Advances In Marine Biology, Volume 58

Advances in MARINE BIOLOGY Series Editor MICHAEL LESSER Department of Molecular, Cellular, and Biomedical Sciences Uni...

Author: Michael Lesser

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Advances in MARINE BIOLOGY Series Editor

MICHAEL LESSER Department of Molecular, Cellular, and Biomedical Sciences University of New Hampshire, Durham, USA Editors Emeritus

LEE A. FUIMAN University of Texas at Austin

CRAIG M. YOUNG Oregon Institute of Marine Biology Advisory Editorial Board

ANDREW J. GOODAY Southampton Oceanography Centre

SANDRA E. SHUMWAY University of Connecticut

Academic Press is an imprint of Elsevier 32 Jamestown Road, London NW1 7BY, UK Radarweg 29, PO Box 211, 1000 AE Amsterdam, The Netherlands Linacre House, Jordan Hill, Oxford OX2 8DP, UK 30 Corporate Drive, Suite 400, Burlington, MA 01803, USA 525 B Street, Suite 1900, San Diego, CA 92101-4495, USA First edition 2010 Copyright # 2010 Elsevier Ltd. 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 (+44) (0) 1865 843830; fax (+44) (0) 1865 853333; email: [email protected]. Alternatively you can submit your request online by visiting the Elsevier web site at http://www.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. Because of rapid advances in the medical sciences, in particular, independent verification of diagnoses and drug dosages should be made. ISBN: 978-0-12-381015-1 ISSN: 0065-2881 For information on all Academic Press publications visit our website at elsevierdirect.com Printed and bound in UK 10 11 12 10 9 8 7 6 5 4 3 2 1

CONTRIBUTORS TO VOLUME 58

Jacopo Aguzzi Institut de Cie`ncies del Mar (ICM-CSIC), Passeig Marı´tim de la Barceloneta 37-49, Barcelona 08003, Spain D. M. Bailey Division of Ecology and Evolutionary Biology, University of Glasgow, Glasgow, United Kingdom Mark Belchier British Antarctic Survey, NERC, High Cross, Madingley Road, Cambridge, CB3 0ET, UK D. S. M. Billett National Oceanography Centre, Southampton, University of Southampton Waterfront Campus, European Way, Southampton, United Kingdom Paul Brickle Fisheries Department, Directorate of Natural Resources, FIPASS, Falkland Islands, FIQQ 1ZZ, and School of Biological Sciences (Zoology), University of Aberdeen, Tillydrone Avenue, Aberdeen, Scotland, AB24 2TZ, UK Judith Brown Government of South Georgia and the South Sandwich Islands, Government House, Stanley, Falkland Islands, FIQQ 1ZZ, and Fisheries Department, Directorate of Natural Resources, FIPASS, Falkland Islands, FIQQ 1ZZ, and School of Biological Sciences (Zoology), University of Aberdeen, Tillydrone Avenue, Aberdeen, Scotland, AB24 2TZ, UK P. Chevaldonne´ CNRS—UMR DIMAR, Station Marine d’Endoume, Centre d’Oce´anologie de Marseille, Rue de la Batterie des Lions, Marseille, France A. Colac¸o IMAR and Department of Oceanography and Fisheries, University of Azores, Cais de Sta Cruz, Horta, Portugal Martin A. Collins Government of South Georgia and the South Sandwich Islands, Government House, Stanley, Falkland Islands, FIQQ 1ZZ, and School of Biological Sciences (Zoology), University of Aberdeen, Tillydrone Avenue, Aberdeen, Scotland

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Contributors

Joan B. Company Institut de Cie`ncies del Mar (ICM-CSIC), Passeig Marı´tim de la Barceloneta 37-49, Barcelona 08003, Spain J. Copley School of Ocean and Earth Science, University of Southampton, National Oceanography Centre, Southampton, United Kingdom D. Cuvelier IMAR and Department of Oceanography and Fisheries, University of Azores, Cais de Sta Cruz, Horta, Portugal D. Desbruye`res IFREMER -Centre de Brest, BP 70, De´partement Etude des Ecosyste`mes Profonds, Laboratoire Environnement Profond, Plouzane, France A. G. Glover Zoology Department, The Natural History Museum, London, United Kingdom A. J. Gooday National Oceanography Centre, Southampton, University of Southampton Waterfront Campus, European Way, Southampton, United Kingdom V. Kalogeropoulou Hellenic Centre for Marine Research, Heraklion, Crete, Greece M. Klages Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen, Bremerhaven, Germany N. Lampadariou Hellenic Centre for Marine Research, Heraklion, Crete, Greece C. Lejeusne CNRS—UMR DIMAR, Station Marine d’Endoume, Centre d’Oce´anologie de Marseille, Rue de la Batterie des Lions, Marseille, France N. C. Mestre School of Ocean and Earth Science, University of Southampton, National Oceanography Centre, Southampton, United Kingdom Hilario Murua AZTI Tecnalia, Herrerra Kaia, Portualde z/g, Pasaia (Basque Country), Spain G. L. J. Paterson Zoology Department, The Natural History Museum, London, United Kingdom T. Perez CNRS—UMR DIMAR, Station Marine d’Endoume, Centre d’Oce´anologie de Marseille, Rue de la Batterie des Lions, Marseille, France

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H. Ruhl National Oceanography Centre, Southampton, University of Southampton Waterfront Campus, European Way, Southampton, United Kingdom J. Sarrazin IFREMER -Centre de Brest, BP 70, De´partement Etude des Ecosyste`mes Profonds, Laboratoire Environnement Profond, Plouzane, France T. Soltwedel Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen, Bremerhaven, Germany E. H. Soto Facultad de Ciencias del Mar y de Recursos Naturales, Universidad de Valparaı´so, Vin˜a del Mar, Chile S. Thatje School of Ocean and Earth Science, University of Southampton, National Oceanography Centre, Southampton, United Kingdom A. Tselepides University of Piraeus, Deptment of Maritime Studies, Piraeus, Greece S. Van Gaever Ghent University, Biology Department, Marine Biology Section, Krijgslaan 281/S8, Ghent, Belgium A. Vanreusel Ghent University, Biology Department, Marine Biology Section, Krijgslaan 281/S8, Ghent, Belgium

SERIES CONTENTS

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LAST FIFTEEN YEARS*

Volume 30, 1994. Vincx, M., Bett, B. J., Dinet, A., Ferrero, T., Gooday, A. J., Lambshead, P. J. D., Pfannku¨che, O., Soltweddel, T. and Vanreusel, A. Meiobenthos of the deep Northeast Atlantic. pp. 1–88. Brown, A. C. and Odendaal, F. J. The biology of oniscid isopoda of the genus Tylos. pp. 89–153. Ritz, D. A. Social aggregation in pelagic invertebrates. pp. 155–216. Ferron, A. and Legget, W. C. An appraisal of condition measures for marine fish larvae. pp. 217–303. Rogers, A. D. The biology of seamounts. pp. 305–350. Volume 31, 1997. Gardner, J. P. A. Hybridization in the sea. pp. 1–78. Egloff, D. A., Fofonoff, P. W. and Onbe´, T. Reproductive behaviour of marine cladocerans. pp. 79–167. Dower, J. F., Miller, T. J. and Leggett, W. C. The role of microscale turbulence in the feeding ecology of larval fish. pp. 169–220. Brown, B. E. Adaptations of reef corals to physical environmental stress. pp. 221–299. Richardson, K. Harmful or exceptional phytoplankton blooms in the marine ecosystem. pp. 301–385. Volume 32, 1997. Vinogradov, M. E. Some problems of vertical distribution of mesoand macroplankton in the ocean. pp. 1–92. Gebruk, A. K., Galkin, S. V., Vereshchaka, A. J., Moskalev, L. I. and Southward, A. J. Ecology and biogeography of the hydrothermal vent fauna of the Mid-Atlantic Ridge. pp. 93–144. Parin, N. V., Mironov, A. N. and Nesis, K. N. Biology of the Nazca and Sala y Gomez submarine ridges, an outpost of the Indo-West Pacific fauna in the eastern Pacific Ocean: composition and distribution of the fauna, its communities and history. pp. 145–242. Nesis, K. N. Goniatid squids in the subarctic North Pacific: ecology, biogeography, niche diversity, and role in the ecosystem. pp. 243–324. Vinogradova, N. G. Zoogeography of the abyssal and hadal zones. pp. 325–387. Zezina, O. N. Biogeography of the bathyal zone. pp. 389–426. *The full list of contents for volumes 1–37 can be found in volume 38.

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Sokolova, M. N. Trophic structure of abyssal macrobenthos. pp. 427–525. Semina, H. J. An outline of the geographical distribution of oceanic phytoplankton. pp. 527–563. Volume 33, 1998. Mauchline, J. The biology of calanoid copepods. pp. 1–660. Volume 34, 1998. Davies, M. S. and Hawkins, S. J. Mucus from marine molluscs. pp. 1–71. Joyeux, J. C. and Ward, A. B. Constraints on coastal lagoon fisheries. pp. 73–199. Jennings, S. and Kaiser, M. J. The effects of fishing on marine ecosystems. pp. 201–352. Tunnicliffe, V., McArthur, A. G. and McHugh, D. A biogeographical perspective of the deep-sea hydrothermal vent fauna. pp. 353–442. Volume 35, 1999. Creasey, S. S. and Rogers, A. D. Population genetics of bathyal and abyssal organisms. pp. 1–151. Brey, T. Growth performance and mortality in aquatic macrobenthic invertebrates. pp. 153–223. Volume 36, 1999. Shulman, G. E. and Love, R. M. The biochemical ecology of marine fishes. pp. 1–325. Volume 37, 1999. His, E., Beiras, R. and Seaman, M. N. L. The assessment of marine pollution—bioassays with bivalve embryos and larvae. pp. 1–178. Bailey, K. M., Quinn, T. J., Bentzen, P. and Grant, W. S. Population structure and dynamics of walleye pollock, Theragra chalcogramma. pp. 179–255. Volume 38, 2000. Blaxter, J. H. S. The enhancement of marine fish stocks. pp. 1–54. Bergstro¨m, B. I. The biology of Pandalus. pp. 55–245. Volume 39, 2001. Peterson, C. H. The ‘‘Exxon Valdez’’ oil spill in Alaska: acute indirect and chronic effects on the ecosystem. pp. 1–103. Johnson, W. S., Stevens, M. and Watling, L. Reproduction and development of marine peracaridans. pp. 105–260.

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Rodhouse, P. G., Elvidge, C. D. and Trathan, P. N. Remote sensing of the global light-fishing fleet: an analysis of interactions with oceanography, other fisheries and predators. pp. 261–303. Volume 40, 2001. Hemmingsen, W. and MacKenzie, K. The parasite fauna of the Atlantic cod, Gadus morhua L. pp. 1–80. Kathiresan, K. and Bingham, B. L. Biology of mangroves and mangrove ecosystems. pp. 81–251. Zaccone, G., Kapoor, B. G., Fasulo, S. and Ainis, L. Structural, histochemical and functional aspects of the epidermis of fishes. pp. 253–348. Volume 41, 2001. Whitfield, M. Interactions between phytoplankton and trace metals in the ocean. pp. 1–128. Hamel, J.-F., Conand, C., Pawson, D. L. and Mercier, A. The sea cucumber Holothuria scabra (Holothuroidea: Echinodermata): its biology and exploitation as beche-de-Mer. pp. 129–223. Volume 42, 2002. Zardus, J. D. Protobranch bivalves. pp. 1–65. Mikkelsen, P. M. Shelled opisthobranchs. pp. 67–136. Reynolds, P. D. The Scaphopoda. pp. 137–236. Harasewych, M. G. Pleurotomarioidean gastropods. pp. 237–294. Volume 43, 2002. Rohde, K. Ecology and biogeography of marine parasites. pp. 1–86. Ramirez Llodra, E. Fecundity and life-history strategies in marine invertebrates. pp. 87–170. Brierley, A. S. and Thomas, D. N. Ecology of southern ocean pack ice. pp. 171–276. Hedley, J. D. and Mumby, P. J. Biological and remote sensing perspectives of pigmentation in coral reef organisms. pp. 277–317. Volume 44, 2003. Hirst, A. G., Roff, J. C. and Lampitt, R. S. A synthesis of growth rates in epipelagic invertebrate zooplankton. pp. 3–142. Boletzky, S. von. Biology of early life stages in cephalopod molluscs. pp. 143–203. Pittman, S. J. and McAlpine, C. A. Movements of marine fish and decapod crustaceans: process, theory and application. pp. 205–294. Cutts, C. J. Culture of harpacticoid copepods: potential as live feed for rearing marine fish. pp. 295–315.

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Volume 45, 2003. Cumulative Taxonomic and Subject Index. Volume 46, 2003. Gooday, A. J. Benthic foraminifera (Protista) as tools in deep-water palaeoceanography: environmental influences on faunal characteristics. pp. 1–90. Subramoniam, T. and Gunamalai, V. Breeding biology of the intertidal sand crab, Emerita (Decapoda: Anomura). pp. 91–182 Coles, S. L. and Brown, B. E. Coral bleaching—capacity for acclimatization and adaptation. pp. 183–223. Dalsgaard J., St. John M., Kattner G., Mu¨ller-Navarra D. and Hagen W. Fatty acid trophic markers in the pelagic marine environment. pp. 225–340. Volume 47, 2004. Southward, A. J., Langmead, O., Hardman-Mountford, N. J., Aiken, J., Boalch, G. T., Dando, P. R., Genner, M. J., Joint, I., Kendall, M. A., Halliday, N. C., Harris, R. P., Leaper, R., Mieszkowska, N., Pingree, R. D., Richardson, A. J., Sims, D.W., Smith, T., Walne, A. W. and Hawkins, S. J. Long-term oceanographic and ecological research in the western English Channel. pp. 1–105. Queiroga, H. and Blanton, J. Interactions between behaviour and physical forcing in the control of horizontal transport of decapod crustacean larvae. pp. 107–214. Braithwaite, R. A. and McEvoy, L. A. Marine biofouling on fish farms and its remediation. pp. 215–252. Frangoulis, C., Christou, E. D. and Hecq, J. H. Comparison of marine copepod outfluxes: nature, rate, fate and role in the carbon and nitrogen cycles. pp. 253–309. Volume 48, 2005. Canfield, D. E., Kristensen, E. and Thamdrup, B. Aquatic Geomicrobiology. pp. 1–599. Volume 49, 2005. Bell, J. D., Rothlisberg, P. C., Munro, J. L., Loneragan, N. R., Nash, W. J., Ward, R. D. and Andrew, N. L. Restocking and stock enhancement of marine invertebrate fisheries. pp. 1–358. Volume 50, 2006. Lewis, J. B. Biology and ecology of the hydrocoral Millepora on coral reefs. pp. 1–55.

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Harborne, A. R., Mumby, P. J., Micheli, F., Perry, C. T., Dahlgren, C. P., Holmes, K. E., and Brumbaugh, D. R. The functional value of Caribbean coral reef, seagrass and mangrove habitats to ecosystem processes. pp. 57–189. Collins, M. A. and Rodhouse, P. G. K. Southern ocean cephalopods. pp. 191–265. Tarasov, V. G. EVects of shallow-water hydrothermal venting on biological communities of coastal marine ecosystems of the western Pacific. pp. 267–410. Volume 51, 2006. Elena Guijarro Garcia. The fishery for Iceland scallop (Chlamys islandica) in the Northeast Atlantic. pp. 1–55. JeVrey, M. Leis. Are larvae of demersal fishes plankton or nekton? pp. 57–141. John C. Montgomery, Andrew Jeffs, Stephen D. Simpson, Mark Meekan and Chris Tindle. Sound as an orientation cue for the pelagic larvae of reef fishes and decapod crustaceans. pp. 143–196. Carolin E. Arndt and Kerrie M. Swadling. Crustacea in Arctic and Antarctic sea ice: Distribution, diet and life history strategies. pp. 197–315. Volume 52, 2007. Leys, S. P., Mackie, G. O. and Reiswig, H. M. The Biology of Glass Sponges. pp. 1–145. Garcia E. G. The Northern Shrimp (Pandalus borealis) Offshore Fishery in the Northeast Atlantic. pp. 147–266. Fraser K. P. P. and Rogers A. D. Protein Metabolism in Marine Animals: The underlying Mechanism of Growth. pp. 267–362. Volume 53, 2008. Dustin J. Marshall and Michael J. Keough. The Evolutionary Ecology of Offspring Size in Marine Invertebrates. pp. 1–60. Kerry A. Naish, Joseph E. Taylor III, Phillip S. Levin, Thomas P. Quinn, James R. Winton, Daniel Huppert, and Ray Hilborn. An Evaluation of the Effects of Conservation and Fishery Enhancement Hatcheries on Wild Populations of Salmon. pp. 61–194. Shannon Gowans, Bernd Wu¨rsig, and Leszek Karczmarski. The Social Structure and Strategies of Delphinids: Predictions Based on an Ecological Framework. pp. 195–294.

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Volume 54, 2008. Bridget S. Green. Maternal Effects in Fish Populations. pp. 1–105. Victoria J. Wearmouth and David W. Sims. Sexual Segregation in Marine Fish, Reptiles, Birds and Mammals: Behaviour Patterns, Mechanisms and Conservation Implications. pp. 107–170. David W. Sims. Sieving a Living: A Review of the Biology, Ecology and Conservation Status of the Plankton-Feeding Basking Shark Cetorhinus Maximus. pp. 171–220. Charles H. Peterson, Kenneth W. Able, Christin Frieswyk DeJong, Michael F. Piehler, Charles A. Simenstad, and Joy B. Zedler. Practical Proxies for Tidal Marsh Ecosystem Services: Application to Injury and Restoration. pp. 221–266. Volume 55, 2008. Annie Mercier and Jean-Franc¸ois Hamel. Introduction. pp. 1–6. Annie Mercier and Jean-Franc¸ois Hamel. Gametogenesis. pp. 7–72. Annie Mercier and Jean-Franc¸ois Hamel. Spawning. pp. 73–168. Annie Mercier and Jean-Franc¸ois Hamel. Discussion. pp. 169–194. Volume 56, 2009. Philip C. Reid, Astrid C. Fischer, Emily Lewis-Brown, Michael P. Meredith, Mike Sparrow, Andreas J. Andersson, Avan Antia, Nicholas R. Bates, Ulrich Bathmann, Gregory Beaugrand, Holger Brix, Stephen Dye, Martin Edwards, Tore Furevik, Reidun Gangst, Hja´lmar Ha´tu´n, Russell R. Hopcroft, Mike Kendall, Sabine Kasten, Ralph Keeling, Corinne Le Que´re´, Fred T. Mackenzie, Gill Malin, ´ lafsson, Charlie Paull, Eric Rignot, Koji Cecilie Mauritzen, Jo´n O Shimada, Meike Vogt, Craig Wallace, Zhaomin Wang and Richard Washington. Impacts of the Oceans on Climate Change. pp. 1–150. Elvira S. Poloczanska, Colin J. Limpus and Graeme C. Hays. Vulnerability of Marine Turtles to Climate Change. pp. 151–212. Nova Mieszkowska, Martin J. Genner, Stephen J. Hawkins and David W. Sims. Effects of Climate Change and Commercial Fishing on Atlantic Cod Gadus morhua. pp. 213–274. Iain C. Field, Mark G. Meekan, Rik C. Buckworth and Corey J. A. Bradshaw. Susceptibility of Sharks, Rays and Chimaeras to Global Extinction. pp. 275–364. Milagros Penela-Arenaz, Juan Bellas and Elsa Va´zquez. Effects of the Prestige Oil Spill on the Biota of NW Spain: 5 Years of Learning. pp. 365–396.

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Volume 57, 2010. Geraint A. Tarling, Natalie S. Ensor, Torsten Fregin, William P. Goodall-Copestake and Peter Fretwell. An Introduction to the Biology of Northern Krill (Meganyctiphanes norvegica Sars). pp. 1–40. Tomaso Patarnello, Chiara Papetti and Lorenzo Zane. Genetics of Northern Krill (Meganyctiphanes norvegica Sars). pp. 41–58. Geraint A. Tarling. Population Dynamics of Northern Krill (Meganyctiphanes norvegica Sars). pp. 59–90. John I. Spicer and Reinhard Saborowski. Physiology and Metabolism of Northern Krill (Meganyctiphanes norvegica Sars). pp. 91–126. Katrin Schmidt. Food and Feeding in Northern Krill (Meganyctiphanes norvegica Sars). pp. 127–172. Friedrich Buchholz and Cornelia Buchholz. Growth and Moulting in Northern Krill (Meganyctiphanes norvegica Sars). pp. 173–198. Janine Cuzin-Roudy. Reproduction in Northern Krill. pp. 199–230. Edward Gaten, Konrad Wiese and Magnus L. Johnson. LaboratoryBased Observations of Behaviour in Northern Krill (Meganyctiphanes norvegica Sars). pp. 231–254. Stein Kaartvedt. Diel Vertical Migration Behaviour of the Northern Krill (Meganyctiphanes norvegica Sars). pp. 255–276. Yvan Simard and Michel Harvey. Predation on Northern Krill (Meganyctiphanes norvegica Sars). pp. 277–306.

C H A P T E R

O N E

Temporal Change in Deep-Sea Benthic Ecosystems: A Review of the Evidence From Recent Time-Series Studies A. G. Glover,* A. J. Gooday,†,1 D. M. Bailey,‡ D. S. M. Billett,† P. Chevaldonne´,§ A. Colac¸o,} J. Copley,§§ D. Cuvelier,} D. Desbruye`res,k V. Kalogeropoulou,# M. Klages,** N. Lampadariou,# C. Lejeusne,§ N. C. Mestre,§§ G. L. J. Paterson,* T. Perez,§ H. Ruhl,† J. Sarrazin,k T. Soltwedel,** E. H. Soto,†† S. Thatje,§§ A. Tselepides,}} S. Van Gaever,‡‡ and A. Vanreusel‡‡ Contents 3 5 7 10 13 15 15 25

1. Introduction 2. Theoretical Framework 2.1. Biological processes and temporal scaling 2.2. Biological drivers 2.3. Geological drivers 3. Case Studies: Sedimented Environments 3.1. Bathyal sites 3.2. Abyssal sites

* Zoology Department, The Natural History Museum, London, United Kingdom National Oceanography Centre, Southampton, University of Southampton Waterfront Campus, European Way, Southampton, United Kingdom { Division of Ecology and Evolutionary Biology, University of Glasgow, Glasgow, United Kingdom } CNRS—UMR DIMAR, Station Marine d’Endoume, Centre d’Oce´anologie de Marseille, Rue de la Batterie des Lions, Marseille, France } IMAR and Department of Oceanography and Fisheries, University of Azores, Cais de Sta Cruz, Horta, Portugal k IFREMER -Centre de Brest, BP 70, De´partement Etude des Ecosyste`mes Profonds, Laboratoire Environnement Profond, Plouzane, France # Hellenic Centre for Marine Research, Heraklion, Crete, Greece ** Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen, Bremerhaven, Germany {{ Facultad de Ciencias del Mar y de Recursos Naturales, Universidad de Valparaı´so, Vin˜a del Mar, Chile {{ Ghent University, Biology Department, Marine Biology Section, Krijgslaan 281/S8, Ghent, Belgium }} School of Ocean and Earth Science, University of Southampton, National Oceanography Centre, Southampton, United Kingdom }} University of Piraeus, Deptment of Maritime Studies, Piraeus, Greece 1 Corresponding author: Email: [email protected] {

Advances in Marine Biology, Volume 58 ISSN 0065-2881, DOI: 10.1016/S0065-2881(10)58001-5

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2010 Elsevier Ltd. All rights reserved.

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4. Case Studies: Chemosynthetic Ecosystems 4.1. Hydrothermal vents 4.2. Cold seeps 4.3. Whale-falls 5. Discussion 5.1. Biological responses to environmental change 5.2. Broader context: Climate, evolution and stochastic events 5.3. Temporal change in shallow-water versus deep-water settings 6. Conclusions 6.1. Hypotheses 6.2. Future directions Acknowledgements References

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Abstract Societal concerns over the potential impacts of recent global change have prompted renewed interest in the long-term ecological monitoring of large ecosystems. The deep sea is the largest ecosystem on the planet, the least accessible, and perhaps the least understood. Nevertheless, deep-sea data collected over the last few decades are now being synthesised with a view to both measuring global change and predicting the future impacts of further rises in atmospheric carbon dioxide concentrations. For many years, it was assumed by many that the deep sea is a stable habitat, buffered from short-term changes in the atmosphere or upper ocean. However, recent studies suggest that deep-seafloor ecosystems may respond relatively quickly to seasonal, inter-annual and decadal-scale shifts in upper-ocean variables. In this review, we assess the evidence for these long-term (i.e. inter-annual to decadal-scale) changes both in biologically driven, sedimented, deep-sea ecosystems (e.g. abyssal plains) and in chemosynthetic ecosystems that are partially geologically driven, such as hydrothermal vents and cold seeps. We have identified 11 deep-sea sedimented ecosystems for which published analyses of long-term biological data exist. At three of these, we have found evidence for a progressive trend that could be potentially linked to recent climate change, although the evidence is not conclusive. At the other sites, we have concluded that the changes were either not significant, or were stochastically variable without being clearly linked to climate change or climate variability indices. For chemosynthetic ecosystems, we have identified 14 sites for which there are some published long-term data. Data for temporal changes at chemosynthetic ecosystems are scarce, with few sites being subjected to repeated visits. However, the limited evidence from hydrothermal vents suggests that at fast-spreading centres such as the East Pacific Rise, vent communities are impacted on decadal scales by stochastic events such as volcanic eruptions, with associated fauna showing complex patterns of community succession. For the slow-spreading centres such as the Mid-Atlantic Ridge, vent sites appear to be stable over the time periods measured, with no discernable long-term trend. At cold seeps, inferences based on spatial studies in the Gulf of Mexico, and data on organism longevity, suggest that these

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sites are stable over many hundreds of years. However, at the Haakon Mosby mud volcano, a large, well-studied seep in the Barents Sea, periodic mud slides associated with gas and fluid venting may disrupt benthic communities, leading to successional sequences over time. For chemosynthetic ecosystems of biogenic origin (e.g. whale-falls), it is likely that the longevity of the habitat depends mainly on the size of the carcass and the ecological setting, with large remains persisting as a distinct seafloor habitat for up to 100 years. Studies of shallow-water analogs of deep-sea ecosystems such as marine caves may also yield insights into temporal processes. Although it is obvious from the geological record that past climate change has impacted deep-sea faunas, the evidence that recent climate change or climate variability has altered deep-sea benthic communities is extremely limited. This mainly reflects the lack of remote sensing of this vast seafloor habitat. Current and future advances in deep-ocean benthic science involve new remote observing technologies that combine a high temporal resolution (e.g. cabled observatories) with spatial capabilities (e.g. autonomous vehicles undertaking image surveys of the seabed).

1. Introduction The recent rise of ‘global change science’, fuelled by concerns over the Earth’s changing climate, has demanded a more integrated and holistic outlook from ecologists. Within the working lifetimes of scientists, large-scale climatic changes are occurring as a result of radiative forcing caused mainly by the rapid rise in atmospheric concentrations of carbon dioxide, methane, and nitrous oxide (IPCC, 2007). Although computer-based modelling approaches have been the mainstay of climate science itself, the enormously complex nature of the biosphere and its interacting ecosystems, communities, and populations has made modelling the actual impacts of climate change notoriously difficult. Furthermore, ecologists have struggled to either maintain or activate the longterm ecological monitoring stations that are required to validate any predictive models. Nowhere is this more of an issue than in the deep ocean, an environment that covers approximately 60% of the Earth’s surface. Deep-sea biology is a relatively young science. Prior to the nineteenth century, almost nothing was known about environments deeper than the shallow sub-tidal. The industrial revolution, the rise of evolutionary theory, and the laying of deep telegraphic cables led to the first deep-sea biology expeditions of the nineteenth century, and the discovery of abundant, diverse life at all depths of the ocean. The twentieth century saw the detection of high biodiversity in deep-sea sediments (Hessler and Sanders, 1967; Grassle, 1991) and the paradigm-shifting discovery of life at deep hydrothermal vents (Lonsdale, 1977) and cold hydrocarbon seeps (Paull et al., 1984). Yet, we enter the twenty-first century—perhaps, the climate-change century— knowing little about temporal processes in deep ecosystems, and even lacking

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basic knowledge of their biological composition. Without doubt, there is a pressing need for both data-mining of existing collections, and the initiation of new, science and technology-driven monitoring programmes in the deep ocean. This review of long-term change in deep-sea benthic ecosystems is intended to highlight these gaps, and to draw together data from a diverse range of ongoing temporal studies in the deep sea. Historically, the deep ocean was considered a relatively stable environment, buffered from the climatic and geological drivers that dominate terrestrial and littoral marine ecosystems. This view led nineteenth and early twentieth century deep-sea explorers to believe that relic faunas known only from the fossil record might still exist in isolated deep-sea basins (reviewed in Koslow, 2007). More recent studies have failed to find much support for this; deep-sea faunas are often remarkably similar in higher-level taxonomic composition to those in shallow sub-tidal and even inter-tidal systems. Even at deep-sea hydrothermal vents, the hard-substrate community often shows both evolutionary and ecological links to analogous communities in shelf habitats. Process-based ecological studies are now starting to show that far from being a stable, buffered system, the deep ocean is ‘punctuated’ in time and space by a range of powerful drivers, which include pulses of sinking phytodetritus, emissions from volcanic vents, large carcass-falls, turbidity currents, shifts in ocean currents and oxygen stress, as well as present and possible future human impacts such as deep-water fishing and mining (Smith, 1994; Gooday, 2002; Glover and Smith, 2003). These processes span a range of temporal and spatial scales and as such are significant on both ecological and evolutionary timescales. Historically, ecological studies in the deep sea have often been habitat focused, while evolutionary studies have generally been taxon focused. In this review, we bring together studies from a range of habitats and taxa that address the theme of long-term (inter-annual to multi-decadal) temporal trends in benthic ecosystems. This time-scale is too short to be normally resolved in the deep-sea sediment record and yet too long to have been addressed by most ecological monitoring programmes. Whilst there have been several studies of long-term changes in shallow-water marine ecosystems (e.g. Southward et al., 2005; Robinson and Frid, 2008), it is only recently that long-term sampling has started to reveal coherent trends at a number of deep-sea sites (Billett et al., 2001, 2010; K. L. Smith et al., 2006). Furthermore, the first data from satellite-based ocean productivity sensors only now approach decadal scales (Behrenfeld et al., 2006). Thus, now is an appropriate moment to assess possible links between decadal-scale climate change and deep-sea ecosystems. We review a range of studies addressing multi-year to multi-decadal scale changes at deep-sea chemosynthetic and non-chemosynthetic ecosystems. Although deep-sea chemosynthetic ecosystems, such as hydrothermal vents and seeps, are driven by quite different physical and chemical processes to sedimented habitats, their fauna share a relatively recent evolutionary

Temporal Change in Deep-Sea Ecosystems

5

origin (Little and Vrijenhoek, 2003) and are likely to show some of the same physiological and metabolic constraints as communities depending on sinking organic particles. New data are emerging on long-term changes at vents, highlighting how geology dynamically influences biology over decadal scales (Cuvelier et al., submitted for publication; Sarrazin et al., 1997). Rather than treating this ecosystem in isolation, we believe that understanding the adaptations of organisms to radical changes in temperature and water chemistry can inform our studies of how lineages and species will respond to the rapid changes predicted by some scenarios (IPCC, 2007). Our review builds on existing knowledge of seasonal variability in the deep sea (Tyler, 1988; Gooday and Turley, 1990; Beaulieu, 2002; Gooday, 2002) and places recent findings in the context of palaeoenvironmental data obtained from deep sediment cores (Discussion Section 5.2.1). However, we do not consider in detail the evidence from the palaeoceanographic record for faunal change occurring over geological time scales. Our review also touches on fisheries data only where they relate to one of our study sites (Section 3.2.1). This topic is reviewed more fully elsewhere in the context of human impacts (Koslow et al., 2000; C. R. Smith et al., 2008). In summary, we will evaluate the following four hypotheses: 1. Deep-sea sedimented ecosystems are subject to biologically driven forcing events induced by climate change or climate variability in recent decades. 2. Chemosynthetic ecosystems are subject to stochastic geological forcing events, which override climatically induced biological processes. 3. Although the drivers are different, there are commonalities in the biological responses observed in these contrasting settings. 4. The deep-sea benthos embodies the influences of climatic changes that have occurred over both geological (evolutionary) and decadal (ecological) timescales.

2. Theoretical Framework The last century saw a revolution in our understanding of the deep ocean, and the animals that live in it. Among the key technical developments that facilitated this new vision was our ability to actually observe deep-sea organisms in their natural habitat (Fig. 1.1). These included firsthand observations through the windows of deep-sea submersibles and the more recent use of remotely operated vehicles (ROVs) and free-vehicle ‘landers’ equipped with cameras and other useful sensors. In two very different environments, direct visual observation was the vital clue to paradigm-shifting discoveries. At the hydrothermal vents of the Galapagos

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B

A

C

D

E

Figure 1.1 Direct visual observation of deep-sea habitats, and shallow-water deep-sea analogs. (A) The Porcupine Abyssal Plain in the north-east Atlantic (4800 m) with visible (green) phytodetritus and three individuals of the elasipodid holothurian Amperimsa rosea, with a coiled gut visible through the transparent bodywall. (B) A field of siboglinid tube worms on the Haakon Mosby Mud Volcano, a 1 km2 construct associated with methane seepage, located at 1255 m depth on the Barents Sea continental slope (C) ‘Lucky Strike’ hydrothermal vent on the Mid-Atlantic Ridge (1690 m). (D) Deep-sea glass sponges (Oopsacas minuta) found in a shallow-water marine cave at 15–25 m depth in the Mediterranean, where habitat conditions are analagous to those in the deep sea. (E) a ‘whale-fall’ (the remains of a dead whale) on the seafloor of the Santa Cruz Basin (NE Pacific; 1600 m depth). Images courtesy of the National Oceanography Centre, Southampton (A), Vicking Cruise 2006 #Ifremer (B), MoMARETO Cruise 2006 #Ifremer (C), Jean-Georges Harmelin, CNRS (D) and Craig R. Smith, University of Hawaii (E).

Rift, the first observations of large clam shells clustering around a venting region were made using a towed video system (Lonsdale, 1977). On the deep abyssal plain of the north-east Atlantic, the first direct observations of the seasonal input of green ‘phytodetritus’ from surface waters were made using a free-vehicle lander with a time-lapse camera (Billett et al., 1983). Both of these discoveries contributed to a new acknowledgement that the deep sea is not quiescent, and that environmental perturbations over different temporal scales are likely to be very important in structuring the deep-sea biological community. In this section, we outline a theoretical framework that deals with change over these temporal scales, and in particular the relative roles of biologically driven and geologically driven processes.

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2.1. Biological processes and temporal scaling Space and time form convenient dimensions upon which to classify natural phenomena, ranging from the diurnal migration of zooplankton, the seasonal impact of hurricanes, the climatic shifts of the Quaternary to the mass extinctions recorded in the deep geological record. In the past, the deep sea was often viewed as a quiescent habitat; the vast, sedimented plains of the abyss undisturbed over millions of years (e.g. Menzies, 1965). This generalisation has been firmly rejected. We now know that the ocean floor is subjected to a variety of disturbances that operate across very broad temporal scales. In this sense, the deep sea can be thought of as encompassing two end-members, namely the abyssal sediments underlying the oligotrophic gyres, where sedimentation is often virtually zero, and the highly dynamic hydrothermal vents, where organism growth rates may be amongst the highest ever recorded. The types of disturbances (or drivers) that impact the deep sea can be arranged on a temporal scale (Table 1.1). Benthic storms (temporally variable periods of high current speeds) can resuspend sediments on daily timescales (Thistle et al., 1991). Food availability can lead to recruitment pulses on intraannual, seasonal scales (Tyler, 1988; Gooday, 2002). Inter-annual shifts in production can cause migrations or changes in the local abundance of some species (Billett et al., 2001). Over decadal scales, changes in oceanic temperature patterns, such as the El Nin˜o Southern Oscillation (ENSO), may cause widespread changes in abyssal food supply (e.g. Levin et al., 2002; Arntz et al., 2006; Ruhl et al., 2008). Also over decadal scales, hydrothermal vents may change in their activity patterns, with consequences for the fauna dependent on them (Van Dover, 2000). Human-induced climate change, acting over periods of 50–100 years (IPCC, 2007), is also thought to be capable of impacting on the deep seafloor, although data are still insufficient to demonstrate this (C. R. Smith et al., 2008; K. L. Smith et al., 2009). Over geological time, orbital periodicity on 100,000-year timescales is probably largely responsible for the glacial/interglacial climatic shifts of the Pleistocene. At the 1–100-My scale, large climatic shifts, continental drift, and episodes of widespread deep-ocean anoxia are believed to have had global-scale impacts on the deep-sea fauna (e.g. Jacobs and Lindberg, 1998). These deep-sea drivers can also be plotted using a range of estimates for both their temporal and spatial impact (Fig. 1.2). Plotted in log–log space, a positive relationship is found between the temporal spacing (i.e. the timescale) of the events and their spatial impact, which for the very large events is limited by the size of the planet. Although the errors are large, and the number of disturbance types limited, the data suggest a predictable powerlaw relationship between the frequency and the severity of the disturbance, and a degree of scale-invariance (i.e. the relationship does not change across spatial or temporal scales). Such power-law relationships can be commonly

Table 1.1 Temporal scales of deep-sea environmental drivers of change, estimated severity and frequency and relevance to ecological and evolutionary scale processes Temporal scale (years)

Spatial scale (km2) 6

0.01 0.1

1 10 1–100

0.5

1 104–1 106

1–5

1 105–1 107

10–20

1 105–1 107

50–100

global

100–100,000

global

1 106– 1 109

global

Driver

Impact

Relevance

Local predation, disturbance Benthic storms, down-slope or canyon sediment transport Seasonal food supply, phytoplankton blooms Inter-annual variability in food supply driven by surface processes or geological stochastic events Decadal shifts including geological stochastic events, trends in surface processes (ENSO, NAO, MEI) Anthropogenically induced rapid climate change Climate change caused by orbital periodicity, solar activity Continental drift, formation of spreading centres

Local disturbance Resuspension of sediments, organic enrichment, disturbance Food availability, growth, recruitment pulse, seasonal migration Food availability, growth, long-term migration

Ecology Ecology

Long-term shifts in community structure and abundance

Ecology - Evolution

Range shifts, local extinction

Ecology - Evolution

Extinction and speciation

Evolution

Speciation and adaptive radiation (e.g. at vent sites)

Evolution

Ecology Ecology

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Temporal Change in Deep-Sea Ecosystems

‘Human’ climate change?

1 × 108

Space (km2)

100

1

‘Natural’ climate change

Inter-annual productivity

1 × 106

1 × 104

C

B

Continental drift, abyssal anoxia

ENSO

Seasonal surface productivity Surface-water blooms

Major sediment slumps

A Local sediment resuspension

Turbidity currents

Minor sediment slides A = Experimental and observational ecology

0.01

B = Remote sensing C = Palaeontological proxies

1 × 10−4 Local disturbance (competition, predation) −6

1 × 10 1 × 10−4

0.01

1

1 × 104 100 Time (yrs)

1 × 106

1 × 108

Figure 1.2 Deep-sea environmental forcing factors (biological as green circles, geological as brown circles) plotted against space (km2 of potential impact) and time (frequency of occurrence) in log–log space. A scale-invariant power-law relationship is evident until the spatial extent of the forcing factor reaches a maximum at the total size of Earth’s marine environment. The time–space scales for human measurement methods are observational and experimental ecology (Box A), remote sensing, for example, satellite ocean colour, (Box B) and palaeontological proxies from deep-sea sediment records and ice cores (Box C). The temporal scale of human-induced climate change (red circle) potentially lies between B and C in a region difficult to monitor using existing technologies.

found in natural systems such as earthquake frequency (Bak and Tang, 1989) and in ecological communities (Pascual and Guichard, 2005). The space–time plot also serves as useful template to assess the human ability to measure these drivers and their impacts (Fig. 1.2—boxes). Measurement methods could include either experimental and observational ecology, remote sensing or the use of palaeontological and geochemical proxies preserved in the sediment record. It is significant that there is little overlap on the space–time plot between these methods. In particular, there is a temporal gap between the time scale for remote sensing, and that for the resolution of palaeontological proxies. Most remote sensing data—for example, ocean colour—are available only for the last 10–15 years (Behrenfeld et al., 2006). With a few exceptions, notably varved sediments in hypoxic basins such as the Cariaco Basin (Black et al., 2007; Section 3.1.3),

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marine sediments yield temporal records with a resolution in excess of 250 years. Within this gap lies the forcing factor of human-induced climate change, where most models forecast significant global changes over the next 50–100 years (IPCC, 2007). It is clear that long-term datasets are required in order to understand the impacts of current warming trends, and projected models. It is no surprise that rather few studies have been conducted in the deep sea, the planet’s remotest and least-accessible ecosystem. Yet it is surprising that few longterm ecological time series studies are available even for shallow-water settings. The best are from the continuous plankton surveys of the North Atlantic (Richardson and Schoeman, 2004) and the north-east Pacific (Roemmich and McGowan, 1995), which have run for over 50 years and show trends that co-vary with recent climatic shifts. For non-pelagic ecosystems, rather little is known on the 50–100 year scale. The longest concerted time series that involve sampling soft-bottom (sediment) communities in coastal and shallow-water settings span shorter periods, for example, 36 years in the North Sea off the Northumberland coast (Frid et al., 2008). Fisheries biologists have collected quantitative data on the benthos in some areas since the 1920s, and qualitative information can be derived from historical sources over centennial time scales (e.g. Jackson et al., 2001; Holm, 2005; Robinson and Frid, 2008). Monitoring of intertidal habitats in SW England since the 1950s has revealed striking changes in the distribution and abundance of barnacle species (Southward et al., 2005). The majority of shallow-water studies, however, fall within the decadal or sub-decadal range, where the influence of climate change is hard to separate from other climatic variations such as ENSO and stochastic shifts in new production and food supply. Even for major variables, such as global ocean productivity, there are currently no more than about 10 years of analysed remote-sensing data (Behrenfeld et al., 2006).

2.2. Biological drivers With few exceptions, the deep sea is a food-limited environment. The sedimented abyssal plains, which constitute the most widespread deepocean environment, are dependent on an allochthonous supply of food in the absence of sunlight and new production. It is therefore a central hypothesis that benthic density and biomass are correlated with the amount of organic material raining down from the surface waters, or transported in by ocean currents (Fig. 1.3). A number of studies support this idea (Thiel, 1979; Rowe, 1983; Sibuet et al., 1989; Gooday and Turley, 1990; Thurston et al., 1994; Rex et al., 2006). Over spatial scales, benthic abundance is expected to be highest where surface productivity is highest. Likewise, changes in surface productivity over time should lead to changes in benthic abundance. But this relationship may be obscured by variations in the

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Temporal Change in Deep-Sea Ecosystems

Solar energy Time

Upper ocean biology

Marine cave

Time

Cold seep Mid-water biology and poc flux

Hydrocarbon (CH4) seeps

Time

Time Time

Hydrothermal vent Benthic biology and sediments

Time

Benthic sediment community

Time

Hydrothermal energy (H2S)

Figure 1.3 Schematic cross-section of the ocean floor, with vertical scale exaggerated, illustrating the typical location of soft-sedimented abyssal plains, regions of hydrothermal venting and cold seep habitats. Shallow-water marine caves, buffered from the effects of solar radiation and shifting temperatures, can provide habitats that are deep-sea analogs. Major energy fluxes illustrated by arrows (yellow—solar radiation, green—biologically mediated processes, brown—geologically mediated processes). For sedimented environments, stochastic shifts, seasonal shifts, inter-annual shifts and climatic trends (illustrated by the graphs of generalised environmental change over time) are transmitted to the upper ocean through atmosphere–ocean dynamics, these shifts are then transmitted through benthic–pelagic coupling to the seafloor several km below, where stochastic variation and climatic trends may be evident in the benthos, albeit muted in response relative to the surface. At hydrothermal vents and hydrocarbon seeps, the energy sources are geological, and temporal changes are stochastic and less influenced by climatic trends. POC refers to Particulate Organic Carbon.

efficiency of export to the deep-sea floor. Quantifying export production using sediment traps and benthic proxies is essential to understanding deepsea benthic–pelagic coupling, which in turn underpins our understanding of how surface-water climate and ‘biological forcing’ drives deep-sea processes over the temporal scales associated with climatic shifts. Studies of export production have usually relied on measuring the amount of particulate organic carbon (POC) flux to the seabed using mid-water moored sediment traps. When reviewed, these data suggest that there is a link between POC flux and surface water productivity, but

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at high levels of production other variables may be more important (Lampitt and Antia, 1997). Thus an increase in primary productivity, over both spatial and temporal scales, may not always be reflected in an increase in POC flux. Likewise, increased POC flux may not necessarily coincide with a peak in surface productions (e.g. Lampitt et al., in press). This is because of the nature of primary production, the efficiency of the biological pump, the great distance the organic material has to sink (over 4 km in the abyss) and the resulting action of mid-water variables such as horizontal transport caused by currents and consumption by pelagic animals. The settling particles are of four main types: (1) fine particulates, (2) visible macroaggregates of microscopic plant and animal remains known as phytodetritus (Fig. 1.4), (3) large plant remains such as macroalgae, seagrasses, and wood of terrestrial origin, and (4) large animal remains such as vertebrate carcasses (see Section 4.3). Down-slope transport, submarine slides, and turbidity currents may also inject organic materials into the deep sea (Carey, 1981). Phytodetritus accounts for much of the organic input to the deep seafloor. It generally comprises a wide variety of planktonic remains, including diatoms, coccolithophores, dinoflagellates, foraminferans, and faecal pellets embedded within a gelatinous matrix (Thiel et al., 1989). Intact specimens of the diatom Rhizosolenia sp., recorded in box cores from 4400 m depth in the central Pacific, could be directly correlated with an observed bloom of this species in surface waters (C. R. Smith et al., 1996). On both the Atlantic and Pacific seafloor, phytodetritus has been observed accumulating

A

B

Figure 1.4 In deep-sea sedimented environments, food for benthos on the seafloor arrives in temporally variable pulses of green-tinted phytodetritus, macro-aggregates of microscopic plant remains and biological detritus produced in the upper water column. (A) Image of a 2.5 cm layer of intact phytodetritus recovered from a multi-core tube in 600 m water depth from the Southern Ocean (B) Seafloor at 600 m, Southern Ocean, showing thick layer of phytodetritus and evidence of phytodetritus consumption by surface deposit feeders. Scale bars (A) 2.5 cm, (B) 10 cm. Photos A and B courtesy of Craig R. Smith, University of Hawaii.

Temporal Change in Deep-Sea Ecosystems

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in biogenic depressions, tracks, and holes leading to a patchy distribution of the material (Billett et al., 1983; C. R. Smith et al., 1996). Phytodetritus is eventually consumed by motile surface deposit feeders, incorporated into the sediment through bioturbation, or washed away by deep-sea currents. Timelapse imagery has shown that the residence time for phytodetritus is on a scale of days to months (Rice et al., 1994; Smith and Druffel, 1998). The best evidence for a direct link between surface waters and the deep sea has come from studies of the impact of seasonal phytodetritus deposition in the northeast Atlantic and central and northeast Pacific (Gooday and Turley, 1990; Gooday, 2002; Smith et al., 2009). Holothurians may actively select and consume phytodetritus (Billett et al., 1988). Echinoids may exhibit seasonal to interannual reproductive strategies in response to phytodetrital input (Tyler, 1988; Booth et al., 2008). Benthic abundance is higher in phytodetritus-rich sites compared to those without phytodetritus (Paterson et al., 1994a,b; Sibuet et al., 1989; Glover et al., 2001, 2002). Data from these short intra-annual studies of seasonality, or inferences based on spatial patterns, strongly suggest that changes in surface-water biology associated with climatic perturbations, such as the North Atlantic Oscillation (NAO), ENSO, and human-induced climate change, will influence deep-sea benthic abundance and diversity. Temporal shifts in benthic parameters (e.g. abundance patterns, sediment respiration, and inventories of organic matter) almost certainly will reflect changes in the upper water column. As surface production changes as a result of ocean–atmosphere processes and climate change, benthic parameters may act as a useful measure of longer-term (inter-annual to decadal) shifts in surface-water production caused by climate change (K. L. Smith et al., 2006). The majority of studies have examined only short-term, seasonal trends. As some studies now have data spanning a decade or more we are now in a position to assess the longerterm, decadal-scale changes that may reflect climatic influences.

2.3. Geological drivers In contrast to the sedimented ecosystems that make up most of the deep seafloor, hydrothermal vents found at mid-ocean ridges are dependent on a geologically controlled supply of chemically enriched fluids. In this sense, temporal processes at vents are ‘geologically forced’ (Fig. 1.3). Whilst vents make up only a tiny fraction of the deep-ocean environment, they are sites of remarkable biological activity and concentrated biomass relative to the sedimented plains that surround them (Fig. 1.1C). The discovery of rich biological communities on hydrothermal vents in 1977 was a surprise as hitherto, nobody had considered geologically derived sulphide as an energy source for the production of organic carbon. The conversion of inorganic to organic carbon by chemical means (i.e. chemosynthesis) was already known from studies of shallow-water microbial

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sulphur cycles. But in shallow-water systems, the sulphide is created from the degradation of organic materials and there is no net gain of organic carbon. At hydrothermal vents, a geochemical interaction between seawater and hot rocks in the Earth’s crust creates the sulphide, resulting in a net gain of organic carbon (Van Dover, 2000). Hydrothermal activity in the deep sea is associated with spreading centres on mid-oceanic ridges, back-arc basins, arc and fore-arc volcanoes, as well as active intra-plate seamounts. The hydrothermal habitat is characterised by strong environmental variables that influence the composition, distribution, and dynamics of associated communities (Tunnicliffe, 1991). These factors include the spatially irregular distribution of active vent sites, the temporal variability of hydrothermal activity and, at smaller scales, the local physical and chemical conditions experienced by vent fauna ( Juniper and Tunnicliffe, 1997). In terms of chemistry, time-series measurements show the relative stability of the pure hydrothermal fluid composition within a site over decadal scales. It is only when eruptive or intrusive catastrophic events occur that large changes in hydrothermal systems are triggered and cause temporal variability (reviewed by Von Damm, 1995). Along continental margins and subduction zones, the seepage of hydrocarbons (especially methane) upwards and along fault planes can create coldseep habitats, usually in deep-water environments along continental slopes. Sulphate-reducing bacteria produce sulphide using methane as a carbon substrate (Van Dover, 2000). Rich biological communities of chemosynthetic organisms have been found in these habitats, utilising both methanotrophic and thiotrophic microbes (Levin, 2005). Although the majority of seep-dwelling species are distinct from those at vents, they are usually phylogenetically closely related, and utilise similar symbiotic or free-living bacteria as a source of energy. Although not all vent and seep animals rely on chemosynthesis directly, it has long been recognised that the communities are highly dependent on the ephemeral nature of chemical fluid venting (Van Dover, 2000). In theory, the creation and cessation of vents over time should have drastic consequences for the associated communities and their successional processes. The very first discoveries of hydrothermal vent ecosystems showed how the cessation of vent flow could cause the death of these localised habitats (Corliss et al., 1979). It was quickly realised that the ephemeral hydrothermal vents, in particular, may exist in a non-equilibrium successional state (Hessler et al., 1988). The first hypotheses were based around an ordered succession from initial colonisation by opportunistic tubeworms, followed by clams and finally mussels. More detailed studies involving the mapping of assemblages on vent edifices over time has suggested that vent ecosystems conform to a chronic disturbance model, where one assemblage may be replaced by another without intermediary stages (Sarrazin et al., 1997; and Section 4.1).

Temporal Change in Deep-Sea Ecosystems

15

Over time, evidence suggests that changes in the chemistry of vent fluids, or in the amounts of pore-water methane at cold seeps, will drive changes in the structure of chemosynthetic ecosystems in the same way that changes in POC flux drive shifts in sedimented environments. Some vent sites, in particular those underlying high productivity regimes and those in shallower water, may host a range of species that utilise heterotrophy of photosynthetically derived food in addition to chemosynthesis. Such environments will experience a combination of geological and biological forcing mechanisms. Although the drivers may vary, the common evolutionary heritage and ecological constraints of deep-sea faunas, whether from vents or sediments, will create commonalities in the response to changes.

3. Case Studies: Sedimented Environments Muddy, deep-sea sediments represent the most widespread habitat on the Earth’s solid surface, occupying approximately 96% of the ocean floor (Glover and Smith, 2003). With an average ocean depth of 3800 m, they are also one of the least accessible of habitats. Modern quantitative deep-sea biology only started in earnest during the 1960s with pioneering studies on the small infauna of the deep north-west Atlantic (Hessler and Sanders, 1967). The majority of these and subsequent studies have not included a long time-series element. Proxy records from long deep-sea sediment cores have yielded a large body of data on long-term change on the planet (Section 5.2.1), but on shorter ecological time-scales rather little is known. Deep-sea sedimented environments are found in bathyal, abyssal, and hadal (trench) settings (Fig. 1.5). Bathyal environments, which are closer to land and often characterised by steep slopes, irregular topography, greater sediment heterogeneity, and a more complex water-mass architecture, are subject to a broader range of drivers. These include highly variable POC fluxes, down-shelf cascades, sediment slumps, turbidity currents, benthic storms, and organic inputs from river and canyon systems. In contrast, abyssal sites are usually (but not always) less influenced by horizontal transport and are more closely linked to the surface waters directly above them. Since nothing is known about temporal change in trenches, they are omitted from consideration in this review.

3.1. Bathyal sites The bathyal region of the deep sea, being close to land and the home ports of nations actively involved in deep-sea work, has been better sampled than the abyss or hadal regions. However, the majority of sampling programmes have focussed on expanding our ecological or biogeographic knowledge

BATHYAL - NW PACIFIC

ABYSSAL - NE ATLANTIC BATHYAL ARCTIC - FRAM STRAIT

Sagami Bay

PAP

75⬚N

Hausgarten study region 60⬚N

45⬚N

ABYSSAL - NE PACIFIC 30⬚N

BATHYAL - BISCAY SLOPE

15⬚N 0⬚

Station M Biscay site

15⬚S

30⬚S

BATHYAL EASTERN MEDITERRANEAN

45⬚S

BATHYAL - ANTARCTIC Cretan Sea

FOODBANCS study region

120⬚E

140⬚E

160⬚E

180⬚E

160⬚W

140⬚W

120⬚W

60⬚S

75⬚S

100⬚W

80⬚W

60⬚W

40⬚W

20⬚W

W0⬚E

20⬚E

40⬚E

60⬚E

80⬚E

100⬚E

Figure 1.5 Geographic and bathymetric localities for known deep-sea sedimented environments with benthic time-series data. All bathymetric contours are 500 m interval. Data from GeoMapApp (http://www.geomapapp.org).

Temporal Change in Deep-Sea Ecosystems

17

through broad spatial coverage rather than repeat visits. We have identified only 7 bathyal sites for which benthic biological time-series data is available. 3.1.1. HAUSGARTEN The Alfred Wegener Institute for Polar and Marine Research in Germany has established the deep-sea long-term observatory ‘HAUSGARTEN’ west of Svalbard (Soltwedel et al., 2005a). One of the main goals of the study is to measure the impact of large-scale environmental changes over time on a deep-sea ecosystem, and to determine experimentally factors that influence deep-sea biodiversity. The observatory includes 16 permanent sampling sites along a depth transect from 1000 to 5500 m and a latitudinal transect following the 2500 m isobaths for approximately 125 km (Fig. 1.5). The central HAUSGARTEN station at 2500 m water depth serves as an experimental area for in situ biological experiments (e.g. Premke et al., 2003, 2006; Kanzog et al., 2008; Gallucci et al., 2008a,b). Multidisciplinary research activities at HAUSGARTEN started in 1999 and cover almost all compartments of the marine ecosystem from the pelagic zone to the benthic realm, with some focus on benthic processes. The HAUSGARTEN observatory is located in Fram Strait, the only connection between the central Arctic Ocean and the Northern North Atlantic where exchanges of intermediate and deep waters take place. The main topographic features in the area are the Vestnesa Ridge, a submarine projection from the Svalbard continental margin (1000–2000 m water depth), and the Molloy Hole, a deep depression with a maximum depth of 5669 m, adjoining the ridge to the west. The hydrography is characterised by the inflow of relatively warm and nutrient-rich Atlantic Water into the central Arctic Ocean. The advection of these waters exerts a strong influence on the climate of the Nordic Seas and the entire Arctic Ocean (Hassol, 2004). HAUSGARTEN is also located in the highly productive Marginal Ice Zone (MIZ), where the dramatic decrease in the extent of summer sea-ice observed over the last decades causes an ongoing northward shift of the ice-edge related primary production. Water column studies at HAUSGARTEN include the assessment of physico-chemical parameters as well as flux measurements of particulate organic matter to the deep seafloor. Water temperatures in the Fram Strait have increased significantly in recent years. Between the summers of 2003 and 2004, a relatively large temperature increase of 0.6 C was observed within the upper 500–1000 m of the water column. At the central HAUSGARTEN site, temperature records covering the years 2000 through 2008 exhibited small seasonal variations, and an overall slight temperature increase, even at 2500 m (Fig. 1.6). Between 2000 and 2005, settling particulate matter at HAUSGARTEN showed seasonal patterns with elevated fluxes during May/June and at the end of the growth season (Bauerfeind et al., 2009). The export flux of POC was rather low suggesting

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−0.76

0

20

Running month 60 40

80

100

−0.78

Temperature (⬚C)

−0.80 −0.82 −0.84 −0.86 −0.88 −0.90

Figure 1.6 Bottom-water temperature (2 m above seafloor) at the central HAUSGARTEN site (2500 m) between the summers of 2000–2008.

a large retention and recycling of particulate organic matter in the water above 300 m. Based on the composition of the settled matter, the working hypothesis is that export of organic carbon is mainly governed by noncalcareous organisms. Furthermore, variations in the surface currents and ice regime appear to trigger changes in the patterns and composition of settling matter in the eastern Fram Strait. Benthic investigations at HAUSGARTEN include analyses of biogenic sediment compounds to estimate organic matter input to the deep seafloor (using sediment-bound pigments as indicators of phytodetrital matter) as well as the activity, biomass, numerical abundance, and diversity of the benthic fauna from bacteria to megafauna. Biochemical analyses between the summers of 2000 and 2004 revealed a generally decreasing flux of phytodetrital matter to the seafloor, and subsequently, a decreasing trend in sediment-bound organic matter and the total microbial biomass in the sediments (Fig. 1.7). Over the spatial depth transect, mean metazoan meiobenthic (mainly nematode and copepod) densities ranged from 149 to 3409 individuals per 10 cm2 (Hoste et al., 2007). Although there was a significant correlation between meiobenthic densities, microbial exo-enzymatic activity (esterase turnover), and phytodetrital food availability (chlorophyll a and phaeophytines), there was no consistent relationship between nematode or copepod densities and measures for organic matter input. However, significant inter-annual variations in meiofaunal abundance were observed.

19

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Figure 1.7 Temporal changes in sediments at the HAUSGARTEN site. Decreasing concentrations of photosynthetic pigments (top), organic carbon (middle) and total microbial biomass (bottom) recorded over the 2000–2005 time series are associated with increasing bottom water temperatures (Fig. 1.6). Figure adapted from Soltwedel et al. (2005a).

The species composition of nematode communities was studied along the complete HAUSGARTEN bathymetric gradient for the year 2000, and three stations (1200, 2500, and 4000 m) were sub-sampled for detailed species-level analysis over the 5-year time series. Although depth-related changes were more prominent than shifts according to sampling year, interannual variability in nematode community structure was clearly apparent.

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Between-sample variability tended to increase with increasing water depth, and inter-annual variability was most pronounced at 2000 and 2500 m for nematode abundance (Hoste et al., 2007). The 4000 m station was characterised by the highest variation within the same year, suggesting high spatial patchiness. However, parallel observations at several water depths indicate that most of the variation over the time series was the result of real temporal shifts in food availability as measured by sediment-bound phaeopigment and chlorophyll a concentrations (Hoste et al., 2007). Nematode genera such as Microlaimus, Dichromadora, and Tricoma likewise seemed to be related to high food availability as they were present in the year 2000 and replaced, especially at 4000 m, by more typical deep-sea taxa such as Monhysteridae, Cyartonema, Theristus, Halalaimus, and Acantholaimus. One explanation for the high interannual variability at 4000 m is sediment disturbance caused by the steep slope (up to 40 inclination, Soltwedel et al., 2005a) between the 4000 and 5000 m stations. For the larger organisms, the abundance and distribution of epifaunal megafauna were assessed over the time-series using a towed camera system, taking seafloor images at regular intervals 1.5 m above the seafloor. A comparison of footage taken in 2002 and 2004 demonstrated a significant decrease (from 8.6 to 4.2 individuals per square meter) in megafauna densities at 2500 m (Soltwedel, unpublished data). Lower values in 2004 for the vagile megafauna (e.g. holothurians, gastropods, isopods) might reflect horizontal migrations of organisms. However, as densities of the sessile megafauna (i.e. poriferans, crinoids, and anthozoans) were also clearly lower in 2004 (a drop of 46.5%), this may be a general trend related to decreased food availability and higher bottom temperatures at the deep Arctic seafloor. Similar observations of decreasing megafaunal densities were made by other scientists in the nearby Kongsfjord during roughly the same period ( J.M. Weslawski, personal communication). Studies of meiofaunal changes at HAUSGARTEN are ongoing. 3.1.2. Eastern Mediterranean The Eastern Mediterranean deep sea is characterised by relatively high bottom temperatures (14 C) and recent notable changes in its thermohaline properties observed by time-series studies (Theocharis et al., 1999; Danovaro et al., 2004). During the period 1991–1995 the bottom temperature dropped by around 0.4 C, and subsequently increased from 1995 to 1999 by about 0.2 C (Danovaro et al., 2004). Because the deep sea is normally characterised by very stable temperatures over long periods (although data are scarce for the Mediterranean; Lejeusne et al., 2010), some benthic biotic response might be expected. Nematode abundance and diversity data from seven cruises between 1989 and 1998 revealed an increase in diversity during the 1990–1994 cooling period and a subsequent decrease during the ‘re-warming’ that followed (Danovaro et al., 2004).

Temporal Change in Deep-Sea Ecosystems

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The degree of background stochastic variation in nematode diversity at these sites is unknown, so it is difficult to know whether this represents a long-term trend or a normal level of spatial or temporal variation. However, the potential link between hydrographic conditions, bottom-water temperature and benthic diversity is intriguing and merits continued monitoring. In the seas to the south of Crete, long-term monitoring has been undertaken for the last 20 years in the Ierapetra Basin at 2500–4500 m. Data on pigment concentrations in surface sediments indicate that the Eastern Mediterranean, normally a highly oligotrophic area, may occasionally experience periods of very high organic-matter input (Fig. 1.8). Unusually, high concentrations of phytopigments have been reported in sediments (Tselepides et al., 2000). These events could be linked to hydrographic shifts such as an increasing outflow of nutrient rich water masses into the Levantine Basin (Roether et al., 1996; Klein et al., 1999; Theocharis et al., 1999), resulting in enhanced biological productivity and organic matter flux to the seabed. In 1993, this enhanced flux caused significant changes in the abundance and composition of the meiobenthic assemblages (Tselepides and Lampadariou, 2004; Lampadariou et al., 2009). It also affected the planktonic (Weikert et al., 2001) and the macrobenthic (Kro¨ncke et al., 2003) communities. These large changes in the physiochemical characteristics of the eastern Mediterranean (Roether et al., 1996) provide a striking example of how large-scale, oceanclimate changes may abruptly convert a deep-sea ‘desert’ into an ‘oasis’ or a monoculture of opportunistic species, such as the polychaete Myriochele fragilis or the crustacean Chaceon mediterraneus. These species were once known only from the western Mediterranean basin, but are now found in high numbers also in the deep eastern basin (Sarda` et al., 2004). 3.1.3. Peru and Chile margin Time-series studies at bathyal depths off the Peru and Chile margin have focused on how interactions between the well-developed oxygen minimum zone (OMZ) and decadal-scale ENSO impact the benthic fauna (Sellanes et al., 2007; Arntz et al., 2006). OMZs are layers of the water column, typically located between 50 and 1000 m depth, where dissolved oxygen (DO) concentrations fall below 0.5 ml L 1 (<22 mM). They are major oceanographic features on the eastern margins of ocean basins, notably the Pacific, as well as in the northern Indian Ocean (Kamykowski and Zentara, 1990; Paulmier and Ruiz-Pino, 2008). OMZs persist over geological time scales and are maintained by a combination of factors, particularly high surface productivity and water-column stratification. Where they intersect the seafloor on the outer shelf, upper slope, and oceanic seamounts (Helly and Levin, 2004), OMZs strongly influence the abundance, diversity, and composition of benthic faunas, mainly as a result of oxygen depletion and organic matter enrichment (Levin, 2003; Murty et al., 2009; Gooday et al., 2009).

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30 A

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Figure 1.8 Temporal changes in sediments at the Eastern Mediterranean Ierapetra Basin sites over the 1987–1999 period: (A) photosynthetic pigment concentrations in surface sediments measured at three time points, indicating large inter-annual shifts in food flux to the seafloor, (B) changes in metazoan meiofaunal abundance associated with changes in food availability at the deep seafloor.

Of particular interest in the context of this review is the impact of ENSO on the OMZ upper boundary. This boundary is depressed during warm El Nin˜o (EN) events on the Peru-Chile margin (Helly and Levin, 2004). Off Concepc¸ion (central Chile), the upper OMZ boundary was located 80 m between May 1997 and August 1998 (EN period) compared to 30 m between November 2003 and March 2003 (non-EN period) (Sellanes et al.,

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2007). The cooler non-EN period was further characterised by a higher total organic carbon and phytodetritus content of the sediment compared to the EN period. These environmental changes were accompanied by a decrease in the abundances of total macrofauna and certain polychaete species, the disappearance of an ampeliscid amphipod, and a shallowing of the macrofaunal living depth (Sellanes et al., 2007). The 1997–1998 EN was also associated with changes among the meiofauna off Peru and Chile (reviewed by Arntz et al., 2006). Although EN-related oxygenation is felt most strongly on the shelf, it also extends deeper. On the Peru margin (12 300 S), the 1982–1983 EN event depressed the upper boundary of the OMZ from the shelf (50–100 m) onto the upper slope (nearly 300 m) (Arntz et al., 1991). The 1997–1998 event lowered the boundary to 200 m and is believed to have led to a slight increase in oxygen levels to 300 m depth (Levin et al., 2002). Although rises in oxygen concentrations during EN periods probably do not penetrate below the upper slope, the associated reduction in surface productivity leading to a decline in carbon flux will have consequences for deeper benthic communities as well as those in shallower water. Arntz et al. (2006) conclude that ‘it is likely that large areas of the margin below the OMZ should respond to ENSO-related changes in hydrography and productivity.’ 3.1.4. Bay of Biscay At temperate slope sites, a pronounced seasonal signal may also be accompanied by inter-annual variability in surface production. Oscillations in the strength of this seasonal and inter-annual production are quickly transmitted to the bathyal seafloor. A time-series study in the Bay of Biscay has identified a spring-bloom related increase in chlorophyll a concentrations in the sediments. The response of the ‘live’ benthic foraminifera (63–150 and >150 mm size fractions) to this bloom was analysed in multi-year time-series samples from two bathyal sites, located at 550 m (October 1997–April 2000) and 1000 m (October 1997–April 2001) (Fontanier et al., 2003, 2006). Although total foraminiferal densities varied considerably between cores at 550 m, a principal component analysis suggested that temporal variability was more important than spatial variability, even in the finer (63–150 mm) fraction. At both sites, a pronounced spring bloom led to phytodetritus deposition to the seafloor, which induces strong seasonal fluctuations among foraminifera, particularly small opportunistic species living close to the sediment surface. However, although there are some inter-annual differences, there is no evidence for longer-term trends at these two bathyal localities. 3.1.5. Sagami Bay A permanent bathyal station (1430 m water depth) in Sagami Bay, a deepwater embayment on the Japanese margin near Tokyo, has been sampled repeatedly for foraminifera since 1991 (Kitazato and Ohga, 1995; Ohga and

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Kitazato, 1997). Data on surface productivity, fluxes through the water column, and dynamic processes at the sediment–water interface, were gathered regularly since 1996, the 1997/1998 period being studied in particular detail (Kitazato et al., 2000, 2003). The area is characterised by a seasonal deposition of fresh phytodetritus, which causes changes in the thickness of the oxygenated layer of the sediment. Corresponding to these annual cycles, there are clear fluctuations in the population densities of foraminifera (Kitazato et al., 2000), changes in the vertical distributions of harpacticoid copepods and kinorhynchs (Shimanaga et al., 2000), but no obvious seasonality in the species composition and diversity of copepods (Shimanaga et al., 2004). Thus, as on the Biscay margin, this intensively studied deep-water embayment is dominated by seasonal processes with no evidence to yet emerge for longer-term faunal changes. 3.1.6. Rockall Trough Another bathyal site with long-term temporal data is the Rockall Trough off the west coast of Scotland. The site was established in 1973 and includes the Scottish Association for Marine Science Permanent Station at 2990 m and a Station ‘M’ on the Hebridean Slope (Gage et al., 1980; Tyler, 1988). The main focus of these studies was not the investigation of long-term change, but the impacts of seasonality, which required sampling over several years. The results from many studies indicate that there is an obvious seasonal response that manifests itself in seasonal reproductive patterns of species such as the ophiuroids Ophiura ljungmani, Ophiocten gracilis, echinoid Echinua affinis, asteroid Plutonaster bifrons, the bivalves Ledella messanensis and Yoldiella jeffreysi (Lightfoot et al., 1979; Tyler and Gage, 1980; Tyler et al., 1982), variation in recruitment in the ophiuroid Ophiomusium lymani (Gage and Tyler, 1982) and differences in breeding intensity in isopods (Harrison, 1988). In a similar pelagic time series, Gordon (1986) studied fish reproductive cycles in the Rockall Trough reporting that Nezumia aequalis, Trachyrhynchus murrayi and Lepidon eques showed seasonal reproduction spawning in spring. The majority of these species have synchronised their breeding cycles to coincide with the annual increase in surface production; and food supply from surface waters was thought therefore to be a key factor in these life histories. Such observations indicate a close link between reproduction, recruitment and survivorship and variations in surface production. Although these data were not collected with climate change in mind, it is clear that changes in climate affecting surface production are likely to impact on organisms that show such close benthic–pelagic coupling. 3.1.7. West Antarctic Peninsula A final ‘bathyal’ site of interest is located on the West Antarctic Peninsula continental shelf; we classify it bathyal owing to the greater depth of the Antarctic shelf (500–1000 m) caused by the ice-loading of the Antarctic

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continent. The region to the west of the US Palmer Station is targeted as a Long-Term Ecosystem Research site (the LTER programme, funded by the US National Science Foundation) and has been subject to 12 years of upper-ocean monitoring (C. R. Smith et al., 2006). Sediment-trap monitoring of POC flux to the seafloor has revealed intense seasonal pulses of food input, as might be expected given the pronounced variation in photoperiod and sea-ice cover in high latitude marine environments (C. R. Smith et al., 2006). Benthic studies in the form of the ‘Food for Benthos on the Antarctic Shelf’ (FOODBANCS) programme only commenced in 1999, but have already revealed that the seasonal pulse in food is strongly buffered in benthic sediments by the presence of a persistent ‘food bank’ that allows detritivores to continue feeding and reproducing year-round (Mincks and Smith, 2007; Glover et al., 2008; Sumida et al., 2008). However, over the study period (1999–2001), strong inter-annual variability in the quantity of phytodetritus was observed at the ocean floor, hinting at major shifts occurring on potentially decadal scales (C. R. Smith et al., 2006). Ongoing sampling over inter-annual scales (FOODBANCS 2) is expected to provide a new decadallevel benthic dataset in the Southern Ocean.

3.2. Abyssal sites The abyssal plains are the most extensive of deep-sea habitats. Their distance from land, and great depth, creates major sampling problems in terms of technical and financial logistics. Even with modern winches, it requires over 4 h to take a simple spade box core in 5000 m of water. An abyssal trawl usually takes at least 8–12 h and the majority of ROVs are unable to reach such depths. Nevertheless, long-term monitoring has been carried out in two principal abyssal settings. The Porcupine Abyssal Plain (PAP) is centred in the north-east Atlantic and has been the focus of mainly British oceanographic cruises. The second, ‘Station M’, is in the north-east Pacific and has been sampled mainly by US cruises. Both these sites have been sampled, mainly on a semi-regular basis, by researchers over the last two decades. Government funding for such cruises has been intermittent, and it is only recently that the value of these long-term datasets has been fully realised. The PAP and Station M are now considered ‘observatories’ and as such are key sites for the study of long-term change in the abyss. 3.2.1. Porcupine Abyssal Plain sustained observatory The PAP site lies at 4850 m water depth in the north-east Atlantic (Fig. 1.5). This important site has been studied in different ways and at various frequencies over a period of more than 20 years. The most complete benthic datasets are for invertebrate megafauna (1989–2005) and fish (1977–1989 and 1997–2002) collected using a semi-balloon otter trawl. From 1989 to 2002, there was a threefold increase in megafaunal abundance

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and major changes in species composition (Fig. 1.9; Billett et al., 2001, 2010). Evidence from time-lapse photography indicates that the increase was even more dramatic than suggested by the trawl samples (Bett et al., 2001). The most obvious changes were seen among holothurians, notably Amperima rosea and Ellipinion molle, small species that both showed rapid abundance increases in 1996/1997 followed by a decline that was particularly precipitate in the case of E. molle. This period (1997–1999) has been termed the ‘Amperima event’ (Fig. 1.9D). Amperima densities underwent a second ‘boom-bust’ cycle in 2002–2005. Two larger holothurian species (Psychropotes longicauda and Pseudostichopus aemulatus) exhibited more modest increases during the Amperima event, while a third (Oneirophanta mutabilis) underwent a significant decrease over the entire time series. Tunicates and actiniarians increased in abundance at the same time as Amperima and maintained higher densities after the Amperima event; pycnogonids showed a sharp increase during the Amperima event, but no significant trend over the time series as a whole. The increases in densities of holothurians, in particular A. rosea, led to an increase in the extent to which surface sediments, and particularly phytodetritus deposits, were reworked during the Amperima event (Bett et al., 2001). Probably as a result of these activities, there was little sign of phytodetritus on the seafloor between 1997 and 1999. Changes in other elements of the benthic fauna, the foraminifera, metazoan meiofauna and macrofaunal polychaetes, were also observed during the 1990s at the PAP. Foraminiferal densities (0–1 cm sediment layer, >63 mm fraction) were significantly higher in 1996–2002 compared to 1989–1994 (Gooday et al., 2010). Over the same period, species richness and diversity decreased and dominance increased, although not significantly. Species-level multivariate analyses revealed three assemblages represented by samples collected in 1989–1994, September 1996–July 1997 and October 1997–October 2002 (Fig. 1.10). These reflected temporal changes in the densities of higher taxa and species. The abundance of Trochamminacea, notably a small undescribed species, increased substantially. Species of Hormosinacea and Lagenammina also tended to increase in density from 1996/1997 onwards. Rotaliida, dominated by Alabaminella weddellensis and Epistominella exigua, showed a bimodal distribution over time with peak densities in May 1991 and September 1998 and lowest densities in 1996–1997. Short-term responses to seasonal phytodetritus inputs probably explain the relative abundance of E. exigua, and to a lesser extent A. weddellensis, in 1989 and 1991 when phytodetritus was present. A qualitative change in the phytodetrital food, repackaging of food by megafauna, increased megafaunal disturbance of the surficial sediment, or a combination of these factors, are possible explanations for the dominance of trochamminaceans from 1996 onwards. Horizontally sliced box-core samples (0–5 cm, >250 mm fraction) revealed that the miliolid Quinqueloculina sp. was more abundant in March 1997, and also concentrated in

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Temporal Change in Deep-Sea Ecosystems

Figure 1.9 Climatic and abyssal time-series data for Station M in the NE Pacific and PAP in the NE Atlantic with (A) the ENSO indicator the Northern Oscillation Index (NOI) with monthly (light dashed line) and 13-month running mean (compound line), and POC flux to 4050 m depth at Station M; (B) mobile megafauna variation at Sta. M including Elpidia minutissima abundance (crosses), Echinocrepis rostrata abundance (open circles), and an index of species composition similarity of the top ten most abundant megafauna (solid circles); (C) the NAO index with monthly (light dashed line) and 13-month running mean (bold dashed line), and POC flux to 3000 m depth at the PAP; and (D) total megafauna variation at Station M including Oneirophanta mutabilis abundance (crosses), Amperima rosea abundance (open circles), and an index of species composition similarity of the benthic megafauna (solid circles).

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Ma97 Ju97 Oc97 Ma97 Ju97 Se96 Se96 Se98 Se98 Ap99 Oc97 Oc02 Oc02 Ma98 Ma98 Ap99 Ap94 Ap94 Au89 Au89 Au89 Ma91 Ma91

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Figure 1.10 Cluster analysis (A) and non-metric multi-dimensional scaling ordination (B) based on square root transformed abundance (density) for foraminiferal assemblages from the Porcupine Abyssal Plain. Different symbols indicate different cruises. Note the change in assemblage composition over time. Figure from Gooday et al., 2010.

deeper sediment layers, than in September 1996. This species apparently migrated to the sediment surface in response to a 1996 flux event, grew and reproduced, before migrating back into deeper layers as the phytodetrital food became exhausted. These time-series samples therefore suggest that decadal-scale changes have occurred among shallow-infaunal foraminifera at the PAP site, more or less coincident with changes in the megafauna, as well as indications of shorter-term events related to seasonally pulsed phytodetrital inputs. Densities of metazoan meiofauna (32–1000 mm) increased significantly between 1989 and 1999, driven mainly by the dominant taxon, the nematodes, and to a lesser extent the polychaetes (Kalogeropoulou et al., 2010). Ostracods showed a significant decrease while most other taxa, including the second-ranked group the copepods (harpacticoids and their nauplii), did not exhibit significant temporal changes in abundance. MDS ordination of

Temporal Change in Deep-Sea Ecosystems

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higher taxon composition showed a significant shift at this taxonomic level in meiofaunal species composition from the pre-Amperima to the Amperima periods. There were also significant increases in the proportion of total meiofauna, nematodes, and copepods (but not polychaetes) inhabiting the 0–1 cm layer over time. In addition, seasonal changes in the vertical distribution patterns of total meiofauna and nematodes within the sediment were apparent during the intensively sampled period (1996–1997). Macrofaunal polychaetes exhibited a more muted response to changes at PAP. Soto et al. (2010) found that the abundance of the whole assemblage increased significantly before and after the Amperima event. These differences were localised to the upper 3 cm of the sediment and the increase in the assemblage density was less than that of the megafauna. Analyses of the polychaete faunal composition indicated that only certain taxa and trophic groups responded. The families Cirratulidae, Spionidae, and Opheliidae had significantly higher abundances during the Amperima event that before, while others, such as the Paraonidae, showed no obvious change during this time. The Opheliidae response was characterised by an influx of juveniles, probably all of the same species (Vanreusel et al., 2001). Significant increases were also detected in two trophic groups, surface deposit feeders and predators. Although polychaete assemblages exhibited an overall change at the higher taxon and functional group level at the PAP during the period 1989–1998, the response was much less obvious at the species level (Soto, 2008). The same dominant species occurred throughout the study period, with the exception of the Paraonidae, where the dominant species of the genus Aricidea declined prior to the Amperima event and was replaced by two other species. While the 12 most abundant species all exhibited some interannual variation, only 6 showed a significant response during the Amperima event. All had the highest abundance in July 1997 and September 1998 corresponding to the highest values of phytopigment fluxes, carbon and nitrogen in the water column. The increase in abundance of these species, however, was quite low and often only slightly higher than preAmperima event densities. The fact that only some polychaete species responded may be related to greater foraging efficiency by megafaunal deposit feeders that sequestered and repackaged nutrients, with the result that fewer nutrients reached smaller organisms. Surface deposit-feeding polychaetes increased during the Amperima event, at the same time as disturbance of the surficial sediment by holothurians and ophiuroids was presumed to be increasing. The extent to which the above-mentioned changes in the benthic community affect the associated fish communities remains unclear. As described above, the main factor driving change in abyssal communities is temporal variability of food availability. A study of muscle tissue RNA and protein content for abyssal fishes caught in spring suggested lower growth

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rates than conspecifics caught during the preceding autumn (Kemp et al., 2006). This suggests that temporal changes in benthic food availability could potentially affect fish, as growth rates were highest just after the summer peak in POC flux. As most fish do not feed directly on phytodetritus, any trophic link would depend on changes to prey animal availability or composition as a result of these animals feeding on phytodetritus. Such changes were not observed in previous studies in the Pacific (see Section 3.2.2), but the greater seasonal variability in primary productivity in the North Atlantic could explain this (Kemp et al., 2006). Cyclic changes in the melatonin content of the isolated pineal glands of the bathyal eel Synaphobranchus kaupii indicate that these fish may have retained a biochemical rhythm linked to monthly tidal-cycle variations (Wagner et al., 2007). Such a time-keeping system might allow a fish to schedule its growth and reproduction to times when food is most available, or even migrate to areas where seasonal increases in food occur. Like the invertebrate fauna, the abundance and composition of the fish community of the PAP and the adjacent slope (Porcupine Seabight, PSB) have been subject to studies using trawling (Merrett, 1992; Collins et al., 2005). They have also been studied with baited landers (Bailey et al., 2007). These studies have told us much about the spatial distribution and behaviour of these fishes, but as yet very little about natural temporal change. Commercial fisheries landing data for the upper slopes of PSB reveal declines in the abundance of target species (Basson et al., 2002) but we know little about natural drivers of temporal change in these fishes, or about changes at lower bathyal and abyssal depths. A recently studied long-term dataset of 161 trawls at depths of 800–4800 m, conducted from 1977 to 2002, reveals a decline in fish abundances between 800 and 2500 m, but no changes deeper than this (Bailey et al., 2009). Changes were observed in both fisheries target and non-target species, as long as a portion of their range fell within the fishing grounds (<1500 m). This may reflect fishing on the upper slope preventing these fish from spreading down-slope to populate deeper areas (Bailey et al., 2009). In this way fishing effects are transmitted down-slope, effectively removing fish from areas tens of kilometres from the fishing grounds themselves. However, the PAP site is well below the depth at which these effects are visible. The dataset for PAP consists of only 35 research trawls targeting fish at >4000 m over the period 1978–2002. We have not discerned any temporal patterns in these data. If changes have occurred they may be obscured by the low numbers of fish caught in most of these trawls, gaps in the dataset and the difficulty in accurately estimating the area sampled. If there is a role for seasonal changes in food availability in the ecology of these fishes (Kemp et al., 2006) it is reasonable to assume that longer-term changes in food inputs could affect fish numbers and community structure in the same way as has been seen in the invertebrates.

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3.2.2. North-east Pacific Station M, in the north-east Pacific has been monitored since 1989. This site is located 220 km off the coast of Point Conception, California in 4100 m of water. The region has been shown to exhibit pronounced seasonal and interannual climate variability (Smith and Druffel, 1998). The site is also in the vicinity of the California Current Oceanic Fisheries Investigations (CalCOFI), a programme of biological oceanographic research that has been conducted seasonally in surface waters since 1949. A partner programme to CalCOFI, operating in the same vicinity since 2004, is California Current Ecosystem Long-Term Ecological Research (LTER) programme (Ohman and Hsieh, 2008). The Station M time-series programme has revealed substantial variations in mega and macrofaunal abundance and size from the species to community level, along with shifts in ecosystem functions such as bioturbation rate and sediment community oxygen consumption (SCOC) (Drazen et al., 1998; Ruhl, 2008; Ruhl et al., 2008; Vardaro et al., 2009; Fig. 1.9). It is believed that these changes are linked to fluctuations in the availability of food at the seafloor. The data suggest that changes in food supply influence the smaller fauna more rapidly. Over a period of nearly 2 years, beginning in June 1989, significant seasonal variations in macrofauna were observed (Drazen et al., 1998). Protozoans (especially agglutinating foraminifera) and major metazoan groups including nematodes, polychaetes, harpacticoids, tanaids, and isopods retained on a 300-mm sieve, exhibited seasonal variations with maximum abundances following peaks in food supply. Also, the arrival of a pulse of phytodetritus on the seafloor was followed within weeks by a significant increase in protozoan densities (Drazen et al., 1998). A longer-term (1989– 1998) analysis of metazoan macrofaunal data also revealed that metazoans first responded after 3–4 months in terms of density and after 7–8 months in terms of total biomass and individual biomass. This would be expected if the dominant faunal response was reproduction and recruitment followed by individual increases in body size (Ruhl, 2008; Ruhl et al., 2008). Given that abyssal fauna are thought to be food-limited ( Johnson et al., 2006; C. R. Smith et al., 2008; K. L. Smith et al., 2009), it has been hypothesised that inter-annual and longer-term variation in food supply would have implications for abundance and community structure similar to those observed in the seasonal studies. Longer-term analysis indicates that, in addition to the seasonal trends, the observed variations in metazoan abundances extended to interannual periods where food supplies were higher or lower (Ruhl et al., 2008). For example, the food supply in 1991 was approximately twice that in 1992, with comparable differences in metazoan macrofaunal abundance. This change is similar to that observed for macrofaunal polychaetes at the PAP site. Furthermore, there were significant changes in dominance and community structure, even at the phylum level. Community changes were seen in the relative abundance of specific phyla, as well as in the

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rank abundance distributions, a biodiversity indicator of relative abundance and evenness. The changes included a switch from dominance by the larger annelids during periods (e.g. 1991) of higher food supply to dominance by smaller arthropods when food was scarcer (e.g. 1992). So, even though the total abundance of the metazoan macrofauna increased both in terms of biomass and density, the response was not consistent across phyla, with larger fauna apparently gaining competitive advantage during higher food flux conditions. For several species of mobile megafauna, abundance was correlated with food supply over the 1989–2004 study period (Ruhl and Smith, 2004; Ruhl, 2007). Shifts in species composition, and the relative evenness of species abundances, were also noted. The elasipod holothurian Elpidia minutissima grew in abundance from 1989 to 1998 to almost 1 indiv. m 2, but then showed a precipitous decline to nearly 1 indiv. ha 1 (Fig. 1.9B). Another elasipod, Peniagone vitrea, showed a similar trend. Other species (e.g. the irregular urchin Echinocrepis rostrata) exhibited the opposite tendency, occurring in relatively lower abundances over the early part of the time series, but showing an order of magnitude increase during the 2001–2004 period. The larger holothurian Psychropotes longicaudata showed a similar, albeit less variable trend. As with the metazoan macrofauna, the abundance of many dominant epibenthic megafaunal species was linked to the food supply. However, the echinoderms exhibited much larger abundance variations (up to three orders of magnitude) compared to a factor of two in the case of the macrofauna. Additionally, the megafauna had longer temporal lags (several months on average) in their apparent responses to the variable food supply. An analysis of the body-size distributions of the most abundant mobile megafauna suggested that increases in abundance were negatively correlated to decreases in the average body size in seven of the ten species (Ruhl, 2007). This increased proportion of smaller individuals suggests that reproduction and recruitment probably play an important role in abyssal population dynamics. Migration and mortality are also likely to influence the declines in abundance. However, except for Peniagone spp., which have been observed swimming above the seafloor, adult stages of these species are thought to move too slowly for mass migrations to be an important factor. Estimates from time-lapse photography have put the speed of megafaunal movement at 0.4–5.7 km yr 1 (Kaufmann and Smith, 1997). A more detailed investigation of the size distribution dynamics of the ophiuroids did not reveal any seasonal trends, although there were significant correlations between the body-size distribution shifts and food supply (Booth et al., 2008). The lack of a detectable correlation at the seasonal scale may reflect the fact that the interannual variation in food supply observed at Station M is greater than in the Rockall Trough, where seasonality in ophiuroid recruitment was frequently observed.

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Recent data have suggested that there are temporal trends among abyssal Pacific fish populations, although the reasons behind them are not fully understood. The behaviour, abundance, and biochemical composition of abyssal fish change temporally, over both seasonal and interannual timescales. Baited camera observations suggest that grenadier swimming activity at Station M vary between seasons (Priede et al., 1994a), while seasonal changes in size frequency were observed in the Central North Pacific (CNP) (Priede et al., 2003). These observations led Drazen (2002) to test for seasonal differences in the body compositions of three grenadier species. After examining a whole suite of biochemical indicators of nutrition and growth, Drazen (2002) concluded that seasonal changes in productivity have no measureable effect on the fish, perhaps because fish are able to switch between prey types, and eat mid-water fish or squid. Interestingly, there were indications of interannual variability in biochemical composition, which might indicate changes in food availability, or a spawning cycle. A camera sled has also been used to estimate benthopelagic fish abundance in the Station M region (Bailey et al., 2006). Only fish within 2 m of the seafloor were visible, and the majority of these were grenadiers (Coryphaenoides spp.). The numbers of these fish more than doubled over the period 1989–2004 (Bailey et al., 2006). Fish numbers also correlated with the abundances of benthic echinoderms but with changes in the fish lagging behind changes in echinoderms by 9–20 months (Bailey et al., 2006). Although echinoderms are not normally considered a major source of food for grenadiers, a predator–prey relationship is the simplest explanation for the correlation. However, recent dietary studies based on stomach contents, stable isotope analysis (Drazen et al., 2008) and fatty acid profiles (Drazen et al., 2009) seem to show that these abyssal fish are much more dependent on carrion than was previously thought, and do not feed primarily on echinoderms. These findings lead to the intriguing idea that abyssal fish communities might be affected strongly by sinking fish carrion derived from stocks in the photic zone. On an ecosystem level, the broad faunal changes noted above could have consequences for ecosystem function, such as organic matter remineralisation rates and sediment bioturbation. Shifts in ecosystem functioning could have important impacts on the proportion of organic carbon that is either remineralised or becomes buried in marine sediments. Research into ecosystem function at Station M has focused on a few key areas, including SCOC, bioturbation, and links between biodiversity and ecosystem function. SCOC is indicative of food demand and also is an indicator of organic carbon remineralisation. After the initial 10 years of measurements at Station M (1989–1998), two features of SCOC variability became apparent. There were distinct seasonal cycles in SCOC that were less variable between years relative to POC flux, and the ratio of POC flux to SCOC declined over time, suggesting that there was a trend towards less food availability to support the

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demand implied by the SCOC measurements (Smith and Kaufmann, 1999; K. L. Smith et al., 2001). These studies hinted at a potential long-term change in community structure and/or function, even if some food derived from high flux pulses remained in the sediment. Although the food supply did increase in the more recent 2001–2006 period, POC flux:SCOC ratios in the limited data collected during that period still showed a deficit (K. L. Smith et al., 2008). Nevertheless, SCOC is positively correlated to POC flux with no discernable time lag (Ruhl et al., 2008). Because the detrital aggregates may have represented an underestimated part of the POC flux input, an empirical estimation of aggregate POC flux was also made with the available data. Even including the occasional intense pulses of POC seen in the aggregate coverage data, there is still an overall deficit (K. L. Smith et al., 2008). Over the same period, the metazoan community did change (as described above) but there was no correlation between the synoptically observed SCOC and macrofaunal abundance or biomass. Thus, the microbial, meiofaunal, and protistan community are likely to dominate abyssal SCOC dynamics with macrofauna, like the megafauna, having a primary functional role of bioturbation.

4. Case Studies: Chemosynthetic Ecosystems Whilst the sedimented abyssal plains and bathyal slopes are dependent on a steady ‘rain’ of organic detritus from surface waters, chemosynthetic ecosystems can utilise in situ energy sources of reduced compounds, most often hydrogen sulphide or methane. These chemicals may have a geological source (e.g. at hydrothermal vents and cold seeps) or a biogenic origin— such as the carcass of a dead whale, a sunken log or even a shipwreck with an organic-rich cargo. The considerable similarities between these ecosystems in terms of the chemical habitat have created taxonomic affinities, functional similarities and in some cases species overlap between habitats that may initially appear quite different. Whilst chemosynthetic ecosystems are globally widespread (Fig. 1.11 illustrates those that are discussed in this review), they are often relatively isolated from each other, creating habitat ‘islands’ on the deep seafloor. A number of faunistic compositional and biogeographical paradoxes have emerged with the recent study of chemosynthetic ecosystems that must to some extent be explained by their geographic isolation and unique habitat conditions. The dramatic differences in species composition may also reflect differing scales of temporal change that depend on the geological or biological drivers that are prevalent. Studies of chemosynthetic ecosystems, in particular those with hardsubstrates, was more or less impossible prior to the invention of deep-water

VENT - NORTH-EAST PACIFIC RISE

WHALE FALL - NORTH ATLANTIC

SEEP - FLORIDA ESCARPMENT

Tjärnö

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CoAxial site Axial volcano Northern cleft

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45⬚N WHALE FALL - SOUTHERNCALIFORNIA Monterey canyon

Menez Gwen Lucky strike

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Rainbow 15⬚N 0⬚

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Figure 1.11 Geographic and bathymetric localities for known deep-sea chemosynthetic ecosystems with benthic time-series data. Bathymetric countours are 500 m interval (or 1000 m in some instances for clarity). Data from GeoMapApp (http://www.geomapapp.org).

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video systems, submersibles and most recently ROVs. For these reasons, it is a young and constantly shifting scientific field. Entire ocean basins remain almost completely unstudied, and our knowledge of temporal patterns comes from the relatively few sites described here, the majority of them hydrothermal vents.

