic region seabirds captured in May-June 1998 from Baffin Bay, Canada, usually contained 0.001-0.002 mg La/kg FW; however, liver of Thayer’s gull, Larus thayeri, contained 0.006 mg La/kg FW (Borga et al., 2006).
5.19 Lead Waterfowl deaths from the ingestion of spent lead shot pellets from shotgun shells were discovered more than 100 years ago in Italy and the United States; since then, lead poisoning of waterfowl has occurred in 20 countries (Pain et al., 1995). In North America alone, about 3000 tons of lead shot are expended annually into lakes, marshes, and estuaries by several million waterfowl hunters (USFWS, 1986, 1987). Spent pellets are eaten by waterfowl and other birds because they mistake them for seeds or for pieces of grit. These pellets may be retained in the gizzard for weeks, where they are reduced chemically and mechanically to form toxic soluble salts, and cause characteristic signs of lead intoxication, especially lethargy and emaciation (Street, 1983). At least 2% of all North American waterfowl—or about 2 million ducks, geese, and swans (Lumeij, 1985)—die each year as a direct result of ingesting lead shot (Bellrose, 1951). These deaths contribute to the decline of some species, such as the canvasback, Aythya valisineria (Dieter, 1979), pintail, Anas acuta (Mateo et al., 1997b; White and Stendell, 1977), black duck, A. rubripes (Pain and Rattner, 1988), common pochard, Aythya ferina (Mateo et al., 1997b), spectacled eider, Somateria fischeri (Flint et al., 1997), graylag goose, Anser anser (Mateo et al., 1998), and mute swan, C. olor (Blus, 1994; O’Halloran et al., 1988). Up to seven times more waterfowl died from lead toxicosis as a result of ingesting spent lead pellets than from wounding by hunters (Zwank et al., 1985). In addition, lead-poisoned waterfowl show delayed mortality from lead-induced starvation, are readily captured by predators, are susceptible to disease, and reproduce poorly (Dieter, 1979). Susceptibility is markedly influenced by species, by the number and size of shot ingested, and by the types of foods eaten (White and Stendell, 1977). Swans are among the more vulnerable waterfowl. In England, lead poisoning through the ingestion of discarded lead fishing sinkers was the major cause of death in the mute swan (Birkhead, 1983). In Washington State, USA, 30% of the endangered trumpeter swans (Cygnus buccinator) found dead had died of lead poisoning from ingesting lead shot (Blus, 1994; Kendall and Driver, 1982; Lagerquist et al., 1994). Fatal lead poisoning of swans through ingestion of shotgun pellets, fishing sinkers, and lead-contaminated sediments is reported in several geographic locations (Beyer et al., 1998a; Blus et al., 1989, 1991; Degernes, 1991; Koh and Harper, 1988; Lesher, 1991; Sears, 1988; Spray and Milne, 1988). Shot densities of more than 2.6 million shot/ha were estimated for the Ebro Delta, Spain in 1992-1993 (Mateo et al., 1997b). In 1991-1992, as many as 27% of the mallards
284 Chapter 5 (A. platyrhynchos) at the Ebro Delta had tissue lead concentrations sufficiently elevated to qualify as clinically lead-poisoned, that is, more than 1.5 mg Pb/kg fresh weight liver or more than 3.0 mg Pb/kg fresh weight kidney (Guitart et al., 1994). Shot ingestion in waterfowl is higher where shot densities in sediments are high and grit is absent (Pain, 1996), and higher during spring than in autumn for diving ducks (Havera et al., 1992). Incidence of ingested shot in five species of waterfowl in Yucatan, Mexico in 1986-1988 was 10.3% (Thompson et al., 1989); the incidence was much higher in hunter-shot waterfowl in Japan and Europe, ranging from >22% to almost 100% (Lumeij and Scholten, 1989; Mateo et al., 1998; Ochiai et al., 1993a; Pain and Handrinos, 1990). Crop stasis in birds, which is characterized by paralysis of the alimentary tract, impaction of food in the gizzard and proventriculus, and regurgitation of crop fluid, has been produced by lead shot or lead acetate solutions. Lead induces crop dysfunction by acting either directly on the smooth muscle or on associated nerve plexuses of crop tissues, depending on route of administration (Boyer and Di Stefano, 1985; Boyer et al., 1985; Clemens et al., 1975). Beyer et al. (1998c) aver that the most reliable indicators of lead poisoning in waterfowl include impaction of the upper alimentary tract, submandibular edema, myocardial necrosis, biliary discoloration of the liver, and hepatic lead concentrations of at least 30.0 mg/kg dry weight or 10.0 mg/kg fresh weight. Thousands of wing bones from seven species of ducks collected in 1972 and 1973 contained from <0.5 to 361.0 mg Pb/kg dry weight. This range reflected the history of exposure to lead from ingested shotshell pellets and other sources (Stendell et al., 1979). Highest lead concentrations were in wing bones of mottled ducks, Anas fulvigula and lowest in lesser scaup A. affinis. Intermediate values were measured in redheads, black ducks, mallards, canvasbacks, and pintails. Adults contained higher lead concentrations in bone than did immatures (Stendell et al., 1979). Elevated lead burdens were also observed in bone of coastal birds collected from New Zealand estuaries (Table 5.6) and is consistent with the reports of other investigators who found comparatively high lead burdens in bone of marine fishes and mammals. Abnormally high lead concentrations—up to 630.0 mg Pb/kg fresh weight—were also observed in blood of canvasbacks from Chesapeake Bay, Maryland; this concentration was associated with at least a 50% reduction in delta-amino-levulinic acid dehydrogenase (ALAD) activity (Dieter et al., 1976). It is probable that these elevated blood lead concentrations were a direct result of ingested lead shot, as was evident for mallards and other species of waterfowl (Finley et al., 1976; Stendell et al., 1979). The findings of Bellrose (1951) show that about 8% of mallards trapped contained ingested lead shot; moreover, tagged ducks fed ingested lead shot were captured in significantly greater numbers than controls. The organolead mode of action is poorly understood; however, they are known to inhibit amino acid transport, uncouple oxidative phosphorylation, and inhibit glucose metabolism
Birds
285
Table 5.6: Lead Concentrations in Field Collections of Birds Organism Alaska; eiders; 1992-1994; found dead or moribund Spectacled eider, Somateria fischeri Blood Liver Common eider, Somateria mollissima; liver Alaska; Prince William Sound; 2004; breast feathers Black oystercatcher, Haematopus bachmani Black-legged kittiwake, Rissa tridactyla; oiled vs. nonoiled Aleutian Islands; summer 2004; egg contents Common eider, Somateria mollissima Glaucous-winged gull, Larus glaucescens Blue-winged teal, Anas discors; liver; 1998-1999; southern Texas Mallard, Anas platyrhynchos Virginia; 1986; lead-poisoned from ingested skeet shot; liver Ebro Delta; Spain; 1991-1992; from lead shot areas containing 60,000-544,750 shot pellets/ha Bone Brain Kidney Liver Pancreas Spleen California; August 1987; National Wildlife Refuges; blood 69% (background) 12% (elevated) 19% (toxic)
Concentration
Reference
81.5 FW 26.0-38.0 FW 52.0 FW
11 11 11
1.25 DW
48
1.1-1.4 DW vs. 0.71 DW
48
0.211 DW
35
0.016 DW
35
0.12 (0.01-1.8) FW
41
21.0 FW
12
42.0 (8.0-211.0) FW 1.0 (0.1-117.0) FW 1.0 (0.05-30.0) FW 0.8 (0.06-22.0) FW 3.0 (1.0-14.0) FW 1.0 (0.1-2.0) FW
13 13 13 13 13 13
<0.2 FW 0.2-0.5 FW >0.5 FW
14 14 14
a
(Continues)
286 Chapter 5 Table 5.6: Organism Antarctica; molting feathers; 2002 vs. 2003 Gentoo penguin, Pygoscelis papua Chinstrap penguin, Pygoscelis antarctica
Cont’d
Concentration
a
Reference
1.7 DW vs. 1.7 DW 1.8 DW vs. 1.7 DW
37 37
0.01-0.02 FW
43
Arctic region seabirds; 6 spp.; Baffin Bay, Canada; May-June 1988 Muscle Liver
0.001-0.09 FW 0.014-0.27 FW
43 43
Australia; Victoria; 1992; hunterkilled waterfowl; 3 spp. Bone Liver
22.0-39.0 (0.1-168.0) DW 8.0-25.0 (0.05-94.0) FW
15 15
Greater scaup, Aythya marila; British Columbia; Iona Island vs. Roberts Bank Liver Diet
1.3 FW vs. 0.35 FW 3.8-5.4 FW vs. 6.4 FW
1 1
0.059-0.064 FW vs. 0.263 FW
2
Arctic region seabirds; 3 spp.; Barents Sea; May 1999; muscle
Canvasback, Aythya valisineria Blood; Chesapeake Bay; normal vs. elevated (17%) Blood; Louisiana; 1991-1994; elevated (60%) Liver Wing bone
>0.2 FW 0.14-0.25 FW 7.8 DW
16 3 3
Pigeon guillemot, Cepphus columba; feather; Alaska; summer 2004 Prince William Sound Amchitka Kiska
1.02 DW 0.90 DW 1.72 DW
38 38 38
Mute swan, Cygnus olor Chesapeake Bay, Maryland; 1995; suspected of having ingested lead shot or sinkers vs. no evidence of lead intoxication Intestinal digesta Liver
36.0 DW vs. 1.6 (<1.5-6.4) DW 7.6 DW vs. 1.5 (<1.0-6.3) DW
17 17 (Continues)
Birds Table 5.6: Organism Ireland; found dead from lead poisoning Gizzard Heart Kidney Liver Muscle Pancreas Scotland; 1980-1996; died of lead poisoning Blood Kidney Laysan albatross, Diomedea immutabilis; chicks; Hawaii; 1994 Blood Liver Diving ducks; Baltic Sea; 2000-2004; found drowned in fishing nets; bone vs. cartilage Scaup, Aythya marila Pochard, Aythya ferina Little egret, Egretta garzetta; egg contents; China; 2000
287
Cont’d
Concentration
Reference
13.0 (6.0-85.0) FW 14.0 (6.0-730.0) FW 113.0 (40.0-350.0) FW 315.0 (93.0-450.0) FW 19.0 (8.0-273.0) FW 67.0 (20.0-155.0) FW
18 18 18 18 18 18
0.52 FW 662.0 DW
19 19
74% had >0.2 FW; max 26.7 FW 74% had >2.0 FW; max. 70.5 FW
20 20
8.5 (1.8-27.6) DW vs. 17.8 (2.5-76.8) DW 14.0 (1.7-56.2) DW vs. 27.1 (2.3-101.1) DW
40
a
40
0.06 (0.05-0.09) DW
36
Little penguin, Eudyptula minor; Victoria, Australia; 2005; found dead Muscle Liver
0.58 FW; max. 2.89 FW Not detectable
33 33
Korea; 2001; chicks; black-crowned night heron, Nycticorax nycticorax vs. gray heron, Ardea cinerea Liver Kidney Muscle Bone Feather
1.7 FW vs. 2.0 FW 0.08 FW vs. 0.03 FW 0.25 FW vs. 0.15 FW 0.11 FW vs. 0.61 FW 0.33 FW vs. 0.25 FW
46 46 46 46 46 (Continues)
288 Chapter 5 Table 5.6: Organism Herring gull, Larus argentatus Eggs; Long Island, New York 1989 1991-1993 1994 Feathers; fledglings; 1990 New York New York-New Jersey harbor New Jersey Virginia Laughing gull, Larus atricilla Downy young Brain Bone Heart Kidney Liver Muscle Prefledglings Brain Bone Heart Kidney Liver Muscle Adults Brain Bone Heart Kidney Liver Muscle Stomach contents Fish, 5 spp. Insects Common black-headed gull, Larus ridibundus; Mediterranean Sea coast of Italy Liver Muscle Kidney Brain
Cont’d
Concentration
a
Reference
2.5 DW 0.5-0.9 DW 0.4 DW
21 21 21
1.7-2.5 DW 1.8-3.5 DW 1.0-1.5 DW 1.6 DW
22 22 22 22
<0.01 FW 0.66 (0.24-1.04) FW <0.01 FW <0.01 FW 1.84 FW <0.01 FW
6 6 6 6 6 6
1.68 3.85 1.18 1.33 3.13 1.07
(0.96-3.19) FW (2.42-6.13) FW (0.32-2.16) FW (0.9-2.8) FW (2.2-4.5) FW (0.8-1.48) FW
6 6 6 6 6 6
1.61 6.93 1.08 2.10 5.31 0.78
(0.30-11.36) FW (1.61-20.11) FW (0.09-3.79) FW (<0.01-13.37) FW (0.33-13.81) FW (0.06-1.95) FW
6 6 6 6 6 6
1.46-4.91 FW 2.00 FW
6 6
2.0-18.3 FW 2.4-11.0 FW 1.5-40.0 FW 30.0 FW
7 7 7 7 (Continues)
Birds Table 5.6:
Cont’d
Organism
Concentration
Gull, Larus sp.; Irish Sea; egg
<0.001-0.16 FW
8
Surf scoter, Melanitta perspicillata; British Columbia; Iona Island vs. Roberts Bank Liver Diet
0.24 FW vs. 0.14 FW 3.8 FW vs. 0.3-2.6 FW
1 1
Mexico; Gulf of California; 1999-2000; muscle Brown pelican, Pelecanus occidentalis Cormorant, Phalacrocorax brasilianus Netherlands; 1991; found dead Gray heron, Ardea cinerea Bone Kidney Liver Common eider, Somateria mollissima Bone Kidney Liver Black-crowned night-heron, Nycticorax nycticorax; 1998-1999; nestlings; feathers Baltimore Harbor, Maryland Holland Island, Maryland Pea Patch Island, Delaware Osprey, Pandion haliaetus Liver Nestlings; Chesapeake Bay, 20002001 vs. Delaware Bay, 2002; max. values Blood Feathers Greater flamingo, Phoenicopterus ruber; Spain; liver 1991; gizzards with 18-37 ingested shot pellets; found dead 1992-1994; lead-poisoned
289
Reference
4.2 DW 1.7 DW
47 47
1.0 DW; max. 1.4 DW 1.0 (0.2-2.6) DW 1.4 (0.4-2.1) DW
23 23 23
3.0 (1.1-8.1) DW 0.7 (0.3-2.6) DW 0.7 (<0.1-4.9) DW
23 23 23
0.3 (0.2-0.6) DW 0.1 (0.07-0.18) DW 0.4 (0.2-0.8) DW
52 52 52
<0.06-0.41 FW
a
9
0.10 DW vs. 0.05 DW 8.1 DW vs. 5.9 DW
44 44
37.0-112.0 FW
24
192.0 (2.5-999.2) DW
25 (Continues)
290 Chapter 5 Table 5.6:
Cont’d a
Organism
Concentration
Caribbean flamingo, Phoenicopterus ruber ruber; Yucatan, Mexico; 1989; dead of lead poisoning; liver
313.0 DW
26, 27
Sora rail, Porzana carolina; no lead shot in gizzard vs. some lead shot in gizzard Liver Bone
<0.01-0.82 FW vs. 0.1-17.0 FW <0.4-42.0 DW vs. 0.8-127.0 DW
10 10
Clapper rail, Rallus longirostris; eggshell; Georgia; 2000 Metals-contaminated marsh Reference site
0.4 (0.08-2.0) DW 0.2 (0.1-0.5) DW
53 53
<0.1-0.26 DW
49
Max. 0.08 FW Max. 0.05 FW <0.02 FW 1.4-2.7 DW
28 28 28 29
0.3-6.7 DW vs. 0.8-4.1 DW
30
Max. 0.019 DW
39
(0.006-0.09) FW (0.01-0.46) FW
50 50
Seabirds Canadian Arctic; 1991-1993; 5 spp.; liver Greenland; 1978-1993; 4 spp. Kidney Liver Muscle Mid-Pacific Ocean; 1990; 5 spp.; adults; feather New York Bight; 1989; 5 spp.; eggs vs. fledgling feathers Spain; 3 spp.; 2002-2003; liver Sea ducks; breeding females; Canada; 2001-2003; blood King eider, Somateria spectabilis White-winged scoter, Melanitta fusca Shorebirds 5 spp; New Zealand estuaries; bone 7 spp; Corpus Christi, Texas; liver 5 spp.; Yeongjong Island, Korea; autumn migration; 1994-1995 Liver Kidney Muscle Bone Feathers
Reference
Means 0.12-451.9 AW; max. 1918.0 AW 0.05-28.5 FW
4
2.05-4.76 FW; max. 12.0 FW 4.87-27.9 FW; max. 44.5 FW 0.68-4.25 FW; max. 7.49 FW 5.1-21.2 FW; max. 42.7 FW 3.3-20.8 (0.02-41.6) FW
34 34 34 34 45
5
(Continues)
Birds Table 5.6:
Cont’d
Organism
Concentration
Common tern, Sterna hirundo Egg contents Feathers; males vs. females
0.09 FW 1.3 DW vs. 1.6 DW
31 31
Common eider, Somateria mollissima; summer 2007; Aleutian Islands, Alaska; females Feathers Eggs
0.53 DW 0.31 DW
51 51
Red-footed booby, Sula sula; South China Sea; 2003 Feces Wing bone Eggshell Feather
1.6 (0.9-3.7) DW 2.2 DW 3.2 DW 2.4 DW
42 42 42 42
11.0 FW 4.0 FW 0.3 FW
32 32 32
6.0 FW 5.0 FW <0.1 FW
32 32 32
6.0 FW 2.0 FW <0.1 FW
32 32 32
Texas; Galveston Bay; 1980-1981 Probers with lead shot in gizzards Bone Feather Liver Probers without lead shot in gizzards Bone Feather Liver Nonprobers Bone Feathers Liver
291
Reference
a
Values are in mg Pb/kg fresh weight (FW), dry weight (DW), or ash weight (AW). a 1, Vermeer and Peakall, 1979; 2, Dieter et al., 1976; 3, White et al., 1979; 4, Turner et al., 1978; 5, White et al., 1980; 6, Hulse et al., 1980; 7, Vannucchi et al., 1978; 8, Bernhard and Zattera, 1975; 9, Wiemeyer et al., 1980; 10, Stendell et al., 1980; 11, Franson et al., 1995a; 12, Schwab and Padgett, 1988; 13, Guitart et al., 1994a; 14, Mauser et al., 1990; 15. Norman et al., 1993; 16, Franson et al., 1996; 17, Beyer et al., 1998b; 18, O’Halloran et al., 1989; 19, Spray and Milne, 1988; 20, Work and Smith, 1996; 21,Burger and Gochfeld, 1995; 22, Burger, 1997; 23, Hontelez et al., 1992; 24, Ramo et al., 1992; 25, Mateo et al., 1997a; 26, Schmitz et al., 1990; 27, Aguirre-Alvarez, 1989; 28, Dietz et al., 1996; 29, Burger et al., 1992; 30, Burger and Gochfeld, 1993; 31, Burger and Gochfeld, 1991; 32, Hall and Fisher, 1985; 33, Choong et al., 2007; 34, Kim et al., 2007; 35, Burger and Gochfeld, 2007; 36, Zhang et al., 2006; 37, Metcheva et al., 2006; 38, Burger et al., 2007; 39, Perez-Lopez et al., 2006; 40, Kalisinska et al., 2007; 41, Fedynich et al., 2007; 42, Liu et al., 2006; 43, Borga et al., 2006; 44, Rattner et al., 2008; 45, Kim and Koo, 2008b; 46, Kim and Koo, 2008a; 47, Ruelas-Inzunza and Paez-Osuna, 2008; 48, Burger et al., 2008; 49, Braune and Scheuhammer, 2008; 50, Wayland et al., 2008; 51, Burger et al., 2008a; 52, Custer et al., 2008; 53, RodriguezNavarro et al., 2002.
292 Chapter 5 (Hong et al., 1983). Organoleads, especially trialkylleads and dialkylleads, rapidly traverse biological membranes in bird eggs, accumulating in the yolk and developing embryo (Forsyth et al., 1985). Some alkyllead compounds have been implicated in bird kills. In autumn 1979, about 2400 birds of many species were found dead or disabled on the Mersey estuary, England, an important waterfowl and marsh bird wintering area; smaller kills were observed in 1980 and 1981 (Bull et al., 1983). Affected birds contained elevated lead concentrations in liver (>7.5 mg/kg fresh weight), mostly as organolead. Bull et al. (1983) suggested that trialkyllead compounds were discharged from a petrochemical factory producing alkylleads into the estuary, where they were accumulated (up to 10.0 mg Pb/kg fresh weight) by clams (Macoma balthica) and other invertebrates on which the birds could feed. Birds dosed experimentally with trialkyllead compounds died with the same behavioral and internal signs found in Mersey casualties; tissue levels of trialkyllead were similar in the two groups (Osborn et al., 1983). Sublethal effects that might influence survival in the wild were found in both sublethally dosed and apparently healthy wild birds when tissue levels of trialkyllead compounds were matched in the two groups. It was concluded that trialkyllead compounds were the main cause of the observed mortalities and that many apparently healthy birds were still at risk (Osborn et al., 1983). Lead concentrations in feathers seemed to reflect population increases or declines of common terns (Sterna hirundo) from Long Island, New York. Lead burdens in feathers of adult terns decreased from 5.8 mg/kg DW in 1978 to 1.0 mg/kg DW in 1985, were stable until 1988, and then increased to 3.0 mg/kg DW through 1992 (Burger et al., 1994). Lead declines in feathers coincided with environmental decreases in lead from the gradual elimination of leaded gasoline in vehicles. Sources of the increased lead from 1989 to 1994 is unclear, but may have resulted from increased dredging in the New York area in the early 1990s and from increased amounts of lead paint removed from bridges during repainting operations in the late 1980s and early 1990s (Burger et al., 1994). There was a positive correlation between lead concentrations in maternal feathers of common terns and their eggs (Burger and Gochfeld, 1991). The decline in submerged aquatic vegetation in Chesapeake Bay and the later shift in diet of some waterfowl species of Chesapeake Bay from the vegetation (2.2-18.9 mg Pb/kg dry weight) to the softshell clam, Mya arenaria (1.3-7.6 mg Pb/kg DW) or to other bivalve molluscs (0.8-20.4 mg Pb/kg DW) probably did not increase dietary lead burdens in these species (Di Giulio and Scanlon, 1985). Laboratory studies demonstrate conclusively the harmful effects of lead on gulls, mallards, and terns when administered orally or via injection. Adverse effects of ingestion on mallards (A. platyrhynchos) of a single lead shot pellet weighing about 200 g (a No. 4 lead shot) includes the following: 19% dead in 20 days (Longcore et al., 1974b); lead concentrations, in mg/kg FW, of >3.0 in brain, >10.0 in clotted heart blood, >6.0 in kidney, and up to 20.0 in
Birds
293
liver (Longcore et al., 1974a); blood ALAD activity depressed 30% after 3 months and 15% after 4 months (Dieter and Finley, 1978, 1979); and femur burdens of 488.0 mg Pb/kg dry weight in laying hen, 114.0 in nonlaying hen, and 9.0 in drake (Finley and Dieter, 1978). Conversely, Frederick (1976) found no adverse effects on 9-day-old mallard ducklings fed diets containing up to 500.0 mg Pb/kg. But young Pekin ducklings had 360.0-370.0 mg Pb/total body 16 days after three to six lead shot had been forced down their throats; all of these ducks showed signs of lead poisoning (Goldman et al., 1977). In mallard kidney, lead tends to accumulate in the proximal convoluted tubule of the renal cortex, producing morphological changes such as interstitial fibrosis, edema, and acid-fast intranuclear inclusions, as well as biochemical changes; renal intranuclear inclusion bodies occurred in 83% of mallards experimentally poisoned by dietary lead acetate or lead shot (Beyer et al., 1988). Lead-induced depression in ALAD activity in mallard ducklings was not associated with significant toxicity (Eastin et al., 1983), and the physiological significance of depressed ALAD activity levels, except perhaps as an early indicator of lead exposure is debatable. However, ionic lead is known to be 10-100 times more effective in reducing avian blood ALAD activity than were ionic copper, cadmium, and inorganic and organic mercurials (Scheuhammer, 1987a). Chicks of the herring gull (Larus argentatus) given intraperitoneal (ip) injections of 0.1 or 0.2 mg Pb/kg body weight as lead nitrate and killed after 45 days had dose-dependent increases in all tissues measured (Burger and Gochfeld, 1990). Largest changes were in bone with controls at 0.8 mg Pb/kg DW, the 0.1 mg/kg group at 54.0, and the high dose group at 131.0 mg/kg DW; for liver, these values were 0.05, 7.0, and 27.0; for blood, 0.01, 0.07, and 0.2; for kidney, 0.1, 7.0, and 41.0; for brain, 0.01, 0.3, and 1.6; and for muscle, 0.01, 0.07, and 0.17 mg/kg DW, respectively (Burger and Gochfeld, 1990). Herring gull chicks given higher doses of 100.0 or 200.0 mg Pb/kg body weight as lead nitrate via ip injection had reduced growth, abnormal bone development, and disrupted locomotion (Burger, 1990; Burger and Gochfeld, 1988b, 1995). Chicks of the common tern (S. hirundo) injected with >100.0 mg Pb/kg BW as lead nitrate had reduced growth and low survival (Burger and Gochfeld, 1988a; Gochfeld and Burger, 1988). Fatal lead poisoning (50% kill) is documented for a captive colony of Gentoo penguins (Pygoscelis papua) in a zoo in Omaha, Nebraska. The source of lead was ankle weights worn by divers who cleaned the pool; the weights contained 1- to 2-mm lead pellets that were expelled through faulty seams and ingested by the penguins (Brown et al., 1996). Many species of zoo animals, including parrots, have been fatally poisoned from ingestion of flaking lead-based paint on the walls and bars of their cages (NRCC, 1973). Ingestion of lead-based paint chips was one cause of epizootic mortality of fledgling Laysan albatross, Diomedea immutabilis, at Midway Atoll in 1983 (Sileo and Fefer, 1987). Lead contamination of seabirds from the use of lead shot is an important source of lead in the diet of Greenland residents (Johansen et al., 2001). In Greenland, the thick-billed murre, Uria lomvia, is the most frequently hunted seabird. Breast meat of murres killed by lead shot had 0.22 mg Pb/kg FW, usually as small lead fragments. Humans ingesting one boiled murre with
294 Chapter 5 soup receive about 0.05 mg of lead, or about twice the daily average lead intake from all dietary sources in Denmark, about 25 times the daily lead intake from other marine food items in Greenland, and about 25% of the accepted tolerable daily intake (Johansen et al., 2001). As a public health measure, the use of lead shot ammunition in Greenland should be restricted or banned. Proposed lead criteria to protect mallards and other shorebirds include less than 5.0 mg total lead/kg dry weight ration (Scheuhammer, 1987a,b), 0.1 to less than 0.2 mg/L blood (Mauvais and Pinault, 1993; Pain, 1996; Pokras and Chafel, 1992; Scheuhammer, 1987b), and less than 2.0 to less than 2.3 mg total Pb/kg DW liver (Blus et al., 1991; Pain, 1996; Pokras and Chafel, 1992) to less than 5.0 mg total Pb/kg DW liver (Mateo et al., 1998). Legislation limiting the content of lead in paints, reducing the lead content in gasoline, and eliminating the use of lead shot in the United States (phase out initiated in 1986 and fully implemented in 1991) has substantially reduced environmental burdens of lead (Eisler, 2000c).
5.20 Lithium Liver of gray heron, A. cinerea, from Japan contained up to 0.15 mg Li/kg dry weight (Horai et al., 2007). Arctic region seabirds had up to 0.27 mg Li/kg FW in muscle and 0.28 mg Li/kg FW in liver (Table 5.7). Table 5.7: Lithium and Manganese Concentrations in Field Collections of Birds Element and Organism
Concentration
Reference
a
Lithium Arctic region seabirds; Barents Sea; May 1999; muscle Dovekie, Alle alle Thick-billed murre, Uria lomvia Black guillemot, Cepphus grylle Arctic region seabirds; Baffin Bay, Canada; May-June 1998; muscle vs. liver Dovekie Black-legged kittiwake, Rissa tridactyla Thick-billed murre Black guillemot Northern fulmar, Fulmaris glacialis Thayer’s gull, Larus thayeri
0.271 FW 0.018 FW 0.034 FW
7 7 7
0.18 FW vs. 0.28 FW 0.02 FW vs. 0.08 FW
7 7
0.04 FW 0.02 FW 0.16 FW 0.01 FW
7 7 7 7
vs. vs. vs. vs.
0.06 FW 0.04 FW 0.20 FW 0.01 FW
(Continues)
Birds Table 5.7: Element and Organism
295
Cont’d
Concentration
Reference
a
Manganese Alaska; Prince William Sound; 2004; breast feathers Black oystercatcher, Haematopus bachmani Black-legged kittiwake, Rissa tridactyla; oiled vs. nonoiled
1.1 DW
10
1.1 DW vs. 0.75 DW
10
1.5 DW vs. 2.6 DW 1.6 DW vs. 1.6 DW
3 3
Arctic region seabirds; Barents Sea; May 1999; muscle Dovekie Thick-billed murre Black guillemot
0.72 FW 0.46 FW 0.54 FW
7 7 7
Arctic region seabirds; Baffin Bay, Canada; May-June 1998; muscle vs. liver Dovekie Black-legged kittiwake Thick-billed murre Black guillemot Northern fulmar Thayer’s gull
0.06 FW 0.52 FW 0.49 FW 0.61 FW 0.68 FW 0.49 FW
Gray heron, Ardea cinerea; Kanto area, Japan Liver Kidney Muscle Lung Brain
13.4 DW; max. 21.0 DW 8.4 DW; max. 26.5 DW 1.7 DW; max. 3.5 DW 6.7 DW; max. 126.0 DW 1.8 DW
5 5 5 5 5
Pigeon guillemot, Cepphus columba; feather; Alaska; summer 2004 Prince William Sound Amchitka Kiska
1.75 DW 0.90 DW 1.24 DW
4 4 4
Antarctica; molting feathers; 2002 vs. 2003 Gentoo penguin, Pygoscelis papua Chinstrap penguin, Pygoscelis antarctica
vs. vs. vs. vs. vs. vs.
3.3 FW 3.5 FW 3.5 FW 2.7 FW 4.3 FW 4.3 FW
7 7 7 7 7 7
(Continues)
296 Chapter 5 Table 5.7:
Cont’d
Element and Organism
Concentration
Little penguin, Eudyptula minor; Australia; 2005; found dead Muscle Liver
0.6 FW; max. 4.36 FW 2.5 FW; max. 4.50 FW
2 2
2.4 FW 2.0 FW 1.2 FW 2.0 FW 2.3 FW 1.9 FW
1 1 1 1 1 1
1.5 FW 1.7 FW 1.0 FW 1.8 FW 1.6 FW 0.6 FW
1 1 1 1 1 1
1.0 1.4 0.5 1.7 2.3 0.6
1 1 1 1 1 1
Laughing gull, Larus atricilla Downy young Brain Bone Heart Kidney Liver Muscle Prefledglings Brain Bone Heart Kidney Liver Muscle Adults Brain Bone Heart Kidney Liver Muscle Stomach contents Fish, 5 spp. Insects
3.4-11.3 FW 5.4 FW
Black-crowned night-heron, Nycticorax nycticorax; 1998-1999; nestlings; feathers Baltimore Harbor, Maryland Holland Island, Maryland Pea Patch Island, Delaware
2.3 (1.6-3.2) DW 3.1 (1.6-5.9) DW 7.6 (4.9-11.7) DW
Osprey, Pandion haliaetus; nestlings; Chesapeake Bay; 2000-2001 vs. Delaware Bay 2002; max. values Blood Feathers
0.77 DW vs. 0.77 DW 99.2 DW vs. 58.9 DW
(0.1-1.4) FW (0.1-4.2) FW (<0.1-1.3) FW (0.5-4.1) FW (0.5-5.4) FW (<0.1-1.3) FW
Reference
a
1 1
12 12 12
8 8 (Continues)
Birds Table 5.7:
Cont’d
Element and Organism
Concentration
Clapper rail, Rallus longirostris; eggshell; Georgia; 2000 Metals-contaminated marsh Reference site
7.0 (3.0-13.0) DW 5.0 (2.0-11.0) DW
Seabirds; 3 spp.; Reunion Island, western Indian Ocean; 2002-2004; juveniles vs. adults Barau’s petrel, Pterodroma baraui Liver Kidney Muscle Audubon’s shearwater, Puffinus lherminieri bailloni Liver Kidney Muscle White-tailed tropicbird, Phaethon lepturus Liver Kidney Muscle
297
Reference
a
13 13
7.3 DW vs. 11.1 DW 6.3 DW vs. 8.3 DW 1.4 DW vs. 1.7 DW
6 6 6
11.1 DW vs. 13.4 DW 6.2 DW vs. 8.9 DW 1.5 DW vs. 1.9 DW
6 6 6
27.9 DW vs. 17.9 DW 7.7 DW vs. 73.3 DW 1.6 DW vs. 2.3 DW
6 6 6
Shorebirds; 5 spp.; Korea; 1994-1995 Feathers Liver
2.6-8.5 (1.1-18.1) FW 1.1-3.1 (0.01-3.7) FW
9 9
Common eider, Somateria mollissima; Aleutian Islands, Alaska; summer 2007; females Feathers Eggs
10.5 DW 1.5 DW
11 11
Values are in mg Mn/kg fresh weight (FW) or dry weight (DW). a 1, Hulse et al., 1980; 2, Choong et al., 2007; 3, Metcheva et al., 2006; 4, Burger et al., 2007; 5, Horai et al., 2007; 6, Kojadinovic et al., 2007a; 7, Borga et al., 2006; 8, Rattner et al., 2008; 9, Kim and Koo, 2008b; 10, Burger et al., 2008; 11, Burger et al., 2008a; 12, Custer et al., 2008; 13, Rodriguez-Navarro et al., 2002.
5.21 Manganese Maximum concentrations of manganese—in mg Mn/kg DW—were measured in feathers of adult ospreys (58.9), nestling ospreys (11.7), eggshell of clapper rails (13.0), liver of Barau’s petrel (11.1), kidney of Audubon’s shearwater (8.9), and liver (27.9) and kidney (73.3) of the white-tailed tropicbird (Table 5.7).
298 Chapter 5 Liver, kidney, and bone tissues of adult laughing gulls, Larus atricilla, contained elevated manganese concentrations, up to 5.4 mg Mn/kg fresh weight in liver (Table 5.7). Fish and insects seem to be the major dietary source of manganese in laughing gulls (Hulse et al., 1980). However, maximum concentrations of manganese were similar in muscle and liver of the little penguin, E. minor (Table 5.7).
5.22 Mercury In seabirds, mercury concentrations were highest in tissues and feathers of species that ate fish and benthic invertebrates and lowest in birds that ate mainly pelagic invertebrates (Braune, 1987; Eisler, 2006; Kim et al., 1996a; Liu et al., 2006; Lock et al., 1992). In seabirds, the relation between tissues and total mercury concentration is frequently 7:3:1 between feather, liver, and muscle; however, these ratios are affected by the chemical form of mercury present in liver, the sampling date relative to stage of the molt sequence, and the types of feathers used for analysis (Thompson et al., 1990). Almost all mercury in body feathers of seabirds examined is organic mercury; however, more than 90% of liver mercury is inorganic (Thompson and Furness, 1989). Mercury residues are frequently highest in kidney and liver, but are modified by food preference and availability, and by migratory patterns (Delbekke et al., 1984; USNAS, 1978). Eggs of the common eider and the glaucous-winged gull from the Aleutian Islands in summer 2004 contain mean concentrations up to 0.68 mg Hg/kg DW (Table 5.8). Eggs of both species are dietary staples of the Aleutian residents, with possible attendant health risks (Burger and Gochfeld, 2007; Burger et al., 2007a). Mercury concentrations in eggs of the thick-billed murre, U. lomvia, and the northern fulmar, Fulmaris glacialis, but not in the black-legged kittiwake, Rissa tridactyla, from the Canadian Arctic show significant increases between 1975 and 2003 (Braune, 2007; Table 5.8), with some risk to health of human consumers. Mercury concentrations in Canadian waterfowl breast muscle were either low, that is, less than 1.0 mg total Hg/kg FW or below detection limits, with the exception of some mergansers from eastern Canada which contained mercury burdens of 1.0-1.5 mg Hg/kg FW (Table 5.8); human consumers of merganser breast muscle containing elevated mercury burdens may be at risk (Braune and Malone, 2006). Total mercury concentrations in eggs of the ivory gull, Pagophila eburnea, between 1976 and 2004 (Table 5.8) are among the highest reported for seabird eggs from the Arctic region marine environment (Braune, 2004; Braune et al., 2006). Ivory gulls have a higher metabolic rate than most other gulls (Gabrielsen and Mehlum, 1989) and therefore require a higher caloric intake which could be achieved on lipid-rich food (Braune et al., 2006). Ivory gulls are known to scavenge carcasses of marine mammals (Haney and MacDonald, 1995) which generally have elevated mercury concentrations when compared to other prey items (Atwell et al., 1998; Campbell et al., 2005). It has been suggested that concentrations of
Birds
299
Table 5.8: Mercury Concentrations in Field Collections of Birds Organism Aleutian Islands, Alaska; edible portions; 2004-2005 Tufted puffin, Fratercula cirrhata; muscle Common eider, Somateria mollissima Muscle Egg Glaucous-winged gull, Larus glaucescens Muscle Egg Pigeon guillemot, Cepphus columba; muscle Admiralty Bay, Antarctica; January 2004 Adelie penguin, Pygoscelis adeliae Egg Feather Kelp gull, Larus dominicanus; feather Alaska; Prince William Sound; 2004; breast feathers Black oystercatcher, Haematopus bachmani Black-legged kittiwake, Rissa tridactyla; oiled vs. nonoiled Aleutian Islands; summer 2004; egg contents Common eider, Somateria mollissima Glaucous-winged gull, Larus glaucescens Antarctica and environs; seabirds; 1978-1983; 15 spp.; eggs Antarctic region; seabirds; liver 1977-1979 4 spp. 3 spp. 1980; 5 spp.
Concentration
Reference
0.12 FW; max. 0.26 FW
75
0.12 FW; max. 0.18 FW 0.19 FW; max. 0.41 FW
75 75
0.33 FW; max. 0.85 FW 0.36 FW; max. 0.81 FW 0.49 FW; max. 0.85 FW
75 75 75
0.005 DW 0.5-1.4 DW 2.4 DW
64 64 64
1.2 DW
94
1.1-1.4 DW vs. 2.9 DW
94
0.431 DW 0.68 DW
67 67
0.02-1.8 FW; max. 2.7 FW
22
0.5-1.3 FW 2.7-2.9 FW 0.5-2.1 FW
23 23 24
a
(Continues)
300 Chapter 5 Table 5.8: Organism Antarctic region; February-March 1989 Adelie penguin, Pygoscelis adeliae; muscle vs. liver Chinstrap penguin, Pygoscelis antarctica; feces Gentoo penguin, Pygoscelis papua; liver
Cont’d
Concentration
Reference
Max 0.7 DW vs. max. 2.0 DW
25
1.6 DW
25
34.7 DW
25
0.6 DW vs. 0.5 DW
26
Antarctica; Terra Nova Bay; 1989-1991 Petrel, Pagodroma nivea; eggs vs. feathers Skua, Catharacta maccormicki Eggs Feathers Guano Chick plumage Adelie penguin, Pygoscelis adeliae Egg Feathers Guano Chick plumage Stomach contents Muscle Liver Kidney Brain Testis
1.6 DW 2.9 DW 0.2 DW 1.9 DW
26 26 26 26
0.3 DW 0.8 DW 0.2 DW 0.4 DW 0.08 DW 0.6 DW 1.6 DW 1.2 DW 0.4 DW 0.4 DW
26 26 26 26 26 26 26 26 26 26
Mallard, Anas platyrhynchos Whole body Liver Kidney
<0.5 FW 0.06 FW 0.07 FW
1 1 1
Black duck, Anas rubripes; egg
0.07-0.34 FW
2
King penguin, Aptenodytes patagonicus; sub-Antarctica islands; breast feathers; 1966-1974 vs. 2000-2001
2.7 DW vs. 2.0 DW
27
1.3 DW; max. 6.8 DW 0.49 DW; max. 1.9 DW 0.34 DW; max. 1.4 DW 0.56 DW; max. 2.9 DW 0.09 DW; max. 0.22 DW
74 74 74 74 74
Gray heron, Ardea cinerea; Kanto area, Japan Liver Kidney Muscle Lung Brain
a
(Continues)
Birds Table 5.8:
Cont’d
Organism
Concentration
Atlantic Ocean; north/northeast regions; feathers; from pre-1930s museum specimens vs. post-1980 collections Great skua, Catharcta skua Atlantic puffin, Fratercula arctica Northern fulmar, Fulmaris glacialis Manx shearwater, Puffinus puffinus Atlantic gannet, Sula bassana
3.7 FW vs. 5.6 FW 1.8 FW vs. 4.0 FW 4.0-4.4 FW vs. 1.4-2.9 FW 1.3-1.5 FW vs. 3.3-4.2 FW 6.0 FW vs. 7.2 FW
28 28 28 28 28
1.3 (0.5-3.7) DW
93
Lesser scaup, Aythya affinis; males; 20042005; kidney
Reference
Greater scaup, Aythya marila; British Columbia; Iona Island vs. Roberts Bank Liver Diet
0.24 FW vs. 0.26 FW 0.014-0.016 FW vs. <0.005 FW
7 7
Canvasback, Aythya valisineria; liver
0.24 FW
8
Azores; 1990-1992; feathers; adults; 7 spp. Petrels Shearwaters Terns
12.5-22.1 DW; max. 35.9 DW 2.1-6.0 DW; max. 12.4 DW 2.0-2.3 DW; max. 4.0 DW
29 29 29
0.06-0.34 FW
30
Bulwer’s petrel, Bulweria bulwerii; North Atlantic Ocean; methylmercury; feathers; from museum specimens 18851994; max. concentrations; compared to Cory’s shearwater, Calonectris diomedia borealis 1885-1900 1900-1931 1950-1970 1992-1994
5.0 FW vs. 2.0 FW 8.0 FW vs. 3.0 FW 17.0 FW vs. 4.0 FW 23.0 FW vs. 5.5 FW
31 31 31 31
Knot, Calidris alpina; liver September/October October November January March
1.9 (0.8-3.3) 1.7 (0.7-2.6) 3.3 (3.1-3.5) 6.9 (4.8-9.2) 10.5 DW
Barents Sea; seabirds; 1993; 10 spp.; eggs
301
DW DW DW DW
a
3 3 3 3 3 (Continues)
302 Chapter 5 Table 5.8:
Cont’d
Organism
Concentration
Red knot, Calidris canutus; liver August September/October January February Mid-March Late-March
1.0 (0.4-1.5) DW 1.3 (0.8-1.7) DW 7.3 (6.6-8.0) DW 9.8 (5.1-12.9) DW 14.4 (5.6-24.9) DW 18.5 (16.5-20.5) DW
California; diving ducks; 1989; liver; Tomales Bay vs. Suisin Bay Greater scaup, Aythya marila Surf scoter, Melanitta perspicillata Ruddy duck, Oxyura jamaicensis Canada; New Brunswick; seabirds; 9 spp.; 1978-1984 Brain Kidney Liver Muscle
Reference
a
3 3 3 3 3 3
19.0 (5.0-66.0) DW vs. 6.0 (3.0-11.0) DW 19.0 (3.0-35.0) DW vs. 10.0 (5.0-21.0) DW 6.0 (4.0-9.0) DW vs. 4.0 (2.0-7.0) DW
32
0.04-0.36 FW 0.24-5.3 FW 0.05-0.61 FW 1.5-30.7 FW
33 33 33 33
1.6 (0.9-3.7) DW 1.4 (0.9-3.2) DW
85 85
3.8 DW vs. 2.1 DW 3.0 DW vs. 1.7 DW
85 85
32 32
Canadian Arctic; June 1997; liver Common eider, Somateria mollissima; females Total mercury Organic mercury King eider, Somateria spectabilis; males vs. females Total mercury Organic mercury Great skua, Catharcta skua Total mercury; feather; adults vs. chicks Total mercury vs. inorganic mercury; adults Kidney Liver Muscle
7.0 (1.0-32.4) FW vs. 1.3 (0.7-2.4) FW
34
9.7 DW vs. 5.0 DW 11.6 DW vs. 6.2 DW 2.3 DW vs. 2.3 DW
34 34 34
Pigeon guillemot, Cepphus columba; feather; Alaska; summer 2004 Prince William Sound Amchitka Kiska
2.8 DW 7.72 DW 6.36 DW
72 72 72 (Continues)
Birds Table 5.8: Organism Black-footed albatross, Diomedea nigripes; Sanriku, Japan; 1997-1998 Liver, whole Liver nuclei; lysosomes and mitochondria Liver, whole Kidney Diving ducks; coastal California; December 1986-March 1987; liver Canvasback, Aythya valisineria; early winter Adult males Adult females Juvenile males Juvenile females Greater scaup, Aythya marila Early winter Adult males Juvenile males Late winter Adult females Adult males Juvenile females Lesser scaup, Aythya affinis; late winter Adult males Juvenile males
Cont’d
Concentration
Reference
94.0 (36.0-150.0) FW 78.0 (20.0-127.0) FW
35 35
220.0 DW 20.0 DW
56 56
0.6 1.3 0.2 0.2
84 84 84 84
(0.2-4.2) DW (0.4-4.2) DW (<0.01-0.9) DW (<0.01-1.3) DW
3.4 (2.8-4.2) DW 2.9 (1.8-5.2) DW
84 84
9.6 (1.9-48.0) DW 10.8 (8.1-19.5) DW 4.4 DW
84 84 84
5.6 (3.6-9.8) DW 7.6 (5.8-9.9) DW
84 84
Little egret, Egretta garzetta; Pearl River Delta, China; May 2000 Egg contents Chick feather
0.36 (0.23-0.64) DW 2.1 (1.1-3.6) DW
69 69
Little penguin, Eudyptula minor; Australia; 2005; found dead Muscle Liver
0.3 FW; max. 0.6 FW 1.0 FW; max. 3.3 FW
66 66
17.4 DW vs. 16.9 DW
9
Gull; feathers; total mercury vs. methylmercury Germany; chicks; down; 1991 Common tern, Sterna hirundo Black-headed gull, Larus ridibundus Herring gull, Larus argentatus
303
5.9 (2.7-10.2) FW 1.0 (0.1-3.6) FW 1.4 (0.4-2.9) FW
a
36 36 36 (Continues)
304 Chapter 5 Table 5.8: Organism Germany; North Sea coast; feathers; pre-1940 vs. post-1941 Herring gull, Larus argentatus Adults Juveniles Common tern, Sterna hirundo Adults Juveniles Germany; 1991; maximum concentrations Herring gull, Larus argentatus; adults Eggs Down Liver Black-headed gull, Larus ridibundus; chick; body feathers Common tern, Sterna hirundo Eggs Down Liver Greenland; seabirds; 1983-1991; 10 spp. Kidney Liver Muscle Greenland; seabirds; 1984-1987; liver; total mercury vs. methylmercury Gulf of California; shore birds; 2000; 5 spp. of nonmigratory birds vs. 4 spp. of migratory birds Feathers Liver Muscle Heart Viscera
Cont’d
Concentration
4.6 (1.0-7.8) FW vs. 7.9 (2.1-21.2) FW 2.0 FW vs. 4.0 FW
Reference
37 37
1.0 (0.2-2.3) FW vs. 3.5 (0.4-13.9) FW 2.0 (0.4-4.9) FW vs. 4.8 (1.5-18.4) FW
37
2.8 FW 58.0 FW 4.0 FW 8.0 FW
38 38 38 38
4.0 FW 20.0 FW 16.0 FW
38 38 38
0.1-2.1 FW 0.04-2.7 FW 0.02-0.67 FW
39 39 39
Max. 2.3 FW vs. 0.45 (0.1-1.5) FW
40
3.0 DW 5.0 DW 2.0 DW 1.9 DW 1.1 DW
65 65 65 65 65
vs. vs. vs. vs. vs.
4.0 DW 3.2 DW 1.8 DW 1.9 DW 0.8 DW
a
37
(Continues)
Birds Table 5.8: Organism White-tailed sea eagle, Haliaeetus albicilla Gulf of Bothnia, Finland Dead birds and addled eggs Muscle of prey bird West Greenland; primary feather 5; 1875-2004; juveniles vs. adults 1875-1884 1885-1894 1895-1904 1905-1914 1915-1924 1925-1934 1935-1944 1975-1984 1985-1994 1995-2004 Herring gull, Larus argentatus Denmark; 1976-1976; liver Germany; Wadden Sea Egg vs. ovary Males vs. females Feather Liver Muscle Muscle Liver Kidney Brain Heart Blood Spleen Audouin’s gull, Larus audouinii; western Mediterranean Sea Feather; adults; 2002 Feather; chicks; 2004 Egg content; 1992 Lesser black-backed gull, Larus fuscus; muscle
Cont’d
Concentration
Reference
Max. 26.0 FW 0.05-0.93 FW
10 10
2.6 DW 2.0 DW 1.1 DW 1.2 DW 2.0 DW 1.5 DW 5.6 DW 1.3 DW 5.6 DW 3.0 DW
90 90 90 90 90 90 90 90 90 90
vs. vs. vs. vs. vs. vs. vs. vs. vs. vs.
305
4.6 DW 4.2 DW 5.1 DW 6.6 DW 5.3 DW 9.0 DW 5.7 DW 6.2 DW 11.9 DW 10.8 DW
0.6 (0.08-2.3) FW
41
1.4 DW vs. 1.9 DW
42
6.4 DW vs. 4.9 DW 4.7 DW vs. 4.4 DW 2.6 DW vs. 2.0 DW 2.66 FW 6.89 FW 5.36 FW 1.33 FW 2.86 FW 2.42 FW 2.05 FW
42 42 42 12 12 12 12 12 12 12
16.2 (11.9-22.1) DW 5.1 (4.7-5.5) DW 4.9 (4.4-5.5) DW
62 62 63
0.3 FW
13
a
(Continues)
306 Chapter 5 Table 5.8: Organism Bonaparte’s gull, Larus philadelphia; New Brunswick, Canada; autumn 1978-1984 Feather parts Quill Rachis Vane Feather groups Secondaries Wing coverts Primaries Retrices All feathers Juveniles Second year Adults Adults; females vs. males
Cont’d
Concentration
Reference
2.3 DW 3.3 DW 3.5 DW
43 43 43
1.9 DW 2.3 DW 2.5 DW 2.8 DW
43 43 43 43
2.0 DW 2.5 DW 4.1 DW 4.8 DW vs 3.5 DW
43 43 43 43
Common black-backed gull, Larus ridibundus; Mediterranean Sea coast of Italy Liver Muscle Kidney Brain
1.3-2.4 FW 0.9-1.8 FW 0.6-1.4 FW 0.65 FW
14 14 14 14
Bar-tailed godwit, Limosa lapponica; liver
1.3 DW
Hooded merganser, Lophodytes cucullatus Muscle Liver
0.53-0.63 FW; 2.1-2.2 DW 5.4 DW
Surf scoter, Melanitta perspicillata British Columbia; Iona Island vs. Roberts Bank Liver Diet Liver SE Alaska; 1990-1991 Oregon/Washington; 1984-1985 California, San Francisco Bay 1982 1985 British Columbia; 1998-2001
2.12 FW vs. 0.93 FW 0.039 FW vs. <0.005-0.017 FW
a
3 11 11
7 7
0.4-2.2 FW 0.12-1.3 FW
78 79
0.5-9.6 FW 1.5-4.6 FW 1.0-2.9 (0.19-5.9) DW
80 81 83 (Continues)
Birds Table 5.8:
Cont’d
Organism
Concentration
Red-breasted merganser, Mergus serrator Muscle Liver
0.74-0.91 FW; 3.7-3.8 DW 46.0 DW
11 11
Gannet, Morus bassanus; egg
0.45-0.94 FW
15
New Zealand; liver Albatrosses; 8 spp. Shearwaters; 3 spp. Petrels; 19 spp. Penguins; 4 spp.
17.0-295.0 DW 0.8-1.3 DW 0.2-140.0 DW 0.5-2.4 DW
44 44 44 44
Reference
Ivory gull, Pagophila eburnean Greenland; spring; 1984 Liver Muscle Baffin Bay; spring; 1998 Liver Muscle
0.90 FW 0.32 FW
60 60
0.68-0.93 FW 0.21 FW
61 61
Black-crowned night-heron, Nycticorax nycticorax; 1998-1999; nestlings; feathers Baltimore Harbor, Maryland Holland Island, Maryland Pea Patch Island, Delaware
0.8 (0.6-1.1) DW 0.8 (0.7-1.0) DW 1.3 (0.8-1.9) DW
57 57 57
0.06 FW 0.1 (0.04-0.2) FW 0.05 FW vs. 0.1 (0.07-0.2) FW 0.06 FW (0.05-0.25) FW 0.1 (0.05-0.2) FW
45 45 46 46 45 46
0.29 DW 0.09 FW; 0.45 (0.16-1.01) DW <1.0-67.5 FW 0.19-130.0 FW
91 91 16 16
0.47 DW vs. 1.8 DW 2.4 DW vs. 4.2 DW
92 92
Osprey, Pandion haliaetus Egg contents; USA Idaho; 1973 Florida Everglades; 1973 Maryland; 1973 vs. 1986 Massachusetts; 1986-1987 New Jersey; 1978 Virginia; 1987 Columbia River 1997-1998 2004 Liver Kidney Nestlings; Chesapeake Bay, 2000-2001 vs. Delaware Bay 2002; max. values Blood Feathers
307
a
(Continues)
308 Chapter 5 Table 5.8: Organism White pelican, Pelecanus erythrorhynchos Egg, less shell Adults Whole body Muscle Liver Kidney Nestlings Whole body Liver Brown pelican, Pelecanus occidentalis Liver Kidney Feather White-necked cormorant, Phalacrocorax carbo; England; 1992-1993; eggs that failed to hatch; rapidly-expanding colony White-faced ibis, Plegadis chihi Whole body less brain Egg
Cont’d
Concentration
Reference
0.22 FW
17
0.64 FW 0.78 FW 7.98 FW 1.51 FW
17 17 17 17
0.06 FW 0.28 FW
17 17
0.75 DW 0.68 DW 0.97 DW
47 47 47
2.6 (1.4-7.7) DW
48
0.06-4.0 FW 0.01-0.21 FW
19 19
2.0 DW 0.44 DW
49 49
Black-legged kittiwake, Rissa tridactyla; Helgoland Island; North Sea; 19921994; nestlings; found dead Brain Age 1 day Age 21-40 days Feathers Age 1 day Age 6-10 days Age 21-40 days Liver vs. kidney Age 1 day Age 6-10 days Age 21-40 days
4.6 DW 4.0 DW 2.3 DW
49 49 49
2.8 DW vs. 2.0 DW 1.8 DW vs. 1.4 DW 1.1 DW vs. 0.9 DW
49 49 49
Clapper rail, Rallus longirostris; eggshell; Georgia; 2000 Metals-contaminated marsh Reference site
0.37 (0.09-0.77) DW 0.11 (0.04-0.24) DW
55 55
a
(Continues)
Birds Table 5.8:
Cont’d
Organism
Concentration
Seabirds Feathers; 10 spp. Liver; 9 spp.
1.5-30.7 FW 4.9-306.0 DW
50 51
4.53 (1.80-8.52) DW 5.03 (2.24-6.74) DW 6.37 (1.59-15.3) DW 2.57 DW 0.82 DW
58 58 58 59 59
1.41-1.57 DW
59
0.56-1.33 DW
59
0.39 DW 9.78 DW 0.88 DW 0.62 DW 0.64 DW 0.82 DW
82 82 82 82 82 82
0.86 DW 1.06 DW 0.74 DW 1.13 DW 1.19 DW 1.36 DW 1.41 DW
82 82 82 82 82 82 82
0.60 DW 0.78 DW 0.46 DW 0.98 DW 0.97 DW 1.13 DW 1.19 DW 1.33 DW
82 82 82 82 82 82 82 82
Seabirds; Canadian Arctic; eggs Ivory gull, Pagophila eburnean 1976 1987 2004 Glaucous gull, Larus hyperboreus; 2003 Black-legged kittiwake, Rissa tridactyla; 2003 Northern fulmar, Fulmarus glacialis; 2003 Thick-billed murre, Uria lomvia; 2003 Seabirds; Canadian Arctic; 1975-2003; egg contents Black-legged kittiwake, Rissa tridactyla 1975 1976 1987 1993 1998 2003 Northern fulmar, Fulmaris glacialis 1975 1976 1977 1987 1993 1998 2003 Thick-billed murre, Uria lomvia 1975 1976 1977 1987 1988 1993 1998 2003
309
Reference
a
(Continues)
310 Chapter 5 Table 5.8:
Cont’d
Organism
Concentration
Seabirds; Barents Sea; May 1999; muscle Dovekie, Alle alle Thick-billed murre Black guillemot, Cepphus grille
0.12 FW 0.12 FW 0.05 FW
Seabirds; Baffin Bay, Canada; May-June 1998; muscle vs. liver Dovekie Black-legged kittiwake Thick-billed murre Black guillemot Northern fulmar Thayer’s gull, Larus thayeri
0.08 FW 0.30 FW 0.33 FW 0.34 FW 0.39 FW 0.48 FW
Seabirds; western Indian Ocean; breast feathers; 6 spp.; 5 sites; juveniles vs. adults; 2001-2004 Sooty tern, Sterna fuscata Brown noddy, Anous stolidus Lesser noddy, Anous teuirostris Audubon’s shearwater, Puffinus lherminieri bailloni Barau’s petrel, Pterodroma baraui White-tailed tropicbird, Phaethon lepturus Seabirds; 3 spp.; Reunion Island, western Indian Ocean; 2002-2004; juveniles vs. adults Barau’s petrel Liver Kidney Muscle Audubon’s shearwater Liver Kidney Muscle White-tailed tropicbird Liver Kidney Muscle
Reference
a
89 89 89
vs. vs. vs. vs. vs. vs.
0.27 FS 1.0 FW 1.1 FW 1.2 FW 3.4 FW 1.9 FW
89 89 89 89 89 89
0.05 DW vs. 0.18-0.39 DW 0.06-0.42 DW vs. 0.24-0.40 DW No data vs. 0.27 DW 0.07 DW vs. 0.25 DW
71 71 71 71, 76
0.30 DW vs. 0.96 DW 0.29 DW vs. 0.84 DW
71, 76 71, 76
1.1 DW vs. 24.3 DW 0.6 DW vs. 24.2 DW 0.1 DW vs. 2.8 DW
76 76 76
0.26 DW vs. 1.7 DW 0.17 DW vs. 1.2 DW 0.06 DW vs. 0.38 DW
76 76 76
1.3 DW vs. 1.9 DW 0.9 DW vs. 1.9 DW 0.3 DW vs. 0.75 DW
76 76 76 (Continues)
Birds Table 5.8:
Cont’d
Organism
Concentration
Sea ducks; breeding females; 2001-2003; Canada; blood King eider, Somateria spectabilis White-winged scoter, Melanitta fusca
(0.06-0.33) FW (0.05-0.47) FW
96 96
Seabirds; 3 spp.; Spain; 2002-2003; liver; found dead or dying after oil spill
1.2-2.2 (0.1-12.8) DW
73
Seabirds; Canadian Arctic; 1991-1993; 5 spp.; breeding season; liver
2.6-8.1 DW
95
Shorebirds Baltic Sea; fish-eating; migratory; muscle New Zealand; 5 spp.; feathers vs. liver Texas; 7 spp.; liver San Francisco Bay, California; 2005-2006; blood Black-necked stilt, Himantopus mexicanus All Males Females Southern end American avocet, Recurvirostra americana All Males Females Southern end Common eider, Somateria mollissima Muscle Liver Egg yolk vs. egg white Egg Liver Kidney Adrenal gland Pectoral muscle, heart, lung Aleutian Islands, Alaska; summer 2007; females Feathers Eggs
311
Reference
0.29 FW
4
0.10-8.0 FW vs. 0.01-1.2 FW 0.05-5.45 FW
5 6
1.09 FW 1.32 FW 1.15 FW 3.31 FW
70 70 70 70
0.25 FW 0.32 FW 0.21 FW 0.58 FW
70 70 70 70
0.2 FW 0.6 FW 0.3 FW vs. 0.2 FW 0.33 FW 0.58 FW; 2.14 DW 0.37 FW; 1.83 DW 1.22 FW; 6.91 DW <0.001 FW
13 13 13 18 20 20 20 20
0.98 DW 0.43 DW
97 97
a
(Continues)
312 Chapter 5 Table 5.8: Organism Northern common eider, Somateria mollissima borealis; eastern Canadian Arctic; liver 1998-1999 Females; 1998 vs. 1999 Males; 1999 Females; 1997-2000; prenesting vs. nesting Little tern, Sterna albifrons; feathers; Portugal; 2000-2002; small chicks vs. large chicks 2000 2001 2002 Caspian tern, Sterna caspia; eggs; Texas; Laguna Madre; 1993-1994 Common tern, Sterna hirundo Normal vs. terns with abnormal feather loss Blood Liver Kidney Muscle Brain Feathers Muscle Liver Kidney Brain Heart Egg Northern gannet, Sula bassanus; liver; dead or moribund birds Red-footed booby, Sula sula; Dongdao Island; South China Sea; March-April 2003 Feces Wing bone Eggshell Feather
Cont’d
Concentration
3.7 2.6 2.7 2.0 3.5
(2.5-5.8) (1.0-3.9) (1.3-6.5) (1.7-2.4) (3.0-4.0)
DW vs. DW DW DW vs. DW
Reference
86 86 87
5.2-6.7 vs. 4.0-4.2 FW 4.0-5.8 FW vs. 3.1-4.3 FW 5.4-11.6 FW vs. 1.9-5.5 FW
52 52 52
0.6 (0.4-0.8) FW
53
0.37 FW vs. 0.64 FW 1.06 FW vs. 2.22 FW 0.99 FW vs. 1.56 FW 0.68 FW vs.1.16 FW 0.42 FW vs. 0.85 FW 1.27 DW vs. 1.75 DW 0.31 FW 1.86 FW 0.87 FW 0.32 FW 0.34 FW 0.12-0.87 FW
21 21 21 21 21 21 12 12 12 12 12 12
5.9-97.7 DW
107.8 (83.0-120.0) DW 60.0 DW 30.0 DW 1600.0 DW
a
3
88 88 88 88 (Continues)
Birds Table 5.8: Organism Texas; eggs Black skimmer, Rynchops niger; Lavaca Bay vs. Laguna Vista (nest success lower at Lavaca colony) Forster’s tern, Sterna forsteri; Lavaca Bay vs. San Antonio Bay (nesting success similar)
Cont’d
Concentration
Reference
0.5 (0.2-0.8) FW vs. 0.19 (0.05-0.31) FW
54
0.40 FW vs. 0.22 FW
54
Royal tern, Thalasseus maximus; egg
0.8 FW
18
Redshank, Tringa totanus; liver August November March
1.6 (1.3-1.9) DW 2.7 (1.2-4.8) DW 12.3 (5.7-2.6) DW
Waterfowl; coastal Canada; breast muscle; 1992-1995 Dabbling ducks; 8 spp. Bay ducks; 3 spp. Sea ducks; 6 spp. Mergansers; 3 spp.
0.015-0.188 FW; max. 0.704 FW 0.03-0.11 FW; max. 0.29 FW 0.11-0.23 FW; max. 0.92 FW 0.43-0.66 FW; max. 1.52 FW
68 68 68 68
Usually, 1.0 FW; max. 1.9 FW
77
Waterfowl; 8 spp.; northern Canada; 12 sites; 1988-1994; liver
313
a
3 3 3
Values are in mg Hg/kg fresh weight (FW) or dry weight (DW). a 1, Stickel et al., 1977; 2, Haseltine et al., 1980; 3, Parslow, 1973; 4, Nuorteva et al., 1975; 5, Turner et al., 1978; 6, White et al., 1980; 7, Vermeer and Peakall, 1979; 8, White et al., 1979; 9, Ui and Kitamuri, 1971; 10, Koivusaari et al., 1976; 11, Bernhard and Zattera, 1975; 12, Renzoni et al., 1973; 13, Lande, 1977; 14, Vannucchi et al., 1978; 15, Fimreite et al., 1980; 16, Wiemeyer et al., 1980; 17, Greichus et al., 1973; 18, Holden, 1973; 19, King et al., 1980; 20, Jones et al., 1972; 21, Gochfeld, 1980; 22, Luke et al., 1989; 23, Norheim et al., 1982; 24, Norheim and Kjos-Hanssen, 1984; 25, Szefer et al., 1993; 26, Bargagli et al., 1998; 27, Scheifler et al., 2005; 28, Thompson et al., 1992; 29, Monteiro et al., 1995; 30, Barrett et al., 1996; 31, Monteiro and Furness, 1997; 32, Hoffman et al., 1998; 33, Braune, 1987; 34, Thompson et al., 1991; 35, Ikemoto et al., 2004; 36, Becker et al., 1994; 37, Thompson et al., 1993; 38, Becker et al., 1993; 39, Dietz et al., 1996; 40, Dietz et al., 1990; 41, Karlog and Clausen, 1983; 42, Lewis et al., 1993; 43, Braune and Gaskin, 1987; 44, Lock et al., 1992; 45, Wiemeyer et al., 1988; 46, Audet et al., 1992; 47, Ohlendorf et al., 1985; 48, Mason et al., 1997; 49, Wenzel et al., 1996; 50, Thompson and Furness, 1989; 51, Kim et al., 1996a; 52, Tavares et al., 2005; 53, Mora, 1996; 54, King et al., 1991; 55, Rodriguez-Navarro et al., 2002; 56, Arai et al., 2004; 57, Custer et al., 2008; 58, Braune et al., 2006; 59, Braune, 2004; 60, Dietz et al., 1990; 61, Campbell et al., 2005; 62, Sanpera et al., 2007; 63, Sanpera et al., 2000; 64, Santos et al., 2006; 65, Ruelas-Inzunza et al., 2007; 66, Choong et al., 2007; 67, Burger and Gochfeld, 2007; 68, Braune and Malone, 2006; 69, Zhang et al., 2006; 70, Ackerman et al., 2007; 71, Kojadinovic et al., 2007; 72, Burger et al., 2007; 73, Perez-Lopez et al., 2006; 74, Horai et al., 2007; 75, Burger et al., 2007; 76, Kojadinovic et al., 2007a; 77, Braune and Malone, 2006a; 78, Henny et al., 1995; 79, Henny et al., 1991; 80, Ohlendorf et al., 1986; 81, Ohlendorf et al., 1988; 82, Braune, 2007; 83, Elliott et al., 2007; 84, Takekawa et al., 2002; 85, Wayland et al., 2001; 86, Wayland et al., 2002; 87, Wayland et al., 2005; 88, Liu et al., 2006; 89, Borga et al., 2006; 90, Dietz et al., 2006; 91, Henny et al., 2008; 92, Rattner et al., 2008; 93, Pollock and Machin, 2008; 94, Burger et al., 2008; 95, Braune and Scheuhammer, 2008; 96, Wayland et al., 2008; 97, Burger et al., 2008a.
