Compendium of Trace Metals and Marine Biota: Volume 2: Vertebrates

Compendium of Trace Metals and Marine Biota Volume 2: Vertebrates

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Compendium of Trace Metals and Marine Biota Volume 2: Vertebrates

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 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 Morton I. Grossman Clarence P. Idyll Frank G. Lowman James E. Lynch Lionel A. Walford

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Contents Acknowledgments ............................................................................................ xiii Books by Ronald Eisler ..................................................................................... xv About the Author........................................................................................... xvii List of Tables – Vol. 2 .................................................................................... xix Chapter 1 Introduction ...................................................................................... 1 1.1

Literature Cited...........................................................................................................6

Chapter 2 Elasmobranchs .................................................................................. 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

Americium ..................................................................................................................7 Arsenic........................................................................................................................7 Cadmium ..................................................................................................................11 Cerium ......................................................................................................................14 Cesium ......................................................................................................................14 Chromium .................................................................................................................14 Cobalt........................................................................................................................15 Copper.......................................................................................................................15 Iron............................................................................................................................18 Lead ..........................................................................................................................20 Manganese ................................................................................................................20 Mercury.....................................................................................................................20 Nickel........................................................................................................................27 Plutonium..................................................................................................................30 Ruthenium.................................................................................................................30 Selenium ...................................................................................................................30 Silver .........................................................................................................................30 Strontium ..................................................................................................................31 Tin .............................................................................................................................31 Zinc ...........................................................................................................................31 Literature Cited........................................................................................................35

vii

viii

Contents

Chapter 3 Fishes............................................................................................. 39 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 3.21 3.22 3.23 3.24 3.25 3.26 3.27 3.28 3.29 3.30 3.31 3.32 3.33 3.34 3.35 3.36 3.37 3.38 3.39 3.40 3.41 3.42 3.43

Aluminum .................................................................................................................39 Americium ................................................................................................................40 Antimony ..................................................................................................................40 Arsenic......................................................................................................................40 Barium ......................................................................................................................51 Beryllium ..................................................................................................................51 Bismuth.....................................................................................................................52 Boron ........................................................................................................................52 Cadmium ..................................................................................................................52 Cerium ......................................................................................................................65 Cesium ......................................................................................................................66 Chromium .................................................................................................................67 Cobalt........................................................................................................................72 Copper.......................................................................................................................75 Gallium .....................................................................................................................89 Germanium ...............................................................................................................89 Gold...........................................................................................................................90 Indium .......................................................................................................................90 Iron............................................................................................................................90 Lead ..........................................................................................................................96 Lithium....................................................................................................................105 Manganese ..............................................................................................................106 Mercury...................................................................................................................110 Molybdenum ...........................................................................................................141 Neptunium ..............................................................................................................142 Nickel......................................................................................................................143 Niobium ..................................................................................................................143 Palladium ................................................................................................................143 Plutonium................................................................................................................147 Polonium.................................................................................................................148 Radium....................................................................................................................148 Rhenium..................................................................................................................148 Rubidium ................................................................................................................148 Ruthenium...............................................................................................................150 Scandium ................................................................................................................150 Selenium .................................................................................................................150 Silver .......................................................................................................................154 Strontium ................................................................................................................157 Tellurium ................................................................................................................159 Thallium..................................................................................................................159 Tin ...........................................................................................................................159 Titanium..................................................................................................................167 Tungsten..................................................................................................................168

Contents ix 3.44 3.45 3.46 3.47 3.48 3.49

Uranium ..................................................................................................................168 Vanadium................................................................................................................168 Yttrium....................................................................................................................168 Zinc .........................................................................................................................169 Zirconium................................................................................................................191 Literature Cited.......................................................................................................191

Chapter 4 Reptiles ........................................................................................ 221 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 4.22 4.23 4.24 4.25 4.26

Aluminum ...............................................................................................................222 Antimony ................................................................................................................227 Arsenic....................................................................................................................227 Barium ....................................................................................................................228 Beryllium ................................................................................................................228 Cadmium ................................................................................................................228 Cesium ....................................................................................................................231 Chromium ...............................................................................................................231 Cobalt......................................................................................................................231 Copper.....................................................................................................................231 Iron..........................................................................................................................235 Lead ........................................................................................................................235 Manganese ..............................................................................................................239 Mercury...................................................................................................................239 Molybdenum ...........................................................................................................243 Nickel......................................................................................................................244 Rubidium ................................................................................................................244 Selenium .................................................................................................................246 Silver .......................................................................................................................246 Strontium ................................................................................................................246 Thallium..................................................................................................................246 Titanium..................................................................................................................246 Uranium ..................................................................................................................246 Vanadium................................................................................................................246 Zinc .........................................................................................................................247 Literature Cited.......................................................................................................249

