No title

Advances in MARINE BIOLOGY VOLUME 47

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Advances in MARINE BIOLOGY Edited by

A. J. SOUTHWARD Marine Biological Association, The Laboratory, Citadel Hill, Plymouth, PL1 2PB, UK

P. A. TYLER School of Ocean and Earth Science, University of Southampton, Southampton Oceanography Centre, European Way, Southampton, SO14 3ZH, UK

C. M. YOUNG Oregon Institute of Marine Biology, University of Oregon, P.O. Box 5389, Charleston, Oregon 97420, USA

and

L. A. FUIMAN Marine Science Institute, University of Texas at Austin, 780 Channel View Drive, Port Aransas, Texas 78372, USA

Elsevier Academic Press 525 B Street, Suite 1900, San Diego, California 92101-4495, USA 84 Theobald’s Road, London WC1X 8RR, UK

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CONTRIBUTORS TO VOLUME 47

James Aiken, Plymouth Marine Laboratory, Prospect Place, Plymouth, PL1 3DH, UK Jack Blanton, Skidaway Institute of Oceanography, Savannah, Georgia 31411, USA Gerald T. Boalch, Marine Biological Association of the UK, Citadel Hill, Plymouth, PL1 2PB, UK R. A. Braithwaite,* North Atlantic Fisheries College, Port Arthur, Scalloway, Shetland ZE1 OUN, UK E. D. Christou, Hellenic Centre for Marine Research, Institute of Oceanography, Anavissos 19013, Attiki, Greece Paul R. Dando, Marine Biological Association of the UK, Citadel Hill, Plymouth, PL1 2PB, UK and School of Ocean Science, University of Wales Bangor, Menai Bridge, Anglesey, LL59 5AB, UK C. Frangoulis, Hellenic Centre for Marine Research, Institute of Oceanography, Anavissos 19013, Attiki, Greece Martin J. Genner, Marine Biological Association of the UK, Citadel Hill, Plymouth, PL1 2PB, UK Nicholas C. Halliday, Marine Biological Association of the UK, Citadel Hill, Plymouth, PL1 2PB, UK Nicholas J. Hardman-Mountford, Plymouth Marine Laboratory, Prospect Place, Plymouth, PL1 3DH, UK Roger P. Harris, Plymouth Marine Laboratory, Prospect Place, Plymouth, PL1 3DH, UK Stephen J. Hawkins, Marine Biological Association of the UK, Citadel Hill, Plymouth, PL1 2PB, UK J. H. Hecq, MARE Centre, Laboratory of Oceanology, Ecohydrodynamics Unit, University of Lie`ge, B6, 4000 Lie`ge, Belgium Ian Joint, Plymouth Marine Laboratory, Prospect Place, Plymouth, PL1 3DH, UK Michael A. Kendall, Plymouth Marine Laboratory, Prospect Place, Plymouth, PL1 3DH, UK Olivia Langmead, Marine Biological Association of the UK, Citadel Hill, Plymouth, PL1 2PB, UK Rebecca Leaper, Marine Biological Association of the UK, Citadel Hill, Plymouth, PL1 2PB, UK *Current

address: School of Ocean Sciences, University of North Wales Bangor, Menai Bridge, Gwynedd, LL59 5AB, UK

vi

CONTRIBUTORS TO VOLUME 47

L. A. McEvoy, North Atlantic Fisheries College, Port Arthur, Scalloway, Shetland, ZE1 0UN,UK Nova Mieszkowska, Marine Biological Association of the UK, Citadel Hill, Plymouth, PL1 2PB, UK Robin D. Pingree, Marine Biological Association of the UK, Citadel Hill, Plymouth, PL1 2PB, UK Henrique Queiroga, Departmento de Biologia, Universidade de Aveiro, Campus Universita´rio de Santiago, 3810-193 Aveiro, Portugal Anthony J. Richardson, Sir Alister Hardy Foundation for Ocean Science, Citadel Hill, Plymouth, PL1 2PB, UK David W. Sims, Marine Biological Association of the UK, Citadel Hill, Plymouth, PL1 2PB, UK Tania Smith, Plymouth Marine Laboratory, Prospect Place, Plymouth, PL1 3DH, UK Alan J. Southward, Marine Biological Association of the UK, Citadel Hill, Plymouth, PL1 2PB, UK Anthony W. Walne, Sir Alister Hardy Foundation for Ocean Science, Citadel Hill, Plymouth, PL1 2PB, UK