314 Chapter 5 0.5-2.0 mg total mercury/kg FW in eggs are sufficient to induce impaired reproductive success in a variety of avian species (Thompson, 1996). It is noteworthy that most of the ivory gull eggs collected in 2004 exceeded 0.5 mg total mercury/kg FW and 33% exceeded 2.0 mg/kg FW (Braune et al., 2006). The increasing mercury concentrations over a 30-year period in eggs of ivory gulls from the Canadian Arctic—a gull population in decline— suggest that mercury is an important stressor contributing to population decline (Braune et al., 2006). Egg laying is an important route in reducing the female’s mercury body burden, especially the first egg, because egg mercury levels decline with laying sequence in gulls and terns (Becker, 1992; Lewis et al., 1993). In gulls and terns, 90% of the mercury in eggs is in the form of methylmercury (Becker et al., 1993). In kittiwakes, R. tridactyla, mercury concentrations in feathers and tissues decreased with increasing age, suggesting that egg contamination was more important in chicks than consumption of mercury-contaminated food (Wenzel et al., 1996). Eggs of fish-eating birds, including herons and grebes, collected near mercury point source discharges contained abnormal levels of mercury: 29% of eggs had more than 0.5 mg Hg/kg fresh weight and 9% had more than 1.0 mg/kg (Faber and Hickey, 1973). Parslow (1973) concludes that the main source of mercury in estuaries is probably from the direct discharge of effluents from manufacturing and refining industries into rivers. The high levels of mercury detected in eggs of the gannet, Morus bassanus, (Table 5.8) are within the range associated with adverse effects on hatchability in pheasants and sublethal effects in mallards (Fimreite et al., 1980); however, the gannets seem to reproduce normally at these levels. Some evidence exists linking eggshell thinning in ducks with increased concentrations of dietary methylmercury (Heinz, 1980b), but this requires verification. Mercury concentrations in livers of some Antarctic birds reflect mercury body burdens accumulated during migration while the birds were overwintering near industrialized areas; concentrations were highest in species that ate higher trophic levels of prey and this was especially pronounced in skuas, Catharcta spp. (Norheim and Kjos-Hanssen, 1984; Norheim et al., 1982). Increased concentrations of total mercury in livers of diving ducks were associated with lower weights of whole body, liver, and heart, with decreased activities of enzymes related to glutathione metabolism and antioxidant activity (Hoffman et al., 1998), and to decreased pancreas mass (Takekawa et al., 2002). Mercury levels were comparatively elevated in livers from three species of seabirds found dead or dying as a result of an oil spill in northwestern Spain in September 2002 (Perez-Lopez et al., 2006). Some seabirds demethylate methylmercury in the liver and other tissues, and store mercury as an immobilizable inorganic form in the liver; species with a high degree of demethylation capacity and slow molting patterns had low mercury burdens in feathers (Kim et al., 1996b). The recorded value of 97.7 mg Hg/kg dry weight in liver of dead or dying gannets, Sula bassanus (Table 5.8) requires clarification. It is possible that mercury accumulations of that magnitude were a contributory factor to death in this instance; however, the probable cause of death is from polychlorinated biphenyl poisoning (Parslow, 1973). Moreover, large
Birds
315
variations in mercury content in gannet liver were positively correlated with liver weight and negatively to fat content (Parslow, 1973). In osprey, P. haliaetus, the highest values recorded of 67.5 mg Hg/kg fresh weight in liver and 130.0 mg Hg/kg fresh weight in kidney are attributed to a single bird of 18 examined. These levels are clearly excessive, reflect high environmental exposure, and are similar to concentrations found in mercury-poisoned birds (Wiemeyer et al., 1980). The other 17 ospreys examined had maximum concentrations of 6.2 mg Hg/kg fresh weight in liver and 6.5 in kidney (Wiemeyer et al., 1980). Birds that eat aquatic fauna show markedly increased mercury accumulations when compared to terrestrial raptors (Greichus et al., 1973; Johnels and Westermark, 1969; Karppanen and Henriksson, 1970; Parslow, 1973). For example, mercury was highest in liver of cormorants and pelicans, with concentration factors for mercury of 14 over prey fish evident in cormorants and 6 in pelicans (Greichus et al., 1973). Seasonal variations in mercury levels are recorded in livers of aquatic birds (Table 5.8). Higher levels occurred in winter when birds were exclusively estuarine, and drastically lower in summer when birds migrated to inland Arctic region and sub-Arctic region breeding grounds (Parslow, 1973). It is possible that wintering populations—for example, knots Calidris spp.—may previously have accumulated mercury while molting in western European estuaries, notably on the Dutch Waddenzee (Parslow, 1973). Body condition and reproductive stage need to be considered when interpreting the significance of mercury burdens in tissues of eiders (Wayland et al., 2005). Hepatic mercury burdens were lower in prenesting birds than nesting birds, and change in response to normal changes in body and organ mass that occur during the reproductive period (Wayland et al., 2005). Total mercury and organic mercury were positively correlated in livers from eiders taken from the Canadian Arctic in June 1997 (Wayland et al., 2001). The number of nematode parasites was positively correlated with total and organic mercury. And body mass and spleen mass of eiders both decreased with increasing mercury burdens (Wayland et al., 2001). In 1999, hepatic mercury was negatively related to mass of abdominal fat, spleen, and body mass at capture in prenesting eiders (Wayland et al., 2002). There is considerable variability in mercury content of seabird feathers: concentrations in adults were higher than those in chicks, independent of adult age or gender (Kojadinovic et al., 2007; Thompson et al., 1991), and lower in spring breeders than autumn breeders (Monteiro et al., 1995). Mercury concentrations in feathers of little tern chicks, Sterna albifrons, were higher in smaller chicks than larger chicks and higher in early broods (1-3) than later broods (4-7), suggesting depletion of maternal transfer of mercury (Tavares et al., 2005). Methylmercury concentrations in feathers from two species of north Atlantic Ocean seabirds increased about 4.8% yearly between 1884 and 1994; increases were attributed to global increases in mercury loadings rather than to local or regional sources (Monteiro and Furness, 1997). Mercury concentrations in breast feathers of the king penguin were significantly lower in 2000-2001 (1.98 mg Hg/kg DW) than those collected from the same colony
316 Chapter 5 between 1966 and 1974 (2.66 mg/kg DW), and suggest that mercury concentrations in southern hemisphere seabirds do not increase significantly over time, which is in contrast to trends documented in the northern hemisphere (Scheifler et al., 2005). Mercury concentrations in feathers of herring gulls, L. argentatus, from the German North Sea coast were higher in adults than in juveniles and twice as high after 1940 than in earlier years (Thompson et al., 1993). A maximum of 12.0 mg Hg/kg fresh weight feathers during the 1940s was recorded, presumably due to high discharges of mercury during World War II (1939-1945). Concentrations dropped in the 1950s, increased in the 1970s to 10.0 mg Hg/kg FW before falling in the late 1980s; this pattern correlates well with known discharges of mercury into the Elbe and Rhine (Thompson et al., 1993). The extremely high levels in feathers of the endangered Audouin’s gull, Larus audouinii, from the western Mediterranean Sea—up to 22.1 mg Hg/kg DW in adults and 5.5 mg Hg/kg DW in chicks (Table 5.8)—is attributed to a fish diet from mercury-enriched waters, and to local pollution (Sanpera et al., 2007). Mercury concentrations in feathers of pigeon guillemots (Cepphus columba) collected in summer 2004 from various locations in Alaska were higher in females than in males (Burger et al., 2007), and significantly higher in Amchitka and Kiska Islands than Prince William Sound (Table 5.8). Molting is a major excretory pathway for mercury (Honda et al., 1986). Down and feathers were effective excretion routes of mercury in contaminated gull and tern chicks (Becker et al., 1994). After molting, new feathers contained up to 93% of the mercury body burden in gulls (Braune and Gaskin, 1987). Feathers represent the major pathway for elimination of mercury in seabirds, and body feathers are useful indicators for assessment of whole bird mercury burdens (Furness et al., 1986; Liu et al., 2006; Thompson et al., 1990); almost all mercury in feathers is present as methylmercury (Thompson and Furness, 1989). The keratin in bird feathers is not easily degradable, and mercury is probably associated with the disulfide bonds of keratin. Consequently, it is possible to compare mercury contents in feathers recently sampled with those from museum birds, thereby establishing a time series (Applequist et al., 1984; Monteiro and Furness, 1995; Odsjo et al., 1997; Thompson et al., 1992). It is generally acknowledged that feathers contain most of the total body burden of mercury, but comprise less than 15% of the body weight (Parslow, 1973). Mercury excretion is mainly via the feathers in both sexes, and also via the eggs (Parslow, 1973; Burger, 1994). Laboratory studies with the great skua, Catharcta skua, fed mercury-contaminated prey excreted mercury via feathers (Bearhop et al., 2000). Fish-eating birds from Sweden have higher concentrations of mercury in feathers than terrestrial raptorial species. Ospreys, which prey almost exclusively on larger fish of about 0.3 kg have higher mercury concentrations than the great crested grebe, Podiceps cristata, which feed mostly on small fish and insect larvae (Johnels and Westermark, 1969). Since larger fish contain more mercury per unit weight than smaller fish, diet must be considered an important factor to account for differences in mercury concentrations of ospreys and grebes. Based on samples from museum collections, it was shown that mercury content in feathers from fish-eating birds was comparatively low in the
Birds
317
period 1815 through 1940. However, since 1940 which marked the advent of the chloralkali industry, mercury concentrations in aquatic and fish-eating birds were elevated in the vicinity of chloralkali plants where mercury is used as a catalyst (Fimreite, 1974; Fimreite et al., 1971); these differences were detectable up to 300 km from the chloralkali plant (Fimreite and Reynolds, 1973). The most important variables in assessing blood mercury levels of shorebirds from San Francisco Bay in 2005-2006 were inherent species differences (higher in black-necked stilts, Himantopus mexicanus than in American avocet, Recurvirostra americana), higher in males than in females, and highest in birds from the southern end of San Francisco Bay (Ackerman et al., 2007; Table 5.8). Mercury-selenium interactions are significant in marine mammals; however, this is not always the case in oceanic birds. Mercury concentrations in oceanic birds—unlike results of laboratory studies with mallards—were usually not correlated with selenium burdens, as evidenced by values in livers of murres (Uria spp.) and razorbills (Alca torda), and in breast muscle of sooty terns (Sterna fuscata; Ohlendorf et al., 1978). However, in Braune’s petrel, P. baraui, mercury and selenium were significantly correlated in tissues analyzed; this was not the case in Audubon’s shearwater and the white-tailed tropicbird (Kojadinovic et al., 2007b). A mercury-selenium detoxifying interaction exists in at least two species of seabirds (Kojadinovic et al., 2007b). Mercury and selenium concentrations over the past 1500 years in Antarctic lake sediments amended by penguin excrements are positively correlated, suggesting a self-protection mechanism against mercury poisoning in penguins (Yin et al., 2007). Populations of the lesser scaup, A. affinis, and the greater scaup, Aythya marila have decreased from the 1980s and the 1990s and have not recovered (Pollock and Machin, 2008). Selenium, cadmium, and mercury interact and affect seminiferous tubule diameter in scaups; however, contaminant and trace element interactions were detected only in unpaired males. More research is merited on whether contaminants affect unpaired male scaups or whether unpaired males are predisposed to contaminant effects (Pollock and Machin, 2008). In laboratory studies mercury, as methylmercury, is lethal to mallards (A. platyrhynchos) given a single oral dose of 2.2-23.5 mg Hg/kg body weight, with 50% dead within 14 days (Hudson et al., 1984); for ethylmercury, this was 75.7 mg Hg/kg body weight, and for phenylmercury it was 524.7 mg Hg/kg body weight (Hudson et al., 1984). Pekin duck—a color variant of the mallard—age 6 months fed a diet containing 8.0 mg Hg/kg ration as methylmercury chloride for 12 weeks developed kidney histopathology; effects were exacerbated when diets also contained 80.0 mg/kg of lead or 80.0 mg/kg of cadmium (Rao et al., 1989). Interaction effects of mercury with selenium in mallard adults are documented (Heinz and Hoffman, 1998). In one 10-week study, mallards fed diets containing 10.0 mg Hg/kg dry weight as methylmercury chloride, 10.0 mg Se/kg as seleno-DL-methionine, or a mixture of the two, resulted in leg paralysis in the mercury diet but not in the mixture. Both the mercury and the selenium diets
318 Chapter 5 alone lowered duckling production through reduced hatching success and lowered survival; the mixture diet produced a dramatic decrease in duckling production and increased incidence of deformities. Other studies (Hoffman and Heinz, 1988) showed that the ability of selenoDL-methionine to restore the glutathione status involved in antioxidant defense mechanisms is important in protecting against the toxic action of methylmercury. Factors that affect the toxicity of methylmercury injected into eggs of the double crested cormorant, Phalacrocorax auritus, and mallards, A. platyrhynchos, include the embryonic stage of treatment, type and quantity of methylmercury solvent, formation of air bubbles in albumen, orientation during incubation, temperature and humidity during incubation, and site of injection (Heinz et al., 2006). These factors need to be considered in meaningful risk assessment studies of methylmercury and other toxicants to avian embryos. Accumulation and retention of mercury in ducks fed mercury-laden diets was investigated by Stickel et al. (1977), Finley and Stendell (1978), and Heinz (1979, 1980a). Mallard ducklings fed diets containing 8.0 mg Hg/kg fresh weight diet for 2 weeks contained—in mg Hg/kg fresh weight—16.5 in liver, 17.6 in kidney, 9.1 in carcass, and 4.4 in whole body (Stickel et al., 1977). After 16 weeks on a mercury-free diet, mercury concentrations in all tissues dropped, more or less progressively, to 25% of the 2-week concentrations. In another study, black duck adults were fed diets containing 3.0 mg Hg/kg fresh weight for 28 weeks (Finley and Stendell, 1978). Final maximum concentrations—in mg Hg/kg fresh weight—were 23.1 in liver, 65.7 in feathers, 3.8 in brain, 4.5 in muscle, and 16.0 in kidney. Breeding pairs fed this diet, when compared to controls, produced fewer eggs, lower egg hatch, and reduced duckling survival. Brains from dead ducklings from mercuryinsulted parents had lesions and contained 3.2-7.0 mg Hg/kg fresh weight (Finley and Stendell, 1978). However, methylmercury at 0.5 mg Hg/kg diet fresh weight had little measurable effect on mallards. In that study, three generations of game-farm mallards fed diets containing 0.5 mg Hg/kg diet as methylmercury, had elevated mercury burdens when compared to controls, but with little change between generations: 9.0-11.2 mg Hg/kg fresh weight in primary feathers, 1.5-1.8 in kidney, 0.9-1.6 in liver, and <0.9 in all other tissues. Mercury-dosed ducks weighed about the same as controls but laid fewer eggs and produced fewer ducklings (Heinz, 1979). Similar results were obtained with wildstrain ducks (Heinz, 1980a).
5.23 Molybdenum The highest concentration of molybdenum recorded in avian tissues is 8.0 mg/kg dry weight in kidney of the common merganser, Mergus merganser (Table 5.9). Data are missing on the effects of molybdenum on marine birds under controlled conditions; all studies conducted to date with molybdenum and birds have been restricted to domestic poultry (Eisler, 2000).
Birds
319
Table 5.9: Molybdenum, Nickel, and Rubidium Concentrations in Field Collections of Birds Element and Organism
Concentration
Reference
a
Molybdenum Alaska, near Ketchikan; 1980-1982 Barrows goldeneye, Bucephala islandica Kidney Liver Common merganser, Mergus merganser Kidney Liver
5.2-7.8 DW 4.8-6.2 DW
2 2
2.4-8.0 DW <1.9-5.7 DW
2 2
Arctic region seabirds; Barents Sea; May 1999; muscle Dovekie, Alle alle Thick-billed murre, Uria lomvia Black guillemot, Cepphus grylle
0.043 FW 0.034 FW 0.028 FW
Arctic region sea birds; Baffin Bay, Canada; May-June 1998; muscle vs. liver Dovekie Black-legged kittiwake, Rissa tridactyla Thick-billed murre Black guillemot Northern fulmar, Fulmaris glacialis Thayer’s gull, Larus thayeri
0.04 FW 0.04 FW 0.04 FW 0.03 FW 0.04 FW 0.04 FW
Gray heron, Ardea cinerea; Kanto area, Japan Liver Kidney Muscle Lung Brain
3.2 (2.0-5.1) DW 2.6 (1.8-4.7) DW 0.06 DW; max. 0.16 DW 0.19 DW 0.11 DW
14 14 14 14 14
Little penguin, Eudyptula minor; Australia; 2005; found dead Muscle Liver
0.5 FW; max. 4.4 FW 0.7 FW; max. 0.9 FW
12 12
Osprey, Pandion haliaetus; nestlings; Chesapeake Bay, 2000-2001 vs. Delaware Bay, 2002; max. values Blood Feathers
2.3 DW vs. 0.06 DW 0.52 DW vs. 1.6 DW
16 16
vs. vs. vs. vs. vs. vs.
15 15 15
0.69 FW 0.62 FW 0.76 FW 0.71 FW 0.54 FW 0.86 FW
15 15 15 15 15 15
(Continues)
320 Chapter 5 Table 5.9: Element and Organism
Cont’d
Concentration
Reference
a
Nickel Antarctica; February-March 1989 Gentoo penguin, Pygoscelis papua; muscle vs. liver Adelie penguin, Pygoscelis adeliae; muscle vs. liver Chinstrap penguin, Pygoscelis Antarctica Feces Liver Muscle Blue eyed cormorant, Phalacrocorax atriceps; muscle South giant petrel, Macronectes giganteus; muscle
<0.03 DW vs. 0.09 DW <0.03 D vs. 0.06 DW
3 3
3.5 (3.2-3.7) DW 0.07 DW <0.03 DW 0.29 DW
3 3 3 3
0.06 DW
3
Antarctica; molting feathers; 2002 vs. 2003 Chinstrap penguin Gentoo penguin
0.65 DW vs. 0.75 DW 0.8 DW vs. 2.2 DW
13 13
Arctic region seabirds; Barents Sea; May 1999; muscle Dovekie Thick-billed murre Black guillemot
0.045 FW 0.033 FW 0.038 FW
15 15 15
Arctic region sea birds; Baffin Bay, Canada; May-June 1998; muscle vs. liver Dovekie Black-legged kittiwake Thick-billed murre Black guillemot Northern fulmar Thayer’s gull
0.03 FW 0.02 FW 0.03 FW 0.03 FW 0.03 FW 0.02 FW
Gray heron, Ardea cinerea; liver; Japan
0.20 (0.02-2.5) DW
Redhead, Aythya americana; Texas and Louisiana; liver; winter 1987-1988
<4.0 DW
Canvasback, Aythya valisineria; Louisiana; liver; winter 1987-1988
Usually <1.0 DW; max. 2.0 DW
Herring gull, Larus argentatus; feathers; Arctic region; Spitsbergen, Svalbard; summer 1988
1.9-9.9 DW
5
1.0 DW 2.0 DW 5.0 DW
1 1, 6 1, 6
Lesser black-backed gull, Larus fuscus Muscle Liver Kidney
vs. vs. vs. vs. vs. vs.
0.09 FW 0.06 FW 0.04 FW 0.03 FW 0.03 FW 0.09 FW
15 15 15 15 15 15 14 4 11
(Continues)
Birds Table 5.9:
Cont’d
Element and Organism
Concentration
New Jersey; Raritan Bay; liver vs. salt gland Mallard, Anas platyrhynchos Black duck, Anas rubripes Greater scaup, Aythya marila
0.1-2.5 FW vs. 9.7 FW 0.2-2.7 FW vs. 15.2 FW 0.3-3.6 FW vs. 2.7 FW
Osprey, Pandion haliaetus; nestlings; Chesapeake Bay, 2000-2001 vs. Delaware Bay, 2002; max. values Blood Feathers
0.52 DW vs. 0.18 DW 4.1 DW vs. 41.4 DW
Common eider, Somateria mollissima Muscle Liver Kidney Egg
2.0 DW 1.0 DW 2.0 DW 1.0 DW
1 1 1 1
Max. 1.0 DW vs. 0.8-2.1 DW
9
Max. 36.0 DW Max. 26.0 DW <5.0 DW <2.0 DW
10 10 10 10
Arctic region seabirds; Barents Sea; May 1999; muscle Dovekie, Alle alle Thick-billed murre, Uria lomvia Black guillemot, Cepphus grylle
1.9 FW 1.4 FW 1.6 FW
15 15 15
Arctic region seabirds; Baffin Bay, Canada; May-June 1998; muscle vs. liver Dovekie Black-legged kittiwake, Rissa tridactyla Black guillemot Northern fulmar, Fulmaris glacialis Thayer’s gull, Larus thayeri
1.7 FW 1.4 FW 1.7 FW 2.2 FW 1.6 FW
Common tern, Sterna hirundo Rhode Island; immatures; liver vs. diet Long Island Sound, New York Bone Kidney Liver Muscle
321
Reference
a
7, 8 7, 8 7, 8
16 16
Rubidium
vs. vs. vs. vs. vs.
1.9 FW 1.9 FW 2.0 FW 2.7 FW 1.9 FW
15 15 15 15 15
Values are in mg element/kg dry weight (DW) or fresh weight (FW). a 1, Lande, 1977; 2, Franson et al., 1995; 3, Szefer et al., 1993a; 4, Michot et al., 1994; 5, Drbal et al., 1992; 6, Jenkins, 1980; 7, Burger and Gochfeld, 1985; 8, Gochfeld and Burger, 1987; 9, Custer et al., 1986; 10, Connors et al., 1975; 11, Custer and Hohman, 1994; 12, Choong et al., 2007; 13, Metcheva et al., 2006; 14, Horai et al., 2007; 15, Borga et al., 2006; 16, Rattner et al., 2008.
322 Chapter 5
5.24 Nickel Nickel concentrations in the organs of most avian wildlife species in unpolluted ecosystems range from about 0.1 to 2.0 mg/kg DW and occasionally reach 5.0 mg/kg DW (Eisler, 2000d; Outridge and Scheuhammer, 1993a; Table 5.9); however, ducks collected near a nickel smelter contained up to 12.5 mg Ni/kg dry weight in primary feathers (Ranta et al., 1978), herring gulls from Spitsbergen had up to 9.9 mg Ni/kg DW feather (Drbal et al., 1992), and salt glands of mallards and black ducks had 9.7-15.2 mg Ni/kg fresh weight (Table 5.9). Mallard (A. platyrhynchos) ducklings from fertile eggs treated at age 72 h with 0.0007 mg nickel as nickel mesotetraphenylporphine show a marked decrease in survival. Among survivors, there was a significant increase in the frequency of developmental abnormalities, a reduction in bill size, and a reduction in weight (Hoffman, 1979). Mallard ducklings, age 1 day, fed diets containing 0.0, 200.0, 800.0, or 1200.0 mg Ni/kg fresh weight ration, as nickel sulfate, for 90 days showed some effects at the high-dose diets (Cain and Pafford, 1981). At 800.0 mg/kg and lower, there was no effect on growth or survival, but a lower bone density in females at day 60; the 1200.0 mg/kg group experienced tremors, paresis, and 71% mortality by day 60. Livers and kidneys of survivors had 1.0 mg Ni/kg FW; dead birds had up to 22.7 mg Ni/kg liver FW, and 74.4 mg Ni/kg FW kidney (Cain and Pafford, 1981). In other feeding studies with mallards, breeding adults were fed diets containing up to 800.0 mg Ni/kg ration for 90 days (Eastin and O’Shea, 1981; Outridge and Scheuhammer, 1993a). There was no measurable effect on egg production, hatchability, or survival or resultant ducklings. Adults had normal blood chemistry and no organ histopathology. In the 50.0 mg Ni/kg diet group, nickel accumulated in feathers (5.2 mg Ni/kg DW vs. 0.9 in controls), in the 800.0 mg/kg group, birds had black tarry feces and elevated nickel burdens in kidneys (1.9 mg Ni/kg fresh weight vs. 0.09 in controls), liver (0.52 vs. 0.12), and blood (0.14 vs. 0.005); newly grown feathers had 68.0 mg Ni/kg dry weight (range 8.0-558.0) versus 0.9 (0.5-1.6) DW in controls. To protect birds, diets should contain at least 0.05 mg Ni/kg ration to prevent nickel deficiency, but less than 200.0 mg Ni/kg ration in the case of young birds and less than 800.0 mg/kg ration in the case of adults to prevent adverse effects on growth and survival (Cain and Pafford, 1981; Outridge and Scheuhammer, 1993a). It is emphasized that nickel accumulates in kidneys of mallards at dietary concentrations as low as 12.5 mg/kg ration (Eastin and O’Shea, 1981). Nickel concentrations in avian kidney in excess of 10.0 mg Ni/kg DW or in liver in excess of 3.0 mg/kg DW are sometimes associated with adverse effects (Outridge and Scheuhammer, 1993a); for mallards, these values are more than 1.0 mg/kg fresh weight for both kidney and liver (Cain and Pafford, 1981).
Birds
323
5.25 Plutonium Seabirds collected from the vicinity of Bylot Sound, Greenland, following accidental release of radioplutonium into that area, had normal background levels of that isotope; however, other taxonomic groups—mostly benthic invertebrates—had significantly elevated radioplutonium burdens (Aarkrog, 1971). Oystercatchers, H. ostralegus, from the vicinity of the Ravenglass nuclear facility in England, when compared to conspecifics from a reference site, had 20 and 45 times more 238Pu in muscle and liver, respectively; for 239þ240Pu, these values were 12 in muscle and 46 in liver (Lowe, 1991). Radioplutonium levels increased in eggshells of the black-headed gull, L. ridibundus ridibundus, after the Chernobyl nuclear reactor accident by factors up to 2.3 for 238Pu and 2.7 for 239þ240Pu (Lowe and Horrill, 1991). Four species of seabirds collected from the Aleutian Islands in summer 2004, with one exception, had no measurable levels of plutonium-238 or 239þ240Pu in breast muscle or bone, including samples from Amchitka Island—the site of underground nuclear tests between 1965 and 1971. The exception was bone of pigeon guillemot, C. columba, with above background levels of 239þ240Pu (Burger and Gochfeld, 2007).
5.26 Rubidium Livers from gray herons, A. cinerea, collected from a contaminated Japanese estuary contained an average of 39.4 mg Rb/kg dry weight, and a maximum of 75.7 mg Rb/kg DW; authors suggest that the elevated levels are due to ingestion of Rb-contaminated sediments (Horai et al., 2007). Rubidium was measurable in muscle and liver of all species of Arctic region seabirds analyzed in 1998-1999 at concentrations ranging from 1.4 to 2.7 mg Rb/kg FW (Table 5.9).
5.27 Selenium Kidneys from five species of shorebirds—including gulls, stilts, and an oystercatcher— collected from seven New Zealand estuaries contained mean selenium concentrations from each site that ranged from 1.18 to 4.10 mg Se/kg fresh weight (Table 5.10). Similar results for kidney were documented in seven species of shorebirds from Corpus Christi, Texas, during the winters of 1976 and 1977 (White et al., 1980). Selenium concentrations in feathers of the pigeon guillemot, C. columba, collected in summer 2004 from various locations in Alaska were higher in females than in males and sufficiently elevated (3.9 mg Se/kg DW) to pose a risk to health of the bird and their predators (Burger et al., 2007). In wild waterfowl, poor winter body condition may negatively affect migration, survival, and reproduction. In coastal California, total ash free protein in liver of the canvasback,
324 Chapter 5 Table 5.10: Selenium Concentrations in Field Collections of Birds Organism
Concentration
Western grebe, Aechmophorus occidentalis; Puget Sound, Washington; 1986; liver
7.6-9.3 (2.2-24.0) DW
10
8.0 DW 7.2-8.7 DW vs. 2.4 DW
38 38
1.5 (0.4-5.1) FW
27
Antarctica; molting feathers; 2002 vs. 2003 Chinstrap penguin, Pygoscelis Antarctica Gentoo penguin, Pygoscelis papua
No data vs. <0.8 DW 2.0 DW vs. 1.8 DW
18 18
Arctic region seabirds; Barents Sea; May 1999; muscle Dovekie, Alle alle Thick-billed murre, Uria lomvia Black guillemot, Cepphus grylle
2.3 FW 0.96 FW 1.1 FW
34 34 34
Arctic region seabirds; Baffin Bay, Canada; May-June 1998; muscle vs. liver Dovekie Black-legged kittiwake, Rissa tridactyla Thick-billed murre Black guillemot Northern fulmar, Fulmaris glacialis Thayer’s gull, Larus thayeri
2.0 FW 5.8 FW 1.3 FW 1.5 FW 4.1 FW 1.8 FW
Gray heron, Ardea cinerea; Kanto area, Japan Liver Kidney Muscle Lung Brain
9.8 DW; 7.4 DW; 1.8 DW; 3.9 DW; 1.1 DW;
Alaska; Prince William Sound; 2004; breast feathers Black oystercatcher, Haematopus bachmani Black-legged kittiwake, Rissa tridactyla; oiled vs. nonoiled Blue-winged teal, Anas discors; liver; 1998-1999; southern Texas
Lesser scaup, Aythya affinis; 2004-2005; males; kidney
vs. vs. vs. vs. vs. vs.
Reference
3.9 FW 11.2 FW 2.8 FW 4.8 FW 10.0 FW 4.7 FW
max. max. max. max. max.
39.7 DW 11.8 DW 3.1 DW 7.4 DW 1.7 DW
a
15 15 15 15 15 15 20 20 20 20 20
4.3 (2.1-12.7) DW
37
Canadian Arctic; June 1997; liver Common eider, Somateria mollissima; females King eider, Somateria spectabilis; males vs. females
19.4 (10.7-31.5) DW 19.9 DW vs. 18.7 DW
31 31
Great skua, Catharcta skua Kidney Liver
32.8 (13.3-89.1) DW 19.7 (6.7-34.6) DW
4 4 (Continues)
Birds Table 5.10:
Cont’d
Organism
Concentration
Pigeon guillemot, Cepphus columba; feather; Alaska; summer 2004 Prince William Sound Amchitka Kiska
2.61 DW 2.91 DW 3.90 DW
19 19 19
Black-footed albatross, Diomedea nigripes Liver Kidney
94.0 DW 62.0 DW
43 43
6.9 6.9 4.0 3.4
29 29 29 29
Diving ducks; coastal California; December 1986-March 1987; liver Canvasback, Aythya valisineria; early winter Adult females Adult males Juvenile females Juvenile males Greater scaup, Aythya marila Early winter Adult males Juvenile males Late winter Adult females Adult males Juvenile females Lesser scaup, Aythya affinis; late winter Adult males Juvenile males
325
(3.7-13.0) DW (3.4-18.0) DW (1.9-8.3) DW (0.9-13.0) DW
Reference
13.4 (7.6-23.7) DW 12.8 (5.8-22.3) DW
29 29
16.6 (8.9-31.0) DW 47.9 (13.0-140.0) DW 27.0 DW
29 29 29
a
11.2 (7.1-19.0) DW 11.9 (8.9-16.0) DW
Little egret, Egretta garzetta; Pearl River Delta, China; May 2000 Egg contents Chick feather
3.6 (2.0-5.9) DW 2.4 DW; max. 41.1 DW
Greenland; 1975-1991; seabirds; 9 spp. Kidney Liver Muscle
3.7-17.6 FW 1.9-14.1 FW 0.5-4.4 FW
3 3 3
Oystercatcher, Haematopus ostralegus Kidney Liver
12.7 (2.3-17.5) DW 12.8 (5.0-25.0) DW
5 5
Herring gull, Larus argentatus Kidney
14.1 (8.6-19.4) DW
5
17 17
(Continues)
326 Chapter 5 Table 5.10: Cont’d Organism Liver Egg; Long Island, New York; 1989-1991 Surf scoter, Melanitta perspicillata; liver SE Alaska; 1990-1991 Oregon/Washington; 1984-1985 California, San Francisco Bay 1982 1985 British Columbia; 1998-2001 White-winged scoter, Melanitta fusca; liver; declining populations
Concentration 7.9 (6.9-9.3) DW 1.0-2.1 DW
Reference 5 6
42.0 FW 6.5-13.0 FW
23 24
4.8-18.0 FW 15.0-22.0 FW 15.5-60.0 (9.8-128.0) DW
25 26 29
32.6 (28.4-37.3) DW
35
1.8 FW vs. 1.3 FW 16.9 DW vs. 8.9 DW
16 16
Norway; northern regions; summer 1992-1993 Kittiwake, Rissa tridactyla; adults vs. fledglings Feather Liver Common guillemot, Uria aalge Feather Gonad Kidney Liver Thick-billed murre, Uria lomvia Feather Gonad Kidney Liver
2.6 FW 21.9 DW 43.7 DW 17.6 DW
16 16 16 16
2.7 FW 12.2 DW 15.6 DW 17.6 DW
16 16 16 16
Black-crowned night-heron, Nycticorax nycticorax; 1998-1999; nestlings; feathers Baltimore Harbor, Maryland Holland Island, Maryland Pea Patch Island, Delaware
2.2 (1.8-2.7) DW 2.1 (1.9-2.3) DW 2.2 (1.9-2.5) DW
42 42 42
Osprey, Pandion haliaetus; nestlings; Chesapeake Bay, 2000-2001 vs. Delaware Bay, 2002; max. values Blood Feathers
18.2 DW vs. 21.2 DW 3.1 DW vs. 2.6 DW
36 36
12.9 (7.0-20.2) DW 11.1 (5.5-15.3) DW
12 12
9.4 (5.8-29.9) DW
12
Pacific Ocean coast; USA; 1984-1985; liver Dunlin, Calidris alpine Long-billed dowitcher, Limnodromus scolopaceus Black-bellied plover, Pluvialis squatorola
a
(Continues)
Birds Table 5.10:
Cont’d
Organism
Concentration
White-faced ibis, Plegadis chihi; egg
0.3-1.1 FW
Seabirds Liver; 11 spp. Most tissues; 3 spp.
Means 17.0-107.0 DW Max. 2.0-34.0 DW
15 15
Clapper rail, Rallus longirostris; eggshell; Georgia; 2000 Metals-contaminated marsh Reference site
0.9 (0.5-1.6) DW 0.7 (0.4-1.4) DW
44 44
36.1 DW vs. 81.7 DW 50.9 DW vs. 148.0 DW 15.8 DW vs. 37.9 DW
21 21 21
48.5 DW vs. 57.3 DW 89.9 DW vs. 145.0 DW 16.5 DW vs. 25.7 DW
21 21 21
43.7 DW vs. 68.5 DW 97.7 DW vs. 160.0 DW 11.2 DW vs. 23.3 DW
21 21 21
2.4-4.6 DW 3.3-4.5 DW 2.2-3.0 DW
28 28 28
5.3-36.2 DW
39
(1.0-15.0) FW (1.0-19.0) FW
40 40
0.3-1.1 FW 0.7-5.1 (0.2-7.3) FW 1.3-6.2 DW
2 4 11
Seabirds; 3 spp.; Reunion Island, western Indian Ocean; 2002-2004; juveniles vs. adults Barau’s petrel, Pterodroma baraui Liver Kidney Muscle Audubons’s shearwater, Puffinus lherminieri bailloni Liver Kidney Muscle White-tailed tropicbird, Phaethon lepturus Liver Kidney Muscle Seabirds; 3 spp.; Canadian Arctic; 1975-2003; egg contents Black-legged kittiwake, Rissa tridactyla Northern fulmar, Fulmaris glacialis Thick-billed murre, Uria lomvia Seabirds; 5 spp.; Canadian Arctic; 1991-1993; 5 spp.; liver Sea ducks; breeding females; 2001-2003; Canada; blood King eider, Somateria spectabilis White-winged scoter, Melanitta fusca Shorebirds 5 spp.; New Zealand estuaries; kidney 5 spp.; Baja California; 1986; liver 3 spp.; Cape May, New Jersey; 1991-1992; feathers
327
Reference
a
1
(Continues)
328 Chapter 5 Table 5.10: Cont’d Organism
Concentration
Black skimmer, Rynchops niger; New York; breast feathers
1.1-1.3 DW
14
1.6 DW 1.7 DW
41 41
17.2 14.1 32.1 16.6 16.6
32
Common eider, Somateria mollissima; summer 2007; Aleutian Islands, Alaska; females Feathers Eggs Northern common eider, Somateria mollissima borealis; eastern Canadian Arctic; liver 1998-1999 Females; 1998 vs. 1999 Males; 1999 Females; 1997-2000; prenesting vs. nesting Sooty tern, Sterna fuscata; egg
(11.2-47.0) DW vs. (8.5-31.5) DW (12.9-75.9) DW (14.2-19.6) DW vs. (14.3-19.3) DW
Reference
32 33
1.1-1.4 FW
7
0.8 DW
8
1.3 DW 2.1 DW 2.4 DW
8 8 8
Royal tern, Sterna maxima; egg
0.4-2.1 FW
9
Red-footed booby, Sula sula; egg
0.8-0.9 FW
7
Texas; 1984; mercury-contaminated bay vs. reference site; eggs minus shell Forster’s tern, Sterna forsteri Black skimmer, Rynchops niger
0.71 FW vs. 0.68 FW 0.8 FW vs. 0.3 FW
13 13
Usually <3.0 FW; frequently >3.0 FW; sometimes >10.0 FW
22
Common tern, Sterna hirundo; Massachusetts; May-June; feathers Fledglings; age 20-23 days Adults; various ages 2-3 years 9-10 years 16-21 years
Waterfowl; 8 spp.; northern Canada; 12 sites; 1988-1994; liver
a
Values are in mg Se/kg fresh weight (FW) or dry weight (DW). a 1, King et al., 1980; 2, Turner et al., 1978; 3, Dietz et al., 1996; 4, Mora and Anderson, 1995; 5, Hutton, 1981; 6, Burger and Gochfeld, 1995; 7, Ohlendorf and Harrison, 1986; 8, Burger et al., 1994; 9, King et al., 1983; 10, Henny et al., 1990; 11, Burger et al., 1993b; 12, Custer and Meyers, 1990; 13, King et al., 1991; 14, Burger and Gochfeld, 1992; 15, Kim et al., 1998; 16, Wenzel and Gabrielsen, 1995; 17, Zhang et al., 2006; 18, Metcheva et al., 2006; 19, Burger et al., 2007; 20, Horai et al., 2007; 21, Kojadinovic et al., 2007a; 22, Braune and Malone, 2006a; 23, Henny et al., 1995; 24, Henny et al., 1991; 25, Ohlendorf et al., 1986; 26, Ohlendorf et al., 1988; 27, Fedynich et al., 2007; 28, Braune, 2007; 29, Elliott et al., 2007; 30, Takekawa et al., 2002; 31, Wayland et al., 2001; 32, Wayland et al., 2002; 33, Wayland et al., 2005; 34, Borga et al., 2006; 35, DeVink et al., 2008; 36, Rattner et al., 2008; 37, Pollock and Machin, 2008; 38, Burger et al., 2008; 39, Braune and Scheuhammer, 2008; 40, Wayland et al., 2008; 41, Burger et al., 2008a; 42, Custer et al., 2008; 43, Arai et al., 2004; 44, Rodriguez-Navarro et al., 2002.
Birds
329
A. valisineria, decreased with increasing selenium burdens (Takekawa et al., 2002). Fatal chronic selenosis in aquatic birds is characterized by low body weight or emaciation, liver necrosis, enlarged kidneys (up to 40% heavier than normal), and more than 66.0 mg Se/kg dry weight liver (Albers et al., 1996). Selenomethionine was the most toxic form of selenium tested against mallards (Lemly et al., 1993). Mallard ducklings fed 8.0 mg Se/kg ration as selenomethionine for 120 days had hepatotoxicity as adults; 10.0 mg ration for 120 days inhibited reproduction; 15.0 mg/kg ration for 28 days inhibited growth; and 60.0 mg/kg ration for 60 days was fatal to all ducklings (Eisler, 2000a; Lemly et al., 1993). All fatal cases of selenomethionine-induced poisoning in mallards were characterized by histologic lesions of the liver, pancreas, spleen, and lymph nodes, and severe atrophy and degeneration of fat (Green and Albers, 1997). Stress response in eiders was related to hepatic selenium burdens (Wayland et al., 2002). Cell-mediated immunity, measured as the skin-swelling response to an intradermal injection of phytohemagglutinin-P was positively related to hepatic selenium. The heterophil/ lymphocyte ratio was inversely related to hepatic selenium. In 1998, selenium was positively related to mass of whole body, abdominal fat, kidney, and liver (Wayland et al., 2002). Breeding white-winged scoters, Melanitta fusca, and females with greater lipid mass had higher selenium burdens in liver than nonbreeders (max. 37.3 mg Se/kg DW), but there is no support for a relation between selenium and scoter population declines (DeVink et al., 2008; Wayland et al., 2008). Selenium burdens in other species of diving ducks were lower (max. 7.0 mg Se/kg DW) and these were unrelated to breeding status, lipid and protein levels, and mercury concentrations (DeVink et al., 2008). Embryotoxic and teratogenic effects of selenomethionine were observed in mallards at dietary concentrations exceeding 4.0 mg Se/kg dry weight ration in the laboratory, causing effects similar to those found in field studies (Heinz et al., 1987, 1989; Hoffman and Heinz, 1988, 1998). Excess dietary selenium as seleno-DL-methionine has a more pronounced effect on hepatic glutathione metabolism and lipid peroxidation than selenite (Hoffman et al., 1989), and may enhance selenium accumulation (Hoffman et al., 1989; Moksnes, 1983). In aquatic birds, developmental malformations were associated with lipid peroxidation in livers. Selenomethionine causes lipid peroxidation in livers of aquatic birds and this is consistent with the observation that selenomethionine is the primary causative agent of seleniuminduced embryonic mortality and overt teratogenesis in waterfowl (Hoffman et al., 1991a). Dietary selenomethionine effects were modified by salts of boron (Hoffman et al., 1991b; Stanley et al., 1996), arsenic (Hoffman et al., 1992a; Stanley et al., 1994), and protein composition (Hoffman et al., 1992b, 1996), with significant interactions between mixtures. Proposed dietary selenium criteria to protect mallards include: <10.0 mg/kg dry weight ration as the maximum tolerated concentration (Wiemeyer and Hoffman, 1996); <7.0<11.0 mg Se, as selenomethionine/kg dry weight for successful reproduction (Heinz and
330 Chapter 5 Fitzgerald, 1993a,b; Heinz et al., 1996; Lemly, 1996); <16.0 mg Se, as selenomethionine/kg dry weight ration to prevent formation of malformed embryos (Heinz and Fitzgerald, 1993b); and <10.0-<20.0 mg Se, as selenomethionine/kg dry weight ration to avoid lethality (Heinz and Fitzgerald, 1993a).
5.28 Silver Available data indicates that silver concentrations were highest (44.0 mg Ag/kg dry weight) in liver of the common eider, S. mollissima (Table 5.11), and that diet is implicated as the major source of elevated silver levels (Vermeer and Peakall, 1979). Eiders with elevated silver burdens in liver appear outwardly normal (Bryan and Langston, 1992). Silver concentrations Table 5.11: Silver, Strontium, and Tin Concentrations in Field Collections of Birds Element and Organism
Concentration
Reference
a
Silver Antarctica; February-March 1989 Southern giant petrel, Macronectes giganteus; muscle Blue-eyed cormorant, Phalacrocorax atriceps; muscle Adelie penguin, Pygoscelis adeliae Liver Muscle Chinstrap penguin, Pygoscelis antarctica Feces Liver Muscle Gentoo penguin, Pygoscelis papua Liver Muscle Arctic region seabirds; 1998-1999 Muscle Liver
0.001-0.003 FW 0.003-0.026 FW
Gray heron, Ardea cinerea; Kanto area, Japan Liver Kidney Muscle Lung Brain
2.2 DW; max. 20.1 DW 0.02 DW 0.006 DW 0.03 DW 0.06 DW
0.018 (0.017-0.020) DW
3
0.01 DW
3
0.02 DW 0.01 DW
3 3
0.18 (0.13-0.22) DW 0.05 DW 0.009 DW
3 3 3
0.43 (0.41-0.46) DW 0.01 DW
3 3 12 12
9 9 9 9 9 (Continues)
Birds Table 5.11: Element and Organism Greater scaup, Aythya marila British Columbia; Iona Island vs. Roberts Bank Liver Diet San Francisco Bay; March-April 1982; liver Lesser black-backed gull, Larus fuscus Muscle Liver Kidney Surf scoter, Melanitta perspicillata British Columbia; Iona Island vs. Roberts Bank Liver Diet San Francisco Bay; March-April 1982 Kidney Liver
331
Cont’d
Concentration
Reference
0.32 FW vs. 0.04 FW 0.015-0.029 FW vs. 0.006 FW 1.0 (0.4-3.1) DW
1 1 4, 5
3.0 DW 2.0 DW 1.0 DW
2 2 2
0.14 FW vs. 0.03 FW 0.026 FW vs. 0.004-0.01 FW
1 1
Max. 3.7 DW 0.9 (0.3-3.7) DW
4 4
Seabirds Liver; 11 spp. 3 spp.; max. values Most tissues Liver, gonad, fat
0.04-0.6 DW; max. 7.8 DW
6
<0.1 DW 0.1-0.2 DW
6 6
Common eider, Somateria mollissima Muscle Liver Kidney Egg
2.0 DW 44.0 DW 7.0 DW 1.0 DW
2 2 2 2
18.7 DW vs. 23.0 DW 47.0 DW vs. 59.0 DW
8 8
a
Strontium Antarctica; molting feathers; 2002-2003 Chinstrap penguin, Pygoscelis Antarctica Gentoo penguin, Pygoscelis papua Arctic region seabirds; Barents Sea; May 1999; muscle; 3 spp. Arctic region seabirds; Baffin Bay, Canada; May-June 1998; 6 spp. Muscle Liver
0.034-0.060 FW
12
0.02-0.19 FW 0.14-0.58 FW
12 12 (Continues)
332 Chapter 5 Table 5.11: Cont’d Element and Organism
Concentration
Reference
Black-crowned night-heron, Nycticorax nycticorax; 1998-1999; nestlings; feathers Baltimore Harbor, Maryland Holland Island, Maryland Pea Patch Island, Delaware
4.6 (2.4-8.8) DW 5.1 (3.9-6.8) DW 7.7 (5.3-11.2) DW
14 14 14
Osprey, Pandion haliaetus; nestlings; Chesapeake Bay, 2000-2001 vs. Delaware Bay, 2002; max. values Blood Feathers
0.88 DW vs. 0.72 DW 9.7 DW vs. 4.8 DW
13 13
0.009-0.056 FW; max. 0.76 FW 0.008-0.069 FW; max. 0.71 FW 0.01-0.13 (<0.008-1.49) FW
10 10 10
Not detected
11
0.034 (0.027-0.041) FW
11
0.021 (0.01-0.03) FW 0.018 (0.005-0.025) FW 0.004 (<0.005-0.008) FW 0.043 (0.015-0.064) FW 0.016 FW
11 11 11 11 11
(0.002-0.18) FW vs. (0.02-0.70) FW (0.02-0.39) FW vs. 0.01-0.30) FW (0.003-0.02) FW vs. (0.003-0.035) FW
11
a
Tin Surf scoter, Melanitta perspicillata; south coast British Columbia, Canada; 4 sites; 1998-2001; liver; butyltins Monobutyltins Dibutyltins Total butyltins Seabirds; coastal and inland species; adults Steller’s sea eagle, Haliaeetus pelagicus; Japan; April, 1991; kidney and liver Herring gull, Larus argentatus; Korea; March, 1993; kidney; total butyltins Black-tailed gull, Larus crassirostris; Korea; March 1993; kidney Monobutyltins Dibutyltins Tributyltins Total butyltins Black-headed gull, Larus ridibundus; Korea; March 1993; kidney; total butyltins Common cormorant, Phalacrocorax carbo; Japan; 1993-1994; kidney vs. Liver Monobutyltins Dibutyltins Tributyltins
11 11 (Continues)
Birds Table 5.11: Element and Organism Total butyltins Thick-billed murre, Uria lomvia; April 1991; Japan; total butyltins Kidney Liver Seabirds; adults; North Pacific Ocean 4 spp.; 1985-1989; kidney; total butyltins; maximum concentrations Laysan albatross, Diomedea immutabilis Kidney; 1985 Monobutyltins Dibutyltins Tributyltins Total butyltins Liver; 1989 Monobutyltins Dibutyltins Tributyltins Total butyltins Seabirds; adults; South Indian Ocean; 1992-1994; total butyltins Kidney Albatrosses, Diomedea spp.; 4 spp. Northern giant petrel, Macronectes halli Royal albatross, Diomedea epomophora Kidney Liver Light-mantled sooty albatross, Phoebetria palpebrata Kidney Liver Waterfowl; livers; 1995; butyltins Maine British Columbia; west coast
333
Cont’d
Concentration
Reference
0.09-0.30 FW; max. 0.54 FW vs. 0.28 FW; max. 1.01 FW
11
0.06 (0.03-0.09) FW 0.08 (0.03-0.17) FW
11 11
0.007-0.016 FW
11
0.006 (<0.005-0.010) FW 0.002 (<0.003-0.003) FW 0.001 (<0.000-0.002) FW 0.0085 (0.003-0.013) FW
11 11 11 11
0.028 (<0.005-0.071) FW 0.015 (0.007-0.031) FW 0.0004 (<0.001-0.004) FW 0.043 (0.007-0.110) FW
11 11 11 11
0.004-0.017 (0.001-0.029) FW 0.013 (0.006-0.022) FW
11 11
0.062 FW 0.058 FW
11 11
0.011 FW 0.010 FW
11 11
Max. 0.09 FW Max. 1.1 FW
a
7 7
Values are in mg Ag/kg fresh weight (FW) or dry weight (DW). a 1, Vermeer and Peakall, 1979; 2, Lande, 1977; 3, Szefer et al., 1993a; 4, Ohlendorf et al., 1986; 5, Bryan and Langston, 1992; 6, Kim et al., 1998; 7, Kannan et al., 1998; 8, Metcheva et al., 2006; 9, Horai et al., 2007; 10, Elliott et al., 2007; 11, Guruge et al., 1997; 12, Borga et al., 2006; 13, Rattner et al., 2008; 14, Custer et al., 2008.
334 Chapter 5 in muscle of Antarctic region birds were low (0.01 mg/kg DW) when compared to livers (0.02-0.46 DW), or feces (0.18 mg/kg DW; Szefer et al., 1993). Silver concentrations in avian tissues, especially in livers, were elevated in the vicinity of metals-contaminated areas and in diving ducks from the San Francisco Bay area (Table 5.11). No data were found on effects of silver compounds on avian wildlife under controlled conditions. On the basis of studies with domestic poultry, proposed silver criteria to protect avian wildlife is <100.0 mg total silver/L drinking water, and <200.0 mg total silver/kg diet (Eisler, 2000e).
5.29 Strontium Stable strontium concentrations in molting feathers of penguins in the Antarctica region in 2002 and 2003 ranged from 18.7 to 59.0 mg Sr/kg DW, and differed between species and years (Table 5.11; Metcheva et al., 2006). Analysis of muscle and bone from four species of seabirds collected in the Aleutian Islands during 2004 showed no 90Sr in any tissue or location, including Amchitka Island, the site of nuclear tests between 1965 and 1971 (Burger and Gochfeld, 2007).
5.30 Technetium As was true for 90Sr (see Section 5.29), no 99Tc was found in any seabird sample from any Aleutian Island collected during summer 2004 (Burger and Gochfeld, 2007).
5.31 Thallium Thallium burdens in muscle and liver from Arctic region seabirds captured in 1998-1999 ranged between 0.001 and 0.002 mg Tl/kg fresh weight (Borga et al., 2006). A maximum concentration of 0.10 mg Tl/kg dry weight in liver was measured in gray herons, A. cinerea, from a Japanese estuary (Horai et al., 2007).
5.32 Thorium A maximum concentration of 0.021 mg Th/kg dry weight liver was found in gray herons from a Japanese estuary (Horai et al., 2007).
5.33 Tin Oceanic birds, when compared to inland and coastal species, take up butyltins through feeding during breeding and migration in organotin-polluted coastal waters (Table 5.11). Oceanic species, however, have lower butyltin burdens than do inland species due, in part, to greater metabolism of butyltins and higher capacity to eliminate butyltins through molting and egg laying (Guruge et al., 1997).
Birds
335
Seaducks from western British Columbia contained up to 1.49 mg Sn (as butyltins)/kg FW liver (Table 5.11). Butyltin concentration in liver of the surf scoter, M. perspicillata, collected from industrialized harbors in British Columbia between 1998 and 2001 were comparatively elevated (Elliott et al., 2007; Table 5.11). Diet and proximity to tributyltin (TBT) affect butyltin concentrations in waterfowl (Kannan et al., 1998). Seaducks that feed mainly on molluscs had higher concentrations of butyltins in tissues than did predatory birds feeding on fish, other birds, and small mammals. Continued exposure of birds to butyltin compounds occurs in harbors and marinas where TBT is used in antifouling paints on vessels longer than 25 m (Kannan et al., 1998). Biomagnification of organotins in the food chain of common tern, S. hirundo on secondary carnivorous fish (flounder, cod, whiting, sole, etc.) is low (Veltman et al., 2006). Eggs of the common tern had biomagnification factors of 0.01 for TBTs and 0.18 for triphenyltins (TPT). Low biomagnification may be due to high metabolism of TBT and TPT by birds, high loss rate through molting of feathers, and preferential accumulation of organotins in liver and kidney (Veltman et al., 2006). Triorganotin compounds were especially toxic to aquatic birds (Eisler, 2000f). Among triorganotin compounds tested for toxicity to mallards, A. platyrhynchos, trimethyltins (and to a lesser extent, triethyltins) were the most toxic (Fleming et al., 1991). In a 75-day feeding study with mallard ducklings and 12 organotin compounds, the authors concluded that (1) trimethyltin was the most toxic compound tested; (2) a dietary level of 50.0 mg Sn (as trimethyltin chloride)/kg ration was fatal to all ducklings in 60 days; (3) 5.0 mg Sn (as trimethyltin chloride)/kg killed 40% of the ducklings, but all survived at 0.5 mg/kg diet; (4) death was preceded by mild to severe tremors, progressing to ataxia and lethargy; (5) trimethyltin-stressd ducklings showed degeneration of the large neurons of the pons, medulla oblongata, gray matter of the spinal cord, and pyramidal cells of the cerebral cortex; (6) all ducklings survived exposure to 50.0 mg Sn/kg ration of tetraethyltin, tetrabutyltin, tetraphenyltin, triethyltin chloride, tripropyltin chloride, TBT chloride, TBT oxide, TPT chloride, tricyclohexyltin chloride, dimethyltin chloride, and dibutyltin chloride; and (7) sublethal effects were recorded at 50.0 mg triethyltin chloride/kg ration (low body weight, vacuolization of spinal cord, and brain white matter), at 50.0 mg TBT chloride/kg ration (enlarged liver) and at 50.0 mg tetrabutyltin/kg diet (elevated kidney weight) (Fleming et al., 1991).
5.34 Tungsten Lead shot has been replaced largely by sintered-bronze spheres containing copper, tungsten, tin, and iron and would not pose a toxic risk to waterfowl when ingested (Thomas and McGill, 2008; USFWS, 2006). This decision is based, in part, on the studies of Mitchell et al. (2001a-c) on physiological effects of ingested tungsten-iron shot in mallards A. platyrhynchos over a period of 150 days.
336 Chapter 5 Mitchell et al. (2001a-c) found that continuous presence of tungsten-iron shot in duck gizzard for 150 days had no adverse effect on survival; mass of body, spleen, and gizzard; or architecture of liver and kidneys. About 28% of the initial tungsten was released into the gizzard, but had no toxic effects on adults, their reproduction, or their progeny; moreover, blood chemistry was unaffected. Tungsten was present in bone, liver, and kidney of adult ducks, but was not associated with adverse effects. Transfer of tungsten from adult females dosed from 150 days to eggs and ducklings did not affect egg production, fertility, and egg hatchability. Ducklings from mallards given the tungsten-iron shot had the same survivability, body mass, and blood chemistry as the controls. Authors concluded that tungsten as a tungsten-iron alloy shot present in adult ducks over 150 days had no significant effect on adult birds, their reproduction, and the viability of their progeny (Mitchell et al., 2001a-c).
5.35 Uranium Uranium concentrations in muscle samples from Arctic region seabirds captured in 19981999 ranged from 0.001 to 0.003 mg U/kg FW; for livers, this range was 0.001-0.004 mg U/kg FW (Borga et al., 2006). Livers from gray herons, A. cinerea, at a Japanese estuary had a mean content of 0.006 mg U/kg dry weight, and a maximum of 0.02 mg U/kg DW (Horai et al., 2007). No radiouranium-234, -235, or -236 was found in breast muscle or bone of four species of seabirds collected from the Aleutian Islands during summer 2004, including Amchitka Island, the site of nuclear tests between 1965 and 1971 (Burger and Gochfeld, 2007). However, measurable levels of 238U were found in one sample of tufted puffin, Fratercula cirrhata, and two samples from glaucous-winged gulls, Larus glaucescens (Burger and Gochfeld, 2007).
5.36 Vanadium Rattner et al. (2008) measured vanadium content in blood and feathers of nestling ospreys, P. haliaetus, from Chesapeake Bay and Delaware Bay during 2000-2002. The maximum concentration of vanadium in blood was 0.49 mg/kg DW; in feathers, it was 12.9 mg V/kg DW in Chesapeake Bay, and 1.1 mg V/kg DW in Delaware Bay. Vanadium content of liver in gray heron, A. cinerea, from a Japanese estuary had up to 0.38 mg V/kg dry weight (Horai et al., 2007). Livers from seven species of wintering shorebirds collected at Corpus Christi, Texas, during 1976-1977 contained between 0.02 and 1.20 mg V/kg fresh weight on average (White et al., 1980). Mean concentrations were highest in sanderlings Calidris alba, and in western sandpipers Calidris mauri, with some values in excess of 0.5 mg V/kg fresh weight liver. It was suggested that lipid metabolism in laying females are altered when liver vanadium content approaches or exceeds 0.5 mg/kg (White et al., 1980).
Birds
337
5.37 Zinc The coastal marine ecosystem of the United States receives at least 21,000 metric tons of zinc annually of which 21% is from atmospheric sources (Young et al., 1980), suggesting that avian coastal wildlife may be at increased risk to zinc via respiration. Zinc concentrations in marine birds normally range from 12.2 mg Zn/kg fresh weight in gull eggs to 87.6 mg Zn/kg fresh weight in liver of various species of New Zealand saltmarsh birds; however, elevated concentrations of 885.0 mg/kg dry weight in livers of herons from Rhode Island, and of 977.0 mg/kg dry weight in primary feathers of knots from the contaminated Dutch Wadden Sea are also documented (Table 5.12). In general, liver and kidney contain the highest concentrations of zinc, and muscle the lowest (Table 5.12). Increasing concentrations of zinc in livers of three species of diving ducks (Aythya spp.) overwintering in coastal California in Table 5.12: Zinc Concentrations in Field Collections of Birds Organism
Concentration
Blue-winged teal, Anas discors; Texas; 1983 Muscle; males vs. females Liver; autumn vs. spring
13.8 FW vs. 11.3 FW 41.4 FW vs. 33.7 FW
Admiralty Bay, Antarctica; January 2004 Adelie penguin, Pygoscelis adeliae Egg Feathers Kelp gull, Larus dominicanus; feather
8.3 DW 61.5-90.7 DW 93.5 DW
20 20 20
Antarctica; molting feathers; 2002 vs. 2003 Gentoo penguin, Pygoscelis papua Chinstrap penguin, Pygoscelis antarctica
106.0 DW vs. 89.0 DW 99.0 DW vs. 75.0 DW
24 24
Arctic region seabirds; Barents Sea; May 1999; muscle Dovekie, Alle alle Thick-billed murre, Uria lomvia Black guillemot, Cepphus grylle
11.9 FW 14.0 FW 14.6 FW
35 35 35
Arctic region seabirds; Baffin Island, Canada; May-June 1998; muscle vs. liver Dovekie Black-legged guillemot, Rissa tridactyla Thick-billed murre Black guillemot Northen fulmar, Fulmaris glacialis Thayer’s gull, Larus thayeri
11.2 FW 16.0 FW 14.2 FW 13.3 FW 20.5 FW 26.7 FW
vs. vs. vs. vs. vs. vs.
32.3 FW 35.6 FW 45.2 FW 35.8 FW 63.2 FW 44.3 FW
Reference
a
8 8
35 35 35 35 35 35 (Continues)
338 Chapter 5 Table 5.12: Cont’d Organism
Concentration
Gray heron, Ardea cinerea; Kanto area, Japan Liver Kidney Muscle Lung Brain
236.0 (79.3-1890.0) DW 99.4 DW; max. 407.0 DW 74.0 DW; max. 102.0 DW 50.9 DW; max. 104.0 DW 51.3 DW; max. 65.0 DW
Greater scaup, Aythya marila; British Columbia; Iona Island vs. Roberts Bank Liver Diet
41.6 FW vs. 40.2 FW 3.4-5.2 FW vs. 10.5 FW
1 1
Canvasback, Aythya valisineria; liver
41.0 FW
2
Cory’s shearwater, Calonectris diomedea; Azores; Portugal; 1992-1993; fledglings age 12 weeks Kidney Liver
111.0 (40.0-194.0) DW 199.0 (39.0-389.0) DW
10 10
99.3-106.0 FW vs. 99.6-97.4 FW 94.0 FW vs. 77.8 FW
32
119.4-139.0 FW vs. 116.0-130.4 FW 96.1-144.0 FW
32
120.5 (85.6-157.2) DW
33
188.2 DW vs. 135.3 DW
33
22.0 DW vs. 79.0 DW 57.0 DW vs. 170.0 DW
19 19
Canada; Pacific Northwest; 1989-1994; adults White-winged scoter, Melanitta fusca; males vs. females Kidney Liver Surf scoter, Melanitta perspicillata Liver; males vs. females Kidney Canadian Arctic; June 1997; liver Common eider, Somateria mollissima; females King eider, Somateria spectabilis; males vs. females Willet, Catoptrophorus semipalmatus;1994; San Diego Bay; sediments vs. stomach contents Naval air station Tijuana Slough National Wildlife Refuge
Reference
a
26 26 26 26 26
32
32
(Continues)
Birds Table 5.12: Organism Diving ducks; Baltic Sea; 2000-2004; found drowned in fishing nets; bone (tarsometatarsus) vs. cartilage (trachea) Scaup, Aythya marila Pochard, Aythya ferina Diving ducks; coastal California; December 1986-March 1987; liver Canvasback, Aythya valisineria; early winter Adult females Adult males Juvenile females Juvenile males Greater scaup, Aythya marila Early winter Adult males Juvenile males Late winter Adult females Adult males Juvenile females Lesser scaup, Aythya affinis; late winter Adult males Juvenile males Dutch Wadden Sea Knots; 3 spp.; recently formed primary feathers; juveniles vs. adults Geese; 3 spp; feather vane
Cont’d
Concentration
Reference
97.5 (61.3-137.6) DW vs. 150.6 (111.0-196.8) DW 103.5 (75.7-134.0) DW vs. 167.8 (124.5-229.1) DW
193.1 179.8 156.0 166.1
339
(160.0-233.0) (116.0-259.0) (153.0-159.0) (138.0-199.0)
27 27
DW DW DW DW
31 31 31 31
181.1 (170.0-193.0) DW 156.9 (134.0-175.0) DW
31 31
134.0 DW 170.0 (148.0-186.0) DW 157.0 DW
31 31 31
159.5 (148.0-183.0) DW 148.4 (142.0-155.0) DW
31 31
100.0-400.0 DW vs. max. 977.0 DW 93.0-164.0 DW; max. 330.0 DW
a
9 9
Little egret, Egretta garzetta; Pearl River Delta, China; May 2000 Egg contents Chick feather
8.7 DW; max. 556.0 DW 18.7 DW; max. 1030.0 DW
22 22
Little penguin, Eudyptula minor; Australia; 2005; found dead Muscle Liver
10.0 FW; max. 12.8 FW 39.0 FW; max. 66.9 FW
21 21 (Continues)
340 Chapter 5 Table 5.12: Cont’d Organism
Concentration
Korea; 2001; chicks; black-crowned night heron, Nycticorax nycticorax vs. gray heron, Ardea cinerea Liver Kidney Muscle Bone Feather
40.2 FW 28.3 FW 16.0 FW 40.9 FW 38.3 FW
Herring gull, Larus argentatus; egg
12.2-12.5 FW
4
Lesser black-backed gull, Larus fuscus Muscle Liver Kidney
55.0 DW 89.0 DW 116.0 DW
5 5 5
Glaucous gull, Larus hyperboreus Liver Kidney
32.0 (26.0-47.0) FW 46.0 (37.0-57.0) FW
Surf scoter, Melanitta perspicillata British Columbia; Iona Island vs. Roberts Bank Liver Diet Strait of Georgia, Pacific Ocean coast of Canada; winter 1998-2001; kidney; Females; juveniles vs. adults Males; juveniles vs. adults Mexico; Gulf of California; 1999-2000; muscle Brown pelican, Pelecanus occidentalis Cormorant, Phalacrocorax brasilianus Black-crowned night-heron, Nycticorax nycticorax Liver; prefledglings; 1979 Massachusetts North Carolina Rhode Island Feathers; nestlings; 1998-1999 Baltimore Harbor, Maryland Holland Island, Maryland Pea Patch Island, Delaware
vs. vs. vs. vs. vs.
39.2 FW 22.8 FW 14.8 FW 44.4 FW 50.9 FW
35.9 FW vs. 3.0-21.3 FW 12.5 FW vs. 31.0 FW
105.0 114.0 103.0 129.0
(90.0-117.0) DW vs. (105.0-167.0) DW (88.0-121.0) DW vs. (60.0-195.0) DW
Reference
a
38 38 38 38 38
11 11
1 1
23, 29 23, 29
23.3 DW 35.0 DW
39 39
602.0 (482.0-784.0) DW 649.0 (479.0-857.0) DW 503.0 (246.0-885.0) DW
12 12 12
127.4 (102.1-159.1) DW 155.1 (143.1-168.1) DW 168.8 (149.8-190.1) DW
41 41 41 (Continues)
Birds Table 5.12: Organism
Cont’d
Concentration
Reference
Osprey, Pandion haliaetus; liver Immatures vs. adults Eastern USA; 1975-1982 Maryland Massachusetts New Jersey North Carolina South Carolina Virginia Eastern USA; 1964-1973 Florida Maryland New Jersey
19.0-34.0 FW 89.0 FW 61.0-120.0 FW 69.0 FW 73.0 FW 27.0-150.0 FW
13 13 13 13 13 13
(27.0-36.0) FW (18.0-93.0) FW 22.0 FW
6 6 6
Osprey; nestlings; Chesapeake Bay, 2000-2001 vs. Delaware Bay, 2002; max. values Blood Feathers
30.5 DW vs. 54.0 DW 131.0 DW vs.128.0 DW
36 36
6.4 (5.5-8.0) FW 6.4 (4.3-8.3) FW
14 14
26.0 FW 41.0-50.0 FW 33.0 FW
14 14 14
32.0-55.0 FW 31.0-38.0 FW
14 14
Clapper rail, Rallus longirostris; eggshell; Georgia; 2000 Metals-contaminated marsh Reference site
6.3 (2.2-19.4) DW 4.8 (2.2-11.7) DW
42 42
Black-legged kittiwake, Rissa tridactyla; nestlings; Germany; 1992-1994; age 1 day vs. age 21-40 days Brain Feather Kidney Liver
69.0 DW vs. 66.0 DW 79.0 DW vs. 116.0 DW 104.0 DW vs. 120.0 DW 66.0 DW vs. 111.0 DW
15 15 15 15
Brown pelican, Pelecanus occidentalis Egg contents South Carolina; 1971-1972 Florida; 1969-1970 Liver; found dead South Carolina; 1973 Florida; 1972-1973 Georgia; 1972 Liver; shot Florida; 1970 South Carolina; 1973
341
67.0 FW vs. 38.0 FW
a
6
(Continues)
342 Chapter 5 Table 5.12: Cont’d Organism Seabirds Albatrosses; 3 spp.; liver vs. kidney Fulmars; 2 spp; liver vs. kidney Penguins; 4 spp.; liver vs. kidney Petrels; 7 spp.; liver vs. kidney Seabirds; 3 spp.; Reunion Island, western Indian Ocean; 2002-2004; juveniles vs. adults Barau’s petrel, Pterodroma baraui Liver Kidney Muscle Audubon’s shearwater, Puffinus lherminieri bailloni Liver Kidney Muscle White-tailed tropicbird, Phaethon lepturus Liver Kidney Muscle
Concentration
(29.0-66.0) FW vs. (31.0-65.0) FW 36.0-95.0 FW vs. 32.0-96.0 FW (27.0-73.0) FW vs. (25.0-71.0) FW (28.0-81.0) FW vs. (15.0-78.0) FW
Reference
11 11 11 11
119.0 DW vs. 316.0 DW 137.0 DW vs. 235.0 DW 73.1 DW vs. 101.0 DW
28 28 28
209.0 DW vs. 288.0 DW 110.0 DW vs. 224.0 DW 55.6 DW vs. 73.0 DW
28 28 28
528.0 DW vs. 305.0 DW 193.0 DW vs. 241.0 DW 101.0 DW vs. 86.7 DW
28 28 28
Means 108.0-186.0 DW 208.0 DW 101.0-200.0 DW
16 16 16
<100.0 DW
16
Seabirds; South Atlantic Ocean; adults; 15 spp.; kidney vs. liver
28.0-63.0 (15.0-88.0) FW vs. 27.0-67.0 (18.0-86.0) FW
17
Seabirds; 3 spp.; Spain; 2002-2003; found dead or dying after oil spill; liver
27.0-73.0 (14.9-100.2) DW
25
Seabirds; 5 sp.; Canadian Arctic; 1991-1993; breeding season; kidney
106.0-199.0 (84.4-254.0) DW
40
Seabirds; 14 spp. Liver; 11 spp. Pancreas; 3 spp. Intestine, liver, spleen, kidney, bone eyeball; 3 spp. Brain, lung, heart, gonad, muscle, skin, gall bladder, uropygial gland, stomach, feather trachea, esophagus; 3 spp.
a
(Continues)
Birds Table 5.12:
Cont’d
Organism
Concentration
Shearwaters; 2 spp.; liver vs. kidney
(28.0-54.0) FW vs. (27.0-88.0) FW
11
Shorebirds; 5 spp.; Korea; 1994-1995 Feathers Liver
67.9-88.4 (43.3-132.0) FW 20.6-39.5 (10.6-43.6) FW
37 37
Shorebirds; 5 spp.; New Zealand; liver
21.1-87.6 FW
Skuas; 3 spp.; liver vs. kidney
(21.0-51.0) FW vs. (22.0-53.0) FW
Common eider, Somateria mollissima Muscle Liver Kidney Egg Northern gannet, Sula bassanus; liver; dead or dying birds
Reference
a
3 11
33.0 DW 204.0 DW 117.0 DW 56.0 DW
5 5 5 5
100.0-541.0 DW
7
Red-footed booby, Sula sula; South China Sea; 2003 Feces Wing bone Eggshell Feather
419.4 (135.0-574.0) DW 160.0 DW 20.0 DW 50.0 DW
34 34 34 34
Guillemot, Uria aalge; Belgium; winter; 1993-1998; normal vs. severely emaciated Liver Kidney Muscle
138.4 DW vs. 203.6 DW 157.6 DW vs. 201.7 DW 63.9 DW vs. 79.3 DW
30 30 30
9.2-13.4 (7.2-21.0) FW
18
Waterbirds; lower Laguna Madre, Texas; 4 spp.; 1993-1994; egg contents
343
Values are in mg Zn/kg fresh weight (FW) or dry weight (DW). a 1, Vermeer and Peakall, 1979; 2, White et al., 1979; 3, Turner et al., 1978; 4, Peden et al., 1973; 5, Lande, 1977; 6, Wiemeyer et al., 1980; 7, Parslow et al., 1973; 8, Warren et al., 1990; 9, Goede, 1985; 10, Stewart et al., 1997; 11, Thompson, 1990; 12, Custer and Mulhern, 1983; 13, Wiemeyer et al., 1987; 14, Blus et al., 1977; 15, Wenzel et al., 1996; 16, Kim et al., 1998; 17, Muirhead and Furness, 1988; 18, Mora, 1996; 19, Hui and Beyer, 1998; 20, Santos et al., 2006; 21, Choong et al., 2007; 22, Zhang et al., 2006; 23, Harris et al., 2007; 24, Metcheva et al., 2006; 25, Perez-Lopez et al., 2006; 26, Horai et al., 2007; 27, Kalisinska et al., 2007; 28, Kojadinovic et al., 2007a; 29, Elliott et al., 2007; 30, Debacker et al., 2000; 31, Takekawa et al., 2002; 32, Barjaktarovic et al., 2002; 33, Wayland et al., 2001; 34, Liu et al., 2006; 35, Borga et al., 2006; 36, Rattner et al., 2008; 37, Kim and Koo, 2008b; 38, Kim and Koo, 2008a; 39, Ruelas-Inzunza and Paez-Osuna, 2008; 40, Braune and Scheuhammer, 2008; 41, Custer et al., 2008; 42, Rodriguez-Navarro et al., 2002.