Chapter 5 Birds............................................................................................ 253 5.1 5.2 5.3 5.4 5.5 5.6 5.7 5.8 5.9

Aluminum ...............................................................................................................253 Americium ..............................................................................................................253 Antimony ................................................................................................................253 Arsenic....................................................................................................................257 Barium ....................................................................................................................258 Beryllium ................................................................................................................258 Bismuth...................................................................................................................258 Boron ......................................................................................................................259 Cadmium ................................................................................................................259

x

Contents 5.10 5.11 5.12 5.13 5.14 5.15 5.16 5.17 5.18 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 5.34 5.35 5.36 5.37 5.38

Cesium ....................................................................................................................269 Chromium ...............................................................................................................269 Cobalt......................................................................................................................273 Copper.....................................................................................................................273 Europium ................................................................................................................280 Gallium ...................................................................................................................280 Indium .....................................................................................................................280 Iron..........................................................................................................................280 Lanthanum ..............................................................................................................283 Lead ........................................................................................................................283 Lithium....................................................................................................................294 Manganese ..............................................................................................................297 Mercury...................................................................................................................298 Molybdenum ...........................................................................................................318 Nickel......................................................................................................................322 Plutonium................................................................................................................323 Rubidium ................................................................................................................323 Selenium .................................................................................................................323 Silver .......................................................................................................................330 Strontium ................................................................................................................334 Technetium .............................................................................................................334 Thallium..................................................................................................................334 Thorium ..................................................................................................................334 Tin ...........................................................................................................................334 Tungsten..................................................................................................................335 Uranium ..................................................................................................................336 Vanadium................................................................................................................336 Zinc .........................................................................................................................337 Literature Cited.......................................................................................................345

Chapter 6 Mammals ..................................................................................... 363 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

Aluminum ...............................................................................................................363 Americium ..............................................................................................................363 Antimony ................................................................................................................368 Arsenic....................................................................................................................368 Barium ....................................................................................................................369 Beryllium ................................................................................................................369 Bismuth...................................................................................................................370 Boron ......................................................................................................................370 Cadmium ................................................................................................................370 Cesium ....................................................................................................................380 Chromium ...............................................................................................................381 Cobalt......................................................................................................................393 Copper.....................................................................................................................393

Contents xi 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 6.28 6.29 6.30 6.31 6.32 6.33 6.34 6.35 6.36 6.37

Gold.........................................................................................................................395 Indium .....................................................................................................................395 Iron..........................................................................................................................395 Lead ........................................................................................................................399 Lithium....................................................................................................................406 Manganese ..............................................................................................................406 Mercury...................................................................................................................410 Molybdenum ...........................................................................................................438 Nickel......................................................................................................................438 Palladium ................................................................................................................444 Platinum ..................................................................................................................444 Plutonium................................................................................................................444 Polonium.................................................................................................................444 Rubidium ................................................................................................................445 Selenium .................................................................................................................445 Silver .......................................................................................................................453 Strontium ................................................................................................................464 Thallium..................................................................................................................464 Tin ...........................................................................................................................465 Titanium..................................................................................................................466 Uranium ..................................................................................................................466 Vanadium................................................................................................................466 Zinc .........................................................................................................................467 Literature Cited.......................................................................................................476

Chapter 7 Concluding Remarks...................................................................... 491 7.1 7.2 7.3 7.4

General......................................................................................................................491 Breadth of Coverage ................................................................................................492 Depth of Coverage ...................................................................................................493 Literature Cited.........................................................................................................493

Subject Index ............................................................................................... 495

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Acknowledgments Early work on this project was conducted at research libraries of the U.S. Environmental Protection Agency, the U.S. 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 U.S. Department of Agriculture located in Beltsville, Maryland. I am obligated to the librarians and staff of the NAL for their assistance in procuring needed research materials.

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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.

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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 research scientist, he served with the U.S. Department of the Interior in the Territory of Alaska (Bristol Bay), New Jersey (Highlands), Maryland (Laurel), and Washington, DC; the U.S. Environmental Protection Agency in Rhode Island (Narragansett); and military service in the U.S. 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 has 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 U.S. 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 several 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.