CONTENTS

CONTRIBUTORS TO VOLUME 47 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . SERIES CONTENTS FOR LAST TEN YEARS . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . .

v ix

Long-Term Oceanographic and Ecological Research in the Western English Channel Alan J. Southward, Olivia Langmead, Nicholas J. Hardman-Mountford, James Aiken, Gerald T. Boalch, Paul R. Dando, Martin J. Genner, Ian Joint, Michael A. Kendall, Nicholas C. Halliday, Roger P. Harris, Rebecca Leaper, Nova Mieszkowska, Robin D. Pingree, Anthony J. Richardson, David W. Sims, Tania Smith, Anthony W. Walne and Stephen J. Hawkins 1. 2. 3. 4. 5.

Introduction and Historical Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . MBA. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . PML and the Former IMER . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . SAHFOS. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Overview . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

3 9 56 61 76 83 84

Interactions Between Behaviour and Physical Forcing in the Control of Horizontal Transport of Decapod Crustacean Larvae Henrique Queiroga and Jack Blanton 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11.

Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Definitions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Marine Physical Processes and Larval Transport Mechanisms . . . . . . . . . . . . . . . . . . . . . . Cyclic Vertical Migration in the Natural Environment. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ontogenetic Migration and the Extent of Vertical Movements . . . . . . . . . . . . . . . . . . . . . . Significance of Vertical Migration in Dispersal: Evidence from Field Studies . . . . . . . . Proximate Factors Controlling Vertical Migration: Environmental Factors and Endogenous Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Behavioural Control of Vertical Migration: Evidence from Laboratory Studies . . . . . Nonrhythmic Vertical Migration. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Mechanism for Depth Regulation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Modifiers of Vertical Migration Pattern: Temperature, Salinity, and Food . . . . . . . . . .

109 113 118 137 143 148 161 164 186 187 188

CONTENTS

12. Vertical and Horizontal Swimming Velocities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13. Measurements of Horizontal Transport. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

190 192 196 196

Marine Biofouling on Fish Farms and Its Remediation R. A. Braithwaite and L. A. McEvoy 1. 2. 3. 4. 5.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nature and Extent of Problem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The Fouling Community of Fish-Cage Netting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Antifouling Technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

216 218 223 231 241 243 243

Comparison of Marine Copepod Outfluxes: Nature, Rate, Fate and Role in the Carbon and Nitrogen Cycles C. Frangoulis, E. D. Christou and J. H. Hecq 1. 2. 3. 4. 5. 6.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nature of Copepod Outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Factors Controlling the Rate of Copepod Outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Vertical Flux. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Role of Copepod Outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

254 256 263 269 280 285 293 293

Taxonomic Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 311 Subject Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 317

Series Contents for Last Ten 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 meso- and 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. 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.

SERIES CONTENTS FOR LAST TEN YEARS

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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. VOLUME 45, 2003. Cumulative Taxonomic and Subject Index.

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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.