344 Chapter 5 1986-1987 were associated with decreases in total carcass fat, pancreas mass, and carcass mass (Takekawa et al., 2002). A high concentration of zinc of 541.0 mg Zn/kg dry weight liver is recorded in northern gannets found dead or dying; death was not from zinc poisoning but from polychlorinated biphenyls (Parslow et al., 1973). It is possible that the elevated zinc concentrations in these birds were a manifestation of toxicant-induced stress, as has been proposed for several taxonomic groups. Zinc concentrations in avian tissues are usually less than 210.0 mg/kg dry weight, but are elevated near zinc-contaminated sites, and are modified—with no clear trend—by a host of biological and abiotic variables (Eisler, 2000g). In diving ducks, Aythya spp., from the Baltic Sea between 2000 and 2004, zinc was significantly higher in cartilage tissue (trachea) than bone (tarsometatarsus), and higher than iron, lead, copper, and cadmium, in that order; this pattern held for all metals and tissues (Kalisinska et al., 2007). In nestling kittiwakes, R. tridactyla, zinc concentrations increased in liver and feathers throughout chick growth (Wenzel et al., 1996). In black-crowned night-herons, N. nycticorax, zinc concentrations were usually higher in younger birds, although weight and gender had no direct effect on zinc content (Custer and Mulhern, 1983). Zinc concentrations in liver of osprey, P. haliaetus, were similar between age groups and genders (Wiemeyer et al., 1987). In the blue-winged teal, A. discors, zinc concentrations were higher in liver than in muscle, higher in males than in females, and higher in autumn than in the spring (Warren et al., 1990). Zinc concentrations in sediments of the Rhine River increased about sixfold between 1900 and 1950 and have remained stable since then; however, migratory waterfowl from this collection locale do not have elevated zinc concentrations in their primary feathers (Goede, 1985). Seabirds with high zinc concentrations in liver and kidney tend to have high cadmium levels in these tissues (Muirhead and Furness, 1988). In ducks, zinc selectively competes with cadmium in high and low molecular weight protein pools in kidney and liver. Once the high molecular weight protein pool is zinc-saturated, excess zinc is stored in metal-binding proteins, with serious implications for waterfowl stressed simultaneously with cadmium and zinc (Brown et al., 1977). Conversely, a cadmium-induced disease in bone collagen of chicks was prevented by zinc (Kaji et al., 1988). Low molecular weight proteins called metallothioneins play an important role in zinc homeostasis and in protection against zinc poisoning; zinc is a potent inducer of metallothioneins (Eisler, 2000g; Kojadinovic et al., 2007b). To prevent zinc deficiency in ducklings, diets should contain 25.0-38.0 mg Zn/kg DW ration; for adequate to optimal growth, diets should contain 93.0-128.0 mg Zn/kg DW; to prevent marginal sublethal effects, diets need to contain less than 178.0 mg Zn/kg DW; and to prevent death, diets should have less than 2000.0 mg Zn/kg DW (Eisler, 2000g; Gasaway and Buss, 1972; Grandy et al., 1968; Kazacos and Van Vleet, 1989; USNAS, 1979). Dietary zinc absorption is highly variable; in general, it increases with low body weight and low zinc status, and decreases with excess calcium or phytate and by deficiency of pyridoxine or tryptophan (Eisler, 2000g).
Birds
345
Mallards given a single oral dose of 517.0-742.0 mg Zn/kg body weight were poisoned (Eisler, 2000g; Grandy et al., 1968). Zinc-poisoned mallards force-fed zinc shot pellets developed ataxia, paresis, and total loss of muscular control in their legs, including the ability to swim (Wobeser, 1981). Mallards force-fed zinc metal shot equivalent to 450.0 mg Zn/kg body weight all survived for 28 days; tissue burdens at day 28, in mg Zn/kg DW, were 217.0 in liver, 79.0 in kidney, and 126.0 in feather (French et al., 1987). Ducks, Anas spp., had reduced survival, elevated tissue zinc concentrations, and pancreas histopathology when fed diets containing 2500.0-3000.0 mg Zn/kg DW ration or when force-fed zinc metal shot equivalent to 742.0-990.0 mg Zn/kg body weight (French et al., 1987; Grandy et al., 1968; Kazacos and Van Vleet, 1989; USNAS, 1979). Mallards fed 3000.0 mg Zn/kg DW ration for 60 days had diarrhea after 15 days, leg paralysis in 20 days, high mortality after 30 days, and zinc residues at day 60 that were 14 times higher in pancreas than in controls, 7 times higher in liver, 15 times higher in kidney, and 2-4 times higher in adrenals, muscle, testes, and ovary (Gasaway and Buss, 1972). The pancreas seems to be a primary target organ of zinc intoxication in birds, followed by bone (Eisler, 2000g). Pancreas pathology is documented in experimentally induced zinc toxicosis in ducklings. Pancreatic changes were limited to aciner cells, specifically, cytoplasmic vacuolation, cellular atrophy, and eventually cell death (Kazacos and Van Vleet, 1989; Lu and Combs, 1988). Zinc excess may cause stimulation of bone resorption and inhibition of bone formation in chicks (Kaji et al., 1988). Biological effects of excess zinc are modified by numerous variables, especially interactions with other chemicals, Interactions frequently produce radically altered patterns of accumulation, metabolism, and toxicity. Some are beneficial to the organism while others are harmful (Eisler, 2000g). Zinc-poisoned birds frequently contain 75.0-156.0 mg Zn/kg DW liver versus 21.0-33.0 in controls (Reece et al., 1986), and 15.5 mg Zn/L plasma versus <0.002 mg/L in controls (Morris et al., 1986). Although tissue residues are not yet reliable indicators of zinc contamination, there is general agreement that zinc-poisoned birds contain more than 2100.0 mg Zn/kg DW in liver or kidney (Eisler, 2000g).
5.38 Literature Cited Aarkrog, A., 1971. Radioecological investigations of plutonium in an arctic marine environment. Health Phys. 20, 31–47. Ackerman, J.T., Eagles-Smith, C.A., Takekawa, J.Y., Demers, S.A., Adelsbach, T.L., Bluso, J.D., et al., 2007. Mercury concentrations and space use of pre-breeding American avocets and black-necked stilts in San Francisco Bay. Sci. Total Environ. 384, 452–466. Aguirre-Alvarez, A.A., 1989. Clinical and toxicological findings in Caribbean flamingos (Phoenicopterus ruber ruber) during a recent outbreak of lead poisoning in Yucatan, Mexico. In: Proc. 1989 Ann. Meet. Amer. Assn. Zoo Veterin., Greensboro, North Carolina, 14–19 October 1989, pp. 209–212. Albers, P.H., Green, D.E., Sanderson, C.J., 1996. Diagnostic criteria for selenium toxicosis in aquatic birds: dietary exposure, tissue concentrations, and macroscopic effects. J. Wildl. Dis. 32, 468–485; 725–726.
346 Chapter 5 Anteau, M.J., Afton, A.D., Custer, C.M., Custer, T.W., 2007. Relationships of cadmium, mercury, and selenium with nutrient reserves of female lesser scaup (Aythya affinis) during winter and spring migration. Environ. Toxicol. Chem. 26, 515–520. Applequist, H., Asbirk, S., Draback, I., 1984. Mercury monitoring: mercury stability in bird feathers. Mar. Pollut. Bull. 15, 22–24. Arai, T., Ikemoto, T., Hokura, A., Terada, Y., Tanabe, S., Nakai, I., 2004. Chemical forms of mercury and cadmium accumulated in marine mammals and seabirds as determined by XAFS analysis. Environ. Sci. Technol. 38, 6468–6474. Atwell, L., Hobson, K.A., Welch, H.E., 1998. Biomagnification and bioaccumulation of mercury in an arctic marine food web: insights from stable nitrogen analysis. Can. J. Fish. Aquat. Sci. 55, 1114–1121. Audet, D.J., Scott, D.S., Wiemeyer, S.N., 1992. Organochlorines and mercury in osprey eggs from the eastern United States. J. Raptor Res. 26, 219–224. Bargagli, R., Monaci, F., Sanchez-Hernandez, J.C., Cateni, D., 1998. Biomagnification of mercury in an Antarctic marine coastal food web. Mar. Ecol. Prog. Ser. 169, 65–76. Barjaktarovic, L., Elliott, J.E., Scheuhammer, A.M., 2002. Metal and metallothionein concentrations in scoter (Melanitta spp.) from the Pacific northwest of Canada, 1989–1994. Arch. Environ. Contam. Toxicol. 43, 486–491. Barrett, R.T., Skaare, J.U., Gabrielsen, G.W., 1996. Recent changes in levels of persistent organochlorines and mercury in eggs of seabirds from the Barents Sea. Environ. Pollut. 92, 13–18. Bearhop, S., Ruxton, G.D., Furness, R.W., 2000. Dynamics of mercury in blood and feathers of great skuas. Environ. Toxicol. Chem. 19, 1638–1643. Becker, P.H., 1992. Egg mercury levels decline with the laying sequence in charadriiformes. Bull. Environ. Contam. Toxicol. 48, 762–767. Becker, P.H., Furness, R.W., Henning, D., 1993. The value of chick feathers to assess spatial and interspecific variation in the mercury contamination of seabirds. Environ. Monitor. Assess. 28, 255–262. Becker, P.H., Henning, D., Furness, R.W., 1994. Differences in mercury contamination and elimination during feather development in gull and tern broods. Arch. Environ. Contam. Toxicol. 27, 162–167. Bellrose, F.C., 1951. Effects of ingested lead shot upon waterfowl populations. Trans. 16th N. Am. Wildl. Conf. 125–135. Bernhard, M., Zattera, A., 1975. Major pollutants in the marine environment. In: Pearson, E.A., Frangipane, E.D. (Eds.), Marine Pollution and Marine Waste Disposal. Pergamon, Elmsford, NY, pp. 195–300. Beyer, W.N., Spann, J.W., Sileo, L., Franson, J.C., 1988. Lead poisoning in six captive avian species. Arch. Environ. Contam. Toxicol. 17, 121–130. Beyer, W.N., Audet, D.J., Morton, A., Campbell, J.K., LeCaptain, L., 1998a. Lead exposure of waterfowl ingesting Coeur d’Alene River Basin sediments. J. Environ. Qual. 27, 1533–1538. Beyer, W.N., Day, D., Morton, A., Pachepsky, Y., 1998b. Relation of lead exposure to sediment ingestion in mute swans on the Chesapeake Bay, USA. Environ. Toxicol. Chem. 17, 2298–2301. Beyer, W.N., Franson, J.C., Locke, L.N., Stroud, R.K., Sileo, L., 1998c. Retrospective study of the diagnostic criteria in a lead-poisoning survey of waterfowl. Arch. Environ. Contam. Toxicol. 35, 506–512. Birkhead, M., 1983. Lead levels I the blood of mute swans Cygnus olor on the River Thames. J. Zool. (London) 199, 59–73. Blus, L.J., 1994. A review of lead poisoning in swans. Comp. Biochem. Physiol. 108C, 259–267. Blus, L.J., Neely Jr., B.S., Lamont, T.G., Mulhern, B.M., 1977. Residues of organochlorines and heavy metals in tissues and eggs of brown pelicans, 1969–73. Pestic. Monit. J. 11, 40–53. Blus, L.J., Stroud, R.K., Reiswig, B., McEneaney, T., 1989. Lead poisoning and other mortality factors in trumpeter swans. Environ. Toxicol. Chem. 8, 263–271. Blus, L.J., Henny, C.J., Hoffman, D.J., Grove, R.A., 1991. Lead toxicosis in tundra swans near a mining and smelting complex in northern Idaho. Arch. Environ. Contam. Toxicol. 21, 549–555.
Birds
347
Borga, K., Campbell, L., Gabrielsen, G.W., Norstrom, R.J., Muir, C.G., Fiske, A.T., 2006. Regional and species specific bioaccumulation of major and trace elements in Arctic seabirds. Environ. Toxicol. Chem. 25, 2927–2936. Boyer, I.J., Di Stefano, V., 1985. An investigation of the mechanism of lead-induced relaxation of pigeon crop smooth muscle. J. Pharmacol. Exp. Ther. 234, 616–623. Boyer, I.J., Cory-Slechta, D.A., Di Stefano, V., 1985. Lead induction of crop dysfunction in pigeons through a direct action on neural or smooth muscle components of crop tissue. J. Pharmacol. Exp. Ther. 234, 607–615. Braune, B.M., 1987. Comparison of total mercury levels in relation to diet and molt for nine species of marine birds. Arch. Environ. Contam. Toxicol. 16, 217–224. Braune, B., 2004. Contaminants in Arctic seabird eggs. In: Smith, S., Stow, J., Carillo, F. (Eds.), Synopsis of Research Conducted Under the 2003-2004 Northern Contaminants Program. Indian and Northern Affairs Canada, Ottawa, Canada, pp. 115–120. Braune, B.M., 2007. Temporal trends of organochlorines and mercury in seabird eggs from the Canadian Arctic, 1975–2003. Environ. Pollut. 148, 599–613. Braune, B.M., Gaskin, D.E., 1987. Mercury levels in Bonaparte’s gulls (Larus philadelphia) during autumn molt in the Quoddy region, New Brunswick, Canada. Arch. Environ. Contam. Toxicol. 16, 539–549. Braune, B.M., Malone, B.J., 2006b. Organochlorines and mercury in waterfowl harvested in Canada. Environ. Monit. Assess. 114, 331–359. Braune, B.M., Malone, B.J., 2006a. Mercury and selenium in livers of waterfowl harvested in northern Canada. Arch. Environ. Contam. Toxicol. 50, 284–289. Braune, B.M., Scheuhammer, A.M., 2008. Trace element and metallothionein concentrations in seabirds from the Canadian Arctic. Environ. Toxicol. Chem. 27, 645–651. Braune, B.M., Mallory, M.L., Gilchrist, H.G., 2006. Elevated mercury levels in a declining population of ivory gulls in the Canadian Arctic. Mar. Pollut. Bull. 52, 969–987. Brown, D.A., Chatel, K.W., 1978. Interactions between cadmium and zinc in cytoplasm of duck liver and kidney. Chem. Biol. Interact. 22, 271–279. Brown, D.A., Bawden, C.A., Chatel, K.W., Parsons, T.R., 1977. The wildlife community of Iona Island jetty, Vancouver B.C., and heavy-metal pollution effects. Environ. Conserv. 4, 213–216. Brown, C.S., Wallner-Pendleton, E., Armstrong, D., Carlson, M., Cuevas, L.A., Simmons, L., 1996. Lead poisoning in captive Gentoo penguins (Pygoscelis papua papua). Proc. Am. Assoc. Zoo Vet. 1996, 298–301. Bryan, G.W., Langston, W.J., 1992. Bioavailability, accumulation and effects of heavy metals in sediments with special reference to United Kingdom estuaries: a review. Environ. Pollut. 76, 89–131. Bull, K.R., Murton, R.K., Osborn, D., Ward, P., Cheng, L., 1977. High levels of cadmium in Atlantic seabirds and sea-skaters. Nature 269, 507–509. Bull, K.R., Avery, W.J., Freestone, P., Hall, J.R., Osborn, D., Cooke, A.S., et al., 1983. Alkyl lead pollution and bird mortalities on the Mersey estuary, UK, 1979–1981. Environ. Pollut. 31A, 239–259. Burger, J., 1990. Behavioral effects of early postnatal lead exposure in herring gull (Larus argentatus) chicks. Pharmacol. Biochem. Behav. 35, 7–13. Burger, J., 1994. Heavy metals in avian eggshells: another excretion method. J. Toxicol. Environ. Health 41, 207–220. Burger, J., 1997. Heavy metals and selenium in herring gulls (Larus argentatus) nesting in colonies from eastern Long Island to Virginia. Environ. Monit. Assess. 48, 285–296. Burger, J., Gochfeld, M., 1985. Comparisons of nine heavy metals in salt gland and liver of greater scaup (Aythya marila), black duck (Anas rubripes) and mallard (A. Platyrhynchos). Comp. Biochem. Physiol. 81C, 287–292. Burger, J., Gochfeld, M., 1988a. Lead and behavioral development: effects of varying dosage and schedule on survival and performance of young common terns (Sterna hirundo). J. Toxicol. Environ. Health 24, 173–182. Burger, J., Gochfeld, M., 1988b. Effects of lead on growth in young herring gulls (Larus argentatus). J. Toxicol. Environ. Health 25, 227–236. Burger, J., Gochfeld, M., 1990. Tissue levels of lead in experimentally exposed herring gull (Larus argentatus) chicks. J. Toxicol. Environ. Health 29, 219–233.
348 Chapter 5 Burger, J., Gochfeld, M., 1991. Cadmium and lead in common terns (Aves: Sterna hirundo): relationship between levels in parents and eggs. Environ. Monit. Assess. 16, 253–258. Burger, J., Gochfeld, M., 1992. Heavy metal and selenium concentrations in black skimmers (Rynchops niger): genetic differences. Arch. Environ. Contam. Toxicol. 23, 431–434. Burger, J., Gochfeld, M., 1993. Lead and cadmium accumulation in eggs and fledgling seabirds in the New York Bight. Environ. Toxicol. Chem. 12, 261–267. Burger, J., Gochfeld, M., 1995. Heavy metal and selenium concentrations in eggs of herring gulls (Larus argentatus): temporal differences from 1989 to 1991. Arch. Environ. Contam. Toxicol. 29, 192–197. Burger, J., Gochfeld, M., 2007. Metals and radionuclides in birds and eggs from Amchitka and Kiska Islands in the Bering Sea/Pacific Ocean ecosystem. Environ. Monit. Assess. 127, 105–117. Burger, J., Schreiber, E.A.E., Gochfeld, M., 1992. Lead, cadmium, selenium and mercury in seabird feathers from the tropical mid-Pacific. Environ. Toxicol. Chem. 11, 815–822. Burger, J., Laska, M., Gochfeld, M., 1993a. Metal concentrations in feathers of birds from Papua New Guinea forests: evidence of pollution. Environ. Toxicol. Chem. 12, 1291–1296. Burger, J., Seyboldt, S., Morganstein, N., Clark, K., 1993b. Heavy metals and selenium in feathers of three shorebird species from Delaware Bay. Environ. Monit. Assess. 28, 189–198. Burger, J., Nisbet, I.C.T., Gochfeld, M., 1994. Heavy metals and selenium levels in feathers of known-aged common terns (Sterna hirundo). Arch. Environ. Contam. Toxicol. 26, 351–355. Burger, J., Gochfeld, M., Jeitner, C., Burke, S., Stamm, T., Snigaroff, R., et al., 2007a. Mercury levels and potential risk from subsistence foods from the aleutian. Sci. Total Environ. 38, 93–105. Burger, J., Gochfeld, M., Sullivan, K., Irons, D., 2007b. Mercury, arsenic, cadmium, chromium, lead, and selenium in feathers of pigeon guillemots (Cepphus columba) from Prince William Sound and the Aleutian Islands of Alaska. Sci. Total Environ. 387, 175–184. Burger, J., Gochfeld, M., Jeitner, G., Snigaroff, D., Snigaroff, R., Stamm, T., et al., 2008a. Assessment of metals in down feathers of female common eiders and their eggs from the Aleutian Islands: arsenic, cadmium, chromium, lead, manganese, mercury, and selenium. Environ. Monit. Assess. 143, 247–256. Burger, J., Gochfeld, M., Sullivan, K., Irons, D., McKnight, A., 2008b. Arsenic, cadmium, chromium, lead, manganese, mercury, and selenium in feathers of black-legged kittiwake (Rissa tridactyla) and black oystercatcher (Haematopus bachmani) from Prince William Sound, Alaska. Sci. Total Environ. 398, 20–25. Cain, B.W., Pafford, E.A., 1981. Effects of dietary nickel on survival and growth of mallard ducklings. Arch. Environ. Contam. Toxicol. 10, 737–745. Cain, B.W., Sileo, L., Franson, J.C., Moore, J., 1983. Effects of dietary cadmium on mallard ducklings. Environ. Res. 32, 286–297. Camardese, M.B., Hoffman, D.J., LeCaptain, L.J., Pendleton, G.W., 1990. Effects of arsenate on growth and physiology in mallard ducklings. Environ. Toxicol. Chem. 9, 785–795. Campbell, L.M., Norstrom, R.J., Hobson, K.A., Muir, D.C.G., Backus, S., Fisk, A.T., 2005. Mercury and other trace elements in a pelagic Arctic marine food web (Northwater Polynya, Baffin Bay). Sci. Total Environ. 342, 247–263. Choong, B., Allinson, G., Salzman, S., Overeem, R., 2007. Trace metal concentrations in the little penguin (Eudyptula minor) from southern Victoria, Australia. Bull. Environ. Contam. Toxicol. 78, 53–57. Clemens, E.T., Krook, L., Aronson, A.L., Stevens, C.E., 1975. Pathogenesis of lead shot poisoning in the mallard duck. Cornell Vet. 65, 248–285. Connors, P.G., Anderlini, V.C., Risebrough, R.W., Gilbertson, M., Hays, H., 1975. Investigations of heavy metals in common tern populations. Can. Field-Nat. 89, 157–162. Custer, T.W., Hohman, W.L., 1994. Trace elements in canvasbacks (Aythya valisineria) wintering in Louisiana, USA, 1987-1988. Environ. Pollut. 84, 53–259. Custer, T.W., Meyers, J.P., 1990. Organochlorines, mercury, and selenium in wintering shorebirds from Washington and California. Calif. Fish Game 76, 118–125. Custer, T.W., Mulhern, B.M., 1983. Heavy metal residues in prefledgling black-crowned night-herons from three Atlantic coast colonies. Bull. Environ. Contam. Toxicol. 30, 178–185.
Birds
349
Custer, T.W., Franson, J.C., Moore, J.F., Myers, J.E., 1986. Reproductive success and heavy metal contamination in Rhode Island common tern. Environ. Pollut. 41A, 23–52. Custer, T.W., Golden, N.H., Rattner, B.A., 2008. Element patterns in feathers of nestling black-crowned nightherons, Nycticorax nycticorax L., from four colonies in Delaware, Maryland, and Minnesota. Bull. Environ. Contam. Toxicol. 81, 147–151. Debacker, V., Jauniaux, T., Coignoul, F., Bouquegneau, J.M., 2000. Heavy metals contamination and body condition of wintering guillemots (Uria aalge) at the Belgian coast from 1993 to 1998. Environ. Res. 84A, 310–317. Degernes, L.A., 1991. The Minnesota trumpeter swan lead poisoning crisis of 1988-89. In: Englund, J.V. (Ed.), Proceedings and Papers of Twelfth Trumpeter Swan Society Conference. Restoring the Trumpeter Swan to the Upper Midwest, Minneapolis, MN, 6-9 September 1989. Available from The Trumpeter Swan Society, 3800 County Road 24, Maple Plain, Minnesota, pp. 114–118. Delbekke, K., Joiris, C., Decadt, G., 1984. Mercury contamination of the Belgian avifauna 1970-1981. Environ. Pollut. 7B, 205–221. DeVink, J.M.A., Clark, R.G., Slattery, S.M., Wayland, M., 2008. Is selenium affecting body condition and reproduction in boreal breeding scaup, scoters, and ring-necked ducks? Environ. Pollut. 152, 116–122. Dieter, M.P., 1979. Blood delta aminolevulinic acid dehydratase (ALAD) to monitor lead contamination in canvasback ducks (Aythya valisineria). In: Animals as Monitors of Environmental Pollutants. National Academy of Sciences, Washington, DC, pp. 177–191. Dieter, M.P., Finley, M.T., 1978. Erythrocyte d-aminolevulinic acid dehydratase activity in mallard ducks: duration of inhibition after lead shot dosage. J. Wildl. Manage. 42, 621–625. Dieter, M.P., Finley, M.T., 1979. D aminolevulinc acid dehydratase enzyme activity in blood, brain, and liver of lead-dosed ducks. Environ. Res. 19, 127–135. Dieter, M.P., Perry, M.C., Mulhern, B.M., 1976. Lead and PCB’s in canvasback ducks: relationship between enzyme levels and residues in blood. Arch. Environ. Contam. Toxicol. 5, 1–13. Dietz, R.O., Nielsen, C.O., Hansen, M.M., Hansen, C.T., 1990. Organic mercury in Greenland birds and mammals. Sci. Total Environ. 95, 41–51. Dietz, R., Riget, F., Johansen, P., 1996. Lead, cadmium, mercury and selenium in Greenland marine animals. Sci. Total Environ. 186, 67–93. Dietz, R., Riget, F.F., Boertmann, D., Sonne, C., Olsen, M.T., Fjeldsa, J., et al., 2006. Time trends of mercury in feathers of West Greenland birds of prey during 1851-2003. Environ. Sci. Technol. 40, 5911–5916. Di Giulio, R.T., Scanlon, P.F., 1985. Heavy metals in aquatic plants, clams, and sediments from the Chesapeake Bay, USA. Implications for waterfowl. Sci. Total Environ. 41, 259–274. Drbal, K., Elster, J., Komarek, J., 1992. Heavy metals in water, ice and biological material from Spitsbergen, Svalbard. Polar Res. 11, 99–101. Eastin Jr., W.C., O’Shea, T.J., 1981. Effects of dietary nickel on mallards. J. Toxicol. Environ. Health 7, 883–892. Eastin Jr., W.C., Haseltine, S.D., Murray, H.C., 1980. Intestinal absorption of 5 chromium compounds in young black ducks (Anas rubripes). Toxicol. Lett. 6, 193–197. Eastin Jr., W.C., Hoffman, D.J., O’Leary, C.T., 1983. Lead accumulation an depression of D-aminolevulinic acid dehydratase (ALAD) in young birds fed automotive waste oil. Arch. Environ. Contam. Toxicol. 12, 31–35. Eisler, R., 1984. Trace metal changes associated with age of marine vertebrates. Biol. Trace Elem. Res. 6, 165–180. Eisler, R., 1995. Ecological and toxicological aspects of the partial meltdown of the Chernobyl nuclear reactor. In: Hoffman, D.J., Rattner, B.A., Burton Jr., G.A, Cairns Jr, J. (Eds.), Handbook of Ecotoxicology. Lewis Publishers, Boca Raton, FL, pp. 549–564. Eisler, R., 2000a. Selenium. In: Handbook of Chemical Risk Assessment, vol. 3. Lewis Publishers, Boca Raton, FL, pp. 1649–1705. Eisler, R., 2000b. Chromium. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 45–92.
350 Chapter 5 Eisler, R., 2000c. Lead. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 201–311. Eisler, R., 2000d. Nickel. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 411–497. Eisler, R., 2000e. Silver. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 499–550. Eisler, R., 2000f. Tin. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 551–603. Eisler, R., 2000g. Zinc. In: Handbook of Chemical Risk Assessment, vol. 1. Lewis Publishers, Boca Raton, FL, pp. 605–714. Eisler, R., 2000h. Molybdenum. In: Handbook of Chemical Risk Assessment, vol. 3. Lewis Publishers, Boca Raton, FL, pp. 1613–1647. Eisler, R., 2003. The Chernobyl nuclear power plant reactor accident: ecotoxicological update. In: Hoffman, D.J., Rattner, B.A., Burton Jr., G.A., Cairns Jr., J. (Eds.), Handbook of Ecotoxicology. second ed. Lewis Publishers, Boca Raton, FL, pp. 703–736. Eisler, R., 2006. Mercury Hazards to Living Organisms. CRC Press, Boca Raton, FL. 312 pp. Elliott, J.E., Scheuhammer, A.M., Leighton, F.A., Pearce, P.A., 1992. Heavy metal and metallothionein concentrations in Atlantic Canadian seabirds. Arch. Environ. Contam. Toxicol. 22, 63–73. Elliott, J.E., Harris, M.L., Wilson, L.K., Smith, B.D., Batchelor, S.P., Maguire, J., 2007. Butyltins, trace metals and morphological variables in surf scoter (Melanitta perspicillata) wintering on the south coast of British Columbia, Canada. Environ. Pollut. 149, 114–124. Faber, R.A., Hickey, J.J., 1973. Eggshell thinning, chlorinated hydrocarbons, and mercury in inland aquatic bird eggs, 1969 and 1970. Pestic Monit. J. 7, 27–36. Fedynich, A.M., Ballard, B.M., McBride, T.J., Estrella, J.A., Garvon, J.M., Hooper, M.J., 2007. Arsenic, cadmium, copper, lead, and selenium in migrating blue-winged teal (Anas discors L.). Arch. Environ. Contam. Toxicol. 53, 662–666. Ferns, P.N., Anderson, J.I., 1994. Cadmium in the diet and body tissues of dunlins Calidris alpina, from the Bristol Channel, U.K. Environ. Pollut. 86, 225–231. Fimreite, N., 1974. Mercury contamination of aquatic birds in northwestern, Ontario. J. Wildl. Manage. 38, 120–131. Fimreite, N., Reynolds, L.M., 1973. Mercury contamination of fish in Northwestern Ontario. J. Wildl. Manage. 37, 62–68. Fimreite, N., Holsworth, W.N., Keith, J.A., Pearce, P.A., Gruchy, I.M., 1971. Mercury in fish and fish-eating birds near sites of industrial contamination in Canada. Can. Field Nat. 85, 211–220. Fimreite, N., Kveseth, N., Brevik, E.M., 1980. Mercury, DDE, and PCBs in eggs from a Norwegian gannet colony. Bull. Environ. Contam. Toxicol. 24, 142–144. Finley, M.T., Dieter, M.P., 1978. Influence of laying on lead accumulation in bone of mallard ducks. J. Toxicol. Environ. Health 4, 123–129. Finley, M.T., Stendell, R.C., 1978. Survival and reproductive success of black ducks fed methyl mercury. Environ. Pollut. 16, 51–64. Finley, M.T., Dieter, M.P., Locke, L.N., 1976. Lead in tissues of mallard ducks dosed with two types of lead shot. Bull. Environ. Contam. Toxicol. 16, 261–269. Fleming, W.J., Hill, E.F., Momot, J.F., Pang, V.F., 1991. Toxicity of trimethyltin and triethyltin to mallard ducklings. Environ. Toxicol. Chem. 10, 255–260. Flint, P.L., Petersen, M.R., Grand, J.B., 1997. Exposure of spectacled eiders and other diving ducks to lead in western Alaska. Can. J. Zool. 75, 439–443. Forsyth, D.S., Marshall, W.D., Collette, M.C., 1985. Interaction of alkyllead salts with avian eggs. J. Environ. Sci. Health 20A, 177–191. Franson, J.C., Petersen, M.R., Meteyer, C.U., Smith, M.R., 1995a. Lead poisoning of spectacled eiders (Somateria fischeri) and a common eider (Somateria mollissima) in Alaska. J. Wildl. Dis. 31, 268–271.
Birds
351
Franson, J.C., Koehl, P.S., Derksen, D.V., Rothe, T.C., Bunck, C.M., Moore, J.F., 1995b. Heavy metals in seaducks and mussels from Misty Fjords National Monument in southeast Alaska. Environ. Monit. Assess. 36, 149–167. Franson, J.C., Hohman, W.L., Moore, J.L., Smith, M.R., 1996. The efficacy of protoporphyrin as a predictive biomarker for lead exposure in canvasback ducks: effect of sample storage time. Environ. Monit. Assess. 43, 181–188. Frederick, R.B., 1976. Effects of lead nitrate ingestion on open-field behavior of mallard ducklings. Bull. Environ. Contam. Toxicol. 16, 739–742. French, M.C., Haines, C.W., Cooper, J., 1987. Investigation into the effects of ingestion of zinc shot by mallard ducks (Anas platyrhynchos). Environ. Pollut. 47, 305–314. Furness, R.W., 1996. Cadmium in birds. In: Beyer, W.N., Heinz, G.H., Redmon-Norwood, A.W. (Eds.), Environmental Contaminants in Wildlife: Interpreting Tissue Concentrations. CRC Press, Boca Raton, FL, pp. 389–404. Furness, R.W., Muirhead, S.J., Woodburn, M., 1986. Using bird feathers to measure mercury in the environment: relationships between mercury content and moult. Mar. Pollut. Bull. 17, 27–30. Gabrielsen, G.W., Mehlum, F., 1989. Thermoregulation and energetics of arctic seabirds. In: Bech, C., Reinertsen, R.E. (Eds.), Physiology of Cold Adaptation in Birds. Pergamon, Elmsford, NY, pp. 137–145. Gasaway, W.C., Buss, I.O., 1972. Zinc toxicity in the mallard duck. J. Wildl. Manage. 36, 1107–1117. Gochfeld, M., 1980. Tissue distribution of mercury in normal and abnormal young common terns. Mar. Pollut. Bull. 11, 362–366. Gochfeld, M., Burger, J., 1987. Heavy metal concentrations in the liver of three duck species: influence of species and sex. Environ. Pollut. 45, 1–14. Gochfeld, M., Burger, J., 1988. Effects of lead on growth and feeding behavior of young common terns (Sterna hirundo). Arch. Environ. Contam. Toxicol. 17, 513–517. Goede, A.A., 1985. Mercury, selenium, arsenic and zinc in waders from the Dutch Wadden Sea. Environ. Pollut. 37A, 287–309. Goldman, M., Dillon, R.D., Wilson, R.M., 1977. Thyroid function in Pekin ducklings as a consequence of erosion of ingested lead shot. Toxicol. Appl. Pharmacol. 40, 241–246. Grandy, I.V., Locke, J.W.L.N., Bagley, G.E., 1968. Relative toxicity of lead and five proposed substitute shot types to pen-reared mallards. J. Wildl. Manage. 32, 483–488. Green, D.E., Albers, P.H., 1997. Diagnostic criteria for selenium toxicosis in aquatic birds: histologic lesions. J. Wildl. Dis. 33, 385–404. Greichus, Y.A., Greichus, A., Emerick, R.J., 1973. Insecticides, polychlorinated biphenyls and mercury in wild cormorants, pelicans, their eggs, food and environment. Bull. Environ. Contam. Toxicol. 9, 321–328. Guitart, R., To-Figueras, J., Mateo, R., Bertolero, A., Cerradelo, S., Martinez-Vilalta, A., 1994a. Lead poisoning in waterfowl from the Ebro Delta, Spain: calculation of lead exposure threshold of mallards. Arch. Environ. Contam. Toxicol. 27, 289–293. Guitart, R., Torra, M., Cerradelo, S., Puig-Casado, P., Mateo, R., To-Figueras, J., 1994b. Pb, Cd, As, and Se concentrations in livers of dead wild birds from the Ebro Delta, Spain. Bull. Environ. Contam. Toxicol. 52, 523–529. Guruge, K.S., Iwata, H., Tanaka, H., Tanabe, S., 1997. Butyltin accumulation in the liver and kidney of seabirds. Mar. Environ. Res. 44, 191–199. Hall, S.L., Fisher Jr., F.M., 1985. Lead concentrations in tissues of marsh birds: relationship of feeding habits and grit preference to spent shot ingestion. Bull. Environ. Contam. Toxicol. 35, 1–8. Haney, J.C., MacDonald, S.D., 1995. Ivory gull (Pagophila eburnea). In: Poole, A., Gill, F. (Eds.), The Birds of North America, No. 175. Academy of Natural Sciences, Philadelphia American Ornithologists’ Union, Washington, DC, pp. 1–24. Harris, M.L., Wilson, L.K., Trudeau, S.F., Elliott, J.E., 2007. Vitamin A and contaminant concentrations in surf scoters (Melanitta perspicillata) wintering on the Pacific coast of British Columbia, Canada. Sci. Total Environ. 378, 366–375.
352 Chapter 5 Haseltine, S.D., Mulhern, B.M., Stafford, C., 1980. Organochlorine and heavy metal residues in black duck eggs from the Atlantic flyway, 1978. Pestic Monit. J. 15, 53–57. Havera, S.P., Whitton, R.M., Shealy, R.T., 1992. Blood lead and ingested and embedded shot in diving ducks during spring. J. Wildl. Manage. 56, 539–549. Heinz, G.H., 1979. Methylmercury: reproductive and behavioral effects on three generations of mallard ducks. J. Wildl. Manage. 43, 394–401. Heinz, G.H., 1980a. Comparison of game-farm and wild-strain of mallard duck in accumulation of methylmercury. J. Environ. Pathol. Toxicol. 3, 379–386. Heinz, G.H., 1980b. Eggshell thickness in mallards fed methylmercury. Bull. Environ. Contam. Toxicol. 25, 498–502. Heinz, G.H., Fitzgerald, M.A., 1993a. Overwinter survival of mallards fed selenium. Arch. Environ. Contam. Toxicol. 25, 90–94. Heinz, G.H., Fitzgerald, M.A., 1993b. Reproduction of mallards following overwinter exposure to selenium. Environ. Pollut. 81, 117–122. Heinz, G.H., Haseltine, S.D., 1981. Avoidance behavior of young black ducks treated with chromium. Toxicol. Lett. 8, 307–310. Heinz, G.H., Hoffman, D.J., 1998. Methylmercury chloride and selenomethionine interactions on health and reproduction in mallards. Environ. Toxicol. Chem. 17, 139–145. Heinz, G.H., Hoffman, D.J., Krynitsky, A.J., Weller, D.M.G., 1987. Reproduction in mallards fed selenium. Environ. Toxicol. Chem. 6, 423–433. Heinz, G.H., Hoffman, D.J., Gold, L.G., 1989. Impaired reproduction of mallards fed an organic form of selenium. J. Wildl. Manage. 53, 418–428. Heinz, G.H., Hoffman, D.J., LeCaptain, L.J., 1996. Toxicity of seleno-L-methionine, seleno-DL-methionine, high selenium wheat, and selenized yeast to mallard ducklings. Arch. Environ. Contam. Toxicol. 30, 93–99. Heinz, G.H., Hoffman, D.J., Konrad, S.L., Erwin, C.A., 2006. Factors affecting the toxicity of methylmercury injected into eggs. Arch. Environ. Contam. Toxicol. 50, 264–279. Henny, C.J., Blus, L.J., Grove, R.A., 1990. Western grebe, Aechmophorus occidentlis, wintering biology and contaminant accumulation in Commencement Bay, Puget Sound, Washington. Can. Field Nat. 104, 460–472. Henny, C.J., Blus, L.J., Grove, R.A., Thompson, S.P., 1991. Accumulation of trace elements and organochlorines by surf scoters wintering in the Pacific Northwest. Northwest Nat. 72, 43–60. Henny, C.J., Rudis, D.D., Roffe, T.J., Robinson-Wilson, E., 1995. Contaminants and sea ducks in Alaska and the circumpolar region. Environ. Health Perspect. 103 (Suppl. 4), 41–49. Henny, C.J., Grove, R.A., Kaiser, J.L., 2008. Osprey distribution, abundance, reproductive success and contaminant burdens along lower Columbia River, 1997/1998 versus 2004. Arch. Environ. Contam. Toxicol 54, 525–534. Hoffman, D.J., 1979. Embryotoxic effects of crude oil containing nickel and vanadium in mallards. Bull. Environ. Contam. Toxicol. 23, 203–206. Hoffman, D.J., Heinz, G.H., 1988. Embryotoxic and teratogenic effects of selenium in the diets of mallards. J. Toxicol. Environ. Health 24, 477–490. Hoffman, D.J., Heinz, G.H., 1998. Effects of mercury and selenium on glutathione metabolism and oxidative stress in mallard ducks. Environ. Toxicol. Chem. 17, 161–166. Hoffman, D.J., Heinz, G.H., Krynitsky, A.J., 1989. Hepatic glutathione metabolism and lipid peroxidation in response to excess dietary selenomethionine and selenite in mallard ducklings. J. Toxicol. Environ. Health 27, 263–271. Hoffman, D.J., Camardese, M.B., LeCaptain, L.J., Pendleton, G.W., 1990. Effects of boron on growth and physiology in mallard ducklings. Environ. Toxicol. Chem. 9, 335–346. Hoffman, D.J., Heinz, G.H., LeCaptain, L.J., Bunck, C.M., 1991a. Subchronic hepatotoxicity of selenomethionine ingestion in mallard ducks. J. Toxicol. Environ. Health 32, 449–464. Hoffman, D.J., Sanderson, C.J., LeCaptain, L.J., Cromartie, E., Pendleton, G.W., 1991b. Interactive effects of boron, selenium, and dietary protein on survival, growth, and physiology in mallard ducklings. Arch. Environ. Contam. Toxicol. 20, 288–294.
Birds
353
Hoffman, D.J., Sanderson, C.J., LeCaptain, L.J., Cromartie, E., Pendleton, G.W., 1992a. Interactive effects of arsenate, selenium, and dietary protein on survival, growth, and physiology in mallard ducklings. Arch. Environ. Contam. Toxicol. 22, 55–62. Hoffman, D.J., Sanderson, C.J., LeCaptain, L.J., Cromartie, E., Pendleton, G.W., 1992b. Interactive effects of selenium, methionine, and dietary protein on survival, growth, and physiology in mallard ducklings. Arch. Environ. Contam. Toxicol. 23, 163–171. Hoffman, D.J., Heinz, G.H., LeCaptain, L.J., Eisemann, J.D., Pendleton, G.W., 1996. Toxicity and oxidative stress of organic selenium and dietary protein in mallard ducklings. Arch. Environ. Contam. Toxicol. 31, 120–127. Hoffman, D.J., Ohlendorf, H.M., Marn, C.M., Pendleton, G.W., 1998. Association of mercury and selenium with altered glutathione metabolism and oxidative stress in diving ducks from the San Francisco Bay region, USA. Environ. Toxicol. Chem. 17, 167–172. Holden, A.V., 1973. International cooperative study of organochlorine and mercury residues in wildlife, 1969-71. Pestic Monit. J. 7, 37–52. Honda, K., Nasu, T., Tatsukawa, R., 1986. Seasonal changes in mercury accumulation in the black-eared kite, Milvus migrans lineatus. Environ. Pollut. 42A, 325–334. Honda, K., Marcovecchio, J.E., Kan, S., TAtsukawa, R., Ogi, H., 1990. Metal concentrations in pelagic seabirds from the north Pacific Ocean. Arch. Environ. Contam. Toxicol. 19, 704–711. Hong, J.S., Tilson, H.A., Hudson, P., Ali, S.F., Wilson, W.E., Hunter, V., 1983. Correlation of neurochemical and behavioral effects of triethyl lead chloride in rats. Toxicol. Appl. Pharmacol. 69, 471–479. Hontelez, L.C.M.P., van den Dungen, H.M., Baars, A.J., 1992. Lead and cadmium in birds in the Netherlands: a preliminary survey. Arch. Environ. Contam. Toxicol. 23, 453–456. Horai, S., Watanabe, I., Takada, H., Iwamizu, Y., Hayashi, T., Tanabe, S., et al., 2007. Trace element accumulations in 13 avian species collected from the Kanto area, Japan. Sci. Total Environ. 373, 512–525. Hudson, R.H., Tucker, R.K., Haegele, M.A., 1984. In: Handbook of Toxicity of Pesticides to Wildlife. U.S. Fish Wildl. Serv. Resour. Publ. 153, 99 pp. Hui, C.A., Beyer, W.N., 1998. Sediment ingestion of two sympatric shorebird species. Sci. Total Environ. 224, 227–233. Hulse, M., Mahoney, J.S., Schroder, G.O., Hacker, C.S., Pier, S.M., 1980. Environmentally acquired lead, cadmium, and manganese in the cattle egret. Bubulcus ibis, and the laughing gull, Larus atricilla. Arch. Environ. Contam. Toxicol. 9, 65–78. Hutton, M., 1981. Accumulation of heavy metals and selenium in three seabird species from the United Kingdom. Environ. Pollut. 26A, 129–145. Ikemoto, T., Kunito, T., Tanaka, H., Baba, N., Miyazaki, N., Tanabe, S., 2004. Detoxification mechanism of heavy metals in marine mammals and seabirds: interaction of selenium with mercury, silver, zinc, and cadmium in liver. Arch. Environ. Contam. toxicol. 47, 402–413. Jenkins, D.W., 1980. Biological Monitoring of Toxic Trace Metals. Volume 2. Toxic Trace Metals in Plants and Animals of the World. Part II. U.S. Environ. Protect. Agen. Rep. 600/3-80-091, 505–618. Johansen, P., Asmund, G., Riget, F., 2001. Lead contamination of seabirds harvested with lead shot–implications to human diet in Greenland. Environ. Pollut. 112, 501–504. Johnels, A.G., Westermark, T., 1969. Mercury contamination of the environment in Sweden. In Miller, M.W., Berg, G.G. (Eds.), Chemical Fallout, Current Research on Persistent Pesticides. Charles C Thomas, Springfield, IL, pp. 221–239. Jones, A.M., Jones, Y., Stewart, W.D.P., 1972. Mercury in marine organisms of the Tay region. Nature 238, 164–165. Kaji, T., Kawatani, R., Takata, M., Hoshino, T., Miyahara, T., Konzuka, H., et al., 1988. The effects of cadmium, copper or zinc on formation of embryonic chick bone in tissue culture. Toxicology 50, 303–316. Kalisinska, E., Salicki, W., Kavetska, K.M., Ligocki, M., 2007. Trace metal concentrations are higher in cartilage than in bones of scaup and pochard wintering in Poland. Sci. Total Environ. 388, 90–103.
354 Chapter 5 Kannan, K., Senthilkumar, K., Elliott, J.E., Feyk, L.A., Giesy, J.P., 1998. Occurrence of butyltin compounds in tissues of water birds and seaducks from the United States and Canada. Arch. Environ. Contam. Toxicol. 35, 64–69. Karlog, O., Clausen, B., 1983. Mercury and methylmercury in liver tissue from ringed herring gulls collected in three Danish localities. Nord. Vet. Med. 35, 245–250. Karppanen, E., Henriksson, K., 1970. Mercury content of game birds in Finland. Nord. Med. 84(35), 1097–1098. Kazacos, E.A., Van Vleet, J.F., 1989. Sequential ultrastructural changes of the pancreas in zinc toxicosis in ducklings. Am. J. Pathol. 134, 581–595. Kendall, R.J., Driver, C.D., 1982. Lead poisoning in Washington State. J. Wildl. Dis. 18, 385–387. Kim, J., Koo, T.H., 2008a. Heavy metal distribution in chicks of two heron species from Korea. Arch. Environ. Contam. Toxicol. 54, 740–747. Kim, J., Koo, T.H., 2008b. Heavy metal concentrations in feathers of Korean shorebirds. Arch. Environ. Contam. Toxicol. 55, 122–128. Kim, E.Y., Saeki, K., Tanabe, S., Tanaka, H., Tatsukawa, R., 1996a. Specific accumulation of mercury and selenium in seabirds. Environ. Pollut. 94, 261–265. Kim, E.Y., Murakami, T., Saeki, K., Tatsukawa, R., 1996b. Mercury levels and its chemical form in tissues and organs of seabirds. Arch. Environ. Contam. Toxicol. 30, 259–266. Kim, E.Y., Goto, R., Tanabe, S., Tanaka, H., Tatsukawa, R., 1998. Distribution of 14 elements in tissues and organs of oceanic seabirds. Arch. Environ, Contam. Toxicol. 35, 638–645. Kim, J., Park, S.K., Koo, T.H., 2007. Lead and cadmium concentrations in shorebirds from the Yeongjong Island, Korea. Environ. Monit. Assess. 134, 355–361. King, K.A., Meker, D.L., Swineford, D.M., 1980. White-faced ibis populations and pollutants in Texas, 19691976. Southwestern Nat. 25, 225–240. King, K.A., Lefever, C.A., Mulhern, B.M., 1983. Organochlorine and metal residues in royal terns nesting on the central Texas coast. J. Field Ornithol. 54, 295–303. King, K.A., Custer, T.W., Quinn, J.S., 1991. Effects of mercury, selenium, and organochlorine contaminants on reproduction of Forster’s terns and black skimmers nesting in a contaminated Texas Bay. Arch. Environ. Contam. Toxicol. 20, 32–40. Koh, T.S., Harper, M.J., 1988. Lead-poisoning in black swans, Cygnus atratus, exposed to spent lead shot at Bool Lagoon Game Reserve, South Australia. Aust. Wildl. Res. 15, 395–403. Koivusaari, J., Nuuja, I., Palokangas, R., Hattula, M.L., 1976. Chlorinated hydrocarbons and total mercury in the prey of the white tailed eagle (Haliaeetus albicilla L.) In the Quarken Straits of the Gulf of Bothnia, Finland. Bull. Environ. Contam. Toxicol. 15, 235–241. Kojadinovic, J., Le Corre, M., Cosson, R.P., Bustamante, P., 2007a. Trace elements in three marine birds breeding on Reunion Island (western Indian Ocean): part 1—factors influencing their bioaccumulation. Arch. Environ. Contam. Toxicol. 52, 418–430. Kojadinovic, J., Bustamante, P., Le Corre, M., Cosson, R.P., 2007b. Trace elements in three marine birds breeding on Reunion Island (western Indian Ocean): part 2—factors influencing their detoxification. Arch. Environ. Contam. Toxicol. 52, 431–440. Kojadinovic, J., Bustamante, P., Churlaud, C., Cosson, R.P., Corre, M.L., 2007c. Mercury in seabird feathers: insight on dietary habits and evidence for exposure levels in the western Indian Ocean. Sci. Total Environ. 384, 194–204. Lagerquist, J.E., Davison, M., Foreyt, W.J., 1994. Lead poisoning and other causes of mortality in trumpeter (Cygnus buccinator) and tundra (C. Columbianus) swans in western Washington. J. Wildl. Dis. 30, 60–64. Lande, E., 1977. Heavy metal pollution in Trondheimsfjorden, Norway, and the recorded effects on the fauna and flora. Environ. Pollut. 12, 187–198. Lemly, A.D., 1996. Selenium in aquatic organisms. In: Beyer, W.N., Heinz, G.H., Redmon-Norwood, A. (Eds.), Environmental Contaminants in Wildlife: Interpreting Tissue Concentrations. CRC Press, Boca Raton, FL, pp. 427–445. Lemly, A.D., Finger, S.E., Nelson, M.K., 1993. Sources and impacts of irrigation drainwater contaminants in arid wetlands. Environ. Toxicol. Chem. 12, 2265–2279.
Birds
355
Lesher, F., 1991. Trumpeter swan dies of lead poisoning. Passen. Pigeon 53, 274. Lewis, S.A., Becker, P.H., Furness, R.W., 1993. Mercury levels in eggs, tissues, and feathers of herring gulls, Larus argentatus from the German Wadden Sea coast. Environ. Pollut. 80, 293–299. Liu, X., Zhao, S., Sun, L., Yin, X., Xie, Z., Honghao, L., et al., 2006. P and trace metals in biomaterials, soils, sediments and plants in colony of red-footed booby (Sula sula) in the Dongdao Island of South China Sea. Chemosphere 65, 707–715. Lock, J.W., Thompson, D.R., Furness, R.W., Bartle, J.A., 1992. Metal concentrations in seabirds of the New Zealand region. Environ. Pollut. 75, 289–300. Longcore, J.R., Locke, L.N., Bagley, G.E., Andrews, R., 1974a. Significance of lead residues in mallard tissues. U.S. Fish Wildl. Serv. Spec. Sci. Rep.—Wildl. 182, 24. Longcore, J.R., Andrews, R., Locke, L.N., Bagley, G.E., Young, L.T., 1974b. Toxicity of lead and proposed substitute shot to mallards. U.S. Fish Wildl. Serv. Spec. Sci. Rep.—Wildl. 183, 23. Lowe, V.P.W., 1991. Radionuclides and the birds at Ravenglass. Environ. Pollut. 70, 1–26. Lowe, V.P.W., Horrill, A.D., 1991. Caesium concentration factors in wild herbivores and the fox (Vulpes vulpes L.). Environ. Pollut. 70, 93–107. Lu, J., Combs, G.F., 1988. Effects of excess dietary zinc on pancreatic exocrine function in the chick. J. Nutr. 118, 681–689. Luke, B.G., Johnstone, G.W., Woehler, E.J., 1989. Organochlorine pesticides, pcbs and mercury in Antarctic and Subantarctic seabirds. Chemosphere 19, 2007–2021. Lumeij, J.T., 1985. Clinicopathologic aspects of lead poisoning in birds: a review. Vet. Q. 7, 133–138. Lumeij, J.T., Scholten, A.J.H., 1989. A comparison of two methods to establish the prevalence of lead shot ingestion in mallards (Anas platyrhynchos) from the Netherlands. J. Wildl. Dis. 25, 297–299. Lunde, G., 1977. Occurence and transformation of arsenic in the marine environment. Environ. Health Perspec. 19, 47–52. Mason, C.F., Ekins, G., Ratford, J.R., 1997. PCB congeners, DDE, dieldrin, and mercury in eggs from an expanding colony of cormorants (Phalacrocorax carbo). Chemosphere 34, 1845–1849. Mateo, R., Dolz, J.C., Serano, J.M.A., Belliure, J., Guitart, R., 1997a. An epizootic of lead poisoning in greater flamingos (Phoenicopterus ruber roseus) in Spain. J. Wildl. Dis. 33, 131–134. Mateo, R., Martinez-Vilalta, A., Guitart, R., 1997b. Lead shot pellets in the Ebro delta, Spain: densities in sediments and prevalence of exposure in waterfowl. Environ. Pollut. 96, 335–341. Mateo, R., Belliure, J., Dolz, J.C., Serrano, J.M.A., Guitart, R., 1998. High prevalences of lead poisoning in wintering waterfowl in Spain. Arch. Environ. Contam. Toxicol. 35, 342–347. Mauser, D.M., Rocke, T.E., Mensik, J.G., Brand, C.J., 1990. Blood lead concentrations in mallards from Delevan and Colusa National Wildlife Refuges. Calif. Fish Game 76, 132–136. Mauvais, G., Pinault, L., 1993. Le saturnisme des anatides (anatidae) sur le site du Lac de Grand-Lieu (LoireAtlantique). Gibier Faune Sauvage 10, 85–101. Metcheva, R., Yurukova, L., Teodorova, S., Nikolova, E., 2006. The penguin feathers as bioindicator of Antarctica environmental state. Sci. Total Environ. 362, 259–265. Michot, T.C., Custer, T.W., Nault, A.J., Mitchell, C.A., 1994. Environmental contaminants in redheads wintering in coastal Louisiana and Texas. Arch. Environ. Contam. Toxicol. 26, 425–434. Mitchell, R.R., Fitzgerald, S.D., Aulerich, R.J., Balander, R.J., Powell, D.C., Templeman, R.J., et al., 2001a. Health effects following chronic dosing with tungsten-iron and tungsten-polymer shot in adult game-farm mallards. J. Wildl. Dis. 37, 451–458. Mitchell, R.R., Fitzgerald, S.D., Aulerich, R.J., Balander, R.J., Powell, D.C., Templeman, R.J., et al., 2001b. Hematological effects and metal residue concentrations following chronic dosing with tungsten-iron and tungsten-polymer shot in adult game-farm mallards. J. Wildl. Dis. 37, 459–467. Mitchell, R.R., Fitzgerald, S.D., Aulerich, R.R., Balander, R.J., Powell, D.C., Templeman, R.J., et al., 2001c. Reproductive effects and duckling survivability following chronic dosing with tungsten-iron and tungstenpolymer shot in adult game-farm mallards. J. Wildl. Dis. 37, 468–474. Moksnes, K., 1983. Selenium deposition in tissues and eggs of laying hens given surplus of selenium as selenomethionine. Acta Vet. Scand. 24, 34–44.
356 Chapter 5 Monteiro, L.R., Furness, R.W., 1995. Seabirds as monitors of mercury in the marine environment. Water Air Soil Pollut. 90, 851–870. Monteiro, L.R., Furness, R.W., 1997. Accelerated increase in mercury contamination in North Atlantic mesopelagic food chains as indicted by time series of seabird feathers. Environ. Toxicol. Chem. 16, 2489–2493. Monteiro, L.R., Furness, R.W., del Novo, A.J., 1995. Mercury levels in seabirds from the Azores, mid-north Atlantic Ocean. Arch. Environ. Contam. Toxicol. 28, 304–309. Mora, M.A., 1996. Organochlorines and trace elements in four colonial waterbird species nesting in the lower Laguna Madre, Texas. Arch. Environ. Contam. Toxicol. 31, 533–537. Mora, M.A., Anderson, D.W., 1995. Selenium, boron, and heavy metals in birds from the Mexicali Valley, Baja California, Mexico. Bull. Environ. Contam. Toxicol. 54, 198–206. Morris, P.J., Jensen, J., Applehans, F., 1986. Lead and zinc toxicosis in a blue and gold macaw (Ara ararauna) caused by ingestion of hardware cloth. Ann. Proc. Am. Assoc. Zoo Vet. 1985, 13–17. Muirhead, S.J., Furness, R.W., 1988. Heavy metal concentrations in the tissues of seabirds from Gough Island, South Atlantic Ocean. Mar. Pollut. Bull. 19, 278–283. National Research Council of Canada (NRCC), 1973. Lead in the Canadian environment. NRCC Publ., BY73-7 (ES), pp. 1–116. National Research Council of Canada (NRCC), 1978. In: Effects of arsenic in the Canadian environment. NRCC Publ., NRCC 15391, pp. 1–349. Norheim, G., Kjos-Hanssen, B., 1984. Persistent chlorinated hydrocarbons and mercury in birds caught off the west coast of Spitsbergen. Environ. Pollut. 33A, 143–152. Norheim, G., Some, L., Holt, G., 1982. Mercury and persistent chlorinated hydrocarbons in Antarctic birds from Bouvetoya and Dronning Maud Land. Environ. Pollut. 28A, 233–240. Norman, F.I., Garnham, J.S., Lowe, K.W., 1993. Further notes on lead concentrations in tissues of waterfowl in Victoria. Wildl. Res. 20, 621–624. Nuorteva, P., Hasanen, E., Nuorteva, S.L., 1975. The effectiveness of the Finnish anti-mercury measurements in the moderately polluted area of Hameenkyro. Ymparisto ja Terveys 6(8), 611–615. Nystrom, R.R., 1984. Cytological changes occurring in the liver of coturnix quail with an acute arsenic exposure. Drug Chem. Toxicol. 7, 587–594. Ochiai, K., Hoshiko, K., Jin, K., Tsuzuki, T., Itakura, C., 1993. A survey of lead poisoning in wild waterfowl in Japan. J. Wildl. Dis. 29, 349–352. Odsjo, T., Bignert, A., Olsson, M., Asplund, L., Eriksson, U., Haggberg, L., et al., 1997. The Swedish environmental specimen bank—application in trend monitoring of mercury and some organohalogenated compounds. Chemosphere 34, 2059–2066. O’Halloran, J., Myers, A.A., Duggan, P.F., 1988. Lead poisoning in swans and sources of contamination in Ireland. J. Zool. (London) 216, 211–213. O’Halloran, J., Myers, A.A., Duggan, P.F., 1989. Some sub-lethal effects of lead on mute swan Cygnus olor. J. Zool. (London) 218, 627–632. Ohlendorf, H.M., Harrison, C.S., 1986. Mercury, selenium, cadmium, and organochlorines in eggs of three Hawaiian seabird species. Environ. Pollut. 11B, 169–191. Ohlendorf, H.M., Risebrough, R.W., Vermeer, K., 1978. Exposure of marine birds to environmental pollutants. U.S. Fish Wildl. Serv. Wildl. Rep. 9, 1–40. Ohlendorf, H.M., Anderson, D.W., Boellstorff, D.E., Mulhern, B.M., 1985. Tissue distribution of trace elements and DDE in brown pelicans. Bull. Environ. Contam. Toxicol. 35, 183–192. Ohlendorf, H.M., Lowe, R.W., Kelly, P.R., Harvey, T.E., 1986. Selenium and heavy metals in San Francisco Bay diving ducks. J. Wildl. Manage. 50, 64–71. Ohlendorf, H.M., Kilness, A.W., Simmons, J.L., Stroud, R.K., Hoffman, D.J., Moore, J.F., 1988. Selenium toxicosis in wild aquatic birds. J. Toxicol. Environ. Health 24, 67–92. Ohlendorf, H.M., Marois, K.C., Lowe, R.W., Harvey, T.E., Kelly, P.R., 1991. Trace elements and organochlorines in surf scoters from San Francisco Bay, 1985. Environ. Monit. Assess. 18, 105–122. Osborn, D., Eney, W.J., Bull, K.R., 1983. The toxicity of trialkyl lead compounds to birds. Environ. Pollut. 31A, 261–275.
Birds
357
Outridge, P.M., Scheuhammer, A.M., 1993b. Bioaccumulation and toxicology of chromium: implications for wildlife. Rev. Environ. Contam. Toxicol. 130, 31–77. Outridge, P.M., Scheuhammer, A.M., 1993a. Bioaccumulation and toxicology of nickel: implications for wild mammals and birds. Environ. Rev. 1, 172–197. Pain, D.J., 1996. Lead in waterfowl. In: Beyer, W.N., Heinz, G.H., Redmon-Norwood, A.W. (Eds.), Environmental Contaminants in Wildlife: Interpreting Tissue Concentrations. CRC Press, Boca Raton, FL, pp. 251–264. Pain, D.J., Rattner, B.A., 1988. Mortality and hematology associated with the ingestion of one number four lead shot in black ducks, Anas rubripes. Bull. Environ. Contam. Toxicol. 40, 159–164. Pain, D.J., Handrinos, G.I., 1990. The incidence of ingested lead shot in ducks of the Evros Delta, Greece. Wildfowl 41, 167–170. Pain, D.J., Sears, J., Newton, I., 1995. Lead concentration in birds of prey in Britain. Environ. Pollut. 87, 173–180. Parslow, J.L.F., 1973. Mercury in waders from the Wash. Environ. Pollut. 5, 295–304. Parslow, J.L.F., Jefferies, D.J., Hanson, H.M., 1973. Gannet mortality incidents in 1972. Mar. Pollut. Bull. 4, 41–43. Peden, J.D., Crothers, J.H., Waterfall, C.E., Beasley, J., 1973. Heavy metals in Somerset marine organisms. Mar. Pollut. Bull. 4, 7–10. Pendleton, G.W., Whitworth, M.R., Olsen, G.H., 1995. Accumulation and loss of arsenic and boron, alone and in combination, in mallard ducks. Environ. Toxicol. Chem. 14, 1357–1364. Perez-Lopez, M., Cid, F., Oropesa, A.L., Fidalgo, L.E., Beceiro, A.L., Soler, F., 2006. Heavy metal and arsenic content in seabirds affected by the Prestige oil spill on the Galician coast (NW Spain). Sci. Total Environ. 359, 209–220. Pokras, M.A., Chafel, C., 1992. Lead toxicosis from ingested fishing sinkers in adult common loons (Gavia immer) in New England. J. Zoo Wildl. Med. 23, 92–97. Pollock, B., Machin, K.L., 2008. Effects of cadmium, mercury, and selenium on reproductive indices in male lesser scaup (Aythya affinis) in the western boreal forest. Arch. Environ. Contam. Toxicol. 54, 730–739. Ramo, C., Sanchez, C., Saint-Aubin, L.H., 1992. Lead poisoning of greater flamingos Phoenicopterus ruber. Wildfowl 43, 220–222. Ranta, W.B., Tomassini, F.D., Niebeer, E., 1978. Elevation of copper and nickel levels in primaries from black and mallard ducks collected in the Sudbury district, Ontario. Can. J. Zool 56, 581–586. Rao, R.V.V.P., Jordan, S.A., Bhatnagar, M.K., 1989. Ultrastructure of kidney of ducks exposed to methylmercury, lead and cadmium in combination. J. Environ. Pathol. Toxicol. Oncol. 9, 19–44. Rattner, B.A., Golden, N.H., Toschik, P.C., McGowan, P.C., Custer, T.W., 2008. Concentrations of metals in blood and feathers of nestling ospreys (Pandion haliaetus) in Chesapeake and Delaware Bays. Arch. Environ. Contam. Toxicol. 54, 114–122 Erratum. 2008. Arch. Environ. Contam. Toxicol. 54, 758-759. Reece, R.L., Dickson, D.B., Bunowes, P.J., 1986. Zinc toxicity (new wire disease) in aviary birds. Aust. Vet. J. 63, 199. Renzoni, A., Bacci, E., Falciai, L., 1973. Mercury concentration in the water, sediments, and fauna of an area of the Tyrrhenian coast. In: 6th International Symposium on Medical Oceanography. Portoroz, Yugoslavia, 26-30 September 1973, pp. 17–45. Robertson, D.E., Rancitelli, L.A., Langford, J.C., Perkins, R.W., 1972. Battelle-Northwest Contribution to the IDOE Base-Line Study. Battelle Pac. Northwest Lab., Richland, WA, pp. 1–40. Rodriguez-Navarro, A.B., Gaines, K.F., Romanek, C.S., Masson, G.R., 2002. Mineralization of clapper rail eggshell from a contaminated salt marsh system. Arch. Environ. Contam. Toxicol. 43, 449–460. Rowe, B.L., Prince, H.H., 1983. Behavioral response of mallards to contaminated drinking water. Bull. Environ. Contam. Toxicol. 30, 505–510. Ruelas-Inzunza, J., Paez-Osuna, F., 2008. Trophic distribution of Cd, Pb, and Zn in a food web from Altata-Ensenada del Pabellon subtropical lagoon, SE Gulf of California. Arch. Environ. Contam. Toxicol. 54, 584–596. Ruelas-Inzunza, J., Paez-Osuna, F., Arvizu-Merin, M., 2007. Mercury distribution in selected tissues of migratory and resident avifauna from Altata-Ensenada del Pabellon Lagoon, southeast Gulf of California. Bull. Environ. Contam. Toxicol. 78, 39–42.
358 Chapter 5 Sanpera, C., Morera, M., Ruiz, X., Jover, L., 2000. Variability in mercury and selenium levels in clutches of Audouin’s gulls (Larus audouinii) breeding at the Chafarinas Islands, Southwest Mediterranean. Arch. Environ. Contam. Toxicol. 39, 119–123. Sanpera, C., Moreno, R., Ruiz, X., Jover, L., 2007. Audouin’s gull chicks as bioindicators of mercury pollution at different breeding locations in the western Mediterranean. Mar. Pollut. Bull. 54, 691–696. Santos, I.R., Silva-Filho, E.V., Schaefer, C., Sella, S.M., Silva, C.A., Gomes, V., et al., 2006. Baseline mercury and zinc concentrations in terrestrial and coastal organisms of Admiralty Bay, Antarctica. Environ. Pollut. 140, 304–311. Scheifler, R., Gauthier-Clerc, M., Le Bohec, C., Crini, N., Coeurdassier, M., Badot, P.M., et al., 2005. Mercury concentrations in king penguin (Aptenodytes patagonicus) feathers at Crozet Islands (sub-Antarctic): temporal trend between 1966-1974 and 2000-2001. Environ. Toxicol. Chem. 24, 125–128. Scheuhammer, A.M., 1987a. Erythrocyte delta-aminolevulinic acid dehydratase in birds. I. The effects of lead and other metals in vitro. Toxicology 45, 155–163. Scheuhammer, A.M., 1987b. Erythrocyte delta-aminolevulinic acid dehydratase in birds. II. The effects of lead exposure in vivo. Toxicology 45, 165–175. Scheuhammer, A.M., 1991. Effects of acidification on the availability of toxic metals and calcium to wild birds and mammals. Environ. Pollut. 71, 329–375. Schmitz, R.A., Aguirre, A.A., Cook, R.S., Baldassarre, G.A., 1990. Lead poisoning in Caribbean flamingos in Yucatan, Mexico. Wildl. Soc. Bull. 18, 399–404. Schwab Sr., D., Padgett, T.M., 1988. Lead poisoning in a free ranging pekin duck (Anas platyrhynchos) from Chesapeake, Virginia. Va. J. Sci. 39, 412–413. Sears, J., 1988. Regional and seasonal variations in lead poisoning in the mute swan Cygnus olor in relation to the distribution of lead and lead weights in the Thames area, England. Biol. Conserv. 46, 115–134. Sileo, L., Fefer, S.I., 1987. Paint chip poisoning of Laysan albatross at Midway Atoll. J. Wildl. Dis. 23, 432–437. Smith, G.J., Anders, V.P., 1989. Toxic effects of boron on mallard reproduction. Environ. Toxicol. Chem. 8, 943–950. Sparling, D.W., Lowe, T.P., 1996. Environmental hazards of aluminum to plants, invertebrates, fish, and wildlife. Rev. Environ. Contam. Toxicol. 145, 1–127. Spray, C.J., Milne, H., 1988. The incidence of lead poisoning among whooper and mute swans Cygnus cygnus and C. olor in Scotland. Biol. Conserv. 44, 265–281. Stanley Jr., T.R., Spann, J.W., Smith, G.J., Rosscoe, R., 1994. Main and interactive effects of arsenic and selenium on mallard reproduction and duckling growth and survival. Arch. Environ. Contam. Toxicol. 26, 444–451. Stanley Jr., T.R., Smith, G.J., Hoffman, D.J., Heinz, G.H., Rosscoe, R., 1996. Effects of boron and selenium on mallard reproduction and duckling growth and survival. Environ. Toxicol. Chem. 15, 1124–1132. Stendell, R.C., Smith, R.I., Burnham, K.P., Christensen, R.E., 1979. Exposure of waterfowl to lead: a nationwide survey of residues in wingbones of seven species, 1972-73. U.S. Fish Wildl. Serv. Spec. Sci. Rep.—Wildl. 233, 1–12. Stendell, R.C., Artmann, J.W., Martin, E., 1980. Lead residues in sora rails from Maryland. J. Wildl. Manage. 44, 525–527. Stewart, F.M., Thompson, D.R., Furness, R.W., Harrison, N., 1994. Seasonal variation in heavy metal levels in tissues of common guillemots Uria aalge from northwest Scotland. Arch. Environ. Contam. Toxicol. 27, 168–175. Stewart, F.M., Monteiro, L.R., Furness, R.W., 1997. Heavy metal concentrations in Cory’s shearwater, Calonectris diomedea, fledglings from the Azores, Portugal. Bull. Environ. Contam. Toxicol. 58, 115–122. Stickel, L.F., Stickel, W.H., McLane, M.A.R., Bruns, M., 1977. Prolonged retention of methyl mercury by mallard drakes. Bull. Environ. Contam. Toxicol. 18, 393–400. Street, M., 1983. The assessment of mortality resulting from ingestion of spent lead shot by mallard wintering in South East England. Congr. Int. Fauna Cinegetica y Silvestre 15(1981), 161–167. Szefer, P., Pempkowiak, J., Skwarzec, B., Bojanowski, R., Holm, E., 1993a. Concentration of selected metals in penguins and other representative fauna of the Antarctica. Sci. Total Environ. 138, 281–288.