4.1. Hydrothermal vents When hydrothermal vents were first discovered it was quickly realised that, although biologically rich, they were likely to be ephemeral both in space and time. In particular, the fields of dead clams first noticed near the Galapagos in 1977 suggested that cessation of fluid flow, or eruptions, may periodically wipe out entire local populations. However, it has proved difficult to mount expeditions with a sufficient temporal resolution to truly study successional processes at vents. This has been achieved at only a handful of better-known sites. There has always been a trade-off in terms of the allocation of ship-time between repeat visits and searching for new vents, especially as vent fauna exhibit such intriguing biogeographic patterns. In general, time-series data has been obtained from cruises that were launched in response to a major eruption (e.g. the famous 1991 eruption at 9 N), or by piecing together data from a series of discrete cruises that were not originally designed for temporal studies. In almost all cases, biological data is in the form of video surveys, with only small samples being taken for the obvious reason that major sampling would severely impact on the studied community. Major problems with such image sampling include the difference between videos taken from manned submersibles and ROVs. In the former case, the video is often secondary to the personal notes and observations of the observer. In the latter case, the video is the basis for all observations. Additional problems include locating the same vent edifices and communities after major geological changes. Despite the many recent vent discoveries in the west Pacific, Indian Ocean and southern Atlantic, the only real long-term study sites are in the East Pacific and North Atlantic. 4.1.1. East Pacific Rise The East Pacific Rise (EPR) is a mid-oceanic ridge that extends continuously along the floor of the Pacific Ocean (Fig. 1.11). It lies 2–3 km below sea level and rises above the surface to form Easter Island and the Galapagos Islands. This divergent tectonic plate boundary separates the Pacific Plate from the North American, Rivera, Cocos, Nazca, and Antarctic Plates. The EPR was the site of the first hydrothermal vent discovery in 1977, at the Galapagos Spreading Centre (GSC) ‘Rose Garden’ (Lonsdale, 1977). Since that time,

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several more vent fields have been discovered and named for the degree of latitude that they lie closest to. The best studied are at 21 , 13 , and 9 N. Rose Garden (GSC): This famous ‘textbook’ vent site was visited in 1979, 1985, 1988, 1990, and 2002. It represents a typical low-temperature site with community zonation from the vent to the periphery (Van Dover, 2000). During the two first visits, no major venting fluctuations were observed but the Riftia pachyptila tube-worm population, which was luxuriant in 1979 (and thought to be the first coloniser) had been outcompeted by Bathymodiolus thermophilus mussels (Hessler et al., 1985). These mytilid mussels harbour a mixotrophic type of symbiosis. In 1988, the population of Calyptogena magnifica clams had grown dramatically and surrounded the mussel beds probably due to a decrease in fluid flow (clams are able to insert their foot in cracks to pump the sulphide). In 1990, the peripheral fauna (anchored siphonophores, serpulids, anemones) had moved into the active area and the whelk (Phymorhynchus sp.) and squat lobster (Munidopsis sp.) populations increased. In 2002, the community was buried by fresh basaltic sheet flow and a nascent site ‘Rosebud’, which includes an assemblage of young vent animals (Shank et al., 2003), was discovered 300 m northwest of the last known position of the Rose Garden site. 21 N: This vent field is characterised by tall sulphide mounds and is dominated by large fields of clams (Van Dover, 2000). The site was visited in 1979, 1982, and 1990. Beds of dead clams indicate that the segment has been active for at least 300 years based on the dissolution rates of the clam shells (Kennish and Lutz, 1999). The comparison of venting patterns and community distribution between 1979 and 1990 demonstrates temporal stability on at least a decadal scale (Desbruye`res, 1998; Hessler et al., 1985). 13 N: This complex set of seven active vent sites, dominated by tubeworms, mussels, and alvinellid polychaetes, was visited in 1982, 1984, 1987, 1991, 1992, 1996, and 2002. Between 1984 and 1987, a rearrangement of subsurface circulation led to the collapse of two active sites and the reactivation of a previously dead area. Conversely, some sites situated 100 m north of this field were not affected. The reactivated site ‘Genesis’ was previously visited in 1984 and showed no measurable temperature anomaly. The fauna was composed of only a small clump of small-sized mussels and some groups of rusty and empty tubes of the siboglinid Tevnia jerichonana. By 1987, warm water (23 C) venting covered an extensive area and whitish microbial mats and deposits were observed around the vent openings. The fauna was dominated now by the vent crab Bythograea thermydron and widespread populations of T. jerichonana mixed with young individuals of Riftia pachyptila (Desbruye`res, 1998). In 1990, diffuse emissions were concentrated at several points at the Genesis

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site. The extensive population of T. jerichonana had collapsed and was replaced by small clumps of R. pachyptila. Active chimneys up to 5 m high developed and were colonised by large alvinellid populations dominated by Alvinella pompejana. During the following decade, no major large-scale changes occurred and the site was stable. 9 N: This site comprises multiple black smokers and low-temperature vents within an axial valley, and is the site of a long-tem monitoring transect (the BioGeoTransect) established after the April 1991 eruption. This event covered a large proportion of the ridge crest with a fresh basaltic sheet and wiped out some of the established vent communities. Nevertheless, in some places, clumps of worms and mussels survived the eruption and the lava flow. These cruises led to the first documentation of surprisingly fast rates of temporal succession in vent communities (Shank et al., 1998; Fig. 1.12). Nascent hydrothermal vents and adjacent glassy basalts were covered by an extensive and patchy white bacterial ‘floc’ and the water was cloudy with apparent ‘floc’ (Desbruye`res, personal observation and Haymon et al., 1993). Large populations of Bythograea thermydron and other mobile species, probably feeding on increased biological production, were observed. Nine months later, the microbial coverage had decreased (60%) and the venting focused on restricted areas; the level of hydrogen sulphide decreased by almost half. Numerous venting fissures were occupied by dense populations of T. jerichonana (Desbruye`res, 1998) with tubes up to 30 cm long. Less than 32 months after the eruption, dramatic changes in the vent community were observed at the same location (Shank et al., 2003). Large clumps of R. pachyptila had settled, reaching lengths of 1.5 m, suggesting that individuals reached maturity in less than 20 months. The smokers had grown rapidly and their walls were colonised by alvinellid polychaetes. Fifty-five months after the initiation of venting, Bathymodiolus thermophilus colonised the seafloor around the live vestimentiferan clumps. 4.1.2. North-East Pacific The Juan de Fuca Ridge (JdF) in the north-east Pacific has hosted several decades of hydrothermal vent research. This ridge is bordered by the Explorer Ridge to the north and by Gorda Ridge to the south (Fig. 1.11). It is formed of seven different segments, most of them harbouring active vent sites (Baker and Hammond, 1992). These segments appear to be at different stages of magmatic and tectonic evolution, resulting in differences in hydrothermal activity (Delaney et al., 1992; Embley et al., 1990, 1991). The vents are linearly distributed along the ridge axis (Tunnicliffe, 1991) and their depths vary from 1500 to 2400 m. while individual vents can be separated by a few metres or kilometres within a single vent field, vent fields may be separated by tens to hundreds of kilometres on one segment (Tsurumi and Tunnicliffe, 2001).

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A

B

C

D

E

Figure 1.12 Five years of community change at a specific hydrothermal vent (Biomarker #9) following the April 1991 eruption at 9 N on the East Pacific Rise. (A) April 1991, flocculent bacterially generated material visible in the days/weeks after the eruption; (B) March 1992, biomarker is in place and tubeworms (Tevnia jerichonana) colonising the fissure; (C) December 1993, the giant tubeworm Riftia pachyptila has colonised, overgrowing the population of Tevnia; (D) October 1994, the R. pachyptila population has recruited and continues to grow; (E) November 1995, the population of R. pachyptila is now over 2000 individuals and the tubes are stained with rust-coloured ferrous oxide precipitate. Arrow in C, D and E indicate a common reference point. Image courtesy of Tim Shank, Woods Hole Oceanographic Institution and adapted from Shank et al. (1998).

In the north-east Pacific, several studies have assessed the temporal variability of hydrothermal ecosystems, most of them related to catastrophic events on the seafloor. The first identified eruption on mid-ocean ridges occurred in 1986 on the northern Cleft segment of the Juan de Fuca ( JdF) (Baker et al., 1989). It initiated a 6-year study of successional patterns at vents (Tsurumi and Tunnicliffe, 2001). Additional studies at NEP sites

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followed different eruption events: two on the Axial Volcano after the 1986 (Tsurumi et al., 1998) and 1998 eruptions (Levesque et al., 2006) and one on the CoAxial segment after the 1993 eruption (Tunnicliffe et al., 1997). Finally, a 4-year study was initiated on the Endeavour segment to assess the dynamics of a sulphide edifice and its inhabitants through repeated visits (Sarrazin and Juniper, 1999; Sarrazin et al., 1997). As on the EPR, most of these time-series studies are based on discrete annual or sub-annual observations, not on continuous temporal monitoring. North Cleft segment: The 1986 eruption on the Cleft segment led to the formation of an extensive megaplume whose characteristics suggested a sudden expulsion of fluids from an ancient hydrothermal system, initiated by an episode of seafloor extension (Baker et al., 1989; Embley and Chadwick, 1994). Following the disturbance, new lava flows and vigorous hydrothermal activity were observed. This eruption provided the opportunity to observe potential successional patterns of vent fauna from 1988 to 1994 (Tsurumi and Tunnicliffe, 2001). The communities found at Cleft in 1988 were characteristic of those found 2 years after an eruption on CoAxial segment (Tunnicliffe et al., 1997) and Axial Volcano (Tsurumi et al., 1998): extensive microbial mats, large Ridgeia piscesae tube worm bushes, abundant and well dispersed Paralvinella pandorae polychaetes and ‘floc’ particulates within the cracks (Tsurumi and Tunnicliffe, 2001). Between 1988 and 1990, the microbial coverage decreased, the siboglinid and alvinellid polychaetes changed and flocculated particles disappeared. Within 5 years, most diffuse habitats were lost and the whole community became extinct probably due to the progressive decline in hydrogen sulphide concentrations (Butterfield and Massoth, 1994). On the other hand, areas of focused flow on hightemperature chimneys remained active on the Cleft segment but were only colonised by a limited number of species. The extreme unevenness of the Cleft community reflects dominance patterns that may be observed in frequently disturbed habitats, suggesting that the Cleft fauna appears to be ‘adapted’ to episodic eruptive events (Tsurumi and Tunnicliffe, 2001). Coaxial segment: Extensive accumulation of microbial-mineral ‘floc’ in association with abundant diffuse venting on new lava flows were observed after an eruption at this site in July 1993 ( Juniper et al., 1995). This eruption was the third to occur on this segment since 1981 (Embley et al., 2000). At the Floc site, rapid colonisation was observed despite the lack of adjacent vent communities (Tunnicliffe et al., 1997). Seven months after the eruption, several species had colonised the active sites, Ridgeia piscesae tube worms, alvinellid polychaetes (Paralvinella pandorae) and nemertean worms (Thermanemertes valens) being the most abundant. The greatest faunal recruitment occurred in the area where the microbes were most abundant (Tunnicliffe et al., 1997). The sulphide

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concentrations and temperature increased during the 1993–1995 interval. In July 1995, the biomass had increased and more polynoid predators, copepods, and gastropods were observed. At least 16 species colonised the site, most of them living in R. piscesae bushes (Tunnicliffe et al., 1997). A possible competitor of P. pandorae, Paralvinella palmiformis (Levesque et al., 2006), appeared in 1995. One-third of the NEP species had arrived within 2 years. Axial Volcano: Axial Volcano is an active volcano located at 1800 m depth on the central part of the JdF ( Johnson and Embley, 1990). In 1990, the summit was colonised by a few sessile animals and also by white microbial mats and crabs, indicating the presence of venting activity, whilst the vertical walls of the caldera were supporting a normal deep-sea fauna dominated by suspension feeders (Tunnicliffe et al., 1990). In 1986, a time-lapse camera was deployed over periods of 1, 5, and 26 days on the Mushroom vent. The most striking phenomenon was the rapid growth and collapse of anhydrite spires, which may have caused the mortality of 44% of the Ridgeia piscesae tube worms studied within the 26-day period (Tunnicliffe, 1990). Mass removal of animals by falling chimney fragments or landslides may be common in these vent habitats and significantly impact on the vent communities (Tunnicliffe, 1990; Sarrazin et al., 1997). A volcanic eruption occurred in 1998 on the South Rift Zone covering most of this 2 km2 areas with new lavas (Fig. 1.13). New venting activity of warm hydrothermal fluids (80 C) attracted a suite of hydrothermal species (Embley et al., 1999) and the basaltic seafloor was covered with white microbial mats. In June 1999, R. piscesae tube worms and additional consumer species had colonised the site (Levesque and Juniper, 2002; Fig. 1.13). A recent study, based on the 1998 eruption, proposes a general model of post-eruption succession for JdF macrofaunal communities at diffuse flow vents (Marcus et al., 2009). The model identifies six successional stages that are driven, on the one hand, by fluid conditions, and on the other hand, by biotic factors such as the provision of space by tube worms and intra- and inter-specific competition. This study further highlights the ability of the vent communities to rapidly colonise newly formed sites (Marcus et al., 2009). Endeavour segment: At Endeavour, vent communities are found either on the large sulphide edifices or in diffuse flow areas emanating from cracks in the basaltic seafloor (Tunnicliffe, 1990; Sarrazin et al., 1997). The edifices are colonised by mosaics of faunal assemblages where alvinellid and siboglinid polychaetes are important key-species (Sarrazin and Juniper, 1999; Sarrazin et al., 1997). The basaltic seafloor communities are dominated by Ridgeia piscesae tube worm communities (Urcuyo et al., 2003; Tsurumi and Tunnicliffe, 2003). The Sarrazin et al. model (Sarrazin et al., 1997, 1999, 2002; Sarrazin and Juniper, 1999) recognises six distinct faunal assemblages that form a mosaic community on the large

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A

B

Figure 1.13 Clusters of the tubeworm Ridgeia piscesae photographed on the Axial Volcano caldera hydrothermal vent. (A) Image taken shortly after the 1998 eruption (B) image taken 6 years after the eruption. Both images taken by ROV ROPOS and courtesy of the NOAA VENTS programme and Canadian Scientific Submersible Facility.

hydrothermal edifices of the Main Endeavour field. These assemblages appear to be representative of different successional stages that are primarily initiated by variations in hydrothermal fluid flow and substratum porosity. Thus, the progressive mineralisation of hydrothermal edifices contributes to fluid-flow modification at small spatial scales and faunal succession proceeds as the substratum matures (Sarrazin et al., 2002). Moreover, biotic processes such as particulate food diversification, growth of structuring species, or facilitation interact with abiotic conditions in driving successional patterns (Sarrazin et al., 1997, 2002). As mineralisation and succession progress on the edifice, the influence of other biotic factors such as predation and competition, becomes stronger. While abiotic factors appear to predominate in earlier successional stages, biotic factors modulate later successional stages such as the R. piscesae tube worm assemblages. Recent observations suggest that the hydrothermal activity of the southern part of this vent field may be waning substantially

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(K. Juniper, personal communication). Because of the dynamics of this fast-spreading ridge, most vent communities probably fail to reach stable or equilibrium conditions ( Juniper and Tunnicliffe, 1997). 4.1.3. Mid-Atlantic Ridge The Mid-Atlantic Ridge (MAR) is a long mountain range extending for about 16,000 km in a curving path from the Arctic Ocean to the southern extremity of Africa (Fig. 1.11). The ridge is equidistant between the continents on both sides. It mostly runs under the water but portions of it extend above sea level, forming the archipelago of the Azores and the Ascension and St. Helena islands, among others. The spatial frequency of venting on the MAR is on the order of one field every 100–350 km while in the Pacific Ocean, it can be as high as one active vent field every 5 km of ridge axis (Haymon et al., 1991; Murton et al., 1994; German et al., 1996). Mid-ocean ridge spreading rate exerts a geological control on the temporal variability of hydrothermal activity at the vent field scale. The interannual to decadal-scale ecological dynamics observed at several hydrothermal vent communities on the fast-spreading East Pacific Rise are associated with local interruptions of hydrothermal activity or disruption by volcanic events (Desbruye`res, 1998). In contrast, tectonic and volcanic events that can disrupt the pathways for vent fluids are less frequent on the slow-spreading Mid-Atlantic Ridge, resulting in greater temporal stability in the location and activity of vent fields. A large part of the northern MAR (15–35 N) has been monitored for 2 years for seismic events (D. K. Smith et al., 2003) and some variability in event rate along the MAR axis was observed. Groups of neighbouring segments appeared to behave similarly, producing an along-axis pattern with high and low levels of seismic activity (D. K. Smith et al., 2003). Moreover, due to differences in water depth, the geology of source rocks, and to hydrothermal deposits, vent habitats among MAR fields vary in their fluid chemistry and the distribution of minerals (Desbruye`res et al., 2000). Stochastic disturbance events (e.g. eruptions) are certainly less frequent on the MAR than in the Pacific. However, in 2001 a dike intrusion caused the largest teleseismic earthquake swarm recorded at Lucky Strike in more than 20 years, an one of the largest ever recorded on the northern MAR (Dziak et al., 2004). There were no obvious catastrophic consequences for the hydrothermal edifices, but independent observations reported an increase in the extent of microbial mats and diffuse venting, the latter especially along the sides and base of black smoker mounds, 3 months and 1 year after the dike intrusion (Dziak et al., 2004). Two groups of vent communities at different water depths are presently recognised among the hydrothermal vent fields of the Mid-Atlantic Ridge (Desbruye`res et al., 2001; Van Dover et al., 2002). The shallower vent fields

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include ‘Lucky Strike’ and ‘Menez Gwen’ on the plateau south of the Azores, while the other spans the deeper vent fields (>2500 m) located further to the south (TAG, Broken Spur; Fig. 1.13). In general, the shallower vent fields are dominated by Bathymodiolus azoricus mussels, with the deeper more southerly sites dominated by swarming shrimps, Rimicaris exoculata. TAG mound: The TAG site is a large hydrothermal sulphide mound and black smoker complex in the deep Mid-Atlantic (3600 m) and is the longeststudied vent community on the MAR (Rona et al., 1986). A quantitative comparison between 1994 and 2004 of the distribution and abundance of the fauna that occupies the central chimneys and the periphery on the upper terrace of the mound shows decadal-scale constancy in community structure at TAG (Copley et al., 2007). No significant difference in the coverage and abundance of the shrimp Rimicaris exoculata and the sea anemone Mariactis rimicarivora were observed over that period. Although not quantified, similar distributions of these species were noted in 1985 (Rona et al., 1986), suggesting these patterns may have persisted over two decades. In addition, TAG exhibits consistency in physical parameters on decadal timescales. The rise height of the hydrothermal plume, which is indicative of heat flux, appears to have been invariant over 10 years (Wichers et al., 2005), along with the geochemistry of high-temperature vent fluids (Parker et al., 2005). At the within-vent-field spatial scale and on shorter timescales, following Ocean Drilling Project (ODP) drilling at TAG in 1994 and a rise in seafloor temperature, dense aggregations of vent shrimps appeared over the 9 months that a time-lapse video camera was deployed, while the distribution of sessile species remained more or less the same (Copley et al., 1999). However, this change was transient and the central black smoker complex remained the focal point of high-temperature hydrothermal discharge at TAG. The NE quadrant had returned to relative quiescence, with aggregations of shrimp no longer present, by 2004 (Copley et al., 2007). Broken Spur: Initial submersible dives at the Broken Spur vent field (3100 m) found Rimicaris exoculata to be present but not in the dense aggregations seen at the TAG and Snake Pit sites. Subsequent observations at Broken Spur, including the discovery of sulphide structures with differing morphologies (Copley et al., 1997) and the evolution of single chimneys into structures with flanges (Allen Copley et al., 1998), suggest that aggregations of R. exoculata require substratum that is exposed to hydrothermal fluid flow (Ravaux et al., 2003). At individual chimneys, where most vent fluid is expelled from the summit, such habitat is not available and shrimp aggregations are reduced or absent, as confirmed by observations at other hydrothermal fields within the same province such as Logatchev (Gebruk et al., 2000). Dense aggregations of shrimp appear when accretion of sulphides on a single edifice leads to the production of over-flowing flanges. This geological control on shrimp populations operates over the timescale corresponding to the evolution of edifice morphology (Allen Copley et al., 1998).

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Temporal Change in Deep-Sea Ecosystems

Menez Gwen, Lucky Strike, and Rainbow: In contrast to the deep Atlantic vent sites (e.g. TAG), the shallower vent fields of Menez Gwen (850 m) and Lucky Strike (1700 m) are dominated by Bathymodiolus azoricus mussel assemblages (Fig. 1.14). Rainbow vent field (2300 m) could be regarded as intermediate between deep and shallow MAR fields. Hence, it harbours

A

B

C

D

E

F

Figure 1.14 Spatial and temporal heterogeneity at the Lucky Strike hydrothermal vent field, Mid-Atlantic Ridge. This vent is characterised by a high degree of patchiness (A), including bare rock surrounding the hot fluid exits (B), abundant populations of Bathymodiolus (C, D), and patches of vent shrimps and bacterial mats (D). It is thought that the vents on the Mid-Atlantic Ridge are more stable over long time periods than those of the East Pacific; here abundant mussel populations can be seen on the same region of the vent edifice during a dive in 1994 (E) and 2008 (F) suggesting stability over 10–15 year time periods. Images all #Ifremer.

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tall sulphide chimneys that host B. azoricus assemblages and Rimicaris exoculata aggregations, but both in lower densities than in respectively shallower and deeper hydrothermal vent sites. No detailed micro-distribution or temporal evolution studies have been published on Menez Gwen or Rainbow. However, at Rainbow vent field, changes in the form of broken chimneys have been observed between cruises, which might be caused by stochastic geological events (see Section 5.2.6), or the normal evolution and development of the spire chimneys. Lucky Strike is one of the largest known vent fields and one of the most visited in the Atlantic Ocean. It features several well-defined and active edifices, one of which, ‘Eiffel Tower’, is considered representative for the entire vent field (Desbruye`res et al., 2001). Faunal assemblages visibly dominated by either Bathymodiolus azoricus mussels or by alvinocaridid shrimps (Mirocaris fortunata and less abundant Chorocaris chacei) are distributed according to their access to resources, their tolerance and a viable position on the edifice (Cuvelier et al., 2009; Fig. 1.14). Change in any of these factors might shift the local equilibrium and induce a reorganisation or mortality. Von Damm et al. (1998) showed that short-term (3-year scale) changes in fluid composition and temperature at Lucky Strike were probably a result of the geological history (formation, age) of the seafloor and longevity of the current period of hydrothermal activity. Despite 17 international cruises to the Lucky Strike vent field, there has been a lack of synthesis on the temporal evolution of this site compared to the similarly well-visited north Pacific vent sites. A recent study has been undertaken of 14 years of temporal data from Lucky Strike. At a decadal-scale, the vent edifice is in general quite stable, while on shorter time-scales as well as at the smaller assemblage and patch-dynamic scales, changes do occur (Cuvelier et al., submitted). This first long time-series quantification of the rate of change at a slow-spreading MAR ridge supports the hypotheses that community dynamics are effectively slower compared to faster-spreading ridges such as those on the EPR (Cuvelier et al., submitted).

4.2. Cold seeps Cold seep and vent communities share many taxonomic and functional attributes, reflecting their similar evolutionary histories and use of chemoautotrophic symbioses. Like vents, the processes creating the seeps are predominantly geological, and hence we consider seeps to be ‘geologically forced’. However, the geological and chemical milieu in which they exist is quite different. Unlike vents, cold seeps are formed by a variety of different processes and have been recorded from a wide range of tectonic settings, including both active and passive margins (Levin, 2005; Sibuet and Olu, 1998). Furthermore, most of the methane and sulphide that sustain seep communities is ultimately of biological origin, although the proportion may

Temporal Change in Deep-Sea Ecosystems

47

vary between seeps. In addition to soft sediments, the precipitation of authigenic carbonate to form pavements, chimneys, and other constructs is a feature of many seeps (Foucher et al., 2009). Cold-seep communities were first discovered at the base of the Florida Escarpment, a dramatically steep slope in the Gulf of Mexico (Paull et al., 1984; Fig. 1.11). These communities were feeding on sulphide, methane, and ammonia-rich hypersaline brines that seep out of the base of the escarpment (Van Dover, 2000). In recent years, mud volcanoes and pockmarks associated with fluid and gas discharges on continental margins have also attracted a considerable research effort (e.g. Foucher et al., 2009; Vanreusel et al., 2009). Cold-seep communities include characteristic chemosynthetic taxa such as vestimentiferan siboglinids, vesicomyid clams, bathymodiolid mussels and alvinocarid shrimp, as well as polychaetes, nematodes and foraminifera among the smaller size classes (Sibuet and Olu, 1998; Levin, 2005; Vanreusel et al., 2009). Species are often congeneric with those found at vents, although rarely conspecific. Unfortunately, there are no real ecological time-series studies at seeps, and we must rely on inferences based on other lines of evidence to understand temporal trends. Fluid flow at cold seeps is variable, which results in a temporal variation in availability of methane, sulphide, and other porewater constituents (Levin, 2005). The seep fauna responds to this fluid flow variability with behavioural and physiological adaptations that either limit the exposure to toxic compounds or that enhance access to required compounds. Functional responses, such as small-scale migration (e.g. vertical movement within sediment) or numerical responses, including reproduction, recruitment, colonisation, and succession, are expected in the mobile or opportunistic taxa. Changes in diet, as reflected by carbon and nitrogen isotopic signatures, have also been observed in seep mussels (Dattagupta et al., 2004). The meso-timescale history of the fluid discharge at cold-seep sites can be reconstructed from the barium to calcium (Ba/Ca) ratio in vesicomyid clam shells. Hydrogen sulphide discharge is recorded as an enrichment in the Ba/ Ca ratio in clam shells collected live from cold seeps in Monterey Canyon and the Cascadia margin. For the Monterey canyon site, a 2-year episode of high fluid flow centred on 1993 was inferred from coherent changes in the Ba/Ca profiles of three Calyptogena kilmeri shells (Torres et al., 2001). 4.2.1. Gulf of Mexico The hydrocarbon and saline seeps of the Gulf of Mexico contain some of the best-described seep communities in the world. Cordes et al. (2009) proposed a theoretical framework for seep community succession based on hypotheses generated from the seeps on the upper Louisiana slope between 500 and 1000 m depth prior to the year 2000, and tested in a series of subsequent studies (Fig. 1.15). The earliest stage of a cold seep is characterised by a high seepage rate and the release of large amounts of biogenic

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A. G. Glover et al.

** * * * * * ** * * GC354 GB425 GB535 GB543 GB544

GC234 GC233 GC232 GC184

* *

VK825 MC885

Figure 1.15 Successional processes at Gulf of Mexico cold seeps inferred from community composition plotted using multi-dimensional scaling and ages of tubeworm aggregations (size of the circles). Seeps are initially colonised by mussel-dominated assemblages (asterisks), followed by tubeworm-dominated assemblages (circles), as the seeps age the tubeworms get larger and the community composition shifts. Figure modified from Cordes et al. (2009).

and thermogenic methane and oil (Sassen et al., 1994). As authigenic carbonates start to precipitate, they provide the necessary hard substrate for the settlement of vestimentiferans and mussels (Tyler and Young, 1999). These communities begin with mussel (Bathymodiolus childressi) beds containing high biomass communities of low diversity and high endemicity (Bergquist et al., 2003). Individual mussels live for 100–150 years, whereas mussel beds may persist for even longer periods (Nix et al., 1995). The next successional stage consists of vestimentiferan tubeworm aggregations dominated by Lamellibrachia luymesi and Seepiophila jonesi (Bergquist et al., 2003). Young tubeworm aggregations often overlap in time with, and normally persist past, mussel beds. These tubeworm aggregations and their associated faunas go through a series of successional stages over a period of hundreds of years. Declines in seepage rates result from ongoing carbonate precipitation (Sassen et al., 1994) as well as the influence of L. luymesi on the local biogeochemistry. In older tubeworm aggregations, biomass, density, and number of species per square meter, decline in response to reduced sulphide concentrations (Cordes et al., 2009). Once habitat space is made available, more of the non-endemic background species, such as amphipods, chitons, and limpets, are capable of colonising the aggregations. Due to the lower concentrations of sulphide and methane, the free-living

Temporal Change in Deep-Sea Ecosystems

49

microbial primary productivity is reduced. The number of associated taxa is positively correlated with the size of the tubeworm-generated habitat, so diversity in this stage remains fairly high although the proportion of endemic species is smaller in the older aggregations. This final stage may last for centuries, as the vestimentiferan tubeworms can live for over 400 years (Cordes et al., 2009). Once the seepage of hydrocarbons has declined, the authigenic carbonates of the relict seeps may provide a substrate for cold-water corals. The scleractinians Lophelia pertusa and Madrepora oculata, several gorgonian, anthipatharian, and bamboo coral species form extensive reef structures on the upper slope of the Gulf of Mexico (Schroeder et al., 2005). They also harbour distinct associated assemblages consisting mainly of the general background fauna, but also contain a few species exclusively associated with the corals and a few species that are common to both coral and seep habitats (Cordes et al., 2008). Unfortunately, in the absence of time-series studies at cold seeps, the reconstruction of the community succession proposed by Cordes et al. (2009) remains hypothetical.

4.2.2. Haakon Mosby Mud Volcano (HMMV) In addition to successional sequences driven by changes in seepage rates and biological interactions, temporal changes at seeps probably arise from physical processes associated with the fluid discharges. These are likely to be particularly prevalent on large mud volcanoes, such as the well-studied HMMV, located on the Barents Sea continental slope at 1270 m water depth (Fig. 1.1B). This structure is characterised by a central muddy area devoid of chemosynthetic organisms and with strong concentrations of methane, a rather flat inner zone with variable densities of the filamentous bacterium Beggiatoa, and a hummocky outer zone with variable densities of siboglinid polychaete tubes, sometimes accompanied by Beggiatoa (Gebruk et al., 2003; Soltwedel et al., 2005b). A moat-like feature encircles the mud volcano. High-resolution microbathymetry of the HMMV has revealed flat features, interpreted as recent mud flow, that protrude into peripheral hummocky areas, which are believed to represent old mud flows ( Jerosch et al., 2007). The HMMV is a highly active mud volcano characterised by high rates of discharge of methane-laden mud, fluid, and gas (Sauter et al., 2006). These discharges cause mudflows on a time-scale of a few years (Foucher et al., 2009) that are likely to severely disturb the benthic communities occupying the outer parts of the mud volcano. Indeed, preliminary evidence suggests that changes occurred in the distribution of microbial mats and siboglinids between 2003 and 2006 (Vanreusel et al., 2009). Similar processes may occur on other mud volcanoes, for example, in the eastern Mediterranean (Foucher et al., 2009).

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4.3. Whale-falls When whales die they sink to the seafloor, creating ‘whale-falls’ that provide enormous point-sources of organic carbon in an otherwise foodpoor deep sea. The huge size of the great whales has led many to speculate on their final fate, and the organisms that may consume them (Smith and Baco, 2003). This debate has become even more relevant since we now understand that pre-whaling whale population sizes (and hence whale-fall habitats) were likely orders of magnitude greater than previously thought (Roman and Palumbi, 2003). The first species found associated with a whale-fall was a small mytilid mollusc, Idas simpsoni, found clinging to a whalebone trawled up by a Scottish fisherman (Marshall, 1900). This species is now known to belong to a genus of mytilids that use chemosynthesis to gain energy (Distel et al., 2000). In 1987, the remains of a large balaeonopterid whale were discovered by scientists in the DSV Alvin in 1200 m of water in the Santa Catalina Basin (Smith et al., 1989). In the 1990s and more recently, several studies have been undertaken of temporal succession on whale-carcasses in both deep and shallow-water, mainly using dead stranded whales that are deliberately sunk at a known location. Unlike a hydrothermal vent, a whale-fall habitat can be artificially created (by sinking a whale) and as such they are amenable to temporal studies, especially as the time point of origin is known.

4.3.1. Southern California whale-falls Studies conducted over a period of more than a decade, mainly of implanted whale remains in southern California (Fig. 1.11), have shown that large whale-falls may be extremely persistent in the deep sea, and support quite long-lived faunas that are partly heterotrophic and partly chemosynthetic (Smith and Baco, 2003). The initial scavenging stage of whale-fall succession may take between 6 and 18 months, during which time the remains are skeletonised mainly by the actions of scavenging hagfish (Eptatretus deani and Myxine circifrons), sleeper sharks (Somniosus pacificus) and lithodid crabs (e.g., Paralomis multispina). The scavenging stage is followed by a period where opportunistic species may consume the highly enriched sediments and organics leaching from the bones. This includes large numbers of the well-known opportunistic polychaete Ophryotrocha sp., as well as very high numbers of ‘carpet worms’ (Chrysopetalidae, Vigtorniella flokati and Vigtorniella ardabilia) (Wiklund et al., 2009). The enrichment opportunist stage is then followed by a relatively long period where chemosynthetic organisms can take advantage of hydrogen sulphide flux from the bones and enriched sediments around the bones, known as the ‘sulphophilic’ stage (Smith and Baco, 2003). These include vesicomyid clams and vestimentiferan siboglinids, some conspecific with those found at vents and seeps.

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51

During both the enrichment opportunist stage and the sulphophilic stage, the whale bones of most whale-falls are consumed by Osedax sp., a clade of heterotrophic siboglinid polychaetes that has only recently been discovered (Rouse et al., 2004; Glover et al., 2005; Fujikura et al., 2006). These animals possess symbiotic bacteria housed within a root system that dissolves and penetrates the bone itself, possibly using lipids and/or bone protein as an energy source (Goffredi et al., 2007). It might be expected that the prevalence of Osedax sp. on whale-falls would result in the bones becoming rapidly eaten and the whale-falls relatively short-lived (e.g. Braby et al., 2007). But experiments based on radioisotope dating of bones suggest that bones from natural whalefalls may have been on the seabed for 40–80 years (Schuller et al., 2004). The degree of Osedax sp. consumption may be quite different depending on the ecological setting of the whale fall, and other factors such as the degree of bone calcification. In a deep shelf (120 m) environment of the west coast of Sweden, a small minke whale has been supporting a specialist whale-fall fauna (including Ophryotrocha sp., Vigtorniella sp., and Osedax sp.) for over 5 years, despite the location being hydrodynamically complex, subject to a high degree of sedimentation and an extensive benthic scavenging fauna (Fig. 1.16; Dahlgren et al., 2006; Dahlgren and Glover unpublished observations).

Figure 1.16 Temporal change over 6 years at a single whale-fall site in Kosterfjord, Sweden: (A) remains of a dead 5 m long minke whale at 125 m at time of implantation; (B) 2 weeks following implantation, hagfish (Myxine glutinosa) and shark bites visible; (C) 6 months following implantation, complete skeletonisation and first colonisation by Osedax mucofloris; (D) 3 years since implantation, skeleton starting to become covered by sediment, still supporting Osedax population; (E) 4 years since implantation, bone processes becoming degraded by Osedax activity (arrowed specimens); (F) 5.5 years since implantation, skull and mandibles partially covered by sediment, Osedax still growing on underside of skull. All images courtesy of Thomas Dahlgren, Go¨teborg University and Dahlgren et al. (2006).

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5. Discussion The deep sea is isolated from us by a thick layer of water, opaque to almost any instruments we deploy in space, the atmosphere or on the surface of the ocean. This simple fact made it impossible to appreciate the dynamic nature of most deep-sea environments until very recently. Images of the deep seafloor did not become available until the 1960’s, and time-series studies did not start until the mid 1970s. Even these studies were not designed for long-term monitoring. In most cases they were located at the most convenient area of deep ocean to reach from a ship’s home port, and were hence subject to repeat opportunistic sampling. There has been a constant trade-off between the need to increase spatial coverage of sampling with the need to take repeat measurements at a single site. The fact that in the Earth’s largest habitat—the abyss—there are only two sites with more than 10 years of benthic data suggests that in general our efforts have been greater with regard to geographic coverage. However, vast areas of the abyss (e.g. the entire south Pacific Ocean) still remain essentially unexplored. Chemosynthetic ecosystems, such as hydrothermal vents, are so isolated and difficult to find that in many cases repeat visits have been made for reasons unrelated to time-series analysis, such as analyses of local species diversity and ecology. These early repeat visits, to sites such as 9 N and Lucky Strike, have since evolved into more directed long-term programmes. Climate change has forced ecological researchers to look again at what long-term data are available for ecosystems. The deep sea is no exception. As a major carbon sink, and a potential repository for carbon dioxide via bio- or geo-engineering schemes, it is clear that improved understanding of natural benthic processes is needed. In particular, it has become apparent that benthic processes are tightly coupled to pelagic ones, and that the deepsea should not be ignored in the crucial science of ocean–atmosphere interactions (C. R. Smith et al., 2008; K. L. Smith et al., 2009). Here, we consider first the long-term responses seen in deep-sea ecosystems driven by biology and geology. We then discuss the potential impacts of climate change, and finally the role of stochastic and successional processes in shaping the deep-sea biology that we observe.

5.1. Biological responses to environmental change The science of environmental change uses a variety of terms which can be confusing, and refer to conceptual ideas that inevitably overlap. For example, there is a distinction made between climate change and climate variability, the former referring to a secular trend over time, the latter to changes that exhibit some periodicity on a particular scale. In the science

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of climate-change impacts, the crucial question is usually whether a change observed is a ‘real’ change or just a snapshot of natural variability about a mean, or variability associated with some periodic driver (e.g. ENSO). The term variability is often applied to short-term fluctuations (daily, monthly, or inter-annually), and change is used to describe long-term change (decades to millions of years) (Murray, 2000). The temporal perspective of observation is crucial. It is hard to think of the change from a Pleistocene glacial to an inter-glacial as anything other than a significant, large scale change over thousands of years, but on a scale of millions of years, such glacial-scale change can appear as variability (albeit with periodicity) around a mean. Likewise, the ‘variability’ we associate with ENSO events on decadal scales are in fact a series of changes over interannual time periods with major, global-scale consequences for ecosystems and human activities. More important than the difference between short-term change and long-term change is whether the change is stochastic, cyclic or progressive (Fig. 1.17). Volcanic eruptions are stochastic, although with a predictable power-law frequency. Both ENSO events and glacial– interglacial events are cyclic; human-induced climate change is (at present) a progressive trend. However, any cyclic event includes periods that are progressive trends, such as the warming of the planet as it comes out of a glacial period.

ive

ss

re og

Variable

Pr

Cyclic Stochastic

Time

Figure 1.17 Changes in a variable over time viewed as cyclic (blue), stochastic (green) or progressive (red) dependent on the scale of observation.

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We discuss here the published data for changes observed at sedimented ecosystems and chemosynthetic ecosystems. We focus on examining whether the changes are significant, whether they are likely to be progressive, cyclic or stochastic and if a specific driver can be identified. 5.1.1. Biological responses at sedimented ecosystems We identified 11 sites where data on recent long-term change were available (Table 1.2, Fig. 1.5). The earliest time point was 1973 (for the Rockall Trough), and the longest time series are for the PAP (16 years) and Station M (20 years). Apart from these two sites, only three sites have more than 5 years of data, and the remainder less than 5. There is only a single site in the southern hemisphere, and it has only 3 years of temporal data (although studies are ongoing). The sites for which there is some evidence for progressive trends are HAUSGARTEN, the Cretan Sea, PAP, and Pacific Station M (Table 1.2, and references therein). HAUSGARTEN provides the clearest evidence yet that bottom waters are warming in response to climatic change (Fig. 1.6). This warming trend is associated with a decrease in deep POC flux, and hence food availability, at the seafloor. However, the evidence for a dramatic change in benthic biology (e.g. community structure) in response to this change is so far inconclusive. For the Cretan Sea site, significant changes in bottom-water temperature were recorded that were correlated with significant changes in nematode species diversity. A cooling period was associated with an increase in diversity and a warming period with a decrease in diversity (Section 3.1.2). However, for the cooling period, the diversity change is only based on two measurement periods (1989 and 1994), while for the warming period, the change is very small. These data therefore represent only preliminary evidence for a change in benthic biology in response to a climate variable. At PAP, the time series is much longer (16 years) and based mainly on megafaunal abundance surveys derived from trawl samples, supplemented by core material for smaller faunal groups. A progressive trend from 1989 to 2002 involved a marked increase in the abundance of several key megafaunal taxa—the ‘Amperima event’ (Section 3.2.1, Table 1.2 and references therein). Later analysis of video data, and samples from other taxa (fish, polychaetes, nematodes, and foraminifera) have supported the view of a long-term change in community structure at PAP, possibly in response to changes in food supply linked to the NAO index (Fig. 1.9). However, the apparent reversion in more recent samples of the community composition to levels closer to those in 1989 suggests that the observed changes may be either stochastic or cyclic. Only longer-term data will resolve this question. For the Pacific Station M site, a long (17 years for Booth et al., 2008; K. L. Smith et al., 2008; Smith et al., 2008c) time series is also available, again

Table 1.2 Summary of data availability and key identified parameters and long-term temporal trends at sedimented ecosystems

Habitat

Site

Latitude

Longitude

Depth (m)

Key Oceanographic data

Key Benthic biological data

Temporal scale

Key identified longterm trend and forcing factor

Type of longterm change

Key references

Bathyal–Abyssal Arctic sediment

HAUSGARTEN

79 N

4 E

1200– 5500

Pelagic and benthic POC flux and composition; temperature

Sediment pigments; nematode and megafaunal abundance and diversity

2000–2008 (temperature); 2000–2005 (sediment flux); 2002–2004 (megafauna)

Progressive Decrease in deep POC flux driven by trend? increase in temperature; potential shift in community structure

Soltwedel et al. (2005a); Hoste et al. (2007); Bauerfeind et al. (2009)

Bathyal Mediterranean sediment

Cretan Sea

35 760 N

25 100 E

1540

Bottom-water temperature

Nematode abundance and diversity

1989–1998

Increase in nematode Progressive trend? diversity during cooling (1990– 1994), decrease during re-warming

Danovaro et al. (2004)

Bathyal–Abyssal Mediterranean sediment

Ierapetra Basin

33 440 N 34 300 N

26 080 E 26 110 E

2500– 4500

POC flux (inferred from hydrographic context)

Sediment phytopigments; meiofauna

1987–1999

Stochastic Increase in shifts opportunistic species in response to stochastic shifts in POC flux

Tselepides and Lampadariou (2004); Lampadariou et al. (2009)

Bathyal oxygen minimum zone sediments

Globally distributed along margins

n/a

n/a

50– 1000

Surface production, benthic oxygen, temperature,

Faunal abundance and diversity across the OMZ region (spatial)

Inferences based on change in OMZs; 1997– 2003 ENSO shift

Shift in foraminferal Stochastic species composition shifts driven by hypoxia; decrease in macro and megafaunal

Levin (2003); Gooday et al. (2009)

Bathyal Atlantic sediment

Bay of Biscay

43 500 N

2 230 W

550

Surface production inferred from SeaWIFS

Sediment oxygen profiles, foraminiferal abundance

1997–2001

No change No obvious longterm trend (seasonal only)

Fontanier et al. (2003, 2005)

Bathyal Atlantic sediment

Rockall Trough: 57 180 N 54 400 N ‘Station M’ Permanent Station

10 110 W 12 160 W

2200– 2900

Limited hydrographic Macrofauna and and sediment data megafauna abundance, reproductive condition

1973–1984 (sporadically thereafter)

Initial analyses indicated interannual variation but analyses of longer time series needed.

Stochastic shfits

Gage et al. (1980), Tyler (1988)

(continued)

Table 1.2

(continued) Key Oceanographic data

Key Benthic biological data

Temporal scale

Key identified longterm trend and forcing factor

Type of longterm change

Habitat

Site

Latitude

Longitude

Depth (m)

Bathyal Pacific sediment

Sagami Bay

35 N

139 220 E

1400

Surface production, POC flux

Sediment chloroplastic pigment; foraminferal and copepod abundance

Bathyal Antarctic sediment

FOODBANCS

65 S

65 W

500–600

Surface production (LTER data), POC flux

1999–2001 (and Video and ongoing) photography; faunal abundance; microbial biomass; sediment quality; reproduction

Buffered seasonal signal (sediment foodbank) with major inter-annual shifts

Abyssal Atlantic sediment

PAP

48 500 N

16 300 W

4850

Surface production, POC flux

1989–2005 Video and (and ongoing) photography; faunal abundance and diversity; microbial biomass; sediment quality; reproductive condition

Increase in Progressive megafaunal trend, abundance and amidst composition shift stochastic from 1989–2002 variation (‘Amperima event’). Species-level shifts in foraminiferal and polychaete abundance and composition; shifts in abundance of major meiofaunal taxa.

Billett et al. (2001, 2010); Gooday et al. (2010); Kalogeropoulou et al. (2010); Soto et al. (2010)

Abyssal Pacific sediment

Station M

34 500 N

123 W

4100

Surface production, POC flux

Sediment community oxygen consumption; bioturbation; macro/ megafaunal abundance; fish abundance and composition

Progressive Shifts in faunal abundance and size, trend, amidst and ecosystem stochastic functions—all signal related to availability of food at the seafloor.

Ruhl et al. (2008), Ruhl and Smith (2004)

1996–1998

1989–2004 (and ongoing)

No obvious longNo change term trend (seasonal only)

Stochastic shifts

Key references

Kitazato et al. (2000, 2003)

C. R. Smith et al. (2006)

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mainly covering the mobile megafauna. This faunal component exhibits significant changes in community composition that are correlated with changes in food availability at the seafloor. As with the PAP, it is not clear if the variations have a progressive trend related to long-term climate change or are part of a stochastic or cyclic variation (climate variability). The link between the ENSO index (NOI), surface production, export flux, POC flux to the seafloor, and the shifts in community composition suggest that if a trend does become apparent in surface productivity, the signal would be transmitted by POC flux to the seafloor biota. Again, longer-term data will be needed to determine if climate change will indeed alter the composition and/or functioning of abyssal communities. Discounting seasonal signals (not discussed here), two sites (Bay of Biscay and Sagami Bay) exhibit no significant long-term changes (Table 1.2). For the remainder of the sites, changes are observed but it is very difficult to ascertain whether they represent any long-term trend owing to lack of data. For the Ierapetra Basin site, the data suggest that, at the very least, stochastic shifts in food availability occur in the abyssal Mediterranean, and that the benthic community can respond quickly. For bathyal OMZs, we can infer the type of changes that must take place based on evidence from the local impact of the hypoxia (measured in space) with our hypothesised frequency and severity of hypoxic events in the past. A level of inter-annual variability has been detected at both the Rockall Trough and FOODBANCS sites, but the time-series are either not yet long enough to have detected any progressive trends (FOODBANCS) or have been discontinued (Rockall Trough). 5.1.2. Biological responses at chemosynthetic ecosystems Twelve hydrothermal vent sites were identified as yielding useful long-term data (Table 1.3). For cold seeps, repeat visits to the same sites are scarce, or have gone unpublished, and inferences are made based on what is known about cold seep biology. For chemosynthetic ecosystems of biogenic origin (e.g. whale-falls), time-series data are available for sites in the north-east Pacific, and fjords of the Swedish west coast. The earliest major biological studies at a vent ecosystem took place in 1979 at Rose Garden on the EPR, not long after their discovery by geologists in 1977. Not surprisingly, this is the site for which we have the longest data set (1979–2002) but there are enormous gaps in the data (e.g. a 12-year gap between 1990 and 2002). The main reason for such gaps is the difficulty in getting funding for repeat visits as opposed to searching for new vents. Probably, the best temporally resolved dataset for a hydrothermal vent is that for the 9 N site (also on the EPR), where surveys were taken every year for 5 years following the April 1991 eruption (Shank et al., 1998; Fig. 1.12). For the Mid-Atlantic Ridge sites, despite many repeat visits under different oceanographic programmes, there has been a lack of

Table 1.3 Summary of data availability and key identified parameters and long-term temporal trends at hydrothermal vents. Geographic data and geological notes from Van Dover (2000). In almost all cases, biological data is in the form of video observations from ROVs or submersibles, with faunal sampling Habitat

Site

Latitude

0

Depth (m)

Key geological features

Temporal scale

109 5 W

2600

Tall sulphide edifices

1979–1990

Longitude 0

20 49 –50 N

0

East Pacific Rise Vent East Pacific Rise Vent

21 N

Rose Garden 00 480 N

86 130 W

2500

Absence of hightemperature vents

1979–2002

East Pacific Rise Vent

13 N

12 38–540 N

103 500 – 104 10 W

2600

Tall sulphide edifices

1982–2002

East Pacific Rise Vent

9 N

9 45–500 N

104 17W

2500

North-east Pacific Vent

North Cleft

44 38–410 N

130 230 W

2250

Black smokers and 1991–ongoing low-temp vents in a linear array within axial trough; 1991 eruption Cleft centre of axial 1988–1994 valley, large sulphide edifices

North-east Pacific Vent

Coaxial segment

46 200 N

129 400 W

2200

Eruption in 1993, with 1993–1995 diffuse venting on new lava flows following

Key identified long-term trend and forcing factor

Apparently stable over decadal scales Succesion from luxuriant Riftia to dominance by Bathymodiolus, then Calyptogena. Buried by lava flow in 2002, with recolonisation by juveniles at nearby ‘Rosebud’ site. Several rapid shifts in community composition observed in response to stochastic changes in fluid flow A major eruption in 1991 led to observations of succession, from initial flocs of bacterial mat to Tevnia, Riftia and Bathymodiolus.

Key references

Hessler et al. (1985); Desbruye`res (1998) Hessler et al. (1985); Shank et al. (2003)

Desbruye`res (1998)

Shank et al. (1998); Desbruye`res (1998)

Successional patterns following Tsurumi and eruption in 1986- initial Tunnicliffe (2001) observations of bacterial mats, Ridgeia, Paralvinella, followed eruption, with subsequent decrease in biological activity driven by reduction in sulphide availability. Rapid colonisation following Tunnicliffe et al. eruption by Ridgeia, Paralvinella (1997) and nemertean worms, linked to microbial abundance

North-east Pacific Vent

Axial volcano

45 570 N

130 020 W

1800

North-east Pacific Vent

Endeavour segment

47 570 N

129 400 W

2250

Mid-Atlantic Ridge Vent

TAG Mound

26 080 N

44 490 W

3600

Mid-Atlantic Ridge Vent

Broken Spur 29 100 N

43 100 W

2200

Mid-Atlantic Ridge Vent

Menez Gwen

37 17.5 N

32 160 W

1700

Small sulphide mounds 1994–2006 on the flanks of a volcano

Mid-Atlantic Ridge Vent

Lucky Strike 37 17.50 N

32 160 W

1700

Multiple sulphide 1994–2008 edifices around a lava lake

Active volcano. Noted 1986–2002 rapid growth and collapse in anhydrite spires. Eruption in 1998. Large sulphide 1991–1995 edifices, with flanges and pooled hot water

Large sulphide mound 1994–2004 with black smoker complex and periphery Multiple sulphide 1994–1997 mounds

On short-time scales (days) major Tunnicliffe (1990); distubances from collapsing Embley et al. (1999); spires. On longer-scales (years?) Marcus et al. (in periodic eruptions and rapid press) recolonisation. Successional model proposed Sarrazin et al. (1997, based on variations in fluid flow 2002) and substrate porosity. Potential for Southern part of vent possibly waning. Evidence suggests decadal-scale Copley et al. (2007) constancy of venting and of community structure. Aggregations of the shrimp Allen Copley et al. Rimicaris exoculata are variable (1998) depending on the shifts in fluid flow, which are driven by the production of overflowing flanges. Dominance of the mussel Colac¸o et al. (1998); Bathymodiolus azoricus. Covering Desbruye`res et al. the sulphides and some fresh (2001) pillow lavas. Synthesis of long-term temporal Cuvelier et al. evolution at this site is lacking, (submitted) studies are underway.

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synthesis of temporal data. This is now being addressed through a major study of the Eiffel Tower hydrothermal construct in the Lucky Strike vent field (Cuvelier et al., submitted). In summary, none of the investigated sites show an obvious progressive trend. Neither are changes apparently cyclic, for example associated with some regular and periodic switching on and off of hydrothermal fluid flow. Where changes have been observed, they appear to be stochastic shifts associated with major eruptions, seismic swarms or redirections of hydrothermal vent ‘plumbing’. At two sites on the EPR (Rose Garden and 9 N) and two sites on the NEP (North Cleft and Axial Volcano) major eruptions have been observed and the successional processes following those eruptions monitored. These sites have led to a model of EPR (but not NEP) vent succession from a microbe-dominated community, to one dominated by siboglinid tubeworms, and finally by chemosynthetic molluscs. These changes are thought to occur over a period of a few years following an eruption. On a finer scale, a successional model has been proposed to account both for the spatial mosaic and temporal changes on vent edifices of the NEP (Sarrazin et al., 1997, 2002). In this more complex scenario, changes at individual vent edifices can occur quite rapidly on small scales following shifts in fluid flow, substratum porosity and vent mineralisation. Changes are not thought to be in the form of linear succession, with the early dominance of abiotic factors becoming less significant as biological interactions predominate on more biologically active patches. In general, EPR and NEP vent habitats are unlikely to be in stable or equilibrium conditions. In contrast to the Pacific sites, the Mid-Atlantic Ridge vents show little evidence for major stochastic events such as eruptions. This may be simply because they have not yet been observed. However, repeat visits to sites such as TAG mound do suggest decadal-scale constancy of venting and community structure (Copley et al., 2007). On a finer scale, changes have been observed in the patch-mosaic structure of vent animals at Lucky Strike (Cuvelier et al., 2009) and in the response of swarming shrimp to the changes in fluid flow associated with flanges at Broken Spur (Allen Copley et al., 1998). In the more stable vent ecosystems of the MAR, biotic factors such as competition and predation may be more important than abiotic factors such as eruptions, which are more frequent on the EPR and NEP. Future studies with better sampling resolution, as well as data-mining results from previous expeditions, will greatly improve our knowledge of changes at the MAR sites. Our understanding of temporal changes at cold seeps is rudimentary, principally because the frequency and severity of change is apparently much lower than that at vents. The model (outlined above; Section 4.2.1) recently proposed for the Gulf of Mexico seeps is based on inferences mainly derived from spatial studies and knowledge of seep fauna longevity (Cordes et al.,

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2009). In summary, the model involves initial carbonate precipitation, followed by mussel-bed colonisation, and long-lived siboglinid tubeworm aggregations, which may last many centuries. The likely final stage of seep succession is colonisation of the remaining authigenic carbonates by hardsubstrate faunas (e.g. corals). These data, and inferences based on them, would suggest that cold seeps are among the most stable of deep-sea ecosystems. However, it is likely that future studies from a wider variety of seep settings will show that the amount and periodicity of hydrocarbon flow is spatially very variable, and that the simple model proposed above is not universally applicable. At chemosynthetic ecosystems of biogenic origin, such as whale-carcasses on the seafloor (‘whale-falls’), we have quite good data on successional processes, mainly derived from experimentally implanted whales, an approach that is impossible to replicate in the case of vents and seeps. This had led to the successional model of skeletonisation by scavengers (months), feeding by opportunistic species (years), colonisation of sulphide-eating chemosynthetic species (tens of years) to a final ‘reef’ stage where whalebones may lie on the seabed for hundreds of years (Smith and Baco, 2003). Complicating this picture is the degree of attack by the specialist bone-eating worm Osedax, which in some instances has been shown to degrade whale bones over just a few years (Braby et al., 2007), while in others it has been growing on bones for perhaps 50–80 years (A. Glover, personal observation). It appears that for very large carcasses, with well calcified bones, the whale-fall habitat may be persistent as a bone ‘reef’ for hundreds of years, and as such may be a relatively widespread habitat.

5.2. Broader context: Climate, evolution and stochastic events The time-series studies reviewed above have provided the first datasets on actual measured change in deep-sea ecosystems within the working lifetimes of scientists. Although sparse, intriguing evidence of possible links between climatic forcing and remote deep-sea ecosystems is emerging. But these are not the only data available on long-term change in the deep sea. The deep sea is one of the best-studied palaeoenvironments, and a repository of long-term sedimentary records that contain microfaunal and isotopic proxies of past climate. These deep-sea palaeoenvironmental data have made a major contribution to our understanding of past climates, and hence the predicted impacts of future climatic change. In this section, we place recent evidence for the role of climate forcing on deep-sea ecosystems in this palaeoenvironmental context. In addition, we discuss evidence for recent climate change, examine shallow-water systems for potential analogues, and examine the role of evolutionary constraints and stochastic processes.

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5.2.1. Impacts of past climate change on the deep sea One way to address the effects of environmental change in the deep sea is to analyse microfossils recovered in long sediment cores. These records reveal faunal changes occurring over much longer (geological) time scales than can be addressed in ecological studies. They include major extinction events reflecting large-scale environmental changes, as well as subtler shifts in diversity and assemblage composition. Foraminifera, particularly the calcareous species, are usually the most abundant benthic organisms to be preserved as fossils in deep-sea sediments, the other important group being the Ostracoda. These microfossils provide indicators of important environmental variables and are widely used, together with geochemical, sedimentological, and planktonic faunal proxies, in palaeoceanographic reconstructions. As a result, an extensive body of literature exists regarding fluctuations in the abundance of foraminiferal (e.g. Gooday, 2003; Jorissen et al., 2007) and ostracod (e.g. Yasuhara and Cronin, 2008; Yasuhara et al., 2009) species over time, particularly during the Quaternary. These faunal oscillations and trends can be interpreted within the context of contemporary climatic and oceanographic changes, for example, in productivity and temperature, revealed by the palaeoceanographic record. In coastal regions, where sedimentation rates are high, sediments yield a record of events occurring on time-scales as short as a few years, at least for the twentieth century (Cronin and Vann, 2003). However, in the deep sea, sedimentation rates are considerably slower and mixing of the sediment by bioturbating organisms means that the temporal resolution is usually much coarser. Thus, studies of fossil deep-sea foraminifera often document changes that took place over millions of years. For example, Thomas and Gooday (1996) showed that foraminiferal diversity declined steadily at high latitudes from about 50 to 30 million years ago (middle Eocene to early Oligocene), probably related to cooling of deep water around the Antarctic continent. Samples taken at 1.5 m intervals from an ODP core revealed that many species became extinct during a period of <25,000 years across the Palaeocene/Eocene boundary and that diversity remained low for the next 260,000 years (Thomas, 1990). It is believed that the main underlying cause of the end-Palaeocene extinctions was a global warming event, although the precise mechanism remains unclear (Thomas, 2007). Yasuhara and Cronin (2008) describe fluctuations in late Quaternary ostracod species diversity (low during glacial periods, high during interglacials) in the equatorial Atlantic, which may have been caused by climaticallyinduced temperature changes. In this case, the sampling resolution was 5000 years. Higher resolution of sediment records can be achieved by taking sampling cores at closely spaced intervals in areas with a high enough

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sedimentation rate. Hayward (2002) documented the decline and extinction of elongate, cylindrical foraminiferal morphotypes (stylostomellids and similar taxa) between the late Pliocene and middle Pleistocene at a resolution of approximately 1000 years (Hayward, 2002, Fig. 1.11 therein). The causes of synchronous stylostomellid decline and extinction events are unclear but possibly related to enhanced surface productivity or cooling and increased oxygenation of bottom water. Smart (2008) analysed subsamples extracted at 2-cm intervals along the length of a Kasten core recovered from the PAP. The subsamples spanned the last 15,000 years with a resolution of 250–300 years. Sharp fluctuations in the taxon-specific abundance, total abundance, and accumulation rates of species known to be associated with seasonal phytodetritus inputs were observed. These were interpreted to indicate variations in the intensity of phytodetritus deposition to the seafloor, and hence seasonal variability in the upper ocean. Yasuhara and Cronin (2008) report abrupt shifts in ostracod species diversity on millennial and centennial (300 years) time scales during the last 20,000 years, as well as over longer time scales during glacial–interglacial cycles. These changes in diversity coincided with climatic oscillations and were possibly related to corresponding fluctuations in surface productivity, with high productivity (i.e. high food supply) tending to depress benthic diversity. There is also evidence that bottomwater temperature fluctuations were important drivers of diversity over millennial time scales (Yasuhara and Cronin, 2008). On the Pakistan margin, changes in the quantity and quality of organic matter arriving at the sea floor, and corresponding variations in the thickness and intensity of the OMZ over a period of 120,000 years spanning glacial/ interglacial cycles, have been inferred from shifts in foraminiferal diversity (Den Dulk et al., 1998). A multiproxy study of shorter cores (spanning the last 30,000 years) from the same hypoxic margin revealed a switch from low to high foraminiferal diversity during brief, late Quaternary to early Holocene climatic oscillations (Younger Dryas, Heinrich Events 1 and 2) believed to be characterised by unusually low surface productivity and hence a weaker development of the OMZ (von Rad et al., 1999). In both studies, the temporal resolution of the samples was <1000 years for some intervals. Mediterranean sapropels also yield high resolution records of foraminiferal responses to declining oxygen concentrations ( Jorissen et al., 2007; Schmiedl et al., 2003). The studies reviewed above have a resolution that is at least an order of magnitude greater than the 10–20 year time scales of modern deep-sea faunal time series. The mixing of sediments by bioturbation usually makes it impossible to close further the gap between sediment records and modern time series. There are some settings, however, notably bathyal anoxic or hypoxic basins with high sedimentation rates, in which varved (laminated) sediments provide a much higher temporal resolution. Anoxic basins, such

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as the Guaymas and Cariaco Basins, contain laminated sediments in which each varve corresponds to a single year (Pike and Kemp, 1997; Kemp, 2003). These sediments yield highly detailed records of rapid climatic changes during the Quaternary. For example, Black et al. (2007) reported a proxy record with a resolution of 1–1.5 years for sea surface temperatures over the last 800 years, based on Mg/Ca ratios from planktonic foraminiferal shells in laminated sediments from the Cariaco Basin. High-resolution, temporal analyses of benthic microfossils in hypoxic basins are less common. The study most relevant to the present review is that of Cannariato et al. (1999). They analysed benthic foraminiferal assemblages in rapidly deposited (>120 cm ky 1) late Quaternary sediments in the Santa Barbara Basin, which at present is severely hypoxic (DO < 0.1 ml L 1). These authors were able to resolve events occurring on time scales as short as a few decades. Assemblages characteristic of hypoxic conditions corresponded to interstadial intervals, when ventilation on the California margin was weak, while those characteristic of oxic conditions corresponded to glacial intervals, when ventilation was strong. The switches from oxic to hypoxic assemblages occurred over a period of between 40 and 400 years. None of these changes involved extinctions. Rather, it seems that species were able to migrate rapidly from refugia to occupy habitats opportunistically as conditions changed. Laminated sediments in other California borderland basins, and elsewhere, have also yielded benthic foraminifera (e.g. Hagadorn, 1996), although these have not been analysed in the same detail as the Santa Barbara records. These palaeoceanographic studies are important because they reveal the kinds of natural, and sometimes dramatic, faunal changes that have occurred in response to past climatic shifts leading to changes in bottom-water characteristics (notably temperature and oxygenation) and the magnitude and nature of organic matter fluxes to the seafloor. Studies such as that of Cannariato et al. (1999), conducted on a bathyal continental margin influenced by an OMZ, suggest that climate changes occurring over a period of decades can impact the ocean floor and lead to faunal changes on time scales similar to those of modern ecological time series. Responses were probably slower in the case of well-ventilated central oceanic abyssal ecosystems, although the evidence is lacking. Whether temporal patterns observed in the palaeoceanographic records can be extrapolated to benthic communities as a whole is an open question. Small organisms with short generation times probably responded in a similar way to foraminifera and ostracods. The responses of the larger macrofaunal and megafaunal animals may have been different, although they would undoubtedly have been affected by major oceanographic changes.

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5.2.2. Impacts of recent climate change on the deep-sea benthos Current concerns about global climate change have heightened awareness of possible climatic impacts on deep-sea ecosystems. As discussed above, it is abundantly clear from the deep-sea fossil record that major shifts, often involving extinctions, have occurred in the composition and structure of deep-sea communities, and that these were linked ultimately to climatic changes. If they persist, current trends in global warming, caused by the increasing concentration of greenhouse gases in the atmosphere, are likely to have similar major consequences for upper-ocean and deep-seafloor communities. Predicted changes include a decrease in surface productivity and decreased dominance by diatoms phytoplankton assemblages, which form fast-sinking aggregates, relative to smaller plankton (Bopp et al., 2005; Smith et al., 2008b). The net result is anticipated to be a decrease in the export flux and hence the amount of food reaching the ocean floor, particularly at abyssal depths. Although the only firm evidence that global climate change has impacted deep-sea ecosystems comes from the fossil record, there are strong indications that, interannual-scale climatic oscillations, notably the ENSO, influence the deep-sea benthos. Estimates of net global primary production obtained from satellite measurements of ocean colour have demonstrated a link between climate variability, represented by the Multivariate ENSO Index (MEI, incorporating data on sea-level pressure, surface winds, sea-surface temperature and cloudiness) and ocean productivity represented by upper-ocean chlorophyll concentrations (Behrenfeld et al., 2006; K. L. Smith et al., 2006). Changes in ocean productivity, in turn, have been linked changes in the amount and quality of organic material reaching the deep-ocean floor (K. L. Smith et al., 2006). Links between climate, food supply, and the composition and functioning of abyssal ecosystems have been explored at Station M (NE Pacific) and the PAP (NE Atlantic). At interannual scales, the food supply (POC flux) to the benthic community at Station M showed a lagged response at different time intervals with the MEI and two other ENSO-related climatic indices, the Northern Oscillation Index (NOI) and the Backum upwelling index (BUI) (Ruhl and Smith, 2004; K. L. Smith et al., 2006, 2008). During negative deviations in the NOI index (El Nin˜o), wind-driven upwelling tends to decrease, resulting in less primary production and less export flux to the deep sea. Conversely, during positive phases of the NOI index (La Nin˜a), increases in southerly winds along the coast and upwelling ultimately lead to increased POC flux to the abyssal seafloor. The atmospheric air pressure anomalies reflected in the NOI can influence surface conditions within weeks to a few months and changes in primary production export flux lead to changes in POC flux to the seafloor within 1–3 months (K. L. Smith et al., 2006). Changes in the NOI have been related to abyssal POC flux variation with a time lag of about 6 months (Ruhl and

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Smith, 2004; K. L. Smith et al., 2006). Major changes in the densities of some megafaunal species, notably the holothurians Elpidia minutissima and Peniagone vitrea and the echinoid Echinocrepis rostrata, were linked to the NOI with a lag of 14–18 months. Smaller organisms, the macrofauna and meiofauna, showed similar responses, albeit with shorter lag times than the megafauna, to climatic oscillations. At the PAP, variations in the export of POC from the euphotic zone (i.e. the export flux) and hence to the seafloor, as well as in the quality (e.g. content of pigments necessary for reproduction) of the material that reaches the seafloor, appear to be linked to the NAO, a climatic phenomenon that is related to ENSO and affects winds, precipitation, and storm intensity and frequency (Smith et al., 2009; Lampitt et al., 2010). These changes in food quantity and quality are believed to underlie the ‘boom-bust’ cycles observed in Amperima rosea and Ellipinion molle (Wigham et al., 2003). Vastly increased populations of these small surface-feeding holothurians may, in turn, have affected foraminiferal and meiofaunal populations through depletion of food resources and sediment disturbance. POC flux to the seafloor, macrofaunal abundance and community structure may all be useful indicators of abyssal ecosystems responses to fluctuations in the climate as well as to more permanent climatic change (C. R. Smith et al., 2008b). The conclusions of much of the research at Station M, however, come from correlations that often have important unexplained variation. More research is needed to understand this variation and the mechanisms underlying it so that robust biogeochemical models can be created and used more broadly. Clearly, the results from Station M and the PAP indicate that models assuming constant rates of almost any ecological parameter at abyssal depths are flawed. If climate change continues as projected through 2300, then changes in abyssal ecosystem function could also be occurring on timescales that approach the approximate age for water masses below 1500 m depth (Matsumoto, 2007). Even subtle changes that persist for decades to centuries could have an impact on biogeochemical dynamics in the longer term. Long-term time series studies such as those at the PAP and Station M provide essential ecological baseline information necessary to predict ecosystem responses to climate change and human impacts in the deep sea (Glover and Smith, 2003; C. R. Smith et al., 2008a; K. L. Smith et al., 2008). As discussed above, temporal change includes cyclical change over seasonal to decadal time scales (environmental variability) as well as a persistent change in the mean attributes of a system over time (Fig. 1.17). Climatic oscillations such as ENSO are a form of environmental variability, while global climate change inferred from the fossil record constitutes a larger time and space scale environmental change. The shifts in deep-sea benthic ecosystems at the PAP and Station M sites seem to represent an example of interannual to decadal-scale variability. Distinguishing these

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fluctuations from persistent faunal change caused by contemporary global warming represents a formidable challenge requiring a shift in research frameworks. 5.2.3. Climate change at high latitudes At high latitudes, the melting of sea ice will probably be the main mechanisms linking long-term climate change to benthic ecosystems. In the Arctic Ocean, climate models forecast rapid change, and empirical studies corroborate these projections. Since the beginning of satellite remote sensing in 1979, the Arctic summer minimum sea-ice area has decreased by 10% per decade. There is a general consensus that the reduction in the amount of Arctic sea-ice is a manifestation of global warming. Further alterations in sea-ice cover, water temperature, and primary production are expected. Although the consequences for benthic ecosystems are still unclear, it is likely that this environmental change will lead to a massive response in the Arctic (Anderson and Kaltin, 2001; Hassol, 2004). In the Antarctic, the climate-related disintegration of ice shelves, which has already happened in the case of the Larsen B ice shelf (Scambos et al., 2003; Domack et al., 2005), will undoubtedly have important consequences for the underlying benthic communities (Domack et al., 2007; Smith et al., 2007). This could come from increased scouring of tabular icebergs that can reach down hundreds of metres or through biogeochemical changes in surface production imparted by their presence. 5.2.4. Lessons from shallow-water analogues It is clear from our review that, despite an enormous research effort, our knowledge of temporal trends on the ocean floor remains poor. The great depth and often distant location of deep-sea sites precludes time-series sampling for all but the most well-funded programmes. Even for these, the majority of funding cycles are too short to support decadal-scale studies. One solution is to use shallow-water sites that are more accessible as analogues of deep-sea environments. Most time-series studies in shallow water are from systems that are very different from the deep sea and influenced by climatic and other environmental drivers that exert little or no influence in deep-water environments. However, in recent years, a few shallow-water sites with deep-sea characteristics have been identified. Among the most promising analogues are marine caves, some of which resemble the deep sea in the permanent absence of light, the lack of high energy currents and waves, and their oligotrophic character. In one Mediterranean cave, the allochthonous organic-matter inputs are equivalent to those at a depth of 1000 m (Fichez, 1990a). Chlorophyll a values further demonstrate the marked oligotrophic character of the inner parts of dark caves (Fichez, 1990b). On the other hand, marine caves have a very limited

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spatial extent and the water is usually much warmer than in the deep sea. However, well-studied caves located in the northwestern Mediterranean have winter water temperatures (13 C) similar to that of the deep Mediterranean. Of particular interest is the 3PP cave near Marseille (Vacelet, 1996; Vacelet et al., 1994), the descending profile of which traps cold (ca. 13–15 C) water year round. More caves of this type have now been discovered (Bakran-Petricioli et al., 2007), all of them characterised by faunal (Fig. 1.18) and ecological parallels to the deep sea. In particular, a significant number of faunistic components are either phylogenetically related to deepsea fauna (e.g. Iliffe et al., 1984; Calado et al., 2004), or are truly bathyal or abyssal species sheltered in these ‘deep-sea islands’ of the littoral zone. The most striking examples are the carnivorous sponge Asbestopluma hypogea (Fig. 1.17A) and the hexactinellid sponge Oopsacas minuta, both also found in the bathyal Mediterranean (Vacelet et al., 1994; Vacelet, 1996; Bakran-Petricioli et al., 2007). Other examples include less conspicuous taxa such as bryozoans and brachiopods. It seems therefore that the 3PP and similar caves shelter an interesting combination of successfully established true deep-sea species as well as mobile shallow-water taxa using caves as a shelter from predators (Harmelin et al., 1985).

A

B

C

Figure 1.18 Shallow water caves of the Mediterranean as analogs to the deep sea. (A) The carnivorous sponge Asbestopluma hypogea belongs to the exclusively bathyal and abyssal sponge family Cladorhizidae; however, dense populations thrive at 15–25 m depth in some particular caves of the Mediterranean. (B) Marine cave Mysidacea of the genus Hemimysis are a unique example of a species shift potentially linked to climate warming. (C) Recent efforts conducted at caves have focused on SCUBA sampling the foraminiferan and metazoan meiobenthos living in cave sediments that are remarkably similar to deep-sea sediments. Images courtesy of Jean-Georges Hermelin, CNRS (A) and Roland Graille, CNRS (B,C).

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Marine caves are tempting sites in which to conduct in situ experiments or temporal surveys relevant to deep-sea biology. However, faunistic studies have concentrated mostly on the hard substrate sessile invertebrates covering the walls and ceiling, and mobile fauna such as crustaceans and teleost fish, making quantitative or even qualitative comparisons with deep-sea data difficult. Recent research (Fig. 1.18) has investigated the sediment-dwelling foraminiferan and metazoan meiobenthos, mainly harpacticoid copepods, nematodes, and annelids. This effort, primarily concentrated on the 3PP cave, is directed at providing baseline data on cave-sediment taxa prior to initiating a temporal survey and later comparisons with deep-sea time series. Preliminary results show a strong gradient in meiofaunal composition between the cave’s entrance and the darkest parts, with a prevalence of deep-sea components (at least families and genera) in the latter (Chevaldonne´ et al., 2008). Little is currently known about temporal trends in marine caves. There is no evidence for seasonal variations in the supply of food (e.g. Fichez, 1990b), which is probably introduced by the slow advection of material from outside and the movements of some mobile residents, such as fish and mysids (Fig. 1.18B; Coma et al., 1997). However, it appears that some marine caves are being affected by climatic warming. Following unusually hot summers, one cave mysid species has recently been replaced by a congener in the majority of NW Mediterranean caves (Fig. 1.18B). Caves such as 3PP may act as a shelter, possibly temporary, from such episodes of warming (Chevaldonne´ and Lejeusne, 2003; Lejeusne et al., 2010). Signs of mortality during mild winters suggests that some deep-sea taxa, particularly sponges, are probably living near their thermal limit in “cold-water” marine caves (T. Perez, P. Chevaldonne´, personal observation). Temperature has been monitored in several NW Mediterranean caves since 2001 (since 1995 at 3PP, with gaps). Time-series sampling of the sediment meiobenthos, as well as measurements of additional physical and chemical parameters, would be a logical next step, particularly if caves are to serve as mesocosms of deepsea sedimented habitats. However, although some marine cave taxa function as metapopulations (Lejeusne and Chevaldonne´, 2006), true deep-sea taxa living in caves may actually follow a source-sink population model. In this case, the temporal patterns observed in caves might be misleading. These questions remain to be tested. Other shallow-water analogues of deep-water ecosystems are located at high latitudes, where relatively stable low temperatures and a more or less isothermal water column facilitates the interchange of shallow- and deepwater species (Tyler and Young, 1999; Brandt et al., 2007) and makes deepsea animals available for study (e.g. Hessler and Stro¨mberg, 1989). The occurrence of hexactinellid sponges, an essentially deep-sea group, within SCUBA-diving depths as shallow as 18 m in fjords around Vancouver on the Canadian Pacific coast is well-established (Leys et al., 2004).

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In somewhat deep water (150–250 m) in the same area, hexactinellids form massive reefs (Conway et al., 2001). The western side of McMurdo Sound (Antarctica) is another interesting area. This part of the Ross Sea has a semi-permanent ice cover, a very stable physical regime including uniformly low temperatures, and is influenced by nutrient-depleted water originating to some extent from under the Ross Ice Shelf. Water column and benthic primary production, rates of heterotrophic microbial activity, and densities of benthic macro- and megafauna, are all relatively low compared to the much more productive eastern side of McMurdo Sound (reviewed by Gooday et al., 1996). Dayton and Oliver (1977) noted similarities in macrofaunal densities at western Sound sites and the deep Ross Sea shelf (500 m) and the bathyal NW Atlantic, as well as ‘striking visual parallels’ between seafloor features and faunas in the western Sound and the bathyal deep sea. Benthic foraminifera have been intensively studied since the 1980s in Explorers Cove, a coastal embayment of the western Sound (e.g. DeLaca et al., 1980; Bernhard, 1987; Gooday et al., 1996). This is a relatively tranquil area where the food supply, derived mainly from under-ice, water-column, and benthic production, is highly seasonal, as in parts of the deep sea subject to pulsed inputs of phytodetritus. The foraminiferal assemblages include large agglutinated species, some of them resembling species from sublittoral to bathyal, fjordic, deep shelf and upper slope settings in the Northern Hemisphere (Gooday et al., 1996). Because it is accessible to SCUBA divers, Explorers Cove is a good area in which to study the ecology of benthic communities similar to those living in deeper water. However, important environmental differences exist, notably under-ice and benthic primary production, as well as organic inputs from meltpools that lead to localised, nearshore oxygen depletion. Moreover, longer-term temporal patterns in Explorers Cove are probably strongly influenced by periodic breakouts of the ice cover. These occur every 5–7 years and result in peaks of primary production superimposed on the normal seasonal cycle (Gooday et al., 1996). Like caves, high latitude sites have their own peculiarities and do not provide perfect analogues of deep-sea environments. Results obtained from them therefore must be treated cautiously. 5.2.5. Evolutionary constraints on faunal responses Long-term time-series studies can reveal how species assemblages and ecosystems change over time in relation to environmental perturbations. We know very little, however, about the physiological mechanisms underlying these changes, or about how they are influenced by the evolutionary history of species. Taxonomic and phylogenetic studies have provided insights into the evolutionary origin of species at vents, seeps, and whale-falls. With some

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exceptions, these species share relatively recent ancestors with species from shallow-water settings. Among polychaetes, the dominant family at Pacific vents (Siboglinidae) are also found on seeps, whale-falls (as Osedax) and in shallow-water organic-rich muds (e.g. Siboglinum in the North Sea). The family falls within a globally-distributed clade of polychaetes that includes the Oweniidae and Sabellidae, ubiquitous tube-dwelling worms in all marine environments. Among molluscs, the Bathymodiolinae clade, which includes all the vent, seep, and whale-fall molluscs, is closely related to shallow-water mytilids, including the edible mussel Mytilus edulis (Distel et al., 2000). Among crustaceans, the hydrothermal vent shrimp Mirocaris fortunata is closely related to the shallow-water species Palaemonetes varians (Distel et al., 2000). The overlapping of depth tolerance ranges of the first stage larvae of the two species (Mestre and Thatje, unpublished data; Tyler and Dixon, 2000) suggests that they originated from a common ancestor that was physiologically tolerant to a wide range of pressures (Mestre et al., 2009). Thus, whilst all of these species and clades have evolved unique adaptations to the sulphide-rich settings of vents, seeps, and whale bones, their common evolutionary heritage with shallow-water species is likely to be important in determining their physiological responses to external drivers. Ideas about species’ radiations are still based mainly on biogeographic patterns, in recent years supported by molecular analyses. It is becoming increasingly evident, however, that the radiation and speciation of deep-sea benthic taxa reflects the submergence of species from continental shelf depths into slope and deeper waters, as well as the emergence of taxa into shallower waters (Thatje et al., 2005; Raupach et al., 2009). Tolerance differences among life-history stages in shallow-water species suggest that the restriction of adult bathymetric distributions reflects ecological rather than physiological limitation. When environmental conditions (e.g. temperature) change, ecological limitations may relax, allowing greater bathymetric penetration (Tyler and Young, 1998). Studies of deep-sea invertebrates such as Mirocaris fortunata have demonstrated comparable patterns; adults have defined hyperbaric distributions but the larvae exhibit greater tolerance to lower pressures equivalent to the surface waters where they feed (Pond et al., 1997; Tyler and Dixon, 2000). The ability of deepsea species with shallow-water evolutionary origins to respond to rapid climate change therefore may be influenced by the preservation of physiological tolerances beyond those required by the ecological niche that they currently occupy in the deep ocean (Mestre et al., 2009). These physiological and evolutionary considerations highlight the importance of pressure and temperature tolerance studies, and physiological studies in general, for understanding the capacity of some deep-sea species to respond to possible future environmental changes (Mestre et al., 2009).

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5.2.6. Stochastic events and successional processes Like their counterparts in shallow water, deep-sea communities are controlled by the basic mechanisms of energy availability, biological interactions, heterogeneity, and stochastic disturbances, the latter ranging in scale from the very small (e.g. Jumars and Eckman, 1983; Grassle and MorsePorteous, 1987; Grassle and Maciolek, 1992) to the very large (e.g. Levin et al., 2001). Larger stochastic events include food falls (e.g. whales), episodic benthic storms and strong near-bottom currents, down-slope cascading of shelf water, mass sediment movements (turbidity currents, submarine slumps and slides) and volcanic eruptions or ashfalls. Violent disturbances, such as mass movements (Masson et al., 1996) and volcanic eruptions, can eliminate most benthic life over large tracts of the seafloor. The reestablishment of a new community involves the processes of colonisation and succession. Smaller-scale disturbances can lead to changes in the structure and composition of benthic faunas and influence their dynamics. In some cases, this may take the form of a ‘regime’ or ‘state shift’ (Pascual and Guichard, 2005), a phenomenon often proceeded by a loss of resilience (Scheffer et al., 2001). Although the sedimented deep ocean is generally quiescent, some areas are subject to periods of high current activity that strongly affect benthic communities (reviewed in Levin et al., 2001). Where the currents are strong enough, for example, in the HEBBLE area on the Nova Scotia continental rise, periodic erosion of the seafloor removes much of the benthic fauna, repeatedly creating fresh habitats that are available for recolonisation by opportunistic species. This process is believed to maintain communities in a constant early successional state. Similarly, dense shelf-water cascading (DSWC) can transport large volumes of water and sediment. This climatically-induced phenomenon reshapes submarine canyon floors and impacts deep-sea environments (Canals et al., 2009) and communities (Boetius et al., 1996; Tselepides and Lampadariou, 2004; Tselepides et al., 2007). DSWC has been linked to population collapses of the commercially important deep-sea shrimp Aristeus antennatus, as well as to enhancement of its longer-term recruitment (Company et al., 2008). Strong current flow often characterises the upper reaches of active submarine canyons (Tyler, 2009). In the Nazare´ Canyon on the Portuguese margin, upper-canyon currents erode sediments and deposit them to the middle part of the canyon (De Stigter et al., 2007). Intermittent gravity flows, occurring about once per year, and much rarer major turbidity currents, are the main agents transporting sediment through the lower section of the canyon and onto the adjacent abyssal plain. Gravity and turbidity flows and strong currents must impact on the benthos and lead to a succession of recolonising species. There is evidence for recolonisation and successional processes occurring at bathyal depths in the upper Nazare´

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Canyon (Koho et al., 2007) and the Cap Breton canyon (Anschultz et al., 2002). In the latter case a succession of foraminferal species was observed over a 16 month period following the deposition of a turbidite. A much older turbidite, emplaced ~1000 years ago on the Madeira Abyssal Plain (MAP, NE Atlantic), seems to have had a lasting impact on polychaete and nematode assemblages (Glover et al., 2001; Lambshead et al., 2001), possibly because of its granulometric characteristics. Turbidity currents grade into other types of catastrophic gravity-driven mass movements of sediments, such as slumps, slides, and gravity flows, which occur periodically on continental margins (reviewed in Levin et al., 2001). Some of these events, for example, the series of Holocene (~7000 years BP) slides in the Storegga area on the Norwegian margin, were enormous and must have wiped out the benthic biota over large areas of seafloor. Presumably, the devastated areas were recolonised over time by species from adjacent areas of seafloor. This process has never been documented, although large-scale in situ experimental studies, reviewed by Thiel (2003), provide some indication of how it might proceed. The DISCOL (DISturbance and reCOLonisation of a manganese nodule area in the South Pacific) experiment, in which 11 km2 of seafloor were disturbed, suggested that recovery from disturbance may take years, particularly for the megafauna. In the case of the composite Storegga slide, which covers an area of 90,000 km2 (Canals et al., 2004), recolonisation must have taken much longer. Volcanic ash falls are another kind of sudden event with the potential to wipe out or seriously disturb benthic communities over wide areas. The recovery of foraminiferal communities following the deposition by the 1991 Mt Pinatubo eruption of an ash layer over large areas of the South China Sea is well documented (Hess and Kuhnt, 1996; Hess et al., 2001). Samples collected between 1994 and 1998 revealed a succession of species and increasingly diverse assemblages following this disturbance event. At hydrothermal vents, the relative roles of environmental drivers, biological interactions and random processes remain poorly understood (Desbruye`res, 1995, 2001; Juniper and Tunnicliffe, 1997; Mullineaux et al., 2003; Sarrazin and Juniper, 1999; Sarrazin et al., 1997; Shank et al., 1998). Nevertheless, the ephemeral and unpredictable nature of the habitat is clearly responsible for sequences of extinction and rapid colonisation (Tunnicliffe, 1991; Thie´baut et al., 2002). The mixing of sea water and hydrothermal fluids exposes the vent fauna to strongly fluctuating physicochemical conditions ( Johnson et al., 1986; Luther et al., 2001), while small-scale variations in hydrothermal fluid discharges influence faunal distributions by altering the supply of primary food sources to microbial communities. Over longer timescales, changes in fluid flow resulting from the rearrangement of subsurface plumbing by tectonicism or clogging, as well as submarine volcanic eruptions, can lead to the creation of new

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venting areas or to the cessation of venting activity (Hessler et al., 1985; Tunnicliffe, 1991; Haymon et al., 1993; Grehan and Juniper, 1996; Tunnicliffe et al., 1997; Sarrazin et al., 1997; Shank et al., 1998; Desbruye`res, 1998; Tsurumi and Tunnicliffe, 2001; Embley et al., 2006). These processes lead to major changes in community composition and distribution over months and years. However, the frequency of episodic tectonic and volcanic disturbances varies according to spreading rates (Fornari and Embley, 1995). Catastrophic perturbations occur on time scales of years to decades on fast-spreading mid-ocean ridges, but are far less common on the more stable slow-spreading ridges (Lalou, 1991; Desbruye`res et al., 2001). Tectonic events and heat convection through the oceanic crust may also induce a fast faunal turnover on fast-spreading ridges (Thie´baut et al., 2002). In contrast, community structure and faunal distribution at the TAG site on the Mid-Atlantic Ridge exhibits a decadalscale constancy that may be enhanced by the resilience of a single large mound (Eiffel Tower) to total clogging of vent fluid conduits by mineralisation. This hypothesis could be tested by comparing the decadal-scale ecological dynamics of TAG with those of other deep Mid-Atlantic vent fields, where venting is associated with smaller constructs, such as at Broken Spur, Snake Pit or Logachev. Unfortunately, no relevant data are yet available from these sites.

5.3. Temporal change in shallow-water versus deep-water settings Historically, there has been much greater interest in temporal change at shallow-water habitats compared to those in the deep sea. This has been partly because of the huge economic and societal importance of the continental shelf compared to the inaccessible deep ocean. A large literature exists on the impact of global industrialised fisheries both on fish stocks (e.g. Pauly et al., 1998) and on the entire shelf ecosystem (e.g. Worm et al., 2006). There is no doubt that enormous changes have taken place in shelf ecosystems over the temporal scales considered in this review. However, the majority of these changes have been driven by fisheries and other human activities in the littoral or riverine zone (Table 1.4). Ironically, it is the fisheries themselves that generate most of the data on long-term change in shallow-water, as well as driving the changes that the data reveal. If we are to consider changes brought about by possibly ‘natural’ cycles (e.g. climate cycles), or the regional influences of global rises in carbon dioxide and associated temperature, the results may be much more subtle, and possibly hidden by fisheries or land use impacts (Table 1.4). At abyssal settings, still not directly impacted by commercial fishing, oil and gas exploration or mining (Glover and Smith, 2003), the impacts of these more subtle drivers of temporal change may be much clearer.

Table 1.4

Dominant drivers of inter-annual to decadal-scale temporal change in marine benthic habitats Intertidal

Sub-tidal

Bathyal

Fisheries Hard substrate Human land use Human land/ habitats Fisheries resource use Climate forcing Climate forcing

Stochastic downslope processes Climate forcing

Fisheries Human land use Human land/ Fisheries resource use Climate forcing Climate forcing

Stochastic downslope processes Fisheries Climate forcing

Sedimented habitats

Cold seep habitats

Unknown

Unknown

Hydrothermal vent habitats

Unknown

Large organicfall habitats

Biological succession (scavenging)

Unknown (possible drivers include periodic changes in fluid flow) Biological succession (scavenging)

Abyssal

Hadal

Unknown

Unknown (Drivers may include stochastic downslope processes, (e.g. sediment mass movements) Unknown (Drivers may include stochastic downslope processes, (e.g. sediment mass movements) Unknown

Climate forcing Stochastic downslope processes

Unknown Stochastic events (e.g. Grand Banks turbidite) Methane hydrate release? Fluid flow and Fluid flow and chemistry chemistry Biological succession Biological Volcanic eruptions succession Volcanic eruptions Biological Biological succession succession (scavenging) (scavenging)

Unknown

Unknown

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It is an intriguing thought that the regions of the worlds oceans that are most insulated from change may be the best settings in which to detect it. Just as deep-sea sediment cores have revealed past shifts in the Earth’s climate, modern time-series studies in the deep sea are revealing current changes (K. L. Smith et al., 2009). Summarising the drivers of temporal change reveals four important points (Table 1.4). Firstly, the impacts of the main human drivers (not including climate) are reduced with increasing depth and increasing habitat speciality (i.e. more rare and ephemeral habitats such as vents and seeps). Secondly, the impacts of natural climate cycles and climate change may be a more significant driver of change in the abyss compared to shallow water. Thirdly, it is abundantly clear from this review that deep-sea ecosystems are highly variable over inter-annual, decadal, and centennial scales, both in sedimented regions and those dependent on locally-sourced chemosynthesis. Finally, if climate change does indeed significantly alter the amount or distribution of the POC fluxes that feed most deep-sea areas, then related changes in deep-sea systems would likely occur with a delay that is comparable with most other habitats globally.

6. Conclusions 6.1. Hypotheses Four hypotheses were put forward at the start of this review. These can now be revisited and assessed, based on the literature reviewed above. Deep-sea sedimented ecosystems are subject to biologically driven forcing events induced by climate change or climate variability in recent decades: We find some support for this hypothesis in the case of the two abyssal plain sites for which we have data for a period longer than 10 years. It is clear that deep-sea benthic sedimented environments are being impacted by changes in upper-ocean processes linked to interannual to decadalscale oscillations. However, it is not yet clear to what extent humaninduced climatic changes are impacting on the deep sea. This is largely because we have not been collecting data for long enough to distinguish a long-term, warming-induced trend from natural stochastic and cyclic changes. Chemosynthetic ecosystems are subject to stochastic geological forcing events which override climatically induced biological processes: It is a widely held view that chemosynthetic ecosystems such as hydrothermal vents are unstable, ephemeral habitats that are subject to frequent stochastic disruptions, such as volcanic eruptions. However, the data available suggest that,

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although this may sometimes be the case at fast-spreading centres such as the East Pacific Rise, vent ecosystems at slow-spreading centres such as the Mid-Atlantic Ridge may be quite stable over decadal to century scales. Data are lacking at cold-seeps, but inferences based on the longevity of cold-seep organisms suggest that these environments may be stable for many hundreds of years, except where they are disturbed by sediment flows. For other chemosynthetic ecosystems such as whale-falls, the stability of the habitat may be highly variable depending on the ecological setting and the size of the carcass and bones. We find no evidence for climate-induced temporal change at chemosynthetic ecosystems. Although the drivers are different, there are commonalities in the biological responses observed in these contrasting settings: New data have emerged which suggest a relatively recent ancestry of organisms from vents, seeps, and deep-sea sediments. Species that now inhabit high-sulphide vent sites may have evolved from deep-sea or even shallow-water sediment-dwelling species, and exhibit some similar physiological constraints. Organisms at vents are likely to respond to a waning sulphide supply in the same way as detritivores in sediments respond to reduced organic carbon flux. However, chemosynthetic ecosystems that are driven by geology may be independent of changes in surface waters associated with climatic change, and therefore insulated from these impacts to some degree. The deep-sea benthos embodies the influences of climatic changes that have occurred over both geological (evolutionary) and decadal (ecological) timescales: Traditionally, climate change studies in the deep sea were concerned only with the long-term sediment record revealed in cores. However, the ‘ecologicalscale’ studies at PAP, Station M and other sites are now beginning to suggest that we can identify climate-induced changes in the communities of animals living at the seafloor some 4–5 km below the surface. Given that the palaeoceanographic record yields abundant evidence for climatechange impacts on deep-sea biota, we believe it is essential to determine whether current climatic change is leading to ecological-scale faunal change at deep-sea sites. In addition, as the deep-sea benthos is to some extent ‘buffered’ from seasonal, inter-annual and human (e.g. fisheries) effects in the overlying water column, climate-induced changes may be easier to detect on the ocean floor than in shallow-water marine environments.

6.2. Future directions Our knowledge of temporal changes in the deep sea is extremely poor, to a large extent reflecting our inability to directly observe deep-sea habitats through remote sensing. Surface waters and the terrestrial environment can

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be observed from satellites capable of enormous and rapid spatial coverage. In contrast, even a short series of oceanographic cruises to a single site such as that on the Porcupine Abyssal Plain is a major effort and provides only limited spatial coverage. The observation of the Earth from space, and the ability to measure change over global scales, has been a key factor in our gradual realisation of the significance of human impacts on the Earth’s terrestrial and surface-water ecosystems. An even greater level of observational detail is needed for the deep sea, which covers the other two-thirds of the planet’s surface. Technologies are now arriving that will allow us to make the necessary broader-scale observations. The development of autonomous underwater vehicles (AUV’s), freed from the need to be tethered to the surface, will allow us to image for the first time vast tracts of the seafloor at a resolution sufficient to relate spatial and temporal change across a range of scales. Access to ROVs has also improved, allowing for more creative and experimental approaches to deep-sea research. At the same time, ocean observatories are developing world-wide in major programmes, for example, the US NSF-Ocean Observatories Initiative, the Canadian NEPTUNE programme, and various European (EuroSITES, the European Seas Observatory NETwork (ESONET), and the European Multidisciplinary Seafloor Observatory programmes) and Japanese (DONET) initiatives. Data from these observatories can either be cabled to the shore, using existing fibre-optic networks from industry or by laying new cables, or sent via satellite-based telemetry from buoys. In this way, researchers can monitor oceanographic and biological variables in real-time. These systems, especially when used together in a Global Earth Observation System of Systems (GEOSS), will provide an unprecedented opportunity to examine science questions across disciplines as well as spatial and temporal scales more effectively than ever before. By producing, for example, transformative maps of the deep sea, such developments will improve significantly our ability to gather scientific data and herald a new era of public understanding of the deep ocean.

ACKNOWLEDGEMENTS We acknowledge the support of the European Commission in funding the Marine Biodiversity and Ecosystem Functioning (MARBEF) project and the Deep-Sea and Extreme Environments, Patterns of Species and Ecosystem Time-Series (DEEPSETS) responsive mode project within MARBEF. We thank Drs Tammy Horton and Ian Hudson for their initial work in setting up the DEEPSETS project in 2003. This review chapter originated at a DEEPSETS workshop held in Lisbon in October 2007, and was supported by a further DEEPSETS workshop in Ghent, Belgium in February 2009. We are very grateful in particular to the organisers of these workshops, Ana Colac¸o and Ann Vanreusel. A. Glover acknowledges the Natural History Museum Strategic Innovation Fund and the Climate

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Change Group for useful discussions and the time required to work on this manuscript. ST was supported by a grant from the Total Foundation. Preparation of the manuscript was also supported by the European Seas Observatory NETwork (ESONET) Network of Excellence and the Oceans 2025 project of the Natural Environment Research Council, UK. We are grateful to the following persons for help with this publication: N. Boury-Esnault, T. Dahlgren, C. R. Smith, R. Graille, J. G. Harmelin, P. Martinez Arbizu, J. Pawlowski, T. Shank, J. Vacelet, H. Zibrowius.