Long-Term Oceanographic and Ecological Research in the Western English Channel Alan J. Southward,* Olivia Langmead,* Nicholas J. Hardman-Mountford,{ James Aiken,{ Gerald T. Boalch,* Paul R. Dando,*,x Martin J. Genner,* Ian Joint,{ Michael A. Kendall,{ Nicholas C. Halliday,* Roger P. Harris,{ Rebecca Leaper,* Nova Mieszkowska,* Robin D. Pingree,* Anthony J. Richardson,{ David W. Sims,* Tania Smith,{ Anthony W. Walne,{ and Stephen J. Hawkins*

*Marine Biological Association of the UK, Citadel Hill, Plymouth, PL1 2PB, UK { Plymouth Marine Laboratory, Prospect Place, Plymouth, PL1 3DH, UK { Sir Alister Hardy Foundation for Ocean Science, Citadel Hill, Plymouth, PL1 2PB, UK x School of Ocean Science, University of Wales Bangor, Menai Bridge, Anglesey, LL59 5AB, UK

1. Introduction and Historical Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. MBA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Temperature and salinity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Currents and circulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Nutrients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4. Phytoplankton and productivity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.5. Zooplankton, larval stages of fish, and pelagic fish . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.6. Intertidal observations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.7. Demersal fish . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.8. Benthos . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. PML and the former IMER . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Series at station L4 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Bio-optics and photosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

ADVANCES IN MARINE BIOLOGY VOL. 47 0-12-026148-0

3 9 13 16 19 24 31 43 48 54 56 56 58

ß 2005 Elsevier Ltd. All rights of reproduction in any form reserved

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4. SAHFOS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. CPR methods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Consistency issues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Plankton and mesocale hydrography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4. Phytoplankton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5. Zooplankton species routinely identified . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.6. Zooplankton and ichthyoplankton not routinely identified. . . . . . . . . . . . . . . . . . . . . . . 5. Overview . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Data Availability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

61 63 70 72 73 74 75 76 82 83 84

Long-term research in the western English Channel, undertaken by the marine laboratories in Plymouth, is described and details of survey methods, sites, and time series given in this chapter. Major findings are summarized and their limitations outlined. Current research, with recent reestablishment and expansion of many sampling programmes, is presented, and possible future approaches are indicated. These unique long-term data sets provide an environmental baseline for predicting complex ecological responses to local, regional, and global environmental change. Between 1888 and the present, investigations have been carried out into the physical, chemical, and biological components (ranging from plankton and fish to benthic and intertidal assemblages) of the western English Channel ecosystem. The Marine Biological Association of the United Kingdom has performed the main body of these observations. More recent contributions come from the Continuous Plankton Recorder Survey, now the Sir Alister Hardy Foundation for Ocean Science, dating from 1957; the Institute for Marine Environmental Research, from 1974 to 1987; and the Plymouth Marine Laboratory, which was formed by amalgamation of the Institute for Marine Environmental Research and part of the Marine Biological Association, from 1988. Together, these contributions constitute a unique data series—one of the longest and most comprehensive samplings of environmental and marine biological variables in the world. Since the termination of many of these time series in 1987–1988 during a reorganisation of UK marine research, there has been a resurgence of interest in long-term environmental change. Many programmes have been restarted and expanded with support from several agencies. The observations span significant periods of warming (1921–1961; 1985– present) and cooling (1962–1980). During these periods of change, the abundance of key species underwent dramatic shifts. The first period of warming saw changes in zooplankton, pelagic fish, and larval fish, including the collapse of an important herring fishery. During later periods of change, shifts in species abundances have been reflected in other assemblages, such as the intertidal zone and the benthic fauna.