Birds
359
Szefer, P., Czarnowski, W., Pempkowiak, J., Holm, E., 1993b. Mercury and major essential elements in seals, penguins, and other representative fauna of the Antarctic. Arch. Environ. Contam. Toxicol. 25, 422–427. Takekawa, J.Y., Wainwright-De La Cruz, S.E., Hothem, R.L., Yee, J., Relating body condition to inorganic contaminant concentrations of diving ducks wintering in coastal California. Arch. Environ. Contam. Toxicol. 42, 60–70. Tavares, P.C., Monteiro, L.R., Lopes, R.J., Pereira, M.E., Duarte, A.C., Furness, R.W., 2005. Variation of mercury contamination in chicks of little tern Sterna albifrons in southwest Europe: brood, age and colony related effects. Bull. Environ. Contam. Toxicol. 74, 177–183. Thomas, V.G., McGill, I.R., 2008. Dissolution of copper, tin, and iron from sintered tungsten-bronze spheres in a simulated avian gizzard, and an assessment of their potential toxicity to birds. Sci. Total Environ. 394, 283–289. Thompson, D.R., 1990. Heavy metals in marine vertebrates. In: Furness, R.W., Rainbow, P.S. (Eds.), Heavy Metals in the Marine Environment. CRC Press, Boca Raton, FL, pp. 143–182. Thompson, D.R., 1996. Mercury in birds and terrestrial mammals. In: Beyer, W.N., Heinz, G.H., RedmonNorwood, A.W. (Eds.), Environmental Contaminants in Wildlife: Interpreting Tissue Concentrations. SETAC Special Publication Series, Lewis Publishers, Boca Raton, FL, pp. 341–356. Thompson, D.R., Furness, R.W., 1989. Comparison of the levels of total and organic mercury in seabird feathers. Mar. Pollut. Bull. 20, 577–579. Thompson, J.D., Sheffer, B.J., Baldassarre, G.A., 1989. Incidence of ingested shot in waterfowl harvested in Yucatan. Mexico. Wildl. Soc. Bull. 17, 189–191. Thompson, D.R., Stewart, F.M., Furness, R.W., 1990. Using seabirds to monitor mercury in marine environments. The validity of conversion ratios for tissue comparisons. Mar. Pollut. Bull. 21, 339–342. Thompson, D.R., Hamer, K.C., Furness, R.W., 1991. Mercury accumulation in great skuas Catharcta skua of known age and sex, and its effects upon breeding and survival. J. Appl. Ecol. 28, 672–684. Thompson, D.R., Furness, R.W., Walsh, P.M., 1992. Historical changes in mercury concentrations in the marine ecosystem of the north and north-east Atlantic Ocean as indicated by seabird feathers. J. Appl. Ecol. 29 79–84. Thompson, D.R., Becker, P.H., Furness, R.W., 1993. Long-term changes in mercury concentrations in herring gulls. Larus argentatus and common terns Sterna hirundo from the German North Sea coast. J. Appl. Ecol. 30, 316–320. Turner, J.C., Solly, S.R.B., Mol-Krijnen, J.C.M., Shanks, V., 1978. Organochlorine, fluorine, and heavy-metal levels in some birds from New Zealand estuaries. N.Z. J. Sci. 21, 99–102. Ui, J., Kitamuri, S., 1971. Mercury in the Adriatic. Mar. Pollut. Bull. 2, 56–58. U.S. Fish and Wildlife Service (USFWS), 1986. Migratory bird hunting: availability of a final supplemental environmental impact statement (SEIS) on the use of lead shot for hunting migratory birds in United States. Fed. Reg. 51(124), 23443–23447. U.S. Fish and Wildlife Service (USFWS), 1987. Migratory bird hunting: zones in which lead shot will be prohibited for the taking of waterfowl, coots and certain other species in the 1987-88 hunting season. Fed. Reg. 52(139), 27352–27368. U.S. Fish and Wildlife Service (USFWS), 2006. Migratory bird hunting approval of tungsten-iron-copper-nickel, iron-tungsten-nickel alloy, tungsten-bronze (additional formulation), and tungsten-tin-iron shot types as nontoxic for hunting waterfowl and coots: availability of environmental assessments. Fed. Reg. 71(17), 4294–4297. U.S. National Academy of Sciences (USNAS), 1977. Arsenic. USNAS, Washington, DC, 332 pp. U.S. National Academy of Sciences (USNAS), 1978. In: An Assessment of Mercury in the Environment. USNAS, Washington, DC, 185 pp. U.S. National Academy of Sciences, 1979. Zinc. USNAS, Natl. Res. Coun., Subcommittee Zinc. University Park Press, Baltimore, MD, 471 pp. Van Eeden, P.H., Schoonbee, H.J., 1992. Concentrations of heavy metals in organs and tissues of the redknobbed coot. Ostrich 63, 165–171.
360 Chapter 5 Vannucchi, C., Sivieri, S., Ceccanti, M., 1978. Residues of chlorinated naphthalenes, other hydrocarbons and toxic metals (Hg, Pb, Cd) in tissues of Mediterranean seagulls. Chemosphere 7, 483–490. Veltman, K., Huijbregts, M.A.J., van den Heuvel-Greve, M.J., Vethaak, A.D., Hendriks, A.J., 2006. Organotin accumulation in an estuarine food chain: comparing field measurements with model estimations. Mar. Environ. Res. 61, 511–530. Vermeer, K., Castilla, J.C., 1991. High cadmium residues observed during a pilot study in shorebirds and their prey downstream from the El Salvador copper mine, Chile. Bull. Environ. Contam. Toxicol. 46, 242–248. Vermeer, K., Peakall, D.B., 1979. Trace metals in seaducks of the Fraser River delta intertidal area, British Columbia. Mar. Pollut. Bull 10, 189–191. Vermeer, K., Thompson, J.A.J., 1992. Arsenic and copper residues in waterbirds and their food down inlet from the island copper mill. Bull. Environ. Contam. Toxicol. 48, 733–738. Warren, R.J., Wallace, B.M., Bush, P.B., 1990. Trace elements in migrating blue-winged teal; seasonal-, sex-, and age-class variations. Environ. Toxicol. Chem. 9, 521–528. Wayland, M., Gilchrist, H.G., Dickson, D.L., Bollinger, T., James, C., Carreno, R.A., et al., 2001. Trace elements in king eiders and common eiders in the Canadian Arctic. Arch. Environ. Contam. Toxicol. 41, 491–500. Wayland, M., Gilchrist, H.G., Marchant, T., Keating, J., Smits, J.E., 2002. Immune function, stress response, and body condition in Arctic-breeding common eiders in relation to cadmium, mercury, and selenium concentrations. Environ. Res. 90A, 47–60. Wayland, M., Gilchrist, H.G., Neugebauer, E., 2005. Concentrations of cadmium, mercury and selenium in common eider ducks in the eastern Canadian arctic: influence of reproductive stage. Sci. Total Environ. 351/352, 323–332. Wayland, M., Drake, K.L., Alisauskas, R.T., Kellett, D.K., Traylor, J., Swoboda, C., et al., 2008. Survival rates and blood metal concentrations in two species of free-ranging North American sea ducks. Environ. Toxicol. Chem. 27, 698–704. Welander, A.D., 1969. Distribution of radionuclides in the environment of Eniwetok and Bikini Atolls, August 1964. In: Nelson, D.J., Evans, F.C. (Eds.), Symposium on Radioecology. Proceedings of the Second National Symposium. Available as CONF-370503 from NTIS, Springfield, VA, pp. 346–354. Wenzel, C., Gabrielsen, G.W., 1995. Trace element accumulation in three seabird species from Hornoya, Norway. Arch. Environ. Contam. Toxicol. 29, 198–206. Wenzel, C., Adelung, D., Theede, H., 1996. Distribution and age-related changes of trace elements in kittiwake Rissa tridactyla nestlings from an isolated colony in the German Bight North Sea. Sci. Total Environ. 193, 13–26. White, D.H., Finley, M.T., 1978. Uptake and retention of dietary cadmium in mallard ducks. Environ. Res. 17, 53–59. White, D.H., Stendell, R.C., 1977. Waterfowl exposure to lead and steel shot on selected hunting areas. J. Wildl. Manage. 41, 469–475. White, D.H., Stendell, R.C., Mulhern, B.M., 1979. Relations of wintering canvasbacks to environmental pollutants—Chesapeake Bay, Maryland. Wilson Bull. 91(2), 279–287. White, D.H., King, K.A., Prouty, R.M., 1980. Significance of organochlorine and heavy metal residues in wintering shorebirds at Corpus Christi, Texas, 1976-77. Pestic Monit. J. 14, 58–63. Wiemeyer, S.N., Hoffman, D.J., 1996. Reproduction of eastern screech-owls fed selenium. J. Wildl. Manage. 60, 332–341. Wiemeyer, S.N., Lamont, T.G., Locke, L.N., 1980. Residues of environmental pollutants and necropsy data for eastern United States ospreys, 1964-1973. Estuaries 3, 155–167. Wiemeyer, S.N., Schmeling, S.K., Anderson, A., 1987. Environmental pollutant and necropsy data for ospreys from the eastern United States, 1975-1982. J. Wildl. Dis. 23, 279–291. Wiemeyer, S.N., Bunck, C.M., Krynitsky, A.J., 1988. Organochlorine pesticides, polychlorinated biphenyls, and mercury in osprey eggs—1970-79—and their relationships to shell thinning and productivity. Arch. Environ. Contam. Toxicol. 17, 767–787. Wobeser, G.A., 1981. Diseases of Wild Waterfowl. Plenum Press, New York, pp. 151–163.
Birds
361
Work, T.M., Smith, M.R., 1996. Lead exposure in Laysan albatross adults and chicks in Hawaii: prevalence, risk factors, and biochemical effects. Arch. Environ. Contam. Toxicol. 31, 115–119. Yin, X., Sun, L., Zhu, R., Liu, X., Ruan, D., Wang, Y., 2007. Mercury-selenium association in Antarctic seal hairs and animal excrements over the past 1,500 years. Environ. Toxicol. Chem. 26, 381–386. Young, D.R., Jan, T.K., Hershelman, G.P., 1980. Cycling of zinc in the nearshore marine environment. In: Nriagu, J.O. (Ed.), Zinc in the Environment. Part 1: Ecological Cycling. Wiley, New York, pp. 297–335. Zhang, Y., Ruan, L., Fasola, M., Boncompagni, E., Dong, Y., Dai, N., et al., 2006. Little egrets (Egretta garzetta) and trace-metal contamination in wetlands of China. Environ. Monit. Assess. 118, 355–368. Zwank, P.J., Wright, V.L., Shealy, P.M., Newsom, J.D., 1985. Lead toxicosis in waterfowl on two major wintering areas in Louisiana. Wildl. Soc. Bull. 13, 17–26.
CHAPTER 6
Mammals This group includes the whales, porpoises, seals, dolphins, walruses, sea otters, and their relatives. The majority of the cetaceans and pinnipeds are exclusively marine, some frequenting the coast, but others oceanic, seldom approaching land. Many undertake extensive migrations and are widely distributed. All have been hunted by humans for centuries, sometimes to the point of near extinction of selected species. Recovery of exploited populations is proceeding under the guidance of various international commissions and regulatory groups. There has been a major surge in the literature on trace metal composition of marine mammals during the past 30 years. A significant portion of the variability in trace metal concentrations within and between species of marine mammals is attributed to geographic location, year of capture, season, gender, blubber thickness, age, and fatty acid content (Lahaye et al., 2007).
6.1 Aluminum Mean aluminum content of biopsied skin from bottlenose dolphins, Tursiops truncatus, in the vicinity of Charleston, South Carolina, collected between 2003 and 2005, was highest in pregnant females (14.0 mg Al/kg dry weight (DW)) and lowest in nonpregnant female adults (2.3 mg Al/kg DW); however, the highest concentration recorded was 157.0 mg Al/kg DW in skin of adult males (Table 6.1; Stavros et al., 2007). Lymphocyte proliferation of newborn harbor seals, Phoca vitulina, was unaffected during incubation in 40.0 mg Al/L for 5 days (Kakuschke et al., 2008a).
6.2 Americium Americium-241 levels in lactating gray seals, Halichoerus grypus, from the North Sea and northeast Atlantic Ocean in 1987 were slightly higher in muscle than in milk; for pups, 241 Am activity levels in muscle and liver were about the same (Anderson et al., 1990).
363
364 Chapter 6 Table 6.1: Aluminum, Antimony, Arsenic, and Boron Concentrations in Field Collections of Mammals Element and Organism
Concentration
Reference
a
Aluminum Leopard seal, Hydrurga leptonyx; Antarctica; 1999-2002; adults; serum
0.25 FW
23
Weddell seal, Leptonychotes weddelli; Antarctica; 2002-2003; serum vs. hair
0.08 DW vs. 9.1 DW
23
0.003-0.007 FW Not detectable-0.57 FW 0.0033 (<0.00017-0.126) FW vs. 0.037 (0.004-0.5) FW
19 20 21
0.03 FW; max. 0.06 FW vs. 4.9 (1.7-16.4) FW
22
5.0 DW; max. 8.4 DW 11.0 DW; max. 157.0 DW 7.3 DW; max. 54.0 DW 2.3 DW; max. 4.1 DW 14.0 DW; max. 42.0 DW
12 12 12 12 12
0.001 FW; max. 0.003 FW 0.73 FW; max. 2.1 FW 0.026 FW vs. 0.026 FW
13 13 18
Southern sea otter, Enhydra lutris nereis; found dead; California coast; adult females; 1992-2002; liver
Max. 0.02 DW
16
Striped dolphin, Stenella coeruleoalba; all tissues
Max. 0.01 DW
23
Florida manatee; 2007; Florida; blood vs. skin
0.011 (0.009-0.016) FW vs. 0.024 (0.004-0.047) FW
22
Harbor seal, Phoca vitulina; blood Captive animals; Germany Free-ranging; North Sea Wadden Sea; 2004-2005; German site vs. Danish site Florida manatee, Trichechus manatus latirostris; 2007; Crystal River, Florida; blood vs. skin Bottlenose dolphin, Tursiops truncatus; Skin; 2003-2005; Charleston, South Carolina Male juvenile Male adult Female juvenile Female adult Pregnant female Sarasota Bay, Florida; 2002-2004 Blood Skin Blood; summers 2003-2005; Charleston, South Carolina vs. Indian River, Florida Antimony
(Continues)
Mammals 365 Table 6.1:
Cont’d
Element and Organism
Concentration
Reference
Polar bear, Ursus maritimus; liver; 1993-2002; Beaufort Sea population vs. Chukchi Sea population
0.02 (0.01-0.04) DW vs. 0.03 (0.01-0.09) DW
14
0.8 FW vs. 0.5 FW 0.2 FW vs. 0.1 FW 0.32 FW vs. 0.4 FW
25 25 25
0.3-0.7 FW vs. 0.2-0.3 FW
25
a
Arsenic Australia; 1995-1996; stranded; liver vs. kidney Bottlenose dolphin, Tursiops truncatus aduncus Adult female Female calf Common dolphin, Delphinus delphis; juvenile Melon-headed whale, Peponocephala electra; adults Fin whale, Balaenoptera physalis Muscle Blubber oil
0.36 DW 1.8 FW
1 5
Northern fur seal, Callorhinus ursinus Kidney Liver
<0.2 FW <0.2 FW
2 2
Common dolphin, Delphinus sp.; December 2004; found stranded; New Zealand; max. concentrations Blubber Kidney Liver
1.7 FW 0.13 FW 0.27 FW
10 10 10
0.23 FW; max. 0.82 FW 0.19 FW; max. 0.28 FW 0.23 FW; max. 0.66 FW
11 11 11
Greenland Sea; caught in drift ice between Iceland and East Greenland; March-April 1999; reproductively active females during suckling period Harp seal, Pagophilus groenlandicus; age 12 (6-22) years; weight 111 (88-132) kg Muscle Liver Kidney Hooded seal, Cystophora cristata; age 9 (4-33 years); weight 141 (108-215) kg
(Continues)
366 Chapter 6 Table 6.1: Element and Organism Muscle Liver Kidney
Cont’d
Concentration
Reference
0.10 FW 0.27 FW 0.36 FW
11 11 11
0.17 (0.04-0.42) FW 0.23 (0.05-0.41) FW
17 17
Leopard seal, Hydrurga leptonyx; Antarctica; 1999-2002; adults; serum
0.07 FW
23
Weddell seal, Leptonychotes weddelli; Antarctica; 2002-2003; serum vs. hair
0.05 DW vs. 2.5 DW
23
Hong Kong; found stranded; stomach contents Humpback dolphin, Sousa chinensis Finless porpoise, Neophocaena phocaenoides
Harbor seal, Phoca vitulina Liver Newfoundland and Labrador; Canada; body length 212-402 cm Muscle Liver Kidney Blood Captive animals; Germany Free-ranging; North Sea Wadden Sea; 2004-2005; German site vs. Danish site Pinnipeds and cetaceans; 4 spp.; liver Total arsenic Arsenobetaine Arsenocholine Arsenic acid Arsenous acid Dimethylarsinic acid Methylarsonic acid Trimethylarsonium cation Pinnipeds Cetaceans Unidentified compounds La Plata river dolphin, Pontoporia blainvillei Liver Kidney
0.2-1.7 FW
3
0.08-0.16 FW 0.21-0.95 FW 0.13-0.39 FW
8 8 8
0.08-0.32 FW 0.07-0.24 FW 0.17 (0.04-0.59) FW vs. 0.18 (0.12-0.32) FW
a
19 20 21
0.17-2.4 FW 0.05-1.7 FW 0.005-0.044 FW <0.001 FW <0.001 FW <0.001-0.011 FW <0.001-0.025 FW
6 6 6 6 6 6 6
<0.009-0.043 FW <0.001 FW 0.002-0.027 FW
6 6 6
1.1-1.36 DW 0.7-1.12 DW
7, 9 7, 9 (Continues)
Mammals 367 Table 6.1: Element and Organism Portugal; 1998-2002 Common dolphin, Delphinus delphis Muscle Liver Skin Fat Bottlenose dolphin, Tursiops truncatus Muscle Liver Skin Fat
Cont’d
Concentration
Reference
8.5 7.8 3.7 1.7
(4.5-15.0) DW (3.5-9.1) DW (1.3-12.0) DW (1.6-2.6) DW
24 24 24 24
7.1 2.6 2.8 1.6
(6.0-8.0) (2.2-3.1) (1.1-4.5) (1.0-1.9)
24 24 24 24
DW DW DW DW
Whales; oil
0.6-2.8 FW
Florida manatee, Trichechus manatus latirostris; 2007; Crystal River, Florida; blood vs. skin
0.34 (0.29-0.43) FW vs. 0.05 (0.03-0.08) FW
22
1.8 DW; max. 3.8 DW 2.4 DW; max. 3.9 DW 2.1 DW; max. 4.2 DW 1.8 DW; max. 3.2 DW 2.3 DW; max. 4.4 DW 0.131 FW vs. 0.055 FW
12 12 12 12 12 18
0.131 FW vs. 0.055 FW
18
0.062 FW; max. 0.14 FW 0.32 FW; max. 0.89 FW
13 13
0.6-1.1 (0.5-14.0) FW 0.6-0.8 (0.5-2.0) FW
15 15
Bottlenose dolphin, Tursiops truncatus Skin; 2003-2005; South Carolina Juvenile male Adult male Juvenile female Adult female Pregnant female Blood; summers 2003-2005; Charleston, South Carolina vs. Indian River, Florida Sarasota Bay, Florida; 2002-2004 Blood Skin California sea lion, Zalophus californianus; southern California; found stranded; 2003-2004 Liver Kidney
a
4
Boron Harbor seal, Phoca vitulina Blood Spleen Muscle
2.0 FW 0.5 FW 0.3 FW
5 5 5 (Continues)
368 Chapter 6 Table 6.1: Element and Organism Liver Heart Kidney
Cont’d
Concentration 0.2 FW 0.1 FW 0.01 FW
Reference
a
5 5 5
Values are in mg As/kg fresh weight (FW) or dry weight (DW). a 1, Lunde, 1970; 2, Anas, 1974; 3, Koeman et al., 1973; 4, Lunde, 1967; 5, Jenkins, 1980; 6, Goessler et al., 1998; 7, Seixas et al., 2007; 8, Veinott and Sjare, 2006; 9, Seixas et al., 2007; 10, Stockin et al., 2007; 11, Brunborg et al., 2006; 12, Stavros et al., 2007; 13, Bryan et al., 2007; 14, Kannan et al., 2007; 15, Harper et al., 2007; 16, Kannan et al., 2006; 17, Hung et al., 2007; 18, Stavros et al., 2008b; 19, Kakuschke et al., 2008b; 20, Kakuschke et al., 2005; 21, Griesel et al., 2008; 22, Stavros et al., 2008a; 23, Gray et al., 2008; 23, Agusa et al., 2008; 24, Carvalho et al., 2002; 25, Law et al., 2003.
6.3 Antimony Antimony in liver of the harbor seal, P. vitulina, was less than 0.01 mg/kg fresh weight (FW) (Koeman et al., 1973). Livers of polar bears did not exceed 0.09 mg Sb/kg DW (Table 6.1; Kannan et al., 2007). Skin from bottlenose dolphins, T. truncatus, taken in 2003–2005 near Charleston, South Carolina, had mean antimony concentrations of 0.8–1.0 mg Sb/kg DW, with a maximum value recorded of 1.5 mg Sb/kg DW in skin from a juvenile female (Stavros et al., 2007).
6.4 Arsenic The highest arsenic concentrations recorded in marine mammals were 2.8 mg/kg FW in a sample of whale oil from Norway (Lunde, 1967; Table 6.1) and 9.1–15.1 mg As/kg DW in muscle, liver, and skin tissues of the common dolphin, Delphinus delphis from Portugal in 1998–2002 (Carvalho et al., 2002; Table 6.1). Arsenic concentrations in liver and kidney of the La Plata river dolphin, Pontoporia blainvillei, showed a significant correlation, indicating proportional accumulation (Seixas et al., 2007). Crustaceans are reported to be an important source of arsenic in diets of cetaceans (Kubota et al., 2001, 2002). Antarctic region seal hairs recovered from sediment cores representing the past 1500 years contained 0.2–2.4 mg As/kg DW, with no clear temporal trend (Yin et al., 2006). The potential risks associated with consumption of seafoods containing arsenobetaine—the major arsenic compound in total arsenic burdens—seem to be minor. The chemical was not mutagenic in the bacterial Salmonella typhimurim assay (Ames test), had no effect on metabolic inhibition of Chinese hamster ovary cells at 10,000.0 mg/L, and showed no synergism or antagonism on the action of other contaminants (Jongen et al., 1985). Arsenobetaine was not toxic to mice at oral doses of 10,000.0 mg/kg body weight during a 7-day observation period, rapidly absorbed from the gastrointestinal tract, and rapidly excreted in urine without metabolism owing to its high polar and hydrophilic characteristics
Mammals 369 (Kaise and Fukui, 1992; Kaise et al., 1985). For human adults, seafood contributes 74–96% of the total daily arsenic intake, and rice and rice cereals most of the remainder. For infants, 41% of the estimated total arsenic intake arise from seafood and 34% from rice and rice cereals (Tao and Bolger, 1998). No data were available for arsenic toxicity to marine mammals in the laboratory or under natural conditions (Eisler, 2000a).
6.5 Barium Livers from adult female southern sea otters, Enhydra lutris nereis, found dead along the California coast between 1992 and 2002 contained 0.006–0.16 mg Ba/kg DW (Kannan et al., 2006). Livers from polar bears, Ursus maritimus, from the Beaufort Sea subpopulation collected 1993–2002 contained 0.004 (0.001–0.013) mg Ba/kg DW; however, livers from the Chukchi Sea subpopulation contained 0.046 (0.001–0.56) mg Ba/kg DW and were significantly higher (Kannan et al., 2007). The maximum barium concentration recorded in striped dolphin, Stenella coeruleoalba, from Japanese coastal waters was 0.010 mg Ba/kg DW in muscle (Agusa et al., 2008). Biopsied skin samples from bottlenose dolphins, T. truncatus, were collected between 2003 and 2005 from animals captured off Charleston, South Carolina (Stavros et al., 2007). Mean barium concentrations ranged from 0.05 mg Ba/kg DW in both juvenile males and adult females to 0.16 mg Ba/kg DW in adult males (max. 2.1 mg Ba/kg DW); intermediate mean values were documented for juvenile females (0.13 mg Ba/kg DW), and pregnant females (0.09 mg Ba/kg DW; Stavros et al., 2007). Blood of bottlenose dolphins collected from Florida and South Carolina during summers of 2003–2005 contained mean concentrations of 0.084 mg Ba/L (South Carolina) and 0.088 mg Ba/L (Florida; Stavros et al., 2008b). Mean barium concentrations in serum and hair of Weddell seals from the Antarctic region in 2002–2003 were 0.08 mg Ba/kg DW and 4.8 mg Ba/kg DW, respectively (Gray et al., 2008). Mean (range) barium concentrations in blood of the Florida manatee, Trichechus manatus latirostris, in the Crystal River, Florida, in January 2007 was 0.09 (0.00–0.15) mg Ba/kg FW; skin contained 0.04 (0.01–0.07) mg Ba/kg FW (Stavros et al., 2008a). A tusk from a 55-year-old pregnant dugong, Dugong dugon, contained 4.5 (2.5–8.1) mg Ba/kg FW (Edmonds et al., 1997).
6.6 Beryllium Skin from juveniles and adults of bottlenose dolphins, T. truncatus, from South Carolina in 2003–2005 contained mean beryllium concentrations between 0.06 and 0.08 mg Be/kg DW; a maximum concentration of 0.24 mg Be/kg DW was recorded in skin of an adult male (Stavros et al., 2007).
370 Chapter 6 Blood of captive harbor seals, P. vitulina, held in Germany contained a maximum of 0.0001 mg Be/L FW (Kakuschke et al., 2008b); free-ranging harbor seals from the North Sea contained a maximum of 0.0002 mg Be/kg FW (Kakuschke et al., 2005). Blood of harbor seals from the German section of the Wadden Sea in 2004–2005 had a maximum of 0.0018 mg Be/kg FW; seals from Danish areas had a maximum of 0.00018 mg Be/kg FW (Griesel et al., 2008). Lymphocyte proliferation of newborn harbor seals was inhibited during incubation in 50.0 mg Be/L for 5 days (Kakuschke et al., 2008a).
6.7 Bismuth Livers from adult female southern sea otter, E. lutris nereis, found dead along the central California coast between 1992 and 2002 contained 0.01 (<0.001–0.075) mg Bi/kg DW (Kannan et al., 2006). Bismuth concentrations in livers of polar bears from the Beaufort Sea subpopulation collected during 1993–2002 were 0.002 (0.001–0.005) mg/kg DW; livers from bears of the Chukchi Sea subpopulation had significantly higher bismuth levels at 0.006 (0.002–0.013) mg Bi/kg DW (Kannan et al., 2007). Bismuth concentrations in serum and hair of Antarctic region seals in 1999–2003 were below detection limits of 0.001 mg Bi/kg DW (Gray et al., 2008).
6.8 Boron There is a developing literature on boron essentiality and deficiency, but little is known of boron requirements of marine mammals (Eisler, 2000b). The highest boron concentration recorded in marine mammals is 2.0 mg B/kg FW blood of the harbor seal, P. vitulina (Table 6.1). The risk to aquatic ecosystems from boron is generally considered low (Howe, 1998).
6.9 Cadmium Cadmium concentrations were almost always highest in kidney and liver and lowest in fat and muscle (Dehn et al., 2006b; Table 6.2). The high concentration of 71.3 mg Cd/kg FW reported in kidney of striped dolphin, S. coeruleoalba from Brazil (Table 6.2), is attributed mainly to a diet of squid (Dorneles et al., 2007). In general, increasing body length in seals was associated with increasing cadmium burdens in kidney (Harper et al., 2007; Veinott and Sjare, 2006) and liver (Harper et al., 2007). In some cases, cadmium concentrations in liver were sufficiently elevated, that is, >15.0 mg Cd/kg FW (Table 6.2), as to pose a threat of cadmium poisoning to humans consuming this organ (Eisler, 2007). As was true for kidney, liver cadmium concentrations were higher in older mammals (Dehn et al., 2006b; Endo et al., 2007b; Lavery et al., 2008; Seixas et al., 2007). Cadmium concentrations in the kidney cortex of ringed seals, Phoca hispida, collected in Greenland during 1988 averaged 44.5 mg Cd/kg FW,
Mammals 371 Table 6.2: Cadmium Concentrations in Field Collections of Mammals Organism Alaska; Barrow; 1998-2001 Bowhead whale, Balaena mysticetus Kidney Liver Beluga whale, Delphinapterus leucas Kidney Liver Bearded seal, Erignathus barbatus Kidney Liver Gray whale, Eschrichtius robustus Kidney Liver Ringed seal, Phoca hispida; Holman, Canada Kidney Liver Ringed seal; Barrow, Alaska Kidney Liver Spotted seal, Phoca largha Kidney Liver Polar bear, Ursus maritimus Kidney Liver Australia; 1995-1996; stranded; liver vs. kidney Bottlenose dolphin, Tursiops truncatus aduncus Adult female Female calf Common dolphin, Delphinus delphis; juvenile Melon-headed whale, Peponocephala electra; adults Bowhead whale, Balaena mysticetus; Barrow, Alaska; 1983-2001 Liver Kidney
Concentration
Reference
15.0 (<0.01-64.0) FW 7.3 (0.03-50.9) FW
31 31
10.2 (0.5-20.4) FW 3.0 (0.05-7.1) FW
31 31
31.5 (1.3-94.5) FW 8.7 (0.6-33.6) FW
31 31
1.2 (0.01-5.1) FW 0.5 (0.01-2.2) FW
31 31
30.4 (4.5-77.1) FW 6.6 (1.2-18.1) FW
31 31
14.7 (<0.01-50.7) FW 3.6 (<0.01-11.8) FW
31 31
2.6 (0.8-7.7) FW 0.4 (0.09-2.2) FW
31 31
9.0 (1.4-19.6) FW 0.47 (0.1-1.2) FW
31 31
3.7 FW vs. 15.0 FW 0.07 FW vs. <0.02 FW 0.02 FW vs. 0.07 FW
58 58 58
8.0-21.0 FW vs. 46.0-69.0 FW
58
7.8 (0.03-50.9) FW 16.5 (0.01-64.0) FW
a
17-19, 52 17-19, 52 (Continues)
372 Chapter 6 Table 6.2: Organism Muscle Epidermis Brazil; 9 spp.; cetaceans; Rio de Janeiro state; industrialized area; found stranded; October 1995November 2003; kidney Tucuxi dolphin, Sotalia guianensis Bottlenose dolphin, Tursiops truncatus Rough-toothed dolphin, Steno bredanensis Atlantic spotted dolphin, Stenella fontinalis Pantropical spotted dolphin, Stenella attenuate Spinner dolphin, Stenella longirostris Striped dolphin, Stenella coeruleoalba Long-beaked common dolphin, Delphinus capensis Dwarf sperm whale, Kogia sima
Cont’d
Concentration 0.07 (0.01-0.61) FW 0.01 (0.01-0.07) FW
Reference 17-19 17-19
1.8 (0.004-3.3) FW 1.1 (0.15-2.0) FW 0.82 (0.04-2.4) FW
40 40 40
5.9 (3.4-10.6) FW
40
35.9 FW
40
10.1 FW 71.3 FW 8.8 FW
40 40 40
6.0 (3.5-8.4) FW
40
Northern fur seal, Callorhinus ursinus Kidney Liver Hair; Japan Liver Kidney
0.1-15.6 FW 0.5-4.6 FW 0.63 DW 78.8 DW 255.0 DW
1 1 24 57
Cetaceans; 6 spp.; found stranded; Ligurian Sea; 1990-2004 Muscle Kidney Liver Brain
0.04-0.38 0.04-60.0 0.04-38.0 0.01-0.28
49 49 49 49
Hooded seal, Cystophora cristata; liver; Greenland; March 1984 Beluga whale, Delphinapterus leucas Muscle Liver Kidney Point Lay/Wainwright, Alaska; 1992-1999 Liver Kidney
DW DW DW DW
8.1-25.4 FW
0.007 FW 0.90 FW 1.9 FW
3.1 (0.05-7.1) FW 10.2 (0.5-20.4) FW
a
44
2 2 2
17, 19, 20 17, 19, 20 (Continues)
Mammals 373 Table 6.2: Organism Muscle Epidermis
Cont’d
Concentration
Reference
a
0.06 (0.01-0.21) FW 0.01 (0.01-0.02) FW
17, 19, 20 17, 19, 20
0.12 FW 52.0 FW 21.0 FW
28 28 28
1.1 FW; max. 10.9 FW
48
4.1 FW; max. 20.0 FW
48
6.5 FW; max. 99.9 FW 0.05 FW; max. 0.33 FW
48 48
Southern sea otter, Enhydra lutris nereis; adult females; found dead along central California coast; 1992-2002; liver Nondiseased Emaciated Infectious-diseased
63.0 (0.002-199.0) DW 123.0 (24.4-728.0) DW 89.0 (67.0-402.0) DW
41 41 41
Gray whale, Eschrichtius robustus; Lorino/Lavrentiya, Russia; 2001 Liver Kidney Muscle Epidermis
0.47 (0.01-2.20) FW 1.2 (0.01-5.1) FW 0.02 (0.01-0.05) FW 0.01 (0.01-0.01) FW
17 17 17 17
Pilot whale, Globicephala macrorhynchus Blubber Liver Kidney
0.34-0.75 FW 11.3-19.0 FW 27.1-41.8 FW
Long-finned pilot whale, Globicephala melas; Faroe Islands; 1986 Erythrocytes Kidney
(0.8-699.0) FW 86.0 (2.0-194.0) FW
Common dolphin, Delphinus sp.; found stranded; New Zealand; December 2004; max. concentration Blubber Kidney Liver Dolphins; 3 spp.; South Australia; 1988-2004; found stranded or by-caught Common dolphin, Delphinus delphis; liver Bottlenose dolphin, Tursiops truncatus; liver Dolphin, Tursiops aduncus Liver Bone
3 3 3
11 11 (Continues)
374 Chapter 6 Table 6.2: Organism Liver Plasma
Cont’d
Concentration
Reference
77.0 (2.0-167.0) FW (0.6-238.0) FW
11 11
125.0 DW 109.0 DW
57 57
<0.02-0.4 FW 1.9-36.6 FW 9.0-110.0 FW
12 12 12
Max. 0.1 FW 0.04-14.2 FW 3.0-54.0 FW
12 12 12
Max. 0.02 FW Max. 1.7 FW Max. 18.6 FW
12 12 12
Greenland Sea; March-April 1999; reproductively active females during suckling period Harp seal, Pagophilus groenlandicus Muscle Liver Kidney Hooded seal, Cystophora cristata Muscle Liver Kidney
0.09 FW 23.0 (4.8-59.0) FW 43.0 (13.0-76.0) FW
29 29 29
0.11 FW 28.0 (7.1-79.0) FW 93.0 (43.0-227.0) FW
29 29 29
Gray seal, Halichoerus grypus; liver
0.021 FW
Risso’s dolphin, Grampus griseus Liver Kidney Greenland; 1975-1991 Seals; 3 spp. Muscle Liver Kidney Whales; 4 spp. Muscle Liver Kidney Polar bear Muscle Liver Kidney
Hong Kong; found stranded; stomach contents Humpback dolphin, Sousa chinensis Finless porpoise, Neophocaena phocaenoides Leopard seal, Hydrurga leptonyx; serum
a
2
0.02 (0.003-0.059) FW 0.07 (0.003-0.43) FW
43 43
0.53 FW
53 (Continues)
Mammals 375 Table 6.2:
Cont’d
Organism
Concentration
Northern bottlenose whale; Hyperoodon ampullatus Muscle Liver
0.04 FW 5.6 FW
Weddell seal, Leptonychotes weddelli; Antarctica Hair Serum vs. hair
0.53 FW <0.001 DW vs. 2.8 DW
25 53
Marine mammals Liver 2 spp. 3 spp. 13 spp. Muscle; 3 spp. Spleen; 3 spp. Pancreas; 3 spp. Stomach wall; 3 spp. Fat; 3 spp.
1.26 FW 1.37-11.0 DW Usually <8.0 (0.0-35.0) FW 0.31-1.10 DW 1.56-6.69 DW 0.91-6.33 DW 0.35-3.59 DW 0.14-0.19 DW
7 8 13 8 8 8 8 8
Southern elephant seal, Mirounga leonina; molted fur; Shetland Islands juveniles vs. adult females
Max. 0.12 DW vs. 0.38 (0.21-0.89) DW
22
Mediterranean monk seal, Monachus monachus; Greece; hair
0.21 DW
24
46.5 FW; max. 99.0 FW 9.5 FW; max. 50.0 FW
14 14
6.8 DW 0.7-2.7 DW
15 15
7.8 FW vs. Below Detection Limits (BDL) 9.0 FW vs. BDL BDL vs. BDL
45
Pacific walrus, Odobenus rosmarus divergens 1981-1984 Kidney Liver 1991; spring, Alaska; Bering Sea; diet Clam, Mya sp. Other food items Killer whale, Orcinus orca; found stranded; Japan; February 2005; adults vs. calves Liver Kidney Muscle
Reference
a
2 2
45 45 (Continues)
376 Chapter 6 Table 6.2:
Cont’d
Organism
Concentration
Melon-headed whale, Peponocephala electra; Japan; March 2006; found stranded Liver Kidney Muscle Lung
7.2 FW 24.4 FW <0.05 FW 0.4 FW
54 54 54 54
Ringed seal, Phoca hispida Liver Kidney cortex
0.31 FW 44.5 (0.0-248.0) FW
2 56
Harbor porpoise, Phocoena phocoena Muscle Liver Kidney Kidney Greenland Denmark Ireland Western Europe; found stranded; 1997-2003 Kidney; adult Kidney; fetus vs. mother Harbor seal, Phoca vitulina Liver Liver Liver Kidney Kidney Muscle Dead on collection; adults Liver Blubber Kidney Brain Spleen Heart Placenta Dead on collection; fetuses Liver Brain
0.002-0.006 FW 0.02-0.19 FW 0.08-0.95 FW
Reference
a
2 2 2
55.3 (0.32-210.0) FW 0.25 (0.23-0.81) FW 0.90 (0.09-2.3) FW
33 34 35
1.3 (0.002-11.9) FW 0.05 FW vs. 1.62 FW
32 32
0.05-0.30 FW 1.1 FW 0.01-0.21 FW 1.9 FW 0.06-1.0 FW 0.002-0.08 FW
4 5 2 5 2 2
0.03-0.21 FW <0.01-0.02 FW 0.15-0.17 FW <0.01-0.14 FW 0.04-0.09 FW 0.06-0.47 FW <0.01 FW
6 6 6 6 6 6 6
<0.24 FW <0.01 FW
6 6 (Continues)
Mammals 377 Table 6.2: Organism Labrador and Newfoundland, Canada; body length 212-402 cm Muscle Liver vs. Kidney 212 cm 301 cm 304 cm 335 cm 402 cm Blood Captive animals Free-ranging Wadden Sea; 2004-2005; German site vs. Danish site
Cont’d
Concentration
Reference
0.003-0.32 FW
26
0.15 FW vs. 0.34 FW 0.18 FW vs. 0.25 FW 9.6 FW vs. 20.2 FW 1.6 FW vs. 6.8 FW 0.63 FW vs. 1.6 FW
26 26 26 26 26
Max. 0.0002 FW Max. 0.003 FW (<0.00012-0.0011) FW vs. 0.00014 (<0.00012-0.003) FW
46 47 50
Dall’s porpoise, Phocoenoides dalli; Japan; male; February 2000; harpooned; age 6 years Liver Kidney Muscle Skin Bone Heart Lung Intestine Spleen Pancreas Diaphragm Blubber Cerebrum Stomach
10.3 FW 30.2 FW 0.10 FW 0.009 FW 0.05 FW 0.37 FW 0.75 FW 0.65 FW 1.2 FW 1.8 FW 0.2 FW 0.05 FW 0.06 FW 1.3 FW
42 42 42 42 42 42 42 42 42 42 42 42 42 42
La Plata river dolphin, Pontoporia blainvillei Liver Kidney
0.6-0.96 DW 3.4-4.4 DW
16, 27 16, 27
Striped dolphin, Stenella coeruleoalba; kidney; found stranded; 1999-2004 Bay of Biscay, Atlantic Ocean Immatures Mature
12.9 (0.3-40.2) FW 10.6 (2.1-30.8) FW
21 21
a
(Continues)
378 Chapter 6 Table 6.2: Organism Mediterranean Sea, NW France Immatures Mature Israel, Mediterranean Sea coast
Cont’d
Concentration
Reference
0.1 (0.02-0.18) FW 12.6 (4.9-20.3) FW 14.9 (3.6-30.0) FW
21 21 39
0.007 DW 15.7 DW 18.4 DW
55 55 55
0.14 DW vs. <0.01 DW 104.0 DW vs. 0.003 DW 20.4 DW vs. 0.007 DW 0.37 DW vs. <0.001 DW
55 55 55 55
Florida manatee, Trichechus manatus latirostris; Florida; January 2007 Blood Skin
0.001 (0.001-0.003) FW 0.036 (0.005-0.067) FW
51 51
Bottlenose dolphin, Tursiops truncatus; skin 2003-2005; South Carolina 2002-2004; Sarasota Bay, Florida
0.01-0.015 DW 0.0007 FW; max. 0.004 FW
30 36
Polar bear, Ursus maritimus; liver; Alaska; 1993-2002 Beaufort Sea subpopulation Chukchi Sea subpopulation
1.1 (0.37-1.6) DW 0.98 (0.31-1.7) DW
37 37
Striped dolphin; Japan; 1979 Liver Fetus Juvenile Mature Adult male vs. female fetus Blubber Kidney Liver Muscle
California sea lion, Zalophus californianus Liver Kidney Muscle Heart Cerebellum Cerebrum Fat Mothers with premature pups vs. mothers with normal pups Liver Kidney
2.0-2.6 FW 10.1-10.2 FW 0.07-0.13 FW Max. 0.14 FW 0.05-0.61 FW 0.04-0.17 FW Max. 0.04 FW
10.0 DW vs. 15.1 DW 97.0 DW vs. 115.0 DW
a
9 9 9 9 9 9 9
10 10 (Continues)
Mammals 379 Table 6.2: Organism Found stranded; southern California; 2003-2004 Liver Kidney
Cont’d
Concentration
0.8-16.1 (0.2-142.0) FW 2.3-58.6 (0.2-231.0) FW
Reference
a
38 38
Values are in mg Cd/kg fresh weight (FW) or dry weight (DW). a 1, Anas, 1974; 2, Harms et al., 1978; 3, Stoneburner, 1978; 4, Koeman et al., 1973; 5, Roberts et al., 1976; 6, Duinker et al., 1979; 7, Holden, 1975; 8, Hamanaka et al., 1977; 9, Buhler et al., 1975; 10, Martin et al., 1976; 11, Caurant and AmiardTriquet, 1995; 12, Dietz et al., 1996; 13, Mackey et al., 1996; 14, Taylor et al., 1989; 15, Miles and Hills, 1994; 16, Seixas et al., 2007; 17, Dehn et al., 2006b; 18, Bratton et al., 1997; 19, Woshner et al., 2001; 20, Tarpley et al., 1995; 21, Lahaye et al., 2006; 22, Andrade et al., 2007; 23, Ikemoto et al., 2004a,b; 24, Yediler et al., 1993; 25, Yamamoto et al., 1987; 26, Veinott and Sjare, 2006; 27, Seixas et al., 2007; 28, Stockin et al., 2007; 29, Brunborg et al., 2006; 30, Stavros et al., 2007; 31, Dehn et al., 2006a; 32, Lahaye et al., 2007; 33, Szefer et al., 2002; 34, Das et al., 2004; 35, Das et al., 2003; 36, Bryan et al., 2007; 37, Kannan et al., 2007; 38, Harper et al., 2007; 39, Roditi-Elasar et al., 2003; 40, Dorneles et al., 2007; 41, Kannan et al., 2006; 42, Yang et al., 2006; 43, Hung et al., 2007; 44, Nielsen and Dietz, 1990; 45, Endo et al., 2007b; 46, Kakuschke et al., 2008b; 47, Kakuschke et al., 2005; 48, Lavery et al., 2008; 49, Capelli et al., 2008; 50, Griesel et al., 2008; 51, Stavros et al., 2008a; 52, Rosa et al., 2008; 53, Gray et al., 2008; 54, Endo et al., 2008; 55, Agusa et al., 2008; 56, Sonne-Hansen et al., 2002; 57, Arai et al., 2004; 58, Law et al., 2003.
ranging up to 248.0 mg/kg FW (Sonne-Hansen et al., 2002). Concentrations in the range 50.0–200.0 mg Cd/kg DW in kidney cortex may induce histopathological changes, as evidenced by glomerulonephritis in 10 of the 99 ringed seals seals examined; however, despite high levels of cadmium, no seal showed any sign of cadmium-induced kidney or bone damage (Sonne-Hansen et al., 2002). Antarctic region seal hairs recovered from sediment cores representing the past 1500 years had 0.5–2.7 mg Cd/kg DW, but with no clear temporal trend (Yin et al., 2006). In killer whales, Orcinus orca, found stranded along the coast of Japan in February 2005, there was minimal transfer of cadmium from adult females to their calves (Table 6.2; Endo et al., 2007b). In marine mammals, cadmium is present in all liver and kidney samples analyzed (Taylor et al., 1989). Cadmium concentrations in livers of beluga whales (Delphinapterus leucas) were positively correlated with age, and in ringed seals (P. hispida) with length, increasing from <0.7 to 3.6 mg Cd/kg FW in belugas and <0.14–8.8 mg/kg FW in seals (Mackey et al., 1996). Long-finned pilot whales (Globicephala melas) contained higher concentrations of cadmium in the liver and kidney tissues than did other marine mammals, and this is attributed, in part, to the elevated cadmium (as much as 5.8 mg Cd/kg DW) content in squids (Loligo forbesi)—a major dietary item (Bustamante et al., 1998; Caurant and Amiard-Triquet, 1995). Similarly, elevated levels of cadmium in Pacific walruses (Odobenus rosmarus divergens) are considered related to elevated cadmium burdens in clams (Mya sp.), a major walrus food item (Miles and Hills, 1994). Also, uptake of cadmium from cadmium-contaminated prey by fish—and eventual
380 Chapter 6 consumption by marine mammals—plays an important role in contaminated waters (Kraal et al., 1995). Although cadmium burdens were low in harbor seals, P. vitulina, from the coasts of East Anglia and West Scotland, cadmium tended to accumulate in liver and kidney with increasing age of the seal (Roberts et al., 1976). Movement of cadmium across the placenta was negligible in this species (Roberts et al., 1976). Lymphocyte proliferation of newborn harbor seals was inhibited during exposure to 6.2 mg Cd/L for 5 days (Kakuschke et al., 2008a). Concentrations of cadmium showed a significant relation between liver and kidney in the La Plata river dolphin, P. blainvillei, indicating proportional accumulation (Seixas et al., 2007). In whales, liver cadmium concentrations were positively correlated with both selenium and total mercury concentrations (Dehn et al., 2006b), as well as copper and selenium (Endo et al., 2008). Hepatic cadmium concentrations in southern sea otters, E. lutris nereis, found dead along the California coast between 1992 and 2002 were elevated in diseased and emaciated otters relative to nondiseased otters (Kannan et al., 2006). A similar case is made for manganese, cobalt, and zinc and suggests that induction of metallothionein synthesis and superoxide dismutase is occurring in these otters as a means of protecting the cells from oxidative stress-related injuries. Elevated concentrations of liver cadmium in otters in combination with other metals and several organic chemical pollutants may contribute to oxidative stress-mediated effects (Kannan et al., 2006). In bowhead whales, Balaena mysticetus from Alaska in 1983–2001, liver cadmium concentrations were positively associated with degree of lung fibromuscular hyperplasia and renal fibrosis; histopathology also increased with increasing age of the animal (Rosa et al., 2008).
6.10 Cesium Livers from polar bears, U. maritimus, collected in northern and western Alaska between 1993 and 2002 contained, on average, 0.07 mg stable cesium/kg DW (Kannan et al., 2007). Livers from adult female southern sea otters, E. lutris nereis, found dead along the central California coast between 1992 and 1993 contained a maximum of 0.03 mg Cs/kg DW (Kannan et al., 2006). Stomach contents of humpbacked dolphins, Sousa chinensis, found stranded in Hong Kong had a mean (maximum) concentration of 0.026 (0.074) mg Cs/kg FW; for finless porpoises, Neophocaena phocaenoides, these values were 0.018 (0.033) mg Cs/kg FW (Hung et al., 2007). Maximum cesium concentrations in tissues of striped dolphins, S. coeruleoalba from Japanese coastal waters were 0.02 mg/kg DW in blubber, 0.11 mg Cs/kg DW in liver, 0.13 mg/kg DW in kidney, and 0.23 mg/kg DW in muscle; adults had higher cesium burdens than did fetuses or juveniles (Agusa et al., 2008). Radiocesium-137 tends to accumulate in muscle tissue of fin whales, Balaenoptera physalis, and harp seals, Pagophilus groenlandica (Samuels et al., 1970), and this is consistent with
Mammals 381 the findings of other investigators and various groups of vertebrates. Lactating grey seals, H. grypus, collected in 1987 from the northeast Atlantic Ocean and the North Sea had 300 times more 134Cs in milk than in muscle; for pups, this value was 3 (Anderson et al., 1990). This pattern was different for 137Cs: female muscle contained 5 times more 137Cs than milk; for pups, this value was 1.5. Radiocesium-137 levels in gray seal tissues seem to reflect 137Cs levels in their fish diet; however, there is no biomagnification of 137Cs and other radionuclides (Anderson et al., 1990). An estimated 29% of the 137Cs in the diet of gray seals is from fallout of the Chernobyl nuclear power plant reactor accident of 1986 (Eisler, 1995, 2003), and 71% from the nuclear facility at Sellafield, United Kingdom (Anderson et al., 1990). Muscle samples from polar bears, seals, walrus, and whales collected between 2000 and 2003 from Svalbard, the Barents Sea, and the North Greenland Sea in 2000–2003 were analyzed for 137Cs, an anthropogenic radionuclide (Andersen et al., 2006). Mean concentrations of 137 Cs (in Bq/kg FW, with one Becquerel ¼ 1 disintegration per second) were low: <0.2 in walrus O. rosmarus; 0.22–0.25 in blue whale Balaenoptera musculus, bearded seal Erignathus barbatus, and hooded seal Cystophora cristata; 0.36 in harp seal Pagophilus groenlandicus; 0.49 in ringed seal P. hispida, 0.67 in white whale D. leucas, and 0.72 in polar bear U. maritimus (range 0.2–2.2). Differences between species may be due, in part, to varying diet, and movement and distribution patterns of individual species. Concentration factors from seawater to muscle were 79 for bearded seals sampled in 2002 to 244 for ringed seals sampled in 2003, and are higher than those reported for fish and benthic organisms, suggesting accumulation of 137Cs in marine ecosystems (Andersen et al., 2006). Radiocesium-137 content in muscle, kidney, and liver of Pacific walrus and bearded seal never exceeded 0.17 Bq/kg FW, indicating that ingestion of these tissues by human consumers posed negligible risk to health; bioconcentration factors from seawater to tissues fell between 34 and 87 (Hamilton et al., 2008).
6.11 Chromium Hexavalent chromium is more readily assimilated than the trivalent state and is about 100 times more toxic than trivalent chromium, with high accumulations in erythrocytes (Foster, 1963). However, highly vascularized organs in harbor seals found dead on collection did not contain as much chromium as brain. Chromium concentrations, in mg/kg FW, were 0.15– 0.59 in kidney, 0.7–1.2 in heart, 0.8–1.4 in spleen, and 1.0–2.8 in brain (Duinker et al., 1979). Concentrations were less than 0.5 mg Cr/kg FW in blubber of dead harbor seals (Duinker et al., 1979) and skin of cetaceans taken off Corsica (Viale, 1978). Concentrations up to 5.9 mg Cr/kg DW were recorded in liver of marine mammals found dead along the U.S. Atlantic Ocean coast in 1987–1988 (Table 6.3; Kuehl et al., 1994). Chromium does not biomagnify in marine food chains involving mammals and other marine vertebrates (Outridge and Scheuhammer, 1993).
382 Chapter 6 Table 6.3: Chromium, Cobalt, and Copper Concentrations in Field Collections of Mammals Element and Organism
Concentration
Reference
1.2 FW vs. 0.18 FW 1.0 FW vs. 0.11 FW 0.1 FW vs. 0.6 FW
50 50 50
0.15-0.41 FW vs. 0.14-0.88 FW
50
0.74 DW
22
1.2 (0.16-4.9) FW 0.55 (0.1-1.5) FW
34 34
Leopard seal, Hydrurga leptonyx; serum
0.22 FW
45
Weddell seal, Leptonychotes weddelli; Antarctica; 2002-2003; serum vs. hair
0.37 DW vs. 5.6 DW
45
a
Chromium Australia; 1995-1996; stranded; liver vs. kidney Bottlenose dolphin, Tursiops truncatus aduncus Adult female Female calf Common dolphin, Delphinus delphis; juvenile Melon-headed whale, Peponocephala electra; adults Northern fur seal, Callorhinus ursinus; Japan; hair Hong Kong; found stranded; stomach contents Humpback dolphin, Sousa chinensis Finless porpoise, Neophocaena phocaenoides
Mammals; found dead; 1987-1988; U.S. Atlantic Ocean coast; liver Common dolphin, Delphinus delphis; adult male White-sided dolphin, Lagenorhynchus acutus; adult male Bottlenose dolphin, Tursiops truncates Adult male Adult female Immature female
3.2 DW
6
5.9 DW
6
3.0 DW 3.3 DW 1.0 DW
6 6 6
Common dolphin, Delphinus sp.; found stranded; New Zealand; December 2004; all tissues
<0.1 FW
26
Southern sea otter, Enhydra lutris nereis; found dead; California coast; 1992-2002; adult females; liver
(0.16-2.3) DW
32
(Continues)
Mammals 383 Table 6.3:
Cont’d
Element and Organism
Concentration
Reference
Harbor seal, Phoca vitulina; blood Captive animals Free-ranging Wadden Sea; 2004-2005; German site vs. Danish site
0.002-0.009 FW 0.007-0.050 FW 0.007 FW vs. 0.011 FW
37 38 42
(<0.003-0.48) DW vs. (<0.003-0.74) DW
21
0.52 FW 0.10-0.23 FW
33 33
0.09 FW
33
0.63 DW 0.37 DW 0.59 DW
47 47 47
4.2 DW vs. 6.4 DW 0.75 DW vs. 1.3 DW 0.30 DW vs. 0.63 DW 0.63 DW vs. 0.60 DW
47 47 47 47
0.80-0.98 DW; max. 2.2 DW
27
0.30 (0.22-0.46) DW 0.37 (0.17-0.96) DW
30 30
<0.02 FW 0.03 FW
26 26
Southern elephant seal, Mirounga leonina; molted fur; Shetland Islands; juveniles vs. adult females Dall’s porpoise, Phocoenoides dalli; Japan; February 2006; male; harpooned Blubber Liver, kidney, muscle, skin, bone, intestine, spleen, diaphragm, cerebrum, stomach Heart, lung, pancreas Striped dolphin, Stenella coeruleoalba; Japan; 1979 Liver Fetuses Juveniles Adults Adult male vs. female fetus Blubber Kidney Liver Muscle Bottlenose dolphin, Tursiops truncatus; skin; 2003-2005; South Carolina Polar bear, Ursus maritimus; liver; 1993-2002 Beaufort Sea area Chukchi Sea area
a
Cobalt Common dolphin, Delphinus sp.; New Zealand; found stranded; December 2004 Blubber, liver Kidney
(Continues)
384 Chapter 6 Table 6.3:
Cont’d
Element and Organism
Concentration
Reference
Southern sea otter, Enhydra lutris nereis; adult females; found dead along central California coast; 1992-2002; liver
0.08 DW; max. 0.25 DW
32
Hong Kong; found stranded; stomach contents Humpback dolphin Finless porpoise
0.043 (0.004-0.16) FW 0.027 (0.008-0.068) FW
34 34
Leopard seal, Hydrurga leptonyx; serum
<0.001 FW
45
Weddell seal, Leptonychotes weddelli; Antarctica; 2002-2003; serum vs. hair
<0.001 DW vs. 0.04 DW
45
0.004-0.005 FW 0.014-0.023 FW 0.016-0.025 FW
25 25 26
0.0004-0.005 FW Not detectable-0.008 FW 0.00051 FW vs. 0.00053 FW
37 38 42
0.14 FW 0.01-0.02 FW 0.001-0.009 FW
33 33 33
2.8 (1.4-5.4) DW 3.7 (2.3-7.8) DW 4.2 (2.3-14.2) DW <0.8 DW
49 49 49 49
<1.4 DW <1.2 DW 3.1 (2.4-3.8) DW <0.8 DW
49 49 49 49
Max. 0.04 DW
47
Harbor seal, Phoca vitulina Labrador and Newfoundland, Canada; body lengths 212-402 cm Muscle Liver Kidney Blood Captive animals Free-ranging Wadden Sea; 2004-2005; German site vs. Danish site Dall’s porpoise, Phocoenoides dalli; Japan; 2006; male; age 6 years Bone Liver, kidney, heart, stomach Muscle, skin, lung, intestine, spleen, pancreas, diaphragm, blubber, cerebrum Portugal; 1998-2002 Common dolphin, Delphinus delphis Muscle Liver Skin Fat Bottlenose dolphin, Tursiops truncates Muscle Liver Skin Fat Striped dolphin; all tissues
a
(Continues)
Mammals 385 Table 6.3:
Cont’d a
Element and Organism
Concentration
Reference
Florida manatee, Trichechus manatus latirostris; Florida; 2007 Blood Skin
0.002 (0.000-0.003) FW 0.009 (0.005-0.013 FW)
43 43
0.39-0.73 DW; max. 1.6 DW 0.14 FW; max. 0.34 FW
27 29
0.02 DW 0.02 DW
30 30
8.5 FW vs. 4.7 FW 18.0 FW vs. 10.0 FW 11.0 FW vs. 3.9 FW
50 50 50
2.1-4.9 FW vs. 2.4-2.9 FW
50
9.8 (1.1-203.8) FW 2.4 (0.8-7.9) FW 0.65 (0.47-1.1) FW 0.38 (0.25-0.70) FW
17-19, 44 17-19, 44 17-19 17-19
6.1 DW
22
Cetaceans; 6 spp.; Ligurian Sea; found stranded; 1990-2004 Muscle Kidney Liver Brain
1.6-5.1 DW 6.7-38.9 DW 4.7-43.4 DW 6.3-15.5 DW
41 41 41 41
Beluga whale, Delphinapterus leucas Muscle Liver
1.1 FW 20.4 FW
Bottlenose dolphin, Tursiops truncatus Skin; 2003-2005; South Carolina Skin; 2002-2004; Sarasota Bay, Florida Polar bear, Ursus maritimus; liver; 1993-2002 Beaufort Sea area Chukchi Sea area Copper Australia; 1995-1996; stranded; liver vs. kidney Bottlenose dolphin, Tursiops truncatus aduncus Adult female Female calf Common dolphin, Delphinus delphis; juvenile Melon-headed whale, Peponocephala electra; adults Bowhead, Balaena mysticetus; Barrow, Alaska; 1983-2001 Liver Kidney Muscle Epidermis Northern fur seal, Callorhinus ursinus; hair; Japan
1 1 (Continues)
386 Chapter 6 Table 6.3: Element and Organism Kidney Point Lay/Wainwright, Alaska; 1992-1999 Liver Kidney Muscle Epidermis Common dolphin, Delphinus sp.; found stranded; New Zealand; December 2004; max. concentrations Blubber Kidney Liver Dolphins; 3 spp.; South Australia; 1988-2004; found stranded or bycaught; liver Common dolphin, Delphinus delphis Bottlenose dolphin, Tursiops truncates Dolphin, Tursiops aduncus Southern sea otter, Enhydra lutris nereis; adult females; found dead along central California coast; 1992-2002; liver Nondiseased Emaciated Infectious-diseased Gray whale, Eschrichtius robustus Stranded along North American west coast; 1988-1991 Brain Kidney Liver Stomach contents Lorino/Lavrentiya, Russia; 2001 Liver Kidney Muscle Epidermis Stellar sea lion, Eumetopias jubatus; teeth; North Pacific; 1968-1999
Cont’d
Concentration 3.1 FW
Reference
a
1
25.0 (4.9-156.8) FW 2.0 (1.3-2.9) FW 1.0 (0.4-1.5)FW 0.5 (0.2-0.8) FW
17, 17, 17, 17,
0.59 FW 5.4 FW 14.0 FW
26 26 26
11.3 (3.0-71.2) FW 21.2 (4.9-85.0) FW
40 40
19.7 (0.6-73.7) FW
40
124.0 (45.3-274.0) DW 161.0 (37.4-401.0) DW 115.0 (26.3-337.0) DW
32 32 32
2.4 FW 2.4 (0.5-4.9) FW 9.2 (0.6-25.0) FW 21.0 (3.0-66.0) FW
7 7 7 7
18.9 (0.2-154.5) FW 2.5 (1.3-4.6) FW 3.2 (0.5-8.0) FW 1.6 (0.01-8.3) FW
17 17 17 17
7.7 (1.2-77.0) DW
48
19, 19, 19, 19,
20 20 20 20
(Continues)
Mammals 387 Table 6.3: Element and Organism Pilot whale, Globicephala melaena; stranded on Cape Cod, Massachusetts; 1986-1990 Adults Brain Kidney Liver Ovary Fetuses Brain Kidney Gray seal, Halichoerus grypus Liver Liver British Isles and vicinity; 1988-1989 Blubber Kidney Liver Muscle
Cont’d
Concentration
Reference
9.1 (5.7-12.3) DW 14.7 (7.4-21.0) DW 15.5 (9.9-20.3) DW 5.5 (2.8-8.4) DW
8 8 8 8
5.1 (4.4-6.2) DW 20.0 (8.1-28.1) DW
8 8
14.6 FW 20.9 FW
2 1
<0.1 FW (3.2-27.0) FW (4.0-26.0) FW 2.5 FW
9 9 9, 10 9, 10
Hong Kong; found stranded; stomach contents Humpback dolphin Finless porpoise
7.3 (0.36-36.4) FW 3.4 (0.55-8.5) FW
34 34
Leopard seal, Hydrurga leptonyx; Antarctic region Kidney Liver Muscle Stomach contents Serum
32.6 (22.5-43.8) DW 105.0 (98.0-116.0) DW 4.0 (2.5-8.4) DW 14.4 (13.3-16.4) DW 0.61 FW
11 11 11 11 45
Northern bottlenose whale, Hyperoodon albirostris Muscle Liver
0.55 FW 2.8 FW
1 1
Pigmy sperm whale, Kogia breviceps; Argentina; found dead Heart Kidney Liver Other tissues
6.9 FW 7.4 FW 10.3 FW <2.3 FW
12 12 12 12
a
(Continues)
388 Chapter 6 Table 6.3:
Cont’d
Element and Organism
Concentration
Reference
Whitebeaked dolphin, Lagenorhynchus albirostris Fat, blubber Liver Muscle Testicles Pancreas Kidney Lungs Spleen
<2.0 FW 6.4 FW 1.4 FW 0.9 FW 1.6 FW 2.8 FW 1.4 FW 0.7 FW
Weddell seal, Leptonychotes weddelli; Antarctic region Hair Kidney Liver Muscle Serum vs. hair
4.4 DW 22.8 (21.7-24.5) DW 57.4 (28.0-87.0) DW 2.8 (2.1-3.1) DW 0.36 DW vs. 15.1 DW
24 11 11 11 45
Crabeater seal, Lobodon carcinophagus; Antarctic region; 1989 Kidney Liver Muscle
25.6 (18.9-39.5) DW 71.1 (42.0-105.0) DW 3.3 (2.7-4.3) DW
11 11 11
Marine mammals; 17 spp.; adults; found dead; 1989-1991; coast of Wales and Irish Sea; liver
Usually 3.2-30.0 FW
17
Southern elephant seal, Mirounga leonina; molted fur; Shetland Islands; juveniles vs. adult females
11.2 (2.1-21.7) DW vs. 12.9 (8.3-27.3) DW
21
Mediterranean monk seal, Monachus monachus; Greece; hair
12.6 DW
23
Killer whale, Orcinus orca; found stranded; Japan; March 2005; adults vs. calves Liver Kidney Muscle
11.5 FW vs. 10.4 FW 3.0 FW vs. 3.3 FW 0.7 FW vs. 1.6 FW
35 35 35
Melon-headed whale, Peponocephala electra; Japan; March 2006; found stranded Liver Kidney
5.9 FW 4.2 FW
46 46
a
3 3 3 3 3 3 3 3
(Continues)
Mammals 389 Table 6.3: Element and Organism Muscle Lung Ringed seal, Phoca hispida; liver Harbor seal, Phoca vitulina Liver Muscle Liver Kidney Liver; British Isles; 1988-1989 Dead on collection; adults Blubber Liver Kidney Brain Spleen Heart Placenta Dead on collection; fetuses Liver Brain From Labrador and Newfoundland, Canada; body length 212-402 cm Muscle Liver Kidney Blood Captive animals Free-ranging Wadden Sea; 2004-2005; German site vs. Danish site Harbor porpoise, Phocoena phocoena Blubber Liver Muscle Liver Kidney Liver; England; 1988-1989 Greenland; 1988-1989 Kidney Liver
Cont’d
Concentration
Reference
0.9 FW 0.7 FW
46 46
2.1 FW
1
14.6 FW 0.8-2.5 FW 2.6-17.0 FW 2.3-4.0 FW 7.0-21.0 FW
2 1 1 1 10
0.9-3.0 FW 2.0-20.0 FW 4.8-5.1 FW 2.5-9.5 FW 3.3-4.0 FW 5.8-8.2 FW 2.0 FW
4 4 4 4 4 4 4
49.0 FW <1.0 FW
4 4
1.3-1.9 FW 11.5-19.0 FW 5.4-10.0 FW
25 25 25
0.75-1.0 FW 0.55-1.1 FW 0.88 (0.60-1.37) FW vs. 0.77 (0.53-0.98) FW
37 39 42
1.5 (1.0-2.7) FW 4.5 (2.6-8.3) FW 1.8-2.7 FW 4.0-15.0 FW 1.1-3.2 FW 6.0-160.0 FW
3 3 1 1 1 10
5.5 (3.7-8.0) FW 12.0 (5.0-50.0) FW
13 13
a
(Continues)
390 Chapter 6 Table 6.3: Element and Organism
Cont’d
Concentration
Reference
2.0 (1.1-5.4) FW 1.0 (0.6-1.9) FW
13 13
3.8 (2.1-8.9) FW 12.7 (2.1-194.0) FW 87.2 FW vs. 19.3 FW 1.8 FW vs. 2.9 FW
28 28 28 28
55.9 FW vs. 11.1 FW
28
Dall’s porpoise, Phocoenoides dalli; Japan; male; February 2000; harpooned; age 6 years Liver Kidney Muscle Skin Bone Heart Lung Intestine Spleen Pancreas Diaphragm Blubber Cerebrum Stomach
9.7 5.4 3.2 1.0 1.1 3.9 1.1 1.7 1.0 3.9 1.6 0.3 6.0 3.2
33 33 33 33 33 33 33 33 33 33 33 33 33 33
La Plata river dolphin, Pontoporia blainvillei; Argentina; found dead Kidney Liver Other tissues
14.0 FW 16.0 FW <2.8 FW
12 12 12
8.1 (5.3-20.3) DW 22.0 (7.8-29.3) DW 5.5 (3.8-7.7) DW 2.7 (2.1-3.3) DW
49 49 49 49
7.1 (5.9-8.2) DW 20.0 (16.0-25.0) DW
49 49
Muscle Skin Europe; 1997-2003 Kidney; adults Liver; adults Liver; fetus vs. mother; Irish Sea Kidney; fetus vs. mother; southern Ireland Liver; fetus vs. mother; southern Ireland
Portugal; 1998-2002 Common dolphin, Delphinus delphis Muscle Liver Skin Fat Bottlenose dolphin, Tursiops truncates Muscle Liver
FW FW FW FW FW FW FW FW FW FW FW FW FW FW
a
(Continues)
Mammals 391 Table 6.3: Element and Organism Skin Fat Striped dolphin, Stenella coeruleoalba; Wales; 1989; found dead; blubber vs. liver Striped dolphin; Japanese coastal waters; 1979 Liver Fetuses Juveniles Adults Adult male vs. female fetus Blubber Kidney Liver Muscle
Cont’d
Concentration
Reference
5.9 (7.2-8.6) DW 3.1 (2.9-3.2) DW
49 49
0.3-0.7 FW vs. 2.1 FW
9
326.0 DW 24.7 DW 24.6 DW
47 47 47
0.68 DW vs. 0.67 DW 14.0 DW vs. 9.3 DW 25.1 DW vs. 326.0 DW 7.5 DW vs. 3.7 DW
47 47 47 47
175.0 (4.4-1200.0) DW
14
Florida manatee, Trichechus manatus latirostris; Florida; 2007 Blood Skin
0.77 (0.56-0.93) FW 0.51 (0.31-0.74) FW
43 43
Dolphin, Tursiops gephyreus; Argentina; found dead Blubber Kidney Liver Melon Muscle Stomach contents
4.0 FW 29.5 FW 77.7 FW 2.7 FW 6.3 FW 1.2 FW
12 12 12 12 12 12
4.0-12.0 FW 0.9-1.1 FW vs. 2.5 FW
10 9
1.6 1.5 1.7 0.9 1.6
27 27 27 27 27
Manatee, Trichechus manatus; Florida; 1977-1981; liver
Bottlenose dolphin, Tursiops truncatus Liver; England; 1988-1989 Wales; 1989; blubber vs. muscle Skin; 2003-2005; South Carolina Juvenile males Adult males Juvenile females Adult females Pregnant females Sarasota Bay, Florida; 2002-2004
DW; DW; DW; DW; DW;
max. max. max. max. max.