REFERENCES Allen Copley, C., Copley, J., and Tyler, P. (1998). Return to broken spur. BRIDGE Newsletter 14, 30 University of Leeds, ISSN 1364-8721. Anderson, L. G., and Kaltin, S. (2001). Carbon fluxes in the Arctic Ocean—Potential impact by climate change. Polar Res. 20, 225–232. Anschutz, P., Jorissen, F. J., Chaillou, G., Abu-Zied, R., and Fontanier, C. (2002). Recent turbidite deposition in the eastern Atlantic: early diagenesis and biotic recovery. J. Mar. Res. 60, 835–854. Arntz, W. E., Tarazona, J., Gallardo, V., Flores, L. A., and Salzwedel, H. (1991). Benthos communities in oxygen deficient shelf and upper slope areas of the Peruvian and Chilean Pacific coast and changes caused by El Nin˜o. In “Modern and Ancient Continental Shelf Anoxia” (R. V. Tyson and T. H. Pearson, eds.), pp. 131–154. Geological Society, Tulsa Oklahoma. Arntz, W. E., Gallardo, V. A., Gutie´rrez, D., Isla, E., Levin, L. A., Mendo, J., Neira, C., Rowe, G., Tarazona, J., and Wolff, M. (2006). ENSO and similar perturbation effects on the benthos of the Humboldt, California and Benguela Current upwelling ecosystems. Adv. Geosci. 6, 243–265. Bailey, D. M., Ruhl, H. A., and Smith, K. L. Jr. (2006). Long-term changes in benthopelagic fish abundance in the abyssal Northeast Pacific Ocean. Ecology 87, 549–555. Bailey, D. M., King, N. J., and Priede, I. G. (2007). Cameras and carcasses: Historical and current methods for using artificial food falls to study of deep-water animals. Mar. Ecol. Prog. Ser. 350, 179–191. Bailey, D. M., Collins, M. A., Gordon, J. D. M., Zuur, A. F., and Priede, I. G. (2009). Longterm changes in deep-water fish populations in the northeast Atlantic: A deeper reaching effect of fisheries? Proc. R. Soc. Lond., B, Biol. Sci. 10.1098/rspb.2009.0098. Bak, P., and Tang, C. (1989). Earthquakes as a self-organized critical phenomenon. J. Geophys. Res. Solid Earth Planets 94, 15635–15637. Baker, E. T., and Hammond, S. R. (1992). Hydrothermal venting and the apparent magmatic budget of the Juan de Fuca Ridge. J. Geophys. Res. 97, 3443–3456. Baker, E. T., Lavelle, J. W., Freely, R. A., Massoth, G. J., and Walker, S. L. (1989). Episodic venting on the Juan de Fuca Ridge. J. Geophys. Res. 94, 9237–9250. Bakran-Petricioli, T., Vacelet, J., Zibrowius, H., Petricioli, D., Chevaldonne´, P., and Rada, T. (2007). New data on the distribution of the “deep-sea” sponges Asbestopluma hypogea and Oopsacas minuta in the Mediterranean Sea. Mar. Ecol.—An Evol. Perspect. 28 (suppl. 1), 10–23. Basson, M., Gordon, J. D. M., Large, P., Lorance, P., Pope, J., and Rackham, B. (2002). The effects of fishing on deep-water fish species to the west of Britain. JNCC Report no 324, pp. 1-150. Bauerfeind, E., No¨thig, E.-M., Beszczynska, A., Fahl, K., Kaleschke, L., Kreker, K., Klages, M., Soltwedel, T., Lorenzen, C., and Wegner, J. (2009). Variations in vertical particle flux in the Eastern Fram Strait (79 N/4 E) during 2000–2005. Results from the

80

A. G. Glover et al.

Deep-Sea Long-Term observatory HAUSGARTEN. Deep Sea Res. Part I 56, 1471–1487. Beaulieu, S. E. (2002). Accumulation and fate of phytodetritus on the sea floor. Oceanogr. Mar. Biol. Ann. Rev. 40, 171–232. Behrenfeld, M. J., O’Malley, R. T., Siegel, D. A., McClain, C. R., Sarmiento, J. L., Feldman, G. C., Milligan, A. J., Falkowski, P. G., Letelier, R. M., and Boss, E. S. (2006). Climate-driven trends in contemporary ocean productivity. Nature 444, 752–755. Bergquist, D. C., Andras, J. P., McNelis, T., Howlett, S., van Horn, M. J., and Fisher, C. R. (2003). Succession in Gulf of Mexico cold seep vestimentiferan aggregations: The importance of spatial variability. PSZN I: Mar. Ecol. 24, 31–44. Bernhard, J. M. (1987). Foraminiferal biotopes in Explorers Cove, McMurdo Sound, Antarctica. J. Foramin. Res. 17, 286–297. Bett, B. J., Malzone, M. G., Narayanaswamy, B. E., and Wigham, B. D. (2001). Temporal variability in phytodetritus and megabenthic activity at the seabed in the deep Northeast Atlantic. Prog. Oceanogr. 50, 349–368. Billett, D. S. M., Lampitt, R. S., Rice, A. L., and Mantoura, R. F. C. (1983). Seasonal sedimentation of phytoplankton to the deep-sea benthos. Nature 302, 520–522. Billett, D. S. M., Llewellyn, C., and Watson, J. (1988). Are deep-sea holothurians selective feeders? Echinoderm biology: Proceedings of the Sixth International Echinoderm Conference, Victoria, B.C., 421–429. Billett, D. S. M., Bett, B. J., Rice, A. L., Thurston, M. H., Gale´ron, J., Sibuet, M., and Wolff, G. A. (2001). Long-term change in the megabenthos of the Porcupine Abyssal Plain (NE Atlantic). Prog. Oceanogr. 50, 325–348. Billett, D. S. M., Bett, B. J., Reid, W. D. K., Boorman, B., and Priede, I. G. (2010). Longterm change in the abyssal NE Atlantic: The Amperima Event revisited. Deep Sea Res. Part II, 57, 1406–1417. Black, D. E., Abahazi, M. A., Thunell, R. C., Kaplan, A., Tappa, E. J., and Peterson, L. C. (2007). An 8-century tropical Atlantic SST record from the Cariaco Basin: Baseline variability, twentieth-century warming, and Atlantic hurricane frequency. Paleoceanography 2210.1029/2007PA001427. Boetius, A., Scheibe, S., Tselepides, A., and Thiel, H. (1996). Microbial biomass and activities in deep-sea sediments of the Eastern Mediterranean: Trenches are benthic hotspots. Deep Sea Res. Part I 43, 299–307. Booth, J. A., Ruhl, H. A., Lovell, L., Bailey, D. M., and Smith, K. L. Jr. (2008). Population dynamics of NE Pacific abyssal ophiuroids. Mar. Biol. 154, 933–941. Bopp, L., Aumont, O., Cadule, P., Alvain, S., and Gehlen, M. (2005). Response of diatoms distribution to global warming and potential implications: A global model study. Geophys. Res. Lett. 3210.1029/2005GL023653. Braby, C. E., Rouse, G. W., Johnson, S. B., Jones, W. J., and Vrijenhoek, R. C. (2007). Bathymetric and temporal variation among Osedax boneworms and associated megafauna on whale-falls in Monterey Bay, California. Deep Sea Res. Part I 54, 1773–1791. Brandt, A., Gooday, A. J., Branda˜o, S. N., Brix, S., Bro¨keland, W., Cedhagen, T., Choudhury, M., Cornelius, N., Danis, B., De Mesel, I., Diaz, R. J., Gillan, D. C. et al. (2007). First insights into biodiversity and biogeography of the Southern Ocean deep sea. Nature 447, 307–311. Butterfield, D. A., and Massoth, G. J. (1994). Geochemistry of North Cleft segment vent fluids. Changes in chlorinity and their possible relation to recent volcanism. J. Geophys. Res. Solid Earth 99, (B3), 4951–4968. Calado, R., Chevaldonne´, P., and dos Santos, A. (2004). A new species of the deep-sea genus Bresilia (Crustacea: Decapoda: Bresiliidae) discovered from a shallow-water cave in Madeira. J. Mar. Biolog. Assoc. U.K. 84, 191–199.

Temporal Change in Deep-Sea Ecosystems

81

Canals, M., Lastras, G., Urgeles, R., Casamor, J. L., Mienert, J., Cattaneo, A., De Batist, M., Haflidason, H., Imbo, Y., Laberg, J. S., Locat, J., Long, D. et al. (2004). Slope failure dynamics and impacts from seafloor and shallow sub-seafloor geophysical data: Case studies from the COSTA project. Mar. Geol. 213, 9–72. Canals, M., Danovaro, R., Heussner, S., Lykousis, V., Puig, P., Trincardi, F., Calafat, A. M., De Madron, X. D., Palanques, A., and Sanchez-Vidal, A. (2009). Cascades in Mediterranean submarine grand canyons. Oceanography 22, 26–43. Cannariato, K. G., Kennett, J. P., and Behl, R. J. (1999). Biotic response to late Quaternary rapid climate switches in Santa Barbara Basin: Ecological and evolutionary implications. Geology 27, 63–66. Carey, A. G. Jr. (1981). A comparison of benthic infaunal abundance on two abyssal plains in the northeast Pacific Ocean. Deep Sea Res. 28, 467–479. Chevaldonne´, P., and Lejeusne, C. (2003). Regional warming-induced species shift in north-west Mediterranean marine caves. Ecol. Lett. 6, 371–379. Chevaldonne´, P., Pe´rez, T., Boury-Esnault, N., Harmelin, J. G., Lejeusne, C., Zibrowius, H., Vacelet, J., Lampadariou, N., Janssen, A., and Martı´nez Arbizu, P. (2008). Shallow Marine Caves as Mesocosms of the Deep-Sea: The « 3PP cave » Example. Book of Abstracts, World Conference on Marine Biodiversity, 11–15 November 2008, Valencia, Spain. Colac¸o, A., Desbruye`res, D., Comtet, T., and Alayse, A. M. (1998). Ecology of the Menez Gwen hydrothermal vent field (Mid-Atlantic Ridge/Azores Triple Junction). Cah. Biol. Mar. 39, 237–240. Collins, M. A., Bailey, D. M., Ruxton, G. D., and Priede, I. G. (2005). Trends in body size across an environmental gradient: A differential response in scavenging and non-scavenging demersal deep-sea fish. Proc. R Soc. Lond. B 272, 2051–2057. Coma, R., Carola, M., Riera, T., and Zabala, M. (1997). Horizontal transfer of matter by a cave-dwelling mysid. PSZN I: Mar. Ecol. 18, 211–226. Company, J. B., Puig, P., Sarda`, F., Palanques, A., Latasa, M., and Scharek, R. (2008). Climate influence on deep-sea populations. PLoS ONE 3, e143110.1371/journal. pone.0001431. Conway, K. W., Krautter, M., Barrie, J. V., and Neuweiler, M. (2001). Hexactinellid sponge reefs on the Canadian continental shelf: A unique “Living Fossil”. Geosci. Can. 28, 71–78. Copley, J. T. P., Tyler, P. A., Murton, B. J., and Van Dover, C. L. (1997). Spatial and interannual variation in the faunal distribution at Broken Spur vent field (29 N, MidAtlantic Ridge). Mar. Biol. 129, 723–733. Copley, J. T. P., Tyler, P. A., Van Dover, C. L., Schultz, A., Dickson, P., Singh, S., and Sulanowska, M. (1999). Subannual temporal variation in faunal distributions at the TAG hydrothermal mound (26N, Mid-Atlantic Ridge). PSZN I: Mar. Ecol. 20, 291–306. Copley, J. T. P., Jorgensen, P. B. K., and Sohn, R. A. (2007). Assessment of decadal-scale ecological change at a deep Mid-Atlantic hydrothermal vent and reproductive time-series in the shrimp Rimicaris exoculata. J. Mar. Biol. Assoc. UK 84, 859–867. Cordes, E. E., McGinley, M., Podowski, E. L., Becker, E. L., and Lessard-Pilon, S. (2008). Coral communities of the deep Gulf of Mexico. Deep Sea Res. Part I 55, 777–787. Cordes, E. E., Bergquist, D. C., and Fisher, C. R. (2009). Macro-ecology of Gulf of Mexico cold seeps. Annu. Rev. Mar. Sci. 1, 143–168. Corliss, J. B., Dymond, J., Gordo, L. I., Edmond, J. M., von Herzen, R., Ballard, R. D., Green, K., Williams, D., Bainbridge, A., Crane, K., and van Andel, T. H. (1979). Submarine thermal springs on the Galapagos Rift. Science 203, 1073–1083. Cronin, T. M., and Vann, C. D. (2003). The sedimentary record of climatic and anthropogenic influence on the Patuxent Estuary and Chesapeake Bay ecosystems. Estuaries 26, 196–209.

82

A. G. Glover et al.

Cuvelier, D., Sarrazin, J., Colac¸o, A., Copley, J., Desbruye`res, D., Glover, A., Tyler, P., and Serra˜o Santos, R. (2009). Distribution and spatial variation of faunal assemblages on a hydrothermal edifice at Lucky Strike vent field (Mid-Atlantic Ridge) revealed by highresolution video image analysis. Deep Sea Res. Part I 56, 2026–2040. Cuvelier, D., Sarrazin J., Colac¸o A., Copley J., Glover, A., Tyler, P., Serra˜o Santos, R and Desbruye`res, D., submitted for publication. Community dynamics over 14 years at the Eiffel Tower hydrothermal edifice on the Mid-Atlantic ridge. Dahlgren, T. G., Wiklund, H., Ka¨llstro¨m, B., Lunda¨lv, T., Smith, C. R., and Glover, A. G. (2006). A shallow-water whale-fall experiment in the north Atlantic. Cah. Biol. Mar. 47, 385–389. Danovaro, R., Dell’Anno, A., and Pusceddu, A. (2004). Biodiversity response to climate change in a warm deep sea. Ecol. Lett. 7, 821–828. Dattagupta, S., Bergquist, D. C., Szalai, E. B., Macko, S. A., and Fisher, C. R. (2004). Tissue carbon, nitrogen, and sulfur stable isotope turnover in transplanted Bathymodiolus childressi mussels: Relation to growth and physiological condition. Limnol. Oceanogr. 49, 1144–1151. Dayton, P. K., and Oliver, J. S. (1977). Antarctic soft-bottom benthos in oligotrophic and eutrophic environments. Science 197, 55–58. De Stigter, H. C., Boer, W., De Jesu´s Mendes, P. A., Jesus, C. C., Thomas, L., Van Den Berg, G. D., and Van Weering, T. C. E. (2007). Recent sediment transport and deposition in Nazare´ Canyon, Portuguese continental margin. Mar. Geol. 246, 144–164. DeLaca, T. E., Lipps, J. E., and Hessler, R. R. (1980). The morphology and ecology of a new large agglutinated Antarctic foraminifer (Textulariina: Notodendrodidae nov). Zool. J. Linn. Soc. 69, 205–224. Delaney, J. R., Robigou, V., McDuff, R. E., and Tivey, M. K. (1992). Geology of a vigorous hydrothermal system on the endeavour segment, Juan de Fuca Ridge. J. Geophys. Res. 97, 19663–19682. Den Dulk, M., Reichart, G. J., Memon, G. M., Roelofs, E. M. B., Zachariasse, W. J., and van der Zwaan, G. J. (1998). Benthic foraminiferal response to variations in surface water productivity and oxygenation in the northern Arabian Sea. Mar. Micropaleontol. 35, 43–66. Desbruye`res, D. (1995). Temporal variations of deep-sea hydrothermal communities at 13 N/EPR. InterRidge News 4, 6–10. Desbruye`res, D. (1998). Temporal variations in the vent communities on the East Pacific Rise and Galapagos Spreading Centre: A review of present knowledge. Cah. Biol. Mar. 39, 241–244. Desbruye`res, D., Almeida, A., Biscoito, M., Comtet, T., Khripounoff, A., Le Bris, N., Sarradin, P. M., and Segonzac, M. (2000). A review of the distribution of hydrothermal vent communities along the northern Mid-Atlantic Ridge: Dispersal vs. environmental controls. Hydrobiologia 440, 201–216. Desbruye`res, D., Biscoito, M., Caprais, J. C., Colaco, A., Comtet, T., Crassous, P., Fouquet, Y., Khripounoff, A., Le Bris, N., Olu, K., Riso, R., Sarradin, P. M. et al. (2001). Variations in deep-sea hydrothermal vent communities on the Mid-Atlantic Ridge near the Azores plateau. Deep Sea Res. Part I 48, 1325–1346. Distel, D. L., Baco, A. R., Chuang, E., Morrill, W., Cavanaugh, C., and Smith, C. R. (2000). Marine ecology—Do mussels take wooden steps to deep-sea vents? Nature 403, 725–726. Domack, E., Duran, D., Leventer, A., Ishman, S., Doane, S., McCallum, S., Amblas, D., Ring, J., Gilbert, R., and Prentice, M. (2005). Stability of the Larsen B ice shelf on the Antarctic Peninsula during the Holocene epoch. Nature 436, 681–685. Domack, E., Duran, D., Leventer, A., Ishman, S., Brachfeld, S., Huber, B., Willmott, V., Rebesco, M., Zgur, F., Halverson, G., Rathburn, A., Padman, L. et al. (2007). Beneath

Temporal Change in Deep-Sea Ecosystems

83

the Larsen B Ice Shelf system: A marine perspective on a rapidly changing cryosphere. Geophys. Res. Abstr. 9, 04509. Drazen, J. C. (2002). A seasonal analysis of the nutritional condition of deep-sea macrourid fishes in the north-east Pacific. J. Fish Biol. 60, 1280–1295. Drazen, J. C., Baldwin, R. J., and Smith, K. L. Jr. (1998). Sediment community response to a temporally varying food supply at an abyssal station in the NE Pacific. Deep Sea Res. Part II 45, 893–913. Drazen, J. C., Popp, B. N., Choy, C. A., Clemente, T., De Forest, L., and Smith, K. L. (2008). Bypassing the abyssal benthic food web: Macrourid diet in the eastern North Pacific inferred from stomach content and stable isotopes analyses. Limnol. Oceanogr. 53, 2644–2654. Drazen, J. C., Phleger, C. F., Guest, M. A., and Nichols, P. D. (2009). Lipid compositions and diet inferences of abyssal macrourids in the eastern North Pacific. Mar. Ecol. Prog. Ser. 387, 1–14. Dziak, R. P., Smith, D. K., Bohnenstiehl, D. R., Fox, C. G., Desbruye`res, D., Matsumoto, H., Tolstoy, M., and Fornari, D. J. (2004). Evidence of a recent magma dike intrusion at the slow spreading lucky strike segment, mid-Atlantic ridge. J. Geophys. Res. Solid Earth 109, (B12102), 15. Embley, R. W., and Chadwick, W. W. Jr. (1994). Volcanic and hydrothermal processes on the southern Juan de Fuca Ridge. J. Geophys. Res. 99, 4741–4760. Embley, R. W., Murphy, K. M., and Fox, C. G. (1990). High-resolution studies of the summit of axial volcano. J. Geophys. Res. Solid Earth 95, (B8), 12785–12812. Embley, R. W., Chadwick, W. W., Perfit, M. R., and Baker, E. T. (1991). Geology of the northern Cleft segment, Juan de Fuca Ridge: Recent lava flows, sea-floor spreading, and the formation of megaplumes. Geology 19, 771–775. Embley, R. W., Chadwick, W. W. Jr., Clague, D., and Stakes, D. (1999). 1998 eruption of axial volcano: Multibeam anomalies and seafloor observations. Geophys. Res. Lett. 26, 3425–3428. Embley, R. W., Chadwick, W. W., Perfit, M. R., Smith, M. C., and Delaney, J. R. (2000). Recent eruptions on the CoAxial segment of the Juan de Fuca Ridge: implications for midocean ridge accretion processes. J. Geophys. Res. 105, 16,501–16,526. Embley, R. W., Chadwick, W. W., Baker, E. T., Butterfield, D. A., Resing, J. A., De Ronde, C. E. J., Tunnicliffe, V., Lupton, J. E., Juniper, S. K., Rubin, K. H., Stern, R. J., Lebon, G. T., et al. (2006). Long-term eruptive activity at a submarine arc volcano. Nature 441, 494–497. Fichez, R. (1990a). Decrease in allochthonous organic imputs in dark submarine caves, connection with lowering in benthic community richness. Hydrobiologia 207, 61–69. Fichez, R. (1990b). Les pigments chlorophylliens: Indices d’oligotrophie dans les grottes sous-marines. Comptes Rendus de l’Acade´mie des Sciences de Paris, Se´rie III 310, 155–162. Fontanier, C., Jorissen, F. J., Chaillou, G., David, C., Anschutz, P., and Lafon, V. (2003). Seasonal and interannual variability of benthic foraminiferal faunas at 550 m depth in the Bay of Biscay. Deep Sea Res. Part I 50, 457–494. Fontanier, C., Jorissen, F., Anschutz, P., and Chaillou, G. (2006). Seasonal variability of benthic foraminiferal faunas at 1000 m depth in the Bay of Biscay. J. Foramin. Res. 36, 61–76. Fornari, D. J., and Embley, R. W. (1995). Tectonic and volcanic controls on hydrothermal processes at the mid-ocean ridge: An overview based on near-bottom and submersible studies. In “Seafloor Hydrothermal Systems: Physical, Chemical, Biological and Geological Interactions” (S. E. Humphris, R. A. Zierenberg, L. S. Mullineaux and R. E. Thomson, eds.), (Geophysical Monograph 91.). pp. 1–46. AGU, Washington, DC. Foucher, J.-P., Westbrook, G. K., Boetius, A., Ceramicola, S., Dupre´, S., Mascle, J., Mienert, J., Pfannkuche, O., Pierre, C., and Praeg, D. (2009). Structure and drivers of cold seep ecosystems. Oceanography 22, 92–109.

84

A. G. Glover et al.

Frid, C. L. J., Garwood, P., and Robinson, L. A. (2009). The North Sea benthic system: A 36 year time series. J. Mar. Biol. Assoc. UK 89, 1–10. Fujikura, K., Fujiwara, Y., and Kawato, M. (2006). A new species of Osedax (Annelida: Siboglinidae) associated with whale carcasses off Kyushu, Japan. Zool. Sci. 23, 733–740. Gage, J. D., and Tyler, P. A. (1982). Growth and reproduction of the deep-sea brittlestar Ophiomusium lymani Wyville Thomson. Oceanol. Acta 5, 73–83. Gage, J. D., Lightfoot, R. H., Pearson, M., and Tyler, P. A. (1980). An introduction to a sample time series of abyssal macrobenthos: Methods and principle sources of variability. Oceanol. Acta 3, 169–176. Gallucci, F., Sauter, E., Sachs, O., Klages, M., and Soltwedel, T. (2008a). Caging experiment in the deep sea: Efficiency and artefacts from a case study at the Arctic long-term observatory HAUSGARTEN. J. Exp. Mar. Biol. Ecol. 354, 39–55. Gallucci, F., Fonseca, G., and Soltwedel, T. (2008b). Effects of megafauna exclusion on nematode assemblages at a deep-sea site. Deep Sea Res. Part I 55, 332–349. Gebruk, A. V., Chevaldonne´, P., Shank, T., Lutz, R. A., and Vrijenhoek, R. C. (2000). Deep-sea hydrothermal vent communities of the Logatchev area (14 degree 45 N, Mid-Atlantic Ridge): Diverse biotopes and high biomass. J. Mar. Biol. Assoc. UK 80, 383–393. Gebruk, A. V., Krylova, E. M., Lein, A. Y., Vinogradov, G. M., Enderson, E., Pimenov, N. V., Cherkashev, G. A., and Crane, K. (2003). Methane seep community of the Ha˚kon Mosby mud volcano (the Norwegian Sea): Composition and trophic aspects. Sarsia 88, 394–403. German, C. R., Parson, L. M., Bougault, F., Coller, D., Critchley, M., Dapoigny, A., Day, C., Eardley, D., Fearn, A., Flewellen, C., Kirk, R., Klinkhammer, G. et al. (1996). Hydrothermal exploration near the Azores triple junction: Tectonic control of venting at slow-spreading ridges? Earth Planet. Sci. Lett. 138, 93–104. Glover, A. G., and Smith, C. R. (2003). The deep-sea floor ecosystem: Current status and prospects of anthropogenic change by the year 2025. Environ. Conserv. 30, 219–241. Glover, A., Paterson, G., Bett, B., Gage, J., Sibuet, M., Sheader, M., and Hawkins, L. (2001). Patterns in polychaete abundance and diversity from the Madeira Abyssal Plain, northeast Atlantic. Deep Sea Res. Part I 48, 217–236. Glover, A. G., Smith, C. R., Paterson, G. L. J., Wilson, G. D. F., Hawkins, L., and Sheader, M. (2002). Polychaete species diversity in the central Pacific abyss: Local and regional patterns, and relationships with productivity. Mar. Ecol. Prog. Ser. 240, 157–169. Glover, A. G., Ka¨llstro¨m, B., Smith, C. R., and Dahlgren, T. (2005). World-wide whale worms? A new species of Osedax from the shallow north Atlantic. Proc. R. Soc. Lond., B 272, 2587–2592. Glover, A. G., Smith, C. R., Mincks, S., Sumida, P., and Thurber, A. (2008). Macrofaunal abundance and composition on the West Antarctic Peninsula continental shelf: Evidence for a sediment ‘food bank’ and similarities to deep-sea habitats. Deep Sea Res. Part II 55, 2491–2501. Goffredi, S. K., Johnson, S. B., and Vrijenhoek, R. C. (2007). Genetic and functional diversity of microbial symbionts associated with new species of Osedax polychaete worms. Appl. Environ. Microbiol. 73, 2314–2323. Gooday, A. J. (2002). Biological responses to seasonally varying fluxes of organic matter to the ocean floor: A review. J. Oceanogr. 58, 305–332. Gooday, A. J. (2003). Benthic foraminifera (Protista) as tools in deep-water palaeoceanography: A review of environmental influences on faunal characteristics. Adv. Mar. Biol. 46, 1–90. Gooday, A. J., and Turley, C. M. (1990). Responses by benthic organisms to inputs of organic material to the ocean floor: A review. Philos. Trans. R. Soc. London Ser. A 331, 119–138.

Temporal Change in Deep-Sea Ecosystems

85

Gooday, A. J., Bowser, S. S., and Bernhard, J. M. (1996). Benthic foraminiferal assemblages in Explorer’s Cove, Antarctica: A shallow water site with deep sea characteristics. Prog. Oceanogr. 37, 219–267. Gooday, A. J., Levin, L. A., Aranda da Silva, A., Bett, B. J., Cowie, G. L., Dissard, D., Gage, J. D., Hughes, D. J., Jeffreys, R., Lamont, P. A., Larkin, K. E., Murty, S. J. et al. (2009). Faunal responses to oxygen gradients on the Pakistan Margin: A comparison of foraminiferans, macrofauna and megafauna. Deep Sea Res. Part II 56, 488–502. Gooday, A. J., Malzone, M. G., Bett, B. J., and Lamont, P. A. (2010). Decadal-scale changes in shallow-infaunal foraminiferal assemblages at the Porcupine Abyssal Plain, NE Atlantic. Deep Sea Res. Part II, 57, 1362–1382. Gordon, J. D. M. (1986). The fish populations of the Rockall Trough. Proc. R. Soc. Lond., B, Biol. Sci. 88, 191–204. Grassle, J. F. (1991). Deep-sea benthic biology. Bioscience 41, 464–469. Grassle, J. F., and Maciolek, N. J. (1992). Deep-sea species richness: Regional and local diversity estimates from quantitative bottom samples. Am. Nat. 139, 313–341. Grassle, J. F., and Morse-Porteous, L. S. (1987). Macrofaunal colonization of disturbed deep-sea environments and the structure of deep-sea benthic communities. Deep Sea Res. 34, 1911–1950. Grehan, A. J., and Juniper, S. K. (1996). Clam distribution and subsurface hydrothermal processes at Chowder Hill (Middle Valley), Juan de Fuca Ridge. Mar. Ecol. Prog. Ser. 130, 105–115. Hagadorn, J. W. (1996). Laminated sediments of Santa Monica Basin, California Continental Borderland. : ‘Palaeoclimatology and Palaeoceanography from Laminated Sediments’ (A. E. S. Kemp, ed.), pp. 111–120, Geological Society of London Special Publication. Harmelin, J.-G., Vacelet, J., and Vasseur, P. (1985). Les grottes sous-marines obscures: un milieu extreme et un remarquable biotope refuge. Te´thys 11, 214–229. Harrison, K. (1988). Seasonal reproduction in deep-sea Crustacea (Isopoda, Asellota). J. Nat. Hist. 22, 175–197. Hassol, S. J. (2004). Impacts of a warming Arctic: Arctic Climate Change Assessment. Cambridge University Press, p. 139. Haymon, R. M., Fornari, D., Edwards, M., Carbotte, S., Wright, D., and Macdonald, K. C. (1991). Hydrothermal vent distribution along the East Pacific Rise crest (9 090 –540 N) and its relationship to magmatic and tectonic processes on fast-spreading mid-ocean ridges. Earth Planet. Sci. Lett. 104, 513–534. Haymon, R. M., Fornari, D. J., Von Damm, K. L., Lilley, M. D., Perfit, M. R., Edmond, J. M., Shanks, W. C., Lutz, R. A., Grebmeier, J. M., Carbotte, S., Wright, D., McLaughlin, E. S. M. et al. (1993). Volcanic eruption of the mid-ocean ridge along the East Pacific Rise crest at 9 45–520 N: Direct submersible observations of seafloor phenomena associated with an eruption event in April, 1991. Earth Planet. Sci. Lett. 119, 85–101. Hayward, B. W. (2002). Late Pliocene to middle Pleistocene extinctions of deep-sea benthic foraminifera (“Stilostomella Extinction”) in the Southwest Pacific. J. Foramin. Res. 32, 274–307. Helly, J. J., and Levin, L. A. (2004). Global distribution of naturally occurring marine hypoxia on continental margins. Deep Sea Res. Part I 51, 1159–1168. Hess, S., and Kuhnt, W. (1996). Deep-sea benthic foraminiferal recolonization of the 1991 Mt. Pinatubo ash layer in the South China Sea. Mar. Micropaleontol. 28, 171–197. Hess, S., Kuhnt, W., Hill, S., Kaminski, M. A., Holbourn, A., and de Leon, M. (2001). Monitoring the recolonization of the Mt Pinatubo 1991 ash layer by benthic foraminifera. Mar. Micropaleontol. 43, 119–142. Hessler, R. R., and Sanders, H. L. (1967). Faunal diversity in the deep sea. Deep Sea Res. 21, 65–78.

86

A. G. Glover et al.

Hessler, R. R., and Stro¨mberg, J.-O. (1989). Behavior of janiroidean isopods (Asellota), with special reference to deep-sea genera. Sarsia 74, 145–159. Hessler, R. R., Smithey, W. M., and Keller, C. H. (1985). Spatial and temporal variation of giant clams, tubeworms and mussels at deep-sea hydrothermal vents. Bull. Biol. Soc. Wash. 6, 411–428. Hessler, R. R., Smithey, W. M., Boudrias, M. A., Keller, C. H., Lutz, R. A., and Childress, J. J. (1988). Temporal change in megafauna at the Rose Garden hydrothermal vent (Galapagos Rift—Eastern Tropical Pacific). Deep Sea Res. 35, 1681–1709. Holm, P. (2005). Human impacts on fisheries resources and abundance in the Danish Wadden Sea, c1520 to the present. Helgol. Mar. Res. 59, 39–44. Hoste, E., Vanhove, S., Schewe, I., Soltwedel, T., and Vanreusel, A. (2007). Spatial and temporal variations in deep-sea meiofauna assemblages in the marginal ice zone of the Arctic Ocean. Deep Sea Res. Part I 54, 109–129. Iliffe, T. M., Wilkens, H., Parzefall, J., and Williams, D. (1984). Marine lava cave fauna: Composition, biogeography, and origins. Science 225, 309–311. IPCC. (2007). Intergovernmental Panel on Climate Change Fourth Assessment Report. Jackson, J. B. C., Kirby, M. X., Berger, W. H., Bjorndal, K. A., Botsford, L. W., Bourque, B. J., Bradbury, R. H., Cooke, R., Erlandson, J., Estes, J. A., Hughes, T. P., Kidwell, S. et al. (2001). Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–637. Jacobs, D. K., and Lindberg, D. R. (1998). Oxygen and evolutionary patterns in the sea: Onshore/offshore trends and recent recruitment of deep-sea faunas. Proc. Natl Acad. Sci. USA 95, 9396–9401. Jerosch, K., Schlu¨ter, M., Foucher, J.-P., Allais, A.-G., Klages, M., and Edy, C. (2007). Spatial distribution of mud flows, chemoautotrophic communities, and biogeochemical habitats at Ha˚kon Mosby Mud Volcano. Mar. Geol. 243, 1–17. Johnson, H. P., and Embley, R. W. (1990). Axial Seamount: An active ridge axis volcano on the Central Juan de Fuca Ridge. J. Geophys. Res. 95, (B8), 12689–12696. Johnson, K. S., Beehler, C. L., Sakamoto-Arnold, C. M., and Childress, J. J. (1986). In situ measurements of chemical distributions in a deep-sea hydrothermal vent field. Science 231, 1139–1141. Jorissen, F., Fontanier, C., and Thomas, E. (2007). Paleoceanographical proxies based on deep-sea benthic foraminiferal assemblage characteristics. In “Proxies in Late Cenozoic Paleoceanography” (C. Hillaire-Marcel and A. de Vernal, eds.), pp. 263–325. Elsevier, Amsterdam, Boston, Heidelberg, London, New York, Oxford, Paris, San Diego, San Francisco, Singapore, Sydney, Tokyo. Jumars, P. A., and Eckman, J. E. (1983). Spatial structure within deep-sea benthic communities. In “The Sea: Deep-Sea Biology” (G. T. Rowe, ed.), pp. 399–452. Wiley Interscience, New York, pp. 399–452. Juniper, S. K., and Tunnicliffe, V. (1997). Crustal accretion and the hot vent ecosystem. Philos. Trans. R. Soc. London Ser. A 355, 459–474. Juniper, S. K., Martineu, P., Sarrazin, J., and Ge´linas, Y. (1995). Microbial-mineral floc associated with nascent hydrothermal activity on CoAxial Segment, Juan de Fuca Ridge. Geophys. Res. Lett. 22, 179–182. Kalogeropoulou, V., Bett, B. J., Gooday, A. J., Lamparadariou, N., Martinez Arbizu, P., Vanreusel, A. (2010). Temporal changes during the decade 1989–1999 in deep sea metazoan meiofaunal assemblages at the Porcupine Abyssal Plain, NE Atlantic. Deep Sea Res. Part II, 57, 1383–1395. Kamykowski, D., and Zentara, S. J. (1990). Hypoxia in the world ocean as recorded in the historical dataset. Deep Sea Res. 37, 1861–1874. Kanzog, C., Ramette, A., Que´ric, N. V., and Klages, M. (2008). Response of benthic microbial communities to chitin enrichment: An in situ study in the deep Arctic Ocean. Polar Biol. 32, 105–112.

Temporal Change in Deep-Sea Ecosystems

87

Kaufmann, R. S., and Smith, K. L. Jr. (1997). Activity patterns of mobile epibenthic megafauna at an abyssal site in the eastern North Pacific: Results from a 17-month time-lapse photographic study. Deep Sea Res. Part I 44, 559–579. Kemp, A. E. S. (2003). Evidence for abrupt climate change in annually laminated marine sediments. Philos. Trans. R. Soc. Lond. 361, 1851–1870. Kemp, K. M., Jamieson, A. J., Bagley, P. M., McGrath, H., Bailey, D. M., Collins, M. A., and Priede, I. G. (2006). Consumption of a large bathyal food fall, a six month study in the north-east Atlantic. Mar. Ecol. Prog. Ser. 310, 65–76. Kennish, M. J., and Lutz, R. A. (1999). Calcium carbonate dissolution rates in deep-sea bivalve shells on the East Pacific Rise at 21 N: Results of an 8-year in-situ experiment. Palaeogeogr. Palaeoclimatol. Palaeoecol. 154, 293–299. Kitazato, H., and Ohga, T. (1995). Seasonal changes in deep-sea benthic foraminiferal populations: Results of long-term observations at Sagami Bay, Japan. In “Biogeochemical Processes and Ocean Flux in the Western Pacific” (H. Sakai and Y. Nozami, eds.), pp. 331–342. Terra Scientific Publishing Company, Tokyo. Kitazato, H., Shirayama, Y., Nakatsuka, T., Fujiwara, S., Shimanaga, M., Kato, Y., Okada, Y., Kanda, J., Yamaoka, A., Masuzawa, T., and Suzuki, K. (2000). Seasonal phytodetritus deposition and responses of bathyal benthic foraminiferal populations from Project Sagami 1996–1999. Mar. Micropaleontol. 40, 135–149. Kitazato, H., Nakatsuka, T., Shimanaga, M., Kanda, J., Soh, W., Kato, Y., Okada, Y., Yamaoka, A., Masuzawa, T., Suzuki, K., and Shirayama, Y. (2003). Long-term monitoring of the sedimentary processes in the central part of Sagami Bay, Japan: Rationale, logistics and overview of results. Prog. Oceanogr. 57, 3–16. Klein, B., Roether, W., Manca, B. B., Bregant, D., Beitzel, V., Kovacevic, V., and Luchetta, A. (1999). The large deep water transient in the Eastern Mediterranean. Deep Sea Res. Part I 46, 371–414. Koho, K. A., Kouwenhoven, T. J., de Stigter, H. C., and van der Zwaan, G. J. (2007). Benthic foraminifera in the Nazare Canyon, Portuguese continental margin: Influence of sedimentary disturbance on fauna. Mar. Micropaleontol. 66, 27–51. Koslow, J. A. (2007). The Silent Deep: The Discovery, Ecology and Conservation of the Deep Sea. University of Chicago Press, Chicago. Koslow, J. A., Boehlert, G. W., Gordon, J. D. M., Haedrich, H. L., Lorance, P., and Parin, N. (2000). Continental slope and deep-sea fisheries: Implications for a fragile ecosystem. ICES J. Mar. Sci. 57, 548–557. Kro¨ncke, I., Turkay, M., and Fiege, D. (2003). Macrofauna communities in the Eastern Mediterranean deep sea. Marine Ecology-Pubblicazioni Della Stazione Zoologica Di Napoli I. 24, 193–216. Lalou, C. (1991). Deep-sea hydrothermal venting: A recently discovered marine system. J. Mar. Syst. 1, 403–440. Lambshead, P. J. D., Tietjen, J., Glover, A., Ferrero, T., Thistle, D., and Gooday, A. J. (2001). Impact of large-scale natural physical disturbance on the diversity of deep-sea North Atlantic nematodes. Mar. Ecol. Prog. Ser. 214, 121–126. Lampadariou, N., Tselepides, A., and Hatziyanni, E. (2009). Deep-sea meiofaunal and foraminiferal communities along a gradient of primary productivity in the eastern Mediterranean Sea. Sci. Mar. 73, 337-345. Lampitt, R. S., and Antia, A. N. (1997). Particle flux in deep seas: Regional characteristics and temporal variability. Deep Sea Res. Part I 44, 1377–1403. Lampitt, R. S., et al., (2010). Inter annual variability in downward particle flux at the PAP study site, North-east Atlantic. Deep Sea Res. Part II, 57, 1346–1361. Lejeusne, C., and Chevaldonne´, P. (2006). Brooding crustaceans in a highly fragmented habitat: The genetic structure of Mediterranean marine cave-dwelling mysid populations. Mol. Ecol. 15, 4123–4140.

88

A. G. Glover et al.

Lejeusne, C., Chevaldonne´, P., Pergent-Martini, C., Boudouresque, C. F., and Pe´rez, T. (2010). Climate change effects on a miniature ocean: The highly diverse, highly impacted Mediterranean Sea. Trends Ecol. Evol. 25, 250–260. Levesque, C., and Juniper, S. K. (2002). Particulate matter as a food source at a nascent hydrothermal vent on the Juan de Fuca Ridge. Cah. Biol. Mar. 43, 289–292. Levesque, C., Juniper, S. K., and Limen, H. (2006). Spatial organization of food webs along habitat gradients at deep-sea hydrothermal vents on Axial Volcano, Northeast Pacific. Deep Sea Res. Part I 53, 726–739. Levin, L. A. (2003). Oxygen minimum zone benthos: Adaptation and community response to hypoxia. Oceanogr. Mar. Biol. Annu. Rev. 41, 1–45. Levin, L. A. (2005). Ecology of cold seep sediments: Interactions of fauna with flow, chemistry and microbes. Oceanogr. Mar. Biol.—An Annu. Rev. 43, 1–46. Levin, L. A., Etter, R. J., Rex, M. A., Gooday, A. J., Smith, C. R., Pineda, J., Stuart, C. T., Hessler, R. R., and Pawson, D. (2001). Environmental influences on regional deep-sea species diversity. Annu. Rev. Syst. Ecol. 32, 51–93. Levin, L., Gutierrez, D., Rathburn, A., Neira, C., Sellanes, J., Munoz, P., Gallardo, V., and Salamanca, M. (2002). Benthic processes on the Peru margin: A transect across the oxygen minimum zone during the 1997–98 El Nino. Prog. Oceanogr. 53, 1–27. Leys, S. P., Wilson, K., Holeton, C., Reiswig, H. M., Austin, W. C., and Tunnicliffe, V. (2004). Patterns of glass sponge (Porifera, Hexactinellida) distribution in coastal waters of British Columbia, Canada. Mar. Ecol. Prog. Ser. 283, 133–149. Lightfoot, R. H., Tyler, P. A., and Gage, J. D. (1979). Seasonal reproduction in deep-sea bivalves and brittlestars. Deep Sea Res. 26A, 967–973. Little, C. T. S., and Vrijenhoek, R. C. (2003). Are hydrothermal vent animals living fossils? Trends Ecol. Evol. 18, 582–588. Lonsdale, P. (1977). Deep-tow observations at the mounds abyssal thermal field, Galapagos Rift. Earth Planet. Sci. Lett. 36, 92–110. Luther, G. W., Rozan, T. F., Taillefert, M., Nuzzio, D. B., Di Meo, C., Shank, T. M., Lutz, R. A., and Cary, S. C. (2001). Chemical speciation drives hydrothermal vent ecology. Nature 410, 813–816. Marcus, J., Tunnicliffe, V., and Butterfield, D. (2009). Post-eruption succession of macrofaunal communities at diffuse flow hydrothermal vents on Axial Volcano, Juan de Fuca Ridge, Northeast Pacific. Deep Sea Res. 56, 1586–1598. Marshall, J. T. (1900). On a British species of Myrina, with a note on the genus Idas. J. Malacol. 7, 167–170. Masson, D. G., Kenyon, N. H., and Weaver, P. P. E. (1996). Slides, debris flows, and turbidity currents. In “Oceanography, An Illustrated Guide” (C. P. Summerhayes and S. A. Thorpe, eds.), pp. 136–151. Manson Publishing, London. Matsumoto, K. (2007). Radiocarbon-based circulation age of the world oceans. J. Geophys. Res. 112, C0900410.1029/2007JC004095. Menzies, R. J. (1965). Conditions for the existence of life on the abyssal sea floor. Oceanogr. Mar. Biol.: An Annu. Rev. 3, 195–210. Merrett, N. R. (1992). Demersal icthyofaunal distribution in the abyssal eastern North Atlantic, with special reference to Coryphaenoides (Nematonurus) armatus (Macrouridae). J. Mar. Biol. Assoc. UK 72, 5–24. Mestre, N. C., Thatje, S., and Tyler, P. A. (2009). The ocean is not deep enough: Pressure tolerances during early ontogeny of the blue mussel Mytilus edulis. Proc. R. Soc. Lond., B, Biol. Sci. 276, 717–726. Mincks, S. L., and Smith, C. R. (2007). Recruitment patterns in Antarctic shelf sediments: Evidence of decoupling from seasonal phytodetritus pulses. Polar Biol. 30, 587–600. Mullineaux, L. S., and Peterson, C. H. (2003). Successional mechanism varies along a gradient in hydrothermal fluid flux at deep-sea vents. Ecol. Monogr. 73, 523–542.

Temporal Change in Deep-Sea Ecosystems

89

Murray, J. W. (2000). When does environmental variability become environmental change? In “Environmental Micropaleontology” Volume 15 of Topics in Geobiology (R. E. Martin, ed.), pp. 7–37. Kluwer Academis/Plenum Publishers, New York. Murton, B. J., Klinkhammer, G., Becker, K., Briais, A., Edge, D., Hayward, N., Millard, N., Mitchell, I., Rouse, I., Rudnick, M., Sayanagi, K., Sloan, H. et al. (1994). Direct evidence for the distribution and occurrence of hydrothermal activity between 27 –30 N on the mid-Atlantic Ridge. Earth Planet. Sci. Lett. 125, 119–128. Murty, S. J., Bett, B. J., Gooday, A. J. (2009). Megafaunal responses to strong oxygen gradients on the Pakistan Margin of the Arabian Sea. Deep Sea Res. Part II 56, 472–487. Nix, E. R., Fisher, C. R., Vodenichar, J., and Scott, K. M. (1995). Physiological ecology of a mussel with methanotrophic endosymbionts at 3 hydrocarbon seep sites in the Gulf-of Mexico. Mar. Biol. 122, 605–617. Ohga, T., and Kitazato, H. (1997). Seasonal changes in bathyal foraminiferal populations in response to the flux of organic matter (Sagami Bay, Japan). Terra Nova 9, 33–37. Ohman, M. D., and Hsieh, C.-H. (2008). Spatial differences in mortality of Calanus pacificus within the California Current System. J. Plankton Res. 30, 359–366. Parker, C. M., Von Damm, K. L., Beers, K. A., Green, D. R., Alker, B. J., and German, C. R. (2005). Time series fluid compositions from the TAG hydrothermal mound, MAR: 1986–2004, EOS, Transactions of the American Geophysical Union, 86, Fall Meeting Supplement, Abstract OS22A-07. Pascual, M., and Guichard, F. (2005). Criticality and disturbance in spatial ecological systems. Trends Ecol. Evol. 20, 88–95. Paterson, G. L. J., Thurston, M. H., Gage, J. D., Lamont, P. M., and Bett, B. J. (1994a). Patterns of polychaete assemblage structure from the abyss: Some preliminary observations from NE Atlantic abyssal plains. Polychaete Res. 16, 16–19. Paterson, G. L. J., Gage, J. D., Lamont, P., Bett, B. J., and Thurston, M. T. (1994b). Patterns of abundance and diversity from the abyss—polychaetes from northeastern Atlantic abyssal plains. Me´moires du Muse´um National D’histoire Naturelle 162, 503–509. Paull, C. K., Hecker, B., Commeau, R., Freemanlynde, R. P., Neumann, C., Corso, W. P., Golubic, S., Hook, J. E., Sikes, E., and Curray, J. (1984). Biological communities at the Florida Escarpment resemble hydrothermal vent taxa. Science 226, 965–967. Paulmier, A., and Ruiz-Pino, D. (2008). Oxygen minimum zones (OMZs) in the modern Ocean. Prog. Oceanogr. 10.1016/j.pocean.2008.08.001. Pauly, D., Christensen, V., Dalsgaard, J., Froese, R., and Torres, F. (1998). Fishing Down Marine Food Webs. Science 279, 860–863. Pike, J., and Kemp, A. E. S. (1997). Early Holocene decadal-scale ocean variability recorded in Gulf of California laminated sediments. Paleoceanography 12, 227–238. Pond, D. W., Segonzac, M., Bell, M. V., Dixon, D. R., Fallick, A. E., and Sargent, J. R. (1997). Lipid and lipid carbon stable isotope composition of the hydrothermal vent shrimp Mirocaris fortunata: Evidence for nutritional dependence on photosynthetically fixed carbon. Mar. Ecol. Prog. Ser. 157, 221–231. Premke, K., Muyakshin, S., Klages, M., and Wegner, J. (2003). Evidence for long range chemoreceptive tracking of food odour in deep sea scavengers by scanning sonar data. J. Exp. Mar. Biol. Ecol. 285–286, 283–294. Premke, K., Klages, M., and Arntz, W. E. (2006). Aggregations of Arctic deep-sea scavengers at large food falls: Temporal distribution, consumption rates and population structure. Mar. Ecol. Prog. Ser. 325, 121–135. Priede, I. M., Bagley, P. M., and Smith, K. L. (1994). Seasonal changes in activity of abyssal demersal scavenging grenadiers Coryphaenoides (Nematonurus) armatus in the eastern North Pacific Ocean. Limnol. Oceanogr. 39, 279–285.

90

A. G. Glover et al.

Priede, I. G., Deary, A. R., Bailey, D. M., and Smith, K. L. (2003). Low activity and seasonal change in population size structure of grenadiers in the oligotrophic abyssal Central North Pacific Ocean. J. Fish Biol. 63, 187–196. Raupach, M. J., Mayer, C., Malyutina, M., and Wa¨gele, J. W. (2009). Multiple origins of deep-sea Asellota (Crustacea: Isopoda) from shallow waters revealed by molecular data. Proc. R Soc. Lond. B 276, 799–808. Ravaux, J., Gaill, F., Le Bris, N., Sarradin, P-M., Jollivet, D., and Shillito, B. (2003). Heatshock response and temperature resistance in the deep-sea vent shrimp Rimicaris exoculata. J. Exp. Biol. 206, 2345–2354. Rex, M. A., Etter, R. J., Morris, J. S., Crouse, J., McClain, C. R., Johnson, N. A., Stuart, C. T., Deming, J. W., Thies, R., and Avery, R. (2006). Global bathymetric patterns of standing stock and body size in the deep-sea benthos. Mar. Ecol. Prog. Ser. 317, 1–8. Rice, A. L., Thurston, M. H., and Bett, B. J. (1994). The IOSDL DEEPSEAS programme: Introduction and photographic evidence for the presence and absence of a seasonal input of phytodetritus at contrasting abyssal sites in the northeastern Atlantic. Deep Sea Res. Part I 41, 1305–1320. Richardson, A. J., and Schoeman, D. S. (2004). Climate impact on plankton ecosystems in the Northeast Atlantic. Science 305, 1609–1612. Robinson, L. A., and Frid, C. L. J. (2008). Historical marine ecology: Examining the role of fisheries in changes in North Sea benthos. Ambio 37, 362–371. Roemmich, D., and Mcgowan, J. (1995). Climatic warming and the decline of zooplankton in the California current. Science 268, 352–353. Roether, W., Manca, B. B., Klein, B., Bregant, D., Georgopoulos, D., Beitzel, V., Kovacevic, V., and Luchetta, A. (1996). Recent changes in eastern Mediterranean deep waters. Science 271, 333–335. Roman, J., and Palumbi, S. R. (2003). Whales before whaling in the North Atlantic. Science 301, 508–510. Rona, P. A., Klinkhammer, G., Nelsen, T. A., Trefry, G. H., and Elderfield, H. (1986). Black smokers, massive sulfides and vent biota at the Mid-Atlantic Ridge. Nature 321, 33–37. Rouse, G. W., Goffredi, S. K., and Vrijenhoek, R. C. (2004). Osedax: bone-eating marine worms with dwarf males. Science 305, 668–671. Rowe, G. T. (1983). Biomass and production of the deep-sea macrobenthos. In “Deep-Sea Biology” (G. T. Rowe, ed.), pp. 97–121. John Wiley, New York. Ruhl, H. A. (2007). Abundance and size distribution dynamics of abyssal epibenthic megafauna in the northeast Pacific. Ecology 88, 1250–1262. Ruhl, H. A. (2008). Community change in the variable resource habitat of the abyssal NE Pacific. Ecology 89, 991–1000. Ruhl, H. A., and Smith, K. L. Jr. (2004). Shifts in deep-sea community structure linked to climate and food supply. Science 305, 513–515. Ruhl, H. A., Ellena, J. A., and Smith, K. L. Jr. (2008). Connections between climate, food limitation, and carbon cycling in abyssal sediment communities. Proc. Natl Acad. Sci. USA 105, 17006–17011. Sarda`, F., Calafat, A., Flexas, M. M., Tselepides, A., Canals, M., Espino, M., and Tursi, A. (2004). An introduction to Mediterranean deep-sea biology. Sci. Mar. 68, 7–38. Sarrazin, J., and Juniper, S. K. (1999). Biological characteristics of a hydrothermal edifice mosaic community. Mar. Ecol. Prog. Ser. 185, 1–19. Sarrazin, J., Robigou, V., Juniper, S. K., and Delaney, J. R. (1997). Biological and geological dynamics over four years on a high-temperature sulfide structure at the Juan de Fuca Ridge hydrothermal observatory. Mar. Ecol. Prog. Ser. 153, 5–24.

Temporal Change in Deep-Sea Ecosystems

91

Sarrazin, J., Juniper, S. K., Massoth, G., and Legendre, P. (1999). Physical and chemical factors influencing species distributions on hydrothermal sulfide edifices of the Juan De Fuca Ridge, Northeast Pacific. Mar. Ecol. Prog. Ser. 190, 89–112. Sarrazin, J., Levesque, C., Juniper, S. K., and Tivey, M. K. (2002). Mosaic community dynamics on Juan De Fuca Ridge Sulfide Edifices: Substratum, temperature and implications for trophic structure. Cah. Biol. Mar. 43, 275–279. Sassen, R., Macdonald, I. R., Requejo, A. G., Guinasso, N. L., Kennicutt, M. C., Sweet, S. T., and Brooks, J. M. (1994). Organic geochemistry of sediments from chemosynthetic communities, Gulf-of-Mexico slope. Geo-Mar. Lett. 14, 110–119. Sauter, E. J., Muyakshin, S. I., Charlou, J.-L., Schlu¨ter, M., Boetius, A., Jerosch, K., Damm, E., Foucher, J.-P., and Klages, M. (2006). Methane discharge from a deep-sea submarine mud volcano into the upper water column by gas hydrate-coated methane bubbles. Earth Planet. Sci. Lett. 243, 354–365. Scambos, T., Hulbe, C., and Fahnestock, M. (2003). Climate-induced ice shelf disintegration in the Antarctic Peninsula. Antarctic Res. Ser. 79, 79–92. Scheffer, M., Carpenter, S., Foley, J. A., Folke, C., and Walker, B. (2001). Catastrophic shifts in ecosystems. Nature 413, 591–596. Schmiedl, G., Mitschele, A., Beck, S., Emeis, K. C., Hemleben, C., Schulz, H., Sperling, M., and Weldeab, S. (2003). Benthic foraminiferal record of ecosystem variability in the eastern Mediterranean Sea during times of sapropel S5 and S6 deposition. Palaeogeogr. Palaeoclimatol. Palaeoecol. 190, 139–164. Schroeder, W. W., Brooke, S. D., Olson, J. B., Phaneuf, B., McDonough, J. J., and Etnoyer, P. (2005). Occurrence of deep-water Lophelia pertusa and Madrepora oculata in the Gulf of Mexico. Cold-Water Corals and Ecosystems 297-307, 1243. Schuller, D., Kadko, D., and Smith, C. R. (2004). Use of 210Pb/226Ra disequilibria in the dating of deep-sea whale falls. Earth Planet. Sci. Lett. 218, 277–289. Sellanes, J., Quiroga, E., Neira, C., and Gutie´rrez, D. (2007). Changes of macrobenthos composition under different ENSO cycle conditions on the continental shelf off central Chile. Cont. Shelf Res. 27, 1002–1016. Shank, T. M., Fornari, D. J., Von Damm, K. L., Lilley, M. D., Haymon, R. M., and Lutz, R. A. (1998). Temporal and spatial patterns of biological community development at nascent deep-sea hydrothermal vent (9 500 N, East Pacific Rise). Deep Sea Res. Part II 45, 465–515. Shank, T., Fornari, D. J., Yoerger, D. R., Humphris, S. E., Bradley, A. L., Hammond, S., Lupton, J. E., Scheirer, D., Collier, R., Reysenbach, A. L., Ding, K., Seyfried, W. et al. (2003). Deep submergence synergy: Alvin and Abe explore the Galapagos Rift at 86 W EOS, Transactions, American Geophysical Union 84, 425-440. Shimanaga, M., Kitazato, H., and Shirayama, Y. (2000). Seasonal patterns of vertical distribution between meiofaunal groups in relation to phytodetritus deposition in bathyal Sagami Bay, central Japan. J. Oceanogr. 51, 379–387. Shimanaga, M., Kitazato, H., and Shirayama, Y. (2004). Temporal patterns in diversity and species composition of deep-sea benthic copepods in bathyal Sagami Bay, central Japan. Mar. Biol. 144, 1097–1110. Sibuet, M., and Olu, K. (1998). Biogeography, biodiversity and fluid dependence of deepsea cold-seep communities at active and passive margins. Deep Sea Res. Part II 45, 517–567. Sibuet, M., Lambert, C. E., Chesselet, R., and Laubier, L. (1989). Density of the major size groups of benthic fauna and trophic input in deep basins of the Atlantic Ocean. J. Mar. Res. 47, 851–867. Smart, C. W. (2008). Abyssal NE Atlantic benthic foraminifera during the last 15 kyr: Relation to variations in seasonality of productivity. Mar. Micropaleontol. 69, 193–211.

92

A. G. Glover et al.

Smith, C. R., Kukert, H., Wheatcroft, R. A., Jumars, P. A., and Deming, J. W. (1989). Vent fauna on whale remains. Nature 341, 27–28. Smith, C. R. (1994). Tempo and mode in deep-sea benthic ecology: Punctuated equilibrium revisited. Palaios 9, 3–13. Smith, C. R., Hoover, D. J., Doan, S. E., Pope, R. H., Demaster, D. J., Dobbs, F. C., and Altabet, M. A. (1996). Phytodetritus at the abyssal seafloor across 10 degrees of latitude in the central equatorial Pacific. Deep Sea Res. Part I 43, 1309–1338. Smith, C. R., and Baco, A. R. (2003). The ecology of whale falls at the deep-sea floor. Oceanogr. Mar. Biol. Annu. Rev. 41, 311–354. Smith, C. R., Mincks, S., and DeMaster, D. J. (2006a). A synthesis of bentho-pelagic coupling on the Antarctic shelf: Food banks, ecosystem inertia and global climate change. Deep Sea Res. Part II 53, 875–894. Smith, C. R., De Leo, F. C., Bernardino, A. F., Sweetman, A. K., and Martinez Arbizu, P. (2008a). Abyssal food limitation, ecosystem structure and climate change. Trends Ecol. Evol. 23, 518–528. Smith, C. R., Levin, L. A., Koslow, A., Tyler, P. A., and Glover, A. G. (2008c). The near future of deep sea floor ecosystems. In “Aquatic Ecosystems” (N. V. C. Polunin, ed.), pp. 334–349. Cambridge University Press. Smith, K. L. Jr., and Druffel, E. R. M. (1998). Long time-series studies of the benthic boundary layer at an abyssal station in the NE Pacific. Deep Sea Res. Part II 45, 573–586. Smith, K. L. Jr., and Kaufmann, R. S. (1999). Long-term discrepancy between food supply and demand in the deep eastern North Pacific. Science 284, 1174–1177. Smith, K. L., Kaufmann, R. S., Baldwin, R. J., and Carlucci, A. F. (2001). Pelagic–benthic coupling in the abyssal eastern North Pacific: An eight-year time-series study of food supply and demand. Limnol. Oceanogr. 46, 543–556. Smith, K. L., Baldwin, R. J., Ruhl, H. A., Kahru, M., Mitchell, B. G., and Kaufmann, R. S. (2006b). Climate effect on food supply to depths greater than 4000 meters in the northeast Pacific. Limnol. Oceanogr. 51, 166–176. Smith, K. L. Jr., Ruhl, H. A., Kaufmann, R. S., and Kahru, M. (2008b). Tracing abyssal food supply back to upper-ocean processes over a 17-year time series in the NE Pacific. Limnol. Oceanogr. 53, 2655–2667. Smith, K. L. Jr., Ruhl, H.A., Billett, D. S. M., Bett, B. J., Lampitt, R. S., and Kaufmann, R. S., (2009). Climate, carbon cycling and deep-ocean ecosystems. P. Natl. Acad. Sci. USA 46, 19211–19218. Smith, D. K., Escartin, J., Cannat, M., Tolstoy, M., Fox, C. G., Bohnenstiehl, D. R., and Bazin, S. (2003). Spatial and temporal distribution of seismicity along the northern MidAtlantic Ridge (15 degrees–35 degrees N). J. Geophys. Res. Solid Earth 108, (B3), 2167. Smith, W. O., Ainley, D. G., and Cattaneo-Vietti, R. (2007). Trophic interactions within the Ross Sea continental shelf ecosystem. Philos. Trans. R Soc. B 362, 95–111. Soltwedel, T., Bauerfeind, E., Bergmann, M., Budaeva, N., Hoste, E., Jaeckisch, N., von Juterzenka, K., Matthiessen, J., Mokievsky, V., No¨thig, E.-M., Que´ric, N.-V., Sablotny, B. et al. (2005a). HAUSGARTEN: Multidisciplinary Investigations at a Deep-Sea, Long-Term Observatory in the Arctic Ocean. Oceanography 18, 47–61. Soltwedel, T., Portnova, D., Kolar, I., Mokievsky, V., and Schewe, I. (2005b). The smallsized benthic biota of the Ha˚kon Mosby Mud Volcano (SW Barents Sea slope). J. Mar. Syst. 55, 271–290. Soto, E. H. (2008). Taxonomy and biology of deep-sea polychaetes: temporal variability in polychaete assemblages of the abyssal NE Atlantic Ocean. University of Southampton, Doctoral Thesis, 262pp. Soto, E. H., Paterson, G. L. J., Billett, D. S. M., Hawkins, L. E., Gale´ron, J., and Sibuet, M., (2010). Temporal variability in polychaete assemblages of the abyssal NE Atlantic Ocean. Deep Sea Res. Part II, 57, 1396–1405.

Temporal Change in Deep-Sea Ecosystems

93

Southward, A. J., Langmead, O., Hardman-Mountford, N. J., Aiken, J., Boalch, G. T., Dando, P. R., Genner, M. J., Joint, I., Kendall, M. A., Halliday, N. C., Harris, R. P., Leaper, R. et al. (2005). Long-term oceanographic and ecological research in the western English Channel. Adv. Mar. Biol. 47, 1–105. Sumida, P. Y. G., Bernardino, A. F., Smith, C. R., and Stedall, V. (2008). Temporal changes in benthic megafauna composition and abundance across the West Antarctic Peninsula shelf: Results from video surveys. Deep Sea Res. Part II 55, 2465–2477. Thatje, S., Anger, K., Calcagno, J. A., Lovrich, G. A., Portner, H. O., and Arntz, W. E. (2005). Challenging the cold: Crabs reconquer the Antarctic. Ecology 86, 619–625. Theocharis, A., Balopoulos, E., Kioroglou, S., Kontoyiannis, H., and Iona, A. (1999). A synthesis of the circulation and hydrography of the South Aegean Sea and the Straits of the Cretan Arc (March 1994–January 1995). Prog. Oceanogr. 44, 469–509. Thie´baut, E., Huther, X., Shillito, B., Jollivet, D., and Gaill, F. (2002). Spatial and temporal variations of recruitment in the tube worm Riftia pachyptila on the East Pacific Rise (9 500 N and 13 N). Mar. Ecol. Prog. Ser. 234, 147–157. Thiel, H. (1979). Structural aspects of the deep-sea benthos. Ambio Special Report 6, 25–31. Thiel, H. (2003). Anthropogenic impacts on the deep sea. In “Ecosystems of the World 28. Ecosystems of the Deep Ocean” (P. A. Tyler, ed.), pp. 427–471. Elsevier, Amsterdam, Boston, London, New York, Oxford, Paris, San Diego, San Francisco, Singapore, Sydney, Tokyo. Thiel, H., Pfannkuche, O., Schriever, G., Lochte, K., Gooday, A. J., Hemleben, Ch., Mantoura, R. F. C., Turley, C. M., Patching, J. W., and Riemann, F. (1989). Phytodetritus on the deep-sea floor in a central oceanic region of the Northeast Atlantic. Biol. Oceanogr. 6, 203–239. Thistle, D., Ertman, S. C., and Fauchald, K. (1991). The fauna of the HEBBLE site: Patterns in standing stock and sediment-dynamic effects. Mar. Geol. 99, 413–422. Thomas, E. (1990). Late Cretaceous-early Eocene mass extinctions in the deep sea. In ‘Global Catastrophes’. Geol. Soc. Am. Spec. Publ. 247, 481–496. Thomas, E. (2007). Cenozoic mass extinctions in the deep sea: What perturbs the largest habitat on Earth? In “Large Ecosystem Perturbations: Causes and Consequences” (S. Monechi, R. Coccioni and M. R. Rampino, eds.), Geological Society of America Special Paper 424. pp. 1–23. Thomas, E., and Gooday, A. J. (1996). Cenozoic deep-sea benthic foraminifera: Tracers for changes in oceanic productivity. Geology 24, 355–358. Thurston, M. H., Bett, B. J., Rice, A. L., and Jackson, P. A. B. (1994). Variations in the invertebrate abyssal megafauna in the North Atlantic Ocean. Deep Sea Res. Part I 41, 1321–1348. Torres, M. E., Barry, J. P., Hubbard, D. A., and Suess, E. (2001). Reconstructing the history of fluid flow at cold seep sites from Ba/Ca ratios in vesicomyid clam shells. Limnol. Oceanogr. 46, 1701–1708. Tselepides, A., and Lampadariou, N. (2004). Deep-sea meiofaunal community structure in the Eastern Mediterranean: Are trenches benthic hotspots? Deep Sea Res. Part I 51, 833–847. Tselepides, A., Akoumianaki, I., and Polychronaki, T. (2000). Organic matter variability in sediments of the Aegean Sea. In “Proceedings of the 6th Hellenic Symposium on Oceanography and Fisheries, Chios,” pp. 265–269. Tselepides, A., Lampadariou, N., and Polymenakou, P. N. (2007). Benthic community structure and function of the deep eastern Mediterranean Sea. Rapp. Comm. Int. Mer. Medit. 38, 1. Tsurumi, M., and Tunnicliffe, V. (2001). Characteristics of a hydrothermal vent assemblage on a volcanically active segment of Juan De Fuca Ridge, Northeast Pacific. Can. J. Fish. Aquat. Sci. 58, 530–542.

94

A. G. Glover et al.

Tsurumi, M., and Tunnicliffe, V. (2003). Tubeworm-associated communities at hydrothermal vents on the Juan de Fuca Ridge, Northeast Pacific. Deep Sea Res. Part I 50, 611–629. Tsurumi, M., Marcus, J., and Tunnicliffe, V. (1998). Destruction and rebirth of the hydrothermal vent animal communities on axial volcano EOS, Transactions American Geophysical Union, Juan de Fuca Ridge79(45): F923 (Abstract). Tunnicliffe, V. (1990). Observations on the effects of sampling on hydrothermal vent habitat and fauna of Axial Seamount, Juan-De-Fuca Ridge. J. Geophys. Res. Solid Earth Planets 95, 12961–12966. Tunnicliffe, V. (1991). The biology of hydrothermal vents—Ecology and evolution. Oceanogr. Mar. Biol. 29, 319–407. Tunnicliffe, V., Garrett, J. F., and Johnson, H. P. (1990). Physical and biological factors affecting the behavior and mortality of hydrothermal vent tubeworms (Vestimentiferans). Deep Sea Res. 37, 103–125. Tunnicliffe, V., Embley, R. W., Holden, J. F., Butterfield, D. A., Massoth, G. J., and Juniper, S. K. (1997). Biological colonization of new hydrothermal vents following an eruption on Juan De Fuca Ridge. Deep Sea Res. Part I 44, 1627–1644. Tyler, P. A. (1988). Seasonality in the deep sea. Oceanogr. Mar. Biol.: An Annu. Rev. 26, 227–258. Tyler, P. A., and Dixon, D. R. (2000). Temperature/pressure tolerance of the first larval stage of Mirocaris fortunata from Lucky Strike hydrothermal vent field. J. Mar. Biol. Assoc. UK 80, 739–740. Tyler, P. A., and Gage, J. D. (1980). Reporduction and growth of the deep-sea brittlestar Ohiura ljungmani (Lyman). Oceanol. Acta 3, 177–185. Tyler, P. A., and Young, C. M. (1998). Temperature and pressure tolerances in dispersal stages of the genus Echinus (Echinodermata: Echinoidea): Prerequisites for deep-sea invasion and speciation. Deep Sea Res. Part I 45, 253–277. Tyler, P. A., and Young, C. M. (1999). Reproduction and dispersal at vents and cold seeps. J. Mar. Biol. Assoc. UK 79, 193–208. Tyler, P., Amaro, T., Arzola, R., Cuhna, M. R., De Stigter, H., Gooday, A., Huvenne, V., Ingels, J., Kiriakoulakis, K., Lastras, G., Masson, D., Oliveira, A. et al. (2009). Europe’s Grand Canyon: Nazare´ submarine canyon. Oceanography 22, 46–47. Tyler, P. A., Grant, A., Pain, S. L., and Gage, J. D. (1982). Is annual reproduction in deepsea echinoderms a response to variability in their environment? Nature 300, 747–750. Urcuyo, I., and Massoth, G. (2003). Habitat, growth and physiological ecology of a basaltic community of Ridgeia piscesae from the Juan de Fuca Ridge. Deep Sea Res. Part I 50, 763–780. Vacelet, J. (1996). Deep-sea sponges in a Mediterranean cave. In “Deep-Sea and Extreme Shallow-Water Habitats: Affinities and Adaptations” (F. Uiblein, J. Ott and M. Stachowitsch, eds.), pp. 299–312. Vienna, Austrian Academy of Science. Vacelet, J., Boury-Esnault, N., and Harmelin, J. C. (1994). Hexactinellid Cave, a unique deep-sea habitat in the scuba zone. Deep Sea Res. Part I 41, 965–973. Van Dover, C. L. (2000). The Ecology of Deep-Sea Hydrothermal Vents. Princeton University Press, Princeton New Jersey. Van Dover, C. L. (2002). Community structure of mussel beds at deep-sea hydrothermal vents. Mar. Ecol. Prog. Ser. 230, 137–158. Vanreusel, A., Cosson-Sarradin, N., Gooday, A. J., Paterson, G. L. J., Galeron, J., Sibuet, M., and Vincx, M. (2001). Evidence for episodic recruitment in a small opheliid polychaete species from the abyssal NE Atlantic. Prog. Oceanogr. 50, 285–301. Vanreusel, A., Andersen, A. C., Boetius, A., Connelly, D., Cunha, M. R., Decker, C., Hilario, A., Kormas, K. A., Maignien, L., Olu, K., Pachiadaki, M., Ritt, B. et al. (2009). Biodiversity of cold seep ecosystems along European margins. Oceanography 22, 110–127.

Temporal Change in Deep-Sea Ecosystems

95

Vardaro, M. F., Ruhl, H. A., Smith, K. L. (2009). Climate variation, carbon flux, and bioturbation in the abyssal North Pacific. Limnol. Oceanogr. 54, 2081–2088. Von Damm, K. L. (1995). Controls on the chemistry and temporal variability of seafloor hydrothermal fluids. In “Physical, Chemical, Biological, and Geological Interactions within Seafloor Hydrothermal Systems” ( J. Lupton, L. Mullineaux and R. Zierenberg, eds.), Geophysical Monograph. 91, pp. 222–247. AGU. Von Damm, K. L., Bray, A. M., Buttermore, L. G. et al. (1998). The geochemical controls on vent fluids from the Lucky Strike vent field, Mid-Atlantic Ridge. Earth Planet. Sci. Lett. 160, 521–536. Von Rad, U., Schulz, H., Riech, V., Den Dulk, M., Berner, U., and Sirocko, F. (1999). Multiple monsoon-controlled breakdown of oxygen-minimum conditions during the past 30, 000 years documented in laminated sediments off Pakistan. Palaeogeogr. Palaeoclimatol. Palaeoecol. 152, 129–161. Wagner, H. J., Kemp, K., Mattheus, U., and Priede, I. G. (2007). Rhythms at the bottom of the deep sea: Cyclic current flow changes and melatonin patterns in two species of demersal fish. Deep Sea Res. Part I 54, 1944–1956. Weikert, H., Koppelmann, R., and Wiegratz, S. (2001). Evidence of episodic changes in deep-sea mesozooplankton abundance and composition in the Levantine Sea (Eastern Mediterranean). J. Mar. Syst. 30, 221–239. Wichers, S., Sohn, R. S., and Terray, G. (2005). New constraints on the thermal power of the TAG hydrothermal system and the dynamics of the water column plume. EOS, Transactions of the American Geophysical Union, 86, Fall Meeting Supplement, Abstract OS33A-1466. Wigham, B. D., Hudson, I. R., Billett, D. S. M., and Wolff, G. A. (2003). Is long-term change in the abyssal Northeast Atlantic driven by qualitative changes in export flux? Evidence from selective feeding in deep-sea holothurians. Prog. Oceanogr. 59, 409–441. Wiklund, H., Glover, A. G., Johannessen, P. J., and Dahlgren, T. G. (2009). Cryptic speciation at organic-rich marine habitats: a new bacteriovore annelid from whale-fall and fish farms in the North-East Atlantic. Zool. J. Linn. Soc. 155, 774 –785. Worm, B., Barbier, E. B., Beaumont, N., Emmett Duffy, J. E., Folke, C., Halpern, B. S., Jackson, J. B. C., Lotze, H. K., Micheli, F., Palumbi, S. R., Sala, E., Selkoe, K. A., et al. (2006). Impacts of Biodiversity Loss on Ocean Ecosystem Services. Science 314, 787–790. Yasuhara, M., and Cronin, T. M. (2008). Climatic influences on deep-sea ostracode (Crustacea) diversity for the last three million years. Ecology 89, (Supplement), S53–S65. Yasuhara, M., Hunt, G., Cronin, T. M., and Okahashi, H. (2009). Temporal latitudinalgradient dynamics and tropical instability of deep-sea species diversity. Proc. Natl. Acad. Sci. USA. 106, 21717–21720.

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The Biology and Fisheries of European Hake, Merluccius merluccius, in the North-East Atlantic Hilario Murua

Contents 98 98 100 108 112 112 112 113 120 121 124 135 135 136 139 142 144 144

1. Introduction 1.1. Classification and the origin of ‘hake’ 1.2. Phylogeny and biogeography of hake 1.3. Fisheries and the importance of hake 2. European Hake, Merluccius merluccius 2.1. Taxonomy and identification 2.2. Distribution and habitat 2.3. General hydrography of the area 2.4. Growth 2.5. Feeding 2.6. Reproduction and recruitment 3. Fisheries and the State of the Population 3.1. Population structure in the north-east Atlantic 3.2. The northern stock 3.3. The southern stock 4. Future Perspectives Acknowledgements References

Abstract The aim of this chapter is to review the biology and fishery, including the management, of European hake in the north-east Atlantic. The European hake is widely distributed throughout the north-east Atlantic, from Norway in the north to the Guinea Gulf in the south, and throughout the Mediterranean and Black Sea, being more abundant from the British Isles to the south of Spain. In this area, ICES (International Council for the Exploration of the Sea) recognises the existence of two stocks: the northern stock and the southern stock. Both stocks have been extensively and intensively harvested and since the beginning AZTI Tecnalia, Herrerra Kaia, Portualde z/g, Pasaia (Basque Country), Spain Advances in Marine Biology, Volume 58 ISSN 0065-2881, DOI: 10.1016/S0065-2881(10)58002-7

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of the 90s have been considered to be outside safe biological limits. The northern stock, however, is currently considered to lie within safe biological limits. In any case, recovery plans were implemented for the northern stock in 2004 and for the southern stock in 2006. Despite its commercial importance, knowledge of the biology and ecology of the European hake in the North Atlantic is still quite scarce. For example, recent investigations suggest that European hake grows much faster, by a factor of two, than was considered previously. This faster growth also affects the maturity-at-age pattern of hake and the agreed maturity-at-age ogive used in the assessments. European hake is a top predator in the demersal community in the north-east Atlantic area; mainly preying on blue whiting, horse mackerel and other cupleids. In relation to the reproductive biology, European hake is considered to be a batch spawner species with indeterminate fecundity and spawning activity all year round. All these characteristics could, in turn, be interpreted as European hake adopting a more opportunistic life strategy, which is unusual for a gadoid and demersal species, and raises several questions about hake biology and ecology that require further investigation.

1. Introduction 1.1. Classification and the origin of ‘hake’ According to the American Heritage Dictionary of the English Language, the word ‘hake’ originated from the Old or Middle English word ‘haca’; this means ‘hook’, and defines the form of the shape of its lower jaw. The term ‘hake’ mainly refers to fish of the genera Merluccius, although other cod-like fish are also known as hake, for example, fishes of the genera Urophycis (Flick et al., 1990; Pitcher and Alheit, 1995). The first reference to fish of the actual genera Merluccius is found in the book De aquatibus by Belon (1553), where a fish of the name ‘Marlutiu vulgari’ was described. The origin of the name Merluccius came from the Latin name ‘Marlutiu’ and was described by Belon, who denominated the fish, actually known as Merluccius merluccius, as ‘Marlutiu’—Maris lucium— (Mar: sea; lutiu: pike), due to its similar appearance to pike (Fig. 2.1). In the ‘Sistema Naturae’, the binomial system of nomenclature developed in the mid 1700s by Carlo Linnaus, ‘Marlutio vulgari’ was described and classified as Gadus merluccius; this was included within the Family Gadidae and the genus Gadus, which is closely related to other cod species. This species was raised to the rank of genus by Rafinesque (1810), who first described the genus Merluccius based upon the type species M. smiridus (the actual M. merluccius) inhabiting the north-east Atlantic. The type species used to describe the genus Merluccius for the first time was the same fish first described by Belon (1553), that is, Marlutio vulgari.

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Figure 2.1 Figure of Marlutio vulgari first described in the book De Aquatibus by Belon (1553). Reproduced with the permission of Goettingen State and University Library as the holder of the original De Aquatibus—Belon (1553).

However, at that time, all the known species of the genus Merluccius were included within the Family Gadidae; they were raised to the rank of Family and included in the family Merlucciidae by Adams (1864). The characteristics of the Family Merlucciidae were described by Gill (1884) as ‘Gadidae with a moderate caudal region coniform behind and with the caudal rays procurrent forward, the anus sub-median, moderate sub-orbital bones, terminal mouth, sub-jugular ventrals; dorsal double, a short anterior and long posterior one, a long anal corresponding to the second dorsal; ribs wide, approximated and channeled below or with inflected sides and paired excavated frontal bones with divergent crests continuous from the forked occipital crest’. In recent times, Cohen et al. (1990) included four genera in the Family Merluccidae: the abovementioned Merluccius (Rafinesque, 1810), Macruronus (Gu¨nther, 1873), Lyconus (Gu¨nther, 1887) and Steindachneria (Goode and Bean, 1896). The first three belong to the sub-Family Merlucciinae, with the last under the sub-Family Steindachneriinae. In contrast, Lloris et al. (2003) presented a different classification, where the Family Merlucciidae was divided into five genera (Merluccius, Macruronus, Lyconus, Lyconodes and Steindachneria) included in three sub-Families (Merlucciinae, Macruroninae and Steindachneriinae). The differences in the latter approach are that a new sub-Family is described (Macruroninae) which included three genera (Lyconus, Lyconodes and Macruronus); furthermore, only the genus Merluccius belonged to the sub-Family Merlucciinae. Nevertheless, the evolutionary status of the Family Merlucciidae is still a subject of debate among fish taxonomists in relation to the extent of the Family or the phylogenic

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relationships between different genera of the Family, or the inclusion, or not, within the Family Gadidae. Regardless of such past and ongoing extensive debates, that is, to provide Merlucciidae with a Family status or locate it under the Family Gadidae, most authors give a Family rank to Merluccidae, including the genus Merluccius within this Family. In fact, there are 13 recognised species of the genus Merluccius, which makes it the most diverse genus within the Merlucciidae Family (Table 2.1). Apart from the 13 recognised species, Mathews (1985) postulated a new species, M. hernandezi, separated from M. angustimanus. However, most recent authors considered this species as a sub-population of M. angustimanus (Lloris et al., 2003). The distribution of the extant species of the genus Merluccius is very broad, spanning the continental shelves and slopes of most of the world’s temperate and subtropical regions (Cohen et al., 1990). They are distributed throughout both sides of the Atlantic, along the north-eastern and southeastern, and north-western and south-western Atlantic, the Mediterranean Sea and the Red Sea; along the eastern Pacific Ocean and off southern New Zealand. There have also been isolated observations in the Indian Ocean off the south and south-east of Madagascar (Lloris et al., 2003; Fig. 2.2). The distribution of extant hake occurs in both the northern and southern hemisphere, showing an antitropical distribution (Grant and Leslie, 2001).

1.2. Phylogeny and biogeography of hake Although there is not yet a general consensus, various hypotheses have been proposed in relation to the phylogeny and biogeography of hake. The hypotheses presented up until now were based upon studies using different approaches, such as ichthyological information (Inada, 1981), parasitological information (Ferna´ndez, 1985; Kabata and Ho, 1981; Szidat, 1955), cladistic analysis (Ho, 1990) and the most recent ones based upon genetic studies (Grant and Leslie, 2001; Quinteiro et al., 2000; Rolda´n et al., 1999; Stepien and Rosenblatt, 1996). Most of the authors proposed a north-eastern Atlantic ancestor for the genus Merluccius; this diverged into two major Merluccius lineages which evolved independently: one along the west coast of Europe and the other along the east coast of America to the Pacific, through the Panama seaway. However, there were some major discrepancies between the different views in relation to the evolution of these two major lineages. The exceptions to this general theory were proposed by Szidat (1955, 1961) and Ho (1974, 1990). For example, based upon the distribution of hake parasites, Szidat (1955, 1961) suggested a north Pacific origin, whereas Ho (1974) proposed a western Atlantic origin for Merluccius species. In contrast to latter proposals, Inada (1981) and Kabata and Ho (1981) proposed two different hypotheses for the origin and biogeography of hake;

Table 2.1 Actually recognised species of the genus Merluccius, their distribution as well as the common name Scientific name

Described by

Common name

Distribution

Merluccius albidus

Mitchill (1818)

Offshore hake

Merluccius angustimanus Merluccius australis

Garman (1899) Hutton (1872)

Merluccius bilinearis Merluccius capensis

Mitchill (1814) Castelnau (1861)

Merluccius gayi

Guichenot (1848)

Merluccius hubbsi Merluccius merluccius Merluccius paradoxus

Marini (1933) Linnaeus (1758) Franca (1960)

Merluccius patagonicus Merluccius polli Merluccius productus

Lloris and Matallanas (2003) Cadenat (1950) Ayres (1855)

Panama hake Southern hake Austral hake Antarctic queen hake New Zeeland hake Silver hake Cape hake Shallow-water hake Chilean hake Peruvian hake Argentine hake European hake Deepwater Cape hake Deepwater hake Patagonian hake

North-west, Central-west 20–35 N Atlantic North-Central east Pacific 5–23 N South-east and South-west Pacific South of 51 S 40–57 S South of 40 S North-west Atlantic 36–47 N South-east Atlantic 0–34 S

Merluccius senegalensis

Cadenat (1950)

Benguela hake Merluza norten˜a North Pacific hake Pacific hake Pacific whiting Senegalese hake

Latitude

South-west Atlantic North-east Atlantic South-east Atlantic

23–47 S 3–10 S 25–54 S 21–62 N South of 22 S

South-west Atlantic

45–49 S

South-east Atlantic North-east Pacific

20 N–19 S 25–51 N

South-east Atlantic

10–33 N

South-east Pacific

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60°N

Bilinearis Merluccius

Productus

Albidus Magnoculus Senegalensis

Hernandezi Angustimanus

30°N

Cadenati

0° Polli

Gayi peruanus

Indian Ocean

Capensis

Pacific Ocean

30°S

Gayi gayi Hubbsi Polylepis

Paradoxus

Atlantic Ocean

Australis

60°S

Figure 2.2 Geographical distribution of hakes (genus Merluccius); reproduced from Grant and Leslie (2001).

these were similar in the major points of discussion. For example, both views postulated an eastern North Atlantic origin of hake, with M. merluccius considered as the most ancestral; this was followed by a southward dispersal in two directions (see above). Hake entered the Pacific through the Panama seaway, before the formation of the Panama Isthmus. However, these authors did not agree in relation to the origin of the Argentine hake M. hubbsi. Inada (1981) suggested a south-western Pacific origin for Argentine hake around Cape Horn, whereas Kabata and Ho (1981) proposed that Argentine hake were derived from the western North Atlantic; this was based upon the dissimilarities between Argentine hake and Pacific hake parasites. Other studies utilising the distribution of parasites approach were in agreement with the conclusion of Kabata and Ho (Ferna´ndez, 1985). More recently, Ho (1990) undertook a revision of Inada’s study using cladistic analysis; this model suggested a western North Atlantic origin of hake, with M. albidus being the most ancestral hake species. This ancestral species vicariated in two lineages; one following a northwards dispersal, forming the north-western Atlantic and Pacific species, and the another migrating along South America and then dispersing eastwards across the tropical Atlantic to Africa, whose descendants gave rise to all extant hake in the western South Atlantic and the eastern Atlantic. In contrast to the findings of Inada (1981) and Kabata and Ho (1981), the phylogenic results of Ho (1990) considered M. merluccius as the most recent species and therefore, it could not be considered as the ancestral species. Moreover, Ho (1990) agreed with the postulated western North Atlantic origin of Argentine hake by Kabata and Ho (1981), but differed with the postulated derivation from the eastern South Pacific (Inada, 1981).

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Furthermore, Rolda´n et al. (1999), in a similar way to Ho (1990), based on genetic studies of nine out of the 13 recognised species, concluded that M. merluccius is the most recent derivation of the Euro-African species. As such, these authors supported an eastern Atlantic warm-water origin, beyond the eastern North Atlantic origin postulated by Inada (1981) and Kabata and Ho (1981). However, the findings of Rolda´n et al. (1999) disagreed with Ho’s proposed origin (1990) of the genus within western Atlantic warm waters; this was because they postulated that M. polli and M. paradoxus in the eastern Atlantic as the descendants of an early OldWorld Merluccius. On the contrary, Ho (1990) considered M. albidus as the direct descendant of hake ancestors. Recently, Grant and Leslie (2001) presented a comprehensive genetic study with regard to the origin and biogeography of hake. New genetic data were presented, as well as the revision of data published by Rolda´n et al. (1999), Stepien and Rosenblatt (1996) and Quinteiro et al. (2000). Figure 2.3 of Grant and Leslie (2001) shows hake phylogenic tree summarising their phylogenetic and biogeography hypothesis. In agreement with previous authors, Grant and Leslie (2001) proposed a fundamental subdivision between Euro-African and American (including South Pacific) hake species, identifying them as Old-World and New-World taxa, respectively. This proposed division would have occurred in the Miocene

Paradoxus Polli Cadenati Merluccius Senegalensis Capensis Bilinearis Hubbsi Magnoculus Albidus Productus

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Figure 2.3 Phylogenetic hypothesis of hakes (genus Merluccius) based on all available data (Grant and Leslie, 2001; Rolda´n et al., 1999; Stepien and Rosenblatt, 1996; reproduced from Grant and Leslie, 2001).

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10–15 Ma (million years ago). Furthermore, these authors divided the OldWorld species into two sub-groups: M. Paradoxus, M. polli and M. cadenati formed one group, whereas M. merluccius, M. senegalensis and M. capensis belonged to the second group. This division supported the findings of Rolda´n et al. (1999). With regard to the relationships between the NewWorld species, these investigations reported that M. bilinearis is the most distant species, or the first descendant of the ancestor of the New-World species, followed by M. hubbsi and M. albidus. The rest of the four main species (M. gayi, M. productus, M. polylepis and M. australis) formed a group of derived species, with the first two and last two being sister species, respectively. A similar phylogenetic tree, with respect to the New-World species, was also found by Rolda´n et al. (1999). The phylogenetic tree, in which all the taxa are identified and positioned in a hierarchical system of sister species, is a necessary step towards creating robust biogeographical models. Grant and Leslie (2001) postulated the most recent, and probably the most plausible, biogeographical hypothesis for the origin of hake by using such a phylogenetic tree. In agreement with most of the authors, they proposed a north-eastern Atlantic origin of hake, where the shallow epicontinental seas between Europe and Asia were occupied by ancestral Merluccius. Evidence of a north-eastern Atlantic-Arctic origin of the genus Merluccius was provided when fossils of Merluccius appeared in Middle and Upper Oligocene sediments in Europe (Fedotov, 1976; Inada, 1981; Kabata and Ho, 1981; Svetovidov, 1948). In other words, these authors hypothesised a North Atlantic origin of hake ancestors which gave rise to the lineages of the Old- and New-World hake. The results of Grant and Leslie (2001) are in agreement with most of the biogeographical models, such as those of Kabata and Ho (1981), Inada (1981) and Ferna´ndez (1985); whereas they are in disagreement with those of Szidat (1961), Ho (1990) and Rolda´n et al. (1999). Nevertheless, the genetic evidence, in addition to the European fossil record for hake, places the balance of evidence in favour of a North Atlantic origin of hakes. Grant and Leslie (2001) postulated different tectonic and oceanic events to explain the divergence of hake ancestors into two different lineages, that is, the eastern Atlantic or Old-World hake and the western Atlantic-Pacific or New-World hake. On the one hand, there was the separation of the tectonic plates of Europe and North America and the subsequent expansion of the North Atlantic basin (Van Andel, 1976), and on the other, there was the cooling of North Atlantic waters which started in the Oligocene and finished in the mid-Miocene, around 15 Ma (Savin et al., 1975). The cooling of continental waters acted as a precursor for the southwards migration of the ancestral hake distribution, along the western and eastern Atlantic; this was facilitated by the expansion of the North Atlantic basin (Grant and Leslie, 2001; Fig. 2.4).

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A

Europe

B

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North America

mer bil Atlantic Ocean

Africa

South America Oligocene

Miocene

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Figure 2.4 Theory for the initial separation of the hake ancestor in two different lineages, that is, Old- and New-world hakes (reproduced from Grant and Leslie, 2001).

Contrary to the publications of Kabata and Ho (1981) and Inada (1981), who suggested that African hake species originated from the north-eastern Atlantic ancestors as the hake moved southwards, Grant and Leslie (2001) proposed two different lineages within European and African hake; this was based upon their phylogenic tree of sister taxa and two different radiations of ancestral M. merluccius. In the first radiation, during the mid-Miocene and around 10–15 Ma, an early M. paradoxus was established; it dispersed northwards to form the population of M. cadenati in the late Miocene or early Pliocene. From this population, a recent southerly displacement led to the origination of the last species of the ‘paradoxus’ lineage (M. polli) (Fig. 2.5). In the second radiation, the ancestral M. merluccius spread southwards to form the cape hake, M. capensis, which later back distributed northwards to give rise to M. senegalensis around 2 Ma (the ‘capensis’ lineage). The origin and dispersal of the American hake species, as presented by Grant and Leslie (2001), are similar to the zoogeographical models presented by previous authors (Ho, 1990; Inada, 1981; Kabata and Ho, 1981; Rolda´n et al., 1999). With the exception of Kabata and Ho (1981), who considered M. albidus the ancestor of all extant hake, all of these investigations considered M. bilinearis as inhabiting the north-western Atlantic and being the most ancient precursor of the New-World hake species. Regardless of which species was the ancestor, all of the authors proposed that the ancestor of American hake moved through the submerged Panamanian Isthmus in the mid-to-late Miocene to establish the eastern Pacific species (M. gayi, M. productus, M. albidus and M. angustimanus); this was before the closure of the Panamanian Isthmus around 3.5 Ma (Keigwin, 1978, 1982). However, Grant and Leslie (2001) proposed a slightly different scenario, whereby the ancestor M. bilinearis gave rise to M. productus, M. gayi and M. albidus, and then M. gayi subsequently became the ancestor of M. angustimanus, moving back towards the north (Fig. 2.6).

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Figure 2.5 Geographical reproduction of the dispersal of hake ancestor in the North-east Atlantic postulated by Grant and Leslie (2001): the ‘paradoxus’ lineage (left) and the ‘capensis’ lineage (right) (reproduced from Grant and Leslie, 2001).

60°N

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Figure 2.6 Geographical reproduction of the most recent description of ancestral Atlantic hake dispersal into the eastern Pacific Ocean (reproduced from Grant and Leslie, 2001).

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The main discrepancies between the different authors are centred around the interpretation of the origin of (i) the Argentine hake and (ii) the Australian and South Pacific hake. For example, Kabata and Ho (1981) and Ho (1990) postulated a North Atlantic origin for the Argentine hake, whereas Inada (1981), Stepien and Rosenblatt (1996), Rolda´n et al. (1999), Quinteiro et al. (2000) and Grant and Leslie (2001) suggested a South Pacific origin, around Cape Horn. Genetic evidence recently presented by authors has shown that M. hubbsi and M. bilinearis are the most distant species within phylogenetic trees; as such, the scenario of a North Atlantic origin is improbable. Inada (1981) proposed a South African origin for the Australian lineage. In contrast, Kabata and Ho (1981) and Ho (1990) suggested an Argentine origin for Australian hake due to the southwards dispersal of M. hubbsi, whereas Rolda´n et al. (1999) and Grant and Leslie (2001) postulated that M. gayi was the ancestor of the Australian lineage. Moreover, these latter authors suggested that M. polylepis in South America was established after the return dispersal of M. australis (Fig. 2.6). In summary, most of the authors agreed on a north-eastern origin of hake, with M. merluccius being the most ancestral of the extant hake species, which gave rise to two major lineages: one which formed all of the northeastern Atlantic species and the other which migrated westwards through the North Atlantic to diverge into the north-west Atlantic and Pacific lineages.

1.3. Fisheries and the importance of hake Although the earliest documentation of hake catches dates back to the eighteenth century (Casey and Pereiro, 1995) and contrary to other gadoids such as cod and haddock which supported one of the world’s great fisheries for centuries (Boreman et al., 1997), the large-scale hake fishery only began during the first half of the twentieth century. This fishery developed because of two major events: (i) the technological development of fishing fleets and (ii) the collapse of major cod stocks (Pitcher and Alheit, 1995). During the last half of the twentieth century and the beginning of the twenty-first century, hake were heavily exploited on a global basis. According to FAO statistics (FAO, 2010), the annual world catch of hake increased sharply from around an average of 400,000 tonnes at the beginning of 1960 up to levels of 700,000 and 1 million tonnes in 1963 and 1965, respectively. Catches continued to increase, with the exception of some years, to reach the maximum historic level of 2.2 million tonnes in 1973. Catches then steadily decreased to the levels observed in the mid-sixties and remained at that level of 1.1 million tonnes in the period of 1980–1984. More recently, annual total catches have fluctuated around 1 and 1.5 million tonnes, showing an increasing trend during some periods, whereas they showed a decreasing trend in others. For example, annual catches fluctuated around

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Total catches of Merluccius spp. and total catches by areas (source: FAO).