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Many of these changes appear to be related to climate, manifested as temperature changes, acting directly or indirectly. The hypothesis that climate is a forcing factor is widely supported today and has been reinforced by recent studies that show responses of marine organisms to climatic attributes such as the strength of the North Atlantic Oscillation. The long-term data also yield important insights into the eVects of anthropogenic disturbances such as fisheries exploitation and pollution. Comparison of demersal fish hauls over time highlights fisheries eVects not only on commercially important species but also on the entire demersal community. The eVects of acute (‘‘Torrey Canyon’’ oil spill) and chronic (tributyltin [TBT] antifoulants) pollution are clearly seen in the intertidal records. Significant advances in diverse scientific disciplines have been generated from research undertaken alongside the long-term data series. Many concepts in marine biological textbooks have originated in part from this work (e.g. the seasonal cycle of plankton, the cycling of nutrients, the pelagic food web trophic interactions, and the influence of hydrography on pelagic communities). Associated projects currently range from studies of marine viruses and bacterial ecology to zooplankton feeding dynamics and validation of ocean colour satellite sensors. Recent advances in technology mean these long-term programmes are more valuable than ever before. New technology collects data on finer temporal and spatial scales and can be used to capture processes that operate on multiple scales and help determine their influence in the marine environment. The MBA has been in the forefront of environmental modelling of shelf seas since the early 1970s. Future directions being pursued include the continued development of coupled physical-ecosystem models using western English Channel timeseries data. These models will include both the recent high-resolution data and the long-term time-series information to predict eVects of future climate change scenarios. It would be beneficial to provide more spatial and highresolution temporal context to these data, which are fundamental for capturing processes that operate at multiple scales and understanding how they operate within the marine environment. This is being achieved through employment of technologies such as satellite-derived information and advanced telemetry instruments that provide real-time in situ profile data from the water column. 1. INTRODUCTION AND HISTORICAL BACKGROUND The western English Channel is in a boundary region between oceanic and neritic waters. It also straddles biogeographical provinces, with both boreal/ cold temperate and warm temperate organisms present. Thus it is not surprising that there has been considerable fluctuation of the flora and fauna in the area since formal scientific work began in the late nineteenth century. This review outlines the long-term research that has been conducted

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Figure 1 The Plymouth research vessels that have carried out chemical and physical work in the western English Channel and sampled plankton, fish, and benthos for the long-term studies. (A) the ocean-going steam yacht Oithona, 83 ft (26 m) long, undergoing conversion in Millbay Docks in 1901, sampling from 1902 to 1921; (B) the 115-ft (36-m) North Sea steam trawler Huxley that sampled from 1903 to 1909; (C) the 88-ft (27-m) ex-Naval steam drifter/trawler Salpa, that sampled from 1921 to 1939; (D) the 90-ft (28-m) motor fishing vessel Sabella, leased from the Navy,

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in the western English Channel by the laboratories in Plymouth, the Marine Biological Association of the United Kingdom (MBA), the Institute for Marine Environmental Research (IMER), the Plymouth Marine Laboratory (PML), and the Sir Alister Hardy Foundation for Ocean Science (SAHFOS), whose eVorts complement one another. After the historical background is summarized, data held at Plymouth are described, and details of survey methods, sites, and time series are given. Major findings from long-term studies are summarized, and their limitations are outlined. Current research, with the recent resurgence and expansion of many sampling programmes, is presented, along with future approaches, illustrating how these important and unique data can aid in understanding and predicting complex ecological responses to a changing environment. The review outlines the historical development of ideas and techniques and also charts the vagaries of research funding priorities that have fluctuated as much as the ecosystem itself. Investigation of the western English Channel began when the Plymouth Laboratory of the MBA was opened in 1888. A condition attached by the U.K. Government to substantial financial aid given in the foundation years of the MBA stated that researchers should ‘‘aim at practical results with regard to the breeding and management of food fishes’’ (Southward, 1996). Hence, even before the MBA laboratory building was completed, studies were initiated on the eggs and larval stages of many fish species (Cunningham, 1892a,b,c,d,e,f; Lankester et al., 1900; Garstang, 1903), and there was a study of mackerel that involved bringing over fresh Boston mackerel, in the fast transatlantic passenger ships that then called at Plymouth, for comparison of their meristic characters with the various European races that were also assessed (Garstang, 1898). Although much preliminary work was carried out with the 60-ft (19-m) ‘‘Busy Bee’’ from 1895 to 1901, systematic collection of data on zooplankton, including fish eggs and larvae, became easier when the MBA obtained reliable vessels capable of venturing into open waters (Figure 1): first Oithona in 1902, then Huxley in 1903 (Garstang, 1903; Southward, 1996). These vessels were used to carry out exploratory surveys of the southern North Sea, the English Channel, and the continental shelf that sampled from 1946 to 1953; (E) the 60-ft (19-m) ex-Naval motor fishing vessel Sula that sampled from 1948 to 1972, seen here winning her class at the Brixham trawler race in 1971; (F) the 60-ft (19-m) trawler Squilla that sampled from 1973 to 2003, seen here from Sarsia on a joint fishing operation in October 1979; (G) the specially designed 128-ft (39-m) Sarsia that sampled from 1953 to 1981, seen here on a visit to the RoscoV Laboratory in Brittany in 1978; (H) the 42-ft (13-m) fast motor launch Sepia that sampled plankton from 1968 to 2004, seen in 1979. There was a converted trawler, Frederick Russell, 143 ft (44 m), in use by the Marine Biological Association from 1981 to 1982, as a replacement for Sarsia, but it was converted to general oceanographic research in 1982 and was not available for time series work oV Plymouth afterward. Photos from Marine Biological Association archives.