2.4 2.1 2.4 7.2 1.8
DW DW DW DW DW
a
(Continues)
392 Chapter 6 Table 6.3: Element and Organism Blood Skin Blood; summers 2003-2005; South Carolina vs. Florida Polar bear, Ursus maritimus Canada, Northwest Territories; 1982-1984; liver Svalbard; Arctic Ocean region; 1978-1989; adults vs. juveniles Kidney Liver Liver; Alaska; 1993-2002 Beaufort Sea area Chukchi Sea area Whales; unidentified; 1989; found dead Blubber Liver Muscle California sea lion, Zalophus californianus Mothers with premature pups vs. mothers with normal pups Liver Kidney Premature pups vs. normal pups Liver Kidney Found stranded; southern California; 2003-2004 Liver Kidney
Cont’d
Concentration
Reference
0.87 FW; max. 1.5 FW 0.61 FW; max. 1.33 FW 0.74 FW vs. 0.80 FW
29 29 36
81.0-146.0 DW
15
8.3 FW vs. 6.2 FW 42.0 FW vs. 33.0 FW
16 16
94.7 (50.4-159.0) DW 141.0 (55.9-285.0) DW
30 30
0.2-1.7 FW 6.6-8.7 FW 3.0 FW
9 9 9
135.0 DW vs. 86.0 DW 29.3 DW vs. 22.4 DW
5 5
194.0 DW vs. 146.0 DW 19.0 DW vs. 28.4 DW
5 5
36.3-45.3 (7.6-138.0) FW 8.5-10.3 (3.0-19.8) FW
31 31
a
Values are in mg Cu/kg fresh weight (FW) or dry weight (DW). a 1, Harms et al., 1978; 2, Holden and Topping, 1972; 3, Andersen and Rebsdorff, 1976; 4, Duinker et al., 1979; 5, Martin et al., 1976; 6, Kuehl et al., 1994; 7, Varanasi et al., 1994; 8, Meador et al., 1993; 9, Morris et al., 1989; 10, Law et al., 1991; 11, Szefer et al., 1994; 12, Marcovecchio et al., 1990; 13, Paludan-Muller et al., 1993; 14, O’Shea et al., 1984; 15, Braune et al., 1991; 16, Norheim et al., 1992; 17, Dehn et al., 2006b; 18, Bratton et al., 1997; 19; Woshner et al., 2001; 20, Tarpley et al., 1995; 21, Andrade et al., 2007; 22, Ikemoto et al., 2004a,b; 23, Yediler et al., 1993; 24, Yamamoto et al., 1987; 25, Veinott and Sjare, 2006; 26, Stockin et al., 2007; 27, Stavros et al., 2007; 28, Lahaye et al., 2007; 29, Bryan et al., 2007; 30, Kannan et al., 2007; 31, Harper et al., 2007; 32, Kannan et al., 2006; 33, Yang et al., 2006; 34, Hung et al., 2007; 35, Endo et al., 2007b; 36, Stavros et al., 2008b; 37, Kakuschke et al., 2008b; 38, Kakuschke et al., 2005; 39, Griesel et al., 2006; 40, Lavery et al., 2008; 41, Capelli et al., 2008; 42, Griesel et al., 2008; 43, Stavros et al., 2008a; 44, Rosa et al., 2008; 45, Gray et al., 2008; 46, Endo et al., 2008; 47, Agusa et al., 2008; 48, Ando et al., 2005; 49, Carvalho et al., 2002; 50, Law et al., 2003.
Mammals 393 Acute and chronic adverse effects of chromium on warm-blooded organisms are caused mainly by Cr6+ compounds (Eisler, 2000d). There is little conclusive evidence of toxic effects caused by Cr2+ or Cr3+ compounds (Langard and Norseth, 1986). Lymphocyte proliferation of newborn harbor seals, P. vitulina, was unaffected during exposure to 5.0 mg Cr/L for 5 days (Kakuschke et al., 2008a). Chromium is causally associated with mutations and malignancy (Nieboer and Shaw, 1988; Shimada et al., 1998; USPHS, 1993b). Under appropriate conditions, chromium is a human and animal carcinogen; its biological effects depend on chemical form, solubility, and valence. In general, nearly all hexavalent chromium compounds are potent mammalian mutagens and all forms of hexavalent chromium—both water soluble and water insoluble compounds—are respiratory carcinogens in humans; metallic chromium and trivalent chromium are essentially nontoxic (Gale, 1978; Yassi and Nieboer, 1988). Data are missing on chromium toxicity, mutagenicity, teratogenicity, and carcinogenicity to marine mammals; however, under laboratory conditions, chromium is mutagenic, carcinogenic, and teratogenic to a wide variety of small laboratory mammals, and hexavalent chromium has the greatest biological activity (Eisler, 2000c).
6.12 Cobalt The highest cobalt concentration recorded of 14.2 mg/kg DW is in skin of the common dolphin, D. delphis (Table 6.3; Carvalho et al., 2002). In general, however, cobalt concentrations in tissues of marine mammals were usually less than 0.5 mg Co/kg DW (Table 6.3). For example, cobalt concentrations in all tissues of harbor seals, P. vitulina, from Newfoundland and Labrador waters were always less than 0.025 mg Co/kg FW (Table 6.3). In laboratory studies, lymphocyte proliferation in newborn harbor seals was unaffected during exposure to 10.0 mg Co/L for 5 days (Kakuschke et al., 2008a).
6.13 Copper It is probable that copper is not accumulated by marine mammals in excess of immediate metabolic needs. Copper concentrations from approximately 800 different species of representative plants and animals collected at numerous oceanic and coastal locations demonstrate that copper concentrations in marine mammals and other marine vertebrates are among the lowest recorded in all groups analyzed (Eisler, 1979, 2000i). The highest concentrations of copper recorded in marine mammals were in liver with a maximum concentration reported of 1200.0 mg Cu/kg DW in copper-contaminated manatees, Trichechus manatus from Florida, and 203.8 mg Cu/kg FW in bowhead whales, B. mysticetus (Table 6.3). The use of copper-containing herbicides in Florida to control aquatic plants may be hazardous to the endangered manatee, an aquatic herbivore.
394 Chapter 6 The maximum copper concentration recorded in manatees (1200.0 mg Cu/kg DW liver) from areas of high copper herbicide use are higher than any copper concentration measured in any species of free-ranging mammalian wildlife and are comparable to copper concentrations in livers of some domestic animals poisoned by copper (O’Shea et al., 1984). Copper concentrations in Antarctic region seal hairs recovered from sediment cores representing the past 1500 years ranged from 150.0 to 603.0 mg/kg DW, with no clear temporal trend (Yin et al., 2006). Copper concentrations in tissues of marine vertebrates, including mammals, tend to decrease with increasing age of the organism (Law et al., 1992; Watanabe et al., 1998). Regardless of species or tissue, except brain, concentrations decrease with increasing age; however, brain copper concentrations in marine mammals increase with increasing organism age (Eisler, 1984). Decreases in tissue copper content are also associated with spawning migrations of salmonids when entering freshwater from the sea, and with reproductive cycles of cod and other gadoids (Eisler, 1984). In polar bears, concentrations of copper in liver are 3–5 times higher than their seal diet (Braune et al., 1991). Copper concentrations in liver and kidney of polar bears are lower in juveniles than adults (Norheim et al., 1992), which is contrary to a reverse trend noted in most species of vertebrates. Neonatal marine mammals, for example, have higher concentrations of copper in liver than those found in the mother (Law et al., 1992). Associations of copper with cadmium, zinc, iron, manganese, silver, and other metals in tissues of marine vertebrates are documented. Intercorrelations of copper with cadmium and zinc in livers of polar bears (U. maritimus) are probably mediated by metallothioneins, which may contain all three metals (Braune et al., 1991). In mammals, copper absorption across the intestinal mucosa is inhibited by concomitant high oral intake of zinc (Aaseth and Norseth, 1986). In livers from Weddell seals (Leptonychotes weddelli), copper is positively correlated with zinc (Szefer et al., 1994). In muscle from Weddell seals, copper is positively correlated with iron (Szefer et al., 1994). In general, concentrations of copper in all tissues of all marine vertebrates are positively correlated with iron (Eisler, 1984). The main function of the mammalian red blood cell is to maintain aerobic metabolism while the iron atom of the heme molecule is in the ferrous (Fe2+) oxidation state; however, copper is necessary for this process to occur (USEPA, 1980b). Excess copper within the cell oxidizes the ferrous iron to the ferric (Fe3+) state. This molecule, known as methemoglobin, is unable to bind oxygen or carbon dioxide and is not dissociable (Langlois and Calabrese, 1992). Copper in livers and muscles of Weddell seals was positively correlated with manganese (Szefer et al., 1994). In general, manganese and copper are positively correlated in tissues of marine vertebrates (Eisler, 1984). Silver positively correlates with copper in livers of whales (Dehn et al., 2006b) and Weddell seals, but the correlation is negative in seal muscle (Szefer et al., 1994).
Mammals 395
6.14 Gold Gold had no effect on lymphocyte proliferation in newborn harbor seals, P. vitulina, during exposure for 5 days in 6.2 mg Au/L (Kakuschke et al., 2008a).
6.15 Indium Indium concentrations in livers of polar bears, U. maritimus, collected from various locations in Alaska between 1993 and 2002 averaged between 0.002 and 0.003 mg In/kg DW (Kannan et al., 2007). Livers from adult female southern sea otters found dead along the California coast between 1992 and 2002 had a maximum of 0.028 mg In/kg DW (Kannan et al., 2006).
6.16 Iron Maximum iron concentrations recorded in tissues of various species of marine mammals, in mg Fe/kg FW, were 15,382.0 in tusk of a dugong, 1137.0 in blood of a harbor seal, 600.0 in liver of a harbor seal, 467.0 in skin of a bottlenose dolphin, 466.0 in kidney of a California sea lion, 280.0 in lungs of cetaceans, 180.0 in placenta of a harbor seal, 150.0 in spleen of a harbor seal, 145.0 in muscle of a killer whale, and 26.0 in blubber of a common dolphin (Table 6.4). Maximum iron concentrations on a dry weight basis, in mg Fe/kg, were 12,356.0 in liver, 1450.0 in hair, 1438.0 in skin, 830.0 in muscle, 640.0 in kidney, 382.0 in teeth, and 90.0 in blubber (Table 6.4). In the California sea lion, Zalophus californianus, maximum iron concentrations—in mg Fe/kg DW—in kidney and liver were 446.0 and 4540.0, respectively (Table 6.4). Hepatic iron burdens in sea lions were consistently higher in adult females than in males (Harper et al., 2007). The highest iron concentration was recorded in pups of the California sea lion born prematurely and tends to corroborate the pattern of metal imbalance in liver associated with premature birth of pinnipeds. Without exception, liver samples of the harbor seal and the California sea lion contained 2.5–11.9 times more iron than kidney (Table 6.4); however, this was not the case in cetaceans. Iron concentrations in tissues of killer whales, O. orca, tended to increase with increasing age (Endo et al., 2007b). Stavros et al. (2007) noted that mean iron contents in skin of adult female bottlenose dolphins (T. truncatus) were significantly lower (30.0–33.0 mg Fe/kg DW) than were iron contents of juveniles and adult males (129.0–432.0 DW; Table 6.4). The biopsied skin samples did not result in animal mortality and may be useful for monitoring metals and other chemical burdens in endangered aquatic mammals (Stavros et al., 2007).
396 Chapter 6 Table 6.4: Iron Concentrations in Field Collections of Mammals Organism
Concentration
Reference
Cetaceans; Corsica Liver Muscle Lungs Kidneys Skin
80.0-380.0 FW 66.0-280.0 FW 73.0-280.0 FW 95.0-669.0 FW 18.0-67.0 FW
Cetaceans; 6 spp.; Ligurian Sea; found stranded; 1990-2004 Muscle Kidney Liver Brain
305.0-1144.0 DW 255.0-855.0 DW 797.0-12,356.0 DW 82.0-228.0 DW
Common dolphin, Delphinus sp.; found stranded; December 2004; New Zealand; max. concentrations Blubber Kidney Liver
26.0 FW 150.0 FW 250.0 FW
5 5 5
Dugong, Dugong dugon; Australia; tusk
6428.0 (3201.0-15,832.0) FW
8
Stellar sea lion, Eumetopias jubatus; teeth; North Pacific Ocean; 1968-1999
107.0 (18.0-382.0) DW
19
Weddell seal, Leptonychotes weddelli; fur; Antarctica Hair; January 2004 Serum vs. hair; summers, 2002-2003
1450.0 DW 3.3 DW vs. 73.9 DW
4 17
Killer whale, Orcinus orca; found stranded; Japan; February 2005; adults vs. calves Liver Kidney Muscle
247.0 FW vs. 123.0 FW 94.3 FW vs. 109.0 FW 145.0 FW vs. 56.3 FW
10 10 10
Harbor seal, Phoca vitulina Adults; found dead Blubber Liver Kidney Brain Spleen
27.0-75.0 FW 28.0-600.0 FW 31.0-66.0 FW 62.0-119.0 FW 120.0-150.0 FW
a
1 1 1 1 1
14 14 14 14
2 2 2 2 2 (Continues)
Mammals 397 Table 6.4: Organism Heart Placenta Fetuses; from dead adults Liver Brain Blood Captive animals Wild; North Sea Wadden Sea; 2004-2005; German site vs. Danish site Dall’s porpoise, Phocoenoides dalli; Japan; 6-year old male; February 2000; harpooned Liver Kidney Muscle Skin Bone Heart Lung Intestine Spleen Pancreas Diaphragm Blubber Cerebrum Stomach Portugal; 1998-2002 Common dolphin, Delphinus delphis Muscle Liver Skin Fat Bottlenose dolphin, Tursiops truncatus Muscle Liver Skin Fat
Cont’d
Concentration
Reference
106.0-149.0 FW 180.0 FW
2 2
510.0 FW 13.0 FW
2 2
411.0-887.0 FW 485.0-891.0 FW 760.0 (520.0-1137.0) FW vs. 738.0 (599.0-936.0) FW
425.0 FW 136.0 FW 123.0 FW 4.0 FW 44.6 FW 133.0 FW 359.0 FW 49.8 FW 279.0 FW 59.2 FW 167.0 FW 9.4 FW 28.2 FW 89.5 FW
a
12 13 15
9 9 9 9 9 9 9 9 9 9 9 9 9 9
450.0 (270.0-830.0) DW 595.0 (348.0-1190.0) DW 65.0 (30.0-156.0) DW 15.4 (8.0-24.0) DW
20 20 20 20
571.0 (460.0-675.0) DW 809.0 (482.0-1531.0) DW 40.0 (38.0-41.0) DW 14.2 (12.0-16.0) DW
20 20 20 20 (Continues)
398 Chapter 6 Table 6.4: Organism Striped dolphin, Stenella coeruleoalba; Japan; 1979 Liver Fetus Juvenile Adult Adult male vs. female fetus Blubber Kidney Liver Muscle Florida manatee, Trichechus manatus latirostris; Florida; 2007 Blood Skin Bottlenose dolphin, Tursiops truncatus Skin; 2003-2005; South Carolina Juvenile male Adult male Juvenile female Adult female Pregnant female Blood; summers 2003-2005; South Carolina vs. Florida California sea lion, Zalophus californianus Mothers with premature pups vs. mothers with normal pups Liver Kidney Premature pups vs. normal pups Liver Kidney Found stranded; southern California; 2003-2004 Liver Kidney
Cont’d
Concentration
Reference
580.0 DW 480.0 DW 770.0 DW
18 18 18
70.0 DW vs. 90.0 DW 640.0 DW vs. 370.0 DW 610.0 DW vs. 580.0 DW 830.0 DW vs. 230.0 DW
18 18 18 18
388.0 (323.0-451.0) FW 19.1 (10.1-35.1) FW
16 16
432.0 DW; max. 1438.0 DW 129.0 DW; max. 1298.0 DW 386.0 DW; max. 1080.0 DW 30.0 DW; max. 39.0 DW 33.0 DW; max. 52.0 DW 467.0 FW vs. 449.0 FW
6 6 6 6 6 11
1125.0 DW vs. 2000.0 DW 446.0 DW vs. 448.0 DW
3 3
4540.0 DW vs. 3340.0 DW 413.0 DW vs. 280.0 DW
3 3
44.4-127.0 (44.4-1440.0) FW 106.5-138.2 (48.8-466.0) FW
7 7
a
Values are in mg Fe/kg fresh eight (FW) or dry weight (DW). a 1, Viale, 1978; 2, Duinker et al., 1979; 3, Martin et al., 1976; 4, Santos et al., 2006; 5, Stockin et al., 2007; 6, Stavros et al., 2007; 7, Harper et al., 2007; 8, Edmonds et al., 1997; 9, Yang et al., 2006; 10, Endo et al., 2007b; 11, Stavros et al., 2008b; 12, Kakuschke et al., 2008b; 13, Griesel et al., 2006; 14, Capelli et al., 2008; 15, Griesel et al., 2008; 16, Stavros et al., 2008a; 17, Gray et al., 2008; 18, Agusa et al., 2008; 19, Ando et al., 2005; 20, Carvalho et al., 2002.
Mammals 399
6.17 Lead Lead modifies the function and structure of kidney, bone, the central nervous system, and the hematopoietic system, and produces adverse biochemical, histopathological, neuropsychological, fetotoxic, teratogenic, and reproductive effects (Boggess, 1977; De Michele, 1984; Eisler, 1988, 2000i; Hsu et al., 1998; Nriagu, 1978). The mechanism underlying lead-induced growth suppression is thought to involve disruption of pituitary growth hormone during puberty (Ronis et al., 1998). Inorganic lead absorbed into the mammalian body enters the bloodstream initially and attaches to the red blood cell. There is a further rapid distribution of the lead between blood extracellular fluid and other storage sites that is so rapid that only about half the freshly absorbed lead remains in the blood after a few minutes. The storage sites for lead are uncertain, although they are probably in soft tissues as well as bone; the half-time residence life (Tb ½) of inorganic lead is estimated at 20 days in blood, 28 days in whole body, and 600–3000 days in bone (Harrison and Laxen, 1981). Lead levels in bone exert an influence on plasma lead levels, and there is concern that previously accumulated lead stores in bone may constitute an internal source of exposure, particularly during periods of increased bone mineral loss associated with pregnancy or lactation (Hernandez-Avila et al., 1998). Inorganic lead in the environment can be biologically methylated to produce alkyllead compounds (Walsh and Tilson, 1984). Bile is an important excretory route: ingested lead probably proceeds sequentially from gut, to blood, to bone and soft tissue, and by way of the bile to small intestine and fecal excretion (De Michele, 1984). Concentrations of lead in tissues of various species of marine mammals were highest in bone, with a maximum value of 62.0 mg Pb/kg DW (Table 6.5). In general, lead accumulations were higher in older animals (Lavery et al., 2008). Biomagnification of lead through the food chain may be an important mechanism of accumulation in carnivorous marine mammals (Braham, 1973). Among California sea lions, Z. californianus, lead accumulated in significantly higher concentrations in hard tissues such as bone and teeth, than in soft tissues such as fat and muscle (Braham, 1973); a similar pattern was observed in harbor seals (Roberts et al., 1976). These results are comparable with lead burdens in humans, suggesting that exposure levels of lead may be similar for terrestrial and coastal environmental communities (Braham, 1973). Since lead has no known useful function in biological systems, levels in excess of trace amounts may suggest an abnormal accumulation. It is not known if lead accumulations are due to absorption across the gut epithelium or uptake from air (Braham, 1973). From the viewpoint of reproductive physiology, the movement of lead across the placenta of the harbor seal, P. vitulina, is negligible (Roberts et al., 1976). Lead concentrations found in Antarctic region seal hairs from sediment cores representing the past 1500 years show a sharp increase from 3.9 to 67.0 mg Pb/kg DW since the late 1800s
400 Chapter 6 Table 6.5: Lead Concentrations in Field Collections of Mammals Organism Australia; 16 spp.; most found stranded Blubber Bone Kidney Liver Muscle Australia; 1995-1996; stranded; liver vs. kidney Bottlenose dolphin, Tursiops truncatus aduncus Adult female Female calf Common dolphin, Delphinus delphis; juvenile Melon-headed whale, Peponocephala electra; adults Northern fur seal, Callorhinus ursinus Kidney Liver Hair; Japan Canadian Arctic; 1982-1984; max. values Beluga, Delphinapterus leucas Kidney Liver Muscle Skin Narwhal, Monodon monoceros Kidney Liver Muscle Skin Ringed seal, Phoca hispida Liver Muscle Cetaceans; 6 spp.; Ligurian Sea; found stranded; 1990-2004 Muscle Kidney
Concentration Usually <0.3 FW; (<0.05-3.4) FW 0.0-62.0 FW; usually <4.0 FW Max. 0.77 FW; max. 2.0 DW <0.01-1.0 FW <0.05-0.25 FW
Reference
8 8 8 8 8
0.17 FW vs. <0.03 FW 0.04 FW vs. 0.04 FW <0.04 FW vs. 0.05 FW
35 35 35
<0.04-0.1 FW vs. <0.04 FW
35
0.3-1.8 FW 0.2-0.8 FW 7.68 DW
1 1 14
0.038 FW 0.057 FW 0.44 FW 0.29 FW
9 9 9 9
0.08 FW 0.08 FW 0.04 FW 0.007 FW
9 9 9 9
0.79 FW 0.08 FW
9 9
0.05-0.22 DW 0.06-0.49 DW
a
28 28 (Continues)
Mammals 401 Table 6.5:
Cont’d
Organism
Concentration
Reference
Liver Brain
0.04-2.7 DW Max. 1.1 DW
28 28
Beluga whale, Delphinapterus leucas Muscle Liver Kidney
0.08 FW 0.36 FW 0.13 FW
2 2 2
Common dolphin, Delphinus sp.; December 2004; found stranded; New Zealand; max. concentrations Blubber Kidney Liver
0.03 FW 0.15 FW 0.74 FW
16 16 16
0.06 FW 1.0 FW
27 27
0.07 FW; max. 0.11 FW 0.8 (0.6-1.1) FW
27 27
0.46 (0.004-13.6) FW 2.8 (0.3-16.0) FW
27 27
Southern sea otter, Enhydra lutris nereis; adult females; found dead along California coast; 1992-2002; liver
0.22 (0.02-1.1) DW
23
Stellar sea lion, Eumetopias jubatus; teeth; North Pacific Ocean; 1968-1999
10.4 (2.1-39.5) DW
33
1.03 DW; max. 1.37 DW 0.66 DW; max. 1.79 DW
21 21
0.75 DW; max. 1.52 DW 0.37 DW; 0.62 DW
21 21
0.33 DW; max. 2.25 DW 0.41 DW; max. 1.44 DW
21 21
Dolphins; 3 spp.; South Australia; 1988-2004; found stranded or by-caught Common dolphin, Delphinus delphis Liver Bone Bottlenose dolphin, Tursiops truncatus Liver Bone Dolphin, Tursiops aduncus Liver Bone
Europe; 2001-2002; found stranded Common dolphin, Delphinus delphis Teeth Bone Harbor porpoise, Phocoena phocoena Teeth Bone Striped dolphin, Stenella coeruleoalba Teeth Bone
a
(Continues)
402 Chapter 6 Table 6.5:
Cont’d
Organism
Concentration
Reference
Greenland Sea; March-April 1999; reproductively active females during suckling period Harp seal, Pagophilus groenlandicus Muscle Liver Kidney Hooded seal, Cystophora cristata Muscle Liver Kidney
0.13 FW 0.05 FW 0.09 FW
17 17 17
0.06 FW 0.07 FW 0.04 FW
17 17 17
Gray seal, Halichoerus grypus; liver
0.31 FW
2
Leopard seal, Hydrurga leptonyx; serum
0.01 FW
31
Northern bottlenose whale, Hyperoodon ampullatus Muscle Liver
0.03 FW 0.18 FW
2 2
White-beaked dolphin, Lagenorhynchus albirostris Fascical fat Blubber Liver Muscle Testicles Pancreas Kidney Lungs Spleen
<1.5 FW 5.4 FW 4.5 FW 2.2 FW 1.8-3.0 FW 1.1 FW 2.0 FW 1.7 FW 1.4 FW
3 3 3 3 3 3 3 3 3
Weddell seal, Leptonychotes weddelli; Antarctica; summers 2002-2003 Serum Hair
<0.001 DW 1.3 DW
31 31
Southern elephant seal, Mirounga leonina; molted fur; Shetland Islands; juveniles vs. adult females
<0.05 DW vs. <0.05 DW
13
Mediterranean monk seal, Monachus monachus; Greece; hair
0.78 DW
15
a
(Continues)
Mammals 403 Table 6.5:
Cont’d
Organism
Concentration
Ringed seal, Phoca hispida Liver All tissues; Greenland; 1978-1993
0.24 FW Not detectable-0.06 FW
Harbor seal, Phoca vitulina Dead on collection; adults Blubber Liver Kidney Brain Spleen Heart Placenta Dead on collection; fetuses Liver Brain Claw Rib Muscle Liver Kidney Blood Captive animals Wild; North Sea Wadden Sea; 2004-2005; German site vs. Danish site Harbor porpoise, Phocoena phocoena Blubber Liver Muscle Liver Kidney Dall’s porpoise, Phocoenoides dalli; Japan; 2006; harpooned male Bone Liver, kidney, pancreas, blubber Muscle, skin, heart, lung, intestine, spleen, diaphragm, stomach, cerebrum Portugal; 1998-2002 Common dolphin, Delphinus delphis Muscle
Reference
2 10
<0.05-1.0 FW <0.05-2.3 FW 0.16-0.23 FW <0.05-2.0 FW 0.16-0.40 FW 0.29-0.61 FW <0.05 FW
4 4 4 4 4 4 4
<0.05 FW <0.05 FW 4.0 FW 3.5 FW 0.03-0.10 FW 0.09-0.74 FW 0.08-0.60 FW
4 4 5 5 2 2 2
Not detectable-0.010 FW Not detectable-0.002 FW 0.00098 FW; max. 0.0018 FW vs. max. 0.0045 FW 6.0 (<1.5-12.0) FW 3.5 (1.9-5.3) FW 0.03-0.07 FW 0.17-0.35 FW 0.15-0.17 FW
a
25 26 29
3 3 2 2 2
0.28 FW 0.01-0.03 FW 0.001-0.007 FW
24 24 24
<2.6 DW
34 (Continues)
404 Chapter 6 Table 6.5: Organism Liver Skin Fat Bottlenose dolphin, Tursiops truncatus Muscle Liver Skin Fat Seals; gray seal, harbor seal; liver Striped dolphin, Stenella coeruleoalba; Japan; 1979 Liver Fetus Juvenile Adult Adult male vs. female fetus Blubber Kidney Liver Muscle Florida manatee, Trichechus manatus latirostris; January 2007; Florida Blood Skin Bottlenose dolphin, Tursiops truncatus Liver; South Carolina; found stranded Skin; South Carolina; 2003-2005 Juvenile male Adult male Juvenile female Adult female Pregnant female Captive animal; died after ingesting lead-containing air gun pellets vs. control Kidney cortex Liver
Cont’d
Concentration
Reference
<1.2 DW 5.3 (3.5-9.5) DW <1.1 DW
34 34 34
<2.5 DW <1.0 DW 5.2 (2.6-7.7) DW <1.2 DW
34 34 34 34
8.0 FW
a
6
<0.001 DW 0.04 DW 0.10 DW
32 32 32
0.005 DW vs. 0.002 DW 0.04 DW vs. 0.001 DW 0.07 DW vs. <0.001 DW 0.02 DW vs. 0.004 DW
32 32 32 32
0.013 (0.010-0.019) FW 0.036 (0.006-0.178) FW
30 30
<0.1 FW
11
0.4 DW 0.3 DW 0.48 DW 0.47 DW 0.08 DW
18 18 18 18 18
4.2 FW vs. <0.15 FW 3.6 FW vs. <0.7 FW
12 12 (Continues)
Mammals 405 Table 6.5: Organism Sarasota Bay, Florida; 2002-2004 Blood Skin Polar bear, Ursus maritimus; liver; 1993-2002 Beaufort Sea region Chukchi Sea region California sea lion, Zalophus californianus Humerus Femur Tooth Rib Cerebral hemisphere Small intestine Gonad Cerebellum Kidney cortex Aorta Lung Kidney medulla Hair-skin Large intestine Liver Spleen Muscle Stomach Fat Found stranded; southern California; 2003-2004 Liver Kidney
Cont’d
Concentration
Reference
0.003 FW; max. 0.007 FW 0.017 FW; max. 0.087 FW
19 19
0.29 (0.06-1.1) DW 0.78 (0.06-5.2) DW
20 20
34.2 DW 20.6 DW 12.9 DW 8.7 DW 3.8 DW 3.4 DW 3.0 DW 2.7 DW 2.4 DW 2.2 DW 2.0 DW 2.0 DW 1.6 DW 1.5 DW 1.3 DW 1.3 DW 1.1 DW 0.5 DW 0.3 DW
0.6-7.5 (0.5-179.0) FW 0.6-0.8 (0.5-5.0) FW
a
7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7
22 22
Values are in mg Pb/kg fresh weight (FW) or dry weight (DW). a 1, Anas, 1974; 2, Harms et al., 1978; 3, Andersen and Rebsdorff, 1976; 4, Duinker et al., 1979; 5, Roberts et al., 1976; 6, Holden, 1975; 7, Braham, 1973; 8, Kemper et al., 1994; 9, Wagemann et al., 1996; 10, Dietz et al., 1996; 11, Beck et al., 1997; 12, Schlosberg et al., 1997; 13, Andrade et al., 2007; 14, Ikemoto et al., 2004a,b; 15, Yediler et al., 1993; 16, Stockin et al., 2007; 17, Brunborg et al., 2006; 18, Stavros et al., 2007; 19, Bryan et al., 2007; 20, Kannan et al., 2007; 21, Caurant et al., 2006; 22, Harper et al., 2007; 23, Kannan et al., 2006; 24, Yang et al., 2006; 25, Kakuschke et al., 2008b; 26, Kakuschke et al., 2005; 27, Lavery et al., 2008; 28, Capelli et al., 2008; 29, Griesel et al., 2008; 30, Stavros et al., 2008a; 31, Gray et al., 2008; 32, Agusa et al., 2008; 33, Ando et al., 2005; 34, Carvalho et al., 2002; 35, Law et al., 2003.
406 Chapter 6 to the 1980s, probably due to human activities (Yin et al., 2006). After the 1980s, lead content of seal hairs dropped to 45.0 mg/kg DW, apparently due to reduced usage of leaded gasoline in the southern hemisphere (Yin et al., 2006). Treatment of lead-poisoned animals usually involves the removal of ingested lead objects and treatment with antibiotics. For example, a captive bottlenose dolphin (T. truncatus) that had 40 lead-containing air pellets in its second stomach, as determined by radiography, was treated with 250 mg penicillamine/kg body weight given orally 3 times daily for 5 days after the pellets had been removed from the stomach using an endoscope (Schlosberg et al., 1997). Radiolead-210, as was true for stable lead, concentrates in bony tissues. Radiolead-210 concentrations in bone, when compared to soft tissues, was 20 times higher in the spotted seal, Phoca largha, taken in Alaska in 1963 (Holtzman, 1969). For sperm whales, Physeter macrocephalus, taken in Alaska in 1965, 210Pb levels were 391 times higher in bone than in soft tissues (Holtzman, 1969). Large variations in the ratio of 206Pb/207Pb in bone tissues of stranded cetaceans suggest atmospheric changes; specifically, the negative correlation between 206Pb/207Pb ratios and cetacean age reflect the increasing use of unleaded gasoline in Europe (Caurant et al., 2006).
6.18 Lithium A tusk from a 55-year-old pregnant dugong, D. dugon, contained 1.1 (0.8–1.5) mg Li/kg FW (Edmonds et al., 1997). Mean lithium concentrations in skin of bottlenose dolphins, T. truncatus, taken near Charleston, South Carolina between 2003 and 2005 ranged from 0.08 mg Li/kg DW in female adults to 1.4 mg Li/kg DW (max. 3.7 mg Li/kg DW) in juvenile males (Stavros et al., 2007). Blood and skin of Florida manatees, T. manatus latirostris, taken in the Crystal River, Florida during January 2007 contained 0.007 mg Li/kg FW in blood (max. 0.008 mg Li/kg FW) and 0.007 (0.002–0.019) mg Li/kg FW in skin (Stavros et al., 2008a).
6.19 Manganese Manganese concentrations, in mg Mn/kg DW, tend to be higher in liver tissues of marine mammals and were highest in southern sea otter (47.4), California sea lion (19.2), common dolphin (16.7), polar bear (15.1), and bottlenose dolphin (13.0; Table 6.6). Manganese burdens in livers of normal and premature California sea lion pups seem to reflect maternal liver concentrations (Table 6.6). The relation between low manganese levels in livers of sea lions delivering prematurely and premature birth is unknown. Manganese concentrations in skin of bottlenose dolphins, T. truncatus, were higher in summer relative to winter (Bryan et al., 2007). Blood manganese concentrations in bottlenose dolphins were higher in juveniles than adults (Stavros et al., 2008b).
Mammals 407 Table 6.6: Manganese Concentrations in Field Collections of Mammals Organism
Concentration
Reference
Cetaceans; 6 spp.; Ligurian Sea; found stranded; 1990-2004 Muscle Kidney Liver Brain
0.3-1.1 DW 1.7-3.2 DW 6.1-17.0 DW 1.3-2.4 DW
16 16 16 16
Common dolphin, Delphinus sp.; December 2004; found stranded; New Zealand; max. values Blubber Kidney Liver
0.09 FW 0.78 FW 4.8 FW
4 4 4
Southern sea otter, Enhydra lutris nereis; adult females; found dead along central California coast; 1992-2002; liver Non-diseased Emaciated Infectious-diseased
12.9 (2.4-29.5) DW 19.4 (8.3-45.9) DW 18.0 (6.1-47.4) DW
9 9 9
7.0 (2.2-17.2) DW
21
Hong Kong; stranded; stomach contents Humpback dolphin, Sousa chinensis Finless porpoise, Neophocaena phocaenoides
4.0 (0.54-17.3) FW 4.0 (0.51-12.2) FW
11 11
Leopard seal, Hydrurga leptonyx; serum
0.004 FW
19
Weddell seal, Leptonychotes weddelli; Antarctica; 2002-2003; serum vs. hair
<0.001 DW vs. 0.04 DW
19
Killer whale, Orcinus orca; found stranded; Japan; February 2005; adults vs. calves Liver Kidney Muscle
2.3 FW vs. 2.6 FW 0.69 FW vs. 0.66 FW 0.12 FW vs. 0.25 FW
12 12 12
Harbor seal, Phoca vitulina Adults; dead on collection Blubber Liver Kidney Brain Spleen
<0.04-2.7 FW 2.6 FW 1.9-3.4 FW <0.04-8.0 FW 2.7-4.4 FW
Stellar sea lion, Eumetopias jubatus; teeth; North Pacific Ocean; 1968-1999
a
1 1 1 1 1 (Continues)
408 Chapter 6 Table 6.6: Organism Heart Placenta Fetuses Liver Brain From Labrador and Newfoundland; body length 212-402 cm Muscle Liver Kidney Blood Captive animals Wild; North Sea Wadden Sea; 2004-2005; German site vs. Danish site Dall’s porpoise, Phocoenoides dalli; Japan; February 2006; harpooned 6-year old male Liver Kidney Muscle Skin Bone Heart Lung Intestine Spleen Pancreas Diaphragm Blubber Cerebrum Stomach Portugal; 1998-2002 Common dolphin, Delphinus delphis Muscle Liver Skin Fat Bottlenose dolphin, Tursiops truncatus Muscle Liver
Cont’d
Concentration
Reference
2.6-4.4 FW 0.3 FW
1 1
0.7 FW 0.3 FW
1 1
0.13-0.18 FW 3.0-4.6 FW 0.86-0.96 FW
3 3 3
0.023-0.099 FW 0.06-0.15 FW 0.09 (0.07-0.15) FW vs. 0.08 (0.07-0.10) FW
14 15 17
5.1 FW 0.7 FW 0.3 FW 0.04 FW 1.6 FW 0.5 FW 0.1 FW 0.8 FW 0.3 FW 0.8 FW 0.2 FW 0.06 FW 0.35 FW 0.6 FW
10 10 10 10 10 10 10 10 10 10 10 10 10 10
4.4 (3.0-11.0) DW 12.4 (4.9-16.7) DW 3.5 (3.1-4.6) DW 3.4 (3.1-4.7) DW
22 22 22 22
<4.0 DW 12.0 (11.0-13.0) DW
22 22
a
(Continues)
Mammals 409 Table 6.6: Organism Skin Fat Striped dolphin, Stenella coeruleoalba; Japan; 1979 Liver Fetus Juvenile Adult Adult male vs. female fetus Blubber Kidney Liver Muscle Florida manatee, Trichechus manatus latirostris; January 2007; Crystal River, Florida Blood Skin Bottlenose dolphin, Tursiops truncatus Blood; summers 2003-2005; South Carolina vs. Florida Skin; South Carolina; 2003-2005 Juvenile male Adult male Juvenile female Adult female Pregnant female Skin; Sarasota Bay, Florida; 2002-2004 Polar bear, Ursus maritimus; liver; 1993-2003 Beaufort Sea area Chukchi Sea area California sea lion, Zalophus californianus Mothers with premature pups vs. mothers with normal pups Liver Kidney Premature pups vs. normal pups Liver Kidney
Cont’d
Concentration
Reference
3.5 (3.4-3.6) DW 3.1 (2.8-4.9) DW
22 22
2.8 DW 10.7 DW 8.1 DW
20 20 20
0.17 DW vs. 0.27 DW 3.0 DW vs. 1.3 DW 10.5 DW vs. 2.8 DW 1.0 DW vs. 0.5 DW
20 20 20 20
0.02 (0.01-0.03) FW 0.12 (0.06-0.23) FW
18 18
0.014 FW vs. 0.011 FW
13
0.8 DW; max. 1.2 DW 0.5 DW; max. 1.4 DW 0.8 DW; max. 1.9 DW 0.7 DW; max. 1.6 DW 0.3 DW; max. 0.4 DW 0.054 FW; max. 0.123 FW
5 5 5 5 5 6
12.6 (8.5-15.1) DW 12.0 (6.9-15.1) DW
7 7
15.7 DW vs. 19.2 DW 4.5 DW vs. 4.7 DW
2 2
9.2 DW vs. 12.2 DW 2.7 DW vs. 2.9 DW
2 2
a
(Continues)
410 Chapter 6 Table 6.6: Organism Found stranded; southern California; 2003-2004 Liver Kidney
Cont’d
Concentration
4.2-4.7 (0.5-9.2) FW 0.7-9.0 (0.0-89.0) FW
Reference
a
8 8
Values are in mg Mn/kg fresh weight (FW) or dry weight (DW). a 1, Duinker et al., 1979; 2, Martin et al., 1976; 3, Veinott and Sjare, 2006; 4, Stockin et al., 2007; 5, Stavros et al., 2007; 6, Bryan et al., 2007; 7, Kannan et al., 2007; 8, Harper et al., 2007; 9, Kannan et al., 2006; 10, Yang et al., 2006; 11, Hung et al., 2007; 12, Endo et al., 2007b; 13, Stavros et al., 2008b; 14, Kakuschke et al., 2008b; 15, Kakuschke et al., 2005; 16, Capelli et al., 2008; 17, Griesel et al., 2008; 18, Stavros et al., 2008a; 19, Gray et al., 2008; 20, Agusa et al., 2008; 21, Ando et al., 2005; 22, Carvalho et al., 2002.
6.20 Mercury Mercury concentrations were comparatively elevated in liver tissues of marine mammals. Maximum mercury concentrations recorded, in mg total Hg/kg FW liver, were: 2110.7 in dolphin, Tursiops aduncus, from South Australia; 1033.0–1544.0 in striped dolphin, S. coeruleoalba, from several locations in the Mediterranean Sea; 710.0 in harbor seal, P. vitulina from California; and 442.0 in California sea lion, Z. californianus from California (Table 6.7). Striped dolphins, S. coeruleoalba, found beached in the South Adriatic Sea between 1991 and 1995 contained up to 966.3 mg total mercury/kg FW liver and 53.3 mg/kg FW muscle (Storelli et al., 1998; Table 6.7). Total mercury in liver increased with increasing length of the striped dolphin but percent methylmercury decreased with increasing length. Of total mercury, the percent methylmercury was significantly higher in muscle tissue (88%) than in liver (24%) (Storelli et al., 1998). This is discussed later. In general, mercury concentrations are highest in livers of marine mammals, intermediate in muscle, and lowest in blubber (Table 6.7). In Greenland, for example, low mercury (<0.5 mg/kg FW) concentrations are reported for molluscs, crustaceans, and fishes; grossly elevated (>20.0 mg Hg/kg FW) concentrations in kidney and liver of polar bears and in liver of some species of seals; and intermediate values in tissues of seabirds and various marine mammals (Table 6.7; Dietz et al., 1990, 1996). With minor exceptions mercury content in muscle, blubber, and liver of adult and new-born marine mammals exceed mercury safety guidelines (<0.3–1.0 mg total Hg/kg FW) established by regulatory agencies for human diets (Eisler, 2006). One exception is killer whales, O. orca, found stranded along the coast of Japan in February 2005 in which there was minimal transfer of elevated mercury levels in liver, kidney, and muscle from adult females to their calves (Endo et al., 2007b; Table 6.7). Mercury in pinniped muscle, unlike liver, was mostly methylmercury in both mothers and pups; pups acquired most of their mercury during gestation (Wagemann et al., 1988, 1998). Methylmercury increased in liver of all marine mammals from the Arctic Ocean with
Mammals 411 Table 6.7: Mercury Concentrations in Field Collections of Mammals Organism Alaska; Barrow; 1998-2001 Bowhead whale, Balaena mysticetus Kidney Liver Beluga whale, Delphinapterus leucas Kidney Liver Bearded seal, Erignathus barbatus Kidney Liver Gray whale, Eschrichtius robustus Kidney Liver Ribbon seal, Phoca fasciata Kidney Liver Ringed seal, Phoca hispida; Holman, Canada Kidney Liver Ringed seal; Barrow, Alaska Kidney Liver Spotted seal, Phoca largha Kidney Liver Polar bear, Ursus maritimus Kidney Liver Antarctica; February-March 1989; maximum values Leopard seal, Hydrurga leptonyx Kidney Liver Muscle Stomach contents Weddell seal, Leptonychotes weddelli Kidney Liver Muscle Crabeater seal, Lobodon carcinophagus Kidney
Concentration
Reference
0.03 (<0.01-0.18) FW 0.05 (0.01-0.6) FW
66 66
4.4 (0.1-12.3) FW 15.9 (0.3-72.5) FW
66 66
0.6 (0.21-1.5) FW 3.8 (0.6-20.4) FW
66 66
0.01 (<0.01-0.03) FW 0.02 (<0.01-0.07) FW
66 66
0.5 (0.13-1.6) FW 1.2 (0.18-8.5) FW
66 66
1.9 (0.8-3.7) FW 22.6 (1.5-72.0) FW
66 66
0.45 (0.05-1.1) FW 2.5 (0.06-16.6) FW
66 66
0.3 (0.08-0.90) FW 0.68 (0.1-2.6) FW
66 66
16.6 (1.6-45.9) FW 14.0 (1.5-54.3) FW
66 66
6.1 DW 18.1 DW 3.2 DW 1.2 DW
25 25 25 25
15.9 DW 48.8 DW 3.6 DW
25 25 25
12.5 DW
25
a
(Continues)
412 Chapter 6 Table 6.7: Organism Liver Muscle Arctic Ocean; western region; total mercury vs. methylmercury Beluga, Delphinapterus leucas; 1993-1994 Muscle Liver Skin Blubber Ringed seal, Phoca hispida; 1987-1994 Muscle Liver Arctic Ocean; eastern region; total mercury vs. methylmercury Beluga, Delphinapterus leucas; 1993-1994 Muscle Liver Skin Blubber Narwhal, Monodon monoceros; 1992-1994 Muscle Liver Skin Blubber
Cont’d
Concentration
Reference
16.3 DW 6.2 DW
25 25
1.3 (0.4-3.4) FW vs. 1.3 (0.35-3.2) FW 27.0 (0.3-116.6) FW vs. 1.9 (0.1-6.1) FW 0.8 (0.2-1.9) FW vs. 0.7 (0.1-1.7) FW 0.10 (0.02-0.19) FW vs. no data
80
0.4 (0.1-1.6) FW vs. 0.4 (0.1-1.5) FW 28.6 (0.5-137.2) FW vs. 1.0 (0.2-4.1) FW
80
1.0 (0.4-2.8) FW vs. 1.0 (0.4-2.4) FW 10.2 (1.2-38.6) FW vs. 1.4 (0.4-3.1) FW 0.6 (0.3-1.4) FW vs. 0.5 (0.3-1.1) FW 0.07 (0.01-0.19) FW vs. no data
80
1.0 (0.4-1.9) FW vs. 1.0 (0.4- 1.7) FW 10.8 (0.3-37.2) FW vs. 1.0 (0.2-2.4) FW 0.6 (0.2-1.3) FW vs. 0.5 (0.1-1.2) FW 0.04 (0.003-0.13) FW vs. no data
80
a
80 80 80
80
80 80 80
80 80 80 (Continues)
Mammals 413 Table 6.7: Organism Ringed seal, Phoca hispida; 19921994 Muscle Liver Australian fur seal, Arctocephalus pusilus Muscle Liver Kidney Spleen Brain Fur
Cont’d
Concentration
Reference
0.46 0.43 19.0 0.61
80
(0.05-1.9) FW vs. (0.05-1.8) FW (0.09-149.5) FW vs. (0.04-4.0) FW
a
80
0.9 (0.1-1.9) FW 62.0 (1.0-170.0) FW 0.6 (0.1-1.7) FW 1.3 (0.0-3.8) FW 0.7 (0.0-2.5) FW 9.6 (1.1-19.8) FW
27 27 27 27 27 27
32.0 FW vs. 2.0 FW 0.7 FW vs. 0.3 FW 0.9 FW vs. 0.1 FW
99 99 99
13.0-141.0 FW vs. 2.6-5.1 FW
99
Bowhead whale, Balaena mysticetus; Barrow, Alaska; 1983-2001 Liver Kidney Muscle Epidermis
0.05 0.03 0.02 0.01
49-51, 44 49-51, 44 49-51 49-51
Antarctic minke whale, Balaenoptera bonaerensis; 1980-1999; ages 1-26 years Liver Diet (Antarctic krill)
0.024-0.093 FW; max. 0.31 FW 0.058 (0.002-0.013) FW
60 60
0.06 FW
10
3.3 FW vs. 0.4 FW 5.4 FW vs. 1.4 FW 1.2 FW vs. 0.9 FW
28 28 28
Australia; 1995-1996; stranded; liver vs. kidney Bottlenose dolphin, Tursiops truncatus aduncus Adult female Female calf Common dolphin, Delphinus delphis; juvenile Melon-headed whale, Peponocephala electra; adults
Fin whale, Balaenoptera physalis Muscle Spain and Iceland; 1983-1986; total vs. organic mercury; maximum values Kidney Liver Muscle
(0.001-0.59) FW (0.001-0.18) FW (0.00-0.05) FW (0.00-0.04) FW
(Continues)
414 Chapter 6 Table 6.7: Organism Northern fur seal, Callorhinus ursinus Pups; liver vs. muscle Adult males vs. adult females Liver Muscle Kidney Fetus; liver vs. kidney Nursing cows Hair Blood Milk Newborn pups vs. pups age 2 months; hair Sanriku, Japan; 1997-1998; whole liver vs. liver nuclei, lysosomes, and mitochondria Blood Liver Kidney Cetacean muscle sold for human consumption in Korea; 2003-2005; usually as boiled red meat called “gorae”; total mercury Minke whale, Balaenoptera acuturostrara scammoni Common dolphin, Delphinus delphis Risso’s dolphin, Grampus griseus Pacific white-side dolphin, Lagenorhynchus obliquidens Blainville’s beaked whale, Mesoplodon densirostris Stejneger’s beaked whale, Mesoplodon stejnegeri Finless porpoise, Neophocoena phocaenoides Killer whale, Orcinus orca False killer whale, Pseudorca crassidens Harbour porpoise, Phocoena phocaena Bottlenose dolphin, Tursiops truncatus Cuvier’s beaked whale, Ziphius cavirostris
Cont’d
Concentration
Reference
0.1-0.3 FW vs. 0.1 FW
1
3.0-19.0 FW vs. 7.1-172.0 FW 0.1-0.4 FW vs. 0.2-0.4 FW 0.7 FW vs. 0.6-1.6 FW 0.4 FW vs. 0.2 FW
1 1 1 1
4.9 FW 0.1 FW 0.014 FW 3.7 FW vs. 5.4 FW
2 2 2 2
59.0 (7.6-121.0) FW vs. 39.0 (3.9-83.0) FW
29
0.02 FW vs. 0.07 FW 351.0 DW 6.2 DW
2 97 97
0.22 (0.03-0.43) FW
55
0.91 (0.44-1.89) FW 1.85 FW 1.2 (1.04-1.61) FW
55 55 55
2.66 FW
55
3.57 FW
55
0.68 (0.11-1.81) FW
55
13.3 FW 9.6 (1.39-41.0) FW 0.48 (0.42-0.54) FW 10.6 (1.6-25.0) FW 0.43 FW
55 55 55 55 55
a
(Continues)
Mammals 415 Table 6.7:
Cont’d a
Organism
Concentration
Reference
Cetacean muscle sold for human consumption; Japan False killer whale Bottlenose dolphin Killer whale Risso’s dolphin Harbour porpoise
39.5 (17.4-81.0) FW 17.8 (0.59-98.9) FW 1.27 (1.06-1.46) FW 4.4 (1.7-9.2) FW 0.22 FW
56 56 57 56 58
0.6-166.0 DW vs. 0.6-74.4 DW 0.8-288.0 DW vs. 0.1-64.3 DW 0.1-3737.0 DW vs. 0.1-76.8 DW 1.0-75.2 DW vs. 0.6-12.1 DW
90 90 90
0.08 FW 1.21 FW 37.2 FW 5.1 FW 51.1-100.9 FW
3 3 3 3 85
1.6 FW vs. 4.4 FW 0.97 FW vs. 8.9 FW
4 10
2.7 FW 20.3 FW 2.6 FW
30 30 30
15.9 (0.3-72.5) FW vs. 1.43 (0.19-3.9) FW 4.4 (0.1-12.3) FW vs. 0.5 (0.13-2.4) FW 1.1 (0.13-3.3) FW vs. 1.0 (0.13-2.4) FW 0.63 (0.03-1.52) FW vs. 0.63 (0.06-1.48) FW
49, 51, 52
Cetaceans; 6 spp.; Ligurian Sea; found stranded; 1990-2004; total mercury vs. organic mercury Muscle Kidney Liver Brain Hooded seal, Cystophora cristata Blubber Muscle Liver Hair Liver; Greenland; March 1984 Beluga whale, Delphinapterus leucas Muscle vs. liver Muscle vs. liver Quebec, Canada; 1989-1990 Brain Liver Muscle Point Lay/Wainwright, Alaska; 1992-1999; total mercury vs. methylmercury Liver Kidney Muscle Epidermis
90
49, 51, 52 49, 51, 52 49, 51, 52 (Continues)
416 Chapter 6 Table 6.7:
Cont’d
Organism
Concentration
Reference
Common dolphin, Delphinus sp.; December 2004; New Zealand; found stranded Blubber Kidney Liver
Max. 1.7 FW Max. 8.1 FW Max. 110.0 FW
63 63 63
31.2 (0.15-165.3) FW 213.9 (2.5-771.9) FW
89 89
475.8 (0.3-2110.7) FW
89
0.3 (0.05-1.11) DW vs. 0.09 (0.04-0.28) DW 0.24 DW <0.1-0.22 DW
31
19.3 (0.48-128.0) DW 18.4 (1.4-62.0) DW 15.6 (2.3-72.0) DW
81 81 81
Dolphins; 3 spp.; South Australia; 1988-2004; found stranded or bycaught; liver Common dolphin, Delphinus delphis Bottlenose dolphin, Tursiops truncatus Dolphin, Tursiops aduncus Dugong, Dugong dugon; Queensland, Australia; 1996-2000; liver Mature vs. immature Northern Australia Torres Straits Southern sea otter, Enhydra lutris nereis; found dead along California coast; 1992-2002; adult females; liver Non-diseased Emaciated Infectious-diseased Bearded seal, Erignathus barbatus Claw Liver Muscle Barrow Strait; liver; adult vs. adolescent W. Victoria Island Liver; total mercury vs. methylmercury Muscle Belcher Island Liver; total mercury vs. methylmercury Muscle
a
32, 33 34, 35
0.5-1.9 FW 143.0 FW 0.53 FW 79.2 FW vs. 9.4 FW
5 6 6 7
143.0 FW vs. 0.3 FW
7
0.5 FW
7
26.2 FW vs. 0.12 FW
7
0.09 FW
7 (Continues)
Mammals 417 Table 6.7:
Cont’d
Organism
Concentration
Reference
Gray whale, Eschrichtius robustus; Lorino/Lavrentiya, Russia; 2001 Liver Kidney Muscle Epidermis
0.02 0.01 0.02 0.01
49 49 49 49
Sea lion, Eumetopias jubatus; edible portions; Aleutian Islands, Alaska; 2004-2005 Muscle Liver
1.0 FW 69.5 FW
Pilot whale, Globicephala macrorhynchus Muscle Liver Kidney Blubber Liver Kidney
2.8-5.4 FW 19.2-1570.0 FW 6.0-14.0 FW 0.22-2.37 FW 57.0-454.0 FW 4.8-55.7 FW
Risso’s dolphin, Grampus griseus Liver Kidney
230.0 DW 28.0 DW
97 97
0.09-3.5 FW 0.3-19.9 FW 0.06-3.6 FW
36 36 36
0.18-1.4 FW 0.8-8.2 FW 0.15-0.66 FW
36 36 36
10.8-23.2 FW 7.2-21.6 FW 0.06-0.08 FW
36 36 36
6.4 FW vs. 0.98 FW 174.5 FW vs. 2.1 FW 1.4 FW vs. 1.2 FW
37 37 37
Greenland; 1983-1991 Seals; 4 spp. Kidney Liver Muscle Toothed whales; 3 spp. Kidney Liver Muscle Polar bear, Ursus maritimus Kidney Liver Muscle Greenland; 1984-1987; total mercury vs. methylmercury; maximum concentrations Seals Kidney Liver Muscle
(0.004-0.07) FW (0.001-0.03) FW (0.01-0.04) FW (0.001-0.03) FW
a
67 67 8 8 8 9 9 9
(Continues)
418 Chapter 6
Table 6.7: Organism Toothed whales Kidney Liver Muscle Baleen whales Kidney Liver Muscle Polar bear Kidney Liver Muscle Greenland Sea; caught in drift ice between Iceland and East Greenland; March-April 1999; reproductively active females during suckling period Harp seal, Pagophilus groenlandicus; age 12 (6-22) years; 111 (88-132) kg Muscle Liver Kidney Hooded seal, Cystophora cristata; age 9 (4-33 years); 141 kg, max. 215 kg Muscle Liver Kidney Gray seal, Halichoerus grypus Faroe Islands; summers 1993-1995 Males; mature vs. immature Liver Kidney Muscle Females; mature vs. immature Liver Kidney Muscle
Cont’d
Concentration
Reference
2.9 FW vs. 0.4 FW 16.4 FW vs. 1.6 FW 1.3 FW vs. 1.2 FW
37 37 37
1.1 FW vs. 0.11 FW 1.5 FW vs. 0.4 FW 0.4 FW vs. 0.24 FW
37 37 37
48.6 FW vs. 0.2 FW 23.8 FW vs. 0.6 FW 0.1 FW vs. 0.07 FW
37 37 37
0.14 FW; max. 0.31 FW 0.86 FW; max. 3.3 FW 0.36 FW; max. 0.68 FW
64 64 64
0.16 (0.08-0.31) FW 29.0 (3.5-127.0) FW 2.1 (1.0-4.4) FW
64 64 64
123.0 (46.0-199.0) FW vs. 10.0 (2.0-65.0) FW 8.0 (3.0-16.0) FW vs. 2.0 (0.4-5.0) FW 2.0 (0.6-4.6) FW vs. 0.5 (0.2-1.2) FW
38
133.0 (34.0-238.0) FW vs. 14.0 (1.0-90.0) FW 4.0 (1.0-7.0) FW vs. 1.0 (0.6-4.0) FW 1.0 (0.3-2.6) FW vs. 0.4 (0.2-1.0) FW
38
a
38 38
38 38 (Continues)
Mammals 419 Table 6.7: Organism Muscle Liver Liver Liver Kidney Spleen Blubber Skin and hair Pups Blubber Muscle Liver Fur Claw Liver Kidney Muscle Heart Gonad Blubber Brain Adults Blubber Muscle Liver Adult males vs. adult females Fur Claw Liver Kidney Flipper Muscle Heart Gonad Blubber Brain Maternal females; inorganic mercury vs. methylmercury Liver Bile Pups; liver; inorganic mercury vs. methylmercury
Cont’d
Concentration
Reference
1.1 FW 99.0 FW 19.5 FW 66.0 FW; 224.8 DW 4.8 FW; 23.5 DW 0.7 FW; 2.7 DW 2.7 FW; 3.1 DW 4.4 FW; 8.9 DW
10 10 4 11 11 11 11 11
0.02-0.06 FW 0.17-0.50 FW 0.46-1.18 FW 1.6-1.8 FW 3.2-4.4 FW 2.8-4.1 FW 1.5 FW 0.6-0.7 FW 0.3-0.4 FW 0.2-0.4 FW 0.04-0.06 FW 0.2-0.3 FW
12 12 12 5 5 5 5 5 5 5 5 5
0.04-0.16 FW 0.72-2.35 FW 14.3-387.0 FW
12 12 12
1.4-12.0 FW vs. 3.1-16.0 FW 5.0-9.8 FW vs. 8.4-8.6 FW 10.0-30.0 FW vs. 11.0-26.0 FW 3.0-5.7 FW vs. 2.8-5.0 FW 0.9 FW vs. 0.9 FW 0.9-1.6 FW vs. 0.9-1.6 FW 0.4-0.8 FW vs. 0.4-0.7 FW 0.2-0.4 FW vs. 0.3-0.6 FW 0.06-0.09 FW vs. 0.1 FW 0.3-0.5 FW vs. 0.3-0.4 FW
5 5 5 5 5 5 5 5 5 5
15.0-127.0 FW vs. 3.2-28.0 FW 0.05-0.22 FW vs. 0.02-0.08 FW 0.50-2.3 FW vs. 0.25-2.0 FW
13 13 13
a
(Continues)
420 Chapter 6 Table 6.7: Organism
Cont’d
Concentration
Reference
0.03-0.35 FW vs. 0.11-0.85 FW 0.03-0.11 FW vs. 0.36-1.0 FW 0.09-1.6 FW vs. 0.31-2.8 FW 0.06-3.6 FW vs. 0.25-1.7 FW 0.68-4.9 FW vs. 0.4-4.2 FW 0.65-60.0 FW vs. 0.65-14.0 FW
13
0.07-17.0 FW vs. 0.20-4.2 FW 0.07-0.25 FW vs. 0.15-2.3 FW 1.3 FW vs. 2.5 FW 18.0 FW vs. 7.8 FW 2.5-14.0 FW vs. 0.7-7.8 FW 16.0-250.0 FW vs. 4.3-62.0 FW
13 13 13 13 13 13
0.04 (0.03-0.07) FW 0.14 (0.01-0.52) FW
84 84
0.03 FW
94
Northern bottlenose whale, Hyperoodon ampullatus Muscle Liver
0.33 FW 0.38 FW
4 4
Whitebeaked dolphin, Lagenorhynchus albirostris Fascical fat Blubber Liver Muscle Testicles Kidney Spleen Brain
1.3 FW 0.9 FW 19.0 FW 2.0 FW 0.7 FW 1.6 FW 1.2 FW 3.0 FW
14 14 14 14 14 14 14 14
Juveniles found dead; inorganic mercury vs. methylmercury Brain Blubber Muscle Spleen Kidney Liver Adults found dead; inorganic mercury vs. methylmercury Brain Blubber Muscle Spleen Kidney Liver Hong Kong; found stranded; stomach contents Humpback dolphin, Sousa chinensis Finless porpoise; Neophocoena phocaenoides Leopard seal, Hydrurga leptonyx; serum
a
13 13 13 13 13
(Continues)
Mammals 421 Table 6.7:
Cont’d
Organism
Concentration
Reference
Weddell seal, Leptonychotes weddelli; Antarctica; summers 2002-2003 Serum Hair
0.01 DW 5.6 DW
94 94
1.6 FW 0.14 FW 0.03 FW
15 15 15
96.0 FW 0.29 FW 0.06 FW
15 15 15
178.0 FW 0.34 FW 0.05 FW
15 15 15
1.8 DW 44.0 DW 24.0 DW 1.5 DW 2.1 DW
26 26 26 26 59
1.7 3.4 2.3 3.6 2.5 1.3 3.3
FW FW FW FW FW FW FW
53 53 53 53 53 53 53
0.2 FW
10
Mammals (seals), 2 spp. Body length 84-114 cm Liver Brain Blubber Body length 117-152 cm Liver Brain Blubber Body length 155-254 cm Liver Brain Blubber Weddell seal, Leptonychotes weddelli; adult Terra Nova Bay, Antarctica; 1989-1992 Muscle Liver Spleen Pancreas Admiralty Bay, Antarctica; January 2004; fur Atlantic walrus, Odobenus rosmarus rosmarus; liver; age 9-19 years; northwest Greenland 1977 1978 1987 1988 1989 1999 2003 Humpback whale, Megaptera novaeangliae; muscle
a
(Continues)
422 Chapter 6 Table 6.7: Organism Norway; winter 1989-1990; Arctic Ocean coast; maximum values Grey seal, Halichoerus grypus Brain Kidney Liver Harp seal, Pagophilus groenlandica Brain Kidney Liver Ringed seal, Phoca hispida Brain Kidney Liver Harbor seal, Phoca vitulina Brain Kidney Liver Killer whale, Orcinus orca; Japan; 2005; found stranded; mature females vs. calves Liver Total mercury Methylmercury Kidney Total mercury Methylmercury Muscle Total mercury Methylmercury Lung Total mercury Methyl mercury Blood; total mercury Brain; total mercury Spleen; total mercury Harp seal, Pagophilus groenlandica Pups Brain Liver Kidney Blubber
Cont’d
Concentration
Reference
2.0 FW 16.0 FW 48.3 FW
39 39 39
0.1 FW 0.4 FW 1.1 FW
39 39 39
0.4 FW 0.5 FW 0.7 FW
39 39 39
2.0 FW 8.7 FW 16.0 FW
39 39 39
62.2 FW vs. 0.35 FW 1.1 FW vs. 0.06 FW
57, 86 57
8.1 FW vs. 0.23 FW 0.24 FW vs. 0.04 FW
57, 86 57
1.2 FW vs. 0.08 FW 0.90 FW vs. 0.07 FW
57, 86 57
1.8 FW vs. no data 0.31 FW vs. no data No data vs. 0.06 FW No data vs. 0.04 FW No data vs. 0.04 FW
57 57 57 57 57
0.04-0.13 FW 0.09-0.48 FW 0.04-0.34 FW 0.03 FW
16 16 16 12
a
(Continues)
Mammals 423 Table 6.7: Organism Muscle Liver Fur Claw Liver Kidney Flipper Muscle Heart Stomach Stomach contents Brain Adult females Fur Claw Liver Flipper Muscle Heart Blubber Gulf of St. Lawrence; 1984; mother vs. pup age less than 3 weeks Kidney
Cont’d
Concentration
Reference
0.38 FW 3.63 FW 1.7 FW 1.8 FW 0.5 FW 0.4 FW 0.2 FW 0.2 FW 0.2 FW 0.1 FW 0.09 FW 0.2 FW
12 12 5 5 5 5 5 5 5 5 5 5
3.2 3.7 4.6 0.5 0.5 0.3 0.1
FW FW FW FW FW FW FW
5 5 5 5 5 5 5
0.8 FW vs. 0.29 FW; 3.5 DW vs. 1.2 DW 10.4 FW vs. 0.32 FW; 34.7 DW vs. 1.1 DW 0.38 FW vs. 0.14 FW; 1.3 DW vs. 0.51 DW 0.0065 (0.0026-0.010) FW
40
Melon-headed whale, Peponocephala electra; Japan; March 2006; found stranded; total mercury vs. methylmercury Liver Kidney Muscle Lung
126.0 FW vs. 9.1 FW 6.3 FW vs. 3.5 FW 4.9 FW vs. 3.8 FW 2.7 FW vs. 2.2 FW
95 95 95 95
Ringed seal, Phoca hispida Muscle Liver Claw
197.0 FW 210.0 FW 1.1-3.7 FW
10 10 5
Liver Muscle Mother’s milk
a
40 40 40
(Continues)
424 Chapter 6 Table 6.7: Organism Liver Muscle Muscle Liver Kidney Liver Quebec, Canada; 1989-1990 Brain Kidney Liver Muscle Greenland; liver; age less than 4 years old Northwest Greenland 1984 1985 1994 1998 2004 Central West Greenland 1994 1999 2000 2001 2002 2003 2004 Various Arctic region locations Aston Bay; liver vs. muscle Barrow Strait (age 10 years) Liver; total mercury vs. methylmercury Muscle Arctic Bay (age 3-4 months); liver vs. muscle Pond Inlet (age 5 years) Liver; total mercury vs. methylmercury Muscle Cape Parry (age 1.3 years); liver vs. muscle W. Victoria Island (age 13 years)
Cont’d
Concentration
Reference
27.5 FW 0.72 FW 0.5-1.2 FW 14.0-300.0 FW 2.8-5.2 FW 0.64 FW
6 6 17 17 17 4
0.2 0.2 5.1 0.3
30 30 30 30
FW FW FW FW
2.17 0.99 2.45 3.17 3.66
FW FW FW FW FW
53 53 53 53 53
1.64 1.67 0.76 0.90 1.36 1.45 1.70
FW FW FW FW FW FW FW
53 53 53 53 53 53 53
19.3 FW vs. 0.44 FW
7
16.1 FW vs. 0.89 FW
7
0.91 FW 0.32 FW vs. 0.07 FW
7 7
3.8 FW vs. 0.50 FW
7
0.17 FW 1.0 FW vs. 0.11 FW
7 7
a
(Continues)
Mammals 425 Table 6.7: Organism Liver; total mercury vs. methylmercury Muscle Saimaa ringed seal, Phoca hispida saimensis Muscle Liver Kidney Blubber Harbor seal, Phoca vitulina Liver Liver Liver Liver Blubber Muscle Muscle Hair Maine, USA vs. New Brunswick, Canada Blubber Muscle Liver Cerebrum Found dead; liver vs. brain Liver California Oregon Washington Alaska Fur Claws Liver Kidney Muscle Heart Stomach
Cont’d
Concentration
Reference
27.5 FW vs. 0.96 FW
7
0.72 FW
7
1.3-6.1 FW 72.0-210.0 FW 1.9-13.0 FW 0.14-0.46 FW
17 17 17 17
1.5-160.0 FW 257.0-326.0 FW 110.0 FW 8.9 FW 0.04 FW 1.0-10.0 FW 0.71 FW 1.56 FW
4 8 19 12 12 4 12 12
0.027-0.087 FW vs. 0.036-0.106 FW 0.021-1.54 FW vs. 0.16-0.59 FW 0.52-7.90 FW vs. 1.72-50.9 FW 0.05-0.28 FW vs. 0.15-0.76 FW 225.0-765.0 FW vs. 9.9-31.0 FW
20
81.0-700.0 FW 0.3-68.0 FW 1.3-60.0 FW 0.6-8.9 FW 1.8 FW 1.8 FW 1.0 FW 0.7 FW 0.6 FW 0.2 FW 0.2 FW
a
20 20 20 18
1 1 1 1 5 5 5 5 5 5 5 (Continues)
426 Chapter 6 Table 6.7: Organism Brain Blubber Gonad Spleen Eye Lung Pancreas Intestine; large vs. small Labrador and Newfoundland; body lengths 212-402 cm Muscle vs. kidney 212 cm 301 cm 304 cm 335 cm 402 cm Liver 212 cm 301 cm 304 cm 335 cm 402 cm Pacific harbor seal, Phoca vitulina richardii; dead pups; central California; 2006; total mercury Liver Kidney Pelt (including hair, epidermis, and dermis) Hair Muscle Heart Brain Blubber Bone Harbor porpoise, Phocoena phocoena North Sea; 1987-1990; juveniles vs. adults; maximum values Kidney Liver Muscle
Cont’d
Concentration
Reference
0.2 FW 0.08 FW 0.3 FW 0.2 FW 0.1 FW 0.2 FW 0.3 FW 0.2 FW vs. 0.3 FW
0.35 0.41 0.61 0.38 0.75
FW FW FW FW FW
vs. vs. vs. vs. vs.