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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

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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 relation 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

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

15

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

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

<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

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

Reference

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

Reference

American plaice, Hippoglossoides platessoides; muscle

4.4 FW

11

Atlantic halibut, Hippoglossus hippoglossus; fishmeal Whole Aqueous phase Lipid phase Hexane extract Hexane/isopropanol extract

<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

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

Reference

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

Bluefin tuna, Thunnus thynnus; fishmeal Whole Aqueous phase Lipid phase; hexane extract vs. hexane/ isopropanol extract

<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

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 European bass, Morone labrax; muscle Striped bass, Morone saxatilis 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

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

Concentration

Reference

Alaska, Adak Island; June 2004 Flathead sole, Hippoglossoides elassodon Liver Kidney Muscle Great sculpin, Myoxocephalus polyacanthocephalus Liver Kidney Muscle

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

a

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

Blackfin tuna, Thunnus atlanticus; otoliths; Gulf of Mexico; 2002

0.0032 DW

18

Turkey; 2005; Black Sea vs. Aegean Sea European anchovy, Engraulis encrasicolus Muscle Liver Picarel, Spicara smaris Muscle Liver

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

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

Concentration

Reference

Alaska, Adak Island; June 2004 Flathead sole, Hippoglossoides elassodon Kidney Liver Muscle Great sculpin, Myoxocephalus polyacanthocephalus Kidney Liver Muscle

0.34 FW 0.89 FW 0.36 FW

24 24 24

0.41FW 0.98 FW 0.47 FW

24 24 24

Baltic herring, Clupea harengus; whole

0.45 DW

27

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

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

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

a

115 115 115

(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

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

5

(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

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

7 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

Carangid, Trachurops crumenophthalmus; muscle

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, 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

Concentration

Reference

Alaska, Adak Island; June 2004 Flathead sole, Hippoglossoides elassodon Kidney Liver Muscle Great sculpin, Myoxocephalus polyacanthocephalus Kidney Liver Muscle

5.21 FW 2.60 FW 0.40 FW

26 26 26

1.86 FW 2.08 FW 0.61 FW

26 26 26

Halfbridled goby, Arenigobius frenatus; Australia; industrialized site vs. reference estuary Gonad Muscle

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

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.

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

a

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

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

Leatherback turtle, Dermochelys coriacea United Kingdom coastal waters; found stranded Liver Muscle Blubber Mexico; Pacific Ocean coast; eggshell French Guiana; 2006; females Blood Eggs Olive Ridley turtle; Lepidochelys olivacea India; egg Shell Albumen-yolk Whole

Not detectable Not detectable 0.016 FW

a

9 9 9

0.22 DW 0.06 DW <0.01 DW 0.9 DW

6 6 6 7

0.08 FW 0.02 FW

5 5

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;

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.

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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

Reference

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

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

a

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

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

119.4-139.0 FW vs. 116.0-130.4 FW 96.1-144.0 FW

32 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 (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 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 Osprey; nestlings; Chesapeake Bay, 2000-2001 vs. Delaware Bay, 2002; max. values Blood Feathers

Cont’d

Concentration 67.0 FW vs. 38.0 FW

Reference

a

6

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

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

(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).

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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.

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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

Southern elephant seal, Mirounga leonina; molted fur; Shetland Islands; juveniles vs. adult females

(<0.003-0.48) DW vs. (<0.003-0.74) DW

21

Dall’s porpoise, Phocoenoides dalli; Japan; February 2006; male; harpooned Blubber Liver, kidney, muscle, skin, bone, intestine, spleen, diaphragm, cerebrum, stomach Heart, lung, pancreas

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

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

Stellar sea lion, Eumetopias jubatus; teeth; North Pacific Ocean; 1968-1999

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

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 13 13 13 13 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

(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

0.55 (0.08-1.3) DW

13

Harbor seal, Phoca vitulina; blood Captive animals Wild; North Sea Wadden Sea; 2004-2005; German site vs. Danish site

0.002-0.004 FW 0.001-0.011 FW 0.005 FW vs. 0.006 FW

16 17 19

Dall’s porpoise, Phocoenoides dalli; Japan; 2006; harpooned male Liver Kidney, bone, heart, intestine, pancreas, stomach Muscle, skin, lung, spleen, diaphragm, blubber, cerebrum

1.1 FW 0.01-0.04 FW

14 14

0.004-0.009 FW

14

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

<0.9-17.2 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; mac. 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

Pinnipeds; 4 species; northern Pacific; liver Northern fur seal, Callorhinus ursinus; subadult males; July 1992; Pribilof Islands, Bering Sea

(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

(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.

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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

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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.

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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