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west of Plymouth and represented the English section of the contribution by the United Kingdom to the programme of the International Council for the Exploration of the Sea (ICES). The history of ICES investigations has been reviewed by Rozwadowski (2003). The Plymouth cruise programmes for ICES were partly motivated by the early recognition that continental shelf waters influenced the hydrography and biological communities of the English Channel (Lankester et al., 1900). Results of the plankton surveys from 1903 to 1909 were published semiquantitatively in government papers (Gough, 1905, 1907; Bygrave, 1911), providing a foundation for later, fully quantitative studies (Southward and Roberts, 1987). Early interest by Allen (1922) regarding ‘‘natural fluctuations . . . and the conditions which influence them,’’ coupled with the belief that ‘‘life of the sea must be studied as a whole’’ led to establishment of some of the time series, including that of Russell (1933, 1935a, 1936) on zooplankton and larval fish. Many of the series involved repeat sampling of the ICES stations, some of which had been set up with a chartered tug as early as 1899 (Lankester et al., 1900). Other studies were not designed to be the basis for long-term datasets; the series evolved after early scientists recorded sampling locations, methods, and findings, which were used for comparison by later workers. The benthic data set originated in this way, with historic baseline surveys (Allen, 1899; Smith, 1932) revisited several decades later (Holme, 1961, 1966a). Similarly, the intertidal surveys were built on the classic surveys of Moore (1936), Fischer-Piette (1936), and Moore and Kitching (1939). The early quantitative surveys of demersal fish carried out in 1913–1914 and 1921–1922, with detailed records of catches and sizes, also provided an accurate baseline for later work (Clark, 1914, 1920). A programme of population studies on the Plymouth herring fishery (Figure 2) began in 1913 and was continued up to 1936 (Orton, 1916; Ford, 1933). When the herring fishery declined in the 1930s, interest shifted to a comprehensive study of another abundant pelagic fish in the area, the mackerel (Steven and Corbin, 1939; Steven, 1948, 1949, 1952; Corbin, 1950), which had previously been the subject of less detailed studies going back to the early years of the MBA (Ridge, 1889; Calderwood, 1891). The failure of the herring fishery after 1936, the detection of large changes in the plankton (Russell, 1935a,b), and the replacement of the herring stock by pilchard (Cushing, 1961) showed the importance of continuing these programmes. During World War I (1914–1918), sampling was interrupted when research vessels were requisitioned for the Royal Navy. After 1918, increased funding from the U.K. Government Development Commission allowed programmes to be greatly expanded when research restarted. Work at sea ceased again during World War II (1939–1945), when vessels were again requisitioned by the Navy and fishing activity and sampling were restricted by hostilities.

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Figure 2 Part of the fleet of North Sea steam drifters that came round to fish oV Plymouth, landing herring at the fish market quay in Sutton Harbour, winter 1925. This fishery was virtually extinct by 1937.