1.1 1.8 2.3 2.7 2.4
FW FW FW FW FW
a
5 5 5 5 5 5 5 5
61 61 61 61 61
9.2 FW 1.8 FW 30.6 FW 7.4 FW 39.4 FW
61 61 61 61 61
1.8 (0.08-6.4) FW 1.6 (0.3-6.1) FW 1.5 (0.3-4.8) FW
87 87 87
15.9 (2.9-40.6) FW 0.8 (0.1-2.2) FW 0.4 (0.04-1.1) FW 0.31 (0.30-1.2) FW 0.11 (0.07-0.28) FW 0.04 (0.02-0.06) FW
87 87 87 87 87 87
6.0 DW vs. 23.0 DW 6.0 DW vs. 504.0 DW 3.0 DW vs. 24.0 DW
41 41 41 (Continues)
Mammals 427 Table 6.7: Organism Males vs. females Muscle Liver Blubber Liver Muscle Skin; adult captured 1936 vs. captured 1973 Muscle Liver Europe; found stranded; 1997-2003 Kidney; adults Liver; adults Fetus vs. mother Liver; Irish Sea Liver; S. Ireland Kidney; S. Ireland Liver Greenland USA Denmark Poland Ireland Black Sea Dall’s porpoise, Phocoenoides dalli Sanriku, Japan; 1997-1998; whole liver vs. liver nuclei, lysosomes, and mitochondria Japan; liver Total mercury Organic mercury Inorganic mercury Japan; February 2006; harpooned 6-year-old male Liver Kidney Muscle Skin Bone
Cont’d
Concentration
Reference
0.75 (0.21-1.92) FW vs. 1.0 (0.26-2.58) FW 0.89-18.3 FW vs. 0.55-91.3 FW 0.7 (0.5-0.9) FW 22.0 (1.5-69.0) FW 1.9 (0.8-3.2) FW 12.9 FW vs. 0.54 FW
21
0.15-0.17 FW 28.0 FW
a
21 14 14 14 14 4 4
1.57 (0.11-5.8) FW 17.3 (0.28-165.0) FW
68 68
0.52 FW vs. 69.6 FW 0.65 FW vs. 36.0 FW 0.17 FW vs. 1.96 FW
68 68 68
4.1 (0.5-20.7) FW 9.9 (0.6-38.6) FW 8.5 (0.4-32.8) FW 6.6 (0.5-65.1) FW 21.8 (0.6-190.0) FW 1.9 (0.1-9.9) FW
69 70 71 72 73 74
3.8 (0.6-7.1) FW vs. 1.7 (0.2-4.2) FW
29
26.0 (7.7-96.0) DW 6.7 (2.3-12.0) DW 19.0 (5.2-84.0) DW
78 78 78
15.0 FW 3.3 FW 2.1 FW 1.2 FW 0.1 FW
82 82 82 82 82 (Continues)
428 Chapter 6 Table 6.7: Organism Heart Lung Intestine Spleen Pancreas Diaphragm Blubber Cerebrum Stomach Sperm whale, Physeter macrocephalus; southern Australia; 1976; muscle Breeding vs. nonbreeding females All females Males La Plata river dolphin, Pontoporia blainvillei Liver Kidney Brazil; 2003-2004; southeast Brazil vs. South Brazil Liver Total mercury Organic mercury Kidney Total mercury Organic mercury Portugal; 1998-2002 Common dolphin, Delphinus delphis Muscle Liver Skin Fat Bottlenose dolphin, Tursiops truncatus Muscle Liver Skin Fat
Cont’d
Concentration
Reference
1.7 0.8 0.8 0.8 1.5 2.0 0.3 0.7 1.2
82 82 82 82 82 82 82 82 82
FW FW FW FW FW FW FW FW FW
10.0 (8.0-12.0) DW vs. 6.0 (0.8-10.0) DW 7.0 (0.8-12.0) DW 6.0 (0.9-12.0) DW
42
2.6-5.9 DW 1.4-1.5 DW
49, 62 49, 62
(0.7-9.6) DW vs. (1.2-51.6) DW (0.1-2.4) DW vs. (0.05-4.2) DW
93
(0.4-5.1) DW vs. (0.6-4.7) DW (0.2-1.1) DW vs. (0.3-1.8) DW
93 93
6.3 (0.7-25.0) DW 20.5 (1.3-99.0) DW 2.6 (1.1-4.0) DW 1.7 (0.8-2.5) DW
98 98 98 98
9.5 (2.1-17.0) DW 132.0 (23.0-241.0) DW 11.6 (5.0-12.3) DW 1.3 (1.2-1.3) DW
98 98 98 98
a
42 42
93
(Continues)
Mammals 429 Table 6.7:
Cont’d
Organism
Concentration
Reference
Dolphin, Stenella attenuata; eastern tropical Pacific Ocean; 1977-1985 Blood Brain Blubber Kidney Liver Muscle Pancreas
0.4 FW 2.0 FW 7.6 FW 5.6 FW 62.3 FW; max. 217.5 FW 2.2 FW 6.6 FW
43 43 43 43 43 43 43
9.3 DW 34.0 DW 630.0 DW
96 96 96
10.0 DW vs. 0.22 DW 30.0 DW vs. 2.4 DW 830.0 DW vs. 9.3 DW 43.0 DW vs. 2.7 DW
96 96 96 96
15.2 FW vs. 5.3 FW 205.0 FW vs. 7.0 FW 14.7 FW vs. 3.2 FW
44 44 44
0.8 FW vs. 0.4 FW 1.8 FW vs. 1.0 FW 3.0 FW vs. 1.5 FW 4.5 FW vs. 2.6 FW 10.7 FW vs. 3.5 FW
45 45 45 45 45
Max. 23.6 FW 7.0 FW vs. 30.0 FW; max. 179.0 FW 52.0 FW vs. 346.0 FW; max. 1544.0 FW 0.5 FW vs. 2.0 FW 4.0 FW vs. 28.0 FW; max. 81.0 FW Max. 32.0 FW
46 43, 46
Striped dolphin, Stenella coeruleoalba Japan; 1979 Liver Fetus Juvenile Adult Adult male vs. female fetus Blubber Kidney Liver Muscle Adults; Japan; 1977-1980; total mercury vs. methylmercury Muscle Liver Kidney Whole body; various ages; total mercury vs. methylmercury 1 year 3 years 4 years 14 years 20 years Found stranded on French Atlantic Ocean coast vs. Mediterranean Sea coast; 1972-1980 Intestine Kidney Liver Melon fat Muscle Stomach
a
43, 46 43 43, 46 46 (Continues)
430 Chapter 6 Table 6.7: Organism Found stranded; 1999-2004; liver Bay of Biscay, Atlantic Ocean Immatures Mature Mediterranean Sea, NW France Immatures Mature Found beached; South Adriatic Sea; February-April 1991 and JuneSeptember 1995; total mercury vs. methylmercury Liver Muscle
Cont’d
Concentration
Reference
6.5 (1.2-24.1) FW 138.0 (6.4-317.0) FW
54 54
4.4 (1.1-8.2) FW 373.0 (29.5-1033.0) FW
54 54
277.4 (0.0-966.3) FW vs. 14.8 (0.6-29.7) FW 17.4 (0.56-53.3) FW vs. 14.5 (0.56-45.7) FW
79 79
Spinner dolphin, Stenella longirostris Muscle Blubber Liver Kidney
0.9-1.3 FW <0.1 FW 6.0-13.0 FW 2.3-2.7 FW
Florida manatee, Trichechus manatus latirostris; 2007; Florida Blood Skin
0.008 FW; max. 0.046 FW 0.002 FW; max. 0.003 FW
91 91
0.147 FW vs. 0.086 FW 0.658 FW vs. 0.265 FW 1.0-1.4 FW; 3.3-4.7 DW
88 88 22
1.6 DW; max. 2.4 DW 1.7 DW; max. 4.9 DW 1.2 DW; max. 2.9 DW 2.1 DW; max. 3.3 DW 2.4 DW; max. 4.7 DW 0.005-0.095 FW; max. 0.13 FW
65 65 65 65 65 65
6.5 DW; max. 20.0 DW 6.4 DW; max. 15.0 DW
65 65
Bottlenose dolphin, Tursiops truncatus Blood; summers 2003-2005; total mercury vs. methylmercury Charleston, South Carolina Indian River, Florida Muscle Skin; 2003-2005; South Carolina Juvenile male Adult male Juvenile female Adult female Pregnant female Diet (whole fish); 6 spp. Skin; 2003-2005; Florida Juvenile male Adult male
a
8 8 8 8
(Continues)
Mammals 431 Table 6.7: Organism Juvenile female Adult female Pregnant female Diet (whole fish); 6 spp. Sarasota Bay, Florida; 2002-2004 Blood Skin Polar bear, Ursus maritimus Alaska; 1972; total mercury; young vs. adults Northern area Liver Muscle Western area Liver Muscle Greenland; adults; fur NW Greenland; 1978-1979 Eastern Greenland; 1984-1989 Svalbard; 1980; fur; recently molted Liver; 1993-2002; Alaska Beaufort Sea area Chukchi Sea area East Greenland; hair; 1992-2001 1885-1894 1905-1914 1925-1934 1945-1954 1965-1974 1975-1984 1985-1994 1995-2004 Northwest Greenland; hair; 1300-1994 1300 1915-1924 1935-1944 1955-1964 1985-1994
Cont’d
Concentration
Reference
9.3 DW; max. 31.0 DW 7.9 DW; max. 17.0 DW 5.9 DW 0.06-0.47 FW; max. 2.2 FW
65 65 65 65
0.51 FW; max. 1.8 FW 2.1 FW; max. 6.4 FW
75 75
22.4 FW vs. 38.1 FW 0.15 FW vs. 0.19 FW
47 47
3.9 FW vs. 4.8 FW 0.04 FW vs. 0.04 FW
47 47
8.0 (5.0-14.0) DW 4.6 (2.5-8.8) DW 2.0 (1.0-4.6) DW
48 48 48
33.1 (14.0-99.0) DW 10.1 (3.5-25.0) DW
76 76
1.4 1.1 0.4 1.6 7.2 3.8 5.8 5.4
83 83 83 83 83 83 83 83
(0.94-1.8) DW (0.7-1.6) DW DW (1.0-2.2) DW (1.7-21.6) DW (1.8-5.4) DW (1.1-24.2) DW (0.8-17.7) DW
0.52 (0.47-0.55) DW 1.3 (0.4-2.6) DW 6.3 (2.1-10.6) DW 3.4 DW 7.4 (3.0-14.2) DW
a
83 83 83 83 83 (Continues)
432 Chapter 6 Table 6.7: Organism California sea lion, Zalophus californianus Found stranded; southern California coast; 2003-2004 Liver Kidney Healthy animals Liver Kidney Muscle Heart Cerebellum Cerebrum Fat Sick animals (leptospirosis) Liver Muscle Mothers with premature pups vs. mothers with normal pups Liver Kidney Premature pups vs. normal pups Liver Kidney
Cont’d
Concentration
Reference
2.6-143.4 (0.5-442.0) FW 1.0-3.1 (0.5-10.0) FW
77 77
74.1 FW 7.0 FW 1.2 FW 0.6 FW 0.53 FW 0.48 FW 0.2 FW
23 23 23 23 23 23 23
161.3 FW 1.6 FW
23 23
204.0 DW vs. 747.0 DW 7.1 DW vs. 28.4 DW
24 24
1.8 DW vs. 9.6 DW 0.9 DW vs. 4.6 DW
24 24
a
Values are in mg Hg/kg fresh weight (FW) or dry weight (DW). a 1, Anas, 1974; 2, Kim et al., 1974; 3, Sergeant and Armstrong, 1973; 4, Harms et al., 1978; 5, Freeman and Horne, 1973; 6, Smith and Armstrong, 1975; 7, Smith and Armstrong, 1978; 8, Gaskin et al., 1974; 9, Stoneburner, 1978; 10, Holden, 1973a; 11, Jones et al., 1972; 12, Sergeant and Armstrong, 1973; 13, van de Ven et al., 1979; 14, Andersen and Rebsdorff, 1976; 15, Holden, 1975; 16, Jones et al., 1976; 17, Kari and Kauranen, 1978; 18, Koeman et al., 1973; 19, Roberts et al., 1976; 20, Gaskin et al., 1973; 21, Gaskin et al., 1972; 22, Bernhard and Zattera, 1975; 23, Buhler et al., 1975; 24, Martin et al., 1976; 25, Szefer et al., 1993; 26, Bargagli et al., 1998; 27, Bacher, 1985; 28, Sanpera et al., 1993; 29, Ikemoto et al., 2004a,b; 30, Langlois et al., 1995; 31, Haynes et al., 2005; 32, Denton and Breck, 1981; 33, Denton et al., 1980; 34, Haynes and Kwan, 2001; 35, Gladstone, 1996; 36, Dietz et al., 1996; 37, Dietz et al., 1990; 38, Bustamante et al., 2004; 39, Skaare et al., 1994; 40, Wagemann et al., 1988; 41, Joiris et al., 1991; 42, Cannella and Kitchener, 1992; 43, Andre et al., 1991a; 44, Itano et al., 1984a; 45, Itano et al., 1984b; 46, Andre et al., 1991b; 47, Lentfer and Galster, 1987; 48, Born et al., 1991; 49, Dehn et al., 2006b; 50, Bratton et al., 1997; 51, Woshner et al., 2001; 52, Tarpley et al., 1995; 53, Riget et al., 2007; 54, Lahaye et al., 2006; 55, Endo et al., 2007a; 56, Endo et al., 2005; 57, Endo et al., 2006; 58, Honda, 1990; 59, Santos et al., 2006; 60, Honda et al., 2006; 61, Veinott and Sjare, 2006; 62, Seixas et al., 2007; 63, Stockin et al., 2007; 64, Brunborg et al., 2006; 65, Stavros et al., 2007; 66, Dehn et al., 2006a; 67, Burger et al., 2007; 68, Lahaye et al., 2007; 69, Paludan-Muller et al., 1993; 70, Mackey et al., 1995; 71, Strand et al., 2005; 72, Ciesielski et al., 2006; 73, Law et al., 1992; 74, Joiris et al., 2001; 75, Bryan et al., 2007; 76, Kannan et al., 2007; 77, Harper et al., 2007; 78, Yang et al., 2007; 79, Storelli et al., 1998; 80, Wagemann et al., 1998; 81, Kannan et al., 2006; 82, Yang et al., 2006; 83, Dietz et al., 2006; 84, Hung et al., 2007; 85, Nielsen and Dietz, 1990; 86, Endo et al., 2007b; 87, Brookens et al., 2008; 88, Stavros et al., 2008b; 89, Lavery et al., 2008; 90, Capelli et al., 2008; 91, Stavros et al., 2008a; 92, Rosa et al., 2008; 93, Seixas et al., 2008; 94, Gray et al., 2008; 95, Endo et al., 2008; 96, Agusa et al., 2008; 97, Arai et al., 2004; 98, Carvalho et al., 2002; 99, Law et al., 2003.
Mammals 433 increasing age of the organism. This is attributed to either a decreasing elimination rate of methylmercury with increasing age, a decreasing demethylating efficiency with age, or to increasing uptake of methylmercury with age (Wagemann et al., 1998). Mercury has increased dramatically in the Arctic region and Greenland environments when compared to preindustrial times (Braune et al., 2005; Dietz et al., 2006; Nilsson and Huntington, 2002); as one consequence, many species of marine mammals from those locales contain hazardous levels of mercury in tissues favored by human consumers (Table 6.7). This argument could be made for numerous locales worldwide (Eisler, 2006). Elevated concentrations of total mercury in seal hairs from sediment cores representing the past 2000 years in Antarctica (total mercury concentrations ranged from 0.93 to 1.59 mg/kg DW seal hairs) were associated with extensive gold and silver mining activities using mercury amalgamation from 18 to 300 CE (Roman Empire and Han dynasty), 750 to 900 (Maya period and Tang dynasty), 1200 to 1500 (Incas and Christianity), 1650 to 1800 (New World), and 1840 to the present (modern industry) (Sun et al., 2006). Mercury concentrations in seal hairs were comparatively low during periods of reduced gold and silver mining activities (Sun et al., 2006). The mechanisms to account for mercury accumulation in pinnipeds are similar to those reported by Itano et al. (1984a–c) for the striped dolphin (S. coeruleoalba). Itano and his coworkers showed that tissue concentrations of mercury in striped dolphins: increased with increasing age of the animal, reaching a plateau in 20–25 years; were present in the methylated form in the fetal and suckling stages, but the proportion of methylmercury decreased over time with no absolute increase after 10 years; were excreted slowly by all developmental stages, and slowest in older dolphins (resulting in higher accumulations); and were correlated strongly with selenium concentrations in all age groups. It is probable that inorganic mercury and selenium were complexed in a 1:1 molar ratio, in a form biologically unavailable to marine mammals (and probably other mammals), thereby significantly decreasing the risk of mercury toxicosis to individuals with grossly elevated mercury body burdens (Eisler, 1984, 2006; Nielsen and Dietz, 1990). The Hg:Se ratio was close to 1.0 in adults of four species of Norwegian seals, provided that tissue mercury concentrations were greater than 15.0 mg/kg FW (Skaare et al., 1994). Total mercury in livers of pinniped mothers, but not pups, was correlated positively with selenium (Wagemann et al., 1988). In general, mercury is mainly associated with selenium as HgSe under a detoxified form in the insoluble fraction of the tissues (Das et al., 2002). In gray seals, H. grypus, mercury concentrations were higher in liver, kidney, and muscle of mature males and females when compared to immature individuals; this was especially pronounced in liver, where maximum mercury concentrations of 199.0 and 238.0 mg/kg FW were recorded in mature males and females, respectively (Table 6.7). Mercury concentrations showed a significant correlation between liver and kidney, indicating proportional accumulation (Seixas et al., 2007). Some studies report significant correlations between mercury and cadmium in liver and kidney of cetaceans (Caurant et al., 1994; Monaci et al.,
434 Chapter 6 1998); however, others found a negative relation (Roditi-Elasar et al., 2003; Wagemann et al., 1990). A strong correlation between cadmium, mercury, and zinc in kidney suggests the presence of a detoxification process involving metallothionein proteins; another strong and positive correlation between mercury and selenium and a molecular Hg:Se ratio close to 1.0 in liver of gray seals suggests a demethylation process leading to the formation of mercuric selenide granules (Bustamante et al., 2004). Large colonies of pinnipeds, and to a lesser extent marine birds along the western coast of the United States may make mercury available to California mussels (Mytilus californianus) through fecal elimination of large amounts of mercury, resulting in abnormally high mercury levels in mussels from several west coast sites (Flegal et al., 1981). In polar bears, U. maritimus, collected in Alaska between 1993 and 2000, livers from the Beaufort Sea subpopulation had significantly higher mercury burdens than conspecifics from the Chukchi Sea subpopulation: 33.1 (14.0–99.0) mg Hg/kg DW versus 10.1 (13.5–25.0) DW (Kannan et al., 2007; Table 6.7); the reverse was true for silver, bismuth, barium, copper, and tin for reasons unknown (Kannan et al., 2007). In bottlenose dolphins, T. truncatus, there was a strong positive correlation between blood and skin mercury concentrations; skin had the highest mercury burdens; calves had significantly lower blood mercury levels than did their mothers; and female dolphins had higher mercury burdens in skin and blood than males (Bryan et al., 2007). Blood mercury concentrations in bottlenose dolphins increased with increasing age of the animal (Stavros et al., 2008b); a similar trend was documented in liver (Lavery et al., 2008). The mercury poisoning incident at Minamata Bay, Japan, showed that death and congenital birth defects occur in humans after long-term ingestion of marine fish and shellfish highly contaminated with methylmercury compounds. An outbreak of mercury intoxication occurred in Niigata Prefecture, Japan, in 1964–1965; afflicted individuals exhibited numbness, hearing impairment, cerebellar ataxia, speech disturbance, visual field constriction, and difficulty walking (Tsubaki et al., 1967). Elevated—but not dangerous—concentrations of mercury are reported in coastal populations, especially among fishermen that subsist mainly on marine comestibles (Establier, 1975; Nuorteva et al., 1975; Skerfring et al., 1970; Ui and Kitamuri, 1971). Elevated mercury concentrations in diets of Inuits are not conclusively dangerous. Pregnant Inuit women living in close proximity to the sea and consuming seal meat and blubber on a regular basis contained higher mercury concentrations in maternal and fetal blood and tissues than did similar populations living inland; however, the high mercury concentrations in Inuit infants from mothers who ate seal meat or fish every day during their pregnancy were below toxic limits (Galster, 1976). Inuit sled dogs, subsisting largely on seal meat, contained up to 11.5 mg Hg/kg FW liver without apparent harm (Smith and Armstrong, 1975). Birke et al. (1972) suggest that humans may ingest up to 0.8 mg mercury daily, as
Mammals 435 methylmercury, without experiencing symptoms of mercury poisoning; however, most U.S. authorities agree that this is excessive (Eisler, 2006). Several variables modify mercury uptake and retention in marine mammals. These include diet, age of the mammal, gender, general health, proximity to urban areas, selenium residues, and migrations through high tectonic activity. Diet, for example, is an important concentrating mechanism in seals. Gray seals, hood seals, and harbor seals—which feed on large fish and cephalopods—contain up to 10 times more mercury in their tissues than harp seals, which feed on small pelagic fish and crustaceans (Sergeant and Armstrong, 1973). Fishes are also the main source of mercury for cetaceans (Monteiro-Neto et al., 2003). Striped dolphins, S. coeruleoalba, that feed on prey from the Mediterranean Sea have higher mercury levels in tissues than conspecifics from the Atlantic coast because mercury burdens in Mediterranean Sea fauna are elevated (Lahaye et al., 2006). Concentrations of copper, zinc, cadmium, and lead in muscle and liver tissues of prey fish did not differ significantly from those in corresponding organs of marine mammal consumers; however, mercury concentrations were significantly higher in liver of whales and seals than in their fish diet (Harms et al., 1978). Pregnant or lactating sperm whales (P. macrocephalus) had significantly higher mercury concentrations in muscle than did nonbreeding females (Cannella and Kitchener, 1992). One source of mercury in livers of pilot whales, Globicephala macrorhyncha, may be volcanic activity in areas of mercury ore deposits and through which whales migrate; or exposure over time rather than diet (Gaskin et al., 1974). If correct, this could account, in part, for the elevated mercury concentrations in pilot whales from St. Lucie that reflect uptake from existence in a tectonically active region with a higher than average level of mercury, and exposure to a small fraction of air-transported mercury from outside the region, possibly industrial in origin. Age and tissue specificity also influence mercury residue levels. Increasing concentrations of total and organic mercury in muscle and liver were observed with increasing age of whales (Dehn et al., 2006b; Endo et al., 2007b; Sanpera et al., 1993), striped dolphins (Andre et al., 1991a), ringed seals (Riget et al., 2007), harbor seals (Veinott and Sjare, 2006), and others (Eisler, 2006; Harper et al., 2007). However, in harbor porpoise, Phocoena phocoena, total mercury—but not methylmercury—increased in tissues with increasing age (Joiris et al., 1991). In general, total mercury content in all mammalian tissues increases with increasing age of the animal (Eisler, 1984; Freeman and Horne, 1973; Gaskin et al., 1972; Harms et al., 1978; Holden, 1975; Wagemann et al., 1998). This was especially pronounced for liver (Anas, 1974; Eisler, 1984, 2006; Harms et al., 1978; Holden, 1973a,b, 1975; Jones et al., 1976; Seixas et al., 2007; Sergeant and Armstrong, 1973). In one case, liver from an older gray seal contained 387.0 mg Hg/kg FW, a level substantially in excess of levels found toxic to human consumers (Sergeant and Armstrong, 1973). However, in contrast to fish, a high percentage of the total mercury in liver of seals and whales is in the inorganic form (Harms et al., 1978).
436 Chapter 6 Elevated mercury concentrations in tissues of marine mammals were also associated with poor health due to leptospirosis (Buhler et al., 1975), with proximity to urbanized areas (Anas, 1974; Roberts et al., 1976), with starvation (Jones et al., 1976), and with gender, being higher in females than males (Gaskin et al., 1972). Placental transfer of mercury to developing pups is low (Freeman and Horne, 1973; Jones et al., 1976; Kim et al., 1974), and methylmercury concentrations in seal pups are lower than that of their mothers. The seal fetus did not show a preference for mercury over maternal burdens, suggesting that seals may have enzyme systems that demethylate mercury (Freeman and Horne, 1973). Lymphocyte proliferation was significantly inhibited in newborn harbor seals, P. vitulina; inhibition was recorded during exposure for 5 days in 0.5 mg Hg/L as either ethylmercury, methylmercury, or mercuric chloride (Kakuschke et al., 2008a). In killer whales, the transfer of mercury from mother to fetus via placenta, or via milk is negligible (Endo et al., 2006), as was true for pinnipeds. Mercury and selenium concentrations are positively correlated over the past 1500 years in seal hairs—mainly southern elephant seal, Mirounga leonine—and in the lake sediments amended by seal excrements in West Antarctica, suggesting a self-protection mechanism against mercury poisoning in Antarctic seals (Yin et al., 2007). Mercury and selenium concentrations in livers of marine mammals are positively correlated (Capelli et al., 2008; Endo et al., 2008; Koeman et al., 1973, 1975; Martin et al., 1976; Seixas et al., 2008; Veinott and Sjare, 2006; Wagemann et al., 1998). In liver of Dall’s porpoise, Phocoenoides dalli, the mercury/selenium molar ratio is about 1.0 provided that hepatic total mercury concentration is at least 20.0–30.0 mg Hg/kg DW (Yang et al., 2007). In liver of striped dolphin, S. coeruleoalba, the Hg/Se molar ratio is about 1.0 when a threshold limit of >0.1 mg Hg/kg FW is surpassed (Palmisano et al., 1995). In killer whales, O. orca, the Hg/Se molar ratio in liver of mature females was 1.03, but only 0.11 in liver of calves; this ratio did not hold for any other tissue examined in mature females except liver (Endo et al., 2006). Mercury and selenium in liver and kidney increased with increasing body length in dolphin, P. blainvillei, with a hepatic Se/Hg ratio close to 4 (Seixas et al., 2008). The formation of the HgSe compound increases the hepatic accumulation of mercury (Endo et al., 2006). Koeman et al. (1973) aver that selenium protects these mammals by completely binding to subcellular sulfur sites, the presumed location of mercury’s toxic action. Both ringed and bearded seals accumulate high levels of naturally occurring mercury in liver; however, there was no sign of mercury intoxication in either species after extensive sampling (Smith and Armstrong, 1978). The presence of selenium in a 1:1 atomic ratio with mercury in seal liver suggests a biochemical binding process. The mechanism of mercury detoxification by selenium in seals is not understood, but it appears that when selenium is ingested along with mercury, some mechanism operates in seals which causes both elements to combine and become immobilized in liver (Smith and Armstrong, 1978). The Hg/Se molar ratio in liver tissue of harbor seals is positively correlated with seal length (Veinott and Sjare, 2006).
Mammals 437 Under laboratory conditions, gray seals dosed with methylmercury show a time-related increase in both mercury and selenium in liver and kidney; however, in other tissues examined (brain, thyroid, blood, etc.) only mercury burdens increased (van de Ven et al., 1979). In feral gray seals, selenium shows a positive correlation with mercury concentrations. Atomic ratios of mercury and selenium in liver were near 1.0 in feral seals, as expected, but this ratio exceeded 1.0 in seals fed additional methylmercury (van de Ven et al., 1979). Liver mercury burdens in melon-headed whales, Peponocephala electra, are also positively correlated with cadmium, zinc, and copper, as well as selenium (Endo et al., 2008). The percentage of methylmercury in any tissue from any marine mammal seems to be inversely correlated with total mercury content (Brunborg et al., 2006; Buhler et al., 1975; Gaskin et al., 1972, 1974; Koeman et al., 1975; Sergeant and Armstrong, 1975; Smith and Armstrong, 1975). For example, harbor seal livers from Maine (USA) contained a maximum of 7.8 mg total Hg/kg FW versus 50.9 from New Brunswick, Canada; however, methylmercury accounted for 13–37% of total mercury in livers from the Maine location versus 2–11% in the Canadian group (Gaskin et al., 1972). Among healthy California sea lions, Z. californianus, Buhler et al. (1975) report concentrations of total mercury in tissues— in mg/kg FW and percent methylmercury—as follows: liver 74.0 and 3.7%; kidney 7.0 and 17.2%; muscle 1.2 and 88.6%; and heart 0.59 and 88.1%. In Greenland, seal liver containing 174.0 mg total Hg/kg FW had 1.2% organomercury, seal kidney with 6.4 mg total Hg/kg FW had 15.0% organomercury, and whale muscle with 1.3 mg total Hg/kg FW had 92% organomercury (Dietz et al., 1990, 1996). A different trend was found in belugas captured in Alaska between 1992 and 1999: almost all (96–97%) mercury in epidermis and muscle was in the form of methylmercury and for kidney and liver these values were 13–17% (Dehn et al., 2006b; Table 6.7). There is some evidence that mercury excretion rates follow a biphasic or polyphasic pattern. Tillander et al. (1972), in studies with ringed seals, found that the fastest excreted component took 20 days for complete elimination and the slowest excreted mercury fraction, which comprised 54% of all mercury, took 500 days for 50% elimination. Harp seals, P. groenlandica, were subjects of a 90-day controlled feeding study (Ronald et al., 1977). During this period, seals were fed 0.25 or 25.0 mg of methylmercury per kilogram of body weight daily. At the lower concentration, mercury concentrations at 90 days ranged from 42.7 to 82.5 mg Hg/kg FW in liver, kidney, and muscle; from 13.1–25.0 in adrenal, claws, brain, spleen, lung, small intestine, heart, and blood; 1.6 in hair, and 0.2 mg Hg/kg FW in blubber. At 25.0 mg Hg/kg body weight daily, one seal died in 20 days, another at 26 days. Blood mercury concentrations in these animals shortly before death were 26.8 and 30.3 mg/kg FW. These seals were diagnosed with toxic hepatitis, uremia, and renal failure (Ronald et al., 1977). Histopathological damage was also evident (Ramprashad and Ronald, 1977). Thus, in the 0.25 mg/kg group, 5% of the sensory cells in the cochlea of the
438 Chapter 6 middle ear were damaged (24% in the 25.0 mg/kg group), as well as sensory hair cells along the full length of the cochlea in both groups. It is noteworthy that dead harbor seals, P. vitulina, contained 9.0–31.0 mg total Hg/kg FW in brain and that these brain mercury concentrations were similar to those in brain tissues of animals of various species poisoned experimentally by methylmercury (Koeman et al., 1973). In view of the numerous reported beachings and strandings of many species of large marine mammals, the significance of the findings of Ronald and his coworkers and those of Koeman and his colleagues should not be discounted. The safety limit set by health authorities of South Korea for the fishery industry of 0.5 mg total mercury/kg FW was exceeded by almost all red meat cetacean products (Table 6.7), and all red meat cetacean products exceeded the Japanese safety limit of 0.4 mg Hg/kg FW (Endo et al., 2007a). Cetacean livers sold for human consumption in Korea ranged from 18.7 to 156.0 mg Hg/kg FW in finless porpoise, N. phocaenoides, and 13.2 mg Hg/kg FW in common dolphin, D. delphis (Endo et al., 2007a). In Canada, methylmercury concentrations in muscle of beluga from all locations—with only a few exceptions—exceeded 0.5 mg/kg FW which is the Canadian Federal Guideline for human consumption of fish (Wagemann et al., 1998).
6.21 Molybdenum Molybdenum tends to concentrate in liver tissues of marine mammals. Maximum concentrations of molybdenum in liver, in mg Mo/kg FW, were 1.1 in Dall’s porpoise, P. dalli, and 0.9 in the California sea lion, Z. californianus (Table 6.8). Data for molybdenum and the hump-backed dolphin, S. chinensis, indicate that maximum concentrations in selected food items ranged from 16.4 to 17.2 mg Mo/kg DW, and in dolphin tissues from 0.8 to 1.6 mg Mo/kg DW (Table 6.8). No laboratory data were available for molybdenum and whole marine mammals; almost all studies conducted to date on molybdenum effects on mammals under controlled conditions have been on livestock, especially cattle and sheep (Eisler, 2000c). However, lymphocyte proliferation is significantly stimulated in newborn harbor seals, P. vitulina, when cells were incubated in 25.0 mg Mo/L for 5 days (Kakuschke et al., 2008a).
6.22 Nickel The maximum nickel concentrations documented in tissues of marine mammals were 2.1 mg/kg FW in the liver of a sperm whale, P. macrocephalus found stranded in the North Sea, and 2.1 mg Ni/kg FW in the liver of Irish Sea cetaceans (Table 6.8). Nickel is ubiquitous in the biosphere and essential for the normal growth of many species of plants and vertebrate animals (Eisler, 2000f; USNAS, 1975; USPHS, 1993a, 1995; WHO, 1991).
Mammals 439 Table 6.8: Molybdenum, Nickel, and Rubidium Concentrations in Field Collections of Mammals Element and Organism
Concentration
Reference
a
Molybdenum Southern sea otter, Enhydra lutris nereis; found dead; California coast; 1992-2002; adult females; liver Harbor seal, Phoca vitulina; blood Captive animals Wild; North Sea Wadden Sea; 2004-2005; German site vs. Danish site Dall’s porpoise, Phocoenoides dalli; Japan; 2006; harpooned male Liver Kidney, bone, heart, intestine, pancreas, stomach Muscle, skin, lung, spleen, diaphragm, blubber, cerebrum Hump-backed dolphin, Siusa chinensis; Hong Kong Stomach contents; whole decapod crustaceans vs. fishes Diet, all sources Liver Kidney Blubber Striped dolphin, Stenella coeruleoalba; Japan; 1979 Liver Fetus Juvenile Adult Adult male vs. female fetus Blubber Kidney Liver Muscle Bottlenose dolphin, Tursiops truncates Sarasota Bay, Florida; 2002-2004 Blood Skin
0.55 (0.08-1.3) DW
13
0.002-0.004 FW 0.001-0.011 FW 0.005 FW vs. 0.006 FW
16 17 19
1.1 FW 0.01-0.04 FW
14 14
0.004-0.009 FW
14
<0.9-17.2 DW vs. <0.9-16.4 DW 3.3 DW 0.8 DW; max. 1.6 DW 0.09 DW; max. 0.8 DW 0.3 DW; max. 1.2 DW
1 1 1 1 1
0.16 DW 5.5 DW 4.5 DW
22 22 22
0.03 DW vs. 0.01 DW 0.21 DW vs. 0.14 DW 2.5 DW vs. 0.16 DW 0.02 DW vs. 0.02 DW
22 22 22 22
0.001 FW; max. 0.0015 FW 0.006 FW; max. 0.016 FW
10 10 (Continues)
440 Chapter 6 Table 6.8:
Cont’d
Element and Organism
Concentration
Reference
Polar bear, Ursus maritimus; liver; Alaska; 1993-2002 Beaufort Sea region Chukchi Sea region
1.4 (1.0-1.8) DW 1.5 (0.8-2.3) DW
11 11
California sea lion, Zalophus californianus; found stranded; southern California; 2003-2004 Liver Kidney
0.3-0.4 (0.2-0.9) FW 0.3-0.4 (0.2-0.6) FW
12 12
0.6 FW vs. <0.04 FW 0.12 FW vs. <0.04 FW <0.04 FW vs. 0.25 FW
24 24 24
<0.05-0.05 FW vs. <0.04-0.48 FW
24
a
Nickel Australia; 1995-1996; stranded; liver vs. kidney Bottlenose dolphin, Tursiops truncatus aduncus Adult female Female calf Common dolphin, Delphinus delphis; juvenile Melon-headed whale, Peponocephala electra; adults British Isles; 8 spp.; 1988-1989; liver
<0.5 FW
2
Common dolphin, Delphinus sp.; December 2004; found stranded; New Zealand Blubber Liver, kidney
Max. 0.71 FW <0.1 FW
8 8
Hong Kong; found stranded; stomach contents Humpback dolphin, Sousa chinensis Finless porpoise, Neophocoena phocaenoides
2.5 (0.08-9.8) FW 0.67 (0.19-1.8) FW
15 15
Leopard seal, Hydrurga leptonyx; serum
0.007 FW
21
Weddell seal, Leptonychotes weddelli; Antarctica; 2002-2003 Serum Hair
<0.001 DW 3.5 DW
21 21
Southern elephant seal, Mirounga leonina; molted fur; Shetland Islands; juveniles vs. adult females
Max. 0.92 DW vs. 1.0 (0.3-2.3) DW
7
(Continues)
Mammals 441 Table 6.8:
Cont’d
Element and Organism
Concentration
Harbor seal, Phoca vitulina; blood Captive animals Wild; North Sea Wadden Sea; 2004-2005; German site vs. Danish site
Max. 0.005 FW Max. 0.023 FW 0.002 (0.0009-0.0095) FW vs. (<0.0004-0.026) FW
Vaquita (porpoise), Phocoena sinus; Baja California, Mexico Heart Kidney Liver
0.7 FW 0.5 FW <0.4 FW
4 4 4
0.39 FW; max. 2.1 FW
5
Sperm whale, Physeter macrocephalus; North Sea; 1994-1995; liver; found stranded Portugal; 1998-2002 Common dolphin, Delphinus delphis Muscle Liver Skin Fat Bottlenose dolphin, Tursiops truncates Muscle Liver Skin Fat Sweden; 3 spp. (Harbor seal, Phoca vitulina; gray seal, Halichoerus grypus; ringed seal, Phoca hispida); liver and kidney Florida manatee, Trichechus manatus latirostris; 2007; Crystal River, Florida Blood Skin
Reference
16 17 19
<1.3 DW <1.3 DW 2.3 (1.6-2.9) DW 1.9 (1.2-3.2) DW
23 23 23 23
<1.4 DW <1.2 DW 2.1 (1.8-2.4) DW 1.4 (1.5-2.2) DW
23 23 23 23
Usually <0.006 FW; max. 0.17 FW in liver, 0.08 FW in kidney
0.003 (0.002-0.004) FW 0.023 (0.011-0.040) FW
a
6
20 20
Bottlenose dolphin, Tursiops truncatus; skin
0.03-0.08 DW
9
Wales and Irish Sea; 6 spp.; 1989-1991; liver
Usually <0.5 FW; max. 2.1 FW
3 (Continues)
442 Chapter 6 Table 6.8: Element and Organism
Cont’d
Concentration
Reference
a
Rubidium Southern sea otter, Enhydra lutris nereis; adult females; liver; found dead along California coast; 1992-2002 Non-diseased Emaciated Infectious-diseased
3.1 (0.9-6.3) DW 2.8 (1.8-4.2) DW 2.8 (1.6-4.3) DW
13 13 13
Harbor seal, Phoca vitulina; blood Captive animals Wild; North Sea Wadden Sea; 2004-2005; German site vs. Danish site
0.055-0.130 FW 0.012-0.134 FW 0.07 (0.05-0.15) FW vs. 0.07 (0.05-0.10) FW
16 18 19
3.3 (1.7-4.5) DW 3.4 (1.9-4.6) DW 1.6 (1.0-2.2) DW <1.1 DW
23 23 23 23
3.3 (2.7-3.9) DW 2.9 (2.3-3.7) DW <1.1 DW <1.1 DW
23 23 23 23
0.3 DW 0.4 DW
22 22
Portugal; 1998-2002 Common dolphin, Delphinus delphis Muscle Liver Skin Fat Bottlenose dolphin, Tursiops truncates Muscle Liver Skin Fat Striped dolphin, Stenella coeruleoalba; Japan; 1979 Liver Juvenile Adult Adult male vs. female fetus Blubber Kidney Liver Muscle Bottlenose dolphin, Tursiops truncates Sarasota Bay, Florida; 2002-2004 Blood Skin
0.5 5.3 4.9 4.6
DW DW DW DW
vs. vs. vs. vs.
1.0 5.1 4.3 3.3
DW DW DW DW
0.55 FW; max. 0.78 FW 0.99 FW; max. 1.47 FW
22 22 22 22
10 10 (Continues)
Mammals 443 Table 6.8:
Cont’d
Element and Organism
Concentration
Polar bear, Ursus maritimus; liver; Alaska; 1993-2003 Beaufort Sea area Chukchi Sea area
12.9 (9.3-16.1) DW 11.4 (8.7-14.9) DW
Reference
a
11 11
Values are in mg element/kg fresh weight (FW) or dry weight (DW). a 1, Parsons, 1998; 2, Law et al., 1991; 3, Law et al., 1992; 4, Villa et al., 1993; 5, Law et al., 1996; 6, Frank et al., 1992; 7, Andrade et al., 2007; 8, Stockin et al., 2007; 9, Stavros et al., 2007; 10, Bryan et al., 2007; 11, Kannan et al., 2007; 12, Harper et al., 2007; 13, Kannan et al., 2006; 14, Yang et al., 2006; 15, Hung et al., 2007; 16, Kakuschke et al., 2008b; 17, Kakuschke et al., 2005; 18, Griesel et al., 2006; 19, Griesel et al., 2008; 20, Stavros et al., 2008a; 21, Gray et al., 2008; 22, Agusa et al., 2008; 23, Carvalho et al., 2002; 24, Law et al., 2003.
In Europe, nickel is listed in European Commission List II (Dangerous Substances Directive) and regulated through the Council of European Communities because of its toxicity, persistence, and affinity for accumulation (Bubb and Lester, 1996). In Canada, nickel and its compounds are included in the Priority Substance List under the Canadian Environmental Protection Act (Hughes et al., 1994). The World Health Organization (WHO) classifies nickel compounds in Group 1 (human carcinogens) and metallic nickel in Group 2B (possible human carcinogen; USPHS, 1993a). The U.S. Environmental Protection Agency (USEPA) classifies nickel refinery dust and nickel subsulfide as Group A human carcinogens (USPHS, 1993a), and nickel oxides and nickel halides as Class W compounds, that is, compounds having moderate retention in the lungs and a clearance rate from the lungs of several weeks (USEPA, 1980a). Some nickel compounds are weakly mutagenic, but most of the evidence is inconclusive or negative (Eisler, 2000f). No birth defects of nickel compounds occur in mammals by way of inhalation or ingestion, except from nickel carbonyl—the most hazardous form of nickel. Inhaled nickel carbonyl results in elevated nickel concentrations in lung, brain, kidney, liver, and adrenals (Eisler, 2000f). Nickel crosses the placental barrier (USPHS, 1993a); nickel concentrations in whole blood, plasma, serum, and urine, provide good indices of nickel exposure (Sigel and Sigel, 1988). Toxic and carcinogenic effects of nickel compounds are associated with nickel-mediated oxidation damage to DNA and proteins and to inhibition of cellular antioxidant defenses (Rodriguez et al., 1996). Lymphocyte proliferation in newborn harbor seals, P. vitulina, is stimulated when cells are incubated in 5.0 mg Ni/L for 5 days (Kakuschke et al., 2008a). Only nickel and molybdenum produced lymphocyte stimulation; inhibition was recorded by beryllium (50.0 mg/L), cadmium (6.2 mg/L), various mercurials (0.5 mg/L), and tin (25.0 mg/L). No effect on lymphocyte proliferation was recorded when cells were incubated for 5 days in silver (5.0 mg/L), aluminum (40.0 mg/L), gold (6.2 mg/L), cobalt (10.0 mg/L), chromium (5.0 mg/L), copper (0.5 mg/L), lead (25.0 mg/L), palladium (6.2 mg/L), phenylmercury
444 Chapter 6 (0.5 mg/L), platinum (6.0 mg/L), tin (25.0 mg/L), and titanium (50.0 mg/L); these findings were useful in providing immunological data on developing seals (Kakuschke et al., 2008a).
6.23 Palladium Blood from seven captive harbor seals, P. vitulina, contained a maximum of 0.0004 mg Pd/kg FW (Kakuschke et al., 2008b); free-ranging harbor seals from the North Sea had a maximum of 0.006 mg Pd/kg FW (Kakuschke et al., 2005). Blood from harbor seals captured in the Wadden Sea in 2004–2005 contained 0.00024–0.00041 mg Pd/kg FW (Griesel et al., 2008).
6.24 Platinum Blood of captive harbor seals, P. vitulina, held in Germany contained a maximum of 0.0003 mg Pt/kg FW (Kakuschke et al., 2008b); free-ranging harbor seals from the North Sea contained a maximum of 0.008 mg Pt/kg FW (Kakuschke et al., 2005). Blood from harbor seals captured in the Wadden Sea in 2004–2005 contained <0.00004–0.0083 mg Pt/kg FW (Griesel et al., 2008).
6.25 Plutonium Accidental contamination of the marine environment in 1968 near Thule, Greenland, with radioplutonium has not resulted in significant accumulations in walruses, seals, seabirds, and fishes. The plutonium originating from the accident has been confined to bottom fauna with little risk to mammals consuming affected biota (Aarkrog, 1971, 1977). Plutonium-238 levels were about 2.5 times higher in muscle than in milk of lactating gray seals collected in the northeast Atlantic Ocean in 1987; for pups, 238Pu levels in liver were 2 times higher than muscle (Anderson et al., 1990). Similar findings were documented for 239 + 240 Pu (Anderson et al., 1990).
6.26 Polonium Polonium, as was true for lead, tends to concentrate in bony tissues. Radiopolonium-210 levels in bone of sperm whales taken during 1965 in Alaska were 5 times higher than in soft tissues (Holtzman, 1969). Naturally occurring 210Po concentrations in muscle, liver, and kidney tissues of Pacific walrus, O. rosmarus divergens and bearded seal, E. barbatus from Alaska in May 1996 were comparatively elevated when compared to 137Cs (max. 0.17 Bq/kg FW), with maximum concentrations of 189.0 Bq/kg FW of 210Po in walrus liver and 207.0 Bq/kg FW in seal liver (Hamilton et al., 2008); risks to human consumers of these tissues merits additional research.
Mammals 445 Bioconcentration values from seawater to walrus and seal tissues for 210Po were in the range of 20,000–208,000 (vs. <87.0 for 137Cs) (Hamilton et al., 2008).
6.27 Rubidium Rubidium concentrations are comparatively elevated in livers of nondiseased sea otters versus emaciated of infectious-diseased otters (Kannan et al., 2006; Table 6.8), in muscle and liver tissues of dolphins versus skin and fat (Agusa et al., 2008; Table 6.8), and in livers of polar bears (Kannan et al., 2007; Table 6.8). Blood of bottlenose dolphins, T. truncatus, from Sarasota Bay, Florida in 2002–2004 contains up to 0.78 mg Rb/kg FW; for skin, this was 1.47 mg Rb/kg FW (Bryan et al., 2007; Table 6.8). Rubidium concentrations in skin and blood were strongly and positively correlated; highest in blood during summer and lowest in winter; lower in blood of calves than in their mothers; and higher in skin of subadults and calves than in adults (Bryan et al., 2007).
6.28 Selenium The highest selenium concentration recorded was 1188.4 mg Se/kg FW in liver from a dolphin T. aduncus taken in South Australia (Lavery et al., 2008). Livers from adult seals and whales were comparatively rich in selenium, usually containing 61.6–170.6 mg Se/kg on a fresh weight basis and 79.0–260.0 mg/kg on a dry weight basis; however, liver selenium concentrations in dolphins from the Mediterranean Sea sometimes contained 960.0–2400.0 mg Se/kg DW and 424.0 mg/kg FW (Table 6.9). In general, liver selenium concentrations were higher in older animals (Lavery et al., 2008; Seixas et al., 2007), and strongly correlated with total mercury concentrations (Lavery et al., 2008; Storelli et al., 1998). The higher levels of selenium in liver of maternal females were not reflected in liver of new-born pups (Table 6.9). In gray whales and belugas, selenium concentrations were highest in liver, followed by epidermis, muscle, and kidney, in that order; however, in bowheads, this order was kidney, liver, epidermis, and muscle (Dehn et al., 2006b; Table 6.9). Renal selenium concentrations in bowheads taken from Alaskan waters tended to be higher in autumn than other seasons (Rosa et al., 2008). Elevated selenium concentrations were measured in tissues and diet of two captive California sea lions (Z. californianus) that died shortly after performing at a show in 1988. Selenium concentrations, in mg/kg FW, were 49.0 and 88.0 in liver, 42.0 and 47.0 in kidney, and 5.1 and 5.2 in blood. Selenium concentrations in their fish diet was 2.5 mg/kg FW, and in thawed fish fluids 45.0 mg/kg FW (Alexander et al., 1990). Seafood products designated for human consumption—including edible portions of marine mammals—should not contain more than 2.0 mg Se/kg FW (Bebbington et al., 1977), although this requires verification.
446 Chapter 6 Table 6.9: Selenium Concentrations in Field Collections of Mammals Organism Alaska; liver Bowhead whale, Balaena mysticetus Beluga, Delphinapterus leucas Bearded seal, Erignathus barbatus Ringed seal, Phoca hispida Australia; 1995-1996; stranded; liver vs. kidney Bottlenose dolphin, Tursiops truncatus aduncus Adult female Female calf Common dolphin, Delphinus delphis; juvenile Melon-headed whale, Peponocephala electra; adults Bowhead, Balaena mysticetus; Barrow, Alaska; 1983-2001 Liver Kidney Muscle Epidermis Minke whale, Balaenoptera rostrata; Antarctic Ocean; 1990-1991; urine
Concentration
0.5-1.2 FW 3.0-75.0 FW; usually <20.0 FW 0.5-5.3 FW 1.2-5.7 FW
Reference
6 6 6 6
12.0 FW vs. 3.4 FW 1.5 FW vs. 1.9 FW 1.6 FW vs. 2.6 FW
44 44 44
6.2-58.0 FW vs. 3.4-4.0 FW
44
1.3 1.5 0.2 0.7
14-16, 37 14-16, 37 14-16 14-16
(0.06-4.2) FW (0.21-3.2) FW (0.08-0.77) FW (0.2-1.4) FW
1.5 FW
1
Cetaceans; 6 spp.; Ligurian Sea; found stranded; 1990-2004 Muscle Kidney Liver Brain
0.9-96.9 DW 4.5-101.0 DW 3.2-1408.0 DW 2.6-96.7 DW
34 34 34 34
Northern fur seal, Callorhinus ursinus Liver Kidney
140.0 DW 24.0 DW
42 42
21.0-37.6 FW
29
31.3 (0.9-113.2) FW 5.0 (1.7-10.8) FW 0.4 (0.2-1.3) FW 8.0 (2.7-32.9) FW
14, 14, 14, 14,
Hooded seal, Cystophora cristata; liver; Greenland; March, 1984 Beluga, Delphinapterus leucas; Point Lay/Wainwright, Alaska; 1992-1999 Liver Kidney Muscle Epidermis
a
16, 16, 16, 16,
17 17 17 17 (Continues)
Mammals 447 Table 6.9:
Cont’d
Organism
Concentration
Reference
Common dolphin, Delphinus sp.; December 2004; found stranded; New Zealand Blubber Liver Kidney
Max. 20.0 FW Max. 39.0 FW Max. 6.4 FW
20 20 20
Dolphins; 3 spp.; South Australia; 1988-2004; liver Common dolphin, Delphinus delphis Bottlenose dolphin, Tursiops truncates Dolphin, Tursiops aduncus
14.1 FW; max. 63.4 FW 70.1 FW; max. 253.4 FW 178.9 FW; max. 1188.4 FW
33 33 33
Gray whale, Eschrichtius robustus; Lorino/Lavrentiya, Russia; 2001 Liver Kidney Muscle Epidermis
0.8 1.5 0.2 3.8
14 14 14 14
Pilot whale, Globicephala macrorhynchus Blubber Liver Kidney
0.77-1.35 FW 22.8-61.6 FW 3.0-10.0 FW
Risso’s dolphin, Grampus griseus Liver Kidney
54.0 DW 21.0 DW
Gray seal, Halichoerus grypus Maternal females Liver Bile Pups; liver Juveniles found dead Brain Muscle Spleen Kidney Liver Adults found dead Brain Muscle Kidney Liver
(0.3-1.3) FW (0.5-2.2) FW (0.1-0.3) FW (0.9-10.6) FW
a
4 4 4 42 42
8.6-88.0 FW 0.22-2.4 FW 1.4-2.1 FW
2 2 2
0.4-0.7 FW 1.0-2.5 FW 1.1-2.5 FW 1.2-5.6 FW 2.0-29.0 FW
2 2 2 2 2
0.50-4.2 FW 1.2 FW 7.1 FW 8.1-130.0 FW
2 2 2 2 (Continues)
448 Chapter 6 Table 6.9: Organism Greenland; 1975-1991 Seals; 2 spp. Kidney Liver Muscle Whales; 4 spp. Kidney Liver Muscle Skin Polar bear, Ursus maritimus Kidney Liver Muscle Greenland Sea; March-April 1999; reproductively active females during suckling period Harp seal, Pagophilus groenlandicus Muscle Liver Kidney Hooded seal, Cystophora cristata Muscle Liver Kidney Hong Kong; found stranded; stomach contents Humpback dolphin, Sousa chinensis Finless porpoise, Neophocaena phocaenoides Leopard seal, Hydrurga leptonyx; serum Italy; 1987-1989; found stranded Striped dolphin, Stenella coeruleoalba Brain Kidney Liver Muscle Bottlenose dolphin, Tursiops truncates Brain Kidney
Cont’d
Concentration
Reference
2.6-4.2 FW 1.0-7.6 FW 0.2-0.4 FW
12 12 12
1.5-6.3 FW 1.7-5.0 FW Max. 0.2 FW Max. 47.9 FW
12 12 12 12
6.0-11.6 FW 3.1-9.1 FW <0.2-1.3 FW
12 12 12
0.27 FW 1.8 FW 1.7 FW
21 21 21
0.26 FW 11.0 (2.6-44.0) FW 2.2 (1.1-4.0) FW
21 21 21
0.32 (0.08-0.5) FW 0.35 (0.1-1.0) FW
28 28
0.61 FW
39
9.0 (5.0-36.0) DW 25.0 (50.0-101.0) DW 106.0 (2.0-960.0) DW (10.0-55.0) DW
8 8 8 8
4.9 (3.3-5.2) DW 53.0 (21.0-186.0) DW
8 8
a
(Continues)
Mammals 449 Table 6.9: Organism Liver Muscle
Concentration 139.0 (2.0-2400.0) DW Max. 48.0 DW
Weddell seal, Leptonychotes weddelli; Antarctica; summers 2002-2003 Serum Hair
0.23 DW 3.1 DW
Norway; 1989-1990; 4 spp.; kidney vs. liver; maximum values Gray seal, Halichoerus grypus Ringed seal, Phoca hispida Harp seal, Phoca groenlandica Harbor seal, Phoca vitulina
4.1 5.7 7.2 7.7
Melon-headed whale, Peponocephala electra; Japan; March 2006; found stranded Liver Kidney Muscle Lung
48.7 FW 5.2 FW 2.9 FW 3.3 FW
Ringed seal, Phoca hispida Muscle Liver Kidney Liver Aston Bay Barrow Strait Pond Inlet W. Victoria Island Saimaa ringed seal, Phoca hispida saimensis Muscle Liver Kidney Blubber Harbor porpoise, Phocoena phocoena Ages 1-5 years; kidney vs. liver Western Europe; 1997-2003; found stranded Liver; adults Fetus vs. mother; liver
Cont’d
FW FW FW FW
vs. vs. vs. vs.
Reference
a
8 8
39 39
21.8 FW 3.7 FW 3.4 FW 7.8 FW
10 10 10 10
40 40 40 40
0.44-0.92 FW 6.1-110.0 FW 2.5-3.3 FW
3 3 3
16.3 FW 9.4 FW 4.1 FW 15.2 FW
1 1 1 1
0.24-2.8 FW 29.0-170.0 FW 0.34-3.0 FW 0.06-0.11 FW
3 3 3 3
0.6-8.6 FW vs. 0.7-14.2 FW
11
11.0 (0.3-105.0) FW
23
(Continues)
450 Chapter 6 Table 6.9: Organism Irish Sea S. Ireland Harbor seal, Phoca vitulina Juveniles vs. adults Kidney Liver Brain Labrador and Newfoundland; body length 212-402 cm Muscle Liver vs. kidney 212 cm 301 cm 304 cm 335 cm 402 cm Harbor seal, Phoca vitulina; blood Captive animals Wild; North Sea Wadden Sea; 2004-2005; German site vs. Danish site Dall’s porpoise, Phocoenoides dalli Japan; liver Japan; February 2006; harpooned 6-year-old male Liver Kidney Muscle Skin Bone Heart Lung Intestine Spleen Pancreas Diaphragm Blubber Cerebrum Stomach
Cont’d
Concentration
Reference
0.6 FW vs. 36.8 FW 0.9 FW vs. 23.8 FW
23 23
0.6 (0.0-1.3) FW vs. 3.5 (1.9-7.3) FW 2.8 (2.6-6.5) FW vs. 109.0 FW; Max. 409.0 FW 1.1 (0.0-7.4) FW vs. 3.7 (1.5-8.2) FW
a
9 9 9
0.40-0.61 FW
18
5.5 FW vs. 2.1 FW 2.8 FW vs. 3.6 FW 14.7 FW vs. 3.6 FW 5.3 FW vs. 3.8 FW 19.8 FW vs. 5.0 FW
18 18 18 18 18
0.78-1.83 FW 0.5-2.9 FW 0.90 (0.59-2.3) FW vs. 0.94 (0.52-1.37) FW
31 32 35
15.0 (7.5-33.0) DW
25 25
7.7 FW 7.7 FW 1.0 FW 78.1 FW 4.4 FW 2.6 FW 3.3 FW 1.5 FW 1.9 FW 1.8 FW 1.4 FW 3.1 FW 1.0 FW 3.4 FW
27 27 27 27 27 27 27 27 27 27 27 27 27 27 (Continues)
Mammals 451 Table 6.9: Organism La Plata river dolphin, Pontoporia blainvillei Liver Kidney Brazil; 2003-2004; southeast Brazil vs. south Brazil Liver Kidney Portugal; 1998-2002 Common dolphin, Delphinus delphis Muscle Liver Skin Fat Bottlenose dolphin, Tursiops truncates Muscle Liver Skin Fat Striped dolphin, Stenella coeruleoalba; South Adriatic Sea; found beached February-April 1991 and June-September 1995 Liver Muscle Striped dolphin; Japan; 1979 Liver Fetus Juvenile Adult Adult male vs. female fetus Blubber Kidney Liver Muscle Florida manatee, Trichechus manatus latirostris; January 2007; Crystal River, Florida Blood Skin
Cont’d
Concentration
Reference
3.2-6.5 DW 7.0-7.8 DW
13, 19 13, 19
(0.8-9.1) DW vs. (3.8-54.3) DW (1.5-11.6) DW vs. (6.8-12.3) DW
38 38
3.1 (0.8-14.7) DW 25.0 (1.0-66.0) DW 65.0 (33.0-98.0) DW 4.2 (2.2-7.2) DW
43 43 43 43
2.5 (1.2-3.7) DW 58.0 (12.0-91.0) DW 60.0 (55.0-66.0) DW 2.1 (1.1-3.3) DW
43 43 43 43
141.6 (0.9-424.0) FW 4.5 (1.1-7.8) FW
26 26
16.0 DW 27.0 DW 190.0 DW
41 41 41
16.0 DW vs. 3.2 DW 23.0 DW vs. 0.8 DW 250.0 DW vs.16.0 DW 12.0 DW vs. 4.5 DW
41 41 41 41
0.25 (0.15-0.45) FW 0.72 (0.44-1.6) FW
36 36
a
(Continues)
452 Chapter 6 Table 6.9: Organism Bottlenose dolphin; Tursiops truncatus; Skin; South Carolina; 2003-2005 Juvenile male Adult male Juvenile female Adult female Pregnant female Sarasota Bay, Florida; 2002-2004 Blood Skin Blood; summers 2003-2005; South Carolina vs. Florida California sea lion, Zalophus californianus Mothers with premature pups vs. mothers with normal pups Liver Kidney Pups born prematurely vs. normal pups Liver Kidney
Cont’d
Concentration
24.0 24.0 25.6 24.7 22.1
DW; DW; DW; DW; DW;
max. max. max. max. max.
Reference
36.3 38.8 43.9 35.1 38.7
DW DW DW DW DW
a
22 22 22 22 22
0.72 FW; max. 1.1 FW 5.5 FW; max. 9.6 FW 0.78 FW vs. 0.62 FW
24 24 30
79.0 DW vs. 260.0 DW 12.1 DW vs. 22.0 DW
5 5
2.9 DW vs. 4.1 DW 3.7 DW vs. 6.1 DW
5 5
Values are in mg Se/kg fresh weight (FW) or dry weight (DW). a 1, Smith and Armstrong, 1978; 2, van de Ven et al., 1979; 3, Kari and Kauranen, 1978; 4, Stoneburner, 1978; 5, Martin et al., 1976; 6, Mackey et al., 1996; 7, Hasunuma et al., 1993; 8, Leonzio et al., 1992; 9, Reijnders, 1980; 10, Skaare et al., 1994; 11, Teigen et al., 1993; 12, Dietz et al., 1996; 13, Seixas et al., 2007; 14, Dehn et al., 2006b; 15, Bratton et al., 1997; 16, Woshner et al., 2001; 17, Tarpley et al., 1995; 18, Veinott and Sjare, 2006; 19, Seixas et al., 2007; 20, Stockin et al., 2007; 21, Brunborg et al., 2006; 22, Stavros et al., 2007; 23, Lahaye et al., 2007; 24, Bryan et al., 2007; 25, Yang et al., 2007; 26, Storelli et al., 1998; 27, Yang et al., 2006; 28, Hung et al., 2007; 29, Nielsen and Dietz, 1990; 30, Stavros et al., 2008b; 31, Kakuschke et al., 2008b; 32, Griesel et al., 2006; 33, Lavery et al., 2008; 34, Capelli et al., 2008; 35, Griesel et al., 2008; 36, Stavros et al., 2008a; 37, Rosa et al., 2008; 38, Seixas et al., 2008; 39, Gray et al., 2008; 40, Endo et al., 2008; 41, Agusa et al., 2008; 42, Arai et al., 2004; 43, Carvalho et al., 2002; 44, Law et al., 2003.
Urine is a major excretory route for selenium in marine mammals. Urine in minke whales (Balaenoptera acutorostrata) contains 1.5 mg Se/L, or about 30 times more selenium than human urine (Hasunuma et al., 1993). There are at least five selenium components in urine of minke whales, including trimethylselonium ion; the significance of this observation is imperfectly understood (Hasunuma et al., 1993). A significant positive linear relation exists between the molar concentrations of selenium and mercury in livers of dolphins, Pontoporia spp. (Seixas et al., 2007); similar data exists for other marine mammals (Capelli et al., 2000, 2008; Das et al., 2000; Dehn et al., 2006b; Dietz et al., 2000; Endo et al., 2002; Koeman et al., 1973, 1975; Lavery et al., 2008; Meador
Mammals 453 et al., 1999; Palmisano et al., 1995; Wagemann et al., 1998). This correlation may reflect a causal relation between mercury and selenium in marine mammal tissues as mercuric selenide (HgSe); HgSe is an end product of mercury demethylation in tissues containing equimolar concentrations of total mercury and total selenium (Wagemann et al., 1998). Since selenium has a protective effect against the toxic action of mercury—as shown in experiments with rats and quail—it may have a similar effect in marine mammals. It is suggested that mercury and selenium occur together in animal tissues and are associated to proteins via sulfur. The observation that most of the mercury in seal liver and brain was tightly bound and could not be recovered in the form of methylmercury may support this suggestion. Fish in the diet is usually the main source of selenium for HgSe (Monteiro-Neto et al., 2003). As was true for mercury, a significant positive relation was documented between molar concentrations of selenium and cadmium in livers of Pontoporia spp. (Seixas et al., 2007); similar data are reported for pilot whales (Caurant et al., 1994), striped dolphins (Monaci et al., 1998), and bottlenose dolphins (Meador et al., 1999).
6.29 Silver Silver found in the body of mammals, including humans, has no known biological function and is suspected of being a contaminant (Smith and Carson, 1977). A major source of dietary silver in the human diet is seafood captured from areas near sewage outfalls (USPHS, 1990). Silver in mammalian tissues is usually present at low or nondetectable concentrations (Klaassen et al., 1986). Silver burdens in three species of seals collected in the Antarctic region during 1989 were highest in liver (1.55 mg/kg DW) and lowest in muscle (0.01 mg/kg DW); intermediate values were in kidney (0.29 mg/kg DW) and stomach contents (0.24 mg/kg DW; Szefer et al., 1993; Table 6.10). However, an exceptionally high mean value of 12.8 mg Ag/kg FW liver (max. 50.7) was reported in belugas, D. leucas taken in Alaska between 1992 and 1999; hepatic silver and mercury concentrations were positively correlated and this may account, in part, for the elevated silver burden (Dehn et al., 2006b). The mean concentration of silver in liver from normal female California sea lions, Z. californianus, having normal pups was 0.5 mg/kg DW. Mothers giving birth to premature pups had only 0.4 mg Ag/kg DW liver (Martin et al., 1976). Zalophus mothers delivering premature pups usually had lower concentrations in liver of silver, cadmium, copper, manganese, mercury, and zinc than mothers delivering normal pups (Martin et al., 1976). Silver concentrations in tissues of Antarctic seals were also related to, and possibly governed by, concentrations of other metals (Szefer et al., 1994). For example, in muscle tissues of Antarctic region seals, silver concentrations were inversely correlated with zinc; in liver, silver was positively correlated with nickel, copper, and zinc; and in kidney, correlations between silver and zinc, and between silver and cadmium were negative (Szefer et al., 1994). In terrestrial mammals, silver usually interacts antagonistically with selenium, copper, and vitamin C (Eisler, 2000g).
454 Chapter 6 Table 6.10: Silver, Strontium, Tin, and Vanadium Concentrations in Field Collections of Mammals Element and Organism
Concentration
Reference
a
Silver Alaska; Barrow; 1998-2001; liver Bowhead whale, Balaena mysticetus Beluga, Delphinapterus leucas Bearded seal, Erignathus barbatus Gray whale, Eschrichtius robustus Ringed seal, Phoca hispida; Holman, Canada vs. Barrow, Alaska Spotted seal, Phoca largha Polar bear, Ursus maritimus Antarctica; February-March 1989; pinnipeds; 3 spp. Leopard seal, Hydrurga leptonyx Kidney Liver Muscle Stomach contents Weddell seal, Leptonychotes weddelli Kidney Liver Muscle Crabeater seal, Lobodon carcinophagus Kidney Liver Muscle Australia; 1995-1996; stranded; liver vs. kidney Bottlenose dolphin, Tursiops truncatus aduncus Adult female Female calf Common dolphin, Delphinus delphis; juvenile Melon-headed whale, Peponocephala electra; adults Bowhead whale, Balaena mysticetus; Barrow, Alaska; 1983-2001 Liver Kidney Muscle Epidermis
0.13 (<0.01-2.4) FW 12.8 (1.8-50.7) FW 0.34 (<0.01-1.13) FW 0.1 (<0.01-0.67) FW 0.55 (0.05-2.74) FW vs. 0.11 (0.05-0.69) FW 0.08 (0.01-0.13) FW 0.16 (0.05-0.35) FW
0.15 0.99 0.01 0.22
DW; max. 0.24 DW DW; max. 1.55 DW DW; max. 0.017 DW (0.20-0.24) DW
10 10 10 10 10 10 10
1 1 1 1
0.10 DW; max. 0.29 DW 0.73 DW; max. 0.94 DW Max. 0.012 DW
1 1 1
0.06 DW; max. 0.17 DW 0.81 DW; max. 1.36 DW 0.01 DW; max. 0.022 DW
1 1 1
0.5 FW vs. 0.14 FW <0.01 FW vs. 0.03 FW 0.05 FW vs. <0.01 FW
34 34 34
0.5-1.6 FW vs. 0.02-0.15 FW
34
0.14 (0.002-2.4) FW 0.01 (0.0002-0.06) FW 0.003 (0.001-0.01) FW 0.003 (0.002-0.003) FW
5-7, 5-7, 3-5, 3-5,
29 29 7, 9 7, 9 (Continues)
Mammals 455 Table 6.10:
Cont’d
Element and Organism
Concentration
Beluga, Delphinapterus leucas; Point Lay/Wainwright, Alaska; 1992-1999 Liver Kidney Muscle Epidermis
12.8 0.05 0.01 0.01
Common dolphin, Delphinus sp.; found stranded; December 2004; New Zealand Blubber Kidney Liver
<0.02 FW Max. 0.03 FW Max. 1.2 FW
Southern sea otter, Enhydra lutris nereis; adult females; found dead along California coast; 1992-2002; liver Gray whale, Eschrichtius robustus; Lorino/Lavrentiya, Russia; 2001 Liver Kidney Muscle Epidermis Hong Kong; found stranded; stomach contents Humpback dolphin, Sousa chinensis Finless porpoise, Neophocaena phocaenoides Dall’s porpoise, Phocoenoides dalli; Japan; February 2006; harpooned; 6-year-old male Liver Cerebrum Kidney, pancreas, stomach Muscle, skin, bone, heart, lung, intestine, spleen, diaphragm, blubber Striped dolphin, Stenella coeruleoalba; Japan; 1979 Liver Fetus Juvenile Adult
(1.8-51.7) FW (0.01-0.15) FW (0.01-0.01) FW (0.01-0.01) FW
1.6 (0.2-5.8) DW
Reference
5, 5, 5, 5,
7, 7, 7, 7,
a
8 8 8 8
8 8 8 16
0.11 (0.004-0.67) FW 0.01 (0.003-0.01) FW 0.004 (0.003-0.004) FW 0.01 (0.003-0.01) FW
5 5 5 5
0.007 (0.003-0.018) FW 0.01 (0.003-0.042) FW
20 20
1.75 FW 0.10 FW 0.02-0.03 FW <0.005 FW
18 18 18 18
1.0 DW 2.0 DW 10.0 DW
31 31 31 (Continues)
456 Chapter 6 Table 6.10: Cont’d Element and Organism Adult male vs. female fetus Blubber Kidney Liver Muscle Polar bear, Ursus maritimus Northwest Territories, Canada; 1984; liver Alaska; liver; 1993-2002 Beaufort Sea area Chukchi Sea area
Concentration 0.02 DW vs. <0.001 DW 0.24 DW vs. 0.004 DW 7.6 DW vs. 1.0 DW 0.004 DW vs. <0.001 DW 0.21-0.54 DW
Reference
a
31 31 31 31 2
0.18 (0.1-0.3) DW 0.38 (0.16-0.72) DW
14 14
Dugong, Dugong dugon; Australia; tusk
1717.0 (1294.0-2155.0) FW
15
Southern sea otter, Enhydra lutris nereis; adult females; found dead along California coast; 1992-2002; liver Non-diseased Emaciated Infectious-diseased
1.8 (0.1-19.0) DW 1.7 (0.2-22.9) DW 0.9 (0.08-8.3) DW
16 16 16
297.0 (148.0-595.0) DW
32
Harbor seal, Phoca vitulina; blood Captive animals Wild; North Sea Wadden Sea; 2004-2005; German site vs. Danish site
0.028-0.070 FW 0.017-0.095 FW 0.04 (0.03-0.06) FW vs. 0.05 (0.03-0.07) FW
22 24 27
Dall’s porpoise, Phocoenoides dalli; Japan; February 2006; harpooned male Liver Kidney Muscle Skin Bone Heart Lung Intestine Spleen Pancreas
0.06 FW 0.14 FW 0.02 FW 0.56 FW 217.0 FW 0.05 FW 0.19 FW 0.80 FW 0.06 FW 0.11 FW
18 18 18 18 18 18 18 18 18 18
Strontium
Stellar sea lion, Eumetopias jubatus; teeth; North Pacific; 1968-1999
(Continues)
Mammals 457 Table 6.10: Element and Organism Diaphragm Blubber Cerebrum Stomach Portugal; 1998-2002 Common dolphin, Delphinus delphis Muscle Liver Skin Fat Bottlenose dolphin, Tursiops truncatus Muscle Liver Skin Fat Striped dolphin; Japan; 1979 Liver Fetus Juvenile Adult Adult male vs. female fetus Blubber Kidney Liver Muscle
Cont’d
Concentration 0.11 0.03 0.04 0.10
1.4 3.4 2.8 2.9
Reference
FW FW FW FW
18 18 18 18
(0.7-4.1) DW (0.7-14.1) DW (0.9-8.1) DW (1.8-4.8) DW
33 33 33 33
1.3 (0.0-1.9) DW 1.0 (1.1-2.7) DW 4.6 (1.4-7.8) DW <1.1 DW
33 33 33 33
0.04 DW 1.9 DW 2.3 DW
31 31 31
0.43 0.78 0.24 0.89
DW DW DW DW
a
vs. vs. vs. vs.