1.5 million tonnes in the periods of 1986–1990 and 1994–1999, to about 1.2 million tonnes in the period of 1991–1993 and of 2000–2003 (Fig. 2.7). In 2004 and 2005, catches were around 1.5 million tonnes and decreased again to around 1.2 million tonnes during the most recent period 2006–2008, although the catch figures for the last two years are still considered provisional. The catch of hake in the Atlantic, especially the eastern Atlantic catches, have accounted for the major proportion of the total catch. However, there is an increasing trend in the percentage of hake caught in the Pacific in relation to the total catch, whereas the inverse trend can be observed in catches from eastern Atlantic (Fig. 2.8). The trend in the global hake catch follows a similar trend to that of the eastern Atlantic trend over most of this period; however, the contribution of the eastern Atlantic catch from 1990 onwards has decreased. During the last decade of the twentieth century, the western Atlantic catch contributed the most to the total catch, whereas during 1999–2008, the eastern Pacific hake contributed greatly to the global catch (Fig. 2.8). During the last few years, while the contribution to the total catch of the eastern Pacific was around 40%, the contribution from the eastern and western Atlantic stayed around 30%. The contribution by each species of hake within each of the abovementioned areas to the global catch is shown in Fig. 2.9. In the eastern Atlantic (Fig. 2.9A), from 1950 to 1965, most of the catches consisted of European hake. However, from 1966 onwards, Cape hake was dominant in captures from the eastern Atlantic due to the development of a large fishery for Cape hake (Payne and Punt, 1995). On the other side of the Atlantic (Fig. 9B), silver hake dominated the catches obtained up to 1966 when the

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100% Contribution to total catch

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Figure 2.8

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The contribution to total catches by area (source: FAO).

highest catches of this species were recorded (Helser et al., 1995). Although Argentine hake catches were higher than silver hake in 1967 and 1968, most of the catches of hake in the western Atlantic were comprised of silver hake up until 1975. Argentine hake became increasingly more important from that year onwards with the development of a new offshore fishery (Bezzi et al., 1995), and since the 1990s, more than 90% of the western Atlantic catch has comprised Argentine hake. Finally, in the Pacific (Fig. 2.9C), all catches consisted of Southern Pacific hake up to the development of the Northern Pacific and southern hake fisheries in 1966 and in 1979, respectively (Colman, 1995; Methot and Dorn, 1995). Since then, the contributions by Northern and Southern Pacific hake have fluctuated between 25 and 50% each, whereas the contribution by southern hake has stayed around 15–20%. From 2004 onwards, the contribution by Northern Pacific hake has been around 70%, whereas the contribution by Southern Pacific hake and southern hake has been around 20% and 10%, respectively. Hake constitutes a high-quality fisheries product, although quality and price in the market vary depending upon the species. In the past, most of the hake catch outside of Europe was used for fishmeal production, or animal food; nowadays, most of the hake market is for human consumption (Pitcher and Alheit, 1995). For example, because of its excellent culinary characteristics, it is recommended that European hake and Austral hake are marketed as whole fresh or frozen fish (Lloris et al., 2003). Europe, especially Spain, constitutes the major market for hake in the world, where they import around 700,000 tonnes annually.

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Figure 2.9 Contribution to each species to the total catch of the corresponding area: (A) East Atlantic area; (B) West Atlantic area and (C) Pacific area (source: FAO).

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Figure 2.10 European hake, Merluccius merluccius (AZTI Tecnalia).

2. European Hake, Merluccius merluccius 2.1. Taxonomy and identification In comparison to other Merluccius species, the European hake is characterised by a long slim body (Fig. 2.10). The head is large, being about 25–30% of the body length: the snout and upper jaw are about 30–35% and 48–54% of the head length, respectively (Inada, 1990). The ocular diameter is around 16–21% and the inter-orbital space 22–28% of the head length (Lloris et al., 2003). The total number of grill rakers varies: on the first arch, it can be between 8 and 11 (mostly 9–11), ranging from 1 to 3 on the upper part and from 7 to 9 on the lower part. The first dorsal fin contains 1 spine and 7/10 rays, whilst the second dorsal and anal fins have 36–40 rays. The tip of the pectoral fins reaches the anal opening in fish below the 20 cm standard length, but not in adults. The margin of the caudal fin is normally truncated, but becomes forked with growth. The lateral line contains 127–156 small scales. The total number of vertebrae is 49–54. The colouration of the European hake is grey, in general, becoming lighter on the sides and silvery white on the belly (Cohen et al., 1990).

2.2. Distribution and habitat The European hake is widely distributed throughout the north-east Atlantic, from Norway in the north to the Guinea Gulf in the south, and throughout the Mediterranean and Black Sea, being more abundant from the British Isles to the south of Spain (Casey and Pereiro, 1995). European hake can be found together with other species of hake such as M. senegalensis and M. cadenati at the southern limit of its distribution (Fig. 2.11; Casey and Pereiro, 1995). The European hake is a demersal and benthopelagic species, found mainly between 70 and 370 m depth; however, it also occurs in inshore waters (30 m) and down to depths of 1000 m (Cohen et al., 1990). The maximum length and weight of this medium-large gadoid species are about 140 cm and 15 kg, respectively (ICES, 2009). Presently, it is

The Biology and Fisheries of European Hake

Figure 2.11 FAO).

113

Distribution of European hake (Merluccius merluccius) (reproduced from

thought that the maximum age of the European hake is around 12 years. However, an important controversy exists with regard to its growth rates (see below) (De Pontual et al., 2003, 2006). European hake lives close to the bottom during the daytime but at night they move up and down the water column (Cohen et al., 1990). Juvenile and small European hake usually live on muddy beds on the continental shelf, whereas large adult individuals are found on the shelf slope, where the bottom is rough and associated with canyons and cliffs.

2.3. General hydrography of the area The north-east Atlantic is affected by the North Atlantic current, which is a warm ocean current that carries the Gulf Stream north-east towards the European coast (OSPAR Commission, 2000). The North Atlantic current splits into two branches around west Ireland. While the Canary current takes a southerly direction, the other warm-water branch continues north along the coast of north-western Europe, heating the cold northern atmosphere. Other branches include the Irminger current and the Norwegian current, which sink to the depths of the Greenland and Labrador Seas to form the Labrador current. Most of the waters in the north-east Atlantic region originate from the North Atlantic, although waters found in the more southerly part have either a North Atlantic origin or are the result of a mixture between Atlantic and Mediterranean waters (OSPAR Commission, 2000). The distribution of European hake in the north-east Atlantic comprises four different OSPAR Commission regions: the Atlantic Coast of the Iberian Peninsula, the Bay of Biscay, the Celtic Sea and the North Sea.

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2.3.1. The Bay of Biscay and the Atlantic Coast of the Iberian Peninsula This region comprises the area to the south of 48 N and to the north of 36 N and contains the Bay of Biscay, the European sector of the Gulf of Cadiz and the western Iberian margin (OSPAR Commission, 2000). The Bay of Biscay can be defined as an open oceanic bay; geographically, it is located between France in the eastern part, oriented south–north, and Spain in the southern part, oriented west–east. The Bay consists of an area to the north of 43.5 N and to the south of 48 N, between 1 400 W and 9 200 W (Fig. 2.12). The northern boundary of the Bay of Biscay is approximately located between the Armorican shelf and the Celtic Sea, and can be considered as a natural element (OSPAR Commission, 2000). The southern limit is usually located at Cape Ortegal (Lavin et al., 2004). There are two clearly different sectors, each of them with a different major gradient with regard to topography: longitudinally, there is a southern part with a narrow continental shelf of about 30–40 km, in general, but reaching as narrow as 12 km in parts (Cantabrian Coast); and latitudinally along the French coast with a extended continental shelf in terms of width (150–180 km on average) and length (Koutsikopoulos and Le Cann, 1996). These characteristics affect not only the general water circulation pattern but also the nature of the environmental and biological relationships of the different species inhabiting the Bay of Biscay. One of the main characteristics of the Bay of Biscay is the relatively high amount of freshwater river runoff. Most of this runoff is related to two river systems: the Loire and the Gironde, which are only 220 km apart and contribute an annual mean outflow of about 900 m3 s 1 (Lavin et al., 2000). Seasonal variations in the runoff of both rivers show a maximum runoff exceeding 3,000 m3 s 1 in winter or spring, and a minimum in summer, at around 200 m3 s 1. In contrast, rivers on the Cantabrian coast are small in length, with pronounced slopes because of the orography of the region (Usabiaga et al., 2004). As such, the contribution of these rivers to the total freshwater supply is only 30% in comparison to the Loire and Gironde (Lavin et al., 2000). Due to their characteristics, the Cantabrian coastal rivers can be considered as torrential, with river discharge almost immediately following precipitation (Uriarte et al., 2004). The maximum flow is in spring and autumn and the minimum during summer. The Galician coastline is mountainous and extends 1,354 km first westwards and then southwards. This section of the Iberian Peninsula contains many ‘rias’, which are coastal inlets found around the northwestern and northern Iberian Peninsula, and beaches covering 13.8% of the Galician coast. South of Galicia, but to the north of 41 N, the coastline is mostly rocky and shallow. To the south of 41 N, a sandy coast extends just north of Lisbon and further south it is replaced by cliffs which extend to Cape Raso, at the same latitude as Lisbon. Sandy beaches with dunes and marshes extend to 37 S and further east.

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Figure 2.12 General circulation pattern in the North-east Atlantic (reproduced from Casey and Pereiro, 1995).

Most of the water masses of the Bay of Biscay and the Atlantic Coast of the Iberian Peninsula originate from North Atlantic water masses or are the result of a mixture of North Atlantic water masses and waters of Mediterranean origin (OSPAR Commission, 2000). The main water masses for this area have been summarised by Boucher (1985), Lavin et al. (2004) and Valencia et al. (2004). In general, the water masses in the upper layer, which reaches depths less than 1,000 m, are characterised by north-east Atlantic central water (ENACW) with a

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temperature ranging from 10.5 to 12 C with a salinity of between 35.45 and 35.75 p.s.u. (Koutsikopoulos and Le Cann, 1996; Valencia et al., 2004). Two sources of ENACW water masses can be identified in this area; a colder water mass with a sub-polar origin (ENACWP) and warmer water of a subtropical origin (ENACWT) (Rı´os et al., 1992). The upper ENACW waters, in addition to the surface waters, are mainly affected by seasonal variations in the atmospheric regime (see below). Below 1000 m, the waters are characterised by Mediterranean overflow water (MOV), which spreads into the north-east Atlantic from the Gibraltar Strait; it moves northwards from the Portuguese continental slope, entering into the Bay of Biscay (Lavin et al., 2004). Between 1800 and 2500 m, the Labrador Sea waters appear (Lavin et al., 2004), although some authors have included this water mass with the north-east Atlantic deep water (NEADW) (Koutsikopoulos and Le Cann, 1996; Valencia et al., 2004). The NEADW appears at depths between 2500 and 3500 m and is characterised by a mixture of different water masses: Denmark Strait overflow water (DSOW) and Iceland–Scotland overflow water (ISOW). Koutsikopoulos and Le Cann (1996) presented a synthesis of water circulation patterns in the Bay of Biscay and the seasonally more relevant hydrological features (Fig. 2.13), which can be extended into the eastern Atlantic Iberian coast (Fig. 2.12). The oceanic circulation in the Bay of Biscay is characterised by weak clockwise circulation, with a mean geostrophic current of about 1–2 cm s 1 at depths of around 400 m. However, the mean flow could be stronger in the surface layers (Koutsikopoulos and Le Cann, 1996; Pingree and Le Cann, 1990). Wind forces, heating, rainfall and river runoff strongly influence the generally weak circulation, making the currents very variable spatially, seasonally and inter-annually (Lavin et al., 2004). In addition to the general clockwise circulation, and depending on the season, the circulation can become cyclonic along the Portuguese, Galician and northern Spanish and French continental slopes due to the slope current. The seasonality of the slope current is affected by wind. In winter, when the northerly wind component relaxes, a warm and saline polewards surface flow (ENACWT) takes place at 20–30 cm s 1 (Frouin et al., 1990; Haynes and Barton, 1990) off the Iberian Peninsula; this moves eastwards along the Cantabrian coast to enter into the Bay of Biscay. As this warm water usually reaches the Bay of Biscay around Christmas, it has been referred to as the ‘Navidad’ current (Pingree and Le Cann, 1992). This event results in an anomalous situation: the warmest temperatures, below the seasonal thermocline, along the northern Spanish slope occur in midwinter, whereas the coldest temperatures occur in mid-summer. This latter pattern is due to the intrusion of the polar ENACW and upwelling processes driven by the north/north-east winds in summer (Fig. 2.14). Moreover, in winter, and linked to the slope current, one of the main characteristics of the regional oceanography is the presence of clockwise and

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Shelf residual circulation

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Slope current Tidal currents

Saint-Nazaire Nantes

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Figure 2.13 The main hydrographic features in the Bay of Biscay (reproduced from Koutsikopoulos and Le Cann, 1996 modified by OSPAR Commission, 2000).

anticlockwise eddies; these have been named ‘swoddies’ (slope water oceanic eddies), by Pingree and Le Cann (1992), because they are formed in the continental slope due to the interaction between the slope current and topography. Furthermore, because of their origin and westwards/northwards movement towards oceanic areas, these structures could be very important in relation to biological processes as they may transport biological material (plankton, eggs and larvae) from the continental shelf (Koutsikopoulos and Le Cann, 1996). This pattern could be very important for the life cycle of the European hake, since recruitment success has been associated with eddy structures in the Cantabrian Shelf (Sa´nchez and Gil, 2000). Another characteristic of winter is the presence of low salinity cold waters, with a river origin, on the continental shelf; this produces an inversion of vertical temperature profiles and strong vertical temperature gradients (Fig. 2.14) (Koutsikopoulus and Le Cann, 1996). In spring, the low salinity cold waters are still present over the continental shelf, depending upon the intensity of river runoff and the wind regime

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Figure 2.14 Seasonal variation in the main hydrographic structures in the Bay of Biscay and Atlantic coast of Iberian Peninsula (reproduced from OSPAR Commission, 2000).

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(Lavin et al., 2004). Moreover, a seasonal thermocline over the French shelf forms in April; this reaches the coastal region in May. Interestingly, a cold and relatively homogeneous (<12 C) water mass appears below the thermocline, centred around 100 m depth off the French coast from the south of the Brittany area to the Gironde estuary (Koutsikopoulos and Le Cann, 1996). This cold water mass forms because of the combined effect of ENACWP water intrusion and upwellings once the southerly wind relaxes and northerly/north-easterly winds become predominant. Moreover, this cold water mass is observed all year round and is characterised by a low, less than 1 C, seasonal and inter-annual temperature difference (Valencia and Franco, 2004; Valencia et al., 2004). This pattern could be very important for the European hake life cycle, since spawning of this species takes place at temperatures between 10.5 and 12 C (Ibaibarriaga et al., 2007). The coastal upwelling off the Galician/Portuguese coast starts to appear in late spring and reaches a maximum in summer. Summer coastal upwellings are also important hydrodynamic features within this area (Fig. 2.14). For example, in response to the prevailing northerly and north-westerly winds over the French continental slope, offshore surface water transportation towards the equator is replaced by colder deeper waters (Lavin et al., 2004; Puillat et al., 2003). Moreover, in summer and early autumn, tidal thermal fronts over the continental shelf are formed due to the interactions between tidal currents and bottom topography. 2.3.2. The Celtic Sea and the North Sea The Celtic Sea consists of an area to the north of 48 N and to the south of 59 N, located between 11 W and 1 W, neighbouring the Bay of Biscay. The North Sea is situated on the continental shelf of north-west Europe and links to the Atlantic Ocean in the north and via the channel the south-west and to the Baltic Sea in the east. The Celtic Sea shows oceanic conditions at the shelf break in the west of Ireland and in the relatively shallow semi-enclosed Irish Sea. The general salinity distribution pattern indicates that the water mass of the Celtic Sea has an Atlantic origin (OSPAR Commission, 2000). The sea surface temperatures on the western and southern Irish shelves are warmer than those of the shallow Irish Sea in winter. This is because the waters of the Irish Sea lose heat more rapidly as the influence of the warmer North Atlantic drift is more pronounced west of Ireland and Scotland. The circulation pattern can be described as an overall water movement from south to north. In general, North Atlantic water masses enter from the south and west of the region (i.e. the Bay of Biscay) and progress through the area to the north. The water masses then split into two branches, one entering Arctic waters and the other entering the North Sea. The North Sea waters are a mixture of North Atlantic water and freshwater runoff. Heat exchange with the air and the supply of local

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freshwater strongly affects the characteristics of waters from the different areas in terms of salinity and temperature (OSPAR Commission, 2000). Generally, the deeper water masses of the North Sea are of pure North Atlantic origin, whereas shallower and surface waters are modified by freshwater runoff and surface heat exchange.

2.4. Growth Although a plethora of papers are available in the literature on European hake growth in the north-east Atlantic (Bagenal, 1954; Belloc, 1935; Descamps and Labastie, 1978; Gon˜i, 1983; Gon˜i and Pin˜eiro, 1988; Guichet, 1988; Hickling, 1933; Iglesias and Dery, 1981; Meriel-Busy, 1966; Morales-Nin et al., 1998; Pin˜eiro and Hunt, 1989; Pin˜eiro and Pereiro, 1993; Robles et al., 1975), it was not until recently that an ‘internationally approved’ ageing method from otoliths was accepted (Lucio et al., 2000; Pin˜eiro and Saı´nza, 2003). However, this agreement was reached only to age fish up to 5 years old because ageing older fish is still problematic (de Pontual et al., 2003). The lack of any previous conformity between otolith readers was because interpretation of the otolith ring structure, the definition of the otolith nucleus, the formation of annual or intermediary rings, the presence of false rings associated with changes in feeding or habitat and interpretation of the otolith edge is very difficult (Casey and Pereiro, 1995; Pin˜eiro and Saı´nza, 2003). Regardless of the lack of an established protocol for European hake otolith readings, all authors concluded that males grow faster than females up to a specific age. Most of the authors agreed that this happens at around 3 years old and that the growth rate of males decreases, whereas females grow faster from that age onwards. This change in growth pattern, or growth rate, has been associated with the onset of maturity (Lucio et al., 2000; Recasens et al., 1998). Also, it is well known that females reach a larger size and grow older than males; in other words, the sex ratio is skewed towards females in the largest length classes. In fact, it has been found that all of the largest European hake are consistently female (Casey and Pereiro, 1995). Such a sex ratio pattern may result in an accumulation of males in certain length classes, due to the larger decrease in growth than in females. In fact, the proportion of males in length classes of around 25–45 cm, following the male onset of maturation, is moderately higher than the proportion of females (Farin˜a and Ferna´ndez, 1986; Lucio et al., 2000; Pe´rez and Pereiro, 1985; Pin˜eiro and Saı´nza, 2003). This pattern, coupled with the fact that males do not reach ages older than those of females (Pin˜eiro and Saı´nza, 2003), may suggest that the mortality rate for males is higher than for females. As a result of the inconsistencies in age-reading methods, different authors have proposed very different growth models for European hake in

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north-eastern Atlantic waters. Overall, there are two hypotheses concerning growth: the first classifies European hake as a slow-growing species and the second as a fast-growing species. Authors such as Hickling (1933), Guichet et al. (1973) and Meriel-Busy (1966) (Table 2.2) postulated a slow growth (of around 10 cm per year) for European hake and this has been the main accepted growth model for many years. Previous exceptions to this theory were those presented by Belloc (1935) and Bagenal (1954) who, with the recovery of a tagged fish from a pioneer tagging experiment and otolith readings, respectively, postulated that the European hake was a fast-growing species, with a growth rate of around 20 cm per year. Subsequent studies by Lucio et al. (2000) and Pin˜eiro and Saı´nza (2003) suggested that the growth rate of European hake is even faster than previously estimated ‘slowgrowth’; however, they presented a slower growth pattern than that proposed by the fast-growth hypothesis. However, recent tagging experiments in the Atlantic (de Pontual et al., 2003, 2006; Pin˜eiro et al., 2007), based upon around 51 recoveries, have concluded that the European hake growth rate is twofold compared to previously published data; this provides direct evidence for European hake being a fast-growing species, as proposed by Belloc (1935) and Bagenal (1954). Interestingly, this latter result has recently been confirmed by studies undertaken on European hake larvae and juvenile growth rates using daily otolith growth increments (Kacher and Amara, 2005; Pin˜eiro et al., 2008). In summary, the latest investigations suggest that European hake grows much faster, by a factor of two, than previously considered. In the light of these new studies, there is a need to revise the internationally agreed otolith reading protocol for hake of up to 5 years old, since with the new growth model, this age would correspond to 2–3-year-old fish. The faster growth also affects the maturity-at-age pattern of hake and the agreed maturity ogive at age. This, in turn, would also have great implications for stock assessments, since this is evaluated using catch-at-age based methods, that is, virtual population analysis (VPA) (ICES, 2009).

2.5. Feeding The European hake is a top predator of the demersal community in the north-east Atlantic area, preying on other fish species such as anchovies (Engraulis encrasicholus; Linnaeus, 1758), sardines (Sardina pilchardus; Walbaum, 1792), blue whiting (Micromesistius poutassou; Risso, 1827), horse mackerel (Trachurus trachurus; Linnaeus, 1758) and mackerel (Scomber scombrus; Linnaeus, 1758; Cabral and Murta, 2002; Gonzalez et al., 1985; Guichet, 1995; Pereda and Olaso, 1990; Velasco and Olaso, 1998). A specific characteristic of European hake is that adult hake live and spawn at the shelf edge, whereas juvenile recruitment occurs in specific areas on ´ lvarez et al., 2004; Ibaibarriaga et al., 2007). Thus, the continental shelf (A

Table 2.2 Mean length (cm) at age for European estimated by different authors in different areas; (B) both sexes combined; (F) females and (M) males (modified from Pin˜eiro and Saı´nza, 2003) Age Author

Area

Sex 0

Hickling (1933) Hickling (1933) Bagenal (1954) Guichet et al. (1973)

Ireland Scotland Scotland Ireland

Meriel-Busy (1966) Descamps and Labastie (1978) Guichet (1988)

Bay of Biscay Bay of Biscay Bay of Biscay

B B B M F B M F B

11 15.7 15.9 16.3 24.1

ICES (2000)

Bay of Biscay

B

11.2 20.7 26.9 34.3 41.8

Lucio et al. (2000) Iglesias and Dery (1981)

Bay of Biscay N and NW Iberian waters

Robles et al. (1975)

NW Iberian waters Morocco

B M F B B

13.1 17.8 17.6 19.6 20.2 10.6

Gon˜i (1983)

1

22.3

3

4

5

19.6 20.9 43.2 22.5 19.1 19.6 24.9 25.2 32.3

25.4 25.6 58.7 20.1 27.9 28 32.9 33.7 39.1

35.1 34.6 70 32.5 33.8 36.6 39.8 41.4

43.2 51.4 63.4 68 72.9 Otoliths and scales 42.1 50.9 59.8 67.9 74.1 81.2 Otoliths Otoliths-Petersen 40.1 47.3 53 59.8 63.9 66 Otoliths 42 49.6 56.5 62.2 69.9 76.9 Otoliths 43.5 51.2 58.7 65.1 69.6 80.1 Otoliths 45.7 50.9 55.3 59.1 62.4 65.2 Otoliths 48.4 54.7 60.4 65.6 70.3 74.5 Otoliths NORMSEP Modal Progression 50.4 59.3 63.7 90.3 Otoliths (ALK from 1999) 51.6 60.9 67.7 72.7 85.1 Otoliths 38.6 43.1 45.2 47.8 50.1 Otoliths 38 41.9 45.5 49 52.2 Otoliths 37.3 41 44.4 47.7 50.7 Otoliths 42.7 Otoliths

24.7 23.8 24.7 24.9 19.7

33.1 29.5 29.4 29.3 27.8

42.6 34.4 33.8 33.4 35.2

6

7

8

9

M

16

21.4 26.5 31.3 35.7 39.9 43.8 47.3 50.9

F

15.4 21.4 26.9 32.2 37.1 41.7 46

B

14.8 20.7 26.3 31.4 36.3 40.9 45.2 49.2 53

50

53.8

10

Ageing method

2

Backcalculated/ Otoliths Backcalculated/ Otoliths Backcalculated/ Otoliths

Gon˜i and Pin˜eiro (1988) ICES (1991) ICES (1999a,b) ICES (2000) Pin˜eiro and Saı´nza (2003)

N and NW Iberian waters N and NW Iberian waters N and NW Iberian waters N and NW Iberian waters N and NW Iberian waters

B

15

23

28

32

36

40.5

18

25

30

36

41

45

B

12

49

B

14.9 21.5 29.4 36.8 43

B

12.6 21.4 28.7 33.8 41.8 48.7 53.4 58.1 63.7 69.9 79

M F B

17 21 29.5 36.4 42.7 45.7 49.7 54.2 60 16.8 20.9 28.4 37 44.5 48.7 53.7 56.4 62.3 68.7 75 11.9 20.6 29 36.7 43.8 50 55.4 58.3 63.1 67.1 75

48.6 54.4 58

53

57

60

63.6 67

77

Backcalculated/ Otoliths Kimura and Chikuni (1987) Otoliths (ALK from 1998) Otoliths (ALK from 1999) Otoliths Otoliths Otoliths

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the feeding spectrum of juvenile and adult hake is different. The main food items of juvenile hake (<20 cm) are decapod prawns and euphausiids, whereas the diet of hake between 20 and 40 cm is mainly composed of blue whiting, horse mackerel, mackerel and clupeids, and for hake larger than 40 cm, the main item is blue whiting (Velasco et al., 2003). Velasco and Olaso (1998) also found differences in the diet of hake in relation to depth, with clupeids and horse mackerel being the main items at depths less than 100 m, whereas blue whiting appeared to be the main prey in the deepest strata. Based on previous work, it also seems that there are differences in hake diet between different areas. While Velasco and Olaso (1998) identified blue whiting as the main prey item of hake in the Cantabrian Sea, Guichet (1995) in the Celtic Sea observed that blue whiting only appeared in hake between 35 and 45 cm long, whereas anchovies and horse mackerel were the major prey items in smaller and larger hake, respectively. In this sense, the dependence of hake on blue whiting is especially significant in the Cantabrian Sea (Velasco and Olaso, 1998). Moreover, Trenkel et al. (2005) found in the Celtic Sea that the feeding rate of European hake on horse mackerel and blue whiting was affected by prey density, that is, there was evidence for density-dependent feeding and spatial/seasonal prey-switching behaviours. These authors also found that the feeding habits of European hake followed a seasonal pattern, whereby they were focused upon blue whiting in the summer and mackerel and Trisopterus spp. in winter. The higher predation on blue whiting in summer was associated with the arrival of juveniles to the Celtic Sea. Cannibalism is also observed in hake (Gonzalez et al., 1985; Guichet, 1995; Hickling, 1927; Velasco and Olaso, 1998). However, the percentage of hake in the hake diet varied throughout the areas studied and also by length. For example, while Hickling (1927) found that cannibalism could account for between 15% and 20% of the diet of hake, Velasco and Olaso (1998) observed that it was less than 4% of the total volume of prey in the Cantabrian Sea.

2.6. Reproduction and recruitment Understanding the relative importance of factors responsible for interannual variation in recruitment is a primary objective of fisheries science and management (Chambers and Trippel, 1997; Marshall et al., 1998). Within this context, the relationship between population and recruitment is the central, and generally most difficult, outstanding problem in the study of population dynamics and the management of marine fish stocks (Hilborn and Walters, 1992). Despite the ongoing discussion regarding the relationship between stock spawning biomass and recruitment (Gilbert, 1997; Marshall et al., 2003; Myers, 1997), management of the majority of exploited fish populations is,

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at present, based upon spawner-recruit models. Traditional recruitment models assume that the reproductive potential of a population is proportional to its spawning stock biomass (SSB; Trippel et al., 1997); this is then commonly used to set biological reference points (BRPs) (Fig. 2.15). However, the standard spawner-recruit models developed by Beverton and Holt (1957), Ricker (1954) and Sheperd (1982) originally used the term fecundity (Koslow, 1992; Rothschild and Fogarty, 1989), but afterwards used the term SSB instead as a proxy for fecundity. In such cases, it is assumed that a given weight of adult biomass has the same probability of generating the same level of recruitment. This implies that the survival rates of offspring are independent of parental age, body size or condition (Cardinale and Arrhenius, 2000; Murua et al., 2003) and that total relative fecundity and annual egg production, by length and between years, are invariable (Marshall et al., 2003). However, there is increasing evidence indicating that a direct proportionality between SSB and reproductive potential may not exist. Trippel (1999) introduced the new term, stock reproductive potential (SRP), as an alternative to SSB; this more accurately characterises the capacity of a population to annually produce viable eggs and larvae which may eventually recruit into the adult population or fishery. In this sense, the term SRP has the potential to include early life history stages related to recruitment

Recruits

Quadrant 4

Larvae and juvenile growth and morality

Quadrant 1

Recruited stock. growth, mortality, maturation. Spawning stock

Larvae

Spawning

Hatching

Quadrant 3

Eggs

Quadrant 2

Figure 2.15 Paulik (1973) figure which showed that population assessment advice is normally limited to the un-shaded area (growth, mortality and maturation—quadrant 1) and traditionally does not include subsequent life history stages related to recruitment (quadrants 2–4) (sources: Solemdal, 1997; Ulltang, 1996; reproduced from Trippel, 1999).

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processes (quadrant 2–4, Fig. 2.15). In particular, the reproductive potential of a population is affected by several factors, such as adult age structure and diversity (Marteinsdottir and Steinarsson, 1998), the proportion of first-time and repeat spawners (Evans et al., 1996; Trippel, 1998) and nutritional condition (Hunter and Leong, 1981; Ma et al., 1998); these are poorly reflected when using the SSB to represent the reproductive potential of the species. This limitation could even be more pronounced in the case of indeterminate fecundity species, where the production of eggs per unit SSB may vary substantially between years depending upon environmental conditions (temperature and food availability) during the spawning season (Hunter and Leong, 1981). In these species, feeding conditions greatly influence spawning activity and the rate of recruitment of pre-vitellogenic oocytes into the stock of yolked oocytes (Rinchard and Kestenmont, 2003). It has also been documented that fecundity within a stock varies annually and can undergo long-term changes (Kjesbu et al., 1998; Murua et al., 2006; Rijnsdorp, 1991). In the light of these issues, there is a clear necessity to comprehensively study the inter-annual variations of fecundity and adult egg production; this, in turn, will enable the development of an understanding of the underlying mechanisms regulating annual variability in egg production, as well as improving the capacity to explain variability in recruitment. This component (quadrant 2, Fig. 2.15) represents the production processes which yield a number of potential zygotes, a quantity that becomes modified by mortality processes during early life stage dynamics to ultimately arrive at the number of recruits (quadrants 3 and 4, Fig. 2.15) (Marshall et al., 1998; Ulltang, 1996). Moreover, adult egg production information, in combination with concurrent estimates of egg production at sea (from ichthyoplankton surveys), would enable the estimation of SSB independently of commercial fishery data (Lasker, 1985; Parker, 1980; Saville, 1964). This approach would increase the knowledge with regard to the state of the population, improving the standard assessment of any commercially valuable fish species. 2.6.1. Reproductive biology The quantification of fecundity and the understanding of reproductive strategies are fundamental topics in biology and in population dynamics studies of fish species (Hunter et al., 1992; Murua and Saborido-Rey, 2003). In the case of commercial fish species, reproductive studies (including the assessment of size at maturity, duration of the reproductive season, daily spawning behaviour, spawning fraction and fecundity) permit basic data to be obtained for quantification of the reproductive capacity and also to assess the effects of fishing and other external factors on reproductive potential.

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Despite its commercial importance, the information available on the reproductive biology of European hake in the North Atlantic is not extensive. In particular, little has been published on the seasonal variations in European hake fecundity and spawning activities. Some studies have presented the maturity ogives of European hake in Galician and Bay of Biscay waters (Domı´nguezPetit et al., 2008; Lucio et al., 2000; Martin, 1991; Pin˜eiro and Saı´nza, 2003). According to these studies, males mature at around 35 cm, whereas females mature between 45 and 50 cm total lengths. In general, all the authors agreed that there is a sexual dimorphism with regard to maturation, with males maturing earlier than females. Domı´nguez-Petit et al., 2008 showed that there was a decline of around 10 cm in the size at maturity observed in the Bay of Biscay from 1996 to 2004, which was related to fishing mortality and the age diversity of the stock. Similarly, they showed that size at maturity in the Galician shelf decreased around 15 cm from 1980 to 1988, increased again by about 14 cm until 1998 and decreased again in 1999, since when it has stayed relatively constant. These changes were related to different population biomass levels and environmental conditions in the area. Previous studies into the reproductive biology of European hake have indicated that this species is a batch spawner (Murua et al., 1998; Pe´rez and Pereiro, 1985; Sarano, 1986), spawning several batches within the reproductive season. This interpretation is consistent for other species of the genus Merluccius: Angelescu et al. (1958), Ciechomski (1967) and Christiansen and Cousseau (1971) for M. hubbsi; Balbotin and Fischer (1981) for M. gayi gayi; Alheit (1986) for M. gayi peruanus and Erkamov (1974) and Foucher and Beamish (1977) for M. productus. Moreover, the main spawning season of European hake was identified as lasting from December to July along the shelf edge of the Galician Coast and the Bay of Biscay to the south-west of Ireland (Lucio et al., 2000; Martin, 1991). For example, Pin˜eiro and Saı´nza (2003) defined the hake spawning season from December to May in Iberian waters, with the spawning season in the Bay of Biscay from January to May and a ´ lvarez et al., 2004; defined spawning peak between February and March (A Lucio et al., 2000). Recent investigations, however, have shown that the spawning season of European hake is very protracted on the Galician Coast and in the Bay of Biscay (i.e. spawning activity is observed all year round), although the main spawning season was observed between January and March in the Bay of Biscay and on the Galician shelf with a secondary peak in June–July for the Galician area (Domı´nguez-Petit, 2007; Korta et al., 2010a; Murua and Motos, 2006, Murua et al., 2006). In this sense, the population asynchrony observed in spawning, as well as the extensive spawning season spanning the entire year, was also observed in European hake in the Mediterranean area (Recasens et al., 1998). This protracted spawning season was the longest spawning period reported for species of this genus (Merluccius) (Table 2.3). The long spawning period was also found for M. capensis (Cadenat) (Bianchi et al., 1993).

Table 2.3

Spawning period of different species of the genus Merluccius.

Species

Spawning period

Area

References

M. albi M. angustimanus M. australis M. bilinearis M. polli M. capensis M. gayi M. gayi peruanus M. hubbsi M. productus M. senegalensis

April–August April–June May–August May–October October–March January–December (peak spring and summer) August–November August–March November–April (peak January) January–June September–March (peak November–February)

Mexico–USA Mexico Argentina/Mexico USA/Canada Mauritania/Guinean shelf Namibia/South Africa Chile Peru Argentine Mexico/USA Southern Morocco, Northern Mauritania/Cape Verde

Cohen et al. (1990) Mathews (1985) Cohen et al. (1990) Scotton et al. (1973) Garcia (1982) Bianchi et al. (1993) Cohen et al. (1990) Cohen et al. (1990) Pa´jaro and Macchi (2001) Hart (1973) Wysokinski (1986)

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European hake is characterised by asynchronous oocyte development, where oocytes of all stages are simultaneously present in reproductively active ovaries (Table 2.4 and Fig. 2.16). This has been interpreted as providing evidence for indeterminate annual fecundity (Murua et al., 1998). The term ‘indeterminate’ refers to species in which the potential Table 2.4 Summary of oocyte developmental stages in European hake ovaries (adapted from Murua and Motos, 2006) Oocyte development stage

Characteristics

Previtellogenic Cortical Appearance of cortical alveoli vesicles in the Alveoli cytoplasm in preparatory of yolk development. Oil vesicles begin to accumulate in the cytoplasm. The chorion and follicle layers are apparent. Vitellogenic (yolked) VIT 1 First stages of exogenous vitellogenesis. Yolked oocytes with eosinophilic yolk granules present in the cytoplasm. Oil droplets occupy more cytoplasmic area than yolk granules. VIT 2 Exogenous vitellogenesis continues and oil droplets occupy a similar cytoplasmic area than yolk granules. VIT 3 Exogenous vitellogenesis continues and oil droplets occupy less cytoplasmic area than yolk granules Maturation Early Oil droplets fuse into a unique oil globule and the migration nucleus start to migrate peripherally to the animal pole. Late migration Nuclear migration goes on, yolk granules start to fuse in plates starting in the centre and extending centrifugally. Hydration Once the nucleus migrated to the animal pole, it disintegrated. A rapid uptake of fluid by the oocyte through its follicle occurs and yolk fuses into a homogeneous mass. The cytoplasm and the cortical alveoli are restricted to a thin peripheral layer.

Oocyte diameter (mm)

150–250

250–450

450–550

550–650

650–750

750–950

950–1150

The histological characteristics and the size ranges are given for each stage. Measures are made from histological sections.

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Hilario Murua

1

2

3

4

5

6

7

8

9

Figure 2.16 Oocyte development process (plates 1–9, see below) in European hake, Merluccius merluccius: (1) Primary growth stage oocyte; (2), (3) Cortical alveoli stage oocyte; (4) Cortical alveoli oocyte (left) and early vitellogenic oocyte (right); (5), (6) advanced vitellogenic oocytes; (7) early migration (maturation) stage; (8) migration stage (final maturation) and (9) hydrated oocyte (reproduced from Murua and Motos, 2006). n, nucleus; m, nucleolus; c, cytoplasm; ca, cortical alveoli; pg, primary growth; t, follicle layer; u, envelope of oocyte; y, yolk vesicles; o, oil droplets; mn, migratory nucleus; yp, yolk plates; HO, Hydrated oocyte; bar ¼ 0.1 mm.

annual fecundity is not fixed prior to the onset of spawning (Hunter et al., 1992). In such species, pre-vitellogenic oocytes can develop and be recruited into the yolked oocyte stock at any time during the season (de novo vitellogenesis) (Hunter and Goldberg, 1980). Estimation of total fecundity in the ovary, prior to the onset of spawning, is meaningless if during the spawning season oocytes are recruited to that stock. In these species, annual fecundity should be estimated from the number of oocytes released per spawning (batch fecundity), the percentage of females spawning per day (spawning frequency) and the duration of the spawning season (Hunter and Macewicz, 2003; Hunter et al., 1985; Hunter and Macewicz, 1985; Murua et al., 2003). Further work by Murua and Motos (2006) on the histological examination of ovaries from hake in the Bay of Biscay, sampled on a monthly basis from December 1996 to October 1997, demonstrated that this species exhibits indeterminate fecundity. They showed that oocyte development is asynchronous with a continuous oocyte size-frequency distribution in pre-spawning, spawning and post-spawning females; there

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was a gradual decrease in the mean diameter of advanced yolked oocytes as spawning proceeded, and a generalised atresia at the end of the spawning season was observed. These are considered characteristics of indeterminate fecundity species (Murua et al., 2003). The use of a combination of modern stereological methods and the advanced oocyte packing density (OPD) theory (Kurita and Kjesbu, 2009) by Korta et al. (2010b) corroborated the theory that hake are an indeterminate fecundity species. The fecundity indeterminacy of hake can be explained through the energy allocation to gamete production during the breeding season (Domı´nguez-Petit and Saborido-Rey, 2010) or, in other words, because hake is considered as an income breeder (i.e. adjusts its food intake with breeding, with a minor reliance on energy stores). Murua and Motos (2006) estimated that the spawning fraction, defined as the proportion of females spawning per day, ranged from 0.085 to 0.207 in the Bay of Biscay in 1996/1997, which is equivalent to a batch interval of 5–12 days; the spawning fraction was highest at the peak of spawning from January to March (5 days batch interval) and decreased afterwards as the spawning season progressed (batch interval of around 12 days). European hake in the Galician shelf was also found to spawn with a batch interval of around 5 days between January and March, with a decreasing batch interval afterwards to around 10 days (Domı´nguez-Petit, 2007). Argentine hake, M. hubbsi, were found to spawn once every 7 days during the peak of spawning and every 10 days at the end of the spawning season (Macchi et al., 2004), showing a somewhat similar spawning activity to European hake in the Bay of Biscay. Moreover, Murua et al. (2006) showed that relative batch fecundity varied significantly between months and years, but not between different areas within the Bay of Biscay. They presented two levels of relative batch fecundity for 1997: the highest between January and April (on average, 167 eggs per gram gutted females, SD 5 eggs) and the lowest from May to October (on average, 112 eggs per gram gutted females, SD 3 eggs). They also showed that the relative batch fecundity variation between years was 9% for 1996–1997 and 28% for 1997–1998, which in turn could be related to differences in productivity between years, and that both the intraand inter-annual variations in relative batch fecundity may be due to the differing conditions of the fish. In fact, they illustrated that the difference between the gonado-somatic indexes was around 14% in 1996–1997 and 36% in 1997–1998. The estimation of relative batch fecundity (Murua et al., 2006) in conjunction with spawning fraction estimates and the percentage of active mature females in the adult population (Murua and Motos, 2006) were used to produce population-relative egg production figures. In this sense, they estimated that the relative egg production for this population varied from a high value in January to March (985 eggs per gram gutted female) to a low

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egg production between April and October 1997 (445 eggs per gram gutted female). As such, the maximum egg production figures were for January– March and they were mainly as a consequence of the high spawning fraction and relative batch fecundity values. In their view, the subsequent decrease in relative daily egg production was due to the decline in the spawning fraction, relative batch fecundity and the percentage of mature active females. These results on adult egg production presented by Murua et al. (2006) were in agreement with icthyoplanckton data which showed that the peak of egg ´ lvarez et al., 2001). In abundance occurred in March in the Bay of Biscay (A summary, all of these works showed that the European hake has a protracted spawning season, with spawning females present all year round; however, there were different levels of egg production depending upon the month of the year in the Bay of Biscay (these were highest from January to March and subsequently decreased to low levels during the rest of the year). A similar situation was also observed in the Galician area where females in spawning condition were found all year round, and the spawning fraction and batch fecundity were also highest between January and March with a second smaller peak observed in June and July (Domı´nguez-Petit, 2007). 2.6.2. Recruitment As suggested by egg/larvae and spawning adult distribution studies, the main spawning areas of European hake are concentrated over the shelf break off the French coast in the Bay of Biscay and in the Celtic Sea to the west of Ireland (A´lvarez et al., 2004; Kacher and Amara, 2005). There is also another main spawning area located over the shelf off the north-west coast of the Iberian Peninsula (Casey and Pereiro, 1995). The eggs of European hake are pelagic and their major densities are mainly found in ´ lvarez et al., the upper 200 m of the water column over the shelf break (A 2001; Ibaibarriaga et al., 2007); although, depending upon environmental conditions (upwelling, temperature), the depth distribution throughout the water column can be different. The optimum temperature range for the spawning of European hake appears to be between 10 and 12.5 C (Fig. 2.17), as European hake eggs are mainly distributed in water at such temperatures, although they can be found in temperatures of up to 15 C (A´lvarez et al., 2001; Ibaibarriaga et al., 2007). The main nursery areas have been identified in the north-east Atlantic as located over the shelf along the French coast (Le Grand Vasie´re), the shelf in the Celtic Sea and off the west coast of Ireland (Casey and Pereiro, 1995). After hatching, early European hake larvae are still found over the shelf ´ lvarez et al., 2004; Ibaibarriaga et al., 2007). However, shortly after break (A this, hake larvae appear to undergo a coastward displacement over the ´ lvarez continental shelf, towards the main nursery areas. For example, A et al. (2001) found that smaller hake larvae (< 8 mm total length) were distributed around the spawning area over the shelf break, whereas larger

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Figure 2.17 Quotient lines of European hake egg (solid line) and larval abundance (dashed line) with respect to the logarithm of bottom depth (left) and to sea surface temperature (right). The vertical bars indicated the number of samples taken in each class (reproduced from Ibaibarriaga et al., 2007).

larvae (>8 mm in total length) appeared in shallower waters over the inner part of the continental shelf. Interestingly, Kacher and Amara (2005) found that more 0-group European hake were distributed inshore than in the areas of major larval densities. As the spawning grounds over the shelf are far from the main nursery areas, it is evident that the retention and transportation of

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eggs and larvae, from the spawning grounds towards the nursery areas, are critical processes in the early life history of European hake, as for other fish species, that is, the migration triangle hypothesis (Cowan and Shaw, 2002; Harden Jones, 1968; Miller, 2002; Secor, 2002). In this sense, fish species have adapted their reproductive strategies to match the principal environmental and oceanic events; this leads to retention and transportation towards the main nursery areas (Pianka, 2000; Wootton, 1998). In the case of European hake, the transportation of early life stages from the Bay of Biscay and Celtic Sea spawning grounds coastwards to juvenile recruitment areas can be foreseen in relation to the general water mass circulation, as postulated by Koutsikopoulos and Le Cann (1996). In fact, A´lvarez et al. (2004) inferred a north and north-east dispersion of eggs and larvae due to the main pattern of oceanic processes such as wind-induced currents and geostrophic flow in the Bay of Biscay (Fig. 2.18). Similarly, in the other main spawning nursery area (which corresponds with the southern hake stock) identified over the north and west Iberian Peninsula coast, the transportation of larvae to the open ocean has a negative impact on recruitment, whereas transportation and retention to the nursery area have a positive impact on recruitment (Sa´nchez and Gil, 2000).

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Figure 2.18 Main spawning and nursery areas for European hake in North-east Atlantic waters. D, NOAA winds recorded station; solid black line, the slope current; big grey arrows, geostrophic flow; small grey arrows, residual flow and dotted line, ´ lvarez et al., 2004). 200 m isobath (reproduced from A

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European hake larvae are mainly found in water temperatures of between 10.5 and 13 C (A´lvarez et al., 2001; Ibaibarriaga et al., 2007), and have a pelagic existence until they settle on the seabed, around 40 days ´ lvarez and Cotano, 2005; Kacher and after hatching in the Bay of Biscay (A Amara, 2005) and around 50 days in the north-west Iberian region (Pin˜eiro et al., 2008). The 0-group European hake are found in muddy bottoms, between depths of 70 and 200 m, with the highest densities at a depth of 100 m (Kacher and Amara, 2005) on the continental shelf of the main two nursery areas mentioned earlier. In autumn, the 0-group European hake are recruited into the population (Pereiro et al., 1991). The population spawning asynchrony, as well as the protracted spawning season spanning the entire year for European hake, confront the hypotheses of a critical first-feeding period (Hjort, 1914) and larval match–mismatch (Cushing, 1975, 1990); which state that stocks adapt their spawning season to the peak of plankton production in the area to avoid starvation during the critical first-feeding critical. In the case of European hake, it seems that this could be true for the peak spawning season identified. However, the observation of spawning all year round could be related to the higher probability of hake larvae locating food than the larvae of other species, as mentioned by Bailey (1981). Bailey (1981) suggested that for Pacific hake (M. productus), the first-feeding period may not be as important as for other fish species due to their longer period for locating food based on (1) slow growth, slow metabolic rates and the low daily rations of Pacific hake larvae; (2) the large mouth of first-feeding hake larvae and therefore, larger food items in the diet and (3) the relatively longer starvation time for Pacific hake larvae. In the case of European hake, although it seems that the larvae exhibit fast growth rates (Kacher and Amara, 2005; Pin˜eiro et al., 2008), it has also large mouths at first feeding ´ lvarez and Cotano, 2005). In and a relatively high starvation endurance (A addition, Albaina and Irigoien (2004) found that the shelf edge in the Bay of Biscay is an area of relatively high zooplankton biomass and that larger copepods are found off the shelf edge in the Bay of Biscay where European hake larvae inhabit. Thus, spawning to match peaks in food concentration might not be a limiting factor for first-feeding European hake larvae.

3. Fisheries and the State of the Population 3.1. Population structure in the north-east Atlantic In the north-east Atlantic, ICES (International Council for the Exploration of the Sea) recognises the existence of two stocks: the northern stock (ICES Division IIIa, Sub-areas II, IV, VI and VII and Divisions VIIIa, b, d) and the southern stock (ICES Divisions VIIIc and IXa) (ICES, 2009). The northern

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limit for the northern stock is located on the Norwegian coast in the north-east Atlantic, whereas the southern limit for the southern stock is the Gibraltar Strait. The geographical boundary between these stocks was established as lying at the Cap Breton Canyon (close to the border between the French and Spanish coasts), which was considered as a geographical barrier limiting the exchange between both populations. According to Lundy et al. (1999) and Castillo et al. (2004), there were subtle geographical genetic differences between Atlantic hake populations; however, genetic studies did not reveal any evidence for multiple populations in the north-east Atlantic (Pla and Rolda´n, 1994; Rolda´n et al., 1998). Moreover, Castillo et al. (2005) found that there were no genetic differences between European hake in Divisions VIIIc and VIIIa, b, d, that is, the boundary between northern and southern stocks (see above). A similar conclusion was reached by Mattiucci et al. (2004), who concluded that there were no genetic differences between European hake in the Celtic Sea and in the southern Bay of Biscay. In this sense, it seems that management-focused administrative criteria were preferred when establishing stock boundaries rather than a biologically grounded basis.

3.2. The northern stock 3.2.1. Fisheries The northern stock of European hake supports a major commercial fishery in Atlantic European waters, which has been commercially exploited since the eighteenth century (Casey and Pereiro, 1995). It is especially important for Spanish and French fishing fleets. The annual catch of this stock ranged from 40,400 to 96,000 tonnes, during the 1961–2006 (ICES, 2009) period. Specifically, from 1961 onwards, the catch decreased continuously from its highest level of 96,000 tonnes in 1961 to 51,000 tonnes in 1971. It increased again to reach a second peak of around 78,000 tonnes in 1973, being on average around 70,000 tonnes during the period of 1972–1976. However, it decreased to levels of around 55,000 tonnes in 1977 and remained at around 60,000 tonnes, on average, until 1995. From 1995 onwards, the catch steadily decreased to reach the lowest value in the time series of 35,800 tonnes in 1998; since then it has remained at low levels between 40,000 and 45,000 tonnes (Fig. 2.19). The catch in 2008 was 47,800 tonnes and the provisional catch in 2009 was 42,800 tonnes. Hake are mainly caught in Sub-areas VII and VIII with a relatively low catch level in Sub-areas IV and VI. During the beginning of the time series, the catch was slightly higher in Sub-area VIII than in VII. However, between 1995 and 2001, the decrease in total landings was mainly due to the decline of the total catch in Sub-area VIII, which diminished from around 25,000 to 10,000 tonnes. Since 2002, the catch in Sub-area VIII increased and has remained stable at around 15,000 tonnes, whereas the catch in VII has also remained constant at around 25,000 tonnes.

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Figure 2.19 Total catches of the northern stock of European hake in the North-east Atlantic (source: ICES, 2009).

Historically, Spain, France and the United Kingdom have been the main countries involved in this fishery; however, the relative importance of these contributors, in relation to total landings, has changed during the catch history. In more recent years, Spain has accounted for around 65% of the total catch, France around 25%, the United Kingdom about 7% and Denmark and Ireland 3% each (ICES, 2009). Several fleet segments focus their activities on the northern stock of European hake and most of them catch hake in mixed fisheries. Amongst the other species, megrim, monkfish, nephrops, blue whiting and horse mackerel can be found in the catch of these mixed fisheries. In this sense, various fishery units have been associated with the northern hake fishery in order to investigate the fishing activity in relation to demersal species (ICES, 1991). These fishing units use a combination of fishing areas and mixed gear to harvest European hake and are defined to allow a precise monitoring of hake catches by fleet. Most of the catch is taken by six fishery units (around 90% of the total landings), which comprise three fishing units in Sub-area VII (medium to deep water long lines, gillnets and trawls); two in Sub-area VIII (shallow to medium water gillnets and medium to deep water trawls) and one in Sub-areas IIIa, IV, V and VI (ICES, 2009). 3.2.2. Status of the stock and management The size of the northern hake population declined sharply during the late 1990s; the present level appears to be only 50% of the level in the 1970s. The ICES Working Group on the assessment of southern shelf stocks of hake, monk and megrim, based upon the most recent estimates of SSB and fishing mortality, considers that the northern stock has a full reproductive

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capacity and that it is harvested sustainably (ICES, 2009). The SSB was estimated in 2009 to be just above the precautionary approach BRP (BPA ¼ 140,000 tonnes) and the fishing mortality was estimated to be around the precautionary approach fishing mortality reference point (FPA) since 2001 (Fig. 2.20). Although the stock currently lies within the safe biological limits, at the beginning of the 1990s, the spawning biomass had decreased below the BPA to around the Blim until 2001. However, since 2001, the SSB increased and is presently estimated to be just above the Bpa (ICES, 2009). Due to the critical state of the population during the most recent years of the twentieth century, and in order to assist in its recovery, an emergency plan was introduced in June 2001 (Council Regulation No. 1162/2001). Finally, a recovery plan was implemented for the northern stock of European hake in 2004, under EC Reg. No. 811/2004. Therefore, the present management objectives of this stock are those explicitly established in EC Reg. No. 811/2004. The objective of the European hake recovery plan for the northern stock is to increase the level of spawning biomass to levels equal to or greater than 140,000 tonnes (Bpa) in two consecutive years (EC No. 811/2004). Once the target level has been achieved, the Commission will introduce follow-up management measures to replace the recovery plan. The agreed fishing mortality in the recovery plan was set at lower than or equal to the FPA (0.25), which will

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Figure 2.20 Spawning stock biomass and recruitment (age 0) as well as the biological reference points of the northern stock of European hake. Bpa is the biomass below which the stock would be regarded as potentially depleted or over-fished and it is judged to give a reasonable certainty that, in spite of year-to-year fluctuations, the stock will stay above Blim. Blim is the limit spawning stock biomass, below which recruitment is impaired or the dynamics of the stock are unknown. In the case of northern hake population, Bpa and Blim are set at 140,000 and 100,000 tonnes, respectively (ICES, 2009).

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produce the total allowable catch (TAC). The change in TAC from year-toyear is constrained so that it does not exceed 15% unless the SSB is below 100,000 tonnes. In this case, a lower TAC than implied by the 15% constraint is applied. The northern hake SSB has been estimated to be above the recovery plan target (140,000 tonnes) for the last two years and thus a management plan prescribed in the recovery plan should be implemented soon. The northern hake population, as with the majority of the EU stocks, is managed by TAC and quota regulations. In addition, the following technical measures are in place: minimum length at a landing of 27 cm (30 cm in Division IIIA), minimum mesh size of 70 mm in the Bay of Biscay and minimum mesh size of 100 mm for otter trawls when European hake comprises more than 20% of the total catch (EC No. 811/2004). In specific areas, the minimum mesh size of 100 mm is required for all otter trawls.

3.3. The southern stock 3.3.1. Fisheries The southern stock of European hake supports an important coastal commercial fishery on the Atlantic coast of the Iberian Peninsula, which has been commercially exploited since the eighteenth century (Casey and Pereiro, 1995). It is especially important for Spanish and Portuguese fishing fleets. The annual catch of this stock increased from 26,000 tonnes to the highest level in the time series of 35,000 tonnes in 1973 and then decreased again to 26,000 tonnes in 1976. Since then, the catch has fluctuated between 10,000 and 23,000 tonnes (ICES, 2009). Specifically, from 1976 onwards, the catch decreased continuously from 26,000 to 17,000 tonnes in 1981 and increased again to reach a level of around 23,000 tonnes in 1984, being on average around 19,000 tonnes in the period of 1983–1988. However, it decreased continuously to levels of around 12,000 tonnes in 1995 and again to the lowest level observed, of around 7000 tonnes in 2004. From 2004 onwards, the catch slightly increased to reach levels similar to those in the beginning of the 1980s. The catch in 2008 was 19,200 tonnes and the provisional catch in 2009 was 22,400 tonnes. The southern hake stock is fished by Spanish and Portuguese fleets in a mixed fishery (Fig. 2.21). An industrial and semi-industrial trawler fleet and a very heterogeneous artisanal fleet, using various types of gear (traps, large and small gillnets and long lines, for example), have been identified in both countries (ICES, 2009). The Spanish fleet was responsible for between 60% and 75% of the catch during the 1972–2005 period, whereas it was responsible for more than 80% in 2006 and 85% in 2007 and 2008. The Spanish trawler fleet mainly uses two types of gear, that is, a pair trawl and a bottom trawl, and has been responsible for 67% of the total southern hake Spanish catch during recent times. The percentage of hake present in the landings of the mixed trawl fishery has become smaller during recent years, as the trawl

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Figure 2.21 Total catches of the southern stock of European hake in the Atlantic Iberian Peninsula coast (source: ICES, 2009).

activity has been focused on various other important target species such as anglerfish, megrim, Norway lobster, blue whiting, horse mackerel and mackerel (ICES, 2009). On the contrary, the contribution of the Spanish artisanal fleet to the total Spanish catch has significantly decreased to around 15% of the total catch during recent years, although it reached 43% in 1987. In 2007 and 2008, the contribution of the Spanish artisanal fishery increased again up to 25% and 30%, respectively. Similarly, hake is caught by the Portuguese trawler and artisanal fleets in a mixed fishery together with other fish species and crustaceans. The contribution of the Portuguese catch to the total catch was between 30% and 40% between 1972 and 2004. This contribution decreased to 25% in 2005 and further to around 15% in 2007 and 2008. In this case, however, the contribution of the artisanal fleet was higher in comparison to the trawler fleet, that is, around 60% of the Portuguese catch was made by the artisanal fleet in comparison to 40% by the trawler fleet. 3.3.2. Status of the stock and management The SSB of the southern hake population declined sharply and continuously since 1983 to the lowest observed level of 7,300 tonnes in 1998. The SSB remained relatively stable around 10,000 tonnes from 1999 to 2005 and it increased to around 20,000 tonnes and 25,000 tonnes in 2008 and 2009, respectively (Fig. 2.22). Based on the most recent assessment of this species, the southern hake stock is suffering reduced reproductive capacity and is at risk of being harvested unsustainably (ICES, 2009). The stock is outside the safe biological limits and the spawning biomass had decreased below the precautionary approach level (BPA ¼ 35,000 tonnes) in 1985, and it has remained at that level ever since. Moreover, fishing mortality has increased in recent years and is well above the precautionary fishing mortality level

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Figure 2.22 Spawning stock biomass and recruitment (age 0) as well as the biological reference points of the southern stock of European hake. BPA is the biomass below which the stock would be regarded as potentially depleted or over-fished and it is judged to give a reasonable certainty that, in spite of year-to-year fluctuations, the stock will stay above BLIM. BLIM is the limit spawning stock biomass, below which recruitment is impaired or the dynamics of the stock are unknown. In the case of southern hake population, BPA and BLIM are set at 35,000 and 25,000 tonnes, respectively (ICES, 2009).

(FPA ¼ 0.4) and is near the limit of the fishing mortality reference point (FLIM ¼ 0.55). Due to the critical state of the population and in order to recover the population, a recovery plan was introduced in December 2005 (see Council Regulation No. 2166/2005). Therefore, the present management objectives of this stock are those explicitly established in EC Reg. No. 2166/2005. The objective of the European hake recovery plan for the southern stock is to increase the level of spawning biomass to levels equal to or greater than 35,000 tonnes (BPA) in two consecutive years within a period of 10 years (i.e. by 2016) and to reduce the fishing mortality to 0.27 (Ftarget). Once the biomass target level has been achieved, the Commission will introduce follow-up management measures to replace the recovery plan, as proposed for the northern hake stock. The procedure for setting the TACs will include a 10% annual reduction in fishing mortality and a 15% constraint on TAC changes between years. Although a formal evaluation of the recovery plan has not been attempted yet, it seems that in recent years, the increase in SSB has been mainly due to an improvement in recruitment since recent fishing mortality has been increasing and the TAC has been exceeded throughout the recovery period. The southern hake population is also managed by TAC and quota regulations. In addition, the following technical measures are in place: minimum length at landing of 27 cm, minimum mesh size, effort limitation, seasonal restrictions and closed area (EC No. 850/98).

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4. Future Perspectives Although European hake in the north-east Atlantic is an important fishery resource, knowledge of the biology and ecology of this species is still quite scarce. In contrast to most gadoids and demersal species, European hake appear to exhibit a high growth rate (De Pontual et al., 2003, 2006), indeterminate fecundity (Korta et al., 2010b; Murua and Motos, 1996), a protracted spawning season (Domı´nguez-Petit, 2007; Murua et al., 2006) and energy allocations to reproduction during the spawning season (Domı´nguez-Petit and Saborido-Rey, 2010). This pattern could be interpreted as European hake having adopted a more opportunistic life strategy, which is unusual for a gadoid and a demersal species. In this context, the new findings in relation to European hake growth patterns are of especial importance, because the uncertainties of age determination have hindered the use of catch-based assessment methods and have great implications for correct assessment and hence management of the species. Bertignac and De Pontual (2007) investigated the consequences of growth underestimation in the northern hake stock assessment and concluded that this bias has an effect on the absolute level of fishing mortality and stock biomass, as well as on the SSB trend. Nevertheless, they also showed that the trends in fishing mortality and recruitment are comparable and more importantly, that the population status in relation to precautionary reference points is generally the same. Therefore, the ICES Working Group is still using the ‘old’ growth pattern to carry out assessment of this stock until a new ageing protocol based on a new, validated growth pattern from tagging studies is agreed upon. Therefore, it can be expected that tagging studies will continue into the future to answer the pending questions concerning the growth patterns of hake. Similarly, it is clear that this species is not as ‘simple’ as other gadoids when studying the reproductive biology (Kjesbu et al., 2010). In the case of species of indeterminate fecundity, such as hake, fecundity should be estimated based on batch fecundity and spawning fraction estimations. While the first parameter can be obtained, it is more difficult to carry out the necessary extensive sampling of mature females for spawning fraction estimation due to the high cost of the fish in the market. However, as mentioned earlier, the combination of stereological methods (to estimate volume fractions) and the advanced OPD theory (Kurita and Kjesbu, 2009) make it possible to successfully establish hake oocyte packing densities and oocyte diameter relationships (Korta et al., 2010b) which could be used with ‘next generation’ OPD formulae to predict the total annual fecundity in indeterminate spawners, as done today for determinate spawners such as cod, amongst other species. In any case, it is necessary to continue further studies of the reproductive biology of hake to estimate batch fecundity and

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the spawning fraction because this information, in addition to providing a very useful knowledge of the hake reproductive strategy, can be used to estimate the SSB in combination with egg production estimation at sea. In contrast to normal assessment methods, one advantage of egg production estimation methods is that estimation of SSB is independent of any commercial fishery data (Gunderson, 1993; Somarakis et al., 2004). These methods estimate the SSB based upon concurrent estimates of fecundity and population egg production at sea (Gunderson, 1993; Stratoudakis et al., 2006). Moreover, fishery independent methods, whether using an egg production method (EPM) or any other suitable direct method, allow for contrasting and fine-tuning the estimates of SSB obtained using VPA-based traditional assessment methods (Armstrong et al., 2001). In addition, the application of population egg production estimation methods provides further information about the reproductive biology and reproductive behaviour of a population and about its distribution, mortality and development of early life stages, which are of particular importance in studying the underlying mechanisms of recruitment (Alheit, 1993). In this sense, Murua et al. (2010a) presented, for the first time, an application of the daily egg production method (DEPM) to hake. Despite limitations in the estimation of various parameters, these authors concluded that DEPM can potentially be applied to European hake. However, as European hake was not a target species of the triennial egg research surveys used in this study, they concluded that the egg sampling strategy at sea should be adapted to the spawning behaviour of hake. In any case, it would be convenient to continue with this type of work because an independent estimation may be obtained that would be very useful for comparing with VPA-based assessments, especially considering the problems of age uncertainties which are associated with this species. In the case of European hake, environmental and biological factors may lead to large inter-annual variations in egg production per unit of SSB due to the reproductive strategy described earlier, which could have implications in the assessment of this population, as for other indeterminate species (for northern anchovy, Hunter and Leong, 1981; for European anchovy Engraulis encrasicolus L., Somarakis et al., 2004). As mentioned before, this could also affect the stock-recruitment relationship used in the assessment, as normally, the SSB is estimated without accounting for various reproductive and population characteristics which can influence egg production. In this context, Murua et al. (2010b), using the management strategy evaluation (MSE), concluded that the inclusion of improved biological and fecundity information affected the perception of population dynamics, the BRPs and also the perception of the stock in relation to these BRPs. Similarly, the management performance, that is, the capacity of maintaining the population above BRPs, was different between the SSB estimated in the working group and in the population when realistic reproductive

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characteristics were included. Murua et al. (2010b) concluded that the probability of a wrong perception, that is, the working group population (using the SSB) perception in relation to the BRP was contrary to the perception using alternative reproductive indices, could be different for the different reproductive potential indices studied. They also showed that use of the MSE simulation framework can be regarded as a valuable tool for testing the suitability of including a greater biological reproductive ‘realism’ into assessment strategies, which can be easily extended to investigate the different sources of uncertainty in the data and models during the assessment and management processes of European hake (e.g. growth). In summary, further work in all aspects of European hake biology, ecology and assessment are necessary to address the many questions about this ‘peculiar’ gadoid species, which is a commercially important species that has been harvested since ancient times and was first described as a sea pike in the sixteenth century.

ACKNOWLEDGEMENTS This review has been funded by the Department of Agriculture and Fisheries of Basque Country and Government and various European Union Research projects (Study Contract No. 95/038 ‘BIOSDEF’, Study Contract No. 97/015 ‘DEMASSESS’ and QLRT-200101825 ‘RASER). The author is indebted to all the people who at different stages helped me to carry out the work. I want to thank the colleagues of AZTI Tecnalia who have collaborated in the biological sampling and in the analysis of the samples to carry out some of the work reviewed here. This paper is contribution number 505 from AZTI-Tecnalia (Marine Research Department).

REFERENCES Adams, A. (1864). Manual Nat. Hist., 194. In: G. B. Goode and T. H. Bean, 1895, 386. Albaina, A., and Irigoien, X. (2004). Relationships between frontal structures and zooplankton communities along a cross-shelf transect in the Bay of Biscay (1995 to 2003). Mar. Ecol. Prog. Ser. 284, 65–75. Alheit, J. (1986). A new method for determining batch fecundity of hake (Genus: Merluccidae). ICES CM 1986/G, 62. Alheit, J. (1993). Use of the daily egg production method for estimating biomass of clupoid fishes: A review and evaluation. Bull. Mar. Sci. 53, 750–767. A´lvarez, P., and Cotano, U. (2005). Growth, mortality and hatch-date distributions of European hake larvae, Merluccius merluccius (L.), in the Bay of Biscay. Fish. Res. 76(3), 307–486. ´ lvarez, P., Motos, L., Uriarte, A., and Egan˜a, J. (2001). Spatial and temporal distribution of A European hake, Merluccius merluccius (L.), eggs and larvae in relation to hydrographical conditions in the Bay of Biscay. Fish. Res. 50, 111–128. ´ lvarez, P., Fives, J., Motos, L., and Santos, M. (2004). Distribution and abundance of A European hake Merluccius merluccius (L.), eggs and larvae in the North East Atlantic water in 1995 and 1998 in relation to hydrographic conditions. J. Plankton Res. 26(7), 811–826.

The Biology and Fisheries of European Hake

145

Angelescu, J., Gneri, F. S., and Nani, A. (1958). La merluza del mar Argentino (biologı´a y taxonomı´a). Servicio de Hidrographia Naval, Secretaria de Marina, Buenos Aires Publicacio´n H 1004, 224pp. Armstrong, M. J. P., Conolly, P., Nash, R. D. M., Pawson, M. G., Alesworth, E., Coulahan, P. J., Dickey-Collas, M., Milligan, S. P., O’neill, M. F., Witthames, P. R., and Woolner, L. (2001). An application of the annual egg production method to estimate the spawning biomass of cod (Gadus morhua L), plaice (Pleuronectes platessa L.) and sole (Solea solea L.) in the Irish Sea. ICES J. Mar. Sci. 58, 183–203. Bagenal, T. B. (1954). Growth rate of the hake (Merluccius merluccius L.) in the Clyde and other Scottish areas. J. Mar. Biol. Assoc. UK 33, 69–95. Bailey, K. M. (1981). An analysis of the spawning, early life history and recruitment of the Pacific hake Merluccius productus. University of Washington, Seattle, WA, (Ph. D. Thesis, 156 p). Balbotin, F., and Fischer, W. (1981). Ciclo sexual y fecundidad de la Merluza, Merluccius gayi gayi, en la costa de Chile. Rev. Biol. Mar. Inst. Oceanol. Univ. Valparaı´so 17(3), 285–334. Belloc, G. (1935). E´tude monographique du merlu (Merluccius merluccius L.), 3eme partie. Revue Trav. Off. (Scient. Tech.) Pech. marit. 8(2), 145–202. Belon, P. (1553). De aquatilibus, libri duo cum eiconibus ad viuam ipsorum effigiem, quoad eius fieri potuit, expressis. Ad amplissimum Cardinalem Castillionæum 1–31 (1–448, Parisiis (Stephanus)). Bertignac, M., and de Pontual, H. (2007). Consequences of bias in age estimation on assessment of the northern stock of European hake (Merluccius merluccius) and on management advice. ICES J. Mar. Sci. 64, 981–988. Beverton, R. J. H., and Holt, S. J. (1957). On the dynamics of exploited fish populations. Fish. Invest. Lond., Ser. II 19, 533. Bezzi, S. I., Verazay, G. A., and Dato, C. V. (1995). Biology and fisheries of Argentine hakes. In “Hake: Fisheries, Ecology and Markets”. (J. Alheit and T. J. Pitcher, eds.), Fish and Fisheries Series. 15, pp. 239–263. Chapman and Hall, London. Bianchi, G., Carpenter, K. E., Roux, J. P., Molloy, F. J., Boyer, D., and Boyer, H. J. (1993). FAO species identification field guide for fishery purposes. The living marine resources of Namibia. FAO, Rome, 250 p. Boreman, J. Nakashima, B. S. Wilson, J. A. and Kendall, R. L. (eds.) (1997). Northwest Atlantic Groundfish: Perspectives on a Fishery CollapseAmerican Fisheries Society, Bethesda, Maryland. Boucher, J. (1985). Caracte´ristiques physiques et biologiques. In “Peuplements profonds du golfe de Gascogne” (L. Laubier and C. Monniot, eds.), pp. 25–42. IFREMER, Paris. Cabral, H. N., and Murta, A. G. (2002). The diet of blue whiting, hake, horse mackerel and mackerel off Portugal. J. Appl. Ichthyol. 18(1), 14–23. Cardinale, M., and Arrhenius, F. (2000). The relationship between stock and recruitment: Are the assumptions valid? Mar. Ecol. Prog. Ser. 196, 305–309. Casey, J., and Pereiro, J. (1995). European hake (M. merluccius) in the North-east Atlantic. In “Hake: Fisheries, Ecology and Markets”. (J. Alheit and T. J. Pitcher, eds.), Fish and Fisheries Series. 15, pp. 125–147. Chapman and Hall, London. Castillo, A. G. F., Martinez, J. L., and Garcia-Vazquez, E. (2004). Fine spatial structure of Atlantic hake (Merluccius merluccius) stocks revealed by variation at microsatellite loci. Mar. Biotechnol. 6, 299–306. Castillo, A. G. F., A´lvarez, P., and Garcia-Vazquez, E. (2005). Population structure of Merluccius merluccius along the Iberian Peninsula coast. ICES J. Mar. Sci. 62, 1699–1704 10.1016/j.icesjms.2005.06.001. Chambers, R. C., and Trippel, E. A. (1997). In “Early Life History and Recruitment in Fish Populations” (R. C. Chambers and E. A. Trippel, eds.). Champman and Hall, London.

146

Hilario Murua

Ciechomski, J. D. (1967). Cara´cter del desove y fecundidad de la merluza argentina, Merluccius hubbsi, del sector bonaerense. Bol. Inst. Biol. Mar. 8, 1–123. Christiansen, H. E., and Cousseau, M. B. (1971). Reproduction of the hake in the Argentine Sea. II: Hake reproduction and its relationship with others biological aspects of the species. Bol. Inst. Biol. Mar. 20, 43–75. Cohen, D. M., Inada, T., Iwamoto, T., and Scialabba, N. (1990). FAO Species catalogue. vol. 10. Gadiform fishes of the world (Order Gadiformes). An annotated and illustrated Catalogue of Cods, Hakes, Grenadiers and other Gadiform fishes Known to Date. FAO Fish. Synopsis 125, 10–442. Colman, J. A. (1995). Biology and fisheries of New Zealand hake (M. australis). In “Hake: Fisheries, Ecology and Markets” (J. Alheit and T. J. Pitcher, eds.), Fish and Fisheries Series. 15, pp. 365–387. Chapman and Hall, London. Cowan, J. H., and Shaw, R. F. (2002). Recruitment. In “Fishery Science: The Unique Contributions of Early Life Stages” (L. A. Fuiman and R. G. Werner, eds.), pp. 88–111. Blackwell Publishing, Oxford Chapter 4. Cushing, D. H. (1975). Marine Ecology and Fisheries. Cambridge University Press, Cambridge, England, 278 pp. Cushing, D. H. (1990). Plankton production and year-class strength in fish populations: An update of the match/mismatch hypothesis. Adv. Mar. Biol. 26, 249–292. De Pontual, H., Groison, A. L., Pin˜eiro, C., and Bertignac, M. (2006). Evidence of underestimation of European hake growth in the Bay of Biscay and the relationship with bias in the agreed ageing method. ICES J. Mar. Sci. 63(9), 1674–1681 10.1016/j. icesjms.2006.07.007. De Pontual, H., Bertignac, M., Battaglia, A., Bavouzet, G., Moguedet, P., and Groison, A. L. (2003). A pilot tagging experiment on European hake (Merluccius merluccius): Methodology and preliminary results. ICES J. Mar. Sci. 60, 1318–132710.1016/ S1054-3139(03)00149-8. Descamps, P., and Labastie, J. (1978). Note sur la lecture et l’interpretation des otolithes du merlu. ICES CM 1978/G(41), 21 pp. Domı´nguez-Petit, R., and Saborido-Rey, F. (2010). New bioenergetic perspective of European hake (Merluccius merluccius L.) reproductive ecology. Fish. Res. 10.1016/j. fishres.2009.09.002. Domı´nguez-Petit, R., Korta, M., Saborido-Rey, F., Murua, H., Sainza, M., and Pineiro, C. (2008). Analysis of the influence of stock structure and environmental changes in size at maturity for both European hake Atlantic populations. J. Mar. Syst. 71, 260–278. Domı´nguez-Petit, R. (2007). Study of reproductive potential of Merluccius merluccius in the Galician Shelf. University of Vigo, Spain, (Doctoral Thesis, doi:10261/4377). Erkamov, Y. K. (1974). The biology and fishery of Pacific hake, Merluccius productus. Ph.D. Dissertation. Pac. Sci. Inst. Mar. Fish. Oceanogr. (TINRO), Vladivostok. Evans, R. P., Parrish, C. C., Brown, J. A., and Davis, P. J. (1996). Biochemical composition of eggs from repeat and first-time spawning captive Atlantic halibut (Hippoglossus hippoglossus). Aquaculture 139, 139–149. FAO (2010). Fishery Information. Data and Statistics Unit (FIDI), c2006. Farin˜a, A. C., and Ferna´ndez, A. (1986). Datos biolo´gicos de la merluza del oeste de Irlanda. Informes Te´cnicos Instituto Espan˜ol Oceanografı´a 47, 1–13. Fedotov, V. F. (1976). Gadidae of the palaeogene-neogene from the USSR, 157. Trudy Paleontology Institute of SSR, pp. 1–84. Ferna´ndez, J. (1985). Estudio parasicolo´gico de Merluccius australis (Hutton, 1872) (Pises: Merluccidae): Aspectos sistema´ticos, estadı´sticos y zoogeogra´ficos. Bol. Soc. Biol. Concepcio´n 56, 31–41.

The Biology and Fisheries of European Hake

147

Flick, G. J., Hong, G. P., Hwang, J. W., and Arganosa, G. C. (1990). Groundfish. In “The Seafood Industry” (R. E. Martin and G. J. Flick, eds.), pp. 32–66. Van Nostrand Reinhold, New York. Foucher, R. P., and Beamish, R. J. (1977). A review of oocyte development in fishes with special reference to Pacific hake (Merluccius productus). Fish. Mar. Ser. Tech. Rep. 755, 16. Frouin, R., Fiu´za, A. F. G., A´mbar, I., and Boyd, T. J. (1990). Observations of a poleward surface current off the coasts of Portugal and Spain during winter. J. Geophys. Res. 95 (C1), 679–691. Garcia, S. (1982). Distribution, migration and spawning of the main fish resources in the northern CECAF area. In “FAO CECAF/ECAF Series 82/25” (9 pp., 10 maps). FAO, Rome. Gilbert, D. J. (1997). Towards a new recruitment paradigm for fish stocks. Can. J. Fish. Aqua. Sci. 54, 969–977. Gill, T. (1884). On the Anacanthini fishes. Proc. Acad. Nat. Sci. Philadelphia 36, 167–183. Gon˜i, R. (1983). Growth studies of European hake (Merluccius merluccius L.) from the Northwest African shelf. ICES, CM 1983/G, 10. Gon˜i, R., and Pin˜eiro, C. (1988). Study of the growth pattern of European hake (Merluccius merluccius L.) from the Southern stock: ICES Divisions VIIIc and IXa. ICES, CM 1988/ G(18), 13. Gonzalez, R., Olaso, I., and Pereda, P. (1985). Contribucio´n al conocimiento de la alimentacio´n de la merluza (Merluccius merluccius L.) en la plataforma continental de Galicia y del Canta´brico. Boletı´n del Instituto Espan˜ol de Oceanografı´a 2, 49–60. Goode, G. B., and Bean, T. H. (1896). Oceanic Ichthyology, a treatise on the deep-sea and pelagic fishes of the world, based chiefly upon the collections made by steamers “Blake”, “Albatross” and Fish “Hawk” in the northwestern Atlantic. (Smithson. Contrib. Knowl., 30 y Spec. Bull. U.S. natn. Mus., 1895 y Mem. Mus. Comp. Zool. Harv., 1 (Text): XXXV þ 1-553; 2 (Atlas): XXIII þ -26, 123 pl., 417 fig). Grant, W. S., and Leslie, R. W. (2001). Inter-ocean dispersal is an important mechanism in the zoogeography of hakes (Pisces: Merluccius spp.). J. Biogeogr. 28, 699–721. Guichet, R. (1988). Etude de la croissance du merlu europeen (Merluccius merluccius L.) au cours de ses premieres annees. Analyse pare NORMSEP des distributions en taille observe´es trimestriellement en mer de 1980-87. Working Paper in ICES CM 1988/ WP. Assess: 24. Guichet, R. (1995). The diet of European hake (Merluccius merluccius) in the northern part of the Bay of Biscay. ICES J. Mar. Sci. 52, 21–31. Guichet, R., Quero, J. C., and Labastie, J. (1973). Estimation du stock de merlu au nord et a l’ouest de l’Irlande. ICES CM/G 5, 9. Gunderson, D. R. (1993). Surveys of Fisheries Resources. Wiley, New York, 248 pp. Gu¨nther, A. (1873). Erster ichthyologischer Beitrag nach Exemplaren aus dem Museum Godeffroy. J. Mus. Godeffroy 97–103. Gu¨nther, A. (1887). Report on the Deep-sea Fishes collected by H. M. S. hallenger during the years 1873-76. Challenger Reports Zool. 22, LXV þ 268. Harden Jones, F. R. (1968). Fish Migration. Edward Arnold, London, UK, 325 pp. Hart, J. L. (1973). Pacific fishes of Canada. Fish. Res. Board Can. Bull. 180, 1–740. Haynes, R., and Barton, E. D. (1990). A poleward flow along the Atlantic coast of the Iberian Peninsula. J. Geophys. Res. 95(C7), 11425–11441. Helser, T. E., Almeida, F. P., and Waldron, D. E. (1995). Biology and fisheries of Northwest Atlantic hake (silver hake: M. bilinearis). In “Hake: Fisheries, Ecology and Markets” (J. Alheit and T. J. Pitcher, eds.), Fish and Fisheries Series. 15, pp. 203–233. Chapman and Hall, London. Hickling, C. F. (1927). The natural history of the Hake—Parts I and II. Fish. Invest. Ser. II X (2), 79.

148

Hilario Murua

Hickling, C. F. (1933). The natural history of the hake. Part 3. Seasonal changes in the condition of hake. U.K. Fish. Invest. Ser. II 12(1), 120. Hilborn, R., and Walters, C. J. (1992). Quantitative Fisheries Stock Assessment: Choice, Dynamics and Uncertainty. Chapman and Hall, New York. Hjort, J. (1914). Fluctuations in the great fisheries of northern Europe. ICES Rapports et Proces-Verbaux des Re´unions. Conseil International pour l’E´xploration de la Mer 20, 1–228. Ho, J. S. (1974). Parasitic copepods as indicator of hake’s (Merluccius) zoogeography. Proc. 3rd Int. Congr. Parasitol. 3, 1633–1634. Ho, J. S. (1990). Phylogeny and biogeography of hakes (Merluccius; Teleostei): A cladistic analysis. U.S. Fish. Bull. 88, 95–104. Hunter, J. R., and Goldberg, S. R. (1980). Spawning incidence and batch fecundity in Northern anchovy, Engraulis mordax. Fish. Bull. 77(3), 641–652. Hunter, J. R., and Leong, R. (1981). The spawning energetics of female northern anchovy, Engraulis mordax. Fish. Bull. 79, 215–229. Hunter, J. R., and Macewicz, B. (1985). Measurement of spawning frequency in multiple spawning fishes. In “An Egg Production Method for Estimating Spawning Biomass of Pelagic Fish: Application to the Northern Anchovy, Engraulis mordax”. (R. Lasker, ed.), NOAA Technical Report NMFS. 36, pp. 79–94. Hunter, J. R., and Macewicz, B. J. (2003). Improving the accuracy and precision of reproductive information used in fisheries. In “Modern Approaches to Assess Maturity and Fecundity of Warm- and Cold-Water Fish and Squids” . (S. Kjesbu, J. R. Hunter and P. R. Witthames, eds.), Fisken og havet. 12, pp. 57–68. Hunter, J. R., Lo, N. C. H., and Leong, R. (1985). Batch fecundity in multiple spawning fishes. In “An Egg Production Method for Estimating Spawning Biomass of pelagic fish: Application to the Northern Anchovy, Engraulis mordax”. (R. Lasker, ed.), NOAA Technical Report NMFS. 36, pp. 67–78. Hunter, J. R., Macewicz, B. J., Lo, N. C. H., and Kimbrell, C. A. (1992). Fecundity, spawning, and maturity of female Dover sole, Microstomus pacificus, with an evaluation of assumptions and precision. Fish. Bull. USA 90, 101–128. Ibaibarriaga, L., Irigoien, X., Santos, M., Motos, L., Fives, J. M., Franco, C., Lago de Lanzos, A., Acebedo, S., Bernal, M., Bez, N., Eltink, G.Farinha, A. et al. (2007). Egg and larvae distribution of seven fish species in the North East Atlantic waters. Fish. Oceanogr. 16(3), 284–293. ICES (International Council for the Exploration of the Sea) (1991). Report of the Working Group on the assessment of the stocks of hake. ICES CM 1991/Assess(20), 181 pp. ICES (International Council for the Exploration of the Sea) (1999a). Report of the Working Group on the assessment of southern shelf demersal stocks. ICES CM 1999/ACFM(4), 655 pp. ICES (International Council for the Exploration of the Sea) (1999b). Report of the Working Group on the assessment of southern shelf demersal stocks. ICES CM 2000/ACFM(4). ICES (International Council for the Exploration of the Sea) (2009). Report of the Working Group on the assessment of southern shelf stocks of hake, Monk and Megrim (wghmm). ices advisory committee on fishery management. ICES CM 2009/ACFM. Iglesias, S., and Dery, L. (1981). Age and growth studies of hake (Merluccius merluccius L.) from ICES Divisions VIIIc and IXa. ICES CM 1981/G(38), 6. Inada, T. (1981). Studies on the Merlucciid fish. Bull. Far Seas Fish Res. Lab. Shimizu, Japan 18, 1–172. Inada, T. (1990). Family Merluccidae. In “FAO species catalogue, Gadiform fishes of the world (order Gadiformes). An annotated and illustrated catalogue of cods, hakes, grenadiers and other gadiform fishes known to date” (D. M. Cohen, T. Inada, T. Iwamoto and N. Scialabba, eds.), FAO Fisheries Synopsis. 125, pp. 327–344. FAO, Rome.

The Biology and Fisheries of European Hake

149

Kabata, Z., and Ho, J. S. (1981). The origin and dispersal of hake (genus Merluccius: Pisces: Teleostei) as indicated by its copepod parasites. Oceanogr. Mar. Biol. Annu. Rev. 19, 381–404. Kacher, M., and Amara, R. (2005). Distribution and growth of 0-group European hake in the Bay of Biscay and Celtic Sea: A spatial and inter-annual analyses. Fish. Res. 71, 373–378. Keigwin, L. D. Jr. (1978). Pliocene closing of the Isthmus of Panama, based on biostratigraphic evidence from nearby Pacific Ocean and Caribbean sea cores. Geology 6, 630–634. Keigwin, L. D. Jr. (1982). Isotopic paleooceanography of the Caribbean and East Pacific: Role of Panama uplift in late Neogene time. Science 217, 350–353. Kimura, D. K., and Chikuni, S. (1987). Mixtures of empirical distributions: an iterative application of the age - length key. Biometrics 43, 23–35. Kjesbu, O. S., Witthames, P. R., Solemdal, P., and Greer Walker, M. (1998). Temporal variations in the fecundity of Arcto-Norwegian cod (Gadus morhua) in response to natural changes in food and temperature. J. Sea Res. 40, 303–321. Kjesbu, O. S., Murua, H., Witthames, P., and Saborido-Rey, F. (2010). Method development and evaluation of stock reproductive potential of marine fish. Fisheries Research 104, 1–7. Korta, M., Domı´nguez-Petit, R., Murua, H., and Saborido-Rey, F. (2010a). Regional variability in reproductive traits of European hake Merluccius merluccius L. populations. Fisheries Research 104, 64–72. Korta, M., Murua, H., Kurita, Y., and Kjesbu, O. S. (2010b). How are the oocytes recruited in an indeterminate fish? Applications of stereological techniques along with advanced packing density theory on European hake (Merluccius merlucssius L.). Fisheries Research 104, 56–63. Koslow, J. A. (1992). Fecundity and the stock-recruitment relationship. Can. J. Fish Aqua. Sci. 49, 210–217. Koutsikopoulos, C., and Le Cann, B. (1996). Physical processes and hydrological structures related to the Bay of Biscay anchovy. Sci. Mar. 60, 9–19. Kurita, Y., and Kjesbu, O. S. (2009). Fecundity estimation by oocyte packing density formulae in determinate and indeterminate spawners: Theoretical considerations and applications. J. Sea Res. 61, 188–196. Lasker, R. (1985). An egg production method for estimating spawning biomass of pelagic fish: Application to the northern Anchovy, Engraulis mordax. NOAA Tech. Rep. NMFS 36, 99. Lavin, A., Dı´az del Rı´o, G., Cabanas, J. M., and Casas, G. (2000). Afloramiento en el noroeste de la penı´nsula Ibe´rica. ´Indices de afloramiento para el punto 43 N 11 W. Periodo 1990–1999. Datos y resu´menes Inst. Esp. Oceanogr. 15, 25. Lavin, A., Valdes, L., Sanchez, F., Abaunza, P., Forest, A., Boucher, J., Lazure, P., and Jegou, A. M. (2004). The Bay of Biscay: The encountering of the ocean and the shelf. In “The Sea, 14” (A. R. Robinson and K. H. Brink, eds.), pp. 933–1001 Chapter 24. Linnaeus, C. (1758). Systema Naturae. X edn. vol. 1, 824 p. Nantes y Pisces, 230–338. Lloris, D., and Matallanas, J. (2003). Description of a new species of hake: Merluccius patagonicus sp. nov. (Gadiformes, Merlucciidae) from the waters of Argentina. Sci. Mar. 67(3), 323–326. Lloris, D., Matallanas, J., and Oliver, P. (2003). Merluzas del mundo (Familia Merlucciidae). Cata´logo comentado e ilustrado de las merluzas conocidas. FAO Cata´logo de especies para los fines de la pesca 2, 69. Lucio, P., Murua, H., and Santurtun, M. (2000). Growth and reproduction of hake (Merluccius merluccius) in the Bay of Biscay during the period 1996-1997. Ozeanografika 3, 325–354.

150

Hilario Murua

Lundy, C. J., Moran, P., Rico, C., Millner, R. S., and Hewitt, G. M. (1999). Macrogeographical population differentiation in oceanic environments: A case study of European hake (Merluccius merluccius), a commercially important fish. Mol. Ecol. 8, 1889–1898. Ma, Y., Kjesbu, O. S., and Jorgensen, T. (1998). Effects of ration on the maturation and fecundity in captive Atlantic herring (Clupea harengus). Can. J. Fish Aqua. Sci. 55, 900–908. Macchi, G. J., Pa´jaro, M., and Ehrlich, M. (2004). Seasonal egg production pattern of the Patagonian stock of Argentine hake (Merluccius hubbsi). Fish. Res. 67, 25–38. Marshall, T., Kjesbu, O. S., Yaragina, N. A., Solemdal, P., and Ulltang, O. (1998). Is spawner biomass a sensitive measure of the reproductive and recruitment potential of North-east Arctic cod? Can. J. Fish. Aqua. Sci. 55, 1766–1783. Marshall, T., O’Brien, L., Tomkiewicz, J., Ko¨ster, F. W., Kraus, G., Marteinsdottir, G., Morgan, M. J., Saborido-Rey, F., Blanchard, J. L., Secor, D. H., Wright, P. J. Mukhina, N. V. et al. (2003). Developing alternative indices of reproductive potential for use in fisheries management: Case studies for stocks spanning an information gradient. J. Northwest Atlantic Fish. Sci. 33, 161–190. Marteinsdottir, G., and Steinarsson, A. (1998). Maternal influence on the size and viability of Iceland cod, Gadus morhua, eggs and larvae. J. Fish. Biol. 52, 1241–1258. Martin, I. (1991). A preliminary analisis of some biological aspects of Hake (M. merluccius L. 1758) in the Bay of Biscay. ICES CM 1991/G, 54 (Demersal Fish Commitee). Mathews, C. P. (1985). Meristic studies of the Gulf of California species of Merluccius, with a description of a new species. J. Nat. Hist. 19, 697–718. Mattiucci, S., Abaunza, P., Ramadori, L., and Nascetti, G. (2004). Genetic identification of Anisakis larvae in European hake from Atlantic and Mediterranean waters for stock recognition. J. Fish. Biol. 65(2), 495–510. Meriel-Busy, M. (1966). La croissance du merlu dans le Golfe de Gascogne. ICES CM 1966/G(17), 5. Methot, R. D., and Dorn, M. W. (1995). Biology and fisheries of North Pacific hake (M. productus). In “Hake: Fisheries, Ecology and Markets”. (J. Alheit and T. J. Pitcher, eds.), Fish and Fisheries Series. 15, pp. 389–413. Chapman and Hall, London. Miller, T. J. (2002). Assemblages, communities, and species interactions. In “Fishery Science: The unique contributions of early life stages”. (L. A. Fuiman and R. G. Werner, eds.), pp. 183–205. Blackwell Publishing, Oxford (Chapter 8). Morales-Nin, B., Torres, G. J., Lombarte, A., and Recasens, L. (1998). Otolith growth and age estimation in the European hake. J. Fish Biol. 53(6), 1155–1168. Murua, H., and Motos, L. (1996). Reproductive modality and Batch fecundity of the European hake, Merluccius merluccius. ICES CM 1996/G, 40. Murua, H., and Saborido-Rey, F. (2003). Female reproductive strategies of commercially important fish species in the North Atlantic. J. Northwest Atlantic Fish. Sci. 33, 23–32. Murua, H., and Motos, L. (2006). Reproductive strategy and spawning activity of the European Hake Merluccius merluccius (L.) in the Bay of Biscay. J. Fish Biol. 69, 1288–1303 10.1111/j.1095-8649.2006.01169.x. Murua, H., Motos, L., and Lucio, P. (1998). Reproductive modality and batch fecundity of the European hake (Merluccius merluccius L.) in the Bay of Biscay. Calif. Cooper. Ocean. Fish. Invest. Rep. 39, 196–203. Murua, H., Lucio, P., Santurtun, M., and Motos, L. (2006). Seasonal variation in egg production and batch fecundity of European hake Merluccius merluccius (L.) in the Bay of Biscay. J. Fish. Biol. 69, 1304–131610.1111/j.1095-8649.2006.01209.x. Murua, H., Kraus, G., Saborido-Rey, F., Witthames, P. R., Thorsen, A., and Junquera, S. (2003). Procedures to estimate fecundity of marine fish species in relation to their reproductive strategy. J. Northwest Atlantic Fish. Sci. 33, 33–54.

The Biology and Fisheries of European Hake

151

Murua, H., Ibaibarriaga, L., A´lvarez, P., Santos, M., Korta, M., Santurtun, M., and Motos, L. (2010a). The daily egg production method: A valid tool for application to European hake in the Bay of Biscay? Fish. Res 104, 100–110. Murua, H., Quincoces, I., Garcia, D., and Korta, M. (2010b). Is the northern European hake, Merluccius merluccius, management robust to the exclusion of reproductive dynamics? Fish. Res. 104, 123–135. Myers, R. A. (1997). Comment and reanalysis: Paradigms for recruitment studies. Can. J. Fish Aqua. Sci. 54, 978–981. OSPAR Commission (2000). Quality Status Report 2000: Region IV—Bay of Biscay and Iberian coast OSPAR Commission, London, (134 þ XIII pp). Pa´jaro, M., and Macchi, G. J. (2001). Distribucio´n espacial y estimacio´n de la talla de primera maduracio´n del stock patago´nico de merluza (Merluccius hubbsi) en el perı´odo de puesta Diciembre-Abril 2000-2001. Tech. Rep. INIDEP (Argentina) 100/01, 14. Parker, K. (1980). A direct method for estimating northern anchovy, Engraulis mordax, spawning biomass. Fish. Bull. 78(2), 541–544. Paulik, G. J. (1973). Studies of the possible form of the stock-recruitment curve. ICES Rapp. Proc-Verb. 164, 302–315. Payne, A. I. L., and Punt, A. E. (1995). Biology and fisheries of South African Cape hakes (M. capensis and M. paradoxus). In “Hake: Fisheries, Ecology and Markets”. (J. Alheit and T. J. Pitcher, eds.), Fish and Fisheries Series. 15, pp. 15–44. Chapman and Hall, London. Pereda, P., and Olaso, I. (1990). Feeding of hake and monkfish in the non-trawlable area of the shelf of the Cantabrian Sea. ICES CM 1990/G, 45. Pereiro, F. J., Sanchez, F., and Fontenla, J. (1991). Hake recruitment in the southern stock (Int. Council Explor. Sea Divisions VIIIc and IXa). ICES CM 1991/G(52), 17. Pe´rez, N., and Pereiro, F. J. (1985). Aspectos de la reproduccio´n de la merluza, M. merluccius, de la plataforma gallega y canta´brica. Bol. Ins. Esp. Ocean 3, 39–47. Pianka, E. R. (2000). Evolutionary Ecology. Benjamin-Cummings, USA. Pin˜eiro, C. G., and Hunt, J. J. (1989). Comparative study on growth of European hake (Merluccius merluccius L.) from southern stock using whole and sectioned otoliths, and length frequency distributions. ICES CM 1989/G, 37. Pin˜eiro, C. G., and Pereiro, J. A. (1993). Study on juvenile growth pattern of European hake (Merluccius merluccius L.) using whole otoliths and length frequency distributions from commercial caches and fish surveys. ICES CM 1993/G, 12. Pin˜eiro, C., and Saı´nza, M. (2003). Age estimation, growth and maturity of the European hake (Merluccius merluccius) from Iberian Atlantic waters. ICES J. Mar. Sci. 60, 1086–1102. Pin˜eiro, C., Rey, J., De Pontual, H., and Gon˜i, R. (2007). Tag and recapture of European hake (Merluccius merluccius L.) off the Northwest Iberian Peninsula: First results support fast growth hypothesis. Fish. Res. 88, 150–154. Pin˜eiro, C., Rey, J., de Pontual, H., and Garcia, A. (2008). Growth of Northwest Iberian juvenile hake estimated by combining sagittal and transversal otolith microstructure analyses. Fish. Res. 93, 173–178. Pingree, R. D., and Le Cann, B. (1990). Structure, strength, and seasonality of the slope current in the Bay of Biscay region. J. Mar. Biol. Ass. UK 70, 857–885. Pingree, R. D., and Le Cann, B. (1992). Three anticyclonic slope water oceanic eDDIES (SWODDIES) in the southern Bay of Biscay in 1990. Deep Sea Res. 39, 1147–1175. Pitcher, T. J., and Alheit, J. (1995). What makes a hake? A review of the critical biological features that sustain global hake fisheries. In “Hake: Fisheries, Ecology and Markets”. (J. Alheit and T. J. Pitcher, eds.), Fish and Fisheries Series. 15, pp. 1–13. Chapman and Hall, London. Pla, C., and Rolda´n, M. I. (1994). Estructura gene´tica de la merluza europea (Merluccius merluccius) y su relacio´n con la gestio´n pesquera. In “Estado actual de los conocimientos de las poblaciones de Merluza que habitan la plataforma continental atla´ntica y mediterra´nea

152

Hilario Murua

de la Unio´n Europea con especial atencio´n a la Penı´nsula Ibe´rica". (Vigo, 13 a 17 de Diciembre de 1993)” (A. Gonza´lez-Garce´s and F. J. Pereiro, eds.), p. 327. Publicacio´n Privada, Vigo. Puillat, I., Lazure, P., Je´gou, A. M., Planque, B., and Lampert, L. (2003). Mesoscale, interannual and seasonal hydrological variability over the French continental shelf of the Bay of Biscay during the 1990s. ICES Mar. Sci. Symp. 219, 333–336. Quinteiro, J., Vidal, R., and Rey Me´ndez, M. (2000). Phylogeny and biogeographic history of hake (genus Merluccius), inferred from mitochondrial control-region sequences. Mar. Biol. 136, 163–174. Rafinesque, S. (1810). Caratteri di alcuni nuovi generi e nuove specie di animalie pinte dolla Sicili. Palermo (Reimpresio´n A. Asher, Amsterdam, 1967), 105 pp. Recasens, L., Lombarte, A., Morales-Nin, B., and Torres, G. J. (1998). Spatiotemporal variation in the population structure of the European hake in the NW Mediterranean. J. Fish Biol. 53, 387–401. Ricker, W. E. (1954). Stock and recruitment. J. Fish. Res. Board Can. 11, 559–623. Risso, A. (1827). Histoire naturelle des principales productions de l’Europe me´ridionale, et particulie`rement de celles des environs de Nice et des Alpes maritimes. F. G. Levrault, Paris & Strasbourg. Vol. 3, i-xvi, þ 1-480. Rijnsdorp, A. D. (1991). Changes in fecundity of female North Sea plaice (Pleuronectes platessa L.) between three periods since 1900. ICES J. Mar. Sci. 48(3), 253–280. Rinchard, J., and Kestenmont, R. (2003). Liver changes related to oocyte growth in roach a single spawner fish, and in bleak and white bream, two multiple spawner fish. Int. Rev. Hydrobiol. 88(1), 68–76. Rı´os, A. F., Pe´rez, F. F., and Fraga, F. (1992). Ana´lisis histo´rico de la evolucio´n superficial de los estuarios del Paı´s Vasco. Lurralde 15, 199–227. Robles, R., Pereiro, J. A., Iglesias, S., and Pereiro, F. J. (1975). E´tude sur la croissance du merlu europeen, Merluccius merluccius L. du NW de L’Espagne. ICES CM 8, 17. Rolda´n, M. I., Garcı´a-Marı´n, J. L., Utter, F. M., and Pla, C. (1998). Population genetic structure of European hake, Merluccius merluccius. Heredity 81, 327–334. Rolda´n, M. I., Garcı´a-Marı´n, J. L., Utter, F. M., and Pla, C. (1999). Genetic relationships among Merluccius species. Heredity 83, 79–86. Rothschild, B. J., and Fogarty, M. J. (1989). Spawning stock biomass: A source of error in recruitment/stock relationships and management advice. ICES J. Cons. 45, 131–135. Sa´nchez, F., and Gil, J. (2000). Hydrographic mesoscale structures and Poleward Current as a determinant of hake (Merluccius merluccius) recruitment in southern Bay of Biscay. ICES J. Mar. Sci. 57, 152–170. Sarano, F. (1986). Cycle ovarien du Merlu, M. merluccius, poisson a` ponte Fractione´e. Revue des Travaux de l’Institut des Peches Maritimes 48(1 et 2), 65–76. Saville, A. (1964). Estimation of the abundance of a fish stock from egg and larvae surveys. ICES Rapports et Proces-Verbaux des Re´unions. Conseil International pour l’E´xploration de la Mer 155M, 164–173. Savin, S. M., Douglas, R. G., and Stehli, F. G. (1975). Tertiary marine paleotemperature. Bull. Geol. Soc. Am. 86, 1499–1510. Scotton, L. N., Smith, R. E., Smith N. S., Price, K. S., and De Sylva, D. P. (1973). Pictoral guide to fish larvae of Delaware Bay. Del. Bay. Rep. Ser. Coll. Mar. Stud. Univ. Del. 7, 206 p. Secor, D. H. (2002). Historical roots of the migration triangle. ICES Mar. Sci. Symp. 215, 323–329. Sheperd, J. G. (1982). A versatile new stock-recruitment relationship for fisheries, and the construction of sustainable yield curves. ICES J. Cons. 40, 67–75. Solemdal, P. (1997). Maternal effects—A link between the past and the future. J. Sea Res. 37, 213–227.

The Biology and Fisheries of European Hake

153

Somarakis, S., Palomera, I., Garcia, A., Quintanilla, L., Koutsikopoulos, C., Uriarte, A., and Motos, L. (2004). Daily egg production of anchova in European waters. ICES J. Mar. Sci. 61, 944–958 10.1016/j.icesjms.2004.07.018. Stepien, C., and Rosenblatt, R. H. (1996). Genetic divergence in antitropical pelagic marine fishes (Trachurus, Merluccius, and Scomber) between North and South America. Copeia 1996, 586–598. Stratoudakis, Y., Bernal, M., Ganias, K., and Uriarte, A. (2006). The daily egg production method: Recent advances, current applications and future challenges. Fish Fish. 7, 35–57. Svetovidov, A. N. (1948). Gadiformes. Fauna of the USSR Fishes Zoological Institute. Adad. Nauk. SSSR 9(4), 1–222, (English translation, 1962, Israel Program for Scientific Translation, Jerusalem). Szidat, L. (1955). La fauna de para´sitos de Merluccius hubbsi como cara´cter auxiliar para la solucio´n de los problemas sistema´ticos y zoogeogra´ficos del ge´nero Merluccius L. Comun.. Inst. Nac. Invest. Cienc. Nat., B. Aires 3, 1–54. Szidat, L. (1961). Versuch einer Zoogeographie des Sud-Atlantik mit Hilfe von Leitparasiten der Meeres fische. Parasitol. Schriftenr. 13 (Fischer Verlag, Jena). Trenkel, V. M., Pinnegar, J. K., Dawson, W. A., du Buit, M. H., and Tidd, A. N. (2005). Spatial and temporal structure of predator-prey relationships in the Celtic Sea fish community. Mar. Ecol. Prog. Ser. 299, 257–268. Trippel, E. A. (1998). Egg size and viability and seasonal offspring production of young Atlantic cod. Trans. Am. Fish. Soc. 127, 339–359. Trippel, E. A. (1999). Estimation of stock reproductive potential: History and challenges for Canadian Atlantic gadoid stock assessments. J. Northwest Atlantic Fish. Sci. 25, 61–81. Trippel, E. A., Kjesbu, O. S., and Solemdal, P. (1997). Effects of adult age and size structure on reproductive output in marine fishes. In “Early life history and recruitment in fish populations” (R. C. Chambers and E. A. Trippel, eds.), pp. 31–62. Chapman and Hall, London. Ulltang, ;. (1996). Stock assessment and biological knowledge: Can prediction uncertainty be reduced? ICES J. Mar. Sci. 53, 659–675. Uriarte, A., Collins, M., Cearreta, A., Bald, J., and Evans, G. (2004). Sediment supply, transport and deposition: Contemporary and late quaternary evolution. In “Oceanography and Marine Environment of the Basque Country” (A´. Borja and M. Collins, eds.), Elsevier Oceanography Series. 70, pp. 97–132. ´ . (2004). Climate and meteorolUsabiaga, J. I., Sa´enz Aguirre, J., Valencia, V., and Borja, A ogy, variability and its influence on the Ocean. In “Oceanography and Marine Environment of the Basque Country” (A´. Borja and M. Collins, eds.), Elsevier Oceanography Series. 70, pp. 75–96. Valencia, V., and Franco, J. (2004). Main characteristics of the water massess. In “Oceanography and Marine Environment of the Basque Country” (A´. Borja and M. Collins, eds.), Elsevier Oceanography Series. 70, Elsevier. pp. 197–226. Valencia, V., Franco, J., Borja, A´., and Fonta´n, A. (2004). Hydrography of the southeastern Bay of Biscay. In “Oceanography and Marine Environment of the Basque Country” (A´. Borja and M. Collins, eds.), Elsevier Oceanography Series. 70, pp. 159–194. Elsevier. Van Andel, T. H. (1976). An eclectic overview of plate tectonics, paleogeography, and paleoceanography. In “Historical Biogeography, Plate Tectonics, and the Changing Environment” (J. Gray and A. J. Roucot, eds.), pp. 9–25. Oregon State University Press, Corvallis. Velasco, F., and Olaso, I. (1998). European hake Merluccius merluccius (L., 1758) feeding in the Cantabrian Sea: Seasonal, bathymetric and length variations. Fish. Res. 38, 33–44.

154

Hilario Murua

Velasco, F., Olaso, I., and Sa´nchez, F. (2003). Annual variations in the prey of demersal fish in the Cantabrian Sea and their implications for food web dynamics. ICES Mar. Sci. Symp. 219, 408–410. Walbaum, J. J. (Ed.) (1792). Petri Artedi sueci genera piscium in quibus systema totum ichthyologiae proponitur cum classibus, ordinibus, generum characteribus, specierum differentiis, observationibus plurimis: redactis speciebus 242 ad genera 52: Ichthyologiae pars 3. Ant. Ferdin. Ro¨se: Grypeswaldiae. 723, 3 plates pp. Wootton, R. J. (1998). Ecology of teleost fishes. In “Fish and Fisheries Series 24”. (2nd edn.) Kluwer Academic Publishers, London. Wysokinski, A. (1986). Evaluation des stocks des merlus dans les divisions statistiques 34.1.3 et 34.3.1. du COPACE, base´e sur les donne´s polonaises (1966–1975). FAO COPACE/ PACE Se´rie 86(33), 72–120.

C H A P T E R

T H R E E

Chronobiology of Deep-Water Decapod Crustaceans on Continental Margins Jacopo Aguzzi and Joan B. Company Contents 1. Biological Clock Functioning in Decapod Crustaceans 1.1. A multioscillatory model 1.2. Clock centres 1.3. Input pathways 1.4. Photoperiodism 2. Rhythms in Continental Margins 2.1. The western Mediterranean continental margin scenario 2.2. Geophysical cycles in continental margins 3. Marine Types of Rhythmic Displacement 3.1. Pelagic displacement 3.2. Nektobenthic displacement 3.3. Epibenthic and endobenthic displacements 4. Interpretations of Activity Rhythms from Trawling Data 4.1. Data processing 4.2. A model to interpret the type of rhythmic displacement 5. Metabolism, Morphology, and Adaptations to Different Types of Displacement and Rhythmic Behaviour 5.1. Metabolic convergence in relation to the type of displacement 5.2. Morphological convergence in relation to the type of displacement 5.3. Morphological convergence in relation to the activity rhythm 5.4. The behaviour of decapods as a phenotypic trait 6. Ontogenetic and Gender Modulation of Behavioural Rhythms 6.1. Modulations in epi- and mesopelagic species 6.2. Modulations in benthopelagic species 6.3. Modulations in nektobenthic and endobenthic species

157 157 163 164 164 165 166 169 171 172 183 185 187 188 190 193 193 194 196 197 198 198 199 201

Institut de Cie`ncies del Mar (ICM-CSIC), Passeig Marı´tim de la Barceloneta 37-49, Barcelona 08003, Spain Advances in Marine Biology, Volume 58 ISSN 0065-2881, DOI: 10.1016/S0065-2881(10)58003-9

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2010 Elsevier Ltd. All rights reserved.

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6.4. A general hypothesis on modulation of rhythmic behaviour at adulthood by ontogeny and reproductive cycle 7. Biological Clocks and Bathymetric Ranges of Species’ Distribution 7.1. The effect of season 7.2. Endogenous rhythms and masking as a function of depth 8. Conclusions Acknowledgements References

203 205 205 206 209 210 211

Abstract Species have evolved biological rhythms in behaviour and physiology with a 24-h periodicity in order to increase their fitness, anticipating the onset of unfavourable habitat conditions. In marine organisms inhabiting deep-water continental margins (i.e. the submerged outer edges of continents), day–night activity rhythms are often referred to in three ways: vertical water column migrations (i.e. pelagic), horizontal displacements within benthic boundary layer of the continental margin, along bathymetric gradients (i.e. nektobenthic), and endobenthic movements (i.e. rhythmic emergence from the substrate). Many studies have been conducted on crustacean decapods that migrate vertically in the water column, but much less information is available for other endobenthic and nektobenthic species. Also, the types of displacement and major life habits of most marine species are still largely unknown, especially in deep-water continental margins, where steep clines in habitat factors (i.e. light intensity and its spectral quality, sediment characteristics, and hydrography) take place. This is the result of technical difficulties in performing temporally scheduled sampling and laboratory testing on living specimens. According to this scenario, there are several major issues that still need extensive research in deep-water crustacean decapods. First, the regulation of their behaviour and physiology by a biological clock is almost unknown compared to data for coastal species that are easily accessible to direct observation and sampling. Second, biological rhythms may change at different life stages (i.e. size-related variations) or at different moments of the reproductive cycle (e.g. at egg-bearing) based on different intra- and interspecific interactions. Third, there is still a major lack of knowledge on the links that exist among the observed bathymetric distributions of species and selected autoecological traits that are controlled by their biological clock, such as the diel rhythm of behaviour. Species evolved in a photically variable environment where intra- and inter-specific interactions change along with the community structure over 24 h. Accordingly, the regulation of their biology through a biological clock may be the major evolutionary constraint that is responsible for their reported bathymetric distributions. In this review, our aim is to propose a series of innovative guidelines for a discussion of the modulation of behavioural rhythms of adult decapod crustaceans, focusing on the deep waters of the continental margin areas of the Mediterranean as a paradigm for other marine zones of the world.

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1. Biological Clock Functioning in Decapod Crustaceans Biological rhythms are complex phenomena that are expressed on different temporal and organic scales (Fig. 3.1). Rhythms have been identified at the molecular level in gene expression (i.e. the clock proteins) within the cell and at the physiological level as the release of hormones within tissues. This temporal patterning conditions the rhythmic functioning of secretory, excretory, respiratory, and circulatory systems, the result of which is visible in the diel and seasonal behavioural variations of individuals, populations-species, and then at the level of the whole community ( Joshi, 2005). Biological clocks are responsible for the generation, maintenance, and entrainment that are at the base of the synchronisation of biological rhythms. In vertebrates and invertebrates, the mechanism for the generation of biological rhythms is described according to a scheme that identifies three different major compartments (reviewed by Dunlap et al., 2004; Refinetti, 2006; Tosini and Aguzzi, 2005): (1) an input pathway as the set of sensorial organs responsible for synchronisation, (2) the pacemaker, the property of which is to drive a self-sustained oscillation, and (3) the output pathway. The last is the sum of all neural connections and hormonal signals that convey the information from the pacemaker to the organs and drive the behaviour (considered as the periphery). In marine organisms, diel activity rhythms are often referred to as behavioural fluctuations in the rate of displacement by swimming and walking spontaneous activities (i.e. motility) in relation to day–night or tidal cycles. As already established for vertebrates, walking and swimming are commonly studied in the laboratory as indicators of a biological clock’s functioning on the 24-h scale. That situation is also valid for decapods (Naylor, 1988). In this context, the definition of rhythmic activity refers to diel variations in the rate of these behavioural performances (Nussbeum and Beenhakker, 2002).

1.1. A multioscillatory model One of the marine models for the study of activity rhythms in crustacean decapods at the molecular, physiological, and behavioural level is the coastal horseshoe crab, Limulus polyphemus (Linnaeus, 1758). This species shows circadian and circatidal rhythms in locomotor activity (Chabot et al., 2004) controlled by an endogenous circadian clock (Powers and Barlow, 1985) located in the protocerebrum (Barlow, 1983). Locomotor activity is endogenously modulated on both a circatidal and a circadian basis and that when

Rhythmicity

Organic unit

Studied indicator

Ecological analysis

Scientific Research discipline scenario

Sinecology

Community

Interannual

Ecology Species Population

Growth Reproduction Migration Ethology

Seasonal

Diel

Field

Apparatuses

Metabolism

Physiology

Autoecology

Individual Organism

Behaviour (feedingdisplacing)

Laboratory

Tissues Cells

Proteins DNA/mRNA

Molecular biology

Figure 3.1 Schematic representation of different levels in the analysis of biological rhythms. Consideration was given to the complexity scales in relation to time (i.e. Diel, Seasonal, and Interannual frequencies as representative of ultradian, circadian, and infradian rhythms) and organic units of complexity (i.e. from the cell to the community) by analysing different indicators as time series of data in gene–protein expression, metabolism, physiology, and behaviour at the level of individuals as well as growth, reproduction, migration, and hibernation at the level of populations and species. The scientific disciplines (i.e. from molecular biology to ecology) interested by that analysis and the different research locations (i.e. field or laboratory) are also indicated at each level of organic unit of complexity. Finally, a reference is given to the process of data integration in order to understand the process of rhythms regulation from its mechanical generation to its ecological significance: autoecology refers to the integration of data at different levels of complexity within the same species, as it is the sinecological processing of information based on the identification of repetition in regulatory patterns according to similitude in the ecology of different species.

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the animals are subjected to a light-dark cycle, most activity occurs at night (Chabot et al., 2004). Data accounting for the functioning of biological clocks in deep-water continental margin species are very scant (Aguzzi and Chiesa, 2005). As in the case of L. polyphemus, the majority of experimental evidence exists for coastal species where the day–night cycle and the tides are co-dominant cycles (reviewed by Palmer, 2000; Thurman, 2004a; Wilcockson and Zhang, 2008; Last et al., 2009). Animals are mostly exposed to lightintensity fluctuations, cyclic changes in pressure, salinity, and temperature. Tides produce two events of water rise and fall per day. However, the tidal day is different from the solar day, as it is chiefly controlled by the moon. While the day–night cycle lasts 24 h (i.e. the solar day), the tidal cycle is 24.8 h (i.e. the lunar day), and the two events of water rise or fall are located 12.4 h apart. As a consequence, a particular tidal rise event a day before will be delayed 50 min the next day (reviewed by Palmer, 2000). Under constant laboratory conditions, the tidal activity of crabs occurs under the form of two increases coupled in phase opposition, at 12.4 h of distance. As a result, the displayed rhythms are bimodal over the 24.8 h. In that manner, 28.8 days are required by the two tidal peaks to completely scan the solar day. Both peaks keep their phase relationship constant, so they could be considered as the result of a single controlling clock that activates itself according to optimum tidal conditions. In some cases, one of the two peaks can scan the day at a different periodicity, altering the period of its fluctuation in comparison to the other, being in some cases also dampened (Palmer, 2000). Palmer and Williams (1986a,b) proposed the existence of a “circalunidian” clock to account for the regulation of tidal locomotor activity rhythms. Apparently, there are two coupled oscillators, each one controlling the activity rhythm at each tidal event in an independent manner. Recently, Thurman (2004b) suggested that tidal crabs possess at least two different biological clocks: one entrained by the day–night cycle, the other entrained by water characteristics which vary in response to tides. In laboratory-constant conditions, decapods temporarily show the presence of entrained locomotor activity peaks at tidal and day–night periodicities, the phase of which may be coincidental or not, depending on the lunar day at the time of sampling (Thurman, 2004a). Often, the tidal rhythmicity overcomes the day–night one; as a consequence, the circadian regulation produces marked peaks every 24 h only when it coincides with a moment of high tide (Reid and Naylor, 1994). This phenomenon produces a considerable quantity of noise in recorded locomotor activity data (Dowse and Palmer, 1990; Thurman and Broghammer, 2001). Reid and Naylor (1994) already hypothesised the presence of two clocks in the green crab Carcinus maenas, where activity peaks related to tides can be suppressed or exaggerated depending on their phase coincidence with circadian rhythms (e.g. at night-time).

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In this context, the study of the biological clocks of deep-water decapods acquires a strategic importance. The light-intensity cycle is the strongest geophysical entraining agent on shelves and upper slopes (Naylor, 2005; Waterman, 2001). In the dark deep sea, marked variations in hydrodynamism (and not only in salinity or temperature) can occur at a diel base in relation to internal tides and atmospheric-driven inertial currents (Aguzzi et al., 2009d) (see Section 2.2). As a consequence, circadian oscillators should play a central role in the regulation of activity rhythms from subtidal zones down to the deepest limit of the twilight zone, where the last photons are ultimately present. Most of decapod species currently object of studies on behavioural, physiological, and molecular rhythms are from shallow-water habitats. These species are from inland water areas, such as the freshwater crayfish Procambarus clarkii Girard (1852) (Agapito et al., 1995; Balzer et al., 1997; Fanjul-Moles et al., 2004; Fernande´z de Miguel and Are´chiga, 1994). In marine field studies, clawed lobsters, palinurid and panulirid lobsters, as well as penaeid prawns, were often the most studied species due to their elevated commercial importance. Observations on their behaviour revealed the occurrence of a marked nocturnal activity that was accompanied by strong activity peaks at dusk and dawn with different amplitudes; the former activity peak was the stronger of the two (Table 3.1). Insects like the fruit fly, Drosophila melanogaster (Meigen, 1830), represent the best known invertebrate model for the study of circadian regulation at the molecular and behavioural level. The Drosophila activity pattern is bimodal with pronounced morning and evening peaks (Helfrich-Foster, 2001). Morning and evening oscillators control the activity rhythm with different free-running periodicity (Helfrich-Foster, 2000). The presence of a dual-circadian oscillator as a mechanism of behavioural control has also been suggested for mammals ( Jagota et al., 2000). In contrast to Drosophila, where both circadian oscillators have similar entraining capabilities, the morning-related and the evening-related peaks in crustaceans apparently possess different sensitivities to light (reviewed by Carmona-Alcocer et al., 2005). The down-twilight signal appears to be a more efficient synchroniser of activity (Williams, 1980a,b). Unfortunately, these conclusions are often speculative. The occurrence of an endogenous control by a dual-oscillator is not usually proven by transferring animals from a light-darkness to a constant-darkness protocol. Therefore, the occurrence of a reactive activity response (i.e. masking) at light-darkness transitions cannot be discharged. Several other marine groups apparently have a dual-oscillator organisation in control of their circadian behaviour. Within crustaceans, amphipods have two interacting oscillators that work in a coupled, but independent, fashion. This mechanism controls the separate “evening” and “morning” components of the active phase (Williams, 1980a,b). For polychaete species within families of the Sabellidae (Aguzzi et al., 2006b; Costa et al., 2008) and

Table 3.1 List of marine and freshwater species for which studies on locomotor activity rhythms in the laboratory or in the field have accounted for a putative dual-oscillator organisation of their biological clock at a diel base (i.e. bimodal rises in locomotor activity at sunset and sunrise) Common name

Species

Testing scenario

Phase Peaks timing

Marine Rock crab

Cancer irroratus

Laboratory

N

Cancer novaezelandiae Carcinus maenas Hemisquilla ensigera Homarus americanus

Laboratory

N

Laboratory Field

N N

Field, laboratory

Cancrid crab Shore green crab Mantis shrimp American lobster

Source

Sunset–Sunrise Upper and lower shelf, and slope Sunset Sublittoral

Rebach (1987)

N

Sunset–Sunrise Upper and lower shelf Sunset

Golet et al. (2006), Karnofsky et al. (1988), Lawton (1987) Smith et al. (1999)

European lobster

Homarus gammarus Field

N

Scampi

Metanephrops Field australiensis Nephrops norvegicus Field, laboratory

N N

Caribbean spiny lobster

Panulirus argus

Field, laboratory

N

Western rock lobster

Panulirus longipes

Laboratory

Norway lobster

Depth zone

Chatterton and Williams (1994) Sunset–Sunrise Littoral–Sublittoral Reid and Naylor (1989) Sunset–Sunrise Upper shelf Bash and Engle (1989)

Upper and lower shelf Sunset–Sunrise Upper-, lower shelf and slope Sunset–Sunrise Upper and lower shelf and slope

Sunset–Sunrise Upper shelf

Sunset

Upper shelf

Ward and Davis (1987) Aguzzi et al. (2004b), Aguzzi et al. (2003), Hammond and Naylor (1977) Casterlin and Reynolds (1979), Weiss et al. (2007) Morgan (1978) (continued)

Table 3.1

(continued)

Common name

Species

Testing scenario

Phase Peaks timing

Depth zone

Source

Pink shrimp

Penaeus duorarum

Laboratory

N

Sunset

Upper shelf

Grass prawn

Penaeus monodon

Laboratory

N

Sunset

Upper shelf

Green tiger prawn

Laboratory

N

Sunset–Sunrise Upper shelf

Fiddler crab

Penaeus semisulcatus Uca subcylindrica

Huges (1968), Reynolds and Casterlin (1979) Honculada-Primavera and Lebata (1995) Moller and Jones (1975)

Laboratory

D and Sunset–Sunrise Littoral N

Thurman (1998), Thurman and Broghammer (2001)

Freshwater Freshwater crayfish

Astacus astacus

Field

White-clawed crayfish Red swamp crayfish

Austropotamobius Field pallipes Procambarus clarkii Laboratory

D and Sunset–Sunrise Freshwater N N Sunset–Sunrise Freshwater

Freshwater crab

Pseudothelphusa americana

Bojsen et al. (1998), Westin and Gydemo (1988) Barbaresi and Gherardi (2001) Fanjul-Moles and PrietoSagredo (2003), FanjulMoles et al. (1996), Page and Larimer, 1972 Carmona-Alcocer et al. (2005), Miranda-Anaya et al. (2003a), MirandaAnaya et al. (2003b)

Laboratory

N

Sunset–Sunrise Freshwater

N

Sunset–Sunrise Freshwater

Only studies explicitly stating that activity peaks occur at crepuscular hours with an equal or differential strength are reported.

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Nereidae (Last and Olive, 2004; Last et al., 2009), activity bouts have been reported both at sunset and sunrise. In addition, clams apparently share a similar temporal organisation of their diel behaviour (Wan-Soo et al., 2003).

1.2. Clock centres The definition of a circadian system made by multiple oscillators requires the identification of those components within different tissues that can maintain a self-sustained circadian rhythmicity in isolation and in synchrony with the whole system (reviewed by Rodriguez-Sosa et al., 2008). In several species of insects, including D. melanogaster, the brain holds the central pacemaker that controls behavioural rhythms (reviewed by Paultz et al., 1997). Photoreceptors within the brain send the environmental photic information to the centre that regulates rhythms. Information on light intensity is conveyed to the clock by several circadian photoreceptors within different tissues (Wheeler et al., 1993). Conversely, studies on crabs point out the potential presence of a multioscillatory clock, the components of which are located in the eyestalks and in the supraoesophageal ganglion (as the cerebroid ganglion or brain; Herna´ndez and Fuentes-Pardo, 2003; Miranda-Anaya et al., 2003b). The freshwater crab Pseudothelphusa americana (De Saussure, 1857) preserves its circadian rhythmicity after eyestalk ablation, but its rhythm is no longer bimodal. This suggests that one oscillator may be located within the eyestalks, while the other is in the supraoesophageal ganglion (Carmona-Alcocer et al., 2005). During ontogeny, changes can be observed in the main components of the circadian clock of decapods living in fresh water. Younger crayfish cluster their activity mainly in the photophase, while older animals show clearer bimodal activity at light on and off, as they are fully nocturnal (Fanjul-Moles and Prieto-Sagredo, 2003). From comparisons of the motor patterns in young and adult crayfish, authors supposed that there are two groups of oscillators involved in its generation and expression of movement (FuentesPardo et al., 2003). The first group, appearing very early in ontogeny, would probably be located in the cerebroid ganglion, and it would be responsible for the generation of circadian motor patterns. A second group, appearing later in ontogeny, would be located in the eyestalk (in the sinus gland), and would be responsible for the synchronisation of motor circadian rhythm with external signals. The second is a hypothetical hormonal oscillator that affects the first group, as it is also sensitive to light (Castan˜on-Cervantes et al., 1999). Its effects assume an inhibitory character. At the adult stage, the hormonal oscillator affects the nervous one. Pacemaker neurons undergo circadian rhythms of electrical and secretory activity, which are influenced by neurotransmitters such as serotonin and its derivate hormone melatonin, and convey information on the light-darkness cycle to the internal physiology (reviewed by Benzid et al., 2006; Aguzzi et al., 2009e).

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1.3. Input pathways In crustaceans, there is scant information about circadian photoreceptors and the entrainment pathways that couple the clock to the diel change in light intensity (Fanjul-Moles et al., 2004). The entrainment process occurs via a wide variety of extraocular photoreceptors (Cronin, 1986; Fanjul-Moles and Prieto-Sagredo, 2003a; Sandeman et al., 1990). These photoreceptors are located directly within the supraoesophageal ganglion (reviewed by FanjulMoles et al., 2004) and within the sixth abdominal ganglion (reviewed by Rodriguez-Sosa et al., 2008). For example, totally blind lobsters still retain an abdominal sensitivity to light (Shelton et al., 1985). That sensitivity elicits backward locomotion even after the abdomen has previously been subjected to levels of light that would cause retinal blindness. The effect of radiation at 440–480 nm on the behavioural rhythms of decapods confirms the photoentrainment action of blue light, indicating the presence of a photopigment that is involved in circadian photoreception and absorbs at this range of the spectrum (Fanjul-Moles et al., 2004). Cryptochromes (CRY) are proteins with a dual role in the circadian function of insects and crustaceans, participating in phototransduction and light signalling to the clock and as a transcriptional repressor of clock genes (Escamilla-Chimal and Fanjul-Moles, 2008; Stanewsky et al., 1998). CRY are a blue/UV-A absorbing pigments, being hence putative circadian photoreceptors for the photoentrainment of species both in coastal areas and possibly, also in the deeper water zones of the continental margins. Blue radiation is invariantly present in all depth strata of the water column down to the twilight zone extinction limits (Herring, 2002; Jerlov, 1968). Aguzzi et al. (2006c, 2008b) and Chiesa et al. (2010) recently showed that 480 nm blue light efficiently modulates activity rhythms in deep-water decapods (see also Section 2.2.1).

1.4. Photoperiodism The existence of a common mechanism that controls the behaviour at diel and at seasonal bases through the measurement of the photophase or scotophase duration (i.e. photoperiodism) is currently under discussion. Such a common mechanism could explain the reported rhythms in the growth and reproduction of several vertebrate and invertebrate species (reviewed in Saunders, 2002; Dunlap et al., 2004; Refinetti, 2006). Photoperiodic responses in arthropods involve a circadian clock that is used to determine the qualitative difference between long and short days (i.e. photoperiodic time measurement). Using the measurement of a peak’s reciprocal distance, Antheunisse and van Den Hoven (1971) proposed that the mechanism controlling a bimodal activity rhythm in shrimp with crepuscular peaks may be at the base of decapod seasonal reproduction. In P. americana (de Saussure, 1857), crepuscular peaks seem to be controlled by

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morning and evening oscillators, and the variability in their phase relationship may be a mechanism by which animals could measure seasonal changes in the day length (Miranda-Anaya et al., 2003b). The importance of light in the seasonal rhythms of deep-water continental margin species is demonstrated by the reported marked seasonal cycles in reproduction and growth (Company and Sarda`, 1997, 1998, 2000; Company et al., 2003). The linkage between the light cycle, diel regulation of behaviour, and photoperiodism is demonstrated in the totally blind polychelid lobster, Polycheles typhlops (Heller, 1862). The absence of seasonal rhythmicity in its reproductive pattern is accompanied by an evident atrophy of its eyes (Company et al., 2003). In the dark Deep-sea, where diel temporising variations in downwelling light are absent (the only available light is bioluminescent), most species have continuous or semi-continuous reproductive patterns, but investigations in the last decade have shown that seasonal reproduction is also present (reviewed in Young, 2003). However, the environmental cues used by these species to time their seasonal rhythms are presently unknown. In the Deep- sea, seasonal reproductive cycles have been described in relation to the seasonal peaks of phytodetritus in the water column for a number of species such as the clam Calyptogena kilmeri (Bernard, 1974; Lisin et al., 1997), and the mussel Bathymodiolus childressi (Gustafson, 1998) from the Gulf of Mexico (Tyler et al., 2007). Seasonal patterns in primary production at the superficial layers of the water column apparently provide the organic input that sustains the metabolism of gametogenesis (Eckelbarger and Walting, 1995) and supplies food for the larval phase, increasing the survival rate of the dispersing offspring (Gage and Tyler, 1992; Tyler et al., 1994). In the Mediterranean, seasonal variations in vertical fluxes of organic matter have been reported down to 1000 m depth in association with marked reproductive seasonality in different phylogenetically related decapods (Company et al., 2003). Recently, marked nocturnal activity patterns were reported in the laboratory for the deep-sea shrimp Alvinocaris stactophila (Williams, 1988) from a chemosynthetic cold-seep environment of 600–700 m (Aguzzi et al., 2007b). Animals belong to a deep-sea taxon (Komai and Segonzac, 2005) and they present marked seasonal rhythms in growth and reproduction (Copley and Young, 2006). Taken together, these data suggested that the diel endogenous control of activity might be at the base of the control of seasonal rhythms.

2. Rhythms in Continental Margins To date, chronobiology does not pay enough attention to the ecological significance of activity rhythms. Conversely, ecologists often forget to place their observations within the temporal domain of biological rhythm

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frequencies, mainly the influence of the day–night cycle on the dynamics functioning of the ecosystems (Marques and Waterhouse, 2004). As a result, there have been great advances in the understanding of biological rhythms functioning at the molecular, physiological, and behavioural levels, but their modulation for sociality and demographic variables, such as size, sex, and the stage of the reproductive cycle, remain to date mostly neglected. Chronobiological research in the deep-water continental margin species is still a challenging and poorly explored field of research that has great implications for studies on population distribution and biodiversity (Aguzzi and Sarda`, 2008a; Naylor, 2005). Species within the community are well synchronised spatially and temporally. Diurnal and nocturnal fauna constitute two halves of the community that could share the same habitat resource in antithetic phases of the day–night cycle (Park, 1941). The majority of species competing for the same food items (i.e. overlapping trophic niches) show differences in their periods of activity (Bider, 1962). This has been known for a long time in land communities, where these species show spatial segregation when activity periods occur at the same time (Bider, 1962), but it is apparently also true for demersal communities (e.g. Patterson, 1984; Trenkel et al., 2007) as recently shown for benthic sympatric deep-water fish predators (Colmenero et al., 2010). As a consequence, the presence of species within sampling areas used for population or demographic assessments depends upon the activity rhythms of the individuals. The quantification of animal movement in time and space is fundamental to the study of animal ecology and to the design of effective strategies for resource conservation and management (Pittman and McAlpine, 2001). In this context, it is extremely important to understand the role of different geophysical cycles in the modulation of biological rhythms in the deep-water and deep-sea species that are of ecological and commercial interest (Naylor, 2005). Behavioural differences over tidal and diel time-scales are critical in terms of commercial stock management (Bahamon et al., 2009). The time of day, the day of the season, and the depth are important determinants of the capture rate and the size composition of catches (Aguzzi and Sarda`, 2008b; Hjellvik et al., 2002; Petrakis et al., 2001; Naylor, 2005).

2.1. The western Mediterranean continental margin scenario Continental margins represent the submerged edges of continents, and they account for approximately 21% of the planet’s surface (Waterman, 2001). These are zone of steep or gradual transitions in abiotic factors that cause a depth-related zonation in species distributions. These factors are not only physical (e.g. light intensity, hydrodynamism, or temperature), but also geological (e.g. bottom geomorphology and steepness, sediment morphology, as well as organic and inorganic matter sedimentation and resuspension rates).

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In this scenario, the Western Mediterranean continental margin represents one of the most intensely studied areas of the world (Gage and Tyler, 1992). Numerous submarine canyons heavily incise the margin, and depths greater than 1000 m are reported just a few miles off shore (Sarda` et al., 1994). Studies on species depth ranges of distribution and biomasses as well as community biodiversity have been undertaken since the second half of the 1980s. The resultant data were used as a base of reference for the creation of major depth subdivisions. Identified depth zones were characterised by their own community, each one responding to a unique combination of habitat conditions (Cartes et al., 1994a,b). Generally, these zones were recognised as (Fig. 3.2): (a) shelf areas from 0 to 200 m depth; (b) slope areas, from 200 to approximately 2000 m depth (including the twilight inferior border at 1000 m depth); and finally, (c) the continental rise and abyssal plains. Studies on community structure mostly focused on shelf and slope areas that revealed the presence of complex internal-zone divisions based on the diversity and biomass estimates of benthic decapod crustaceans (reviewed by Cartes and Sarda`, 1993). Depth-related and well-distinguished species associations defined different communities (Abello´ et al., 1988, 2002; Cartes and Sarda`, 1993; Cartes et al., 1994a,b): (a) on the shelf; (b) on the shelf-slope transition zone (from 150 to 300 m depth); (c) on the upper slope (from 200 to 450 m depth); (d) on the middle slope (from 500 to 1200–1300 m depth); and finally, (e) on the lower slope (1300 to 1900–2000 m). Factors causing such depth-related zonation in communities were indicated by geological features, such as the steepness of the seabed as well as sedimentation and re-suspension rates, or by biological features, such as resources availability, predator–prey relationships, and intraspecific competition for the substrate use. Species tropism apparently plays a predominant role in the depth zonation of fauna and results in different communities. Cartes and Sarda` (1993) affirmed that the trophic factor is likely to be the most important cause of the Mediterranean zonation of decapods. Following this observation, they subdivided the middle slope in two zones: the middle slope upper sub-zone and the middle slope lower sub-zone. The first is characterised by eutrophic conditions because of the local influence of marine canyons where the re-suspension of organic matter is caused by the periodical up- and downcanyon-bottom currents. Here, deposit feeders are always present. The second is characterised by oligotrophic conditions, and suspension feeders are not preponderant in this zone. Decapod species in continental margin areas also show a marked horizontal structuring (i.e. along isobaths) in the distribution of their populations. Maynou et al. (1996, 1998) found that decapod populations aggregate in high-density patches with sizes ranging from 10 to 100 km2. Populations of different species showed marginal overlapping with the creation of complex mosaics of transition zones. Species distribution depended on

Wavelengths Red

Green

Day-night regulation

Blue Photic zone (photosynthesis)

Shelf 150–20 m

Internal tide and inertial current regulation

Slope

Twilight zone end

1000 m 2000 m

Continental rise

Deep-sea

Abyssal plain

Figure 3.2 Schematic representation that depicts the continental margin depth zonation of the shelf, the slope, the continental rise, and finally the abyssal plain. Light undergoes a double modification over depth as photons travel within the water column body: intensity decreases and spectral diversity diminishes. The photic zone represents the depth range (0–200 m) where photosynthesis occurs. The twilight zone end border represents the upper limit of the aphotic deep-sea realm, where the last few remaining photons can be detected (Margalef, 1986). From the perspective of biological rhythms regulation, the twilight zone can also be conceived as the border above which the circadian regulation strengthens for a reduction in the depth of sampling from slopes to shelves. As depth progressively increases, other geophysical cycles such as internal tides and inertial currents become relevant; both are likely to be the only geophysical cycles modulating the activity rhythms of deepsea species (Aguzzi et al., 2010).

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seabed morphology and intraspecific competition for substrate use (e.g. substrate sheltering and feeding). These interspecific interactions end up with the formation of species-specific patches, where populations of ecologically equivalent species mutually excluded each other, and hence coexisted at larger geographic scales.

2.2. Geophysical cycles in continental margins Three geophysical cycles are responsible for modulating most of the biological rhythms in deep-water continental margin areas: light intensity, internal tides, and inertial currents (reviewed by Naylor, 2005, 2006; Aguzzi et al., 2009d; Fig. 3.2). The light-intensity cycle exerts a powerful effect on the structure of benthic and pelagic communities (see Section 3). The presence or absence of environmental illumination influences how organisms perceive their environment (McIntosh and Towsend, 1994), and therefore modulates the timing and typology of their intraspecific and interspecific relationships (Pulcini et al., 2008). As depth increases and light cycle is reduced, internal tides and inertial currents come into play (reviewed by Aguzzi et al., 2010). These geophysical forces of variable periodicity (depending on latitude) and strength (depending on local geomorphological conditions) produce fluctuations in the degree of hydrodynamism experienced by organisms that affect their physiological and behavioural rhythms in a still largely unknown fashion. 2.2.1. Light-intensity cycle Light intensity and spectral composition are variable with depth because of the absorption and scattering of photons by the water column molecules and suspended particles (Fig. 3.2; Jerlov, 1968). The depth range where the phytoplankton photosynthetic activity occurs is called the photic zone, and it extends from the water surface down to 100–200 m depth, depending on local turbidity conditions (Herring, 2002). Minima in light intensity are still recordable up to 1000 m depth in oligotrophic areas such as the Mediterranean (Margalef, 1986). The maximum depth where the light is recordable represents the inferior border of the twilight zone limit. That limit designates the onset of the dark deep-sea realm, the most extensive ecosystem on earth (Waterman, 2001). Light penetration in the water column depends upon the position of the sun during its diel trajectory (Herring, 2002). Generally, when the sun is on the zenith (i.e. directly overhead), only 2% of photons are reflected at the air–sea interface. In contrast, when the sun sets at the horizon, photon reflection abruptly increases and light penetration drastically diminishes. The effect of the day–night transition is hence stronger in shallower water areas where the angular distribution of light (i.e. transmission) is still asymmetrical in relation to the depth vertical axis. The light field becomes

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progressively symmetrical in relation to the vertical propagation axis as depth increases. As a result, animals living near the surface experience steeper light-intensity, light-colour, and light-direction transitions at dusk and dawn than deeper-water animals, for which major photic modifications are only related to fluctuations in intensity. Among all wavelengths that constitute sunlight, the blue-light radiation at 470–480 nm is the one with the highest penetration power in the water column in clearest ocean waters (Herring, 2002; Jerlov, 1968). In oceanographic surveys, light is often measured as photosynthetically active radiation (PAR) by sensors that are equally sensitive to wavelengths comprised between 400 and 700 nm and insensitive to those outside this spectrum region (e.g. Aguzzi et al., 2003). The most common units of calibration for broadband PAR are mEi m 2 s 1 (micro-Einsteins). It should be noted that this unit of measure is equal to mmol m 2 s 1 (micromoles). 2.2.2. Internal tides and inertial currents The movement of the Earth in relation to the sun and the moon generates the cyclic displacement of water masses at a periodicity of 12.4 h, which is a phenomenon known as tides (see Section 1.3.1). In deeper shelf and slope areas, tidal currents chiefly occur in the form of internal waves carrying energy from one part of the ocean to another (reviewed by Simmons, 2008). This rhythmic movement of oceanic water masses by internal waves is at the base of a phenomenon known as an internal tide (Garret, 2003). Oceanic internal tides have been reported at all depths of the water column down to seabed areas at thousands of metres (Dickson et al., 1982). The amplitude of these physical fluctuations is strongly influenced by local seabed and coastal topographic conditions. Inertial currents are the product of local gears driven by atmospheric events such as the wind drift at sea surface in combination with the motion of the Earth. Data collected by moored current metres in deep-water Western Mediterranean continental margins clearly demonstrate that the deep-sea flow regime is dominated only by inertial currents up to depths of 3000 m. In the Mediterranean, tidal effects are minimal, and hence, internal tides are replaced by inertial fluctuations (Flexas et al., 2002; Martı´n et al., 2007; Palanques et al., 2005; Petrenko, 2003; van Haren and Millot, 2004). In the absence of strong astronomical tides, inertial currents in the North-western Mediterranean occur as high frequency fluctuations at approximately 18 h periodicity, related with its latitudinal position (around 40 ). In subtidal photic zones, the cycle in the light intensity alone was thought to remain as the major modulator of animal circadian biology (Naylor, 2005; Saigusa et al., 2000). In any case, the light cycle progressively vanishes when moving from shelves to slopes, and other geophysical cycles have been reported as putative environmental agents of entrainment

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(Aguzzi et al., 2009d; Wagner et al., 2007). This leads to interesting questions about the occurrence and evolutionary advantage of any biological rhythmicity at a diel base in the deep sea, far from light-intensity fluctuations. The presence of endogenous rhythms has been reported in terrestrial environments that somehow simulate this marine realm. Evolutionarily specialised troglobitic (i.e. cave restricted) vertebrate and invertebrate fauna (e.g. Reichle et al., 1965; Trajano and Menna-Barreto, 1995) still display endogenous rhythmicity. These observations suggest that a rhythmically fluctuating biology is required for the proper evolution of life in an environmental context where light can be absent. Current speed variations in association with tidal or inertial regimes can alter the activity pattern in deep-sea animals. In situ studies on the behavioural response of Atlantic deep-sea fishes and crustaceans to cycles of a tidal nature in the bottom current suggest a potential modulation of their biorhythms at 12.4-h (e.g. Dickson et al., 1982; Lampitt et al., 1983; Smith and Laver, 1981; Wagner et al., 2007). Unfortunately, the endogenous nature of such rhythmicity was not demonstrated in the laboratory with a chronobiological protocol (i.e. under constant conditions) because of the intrinsic fragility of the tested organisms (Naylor, 2005). A model for hydrodynamic entrainment for deep-water and deep-sea benthic decapods is still missing (Aguzzi et al., 2009d). Macrobenthic species are quite sensitive to changes in the turbulence of the benthic boundary layer (BBL), since water flow mediates the transport of nutrients and other biological signals (Weissemburg and Zimmer-Faust, 1993). The response of Atlantic fishes to near-bottom currents occurs when these represent important directional cues for food detection by dispersing odours (Wilson and Smith, 1984). Entrainment possibly occurs as an adaptive response to water-speed increases in order to feed efficiently and hence has an adaptive value (Wagner et al., 2007). In addition, the anticipation of physiological and behavioural responses to increases in current speed could potentially help animals to maintain their positioning in determined seabed areas.

3. Marine Types of Rhythmic Displacement Different species show a diel regulation of their behaviour that rhythmically impulses thousands of individuals to move over distance ranges that span from tens of metres up to a few kilometres (Cartes et al., 1993; Foxton, 1970a,b; Franqueville, 1971; Jumars, 2007). In contrast to land, such movement can occur in the marine ecosystem in both 2D and 3D fashions. The water column allows the persistence of individuals for variable periods of time at any range of depth, from the layer closest to the surface to the deeper realm, which is in contact with the seabed. The seabed stratum, when

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considered in relation to the analysis of rhythmic behaviour, refers to superficial sediment layers, where signs of bioturbation indicate drilling activity for feeding, burrowing, or burying purposes. The BBL is at the water column– seabed interface (Vereschaka, 1995), and it extends from a few centimetres up to tens of metres above the seabed (Cartes, 1998; Levin et al., 2001; Puig et al., 2001; Vallet and Dauvin, 2001, 2006). In relation to the analysis of rhythmic movements of demersal animals, the BBL zone of interest is the near-bottom stratum within 1–2 m height. Animals from the water column and from the seabed can be cyclically sampled by trawling within that zone. The portion of space that is crossed by animals during the expression of their behavioural rhythms defines a zone of the ecosystem within their sensory range (reviewed by Pittman and McAlpine, 2001). Farina and Belgrano (2004) defined this zone as the “ecofield”: the portion of the ecosystem that is directly perceived by animals during the process of energy collection, preservation, and transformation. In this definition, all abiotic and biotic factors that modulate the behavioural activity of animals are included. Among these factors, variations in light intensity, in the length of the photoperiod, and in water flow by internal tides or inertial currents represent signals that deeply affect the ecofield of decapods inhabiting continental margins and setting the timing of their rhythmic displacements at a diel base. Referring to natantian species (i.e. which show morphologically convergent adaptations for swimming behaviour; see Section 5), autoecological data on rhythmic behaviour in relation to the type of displacement are generally scant. A global list of Atlanto-Mediterranean species for which this information is available is reported in Table 3.2 as an example of how this sample is reduced in comparison to known decapod diversity on continental margins. The idea of a corridor of displacement can then be proposed in relation to the expression of diel rhythms as the portion of space transitorily occupied by animals during the expression of different phases of their diel behavioural activity. That definition is useful since it allows the analysis for each of the different selective forces that animals experience when entering different compartments of that corridor, each one characterised by its own habitat and biotic constraints. It is then possible to perform an ecological classification of species based on the different typologies of corridors crossed by animals during the expression of their activity rhythm (Fig 3.3). This classification identifies four major typologies of corridors and hence, of associated displacements.

3.1. Pelagic displacement Pelagic species are those that live in the water column, many of which perform rhythmic diel vertical displacements into it. These can be functionally classified as “pelagic of benthic habit” (i.e. benthopelagic), when animals enter in contact with the seabed at least once during the 24 h, or

Table 3.2 Biological information concerning the taxonomical status (Tax; Car, Caridea, Pen, Penaeidae) and the activity rhythm (D, diurnal; N, nocturnal; ARR, arrhythmic) of the most-studied pelagic, nektobenthic, and endobenthic (burying) natantian (i.e. the shrimp and prawn morphotypes) decapods of the Atlanto-Mediterranean faunistic area (Longhurst, 2007) Pelagic Taxonomical status Species

Behaviour

Source

Acanthephyra pelagica

N

Acanthephyra purpurea

N

Pen Car Car Car Pen Pen Pen Pen

Bentheogennema intermedia Dichelopandalus bonnieri Ephyrina bifida Ephyrina hoskynii Funchalia villosa Funchalia woodwardi Gennadas brevirostris Gennadas elegans

ARR N ARR D N N N N

Pen Pen

Gennadas tinayrei Gennadas valens

N N

Car Car Car

Hymenodora glacialis Hymenodora gracilis Meningodora vesca

ARR ARR N

Fasham and Foxton (1979), Franqueville (1971), Hargreaves (1999), Koukouras et al. (2000) Fasham and Foxton (1979), Foxton (1970a), Foxton and Roe (1974), Franqueville (1971), Hargreaves (1999), Herring and Roe (1988), Hopkins et al. (1994), Morris (1973), Roe (1974) Johnson et al. (2000) Al-Adhub and Naylor (1977) Fasham and Foxton (1979) Foxton (1970a) Foxton (1970b) Cartes et al. (1993) Heffernan and Hopkins (1981) Andersen et al. (2004), Andersen and Sardou (1992), Cartes (1993a), Fasham and Foxton (1979), Foxton (1970b), Franqueville (1971), Hargreaves (1999), Herring and Roe (1988), Koukouras et al. (2000), Mauchline and Gordon (1991), Roe (1984), Sardou and Andersen (1993) Fasham and Foxton (1979) Fasham and Foxton (1979), Foxton (1970b), Foxton and Roe (1974), Hopkins et al. (1994) Domanski (1986), Mauchline and Gordon (1991) Fasham and Foxton (1979), Johnson et al. (2000) Foxton (1970a), Foxton (1970b)

Car

(continued)

Table 3.2

(continued)

Pelagic Taxonomical status Species

Behaviour

Source

Kruppasamy et al. (2006) Kruppasamy et al. (2006) Frank and Case (1989) Foxton (1970a) Hopkins et al. (1994), Zieman (1975) Fasham and Foxton (1979), Foxton (1970a), Zieman (1975) Vallet and Dauvin (2001) Barr (1970), Heier et al. (1999) Johnson et al. (2000), Vallet and Dauvin (2001) Aguzzi et al. (2009c) Fasham and Foxton (1979), Foxton (1970a), Foxton (1970b), Hopkins et al. (1994), Johnson et al. (2000) Aguzzi et al. (2006d), Cartes (1993a), Cartes et al. (1993), Fasham and Foxton (1979), Frank and Widder (1997), Franqueville (1971), Hargreaves (1999), Kaartvedt et al. (1988), Koukouras et al. (2000), Matthew and Pinnoi (1973), Maynou and Cartes (1998), Myslinski et al. (2005), Roe (1983) Foxton (1970a) Aguzzi et al. (2006d), Franqueville (1971), Koukouras et al. (2000), Matthew and Pinnoi (1973), Roe (1983) Matthew and Pinnoi (1973) Cartes (1993a), Fasham and Foxton (1979), Frank and Widder (2002), Franqueville (1971), Hargreaves (1999), Herring and Roe (1988), Kaartvedt et al. (1988), Koukouras et al. (2000), Madurell and Cartes (2005), Matthew and Pinnoi (1973), Mauchline and Gordon (1991), Myslinski et al. (2005), Roe (1974), Sarda` et al. (2003)

Car Car Car Car Car Car Car Car Car Car Car

Nematocarcinus ensifer Nematocarcinus exilis Notostomus elegans Notostomus longirostris Oplophorus gracilirostris Oplophorus spinosus Pandalina brevirostris Pandalus borealis Pandalus montagui Pandalus propinquus Parapandalus richardi

N N ARR ARR N N D D N N N

Car

Pasiphaea multidentata

N

Car Car

Pasiphaea hoplocerca Pasiphaea sivado

N N

Car Pen

Pasiphaea tarda Sergestes arcticus

ARR N

Pen Pen

Sergestes armatus Sergestes atlanticus

N N

Pen Pen Pen Pen

Sergestes corniculum Sergestes curvatus Sergestes henseni Sergestes pectinatus

N N N N

Pen

Sergestes robustus

N

Pen

Sergestes sargassi

N

Pen

Sergestes vigilax

N

Car Car

Systellaspis braueri Systellaspis debilis

D N

Foxton (1970b), Hopkins et al. (1994) Donaldson (1975), Fasham and Foxton (1979), Foxton and Roe (1974), Hopkins et al. (1994) Donaldson (1975), Fasham and Foxton (1979), Foxton (1970b) Fasham and Foxton (1979), Foxton and Roe (1974), Hopkins et al. (1994) Foxton and Roe (1974), Hopkins et al. (1994) Donaldson (1975), Foxton (1970b), Foxton and Roe (1974), Hopkins et al. (1994) Cartes (1993a), Cartes et al. (1993), Cartes et al. (1994a, 1994b), Donaldson (1975), Foxton (1970b), Hargreaves (1999), Hopkins et al. (1994), Koukouras et al. (2000), Johnson et al. (2000), Vereschaka (1995) Donaldson (1975), Fasham and Foxton (1979), Foxton (1970b), Foxton and Roe (1974), Hopkins et al. (1994) Donaldson (1975), Fasham and Foxton (1979), Foxton (1970b), Hopkins et al. (1994) Fasham and Foxton (1979), Foxton (1970a) Foxton (1970a), Foxton and Roe (1974), Frank and Widder (1994), Hargreaves (1999), Herring and Roe (1988), Hopkins et al. (1994), Johnson et al. (2000), Roe (1984), Zieman (1975)

Nektobenthic Phyl Species

Car Pen Pen Car

Acanthephyra eximia Aristeomorpha foliacea Aristeus antennatus Athanas nitescens

Behaviour Source

D N N N

Cartes (1993a), Cartes et al. (1993), Maynou and Cartes (1998) Cartes (1995), Wadley (1992) Cartes (1993a), Cartes et al. (1993), Sarda` et al. (2003), Tobar and Sarda` (1992) Pallas et al. (2006) (continued)

Table 3.2

(continued)

Nektobenthic Phyl Species

Pen Car Car Car Car Car Car Car Car Car Car Car Car

Benthesicymus iridescens Eualus gaimardii Eualus pusiolus Heterocarpus ensifer Hippolyte inermis Hippolyte garciarasoi Hippolyte holthuisi Hippolyte longirostris Hippolyte niezabitowskii Hippolyte varians Lebbeus polaris Lismata seticaudata Palaemon adspersus

Behaviour Source

D N N N N N N N ARR D N N N

Car Palaemon elegans

N

Car Palaemon longirostris Car Palaemon serratus

N N

Car Car Car Car

Palaemon xiphias Palaemonella vestigialis Palaemonetes antennarius Palaemonetes varians

Car Parapandalus narval

N D N N D

Aguzzi et al. (2009c) Nordtug and Krekling (1989) Nordtug and Krekling (1989) Sardou and Andersen (1993) Raso et al. (2006); Saunders and Hastie (1992) Raso et al. (2006) Raso et al. (2006) Schaffmeister et al. (2006) Raso et al. (2006) Bauer (1985) Aguzzi et al. (2009c) Couturier-Bhaud (1974) Berglund (1980), Guerao and Abello´ (1996), Hagerman and Ostrup (1980), Westin and Aneer (1987) Berglund (1980), Fasham and Foxton (1979), Fincham and Furlong (1984), Rodriguez and Naylor (1972), Schaffmeister et al. (2006); Wassemberg and Hill (1994) Fincham and Furlong (1984), Guerao and Ribera (1996) Fincham and Furlong (1984), Guerao and Ribera (1996), Rodriguez and Naylor (1972) Guerao (1995) Aguzzi et al. (2009c) Guerao (1995) Aguzzi et al. (2005), Antheunisse and van Den Hoven (1971), Bouchon (1991a), Bouchon (1991b), Fincham and Furlong (1984) Aguzzi et al. (2009c)

Pen Car Car Car Car Car

Parapenaeus longirostris Philocheras bispinosus Philocheras echinolatus Philocheras fasciatus Philocheras trispinosus Plesionika acanthonotus

N D D D D N

Car Car Car Car Car

Plesionika antigai Plesionika edwardsii Plesionika gigliolii Plesionika heterocarpus Plesionika martia

D D D D D

Pen Plesiopenaeus edwardsianus Pen Sicyonia carinata Car Spirontocaris liljeborgi Car Spirontocaris spinus Car Thoralus cranchii

N

Carpentieri et al. (2005), Cartes (1995) Raso et al. (2006) San Vicente and Sorbe (2001) San Vicente and Sorbe (2001) Raso et al. (2006), San Vicente and Sorbe (2001) Cartes (1993a), Cartes (1993b), Cartes et al. (1993), Maynou and Cartes (1998), Sarda` et al. (2003) Cartes et al. (1993) Cartes (1993b), Cartes et al. (1993) Aguzzi et al. (2007a), Fanelli and Cartes (2004), Lagarde`re (1977) Fanelli and Cartes (2004) Aguzzi et al. (2007a), Cartes (1993a), Cartes et al. (1993), Fanelli and Cartes (2004), Johnson et al. (2000), Lagarde`re (1977), Maynou and Cartes (1998), Sarda` et al. (2003) Gue´guen (2001)

D N N D

Raso et al. (2006) Aguzzi et al. (2009c) Aguzzi et al. (2009c) Aguzzi et al. (2009c)

Endobenthic Phyl

Species

Behaviour

Source

Car Car Car Car Pen

Aegeon lacazei Alpheus glaber Chlorotocus crassicornis Crangon crangon Lucifer typus

D D N N N

Aguzzi et al. (2009a), Sarda` et al. (2003), Vereshchka (1995) Aguzzi et al. (2009a), Froglia and Gramitto (1987), Moreno-Amich (1994) Aguzzi et al. (2007a) Kuipers and Dapper (1984), Moller and Jones (1975) Oishi and Saigusa (1997) (continued)

Table 3.2

(continued) Endobenthic

Phyl

Species

Behaviour

Source

Pen Car Car Car Car Car Car Car Car

Melicertus keraturus Periclimenes scriptus Pontophilus norvegicus Processa canaliculata Processa edulis Processa macrophthalma Processa modica Processa nouveli Solenocera membranacea

N D D N N N N N N

Karani et al. (2005) Raso et al. (2006) Sarda` et al. (2003), Maynou and Cartes (1998) Aguzzi et al. (2008a) Guerao and Abello´ (1996), Raso et al. (2006) Raso et al. (2006) Raso et al. (2006) Bauer (1985), Guerao and Abello´ (1996) Aguzzi et al. (2006c), Carpentieri et al. (2005), Despalatovic et al. (2006), Froglia and Gramitto (1987), Lagarde`re (1977)

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Water Column

Otter-trawl Otter-trawl sampling sampling zone zone

BenthoBuriers Burrowers Endobenthic

EpiMeso-

BBL Subbenthic

Nektobenthic Epibenthic

Pelagic

Substrate Hydrography

Walking

Rate of behavioural activity

Swimming

Metabolism Morphology

Figure 3.3 Schematic representation of the classified activity rhythms of species in relation to the marine three-dimensional scenario, including the water column, the benthic boundary layer (BBL), and finally, the superficial strata of the seabed (SB). The otter-trawl sampling zone refers to the lower portion of the BBL where the sampling of demersal species takes place with OTMS net (i.e. 1.2 m height according to trawl mouth vertical aperture; Sarda` et al., 1998). The rhythmic displacements of endobenthic (burrowers and buriers), epibenthic, nektobenthic, or pelagic (epi-, meso-, and benthopelagic) species are indicated by thick black (night) and white (day) arrows that depict its direction within corridors (the dashed cylinders). The importance (i.e. the horizontal thin black arrow) of different physical factors (i.e. substratum and hydrography) on decapod performances during the expression of diel activity rhythms is compared with the resulting (the vertical grey arrow) evolutionary trends of adaptation in their activity rate (from walking to swimming), metabolic activity, and morphology.

as “fully pelagic” when animals always reside in the water column body (Fig. 3.3). Meso- and epipelagic species move through the mid- or superficial-depth strata (reviewed by Herring and Roe, 1988; Vereshchka, 1995). The term benthopelagic can be used to describe the rhythmic displacement of pelagic species when sampling is performed by bottom and not pelagic trawling. Species described as fully pelagic in many studies can also appear in trawling when benthic sampling is performed in a rhythmic fashion. This indicates that animals reside in close contact with the seabed at least once during their 24-h cycle of activity. So, the many species classified as epi- or

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mesopelagic can also be classified as benthopelagic if sampling methods other than pelagic sampling are used (i.e. trawling). In the case of Mediterranean studies (see Section 3.2) the Maireta otter-trawl (OTMS, Sarda` et al., 1998), which mouth height ranges from 1 to 1.5 m from the bottom (SCANMAR sensor data) has been used to sample the demersal community at different times of the day. The net mouth immediately collapses under the weight of its heavy doors at its retrieval from the seabed. In this sense, no species above 1.5–2 m height from the seabed as well as no species within the water column can contaminate the demersal sample (Aguzzi et al., 2006d). Vertical movements are referred to as “diel vertical migrations” (DVMs), a terminology that avoids confusion with other types of migrations, which instead occur on a seasonal basis, since it is associated to the concept of movement with a diel character in its repetition. DVMs are a common behaviour that occurs in a wide range of vertebrate and invertebrate taxa of such diversified environments as lakes and oceans. In several natantian Decapoda, it has been observed that DVM spans from less than a few hundred metres up to two kilometres (Table 3.3) with speeds that can reach 300 m h 1 (Raffaelli et al., 2003). These movements can be gradual (slower migrants) or can assume the form of complete population polar displacement (faster migrants), with the consequent accumulation of individuals at one pole of the displacement range (Roe, 1974, 1984). There is still debate about which environmental factors control this behaviour and its evolutionary meaning (reviewed by Frank and Widder, 1997; Ringelberg, 2010). Actual models focus on the interplay of different motivations at the base of the expression of such rhythmic behaviour: feeding, visual predation avoidance, and hence at the basal and evolutionary level, environmental light intensity. Trade-off models that explain the evolution of DVM in pelagic groups assume the motivation at the base of this behaviour in the maximisation of the mortality/energy gain ratio (De Robertis, 2002). Because many species experience predictable daily fluctuations in predation risk, natural selection favoured the evolution of activity patterns that minimise mortality risks, but maximise foraging. 3.1.1. Light control Changes in light intensity at dusk and dawn seem to be the major factor that controls vertical migrations (reviewed by Cohen and Forward, 2002; Ringelberg and Van Gool, 2003). The majority of decapods perform nocturnal DVM (e.g. Herring and Roe, 1988; Kruppasamy et al., 2006). Animals swim upward during the darkness to feed in shallow-water depths (Foxton and Roe, 1974), avoiding visual predators that usually permanently inhabit the upper water column (Roe and Badcock, 1984). Feeding is always performed in the shallow-water strata of the photic zone where

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Table 3.3 Approximate maxima and minima in the depth ranges of some Natantian Decapoda DVMs Species

Depth range Ontogenesis

Source

Acanthephyra pelagica Acanthephyra purpurea Acanthephyra smithi Funchalia villosa Gennadas elegans

100–1400 0–1000 300–900 50–450 100–1400

Gennadas valens Nematoscelis megalops Oplophorus spinosus

200–900 0–2800 0–500

Franqueville (1971) Foxton (1970a) Frank and Case (1988) Foxton (1970b) Foxton (1970a,b), Koukouras et al. (2000) Foxton (1970b) Franqueville (1971) Foxton (1970a), Frank and Case (1988) Foxton (1970a) Foxton (1970a) Reviewed by Aguzzi et al. (2006d) Reviewed by Koukouras et al. (2000) Hargreaves (1999) Franqueville (1971); Roe (1984) Foxton (1970b) Donaldson (1975) Foxton (1970b) Donaldson (1975) Donaldson (1975) Foxton (1970b) Foxton (1970b) Foxton (1970b), Koukouras et al. (2000) Foxton (1970b) Foxton (1970b), Donaldson (1975) Foxton (1970b) Foxton (1970b), Donaldson (1975) Foxton (1970a) Foxton (1970a), Roe and Badcock (1984), Frank and Case (1988)

Yes

Yes

Parapandalus richardi 0–900 Pasiphaea hoplocerca 200–700 Pasiphaea multidentata 0–1400

Yes Yes

Pasiphaea sivado

0–2000

Yes

Pasiphaea sulcatifrons Sergestes arcticus

300–1300 0–1400

Yes

Sergestes armatus Sergestes atlanticus Sergestes corniculum Sergestes cornutus Sergestes grandis Sergestes japonicus Sergestes pectinatus Sergestes robustus

100–600 20–800 60–1000 20–600 300–1000 600–1000 100–700 500–1000

Yes

Sergestes sargassi Sergestes splendens

100–1000 100–900

Yes Yes

Sergestes tenuiremis Sergestes vigilax

600–1000 25–900

Systellaspis cristata Systellaspis debilis

0–3200 0–800

Yes

Species presenting different depth ranges of distribution (Ontogenesis) between smaller and larger adults are reported (yes).

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photosynthesis occurs and carbon contents are higher (reviewed by BenoitBird et al., 2008). The link between light and DVMs of crustaceans (but also fishes) may involve the following of very restricted isolumes (i.e. depth strata with similar light intensity levels) (Herring and Roe, 1988). Data on light intensity and the distributions of mesopelagic species during their migratory rhythms closely resemble the movements of isolumes in the water column. Light attenuation in water is exponential, and the vertical migrations are often described as an attempt to maintain a constant light regime (Aksens and Giske, 1993). However, it is apparently too “simplistic” a hypothesis for animals to follow particular isolumes that rise and fall at different hours in different depths of the water column (Naylor, 2006). Light intensity changes over relatively short vertical distances, and a population should be able to swim fast enough to follow a precise isolume range (Herring and Roe, 1988; Roe, 1984). Roe (1983) analysed the migrations of euphausiids and found that animals were displaced in association with general light regimes that varied over three orders of magnitude, rather than with specific isolumes. Accordingly, it seems more probable that DVMs are more influenced by the rate of change in light intensity than by absolute light levels. One of the light cues that may trigger the vertical migrations of various species is the relative rate of change in irradiance (Frank and Widder, 1997). The rate of change of light intensity may be the dominant force driving vertical migrations, since that rate is the same through a species’ depth zone. Conversely, animals do not respond to transient changes in light intensity caused by clouds since these are too rapid. DVM likely evolved as a direct reaction of pelagic species to light cycles of different intensity at different depths (Myslinski et al., 2005). In any case, laboratory tests in constant conditions with pelagic animals are scant, so the true endogenously controlled nature (i.e. via the biological clock) of DVM is still controversial (Saigusa, 2001). The fragility of the organisms and the necessity to recreate tanks in the laboratory that efficiently allow the proper expression of vertical displacements limit the potential of testing behavioural performances with an adequate chronobiological protocol (i.e. the assessment of an endogenous control over consecutive days in constant conditions). In spite of the present state of knowledge on biological clocks in organisms of different taxa, the absence of an endogenous mechanism generating and controlling such behaviour seems improbable (Moragn, 2004). In the western Mediterranean, pelagic species display a distribution that is limited to the areas of the slope (Abello´ et al., 2002). During a trawl survey continuously repeated during 4 days at 1–2 h frequency on the shelf and the slope, no benthopelagic species was collected on the shallower depth zone by day or night (Aguzzi et al., 2006d). This phenomenon is not of easy explication and it may result from a complex interplay of factors related to

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183

both the sensibility of circadian system to different light levels and to energetic constrains, which set the bathymetric span of their vertical diel migrations (Aguzzi et al., 2009a). 3.1.2. Predator and feeding control The response of vertically displacing organisms to light intensity is apparently modifiable by environmentally contingent factors such as food availability and temperature (Herring and Roe, 1988). In this context, vertical migrations may represent an adaptive strategy to avoid predation (Aksens and Giske, 1993; Naylor, 2006; Zaret and Suffern, 1976). In the literature, there is overwhelming evidence in support of the predator-avoidance hypothesis as the ultimate cause of DVM, since it is generally accepted that light acts at a basal level to control the daily timing of the migrations, which occur to minimise the mortality risk (reviewed in Frank and Widder, 1997, 2002). Fishes are top-level predators in the pelagic environment (Mauchline and Gordon, 1991). Planktivorous fishes feed preferentially upon largebodied and pigmented zooplankton and decapod micronekton (De Robertis, 2002). Small invertebrates that swim by day in transparent seawater can be easily spotted by these predators. In contrast, hiding and swarming just above the bottom by day largely decreases the vulnerability of prey to these visual predators. In the case of visual predation, two conditions must be met for a fish to see its target (Aksens and Giske, 1993): (1) enough light reflected from the target and (2) enough visual contrast so that the target can be distinguished. This latter depends in turn upon both the size and colour of the animal. Colour changes occur based on the bathymetric distribution of decapods from translucent bodies to red-pigmented and dark-brown ones, moving from shallow to deep-water strata (Herring and Roe, 1988).

3.2. Nektobenthic displacement Similar to pelagic displacements (see Section 3.1), nektobenthic movements occur in a rhythmic fashion along depth gradients close to the bottom, but not within the water column (Fig. 3.3). These occur within the inferior limit of the BBL in close contact with the seabed and are typically appreciable by trawl sampling at different depths and timings (e.g. Moreno-Amich, 1994). Movements from several hundreds of metres to a few kilometres can be reported in animals that perform mixed walk-swimming movements in schools or in isolated fashion. Rhythmic back and forth movements occur between shelves and slopes, hence encompassing depth areas of markedly different ecological characterisation (Benoit-Bird and Au, 2006; BenoitBird et al., 2008; Cartes et al., 1993; Sarda` et al., 2003).

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This type of movement can be observed in decapod micronekton populations that inhabit the deep realm of the slope at daytime, being sampled near shore on the upper shelf at night-time (e.g. Benoit-Bird and Au, 2006). At daytime, these species are identifiable by visual predators, such as other nektobenthic fishes, due to the increased environmental illumination (Cartes, 1995; Lagarde`re, 1977). Accordingly, animals reach shallower depths at night-time, where feeding often occurs (e.g. Aguzzi et al., 2007a; Cartes et al., 1993; Fanelli and Cartes, 2004; Sarda` et al., 2003). The presence of predators exerts a major pressure for nektobenthic species to be in deep water during daylight (Al-Adhub and Naylor, 1977; BenoitBird et al., 2008; Bergstrand et al., 2003). In this sense, the rhythmic displacements of nektobenthic organisms should be regulated by the interplay of light-intensity cycles and feeding, as already explained for the DVMs of pelagic species. Accordingly, diel nektobenthic displacements can be similarly explained in the context of mortality/energy-gaining models in relation to experienced light-intensity levels at times of behavioural activity. In this scenario, studies on pandalid shrimp such as Plesionika martia (Milne-Edwards, 1883) and Plesionika gigliolii (Senna, 1902) are of interest to explain how the long-range displacement of nektobenthic species can be modulated by predatory behaviour. Animals of both species perform rhythmic movements in relation to the day–night cycle between the upper and middle slopes, where illumination varies by several orders of magnitude (Aguzzi et al., 2007a; Sarda` et al., 2003). Apparently, their movement is synchronous with the movement of their prey, for example, the glass shrimp Pasiphaea multidentata Esmark, 1866 (Aguzzi et al., 2006d). In particular, P. martia strictly follows the latter prey, since animals show a strong predatory selectivity for that community element (Cartes, 1993b). Mixed nektobenthic and benthopelagic displacements can be contemporarily present in demersal rhythmic movers. Macquart-Moulin and Patriti (1996) reported that, upon reaching the superficial layers of the water column, the vertically migrating micronekton (i.e. benthopelagic) of the western Mediterranean slope drift towards the coast every night because of the local wind-driven water currents. As a consequence, animals may swim down-slope along the seabed during the day to return to their original depth areas, as they are capable of repeating the same behavioural cycle again. While Macquart-Moulin and Patriti (1996) see this process as passive and environmentally driven, Benoit-Bird and Au (2006) see it as an evolutionarily favoured mechanism that pelagic species possess to occupy new habitat contexts, as they accede to food resources that have not previously been exploited. Several pelagic species are usually collected by bottom trawling in the Mediterranean at depths down to 1400 m (e.g. Acanthephyra ssp., Pasiphaea ssp., Sergestidae spp.; Sarda` et al., 2003; Company et al., 2004) (See Section 3.1). This indicates that these species, although reported as fully

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pelagic in the literature (since captured by pelagic nets), may actually come into contact with the sediment at a certain time of the day, thus acquiring a benthopelagic status. Some of these may even conduct a nektobenthic movement (therefore confirming the dynamic of displacement proposed by Macquart-Moulin and Patriti, 1996). This observation is also reinforced by similarities in the morphology of their carapace (see Section 5.1), which share common features with other more demersal nektobenthic and endobenthic species (Aguzzi et al., 2009c). This may indicate a process of morphological convergence of benthopelagic and nektobenthic species, as both can move within the BBL at a certain moment of their diel rhythm of activity.

3.3. Epibenthic and endobenthic displacements Epibenthic decapods or fishes of deep-water continental margins reside on the seabed surface continuously during the 24-h cycle (Aguzzi et al., 2009c) (Fig. 3.3). Animals never retreat into the sediment and their behavioural rhythms are expressed in terms of locomotor/swimming rate increments (when wandering for foraging) or decrements (when resting). In any case, the displacement, if it occurs, takes place in the same depth area, with no bathymetric gradient of reference. In contrast, deep-water endobenthic species perform diel rhythms of retreat and emergence from the seabed substratum, which is chiefly made by silt and clays on deep-water shelves and slopes. In agreement with Bellwood (2002) and McGaw (2005), endobenthic decapods can be functionally classified as burrowers when animals inhabit tunnels and behavioural rhythms are expressed in terms of sedentary and territorial burrow-oriented behaviour, or alternatively as buriers, when animals simply cover themselves with the sediment. Burrowers in deep-water areas are the ecological equivalent of shelter dwellers in shallow waters. The latter occupy natural refuges, being unable to build burrows in the substrate. Lobsters and some species of crabs in coastal and shallow shelf areas show strong shelter-oriented behaviour as burrowers in deeper water areas. The type of displacement of burying species is therefore similar to the one displayed by nektobenthic animals that move within the deepest strata of the BBL, in contact with the seabed. At times of activity, they wander on the seabed surface, within the BBL, alone, or in schools (Aguzzi et al., 2009c). However, there is a difference: endobenthic movers apparently do not follow a particular depth gradient when active, as they show certain site fidelity; the strength of this remains to date untested, given the scarcity of behavioural observations both in the field and the laboratory (Aguzzi et al., 2006c). Burying behaviour has been extensively studied in penaeid prawns given their commercial importance. Most species are nocturnal and use the

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within-sediment retreat as a means to preserve energy and avoid visual predators that are active in the BBL during the daytime (reviewed by Bishop et al., 2008). Penn (1984) classified penaeid species based on the timing of their burying behaviour: strongly nocturnal species are active in a limited moment of the night and are typically found in shallow water sandy substrata; generally, nocturnal species are broadly active during the entire night, as these species are distributed in silt and clay areas; finally, almost continuously active species are also nocturnal, but their emergence can also be induced during the daytime, depending on the turbidity conditions. These are distributed chiefly in river discharge areas. The classification of burying behaviour in Penaeids resembles the reported modification of emergence rhythms in other endobenthic decapods as function of depth. Burying natantians show generally nocturnal emergence from the seabed on continental shelves, tending towards a diurnal activity on the deeper slope (Aguzzi et al., 2009a). Several species of the Mediterranean deep-water continental margin, such as Chlorotocus crassicornis (Costa, 1871), Solenocera membranacea (Risso, 1816), and Processa spp., emerge from the seabed later in the day (i.e. from night-time to daytime) when comparing trawl catch temporal patterns for populations of shelves and slopes (Aguzzi et al., 2006c,d, 2007a, 2009a). A similar trend was also reported for other burrowing species as for example, the Norway lobster, Nephrops norvegicus (Linnaeus, 1758), and the angular crab, Goneplax rhomboides (Linnaeus, 1758) (Aguzzi et al., 2003; Atkinson and Naylor, 1973). N. norvegicus has been used as a model of reference, since populations at different depths emerge at different times of the day, according to the response of animals to diel fluctuations in blue (i.e. 480 nm) light intensity (reviewed by Aguzzi and Sarda`, 2008a; Aguzzi et al., 2008b). Also, the shallower living American lobster, Homarus americanus (Milne Edwards, 1837), shows a similar bathymetric variation in the timing of its out-of-shelter activity, according to the depth of sampling (Golet et al., 2006). Although the dynamics of emergence rhythms regulation by depth are apparently well proven for endobenthic decapods by field data, its endogenous regulation has been sometimes challenged (Saigusa, 2001; Saigusa et al., 2000). Emergence rhythms seem to weaken with increasing depth, according to a concomitant reduction in environmental illumination at photophase. An endogenous component of the emergence behaviour of shelf-living penaeid prawns was found in the laboratory (Moller and Jones, 1975). Referring to nephropid lobsters, for which the population can attain wider depth ranges of distribution, laboratory tests also showed marked circadian locomotor and emergence rhythms (Aguzzi et al., 2004b; Jury et al., 2005). In the case of N. norvegicus, endogenous rhythms are reported in animals on both the shelf and the slope (reviewed by Aguzzi and Sarda`, 2008a). Recently, Aguzzi et al. (2009a) proposed that the endogenous

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regulation of activity rhythms is always active in endobenthic decapods of the shelf and the slope, but the interspecific interactions (e.g. predation and competition for substrate use) may mask such a bathymetric shift in the timing of activity. Atkinson and Naylor (1973) suggested that the presence of the burrow is important for endobenthic decapods since its presence induces quiescence. Laboratory tests on behavioural rhythms showed that burying Penaeids become arrhythmic in the absence of burrowing medium (Moller and Jones, 1975), but this is not the case of N. norvegicus. Rhythms in this species can manifest with equal strength in the presence or absence of burrowing medium (Aguzzi et al., 2004b). This phenomenon has also been reported for shelter-inhabitant lobsters such as Homarus spp. ( Jury et al., 2005). Accordingly, we propose that burrowers present stronger locomotor activity rhythm in the absence of any medium than buriers, as they are fully adapted to a burrowing life style, which imposes the structuring of activity within limited moments of the day–night cycle. Conversely, burying species show a more relaxed approach to that temporal partitioning in their activity, becoming arrhythmic when a suitable substrate medium is not provided.

4. Interpretations of Activity Rhythms from Trawling Data In deep water continental margins, bottom-trawling is often one of the most technologically and economically feasible systems of sampling (Raffaelli et al., 2003). Bottom-trawl surveys provide the majority of the basic data for population dynamics and distribution, as well as biodiversity estimates. While shallow-water ecologists at last have the potential to sample and resample intensively and repeatedly over a wide range of geographic and temporal scales, the costs of sampling in the deeper waters of the continental margins make it prohibitive (Raffaelli et al., 2003). Bottom-trawl surveys on shelves and slopes are the only practical manner to obtain data on diel behavioural rhythms, based on fluctuations in catches (Aguzzi and Sarda`, 2008a,b). Temporally scheduled trawling provides information on the activity and interactions between sizes, classes, and sexes of the same population or among populations of different species (Hjellvik et al., 2002). Bottom-trawling gives indirect information on species behaviour that is based on an animal’s presence or absence in the catch. The locomotor activity rhythms of targeted species are inferred from fluctuations in captures, but this is an active way to sample (Reebs, 2002). Fluctuations in captures do not provide reference to the animals’ activity levels, per se. All animals present over the seabed on the trawl gear trajectory are captured

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independently of their level of behavioural activity (see Section 3.1). Demersal decapods cannot avoid the net at the towing speed of 1.2 knots (Aguzzi et al., 2009b). This is in contrast to pelagic sampling, where the small mesh size of the trawls imposes a reduced towing speed, micronekton swimming fast enough can avoid capture, and contamination through different depth strata can also occur. Broadly speaking, the knowledge of population distribution is inversely proportional to the knowledge of activity rhythms. Most scientific field surveys devoted to the understanding of demersal resource distributions are carried out on large geographic areas at fixed time intervals to obtain comparable results. Conversely, activity rhythms can be assessed by trawling only when sampling is repeated over time into limited portions of the geographical space, but, although the result is more precise, the space is also more limited. As a consequence, sampling for population assessment during limited times of the day–night cycle may produce biases in the detected distributions when activity rhythms are not properly taken into account (Coll et al., 2010). In other words, limiting the sampling for population assessment to only a few hours of the day provides maps of distributions that represent only “half of the story”. To be fully satisfactory, sampling should be repeated during both day and night in each sampling location (Aguzzi and Bahamon, 2009).

4.1. Data processing The processing of time series of trawling data (Fig. 3.4) can be performed using the concepts and statistical tools of chronobiology if fluctuations in the catches within a population are considered as equivalent to fluctuations in locomotor activity in single individuals, as measured in the laboratory (Aguzzi et al., 2003). The waveform analysis is used to assess the coincidence of peaks (or troughs) in catches that are in agreement with the day–night cycle. Catch patterns made by quantities of captured animals (standardised per km2 of swept seabed surface), taken at an approximately constant frequency over consecutive days (Fig. 3.4(1)), can be partitioned in groups of 24 h (Fig. 3.4(2)). A waveform can be computed by averaging all catches that occurred within the same temporal interval (often of 1- or 2-h length) during consecutive days (Fig. 3.4(3)). Mean catch data can be represented with their standard deviation along with the daily mean (Fig. 3.4(4)), as a horizontal line equivalent to the MESOR (midline estimating statistic of rhythm; Aguzzi et al., 2006a). That daily mean is computed by re-averaging all waveform values, and it is used to detect the onset and offset timing of the peak in relation to the geophysical cycle of reference (e.g. the day–night cycle) (Fig. 3.4(5)) (Aguzzi et al., 2005). The phase relationship analysis (Fig. 3.4(6)) can then be performed by repeating the waveform analysis on a time series of catches of different species within samples taken in the same

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2.

3.

no. ind. km−2

Mean no. ind. km−2

1.

24 h Time of trawling (days)

Time of trawling (h)

4. Mean no. ind. km−2

A

Time of trawling (h)

5.

6. B

Species

A B . . . N

Time of trawling (h)

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area. That analysis is necessary in ecology to explain reported rhythm modulation based on a principle of cause-effect between predators and prey, or among competitors for similar food and substrate resources, as well as to evaluate day–night variations on species diversity indices. It is difficult to interpret a nocturnal or diurnal character in the activity rhythm of a species depending on the timing of peaks in their catches. That interpretation depends upon the endobenthic, nektobenthic, or pelagic type of displacement (Fig. 3.5). Peaks in demersal trawl catches coincide with peaks in behavioural activity only for species with an endobenthic type of displacement (Al-Adhub and Naylor, 1977). Burrowing and burying animals need active locomotion in order to emerge from the substrate. At the opposite, peaks in demersal trawl catches of vertically migrating species (i.e. benthopelagic) indicate the moment of behavioural passivity. Animals can only be captured in trawling at the end of a process of descent into the water column when they are hiding and resting in the BBL, close to the seabed (see Section 3.1). These species swim towards the upper layers of the water column and disappear from the seabed surface during phases of behavioural activation (being hence catchable with pelagic nets at that moment).

4.2. A model to interpret the type of rhythmic displacement The determination of the nocturnal or diurnal character of the activity rhythm of decapods depends upon the species type of displacement (i.e. benthopelagic, nektobenthic, epibenthic, and endobenthic) in relation to the used system of sampling (bottom-trawling). Unfortunately, the type of displacement is unknown in several ecologically and commercially important continental margin species. Accordingly, a new model of interpretation of the type of displacement based on the day–night scheduled sampling at different depths of the continental margin can be proposed (Fig. 3.6). That model has been constructed by comparing bottom-trawl catch patterns reported at different depths for several decapod species (Aguzzi et al., 2009c; Cartes et al., 1993; Sarda` et al., 2003). In the case of benthopelagic species, the day–night differential in animal’s catchability preserves its phase over the depth. These species usually move vertically into the water column at all depths, appearing only on the seabed during the daytime. Differently, nektobenthic species present a timing in peaks of catches that varies according to the depth from nocturnal to diurnal hours from shelves to slopes. The phase inversion is produced by a bulk of animals that moves along the seabed towards shallow-water areas at night and migrates to greater depths in the day. Interestingly, temporally scheduled sampling at the intermediate range of this migration produces arrhythmia in catches, since similar quantities of animals are available for capture both when the population is moving upward and when it is

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Figure 3.6 The interpretation of the different typologies of rhythmic displacement based on day- and night-time catches (no. ind. km 2) obtained by repeating the trawl sampling at three hypothetical different depths of continental margins (e.g. the shelf and the upper and middle slopes). Benthopelagic species preserve the phase of catch increases irrespective of the depth of sampling. Conversely, nektobenthic species present an inversion in the phase of maximum captures according to the depth, given the movement of animals between two bathymetric extremes. Captures at intermediate depths of this range are arrhythmic, since equal proportions of animals are captured as individuals of a population swim both up and down the seabed. Epibenthic species always present arrhythmia in time series of catches at any depth, since animals cannot avoid trawl tow capture by retiring into the substrate or swimming up into the water column. Finally, endobenthic species also present a phase inversion of capture according to the depth of sampling (usually from night-time to daytime), but the captures are crepuscular at intermediate depths. Animals of different depths likely follow different light-intensity conditions, the timing of which is controlled by the sun’s movement, which varies the angle and hence, the depth of penetration of light rays into the water column.

descending back to deeper depths. Referring to epibenthic species, no diel differences in catchability are reported for any depth considered. Animals cannot avoid capture by trawling, and their behavioural rhythmicity can only be studied in laboratory conditions. Referring to endobenthic species, a phase shift in peaks in catches occurs over depth, similarly to what is

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reported for nektobenthic animals. Following the behavioural model of N. norvegicus (revised by Aguzzi and Sarda`, 2008a), animals emerge from their burrows (and are hence captured) at night-time on shallow shelves, at crepuscular hours on lower shelves, and at midday on the slopes (see Section 3.3).

5. Metabolism, Morphology, and Adaptations to Different Types of Displacement and Rhythmic Behaviour According to ecological morphology, the form of a species is related to its role within the community (Motta et al., 1995a,b). The form of an organism constrains its use of ecosystem resources and, at the same time, resource accessibility contributes to the construction of its form. That process occurs via evolution through the confrontation of individuals with important ecological tasks such as feeding, mating, displacement, and predatory evasion. The result of that confrontation sets the base of organism fitness and hence their evolutionary destiny (Carroll, 2001). In this context, the whole form of an organism results from the contemporary action of the selective pressures exerted by different habitats and biotic factors on all their structures (Motta and Kotrschal, 1992). It is therefore of interest to analyse how the morphological variations among individuals, populations, or species correspond to the variations in their ecological role (Antonucci et al., 2009; Colmenero et al., 2010; Costa and Cataudella, 2006; Liesler and Winkler, 1985; Recasens et al., 2006; Sarda` et al., 2005). In marine organisms and especially in decapods, that analysis has been mostly performed in relation to several ecological traits but not to the diurnal or nocturnal character of activity.

5.1. Metabolic convergence in relation to the type of displacement Different decapod species of deep-water continental margins share common metabolic adaptations resulting from a process of evolutive convergence to pelagic, nektobenthic, or endobenthic type of displacement (Fig. 3.3). A linkage has been found between the different levels of behavioural activity, as required by walking or swimming, and the underlying metabolism, as measured by body water and lipid contents, as well as oxygen consumption. A physiological and an ecological classification of species was constructed based on a progressive evolutionary trend of adaptation of organisms from a pelagic to a benthic habitat (Company and Sarda`, 1998): (a) species inhabiting the sea floor (i.e. epi- and endobenthic) were

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identified as those having low lipid and high water content as well as low oxygen consumption rates. Their bodies are relatively large and heavy, which in turn results in a poor swimming capability. These species are good walkers. Nektobenthic and epibenthic species, which inhabit the BBL, have intermediate levels of lipid and water content in their bodies. Species within this group use a mixed walking–swimming mode of displacement and their oxygen consumption rates are higher than those of the endobenthic species. Finally, highly motile epi-, meso-, and benthopelagic species rely on prolonged swimming for their vertical displacement, and their body mass is a constraining factor, as it conditions the efficiency of the diel movements. Their body lipid contents are the highest, but they have the lowest water contents. Oxygen consumption rates are also the highest in relation to the other two groups. Maynou and Cartes (1998) confirmed this evolutionary trend by analysing food consumption in relation to the increasing motility of decapods. Endobenthic and nektobenthic species have a less specialised diet with a pronounced scavenging activity. Conversely, mesopelagic migrators have a more specialised diet and are visual predators.

5.2. Morphological convergence in relation to the type of displacement Sarda` et al. (2005) and recently Aguzzi et al. (2009c) measured the morphological convergence of deep-water continental margin decapods within the three recognised typologies of displacement (i.e. pelagic, nektobenthic, and endobenthic). The results indicated that the metabolic convergence was also accompanied by a certain level of morphological specialisation. That morphological analysis was conducted on cephalothorax profiles (by geometric morphometric analysis of landmarks) and several other biometries, including measures taken in the abdomen and the telson (Fig. 3.7). The shape of the cephalothorax has been generally correlated to its hydrodynamism during swimming, while the shape of the rostrum is related to the escape performance from predators (Cartes et al., 1993; Sarda` et al., 2005). Relatively larger cephalothoraxes were found for endobenthic than nektobenthic animals, with the pelagic species being relatively the smallest. Endobenthic decapods use the seabed sediment to shelter (Abele, 1974). Their relatively larger cephalothorax is the product of an enlargement of their branchial chambers, which was driven by the necessity to increase the space where water free from sediment can have contact with the gills. This increases the efficiency of oxygen exchange in the conditions of an animal’s strict association with the sediment (Bellwood, 2002; Swain et al., 1988). The pelagic species are at the opposite extreme of this tendency. Organisms within this group present the relatively smallest cephalothoraxes in terms of its lateral compression, which decreases the body drag and enhances their

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Figure 3.7 The progressive morphological variation depicting the adaptation of Natantian Decapoda according to two different major evolutionary axes: the different typologies of displacement (i.e. endobenthic and pelagic, considering the nektobenthic as an intermediate category) and the nocturnal or diurnal activity rhythm. The morphological variation is represented through splines obtained from carapace profile analyses (by landmarks) of several species of Caridea, Penaeidea, and Sergestoidea (adapted from Aguzzi et al., 2009c).

vertical swimming performance (Kils, 1982; Lighthill, 1969). Nektobenthic species have a cephalothorax of relatively intermediate size for the action of two opposite selective forces. The necessity to increase the swimming ability, as required by the horizontal mode of displacement, is contemporarily accompanied by the necessity to reduce the body drag. This results in laterally flattened and short cephalothoraxes. In Natantian Decapoda, evasion of predators occurs by means of powerful backward–upward swimming bouts (Sarda` et al., 2005). The rostrum shape plays an important role in the swimming performance during evasive responses to predators, since it redirects the trajectory of the animals (Cartes et al., 1993). Nektobenthic species have a relatively greater upward roundness of the rostrum, as the animals move away from the seabed into the water column above during predator evasion (Sarda` et al., 2005). Conversely, in pelagic species that avoid predators with zigzag swimming, the rostrum is relatively shorter, and hence, facilitates a random trajectory of escape (Cartes et al., 1993). In endobenthic species, the rostrum is relatively shortened and thicker. This form is determined by the digging performance requirements rather than those related to the predatory evasion by swimming. Buriers may

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use that structure to bury not only at times of behavioural inactivity, but also in a sudden fashion to avoid predators (Sarda` et al., 2005).