0.01 0.05 0.04 0.02
DW DW DW DW
Bottlenose dolphin, Tursiops truncatus Sarasota Bay, Florida; 2002-2004 Blood Skin
0.08 FW; max. 0.12 FW 0.17 FW; max. 0.25 FW
13 13
Polar bear, Ursus maritimus; liver; Alaska; 1993-2002 Beaufort Sea area Chukchi Sea area
0.14 DW 0.16 DW
14 14
Tin Common dolphin, Delphinus sp.; December 2004; New Zealand; found stranded Blubber Kidney Liver
Max. 0.06 FW Max. 0.06 FW Max. 0.09 FW
8 8 8 (Continues)
458 Chapter 6 Table 6.10: Cont’d Element and Organism Dolphins; 7 spp; Thailand; found stranded; 1997-2003; total butyltins vs. total phenyltins Kidney Muscle Lung Blubber Heart Liver Dugong, Dugong dugon; found dead; coastal areas of Thailand; 1998-2003; total butyltins vs. total phenyltins Blubber Heart Kidney Liver Lung Muscle Sea otter, Enhydra lutris; found dead; liver; 1992-2002 Total tins vs. organotins California Kamchatka Alaska Washington
Concentration
(0.034-0.480) FW vs. (<0.001-0.014) FW (0.016-0.096) FW vs. (<0.001-0.015) FW (0.025-0.095) FW vs. (<0.001-0.012) FW (0.017-0.161) FW vs. (<0.001-0.062) FW (0.019-0.136) FW vs. (<0.001-0.062) FW 0.283 (0.084-1.15) FW vs. 0.005 (0.001-0.019) FW
(<0.014-7.48) FW vs. (<0.001-0.030) FW (0.020-3.36) FW vs. (<0.001-0.009) FW (0.015-14.47) FW vs. (<0.001-0.013) FW (0.017-2.89) FW vs. (<0.001-0.015) FW (0.020-2.81) FW vs. (<0.001-0.015) FW (0.024-9.91) FW vs. (<0.001-0.029) FW
1.3 (0.09-6.0) DW vs. 0.68 (0.03-4.1) DW 0.61 (0.49-0.76) DW vs. 0.036 (0.018-0.080) DW 0.41 (0.036-0.86) DW vs. 0.036 (0.018-0.08) DW 0.14 (0.06-0.27) DW vs. 0.21 (0.16-0.25) DW
Reference
a
26 26 26 26 26 26
11 11 11 11 11 11
21 21 21 21 (Continues)
Mammals 459 Table 6.10: Element and Organism California; infectious diseased vs. noninfectious Butyltins
Cont’d
Concentration
Reference
0.68 (0.03-4.1) DW vs. 0.23 (0.02-0.79) DW 0.0014 (<0.0002-0.005) DW vs. 0.001 (<0.0002-0.006) DW 0.006 (<0.0009-0.002) DW vs. 0.0001 (0.0003-0.007) DW 0.68 (0.034-4.1) DW vs. 0.24 (0.21-0.79) DW 1.3 (0.09-6.0) DW vs. 0.29 (0.08-0.86) DW
21
Southern sea otter;Enhydra lutris nereis; adult females found dead along California coast; 1992-2002; liver
1.0 (0.08-9.9) DW
16
Weddell seal, Leptonychotes weddelli; serum vs. hair
<0.001 DW vs. 1.4 DW
30
Phenyltins
Octyltins
Total organotins Total tin
Killer whale, Orcinus orca; Hokkaido, Japan; February 2005; dead on collection Adults; liver Tributyltin Dibutyltin Monobutyltin Total phenyltins Calves; liver Tributyltin Monobutyltin Dibutyltin Total phenyltins Adults; total butyltins vs. total phenyltins Blubber Liver Lung Muscle
21
21
21 21
0.020 (0.003-0.062) FW 0.210 (0.008-0.650) FW 0.040 (<0.003-0.084) FW Max. 0.0009 FW
4 4 4 4
(0.004-0.007) FW <0.003 FW (0.008-0.016) FW Max. 0.0009 FW
4 4 4 4
0.037-0.090 FW vs. <0.001-0.058 FW 0.385-0.676 FW vs. <0.001-0.014 FW 0.015 FW vs. 0.007 FW 0.026-0.053 FW vs. <0.001-0.004 FW
a
25 25 25 25 (Continues)
460 Chapter 6 Table 6.10: Cont’d Element and Organism Harbor seal, Phoca vitulina All tissues Blood Captive animals Wild; North Sea Wadden Sea; 2004-2005 Dall’s porpoise, Phocoenoides dalli Sanriku cost of Japan; 2006; harpooned 6-year-old male; total butyltins Liver Kidney Muscle Skin Bone Heart Lung Intestine Pancreas Diaphragm Cerebrum Stomach Blubber Mother vs. fetus; Japan; May 2001; harpooned; total butyltins Liver Muscle Blubber Skin Lung Blood Brain Bone Kidney Stomach Heart Intestine Diaphragm Placenta Florida manatee, Trichechus manatus latirostris; 2007; Crystal River, Florida Blood Skin
Concentration <0.1 FW
Reference
a
3
0.0004-0.003 FW Max. 0.0002 FW Max. 0.00047 FW
22 23 27
0.101 0.022 0.004 0.004 0.004 0.007 0.018 0.004 0.006 0.005 0.009 0.011 0.003
FW FW FW FW FW FW FW FW FW FW FW FW FW
18 18 18 18 18 18 18 18 18 18 18 18 18
0.193 0.014 0.007 0.014 0.055 0.004 0.005 0.006 0.038 0.003 0.015 0.003 0.004 0.001
FW FW FW FW FW FW FW FW FW FW FW FW FW FW
vs. vs. vs. vs. vs. vs. vs. vs. vs. vs. vs. vs. vs. vs.
0.0038 FW 0.0017 FW 0.0013 FW 0.0039 FW 0.0026 FW 0.0057 FW 0.0026 FW 0.0029 FW no data no data 0.0079 FW 0.0026 FW 0.0023 FW no data
0.002 FW; max. 0.003 FW 0.012 FW; max. 0.019 FW
19 19 19 19 19 19 19 19 19 19 19 19 19 19
28 28 (Continues)
Mammals 461 Table 6.10:
Cont’d
Element and Organism
Concentration
Bottlenose dolphin, Tursiops truncatus; skin; South Carolina; 2003-2005 Juvenile male Adult male Juvenile female Adult female Pregnant female
0.2 DW; max. 0.9 DW 0.44 DW; max. 1.6 DW 0.31 DW; max. 1.1 DW 0.14 DW; max. 0.6 DW 0.47 DW; max. 1.5 DW
Polar bear, Ursus maritimus; liver; Alaska; 1993-2002 Beaufort Sea area Chukchi Sea area
0.03 (0.02-0.07) DW 0.08 (0.01-0.09) DW
14 14
0.21 0.11 0.16 0.15 0.14 0.08 0.02
FW FW FW FW FW FW FW
vs. vs. vs. vs. vs. vs. vs.
0.87 0.24 0.03 0.20 0.06 0.03 0.25
FW FW FW FW FW FW FW
12 12 12 12 12 12
0.39 0.35 0.07 4.86 0.78 0.73 0.21
FW FW FW FW FW FW FW
vs. vs. vs. vs. vs. vs. vs.
0.16 0.26 0.11 1.14 0.02 0.76 0.41
FW FW FW FW FW FW FW
12 12 12 12 12 12 12
0.32 0.21 0.55 0.19
FW FW FW FW
vs. vs. vs. vs.
0.06 0.06 0.06 0.07
FW FW FW FW
12 12 12 12
0.14 FW vs. 0.41 FW 0.65 FW vs. 0.14 FW
12 12
0.11 FW vs. 0.41 FW
12
Whales; 5 spp.; found stranded on coasts of Thailand; females; 1997-2002; total butyltins vs. total phenyltins Brydes’ whale, Balaenoptera edeni Blubber Heart Kidney Liver Lung Muscle Stomach False killer whale, Pseudorca crassidens Blubber Heart Kidney Liver Lung Muscle Spleen Short-finned pilot whale, Globicephala macrorhynchus Blubber Heart Liver Muscle Pygmy sperm whale, Kogia breviceps Blubber Muscle Sperm whale, Physeter macrocephalus Blubber
Reference
a
9 9 9 9 9
(Continues)
462 Chapter 6 Table 6.10: Cont’d Element and Organism Liver Muscle
Concentration
Reference
0.28 FW vs. 0.11 FW 0.09 FW vs. 0.28 FW
12 12
0.38 DW vs. 0.38 DW 0.77 DW vs. 1.5 DW 2.5 DW vs. 1.8 DW 0.38 DW vs. no data (ND) 0.33 DW vs. ND 0.22 DW vs. ND 0.22 DW vs. 0.05 DW 0.34 DW vs. 0.13 DW 0.34 DW vs. ND 0.11 DW vs. 0.03 DW 0.06 DW vs. 0.12 DW <0.1 DW vs. <0.1 DW
16 16 16 16 16 16 16 16 16 16 16 16
Southern sea otter, Enhydra lutris nereis; adult females found dead along central California coast; 1992-2002; liver Nondiseased Emaciated Infectious-diseased
0.18 (0.03-0.53) DW 0.13 (0.04-0.73) DW 0.24 (0.03-2.8) DW
16 16 16
Hong Kong; found stranded; stomach contents Humpback dolphin Finless porpoise
0.17 (0.016-0.8) FW 0.09 (0.012-0.28) FW
20 20
Leopard seal, Hydrurga leptonyx; serum
0.06 FW
30
Weddell seal, Leptonychotes weddelli; serum vs. hair
0.1 DW vs. 4.2 DW
30
Harbor seal, Phoca vitulina; Wadden Sea; 2004-2005; blood
Max. 0.0013 FW
27
(0.026-2.6) FW
16
a
Vanadium Northern fur seal, Callorhinus ursinus; northeast coast of Japan; April 1990 and 1991; females; age 7 years vs. age 14 years Femur Hair Liver Adrenal Thyroid Amniotic fluid Pancreas Heart Ovary Uterus Kidney Spleen, gallbladder, lung, stomach, esophagus, lymph node, skin
Pinnipeds; 4 species; northern Pacific; liver Northern fur seal, Callorhinus ursinus; subadult males; July 1992; Pribilof Islands, Bering Sea
(Continues)
Mammals 463 Table 6.10: Element and Organism Stellar sea lion, Eumetopias jubatus; 1976-1985; Kodiak Island, Gulf of Alaska Ribbon seal, Phoca fasciata; Bering Sea; 1991 Harbor seal, Phoca vitulina; 1975-1978; Gulf of Alaska Dall’s porpoise, Phocoenoides dalli; Japan; 2006; 6-year-old male; harpooned Bone Liver Kidney, skin, intestine Muscle, heart, lung, spleen, pancreas, diaphragm, blubber, cerebrum, stomach Florida manatee; January 2007; Crystal River, Florida Blood Skin Striped dolphin; Japan; 1979 Liver Fetus Juvenile Adult Adult male vs. female fetus Blubber Kidney Liver Muscle Bottlenose dolphin, Tursiops truncatus Sarasota Bay, Florida; 2002-2004; skin
Cont’d
Concentration
Reference
(0.023-0.43) FW
16
(0.03-1.4) FW
16
(0.015-1.6) FW
16
0.26 FW 0.08 FW 0.01-0.02 FW 0.004-0.009 FW
18 18 18 18
0.003 FW; max. 0.004 FW 0.055 (0.029-0.100) FW
28 28
0.01 DW 0.12 DW 0.33 DW
31 31 31
0.03 DW vs. 0.04 DW 0.03 DW vs. 0.02 DW 0.17 DW vs. 0.01 DW 0.009 DW vs. 0.004 DW
31 31 31 31
0.005 FW; max. 0.012 FW
13
a
Values are in mg Ag/kg fresh weight (FW) or dry weight (DW). a 1, Szefer et al., 1994; 2, Braune et al., 1991; 3, Jenkins, 1980; 4, Kajiwara et al., 2006; 5, Dehn et al., 2006b; 6, Bratton et al., 1997; 7, Woshner et al., 2001; 8, Stockin et al., 2007; 9, Stavros et al., 2007; 10, Dehn et al., 2006a; 11, Harino et al., 2007b; 12, Harino et al., 2007a; 13, Bryan et al., 2007; 14, Kannan et al., 2007; 15, Edmonds et al., 1997; 16, Saeki et al., 1999; 17, Kannan et al., 2006; 18, Yang et al., 2006; 19, Yang and Miyazaki, 2006; 20, Hung et al., 2007; 21, Murata et al., 2008; 22, Kakuschke et al., 2008b; 23, Kakuschke et al., 2005; 24, Griesel et al., 2006; 25, Harino et al., 2008b; 26, Harino et al., 2008a; 27, Griesel et al., 2008; 28, Stavros et al., 2008a; 29, Rosa et al., 2008; 30, Gray et al., 2008; 31, Agusa et al., 2008; 32, Ando et al., 2005; 33, Carvalho et al., 2002; 34, Law et al., 2003.
464 Chapter 6 Marine mammals have comparatively low silver concentrations, with the highest value recorded (except for belugas) being 1.5 mg/kg DW liver (Table 6.10). By comparison, the highest silver concentration recorded in marine teleosts is 6.0 mg/kg DW in bone; for algae and macrophytes, this was 14.0 mg/kg DW whole plant; in annelids, 30.0 mg/kg DW whole worm; in bivalve mollusc soft parts, 185.0 mg/kg DW, and in gastropod molluscs, 320.0 mg/kg DW soft parts (Eisler, 2000g). No data were found on effects of silver compounds on marine mammals under controlled conditions. In studies with terrestrial mammals, however, all data indicate that silver is not mutagenic, carcinogenic, or teratogenic to tested animals by normal routes of exposure (Eisler, 2000g).
6.30 Strontium Strontium concentrations were grossly elevated in calcareous tissues when compared to soft tissues (Table 6.10). The highest strontium concentrations recorded were in tusk of a dugong (2155.0 mg Sr/kg DW), teeth from a stellar sea lion (595.0 mg Sr/kg DW), and bone from a Dall’s porpoise (217.0 mg Sr/kg FW; Table 6.10). Bottlenose dolphins, T. truncatus, contain up to 0.12 mg Sr/kg FW blood; for skin, this value was 0.25 mg Sr/kg FW (Table 6.10; Bryan et al., 2007). Fin whales, B. physalis, and harp seals, P. groenlandica, were examined for 90Sr concentrations. Of all tissues examined, whole blubber contained the highest radiostrontium content (Samuels et al., 1970).
6.31 Thallium Mean thallium concentrations in skin of bottlenose dolphins, T. truncatus, collected near Charleston, South Carolina, between 2003 and 2005, ranged from 0.08 mg Tl/kg DW for pregnant females to 0.41 mg Tl/kg DW for juvenile females; intermediate values were 0.24 in adult males, 0.33 in juvenile males, and 0.38 mg Tl/kg DW skin in female adults (Stavros et al., 2007). The highest thallium value recorded in skin of bottlenose dolphins was 1.0 mg/kg DW (Stavros et al., 2007). Mean thallium concentration in skin of the Florida manatee, T. manatus latirostris, from the Crystal River, Florida in January 2007 was 0.004 mg Tl/kg FW (max. 0.006 mg Tl/kg FW); thallium was below detection limits in blood (Stavros et al., 2008a). Thallium concentrations in blubber, kidney, liver, and muscle of striped dolphins from Japanese coastal waters ranged from 0.001 to 0.09 mg Tl/kg DW, being highest in livers of juveniles (Agusa et al., 2008). Livers from polar bears, U. maritimus, collected between 1993 and 2002 at various locations in Alaska averaged 0.002–0.003 mg Tl/kg DW (Kannan et al., 2007). Livers from adult female southern sea otters, E. lutris nereis, found dead along the central California coast between 1992 and 2002 contained 0.003 (<0.001–0.014) mg Tl/kg DW (Kannan et al., 2006).
Mammals 465
6.32 Tin The highest total inorganic tin concentrations recorded were 9.9 mg Sn/kg DW in livers of sea otters and 1.6 mg Sn/kg DW in skin of bottlenose dolphins (Table 6.10). Total tin concentrations in all tissues of the harbor seal, P. vitulina, were always less than 0.1 mg/kg on a fresh weight basis (Table 6.10). Elevated butyltin concentrations in livers of killer whales, O. orca, were significantly higher than total phenyltins (Table 6.10), and suggests extensive use of tributyltin antifouling paints in killer whale habitats (Kajiwara et al., 2006). The metabolism of tributyltins and triphenyltins in tissues and organs of killer whales, O. orca, is unclear. Until this is clarified, continued monitoring of organotins in killer whales is recommended in their tissues and organs, diets, and ambient seawater (Harino et al., 2008b). Total butyltins in organs and tissues of dugongs, D. dugon, found dead in coastal Thailand waters between 1998 and 2003 were comparatively elevated. Dugong blubber had 7.48 mg butyltin/kg FW, muscle 9.9 and kidney 14.5 mg/kg FW; for phenyltins, this range was <0.001–0.03 mg/kg FW (Table 6.10; Harino et al., 2007b). Dibutyltin and monobutyltin were usually the dominant butyltins, and triphenyltin was dominant among the phenyltins. Concentrations of all organotins in dugong liver decreased between 1998 and 2002 and may reflect decreasing use of organotin compounds in this area (Harino et al., 2007b). Mean concentrations of total butyltins in various whales found stranded along the Thailand coast between 1997 and 2002 ranged from 0.16 to 1.0 mg/kg FW; for total phenyltins this range was 0.02–1.14 mg/kg FW (Table 6.10; Harino et al., 2007a). Butyltins were highest in liver and lowest in lung; phenyltins were highest in liver and blubber and lowest in lung. Monobutyltins and dibutyltins were the dominant butyltins; triphenyltin was dominant in liver compounds. The unusually high concentrations of butyltins (4.86 mg/kg FW) and phenyltins (1.14 mg/kg FW) in livers of the false killer whale (Table 6.10) is attributed to their diet of squid and large fishes, which have comparatively elevated burdens of organotins (Harino et al., 2007a). Placental transfer of butyltin species in Dall’s porpoise (P. dalli), including monobutyltins (MBT), dibutyltins (DBT), and tributyltins (TBT) was demonstrated in a mother-fetus pair collected of coastal Japan in 2001 (Yang and Miyazaki 2006; Table 6.10). Maternal liver was a preferential site for total butyltin accumulation. The transfer rate of total butyltins was about 0.3% to a fetus of about age 6 months, although fetal liver was not a preferential accumulation site. The 100 kg-weight mother contained about 1.3 mg total butyltins (0.6 mg TBT, 0.48 mg DBT, 0.21 mg MBT); the 2.21 kg-weight fetus had 0.0042 mg total butyltins (0.001 mg TBT, 0.002 mg DBT, 0.001 mg MBT) (Yang and Miyazaki, 2006). Muscle was the most important reservoir of butyltins in Dall’s porpoise (Yang et al., 2006). Although total butyltin content in muscle was comparatively low (0.004 mg/kg FW;
466 Chapter 6 Table 6.10), it accounted for 43% of the whole body burden of total butyltins, of which 80% was tributyltin (Yang et al., 2006). Studies with small laboratory mammals suggest that organotin compounds are not mutagenic, teratogenic, or carcinogenic and that some organotins may retard the onset and growth of cancer in these animals, as judged by largely negative but incomplete evidence (Cardarelli et al., 1984a,b; Duncan, 1980; WHO, 1980). Similar data for marine mammals are lacking.
6.33 Titanium Skin from cetaceans captured near Corsica contained 0.6–1.1 mg Ti/kg FW (Viale, 1978). Blood of harbor seals, P. vitulina, from the Wadden Sea in 2004–2005 contained 0.001– 0.011 mg Ti/kg FW (Griesel et al., 2008).
6.34 Uranium Mean uranium concentrations in skin of bottlenose dolphins, T. truncatus, from South Carolina in the period 2003–2005 were highest in juvenile females (0.32 mg U/kg DW skin), lowest in pregnant females (0.13), and intermediate in adult males (0.20), adult females (0.25), and juvenile males (0.29 mg U/kg DW skin) (Stavros et al., 2007). The highest uranium value recorded in skin of bottlenose dolphins was 0.93 mg/kg DW in adult males (Stavros et al., 2007). Mean uranium concentration in skin of the Florida manatee, T. manatus latirostris from the Crystal River, Florida in January 2007 was 0.004 mg U/kg FW (max. 0.005 mg U/kg FW); uranium was below detection limits in blood (Stavros et al., 2008a).
6.35 Vanadium Vanadium tends to concentrate in liver of marine mammals. Among the highest vanadium concentrations of record were: 1.4 mg V/kg FW in liver of ribbon seal, Phoca fasciata; 1.6 mg/kg FW in liver of the harbor seal, P. vitulina; 2.5 mg V/kg DW in liver of the northern fur seal, Callorhinus ursinus; 2.8 mg/kg DW in liver of the southern sea otter, E. lutris nereis; and 4.2 mg V/kg DW in hair of the Weddell seal, L. weddelli (Table 6.10). Viale (1978) reports that vanadium concentrations in skin of cetaceans taken near Corsica ranged from 0.1 to 2.4 mg V/kg FW. Stavros et al. (2007) found that vanadium concentrations in skin of bottlenose dolphins, T. truncatus, from South Carolina in 2003–2005 never exceeded 1.3 mg V/kg DW. Bottlenose dolphins from Sarasota Bay, Florida collected in 2002–2004 had a maximum vanadium content in skin of only 0.012 FW (Table 6.10; Bryan et al., 2007). Bryan et al. (2007), in studies on vanadium in bottlenose dolphins, conclude that there is a strong correlation between skin and blood vanadium concentrations; that skin had comparatively
Mammals 467 elevated vanadium burdens; calves had lower vanadium burdens in blood than their mothers; and that blood vanadium levels were higher in winter than summer. In female northern fur seals, C. ursinus, comparatively high concentrations of vanadium were measured in liver, hair, and bone (Table 6.10). Of the total vanadium body burden in females, 90 percent was concentrated in these three tissues which together comprise less than 20 percent of the total body weight (Saeki et al., 1999). Liver vanadium content increased with increasing age in four species of pinnipeds at different rates, but in the case of northern fur seals accumulation was associated with increased vanadium retention in nuclei and mitochondria. Vanadium concentrations in liver were significantly correlated with mercury, silver, and selenium concentrations in stellar sea lions, harbor seals, and northern fur seals, and with iron in northern fur seals (Saeki et al., 1999), but the significance of this observation is not clear.
6.36 Zinc Zinc concentrations in tissues of marine mammals were usually less than 210.0 mg/kg DW (Eisler, 2000h), but ranged from 1.5 to 1385.0 mg/kg on a dry weight basis (Table 6.11). In one case, a value of 1101.0 mg/kg FW liver was recorded (Thompson, 1990), but this requires verification. In general, liver contained the highest values recorded (Table 6.11; Guinn and Kishore, 1972; Muir et al., 1988; Thompson, 1990; Wagemann, 1989). Zinc concentrations in Antarctic region seal hairs recovered from sediment cores representing the past 1500 years ranged from 16.0 to 116.0 mg/kg DW, with no clear temporal trend (Yin et al., 2006). Concentrations of zinc in tissues of the Stellar sea lion, Eumetopias jubata, were highest in liver and pancreas, followed by kidney, muscle, heart, spleen, and lung; this rank order is comparable to that in human tissues (Hamanaka et al., 1982). There is considerable variation among species in tissue zinc burdens; threefold differences are not uncommon for the same tissue in different species of marine mammals (Muir et al., 1988). Age and proximity to zinc sources may account for some of the variation. In bottlenose dolphins, T. truncatus, for example, zinc concentrations were significantly higher in juveniles than in adults (Beck et al., 1997). In California sea lions, renal zinc increased with increasing age (Harper et al., 2007). Marine mammals collected near heavily urbanized or industrialized areas or near zinc pollution point sources usually had elevated zinc concentrations in tissues when compared to conspecifics of similar age from relatively pristine environments (Eisler, 1984). However, zinc concentrations in tissues of the ringed seal, P. hispida, were the same in seals near a lead-zinc mine outfall and those from a distant reference site, although lead and selenium values were elevated in seals collected near the mine outfall (Wagemann, 1989). Of all groups of marine organisms examined—including plants and invertebrates—mammalian tissues consistently ranked among the lowest in mean zinc content (Eisler, 1980). Since zinc is considered essential to normal life processes in the marine environment, and is usually
468 Chapter 6 Table 6.11: Zinc Concentrations in Field Collections of Mammals Organism Australia; 1995-1996; stranded; liver vs. kidney Bottlenose dolphin, Tursiops truncatus aduncus Adult female Female calf Common dolphin, Delphinus delphis; juvenile Melon-headed whale, Peponocephala electra; adults Bowhead, Balaena mysticetus; Barrow, Alaska; 1983-2001 Liver Kidney Muscle Epidermis Northern fur seal, Callorhinus ursinus; hair; Japan Cetaceans; 6 spp.; Ligurian Sea; found stranded; 1990-2004 Muscle Kidney Liver Brain Hooded seal, Cystophora cristata; liver; Greenland; March 1984 Beluga whale, Delphinapterus leucas Muscle Liver Kidney Point Lay/Wainwright, Alaska; 1992-1999 Liver Kidney Muscle Epidermis Common dolphin, Delphinus sp.; New Zealand; December 2004; found stranded; max. values Blubber
a
Concentration
Reference
41.0 FW vs. 26.0 FW 144.0 FW vs. 40.0 FW 77.0 FW vs. 20.0 FW
52 52 52
22.0-47.0 FW vs. 27.0-30.0 FW
52
36.1 26.9 35.4 14.2
18-20, 46 18-20, 46 18-20 18-20
(7.0-135.1) FW (9.1-56.3) FW (9.5-74.1) FW (10.5-28.8) FW
186.0 DW
24
43.0-143.0 DW 77.0-140.0 DW 29.0-288.0 DW 33.0-64.0 DW
43 43 43 43
50.5-58.6 FW
37
20.0 FW 32.0 FW 29.5 FW
36.2 34.5 31.7 82.5
(18.5-53.2) FW (24.0-49.3) FW (16.3-66.7) FW (12.5-160.1) FW
100.0 FW
1 1 1
18, 18, 18, 18,
20, 20, 20, 20,
21 21 21 21
28 (Continues)
Mammals 469 Table 6.11: Organism
Cont’d
Concentration
Reference
37.0 FW 73.0 FW
28 28
62.2 (26.0-175.2) FW 40.2 (26.2-68.0) FW
42 42
93.4 (24.0-452.9) FW
42
95.0 FW
33
Southern sea otter, Enhydra lutris nereis; adult females; found dead along California coast; 1992-2002; liver Non-diseased Emaciated Infectious-diseased
202.0 (95.0-376.0) DW 248.0 (135.0-440.0) DW 239.0 (117.0-542.0) DW
34 34 34
Gray whale, Eschrichtius robustus; Lorino/Lavrentiya, Russia; 2001 Liver Kidney Muscle Epidermis
41.1 20.1 39.4 16.7
18 18 18 18
Stellar sea lion, Eumetopias jubata Brain Heart Kidney Liver Lung Muscle Pancreas Spleen Teeth
(33.0-51.0) DW (94.0-101.0) DW (99.0-102.0) DW (102.0-247.0) DW (42.0-69.0) DW (90.0-140.0) DW (78.0-262.0) DW (56.0-117.0) DW 109.0 (33.6-243.0) DW
9 9 9 9 9 9 9 9 50
Atlantic pilot whale, Globicephala melaena; Newfoundland, Canada; stranded; 1980-1982 Blubber Kidney Liver Muscle
1.5 (0.6-3.0) DW 99.0 (58.0-139.0) DW 234.0 (68.0-716.0) DW 62.0 (38.0-80.0) DW
10 10 10 10
Kidney Liver Dolphins; 3 sp.; South Australia; 1988-2004; found stranded or by-caught; liver Common dolphin, Delphinus delphis Bottlenose dolphin, Tursiops truncatus Dolphin, Tursiops aduncus Dugong, Dugong dugon; Australia; July 1989; tusk
(9.6-300.5) (14.3-33.3) (19.1-74.8) (0.03-24.0)
FW FW FW FW
a
(Continues)
470 Chapter 6 Table 6.11: Cont’d Organism
Concentration
Reference
Gray seal, Halichoerus grypus Liver Liver Blubber Kidney Liver Muscle
64.0-94.0 FW 61.0 FW 5.0 FW 37.0 FW 84.0 FW 43.0 FW
2 1 11 11 11 11
18.3 (6.9-30.2) FW 18.5 (7.8-38.5) FW
36 36
Leopard seal, Hydrurga leptonyx; serum
0.49 FW
47
Northern bottlenose whale, Hyperoodon ampullatus Muscle Liver
13.5 FW 23.0 FW
1 1
5.0 FW 130.0 FW 24.0 FW 13.0 FW 25.0 FW 35.0 FW 21.0 FW 20.0 FW 18.0 FW
3 3 3 3 3 3 3 3 3
Hong Kong; found stranded; stomach contents Humpback dolphin, Sousa chinensis Finless porpoise, Neophocaena phocaenoides
Whitebeaked dolphin, Lagenorhynchus albirostris Fascical fat Blubber Liver Muscle Testicles Pancreas Kidney Lungs Spleen Newfoundland, Canada; iceentrapped; 1980-1982; age 2-6 years Kidney Liver Muscle Weddell seal, Leptonychotes weddelli; Antarctica; fur Hair Serum Hair
85.0 (68.0-112.0) DW 100.0 (43.0-136.0) DW 53.0 (36.0-89.0) DW
10 10 10
99.0-137.6 DW 0.36 DW 137.0 DW
22, 26 47 47
a
(Continues)
Mammals 471 Table 6.11: Organism
Cont’d
Concentration
Reference
(27.0-97.0) FW; (123.0-406.0) DW (11.0-781.0) FW; (146.0-353.0) DW (14.0-49.0) FW
12
(18.0-109.0) FW (4.0-86.0) FW (7.0-51.0) FW
12 12 12
(58.0-1101.0) FW (14.0-54.0) FW (8.0-28.0) FW
12 12 12
Southern elephant seal, Mirounga leonina; molted fur; Shetland Islands; juveniles vs. adult females
163.9 (34.5-283.4) DW vs. 167.9 (89.8-261.3) DW
23
Mediterranean monk seal, Monachus monachus; Greece; hair
129.0 DW
25
Killer whale, Orcinus orca; found stranded; Japan; February 2005; adults vs. calves Liver Kidney Muscle
74.0 FW vs. 75.4 FW 24.5 FW vs. 18.1 FW 22.9 FW vs. 23.1 FW
38 38 38
Melon-headed whale, Peponocephala electra; Japan; March 2006; found stranded Liver Kidney Muscle Lung
44.7 26.7 21.4 14.3
48 48 48 48
Ringed seal, Phoca hispida Liver Liver Kidney Muscle
40.0 FW 176.0 (121.0-576.0) DW 209.0 (104.0-441.0) DW 79.0 (52.0-135.0) DW
Harbor seal, Phoca vitulina Adults; dead on collection Blubber Liver
3.0-14.0 FW 16.0-64.0 FW
Marine mammals Pinnipeds; 9 spp Liver Kidney Muscle Cetaceans; 9 spp. Liver Kidney Muscle Sirenians Liver Kidney Muscle
FW FW FW FW
a
12 12
1 13 13 13
4 4 (Continues)
472 Chapter 6 Table 6.11: Cont’d Organism Kidney Brain Spleen Heart Placenta Fetuses; dead on collection Liver Brain Liver Muscle Heart Kidney Spleen Brain Blubber Liver Kidney Brain Muscle Liver Kidney Liver Labrador and Newfoundland; seal length 212-402 cm Muscle Liver Kidney Blood Captive animals Wild; North Sea Wadden Sea; 2004-2005; German site vs. Danish site Harbor porpoise, Phocoena phocoena Blubber Liver Muscle Muscle Liver Kidney Blubber Liver Muscle
Concentration
Reference
15.0-25.0 FW 8.0-27.0 FW 26.0-31.0 FW 31.0 FW 11.0 FW
4 4 4 4 4
89.0 FW 8.0 FW 54.0 (43.0-84.0) FW 34.0 (33.0-35.0) FW 31.0 (28.0-32.0) FW 37.0 (28.0-51.0) FW 32.0 (28.0-35.0) FW 26.0 (19.0-36.0) FW 9.0 (4.0-13.0) FW 27.0-56.0 FW 16.3-32.5 FW 10.8-15.0 FW 15.0-36.0 FW 27.0-60.0 FW 15.5-34.4 FW 25.0-34.0 FW
4 4 2 2 2 2 2 2 2 5 5 5 1 1 1 6
16.9-24.1 FW 28.5-49.2 FW 18.1-26.8 FW
27 27 27
2.9-3.5 FW 2.5-6.3 FW 3.4 (2.9-4.5) FW vs. 3.4 (2.7-4.3) FW
40 41 44
290.0 (150.0-600.0) FW 59.0 (45.0-72.0) FW 19.0 (18.0-21.0) FW 12.4-21.0 FW 34.0-50.0 FW 20.0-24.0 FW 4.0 FW 37.0 FW 22.0 FW
3 3 3 1 1 1 11 11 11
a
(Continues)
Mammals 473 Table 6.11: Organism Western Europe; 1997-2003; found stranded Kidney; adults Liver; adults Fetus vs. mother Liver; Irish Sea Liver; S. Ireland Kidney; S. Ireland Dall’s porpoise, Phocoenoides dalli Adults Bone, skin Heart, liver, pancreas, kidney, whole body Brain, lung, testes Blubber, blood, muscle Fetuses Liver Other tissues Japan; February 2006; 6-year-old male; harpooned Liver Kidney Muscle Skin Bone Heart Lung Intestine Spleen Pancreas Diaphragm Blubber Cerebrum Stomach Portugal; 1998-2002 Common dolphin, Delphinus delphis Muscle Liver Skin Fat Bottlenose dolphin; Tursiops truncatus Muscle
Cont’d
Concentration
Reference
22.7 (14.8-63.4) FW 62.2 (12.5-288.0) FW
30 30
25.6 FW vs. 39.3 FW 46.9 FW vs. 26.0 FW 24.7 FW vs. 20.8 FW
30 30 30
270.0-296.0 FW 25.0-51.0 FW
14 14
11.0-20.0 FW 4.0-9.0 FW
14 14
82.0 FW <6.0 FW
14 14
36.4 FW 38.2 FW 10.9 FW 161.0 FW 245.0 FW 24.5 FW 10.3 FW 25.0 FW 21.6 FW 53.7 FW 122.0 FW 3.5 FW 13.0 FW 32.1 FW
35 35 35 35 35 35 35 35 35 35 35 35 35 35
53.0 (31.5-130.0) DW 150.0 (34.5-260.0) DW 512.0 (357.0-1222.0) DW 27.0 (15.7-56.9) DW
51 51 51 51
45.0 (44.0-47.0) DW
51
a
(Continues)
474 Chapter 6 Table 6.11: Cont’d Organism Liver Skin
Concentration
Reference
152.0 (118.0-156.0) DW 180.0 (80.0-122.0) DW
51 51
Seals; 3 spp. Muscle Liver Spleen Pancreas Stomach wall Fat
34.0-171.0 DW 111.0-264.0 DW 43.0-124.0 DW 81.0-106.0 DW 47.0-176.0 DW 1.8 DW
Striped dolphin, Stenella coeruleoalba Blubber Muscle
20.0 FW 11.0 FW
11 11
175.0 DW 153.0 DW 116.0 DW
49 49 49
76.4 DW vs. 26.7 DW 149.0 DW vs. 70.6 DW 147.0 DW vs. 175.0 DW 31.8 DW vs. 94.6 DW
49 49 49 49
11.3 (9.3-12.4) FW 10.5 (7.1-21.5) FW
45 45
20.0 FW 11.0 FW 57.0 (9.0-271.0) FW
11 11 15
748.0 648.0 752.0 717.0 598.0
29 29 29 29 29
Striped dolphin; Japan; 1979 Liver Fetus Juvenile Adult Adult male vs. female fetus Blubber Kidney Liver Muscle Florida manatee, Trichechus manatus latirostris; January 2007; Crystal River, Florida Blood Skin Bottlenose dolphin, Tursiops truncatus Blubber Muscle South Carolina; found stranded; liver South Carolina; 2003-2005; skin Juvenile male Adult male Juvenile female Adult female Pregnant female
DW; DW; DW; DW; DW;
max. 1030.0 DW max.1588.0 DW max. 1385.0 DW max. 1083.0 DW max. 678.0.0 DW
a
7 7 7 7 7 7
(Continues)
Mammals 475 Table 6.11: Organism Florida; found stranded; 1990-1994 Kidney Liver Muscle Blood; summers 2003-2005; South Carolina vs. Florida Polar bear, Ursus maritimus Kidney Liver Liver; Alaska; 1993-2002 Beaufort Sea area Chukchi Sea area California sea lion, Zalophus californianus Stranded; southern California; 2003-2004 Liver Kidney Mothers with premature pups vs. mothers with normal pups Liver Kidney Premature pups vs. normal pups Liver Kidney
Cont’d
Concentration
Reference
114.0 (86.0-176.0) DW 263.0 (80.0-722.0) DW 110.0 (60.0-185.0) DW 2.37 FW vs. 2.73 FW
16 16 16 39
33.0 (20.0-44.0) FW 58.0-63.0 (33.0-100.0) FW
17 12, 17
180.0 (126.0-269.0) DW 184.0 (117.0-363.0) DW
31 31
32.3-42.4 (37.3-184.0) FW 42.9-98.8 (16.5-973.0) FW
32 32
201.0 DW vs. 220.0 DW 149.0 DW vs. 173.0 DW
8 8
425.0 DW vs. 505.0 DW 19.0 DW vs. 28.4 DW
8 8
a
Values are in mg Zn/kg fresh weight (FW) or dry weight (DW). a 1, Harms et al., 1978; 2, Holden, 1975; 3, Andersen and Rebsdorff, 1976; 4, Duinker et al., 1979; 5, Drescher et al., 1977; 6, Koeman et al., 1973; 7, Hamanaka et al., 1977; 8, Martin et al., 1976; 9, Hamanaka et al., 1982; 10, Muir et al., 1988; 11, Morris et al., 1989; 12, Thompson, 1990; 13, Wagemann, 1989; 14, Fujise et al., 1988; 15, Beck et al., 1997; 16, Wood and Van Vleet, 1996; 17, Norheim et al., 1992; 18, Dehn et al., 2006b; 19, Bratton et al., 1997; 20, Woshner et al., 2001; 21, Tarpley et al., 1995; 22, Santos et al., 2006; 23, Andrade et al., 2007; 24, Ikemoto et al., 2004a,b; 25, Yediler et al., 1993; 26, Yamamoto et al., 1987; 27, Veinott and Sjare, 2006; 28, Stockin et al., 2007; 29, Stavros et al., 2007; 30, Lahaye et al., 2007; 31, Kannan et al., 2007; 32, Harper et al., 2007; 33, Edmonds et al., 1997; 34, Kannan et al., 2006; 35, Yang et al., 2006; 36, Hung et al., 2007; 37, Nielsen and Dietz, 1990; 38, Endo et al., 2007b; 39, Stavros et al., 2008b; 40, Kakuschke et al., 2008b; 41, Griesel et al., 2006; 42, Lavery et al., 2008; 43, Capelli et al., 2008; 44, Griesel et al., 2008; 45, Stavros et al., 2008a; 46, Rosa et al., 2008; 47, Gray et al., 2008; 48, Endo et al., 2008; 49, Agusa et al., 2008; 50, Ando et al., 2005; 51, Carvalho et al., 2002; 52, Law et al., 2003.
available and accumulated far in excess of the organism’s immediate needs (Pequegnot et al., 1969), the comparatively low zinc concentrations in tissues of marine mammals merits clarification. Zinc has its primary effect on zinc-dependent enzymes that regulate RNA and DNA. The main target site of zinc intoxication in mammals is pancreas, followed by bone (Eisler,
476 Chapter 6 2000h). Zinc exerts a protective effect on mammalian liver by inhibiting lipid peroxidation and stabilizing lysosomal membranes (Sternlieb, 1988); aids neurotransmission in brain (Smeets et al., 1989); is essential for wound healing (Ireland, 1986); and is used therapeutically in treating zinc deficiency (Mooradian et al., 1988; Sternlieb, 1988). Zinc deficiency is clearly teratogenic in mammals (Dawson et al., 1988; Leonard and Gerber, 1989). Fetal malformations—especially calcification effects—due to maternal zinc deficiency affect almost every tissue (Ferreira et al., 1989). Skeletal malformation is most common, possibly due to a reduction in cellular proliferation and in activity of bone alkaline phosphatase (Leonard and Gerber, 1989). No data are available on zinc deficiency in marine mammals; however, extensive data are available on this subject for humans, laboratory animals, and livestock demonstrating adverse effects on growth, reproduction, survival, metabolism, and well-being (Eisler, 2000h). Tissue residues are not yet reliable indicators of zinc contamination in mammals although zinc intoxication is documented in terrestrial mammals when zinc exceeds—in mg zinc/kg DW—274.0 in kidney, 465.0 in liver, or 752.0 in pancreas (Eisler, 2000h); comparable data for marine mammals were not found. The normal homeostatic range for zinc in liver of harbor porpoise, P. phocoena, is 20.0–100.0 mg/kg FW (Wood and Van Vleet, 1996), and for impaired regulating mechanisms is less than 20.0 (deficiency) or more than 100.0 mg/kg FW (excess) (Wood and Van Vleet, 1996). However, zinc concentrations in many species of marine mammals routinely exceed 100.0 mg/kg FW (Wood and Van Vleet, 1996; Table 6.11) without apparent damage to the animal. Eating seafood that contains elevated concentrations of zinc does not seem to present a threat to human health. However, oysters from Tasmania allegedly caused nausea and vomiting in some human consumers; these oysters had about 20,000.0 mg Zn/kg soft parts FW, or about 500 times more than the Australian seafood regulation of 40.0 mg/kg FW (Eisler, 1981). Comparable data for marine mammals are not available.
6.37 Literature Cited Aarkrog, A., 1971. Radioecological investigations of plutonium in an arctic marine environment. Health Phys. 20, 31–47. Aarkrog, A., 1977. Environmental behaviour of plutonium accidentally released at Thule, Greenland. Health Phys. 32, 271–284. Aaseth, J., Norseth, T., 1986. Copper. In: Friberg, L., Nordberg, G.F., Vouk, V.B. (Eds.), Handbook on the Toxicology of Metals. Second Edition, Volume II: Specific Metals. Elsevier, New York, pp. 233–254. Agusa, T., Nomura, K., Kunito, T., Anan, Y., Iwata, H., Miyazaki, N., et al., 2008. Interelement relationships and age-related variation of trace element concentrations in liver of striped dolphins (Stenella coeruleoalba) from Japanese coastal waters. Mar. Pollut. Bull. 57, 807–815. Alexander, J.W., Solangi, M.A., Edwards, W.C., Whitenack, D., 1990. Selenium toxicosis in two California sea lions (Zalophus californianus). Int. Assoc. Aquat. Anim. Med. (IAAAM) Proc. 21, 25–28. Anas, R.E., 1974. Heavy metals in northern fur seals. Callorhinus ursinus, and harbor seals, Phoca vitulina richardi. U.S. Dept. Commerce Fish. Bull. 72, 133–137.
Mammals 477 Andersen, S.H., Rebsdorff, A., 1976. Polychlorinated hydrocarbons and heavy metals in the harbour porpoise (Phocoena phocoena) and whitebeaked dolphin (Lagenorhynchus albirostris) from Danish waters. Aquat. Mamm. 4, 14–20. Andersen, M., Gwynn, J.P., Dowdall, M., Kovacs, K.M., Lydersen, C., 2006. Radiocaesium (137Cs) in marine mammals from Svalbard, the Barents Sea and the North Greenland Sea. Sci. Total Environ. 363, 87–94. Anderson, S.S., Livens, F.R., Singleton, D.L., 1990. Radionuclides in grey seals. Mar. Pollut. Bull. 21, 343–345. Ando, N., Isono, T., Sakurai, Y., 2005. Trace elements in the teeth of Stellar sea lions (Eumetopias jubatus) from the North Pacific. Ecol. Res. 20, 415–423. Andrade, S., Carlini, A.R., Vodopivez, C., Polijak, S., 2007. Heavy metals in molted fur of the southern elephant seal Mirounga leonina. Mar. Pollut. Bull. 54, 602–605. Andre, J.M., Boudou, A., Ribeyre, F., 1991a. Mercury accumulation in Delphididae. Water Air Soil Pollut. 56, 187–201. Andre, J.M., Boudou, A., Ribeyre, F., Bernhard, M., 1991b. Comparative study of mercury accumulation in dolphins (Stenella coeruleoalba) from French Atlantic and Mediterranean coasts. Sci. Total Environ. 104, 191–209. Arai, T., Ikemoto, T., Hokura, A., Terada, Y., Kunito, T., Tanabe, S., et al., 2004. Chemical forms of mercury and cadmium accumulated in marine mammals and seabirds as determined by XAFS analysis. Environ. Sci. Technol. 38, 6468–6474. Bacher, G.J., 1985. Mercury concentrations in the Australian fur seal Arctocephalus pusillus from SE Australian waters. Bull. Environ. Contam. Toxicol. 35, 490–495. Baeyens, W., Leermakers, M., Papina, T., Saprykin, A., Brion, N., Noyen, J., et al., 2003. Bioconcentration and biomagnification of mercury and methylmercury in North Sea and Scheldt estuary fish. Arch. Environ. Contam. Toxicol. 45, 498–508. Bargagli, R., Monaci, F., Sanchez-Hernandez, J.C., Cateni, D., 1998. Biomagnification of mercury in an Antarctic marine coastal food web. Mar. Ecol. Prog. Ser. 169, 65–76. Bebbington, G.N., Mackey, N.J., Chvojka, R., Williams, R.J., Dunn, A., Auty, E.H., 1977. Heavy metals, selenium and arsenic in nine species of Australian commercial fish. Aust. J. Mar. Freshw. Res. 28, 277–286. Beck, K.M., Fair, P., McFee, W., Wolf, D., 1997. Heavy metals in livers of bottlenose dolphins stranded along the South Carolina coast. Mar. Pollut. Bull. 34, 734–739. Bernhard, M., Zattera, A., 1975. Major pollutants in the marine environment. In: Pearson, E.A., Frangipane, R. (Eds.), Marine Pollution and Marine Waste Disposal. Pergamon, Elmsford, NY, pp. 195–300. Birke, G., Johnels, A.G., Plantin, L.O., Sjostrand, B., Skerfving, S., Westermark, T., 1972. Studies on humans exposed to mercury through fish consumption. Arch. Environ. Health 25, 77–91. Boggess, W.R. (Ed.), 1977. Lead in the environment, Natl. Sci. Found. Rep. NSF/RA-770214, pp. 1–272. Born, E.W., Renzoni, A., Dietz, R., 1991. Total mercury in hair of polar bears (Ursus maritimus) from Greenland and Svalbard. Polar Res. 9, 113–120. Braham, H.W., 1973. Lead in the California sea lion (Zalophus californianus). Environ. Pollut. 5, 253–258. Bratton, G.R., Flory, W., Spainhour, C.B., Haubold, E.M., 1997. Assessment of Selected Heavy Metals in Liver, Kidney, Muscle, Blubber, and Visceral Fat of Eskimo Harvested Bowhead Whales Balaena Mysticetus from Alaska’s North Coast. Department of Wildlife Management, North Slope Borough, Barrow, AL. Braune, B.M., Norstrom, R.J., Wong, M.P., Collins, B.T., Lee, J., 1991. Geographical distribution of metals in livers of polar bears from the Northwest Territories, Canada. Sci. Total Environ. 100, 283–299. Braune, B.M., Outridge, P.M., Fisk, A.T., Muir, D.C.G., Helm, P.A., Hobbs, K., et al., 2005. Persistent organic pollutants and mercury in marine biota of the Canadian Arctic: an overview of spatial and temporal trends. Sci. Total Environ. 351/352, 4–56. Brookens, T.J., O’Hara, T.M., Taylor, R.J., Bratton, G.R., Harvey, J.T., 2008. Total mercury body burden in Pacific harbor seal, Phoca vitulina richardii, pups from central California. Mar. Pollut. Bull. 56, 27–41. Brunborg, L.A., Graff, I.E., Froyland, L., Julshamn, K., 2006. Levels of non-essential elements in muscle from harp seal (Pagophilus groenlandicus) and hooded seal (Cystophora cristata) caught in the Greenland Sea area. Sci. Total Environ. 366, 784–798.
478 Chapter 6 Bryan, C.E., Christopher, S.J., Balmer, B.C., Wells, R.S., 2007. Establishing baseline levels of trace elements in blood and skin of bottlenose dolphins in Sarasota Bay, Florida: implications for non-invasive monitoring. Sci. Total Environ. 388, 325–342. Bubb, J.M., Lester, J.N., 1996. Factors controlling the accumulation of metals within fluvial systems. Environ. Monit. Assess. 41, 87–195. Buhler, D.R., Claeys, R.R., Mate, B.R., 1975. Heavy metal and chlorinated hydrocarbon residues in California sea lions (Zalophus californianus). J. Fish. Res. Bd. Can. 32, 2391–2397. Burger, J., Gochfeld, M., Jeitner, C., Burke, S., Stamm, T., Snigaroff, R., et al., 2007. Mercury levels and potential risk from subsistence foods from the Aleutians. Sci. Total Environ. 384, 93–105. Bustamante, P., Caurant, F., Fowler, S.W., Miramand, P., 1998. Cephalopods as a vector for the transfer of cadmium to top marine predators in the north-east Atlantic Ocean. Sci. Total Environ. 220, 71–80. Bustamante, P., Mortales, C.F., Mikkelsen, B., Dam, M., Caurant, F., 2004. Trace element bioaccumulation in grey seals Halichoerus grypus from the Faroe Islands. Mar. Ecol. Prog. Ser. 267, 291–304. Cannella, E.G., Kitchener, D.J., 1992. Differences in mercury levels in female sperm whale, Physeter macrocephalus (Cetacea; Odontoceti). Aust. Mammal. 15, 121–123. Capelli, R., Drava, G., De Pellegrini, R., Minganti, V., Poggi, R., 2000. Study of trace elements in organs and tissues of striped dolphins (Stenella coeruleoalba) found dead along the Ligurian coasts (Italy). Adv. Environ. Res. 4, 31–43. Capelli, R., Das, K., De Pellegrini, R., Drava, G., Lepoint, G., Miglio, C., et al., 2008. Distribution of trace elements in organs of six species of cetaceans from the Ligurian Sea (Mediterranean), and the relationship with stable carbon and nitrogen ratios. Sci. Total Environ. 390, 569–578. Cardarelli, N.F., Cardarelli, B.M., Libby, E.P., Dobbins, E., 1984a. Organotin implications in anticarcinogenesis. Effects of several organotins on tumor growth rate in mice. Aust. J. Exp. Biol. Med. Sci. 62, 209–214. Cardarelli, N.F., Quitter, B.M., Allen, A., Dobbins, E., Libby, E.P., Hager, O., et al., 1984b. Organotin implications in anticarcinogenesis. Background and thymus involvement. Aust. J. Exp. Biol. Med. Sci. 62, 199–208. Carvalho, M.L., Pereira, R.A., Brito, J., 2002. Heavy metals in soft tissues of Tursiops truncatus and Delphinus delphis from west Atlantic Ocean by X-ray spectrometry. Sci. Total Environ. 292, 247–254. Caurant, F., Amiard-Triquet, C., 1995. Cadmium contamination in pilot whales Globicephala melas: source and potential hazard to the species. Mar. Pollut. Bull. 30, 207–210. Caurant, F., Amiard, J.C., Amiard-Triquet, C., Sariau, P., 1994. Ecological and biological factors controlling the concentrations of trace elements (As, Cd, Cu, Hg, Se, Zn) in delphinids Globicephalas melas from the North Atlantic Ocean. Mar. Ecol. Prog. Ser. 103, 207–219. Caurant, F., Aubail, A., Lahaye, V., Van Canneyt, O., Rogan, E., Lopez, A., et al., 2006. Lead contamination of small cetaceans in European waters—the use of stable isotopes for identifying the sources of lead exposure. Mar. Environ. Res. 62, 131–148. Ciesielski, T., Szefer, P., Bertenyi, Z., Kuklik, I., Skora, K., Namiesnik, J., et al., 2006. Interspecific distribution and co-associations of chemical elements in the liver tissue of marine mammals from the Polish Economical Exclusive Zone, Baltic Sea. Environ. Int. 32, 524–532. Das, K., Debacker, V., Bouquegneau, J.M., 2000. Metallothionein in marine mammals. Cell. Mol. Biol. 46, 283–294. Das, K., Jacob, V., Bouquegneau, J.M., 2002. White-sided dolphin metallothioneins: purification, characterization and potential role. Comp. Biochem. Physiol. 131C, 245–251. Das, K., Beans, C., Holsbeek, L., Mauger, G., Berrow, S.D., Rogan, E., et al., 2003. Marine mammals from northeast Atlantic: relationship between their trophic status as determined by l13C and l15N measurements and their trace metal concentrations. Mar. Environ. Res. 56, 349–365. Das, K., Siebert, U., Fontaine, M., Jauniaux, T., Holsbeek, L., Bouquegneau, J.M., 2004. Ecological and pathological factors related to trace metal concentrations in harbour porpoises Phocoena phocoena from the North Sea and adjacent areas. Mar. Ecol. Prog. Ser. 281, 283–295. Dawson, D.A., Stebber, E.F., Burks, S.L., Bantle, J.A., 1988. Evaluation of the developmental toxicity of metalcontaminated sediments using short-term fathead minnow and frog embryo-larval assays. Environ. Toxicol. Chem. 7, 27–34.
Mammals 479 De Gieter, M., Leermakers, M., Van Ryssen, R., Noyen, J., Goeyens, L., Baeyens, W., 2002. Total and toxic arsenic levels in North Sea fish. Arch. Environ. Contam. Toxicol. 43, 406–417. Dehn, L.A., Follmann, E.H., Thomas, D.L., Sheffield, G.G., Rosa, C., Duffy, L.K., et al., 2006a. Trophic relationships in an Arctic food web and implications for trace metal transfer. Sci. Total Environ. 362, 103–123. Dehn, L.A., Follmann, E.H., Rosa, C., Duffy, L.K., Thomas, D.L., Bratton, G.R., et al., 2006b. Stable isotope and trace element status of subsistence-hunted bowhead and beluga whales in Alaska and gray whales in Chukotka. Mar. Pollut. Bull. 52, 301–319. De Michele, S.J., 1984. Nutrition of lead. Comp. Biochem. Physiol. 78A, 401–408. Denton, G.R.W., Breck, W.G., 1981. Mercury in tropical marine organisms from north Queensland. Mar. Pollut. Bull. 12, 116–121. Denton, G.R.W., Marsh, H., Heinsohn, G.E., Burden-Jones, C., 1980. The unusual metal status of the dugong Dugong dugon. Mar. Biol. 57, 201–219. Dietz, R., Nielsen, C.O., Hansen, M.M., Hansen, C.T., 1990. Organic mercury in Greenland birds and mammals. Sci. Total Environ. 95, 41–51. Dietz, R., Riget, F., Johansen, P., 1996. Lead, cadmium, mercury and selenium in Greenland marine animals. Sci. Total Environ. 186, 67–93. Dietz, R., Riget, F., Born, E.W., 2000. An assessment of selenium to mercury in Greenland marine animals. Sci. Total Environ. 245, 15–24. Dietz, R., Riget, F., Born, E.W., Sonne, E.W., Grandjean, P., Kirkegaard, M., et al., 2006. Trends in mercury in hair of Greenlandic polar bears (Ursus maritimus) during 1892–2001. Environ. Sci. Technol. 40, 1120–1125. Dorneles, P.R., Lailson-Brito, J., dos Santos, R.A., da Costa, P.A.S., Malm, O., Azevedo, A.F., et al., 2007. Cephalopods and cetaceans as indicators of offshore bioavailability of cadmium off Central South Brazil Bight. Environ. Pollut. 148, 352–359. Drescher, H.E., Harms, U., Huschenbeth, E., 1977. Organochlorines and heavy metals in the harbour seal Phoca vitulina from the German North Sea Coast. Mar. Biol. 44, 99–106. Duinker, J.C., Hillebrand, M.T.J., Nolting, R.F., 1979. Organochlorines and metals in harbour seals (Dutch Wadden Sea). Mar. Pollut. Bull. 10, 360–364. Duncan, J., 1980. The toxicology of molluscicides. The organotins. Pharmacol. Ther. 10, 407–429. Eaton, R.D.P., Secord, D.C., Hewitt, P., 1980. An experimental assessment of the toxic potential of mercury in ringed-seal liver for adult laboratory cats. Toxicol. Appl. Pharmacol. 55, 514–521. Edmonds, J.S., Shibata, Y., Prince, R.I.T., Preen, A.R., Morita, M., 1997. Elemental composition of a tusk of a dugong Dugong dugon, from Exmouth, Western Australia. Mar. Biol. 129, 203–214. Eisler, R., 1978. Mercury contamination standards for marine environments. In: Thorp, J.H., Gibbons, J.W. (Eds.), Energy and Environmental Stress in Aquatic Systems. U.S. Dept. Energy Sympos. Ser. 48, pp. 241–277. Available as CONF-771114 from NTIS, U.S. Dept. Commerce, Springfield, VA. Eisler, R., 1979. Copper accumulations in coastal and marine biota. In: Nriagu, J.O. (Ed.), Copper in the Environment; Part 1: Ecological Cycling. Wiley, New York, pp. 383–449. Eisler, R., 1980. Accumulation of zinc by marine biota. In: Nriagu, J.O. (Ed.), Zinc in the Environment; Part 2: Health Effects. Wiley, New York, pp. 259–351. Eisler, R., 1981. In: Trace Metal Concentrations in Marine Organisms. Pergamon, Elmsford, NY, 687 pp. Eisler, R., 1984. Trace metal changes associated with age of marine vertebrates. Biol. Trace Elem. Res. 6, 165–180. Eisler, R., 1988. Lead hazards to fish, wildlife, and invertebrates: a synoptic review. U.S. Fish Wildl. Serv. Biol. Rep. 85(1.14), 1–134. Eisler, R., 1995. Ecological and toxicological aspects of the partial meltdown of the Chernobyl nuclear power plant reactor. In: Hoffman, D.J., Rattner, B.A., Burton Jr., G.A., Cairns Jr., J. (Eds.), Handbook of Ecotoxicology. Lewis Publishers, Boca Raton, FL, pp. 549–565. Eisler, R., 2000a. Arsenic. In: Handbook of Chemical Risk Assessment. Volume 3. Lewis Publishers, Boca Raton, FL, pp. 1501–1566.
480 Chapter 6 Eisler, R., 2000b. Boron. In: Handbook of Chemical Risk Assessment. Volume 3. Lewis Publishers, Boca Raton, FL, pp. 1567–1612. Eisler, R., 2000c. Molybdenum. In: Handbook of Chemical Risk Assessment. Volume 3. Lewis Publishers, Boca Raton, FL, pp. 1613–1647. Eisler, R., 2000d. Chromium. In: Handbook of Chemical Risk Assessment. Volume 1. Lewis Publishers, Boca Raton, FL, pp. 45–92. Eisler, R., 2000e. Lead. In: Handbook of Chemical Risk Assessment. Volume 1. Lewis Publishers, Boca Raton, FL, pp. 201–311. Eisler, R., 2000f. Nickel. In: Handbook of Chemical Risk Assessment. Volume 1. Lewis Publishers, Boca Raton, FL, pp. 411–497. Eisler, R., 2000g. Silver. In: Handbook of Chemical Risk Assessment. Volume 1. Lewis Publishers, Boca Raton, FL, pp. 499–550. Eisler, R., 2000h. Zinc. In: Handbook of Chemical Risk Assessment. Volume 1. Lewis Publishers, Boca Raton, FL, pp. 605–714. Eisler, R., 2000i. Copper. In: Handbook of Chemical Risk Assessment. Volume 1. Lewis Publishers, Boca Raton, FL, pp. 93–200. Eisler, R., 2003. The Chernobyl nuclear power plant reactor accident: ecotoxicological update. In: Hoffman, D.J., Rattner, B.A., Burton Jr., G.A., Cairns Jr., J. (Eds.), Handbook of Ecotoxicology. second ed. Lewis Publishers, Boca Raton, FL, pp. 703–736. Eisler, R., 2006. In: Mercury Hazards to Living Organisms, CRC Press, Boca Raton, FL, 312 pp. Eisler, R., 2007. Chapter 5, Cadmium. In: Eisler’s Encyclopedia of Environmentally Hazardous Priority Chemicals. Elsevier, Amsterdam, pp. 77–93. Endo, T., Haraguchi, K., Sakata, M., 2002. Mercury and selenium concentrations in the internal organs of toothed whales and dolphins marketed for human consumption in Japan. Sci. Total Environ. 300, 15–22. Endo, T., Haraguchi, K., Hotta, Y., Hisamichi, Y., Lavery, S., Dalebout, M.L., et al., 2005. Total mercury, methyl mercury, and selenium levels in the red meat of small cetaceans sold for human consumption in Japan. Environ. Sci. Technol. 39, 5703–5708. Endo, T., Kimura, O., Hisamichi, Y., Minoshima, Y., Haraguchi, K., Kakumoto, C., et al., 2006. Distribution of total mercury, methyl mercury and selenium in pod of killer whales (Orcinus orca) stranded in the northern area of Japan: comparison of mature females and calves. Environ. Pollut. 144, 145–150. Endo, T., Yong-Un, M., Baker, C.S., Funahashi, N., Lavery, S., Dalebout, M.L., et al., 2007a. Contamination level of mercury in red meat products from cetaceans available from South Korea markets. Mar. Pollut. Bull. 54, 669–677. Endo, T., Kimura, O., Hisamichi, Y., Minoshima, Y., Haraguchi, K., 2007b. Age-dependent accumulation of heavy metals in a pod of killer whales (Orcinus orca) stranded in the northern area of Japan. Chemosphere 67, 51–59. Endo, T., Hisamichi, Y., Kimura, O., Haraguchi, K., Baker, C.S., 2008. Contamination levels of mercury and cadmium in melon-headed whales (Peponocephala electra) from a mass stranding on the Japanese coast. Sci. Total Environ. 401, 73–80. Establier, R., 1975. Concentracion de mercurio en los cabellos de la poblacion de Cadiz y pescadores de altura. Invest. Pesq. 39 (2), 509–516. Ferreira, R.M.C.D.C., Marquiegui, I.M., Elizaga, I.V., 1989. Teratogenicity of zinc deficiency in the rat: study of the fetal skeleton. Teratology 39, 181–194. Flegal, A.R., Stephenson, M., Martin, M., Martin, J.H., 1981. Elevated concentrations of mercury in mussels (Mytilus californianus) associated with pinniped colonies. Mar. Biol. 65, 45–48. Foster, R.F., 1963. Environmental behavior of chromium and neptunium. In: Schultz, V., Klement, A.W. (Eds.), Radioecology. Reinhold, New York, pp. 569–576. Frank, A., Galgan, V., Roos, A., Olsson, M., Petersson, L.R., Bignet, A., 1992. Metal concentrations in seals from Swedish waters. Ambio 21, 529–538. Freeman, H.C., Horne, D.A., 1973. Mercury in Canadian seals. Bull. Environ. Contam. Toxicol. 10, 172–180.
Mammals 481 Fujise, Y., Honda, K., Tatsukawa, R., Mishima, S., 1988. Tissue distribution of heavy metals in Dall’s porpoise in the northwestern Pacific. Mar. Pollut. Bull. 19, 226–230. Gale, T.F., 1978. Embryotoxic effects of chromium trioxide in hamsters. Environ. Res. 16, 101–109. Galster, W.A., 1976. Mercury in Alaskan Eskimo mothers and infants. Environ. Health Perspect. 15, 135–140. Gaskin, D.E., Ishida, K., Frank, R., 1972. Mercury in harbour porpoises (Phocoena phocoena) from the Bay of Fundy Region. J. Fish. Res. Bd. Can. 29, 1644–1646. Gaskin, D.E., Frank, R., Holdrinet, M., Ishida, K., Walton, C.J., Smith, M., 1973. Mercury, DDT, and PCB in harbour seals (Phoca vitulina) from the Bay of Fundy Region. J. Fish. Res. Bd. Can. 30, 471–475. Gaskin, D.E., Smith, G.J.D., Arnold, P.W., Louisy, M.V., Frank, R., Holdrinet, M., et al., 1974. Mercury, DDT, dieldrin, and PCB in two species of Odontoceti (Cetacea) from St. Lucia, Lesser Antilles. J. Fish. Res. Bd. Can. 31, 1235–1239. Gladstone, W., 1996. Trace Metals in Sediments, Indicator Organisms and the Traditional Seafoods of the Torres Strait. Great Barrier Reef Marine Park Authority, Townsville, Australia. Goessler, W., Kuehnelt, D., Schlagenhaufen, C., Slejkovec, Z., Irgolic, K.J., 1998. Arsenobetaine and other arsenic compounds in the National Research Council of Canada certified reference materials DORM 1 and DORM 2. J. Anal. Atom. Spectrom. 13, 183–187. Gray, R., Canfield, P., Rogers, T., 2008. Trace element analysis in the serum and hair of Antarctic leopard seal, Hydrurga leptonyx, and Weddell seal, Leptonychotes weddelli. Sci. Total Environ. 399, 202–215. Griesel, S., Mundry, R., Kakuschke, A., Fonfara, S., Siebert, U., Prange, A., 2006. Mineral elements and essential trace elements in blood of seals of the North Sea measured by total-reflection X-ray fluorescence analysis. Spectrochim. Acta 61B, 1158–1163. Griesel, S., Kakuschke, A., Siebert, U., Prange, A., 2008. Trace element concentrations in blood of harbor seals (Phoca vitulina) from the Wadden Sea. Sci. Total Environ. 392, 313–323. Guinn, V.P., Kishore, R., 1972. In: Results from multi-trace element neutron activation analyses of marine biological specimens. Available from NTIS, Springfield, VA as CONF-721010, pp. 1–5. Hamanaka, T., Kato, H., Tsujita, T., 1977. Cadmium and zinc in ribbon seal Histriophoca fasciata, in the Okhotsk Sea. Res. Int. N. Pac. Fish. Hokkaido Univ. Spec. Vol., 547–561. Hamanaka, T., Itoo, T., Mishima, S., 1982. Age-related change and distribution of cadmium and zinc concentrations in the stellar sea lion (Eumetopias jubata) from the coast of Hokkaido, Japan. Mar. Pollut. Bull. 13, 57–61. Hamilton, T., Seagars, D., Jokela, T., Layton, D., 2008. 137Cs and 210Po in Pacific walrus and bearded seal from St. Lawrence Island, Alaska. Mar. Pollut. Bull. 56, 1158–1167. Harino, H., Ohji, M., Wattayakorn, G., Adulyanukosol, K., Arai, T., Miyazaki, N., 2007a. Accumulation of organotin compounds in tissues and organs of stranded whales along the coasts of Thailand. Arch. Environ. Contam. Toxicol. 53, 119–125. Harino, H., Ohji, M., Wattayakorn, G., Adulyanukosol, K., Arai, T., Miyazaki, N., 2007b. Concentrations of organotin compounds in tissues and organs of dugongs from Thai coastal waters. Arch. Environ. Contam. Toxicol. 53, 495–502. Harino, H., Ohji, M., Wattayakorn, G., Adulyanukosol, K., Arai, T., Miyazaki, N., 2008a. Accumulation of organotin compounds in tissues and organs of dolphins from the coasts of Thailand. Arch. Environ. Contam. Toxicol. 54, 145–153. Harino, H., Ohji, M., Brownell, R.L., Arai, T., Miyazaki, N., 2008b. Concentrations of organotin compounds in the stranded killer whales from Rausu, Hokkaido, Japan. Arch. Environ. Contam. Toxicol. 55, 137–142. Harms, U., Drescher, H.E., Huschenbeth, E., 1978. Further data on heavy metals and organochlorines in marine animals from German coastal waters. Meeresforsch 26, 153–161. Harper, E., Leger St., J.A., Westberg, J.A., Mazzaro, L., Schmitt, T., Reidarson, T.H., et al., 2007. Tissue heavy metal concentrations of stranded California sea lions (Zalophus californianus) in southern California. Environ. Pollut. 147, 677–682. Harrison, R.M., Laxen, D.P.H., 1981. Lead Pollution: Causes and Control. Chapman and Hall, New York, 168 pp.