5.3. Morphological convergence in relation to the activity rhythm Organisms adapt their morphology to optimise their ecological tasks such as predator-avoidance, feeding, mating, and habitat use (Ross, 1986; Schoener, 1974). Animals respond to day–night cycles when diel changes in ambient light are sufficient to influence their perception of the surrounding environment (Pittman and McAlpine, 2001). A linkage of morphology to the light-intensity cycle via species activity rhythm may exist in several decapods, although this phenomenon has been poorly investigated. The study of the morphological convergence in different natantian species based on their common nocturnal or diurnal activity is based on the assumption that organisms experiencing similar light-intensity levels during the active phase of their behavioural rhythms are subjected to similar selective pressures, a fact that results into a convergence in their forms (Pulcini et al., 2008). Aguzzi et al. (2009c) explained the process of convergence in natantians within the framework of existing hypotheses on visual predators as modulators of behaviour in species at the midlevel of the marine food web. Since prey experience predictable risks of mortality during a certain moment of the day–night cycle (usually when active), a selection for the temporal concentration of their activity at certain hours as well as a consequent morphological adaptation may take place. This occurs in decapods since species are generally located at intermediate–lower trophic levels (Frederiksen et al., 2006). Visual predators such as fishes (e.g. Roe and Badcock, 1984) surely play an important role in the modulation of their behaviour and hence, in the process of their morphological convergence (Aksens and Giske, 1993; De Robertis, 2002; Zaret and Suffern, 1976). The fitness of species is driven by visual predators that in turn force prey not only towards a temporal patterning of their behaviour (Kronfeld-Schor and Dayan, 2003), but also to their morphological specialisation in order to not be seen, which at the same time makes them more efficient in avoiding capture. Displacement type and light intensity interact in the process of morphological convergence of natantians (Aguzzi et al., 2009c). The process of morphological and behavioural selection is chiefly driven by the efficiency of displacement during the current expression of diel behavioural activity. This selection is also driven by visual predator evasion, and the efficiency of evasion depends upon the surrounding illumination. The approach to categorise species of Caridea, Penaeidea, and Sergestoidea for their ecological function without giving reference to their different phylogenetic origin

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can be a useful tool for the description of a marine community’s structure (Moody and Steneck, 1993). Such structuring is based on the identification of “guilds of movers”: groups of species for which a similar common type of displacement produces a convergence of their metabolism, form, and diurnal or nocturnal character of activity rhythm. Considering that continental margin natantians usually do not show burrowing habits (i.e. species permanently inhabiting burrows of precise architecture) and that most of the studied species are buriers (i.e. animals simply cover themselves by mud a timings of inactivity), we hypothesise that nektobenthic species evolved a burying habit similar to that of crabs and lobsters, hence becoming buriers. The transient sheltering of shrimp-like forms into the substrate is an adaptation to preserve the optimum bathymetry of populations, thus avoiding high-energy and time-consuming diel bathymetric displacements along a depth gradient, as typically performed by the other nektobenthic animals.

5.4. The behaviour of decapods as a phenotypic trait Considerations on the process of morphological convergence in decapods based on the type of displacement and nocturnal or diurnal activity should be formulated in a scenario where the behaviour of species is considered as equivalent to any other phenotypic trait, evolving essentially in a fashion similar to the morphology (Queiroz and Wimberger, 1993). It is still under debate whether behavioural characteristics are inferior to morphological characteristics as indicators of phylogenetic relatedness. Regardless, the behaviour of a species defines many of the selective pressures to which it is subjected (Futuyma and Moreno, 1988). The behaviour is prone to convergence (or divergence) in phylogenetically related taxa, in a fashion similar to morphological characteristics. The limitation on available data on the activity rhythms of deep-water continental margin natantia is clearly a shortcoming of research comparing morphology and diel behaviour. This state of things can be applied to several studies of this kind when these consider a pool of species for which there are marked differences in behavioural data. The taxonomic groups for which more behavioural data are available play a major role in shaping results (Queiroz and Wimberger, 1993). Some superfamilies of Decapoda natantian (e.g. Penaeidea, Sergestoidea, and Caridea) were overrepresented in the morphological and behavioural analysis of convergence by Aguzzi et al. (2009c). The difficulty in recompiling behavioural data on activity rhythms and the type of displacement in deep-water continental margin species conditions the idea that marine biologists have on the evolutionary mechanisms by which light influences behaviour along with the morphology.

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6. Ontogenetic and Gender Modulation of Behavioural Rhythms Ontogenetic modifications of behavioural rhythms in marine organisms generally occur in few representative forms: (1) with the occupation of different habitats, as in the case of pelagic larvae and benthic adults, (2) with shallower living juveniles and deeper living adults (i.e. holoplanktonic species), and (3) for the occupation of the same habitat with a shift in the phase of activity, as animals are active in the same area at different moments of the 24-h cycle. This latter may also occur at the terminal stages of ontogeny, at adulthood, among adults of different size-classes, or in relation to the stage of the reproductive cycle. According to this scenario, we reviewed the presence of ontogenetic- or reproductive-stage-related differences in the behavioural rhythm of deep-water continental margin decapods depending on the species’ type of displacement.

6.1. Modulations in epi- and mesopelagic species Several studies have reported differences in the range of vertical displacement between smaller and larger adult shrimps. A series of classic examples are summarised in Table 3.3. Depth partitioning has been observed between natantias of different-sized individuals during the DVMs, with smaller animals present in shallower depths than large older stages (Foxton, 1970a; Frank and Widder, 2002). In the case of the deep-sea shrimp Systellaspis debilis (Milne-Edwards, 1881), the migratory pattern of juveniles is not coherent, but these occur in shallower water areas than adults during the day (Foxton, 1970a). The shrimp Gennadas elegans (Smith, 1882) does not apparently show size-related differences in behaviour (Roe, 1984), but upon closer analysis, differences in the range of diel migration between larger and smaller individuals are present for only females (Franqueville, 1971). Giske et al. (1990) hypothesised that bathymetric a modification in the ranges of DVMs for natantian individuals of different class-sizes occurs due to their differential visibility in the water column. This behavioural difference results in a developmentally descending pattern: the smaller and less visible juveniles live in the shallow layers, which are characterised by rich food/high predation risks, while the larger and therefore more visible adults live in deep layers, which are characterised by a reduced food supply but also lower predation. Conversely, bathypelagic species show less marked diel migration patterns due to the relaxation of predation pressure under conditions of reduced visibility (Yamaguchi et al., 2004).

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In environments dominated by visual predators, the timing of displacement between the surface and deeper waters should not be identical for all size-classes of preyed decapods (De Robertis, 2002). Planktivorous fishes rely upon visual predation, and size selection is also common in inshore and freshwater fishes. Smaller preys enter surface waters earlier and leave later than larger prey (Frank and Widder, 1997; Roe and Badcock, 1984). When the visual predator risk increases steeply with size, the difference in the timing of vertical migration among size-classes will be larger, since planktonic fishes are highly size selective and inflict disproportionate mortality on large-bodied zooplankton (De Robertis, 2002). Similar trends have been reported in pelagic fishes when they are prey (Petrakis et al., 2001): small planktivorous fishes also reduce the risk of daytime predation by schooling or by performing DVMs as well.

6.2. Modulations in benthopelagic species In contrast to the DVMs of epi- and mesopelagic species that chiefly show size-related modifications in the bathymetric ranges of displacement, benthopelagic species present modifications in their type of displacement (i.e. from benthopelagic to nektobenthic). This may be favoured by their proximity with the seabed in a certain moment of the day–night cycle. A clear example of such size-based modification is represented by the congeneric and benthopelagic glass shrimps, Pasiphaea sivado (Risso, 1816) and P. multidentata (Fig. 3.8). That example is of interest, since the change in the activity rhythm is accompanied by a change in the type of displacement, which is a phenomenon not previously reported for other epi- and mesopelagic species (Aguzzi et al., 2006d). Both species of Pasiphaea reach the superficial water column layers at night-time to feed under the protection of darkness. As illumination rises, animals descend to rest on the seabed (Fig. 3.8(1)). Their bottom-trawl catches are higher at daytime (Fig. 3.8 (2)). Individuals of both species show similar DVM until a certain size threshold is attained in the length of the carapace (Fig. 3.8(3)). When individuals of P. multidentata exceed 30 mm of carapace length, a size not attainable by the smaller P. sivado, their type of displacement transforms into a nektobenthic one (Fig. 3.8(4)). Animals constantly avoid the water column, since they would be visible to pelagic predators both during the day and night, preferring the nektobenthic corridor as the scene of their diel migrations. P. multidentata increases its presence on the upper areas of the slope at night-time to feed in shallow-water areas (Cartes, 1993a), but descends into the depth of the lower slope during the day. That modification in the diel rhythmic behaviour of animals is not only reported in relation to the type of displacement; there is also a change in the response of animals to the light cycle (see Fig. 3.8(4)). Although the activity

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Figure 3.8 Light-intensity measures as the photon fluency rate (PFR) (1), the catchability patterns (no. ind. km 2) (2) of Pasiphaea sivado (grey) and P. multidentata (black), and the class size frequency distribution in their carapace lengths (CL; mm) (3), as measured during 4 days of continuous bottom-trawl sampling on the continental slope (400–430 m) in October (adapted from Company et al., 2001; Aguzzi et al., 2006d). The pattern of capture in P. multidentata changes (i.e. as indicated by oblique dashed arrows) from daytime to night-time as animals exceed the carapace length threshold of 30 mm (as indicated but the horizontal dashed line). The modification in the type of displacement occurs in large adults (4) that shift the expression of their activity rhythm from a

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rhythm preserves its nocturnal character, since large animals swim from the lower to the upper slope at night-time, their sensitivity to light levels triggering such a downward nektobenthic migration is now increased. Large adults are more sensitive to light and avoid it at daytime on the upper slope, which is the depth stratum chosen by smaller individuals in order to rest. Another interesting case may be represented by shrimp Sergestes arcticus (see Section 3.2). This species has been described as fully pelagic with different bathymetric ranges of DVM between juveniles and adults (see Table 3.3). A recent survey on the slope (400 m depth; authors’ unpublished data) reported a selective capture of juveniles by trawling at daytime. At the same time, Sarda` et al. (2003) collected adults of this species in deeper water areas down to 1000 m depth. Possibly, adults DVM takes place within greater depth ranges than the one of juveniles, as the latter are present on the upper slope and the other distributed mainly on the middle and lower slope (Fig. 3.9).

6.3. Modulations in nektobenthic and endobenthic species The majority of to-date-studied nektobenthic species perform diel displacements, reaching the shallow-water areas of the middle slope at night-time and retiring during the daytime to the darker, lower slope zones (Aguzzi et al., 2007a; Sarda` et al., 2003). The size of the benthic animals still matters in relation to the threat of visual predators. Animals mostly follow similar diel migratory behaviour at any size when species are not too large (e.g. Plesionika spp.; Aguzzi et al., 2007a). In contrast, large migrating species, such as the red shrimp, Aristeus antennatus, have different ranges of migration between larger and smaller animals (Sarda` et al., 2003; Tobar and Sarda`, 1992). Juveniles are never captured with adults in bottom-trawling suggesting their confinement in lower slope aphotic zones (i.e. below 1500 m depth). In endobenthic species, differences are reported among burrowers (i.e. tunnel makers) and buriers in relation to the modulation of emergence by size. Generally, all endobenthic species seem to show similar substrate emergence rhythms when specimens do not attain too large sizes at adulthood. In species that attain great sizes, an increase has been reported in the pelagic to a benthic environment, as detected by repeating the day–night sampling at 400 m and 1000 m depth (Aguzzi et al., 2006d; Sarda` et al., 2003). The change from a benthopelagic to a nektobenthic type of displacement is associated with a modification in the sensitivity to light intensity (as indicated by the axis of light-intensity gradient). The isobathic line (400 m depth) is indicated as the zone where the change in the type of displacement was detected. Black, grey, and white arrows indicate respectively, the displacement of individuals at night, day, and crepuscular hours.

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Figure 3.9 Waveform analysis of catchability patterns subdivided by class-size groups (i.e. black thick line, adults; black thin line, juveniles) for different endobenthic (endo), nektobenthic (nekto), and finally, benthopelagic (bentho) decapods sampled during day–night trawling surveys in October and June on the continual shelf (100–110 m) and slope (400–430 m) in the western Mediterranean (adapted from the author’s own unpublished data and from: Aguzzi et al., 2006c, d; 2007a; 2008a; 2009a,b). Species are grouped according to their different type of displacement to evidence the occurrence of potential modulations of their behaviour according to their small and large adult or juvenile status. Dashed vertical rectangles indicate the night duration. For S. arcticus, only small individuals (carapace length less than 5 mm) appeared in both surveys. For P. longirostris, data of class-sizes are presented only for June, when solely juveniles were captured. In October, data (in grey) are presented with no class-size distinction.

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duration of emergence from the substrate for large adults. That phenomenon is reported for both clawed lobsters and penaeid prawns, and it is possibly justified by a behavioural independency from the threat of visual predation and by the increased feeding-metabolic demand. For very large animals such as Homarus spp., the out-of-shelter activity is increased, rather than suppressed, and this serves as an indication that increases in size and predation threat do not comparatively increment in a similar manner. Conversely, adults do not present modifications in diel behaviour within an intermediate range of size-classes. Similarly, there have been several reports that the Norway lobster, N. norvegicus adults can be captured at any time of the day as a marker of an increase in the temporal duration of their emergence (Andersen, 1962; Chapman and Howard, 1979). This same phenomenon was not observed in other field studies (Aguzzi et al., 2003; Farmer, 1974; Froglia, 1972.). Spiny lobsters also undergo a similar ontogenetic reduction in the time of shelter occupancy, which suggests a decrease in the perceived predation risk as animal size increases. An increased feeding demand of large adults may also be involved in emergence rhythms modulation in natantian decapods, where claw weaponry is absent (Weiss et al., 2007). For large species within this group, such as penaeids, the duration of emergence increases with size (Bishop and Khan, 1999; Honculada-Primavera and Lebata, 1995). These species are broadly nocturnal, but large animals may also be captured during the day. This indicates that the need for feeding may overcome limitations to movement that are imposed by visual predator pressure.

6.4. A general hypothesis on modulation of rhythmic behaviour at adulthood by ontogeny and reproductive cycle In natantian and reptantian Decapoda, a modulation of behavioural rhythms according to the size can be reported (Fig. 3.9). We reviewed this aspect by focusing on few selected species of deep-water continental margins, for which sex and size structure of bottom-trawl catches at day and night-time were available. Our comparison was limited to a small sample of species, but the analysis of catch patterns for juveniles and adults or berried and unberried females in taxa performing benthopelagic, nektobenthic, and endobenthic rhythmic displacements seems to indicate what follows. Benthopelagic species show modifications in their type of displacement only when species attain a certain size threshold at adulthood. In this sense, the glass shrimp, P. multidentata, may represent an example of broad interest for other pelagic species (see Fig. 3.9). Not only are different ranges of vertical migrations attained depending from the juvenile or adult conditions, but the water column is also avoided permanently by the larger adults.

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As opposed to the pelagic environment where the increase of size represents a threat for vertical migrators given the presence of visual predators, the seabed provides a better site for protection. In this sense, demersal nektobenthic and endobenthic species present different ontogenetic modulations of their activity rhythms in comparison to benthopelagic ones (Fig. 3.9). Data for nektobenthic species are scant, although juveniles are not often sampled (e.g. A. antennatus) as an indication that possibly, smaller individuals are relegated in certain depth areas (e.g. the Deep-Sea), where trawling is not often performed. Data for endobenthic species are comparatively more abundant. The modification in the expression of their activity rhythms is less a matter of size. Solenocera, Processa, and Chlorotocus burying natantian genera (i.e. shrimp and prawns) do not display ontogenetic differences in emergence rhythmicity, as trawl catch patterns are similar in small and large individuals (Fig. 3.9). This is probably due to the fact that the range of sizes attained at adulthood is reduced compared to other ecologically equivalent species of larger sizes (e.g. clawed lobsters) (e.g. Chapman, 1980; Cobb, 1971, 1977). Visual predators represent a threat only during activity phases, as large or small adults are equally protected by the sediment when resting within it. However, differences in the reported emergence rhythms related to size are reported for some species of endobenthic decapods. These are likely the product of intraspecific competition for cannibalism or aggressive behaviour, as in the case of larger and smaller swimming portunid crab, Liocarcinus depurator (Linnaeus, 1758) (Aguzzi et al., 2009b) and N. norvegicus (Aguzzi et al., 2003). Referring to modifications of behavioural rhythms by the reproductive stage, this aspect has been investigated by temporally scheduled trawling chiefly in endobenthic species. Differently from pelagic and nektobenthic species, endobenthos may present consistent alterations in substrate emergence rhythmicity when eggs are present (Ruiz-Tagle et al., 2002). Animals may force emergence at moments not only related to the biological clock control, but also for the need to increase the oxygenation of egg masses. That modification in the duration of emergence behaviour is apparently different in burrowers and buriers. Gender-related differences in the diel emergence behaviour of the N. norvegicus were hypothesised based on the seasonal fluctuations in the sex-ratio of catches (Aguzzi et al., 2004a; Orsi Relini et al., 1998). N. norvegicus is a burrower and lives in tunnels, the diameters of which are sufficiently large to permit the recirculation of water following body movement (Chapman et al., 1975). Apparently, females do not emerge when berried, as they protect their eggs by remaining in the tunnels for longer periods of time, almost always avoiding trawl tow capture. Berried females may spend periods at the entrance of their burrow (i.e. door-keeping behaviour), as observed in other marine and terrestrial burrowing invertebrates

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(William and Mobberly, 1964; Ennis, 1984; Atkinson et al., 2003). Doorkeeping behaviour is intensified when females are berried and thereby decrease the range and frequency of emergence (Aguzzi et al., 2008b). The burying prawn, Processa canaliculata (Leach, 1815), shows arrhythmia in time series of trawl catches when berried females are considered (Aguzzi et al., 2008a). P. canaliculata cover itself by mud and this can stack around egg masses at times of hiding in the substrate. The presence of eggs apparently forces animals to spend more time out of the sediment in order to improve oxygenation of the egg masses that are attached to their pleopods.

7. Biological Clocks and Bathymetric Ranges of Species’ Distribution The pelagic environment represents an ideal model to explain the rhythmic behaviour of species in the context of variable light intensity ranges (Roe, 1983). Light has been discussed in connection with the diel variation in the distribution of many pelagic species (reviewed by Naylor, 2006). Conversely, comparatively less scientific effort has been devoted to demersal organisms. The dynamic of their population distribution on shelves and slopes in relation to the perceived illumination ranges and the functioning of the circadian biological clock (that regulates behaviour) are still relatively unknown. Currently, the depth distribution of demersal species has been chiefly analysed in relation to trophism, substrate type, and related hydrodynamic factors. Species occurrence should also be considered in relation to the photosensitivity of their circadian system (Waterman, 2001). In contrast to the 2D context of the firm land, where the vertical attenuation of light is negligible (with the exception of particular environments such as for example, the tropical rain forests), the three-dimensional sea imposes an elevated plasticity in the functioning of the circadian system to different lightintensity levels at different depths. Species of continental margins within the twilight zone evolved in a context where light-intensity cycles vary the amplitude of fluctuation at different depths. Possibly, the bathymetric range of species distribution is also conditioned by the amplitude of the lightintensity cycle via the sensitivity of the circadian system.

7.1. The effect of season In a recent work by Aguzzi et al. (2009a), the authors observed how several species of demersal decapods within the western Mediterranean shelf and slope vary their depth range of distribution according to the season. By preserving a constant depth of sampling on the slope (at 400–430 m), temporally scheduled trawling in autumn–winter and spring–summer

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produced differently defined diel patterns in the catchability of several species. In spring–summer, the reduction in sampled animals caused a disruption in the time series of data for the majority of analysed species. An increase in the length of the photoperiod is accompanied at that time by a concomitant decrease in light levels at the bottom (Aguzzi et al., 2003). The phytoplankton biomass rises in the water column and increases its overall turbidity (e.g. Bahamon and Cruzado, 2003). Present results on seasonally dependent trawl catch patterns suggested a scenario where a species’ bathymetric range of distribution is influenced by variations in the light regime. Two different dynamics may account for this phenomenon. First, the seasonal modification in activity rhythms (as photoperiodic response; see Section 1.4) may be related to the processes of reproduction and moulting, which are both still poorly studied for deep-water continental margin decapods (Company et al., 2001, 2003). Second, many species may displace to greater depths in response to the increased photoperiod length, which may augment the chance of a visual predatory threat. This threat may push the more motile and less sedentary populations of burying and nektobenthic decapods into deeper darker realms. The mechanism by which light may affect the bathymetric distribution of a species is probably linked to metabolism. Light regulates behavioural performances during the phases of activity. A decline in protein content with increasing depth is related to a decline in the locomotor capacity of organisms, as provoked by a decline in the vision capability of their predators (Childress, 1995). In this sense, the metabolic requirements to evade predation may increase in a seasonally controlled manner in preyed decapods of the slope, based on increments in the behavioural activity of their predators (likely fishes and cephalopods).

7.2. Endogenous rhythms and masking as a function of depth Activity rhythms are strongly regulated by the entraining action that light exerts on a species’ biological clock on the shelves (Fig. 3.10). Animals found on the shelves have an endogenous control of their behaviour that runs in agreement with the day–night cycle, as their activity is confined to crepuscular or darkness hours. For deeper slope species, such regulation gets weaker compared to other environmental influences (Aguzzi et al., 2009a). The rhythmic regulation of their behaviour in deep-water areas is still active, but its effects may be masked by the overwhelming influence of the surrounding community. On the slope, species modulate the expression of their behavioural rhythms in an increasingly light-independent manner due to interspecific influences such as predation or competition for the substrate. The comparative analysis of activity rhythms in several decapod species of a wide depth range of distribution (on shelves and the slopes) is of interest to

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Figure 3.10 The duration of significant increases in catches (1) as reported during 4 days of trawling on the continental shelf (100–110 m) and slope (400–430 m) in October (adapted from Aguzzi et al., 2009a). Shaded grey rectangles indicate the night duration. The phase of behavioural rhythms for each species was defined using a waveform analysis of the time series of abundance data from trawls (see procedure detailed in Section 4.1; see Fig. 3.4). Species activity rhythms are increasingly masked over the depth by other contingent ecological forces

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identify the presence of a common regulatory pattern of their behaviour under light-intensity cycles of different amplitudes (Fig. 3.10). Endobenthic, territorial, and predatory species such as N. norvegicus can be used as references for chronobiological studies of that kind. Its burrow-emergence rhythmicity at different depths varies from nocturnal to diurnal on the shelves and slopes, respectively (Aguzzi and Sarda`, 2008a). Although substrate emergence tends to be diurnal on the slope, this behaviour is nocturnal on the shelf. N. norvegicus presents clearer rhythmicity at all depths among all other endobenthic decapods of shelf and slope communities tested to date. Other decapods that are distributed on both the shelves and the slopes show activity rhythms that are strongly associated with the day–night cycle only on the former depth (Aguzzi et al., 2009a; Fig. 3.10). N. norvegicus is a megabenthic predator, which exerts strong territorial control on seabed areas that are close to its burrow entrances. All other endobenthic animals are smaller and tend to modify the timing of their emergence with respect to Nephrops and other potentially active predators (e.g. fishes or cephalopods). These species delay their activity towards sunset. The increase in the predatory activity by fishes on the slope may play an important role in this dynamic, but its importance has not yet been properly tested. The phenomenon of rhythms alteration as a function of depth has been related to the combined reduction in light intensity and increases in the interspecific competition for substrate use in sympatric species that always stay in contact with the seabed sediment during the 24-h period. Other species show concomitant increases in their presence at the seabed (i.e. by trawl catchability) and overlap the timing of maximum emergence in Nephrops’ populations (see Fig. 3.10). Interestingly, these species are fully benthopelagic, so the source of conflict due to substrate use when present on the seabed is likely reduced.

such as interspecific competition at activity phases for the substrate use. In this sense, the megabenthic territorial and predator decapod Nephrops norvegicus (in grey) is the only one that presents clear activity rhythms at both depths, as the activity rhythm of all other endobenthic species (in black) is disrupted. Only benthopelagic species (in white) show increases in catchability that coincide with Nephrops, as allowed by the reduced competition for substrate use. That trend of variation in catch patterns according to the depth of sampling (2) is interpreted assuming that the progressive decrement in the experienced intensity of the light cycle (from approx. 10 lx on the lower shelf to values below 0.1 lx on the upper slope) weakens its control on species’ diel behaviours. The species codes are (as they appear in the column) N. nor (Nephrops norvegicus); A. gla (Alpheus glaber); C. cra (Chlorotocus crassicornis); P. can (Processa canaliculata); S. mem (Solenocera membranacea); L. dep (Liocarcinus depurator); P. lon (Parapenaeus longirostris); G. rho (Goneplax rhomboides); C. mac (Calocaris macandrae); M. cou (Monodaeus couchii); M. int (Munida intermedia); M. iri (Munida iris); M. ten (Munida tenuimana); M. tub (Macropipus tuberculatus); P. gig (Plesionika gigliolii); P. mar (Plesionika martia); P. mul (Pasiphaea multidentata); P. siv (Pasiphaea sivado); and S. arc (Sergestes arcticus).

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8. Conclusions In the present review, we presented a synthesis of the current knowledge on activity rhythms of deep water and deep-sea decapods. Behavioural rhythms were discussed not only in relation to geophysical cycles of recognised importance, such as the day–night cycle, but also in relation to novel geophysical modulators such as fluctuations in hydrodynamism, as produced by internal tides and inertial currents. We performed our analysis by subdividing species into different groups based on the different types of displacement (i.e. pelagic, nektobenthic, endobenthic, and epibenthic), with each group characterised by peculiar metabolic and morphological adaptations. Finally, we attempted a generalisation on how activity rhythms are differently influenced by size, sex, and the stage of the reproductive cycle within species of these groups. As result of this effort, it is evident that the current basic knowledge on activity rhythms in species of deep-water continental margins is poor. This is because it is not presently known to what extent light influences the basic life traits of their biology, including diel and seasonal rhythms, metabolic and morphological adaptations, and the associated population distributions. For that reason, the scientific effort, which is devoted to the understanding of rhythms generation as well as control and masking in relation to photic and non-photic geophysical cycles and community influences, is still necessarily placed in the framework of descriptive biology for deep-water organisms. The majority of proposed models for biological clock functioning (at the molecular, hormonal–physiological, and behavioural levels) are chiefly inferred from shallow-water species that live in a bi-dimensional world. In deep-water continental margins, the vertical depth gradient complicates the analysis of biological rhythmicity for the mixing of day–night, tidal, and inertial currents’ geophysical cycles. Presently, there are no models that account for biological clock regulation at diel and seasonal bases for species with wide depth ranges of distribution. In addition, there are no models on rhythm entrainment to current speed variations in the deep sea. The light levels experienced by animals during their phases of behavioural activity determine the type of experienced interspecific interactions. Visual predators play a major role in the determination of prey fitness in photic depth areas of continental margins. Visual selection by predators occurs when animals are actively moving into different compartments of their corridor of displacement. Because decapods are at the intermediate nodes of the marine food webs, the species experience predictable diel fluctuations in predation risk and therefore have evolved activity patterns

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that minimise mortality risks and maximise foraging opportunities. The long evolutionary history that is shared by visual predators and their prey makes predation one of the strongest selective forces that impose the temporal structuring of activity rhythms and depth distribution in decapods. The ecological and habitat constraints, which are associated with the different types of displacement, influence the evolution of activity rhythms in decapods. That process of adaptation occurs in a similar fashion in phylogenetically distinct species (all belonging to the natantian morphotype). Pelagic species are mostly nocturnal unless they occupy very deepwater ranges; hence, they are behaviourally arrhythmic or characterised by an inverse diurnal migration. Similarly, species of more benthic habits, such as nektobenthic movers, swim along the bottom towards shallower seabed areas at night-time in order to feed. In contrast, endobenthic species are mostly nocturnal in shallower areas, but become increasingly diurnal as the depth of sampling increases. Visual predation requires light, so the temporal structuring of prey activity rhythms is ultimately imposed by the day–night cycle, since this cycle drives the functioning of biological clocks in both predators and their prey. Accordingly, the biological clocks of species at different depths have evolved to work within certain ranges of sensitivity for light detection. In this sense, the reported bathymetric distributions of species may primarily depend on the ability of species’ biological clocks to modulate the rhythmic behaviour of local populations in accordance with surrounding photic signals. In spite of these considerations, we judge that the light intensity (via visual predation selection), rather than the trophism alone, may also contribute as a major evolutionary force in the regulation of the reported bathymetric ranges of decapod distributions, as has been the conclusion for the vast majority of oceanic vertically migrating species.

ACKNOWLEDGEMENTS The authors would like to thank Dr. F. Sarda` (ICM-CSIC, Spain) for the collaboration, coordination, help, and scientific advice he provided to our research over the last years. We also extend this acknowledgement to all collaborators that made it possible for us to accomplish this task: Dr. P. Abello´ (ICM-CSIC, Spain), Dr. N. Bahamon (CEAB-CSIC, Spain), Dr. G. Rottllant (IRTA, Spain), Dr. J. J. Chiesa (Universidad Nacional de Quilmes, Argentina), Dr. L. Marotta (Entropia, Italy), and finally, Dr. C. Costa and Dr. P. Menesatti (CRA-ING, Agricultural Research Council, Italy). Special thanks is also given to Mr. J. A. Garcı´a (ICM-CSIC, Spain) for all the technical help he has provided in these years and Prof. E. Naylor for his constant help and advice.

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REFERENCES Abele, L. G. (1974). Species diversity of decapods crustaceans in marine habitats. Ecology 55, 156–161. Abello´, P., Valladares, F. J., and Castello´n, A. (1988). Analysis of the structure of decapod crustacean assemblages off the Catalan coast (North-West Mediterranean). Mar. Biol. 98, 39–49. Abello´, P., Carbonell, A., and Torres, P. (2002). Biogeography of epibenthic crustaceans on the shelf and upper slope off the Iberian Peninsula Mediterranean coasts: implications for the establishment of natural management areas. Sci. Mar. 66, 183–198. Agapito, M. T., Herrero, B., Pablos, M. I., Miguel, J. L., and Recio, J. M. (1995). Circadian rhythms of melatonin and serotonin-N-acetyltransferase activity in Procambarus clarkii. Comp. Biochem. Physiol. 112A, 179–185. Aguzzi, J., and Bahamon, N. (2009). Modeled day-night biases in decapod assessment by bottom trawling survey. Fish. Res. 100, 274–280. Aguzzi, J., and Chiesa, J. J. (2005). The cardiac activity of Nephrops norvegicus (Decapoda: Nephropidae): the relationship between ultradian and circadian rhythms. J. Crustacean Biol. 25, 577–584. Aguzzi, J., and Sarda`, F. (2008a). A history of recent advancements on Nephrops norvegicus behavioural and physiological rhythms. Rev. Fish Biol. Fish. 18, 235–248. Aguzzi, J., and Sarda`, F. (2008b). Biological rhythms in the marine environment: The Norway lobster (Nephrops norvegicus, L.) as a case study. Contrib. Sci. 3, 493–500. Aguzzi, J., Sarda`, F., Abello´, P., Company, J. B., and Rotllant, G. (2003). Diel patterns of Nephrops norvegicus catchability (Decapoda: Nephropidae) in the north-western Mediterranean: a perspective through depth and season. Mar. Ecol. Prog. Ser. 258, 201–211. Aguzzi, J., Allue´, R., and Sarda`, F. (2004a). Characterization of seasonal and diel variations in Nephrops norvegicus (Decapoda: Nephropidae) landings off the Catalan Coasts. Fish. Res. 69, 293–300. Aguzzi, J., Company, J. B., and Abello´, P. (2004b). Locomotor activity of continental slope Nephrops norvegicus (Decapoda: Nephropidae). J. Crustacean Biol. 24, 282–290. Aguzzi, J., Cuesta, J. A., Librero, M., and Toja, J. (2005). Daily and seasonal feeding rhythmicity of Palaemonetes varians (Leach, 1814) from the Southwestern Europe. Mar. Biol. 148, 141–147. Aguzzi, J., Bullock, N., and Tosini, G. (2006a). Spontaneous internal desynchronization of locomotor activity and body temperature rhythms from plasma melatonin rhythm in rats exposed to constant dim light. J. Circadian Rhythms 4, 6. Aguzzi, J., Chiesa, J. J., Caprioli, R., Cascione, D., Magnifico, G., Rimatori, V., and Costa, C. (2006b). Preliminary evidences of circadian fan activity rhythm in Sabella spallanzanii (Gmelin, 1791) (Polychaeta: Sabellidae). Sci. Mar. 70, 724–727. Aguzzi, J., Company, J. B., Abello´, P., and Garcı´a, J. A. (2006c). Rhythmic behaviour of the burying prawn Solenocera membranacea (Decapoda: Penaeoidea: Solenoceridae) in the western Mediterranean: a perspective through depth and season. Bull. Mar. Sci. 7, 353–364. Aguzzi, J., Company, J. B., Abello´, P., and Garcı´a, J. A. (2006d). Ontogenetic changes in the vertical migratory rhythms of benthopelagic shrimps Pasiphaea multidentata and P. sivado (Crustacea: Caridea). Mar. Ecol. Prog. Ser. 335, 167–174. Aguzzi, J., Company, J. B., Abello´, P., and Garcı´a, J. A. (2007a). Rhythmic diel movements of some pandalid shrimps (Decapoda: Caridea) in the western Mediterranean continental shelf and upper slope. J. Zool. 273, 340–349. Aguzzi, J., Ramirez-Llodra, E., Telesnicki, G., and Camps, M. (2007b). Day-night activity rhythm of the cold seep shrimp Alvinocaris stactophila (Caridea: Alvinocarididae) from the Gulf of Mexico. J. Mar. Biol. Assoc. UK 87, 1175–1180.

212

Jacopo Aguzzi and Joan B. Company

Aguzzi, J., Company, J. B., and Garcı´a, J. A. (2008a). The activity rhythm of the western Mediterranean prawn Processa canaliculata Leach, 1815 (Decapoda: Processidae) trough its day-night catchability patterns. Crustaceana 81, 1301–1316. Aguzzi, J., Sarria´, D., Garcı´a, J. A., Del Rio, J., Sarda`, F., and Manuel, A. (2008b). A new tracking system for the measurement of diel locomotor rhythms in the Norway lobster, Nephrops norvegicus (L.). J. Neurosci. Meth. 173, 215–224. Aguzzi, J., Bhamon, N., and Marotta, L. (2009a). Modulation of activity rhythms in continental margin decapods by light availability and predatory behaviour of Nephrops norvegicus. Mar. Ecol. 30, 366–375. Aguzzi, J., Company, J. B., and Garcı´a, J. A. (2009b). Ontogenetic and gender modulated behavioural rhythms in the deep-water decapods Liocarcinus depurator (Brachyura: Portunidae), Munida tenuimana and M. intermedia (Anomura: Galatheidae). Mar. Ecol. 30, 93–105. Aguzzi, J., Costa, C., Antonucci, F., Company, J. B., Menesatti, P., and Sarda`, F. (2009c). Influence of rhythmic behaviour in the morphology of Decapod Natantia. Biol. J. Linn. Soc. 96, 517–532. Aguzzi, J., Puig, P., and Company, J. B. (2009d). Hydrodynamic, non-photic modulation of biorhythms in the Norway lobster, Nephrops norvegicus (L.). Deep-Sea Res. Part I 56, 366–373. Aguzzi, J., Sanchez-Pardo, J., Garcı´a, J. A., and Sarda`, F. (2009e). Day-night and depth differences in haemolymph melatonin of the Norway lobster, Nephrops norvegicus (L.). Deep Sea Res. Part I 56, 1894–1905. Aguzzi, J., Company, J. B., Costa, C., Menesatti, P., Bahamon, N., and Sarda´, F. (2010). Activity rhythms in the deep-sea crustacen: chronobiological challenges and potenial technolgoical scenarios. Front. Biosci (In Press). Aksens, D. L., and Giske, J. (1993). A theoretical model for aquatic visual feeding. Ecol. Modell. 67, 233–250. Al-Adhub, A. H. Y., and Naylor, E. (1977). Daily variation in Dichelopandalus bonnieri (Caullery) as a component of the epibenthos. In “Biology of Benthic Organisms” (B. F. Keegan, P. O’ Ceidigh and P. J. S. Boaden, eds.), pp. 1–6. Pergamon Press, New York. Andersen, F. S. (1962). The Norway lobster in the Faroe waters. Medd Danese Fiskerie Havunders (Ny Ser.) 3, 265–326. Andersen, V., and Sardou, J. (1992). The diel migrations and the vertical distributions of zooplankton and micronekton in the Northwester Mediterranean Sea. 1. Euphausiids, mysids decapods and fishes. J. Plankton Res. 14, 1129–1154. Andersen, V., Devey, C., Gubanova, A., Picheral, M., Melnikov, V., Tsarin, S., and Prieur, L. (2004). Vertical distribution of zooplankton across the Almery-Oran frontal zone (Mediterranean Sea). J. Plankton Res. 26, 275–293. Antheunisse, L. J., and van Den Hoven, N. P. (1971). Diurnal activities and tidal migrations of the brackish water prawn Palaemonetes varians (Leach) (Decapoda: Caridea). Crustaceana 21, 203–217. Antonucci, F., Costa, C., Aguzzi, J., and Cataudella, S. (2009). Ecomorphology of morphofunctional relationships in the family of Sparidae: a quantitative statistic approach. J. Morphol. 270, 843–855. Atkinson, R. J. A., and Naylor, E. (1973). Activity rhythm in some burrowing decapods. Helgola¨nder wiss. Meeresunters 24, 192–201. Atkinson, R. J. A., Gramitto, M. E., and Froglia, C. (2003). Aspects of the biology of the burrowing shrimp Alpheus glaber (Olivi) (Decapoda: Caridea: Alpheidae) from the Central Adriatic. Ophelia 57, 27–42. Bahamon, N., and Cruzado, A. (2003). Modelling nitrogen fluxes in oligotrophic environments: NW Mediterranean and NE Atlantic. Ecol. Modell. 163, 223–244.

Biological Rhythms in Continental Margins

213

Bahamon, N., Aguzzi, J., and Sarda`, F. (2009). Fuzzy diel pattern in commercial catchability of deep water continental margin species. ICES J. Mar. Sci. 66, 2211–2218. Balzer, I., Espı´nola, I. R., and Fuentes-Pardo, B. (1997). Daily variations of immunoreactive melatonin in the visual system of crayfish. Biol. Cell 89, 539–543. Barbaresi, S., and Gherardi, F. (2001). Daily activity of the white-clawed crayfish, Austropotamobius pallipes (Lereboullet): a comparison between field and laboratory studies. J. Nat. Hist. 35, 1861–1871. Barlow, R. B. (1983). Circadian rhythms in the Limulus visual system. J. Neurosci. 3, 856–870. Barr, L. (1970). Diel vertical migration of Pandalus borealis in Kachemak Bay, Alaska. J. Fish. Res. Board Canada 27, 669–676. Bash, L. V., and Engle, J. M. (1989). In “Aspects of the Ecology and Behaviour of the Stomatopod Hemisquilla ensigera californinensis (Gonodactyloidea: Hemisquillidae): Biology of Stomatopods” (E. A. Ferrero, ed.), pp. 199–212. Mucchi, Modena. Bauer, R. T. (1985). Diel and seasonal variation in species composition and abundance of caridean shrimps (Crustacea, Decapoda) from seagrass meadows on the north coast of Puerto Rico. Bull. Mar. Sci. 36, 150–162. Bellwood, O. (2002). The occurrence, mechanics and significance of burying behaviour in crabs (Crustacea: Brachyura). J. Nat. Hist. 36, 1223–1238. Benoit-Bird, K. J., and Au, W. W. (2006). Extreme diel horizontal migrations by a tropical nearshore resident micronekton community. Mar. Ecol. Prog. Ser. 319, 1–14. Benoit-Bird, K. J., Zirbel, M. J., and McManu, M. A. (2008). Diel variation of zooplankton distributions in Hawaiian waters favours horizontal diel migration by midwater micronekton. Mar. Ecol. Prog. Ser. 367, 109–123. Benzid, D., De Jong, L., Lejeusne, C., Chevaldonne´, P., and Moreau, X. (2006). Serotonin expression in the optic lobes of cavernicolous crustaceans during the light–dark transition phase: Role of the lamina ganglionaris. J. Exp. Mar. Biol. Ecol. 335, 74–81. Berglund, A. (1980). Niche differentiation between two littoral prawns in Gullmar Fjord, Sweden: Palaemon adspersus and P.squilla. Ecography 3, 111–115. Bergstrand, A. O., Wik, A. D., and Hildre, O. (2003). Predator–prey relationships and food source of the Skagerrak deep-water fish assemblage. J. Northwest. Atl. Fish. Sci. 31, 165–180. Bider, R. J. (1962). Dynamics and then tempore-spatial relations of a vertebrate community. Ecology 43, 634–646. Bishop, J. M., and Khan, M. H. (1999). Use of intertidal and adjacent mudflats by juvenile penaeid shrimps during 24-h tidal cycles. J. Exp. Mar. Biol. Ecol. 232, 39–60. Bishop, J. M., Ye, Y., Alsaffa, A. H., Al-Foundari, A. H., and Al-Jazzaf, S. (2008). Diurnal and nocturnal catchability of Kuwait’s commercial shrimps. Fish. Res. 94, 58–72. Bojsen, B. H., Witthofft, H., Styrishave, B., and Andersen, O. (1998). In situ studies on heart rate and locomotor activity in the freshwater crayfish, Astacus astacus (L.) in relation to natural fluctuations in temperature and light intensity. Freshw. Biol. 39, 455–465. Bouchon, D. (1991a). Biological clock in seasonal reproductive cycle in the ditch shrimp Palaemonetes varians Leach. I. Photoperiodic time measurement. J. Exp. Mar. Biol. Ecol. 146, 1–12. Bouchon, D. (1991b). Biological clock in seasonal reproductive cycle in the ditch shrimp Palaemonetes varians Leach. II. Ovarian state-dependent response to non-diel light-dark cycles. J. Exp. Mar. Biol. Ecol. 146, 13–26. Carmona-Alcocer, V., Miranda-Anaya, M., and Barrera-Mera, B. (2005). Shfting phase of circadian locomotor activity by light in the freshwater crab Pseudothelphusa americana. Biol. Rhythm Res. 36, 123–129.

214

Jacopo Aguzzi and Joan B. Company

Carpentieri, P., Colloca, F., and Ardizzone, G. D. (2005). Day-night variations in the demersal nekton assemblage on the Mediterranean shelf-break. Estuar. Coast. Shelf Sci. 63, 577–588. Carroll, S. B. (2001). Chance and necessity: the evolution of morphological complexity and diversity. Nature 409, 1102–1109. Cartes, J. E. (1993a). Day-night feeding by decapods crustaceans in a deep-water bottom community in the Western Mediterranean. J. Mar. Biol. Assoc. UK 73, 795–811. Cartes, J. E. (1993b). Diets of deep-water pandalid shrimps on the western Mediterranean slope. Mar. Ecol. Prog. Ser. 96, 49–61. Cartes, J. E. (1995). Diets of, and trophic resources exploited by, bathyal penaeoidean shrimps from the western Mediterranean. Mar. Freshwater Res. 46, 889–996. Cartes, J. E. (1998). Dynamics of the bathyal Benthic Boundary Layer in the northwestern Mediterranean: depth and temporal variations in macrofaunal-megafaunal communities and their possible connections within deep-sea trophic webs. Prog. Oceanogr. 41, 111–139. Cartes, J. E., and Sarda`, F. (1993). Zonation of deep-sea decapod fauna in the Catalan Sea (Western Mediterranean). Mar. Ecol. Prog. Ser. 94, 27–34. Cartes, J. E., Sarda`, F., Company, J. B., and Llenorat, J. (1993). Day-night migrations by deep-sea decapod crustaceans in experimental samplings in the Western Mediterranean sea. J. Exp. Mar. Biol. Ecol. 171, 63–73. Cartes, J. E., Company, J. B., and Maynou, F. (1994a). Deep-water decapod crustaceans communities in the Northwester Mediterranean: influence of submarine canyons and season. Mar. Biol. 120, 221–229. Cartes, J. E., Sorbe, J. C., and Sarda`, F. (1994b). Spatial distribution of deep-sea decapods and euphausiids near the bottom in the Northwester Mediterranean. J. Exp. Mar. Biol. Ecol. 179, 131–144. Casterlin, M. E., and Reynolds, W. W. (1979). Diel activity in the spiny lobster Palinurus argus (Lartreille). Contrib. Mar. Sci. 22, 173–177. Castan˜on-Cervantes, O., Battelle, B. A., and Fanjul-Moles, M. L. (1999). Rhythmic changes in the serotonin content of the brain and eyestalk of crayfish during development. J. Exp. Biol. 202, 2823–2830. Chabot, C. C., Kent, J., and Watson, W. H. III (2004). Circatidal and circadian rhythms of locomotion in Limulus polyphemus. Biol. Bull. 207, 72–75. Chapman, C. J. (1980). Ecology of juvenile and adult Nephrops. In “The Biology and Management of Lobsters” (J. S. Cobb and B. F. Phillips, eds.), pp. 143–178. Academic Press, New York. Chapman, C. J., and Howard, F. G. (1979). Field observations on the emergence Rhythm of the Norway Lobster Nephrops norvegicus, using different methods. Mar. Biol. 51, 157–165. Chapman, C. J., Johnstone, A. D. F., and Rice, A. L. (1975). The behaviour and ecology of the Norway lobster, Nephrops norvegicus (L.). Proc. Eur. Mar. Biol. Symp. 9, 59–74. Chatterton, T. D., and Williams, B. G. (1994). Activity patterns of the New Zealand cancrid crab Cancer novaezelandiae (Jaquinot) in the field and laboratory. J. Exp. Mar. Biol. Ecol. 178, 261–274. Chiesa, J. J., Aguzzi, J., Garcı´a, J. A., Sarda`, F., and de la Iglesia, H. (2010). Light intensity determines temporal niche switching of behavioral activity in deep water Nephrops norvegicus (Crustacea: Decapoda). J. Biol. Rhythms. 25, 277–287. Childress, J. J. (1995). Do animals present biochemical adaptations to depths? Trends Ecol. Evol. 10, 30–36. Cobb, S. (1971). The shelter-related behaviour of the lobster, Homarus americanus. Ecology 52, 110–115. Cobb, S. (1977). View of the habitat behaviour of the clawed lobsters (Homarus and Nephrops). In “Workshop on Lobster and Rock Lobster Ecology and Physiology,” (CSIRO circular no. 7). Melbourne Australia.

Biological Rhythms in Continental Margins

215

Cohen, J. H., and Forward, R. B. (2002). Spectral sensitivity of vertically migrating marine copepods. Biol. Bull. 203, 307–314. Coll, M., Piroddi, C., Steenbeek, J., Kaschner, K., Ben Rais Lasram, F., Aguzzi, J., Ballesteros, E., Bianchi, C. N., Corbera, J., Dailianis, T., Danovaro, R., Dimitris, V. et al. (2010). Biodiversity of the Mediterranean Sea: status, patterns & threats. Plos-One 5, e11842. Colmenero, A., Aguzzi, J., Lombarte, A., and Bozzano, A. (2010). Sensory constraints in temporal segregation in two species of anglerfish (Lophius budegassa and L. piscatorius). Marine Ecology Progress Series. In Press. Company, J. B., and Sarda`, F. (1997). Reproductive patterns and population characteristics in five deep-water pandalid shrimps in the Western Mediterranean along a depth gradient (150–1100 m). Mar. Ecol. Prog. Ser. 148, 49–58. Company, J. B., and Sarda`, F. (1998). Metabolic rates and energy content of deep-sea benthic decapod crustaceans in the western Mediterranean Sea. Deep Sea Res. Part I 45, 1861–1880. Company, J. B., and Sarda`, F. (2000). Growth parameters of deep-water decapod crustaceans in the Northwester Mediterranean Sea: a comparative approach. Mar. Biol. 136, 79–90. Company, J. B., Cartes, J. E., and Sarda`, F. (2001). Biological patterns and near-bottom population characteristics of two pasiphaeid decapod crustacean species, Pasiphaea sivado and P. multidentata, in the north-western Mediterranean Sea. Mar. Biol. 139, 61–73. Company, J. B., Sarda`, F., Puig, P., Cartes, J. E., and Palanques, A. (2003). Duration and timing of reproduction in decapod crustaceans of the NW Mediterranean continental margin: is there a general pattern? Mar. Ecol. Prog. Ser. 261, 201–216. Company, J. B., Maiorano, P., Tselepides, A., Politou, C. H.-Y., Plaity, W., Rotllant, G., and Sarda`, F. (2004). Deep-sea decapod crustaceans in the western and central Mediterranean Sea: preliminary aspects of species distribution, biomass and population structure. Sci. Mar. 68, 73–86. Copley, J. T. P., and Young, C. M. (2006). Seasonality and zonation in the reproductive biology and population structure of the shrimp Alvinocaris stactophila (Caridea: Alvinocarididae) at a Louisiana slope cold seep. Mar. Ecol. Prog. Ser. 315, 199–209. Costa, C., and Cataudella, S. (2006). Relationship between shape and trophic ecology of selected species of Sparids of the Caprolace coastal lagoon (Central Tyrrhenian sea). Environ. Biol. Fish. 78, 165–175. Costa, C., Aguzzi, J., Chiesa, J. J., Magnifico, G., Cascione, D., and Caprioli, R. (2008). Evidences on the transient disruption of Sabella spallanzanii (Polychaeta: Sabellidae) endogenous fan activity rhythm as result of stress of capture and acclimation to laboratory. Ital. J. Zool. 75, 337–344. Couturier-Bhaud, Y. (1974). Cycle biologique de Lysmata seticaudata Risso (Crustace´, De´capode) I. Cycle biologique des animaux adultes. Vie et Milieu A 24, 413–422. Cronin, T. W. (1986). Photoreception in marine invertebrates. Am. Zool. 26, 403–415. De Robertis, A. (2002). Size-dependent visual predation risk and the timing of vertical migration: An optimized model. Limnol. Oceanogr. 47, 925–933. Despalatovic, M., Grubelic, I., and Simunovic, A. (2006). Distribution and abundance of the Atlantic mud shrimp, Solenocera membranacea (Risso, 1816) (Decapoda, Solenoceridae) in the Northern and Central Adriatic Sea. Crustaceana 79, 1025–1032. Dickson, R. R., Gould, W. J., Gurbutt, P. A., and Killworth, P. D. (1982). A seasonal signal in ocean currents at abyssal depths. Nature 295, 193–198. Domanski, P. (1986). The near-bottom shrimp faunas (Decapoda: Natantia) at two abyssal sites in the Northeast Atlantic Ocean. Mar. Biol. 93, 171–180. Donaldson, H. A. (1975). Vertical distribution and feeding of Sergestid shrimps (Decapoda: Natantia) collected near Bermuda. Mar. Biol. 31, 37–50.

216

Jacopo Aguzzi and Joan B. Company

Dowse, A., and Palmer, J. D. (1990). Evidence for ultradian rhythmicity in an intertidal crab. In “Chronobiology: Its Role in Clinical Medicine, General Biology, and Agriculture” (D. K. Hayes, J. P. Pauly and R. J. Reiter, eds.), pp. 691–697. B. Wiley-Liss, New York. Dunlap, J. C., Loros, J. J., and DeCursey, P. (2004). Chronobiology: Biological timekeeping. Sinauer Associates Incorporated Publishing, Sunderland, Massachusetts. Eckelbarger, K. J., and Walting, L. (1995). Role of phylogenetic constrains in determining the reproductive patterns in deep-sea invertebrates. Invertebr. Biol. 114, 256–269. Ennis, G. P. (1984). Territorial behaviour of the American lobster Homarus americanus. Trans. Am. Fish. Soc. 113, 330–335. Escamilla-Chimal, E. G., and Fanjul-Moles, M. L. (2008). Daily and circadian expression of cryptochrome during the ontogeny of crayfish. Comp. Biochem. Physiol. A 151, 461–470. Fanelli, E., and Cartes, J. E. (2004). Feeding habits of pandalid shrimps in the Alboran Sea (SW Mediterranean): influence of biological and environmental factors. Mar. Ecol. Prog. Ser. 280, 227–238. Fanjul-Moles, M. L., and Prieto-Sagredo, J. (2003). The circadian system of crayfish: a developmental approach. Microsc. Res. Tech. 60, 291–301. Fanjul-Moles, M. L., Miranda-Ayana, M., and Prieto-Sagredo, J. (1996). Circadian locomotor activity rhythm during ontogeny in crayfish Procambarus clarkii. Chronobiol. Int. 13, 15–26. Fanjul-Moles, M. L., Escamilla-Chimal, E. G., Gloria-Soria, A., and Hernandez-Herrera, G. (2004). The crayfish Procambarus clarkii CRY shows daily and circadian variation. J. Exp. Biol. 207, 1453–1460. Farina, A., and Belgrano, A. (2004). The eco-field: A new paradigm for landscape ecology. Ecol. Res. 19, 107–110. Farmer, A. S. D. (1974). Burrowing behaviour of the Norway lobster, Nephrops norvegicus (L.) (Decapoda: Nephropidae). Estuar. Coast. Mar. Sci. 2, 49–58. Fasham, M. J. R., and Foxton, P. (1979). Zonal distribution of pelagic Decapoda (Crustacea) in the eastern north Atlantic and its relation to the physical oceanography. J. Exp. Mar. Biol. Ecol. 37, 225–253. Fernande´z de Miguel, F., and Are´chiga, H. (1994). Circadian locomotor activity and its entrainment by food in the crayfish Procambarus clarkii. J. Exp. Biol. 190, 9–21. Fincham, A. A., and Furlong, J. A. (1984). Seasonal swimming rhythms of female palaemonid estuarine prawns and shrimps. J. Nat. Hist. 18, 425–439. Flexas, M. M., Durrieu de Madron, X., Garcia, M. A., Canals, M., and Arnau, P. (2002). Flow variability in the Gulf of Lions during the MATER HFF experiment (March–May 1997). J. Mar. Syst. 33–34, 197–214. Foxton, F. (1970a). The vertical distribution of pelagic decapods (Crustacea: Natantia) collected on the second cruise 1965. I. The Caridea. J. Mar. Biol. Assoc. UK 50, 939–960. Foxton, F. (1970b). The vertical distribution of pelagic decapods (Crustacea: Natantia) collected on the second cruise 1965. II. The Penaeidea and general discussion. J. Mar. Biol. Assoc. U.K. 50, 961–1000. Foxton, F., and Roe, H. S. J. (1974). Observations on the nocturnal feeding of some mesopelagic decapod crustacean. Mar. Biol. 28, 37–49. Frank, T. M., and Case, J. (1988). Visual spectral sensitivities of bioluminescent deep-sea crustaceans. Biol. Bull. 175, 261–273. Frank, T. M., and Widder, E. A. (1994). Evidence for behavioural sensitivity to near-UV light in the deep-sea crustacean Systellaspis debilis. Mar. Biol. 118, 279–284. Frank, T. M., and Widder, E. A. (1997). The correlation of downwelling irradiance and staged vertical migration patterns of zooplankton in Wilkinson basin, Gulf of Maine. J. Plankton Res. 19, 1975–1991.

Biological Rhythms in Continental Margins

217

Frank, T. M., and Widder, E. A. (2002). Effects of a decrease in downwelling irradiance on the daytime vertical distribution patterns of zooplankton and micronekton. Mar. Biol. 140, 1181–1193. Franqueville, C. (1971). Macroplancton profond (Inverte´bre´s) de la Me´diterrane´e nord occidentale. Te´thys 3, 11–56. Frederiksen, M., Edwards, M., Richardson, A. J., Halliday, N. C., and Wanless, S. (2006). From plankton to top predators: bottom-up control of a marine food web across four trophic levels. J. Anim. Ecol. 75, 1259–1268. Froglia, C. (1972). Osservazioni sulle variazioni di cattura dello scampo Nephrops norvegicus (L.) in riferimento all’etologia ed alla biologia della specie. Quaderni del Laboratorio de Tecnologia della Pesca. Ancona 1, 83–99. Froglia, C., and Gramitto, M. E. (1987). Notes on growth and biology of Solenocera membranacea (Risso, 1816) in the central Adriatic Sea (Decapoda: Solenoceridae). Investigacio´n Pesquera 51, 189–199. Fuentes-Pardo, B., Guzma´n Go´mez, A. M., Lara Aparicio, M., and Lo´pez de Medrano, S. (2003). A qualitative model of a motor circadian rhythm. BioSystems 71, 61–69. Futuyma, D. J., and Moreno, G. (1988). The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19, 207–233. Gage, J. D., and Tyler, P. A. (1992). Deep-sea biology. A natural history of organisms at the deep-sea floor. Cambridge University Press, Cambridge. Garret, C. (2003). Internal ties and ocean mixing. Science 301, 1858–1859. Giske, J., Aksens, D. L., Balin˜o, B., Kaartvedt, S., Lie, U., Nordeide, J. T., Gro Vea Salvanes, A., Wakili, S. M., and Aadnesen, A. (1990). Vertical distribution and trophic interactions of zooplankton and fish in Masfjorden, Norway. Sarsia 75, 65–81. Golet, W. J., Scopel, D. A., Cooper, A. B., and Watson, W. H. III (2006). Daily patterns of locomotor expressed by American lobsters (Homarus americanus) in their natural habitat. J. Crustacean Biol. 26, 610–620. Gue´guen, F. (2001). Niotes sur la biologie de la crevette de profondeur Aristeus antillensis en Guyane franc¸aise. Acade´mie de la Science, Paris (Sciences de la Vie) 324, 689–700. Guerao, G. (1995). Locomotor activity patterns and feeding habits in the prawn Palaemon xiphias (Crustacea: Decapoda: Palaemonidae) in Alfacs Bay, Ebro Delta (Northwest Mediterranean). Mar. Biol. 122, 115–119. Guerao, G., and Abello´, P. (1996). Patterns of activity in the sympatric prawns Palaemon adspersus and Processa edulis (Decapoda, Caridea) from a shallow Mediterranean bay. Sci. Mar. 60, 319–324. Guerao, G., and Ribera, C. (1996). Locomotor activity patterns and feeding habits in the prawn Palaemon serratus (Pennant, 1777) in the Alfacs Bay, Ebro Delta, Spain. Crustaceana 69, 101–112. Hagerman, L., and Ostrup, J. (1980). Seasonal and diel activity variations in the shrimp Palaemon adspersus from a brackish non-tidal area. Mar. Ecol. Prog. Ser. 2, 329–335. Hammond, R. D., and Naylor, E. (1977). Effects of dusk and down on locomotor activity rhythms in the Norway lobster Nephrops norvegicus. Mar. Biol. 39, 253–260. Hargreaves, P. M. (1999). The vertical distribution of micronektonic decapod and mysid crustaceans across the Goban. Spur of the Porcupine Seabight. Sarsia 84, 1–18. Heffernan, J. J., and Hopkins, T. L. (1981). Vertical distribution of the shrimp genera Gennadas and Bentheogennema (Decapoda: Penaeidae) in the eastern Gulf of Mexico. J. Crustacean Biol. 1, 461–473. Heier, L., Linder, E., and Nilsen, M. (1999). Population parameters of deep-water shrimp (Pandalus borealis) and fish community in Isford and Jan Mayen area. In “Marine Benthic Fauna of Svalbard (Cruise Report AB301A),”The Univ. Courses on Svalbard. Helfrich-Foster, C. (2000). Differential control of morning and evening components in the activity rhythm of Drosophila melanogaster-sex specific differences suggest a different quality of activity. J. Biol. Rhythms 15, 135–154.

218

Jacopo Aguzzi and Joan B. Company

Helfrich-Foster, C. (2001). The locomotor activity rhythm of Drosophila melanogaster is controlled by a dual oscillator system. J. Insect Physiol. 47, 877–887. Herna´ndez, O. H., and Fuentes-Pardo, B. (2003). Cerebroid Ganglion is the Presumptive Pacemaker of the Circadian Rhythm of Electrical Response to Light in the Crayfish. Biol. Rhythm Res. 32, 125–144. Herring, P. (2002). The Biology of the Deep Ocean. Oxford University Press, Oxford. Herring, P. J., and Roe, H. S. J. (1988). The photoecology of pelagic oceanic decapods. Symp. Zool. Soc. Lond. 59, 263–290. Hjellvik, V., Godo, O. R., and Tjostheim, D. (2002). Diurnal variation in bottom trawl survey catches: does it pay to adjust? Can. J. Fish. Aquat. Sci. 59, 33–48. Honculada-Primavera, J., and Lebata, J. (1995). Diel activity patterns in Metapenaeus and Penaeus juveniles. Hydrobiologia 295, 295–302. Hopkins, T. L., Flock, M. E., Gartner, J. V., and Torres, J. J. (1994). Structure and trophic ecology of a low latitude midwater decapod and mysid assemblage. Mar. Ecol. Prog. Ser. 109, 143–156. Huges, D. A. (1968). Factors controlling emergence of the pinks shrimp Penaeus duorarum, from the substrate. Biological Bulletin of Marine Biology Laboratory, Woods Hole 134, 48–59. Jagota, A., de la Iglesia, H. O., and Schwartz, W. J. (2000). Morning and evening circadian oscillations in the suprachiasmatic nucleus in vitro. Nat. Neurosci. 3, 372–376. Jerlov, N. G. (1968). Optical Oceanography. Elsevier, Amsterdam. Johnson, M. L., Shelton, P. M. J., and Gaten, E. (2000). Temporal resolution in the eyes of marine decapods from coastal and deep-sea habitats. Mar. Biol. 136, 243–248. Joshi, A. (2005). Behaviour genetic in the post-genomics era: From genes to behaviour and vice versa. Curr. Sci. 89, 1128–1135. Jumars, P. A. (2007). Habitat coupling by mid-latitude, sub tidal marine mysids: importsubsidised omnivores. Oceanogr. Mar. Biol. Adv. Rev. 45, 89–138. Jury, S. H., Chabot, C. C., and Watson, W. H. III (2005). Daily and circadian rhythms of locomotor activity in the American lobster, Homarus americanus. J. Exp. Mar. Biol. Ecol. 318, 61–70. Kaartvedt, S., Aksnes, D. L., and Aadnesen, A. (1988). Winter distribution of macroplankton and micronekton in Masfjorden, western Norway. Mar. Ecol. Prog. Ser. 45, 45–55. Karani, I., Kitsos, M. S., Chartosia, N., and Koukouras, A. (2005). Diet Composition of the Penaeid Shrimp, Melicertus kerathurus (Forska˚l, 1775) (Decapoda, Penaeidae) in the Aegean Sea. Crustaceana 78, 385–396. Karnofsky, E. B., Atema, E., and Randall, H. E. (1988). Field observations of social behaviour, shelter use, and foraging in the lobster, Homarus americanus. Biol. Bull. 176, 239–246. Kils, U. (1982). Swimming behaviour, swimming performance and energy balance of Antarctic krill, Euphausia superba. BIOMASS 3, 1–121. Komai, T., and Segonzac, M. (2005). A revision of the genus Alvinocaris Williams and Chace (Crustacea: Decapoda: Caridea: Alvinocarididae), with descriptions of a new genus and a new species of Alvinocaris. J. Nat. Hist. 39, 1111–1175. Koukouras, A., Doulgeraki, S., and Kitsos, M. S. (2000). Notes on the distribution of pelagic shrimps (Decapoda, Natantia) in the Aegean Sea. Crustaceana 78, 979–993. Kronfeld-Schor, N., and Dayan, T. (2003). Partitioning of time as an ecological resource. Annu. Rev. Ecol. Syst. 34, 153–181. Kruppasamy, P. K., Menon, N. G., Nair, C., and Achuthankutty, C. T. (2006). Distribution and abundance of pelagic shrimps from the deep scattering layer of the Eastern Arabian Sea. J. Shellfish Res. 25, 1013–1019. Kuipers, B. R., and Dapper, R. (1984). Nursery function of Wadden Sea tidal flats for the brown shrimp Crangon crangon. Mar. Ecol. Prog. Ser. 36, 55–64.

Biological Rhythms in Continental Margins

219

Lagarde`re, J. P. (1977). Recherches sur le re´gime alimentaire et le comportement pre´dateur des de´capodes benthiques de la pente continentale de l’Atlantique Nord Oriental (Golfe de Gascogne et Maroc). In “Biology of Benthic Organisms” (B. F. Keegan, P. O. Ceidigh and P. J. S. Boaden, eds.), pp. 397–408. Pergamon Press, Oxford. Lampitt, R. S., Merret, N. R., and Thurston, M. H. (1983). Interrelation of necrophagous amphipods, a fish predator and tidal currents in the deep-sea. Mar. Biol. 74, 73–78. Last, K. S., and Olive, P. J. W. (2004). Interaction Between photoperiod and an endogenous seasonal factor in influencing the diel locomotor activity of the benthic polychaete Nereis virens Sars. Biol. Bull. 206, 103–112. Last, K. S., Bailhache, T., Kramer, C., Kyriacou, C. P., Rosato, E., and Olive, P. J. W. (2009). Tidal, daily, and lunar-day activity cycles in the marine polychaete Nereis virens. Chronobiol. Int. 26, 167–183. Lawton, P. (1987). Diel activity and foraging behaviour of juvenile American lobster, Homarus americanus. Canadian J. Fish. Aquat. Sci. 44, 1195–1205. Levin, L. A., Etter, R. J., Rex, M., Gooday, A. J., Smith, C. R., Pineda, J., Stuart, C. T., Hessler, R. R., and Pawson, D. (2001). Environmental influences on regional deep-sea species diversity. Annu. Rev. Ecol. Syst. 35, 51–93. Liesler, B., and Winkler, H. (1985). Ecomorphology. (R. F. Johnston, ed.), Current ornithology. Vol. 2, pp. 155–186. Plenum Press, New York. Lighthill, M. J. (1969). Hydromechanics of aquatic animal propulsion. Annu. Rev. Fluid Mech. 1, 413–446. Lisin, S. E., Hannan, E. E., Kockevar, R. E., Harrold, C., and Barry, J. P. (1997). Temporal variation in gametogenic cycles of vesicomyd clams. Invertebr. Reprod. Dev. 31, 307–318. Longhurst, A. (2007). Ecological Geography of the Sea. Academic Press, Burlington. Macquart-Moulin, C., and Patriti, G. (1996). Accumulation of migratory micronekton crustaceans over the upper slope and submarine canyons of the northwestern Mediterranean. Deep Sea Res. Part I 43, 579–60149. Madurell, T., and Cartes, J. E. (2005). Temporal differences in feeding habits and daily rations of Hoplostheus mediterraneaus in the bathyal Ionian Sea (eastern Mediterranean). Mar. Biol. 146, 951–962. Margalef, R. (1986). Ecologı´a. Ediciones Omega, Barcelona. Marques, M. D., and Waterhouse, J. M. (2004). Rhythms and the ecology,-do chronobiologists still remember nature? Biol. Rhythms Res. 35, 1–2. Martı´n, J., Palanques, A., and Puig, P. (2007). Near-bottom horizontal transfer of particulate matter in the Palamo´s Submarine Canyon (NW Mediterranean). J. Mar. Res. 65, 193–218. Matthew, J. B. L., and Pinnoi, S. (1973). Ecological studies on the deep-water pelagic community of Korsfjorden, western Norway. The species of Pasiphaea and Sergestes (Crustacea: Decapoda) recorded in 1968 and 1969. Sarsia 52, 123–144. Mauchline, J., and Gordon, D. M. (1991). Oceanic pelagic prey of benthopelagic fish in the benthic boundary layer of marginal oceanic region. Mar. Ecol. Prog. Ser. 74, 109–115. Maynou, F., and Cartes, J. E. (1998). Daily ratio estimates and comparative study of food consumption in nine species of deep-water decapod crustaceans of the NW Mediterranean. Mar. Ecol. Prog. Ser. 171, 221–231. Maynou, F. X., Conan, G. Y., Cartes, J. E., Company, J. B., and Sarda`, F. (1996). Spatial structure and seasonality of decapods crustacean populations on the northwestern Mediterranean slope. Limonol. Oceanogr. 41, 113–125. Maynou, F. X., Sarda`, F., and Conan, G. Y. (1998). Assessment of the spatial structure and biomass evaluation of Nephrops norvegicus (L.) populations in the Northwester Mediterranean by geostatistic. ICES J. Mar. Sci. 55, 102–120. McGaw, I. J. (2005). Burying behaviour of two sympatric crab species: Cancer magister and Cancer productus. Sci. Mar. 69, 375–381.

220

Jacopo Aguzzi and Joan B. Company

McIntosh, A. R., and Towsend, C. R. (1994). Interpopulation variation in mayfly antipredator tactics: differential effects of contrasting predatory fish. Ecology 75, 2078–2090. Miranda-Anaya, M., Barrera-Mena, B., and Ramirez-Lomeli, E. (2003a). Circadian locomotor activity in the freshwater crab Pseudothelphusa americana (De Saussure, 1857): effect of Eyestalk Ablation. Biol. Rhythms Res. 34, 167–176. Miranda-Anaya, M., Ramı´rez-Lomelı´, E., Carmona-Alcocer, V. P., and Barrera-Mera, B. (2003b). Circadian Locomotor Activity under artificial light in the freshwater crab Pseudothelphusa americana. Biol. Rhythms Res. 34, 447–458. Moller, T. H., and Jones, D. A. (1975). Locomotor rhythms and burrowing habits of Penaeus semisulcatus (de Haan) and P. monodon (Fabricius) (Crustacea: Penaeidae). J. Exp. Mar. Biol. Ecol. 18, 61–77. Moody, K. E., and Steneck, R. (1993). Mechanisms of predation among large decapod crustaceans of the Gulf of Maine coast: functional vs. phylogenetic patterns. J. Exp. Mar. Biol. Ecol. 168, 111–124. Moragn, E. (2004). Ecological significance of biological clocks. Biol. Rhythms Res. 35, 3–12. Moreno-Amich, M. R. (1994). Feeding habits of the grey gurnard, Eutrigla gurnardus (L., 1758) along the Catalan coast (Northwestern Mediterranean). Hydrobiologia 273, 57–66. Morgan, G. R. (1978). Locomotor activity in the Western Rock Lobster Panulirus longipes cygnus. Aust. J. Mar. Freshw. Res. 29, 169–174. Morris, R. J. (1973). Changes in the lipidic composition of Acanthephyra purpurea Milne Edwards (Crustacea: Decapoda) during its diurnal migration: a preliminary investigation. J. Exp. Mar. Biol. Ecol. 13, 55–61. Motta, P. J., and Kotrschal, K. M. (1992). Correlative, experimental, and comparative experimental approaches in ecomorphology. Neth. J. Zool. 42, 400–415. Motta, P. J., Clifton, K. B., Hernandez, P., and Eggold, B. T. (1995a). Ecomorphological correlates in ten species of subtropical seagrass fishes: diet and microhabitat utilization. Environ. Biol. Fish. 44, 37–60. Motta, P. J., Norton, S. F., and Luczkovich, J. J. (1995b). Perspectives on the ecomorphology of bony fishes. Environ. Biol. Fish. 44, 11–20. Myslinski, T. J., Frank, T., and Widder, E. A. (2005). Correlation between photosensitivity and downwelling irradiance in mesopelagic crustaceans. Mar. Biol. 147, 619–629. Naylor, E. (1988). Rhythmic behaviour of Decapod Crustaceans. Symp. Zool. Soc. Lond. 59, 177–199. Naylor, E. (2005). Chronobiology: implications for marine resources exploitation and management. Sci. Mar. 69, 157–167. Naylor, E. (2006). Orientation and navigation in coastal and estuarine zooplankton. Mar. Freshw. Behav. Physiol. 39, 13–24. Nordtug, T., and Krekling, S. (1989). Steady-state and dynamic properties of photomechanical light and dark adaptation in the eye of the shrimp Eualus gaimardii (Crustacea, Natantia). J. Exp. Zool. 250, 117–127. Nussbeum, M. P., and Beenhakker, M. P. (2002). A small system approach to motor pattern generation. Nature 417, 343–350. Oishi, K., and Saigusa, M. (1997). Nighttime emergence patterns of planktonic and benthic crustaceans in a shallow subtidal environment. J. Oceanogr. 53, 611–621. Orsi Relini, L., Zamboni, A., Fiorentino, F., and Massi, D. (1998). Reproductive patterns in Norway lobster Nephrops norvegicus (Crustacea, Decapoda, Nephropidae) of different Mediterranean areas. Sci. Mar. 62, 25–41. Page, T. L., and Larimer, J. L. (1972). Entrainment of the circadian locomotor activity rhythm in crayfish. J. Comp. Physiol. 78, 97–107. Palanques, A., Garcia-Ladona, E., Gomis, D., Martı´n, J., Marcos, M., Pascual, A., Puig, P., Emelianov, M., Guille´n, J., Gili, J. M., Tintore´, J.Jordi, A. et al. (2005). General patterns

Biological Rhythms in Continental Margins

221

of circulation, sediment fluxes and ecology of the Palamo´s (La Fonera) submarine canyon, north-western Mediterranean. Prog. Oceanogr. 66, 89–119. Pallas, A., Garcia-Calvo, B., Corgos, A., Bernardez, C., and Freire, J. (2006). Distribution and habitat use patterns of benthic decapod crustaceans in shallow waters: a comparative approach. Mar. Ecol. Prog. Ser. 324, 173–184. Palmer, J. D. (2000). The clocks controlling the tide-associated rhythms of intertidal animals. BioEssays 22, 32–37. Palmer, J. D., and Williams, B. G. (1986a). Comparative studies of tidal rhythms. I. The characterisation of the activity rhythm of the pilan-pendulum crab, Helice crassa. Mar. Behav. Physiol. 12, 197–207. Palmer, J. D., and Williams, B. G. (1986b). Comparative studies of tidal rhythms. II. The dual clock control of the locomotor rhythm of two decapod crustaceans. Mar. Behav. Physiol. 12, 269–278. Park, O. (1941). Concerning the community symmetry. Ecology 22, 164–167. Patterson, K. R. (1984). Distribution patterns of some epifauna in the Irish Sea and their ecological interactions. Mar. Biol. 83, 103–108. Paultz, J. D., Kaneko, M., Hall, J. C., and Kay, S. A. (1997). Independent Photoreceptive Circadian Clocks Throughout Drosophila. Science 278, 1632–1635. Penn, J. W. (1984). The behaviour and catchability of some commercially exploited penaeids and their relationship to stock and recruitment. In “Penaeids-Shrimps—The Biology and Management” ( J. A. Gulland and B. J. Rothschild, eds.), pp. 173–186. Fishing New Books Limited, Farman, Surrey. Petrakis, G., MacLennan, D. D., and Newton, A. W. (2001). Day-night and depth effects on catch rates during trawl surveys in the North Sea. ICES J. Mar. Sci. 58, 50–60. Petrenko, A. A. (2003). Variability of circulation features in the Gulf of Lion NW Mediterranean Sea. Importance of inertial currents. Oceanol. Acta 26, 323–338. Pittman, S. J., and McAlpine, C. A. (2001). Movements of marine fish and decapods crustaceans: Process, theory and application. Adv. Mar. Biol., An Annu. Rev. 44, 206–295. Powers, M. K., and Barlow, R. B. (1985). Behavioral correlates of circadian rhythms in the Limulus visual system. Biol. Bull. 169, 578–591. Puig, P., Company, J. B., Sarda`, F., and Palanques, A. (2001). Responses of deep-water shrimp populations to intermediate nepheloid layer detachments on the Northwestern Mediterranean continental margin. Deep Sea Res. Part I 48, 2195–2207. Pulcini, D., Costa, C., Aguzzi, J., and Cataudella, S. (2008). Light and shape: a contribution to demonstrate morphological differences in diurnal and nocturnal teleosts. J. Morphol. 269, 375–385. Queiroz, De.A., and Wimberger, P. (1993). The usefulness of behaviour for phylogenetic estimation: levels of homoplasy in behavioural and morphological characters. Evolution 47, 46–60. Raffaelli, D., Bell, E., Weithoff, G., Matsumoto, A., Cruz-Motta, J. J., Kershaw, P., Parker, R., Parry, D., and Jones, M. (2003). The ups and downs of benthic ecology: considerations of scale, heterogeneity and surveillance for benthic-pelagic coupling. J. Exp. Mar. Biol. Ecol. 285–286, 191–203. Raso, G., Martin, M. J., Diaz, V., Cobos, V., and Manjon-Cabeza, M. E. (2006). Diel and seasonal changes in the structure of a Decapod (Crustacea: Decapoda) community of Cymodocea nodosa from the South eastern Spain (West Mediterranean Sea). Hydrobiologia 557, 59–68. Rebach, S. (1987). Entrainment of seasonal and non seasonal rhythms by the rock crab Cancer irroratus. J. Crustacean Biol. 7, 581–594.

222

Jacopo Aguzzi and Joan B. Company

Recasens, L., Lombarte, A., and Sanchez, P. (2006). Teleostean fish assemblages in an artificial reef and a natural rocky area in Catalonia (Nortwestern Mediterranean): An ecomorphological approach. Mar. Sci. 78, 71–82. Reebs, S. G. (2002). Plasticity of diel and circadian activity rhythms in fishes. Rev. Fish Biol. Fish. 12, 349–371. Refinetti, R. (2006). Circadian physiology. Francis and Taylor, New York. Reichle, D. E., Palmer, J. D., and Park, O. (1965). Persistent Rhythmic Locomotor Activity in the Cave Cricket, Hadenoecus subterraneus, and its Ecological Significance. Am. Midl. Nat. 74, 57–66. Reid, D. G., and Naylor, E. (1989). Are there separate circatidal and circadian clocks in the shore crab Carcinus maenas ? Mar. Ecol. Prog. Ser. 52, 1–6. Reid, D. G., and Naylor, E. (1994). Are there separate circatidal and circadian clocks in the shore crab Carcinus maenas? Mar. Ecol. Prog. Ser. 52, 1–6. Reynolds, W. W., and Casterlin, M. E. (1979). Diel activity of the pink shrimp Penaeus duorarum. Hydrobiologia 66, 223–226. Ringelberg, J. (2010). Diel vertical migration of zooplankton in lakes and oceans: causal explanations and adaptive significances. Springer, Holland. Ringelberg, J., and Van Gool, E. (2003). On the combined analysis of proximate and ultimate aspects in diel vertical migration (DVM) research. Hydrobiologia 491, 85–90. Rodriguez, G., and Naylor, E. (1972). Behavioural rhythms in littoral prawns. J. Mar. Biol. Assoc. UK 52, 81–95. Rodriguez-Sosa, L., Calderon-Rosete, G., and Flores, G. (2008). Circadian and Ultradian Rhythms in the Crayfish Caudal photoreceptor. Synapse 62, 634–652. Roe, H. S. J. (1974). Observations on the diurnal vertical migrations of an oceanic animal community. Mar. Biol. 28, 99–113. Roe, H. S. J. (1983). Vertical distributions of euphausiids and fish in relation to light intensity in the Northeastern Atlantic. Mar. Biol. 77, 287–298. Roe, H. S. J. (1984). The diel migrations and distributions within a mesopelagic community in the north east Atlantic. 2. Vertical migrations and feeding of mysids and decapod crustacea. Prog. Oceanogr. 13, 269–318. Roe, H. S. J., and Badcock, J. (1984). The diel migrations and distributions within a mesopelagic community in the north east Atlantic. 5. Vertical migrations and feeding of fish. Prog. Oceanogr. 13, 389–424. Ross, S. T. (1986). Resource petitioning in fish assemblages: a review of field studies. Copeia 2, 352–388. Ruiz-Tagle, N., Ferna´ndez, M., and Po¨rtner, H. O. (2002). Full time mothers: daily rhythms in brooding and non-brooding behaviours of brachyuran crabs. J. Exp. Mar. Biol. Ecol. 276, 31–47. Saigusa, M. (2001). Daily rhythms of emergence of small invertebrates inhabiting shallow subtidal zones: A comparative investigation at four locations in Japan. Ecol. Res. 16, 1–28. Saigusa, M., Oishi, K., Ikumoto, A., Iwasaki, H., and Terajima, M. (2000). Emergence patterns of small subtidal arthropods in relation to day/night, tidal and surface/bottom factors: Investigations in the Boreal Sea, Japan (Akkeshi, Hokkaido). J. Oceanogr. 56, 295–310. San Vicente, J., and Sorbe, C. C. (2001). Temporal changes in the structure of the suprabenthic community from Hendaya beach (southern Bay of Biscay): A comparison with northwestern Mediterranean beach community. Boletı´n del Instituto Espan˜ol de Investigacio´n Oceanogra´fica 17, 107–120. Sandeman, D. C., Sandeman, R. E., and de Couet, H. G. (1990). Extraretinal photoreceptors in the brain of the crayfish Cherax destructor. J. Neurobiol. 21, 619–629.

Biological Rhythms in Continental Margins

223

Sarda`, F., Cartes, J. E., and Company, J. B. (1994). Spatio-temporal variations in megabenthos abundance in three different habitats of the Catalan deep-sea (Western Mediterranean). Mar. Biol. 120, 211–219. Sarda`, F., Cartes, J. E., Company, J. B., and Antoni, A. (1998). A modified commercial trawl used to sample deep-sea megabenthos. Fish. Sci. 64, 492–493. Sarda`, F., Company, J. B., and Castello´n, A. (2003). Intraspecific aggregation structure of a shoal of Western Mediterranean (Catalan coast) deep-sea shrimp, Aristeus antennatus (Risso, 1816), during the reproductive period. J. Shellfish Res. 22, 569–579. Sarda`, F., Company, J. B., and Costa, C. (2005). A morphological approach for relating decapod crustacean cephalothorax shape with distribution in the water column. Mar. Biol. 147, 611–618. Sardou, J., and Andersen, V. (1993). Micronekton and macroplankton in the Ligurian Sea (Mediterranean Sea): Diel migrations and vertical distributions. Oceanol. Acta 16, 381–392. Saunders, D. S. (2002). Insect clocks. Elsevier, Amsterdam. Saunders, W. B., and Hastie, L. C. (1992). Remote camera and trapping survey of the deepwater shrimps Heterocarpus laevigatus and H. ensifer and the geryonid crab Chaceon granulatus in Palau. Mar. Fishery Res. 54, 15–25. Schaffmeister, B. E., Hiddink, J. G., and Wolff, W. J. (2006). Habitat use of shrimps in the intertidal and shallow subtidal seagrass beds of the tropical Banc d’Arguin, Mauritania. J. Sea Res. 55, 230–243. Schoener, T. W. (1974). Resource partitioning in ecological communities. Science 185, 27–39. Shelton, P. M. J., Gaten, E., and Chapman, C. J. (1985). Light and retinal damage in Nephrops norvegicus (L.) (crustacea). Proc. R. Soc. Lond. B 226, 217–236. Simmons, H. L. (2008). Spectral modification and geographic redistribution of the semidiurnal internal tide, Ocean Modelling. Ocean Model. 21, 126–138. Smith, K. L., and Laver, M. B. (1981). Respiration of the bathypelagic fish Cyclothone acclinidens. Mar. Biol. 61, 261–266. Smith, I. P., Collins, K. J., and Jensen, A. C. (1999). Seasonal changes in the level and diel pattern of activity in the European lobster Homarus gammarus. Mar. Ecol. Prog. Ser. 186, 255–264. Stanewsky, R., Kaneko, M., Emery, P., Beretta, B., Wager-Smith, K., Kay, M., Rosbash, S. A., and Hall, J. C. (1998). The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95, 681–692. Swain, R., Marker, P. F., Alastair, M., and Richardson, M. (1988). Comparison of the gill morphology and branchial chambers in two fresh-water crayfishes from Tasmania: Astacopsis franklinii and Parastacoides tasmanicus. J. Crustacean Biol. 8, 355–363. Thurman, C. L. (1998). Locomotor rhythms in the fiddler crab Uca subcylindrica. Biol. Rhythm Res. 29, 179–196. Thurman, C. L. (2004a). Unraveling the ecological significance of endogenous rhythms in intertidal crabs. Biol. Rhythm Res. 35, 43–67. Thurman, C. L. (2004b). Locomotor activity of the fiddler crab Uca subcylindrica (Stimpson), under artificial illumination. Biol. Rhythm Res. 32, 85–99. Thurman, C. L., and Broghammer, A. (2001). Locomotor activity of the fiddler crab Uca subcyclindrica under artificial illumination. Biol Rhythm. Res. 32, 85–99. Tobar, R., and Sarda`, F. (1992). Annual and diel light intensity cycle as a predictive factor in deep-water fisheries for the prawn Aristeus antennatus Risso, 1816. Fish. Res. 15, 169–179. Tosini, G., and Aguzzi, J. (2005). Effects of space flight on circadian rhythms. (G. Sonnenfeld, ed.), Experimentation with the Animal Model in Space. Vol. 10, pp. 165–174. Elsevier, Amsterdam.

224

Jacopo Aguzzi and Joan B. Company

Trajano, L., and Menna-Barreto, E. (1995). Locomotor activity pattern of Brazilian cave catfishes under constant darkness (Siluriformes, Pimelodidae). Biol Rhythm Res 26, 341–353. Trenkel, V. M., Le Loch, F., and Rochet, M. J. (2007). Small scale spatial and temporal interactions among benthic crustaceans and one fish species in the Bay of Biscay. Mar. Biol. 151, 2207–2215. Tyler, P. A., Campos-Creasy, L. S., and Giles, L. A. (1994). Environmental control of quasicontinuous and seasonal reproduction in deep-sea benthic invertebrates. In “Reproduction, Larval Biology and Recruitment of the Deep-Sea Benthos” (C. M. Young and K. J. Eckelbarger, eds.), pp. 158–178. Columbia University Press, New York. Tyler, P. A., Young, C. M., Dolan, E., Arellano, S. M., Brooke, S. D., and Baker, M. C. (2007). Gametogenic periodicity in the chemosynthetic cold mussel Bathymodiolus childressi. Mar. Biol. 150, 829–840. Vallet, C., and Dauvin, J. C. (2001). Biomass changes and bentho-pelagic transfer throughout the benthic boundary layer in the English Channel. J. Plankton Res. 23, 903–922. Vallet, C., and Dauvin, J. C. (2006). The near-bottom layer as an ecological boundary in marine ecosystems: diversity, taxonomic composition and community definitions. Hydrobiologia 555, 49–58. van Haren, H., and Millot, C. (2004). Rectilinear and circular inertial motions in the Western Mediterranean Sea. Deep Sea Res. Part I 51, 441–1455. Vereschaka, A. L. (1995). Macroplankton in the near bottom layer of continental slope and seamounts. Deep Sea Res. Part I 42, 1639–1668. Wadley, V. (1992). The biology of scampi, prawns, carids, bugs and crabs exploited by deepwater trawling. In “The Fisheries Biology of Deepwater Crustacea and Finfish on the Continental Slope of Western Australia” (S. F. Rainer, ed.), pp. 95–122Final Report FRDC. Wagner, H. J., Kemp, K., Mattheus, U., and Priede, I. G. (2007). Rhythms at the bottom of the deep-sea: Cyclic current flow changes and melatonin patterns in two species o demersal fish. Deep Sea Res. Part I 54, 1944–1956. Wan-Soo, K., Hyung-Tack, H., Jong-Geel, J., and Kyung-Nam, H. (2003). Evidence of two-clock control of endogenous rhythm in the Washington clam, Saxidomus purpuratus. Mar. Biol. 142, 305–309. Ward, T. J., and Davis, T. L. O. (1987). Diel periodicity of Metanephrops australiensis and other deep-water crustaceans of the Northwest Australia. Fish. Res. 5, 91–97. Wassemberg, T. J., and Hill, B. J. (1994). Laboratory study of the effect of light on the emergence behaviour of eight species of commercially important adult penaeid prawns. Aust. J. Mar. Freshw. Res. 45, 43–50. Waterman, T. (2001). Evolutionary challenges of extreme environments (Part 1). J. Exp. Zool. 291, 130–168. Weiss, H. M., Lozano-Alvarez, E., and Briones-Fourzan, E. (2007). Circadian shelter occupancy patterns and predatory-prey interactions of juvenile Caribbean spiny lobsters in a reef lagoon. Mar. Biol. 153, 953–963. Weissemburg, M. J., and Zimmer-Faust, R. K. (1993). Life and death in moving fluids: hydrodynamic effects on chemosensory-mediated predation. Ecology 74, 1428–1443. Westin, L., and Aneer, G. (1987). Locomotor activity patterns of nineteen fish and five crustaceans species from the Baltic Sea. Environ. Biol. Fish. 20, 49–65. Westin, L., and Gydemo, R. (1988). The locomotor activity patterns of juvenile crayfish (Astacus astacus) and effect of shelter availability. Aquaculture 68, 361–367. Wheeler, M. J., Hamblen-Coyle, M. J., Dushay, M. S., and Hall, J. C. (1993). Behaviour in light-dark cycles of Drosophila mutants that are arrhythmic, blind, or both. Biol Rhythm Res 8, 67–94. Wilcockson, D., and Zhang, L. (2008). Circatidal clocks. Curr. Biol. 18, 753–755.

Biological Rhythms in Continental Margins

225

William, C., and Mobberly, J. R. (1964). The effect of constant conditions of light and darkness on the diurnal rhythm of the distal retinal pigment of the crayfish Faxonella clipea. Ohio J. Sci. 64, 185–194. Williams, J. A. (1980a). The light-response rhythm and seasonal entrainment of the endogenous circadian locomotor rhythm of Talitrus saltator (Crustacea: Amphipoda). J. Mar. Biol. Assoc. U.K. 60, 773–785. Williams, J. A. (1980b). The effect of dusk and down on the locomotor activity rhythm of Talitrus saltator (Montagu) (Crustacea: Amphipoda). J. Exp. Mar. Biol. Ecol. 42, 285–297. Wilson, R. R., and Smith, K. L. (1984). Effect of near-bottom currents on the detection of bait by the abyssal grenadier fishes Coryphaenoides spp., recorded by in situ with a video camera free-vehicle. Mar. Biol. 84, 83–91. Yamaguchi, A., Tsutomu, I., Watanabe, Y., and Ishizaka, J. (2004). Vertical distribution patterns of pelagic copepods as viewed from the predation pressure hypothesis. Zool. Stud. 43, 475–485. Young, C. M. (2003). Reproduction, development and life-history traits. In “Ecosystems of the Deep Oceans” (P. A. Tyler, ed.), pp. 381–426. Elsevier, Amsterdam. Zaret, T. M., and Suffern, J. S. (1976). Vertical migration in zooplankton as a predator avoidance mechanism. Limnol. Oceanogr. 21, 804–813. Zieman, D. A. (1975). Pattern of vertical distribution, vertical migration, and reproduction in the Hawaiian mesopelagic shrimp of the family Oplophoridae Ph.D. Thesis, Univ. Hawaii, Honolulu.

C H A P T E R

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The Patagonian Toothfish: Biology, Ecology and Fishery Martin A. Collins,*,‡ Paul Brickle,†,‡ Judith Brown,*,†,‡ and Mark Belchier§

Contents 229 230 232 232 233 234 236 236 238 240 241 241 241 241 242 242 244 245 247 247 247 248 249 250 251

1. Introduction 2. Taxonomy and Systematics 3. Distribution and Life Cycle 3.1. Determining distribution and abundance 3.2. Geographic distribution 3.3. Life cycle and bathymetric distribution 3.4. Recruitment variability 4. Population Structure, Movements and Migration Patterns 4.1. Population structure 4.2. Tagging studies and small-scale movements 5. Age and Growth 5.1. Estimating age and growth 5.2. Length-frequency data 5.3. Direct ageing methods 5.4. Otolith preparation methods 5.5. Validation 5.6. Age and growth from otoliths 5.7. Growth estimates from tagging 5.8. Larval and juvenile growth 6. Reproduction 6.1. Size at maturity 6.2. Fecundity 6.3. Timing of spawning 6.4. Eggs and larvae 7. Trophic ecology

* Government of South Georgia and the South Sandwich Islands, Government House, Stanley, Falkland Islands, FIQQ 1ZZ Fisheries Department, Directorate of Natural Resources, FIPASS, Falkland Islands, FIQQ 1ZZ { School of Biological Sciences (Zoology), University of Aberdeen, Tillydrone Avenue, Aberdeen, Scotland, AB24 2TZ, UK } British Antarctic Survey, NERC, High Cross, Madingley Road, Cambridge, CB3 0ET, UK {

Advances in Marine Biology, Volume 58 ISSN 0065-2881, DOI: 10.1016/S0065-2881(10)58004-0

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2010 Elsevier Ltd. All rights reserved.

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7.1. Toothfish diet 7.2. Feeding rates 7.3. Foraging behaviour 7.4. Predators of toothfish 7.5. Accumulation of mercury in toothfish tissue 8. Parasites 8.1. Parasite fauna and host specificity 8.2. Geographical differences in parasite fauna 8.3. Ontogenetic changes in parasite fauna 9. Physiology 9.1. Buoyancy 9.2. Antifreeze glycopeptides 9.3. Vision 10. Behaviour 10.1. Methods of studying behaviour 10.2. Baited camera systems 10.3. General behaviour patterns 10.4. Swimming form and speeds 11. Fishery 11.1. History of the fishery 11.2. Fishing methods and gears 11.3. Illegal, unreported and unregulated (IUU) fishing 11.4. By-catch issues 11.5. Interactions with seabirds 11.6. Interactions with marine mammals 12. Stock Assessment 13. Concluding Remarks Acknowledgements References

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Abstract Patagonian toothfish (Dissostichus eleginoides) is a large notothenioid fish that supports valuable fisheries throughout the Southern Ocean. D. eleginoides are found on the southern shelves and slopes of South America and around the subAntarctic islands of the Southern Ocean. Patagonian toothfish are a long-lived species (> 50 years), which initially grow rapidly on the shallow shelf areas, before undertaking an ontogenetic migration into deeper water. Although they are active predators and scavengers, there is no evidence of large-scale geographic migrations, and studies using genetics, biochemistry, parasite fauna and tagging indicate a high degree of isolation between populations in the Indian Ocean, South Georgia and the Patagonian Shelf. Patagonian toothfish spawn in deep water (ca. 1000 m) during the austral winter, producing pelagic eggs and larvae. Larvae switch to a demersal habitat at around 100 mm (1-year-old) and inhabit relatively shallow water (<300 m) until 6–7 years of age, when they begin a gradual migration into deeper water. As juveniles in shallow water, toothfish are

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primarily piscivorous, consuming the most abundant suitably sized local prey. With increasing size and habitat depth, the diet diversifies and includes more scavenging. Toothfish have weakly mineralised skeletons and a high fat content in muscle, which helps neutral buoyancy, but limits swimming capacity. Toothfish generally swim with labriform motion, but are capable of more rapid sub-carangiform swimming when startled. Toothfish were first caught as a by-catch (as juveniles) in shallow trawl fisheries, but following the development of deep water longlining, fisheries rapidly developed throughout the Southern Ocean. The initial rapid expansion of the fishery, which led to a peak of over 40,000 tonnes in reported landings in 1995, was accompanied by problems of bird by-catch and overexploitation as a consequence of illegal, unreported and unregulated fishing (IUU). These problems have now largely been addressed, but continued vigilance is required to ensure that the species is sustainably exploited and the ecosystem effects of the fisheries are minimised.

1. Introduction Toothfish, named for the sharp teeth on their upper jaw, belong to the genus Dissostichus in the Family Nototheniidae (Antarctic cods) that are endemic to the southern hemisphere and dominate Antarctic fish assemblages (Gon and Heemstra, 1990; Kock, 1992). There are two species of toothfish; the Antarctic toothfish (Dissostichus mawsoni), which is found at high latitudes around Antarctica, and the Patagonian toothfish (D. eleginoides; Fig. 4.1), which occurs further north around sub-Antarctic islands

Figure 4.1 Photograph of a Patagonian toothfish (Dissostichus eleginoides) taken with a baited camera at 1000 m depth on the Patagonian Shelf.

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such as South Georgia and around the southern tip of South America. There is, however, some overlap in their distribution in intermediate areas. Both species grow to large size, reaching lengths in excess of 2.3 m and weights greater than 200 kg, and are the target of valuable commercial fisheries. Patagonian toothfish were first described in 1898 (Smitt, 1898), but interest in the species was limited until toothfish were caught as a by-catch in trawl fisheries off the South American coasts. The large size of Patagonian toothfish, coupled with high quality flesh, led to the development, in the mid 1980s, of a valuable longline fishery, targeting large adult Patagonian toothfish in deep water (>500 m; Agnew, 2004). As with many new fisheries, the fishery developed ahead of the essential knowledge of the biology and ecology of the target species that is necessary to facilitate good management practices. Initially, the longline fishery caused extremely high incidental mortality to seabirds and while this problem has been largely overcome, there are still concerns about the sustainability of the various fisheries. In some areas, illegal, unreported or unregulated (IUU) fishing remains a major problem. Here, we synthesise existing data on the biology, ecology and fishery for Patagonian toothfish, highlighting areas where the knowledge is lacking. We also review the management of stocks of this valuable species in different parts of its range. We have, where possible, attempted to avoid grey literature. However there is much valuable information in working group papers from the Commission for the Conservation of Antarctic Marine Living Resources (CCAMLR). CCAMLR manges marine living resources south of the Antarctic Polar Front (APF) and, where necessary, we have cited this work.

2. Taxonomy and Systematics Order: Perciformes Sub-order: Notothenioidei Family: Nototheniidae Genus: Dissostichus Norman, 1937 Species: Dissostichus eleginoides Smitt, 1898 The Notothenioidei are a suborder of the Perciformes that dominate the waters of the Southern Ocean. They are an acanthomorph clade of teleost fish that contain over 120 species (Eastman and Eakin, 2000; Eastman and McCune, 2000). Within this, the Family Nototheniidae is considered to be the most speciose and initially included the Eleginopinae, the Nototheniinae, the Trematominae and the Pleuragramminae (DeWitt et al., 1990).On the basis of morphological and molecular data, the genus Eleginops was removed from the family (Balushkin, 2000; Bargelloni et al., 1998, 2000; Near and Cheng, 2008; Near et al., 2004; Sanchez et al., 2007). Eleginops appears as the sister group to all of the nonbovichthid notothenioids, and

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this is consistent with the fact that Eleginops is a sub-Antarctic, basal notothenioid lacking antifreeze proteins. The nototheniids, without Eleginops, are thus divided into three subfamilies based on De Witt et al. (1990) and Balushkin (2000). These are the Nototheniinae (Notothenia, Paranotothenia, Gobionotothen, Lepidonotothen and Patagonotothen), the Trematominae (Trematomus and Pagothenia) and the Pleuragramminae (De Witt et al., 1990) or Pleuragrammatinae (Balushkin, 2000) (Dissostichus, Pleuragramma, Aethotaxis and Gvodarus). Using molecular data (sequences of MLL, rhodopsin, cytochrome b and mitochondrial d-loop genes) Sanchez et al. (2007) confirmed Balushkin’s Pleurammatinae and postulated that neutral buoyancy was gained from common ancestry as all of the species in this subfamily have this feature. However they pointed out that the anatomical features of neutral buoyancy are not the same in Dissostichus, Pleuragramma and Aethotaxis suggesting parallelisms in neutral buoyancy. Near and Cheng (2008) examined the phylogenetics of notothenioid fishes using both nuclear and mitochondrial gene sequences and found the clade containing neutrally buoyant notothenioids present in their mitochondrial dataset but not well resolved in their nuclear data. They found that, despite common notothenioid clades in both the nuclear and mitochondrial gene phylogenies, large differences exist in the phylogenies inferred from each of their two datasets with regard to the presence of particular clades and the overall phylogenetic resolution. They concluded that the absence of a monophyletic Nototheniidae and the neutrally buoyant clade in their nuclear gene tree was a result of a lack of phylogenetic resolution and not strong support of the paraphyly of these two groups. The genus Dissostichus includes two species: the Antarctic toothfish D. mawsoni and the Patagonian toothfish D. eleginoides. D. eleginoides was described by Fredrick Adam Smitt in 1898. Smitt (1898) failed to designate a holotype, but two syntypes were deposited at the Swedish Museum of Natural History (Naturhistoriska riksmuseet) (NRM 3235 (1), 3236 (1)). These specimens came from Puerto Torro (55 240 S, 068 170 W) on 11th December 1895 and from Lagotoaia on 10th February 1896. The etymology of Dissostichus comes from the Greek disso, meaning double and stichus, meaning row or line referring to its two lateral lines, whilst eleginoides refers to its morphological affinities to the genus Eleginops. Subsequently, Gill and Townsend (1901) reported the capture of a fish of nearly five feet in length from 1900 m by the RV Albatross in 1888 in the SE Pacific Ocean. Although the specimen was thrown overboard, a photograph was taken of it. The specimen was caught at dredge station 2788, off the Chonos Archipelago, Southern Chile (45 350 S, 075 550 W). The authors described it from the photograph as Macrias amissus, with the generic name a reference to its length and bulk, and the specific name reflecting the

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geographic distance from its relatives as well as the loss of the type. When DeWitt saw the photograph, he was reminded of the illustrations of D. eleginoides published by F. A. Smitt in 1888, and after some comparison of the two, concluded that Macrias amissus was congeneric with Smitt’s species. De Witt (1962) considered that it should be considered a distinct species, D. amissus (Gill and Townsend, 1901), differing from D. eleginoides and D. mawsoni in several ways. De Witt (1962) stated that D. eleginoides differed from D. amissus in having a longer lower lateral line, a longer head and snout, a larger eye and longer pectoral fin. Whereas D. mawsoni (Norman, 1937) differed from D. amissus in having a shorter lower lateral line, a larger eye, a longer pectoral fin and smaller, more numerous scales. Using morphometric analyses, Oyarzun and Campos (1987) concluded that D. amissus is a junior synonym of D. eleginoides by Rule of Priority. They concluded that the characters used to distinguish between the species such as eye size, relative head length and the relative lengths of the lateral lines showed great variability and could not be used to separate the two. D. eleginoides differs from D. mawsoni by having several elongate scaleless areas on the dorsal side of its head and by having a longer lower lateral line (Gon and Heemstra, 1990).

3. Distribution and Life Cycle 3.1. Determining distribution and abundance A range of methods have been used to sample toothfish and determine distribution patterns. Initially, toothfish were caught as a by-catch in trawl fisheries (on the Patagonian shelf and around South Georgia) but, following the development of the longline fishery in Chile, longlining became the main fishing method especially in deeper water. Pots have also been trialled with varying success (Agnew et al., 2001). Baited cameras have been used to examine distribution and to try to determine density (Collins et al., 1999, 2006; Yau et al., 2002). Given the broad bathymetric range of toothfish, determination of abundance has proved problematic. Trawl surveys have been undertaken to depths of around 1000 m (e.g. Coggan et al., 1996), but fishing deeper requires large amounts of trawl warp, is time consuming and in many areas the ground is too rough for trawl gear. Baited cameras were initially trialled on the South Georgia and Falkland Islands slopes (Collins et al., 1999; Yau et al., 1997, 2002), as a means to estimate abundance. With the baited camera systems, either the first arrival time of fish at the bait or the total number attracted from the estimated area of odour plume can be used to estimate abundance (Priede and Merrett, 1996). However, the initial results indicated that toothfish may be deterred from attending the bait by the

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bright flashes of the camera every 60 s. A follow-up study, which used a video camera with low-illumination levels, had slightly better results (Collins et al., 2006), but toothfish attended the bait only briefly, and with the camera alternating on and off, toothfish may have been missed, so a reliable estimate of abundance was not possible. An alternative method to assess adult population size is a mark and recapture method, using external tags (see Section 4.2). Toothfish are extremely resilient and post-tagging survivorship is reported as high from both longlines and short-duration trawls (Agnew et al., 2006a; Williams et al., 2002). Tuck et al. (2003) used a modified (daily) Peterson mark and recapture method to assess the population size of toothfish at Macquarie Island. A length-dependent selectivity model was applied to take account of the movement of tagged fish to deeper water, which was unavailable to the trawl fishery. Mark and recapture methods have subsequently been used to determine adult population size in other areas such as South Georgia and the Ross Sea (Agnew et al., 2006b).

3.2. Geographic distribution Toothfish have a circum-sub-Antarctic distribution, being found on the southern Patagonian and Chilean shelves, and around sub-Antarctic islands (e.g. South Georgia and Shag Rocks, Crozet, Kerguelen, Heard, McDonald, Macquarie and Prince Edward islands), banks (e.g. Banzare Bank) and seamounts (e.g. Ob and Lena Seamounts) between latitudes 45 S and 62 S (Fig. 4.2) in the Southern Ocean (De Witt et al., 1990). The distribution spans the Antarctic Polar Front (APF) and extends north to 35 S on the Patagonian Shelf in the Atlantic Ocean, to 30 S off Chile in the Pacific and to 40 S in the SW Indian Ocean (Abellan, 2005). In the Scotia Sea, the distribution extends from the Scotia Ridge (west of Shag Rocks) to South Georgia and the northern South Sandwich Islands, with the most southerly record in the Scotia Sea being from 61 S at King George Island in the South Orkneys (Arana and Vega, 1999). In the Ross Sea, Patagonian toothfish are common in the northern areas and have been recorded as far south as 75 300 S (Hanchet et al., 2004), with a catch of 14 large individuals taken on a longline from 1000 m at 71 400 S (Stevenson et al., 2008), which was attributed to unusual hydrographic conditions. There remain many places in the Southern Ocean that have not been sampled, so the known distribution may be extended. A single specimen of toothfish was reported from the northern hemisphere (Moller et al., 2003), which was suggested as evidence of longdistance migration. This record must be considered dubious, as the fish would have migrated at least 10,000 km, travelling at depths below the tropical waters.

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Figure 4.2 Polar projection of the southern hemisphere showing the known distribution of Patagonian toothfish (Dissostichus eleginoides). Polar Front indicated by the red dotted line.

Water temperature may be a key factor in limiting distribution. Unlike D. mawsoni, D. eleginoides lacks antifreeze and has at least a few glomeruli in its kidneys (Eastman, 1990), which led to the suggestion that toothfish were unlikely to occur in water cooler than 2 C (Eastman, 1990). Collins et al. (2006) photographed Patagonian toothfish at depth in temperatures as low as 1.4 C, but did not encounter toothfish when the temperature was less than this.

3.3. Life cycle and bathymetric distribution Toothfish occupy a broad bathymetric range during their life cycle (Fig. 4.3). They are known to spawn in deep water during winter ( June– September) (Agnew et al., 1999; Evseenko et al., 1995; Laptikhovsky et al., 2006) (see Section 6). Data on the distribution of eggs and larvae are scarce, but eggs (4.3–4.7 mm) have been found in the upper 500 m over deep water (Evseenko et al., 1995) and are thought to hatch (at around 15 mm standard length (SL)) in October–December (Effremenko, 1979; Evseenko et al., 1995; Kellermann, 1989; North, 2002; North and White, 1982). Larvae have been caught from around South Georgia (Efremenko, 1984; Evseenko et al., 1995; North, 2002), Shag Rocks and Burdwood Bank (North, 2002). The majority of larvae have been reported from an area to the NW of South Georgia (North, 2002), but this is a heavily sampled

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Larvae remain in upper water layers

0M Juveniles become benthopelagic

Depth m

500 M

Large yolky pelagic eggs Juveniles migrate into deeper water as they grow

−3 month till hatch

1000 M Adults live in deep water 1000– 2000 m where they feed, moving only slightly shallower during the spawning season in July/August to 800–1000 m

1500 M

Figure 4.3 Schematic illustration of the life cycle of Patagonian toothfish (Dissostichus eleginoides).

location. Of the 43 larvae (18–63 mm SL) reported by North (2002), 40 were captured in the upper 250 m, 23 of which were in the upper 3 m at night. When the pelagic larvae reach a threshold size, they become benthopelagic and are first caught in research bottom trawls in January at Shag Rocks at around 150 mm total length (TL) (age 1þ) (Belchier and Collins, 2008), but smaller fish (80–93 mm TL) have been caught on the bottom near Crozet Islands during February (Duhamel, 1987). The otoliths of the latter fish had no visible growth increment and were thought to be 7–8 months old. The juvenile phase is typically spent in shallow waters and the recruitment of these juveniles may be concentrated over a limited spatial area. For instance, recruitment to the South Georgia population occurs primarily on the Shag Rocks shelf, to the NW of South Georgia (Collins et al., 2007). Juveniles typically remain in shallow water for the next 4–5 years. On the Patagonian Shelf, the Isla de los Estados is the main area of recruitment (Woehler, unpublished), although small numbers of recruits occur across the southern Patagonian Shelf. At a size of 500–700 mm TL, the juvenile toothfish disperse and gradually migrate down the slope, which may be associated with changes in both growth rate and diet. In general, adult toothfish occupy deep water (>500 m), although large fish have been caught in shallow water, close inshore, at South Georgia (Collins et al., 2007). Toothfish thus show the distinct biggerdeeper trend (Coggan et al., 1996; Collins et al., 2007; Laptikhovsky et al., 2006; Lord et al., 2006; Fig. 4.3) that is common in many deep-sea scavenging

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fish (Collins et al., 2005) and often associated with a switch from a predatory role to scavenging (see Section 7, Arkhipkin et al., 2003). The maximum depth for Patagonian toothfish is around 2500 m, but is likely to vary geographically, which may be linked to water temperature (see above). Using baited cameras, Collins et al. (2006) found toothfish as deep as 1600 m around South Georgia, but no fish were seen in deployments deeper than 1800 m. Toothfish have been caught down to 2122 m around the Falkland Islands (Laptikhovsky et al., 2006).

3.4. Recruitment variability Recruitment of juvenile toothfish, associated with the settlement of pelagic larvae, shows tremendous inter-annual variability. This is illustrated at South Georgia, where annual surveys showed a single cohort, first seen in 2003, dominating catches in subsequent years (Fig. 4.4), with little evidence of further recruitment until 2010 (Collins unpublished). The presence of dominant cohorts has also been detected in the fishery and through age determination from otoliths. Recruitment variability at South Georgia appears to be linked to environmental variability (Belchier and Collins, 2008). Abundance of the 1þ juvenile toothfish cohort (13–15 month-old dependent on survey date) was found to vary inter-annually and to be inversely correlated with the sea surface temperatures (SST) experienced by adults prior to spawning. The mean length of 1þ toothfish attained after 13–15 months was higher in years of high juvenile abundance and was significantly inversely correlated with SST in the summer prior to adult spawning. Around the Falkland Islands, peaks in toothfish recruitment have also been identified, occurring approximately every 4 years (Laptikhovsky and Brickle, 2005).

4. Population Structure, Movements and Migration Patterns Understanding the movements of toothfish at different temporal and spatial scales is essential to the management of this species. Although the Patagonian toothfish have a broad circum-Antarctic distribution, the bathymetric range of the juveniles and adults means that many island (adult) populations are potentially isolated from other populations by areas of deep ocean. Discrimination between different populations/stocks of Patagonian toothfish is an important part of the management process, as it is important to understand whether individual populations should be managed in isolation from other stocks. This has stimulated a range of studies that

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10 2000 5 0 2002

10 5

% Frequency

0 15 10 5 0 15 10 5 0

1+

2003

2004

2+

3+

10

2005

5 0 2006

4+

10 5 0 10

5+

2007

5 0 6+

10

2008

5 0 2009

10 5 0 20

40

60

80

100

Length class (cm)

Figure 4.4 Length-frequencies of Patagonian toothfish (Dissostichus eleginoides) from trawl surveys (100–350 m) on the South Georgia and Shag Rocks shelves (modified from Belchier and Collins, 2008).

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have investigated the degree of mixing between populations throughout the Southern Ocean and on the Patagonian Shelf. At a smaller scale, knowledge of the movements of larvae, juveniles and adults is key to understanding the life cycle. Various methods have been undertaken to examine connectivity between potential populations, including studies on genetics (Appleyard et al., 2002, 2004; Rogers et al., 2006; Shaw et al., 2004), parasite fauna (Brickle et al., 2005), biochemical markers in otoliths (Ashford and Jones, 2007; Ashford et al., 2006) and tagging studies (Marlow et al., 2003; Tuck et al., 2003; Williams et al., 2002), although tagging studies tend to be informative over shorter temporal and spatial scales.

4.1. Population structure Genetic studies indicate that a high degree of isolation exists between Patagonian toothfish populations from different locations, with distinct populations identified in the southern Indian Ocean (comprising Heard, Crozet, Kergeluen, Prince Edward and Marion islands), the Atlantic Sector (South Georgia and the South Sandwich Islands) and the Patagonian Shelf (Appleyard et al., 2002, 2004; Rogers et al., 2006; Shaw et al., 2004; Smith and McVeagh, 2000). Using mitochondrial DNA and micosatellites, initially developed by Reilly and Ward (1999), Appleyard et al. (2002) found distinct differences in toothfish populations from Macquarie Island, Heard and McDonald Islands and South Georgia/Shag Rocks. Greater differentiation of mitochondrial DNA was detected and could be explained by either female philopatry or greater male dispersal. Subsequently, Appleyard et al. (2004) used the same approach to compare samples from populations at Crozet, Kerguelen, Prince Edward, Marion and Heard and McDonald islands, and found no evidence of genetic differentiation between these sites in the western Indian Ocean. Genetic studies using mitochondrial DNA sequences (12S rRNA) have shown a distinct difference between toothfish populations on the Patagonian Shelf and those at South Georgia and on the North Scotia Ridge (Rogers et al., 2006; Shaw et al., 2004). Differences were attributed to the deep-ocean areas between the sites, which prevent adult migration, and the APF and sub-Antarctic Front and the associated high-velocity Antarctic Circumpolar Current, which limits larval dispersal. However, using microsatellites, Shaw et al. (2004) found much less distinct population structuring in the North Scotia Ridge samples and suggested that differences between mtDNA and nuclear DNA population patterns may reflect either genome population size effects or (putative) male-biassed dispersal. Rogers et al. (2006) found that samples from south of the APF (South Georgia, Bouvet and Ob Seamount) had an identical 12S rRNA haplotype.

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However, microsatellite genotype frequencies showed genetic differentiation between South Georgia samples and those obtained from around Bouvet Island and nearby seamounts. Large geographic distances and water depths in excess of 3000 m (below the bathymetric range of toothfish) separate these areas. The composition of the parasite fauna of toothfish has also been used for stock discrimination and generally supports the genetic results. Drawing on previous studies, Brickle (2003) and Brickle et al. (2005) clearly demonstrated that parasites can be used to separate D. eleginoides populations from around the Southern Ocean and the Falkland Islands. They showed that there were significant differences between populations studied, with those around Heard Island and Macquarie Island showing some similarities. Based on infra-community structure, they also concluded that a number of individual toothfish had, relatively recently, migrated from Heard to Prince Edward Island. Oliva et al. (2008) examined the metazoan parasites of D. eleginoides taken from 629 individuals caught in two localities in southern Chile (Lebu 36 S and Quello´n 48 490 ). They recovered 58,000 parasites from five taxa and concluded that their data did not support discrete stocks or provide evidence of any movement between the two localities. Elemental signatures of otolith margins (Ashford et al., 2005b) and nuclei (Ashford et al., 2006), determined using an inductively coupled plasma mass spectrometer (ICP-MS), have also been used to distinguish Patagonian toothfish from different locations in the Southern Ocean. Otolith margin signatures of calcium, strontium, magnesium and barium showed differences between capture areas (Chile, Falklands, South Georgia, Kerguelen and Macquarie) and between years from the same location (South Georgia). Otolith nuclei showed clear differences between fish from South Georgia and the Patagonian Shelf, with a discontinuity at the APF. Analysis of stable isotopes (dC13, dO18) in whole otoliths of D. eleginoides also demonstrated a distinct separation between stocks at South Georgia and those on the Patagonian Shelf (Ashford and Jones, 2007). Differences in O18 were attributed to ambient temperatures of water masses (Antarctic Intermediate water in the Patagonian shelf region; Circumpolar Deep Water in South Georgia), whilst differences in C13 were attributed to dietary differences. In summary, the data from a range of sources indicate that separate toothfish stocks exist in the western Indian Ocean (Prince Edward, Marion, Crozet, Kerguelen, Heard and McDonald islands), Macquarie Island, the Atlantic sector (South Georgia and the South Sandwich Islands) and the Patagonian/Chilean shelf. Fish from Bouvet Island are similar to the South Georgia population. The relationship between the Ross Sea population and the Macquarie Island stock is not known.

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4.2. Tagging studies and small-scale movements Toothfish have been tagged with traditional T-bar (Agnew et al., 2006b), dart, passive integrated transponder (PIT), data logging (Williams and Lamb, 2002) and more recently, pop-up archival tags (Brown et al., unpublished). Tagging is an adaptable tool and has been utilised to examine geographic and bathymetric movements, growth, behaviour and to estimate population size but all methods can provide data on movements. Toothfish are relatively robust and, given the lack of a swim bladder, do not suffer serious decompression injuries when brought to the surface from depth (Agnew et al., 2006a). Trawl, longline and potcaught fish have been successfully tagged and recaptured. Trawl caught fish are best selected from short-duration trawls, when trauma injuries are less likely. Longline caught fish can suffer hook damage but survive well, providing animals in good condition are selected (Agnew et al., 2006a). Pot-caught animals are generally in good condition, but potting is not always a commercially viable method of capture. Post-tagging survival is high and fish have been recaptured after 5 years at liberty (Agnew et al., 2006b). Tagging is now widely used in assessing population sizes (Hillary et al., 2006; Tuck et al., 2003), but here, we limit our discussion to data on movements, with other uses of tagging data discussed elsewhere. In general, tagging studies indicate that most sub-adult and adult fish remain within a relatively small area (Marlow et al., 2003; Tuck et al., 2003; Williams et al., 2002), although small numbers of tagged fish have been recovered after moving considerable distances. Williams et al. (2002) tagged 5201 (400–1000 mm TL) trawl caught fish on the Heard Island fishing grounds, recapturing 738. Ninety-nine percent (734) of the fish were recaptured within 30 km of their release location after 1–3 years at liberty. However, three fish were caught on the Crozet Plateau having moved over 1850 km, and one was recaptured at Kerguelen, 390 km from the tagging location. Marlow et al. (2003) reported on 37 recaptured fish from the early years of the South Georgia tagging programme. Of these recaptures, 28 (76%) were within 25 km of their release location. Two fish had moved 192 and 163 km in an E or SE direction from Shag Rocks towards South Georgia, consistent with their ontogenetic migration (see above; Collins et al., 2007). Two other fish caught to the E and NE of South Georgia had moved in excess of 100 km in a NW direction. By 2005, over 8000 fish had been tagged in South Georgia, with 304 returns (excluding within year returns) and had moved an average of 27 km (Agnew et al., 2006b). By 2009 over 25,000 fish had been tagged with over 2000 returns (CCAMLR, 2009). The population in the north of the South Sandwich Islands may be an extension of the South Georgia stock. A single fish tagged near the South Sandwich Islands was recaptured in the South Georgia fishery, approximately 740 km from the point of release (Roberts and Agnew, 2008).

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5. Age and Growth 5.1. Estimating age and growth Three principal methods have been applied to determining the age and growth of Patagonian toothfish; direct ageing from otoliths and scales (Horn, 2002; Hureau and Ozouf-Costaz, 1980), tagging studies (e.g. Marlow et al., 2003; Williams et al., 2002) and analysis of length-frequency data (e.g. Belchier and Collins, 2008). Although scales have been used, otolith age readings are the most widely used method of directly determining age and, when validated, provide key data for stock assessments. Length-frequency analysis is a less labour-intensive approach to indicate growth (e.g. Macdonald and Pitcher, 1979), but can be biased by sampling and does not necessarily indicate age.

5.2. Length-frequency data Whilst growth parameters can be determined from analysis of lengthfrequency data (e.g. Collins et al., 2008), in a long-lived species, such as toothfish, cohorts of adult fish are almost impossible to separate. The lengthfrequency data can, however, be informative about growth in the first few years when cohorts are more easily distinguished. It can also assist with the interpretation of the first few annuli of otoliths. From trawl surveys at Shag Rocks and South Georgia, a very strong toothfish cohort was first detected at modal size 220 mm TL in January 2003 (Fig. 4.4) and was tracked during surveys in the following years (Belchier and Collins, 2008; Collins et al., 2007). Given that toothfish spawn in winter and larvae have been caught in January, it is highly likely that these were 1þ fish in 2003 (Belchier and Collins, 2008). The juvenile toothfish cohort grew by around 100 mm TL per year and was still present in the sampled population in 2008 (Fig. 4.4).

5.3. Direct ageing methods The earliest age data were derived from a study undertaken by Zakharov and Frolkina (1976) on specimens caught at South Georgia, although little methodological detail was provided. Hureau and Ozouf-Costaz (1980) subsequently used both otoliths and scales to estimate the age of D. eleginoides caught at Kerguelen and Crozet islands, whilst Young et al. (1995) compared the utility of scales and otoliths for age determination of toothfish caught off southern Chile and found that scales gave significantly lower age estimates than otoliths in older fish. However, further work by Cassia (1998) on specimens caught at South Georgia found complete agreement between ages from scales and otoliths. A detailed comparison undertaken by Ashford et al. (2001) and lead–radium dating by Andrews

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et al. (2010) both concluded that the use of scales was likely to lead to an underestimation of true age in D. eleginoides. Since 2000, all studies on age and growth of toothfish have relied on age estimates derived from the analysis of otoliths. In 2001, a workshop on estimating age in Patagonian toothfish was held in the Centre for Quantitative Fisheries Ecology with 17 participants from several countries who were involved in ageing of toothfish. The aims were to consider toothfish otolith collection and preparation techniques as well as discuss quality control and validation.

5.4. Otolith preparation methods Whilst different authors have advocated different methods for otolith preparation, most involve mounting the otolith in epoxy resin and then sectioning it transversely through the nucleus. In some cases, the otoliths are first baked whole for short periods at around 275 C. Sections are then mounted on slides and examined with reflected light under a binocular microscope (Ashford et al., 2002; Horn, 2002), although some readers prefer to use transmitted light (Brown and Belchier, unpublished) (see Fig. 4.5). Although interpretation of ring patterns in toothfish otoliths can be problematic (Horn, 2002), they often show clear banding patterns that reflect the somatic growth of the animal. Wide annuli are deposited during the first few years of life, a period of fast growth, before slowing at or following a change in habitat, which is manifested in a transition zone in the otoliths (Horn, 2002). Horn (2002) reported discrepancies between readers often caused by interpretation of the location of the first annulus (causing at least a 1 year error) and the presence of false rings between the first 3–5 years (leading to larger ageing errors).

5.5. Validation The use of inaccurate ages has caused serious errors in the management and understanding of fish populations (Beamish and McFarlane, 1983) and can be particularly problematic in long-lived fish (Calliet and Andrews, 2008). Validation of the periodicity of increment formation is therefore essential before a particular method can be used to provide reliable age estimates of a species. Validation that the formation of rings occurs annually in Patagonian toothfish has been attempted using nuclear bomb radiocarbon tracing (Kalish and Timmiss, 1998), marginal increment analysis (Horn, 2002), comparison with length-frequency data and by injecting calcium binding fluorescent dyes to mark otoliths of fish in tagging programmes (Krusic-Golub and Williams, 2004, 2005). Kalish and Timmiss (1998) used ‘bomb 14C’ methods on the otolith cores of D. eleginoides, which were

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A

B

1 mm

Figure 4.5 Patagonian toothfish (Dissostichus eleginoides) otoliths: (A) photograph of whole otolith; (B) photomicrograph of a thin transverse section of the dorsal section of an otolith of fish estimated to be 16 years old. The arrow indicates the position of first complete annulus and the star indicates the location of the otolith core. Scale bar ¼ 1 mm.

elevated following nuclear testing in the 1960s, to calibrate growth ring counts, concluding that the counting of annual zones is probably accurate. Andrews et al. (2010) analysed the Pb/Ra of otoliths from South Georgia, Heard Island and Kerguelen, providing further confirmation of the annual deposition of growth increments. Krusic-Golub et al. (2005) used counts of daily micro-increments in otoliths of fish from Heard Island to validate the location of the first annulus and found that the average distance from the primordium to the outer edge of the first translucent zone was 0.630 mm. Krusic-Golub and Williams (2004, 2005) examined otoliths from 142 strontuim chloride injected and tagged fish (4–18 years old) from the Heard and McDonald Islands that were recaptured after 350–2571 days at liberty, to further validate the annual formation of growth rings. In most cases (88%), the number of rings after the strontium mark corresponded to the,

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time at liberty, although this accuracy was reduced (52%) when the reader was unaware of the time at liberty. Errors were usually of 1 year. Horn (2002) demonstrated that opaque zones were laid down at the otolith margins between September and February, with translucent zones laid down from February to June. All otoliths in June were found to have a translucent margin, indicating that one translucent zone was laid down annually. However in this study, there were only three samples from August and none from July or September, and the samples were aggregated over a number of years. Ashford et al. (2002) and Belchier and Collins (2008) used the clear modal separation of length cohorts of juvenile toothfish caught in trawl surveys at South Georgia to provide further indirect validation of the otolith ageing methods. However, Ashford et al. (2002) interpreted the first year class (200 mm TL) as being 0þ fish, but these are almost certainly 1þ.

5.6. Age and growth from otoliths Otolith-based analyses of the age and growth of toothfish have now been conducted in all of the major fishery regions since 2000, including the Ross Sea, South Macquarie Ridge and Southern Campbell Plateau (Horn, 2002), South Georgia (Ashford et al., 2002; Belchier, 2004) and the Kerguelen Plateau (Ashford et al., 2005a). In general, growth is initially fast, with juveniles growing in excess of 120 mm year 1 (Belchier and Collins, 2008), but the growth pattern changes at ages of 4–8 years, probably associated with a change in habitat and the ontogenetic down-slope migration. Longevity varies between regions, but this may be related to sampling bias, as commercial fisheries may not sample larger, older fish in deep water. Horn (2002) reported that D. eleginoides from Macquarie Island and the northern Ross Sea reached 54 years of age. Toothfish are reported to reach 33 years on the Patagonian Shelf (Laptikhovsky et al., 2006), 36 years around Kerguelen Island (Ashford et al., 2005a) and over 50 years of age at South Georgia (Belchier, 2004). Growth typically follows the von Bertalanffy pattern, reaching an average asymptotic size and, in common with many teleost fish, growth rates (and von Bertalanffy parameters) vary regionally and between sexes (Table 4.1; Fig. 4.6). Females generally grow quicker and reach larger size than males (Horn, 2002). However, Aguayo (1992) and Young et al. (1992) found no sexual differences in growth for fish off southern South America, although females are known to attain a greater size than males in this region (see Moreno, 1998). Regional differences in growth rate (Table 4.1; Fig. 4.6) may be attributed to differences in environmental conditions and prey availability between locations. However, the wide variation in growth parameters within and between locations suggests that sampling biases and to a lesser

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Table 4.1 Von Bertalanffy growth parameters, derived from otolith increment counts, for Patagonian toothfish (Dissostichus eleginoides) from different locations and studies Regions

Patagonian Shelf South Georgia

Sex

Female Male Female Male South Georgia Combined South Georgia Combined Southern Chile Female Male Heard Island Female Male Kerguelen Female Male Macquarie Female Male Macquarie/NZ Female EEZ Male

L1

K

t0

Author

141.4 120.7 177.5 170.3 150 132 209.7 195.6 74.4 73.9 103.5 95.9 205.3 138.4 158.3 134.3

0.1500 0.1300 0.0820 0.0860 0.073 0.08 0.0641 0.0742 0.4800 0.3100 0.1100 0.1200 0.0450 0.0720 0.0850 0.1180

1.1000 1.5500 0.3500 0.0150 0.792 0.3 1.1508 0.7205 0.4600 1.7100 4.7000 4.6000 1.5400 1.3700 0.3500 0.0800

Ashford et al. (2001) Aguayo (1992) Belchier (2004) CCAMLR 2009 Young et al. (1992) Ashford et al. (2001) Ashford et al. (2005a) Kalish and Timmiss (1998) Horn (2002)

extent variability in otolith annuli interpretation have given rise to some of the observed differences. Ashford et al. (2005a) noted differences in the age composition of the catch of toothfish caught by different vessels fishing within the same region and noted that sampling effects, possibly caused by differences in fishing gear could generate biases in estimates of age structure. Unrealistically low estimates of asymptotic length and t0 (Table 4.1) are most likely a result of bias from sampling only the fished population for the derivation of growth curves (Belchier, 2004). Candy et al. (2007) noted that poor fits of the von Bertalanffy model are in part a result of fishing gear selectivity, leading to under sampling of both the younger and older parts of the toothfish population.

5.7. Growth estimates from tagging With the increase in tagging effort on many toothfish populations, it has been possible to obtain direct validation of otolith-derived growth models using mark recapture data. Such an approach has been undertaken for both Heard and McDonald Islands (HIMI) (Candy et al., 2007) and South Georgia (Agnew et al., 2006b; Marlow et al., 2003). In both regions, growth in fish length observed during the time at liberty (i.e. between tagging and recapture) has been compared with a predicted growth increment based on the otolith-

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180

Females

160

160

140

140

Total length (cm)

Total length (cm)

180

120 100 80 60

South Georgia (Ashford et al., 2001) Macquarie (Kalish and Timimiss, 1998) South Georgia (Aguayo, 1992) Ross Sea (Horn, 2002) South Georgia (Belchier and Agnew, 2009)

40 20 0

0

10

20

30

40

Males

120 100 80 60

South Georgia (Ashford et al., 2001) Macquarie (Kalish and Timimiss, 1998) South Georgia (Aguayo, 1992) Ross Sea (Horn, 2002) South Georgia (Belchier and Agnew, 2009)

40 20 0

50

0

10

220 Females 200 180 160 140 120 100 80 60 40 20 0 0 10

20

30

40

50

Age (years)

Total length (cm)

Total length (cm)

Age (years)

Southern Chile (Young, 1992) Southern Chile (Aguayo and Cid, 1991) Central Chile (Rubliar, in preparation) Falklands (CAF, 1998)

20 30 Age (years)

40

50

220 Males 200 180 160 140 120 100 80 60 40 20 0 0 10

Southern Chile (Young, 1992) Southern Chile (Aguayo and Cid, 1991) Central Chile (Rubliar, in preparation) Falklands (CAF, 1998)

30 20 Age (years)

40

50

200

Total length (cm)

180

Kerguelen females (Ashford et al., 2005a) Kerguelen males (Ashford et al., 2005a) Heard females (Ashford et al., 2005a) Heard males (Ashford et al., 2005a)

160 140 120 100 80 60 40 20 0

0

10

20

30

40

50

Age (years)

Figure 4.6 Comparison of von Bertalanffy growth curves of Patagonian toothfish (Dissostichus eleginoides), derived from otolith-based age studies in different geographic areas. CAF= Central Ageing Facility, Melbourne, Australia.

derived growth parameters. At both South Georgia (Agnew et al., 2007) and HIMI (Candy et al., 2007), there has been generally good agreement between estimates, but there is some evidence that otolith-derived growth parameters overestimate toothfish growth when compared to the mark recapture data. Candy et al. (2007) suggest that this may also be attributed to sampling bias. However, it is also likely that tagged fish experience some degree of growth retardation or ‘tag shock’ in which somatic growth is suppressed for an extended period (as much as a year) post-tagging. Growth retardation from

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tagging has been well documented for other fish species (McFarlane and Beamish, 1990) and it is therefore advisable to exercise caution when estimating growth from mark-recaptured individuals.

5.8. Larval and juvenile growth Studies relating to the growth of larval and juvenile toothfish have been restricted to work on the South Georgia shelf. North (2002) estimated growth of larval and early juvenile toothfish at 0.8% SL d 1 from pelagic net samples taken from the north of South Georgia. This growth rate is around the mid-range of growth rates, of between 0.3% SL d 1 and 2% SL d 1 estimated for other larval notothenioids at South Georgia during summer (North, 1998). North (2002) observed annual growth of around 160 mm TL for the first year and noted that this was greater than predicted from the growth model. However, Belchier and Collins (2008) showed that there is considerable variability in the mean length attained by juvenile toothfish in their first year of growth at Shag Rocks. In this study, it was shown that mean fish length attained after 14 months can vary interannually by greater than 50 mm (TL). It is suggested that growth variability is related either directly or indirectly to environmental conditions. High growth rate was associated with strong cohorts, suggesting a positive correlation between juvenile growth and survivorship.

6. Reproduction Notothenioid reproduction is characterised by protracted gametogensis and low fecundity, with most species not reaching maturity until at least 5 years -old (Kock and Kellermann, 1991). Information on Antarctic and sub-Antarctic fish suggest that spawning occurs in austral autumn and winter (Kock and Kellermann, 1991). There is limited information on the reproductive biology of D. eleginoides in the literature, but some work has been undertaken around the sub-Antarctic islands, on the Patagonian Shelf and off the coast of Chile.

6.1. Size at maturity In Patagonian toothfish, maturity occurs at approximately half of their maximum length with some variation in 50% maturity values from different regions and studies (Table 4.2). Everson and Murray (1999) studied the size at sexual maturity of toothfish caught in the commercial fishery at South Georgia in 1996 and 1997 and found that there was evidence in 1997 that 25–43% of mature female D. eleginoides did not spawn. They noted that if

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Table 4.2 Length at 50% (Lm50) maturity for Patagonian toothfish (Dissostichus eleginoides) from different locations Lm50 (mm) Source

Area

Male

Female

CCAMLR (1987) Moreno (1998) Everson and Murray (1999) Agnew et al. (1999) Laptikhovsky and Brickle (2005) Prenski and Almeyda (2000) Moreno et al. (1997) Young et al. (1999) Oyarzu´n et al. (2003) Arana (2009) Duhamel (1991) Lord et al. (2006)

South Georgia South Georgia South Georgia South Georgia Patagonian Shelf Argentina Chile Chile Chile Chile Kerguelen Kerguelen

577 670 785 750 860 763 1050

1104 860 982 1010 900 871 1170 1287 1130–1170 890 800 850

780–940 810 650 630

Lm50 was calculated without taking this non-spawning into account, it would lead to an overestimation. Analysis of von Bertalanffy growth curves indicates that Lm50 for toothfish is attained between the ages of 6 and 10 for males, and between 10 and 13 years for females. Skipped or incomplete spawning has been reported in numerous species of iteroparous fish (Rideout et al., 2005), with non-spawning occurring due to either retaining or reabsorbing eggs or the fish remaining in a resting stage. Histological analysis is needed to determine the nature of this process in toothfish, and it is likely that in years with higher than average temperatures, a variable number of toothfish skip spawning which in turn will affect the strength of recruitment the following year (Brown and Brickle, unpublished data). This phenomenon has also been suggested by Arana (2009).

6.2. Fecundity The Patagonian toothfish is the most fecund nototheniid, with absolute fecundities ranging from 48,900 to 528,900 on the Kerguelen plateau (Chikov and Mel’nikov, 1990) and between 56,940 and 567,490 in South Georgia (Nevinsky and Kozlov, 2002). The Chikov and Mel’nikov (1990) study indicated that there were two size groups in the measured oocytes in maturing fish caught between March and April. The first mode was between 0.1 and 1.1 mm (protoplasmic oocytes), with the second between 1.4 and 2.9 mm (trophoplasmic), indicating that the maturation of oocytes is

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discontinuous and synchronous during vitillogenesis, which suggests single non-intermittent spawning. Larger vitellogenic oocytes were recorded to increase in volume quickly from a mean diameter of 1.53 mm in March to 1.9 mm in April (Chikov and Mel’nikov, 1990). Of the notothenioids studied to date, most spawn annually, with the vitellogenic process often taking 2 years (Everson, 1977; Kock and Kellermann, 1991; Shandikov and Faleeva, 1992). Therefore, it is probable that the two stocks of ova which are seen ripening at different stages in toothfish are for spawning in the current and following year. Chikov and Mel’nikov (1990) and Nevinsky and Kozlov (2002) investigated the relationship between fecundity and size (Fig. 4.7). The former’s estimates are higher than those of the latter authors, which is probably due to the size range of individuals sampled. Chikov and Mel’nikov (1990) sampled individuals up to 1300 mm TL, whereas Nevinsky and Kozlov (2002) sampled toothfish up to 1600 mm TL.

6.3. Timing of spawning Spawning in Patagonian toothfish generally occurs during the austral winter (June-September) period (Agnew et al., 1999; Laptikhovsky et al., 2006; Lord et al., 2006; Arana, 2009). Laptikhovsky et al. (2006) analysed data collected by observers on longliners operating on the Patagonian Shelf and reported two spawning peaks for toothfish, a small peak in May and a major peak in July/August. Females were found to disperse over a greater depth range than males. They also found that males migrate to the spawning grounds on Burdwood Bank earlier than females and stay at a depth of 1500–2000 m until it is time to spawn at approximately 1000 m. Examination of maturity 700,000 600,000

Chikov and Mel’nikov (1990) Nevinsky and Kozlov (2002)

No of eggs

500,000 400,000 300,000 200,000 100,000 0 800

1000

1200

1400 TL (mm)

1600

1800

2000

Figure 4.7 Relationship between fecundity and size in Patagonian toothfish (Dissostichus eleginoides).

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data of toothfish caught around South Georgia and Shag Rocks revealed a large spawning event in late July/August, with a possible smaller spawning event in April/May, and fish were found to migrate up (females) and down (males) the slope to meet at the spawning grounds at around 800–1200 m (Agnew et al., 1999). Lord et al. (2006) showed that toothfish spawning at Kerguelen occurs between late April/May and mid-July (for females) but begins later for males (end of May). Off the Chilean coast Arana (2009) found toothfish with developing gonads in June and July, mature gonads from July to September, and spent gonads from August to October. Agnew et al. (1999) reported pre-spawning fish to be distributed all around the shelf slopes of South Georgia and Shag Rocks whereas both male and female spent fish were concentrated in the shallower waters to the northeast of Shag Rocks with very few spent fish being found around South Georgia. On the Patagonian Shelf, spawning only occurs to the south of the Falkland Islands. (Laptikhovsky and Brickle, 2005; Laptikhovsky et al., 2006). In the Pacific, spawning is not found north of 50 S and this coupled with the hypothesised reduced migratory capabilities of toothfish, might explain the progressive decline in yields north of 47 S (Arana, 2009). It is likely that toothfish north of the Polar Front are at the edge of their range, thus explaining the southerly location of the spawning grounds in the Pacific and Atlantic Oceans (Brown and Brickle, unpublished data).

6.4. Eggs and larvae Once hydrated and spawned, the eggs are 4.4–4.5 mm in diameter with a rough chorion and large perivitelline space and a homogeneous yolk (Evseenko et al., 1995). A number of authors have described various sizes of toothfish from embryo (Evseenko et al., 1995; Kellermann, 1989), to larvae 11–28 mm (Ciechomski and Weiss, 1976; Evseenko et al., 1995; Kellermann, 1989) to larvae/early juveniles 18–63 mm (Effremenko, 1979; North, 2002). Pigmentation consists of a band on the posterior post-anal section, single pigment spots below the pectoral fin, melanophores along the abdominal region and occipital melanophores on the brain (Kellermann, 1989). Welldeveloped canine teeth are present on the lower jaw once larvae reach 20–22 mm SL. The pigmentation remains unchanged during larval development, except for the formation of a ventral row of melanophores appearing from the posterior pigment band to the anus (Kellermann, 1989). Larvae are thought to occur from November onwards and are in the region of 14 mm at hatching (Kock and Kellermann, 1991). North (2002), using this size at hatching and early larval growth rates, predicted that larvae caught around South Georgia hatch between November and mid December, suggesting a 3.5-month period of embryogenesis. This is rapid in comparison to other notothenioids; 4–6 months in

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Nototheniops nudifrons (Kellermann, 1990) and up to 5 months in Notothenia corriiceps (Everson, 1977; White et al., 1982).

7. Trophic ecology 7.1. Toothfish diet Korovina et al. (1991) described the digestive tract of toothfish as consisting of a large stomach, six to seven pyloric caeca and a digestive tract comprising 87% of the standard body length. A strongly developed muscular membrane in the midgut wall (94% of wall thickness) is present, a morphological adaptation which allows toothfish to consume large quantities of prey. The diet of adult and juvenile toothfish has been studied using conventional stomach contents analysis on trawl, longline and pot-caught fish (Table 4.3), and using biomarkers such as stable isotopes and fatty acids (Stowasser, BAS unpublished). There are clear ontogenetic changes in the diet of toothfish, associated with the down-slope migration and general switch to scavenging as size increases. The diet of larval toothfish has not been studied. The diet of juvenile toothfish (<750 mm TL) has largely been determined from trawl caught specimens, which are primarily piscivorous, usually taking the most abundant small fish in their area (Barrera-Oro et al., 2005; Collins et al., 2007). Zhivov and Krivoruchko (1990) did, however, find that smaller juveniles (250–400 mm TL) at South Georgia and Shag Rocks fed mainly on hyperiid amphipods and euphausids. On the Patagonian Shelf, juveniles take a diverse fish fauna, including Patagonotothen ramsayi and juveniles of other nototheniid species (Arkhipkin et al., 2003); however, with increasing size (and depth of occurrence), the diet changes to include deeper-dwelling and larger species such as hoki (Macruronus magellanicus) and southern blue whiting (Micromesistius australis). Garcia de la Rosa et al. (1997) also found the diet of juveniles to be dominated by fish with cephalopods also taken. In four summer seasons, Collins et al. (2007) found that the diet of juveniles at Shag Rocks was dominated by the abundant yellow-finned notothen (Patagonotothen guntheri), which made up 90% of the diet, whereas at South Georgia, where P. guntheri is absent, other nototheniids were the primary prey. In contrast, during March–April 1996, Barrera-Oro et al. (2005) did not find any Patagonotothen guntheri in the diet, with Lepidonotothen squamifrons the most abundant prey species at Shag Rocks; however, almost 49% of the fish were not identified to species. Some pelagic prey species have been reported to be taken, including myctophids and Antarctic krill (Collins et al., 2007; Garcia de la Rosa et al., 1997). The diet of large, adult toothfish has been studied from both longline and pot-caught fish. In general, adult toothfish are opportunistic carnivores,

Table 4.3

Diet of Patagonian toothfish (Dissostichus eleginoides)

Location

South Georgia, 1985–1986

Shag Rocks

Depth range (numbers sampled)

Gear and size range

Diet summary

Main Prey Species

Source

200–400 m (244)

Trawl

Fish (74 %F); crustaceans (15 %F); cephalopods (5 %F)

Zhivov and Krivoruchko (1990)

400–600 m (217)

Trawl

Fish (56 %F); crustaceans (24 %F); cephalopods (12 %F)

600–1000 m (249)

Trawl

Fish (77 %F); crustaceans (14 %F); cephalopods (7 %F)

1000–1400 m (160)

Trawl

Fish (44 %F); crustaceans (42 %F); cephalopods (12 %F) Fish (70 %F)

Unidentified fish (51 %F); Electrona carlsbergi (9 %F); crabs (5 %F); squid (5 %F) Unidentified fish (28 %F); E. carlsbergi (10 %F); lobsters (24 %F); squid (10 %F) Unidentified fish (47 % F); Patagonotothen guntheri (10 %F); krill (4.8 %F) Unidentified fish (43 %F); crabs (12.5 %F); squid (10 %F) Unidentified fish (49 % F); L. squamifrons, Champsocephalus gunnari and Chaenocephalus aceratus P. guntheri (85 %M); Gymnoscopelus nicholsi (4 %M); Euphausia superba (2 %M)

Trawl; < 750 mm TL.

South Georgia and Shag Rocks

Shag Rocks, Jan (2003–2006)

100–400 m (636)

Trawl; < 750 mm TL

Fish (98 %M); crustaceans (2 % M)

Barrera-Oro et al. (2005)

Collins et al. (2007)

South Georgia, Jan (2003–2006)

100–400 m (159)

Trawl; < 750 mm TL

Fish (89 %M); crustaceans (10 %M)

South Georgia and Shag Rocks, Dec 87–Jan 88

50–500 m (50)

Trawl

Fish (96 %F)

South Georgia and Shag Rocks, March–May 2000

200–1650 m (2268)

Pot; 600–1200 mm TL

Crustaceans (48 %N); fish (34 %N); cephalopods (8 %N)

Shag Rocks, May– August 2000

300–600 m (122)

Longline

Fish (51 %F); crustacean (16 %F); cephalopod (9 %F)

South Georgia and Shag Rocks, February 1994

300 m (129)

Trawl; 180–900 mm TL

Fish (86 %F); krill (20 %F)

Trematomus hansoni (23 %M); Lepidonotothen larseni (22 %M); C. gunnari (13 %M); E. superba (8 %M) Muraenolepis sp. Parachaenichthys georgianus and L. larseni 80% of fish unidentified; P. guntheri; myctophids; Nauticaris sp.; Paralomis sp.; Thymops birsteini; E. superba; Kondakovia longimana; Pareledone turqueti; Gonatus antarcticus Macrourus sp., Muraenolepis spp., nototheniids, channichthyids E. superba; Champsocephalus gunnari; Gobionotothen gibberifrons; Pseudochaenichthys georgianus; Nototheniops nudifrons

McKenna (1991)

Pilling et al. (2001); Xavier et al. (2002)

Pilling et al. (2001)

Garcia de la Rosa et al. (1997)

(continued)

Table 4.3

(continued)

Location

Depth range (numbers sampled)

Gear and size range

Diet summary

Main Prey Species

P. guntheri; myctophids; Antimora rostrata; Macrourus holotrachys; Bathydraco sp., Chionodraco sp., Lycodapus spp., Pachycara brachycephalus, K. longimana Bathylagus sp. (14 %M); Gonatus antarcticus (16 %M); macrourids; nototheniids and myctophids Patagonotothen ramsayi (26 %F), Micromesistius australis; Iluocoetes fimbriatus; Merluccius hubsi; Macruronus magellanicus; Illex argentinus and Loligo gahi

South Georgia and Shag Rocks, March–April 1995

1050–1530 m (226)

Longline

Fish (60 %F); squid (14 %F); crustaceans (22 %F)

Macquarie Island, summer 1995/ 96, 1996/97; 1997/98;

500–1290 m (462)

Trawl; 310–1490 mm TL

Fish (58 %M); squid (32 % M); crustaceans (10 %M)

Argentine Shelf

< 650 m (135)

Shelf. 290–950 mm TL

Fish (95 %F); cephalopods (7 %F)

Source

Goldsworthy et al. (2002)

Garcia de la Rosa et al. (1997)

Falkland Islands, Apr 1999–Aug 2002

< 500 m (135)

< 400 mm TL

Fish (75% F); cephalopods (21% F)

< 500 m (366)

400–600 mm TL

Fish (73 %F); cephalopods (22 %F)

< 500 m (109)

> 600 mm TL

Fish (90% F); cephalopods (7.3 %F)

500–1000 m (62)

400–1600 mm TL

Fish (72% F); crustaceans (15 %F); cephalopods (6 %F)

> 1000 m (63)

500–1900 mm TL

Fish (61 %F); crustaceans (43 %F); cephalopods (5 %F)

P. ramsayi (24 %F); juvenile nototheniids (20 %F); unidentified fish (24 %F); Loligo gahi (24 %F) P. ramsayi (28 %F); juvenile nototheniids (5 %F); unidentified fish (34 %F); L. gahi (21 %F) M. magellanicus (20.2 % F); M. australis (18 % F); unidentified fish (31 %F); Moroteuthis ingens (6 %F) A. rostrata (29 %F); unidentified fish (32 %F); Acanthephyra pelagica (15 %F); M. ingens (5 %F) A. rostrata (11 %F); unidentified fish (37 %F); A. pelagica (41 %F); M. holotrachys (6 %F); unidentified cephalopods (5 %F)

Arkhipkin et al. (2003)

(continued)

Table 4.3

(continued)

Location

Depth range (numbers sampled)

Gear and size range

Diet summary

Main Prey Species

Source

Artisanal fishery; 570–1610 mm TL

Fish (96% IRI)

Macrouridae (22%F); Ophidiidae (16%F); unidentified fish (37 %F); Onychoteuthidae (5 %F) C. gunnari (25 %F) and L. squamifrons (12 %F), myctophids (27 %F) Nototheniids, myctophids and amphipods

Murillo et al. (2008)

Central and Southern Chile, Oct 2001–Oct 2002

> 500 m (203)

Kerguelen

(748)

Fish (90 %F)

Crozet

(31)

Fish (36 %F); crustaceans (37 %F); cephalopods (8 %F)

%F = percent frequency of occurrence; %M = percent by mass; %N = percent numbers.

Duhamel (1981)

Duhamel and Pletikosic (1983)

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feeding on suitably sized locally abundant prey, including a variety of demersal and pelagic fish, crustaceans and cephalopods. Evidence from baited cameras (Collins et al., 1999, 2006) and longline captures indicate the propensity to scavenge food, but the importance of scavenging is not known and may vary spatially, temporally and ontogenetically. Studies of adult diet have been undertaken at South Georgia, the Patagonian Shelf and around Kerguelen. From a study at South Georgia, Pilling et al. (2001) showed that the proportion of empty stomachs was generally higher in longline caught animals than pot-caught animals, which the authors attributed to an increase in stress-induced regurgitation in line caught fish. However, there was also a distinct difference in diet between fish caught by the two methods, with decapod prawns of the genus Nauticaris found in potcaught toothfish stomachs. It is possible that the prawns were attracted to the baited traps and were consumed inside the traps by the toothfish, which would bias the results of the pot-caught fish. Pilling et al. (2001) also found an increase in Nauticaris sp. and cephalopods with size (and depth), with a decrease in the importance of fish. The fish they identified in the diet included myctophids, nototheniids, Muraenolepis sp., morid cods and grenadiers. The cephalopod component of the prey from the Pilling et al. (2001) study was also reported in more detail by Xavier et al. (2002). Garcia de la Rosa et al. (1997) also examined the diet of adult toothfish at South Georgia and found fish (mostly unidentified), isopods and the squid Kondakovia longimanna as the main prey, with lithodid crabs also taken. Less information is available for toothfish diet in the Indian Ocean sector, but on the Kerguelen shelf, the diet was also dominated by fish, with the principal prey being myctophids and the notothenioids Champsocephalus gunnari and Lepidonotothen squamifrons (Duhamel, 1981). A relatively small study at Crozet (74 stomachs) found the main prey (% occurrence) to be amphipods, with nototheniid and myctophids fish also important (Duhamel and Pletikosic, 1983). Many diet studies have focussed on a single season (summer), and diet may change seasonally, but data on seasonal changes is limited. Arkhipkin et al. (2003) reported that toothfish (400–600 mm TL) exhibited seasonal variations in their diet on the Patagonian Shelf. They concluded that seasonal changes in diet reflected the seasonal variations in prey abundance on the shelf. Patagonotothen ramsayi was abundant in the diet throughout the year, whereas Loligo gahi only appeared from February to October during its offshore seasonal migrations. During November to January, Loligo gahi migrate inshore to spawn and subsequently disappeared from toothfish diet. Instead, toothfish consumed southern blue whiting (Micromesistius australis), which spread out over the shelf after spawning to the south west of the Falkland Islands.

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7.2. Feeding rates Tarverdiyeva (1972) calculated daily rations for D. eleginoides as 5.1% of its wet body weight per day (at temperatures of 1.2–1.3 C). In studies of diet of toothfish at South Georgia, Collins et al. (2007) found over 75% of stomachs examined contained food, with the contents averaging around 2% body weight. Trawls were only undertaken during daylight, but there was no relationship between fullness and time of day.

7.3. Foraging behaviour A combination of dietary data, baited cameras and data-logging tags indicate that toothfish forage in the mesopelagic realm as well as on the seafloor. Pelagic prey make up a significant part of the diet, and evidence from datalogging tags shows that toothfish spend some of their time off the seafloor (Williams and Lamb, 2002), perhaps foraging or utilising currents for transport. Scavenging is also important, and baited camera work has shown that large toothfish approach squid or mackerel bait from down current, presumably using olfaction to detect odour plumes from carcasses or bait (Collins et al., 1999, 2006). Toothfish appear cautious and circle the bait before attempting to consume it, but this may be a response to the light, as footage from baited video cameras shows them repeatedly circling the illuminated area, before venturing in to grab the bait (Collins et al., 2006). The bait was attached by wire to a graduated cross and toothfish were seen pulling the bait off with a jerky motion, before swallowing the squid (bait) whole. In one case, a toothfish ‘barrel rolled’ through three complete turns to remove the bait from the cross (Collins et al., 2006). Live fish kept in captivity have been noted to take pieces of food (fish muscle) from the bottom of the tank and midwater as it floats down, and swallow it whole. They initially are seen to ‘smell’ the food. Smaller fish (< 600 mm) were more aggressive during feeding, attempting to take food from other fish in the tank. On numerous occasions, if two fish had a hold of a large piece of bait, fish were recorded to ‘barrel roll’ to break the food (Howes, Falkland Fisheries Department personal communication).

7.4. Predators of toothfish Data on toothfish predators are rather limited. In shallow water, reported predators of juveniles include penguins (Brown and Klages, 1987; Goldsworthy et al., 2001), fur (Green et al., 1989; Reid and Arnould, 1996) and elephant seals (Green et al., 1989; Reid and Nevitt, 1998; Slip, 1995), but with increased size and habitat depth, the range of potential predators is likely to decline (Table 4.4). From extensive studies undertaken at South Georgia,

Table 4.4 Predators of Patagonian toothfish Potential predator

Maximum depth

Comments

Sources

Southern elephant seal Mirounga leonina

Dive to > 2000 m.

Slip (1995); Reid and Nevitt (1998)

Antarctic fur seal Arctocephalus gazella

Dive to 300 m

Weddell seal Leptonychotes weddelli

Dive to 450 m

Reported to consume toothfish, but importance in diet not established; potentially a significant predator Toothfish otoliths occasionally in scats at South Georgia and Heard Island; unlikely to be a significant predator Know to take D. mawsoni in Weddell Sea; small South Georgia population may take D. eleginoides

Hooker’s sea-lions Phocarctos hookeri Sperm whale Physeter macrocephalus

Dive to 500 m

Toothfish otoliths reported in 42% of scats

Dive in excess of 2000 m

Known to consume toothfish; take toothfish from longlines; population size at South Georgia is unknown

Dive to 200 m

Take toothfish off longlines, but do not dive deep enough to catch adults Piscivorous, but pelagic feeders generally taking small fish (myctophids) and squid; no toothfish reported in diet at South Georgia, but reported in diet at Crozet (n = 2, 4.3% occurrence) Not known to take toothfish in South Georgia area, but toothfish recorded in diet at Maquarie Islands (0.1–1.2% occurrence) and Kerguelen (2.5% occurrence). Juvenile toothfish noted in diet around the Falkland Islands

Killer whale Orcinus orca King penguin Aptenodytes patagonicus

Gentoo penguin Pygoscelis papua

Dive to 300 m

Dive to 150 m

Green et al. (1989), Reid (1995); Reid and Arnould (1996) Calhaem and Christoffel (1969); Testa et al. (1985); Plotz (1986); Lake et al. (2003) McMahon et al. (1999) Korabelnikov (1959); Clarke (1980); Abe and Iwami (1989); Watkins et al. (1993); Ashford et al. (1996); Purves et al. (2004); Kock et al. (2006) Ashford et al. (1996); Purves et al. (2004); Kock et al. (2006) Kooyman et al. (1992); Cherel et al. (1996); Olsson and North (1997)

Adams and Klages (1989); Robinson and Hindell (1996); Goldsworthy et al. (2001); Lescroel et al. (2004); Putz et al. (2001) (continued)

Table 4.4

(continued)

Potential predator

Maximum depth

Comments

Sources

Macaroni penguin Eudyptes chrysolophus Magellanic penguin Spheniscus magellanicus Rockhopper penguin Eudyptes chrysocome Black-browed albatross Thalassarche melanophris Grey-headed albatross Thalassarche chrysostoma White chinned petrels Procellaria aequinoctialis Patagonian toothfish Dissostichus eleginoides

Dive to 120 m

Single incidence of toothfish in diet at Marion Islands, never recorded at South Georgia Juvenile toothfish noted in diet around the Falkland Islands Juvenile toothfish noted in diet around the Falkland Islands Toothfish in stomachs probably from hooks and/ or discards from fishing vessels

Brown and Klages (1987)

Kingclip Genypterus blacodes Sleeper sharks Somniosus sp. Giant Antarctic squid Mesonychoteuthis hamiltoni

Dive to 150 m Dive to 150 m Surface feeders

Putz et al. (2001) Putz et al. (2001) Cherel et al. (2000, 2002)

Surface feeders

Toothfish in stomachs probably from hooks and/ or discards from fishing vessels

Cherel et al. (2002); Xavier et al. (2003)

Dive to 10 m

Toothfish in stomachs probably from hooks and/ or discards from fishing vessels Some cannibalism likely, with large fish taking smaller cohorts, but will be limited by the size– depth distribution pattern Occasionally predates on small juvenile toothfish on Falklands Shelf Toothfish recorded in stomachs, but may be net feeding and scavenging on discarded heads Reach large size (> 100 kg); incidentally caught on longline hooks targeting toothfish. Possible predator, abundance unknown

Catard et al. (2000)

2500 m

100–700 m 2000 m Unknown

Arkhipkin et al. (2003)

Nyegaard et al. (2004) Cherel and Duhamel (2004) Collins and Rodhouse (2006); Collins (unpublished)

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toothfish are rarely taken by fur seals or penguins and only are occasionally taken by these species elsewhere (see Table 4.4). The most important predators of adult toothfish are likely to be large, deep-diving vertebrates, such as sperm whales and elephant seals, which have the capacity to dive to the depths which toothfish inhabit. Toothfish have been recorded in sperm whale stomachs (Abe and Iwami, 1989; Clarke, 1980; Korabelnikov, 1959) and, although generally considered squid eaters, they are potentially important toothfish predators. The population size of sperm whales in the Southern Ocean is not, however, known, so the impact is difficult to assess. Elephant seals, particularly males, also have the ability to dive to the depths that adult toothfish occur and toothfish have occasionally been identified in their diet (Reid and Nevitt, 1998; Slip et al., 1994). Sperm and killer whales are both known to take toothfish from longlines during hauling (Ashford et al., 1996; Kock et al., 2006; Purves et al., 2004), but adult toothfish habitat is beyond the normal diving capabilities of killer whales. Antarctic toothfish are known in the diets of Weddell seals (Ainley and Siniff, 2009), and the distribution of Weddell seals overlaps with Patagonian toothfish in some places (e.g. South Georgia), making them a potential predator. Little is known about the ecology of Mesonychoteuthis hamiltoni, but these large squid are probably capable of catching and consuming large toothfish, and are occasionally caught on longline hooks at South Georgia (Collins, unpublished data). Albatross and white-chinned petrels are known to take toothfish (Catard et al., 2000; Cherel et al., 2000, 2002), but these are, almost certainly, fish that escape from hooks or are discards from fishing vessels. A wandering albatross has been witnessed swallowing whole a recently tagged 550 mmTL toothfish (Collins, personal observation).

7.5. Accumulation of mercury in toothfish tissue As toothfish are large, relatively slow growing predatory or scavenging fish and occupy a similar top trophic level to large tunas, swordfish and sharks there has been some concern that their tissues may also accumulate high levels of mercury (Hg) that could be detrimental to human health when consumed. A preliminary study of 18 fish by Mendez et al. (2001) showed that mercury levels ranged between 0.12 and 0.73 mg kg-1 with some samples having levels above the EU and Australian limit for mercury in fish of 0.5mg kg-1. A subsequent study on juveniles caught at Macquarie Island (McArthur et al., 2003) also found mercury levels close to the recommended maximum and concluded that levels of mercury would increase as fish grew larger. A recent study by Guynn and Peterson (2008) demonstrated a clear increase in mercury concentrations in fish muscle with increasing size but also noted that there were distinct regional differences in

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overall levels of mercury found in toothfish tissue. Mercury levels found in fish caught in regions north of the APF (Chilean waters and the Prince Edward Islands) had far higher levels of mercury than those detected in fish caught at South Georgia to the south of the APF.

8. Parasites 8.1. Parasite fauna and host specificity Sixty-two species of parasite have been reported from Patagonian toothfish from different areas of the host’s distribution (Brickle, 2003; Brickle et al., 2005, 2006; Gaevskaya et al., 1990; Hamilton, 1995; Oliva et al., 2008; Parukhin and Lyadov, 1982; Rodriguez and George-Nascimento, 1996) (Table 4.5; Fig. 4.8). Comparisons of these results have demonstrated major differences in the parasite fauna of D. eleginoides from different locations across their range (Brickle, 2003; Brickle et al., 2005; Gaevskaya et al., 1990). Thirteen oioxenic species, comprising two microsporideans, four myxozoans, three digeneans, three monogeneans and one acanthocephalan, have been reported solely from D. eleginoides (Gaevskaya et al., 1990; Brickle, 2003). However, considering that the knowledge of the ichthyoparasite fauna of the sub-Antarctic and Antarctic is poor in comparison to other regions, it is possible that some of these species may be reported from other fish species in the future. Four parasitic species found in D. eleginoides are specific to the Nototheniidae and are thus stenoxenic (Brickle, 2003). These include one nematode, one digenean, one monogenean and one acanthocephalan. The nematode Hysterothylacium nototheniae was reported from the Ob and Lena Banks, the acanthocephalan Metacanthocephalus rennicki was only reported from the Lena Bank and the monogenean Pseudobenedeniella branchialis occurred in South Georgia. Forty-three of the parasites reported from D. eleginoides are considered generalists (eurixenic), which infect fish other than the nototheniids (Brickle et al., 2005; Gaevskaya et al., 1990; Oliva et al., 2008; Rodriguez and George-Nascimento, 1996). Six of these species, appear to be specific to the perciform suborder Notothenioidea. The latter include Dichelyne (Cucullanellus) fraseri, Lecithophyllum champsocephali, Lepidapedon taeniatum, Lepidapedon garrardi, Heterosentis heteracanthus and Eubrachiella antarctica. Clestobothrium crassiceps is considered one of two accidental infections for D. eleginoides. Specimens were found to infect D. eleginoides from the Patagonian Shelf (Brickle, 2003) and in a single fish caught at South Georgia (Gaevskaya et al., 1990). Clestobothrium crassiceps is stenoxenic and usually found in Merluccius spp. (Esch and Fernandez, 1993), so it is little surprising

Table 4.5 Geographical distribution of parasites infecting Dissostichus eleginoides from around the Southern Ocean Geographic range Type

Microsporidia Myxozoa

Digenea

Microsporidean sp. 1 Microsporidean sp. 2 Neoparvicapsula subtile Sphaerospora dissostichi Ceratomyxa dissostichi Alatospora sp. Brachyphallus crenatus (adult) Derogenes varicus (adult) Digenean sp. 1 (adult) Elytrophalloides oatesi (adult) Glomericirrus macrouri (adult) Gonocerca crassa (adult) Gonocerca phycidis (adult) Gonocerca taeniata (adult) Helicometra antarcicae (Dadult) Hirundinella ventricosa (larva) Lecithaster australis (adult) Lecithaster macrocotyle (adult) Lecithochirium genypteri (adult) Lecithochirium sp. (adult) Lecithophyllum champsocephali (adult) Lepidapedon garrardi (adult) Lepidapedon taeniatum (adult)

O O O O O O E E O E E E E E E Acc E E E O E E E

C

PS

SG

OB

LB

PE

HI

MI

RS

■

■

■

■

■

■

■ ■ ■ ■ ■ ■

■

■ ■

■

■

■ ■

■

■

■

■

■

■

■

■

■

■

■

■

■

■ ■

■

■

■

■

■ ■ ■ ■ ■ ■

■

■ ■ ■

■

■

■ ■

■

(continued)

Table 4.5

(continued) Geographic range

Monogenea

Nematoda

Neolepidapedon magnatestis (adult) Neolepidapedon sp. (adult) Neolibouria georgiensis (adult) Stenakron glacialis (adult) Neopavlovskioides georgianus (adult) Neopavlovskioides dissostichi (adult) Pseudobenedenia dissostichi (adult) Pseudobenedeniella branchialis (adult) Anisakis Type 1 (larva) Anisakis Type 2 (larva) Anisakis simplex (larva) Anisakis spp. (larva) Acarophis nototheniae (adult) Capillaria sp. (adult) Contracaecum osculatum (larva) Contracaecum sp. (Nematode, larva) Dichelyne (Cucullanellus) fraseri (adult) Hysterothylacium sp. (adult/larva) Hysterothylacium aduncum (adult/larva) Hysterothylacium nototheniae (adult/larva) Pseudoterranova decipiens (adult)

Type

C

PS

SG

S O E E O O O S E E E E E E E E E E E S E

■

■

■

■

■

OB

LB

PE

■

■

HI

MI

RS ■ ■

■ ■

■

■

■

■

■

■

■

■

■

■

■ ■

■ ■

■ ■ ■

■

■

■

■

■

■

■

■

■

■

■

■

■

■

■

■

■ ■ ■

■

■

■

■

■

■

■

■

■

■

■

■

■

■

■

■

■

■

■ ■

■

■ ■

■

■ ■

■ ■

Cestoda

Acanthocephala

Copepoda

Clestobothrium crassiceps (larva) Grillotia erinaceus (adult) Hepatoxylon trichiuri (adult) Lacistorhynchus tenuis (larva) Phyllobothrium sp.(lava) Pseudophyllidean cercoides (larva) Tetraphyllidean cercoides (larva) Aspersentis megarhynchus (adult) Corynosoma arctocephali (larva) Corynosoma bullosum (larva) Corynosoma hamanni (larva) Corynosoma pseudohamanni (larva) Echinorhynchus longiproboscis (adult) Echinorhynchus petrotschenkoi (adult) Heteracanthocephalus dissostichi (adult) Heterosentis heteracanthus (adult) Metacanthocephalus rennicki (adult) Eubrachiella antarctica (adult)

Acc E E E E E E E E E E E E E O E S E

■

■

■

■

■

■

■

■

■

■

■ ■ ■

■

■

■

■

■ ■

■

■ ■

■

■

■ ■

■

■

■

■

■

■

■

■

■

■

■

■

■

■ ■ ■

■

■

■

■

■ ■ ■

■

■

■

■

■

C = Chile; PS = Patagonian Shelf; SG = South Georgia; OB = Ob Bank; LB = Lena Bank; PE = Prince Edward Islands; HI = Heard Island; MI = Macquarie Island; RS = Ross Sea. Types of parasite: O = oioxenic (D. eleginoides only); S = stenoxenic (Nototheniidae only); E = eurixenic (wider range); Acc = accidental infection.

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A

B

C 200 mm

100 mm

D

100 mm

E

F

50 mm

Figure 4.8 Parasites of Patagonian toothfish (Dissostichus eleginoides): (A) Echinorhynchus longiproboscis vagina and sphincter (Acanthocephala), (B) Corynosoma arctocephali proboscis (Acanthocephala), (C) Pseudoterranova decipiens (Nematoda), (D) Neopavlovskioides georgianus opisthohaptor (scale ¼ 40 mm; Monogenea), (E) Pseudobenedenia dissostichi opisthohaptor (scale ¼ 300 mm; Monogenea), (F) Grillotia erinaceus.

that this parasite was reported from South Georgia (Gaevskaya et al., 1990). Since merluccids are not reported from south of the APF, the only plausible explanations are that either a merluccid species strayed from the Patagonian Shelf or the D. eleginoides in question migrated from the Patagonian Shelf. The other accidental infection was a single Hirudinella ventricosa, a parasite of tunas, recovered from a toothfish on the Patagonian Shelf.

8.2. Geographical differences in parasite fauna Distinct geographic variability has been identified in the parasite fauna of Patagonian toothfish (Brickle et al., 2005; Gaevskaya et al., 1990; Parukhin and Lyadov, 1982). Gaevskaya et al. (1990) reviewed work conducted between 1972 and 1983 from the Patagonian Shelf region, South Georgia, and the Ob and Lena Banks. Thirty-eight parasite species were found in these fish, including myxosporideans (1 species), monogenean trematodes (3), cestodes (5), nematodes (8), acanthocephalans (7), copepods (1) and digenean trematodes (13). Gaevskaya et al. (1990) found that the characteristic feature of the parasite fauna of D. eleginoides was the predominance of helminths, with 92% of them having complex life cycles. They attributed this to the predatory behaviour of the host and examined the parasite fauna of prey species in the Patagonian area, to establish the origin of many of the

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incidental parasite species found in the host. They suggested that the cestode Clestobothrium crassiceps infects D. eleginoides through the ingestion of infected hake (Merluccius spp.), the trematode Gonocerca taeniata through southern blue whiting (Micromesistius australis australis), the trematodes Lepidapedon taeniata and Glomericirrus macrouri through grenadiers (Macrouridae), the trematodes Neolebouria georgiensus and Lecithaster australis from fish of the family Nototheniidae, and acanthocephalans of the genus Corynosoma through amphipods, isopods and fish of the family Nototheniidae. Many of these parasites were found sporadically with low intensities. In the Ob and Lena Banks, Patagonian toothfish appear to obtain the vast majority of their parasites from their principal prey species, Nototheniops larsoni (Gaevskaya et al., 1990), notably Hysterothylacium nototheniae, Cucullanellus fraseri and Corynosoma hammani together with other parasites characteristic of nototheniid fish. In the South Georgia area, where the main prey of toothfish are nototheniid fish, Gaevskaya et al. (1990) identified three trematodes (Neolebouria georgiensus, Lepidapedon antarcticus, Elytrophalloides oatesi), two nematodes (Ascarophis nototheniae and Cucullanellus fraseri) and two acanthocephalans (Echinorhynchus georgianus (¼E. petrotschenkoi) and Corynosoma bullosum). In general, the parasite fauna of D. eleginoides is determined to a significant degree by the ichthyoparasite fauna of the area it inhabits (Gaevskaya et al., 1990) and is richer in the west of its range than in the east, which indicates that the centre of origin of D. eleginoides was the Patagonian Shelf (Gaevskaya et al., 1990). Brickle et al. (2005) reported 32 parasite taxa, including 10 species being reported from D. eleginoides for the first time, from six locations around the sub-Antarctic (Shag Rocks, South Georgia, Prince Edward Island, Heard Island, Macquarie Island and the Ross Sea). Juvenile toothfish from the Shag Rocks area had a lower species diversity than samples collected from the other areas, with the exception of the Ross Sea, and Brickle et al. (2005) suggested that larger fish provide more internal and external space for infection and can support higher infection rates because they consume more infected prey. Brickle et al. (2005) found that some parasite species appeared to be specific to certain localities. The heaviest infections of larval tetraphyllideans occurred in immature fish around Shag Rocks, which may be related to their diet. Microsporidean species and Neolebouria antarctica infected adult toothfish only at South Georgia. Gaevskaya et al. (1990) also found Neolebouria georgiana (¼N. antarctica) around South Georgia and not around the Ob and Lena Banks. Stenakron sp. and Aspersentis megarhynchus were found only around Prince Edward Island at relatively high prevalences. Lecithophyllum champsocephali was restricted to Heard, Macquarie and Prince Edward Islands. Srensen’s similarity index illustrated that the parasite faunas of D. eleginoides were similar around the sub-Antarctic but showed

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greater differences with the Ross Sea. The greatest similarities were between Prince Edward, Heard and Macquarie Island.

8.3. Ontogenetic changes in parasite fauna Brickle et al. (2005) demonstrated that fish size (but not sex) was a significant determinant of the parasite fauna of juvenile Patagonian toothfish from Shag Rocks. There were significant decreases in the abundance and prevalence of tetraphyllidean (Cestoda) plerocercoides with increasing host length, whilst the larval acanthocephalan Corynosoma bullosum, the copepod Eubrachiella antartica, the monogenean Pseudobenedenia dissostichi and the nematode Hysterothylacium sp. increased. The reduction in tetraphyllideans was attributed to the reduction in the eupahasids, intermediate hosts for tetraphyllidean cestodes, in the toothfish diet. Increases in Corynosoma were likely due to the presence of intermediate amphipod hosts in the diet, whilst other increases were associated with increased potential attachment areas. The nematode Anisakis sp. did not show a significant increase in abundance with fish length but did show a pattern of increasing prevalence with increasing fish length. Anisakis spp. use euphausiids as their first intermediate hosts and squid and fish as second intermediate hosts. Their larvae can be passed onto other fish and squid without further moults; these squid and fish, therefore, act as paratenic hosts. Adult Anisakis spp. are parasites of pinnipeds and cetaceans. D. eleginoides will accumulate increasing numbers of Anisakis spp. by feeding on infected euphausiids and, later, by feeding on fish. The digenean Gonocerca physidis and the monogenean Neopavlovskioides georgianus did not show significant correlations of abundance with increasing host length. Although Neopavlovskioides georgianus showed a pattern of increasing prevalence with length, it is likely that older/larger toothfish are more suitable hosts for this parasite, and this is highlighted by the high range of intensities encountered in adult fish around the sub-Antarctic. In a detailed study of the parasites of the Falkand Islands’ toothfish population (11,362 parasites from 27 taxa), Brickle et al. (2006) found correlations between abundance of certain parasitic taxa and increasing host length. They also detected differences in the parasite community with season and depth of capture.

9. Physiology There is a considerable body of literature on the physiological adaptations that have evolved within the Nototheniidae (see Farrell and Steffensen, 2005; Kock, 1992 for reviews). The majority of these studies have focussed on species living at the highest and coldest latitudes where

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issues of freezing resistance and cold adaptation are the most acute. Studies on the physiology of sub-Antarctic and temperate notothens, including D. eleginoides, are more limited. However, aspects of the physiology of the congener D. mawsoni have been studied in greater detail allowing inferences to be made about many, but not all, physiological adaptations to the environment of D. eleginoides.

9.1. Buoyancy The majority of notothenioids are benthic and are heavier than sea water, with all species lacking a swim bladder (Eastman and Devries, 1982). However, in several species, including those of the genus Dissostichus, a range of adaptations and mechanisms have evolved to achieve neutral buoyancy, which conserves muscular energy and enables exploitation of the pelagic realm (Eastman and Sidell, 2002; Near et al., 2003; Oyarzun et al., 1988). To compensate for the lack of a swim bladder, Dissostichus spp., in common with other members of the clade of neutrally buoyant notothens, have much diminished mineralisation of the skeleton (Eastman, 1990). The ash content of the skeleton is only around 6% of the overall body weight. Cartilage is also substituted for bone in some areas such as the skull, pectoral girdle and caudal skeleton. Furthermore, the scales, which also contain heavy bone salts, have an unmineralised portion at their posterior margin (Eastman, 1990; Oyarzun et al., 1988). Large lipid deposits, consisting mainly of triglycerols and a small number of wax esters, also contribute to the buoyancy of D. eleginoides. These lipids have a specific gravity less than sea water (0.93) and therefore provide considerable static lift. In a study of specimens caught in the Chilean fishery, Oyarzun et al. (1988), found that white muscle from the dorsal areas of the body may contain >25% lipid and may rise considerably (>46%) in regions close to the centres of mass and buoyancy such as the origin of the pectoral fin and regions ventral to the pelvic fins. A thick layer of subcutaneous lipid may account for nearly 5% of the overall body weight but decreases towards the caudal zone. In Dissostichus species, lipid is stored in typical adipose cells and is therefore likely to be available for metabolism and hence act as an energy reserve. The loss of subcutaneous and intra-muscular lipid stores through metabolism without replacement can lead to an ‘axe handle’ morphology in D. mawsoni with animals having an associated low condition factor. Emaciation in these fish is most likely caused by the mobilisation of lipid reserves for migration and reproduction and may lead to fluctuations in buoyancy throughout the life of the animal (Fenaughty et al., 2008). The vertebrae of D. eleginoides are also known to contain lipid-filled cavities; however, it is not thought that the relatively small liver is an organ for buoyancy. The large pectoral fins of Dissostichus species are also thought to

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provide lift during forward propulsion assisting the ability to maintain position within the water column. Near et al. (2003) demonstrated that D. mawsoni experience a distinct ontogenetic change in buoyancy with juveniles heavier than water (nonbuoyant) and with adults becoming neutrally buoyant at a mean length of around 810 mm (TL). It is suggested that this could be associated with a change in habitat use, with juveniles exploiting benthic habitats and adults foraging within the entire water column over deeper water. Although directed studies have not been carried out, it is likely that such an ontogenetic change in buoyancy occurs in D. eleginoides associated with a marked change in distribution and trophic ecology with size/age (Belchier and Collins, 2008; Collins et al., 2007). However, in juvenile D. eleginoides, there is little evidence of benthic feeding, as juveniles are known to forage above the seabed and feed predominantly on pelagic and semi-pelagic fish species (Collins et al., 2007). The ontogenetic change in buoyancy may be a result of a change in prey availability with a need to conserve energy as toothfish move to greater depths where prey are more scarce.

9.2. Antifreeze glycopeptides The evolutionary development of antifreeze compounds has been essential for fish survival in many of the colder, higher latitude habitats of the Southern Ocean and has enabled the radiation of many notothenioids into these environments. A major physiological-biochemical adaptation has been the ability to synthesise macromolecular antifreeze substances for circulation in the body fluids. These antifreezes prevent notothenioids freezing when they come into direct contact with ice. However, D. eleginoides, which generally live in water temperatures of 2–11 C, lack antifreeze within their body fluids. The congener D. mawsoni possesses eight antifreeze glycopeptides (AFGPs), which are synthesised in the liver. Ghigliotti et al. (2007) noted that whilst D. mawsoni has high levels of circulatory AFGPs and an associated high level of AFGP genes, D. eleginoides has barely detectable AFGP sequences in its DNA. The authors suggest that despite their close phylogenetic kinship, the evolution of these species in disparate thermal regimes means that they show some distinct genetic and biological characteristics.

9.3. Vision Whilst there have been no studies to date on the optical physiology of D. eleginoides, an extensive comparative study of the ocular morphology of Antarctic notothenioids included a detailed examination of the morphology of the eye of D. mawsoni (Eastman, 1988). As the two congeners show much similarity in behaviour, morphology and ecology, it is likely that the

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adaptations to eye morphology observed in D. mawsoni are also present in D. eleginoides. In a study of the gross and microscopical anatomy of 18 species found in the sea ice zone in McMurdo Sound, Antarctica, D. mawsoni was shown to possess by far the lowest number of cones and the highest ratio of rods/cones in the retina of all species examined. The rod-dominated retina of Dissostichus is especially sensitive and well suited to respond to dim light levels at depth. The huge reduction in the number of cones is typical of deep-water species and serves to increase the sensitivity of the retina whilst reducing the visual acuity. It is not certain whether juvenile Dissostichus have the same eye morphology as adults or whether there is a change in eye development during the ontogenetic movement into deeper water. It is clear that adult toothfish can migrate vertically throughout the water column and have often been caught in relatively shallow depths (< 40 m) close to the shore. Collins et al. (1999, 2006) noted the sensitivity of toothfish to flashes and lights associated with underwater photography, including the ability to rapidly change colour, which clearly indicates a highly developed visual system.

10. Behaviour 10.1. Methods of studying behaviour Data on Patagonian toothfish behaviour come from three main sources, observations of captive animals, baited camera systems (conventional 35 mm and video) and from data-logging tags (Williams and Lamb, 2002) that have been attached to toothfish.

10.2. Baited camera systems Adult toothfish are readily attracted to bait, which makes them susceptible to baited longlines, but also enables them to be studied using baited cameras. Baited cameras have been used to investigate the abundance and behaviour of toothfish on the Patagonian Shelf (Collins et al., 1999) and on the shelf around South Georgia and Shag Rocks (Collins et al., 2006; Yau et al., 2002). The baited camera work was undertaken using autonomous lander systems (Priede and Bagley, 2000) that were dropped to the seafloor, ballasted with scrap metal and remained on the seafloor for periods of a few hours to weeks. Initial work on toothfish utilised a high-resolution 35 mm camera with powerful flash lights (200 J), but the data suggested that the lights discourage the toothfish from attending the bait, and the number of encounters was small (Collins et al., 1999; Yau et al., 2002). Later work utilised a low-light video camera and many more toothfish encounters were recorded (Collins et al., 2006; Yau et al., 2002).

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10.3. General behaviour patterns Toothfish appeared to be solitary and generally avoided one another. Any accidental contact between conspecifics resulted in sudden departure in different directions; similarly, unintended contact with the stone crabs (Lithodidae) also led to the rapid departure of the toothfish. Unlike other deep-water scavengers, toothfish did not accumulate at the bait, instead fish took a piece of bait and rapidly departed. No attempts were made to approach the bait when large numbers of stone crabs were clustered around it (Collins et al., 1999, 2006).

10.4. Swimming form and speeds Observations from baited video cameras (Collins et al., 2006) and captive animals (Brown, unpublished) show that labriform swimming (sculling with the large pectoral fins) is the principal means of locomotion in Patagonian toothfish. This gentle sculling with the pectoral fins produces relatively slow cruising speeds with a mean of 0.17 m s 1 or approximately 0.22 BL s 1 (Collins et al., 2006; Yau et al., 2002). The pectoral fins are also used in a gliding motion, particularly when toothfish swim close to the seafloor. Subcarangiform swimming (using the caudal trunk and fin) was also observed typically during turning or rapid acceleration. The maximum swimming speed recorded was 2.23 m s 1 for an individual of 0.72 cm TL (3.1 BL s 1) when the fish was in ‘panic flight’ (Yau et al., 2002). Using tagging data, Agnew et al. (2006a) reported an average distance moved by toothfish around South Georgia, at 10 km year 1 indicating little large-scale movements. D. mawsoni and D. eleginoides are comprised of a large percent of white muscle (51% of the body weight in D. mawsoni (Eastman and Devries, 1981)), resulting in most of their movement being dominated by small periods of rapid movements, and their reduced amount of red muscle, for slow sustained swimming, explains their strong site fidelity. From archival data storage tags deployed on toothfish around Heard Island (Williams and Lamb, 2002), toothfish of 710–820 mm TL were recorded making daily movements both upwards and downwards, of between 20 and 130 m (mainly <60 m). They concluded that this behaviour was in response to several factors, including environmental parameters (day and lunar phase), behaviour of prey species and bottom topography.

11. Fishery 11.1. History of the fishery Patagonian toothfish were first investigated as a fisheries resource in Chile in the 1950s (Guerrero and Arana, 2009; Moreno, 1991), with exploratory trawling limited to shallow depths. Toothfish were subsequently caught as a by-catch in

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trawl fisheries around Kerguelen Island, on the Patagonian Shelf and around South Georgia in the early 1980s. Development of longline gear capable of operating in deep water, targeting the large adult fish, led to the targeted fishery in Chilean waters, which began in the mid-1980s and quickly spread to other areas such as the Patagonian Shelf, South Georgia and Kerguelen. The high price commanded by toothfish (currently US$15 per kg) led to a rapid expansion in the catches, with new fishing grounds identified and targeted. The FAO reported that landings increased from less than 5000 tonnes in 1983 to 40,000 tonnes in 1992 (Fig. 4.9), although these figures include only the legal catches within the CCAMLR area and national territorial waters. At South Georgia (UK Overseas Territory), the longline fishery began with Soviet Union vessels in late 1988, which were later joined by Chilean, Bulgarian and Ukrainian vessels. In 1993/1994, CCAMLR designated the South Georgia region as a special area for protection and scientific study and undertook a depletion experiment to determine stock size. The depletion experiment was not successful (Parkes et al., 1996), but the presence of observers on board demonstrated the severity of the seabird by-catch problem and led to the fishery being limited to the winter months from 1998 (Agnew, 2004). Since 1999, the season has been restricted to the period from May 1st until August 31st, with opportunities for a season extension of 2 weeks into September and at the end of April for vessels that were fully compliant with management measures the previous year (CCAMLR, 2009). In recent years, the total allowable catch (TAC) in the South Georgia fishery has been around 50,000

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Figure 4.9 Annual landings of Patagonian toothfish (Dissostichus eleginoides) from different regions. Data based on FAO figures. Note that this only includes reported landings.

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3000 tonnes. A small fishery also operates around the northern area of the South Sandwich Islands (Roberts and Agnew, 2008), with the TAC currently 41 tonnes (CCAMLR, 2009). In the southern Indian Ocean, a targeted trawl fishery began on the western Kerguelen shelf (French exclusive economic zone (EEZ)) in 1984/ 1985, when former USSR trawlers found and began to exploit large concentrations of toothfish (Lord et al., 2006). Longlining started in the Kerguelen fishery in 1991, and since 2001/2002, the fishery has been exclusively longliners (Lord et al., 2006). The Kerguelen fishery operates year round, although catch rates are lower in winter, and since 1994, the legal catches have been around 5000 tonnes per year. The Heard and McDonald Islands (HIMI) shelf (Australian EEZ) is contiguous with the Kerguelen shelf and is probably the same population of toothfish. Apart from some Polish research fishing in the 1970s, there was little known exploitation on the HIMI shelf (Williams and de la Mare, 1995) until trawl fisheries developed for toothfish and icefish in 1996. The fishery was opened up to longlining in 2002/2003 and is currently exploited by both trawlers and longliners, with a catch limit of around 2500 tonnes. At Crozet Island (French EEZ), 900 miles west of the Kerguelen Plateau, the longline fishery began in 1996/1997, with reported catches of up to 1200 tonnes, but the fishery suffered from considerable illegal fishing activity from 1995 to 2002. Current legitimate catches are less than 1000 tonnes per year. The Prince Edward Islands (South African EEZ) fishery, which spans the edge of the CCAMLR zone, began in 1996/1997 as a seasonal fishery (May 1st–August 31st), but the fishery suffered from high levels of illegal catches, with an estimated 21,000 tonnes illegally taken in 1997 (Brandao et al., 2002). In an attempt to counter the illegal fishing, the fishery was opened year round in 1998, in the hope that the presence of legal operators would deter the illegal vessels (Brandao et al., 2002), but catch rates and legal catches declined sharply. The TAC in 2002/2003 was set at 400 tonnes and recent estimates of IUU are zero, with legal catches of around 200 tonnes per year. Elsewhere in CCAMLR waters, toothfish fishing has occurred on isolated banks and seamounts, such as Banzarre Bank and the Ob and Lena Seamounts. The fisheries in these areas were rapidly overexploited and stocks remain depleted (McKinlay et al., 2008). The Macquarie Island (Australian EEZ) fishery began in late 1994 in the Aurora Trough and spread to the Macquarie Ridge 2 years later when toothfish aggregations were detected. Initially, catches were over 1000 tonnes per year, but the fishery was closed (except for research fishing) from 1999 to 2003, when it resumed with a reduced TAC (Phillips et al., 2009). Although trawling has been the main method of fishing since 1994, a 3-year longline trial began in August 2007, primarily on the Macquarie Ridge north and south of the island. Current quotas are around 300 tonnes

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from the Aurora Ridge, with 100 tonnes from Macquarie Ridge (Phillips et al., 2009). Toothfish were initially taken as by-catch in trawl fisheries on the Patagonian Shelf, with longline fisheries subsequently established in Argentine and Falkland Island waters. The Argentinian fishery started in the 1990s with the highest catches in 1995 (18,225 tonnes); however, catches have declined since then (Wohler, unpublished data). Based on advice from the National Institute of Fishing Research and Development (INIDEP), new management practices have been enforced by the Fishing Authority since 2000. These include catch documentation scheme (CDS), larger hook sizes, minimum fish size, minimum fishing depths and establishment of a protected juvenile area. The Falklands longline fishery began in 1992 as an experimental fishery and became an established fishery in 1994 (Laptikhovsky and Brickle, 2005). Catches peaked in the first year of the directed fishery (2733 tonnes in 1994) and subsequently stabilised to a level of 1200–1800 tonnes (currently, 1200 tonnes). The Chilean fishery is divided into two zones. The north zone, between Chile’s northern limit (18 210 S) and 47 S, is reserved exclusively for artisanal fishing, whereas in the south zone (47 S to 57 S), the resource is exploited through industrial fishing activities (Guerrero and Arana, 2009). The only gear permitted is the demersal longline, although pots have been trialled (Guerrero and Arana, 2009). The Chilean fishery has also been instrumental in developing new gears, such as the trotline and cachalotera system (Moreno et al., 2006, 2008, see below). Areas in the high seas (outside of national jurisdiction) have also been exploited, notably the Scotia Ridge between Shag Rocks and the Falklands. In these areas, catches have not been limited and stocks quickly depleted.

11.2. Fishing methods and gears The principal method of catching adult toothfish is demersal longlining (see Figs. 4.10 and 4.11), in which a longline of baited hooks are deployed close to the seafloor at depths up to 2000 m. Surface buoys indicate the presence of lines, and vessels typically recover lines after a ‘soak-time’ of 24–48 h. Bait is usually squid or sardine. Longline vessels are generally small vessels (30–80 m; Fig. 4.10). There are three principal types of longlining: the Spanish (double-line) system, autoline and more recently, the trotline system (Fig. 4.11), which often includes cetacean exclusion nets (umbrellas or cachaloteras). In all cases, lines are deployed from the stern of the vessel and recovered via a hauling hatch on the starboard side. The Spanish or double-line system (Fig. 4.11A) uses a strong main- or mother-line attached at each end to an anchor and buoy line. The fishing line is attached to the main line by a series of connecting ropes. The hooks

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A

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Figure 4.10 The fishery for Patagonian toothfish (Dissostichus eleginoides): (A) photograph of an autoliner; (B) aerial photograph of a Spanish double-line longliner, note the hauling area on the starboard side; (C) toothfish being gaffed; (D) circle-type (left) and J-type hooks used in the South Georgia fishery.

are attached to the fishing line with monofilament snoods, with each section of the fishing line comprising around 25 hooks, with around 7000 hooks per line and with vessels deploying 2–3 lines per day. Weights (6–10 kg) are attached between each section of hooks to sink the line and keep it on the seafloor. The hooks are baited by hand, which is relatively labour intensive.

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B

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Figure 4.11 Illustration of the three methods of longlining: (A) Spanish double-line system, (B) autoline system and (C) trotline with net sleeves.

The autoline system (Fig. 4.11B) has a single weighted line (polypropylene line with integrated weight, around 50 gm 1), from which hooks are attached via swivels and multifilament snoods. The line is divided into magazines, each consisting of 1000–1500 hooks, and although the length of lines and hence the number of hooks varies, typically an autoliner will be able to deploy 30,000 baited hooks per day. Hooks on auto-lines are automatically baited. Trotlines (Fig. 4.11C) were initially developed in the Chilean artisanal fishery (Moreno et al., 2008) and are a modification of the Spanish system, in which the hook line is replaced by a series of vertical branch lines, placed at 40 m intervals. Each of the vertical branch lines supports clumps of 8–20 short hook lines and, at its extremity, a bag of weights. In the Falklands, there is one clump of 8 hooks per branch line with a single 6 kg weight at the bottom (Brown et al., 2010). The clumping of the hooks near the weights allows the baited hooks to sink rapidly to avoid seabirds, but the method also allows for the use of net sleeves, umbrellas or cachaloteras to reduce depredation by whales (see below). Each branch line can have a buoyant net or sleeve attached that is able slide up and down the line.