482 Chapter 6 Hasunuma, R., Ogawa, T., Fujise, Y., Kawanashi, Y., 1993. Analysis of selenium metabolites in urine samples of minke whales (Balaenoptera acutorostrata) using ion exchange chromatography. Comp. Biochem. Physiol. 104C, 87–89. Haynes, D., Kwan, D., 2001. Trace Metal Concentrations in the Torres Strait Environment and Traditional Seafood Species, 1997–2000. Torres Strait Regional Authority, Thursday Island, Queensland, Australia. Haynes, D., Carter, S., Gaus, C., Muller, J., Dennison, W., 2005. Organochlorine and heavy metal concentrations in blubber and liver tissue collected from Queensland (Australia) dugong (Dugong dugon). Mar. Pollut. Bull. 51, 361–369. Hernandez-Avila, M., Smith, D., Meneses, F., Sanin, L.H., Hu, H., 1998. The influence of bone and blood lead on plasma lead levels in environmentally exposed adults. Environ. Health Perspect. 106, 473–477. Holden, A.V., 1973a. International cooperative study of organochlorine and mercury residues in wildlife, 1969–71. Pestic. Monit. J. 7, 37–52. Holden, A.V., 1973b. Mercury in fish and shellfish. A review. J. Food Technol. 8, 1–25. Holden, A.V., 1975. The accumulation of oceanic contaminants in marine mammals. Rapp. P.-v. Reun. Const. int. Explor. Mer 169, 353–361. Holden, A.V., Topping, G., 1972. XIV—occurrence of specific pollutants in fish in the Forth and Tay Estuaries. Proc. R. Soc. Edin. 71B, 189–194. Holtzman, R.B., 1969. Concentrations of the naturally occurring radionuclides 226Ra, 210Pb and 210Po in aquatic fauna. In: Nelson, D.J., Evans, F.C. (Eds.), Symposium on radioecology. Proceedings of the Second National Symposium. Available as CONF-670503 from NTIS, Springfield, VA, pp. 535–546. Honda, K., 1990. Contamination of heavy metals in marine mammals. In: Miyazaki, N., Kasuya, T. (Eds.), Biology of Marine Mammals. Scientist Inc., Tokyo, pp. 242–253. Honda, K., Aoki, M., Fujise, Y., 2006. Ecochemical approach using mercury accumulation of Antarctic minke whale, Balaenoptera bonaerensis, as tracer of historical change of Antarctic marine ecosystem during 1980–1999. Bull. Environ. Contam. Toxicol. 76, 140–147. Howe, P.D., 1998. A review of boron effects in the environment. Biol. Trace Elem. Res. 66, 153–166. Hsu, P.C., Hsu, C.C., Liu, M.Y., Chen, L.Y., Guo, Y.L., 1998. Lead-induced changes in spermatozoa function and metabolism. J. Toxicol. Environ. Health 55A, 45–64. Hughes, K., Meek, M.E., Chan, P.K.L., Shedden, J., Bartlett, S., Seed, L.J., 1994. Nickel and its compounds: evaluation of risks to health from environmental exposure in Canada. J. Environ. Sci. Health. Part C. Environ. Carcinogen. Ecotoxicol. Rev. 12, 417–433. Hung, C.L.H., Lau, R.K.F., Lam, J.C.W., Jefferson, T.A., Hung, S.K., Lam, M.H.W., et al., 2007. Risk assessment of trace elements in the stomach contents of Indo-Pacific humpback dolphins and finless porpoises in Hong King waters. Chemosphere 66, 1175–1182. Ikemoto, T., Kunito, T., Tanaka, H., Baba, N., Miyazaki, N., Tanabe, S., 2004a. Detoxification mechanism of heavy metals in marine animals and seabirds: interaction of selenium with mercury, silver, zinc, and cadmium in liver. Arch. Environ. Contam. Toxicol. 47, 402–413. Ikemoto, T., Kunito, T., Watanabe, I., Yasunaga, G., Baba, N., Miyazaki, N., et al., 2004b. Comparison of trace element accumulation in Baikal seals (Pusa sibirica), Caspian seals (Pusa caspica) and northern fur seals (Callorhinus ursinus). Environ. Pollut. 127, 83–97. Ireland, M., 1986. Effects of wound healing on zinc distribution and alkaline phosphatase activity of Helix aspersa (gastropoda: pulmonata). J. Mollus. Stud. 52, 169–173. Itano, K., Kawai, S., Miyazaki, N., Tatsukawa, R., Fujiyama, T., 1984a. Mercury and selenium levels in striped dolphins caught off the Pacific coast of Japan. Agric. Biol. Chem. 48, 1109–1116. Itano, K., Kawai, S., Miyazaki, N., Tatsukawa, R., Fujiyama, T., 1984b. Body burdens and distribution of mercury and selenium in striped dolphins. Agric. Biol. Chem. 48, 1117–1121. Itano, K., Kawai, S., Miyazaki, N., Tatsukawa, R., Fujiyama, T., 1984c. Mercury and selenium levels at the fetal and suckling stages of striped dolphin. Stenella coeruleoalba. Agric. Biol. Chem. 48, 1691–1698. Jenkins, D.W., 1980. Biological Monitoring of Toxic Trace Metals. Volume 2. Toxic Trace Metals in Plants and Animals of the World. Part 1. U.S. Environ. Project. Agen. Rep. 600/3-80-090, pp. 30–138.
Mammals 483 Joiris, C.R., Holsbeck, L., Bouquegneau, J., Bossicart, M., 1991. Mercury contamination of the harbor porpoise Phocoena phocoena and other cetaceans from the North Sea and the Kattegat. Water Air Soil Pollut. 56, 283–293. Joiris, C.R., Holsbeek, L., Bolboa, D., Gascard, C., Stanev, T., Komakhide, A., et al., 2001. Total and organic mercury in the Black Sea harbour porpoise Phocoena phocoena relicta. Mar. Pollut. Bull. 42, 905–911. Jones, A.M., Jones, Y., Stewart, W.D.P., 1972. Mercury in marine organisms of the Tay region. Nature 238, 164–165. Jones, D., Ronald, K., Lavigne, D.M., Frank, R., Holdrinet, M., Uthe, J.F., 1976. Organochlorine and mercury residues in the harp seal (Pagophilus groenlandicus). Sci. Total Environ. 5, 181–195. Jongen, W.M.F., Cardinaals, J.M., Bos, P.M.J., 1985. Genotoxicity testing of arsenobetaine, the predominant form of arsenic in marine fishery products. Food Chem. Toxicol. 23, 669–673. Kaise, T., Fukui, S., 1992. The chemical form and acute toxicity of arsenic compounds in marine organisms. Appl. Organometall. Chem. 6, 155–160. Kaise, T., Watanabe, S., Itoh, K., 1985. The acute toxicity of arsenobetaine. Chemosphere 14, 1327–1332. Kajiwara, N., Kunisue, T., Kamikawa, S., Ochi, Y., Yano, S., Tanabe, S., 2006. Organohalogen and organotin compounds in killer whales mass-stranded in the Shiretoko Peninsula, Hokkaido, Japan. Mar. Pollut. Bull. 52, 1066–1076. Kakuschke, A., Valentine-Thon, E., Griesel, S., Fonfara, S., Siebert, U., Prange, A., 2005. Immunological impact of metals in harbor seals (Phoca vitulina) of the North Sea. Environ. Sci. Technol. 39, 7568–7575. Kakuschke, A., Valentine-Thon, E., Fonfara, S., Griesel, S., Rosenberger, T., Siebert, U., et al., 2008a. Metalinduced impairment of the cellular immunity to newborn harbor seals (Phoca vitulina). Arch. Environ. Contam. Toxicol. 55, 129–136. Kakuschke, A., Valentine-Thon, E., Griesel, S., Rosenberger, T., Mundry, R., Siebert, U., et al., 2008b. Blood metal levels and metal-influenced immune functions of harbour seals in captivity. Mar. Pollut. Bull. 56, 764–769. Kannan, K., Agusa, T., Perrotta, E., Thomas, N.J., Tanabe, S., 2006. Comparison of trace element concentrations in livers of diseased, emaciated and non-diseased southern sea otters from the California coast. Chemosphere 65, 2160–2167. Kannan, K., Agusa, T., Evans, T.J., Tanabe, S., 2007. Trace element concentrations in livers of polar bears from two populations in northern and western Alaska. Arch. Environ. Contam. Toxicol. 53, 473–482. Kari, T., Kauranen, P., 1978. Mercury and selenium contents of seals and fresh and brackish water in Finland. Bull. Environ. Contam. Toxicol. 19, 273–280. Kemper, C., Gibbs, P., Obendorf, D., Marvanek, S., Lenghaus, C., 1994. A review of heavy metal and organochlorine levels in marine mammals in Australia. Sci. Total Environ. 154, 129–139. Kim, K.C., Chu, R.C., Barron, G.P., 1974. Mercury in tissue and lice of northern fur seals. Bull. Environ. Contam. Toxicol. 11, 281–284. Klaassen, C.D., Amdur, M.O., Doull, J. (Eds.), 1986. Casarett and Doull’s Toxicology. The Basic Science of Poisons. third ed Macmillan, New York, 974 pp. Koeman, J.H., Peters, W.H.M., Koudstaal-Jol, C.H.M., Tijoe, P.S., de Goeij, J.J.M., 1973. Mercury-selenium correlations in marine mammals. Nature 245, 385–386. Koeman, J.H., van de Ven, W.S.M., de Goeij, J.J.M., Tijoe, P.S., van Haaften, L.L., 1975. Mercury and selenium in marine mammals and birds. Sci. Total Environ. 3, 279–287. Kraal, M.H., Kraak, M.H.S., De Groot, C.J., Davids, C., 1995. Uptake and tissue distribution of dietary and aqueous cadmium by carp (Cyprinus carpio). Ecotoxicol. Environ. Saf. 31, 179–183. Kubota, R., Kunito, T., Tanabe, S., 2001. Arsenic accumulation in the liver tissue of marine mammals. Environ. Pollut. 115, 303–312. Kubota, R., Kunito, T., Tanabe, S., 2002. Chemical speciation of arsenic in the livers of higher trophic marine animals. Mar. Pollut. Bull. 45, 218–223. Kuehl, D.W., Haebler, R., Potter, C., 1994. Coplanar PCB and metal residues in dolphins from the U.S. Atlantic coast including Atlantic bottlenose obtained during the 1987/88 mass mortality. Chemosphere 28, 1245–1253.
484 Chapter 6 Lahaye, V., Bustamante, P., Dabin, W., Canneyt, O.V., Dhermain, F., Cesarini, C., et al., 2006. New insights from age determination on toxic element accumulation in striped and bottlenose dolphins from Atlantic and Mediterranean waters. Mar. Pollut. Bull. 52, 1219–1230. Lahaye, V., Bustamante, P., Law, R.J., Learmonth, J.A., Santos, M.B., Boon, J.P., et al., 2007. Biological and ecological factors related to trace element levels in harbour porpoises (Phocoena phocaena) from European waters. Mar. Environ. Res. 64, 247–266. Langard, S., Norseth, T., 1986. Chromium. In: Friberg, L., Nordberg, G.F., Vouk, V.B. (Eds.), Handbook of the Toxicology of Metals. 2nd edition, vol. 2, 185–210, Elsevier, Amsterdam. Langlois, C., Langis, R., Perusse, M., 1995. Mercury contamination in northern Quebec environment and wildlife. Water Air Soil Pollut. 80, 1021–1024. Lavery, T.J., Butterfield, N., Kemper, C.M., Reid, R.J., Sanderson, K., 2008. Metals and selenium in the liver and bone of three dolphin species from South Australia, 1998–2004. Sci. Total Environ. 390, 77–85. Law, R.J., Fileman, C.F., Hopkins, A.D., Baker, J.R., Harwood, J., Jackson, D.B., et al., 1991. Concentrations of trace metals in the livers of marine mammals (seals, porpoises and dolphins) from waters around the British Isles. Mar. Pollut. Bull. 22, 183–191. Law, R.J., Jones, B.R., Baker, J.R., Kennedy, S., Milne, R., Morris, R.J., 1992. Trace metals in the livers of marine mammals from the Welsh coast and the Irish Sea. Mar. Pollut. Bull. 24, 296–304. Law, R.J., Stringer, R.L., Allchin, C.R., Jones, B.R., 1996. Metals and organochlorines in sperm whales (Physeter macrocephalus) stranded around the North Sea during the 1994/1995 winter. Mar. Pollut. Bull. 32, 72–77. Law, R.J., Morris, R.J., Allchin, C.R., Jones, B.R., Nicholson, M.D., 2003. Metals and organochlorines in small cetaceans stranded on the east cost of Australia. Mar. Pollut. Bull. 46, 1200–1211. Lentfer, J.W., Galster, W.A., 1987. Mercury in polar bears from Alaska. J. Wildl. Dis. 23, 338–341. Leonard, D., Gerber, G.B., 1989. Zinc toxicity: does it exist? J. Am. Coll. Toxicol. 8, 1285–1290. Leonzio, C., Focardi, S., Fossi, C., 1992. Heavy metals and selenium in stranded dolphins of the northern Tyrrhenian (NW Mediterranean). Sci. Total Environ. 119, 77–84. Lunde, G., 1967. Activation analysis of bromine, iodine, and arsenic in oils from fishes, whales, phyto- and zooplankton of marine and limnetic biotypes. Int. Rev. ges. Hydrobiol. 52, 265–279. Lunde, G., 1970. Analysis of arsenic and selenium in marine raw materials. J. Sci. Food Agric. 21, 242–247. Mackey, E.A., Demiralp, R., Becker, P.R., Greenberg, R.R., Koster, B.J., Wise, S.A., 1995. Trace element concentrations in cetacean liver tissues archived in the National Marine Mammal Tissue Bank. Sci. Total Environ. 175, 25–41. Mackey, E.A., Becker, P.R., Demiralp, R., Greenberg, E.R., Koster, B.J., Wise, S.A., 1996. Bioaccumulation of vanadium and other trace metals in livers of Alaskan cetaceans and pinnipeds. Arch. Environ. Contam. Toxicol. 30, 503–512. Marcovecchio, J.E., Moreno, V.J., Bastida, R.O., Gerpe, M.S., Rodriguez, D.H., 1990. Tissue distribution of heavy metals in small cetaceans from the southwestern Atlantic Ocean. Mar. Pollut. Bull. 21, 299–304. Martin, J.H., Elliot, P.D., Anderlini, V.C., Girvin, D., Jacobs, S.A., Risebrough, R.W., et al., 1976. Mercuryselenium-bromine imbalance in premature parturient California sea lions. Mar. Biol. 35, 91–104. Meador, J.P., Varanasi, U., Robisch, P.A., Chan, S.L., 1993. Toxic metals in pilot whales (Globicephala melaena) from strandings in 1986 and 1990 on Cape Cod, Massachusetts. Can. J. Fish. Aquat. Sci. 50, 2698–2706. Meador, J.P., Ernest, D., Hohn, A.A., Tilbury, K., Gorzelany, J., Worthy, G., et al., 1999. Comparison of elements in bottlenose dolphins stranded on the beaches of Texas and Florida in the Gulf of Mexico over a one-year period. Arch. Environ. Contam. Toxicol. 36, 87–98. Miles, A.K., Hills, S., 1994. Metals in diet of Bering Sea walrus: Mya sp. as a possible transmitter of elevated cadmium and other metals. Mar. Pollut. Bull. 28, 456–458. Monaci, F., Borre, A., Leonzio, C., Marsili, L., Calzada, N., 1998. Trace elements in striped dolphins (Stenella coeruleoalba) from the western Mediterranean. Environ. Pollut. 99, 61–68.
Mammals 485 Monteiro-Neto, C., Itavo, R.V., Moraes, L.E.S., 2003. Concentrations of heavy metals in Sotalia fluviatilis (Cetacea: Delphinidae) of the west coast of Ceara, Northeast Brazil. Environ. Pollut. 123, 319–324. Mooradian, A.D., Norman, D.C., Morley, J.E., 1988. The effect of zinc status on the immune function of diabetic rats. Diabetologia 31, 703–707. Morris, R.J., Law, R.J., Allchin, C.R., Kelly, C.A., Fileman, C.F., 1989. Metals and organochlorines in dolphins and porpoises of Cardigan Bay, West Wales. Mar. Pollut. Bull. 20, 512–523. Muir, D.G.G., Wagemann, R., Grift, N.P., Norstrom, R.J., Simon, M., Lien, J., 1988. Organochlorine chemical and heavy metal contaminants in white-beaked dolphins (Lagenorhynchus albirostris) and pilot whales (Globicephala melaena) from the coast of Newfoundland, Canada. Arch. Environ. Contam. Toxicol. 17, 613–629. Murata, S., Takahashi, S., Agusa, T., Thomas, N.J., Kannan, K., Tanabe, S., 2008. Contamination status and accumulation profiles of organotins in sea otters (Enhydra lutris) found dead along the coasts of California, Washington, Alaska (USA), and Kamchatka (Russia). Mar. Pollut. Bull. 56, 641–649. National Research Council of Canada (NRCC), 1978. Effects of Arsenic in the Canadian Environment, NRCC Publ. 15391, pp. 1–349. Nieboer, E., Shaw, S.L., 1988. Mutagenic and other genotoxic effects of chromium compounds. In: Nriagu, J.O., Nieboer, E. (Eds.), Chromium in the Natural and Human Environments. Wiley, New York, pp. 399–441. Nielsen, C.O., Dietz, R., 1990. Distributional pattern of zinc, cadmium, mercury, and selenium in livers of hooded seal (Cystophora cristata). Biol. Trace Elem. Res. 24, 61–71. Nilsson, A., Huntington, H., 2002. Arctic Pollution 2002. AMAP Arctic Monitoring and Assessment Programme, Oslo, 111 pp. Norheim, G., Skaare, J.U., Wiig, O., 1992. Some heavy metals, essential elements, and chlorinated hydrocarbons in polar bear (Ursus maritimus) at Svalbard. Environ. Pollut. 77, 51–57. Nriagu, J.O. (Ed.), 1978. The Biogeochemistry of Lead in the Environment. Part B. Biological Effects. Elsevier/ North Holland Biomedical Press, Amsterdam, 397 pp. Nuorteva, P., Hasanen, E., Nuorteva, S.L., 1975. The effectiveness of the Finnish anti-mercury measurements in the moderately polluted area of Hameenkyro. Ymparisto ja Terveys 6 (8), 611–635. O’Shea, T.J., Moore, J.F., Kochman, H.I., 1984. Contaminant concentrations in manatees in Florida. J. Wildl. Manage. 48, 741–748. Outridge, P.M., Scheuhammer, A.M., 1993. Bioaccumulation and toxicology of chromium: implications for wildlife. Rev. Environ. Contam. Toxicol. 130, 31–77. Palmisano, F., Cardellicchio, N., Zambonin, P.G., 1995. Speciation of mercury in dolphin liver: a two-stage mechanism for the demethylation accumulation process and role of selenium. Mar. Environ. Res. 40, 109–121. Paludan-Muller, P., Agger, C.T., Deitze, R., Kinze, C.C., 1993. Mercury, cadmium, zinc, copper and selenium in harbour porpoise (Phocoena phocoena) from west Greenland. Polar Biol. 13, 311–320. Parsons, E.C.M., 1998. Trace metal pollution in Hong Kong: implications for the health of Hong Kong’s IndoPacific hump-backed dolphins (Sousa chinensis). Sci. Total Environ. 214, 175–184. Pequegnot, J.E., Fowler, S.W., Small, L.F., 1969. Estimates of the zinc requirements of marine organisms. J. Fish. Res. Bd. Can. 26, 145–150. Ramprashad, F., Ronald, K., 1977. A surface preparation study on the effects of methylmercury on the sensory hair population in the cochlea of the harp seal (Pagophilus groenlandicus Erxleben, 1977). Can. J. Zool. 55, 223–230. Reijnders, P.J.H., 1980. Organochlorine and heavy metal residues in harbour seals from the Wadden Sea and their possible effects on reproduction. Neth. J. Sea Res. 14, 30–65. Riget, F., Dietz, R., Born, E.W., Sonne, C., Hobson, K.A., 2007. Temporal trends of mercury in marine biota of west and northwest Greenland. Mar. Pollut. Bull. 54, 72–80. Roberts, T.M., Heppleston, P.B., Roberts, R.D., 1976. Distribution of heavy metals in tissues of the common seal. Mar. Pollut. Bull. 7, 194–196. Robertson, D.E., Rancitelli, L.A., Langford, J.C., Perkins, R.W., 1972. In: Battelle-Northwest Contribution to the IDOE Base-Line Study. Battelle Pac. Northwest Lab., Richland, WA, pp. 1–46. Roditi-Elasar, M., Karem, D., Hornung, H., Kress, N., Shoham-Frider, E., Goffman, O., 2003. Heavy metal levels in bottlenose and striped dolphins of the Mediterranean coast of Israel. Mar. Pollut. Bull. 46, 503–512.
486 Chapter 6 Rodriguez, R.E., Misra, M., Diwan, B.A., Riggs, C.W., Kasprzak, K.S., 1996. Relative susceptibilities of C57BL/ 6X, (C57BL/6 X C3H/He)F1 and C3H/He mice to acute toxicity and carcinogenicity of nickel subsulfide. Toxicology 107, 131–140. Ronald, K., Tessaro, S.V., Uthe, J.F., Freeman, H.C., Frank, R., 1977. Methylmercury poisoning in the harp seal (Pagophilus groenlandicus). Sci. Total Environ. 8, 1–11. Ronis, M.J.J., Badger, T.M., Shema, S.J., Roberson, P.K., 1998. Endocrine mechanisms underlying the growth effects of developmental lead exposure in the rat. J. Toxicol. Environ. Health 54A, 101–120. Rosa, C., Blake, J.E., Bratton, G.R., Dehn, L.A., Gray, M.J., O’Hara, T.M., 2008. Heavy metal and mineral concentrations and their relationship to histopathological findings in the bowhead whale (Balaena mysticetus). Sci. Total Environ. 399, 165–178. Rouleau, C., Gobeil, C., Tjalve, H., 2006. Cadmium accumulation in costal demersal fish. Mar. Ecol. Prog. Ser. 311, 131–143. Saeki, K., Nakajima, M., Noda, K., Loughlin, T.R., Baba, N., Kiyota, M., et al., 1999. Vanadium accumulation in pinnipeds. Arch. Environ. Contam. Toxicol. 36, 81–86. Samuels, E.R., Cawthorne, M., Lauer, B.H., Baker, B.E., 1970. Strontium-90 and cesium-137 levels in tissues of fin whale (Balaenoptera physalus) and harp seal (Pagophilus groenlandicus). Can. J. Zool. 48, 167–169. Sanpera, C., Capelli, R., Minganti, V., Jover, L., 1993. Total and organic mercury in north Atlantic fin whales. Distribution pattern and biological related changes. Mar. Pollut. Bull. 26, 135–139. Santos, I.R., Silva-Filho, E.V., Schaefer, C., Sella, S.M., Silva, C.A., Gomes, V., et al., 2006. Baseline mercury and zinc concentrations in terrestrial and coastal organisms of Admiralty Bay, Antarctica. Environ. Pollut. 140, 304–311. Schlosberg, A., Belaiche, M., Regev, S., Gal, R., Brizzi, M., Hanji, V., et al., 1997. Lead toxicosis in a captive bottlenose dolphin (Tursiops truncatus) consequent to ingestion of air gun pellets. J. Wildl. Dis. 33, 135–139. Seixas, T.G., Kehrig, H.A., Fillmann, G., DiBeneditto, A.P.M., Souza, C.M.M., Secchi, E.R., et al., 2007. Ecological and biological determinants of trace elements accumulation in liver and kidney of Pontoporia blainvillei. Sci. Total Environ. 385, 208–220. Seixas, T.G., Kehrig, H.A., Costa, M., Fillmann, G., Di Beneditto, A.P.M., Secchi, E.R., et al., 2008. Total mercury, organic mercury and selenium in liver and kidney of a South American coastal dolphin. Environ. Pollut. 154, 98–106. Sergeant, D.E., Armstrong, F.A.J., 1973. Mercury in seals from eastern Canada. J. Fish. Res. Bd. Can. 30, 843–846. Shimada, H., Shiao, Y.H., Shibata, M.A., Waalkes, M.P., 1998. Cadmium suppresses apoptosis induced by chromium. J. Toxicol. Environ. Health 54A, 159–168. Sigel, H., Sigel, A. (Eds.), 1988. Metal Ions in Biological Systems. Volume 23. Nickel and its Role in Biology. Marcel Dekker, New York, 488 pp. Skaare, J.U., Degre, E., Aspholm, P.E., Ugland, K.I., 1994. Mercury and selenium in Arctic and coastal seals off the coast of Norway. Environ. Pollut. 85, 153–160. Skerfring, S., Hansson, K., Lindstem, J., 1970. Chromosome breakage in humans exposed to methyl mercury through fish consumption. Arch. Environ. Health 21, 133–139. Smeets, W.J.A.J., Perez-Clausell, J., Geneser, F.A., 1989. The distribution of zinc in the forebrain and midbrain of the lizard Gekko gecko. Anat. Embryol. 180, 45–46. Smith, T.G., Armstrong, F.A.J., 1975. Mercury in seals, terrestrial carnivores, and principal food items of the Inuit, from Holman, N.W.T.. J. Fish. Res. Bd. Can. 32, 795–801. Smith, T.G., Armstrong, F.A.J., 1978. Mercury and selenium in ringed and bearded seal tissues from Arctic Canada. Arctic 31, 75–84. Smith, I.C., Carson, B.L., 1977. Trace Metals in the Environment. Volume 2. Silver. Ann Arbor Sci. Publ., Ann Arbor, MI, 469 pp. Sonne-Hansen, C., Dietz, R., Leifsson, P.S., Hyldstrup, I., Riget, E.F., 2002. Cadmium toxicity to ringed seals (Phoca hispida): an epidemiological study of possible cadmium-induced neuropathy and osteodystrophy in ringed seals (Phoca hispida) from Qaanaaq in northwest Greenland. Sci. Total Environ. 295, 167–181.
Mammals 487 Stavros, H.W., Bossart, G.D., Hulsey, T.C., Fair, P.A., 2007. Trace element concentrations in skin of freeranging bottlenose dolphins (Tursiops truncatus) from the southeast Atlantic coast. Sci. Total Environ. 388, 300–315. Stavros, H.W., Bonde, R.K., Fair, P.A., 2008a. Concentrations of trace elements in blood and skin of Florida manatees (Trichechus manatus latirostris). Mar. Pollut. Bull. 56, 1221–1225. Stavros, H.W., Bossart, G.D., Hulsey, T.C., Fair, P.A., 2008b. Trace element concentrations in blood of freeranging bottlenose dolphins (Tursiops truncatus): influence of age, sex and location. Mar. Pollut. Bull. 56, 348–379. Sternlieb, I., 1988. Copper and zinc. In: Arias, I.M., Jakoby, W.B., Popper, H., Schachter, D., Shafritz, D.A. (Eds.), The Liver: Biology and Pathobiology, second ed. Raven Press, New York, pp. 525–533. Stockin, K.A., Law, R.J., Duignan, P.J., Jones, G.W., Porter, L., Mirimin, L., et al., 2007. Trace elements, PCBs and organochlorine pesticides in New Zealand common dolphins (Delphinus sp.). Sci. Total Environ. 387, 333–345. Stoneburner, D.L., 1978. Heavy metals in tissues of stranded short-finned pilot whales. Sci. Total Environ. 9, 293–297. Storelli, M.M., Ceci, E., Marcotrigiano, G.O., 1998. Comparison of total mercury, methylmercury, and selenium in muscle tissues and in the liver of Stenella coeruleoalba (Meyen) and Caretta caretta (Linnaeus). Bull. Environ. Contam. Toxicol. 61, 541–547. Strand, J., Larsen, M.M., Lockyer, C., 2005. Accumulation of organotin compounds and mercury in harbour porpoises (Phocoena phocoena) from the Danish waters and West Greenland. Sci. Total Environ. 350, 59–71. Sun, L., Yin, X., Liu, Y., Zhu, R., Xie, X., Wang, Y., 2006. A 2000-year record of mercury and ancient civilizations in seal hairs from King George Island, West Antarctica. Sci. Total Environ. 368, 236–247. Sures, B., Zimmermann, S., Messerschmidt, J., Von Bohlen, A., Alt, F., 2001. First report of automobile catalyst emitted palladium by European eels (Anguilla anguilla) following experimental exposure to road dust. Environ. Pollut. 113, 341–345. Szefer, P., Czarnowski, W., Pempkowiak, J., Holm, E., 1993. Mercury and major essential elements in seals, penguins, and other representative fauna of the Antarctic. Arch. Environ. Contam. Toxicol. 25, 422–427. Szefer, P., Szefer, K., Pempkowiak, J., Skwarzec, B., Bojanowski, R., 1994. Distribution and coassociations of selected metals in seals of the Antarctic. Environ. Pollut. 83, 341–349. Szefer, P., Zdrojewska, I., Jensen, J., Lockyer, C., Skora, K., Kuklik, I., et al., 2002. Intercomparison studies on distribution and coassociations of heavy metals in liver, kidney and muscle of harbor porpoise, Phocoena phocoena, from southern Baltic and coastal waters of Denmark and Greenland. Arch. Environ. Contam. Toxicol. 42, 508–522. Tao, S.S.H., Bolger, P.M., 1998. Dietary intakes of arsenic in the United States. In: SEGH 3rd Inter. Conf. Arsenic Expos. Health Effects, p. 85. Tarpley, R.L., Wade, T.L., Haubold, E.M., 1995. Toxicological studies in tissues of the beluga whale Delphinapterus leucas along northern Alaska with an emphasis on public health implications of subsistence utilization. Final Report to the Alaska Beluga Whale Committee. Department of Wildlife Management, North Slope Borough, Barrow, AL. Taylor, D.L., Schliebe, S., Metsker, H., 1989. Contaminants in blubber, liver and kidney tissues of Pacific walruses. Mar. Pollut. Bull. 20, 465–468. Teigen, S.W., Skaare, J.U., Bjorge, A., Degre, E., Sand, G., 1993. Mercury and selenium in harbor porpoise (Phocoena phocoena) in Norwegian waters. Environ. Toxicol. Chem. 12, 1251–1259. Thompson, D.R., 1990. Metal levels in marine vertebrates. In: Furness, R.W., Rainbow, P.S. (Eds.), Heavy metals in the Marine Environment. CRC Press, Boca Raton, FL, pp. 143–182. Tillander, M., Miettinen, J.K., Koivisto, I., 1972. Excretion rate of methyl mercury in the seal (Pusa hispida). In: Ruivo, M. (Ed.), Marine Pollution and Sea Life. Fishing Trading News (Books), London, pp. 303–305. Tsubaki, T., Sato, T., Kondo, K., Shirakawa, K., Kanbayashi, K., Hirota, K., et al., 1967. Outbreak of intoxication by organic mercury compound in Niigata Prefecture. An epidemiological and clinical study, Japan. J. Med. 6, 132–133.
488 Chapter 6 Tzeng, W.N., Shiao, J.C., Iizuka, Y., 2002. Use of otolith Sr:Ca ratios to study the riverine migratory behaviors of Japanese eel Anguilla japonica. Mar. Ecol. Prog. Ser. 245, 213–221. Ui, J., Kitamuri, S., 1971. Mercury in the Adriatic. Mar. Pollut. Bull. 2, 56–58. U.S. Environmental Protection Agency (USEPA), 1980a. In: Ambient water quality criteria for nickel. USEPA Rep. 440/5–80–060, pp. 1–206. USEPA, 1980b. Ambient water quality criteria for copper. USEPA Rep. 440/5–80–036, pp. 1–162. USEPA, 1985. Ambient water quality criteria for arsenic—1984. USEPA Rep. 440/5–84–033, pp. 1–66. U.S. National Academy of Sciences (USNAS), 1975. Medical and Biological Effects of Environmental Pollutants. Nickel. Nat. Res. Coun., USNAS, Washington, DC, 277 pp. U.S. Public Health Service (USPHS), 1990. Toxicological profile for silver. USPHS Agen. Toxic Subs. Dis. Regis. TP-90-24, pp. 1–145. USPHS, 1993a. Toxicological profile for nickel. USPHS Rep. TP-92/14, pp. 1–158. USPHS, 1993b. Toxicological profile for chromium. Agen. Toxic Subst. Dis. Regis. TP-92/08, pp. 1–238. USPHS, 1995. Toxicological Profile for Nickel (Update). USPHS, Agen. Toxic Substrates, Dis. Regis., Atlanta, GA, pp. 1–244. van de Ven, W.S.M., Koeman, J.H., Svenson, A., 1979. Mercury and selenium in wild and experimental seals. Chemosphere 8, 539–555. Varanasi, U., Stein, J.E., Tilbury, K.L., Mador, J.P., Sloan, C.A., Clark, R.C., et al., 1994. Chemical contaminants in gray whales (Eschrichtius robustus) stranded along the west coast of North America. Sci. Total Environ. 145, 29–53. Veinott, G., Sjare, B., 2006. Mercury, cadmium, selenium, and seven other elements in the muscle, renal, and hepatic tissue of harbor seals (Phoca vitulina) from Newfoundland and Labrador, Canada. Bull. Environ. Contam. Toxicol. 77, 597–607. Viale, D., 1978. Evidence of metal pollution in cetacea of the western Mediterranean. Ann. Inst. Ocean. Monaco 54, 5–16. Villa, R.B., Osuna, F.P., Cortes, M.H.P., 1993. Concentraciones de metales pesados en el tejida cardiaco, hepatio y renal de la vaquita Phocoena sinus (mammalia: phocoenidae). Anales Inst. Biol. Univ. Nac. Auto, Mexico, Ser. Zool. 64, 61–72. Wagemann, R., 1989. Comparison of heavy metals in two groups of ringed seals (Phoca hispida) from the Canadian Arctic. Can. J. Fish. Aquat. Sci. 46, 1558–1563. Wagemann, R., Stewart, R.E.A., Lockhart, W.L., Stewart, B.E., 1988. Trace metals and methylmercury associations and transfer in harp seal (Phoca groenlandica) mothers and their pups. Mar. Mamm. Sci. 4, 339–355. Wagemann, R., Stewart, R.E.A., Beland, P., Desjardins, C., 1990. Heavy metals and selenium in tissues of beluga whales, Delphinapterus leucas, from the Canadian Arctic and the St. Lawrence estuary. Can. Bull. Fish. Aquat. Sci. 224, 191–206. Wagemann, R., Innes, S., Richard, P.R., 1996. Overview and regional and temporal differences of heavy meals in Arctic whales and ringed seals in the Canadian Arctic. Sci. Total Environ. 186, 41–66. Wagemann, R., Trebacz, E., Boila, G., Lockhart, W.L., 1998. Methylmercury and total mercury in tissues of arctic marine mammals. Sci. Total Environ. 218, 19–31. Walsh, T.J., Tilson, H.A., 1984. Neurobehavorial toxicology of the organoleads. Neurotoxicology 5, 67–86. Watanabe, I., Tanabe, S., Amano, M., Miyazaki, N., Petrov, E.A., Tatsukawa, R., 1998. Age-dependent accumulation of heavy metals in Baikal seal (Phoca sibirica) from the Lake Baikal. Arch. Environ. Contam. Toxicol. 35, 518–526. Wood, C.M., Van Vleet, E.S., 1996. Copper, cadmium and zinc in liver, kidney and muscle tissues of bottlenose dolphins (Tursiops truncatus) stranded in Florida. Mar. Pollut. Bull. 32, 886–889. World Health Organization (WHO), 1980. Tin and organotin compounds: a preliminary review. Environ. Health Crit. 15, 1–109. World Health Organization (WHO), 1991. Nickel. Environ. Health Crit. 108, 1–383.
Mammals 489 Woshner, V.M., O’Hara, T.M., Bratton, G.R., Suydam, R.S., Beasley, V.R., 2001. Concentrations and interactions of selected essential and non-essential elements in bowhead and beluga whales of Arctic Alaska. J. Wildl. Dis. 37, 693–710. Yamamoto, Y., Honda, K., Hidaka, H., Tatsukawa, R., 1987. Tissue distribution of heavy metals in Weddell seals (Leptonychotes weddelli). Mar. Pollut. Bull. 18, 164–169. Yang, J., Miyazaki, N., 2006. Transplacental transfer of butyltins to fetus of Dall’s porpoises (Phocoenoides dalli). Chemosphere 63, 716–721. Yang, J., Miyazaki, N., Kunito, T., Tanabe, S., 2006. Trace elements and butyltins in a Dall’s porpoise (Phocoenoides dalli) from the Sanriku coast of Japan. Chemosphere 63, 449–457. Yang, J., Kunito, T., Tanabe, S., Miyazaki, N., 2007. Mercury and its relation with selenium in the liver of Dall’s porpoises (Phocoenoides dalli) off the Sanriku coast of Japan. Environ. Pollut. 148, 669–673. Yassi, A., Nieboer, E., 1988. Carcinogenicity of chromium compounds. In: Nriagu, J.O., Nieboer, E. (Eds.), Chromium in the Natural and Human Environments. Wiley, New York, pp. 443–495. Yediler, A., Panou, A., Shramel, P., 1993. Heavy metals in hair samples of the Mediterranean monk seal (Monachus monachus). Mar. Pollut. Bull. 26, 156–159. Yin, X., Liu, X., Sun, L., Zhu, R., Xie, X., Wang, Y., 2006. A 1500-year record of lead, copper, arsenic, cadmium, zinc level in Antarctic seal hairs and sediments. Sci. Total Environ. 371, 252–257. Yin, X., Sun, L., Zhu, R., Liu, X., Ruan, D., Wang, Y., 2007. Mercury-selenium association in Antarctic seal hairs and animal excrements over the past 1,500 years. Environ. Toxicol. Chem. 26, 381–386.
CHAPTER 7
Concluding Remarks
7.1 General There is a significant increase in the amount of available literature on trace metals and metalloids in tissues of marine vertebrates since publication of Trace Metal Concentrations in Marine Organisms (Eisler, 1981), including tissues of elasmobranchs, fishes, reptiles, birds, and mammals. Researchers from western Europe, North America, Australia, New Zealand, Canada, Japan, and other locations continue to publish technically competent and sophisticated articles in the peer-reviewed scientific literature on trace metals in marine vertebrates, especially on mammals and birds in polar regions, and on migratory fishes. However, there is a disproportionate increase in the scientific literature from other locations during the past 38 years, especially from the Peoples’s Republic of China, India, Korea, parts of South America, Africa, Mexico, eastern Europe, and numerous other locations. This increase in productivity from formerly impoverished regions is due, in part, to a worldwide redistribution of wealth. One result of increasing financial solvency is an increased number of well-trained scientists from these regions, an increased availability of the sophisticated and expensive equipment necessary to conduct baseline and other research on trace metals and metalloids, and the establishment of long-term funding in these disciplines. Also contributing to increased productivity in this subject area is an increasing awareness of the role of trace metals in marine products of commerce as it relates to health of human consumers; to population declines of marine resources; and to an increased overall commitment to quality of life that is supported by the general population and its political leaders. Most of the variability in trace metal burdens in marine tissues is now attributed to the age of the organism, gender, sexual state, tissue analyzed, water pH, temperature, salinity, season, latitude, proximity to industrial, municipal, and other point sources, and interactions with organic and inorganic compounds in the biosphere. Additional research effort seems merited on interaction effects of trace metals with other trace metals, with other inorganic constituents, and with various organic compounds, especially detergents, chelators, pesticides, solvents, cyanides, polychlorinated biphenyls (PCBs), and polycyclic aromatic hydrocarbons (PAHs). With the advent of inductively coupled plasma-mass spectroscopy as a
491
492 Chapter 7 common tool in environmental element research, it is now routine for analytical chemists to produce data on more than 20 elements within a single sample. This provides insight regarding the co-occurrence of trace metals and the mechanisms that regulate their uptake and retention. Most studies of trace metals in biota have been limited to mercury, lead, cadmium, tin, arsenic, chromium, and selenium because of widespread concerns about their toxicity. These interaction effects will assume increasing importance as new technologies are developed and the resultant wastes are discharged into estuarine, coastal, and offshore marine habitats. Future revisions of the role played by trace metals in marine biota should be a team effort, under the guidance of an experienced editor. This task is both daunting and arduous owing to the rapidly growing number of published technical articles in this subject area.
7.2 Breadth of Coverage Breadth of coverage—as indicated by citations of metals and metalloids for each of the five vertebrate groups examined, viz., elasmobranchs, fishes, reptiles, birds, and mammals—was most extensive for arsenic, cadmium, chromium, copper, iron, lead, manganese, mercury, selenium, silver, strontium, and zinc (Table 7.1). The least extensive breadth of coverage was on bismuth, europium, germanium, lanthanum, neptunium, niobium, palladium, platinum, radium, rhenium, scandium, technetium, tellurium, thorium, yttrium, and zirconium (Table 7.1). Acquisition of baseline data for the less-extensively studied metals is strongly recommended. Similar data for marine plants and invertebrates (Eisler, 2009) indicate that breadth of coverage was most extensive for cadmium, copper, iron, nickel, and zinc, and least extensive Table 7.1: Trace Metals and Marine Vertebrates: Breadth of Coverage Trace Element
a
Coverage (%)
Arsenic, cadmium, chromium, copper, iron, lead, manganese, mercury, selenium, silver, strontium, zinc
100
Aluminum, americium, barium, beryllium, cesium, nickel, plutonium, tin, uranium
80
Antimony, boron, cobalt, lithium, molybdenum, polonium, thallium, titanium, vanadium
60
Bismuth, cerium, gallium, gold, indium, palladium, rubidium, ruthenium, tungsten
40
Europium, germanium, lanthanum, neptunium, niobium, platinum, radium, rhenium, scandium, technetium, tellurium, thorium, yttrium, zirconium
20
a
A rating of 100% means that all five major groups (elasmobranchs, fishes, reptiles, birds, and mammals) are represented in the technical literature; ratings of 80%, 60%, 40%, and 20% represent four, three, two, and one major group, respectively.
Concluding Remarks 493 Table 7.2: Trace Metals and Marine Vertebrates: Depth of Coverage Taxonomic Group Elasmobranchs Fishes Reptiles
Approximate Number of References (Percent of Total) 69 (5.0) 632 (45.9) 52 (3.8)
Birds
341 (24.8)
Mammals
282 (20.5)
Total
1376 (100.0)
for dysprosium, erbium, gadolinium, hafnium, holmium, lutetium, neodymium, praseodymium, tantalum, tellurium, and thulium. In fact, most of the least extensively studied elements in this group were absent altogether from citations on marine vertebrates.
7.3 Depth of Coverage Of the 1376 references on vertebrates (Table 7.2), a large percentage (45.9%) is devoted to fishes, as expected, due to their commercial importance. Birds accounted for 24.8%, mammals 20.5%, elasmobranchs 5.0%, and reptiles 3.8%. It is clear that baseline data on elasmobranchs and reptiles require additional effort. Of the 1980 references documented for marine plants and invertebrates (Eisler, 2009), most were devoted to molluscs (38.2% of the total), crustaceans (23.0%), and plants (19.9%), or 81.1% of the total research effort on these three groups. Research effort on annelids (4.8%), protists (4.7%), echinoderms (3.6%), and coelenterates (2.0%) comprised another 15.1% of the total depth of coverage. The remainder was devoted to tunicates (1.7%), sponges (1.4%), chaetognaths (0.3%), and insects (0.3%) (Eisler, 2009).
7.4 Literature Cited Eisler, R., 1981. In: Trace Metal Concentrations in Marine Organisms. Pergamon, Elmsford, NY, 687 pp. Eisler, R., 2009. Compendium of Trace Metals and Marine Biota. Volume 1: Plants and Invertebrates. Elsevier, Amsterdam.
Index A Adak Island, 43, 53, 68, 97, 106, 111, 151 Admiralty Bay, 281, 299, 337, 421 Adriatic Sea, 24, 75, 222, 225, 229, 233, 237, 240, 245, 410, 430, 451 Aegean Sea, 25, 46, 48, 60, 70, 74, 86, 94–5, 103, 109, 183, 186, 188 ALAD, 96, 104, 284, 293 Alaska, 40, 43, 46, 53, 68, 97, 106, 111–2, 117, 121, 136, 141, 151, 254–6, 259–60, 262, 267, 270, 272, 285–6, 291, 295, 297, 299, 306, 316, 319, 324, 326, 328, 371–2, 375, 378, 380, 385–6, 392, 395, 406, 415, 417, 425, 431, 434, 437, 443–4, 446, 453, 456, 458, 464, 468, 475 Albania, 9, 24 Aleutian Islands, 111, 253, 256, 260, 267, 269, 272–3, 280, 285, 291, 297–9, 311, 323, 328, 334, 336, 417 Alexandria, 160 Aluminum, 2, 39–40, 222–4, 253, 363–4, 492 Amchitka, 253, 255, 259, 262, 269–70, 273, 280, 286, 295, 302, 316, 323, 325, 334, 336 American Samoa, 43 Americium, 1, 2, 7, 40, 147–8, 253, 363–8, 492 Ames test, 368 Antarctica, 77, 82, 92, 112, 119, 129, 144–5, 155–6, 175, 254,
260, 272, 274, 281, 286, 295, 320, 324, 330–1, 337, 364, 384, 402, 407, 421, 433, 436, 440, 454 Antarctic region, 299, 300, 334, 368–70, 379, 387–8, 394, 399, 453, 467 Antimony, 2, 40, 41, 224, 253–7, 364, 368, 492 Arabian Gulf, 68 Arabian Sea, 155, 231, 249 Arctic Bay, 424 Arctic Ocean, 392, 410, 412, 422, 446 Arctic region, 253, 255, 260, 268, 270, 272, 274, 280, 283, 286, 294–5, 298–300, 315, 319–21, 323–4, 330–1, 334, 336–7, 368, 370, 379, 388, 394, 424, 433, 453, 467 Argentina, 12, 22, 24, 34, 113, 125, 179, 387, 390, 391 Arsenic, 1, 2, 7–11, 40–51, 224–30, 254, 257–8, 329, 366, 368–9, 492 Arsenobetaine, 10, 11, 40, 42, 50, 51, 227–8, 230, 366, 368 Aston Bay, 424, 449 Atlantic Ocean, 11, 17, 20, 28, 112, 114, 119, 123, 125, 133, 137, 222, 232, 236, 240, 247, 263–4, 271, 301, 315, 342, 363, 377, 381–2, 429, 430, 444 Australia, 24, 42, 43, 50–1, 53–4, 60, 76, 78, 86, 97, 99, 103, 113, 115, 118, 131, 151, 153, 155, 164, 171, 185, 225, 228,
495
231–2, 234–8, 245–6, 248, 256, 262, 271, 276, 281, 286–7, 296, 319, 339, 365, 371, 373, 382, 385–6, 396, 400–1, 410, 413, 416, 428, 440, 445–7, 454, 456, 468–9, 476, 491 Azores, 23, 29, 113, 133, 154, 301, 338
B Baffin Bay, 255, 260, 270, 272, 274, 283, 286, 294, 295, 307, 310, 319–21, 324, 331 Bahia Blanca estuary, 12, 22, 24, 34, 113 Baja California, 223, 228, 235–9, 243–4, 248, 327, 441 Baja California Sur, 239 Baltic Sea, 44–5, 49, 66, 113, 119, 262, 275, 281, 287, 311, 339, 344 Baltimore Harbor, 254, 265, 271, 276, 281, 289, 296, 307, 326, 332, 340 Bangladesh, 117 Barents Sea, 23, 120, 128, 255, 260, 270, 272, 274, 286, 294–5, 301, 310, 319–21, 324, 331, 337, 381 Barium, 1, 2, 51, 221, 225, 228, 258, 369, 434, 492 Barnstaple Bay, 57, 102, 181 Barrow, 319, 371, 385, 411, 413, 416, 424, 446, 449, 454, 468 Barrow Strait, 416, 424, 449 Bay of Bengal, 144 Bay of Biscay, 112, 377, 430
496 Index Bay of Bothnia, 87 Beaufort Sea, 365, 369, 370, 378, 383, 385, 392, 405, 409, 431, 434, 440, 443, 456–7, 461, 475 Belcher Island, 416 Belgium, 54, 68, 99, 118, 267, 279, 282, 343 Benzo(a)pyrene, 63, 167 Bering Sea, 112, 121, 375, 462, 463 Berkelium, 2, 40 Beryllium, 1, 2, 51, 221, 228, 258, 369, 443, 492 Bismuth, 1, 2, 52, 258, 370, 434, 492 Black Sea, 44, 60–1, 65, 70, 74, 77, 86, 95, 103, 109, 147, 172, 186, 190, 427 Bodega Bay, 43 Bohai Bay, 159–60 Boron, 1, 2, 52, 254, 257, 259, 329, 364, 367, 370, 492 Brazil, 20, 24, 27, 370, 372, 428, 451 Bristol Channel, 261 Britain, 17, 27–8, 273 British Columbia, 20, 121, 130, 162, 166, 255, 264, 276, 286, 289, 301, 306, 326, 331–3, 335, 338, 340 Brunswick, 243, 302, 306, 425, 437 Bylot Sound, 323
C Cadiz, 112 Cadmium, 1, 2, 7, 11–3, 27, 52, 53, 61–5, 89, 104, 143, 170, 189–91, 221–2, 228, 249, 259–60, 268, 269, 293, 317, 344, 370, 371, 379–80, 394, 433–5, 437, 443, 453, 492 Calcasieu River Estuary, 178 Calcium, 1, 2, 18, 64, 88, 159, 167, 187, 239, 253, 344 California, 26, 27, 43, 51, 57, 72, 83, 96, 98, 101, 105, 112, 124, 136, 145–6, 159, 178, 223, 228, 235, 236–9, 243–4, 248, 257, 264, 276, 285, 289,
302–4, 306, 311, 323, 325–7, 337, 339–40, 364, 367, 369–70, 373, 378–80, 382, 384–6, 392, 395, 398–9, 401, 405–7, 409–10, 416, 425–6, 432, 434, 437–42, 445, 453–6, 458–9, 462, 464, 467, 469, 475 Californium, 2, 40 Camlik Lagoon, 59, 94, 185 Canada, 160, 255, 259, 260–1, 264, 266, 270–1, 275, 283, 286, 290, 294–5, 298, 302, 306, 310–1, 313, 319–21, 324, 327–8, 331–2, 337–8, 340, 366, 371, 377, 384, 389, 392, 411, 415, 424–5, 437–8, 443, 445, 454, 456, 469–70, 491 Canadian Arctic, 261, 265, 267, 268, 272, 275, 277, 290, 298, 302, 309, 311–2, 314–5, 324, 327–8, 338, 342, 400 Canadian Environmental Protection Act, 443 Canadian Federal Guideline, 438 Canary Islands, 223, 225, 233, 236, 240, 244, 247 Cape Cod, 387 Cape May, 327 Cape Parry, 424 Caspian Sea, 44, 49 Catalase, 62 Catalina Island, 83, 98, 124 Cerium, 1, 2, 14, 65, 492 Cesium, 1, 2, 14, 49, 66, 67, 231, 269, 380–1 Charleston, 363–4, 367–9, 406, 430, 464 Chernobyl, 66, 269, 323, 381 Chesapeake Bay, 65, 89, 124, 254, 256–8, 265, 271, 277, 282, 284, 286, 289, 292, 296, 307, 319, 321, 326, 332, 336, 341 Chile, 278 China, 15, 35, 46, 54, 65, 68, 72, 78, 89, 99, 105, 117, 141, 144, 159, 160, 175, 228, 255, 262, 267, 270, 279, 287, 291, 303, 312, 325, 339, 343, 491
Chromium, 1, 2, 12–15, 67–9, 71–2, 106, 221, 231–2, 269–70, 381–2, 393, 443, 492 Chukchi Sea, 365, 369–70, 378, 383, 385, 392, 405, 409, 431, 434, 440, 443, 456–7, 461, 475 Cobalt, 1, 2, 7, 15, 72–4, 221, 231–2, 270, 272–3, 380, 382–3, 393, 443, 492 Columbia River, 111, 307 Continental Shelf, 145, 170 Copper, 1, 2, 15–16, 61, 63, 75–6, 87–90, 104, 189, 221, 231, 233, 249, 255, 268, 273–4, 278, 280, 293, 335, 344, 380, 382, 385, 393–4, 434–5, 437, 443, 453–4, 492 Corpus Christi, 256, 266, 290, 323, 336 Corsica, 381, 396, 466 Costa Rica, 226, 234, 237, 242, 248 Council of European Communities, 443 Crystal River, 364, 367, 369, 406, 409, 441, 451, 460, 463–4, 466, 474 Curium, 2, 40, 147 Cyclades Islands, 74, 94, 183 Cyprus, 240–2 Cytochrome P450, 167
D Delaware, 254, 256–8, 265, 271, 277, 281–2, 289, 296, 307, 319, 321, 326, 332, 336, 340–2 Delaware Bay, 254, 256–8, 265, 271, 277, 282, 289, 296, 307, 319, 321, 326, 332, 336, 341 Delta amino-levulinic acid dehydratase, 96 Denmark, 294, 305, 376, 427 Derwent estuary, 127 Dodecanese area, 74, 94, 183 Dongdao Island, 267, 312
Index E East Anglia, 112, 380 East Greenland, 365, 418, 431 Ecuador, 235, 238, 249 Egypt, 67, 69, 160 Elbe, 316 England, 44–5, 49, 97, 116, 261, 283, 292, 308, 323, 389, 391 Eniwetok Atoll, 273 Equator area, 23, 29, 133, 154 Ethoxyresorufin O-deethylase, 167 Europe, 41, 43, 47–8, 53, 57, 59, 60, 63–6, 70, 74–6, 82–3, 85–6, 88, 94–5, 97, 101–3, 105, 109, 111, 114, 123–4, 127, 129, 135, 141, 143, 147, 170–1, 178–9, 181, 185–6, 188, 228, 284, 315, 376, 390, 401, 406, 427, 443, 449, 473, 491 European Commission List, 443 European Union, 65, 105, 141 Europium, 1, 3, 280, 492 Everglades National Park, 237
F Faroe Islands, 373, 418 Finland, 66, 78, 99, 118, 305 Firth of Clyde, 118 Florida, 24, 88, 110, 117, 129, 140, 226, 232, 234, 237, 248, 307, 341, 364, 367, 369, 378, 385, 391–3, 398, 404–6, 409, 430–1, 439, 441–3, 451–2, 457, 460, 463–4, 466, 474–5 Florida Bay, 226, 232, 237, 248 Florida Everglades, 307 France, 29, 31, 82, 85, 112, 118, 159, 161, 222, 233, 378, 430 French Guiana, 224, 234, 238, 242, 245
G Gallium, 1, 3, 89, 280 Galveston Bay, 291 Georgia, 20, 241, 243, 254, 256, 277, 282, 290, 297, 308, 327, 340–1 German Bight, 81
Germanium, 1, 3, 89, 492 Germany, 97, 137, 141, 164, 303, 304–5, 341, 364, 366, 370, 444 Ghana, 113, 118, 120 Glomma estuary, 48 Gold, 1, 3, 90, 395, 433, 443, 492 Greece, 9, 67, 375, 388, 402, 471 Greenland, 23, 49, 55, 96, 100, 120, 126, 128, 135, 147, 152, 263, 290, 293, 294, 304–5, 307, 323, 325, 365, 370, 372, 374, 376, 381, 389, 402–3, 410, 415, 417, 418, 421, 424, 427, 431, 433, 437, 444, 446, 448, 468 Greenland Sea, 365, 374, 381, 402, 418, 448 Guam, 46, 80, 155 Gulf of Alaska, 46, 121, 463 Gulf of Bothnia, 54, 78, 99, 118, 305 Gulf of California, 57, 101, 178, 264, 289, 304, 340 Gulf of Finland, 66 Gulf of Guinea, 113, 118, 120 Gulf of Mexico, 22, 39, 52, 60, 74, 86, 89, 98–9, 102–3, 120, 125, 146, 185 Gulf of Oman, 23, 117 Gulf of St. Lawrence, 11, 52, 423 Gulf of Thailand, 118
I
H
J
Hackensack River, 69 Haifa Bay, 116 Hawaii, 40, 136, 222–3, 225, 228–9, 239, 245, 247–8, 287 Helgoland, 308 Holland Island, 254, 265, 271, 277, 281, 289, 296, 307, 326, 332, 340 Hong Kong, 12–13, 15–16, 19–21, 28–30, 32, 34, 222–4, 226, 228, 230–2, 234–5, 237, 239, 242–6, 248, 366, 374, 380, 382, 384, 387, 407, 420, 439–40, 448, 455, 462, 470
497
Iceland, 365, 413, 418 Idaho, 307 India, 54, 68, 73, 78, 99, 107, 117, 118, 144, 161, 175, 180, 224, 491 Indian Ocean, 56, 80, 92, 98–9, 106, 107, 118, 121, 131, 141, 152, 177, 265, 278, 282, 297, 310, 327, 333, 342 Indian River, 364, 367, 430 Indium, 1, 3, 90, 280, 395, 492 Iona Island, 286, 289, 301, 306, 331, 338, 340 Ionian Sea, 10, 13, 18–19, 25, 29, 30, 34 Ireland, 287, 376, 390, 427, 450, 473, 476 Irish Sea, 23, 30, 47, 127, 289, 388, 390, 427, 438, 441, 450, 473 Iron, 1, 3, 18–19, 75, 89–90, 221, 235–6, 239, 268, 280–1, 335–6, 344, 394–5, 467, 492 Ishigaki Island, 226 Iskenderun Bay, 39 Israel, 24, 68, 116, 145, 378 Italy, 9, 24, 95, 104, 109–10, 115, 130, 187, 222, 225, 233, 240–1, 264, 283, 288, 306, 448
Japan, 49, 66, 67, 82, 110, 119, 122, 137, 160, 164, 168, 222–3, 226, 228–30, 233–4, 236–7, 240–2, 244, 247–8, 254–5, 261, 270, 272–3, 275, 280–1, 284, 294–5, 300, 303, 319–20, 324, 330, 332–3, 338, 372, 375–9, 382–5, 388, 390, 396–8, 400, 403–4, 407–10, 414–5, 422–3, 427, 429, 434, 439, 442, 449–51, 455–7, 459–60, 462–3, 465, 468, 471, 473–4, 491
498 Index K Kakadu National Park, 235 Kamchatka, 458 Kanto area, 254–5, 261, 270, 275, 281, 295, 300, 319, 324, 330, 338 Keratin, 316 Ketchikan, 319 Kiska, 255, 259, 262, 270, 286, 295, 302, 316, 325 Kochi Prefecture, 222, 233, 236, 241, 247 Kodiak Island, 463 Korea, 67, 118–9, 164, 266, 276, 278, 281, 287, 290, 297, 332, 340, 343, 414, 438, 491 Kyushu, 110
L La Plata River, 125, 366, 368, 377, 380, 390, 428, 451 Labrador, 366, 377, 384, 389, 393, 408, 426, 450, 472 Laguna Madre, 47, 69, 312, 343 Laguna Vista, 313 Lanthanum, 1, 3, 283, 492 Lavaca Bay, 313 Lead, 3, 19–20, 96–105, 235–9, 283–94, 399–406 Leptospirosis, 432, 436 Ligurian Sea, 372, 385, 396, 400, 407, 415, 446, 468 Lithium, 1, 3, 105, 159, 294, 406, 492 Liverpool Bay, 127 Long Island, 271–2, 288, 292, 326 Long Island Sound, 14, 20, 28, 321 Lorino/Lavrentiya, 373, 386, 417, 447, 455, 469 Los Angeles, 83, 96, 98 Louisiana, 155, 178, 259, 286, 320
M Magdalena Bay, 228 Magnesium, 1, 3, 18 Maine, 333, 425, 437 Malaysia, 54, 99, 118
Manganese, 1, 3, 7, 20–1, 51, 75, 89, 106–10, 221, 236, 238, 239, 268, 294–5, 297–8, 380, 394, 406, 453, 492 Mar Chiquita Lagoon, 125 Marmara Sea, 54, 78, 99, 118 Maryland, 89, 124, 254, 256, 257, 258, 265, 271, 273, 276, 277, 281–2, 284, 286, 289, 296, 307, 326, 332, 340–1 Masculinization, 165 Massachusetts, 127, 307, 328, 340, 341, 387 Mediterranean Sea, 7, 9, 11, 22, 24, 28, 47, 56, 59, 68, 70, 82, 86, 89, 94, 95, 101, 103, 123, 125, 133, 137, 145, 162, 164, 179, 185–6, 264, 288, 305, 306, 316, 378, 410, 429–30, 435, 445 Mercuric selenide, 434, 453 Mercury, 1, 4, 20–7, 110–41, 150, 221, 239–43, 268, 298–318, 329, 380, 410–38, 443, 445, 452–3, 467, 492 Mersey estuary, 292 Metallothionein, 51, 63, 75, 139, 170, 188, 259, 268, 380, 434 Methemoglobin, 394 Methylmercury, 20, 22–5, 27, 110, 112–3, 115–8, 120–4, 128, 131–2, 135, 137–41, 239–40, 243, 301, 303–4, 314–8, 410, 412, 415–7, 419–20, 422–5, 429–30, 433–8, 453 Mexico, 22, 39, 52, 57, 60, 74, 86, 89, 98–9, 101–3, 120, 125, 146, 178, 185, 224, 234–8, 240, 242, 249, 264, 284, 289–90, 340, 441, 491 Midway Atoll, 293 Minamata Bay, 110, 119, 122, 134, 434 Molybdenum, 1, 4, 141–2, 221, 243, 318, 438–9, 443, 492 Morocco, 68, 162 Mozambique Channel, 56, 80, 92, 121, 152, 177
Mumbai, 54, 73, 99, 107, 117, 144, 161, 175
N Nebraska, 293 Neptunium, 1, 4, 142, 492 Netherlands, 45, 289 New Brunswick, 302, 306, 425, 437 New Guinea, 48, 57, 118, 156, 232–4, 237, 241–2, 248, 272 New Jersey, 69, 118, 122, 126, 132, 140, 143, 271, 288, 307, 321, 327, 341 New York, 43, 271–2, 288, 292, 321, 326, 328 New York Bight, 14, 20, 28–30, 146, 154, 189, 266, 290 New Zealand, 87, 89, 145, 256, 266, 273, 277–8, 284, 290, 307, 311, 323, 327, 337, 343, 365, 373, 382–3, 386, 396, 401, 407, 416, 440, 447, 455, 457, 468, 491 Newark Bay, 118 Newfoundland, 45, 155, 366, 377, 384, 389, 393, 408, 426, 450, 469, 470, 472 Nickel, 1, 4, 27, 63, 106, 143, 144, 221, 244, 319, 320, 322, 438–44, 453, 492 Nickel carbonyl, 443 Niigata Prefecture, 434 Niobium, 1, 4, 143, 492 North Carolina, 340–1 North Sea, 8, 23, 46, 55, 118, 119–20, 127, 176, 181, 265, 304, 308, 316, 363, 364, 366, 370, 381, 397, 403, 408, 426, 438, 439, 441–2, 444, 450, 456, 460, 472 Northwest Territories, 392, 456 Norway, 44–5, 48–9, 80, 99, 168, 326, 368, 422, 449 Nowra, 115
Index O
Q
Okinawa, 223, 226, 228, 234, 236–7, 241, 244, 248 Oldbury-on-Severn, 57, 102, 181 Omaha, 293 Oregon, 110, 112, 118, 121, 170, 306, 326, 425
Queen Charlotte Islands, 259
P Pacific Ocean, 105, 125, 224, 234, 259, 277, 290, 326, 333, 340, 396, 401, 407, 429 Palladium, 1, 4, 143–7, 443, 444, 492 Palos Verdes, 124 Papua New Guinea, 48, 57, 156, 232–4, 237, 241–2, 248 Pea Patch Island, 254, 265, 271, 277, 281, 289, 296, 307, 326, 332, 340 Pearl River Delta, 255, 270, 303, 325, 339 Persian Gulf, 50, 118 Peru, 144 Petalion Gulf, 74, 94 Platinum, 1, 4, 143, 147, 444, 492 Plutonium, 1, 4, 30, 147–8, 323, 444, 492 Point Lay/Wainwright, 372, 386, 415, 446, 455, 468 Poland, 427 Polonium, 1, 4, 148, 444–5, 492 Polychlorinated biphenyls, 11, 314, 344, 491 Polycyclic aromatic hydrocarbon, 63, 491 Pond Inlet, 424, 449 Port Phillip Bay, 51 Portugal, 69, 81, 100, 115, 177, 312, 338, 367–8, 384, 390, 397, 403, 408, 428, 441–2, 451, 457, 473 Pribilof Islands, 462 Prince William Sound, 254–5, 259, 260, 262, 270, 285–6, 295, 299, 302, 316, 324–5 Puerto Rico, 124, 144 Puget Sound, 274, 324
R Radium, 1, 4, 148, 492 Raritan Bay, 321 Ravenglass, 323 Reunion Island, 56, 80, 92, 121, 152, 177, 265, 278, 282, 297, 310, 327, 342 Rhenium, 1, 4, 148–9, 492 Rhine, 316, 344 Rhode Island, 321, 337, 340 Rhodium, 4, 147 Rio de Aveiro, 115 Rio de Janeiro, 372 Rio Tinto Estuary, 99 River Tyne, 116 Roberts Bank, 286, 289, 301, 306, 331, 338, 340 Ross Sea, 61 Rubidium, 1, 4, 148, 244, 319, 321, 323, 439, 442, 445, 492 Russia, 67, 373, 386, 417, 447, 455, 469 Ruthenium, 1, 4, 30, 149, 150, 492
S Sacca Sessola, 71, 87, 95, 104, 109, 187 San Antonio Bay, 313 San Diego Bay, 257, 259, 273, 275, 338 San Francisco Bay, 276, 306, 311, 317, 326, 331, 334 San Giuliano, 71, 87, 95, 104, 187 San Simeon, 98 Sanriku, 303, 414, 427, 460 Sarasota Bay, 364, 367, 378, 385, 391, 405, 409, 431, 439, 442, 445, 452, 457, 463, 466 Saudi Arabia, 53, 68, 77, 91, 98, 144, 172 Scandium, 1, 5, 149–50, 492 Scotland, 51, 58, 84, 118, 129, 182, 260, 262–4, 273, 287, 380 Sea of Japan, 66–7
499
Selenium, 1, 5, 28, 30, 150–4, 221, 244–6, 268, 317, 323–4, 329, 380, 433–7, 445–6, 452–3, 467, 492 Selenomethionine, 329 Sellafield, 381 Shetland Islands, 375, 383, 388, 402, 440, 471 Silver, 1, 5, 28–31, 76, 88, 110, 134, 143, 154–7, 171–2, 246, 330, 334, 394, 433–4, 443, 453–64, 467, 492 South Carolina, 77, 83, 85, 146, 241–3, 341, 363–4, 367–9, 378, 383, 385, 391, 398, 404, 406, 409, 430, 452, 461, 464, 466, 474, 475 South China Sea, 267, 312, 343 Spain, 59, 68, 70, 85–6, 94, 99, 102, 110–2, 115, 130, 223, 225, 233, 236, 240, 244, 247, 256, 266, 271, 277, 283, 285, 289–90, 311, 314, 342, 413 Spitsbergen, 320, 322 Sri Lanka, 164 St. Kilda, 260, 262–5 St. Lawrence estuary, 13, 52 St. Lucie, 435 Strait of Georgia, 20, 340 Strontium, 1, 5, 31, 90, 105, 106, 157–9, 168, 221, 246, 330, 331, 334, 454, 456, 464, 492 Suisin Bay, 302 Superoxide dismutase, 380 Svalbard, 320, 381, 392, 431 Sweden, 44–5, 48, 136–7, 141, 316, 441 Sydney, 115
T Taiwan, 46–7, 78, 110, 131, 141, 162–4 Tarragona coast, 99 Tasmania, 127, 476 Technetium, 1, 5, 334, 492 Tellurium, 1, 5, 159, 160, 492 Terra Nova Bay, 61, 112, 300, 421
500 Index Texas, 47, 67, 69, 83, 130, 136, 145–6, 153, 254, 256, 260, 266, 274, 285, 290–1, 311–3, 320, 323–4, 328, 336–7, 343 Thailand, 118, 458, 461, 465 Thallium, 1, 5, 159–60, 246, 334, 464, 492 Thorium, 1, 5, 334, 492 Tijuana Slough, 257, 275, 338 Tin, 1, 5, 28–9, 31, 106, 159–67, 330, 332, 334–5, 434, 443–4, 454, 457, 459, 465, 492 Titanium, 1, 5, 106, 160, 164, 167, 246, 444, 466, 492 Tokushima region, 160 Tomales Bay, 302 Tributyltin, 31, 159–65, 332–3, 335, 459, 465, 466 Tungsten, 1, 5, 160, 164, 168, 335–6, 492 Tunisia, 133, 135 Turkey, 39, 54, 59, 60, 65, 70, 73, 74, 78, 86, 89, 93–5, 99, 103, 105, 108–9, 116, 118, 121, 132, 147, 185–6
U
W
United Kingdom, 30, 127, 137, 144–5, 181, 224, 226, 234, 238, 242, 245, 248, 381 United Kingdom Atomic Energy Authority, 30 United States, 40, 136, 141, 240, 241, 283, 294, 337, 434 Uranium, 1, 6, 168, 246, 336, 466, 492 U.S. Environmental Protection Agency (USEPA), 110, 136, 443 U.S. Food and Drug Administration, 136, 150
W. Victoria Island, 416, 424, 449 Wadden Sea, 305, 337, 339, 364, 366, 370, 377, 383–4, 389, 397, 403, 408, 439, 441–2, 444, 450, 456, 460, 462, 466, 472 Wales, 78, 391 Washington, 112, 121, 274, 283, 306, 324, 326, 425, 458 Willamette Basin, 118 Windscale, 30, 31
V Vanadium, 1, 6, 106, 168, 169, 246, 336, 454, 462, 466–7, 492 Vancouver, 160, 255 Vancouver Island, 255 Venice Lagoon, 71, 87, 95, 104, 109, 187 Victoria, 256, 262, 272, 276, 281, 286, 287, 416, 424, 449 Virginia, 285, 288, 307, 341 Vitellogenin, 61
Y Yaeyama Islands, 226 Yeongjong Island, 266, 290 Yttrium, 1, 6, 168, 492 Yucatan, 284, 290
Z Zinc, 1, 6, 7, 18, 31–5, 61, 63, 65, 75, 89–90, 104, 169–91, 221, 247–9, 259, 268, 337, 344, 345, 380, 394, 434–5, 437, 453, 467–76, 492 Zirconium, 1, 6, 191, 492
![Handbook of Optoelectronics [Vol 1 and 2]](https://epdf.tips/img/300x300/handbook-of-optoelectronics-vol-1-and-2_5acee245b7d7bc0d07fc9cea.jpg)
![The Roman Traitor [Vol. 1 of 2]](https://epdf.tips/img/300x300/the-roman-traitor-vol-1-of-2_5afe14fbb7d7bc7569cf4823.jpg)