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During the set, this sleeve remains at the upper end of the branch line, but when the thick main line is hauled, the movement of the vertical branch line through the water causes the sleeve to slide down the line covering the hooks and any captured fish. Pots were initially trialled as a method of reducing seabird mortality (see below) and also to stop depredation by sperm and killer whales. The traps (Fig. 4.12) used are typically a truncated conical shape, with a circular base of around 1.5 m, an upper part of 0.9 m diameter and 0.9 m high and made of steel and mesh panels (120 mm for the body and 38 mm for the mouth). Pot fishing is used in the fishery on the Patagonian Shelf and southern Chile, but has not proved successful at South Georgia, where catch rates were substantially lower than longlines (Agnew et al., 2001; Guerrero and Arana, 2009). There has been considerable regional variability in the success of different fishing methods, which is probably a consequence of bottom topography, current speeds and, possibly, toothfish behaviour. The autoline system has not been successful in the Falklands, but works well in other areas such as South Georgia and Heard Island. With the trotline system, catches (g/hook) are usually less at high toothfish density, probably because it is rare for each clump of hooks (8–20) to catch more than two fish. In the Falklands the catch per unit effort (CPUE) has been reported to be up to ten times higher with umbrella lines than Spanish longlines (in the same area); however, this is not a linear relationship, with Spanish lines performing better in areas of high local abundance of toothfish (Brown et al., 2010). The Falklands fishery initially used the Spanish system, but has recently switched to using trotlines with cachaloteras.

Figure 4.12 A typical pot used to catch toothfish in the Falkland Islands Patagonian toothfish (Dissostichus eleginoides) fishery.

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Gill nets have also been used to catch toothfish, but are banned throughout CCAMLR waters, as they have the potential to ‘ghost fish’ if the gear is not recovered. Gill nets are, however, used by illegal, unreported and unregulated (IUU) vessels (see below) that fish in the Southern Ocean. Bottom trawling is used to target toothfish on the shelf-slope at Heard Island. However, bottom-trawling is less discriminate than longlining, with a greater by-catch and is also likely to cause considerably more damage to seafloor habitats. Different types and sizes of hooks have been used to catch toothfish. The commonest types are the ‘circle’ and ‘j’ hooks (Fig. 4.11D). The type and size of hook can influence the size and quantity of both target and nontarget species. Bait is usually sardine and/or squid. Sardine, being an oily fish, produce good odour; however, as they have softer flesh than squid, the sardine generally do not last as long on the hooks, as they are consumed by amphipods. A combination of the two types of bait is considered to produce the best catch rates by many fishermen.

11.3. Illegal, unreported and unregulated (IUU) fishing IUU fishing has been a major problem in toothfish fisheries throughout the southern hemisphere (Baird, 2006; Lack, 2008; Lack and Sant, 2001). The high value of the catch and difficulties of enforcing regulations in such a large and inhospitable ocean led to the development of significant illegal fishing in the early 1990s. This undoubtedly had a detrimental effect on the toothfish stocks and, since IUU vessels are unlikely to follow mitigation measures, on by-catch of seabirds (as described later) and non-target species. In CCAMLR waters, IUU fishing started in 1992 around South Georgia (Agnew and Kirkwood, 2005). Following a series of arrests by U.K. authorities in that area, IUU operations moved to the Indian Ocean sector in 1996 and 1997 after the identification of large areas there where toothfish could potentially be caught. Since then, most activity has been concentrated on fishing grounds around Prince Edward and Marion Islands (South Africa), Crozet and Kerguelen Islands (France), Heard Island (Australia) and on oceanic banks in high seas areas such as the Banzare Bank. CCAMLR and its member states have introduced a number of measures designed to reduce the level of IUU. These include the CDS (Agnew, 2000), satellite-derived tamperproof vessel monitoring systems (VMS) and rigorous patrolling, with high-profile arrests and prosecutions. Vessels fishing in CCAMLR waters must also carry an international observer and provide regular catch reports. The CDS, which was adopted in 2000, applies to both species of Dissostichus and is designed to demonstrate if toothfish were caught in compliance with conservation measures by tracking landings and trade. If a consignment of toothfish does not have the necessary documentation, it is assumed to be IUU. Under the VMS, every

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vessel licensed by CCAMLR members to fish in the Convention Area is required to have a VMS, monitored by the flag State and forwarded to the CCAMLR Secretariat. This information can then be used to corroborate toothfish landings in the CDS. Some CCAMLR member states have taken additional steps in the fisheries that they manage in their territory. For instance, in the South Georgia fishery, which has been certified as sustainably managed by the Marine Stewardship Council, all toothfish products are weighed and verified at the end of the season. This ensures that licensed vessels do not exceed their allocated quota. CCAMLR estimate the amount of toothfish taken by IUU vessels and include this data in stock assessments (CCAMLR, 2009), but Lack (2008) analysed trade data and suggested that CCAMLR may underestimate IUU catches by up to 50%. In 2002, a proposal to list toothfish on Appendix II of the Convention on International Trade in Endangered Species (CITES) was subsequently withdrawn, recognising that the CCAMLR CDS already monitors trade in toothfish. Not all Patagonian toothfish fisheries are in the CCAMLR area (e.g. Chile, Argentina, Falklands, Crozet, Macquarie Island), and in these areas, domestic legislation and enforcement are relied upon to address IUU fishing.

11.4. By-catch issues Although more selective than trawling, longlining still generates a by-catch. The principal by-catch species are grenadier (Macrouridae), morid cods such as Antimora rostrata (Moridae) and skates (Rajidae). By-catch levels vary between regions and depths, and also between fishing methods and with hook type and size and bait. At South Georgia, the by-catch of grenadiers is considerably greater with the autoline system than the Spanish double-line system. Species that possess a swim bladder (e.g. macrouids, morids) suffer severe decompression trauma when brought to the surface and will not survive if returned. Survival of species that lack a swim bladder can be high and in CCAMLR fisheries vessels are required to release (some with tags) all skate that are in good condition when caught. Longlines also capture and damage benthic invertebrates and the need to protect Vulnerable Marine Ecosystems (VMEs), such as those associated with cold-water corals, is a high priority within CCAMLR and other fisheries (Martin-Smith, 2009; Sharp et al., 2009).

11.5. Interactions with seabirds Interactions with seabirds are a problem with many longline fisheries (Brothers, 1991). Scavenging seabirds, including many albatross and petrel species, are attracted to baited hooks when they are deployed and, when they dive for the bait, they become hooked, sink with the lines and drown.

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This has been a major problem within the majority of Patagonian toothfish fisheries in the Southern Ocean (Ashford et al., 1994, 1995; Delord et al., 2005, 2010; Moreno et al., 1996; Nel et al., 2002; Reid et al., 2004; Williams and Capdeville, 1996), many of which operate in important foraging areas for threatened albatross and petrel species (Fig. 4.13). In the late 1980s, large numbers of seabirds were killed, but not quantified. 6000 South Georgia 5000 1000 500 0

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In 1992, CCAMLR responded to the seabird mortality issue and adopted a suite of mitigation measures, including the use of streamer lines, night setting and controls on offal discharge. The ad hoc working group on incidental mortality associated with longline fishing (IMALF) was then established in 1993 to monitor the problem and develop further mitigation. The CCAMLR Scientific Observer Scheme, which was also adopted in 1992, ensured 100% observer coverage on toothfish vessels, to monitor mitigation and by-catch. Additional mitigation measures included lineweighting schemes (Agnew et al., 2000; Robertson et al., 2000, 2007; Wienecke and Robertson, 2004) to ensure that hooks sink rapidly, the use of streamer or Tori lines during shooting (Fig. 4.14A) and the ‘Brickle Curtain’ (seven weighted vertically hung lines which form a curtain; Fig. 4.14B) to keep birds from the hauling area. A

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Figure 4.14 Seabird mitigation methods in action on a longliner; (A) streamer or Tori lines; (B) Brickle curtain around hauling area.

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Further restrictions were introduced on fisheries under CCAMLR management, including the closure of the South Georgia fishery during the summer months, when species such as white-chinned petrel are particularly susceptible to capture. The mitigation measures implemented by CCAMLR had the desired effect, with the bird by-catch now close to zero (Fig. 4.13) in areas that CCAMLR is the competent authority (CCAMLR, 2009). Although the EEZ of the French territories of Kerguelen and Crozet fall in or partially in the CCAMLR zone, the French authorities manage the fisheries outside of the CCAMLR framework, and the reduction in seabird mortality has been considerably slower, with considerable numbers of birds still killed in the Kerguelen and Crozet fisheries (Delord et al., 2010). The main species effected are white-chinned petrels (Procellaria aequinoctialis) and grey petrels (Procellaria cinerea), with between 7766 and 10,542 birds estimated to have been killed between September 2003 and August 2006 (Delord et al., 2010). This level of mortality has now been reduced as some of the CCAMLR mitigation measures have been adopted (CCAMLR, 2009; Fig. 4.13). The mitigation measures developed by CCAMLR have gradually been introduced in national EEZs. In the early days of the Falkland Islands fishery, large numbers of seabirds were killed, but mitigation has been introduced, and by 2001, a suite of mitigation was in place and by-catch was reduced (Otley et al., 2007). However, 134 seabirds were estimated to have been killed in 2003/2004 (Otley et al., 2007). With the introduction of the umbrella system, correct line-weighting regimes and the use of well-designed streamer lines and the ‘Brickle Curtain’, seabird mortality was eliminated during the 2007/2008 and 2008/2009 seasons (Brown et al., 2010). In the Chilean fishery, the introduction of trotlines has dramatically reduced the number of seabirds killed (Moreno et al., 2006, 2008). In 2002, 1542 birds were killed, compared to zero in 2006. The difference is attributed to the greater sinking rate of the trotline system, in which the hooks are clumped with weights. A further problem is that of hook ingestion by scavenging birds, particularly wandering albatross, which occurs when hooks are not removed from discarded by-catch and offal (Phillips et al., 2010). The discarding of baited hooks or of hooks in by-catch species is prohibited in many fisheries. However the increased use of trotlines has been implicated as the reason for a recent increase in hooks in wandering albatross regurgitates (Phillips et al., 2010), with a greater number being cut off and discarded when they become tangled with the net-sleeves during hauling.

11.6. Interactions with marine mammals Interactions between marine mammals and fisheries can take the form of competition for resources, incidental by-catch and depredation of fish from fishing gear. Incidental mortality is not a significant problem in Patagonian

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toothfish fisheries, although there have been very occasional reports of sperm whales drowning following entanglement in Spanish-double line gear (CCAMLR, 2009). Competition has been considered in the trophic ecology section, so here, the focus is on the issue of depredation. Marine mammal depredation of line caught fish is a problem throughout the world (Visser, 2000; Yano and Dahlheim, 1995) but has become particularly acute in the high value Patagonian toothfish fishery in recent years. Depredation by killer whales (Orcinus orca) and sperm whales (Physeter macrocephalus) was first reported by observers at South Georgia in 1994 (Ashford et al., 1996) but has since been reported in other fisheries (Nolan et al., 2000), and recent years have seen the problem increase (Ashford et al., 1996; Kock et al., 2006; Nolan et al., 2000; Purves et al., 2004). Depredation is apparent from heads and lips that are left on the line by the cetaceans and, at times, the majority of the catch on a line could be lost to depredation. Depredation from sperm whales and killer whales are rather different. Killer whales operate in pods of 3–15 animals, whilst sperm whales are often solitary. Sperm whales are natural predators of toothfish and can take toothfish from lines at depth, whereas killer whales only dive to 300 m and tend to strip fish from lines close to the surface (Fig. 4.15). Quantifying the lost catch is not straightforward. One approach is to look at catch rates in the presence and absence of both killer and sperm whales. Since sperm whales are natural predators on toothfish, they tend to be abundant in areas where toothfish are abundant, and in some areas, there is no evidence of a reduction in catch rates in the presence of sperm whales (Brown et al., 2010; Hucke-Gaete et al., 2004; Purves et al., 2004).

Figure 4.15 Killer whale (Orcinus orca) with a Patagonian toothfish (Dissostichus eleginoides) depredated from a line. Photo-courtesy of Manuel Sampedro Garcia (FV CFL Gambler).

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However, when killer whales are present, catches can be greatly reduced, and if the vessel does not stop hauling, whole lines may be stripped. In Crozet, the CPUE dropped 22% in the presence of killer whales, 12% in the presence of sperm whales and 42.5% when both were present (Roche et al., 2007). Overall, the level of depredation at Kerguelen (3%) is considerably lower than at Crozet (33%), which is attributed to the lower abundance of killer whales at Kerguelen (Roche et al., 2007). Fishing vessels have responded to the cetacean problem in a number of ways. Fishing with pots prevents both sperm and killer whales from taking the catch, but pot-catch rates are considerably lower than those of longlines. The use of net sleeves or cachaloteras is effective against sperm whales; however, killer whales are learning to bypass the nets and there is evidence of predation by killer whales on umbrella lines (Brown et al., in press). A common practice in response to the presence of killer whales is to stop hauling and buoy the line off, so that the fish are beyond the diving range of the orcas. The vessel will then move to another location at speed and attempt to lose the killer whales, or pass them to another vessel. Acoustic deterrents have been used to mediate the problem of killer whales ( Jefferson et al., 1996; Morton and Symonds, 2002), but whales can quickly become accustomed to such devices. Antarctic fur seals have also been implicated in depredation at Kerguelen (Roche et al., 2007) and occasionally at South Georgia. At South Georgia, depredation by fur seals increased during the 2009 season, when the abundance of Antarctic krill, the primary prey of fur seals, was exceptionally low.

12. Stock Assessment A number of methods, have been used to carry out stock assessments for Patagonian toothfish fisheries around the Southern Ocean, the Patagonian Shelf and Chilean waters. Initially, there were insufficient data to assess the fisheries using conventional stock assessment techniques. As Patagonian toothfish are long lived and slow growing, a reasonable catch and effort dataset combined with a suite of life history parameters is required for any age or length-based assessment methods, and it takes several years to build up these datasets. Early attempts at assessing fisheries used Leslie stock depletion models. Parkes et al. (1996) used the Leslie depletion model to examine local patterns in CPUE of toothfish in longline fisheries around South Georgia and off the Pacific coasts of Chile. They found that 54 out of 107 CPUE series showed a negative trend with cumulative catch, which was less than would be expected by chance according to binomial theory; however, only 18 of these datasets showed a significant negative trend. They concluded that depletion models were not a suitable method for estimating local abundance, and the authors

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cited fish behaviour and the actions of fishermen as complicating factors that made the use of regression models inappropriate. In the same year, des Clers et al. (1996) applied a modified DeLury depletion model to toothfish CPUE in the Falkland Islands longline fishery but also failed to produce reliable results, concluding that the model’s assumptions were not valid and that there was a likely extensive migratory behaviour in the Patagonian toothfish. The rapid expansion of the toothfish fishery in the Southern Ocean in the late 1980s and early 90s was a major concern, which was compounded by the lack of data for traditional stock assessment methods. Also, adult populations were inaccessible to trawl surveys and therefore could not be estimated by traditional swept area methods (Constable et al., 2000). To take into account this lack of data and the fact that the fishery was already in progress, CCAMLR developed two approaches for management, a generalised yield model (GYM) for stock assessment (Constable and de la Mare, 1996) and regulations restricting the development of new fisheries. The GYM was built on the approaches already developed for a krill yield model. As data from the longline fishery were insufficient and fishery independent surveys could not access the adult population, there was no estimate of initial biomass (B0). These problems were overcome by using absolute estimates of recruits (using CMIX, de al Mare, 1994) and projecting those forward using simulations. This allowed for recorded catches to be discounted from the population, and consequently, a long-term yield could be assessed in tonnes rather than as a proportion of B0. In South Georgia, a relatively large number of bottom trawl survey data were available allowing the estimation of recruitment of 4-yearold toothfish. This approach was used to assess the South Georgia stock from 1995 to 2004, when it was replaced by an integrated approach using markrecapture data. Mark and recapture methods have been used to assess toothfish population sizes in Macquarie Island (Tuck et al., 2003) and South Georgia (Agnew et al., 2006a) fisheries. Essentially, exact time of release and recapture data are used in a stock assessment model that unifies a semi-parametric approach with the Petersen method. A maximum likelihood approach is used to estimate the available abundance of toothfish (fishable abundance, which is different to total or spawning biomass). An attempt at estimating adult toothfish densities using baited cameras was conducted by Yau et al. (2001) in the Falkland Islands and South Georgia. They used an autonomous camera system (see Section 10) and attempted to calculate toothfish density based on mean first arrival time, as demonstrated by Priede and Merrett (1996). Yau et al. (2001) data gave estimates of 0.4 and 1.32 toothfish per km2 for South Georgia and the Falkland Islands, respectively. However, the behaviour of the toothfish differed from other scavenging species to which the method had previously been applied, leaving considerable uncertainty about the results.

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Since 2004, many of the major fisheries for Dissostichus spp. in the CCAMLR convention area have used fully integrated age-structured stock assessments with differing complexities and features that can deal with a large variety of age- and length-structured data. CASAL (Bull et al., 2005) (Cþþ algorithmic stock assessment laboratory) is an integrated assessment method that can be used to implement either an age- or length-structured model, with options to structure the population by sex, maturity and/or growth path. CASAL can be used for a single stock or fishery or for multiple stocks, areas and fishing methods. The data can be taken from a number of different sources, including catch-at-age or catch-at-size data from commercial fishing, survey and other biomass indices, survey catch-at-age or catch-at-size data and tag release and recapture data. Estimations can be by least squares, maximum likelihood or Bayesian methods. CASAL can generate point estimates of the parameters of interest and can calculate likelihood or posterior profiles, generating Bayesian posterior distributions using Monte Carlo Markov chain methodologies. It can also project stock status into the future using deterministic or stochastic recruitment and can generate a number of yield measures commonly used in stock assessments. CASAL is now used in the assessment of both the Antarctic (Dunn and Hanchet, 2007; Dunn et al., 2004) and Patagonian (Agnew et al., 2007; Candy and Constable, 2008; Hillary et al., 2006) toothfish. This method differs from the GYM in that many parameters can be estimated within the model, including B0, rather than having to estimate the parameters individually. CCAMLR advocates an ecosystem approach to managing fisheries and all CCAMLR toothfish assessments are highly precautionary. Within CASAL, the historic stock dynamics are projected 35 years into the future under a variety of plausible scenarios. A constant catch projection allows the calculation of a long–term yield that satisfies the CCAMLR decision rules. The yield is chosen such that the probability of spawning stock biomass (SSB) dropping below 20% of its median pre-exploitation level during the 35-year projection is not greater than 10% and that the median escapement in the SSB at the end of the projection is not less than 50%. Age-structured production models (ASPMs) have been used for the assessment of a number of marine resources, including for Patagonian toothfish stocks. Its first application to toothfish was by Gasiukov and Dorovskikh (2000). ASPMs have an advantage over biomass-based (aggregated) production models because they allow for a delay in the reduction of spawning stock biomass (SSB) and thus year class strength as a result of fishing (Brandao et al., 2002). Brandao et al. (2002) used a simple ASPM for the assessment of the toothfish resource within the Prince Edward Islands EEZ, which provided a robust indication that the SSB had been depleted to a few percent of its original level, and their projections suggested that the annual TAC should be reduced to 400 tonnes.

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Payne et al. (2005) used an ASPM based on Brandao et al.’s (2002) work to assess the Patagonian toothfish population in the Falkland Islands. They used two models, one with a Beverton-Holt stock recruitment relationship and another using trawler CPUE to estimate yearly recruitment. The models were fitted to standardised longliner CPUE and catch-at-length data. The two models produced estimates showing similar declines in biomass as the fishery progressed, but the initial and final biomasses varied slightly between models. The models provided estimates of the current biomass at between 38% and 46% of its pre-exploitation level and maximum sustainable yields (MSY) of between 912 and 3000 tonnes. There was a poor fit to CPUE between 1994 and 1996 which Payne et al. (2005) attributed to IUU catches or changes in catchability and/or mortality. During this time (mid 90s), there was considerable IUU activity in the SW Atlantic, and when their model was adjusted to allow an estimated level of extra catch, the fit improved and 5000 tonnes of extra catch was estimated. The ASPM was adapted further by Paya and Brickle (2008) to include updated von Bertalanffy and natural mortality parameters. Further developments in the Paya and Brickle (2008) model included a model to allow both longline and trotline (with cachalotera) CPUE series to be used.

13. Concluding Remarks The initial rapid development of Patagonian toothfish fisheries in the Southern Oceans took place without the requisite knowledge of the biology of the target species or any assessment of the ecosystem impacts of the fisheries. Sustainable management of these fisheries has also been hampered by their remote locations, which have limited both research opportunities and surveillance. Consequently in many areas stocks were rapidly depleted and large numbers of seabirds killed. Knowledge of the biology and ecology of toothfish has expanded considerably in the last decade, with significant advances in stock discrimination; assessments of population size through tagging; growth rates and in trophic ecology. Significant gaps still remain in our knowledge of toothfish. There is still uncertainty about the distribution of Patagonian toothfish, with many parts of the Southern Ocean remaining unexplored. Whilst genetic and other studies have revealed segregation of stocks there are still important questions about linkages between populations in proximate locations. The larval phase of toothfish is poorly known, and whilst links between recruitment and oceanography have been identified the functional relationship is not established. A better knowledge of the larval phase will be key to understanding the potential consequences of climate change, since change is more likely to be manifested in surface temperatures and currents than in the deeper water occupied by adults.

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Fisheries have adapted rapidly and methodology radically changed to limit the negative effects on the ecosystem, but further changes are likely to counter the depredation problem. Finally, stock assessments will continue to be refined by increased knowledge of population parameters and improved estimates of stock size from methods such as tagging. Continued vigilant management and surveillance is essential for the long-term sustainability of the valuable Patagonian toothfish fisheries.

ACKNOWLEDGEMENTS This review was stimulated by discussion at the CCAMLR Working Group on Fish Stock Assessment and benefited from valuable discussions in this forum. In particular the authors wish to thank recent convenors Inigo Everson, Stuart Hanchet and Chris Jones and Karl-Hermann Kock for their encouragement. Thanks to Peter Fretwell in the BAS mapping section for producing Figure 2 and to Jack Fenaughty and Manuel Sampedro Garcia for allowing us to use their photographs. Thanks to the Falkland Islands Fisheries Department for supporting this work.

REFERENCES Abe, T., and Iwami, T. (1989). Notes on fishes from the stomachs of whales taken in the Antarctic II. On Dissostichus and Ceratius, with an appendix (Japanese names of important Antarctic fishes). Proc. NIPR Symp. Polar Biol. 2, 78–82. Abellan, L. J. L. (2005). Patagonian toothfish in international waters of the southwest Indian Ocean (Statistical Area 51). CCAMLR Sci. 12, 207–214. Adams, N. J., and Klages, N. T. (1989). Temporal variation in the diet of the gentoo penguin Pygoscelis papua at Sub-Antarctic Marion Island. Colonial Waterbirds 12, 30–36. Agnew, D. J. (2000). The illegal and unregulated fishery for toothfish in the Southern Ocean, and the CCAMLR catch documentation scheme. Marine Policy 24, 361–374. Agnew, D. J. (2004). Fishing South: History and Management of South Georgia Fisheries. The Penna Press, St Albans, 128pp. Agnew, D. A., and Kirkwood, G. P. (2005). A statistical method for estimating the level of IUU fishing: Application to CCAMLR sub-area 48.3. CCAMLR Sci. 12, 119–141. Agnew, D., Heaps, L., Jones, C., Watson, A., Berkieta, K., and Pearce, J. (1999). Depth distribution and spawning pattern of Dissostichus eleginoides at South Georgia. CCAMLR Sci. 6, 19–36. Agnew, D. J., Black, A. D., Croxall, J. P., and Parkes, G. B. (2000). Experimental evaluation of the effectiveness of weighting regimes in reducing seabird by-catch in the longline toothfish fishery around South Georgia. CCAMLR Sci. 7, 119–131. Agnew, D. J., Daw, T. M., Pilling, G. M., and Purves, M. G. (2001). Fishing for toothfish using pots: Results of trials undertaken around South Georgia, March–May 2000. CCAMLR Sci. 8, 93–105. Agnew, D. J., Clark, J. M., McCarthy, P. A., Unwin, M., Ward, M., Jones, L., Breedt, G., Du Plessis, S., Van Heerdon, J., and Moreno, G. (2006a). A study of Patagonian toothfish (Dissostichus eleginoides) post tagging survivorship in Subarea 48.3. CCAMLR Sci. 13, 279–289. Agnew, D. J., Kirkwood, G. P., Pearce, J., and Clark, J. (2006b). Investigation of bias in the markrecapture estimate of toothfish population size at South Georgia. CCAMLR Sci. 13, 47–63.

290

Martin A. Collins et al.

Agnew, D. A., Hillary, R. M., and Pearce, J. (2007). Preliminary stock assessment of the South Georgia toothfish stock. CCAMLR WG-FSA 07/29. Aguayo, M., and Cid, L. (1991). Recopilacio´n, proceso y ana´lisis de los antecedentes biolo´gico-pesqueros en la pesca exploratoria de bacalao de profundidad realizada por el B/P /Friosur V/. Instituto Fomento Pesquero, Chile. Informe Interno, 63 pp. Aguayo, M. (1992). Preliminary analysis of the growth of Dissostichus eleginoides from the austral zone of Chile and South Georgia. CCAMLR WG-FSA 92/30. Ainley, D., and Siniff, D. B. (2009). The importance of Antarctic toothfish as prey of Weddell seals in the Ross Sea. Antarct. Sci. 21, 317–327. Andrews, A. H., Brooks, C. M., Ashford, J. R., Krusic-Golub, K., Duhamel, G., Belchier, M., Lundstrom, C., and Cailliet, G. M. (2010). Lead-radium dating of Patagonian toothfish (Dissostichus eleginoides) reveals spatial variation in ageing bias on the Kerguelen Plateau. Mar. Freshw. Res. (in press). Appleyard, S. A., Ward, R. D., and Williams, R. (2002). Population structure of the Patagonian toothfish around Heard, McDonald and Macquarie Islands. Antarct. Sci. 14, 364–373. Appleyard, S. A., Williams, R., and Ward, R. D. (2004). Population genetic structure of Patagonian toothfish in the West Indian Ocean sector of the Southern Ocean. CCAMLR Sci. 11, 21–32. Arana, P. (2009). Reproductive aspects of the Patagonian toothfish (Dissostichus eleginoides) off southern Chile. Latin Am. J. Aqua. Res. 37, 381–394. Arana, P. M., and Vega, R. (1999). Exploratory fishing for Dissostichus spp in the Antarctic region (sub-Areas 48.1, 48.2 and 88.3). CCAMLR Sci. 6, 1–17. Arkhipkin, A., Brickle, P., and Laptikhovsky, V. (2003). Variation in the diet of the Patagonian toothfish with size, depth and season around the Falkland Islands. J. Fish Biol. 63, 428–441. Ashford, J., and Jones, C. (2007). Oxygen and carbon stable isotopes in otoliths record spatial isolation of Patagonian toothfish (Dissostichus eleginoides). Geochim. Cosmochim. Acta 71, 87–94. Ashford, J. R., Croxall, J. P., Rubilar, P. S., and Moreno, C. A. (1994). Seabird interactions with long-lining operations for Dissostichus eleginoides at the South Sandwich Islands and South Georgia. CCAMLR Sci. 1, 143–153. Ashford, J. R., Croxall, J. P., Rubilar, P. S., and Moreno, C. A. (1995). Seabird interactions with longlining operations for Dissostichus eleginoides around South Georgia, April to May 1994. CCAMLR Sci. 2, 111–121. Ashford, J. R., Rubilar, P. S., and Martin, A. R. (1996). Interactions between cetaceans and longline fishery operations around South Georgia. Mar. Mamm. Sci. 12, 452–457. Ashford, J. R., Wischniowski, S., Jones, C., Bobko, S., and Everson, I. (2001). A comparison between otoliths and scales for use in estimating the age of Dissostichus eleginoides from South Georgia. CCAMLR Sci. 8, 75–92. Ashford, J., Jones, C., Bobko, S., and Everson, I. (2002). Length-at-age in juvenile Patagonian toothfish (Dissostichus eleginoides). CCAMLR Sci. 9, 1–10. Ashford, J., Duhamel, G., Jones, C., and Bobko, S. (2005a). Age, growth and mortality of Patagonian toothfish (Dissostichus eleginoides) caught off Kerguelen. CCAMLR Sci. 12, 29–41. Ashford, J. R., Jones, C. M., Hofmann, E., Everson, I., Moreno, C., Duhamel, G., and Williams, R. (2005b). Can otolith elemental signatures record the capture site of Patagonian toothfish (Dissostichus eleginoides), a fully marine fish in the Southern Ocean? Can. J. Fish. Aquat. Sci. 62, 2832–2840. Ashford, J. R., Arkhipkin, A. I., and Jones, C. M. (2006). Can the chemistry of otolith nuclei determine population structure of Patagonian toothfish Dissostichus eleginoides? J. Fish Biol. 69, 708–721.

The Patagonian Toothfish: Biology, Ecology and Fishery

291

Baird, R. J. (2006). Aspects of illegal, unreported and unregulated fishing in the Southern Ocean Springer, Netherlands. Balushkin, A. V. (2000). Morphology, classification, and evolution of notothenioid fishes of the Southern Ocean (Notothenioidei, Perciformes). J. Ichthyol. 40, (Supplement), 74–109. Bargelloni, L., Marcato, S., and Patarnello, T. (1998). Antarctic fish hemoglobins: Evidence for adaptive evolution at subzero temperature. Proc. Natl. Acad. Sci. USA 95, 8670–8675. Bargelloni, L., Marcato, S., Zane, L., and Patarnello, T. (2000). Mitochondrial phylogeny of notothenioids: A molecular approach to Antarctic fish evolution and biogeography. Syst. Biol. 49, 114–129. Barrera-Oro, E. R., Casaux, R. J., and Marschoff, E. R. (2005). Dietary composition of juvenile Dissostichus eleginoides (Pisces, Nototheniidae) around Shag Rocks and South Georgia, Antarctica. Polar Biol. 28, 637–641. Beamish, R. J., and McFarlane, G. A. (1983). The forgotten requirement for age validation in fisheries biology. Trans. Am. Fish. Soc. 112, 735–743. Belchier, M. (2004). The age structure and growth rate of Patagonian toothfish (Dissostichus eleginoides) at South Georgia. CCAMLR WG-FSA 04/86. Belchier, M., and Collins, M. A. (2008). Recruitment and body size in relation to temperature in juvenile Patagonian toothfish (Dissostichus eleginoides) at South Georgia. Mar. Biol. 155, 493–503. Belchier, M., and Agnew, D. A. (2009). Adding catch at age survey data to the 48.3 toothfish CASAL assessment. CCAMLR WG-SAM 09/13. Brandao, A., Butterworth, D. S., Watkins, B. P., and Miller, D. G. M. (2002). A first attempt at an assessment of the Patagonian toothfish (Dissostichus eleginoides) resource in the Prince Edward Islands EEZ. CCAMLR Sci. 9, 11–32. Brickle, P. (2003). The parasite ecology of the Patagonian toothfish (Dissostichus eleginoides Smitt, 1898). Aberdeen University, (Ph.D. Thesis, 211 pp.). Brickle, P., MacKenzie, K., and Pike, A. (2005). Parasites of the Patagonian toothfish, Dissostichus eleginoides Smitt 1898, in different parts of the sub-Antarctic. Polar Biol. 28, 663–671. Brickle, P., MacKenzie, K., and Pike, A. (2006). Variations in the parasite fauna of the Patagonian toothfish (Dissostichus eleginoides Smitt, 1898), with length, season, and depth of habitat around the Falkland Islands. J. Parasitol. 92, 282–291. Brothers, N. (1991). Albatross mortality and associated bait loss in the Japanese longline fishery in the Southern Ocean. Biol. Conserv. 55, 255–268. Brown, C. R., and Klages, N. T. (1987). Seasonal and annual variation in diets of macaroni (Eudyptes chrysolophus chrysolophus) and southern rockhopper (E. chrysocome chrysocome) penguins at sub-Antarctic Marion Island. J. Zool. 212, 7–28. Brown J., Brickle P., Hearne S., and French G. (2010). An experimental investigation of the ‘umbrella’ and ‘Spanish’ system of longline fishing for the Patagonian toothfish (Dissostichus eleginoides) in the Falkland Islands: Implications for stock assessment and seabird by-catch. Fish. Res. Doi:10.1016/j.fishres.2010.09.013. Bull, B., Francis, R. I. C. C., Dunn, A., McKenzie, A., Gilbert, D. J., and Smith, M. W. (2005). CASAL User Manual v2.07-2005/07/06 NIWA. Calhaem, I., and Christoffel, D. A. (1969). Some observations of the feeding habits of a Weddell seal, and measurements of its prey, Dissostichus mawsoni, at McMurdo Sound, Antarctica. N. Z. J. Mar. Freshw. Res. 3, 181–190. Calliet, G. M., and Andrews, A. H. (2008). Age-validated longevity of fishes: Its importance for sustainable fisheries. In “Fisheries for Global Welfare and Environment” (K. Tsukamoto, T. Kawamura, T. Takeuchi, T. D. Beard and M. J. Kaiser, eds), 5th World Fisheries Congress 2008. pp. 103–120. Terrapub.

292

Martin A. Collins et al.

Candy, S. G., and Constable, A. (2008). An integrated stock assessment for the Patagonian toothfish (Dissostichus eleginoides) for the Heard and Macdonald Islands using CASAL. CCAMLR Sci. 15, 1–34. Candy, S. G., Constable, A. J., Lamb, T., and Williams, R. (2007). A von Bertalanffy growth model for toothfish at Heard Island fitted to length-at-age data and compared to observed growth from mark-recapture studies. CCAMLR Sci. 14, 43–66. Cassia, M. C. (1998). Comparison of age readings from scales and otoliths of the Patagonian toothfish (Dissostichus eleginoides) from South Georgia. CCAMLR Sci. 5, 191–203. Catard, A., Weimerskirch, H., and Cherel, Y. (2000). Exploitation of distant Antarctic waters and close shelf-break waters by white-chinned petrels rearing chicks. Mar. Ecol. Prog. Ser. 194, 249–261. CCAMLR (1987). Scientific Committee Report, Hobart. CCAMLR (2009). Scientific Committee Report, Annex 5: Report of the Working Group on Fish Stock Assessment, Hobart, 133pp. Cherel, Y., Ridoux, V., and Rodhouse, P. G. (1996). Fish and squid in the diet of king penguin chicks, Aptenodytes patagonicus, during winter at sub-antarctic Crozet Islands. Mar. Biol. 126, 559–570. Cherel, Y., and Duhamel, G. (2004). Antarctic jaws: cephalopod prey of sharks in Kerguelen waters. Deep-Sea Res. 151, 17–31. Cherel, Y., Weimerskirch, H., and Trouve, C. (2000). Food and feeding ecology of the neritic-slope forager black- browed albatross and its relationships with commercial fisheries in Kerguelen waters. Mar. Ecol. Prog. Ser. 207, 183–199. Cherel, Y., Weimerskirch, H., and Trouve, C. (2002). Dietary evidence for spatial foraging segregation in sympatric albatrosses (Diomedea spp.) rearing chicks at Iles Nuageuses, Kerguelen. Mar. Biol. 141, 1117–1129. Chikov, V. N., and Mel’nikov, Y. S. (1990). On the question of fecundity of the Patagonian toothfish, Dissostichus eleginoides, in the region of the Kerguelen Islands. Voprosy ikhtiologii 30, 864–866. Ciechomski, J. D., and Weiss, G. (1976). Desarollo y distribucion de postlarvas del robalo Eleginops maclovinus (Valenciennes, 1830) Dollo1904, de la merluza negra Dissostichus eleginoides Smitt 1898 y de la nototenias Notothenia spp. (Pisces, Nototheniidae). Physis 35, 115–125. Clarke, M. R. (1980). Cephalopods in the diet of sperm whales of the southern hemisphere and their bearing on sperm whale biology. Discov. Rep. 37, 1–324. Coggan, R. A., Nolan, C. P., and George, M. J. A. (1996). Exploratory deep-sea fishing in the Falkland Islands, south-western Atlantic. J. Fish Biol. 49, 298–310. Collins, M. A., and Rodhouse, P. G. (2006). Southern Ocean cephalopods. Adv. Mar. Biol. 50, 191–265. Collins, M. A., Yau, C., Nolan, C. P., Bagley, P. M., and Priede, I. G. (1999). Behavioural observations on the scavenging fauna of the Patagonian slope. J. Mar. Biol. Assoc. UK 79, 963–970. Collins, M. A., Bailey, D. M., Ruxton, G., and Priede, I. G. (2005). Trends in body size across an environmental gradient: A differential response in scavenging and non-scavenging demersal deep-sea fish. Proc. R. Soc. Lond. B 272, 2051–2057. Collins, M. A., Everson, I., Paterson, R., Bagley, P. M., Yau, C., Belchier, M., and Hawkins, S. (2006). In situ observations of the scavenging fauna of the South Georgia slope. In “Deep Sea 2003: Conference on the Governance and Management of Deep-sea Fisheries Part 2: Conference poster papers and workshop papers” (R. Shotton, ed.), pp. 45–53. FAO, Rome. Collins, M. A., Ross, K. A., Belchier, M., and Reid, K. (2007). Distribution and diet of juvenile Patagonian toothfish on the South Georgia and Shag Rocks shelves (Southern Ocean). Mar. Biol. 152, 135–147.

The Patagonian Toothfish: Biology, Ecology and Fishery

293

Collins, M. A., Shreeve, R. S., Fielding, S., and Thurston, M. H. (2008). Distribution, growth, diet and foraging behaviour of the yellow-fin notothen Patagonotothen guntheri on the Shag Rocks shelf (Southern Ocean). J. Fish Biol. 72, 271–286. Constable, A., and de la Mare, W. K. (1996). A generalised model for evaluating yield and the long term status of fish stocks under conditions of uncertainty. CCAMLR Sci. 3, 54–60. Constable, A. J., de la Mare, W. K., Agnew, D. J., Everson, I., and Miller, D. (2000). Managing fisheries to conserve the Antarctic marine ecosystem: practical implementation of the Convention on the Conservation of Antarctic Marine Living Resources (CCAMLR). ICES J. Mar. Sci. 57, 778–791. de al Mare, W. K. (1994). Estimating confidence intervals for fish stock abundance estimates from trawl surveys. CCAMLR Sci. 1, 203–207. De Witt, H. H. (1962). On the probable identity of Macrias amisssus, a deep-water notothenioid fish from the Chilean coast. Copeia 3, 659–687. De Witt, H. H., Heemstra, P. C., and Gon, O. (1990). Nototheniidae. In “Fishes of the Southern Ocean” (O. Gon and P. C. Heemstra, eds), pp. 279–331. J. L. B. Smith Institute of Ichthyology, Grahamstown. Delord, K., Gasco, N., Weimerskirch, H., Barbraud, C., and Micol, T. (2005). Seabird mortality in the Patagonian toothfish longline fishery around Crozet and Kerguelen Islands, 2001–2003. CCAMLR Sci. 12, 53–80. Delord, K., Gasco, N., Barbraud, C., and Weimerskirch, H. (2010). Multivariate effects on seabird bycatch in the legal Patagonian toothfish longline fishery around Crozet and Kerguelen Islands. Pol. Biol. 33, 367–378. Des Clers, S., Nolan, C. P., Baranowski, R., and Pompert, J. (1996). Preliminary stock assessment of the Patagonian toothfish longline fishery around the Falkland Islands. J. Fish Biol. 49, 145–156. Duhamel, G. (1981). Characteristiques biologiques des principals especes de poissons du plateau continental des Iles Kerguelen. Cybium 5, 19–32. Duhamel G. (1987). Ichthyofaune des secteurs indien occidental et atlantique oriental de l’ocean austral: biogeographie, cycles biologiques et dynamique des populations. Ph. D. Thesis (Universite P. et M. Curies, Paris), 687 pp. Duhamel, G. (1991). Biology and harvesting of Dissostichus eleginoides around Kerguelen Islands (Division 58.5.1). CCAMLR WG-FSA 91/7. Duhamel, G., and Pletikosic, M. (1983). Donnes biologiques sur les Notothenidae des Iles Crozet. Cybium 7, 43–57. Dunn A., Hanchet S.M. (2007). Assessment models for Antarctic toothfish (Dissostichus mawsoni) in the Ross Sea including data from the 2006/07 season. CCAMLR WGFSA 07/37. Dunn A., Gilbert D.J., Hanchet S.M., Bull B. (2004). Development of an Antarctic tootfish (Dissostichus mawsoni) stock model for CCAMLR Subareas 88.1 for the years 1997/98 to 2003/04. CCAMLR WG-FSA 04/36. Eastman, J. T. (1988). Ocular morphology in Antarctic notothenioid fishes. J. Morphol. 196, 283–306. Eastman, J. T. (1990). The biology and physiological ecology of notothenioid fishes. In “Fishes of the Southern Ocean” (O. Gon and P. C. Heemstra, eds), pp. 34–51. J.L.B. Smith Institute of Ichthyology, Grahamstown. Eastman, J. T., and Devries, A. L. (1981). Buoyancy adaptations in a swim-bladderless Antarctic fish. J. Morphol. 167, 91–102. Eastman, J. T., and Devries, A. L. (1982). Buoyancy studies of Notothenioid fishes in Mcmurdo Sound, Antarctica. Copeia 6, 385–393. Eastman, J. T., and McCune, A. R. (2000). Fishes on the Antarctic continental shelf: Evolution of a marine species flock? J. Fish Biol. 57, 84–102.

294

Martin A. Collins et al.

Eastman, J. T., and Eakin, R. R. (2000). An updated species list for notothenioid fish (Perciformes; Notothenioidei), with comments on Antarctic species. Arch. Fish. Mar. Res. 48, 11–20. Eastman, J. T., and Sidell, B. D. (2002). Measurements of buoyancy for some Antarctic notothenioid fishes from the South Shetland Islands. Polar Biol. 25, 753–760. Effremenko, V. N. (1979). The larvae of six species of the family Nototheniidae from the Scotia Sea. J. Ichthyol. 19, 95–104. Efremenko, V. N. (1984). Larvae of the family Nototheniidae from the Scotia Sea. J. Ichthyol. 24, 34–43. Esch, G. W., and Fernandez, J. C. (1993). A functional biology of parasitism: Ecological and evolutionary implications, p. 352. Chapman and Hall, London. Everson, I. (1977). Reproduction in Notothenia neglecta Nybelin. Br. Antarct. Surv. Bull. 23, 81–92. Everson, I., and Murray, A. W. A. (1999). Size at sexual maturity of Patagonian toothfish. CCAMLR Sci. 6, 37–46. Evseenko, S. A., Kock, K. H., and Nevinsky, M. M. (1995). Early life history of the Patagonian toothfish, Dissostichus eleginoides Smitt, 1898 in the Atlantic Sector of the Southern Ocean. Antarct. Sci. 7, 221–226. Farrell, A. P., and Steffensen, J. F. (2005). The Physiology of Polar Fishes. Elsevier Academic Press, San Diego, 408 pp. Fenaughty, J. M., Eastman, J. T., and Sidell, B. D. (2008). Biological implications of low condition factor “axe handle” specimens of the Antarctic toothfish, Dissostichus mawsoni, from the Ross Sea. Antarct. Sci. 20, 537–551. Gaevskaya, A. B., Kovaljova, A. A., and Paraukhin, A. M. (1990). Peculiarities and formation of parasitofauna of the Patagonian toothfish Dissostichus eleginoides. Biologiya Morya (Mar. Biol.) 4, 23–28, (In Russian). Garcia de la Rosa, S. B., Sanchez, F., and Figueroa, D. (1997). Comparative feeding ecology of Patagonian toothfish (Dissostichus eleginoides) in the South-western Atlantic. CCAMLR Sci. 4, 105–124. Gasiukov P., Dorovskikh R. (2000). Results of D. eleginoides stock assessment for Subarea 48.3 using a dynamic age-structured production model. CCAMLR WG-FSA 00/46. Ghigliotti, L., Mazzei, F., Ozouf-Costaz, C., Bonillo, C., Williams, R., Cheng, C. H. C., and Pisano, E. (2007). The two giant sister species of the Southern Ocean, Dissostichus eleginoides and Dissostichus mawsoni, differ in karyotype and chromosomal pattern of ribosomal RNA genes. Polar Biol. 30, 625–634. Gill, N. A., and Townsend, S. E. (1901). The largest deep-sea fish. Science 14. Goldsworthy, S. D., He, X., Tuck, G. N., Lewis, M., and Williams, R. (2001). Trophic interactions between the Patagonian toothfish, its fishery, and seals and seabirds around Macquarie Island. Mar. Ecol. Prog. Ser. 218, 283–302. Goldsworthy, S. D., Lewis, M., Williams, R., He, X., Young, J. W., and van den Hoff, J. (2002). Diet of Patagonian toothfish (Dissostichus eleginoides) around Macquarie Island, South Pacific Ocean. Mar. Freshw. Res. 53, 49–57. Gon, O., and Heemstra, P. C. (1990). Fishes of the Southern Ocean. J.L.B. Smith Institute of Ichthyology, Grahamstown. Green, K., Burton, H. R., and Williams, R. (1989). The diet of Antarctic fur seals Arctocephalus gazella (Peters) during the breeding season at Heard Island. Antarct. Sci. 1, 317–324. Guerrero, A., and Arana, P. (2009). Fishing yields and size structures of Patagonian toothfish (Dissostichus eleginoides) caught with pots and longlines off far southern Chile. Latin Am. J. Aqua. Res. 37, 361–370.

The Patagonian Toothfish: Biology, Ecology and Fishery

295

Guynn, K. D., and Peterson, M. S. (2008). Mercury concentrations in the Patagonian toothfish, Dissostichus eleginoides Smitt 1898, among three distinct stocks. Pol. Biol. 31, 269–274. Hamilton, H. F. (1995). A preliminary parasite survey of the Patagonian toothfish (Dissostichus eleginoides Smitt, 1898) from the Falkland Islands with a view to differentiation of stocks in the Antarctic Aberdeen University, (M.Sc. Thesis). Hanchet, S. M., Stevensen, M. L., Phillips, N. L., and Horn, P. L. (2004). A characterisation of the toothfish fishery in sub-areas 88.1 and 88.2 from 1997/98 to 2003/04. CCAMLR WG-FSA 04/20. Hillary, R. M., Kirkwood, G. P., and Agnew, D. J. (2006). An assessment of toothfish in Subarea 48.3 using CASAL. CCAMLR Sci. 13, 65–95. Horn, P. L. (2002). Age and growth of Patagonian toothfish (Dissostichus eleginoides) and Antarctic toothfish (D. mawsoni) in waters from the New Zealand subantarctic to the Ross Sea, Antarctica. Fish. Res. 56, 275–287. Hucke-Gaete, R., Moreno, C. A., and Arata, J. (2004). Operational interactions of sperm whales and killer whales with the Patagonian toothfish industrial fishery off southern Chile. CCAMLR Sci. 11, 127–140. Hureau, J. C., and Ozouf-Costaz, C. (1980). Age determination and growth of Dissostichus eleginoides Smitt, 1898 from Kerguelen and Crozet. Cybium 3, 23–32. Jefferson, T. A., Stacey, P. J., and Baird, R. W. (1996). Acoustic methods of reducing or eliminating marine mammals-fisheryes interactions: do they work? Ocean Coast. Manag. 31, 41–70. Kalish J.M., and Timmiss T.A. (1998). Determination of Patagonian toothfish Dissostichus eleginoides age, growth and population characteristics based on otoliths. CCAMLR WGFSA 98/40. Kellermann, A. (1989). Catalogue of early life stages of Antarctic notothenioid fish. In “ldentification Key and Catalogue of Larval Antarctic Fishes” (A. Kellermann, ed.), BIOMASS Scientific Series. pp. 45–136. Kellermann, A. (1990). Catalogue of early life stages of Antarctic notothenioid fishes. Berichte Polarforschung 67, 45–136. Kock, K. H. (1992). Antarctic fish and fisheries Cambridge University Press, 359 pp. Kock, K. H., and Kellermann, A. (1991). Reproduction in Antarctic notothenioid fish. Antarct. Sci. 3, 125–150. Kock, K. H., Purves, M. G., and Duhamel, G. (2006). Interactions between cetacean and fisheries in the Southern Ocean. Polar Biol. 29, 379–388. Kooyman, G. L., Cherel, Y., Le Maho, Y., Croxall, J. P., Thorson, P. H., Ridoux, V., and Kooyman, C. A. (1992). Diving behaviour and energetics during foraging cycles in king penguins. Ecol. Monogr. 62, 143–163. Korabelnikov, L. V. (1959). The diet of sperm whales in the Antarctic seas. Priroda 3, 103–104. Korovina, V. M., Neyelov, A. V., and Bondarenko, Y. P. (1991). The anatomy and histology of the intestine of the Patagonian toothfish (Dissostichus eleginoides Smitt). Voprosy ikhtiologii 44, 218–224. Krusic-Golub K., and Williams R. (2004). Progress towards validation of ageing of Dissostichus eleginoides using otoliths. CCAMLR WG-FSA 04/67. Krusic-Golub K., and Williams R. (2005). Age validation of Patagonian toothfish (Dissostichus eleginoides) from Heard and Macquarie islands. CCAMLR WG-FSA 05/60. Krusic-Golub K., Green C., and Williams R. (2005). First increment validation of Patagonian toothfish (Dissostichus eleginoides) from Heard Island. CCAMLR WG-FSA 05/61. Lack, M. (2008). Continuing CCAMLR’s Fight against IUU Fishing for Toothfish. WWF Australia and TRAFFIC International, Sydney, 50 pp. Lack, M., and Sant, G. (2001). Patagonian toothfish: Are conservation and trade measures working? TRAFFIC Bull. 19, 15–32.

296

Martin A. Collins et al.

Lake, S., Burton, H., and van den Hoff, J. (2003). Regional, temporal and fine-scale spatial variation in Weddell seal diet at four coastal locations in east Antarctica. Mar. Ecol. Prog. Ser. 254, 293–305. Laptikhovsky, V., and Brickle, P. (2005). The Patagonian toothfish fishery in Falkland islands’ waters. Fish. Res. 74, 11–23. Laptikhovsky, V., Arkhipkin, A., and Brickle, P. (2006). Distribution and reproduction of the Patagonian toothfish Dissostichus eleginoides Smitt around the Falkland Islands. J. Fish Biol. 68, 849–861. Lescroel, A., Ridoux, V., and Bost, C. A. (2004). Spatial and temporal variation in the diet of gentoo penguin (Pygoscelis papua) at Kerguelen Islands. Polar Biol. 27, 206–216. Lord, C., Duhamel, G., and Pruvost, P. (2006). The patagonian toothfish (Dissostichus eleginoides) fishery in the Kerguelen Islands (Indian Ocean sector of the Southern Ocean). CCAMLR Sci. 13, 1–25. Macdonald, P. D. M., and Pitcher, T. J. (1979). Age groups from size frequency data: A versatile and efficient method of analyzing distribution mixtures. J. Fish. Res. Board Can. 36, 987–1001. Marlow, T. R., Agnew, D. J., Purves, M. G., and Everson, I. (2003). Movement and growth of tagged Dissostichus eleginoides around South Georgia and Shag Rocks (Subarea 48.3). CCAMLR Sci. 10, 101–111. Martin-Smith, K. (2009). A risk-management framework for avoiding significant adverse impacts of bottom fishing gear on Vulnerable Marine Ecosystems. CCAMLR Sci. 16, 177–193. Mendez, E., Giudice, H., Pereira, A., Inocente, G., and Medina, D. (2001). Preliminary report on the total mercury content of Patagonian toothfish (Dissostichus eleginoides). J. Food Comp. Anal. 14, 547–549. McArthur, T., Butler, E. C. V., and Jackson, G. D. (2003). Mercury in the marine food chain in the Southern Ocean at Macquarie Island: an analysis of a top predator, Patagonian toothfish (Dissostichus eleginoides) and a mid-trophic species, the warty squid (Moroteuthis ingens). Pol. Biol. 27, 1–5. McFarlane, G. A., and Beamish, R. J. (1990). Effect of an external tag on growth of sablefish (Anoplopoma fimbria), and consequences to mortality and age at maturity. Can. J. Fish. Aqua. Sci. 47, 1551–1557. McKenna, J. E. (1991). Trophic relationships within the Antarctic demersal fish community of South Georgia Island. Fish. Bull. 89, 643–654. McKinlay, J. P., Welsford, D. C., Constable, A. J., and Nowara, G. B. (2008). An assessment of the exploratory fishery for Dissostichus spp. on Banzare Bank (CCAMLR Division 58.4.3b) based on fine-scale catch and effort data. CCAMLR Sci. 15, 55–78. McMahon, C. R., Holley, D., and Robinson, S. (1999). The diet of itinerant male Hooker’s sea lions, Phocarctos hookeri, at sub-Antarctic Macquarie Island. Wildl. Res. 26, 839–846. Moller, P. R., Nielsen, J. G., and Fossen, I. (2003). Patagonian toothfish found off Greenland – This catch is evidence of transequatorial migration by a cold-water Antarctic fish. Nature 421, 599. Moreno, C. (1991). Hook selectivity in the longline fishery of Dissostichus eleginoides (Notothenidae) off the Chilean coast. CCAMLR Sel. Sci. Pap. 8, 107–119. Moreno C. (1998). Do the males of Dissostichus eleginoides grow faster, or only mature before females? CCAMLR WG-FSA 98/17. Moreno, C., Rubilar, P. S., Marschoff, E. R., and Benzaquen, L. (1996). Factors affecting the incidental mortality of seabirds in the Dissostichus eleginoides fishery in the southwest Atlantic (Subarea 48.3, 1995 season). CCAMLR Sci. 3, 79–91. Moreno, C. A., Rubilar, P. S., and Zuleta, A. (1997). Ficha te´cnica del bacalao de profundidad Dissostichus eleginoides Smitt, 1898. CCAMLR WG-FSA 97/42.

The Patagonian Toothfish: Biology, Ecology and Fishery

297

Moreno, C., Arata, J., Rubilar, P. S., Hucke-Gaete, R., and Robertson, G. (2006). Artisanal longline fisheries in southern Chile: Lessons to be learned to avoid incidental seabird mortality. Biol. Conserv. 127, 27–36. Moreno, C., Castro, R., Mujica, L. J., and Reyes, P. (2008). Significant conservation benefits obtained from the use of a new fishing gear in the Chilean Patagonian toothfish fishery. CCAMLR Sci. 15, 78–79. Morton, A. B., and Symonds, H. K. (2002). Displacement of Orcinus orca (L) by high amplitude sound in British Columbia, Canada. ICES J. Mar. Sci. 59, 71–80. Murillo, C., Oyarzun, C., and Fernandez, I. (2008). Latitudinal and temporal variation in the diet of Dissostichus eleginoides Smitt, 1898 (Perciformes: Notothenidaein) deep environments of the south and center coast of Chile. Gayana 72, 94–101. Near, T. J., and Cheng, C. H. C. (2008). Phylogenetics of notothenioid fishes (Teleostei: Acanthomorpha): Inferences from mitochondrial and nuclear gene sequences. Mol. Phylogenet. Evol. 47, 832–840. Near, T. J., Russo, S. E., Jones, C. D., and Devries, A. L. (2003). Ontogenetic shift in buoyancy and habitat in the Antarctic toothfish, Dissostichus mawsoni (Perciformes: Nototheniidae). Polar Biol. 26, 124–128. Near, T. J., Pesavento, J. J., and Cheng, C. H. C. (2004). Phylogenetic investigations of Antarctic notothenioid fishes (Perciformes: Notothenioidei) using complete gene sequences of the mitochondrial encoded 16S rRNA. Mol. Phylogenet. Evol. 32, 881–891. Nel, D. C., Ryan, P. G., and Watkins, B. P. (2002). Seabird mortality in the Patagonian toothfish longline fishery around the Prince Edward Islands, 1996–2000. Antarct. Sci. 14, 151–161. Nevinsky, M. M., and Kozlov, A. N. (2002). The fecundity of the Patagonian toothfish Dissostichus eleginoides around South Georgia Island (South Atlantic). J. Ichthyol. 42, 571–573. Nolan, C. P., Liddle, G. M., and Elliot, J. (2000). Interactions between killer whales (Orcinus orca) and sperm whales (Physeter macrocephalus) with a longline fishing vessel. Mar. Mamm. Sci. 16, 658–664. North, A. W. (1998). Growth of young fish during winter and summer at South Georgia, Antarctica. Polar Biol. 19, 198–205. Norman, J. R. (1937). Coast Fishes Part II. The Patagonian region. Discov. Rep. 16, 1–150. North, A. W. (2002). Larval and juvenile distribution and growth of Patagonian toothfish around South Georgia. Antarct. Sci. 14, 25–31. North, A. W., and White, M. G. (1982). Key to postlarvae from the Scotia Sea, Antarctica. Cybium 6, 13–32. Nyegaard, M., Arkhipkin, A., and Brickle, P. (2004). Variation in the diet of Genypterus blacodes (Ophidiidae) around the Falkland Islands. J. Fish Biol. 65, 666–682. Oliva, M. E., Fernandez, I., Oyarzun, C., and Murillo, C. (2008). Metazoan parasites of the stomach of Dissostichus eleginoides Smitt 1898 (Pisces: Notothenidae) from southern Chile: A tool for stock discrimination? Fish. Res. 91, 119–122. Olsson, O., and North, A. W. (1997). Diet of the king penguin Aptenodytes patagonicus during three summers at South Georgia. Ibis 139, 504–512. Otley, H., Reid, T. A., and Pompert, J. (2007). Trends in seabird and Patagonian toothfish Dissostichus eleginoides longliner interactions in Falkland Island waters, 2002/03 and 2003/ 04. Mar. Ornithol. 35, 47–55. Oyarzun, C., and Campos, P. W. (1987). Dissostichus eleginoides Smitt, 1898; concideraciones sobre su determinacion taxonomica e implicancias biogeographicas (Pisces, Perciformes, Nototheniidae). Rev. Biol. Mar. Valparaiso 23, 173–192. Oyarzun, C., Campos, P. W., and Valeria, H. R. (1988). Adaptaciones para la flotabilidad en Dissostichus eleginoides Smitt, 1898 (Pisces, Perciformes, Nototheniidae). Investigacionnes Pesquana 52, 455–466.

298

Martin A. Collins et al.

Oyarzu´n, C., Gacitu´a, S., Araya, M., Cubillos, L., Salamanca, M., Pino, C., Galleguillos, R., Aedo, G., and Lamilla, J. (2003). Asignacio´n de edades y crecimiento de bacalao de profundidad. Informe Final, Proyecto FIP 2001-17 130. Parkes, G., Moreno, C. A., Pilling, G., and Young, Z. (1996). Use of the Leslie stock depletion model for the assessment of local abundance of Patagonian toothfish (Dissostichus eleginoides). CCAMLR Sci. 3, 55–77. Parukhin, A. M., and Lyadov, V. N. (1982). Helminth fauna of food Nototheniidae fishes from Kerguelen region. Ekologiya Morya, Kiev 10, 49–57(in russian). Paya, I., and Brickle, P. (2008). Stock Assessment and Total Allowable Catch of Toothfish (Dissostichus eleginoides). Falkland Islands Government Fisheries Department Scientific Report. Payne, A. G., Agnew, D. J., and Brandao, A. (2005). Preliminary assessment of the Falklands Patagonian toothfish (Dissostichus eleginoides) population: Use of recruitment indices and the estimation of unreported catches. Fish. Res. 76, 344–358. Phillips K.L., Rodgers M., and Ansell E. (2009). Macquarie Island toothfish fishery. In “Fishery status reports 2007: status of fish stocks managed by the Australian Government” (D. T. Wilson, R. Curtotti, G. A. Begg, and K. L. Phillips, eds), pp. 359–365. Bureau of Rural Sciences, Canberra. Phillips, R. A., Ridley, C., Reid, K., Pugh, P. J. A., Tuck, G. N., and Harrison, N. (2010). Ingestion of fishing gear and entanglements of seabirds: Monitoring and implications for management. Biol. Cons. 143, 501–512. Pilling, G. M., Purves, M. G., Daw, T. M., Agnew, D. A., and Xavier, J. C. (2001). The stomach contents of Patagonian toothfish around South Georgia (South Atlantic). J. Fish Biol. 59, 1370–1384. Plotz, J. (1986). Summer diet of Weddell seals (Leptonychotes weddelli) in the eastern and southern Weddell Sea, Antarctica. Polar Biol. 6, 97–102. Prenski, L. B., and Almeyda, S. M. (2000). Some biological aspects relevant to patagonian toothfish (Dissostichus eleginoides) exploitation in the argentine exclusive economic zone and adjacent ocean sector. Frente Marı´timo 18, 103–124. Priede, I. G., and Bagley, P. M. (2000). In situ studies on deep-sea demersal fishes using autonomous unmanned lander platforms. Oceanog. Mar. Biol. Ann. Rev. 38, 357–392. Priede, I. G., and Merrett, N. R. (1996). Estimation of abundance of abbyssal demersal fishes; a comparison of data from trawls and baited cameras. J. Fish Biol. 49, 207–216. Purves, M. G., Agnew, D. J., Balguerias, E., Moreno, C. A., and Watkins, B. (2004). Killer whale (Orcinus orca) and sperm whale (Physeter macrocephalus) interactions with longline vessels in the Patagonian toothfish fishery at South Georgia, South Atlantic. CCAMLR Sci. 11, 111–126. Putz, K., Ingham, R. J., Smith, J. G., and Croxall, J. P. (2001). Population trends, breeding success and diet composition of gentoo Pygoscelis papua, magellanic Spheniscus magellanicus and rockhopper Eudyptes chrysocome penguins in the Falkland Islands. Polar Biol. 24, 793–807. Reid, K. (1995). The diet of Antarctic fur seals (Arctocephalus gazella Peters 1875) during winter at South Georgia. Antarctic Sci. 7, 241–249. Reid, K., and Arnould, J. P. Y. (1996). The diet of Antarctic fur seals Arctocephalus gazella during the breeding season at South Georgia. Polar Biol. 16, 105–114. Reid, K., and Nevitt, G. A. (1998). Observation of southern elephant seal, Mirounga leonina, feeding at sea near South Georgia. Mar. Mamm. Sci. 14, 637–640. Reid, T. A., Sullivan, B. J., Pompert, J., Enticott, J. W., and Black, A. D. (2004). Seabird mortality associated with Patagonian Toothfish (Dissostichus eleginoides) longliners in Falkland Islands waters. Emu 104, 317–325. Reilly, A., and Ward, R. D. (1999). Microsatellite loci to determine population structure of the Patagonian toothfish Dissostichus eleginoides. Mol. Ecol. 8, 1753–1754.

The Patagonian Toothfish: Biology, Ecology and Fishery

299

Rideout, R. M., Rose, G. A., and Burton, M. P. M. (2005). Skipped spawning in female iteroparous fishes. Fish Fish. 6, 50–72. Roberts, J., and Agnew, D. A. (2008). Proposal for an extension to the mark recapture experiment to estimate toothfish population size in Subarea 48.4. CCAMLR WG-FSA 08/46. Robertson, G. (2000). Effect of line sink rate on albatross mortality in the Patagonian toothfish longline fishery. CCAMLR Sci. 7, 133–150. Robertson, G., Moreno, C. A., Crujeiras, J., Wienecke, B., Gandini, P., McPherson, G., and Pon, J. P. S. (2007). An experimental assessment of factors affecting the sink rates of Spanish-rig longlines to minimize impacts on seabirds. Aqua. Conserv. Mar. Freshw. Ecosyst. 17, S102–S121. Robinson, S. A., and Hindell, M. A. (1996). Foraging ecology of gentoo penguins Pygoscelis papua at Macquarie Island during the period of chick care. Ibis 138, 722–731. Roche, C., Guinet, C., Gasco, N., and Duhamel, G. (2007). Marine mammals and demersal longline fishery interactions in Crozet and Kerguelen exclusive economic zones: An assessment of depredation levels. CCAMLR Sci. 14, 67–82. Rodriguez, L., and George-Nascimento, M. (1996). The Metazoan parasite fauna of the Patagonian toothfish Dissostichus eleginoides Smitt, 1898 (Pisces: Nototheniidae) of central Chile: Taxonomic, ecological and zoogeographic aspects. Rev. Chil. Hist. Natl. 69, 21–33. Rogers, A. D., Morley, S., Fitzcharles, E., Jarvis, K., and Belchier, M. (2006). Genetic structure of Patagonian toothfish (Dissostichus eleginoides) populations on the Patagonian Shelf and Atlantic and western Indian Ocean Sectors of the Southern Ocean. Mar. Biol. 149, 915–924. Sanchez, S., Dettai, A., Bonillo, C., OzoufCostaz, C., Detrich, H. W., and Lecointre, G. (2007). Molecular and morphological phylogenies of the Antarctic teleostean family Nototheniidae, with emphasis on the Trematominae. Polar Biol. 30, 155–166. Shandikov, G. A., and Faleeva, T. I. (1992). Features of gametogenesis and sexual cycles of six notothenioid fishes from East Antarctica. Polar Biol. 11, 615–621. Shaw, P. W., Arkhipkin, A. I., and Al-Khairulla, H. (2004). Genetic structuring of Patagonian toothfish populations in the Southwest Atlantic Ocean: The effect of the Antarctic Polar Front and deep-water troughs as barriers to genetic exchange. Mol. Ecol. 13, 3293–3303. Sharp, B. R., Parker, S. J., and Smith, N. (2009). An impact assessment framework for bottom fishing methods in the CCAMLR convention area. CCAMLR Sci. 16, 195–210. Slip, D. J. (1995). The diet of southern elephant seals (Mirounga leonina) from Heard-Island. Can. J. Zool. 73, 1519–1528. Slip, D. J., Hindell, M. A., and Burton, H. R. (1994). Diving behaviour of southern elephant seals from Macquarie Island: An overview. In “Elephant seals: Population Ecology, Behaviour and Physiology” (B. G. Le Boeuf and R. M. Laws, eds), pp. 253–270. University of California Press, Berkeley. Smith, P., and McVeagh, M. (2000). Allozyme and microsatellite DNA markers of toothfish population structure in the Southern Ocean. J. Fish Biol. 57, 72–83. Smitt FA (1898). Poissons de l’expedition scientifique a la terra de feu. Bihang till Kongl Svenska Vetenskaps-Akademiens Handlingar Brand 24 IV, 1–80. Stevenson, M. L., Hanchet, S. M., and Dunn, A. (2008). A characterisation of the toothfish fishery in Subareas 88.1 and 88.2 from 1997/98 to 2007/08. CCAMLR WG-FSA 08/ 22. Tarverdiyeva, M. I. (1972). Daily food consumption and feeding patterns of the South Georgia cod (Notothenia rossii marmorata) and the Patagonian toothfish (Dissostichus eleginoides) (Fam. Nototheniidae) in the South Georgia area. J. Ichthyol. 12, 684. Testa, J. W., Siniff, D. B., Ross, M. J., and Winter, J. D. (1985). Weddell seal-Antarctic cod interactions in McMurdo Sound, Antarctica. In “Antarctic Nutrient Cycles and Food

300

Martin A. Collins et al.

Webs” (W. R. Siegfried, P. R. Condy and R. M. Laws, eds), pp. 561–565. SpringerVerlag, Berlin. Tuck, G. N., de la Mare, W. K., Hearn, W. S., Williams, R., Smith, A. D. M., He, X., and Constable, A. (2003). An exact time of release and recapture stock assessment model with an application to Macquarie Island Patagonian toothfish (Dissostichus eleginoides). Fish. Res. 63, 179–191. Visser, I. N. (2000). Killer whale (Orcinus orca) interactions with longline fisheries in New Zealand waters. Aqua. Mamm. 26, 241–252. Watkins, W. A., Daher, M. A., Fristrup, K. M., Howald, T. J., and Disciara, G. N. (1993). Sperm whales tagged with transponders and tracked underwater by sonar. Mar. Mamm. Sci. 9, 55–67. White, M. G., North, A. W., Twelves, E. L., and Jones, S. (1982). Early development of Notothenia neglecta from the Scotia Sea, Antarctica. Cybium 6, 43–51. Wienecke, B., and Robertson, G. (2004). Validation of sink rates of longlines measured using two different methods. CCAMLR Sci. 11, 179–187. Williams, R., and Capdeville, D. (1996). Seabird interactions with trawl and longline fisheries for Dissostichus eleginoides and Champsocephalus gunnari. CCAMLR Sci. 3, 93–99. Williams, R., and de la Mare, W. K. (1995). Fish distribution and biomass in the Heard Island zone (Division 58.5.2). CCAMLR Sci. 2, 1–20. Williams R., Lamb T. (2002). Behaviour of Dissostichus eleginoides fitted with archival tags at Heard Island: preliminary results. CCAMLR WG-FSA 02/60. Williams, R., Tuck, G. N., Constable, A. J., and Lamb, T. (2002). Movement, growth and available abundance to the fishery of Dissostichus eleginoides Smitt, 1898 at Heard Island, derived from tagging experiments. CCAMLR Sci. 9, 33–48. Xavier, J. C., Rodhouse, P. G., Purves, M. G., Daw, T. M., Arata, J., and Pilling, G. M. (2002). Distribution of cephalopods recorded in the diet of the Patagonian toothfish (Dissostichus eleginoides) around South Georgia. Polar Biol. 25, 323–330. Xavier, J. C., Croxall, J. P., Trathan, P. N., and Wood, A. G. (2003). Feeding strategies and diets of breeding grey-headed and wandering albatrosses at South Georgia. Mar. Biol. 143, 221–232. Yano, K., and Dahlheim, M. E. (1995). Killer whale, Orcinus orca, depredation on longline catches of bottom fish in the southeastern Bering Sea and adjacent waters. Fish. Bull. 93, 355–372. Yau, C., Collins, M. A., Bagley, P. M., Everson, I., Nolan, C. P., and Priede, I. G. (2001). Estimating the abundance of Patagonian toothfish Dissostichus eleginoides using baited cameras: a preliminary study. Fish. Res. 51, 403–412. Yau, C., Collins, M. A., Bagley, P. M., Everson, I., and Priede, I. G. (2002). Scavenging by megabenthos and demersal fish on the South Georgia slope. Antarct. Sci. 14, 16–24. Young, Z., Gili, R., and Cid, L. (1995). Prospeccio´n de bacalao de profundidad entre las latitudes 43 y 47 S. Informe Te´cnico IFOP, 1-47. Young, Z., Oliva, J., Olivares, A., and Dias, E. (1999). Aspectos reproductivos del recurso bacalao de profundidad en la I a X Regiones. Informe Final Proyecto FIP, 97–16, 51pp. Young Z., Zuleta A., Robotham H., Aguayo M., and Cid L. (1992). Evaluacio´n del stock de bacalao de profundidad entre las latitudes 47 y 57 S. Informe Tecnico IFOP-SUBPESCA, 1-63. Zakharov, G., and Frolkina, Z. (1976). Some data on the distribution and biology of Patagonian toothfish occurring in the southwest Atlantic. Tr. Atlant NIRO 65, 143–150, (in Russian). Zhivov, V. V., and Krivoruchko, V. M. (1990). On the biology of the Patagonian toothfish, Dissostichus eleginoides, of the Antarctic part of the Atlantic. J. Ichthyol. 30, 142–146.

TAXONOMIC INDEX

A Acanthephyra spp., 184 Acantholaimus, 20 Aethotaxis, 231 Alabaminella weddellensis, 26 Alpheus glaber, 208 Alvinella pompejana, 38 Alvinocaris stactophila, 165 Amperima, 26, 29, 54 Amperima rosea, 6, 26–27, 66 Anisakis spp., 268 Antimora rostrata, 280 Aricidea, 29 Aristeus antennatus, 201, 204 Asbestopluma hypogea, 68 Ascarophis nototheniae, 267 Aspersentis megarhynchus, 267 B Bathymodiolinae, 71 Bathymodiolus, 45 Bathymodiolus azoricus, 44–46 Bathymodiolus childressi, 48, 165 Bathymodiolus thermophilus, 37–38 Beggiatoa, 49 Bythograea thermydron, 37–38 C Calocaris macandrae, 208 Calyptogena kilmeri, 47, 165 Calyptogena magnifica, 37 Carcinus maenas, 159 Chaceon mediterraneus, 21 Champsocephalus gunnari, 257 Chlorotocus, 204 Chlorotocus crassicornis, 186, 208 Chorocaris chacei, 46 Chrysopetalidae, 50 Cirratulidae, 29 Clestobothrium crassiceps, 262, 267 Corynosoma, 267–268 Corynosoma arctocephali, 266 Corynosoma bullosum, 267–268 Corynosoma hammani, 267 Coryphaenoides spp., 33 Cucullanellus fraseri, 267 Cyartonema, 20

D Dichelyne (Cucullanellus) fraseri, 262 Dichromadora, 20 Dissostichus, 229, 231, 269, 271, 279 Dissostichus amissus, 232 Dissostichus eleginoides, 229–232, 234–235, 237, 239, 241–249, 258, 262, 266–273, 276, 278, 281, 284, 287 Dissostichus mawsoni, 229, 231–232, 234, 269–272, 287 Dissostichus spp., 269, 286 Drosophila, 160 Drosophila melanogaster, 160, 163 E Echinocrepis rostrata, 27, 32, 66 Echinorhynchus georgianus (¼E. petrotschenkoi), 267 Echinorhynchus longiproboscis, 266 Echinua affinis, 24 Eleginops, 230–231 Ellipinion molle, 26, 66 Elpidia minutissima, 27, 32, 66 Elytrophalloides oatesi, 267 Engraulis encrasicholus, 121, 143 Epistominella exigua, 26 Eptatretus deani, 50 Eubrachiella antarctica, 262, 268 G Gadidae, 99–100 Gadus, 98 Gadus merluccius, 98 Gennadas elegans, 198 Glomericirrus macrouri, 267 Gobionotothen, 231 Goneplax rhomboides, 186, 208 Gonocerca physidis, 268 Gonocerca taeniata, 267 Grillotia erinaceus, 266 Gvodarus, 231 H Halalaimus, 20 Hemimysis, 68 Heterosentis heteracanthus, 262 Hirudinella ventricosa, 266

301

302

Taxonomic Index

Homarus americanus, 186 Homarus spp., 187, 203 Hormosinacea, 26 Hysterothylacium nototheniae, 262, 267 Hysterothylacium spp., 268 I Idas simpsoni, 50 K Kondakovia longimanna, 257 L Lagenammina, 26 Lamellibrachia luymesi, 48 Lecithaster australis, 267 Lecithophyllum champsocephali, 262, 267 Ledella messanensis, 24 Lepidapedon antarcticus, 267 Lepidapedon garrardi, 262 Lepidapedon taeniatum, 262, 267 Lepidon eques, 24 Lepidonotothen, 231 Lepidonotothen squamifrons, 251, 257 Limulus polyphemus, 157, 159 Liocarcinus depurator, 204, 208 Loligo gahi, 257 Lophelia pertusa, 49 Lyconodes, 99 Lyconus, 99 M Macrias amissus, 231–232 Macropipus tuberculatus, 208 Macrouridae, 280 Macruroninae, 99 Macruronus, 99 Macruronus magellanicus, 251 Madrepora oculata, 49 Mariactis rimicarivora, 44 Marlutio vulgari, 98–99 Merlucciidae, 99–100 Merlucciinae, 99 Merluccius, 98–100, 102–104, 127, 129 Merluccius albidus, 102–105 Merluccius angustimanus, 100, 105 Merluccius australis, 104, 108 Merluccius bilinearis, 104–105, 108 Merluccius cadenati, 104–105, 112 Merluccius capensis, 104–105, 129 Merluccius gayi, 104–105, 108 Merluccius gayi gayi, 127 Merluccius gayi peruanus, 127

Merluccius hernandezi, 100 Merluccius hubbsi, 102, 104, 108, 127, 131 Merluccius merluccius, 97–98, 102–105, 108, 112–113, 130 Merluccius paradoxus, 103–105 Merluccius polli, 103–104 Merluccius polylepis, 104, 108 Merluccius productus, 104–105, 127, 135 Merluccius senegalensis, 104–105, 112 Merluccius smiridus, 98 Merluccius spp., 100, 109, 112, 262–267 Mesonychoteuthis hamiltoni, 261 Metacanthocephalus rennicki, 262 Microlaimus, 20 Micromesistius australis, 251 Micromesistius australis australis, 257, 267 Micromesistius poutassou, 121 Mirocaris fortunata, 46, 71 Monhysteridae, 20 Monodaeus couchii, 208 Moridae, 280 Munida intermedia, 208 Munida iris, 208 Munida tenuimana, 208 Munidopsis spp., 37 Muraenolepis spp., 257 Myriochele fragilis, 21 Mysidacea, 68 Mytilus edulis, 71 Myxine circifrons, 50 Myxine glutinosa, 51 N Nauticaris spp., 257 Neolebouria antarctica, 267 Neolebouria georgiana (¼N. antarctica), 267 Neopavlovskioides georgianus, 266, 268 Nephrops, 208 Nephrops norvegicus, 186–187, 193, 203–204, 208 Nezumia aequalis, 24 Notothenia, 231 Notothenia corriiceps, 251 Nototheniidae, 229–230, 267–268 Nototheniops larsoni, 267 Nototheniops nudifrons, 251 O Oneirophanta mutabilis, 26–27 Oopsacas minuta, 6, 68 Opheliidae, 29 Ophiocten gracilis, 24 Ophiomusium lymani, 24 Ophiura ljungmani, 24 Ophryotrocha spp., 50–51 Orcinus orca, 284

303

Taxonomic Index R

Osedax, 71 Osedax mucofloris, 51 Osedax spp., 51 Oweniidae, 71 P Pagothenia, 231 Palaemonetes varians, 71 Paralomis multispina, 50 Paralvinella palmiformis, 41 Paralvinella pandorae, 40–41 Paranotothenia, 231 Paraonidae, 29 Parapenaeus longirostris, 202, 208 Pasiphaea multidentata, 184, 199–200, 203, 208 Pasiphaea sivado, 199–200, 208 Pasiphaea spp., 184, 199 Patagonotothen, 231 Patagonotothen guntheri, 251 Patagonotothen ramsayi, 251, 257 Peniagone spp., 32 Peniagone vitrea, 32, 66 Phymorhynchus spp., 37 Physeter macrocephalus, 284 Plesionika gigliolii, 184, 208 Plesionika martia, 184, 208 Plesionika spp., 201 Pleuragramma, 231 Plutonaster bifrons, 24 Polycheles typhlops, 165 Procambarus clarkii, 160 Procellaria aequinoctialis, 283 Procellaria cinerea, 283 Processa, 204 Processa canaliculata, 205, 208 Processa spp., 186 Pseudobenedenia dissostichi, 266, 268 Pseudobenedeniella branchialis, 262 Pseudostichopus aemulatus, 26 Pseudoterranova decipiens, 266 Pseudothelphusa americana, 163–164 Psychropotes longicauda, 26 Psychropotes longicaudata, 32

Rajidae, 280 Rhizosolenia spp., 12 Ridgeia piscesae, 40–42 Riftia pachyptila, 37–39 Rimicaris exoculata, 44, 46 S Sabellidae, 71 Sardina pilchardus, 121 Scomber scombrus, 121 Seepiophila jonesi, 48 Sergestes arcticus, 201–202, 208 Sergestidae spp., 184 Siboglinidae, 71 Siboglinum, 71 Solenocera, 204 Solenocera membranacea, 186, 208 Somniosus pacificus, 50 Spionidae, 29 Steindachneria, 99 Steindachneriinae, 99 Stenakron spp., 267 Synaphobranchus kaupii, 30 Systellaspis debilis, 198 T Tevnia, 39 Tevnia jerichonana, 37–39 Theristus, 20 Thermanemertes valens, 40 Trachurus trachurus, 121 Trachyrhynchus murrayi, 24 Trematomus, 231 Tricoma, 20 Trisopterus spp., 124 V Vigtorniella ardabilia, 50 Vigtorniella flokati, 50 Vigtorniella sp., 51

Q Quinqueloculina spp., 26

Y Yoldiella jeffreysi, 24

SUBJECT INDEX

A Abyssal sites, deep-sea benthic ecosystems north-east Pacific bioturbation rate, 31 California Current Oceanic Fisheries Investigations (CalCOFI), 31 dietary studies, 33 ecosystem shifts, 33 migration and mortality, 32 POC flux, 34 sediment community oxygen consumption (SCOC), 31 PAP site Amperima event, 26 cluster analysis, 28 fish community, 30 metazoan meiofauna density, 28 north-east Atlantic, 25 polychaetes, 29 target species, 30 time-series data, 27 Amperima event, 26, 29 Antifreeze glycopeptides, 270 Asynchronous oocyte development, Merluccius merluccius, 129–131 Axial volcano, 41–42 B Bathyal sites, deep-sea benthic ecosystems Bay of Biscay, 23 eastern Mediterranean, 20–21 HAUSGARTEN bottom-water temperature, 18 epifaunal megafauna distribution, 20 location, 17 nematodes, 20 POC, export flox, 17 temporal changes, 18–19, 22 Peru and Chile margin El Nin˜o (EN) events, 22 oxygen minimum zone (OMZ), 21, 23 time-series studies, 21 Rockall Trough, 24 Sagami Bay, 23–24 West Antarctic Peninsula, 24–25 Benthopelagic definition, 172–179

ontogenetic and gender modulation, 199–201, 203–204 trawling data interpretation, 190–193 Bimodal activity rhythm, shrimp, 164–165 Biological clocks. See Chronobiology, decapod crustaceans Brickle curtain, 282 C California Current Oceanic Fisheries Investigations (CalCOFI), 31 Cape hakes, 109–110 Chemosynthetic ecosystems biogenic origin, 61 cold seep Gulf of Mexico, 47–49 Haakon Mosby Mud Volcano (HMMV), 49 cold seeps, 60 geographic and bathymetric localities, 35 hydrothermal vents, 58–59 East Pacific Rise (EPR), 36–38 Mid-Atlantic Ridge (MAR), 43–46 north-east Pacific, 38–43 southern California whale-falls, 50–51 whale-falls, 57 Chronobiology, decapod crustaceans bathymetric ranges, species distribution endogenous rhythms and masking, 206–208 season effect, 205–206 clock centres, 163 continental margin species, 165 internal tides and inertial currents, 170–171 light-intensity cycle, 169–170 western Mediterranean region, 166–169 input pathways, 164 metabolic convergence, 193–194 morphological convergence displacement type, 194–196 rhythm activity, 196–197 multioscillatory model, Limulus polyphemus biological clock types, 159 dual-oscillator organisation, 160–163 light-intensity cycle, 160 locomotor activity, 157–159 nocturnal activity, 160 tidal activity, 159 ontogenetic and gender modulation adulthood rhythmic behaviour, 203–205

305

306

Subject Index

Chronobiology, decapod crustaceans (cont.) benthopelagic species, 199–201 epi- and mesopelagic species, 198–199 nektobenthic and endobenthic species, 201–203 phenotypic trait, 197 photoperiodism, shrimp bimodal activity rhythm, 164–165 reproductive pattern, 165 rhythmic displacement types ecosystem zone, 172 epibenthic and endobenthics, 185–187 nektobenthics, 183–185 pelagic species, 172–183 seabed stratum, 171–172 trawling data bottom-trawl surveys, 187–188 data processing, 188–190 interpretation model, 190–193 Climate change, impact of deep-sea ecosystems, 61 faunal responses, evolutionary constraints, 70–71 high latitudes, 67 past events anoxic basins, 63 faunal oscillations, 62 global warming, 62 microfossils analysis, 62 palaeoceanographic studies, 63 synchronous stylostomellid decline, 63 recent events boom-bust cycles, 66 Multivariate ENSO Index (MEI), 65 Northern Oscillation Index (NOI), 65 time series study, 66–67 shallow-water analogues, 67–70 stochastic events and successional processes, 72–74 Coaxial segment, 40–41 Cold seep Gulf of Mexico hydrocarbon and saline seeps, 47 mussel, 48 scleractinians, 49 tubeworm aggregations, 48 Haakon Mosby Mud Volcano (HMMV), 49 Cryptochromes (CRY), 164 D Decapod crustaceans, chronobiology bathymetric ranges, species distribution, 205–208 clock centres, 163 continental margin species, 165–171 input pathways, 164

metabolic convergence, 193–194 morphological convergence, 194–197 multioscillatory model, 157–163 ontogenetic and gender modulation, 199–205 phenotypic trait, 197 photoperiodism, 164–165 rhythmic displacement types, 171–187 trawling data, 187–193 Deep-sea benthic ecosystems biological drivers food-limited environment, 10 particulate organic carbon (POC) flux measurement, 11 phytodetritus, 12 settling particles types, 12 temporal shifts, 13 biological processes and disturbances types, 7 factors, log-log space, 7, 9 plankton surveys, 10 space-time plot, 9 temporal scales, 7–8 broader context climate change, high latitudes, 67 faunal responses, evolutionary constraints, 70–71 past climate change impacts, 62–64 recent climate change impacts, 64–67 shallow-water analogues, 67–70 stochastic events and successional processes, 72–74 chemosynthetic ecosystems cold seep, 46–49 hydrothermal vents, 36–46 whale-falls, 50–51 environmental changes chemosynthetic ecosystems, 57, 60–61 sedimented ecosystems, 54, 57 free-vehicle landers, 5 geological drivers chemosynthesis, 14 hydrothermal activity, 14 sulphate-reducing bacteria, 14 phytodetritus, 6 remotely operated vehicles (ROVs), 5 sedimented environments Abyssal sites, 25–34 Bathyal sites, 15, 17–25 shallow-water vs. deep-water settings, temporal change, 74–76 Diet, Patagonian toothfish, 252–256 Dissostichus eleginoides. See Patagonian toothfish Drosophila melanogaster, dual-circadian oscillator, 160 Dual-oscillator organisation, Limulus polyphemus, 160–163

307

Subject Index E El Nin˜o (EN) events, 22 Endeavour segment, 41–43 Endobenthics ontogenetic and gender modulation, 201–203 rhythmic displacement types, 185–187 Explorer ridge, 38 F Faunal responses, evolutionary constraints, 70–71 Feeding rates, 258 Fishing gears autoline system, 277 catch per unit effort (CPUE), 278 hooks, 276 pot, 278 principal method, 275 Spanish/double-line system, 275 trotlines, 277 types and sizes, 279 Free-vehicle landers, 5 G Geophysical cycles, continental margin internal tides and inertial currents, 170–171 light-intensity cycle, 169–170 Gorda ridge, 38 H Hake fish, European biogeography ancestral Atlantic hake dispersal, 107 distribution and common name of, 101 eastern North Atlantic origin, 103 main discrepancies, 108 Pacific origin, 100 western North Atlantic origin, 102 classification and origin Gadidae family, 99 generas, 99–100 Merluccius, 98–99 fisheries, 112 annual catches fluctuation, 108–109 Atlantic catches, 109–110 Cape and silver hakes, 109–110 importance, 110 Merluccius merluccius Bay of Biscay and Atlantic coast, 114–119 Celtic Sea, 119 distribution and habitat, 112–113 feeding, 121–124 growth, 120–123 North Sea, 119–120 recruitment, 132–135 reproduction, 124–132

taxonomy and identification, 112 northern stock fisheries, 136–137 status and management, 137–139 phylogeny European and African hake, 105–106 phylogenic tree, 103–104 tectonic and oceanic events, 104–105 southern stock fisheries, 139–140 status and management, 140–141 Hydrothermal activity, 14 Hydrothermal vents East Pacific Rise (EPR) Galapagos Spreading Centre (GSC), 36 9 N, 38 13 N, 37–38 21 N, 37 Rose Garden (GSC), 37 Mid-Atlantic Ridge (MAR) broken spur, 44 Lucky strike, 46 Menez Gwen, 45–46 TAG mound, 44 North-East Pacific axial volcano, 41–42 coaxial segment, 40–41 community change, 39 endeavour segment, 41–43 gorda /explorer ridge, 38 north cleft segment, 40 I Illegal, unreported and unregulated (IUU) fishing, 279–280 J Juan de Fuca Ridge (JdF) axial volcano, 41–42 coaxial segment, 40–41 community change, 39 endeavour segment, 41–43 gorda /explorer ridge, 38 north cleft segment, 40 K Killer whale, 284 L Limulus polyphemus, chronobilology biological clock types, 159 dual-oscillator organisation, 160–163 light-intensity cycle, 160 locomotor activity, 157–159 nocturnal activity, 160

308

Subject Index

Limulus polyphemus, chronobilology (cont.) tidal activity, 159 Locomotor activity, Limulus polyphemus, 157–159 M Mercury accumulation, 261–262 Merluccius merluccius, European hake Bay of Biscay and Atlantic coast characteristics, 114 cold water mass, 119 ENACW water masses, 115–116 Galician coastline, 114 geography, 114 swoddies, 117–118 water circulation patterns, 116 Celtic Sea, 119 distribution and habitat, 112–113 feeding, 121–124 growth hypotheses of, 121 males vs. females, 120 mean length (cm) and age, 122–123 North Sea, 119–120 recruitment nursery areas, 132–134 peak spawning season, 135 water temperatures, 135 reproduction adult egg production, 126 asynchronous oocyte development, 129–131 maturity ogives, 127 population assessment advice, 125 population asynchrony, 127–129 quantification factors, 126 relative batch fecundity, 131–132 spawning period, 128 spawning stock biomass (SSB), 124–125 stock reproductive potential (SRP), 125–126 taxonomy and identification, 112 Mesopelagic species, chronobiology, 198–199 Metazoan meiofauna density, 28 N Nektobenthics ontogenetic and gender modulation adulthood behaviour, 204 diel displacements, 201 rhythmic displacement, 175–177 common features with, 184–185 walk-swimming movements, 183–184 Nocturnal activity, Limulus polyphemus, 160

O Ontogenetic changes, parasite fauna, 268 Otolith analyses, 244–245 Oxygen minimum zone (OMZ), 21 P PAP site. See Porcupine Abyssal plain site Parasite infection, 262–266 Parasites, toothfish fauna and host specificity, 262–266 geographical differences, 266–268 ontogenetic changes, 268 Particulate organic carbon (POC) flux, 11 Patagonian toothfish age and growth direct ageing methods, 241–242 estimation, 241 larval and juvenile growth, 247 length-frequency data, 241 otolith-based analyses, 244–245 otolith preparation methods, 242–243 tagging effort, 245–247 validation, 242–244 behaviour baited camera systems, 271 methods, 271 patterns, 272 swimming form and speeds, 272 distribution and life cycle bathymetric distribution, 234–236 determination and abundance, 232–233 geographic distribution, 233–234 recruitment variability, 236 fishery by-catch issues, 280 history, 272–275 illegal, unreported and unregulated (IUU) fishing, 279–280 interactions, seabirds, 280–283 marine mammals interactions, 283–285 methods and gears, 275–279 parasites fauna and host specificity, 262–266 geographical differences, 266–268 ontogenetic changes, 268 physiology antifreeze glycopeptides, 270 buoyancy, 269–270 vision, 270–271 population structure, 238–239 reproduction eggs and larvae, 250–251 fecundity, 248–249 size, maturity, 247–248 spawning, 249–250

309

Subject Index

stock assessments, 285–288 tagging studies and small-scale movements, 240 taxonomy and systematics Eleginops, 230 etymology, 231 morphometric analyses, 232 suborder, nototheniidae, 230 trophic ecology diet, 251–257 feeding rates, 258 foraging behaviour, 258 mercury accumulation, 261–262 predators, 258–261 Pelagic species, chronobiology ontogenetic and gender modulation light and migration, 201 size-based modification, 199–200 rhythmic displacement types, 173–175 benthopelagic, definition of, 172–179 diel vertical migrations, 180 epi- and mesopelagics, 179–180 light control, 180–183 predator and feeding control, 183 Photoperiodism, shrimp bimodal activity rhythm, 164–165 reproductive pattern, 165 Phytodetritus, 12 Plankton surveys, 10 POC. See Particulate organic carbon (POC) flux Porcupine Abyssal plain (PAP) site Amperima event, 26 cluster analysis, 28 fish community, 30 metazoan meiofauna density, 28 north-east Atlantic, 25 polychaetes, 29 target species, 30 time-series data, 27 Predators and feeding control, 183 Natantian decapoda, 195 nektobenthic species, 184 of Patagonian toothfish, 258–261 pelagic environment, 183 sperm whales, 284 visual, 198–199 Q Quaternary sediments, 64 R Remotely operated vehicles (ROVs), 5 Rhythmic displacement types, decapod crustaceans ecosystem zone, 172 epibenthic and endobenthics, 185–187 nektobenthics, 183–185

pelagic species, 172–183 seabed stratum, 171–172 S Seabird mitigation methods, 282 Sedimented ecosystems Amperima event, 54 data availability, 55–56 faunal component, 57 HAUSGARTEN, 54 Shrimp. See also Chronobiology, decapod crustaceans bimodal activity rhythm, 164–165 reproductive pattern, 165 Silver hakes, 109–110 Spawning stock biomass (SSB), Merluccius merluccius, 124–125 Stock assessments, Patagonian toothfish, 285–288 Stock reproductive potential (SRP), European hake, 125–126 T Temporal change, deep-sea ecosystem biological drivers food-limited environment, 10 particulate organic carbon (POC) flux measurement, 11 phytodetritus, 12 settling particles types, 12 temporal shifts, 13 biological processes and disturbances types, 7 factors, log-log space, 7, 9 plankton surveys, 10 space-time plot, 9 temporal scales, 7–8 biological responses, environmental change chemosynthetic ecosystems, 57, 60–61 sedimented ecosystems, 54, 57 broader context climate change, high latitudes, 67 faunal responses, evolutionary constraints, 70–71 past climate change impacts, 62–64 recent climate change impacts, 64–67 shallow-water analogues, 67–70 stochastic events and successional processes, 72–74 chemosynthetic ecosystems cold seep, 46–49 hydrothermal vents, 36–46 whale-falls, 50–51 free-vehicle landers, 5 geological drivers chemosynthesis, 14 hydrothermal activity, 14 sulphate-reducing bacteria, 14

310 Temporal change, deep-sea ecosystem (cont.) phytodetritus, 6 remotely operated vehicles (ROVs), 5 sedimented environments Abyssal sites, 25–34 Bathyal sites, 15, 17–25 shallow-water vs. deep-water settings, temporal change, 74–76 Tidal activity, Limulus polyphemus, 159 Toothfish fishery. See also Patagonian toothfish by-catch issues, 280 history, 272–275 illegal, unreported and unregulated (IUU) fishing, 279–280 interactions, seabirds, 280–283 marine mammals interactions, 283–285 methods and gears, 275–279 Toothfish reproduction eggs and larvae, 250–251

Subject Index

fecundity, 248–249 size, maturity, 247–248 spawning, 249–250 Trawling data, chronobiology bottom-trawl surveys, 187–188 data processing, 188–190 interpretation model, 190–193 Trophic ecology, Patagonian toothfish diet, 251–257 feeding rates, 258 foraging behaviour, 258 mercury accumulation, 261–262 predators, 258–261 V Vessel monitoring systems (VMS), 279 Von Bertalanffy growth parameters, 245–246