Throughout the next 40 years, systematic sampling of the western English Channel was continued by a succession of research vessels (Figure 1), with relatively little disruption. Several expansions were related to advances in technology. For example, in the 1970s, continuous profiling instruments for temperature, salinity, chlorophyll a fluorescence, autoanalysis of inorganic nutrients, and water transparency were introduced as well as underway measurements of all properties along the transect from Plymouth to E1 (Figure 3). The 1980s saw an increase in the number of marine science organisations in Plymouth. The Institute for Marine Environmental Research (IMER) was created in 1970 through the merger of a number of units, the largest of which was the Edinburgh Oceanographic Laboratory, which was then the home of the Continuous Plankton Recorder Survey. There was seen to be a national need for coastal and marine research to be consolidated at one site. The Continuous Plankton Recorder Survey (CPR) had been in operation since 1932 and started sampling in the English Channel in 1957, although it then operated from Edinburgh under the aegis of the Scottish Marine Biological Association. The CPR survey moved to Plymouth in 1976, where it became a major part of IMER. The history of the CPR survey is detailed by Reid et al. (2003). In 1987–1988, there was a major change in funding priorities, and all current MBA long-term series were terminated, with the exception of

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Figure 3 The major long-term sampling stations oV Plymouth, both historic and current. The grey lines mark the Plymouth inshore fishing grounds, shown in larger scale on Figure 27. Station E1 is at 508020 N, 48220 W, nominal depth 72 m.

intertidal studies, which were maintained on a reduced scale without formal funding. The change in funding coincided with creation of the PML in 1988, formed by a merger of IMER and a substantial part of the MBA, although the MBA also retained a separate identity. Many other time series around the world were stopped or curtailed in the 1970s and 1980s because monitoring the environment was seen as poor science by administrators, compared with short-term projects involving ‘‘process’’ studies (Duarte et al., 1992). This attitude altered only in the late 1990s, when the eVects of climate change were seen as important both scientifically and politically.

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Shortly after the merger to form PML, support for the CPR survey was found. In 1990, the SAHFOS was set up as a charity to continue the CPR surveys that had been under threat of being discontinued. Sampling at the coastal station L4 was initiated by PML in 1988, when the MBA series farther oVshore was stopped. Initially, no formal time series was proposed; rather, the L4 time series was developed and maintained through a combination of diVerent research projects, notably phytoplankton and zooplankton species composition, and partly as a component of international programmes, such as Land-Ocean Interaction Study (LOIS) and Global Ocean Ecosystem Dynamics (GLOBEC). Some of the MBA zooplankton sampling at E1 and L5 was resumed as an emeritus venture in 1995. Since 2001, most of the original Plymouth time series have been restarted with funding from a variety of sources, but the period between 1987 and when the full restarts began remains the longest interruption in most of the western English Channel long-term series.

2. MBA The ICES E and L stations (including E1 and L5) were set up when the MBA undertook the English share of the international investigations on behalf of the United Kingdom, following the formation of ICES. This work was carried out by the MBA between 1902 and 1909, working from both the Plymouth Laboratory and a laboratory established at Lowestoft. Station E1 is situated about 22 nautical miles (nm) southwest of Plymouth on a transect that passes through the L stations and ends at Ushant (Figures 3–5). It is well stratified in summer (Harvey, 1923, 1925; Pingree and GriYths, 1978; Southward, 1984). Figure 6 shows satellite pictures of surface temperature in the Celtic Sea in summer and winter. Figure 7 is a satellite picture of sea surface temperature around E1 on a calm day in July; the oVshore water, including E1, is stratified, but the water column becomes increasingly mixed toward the shoreline, with relatively cold surface water inshore. The earliest records for E1, dating back to 1903, are for plankton, temperature, and salinity (Gough, 1905, 1907; Matthews, 1905, 1906, 1911, 1917a,b; Bygrave, 1911). Pioneering work at this station quantified changes in inorganic phosphate in the English Channel, documenting high levels of the phosphate in winter that decreased in spring and were related to changes in plankton abundance (Sections 2.3 and 2.4). Sampling was generally maintained on a monthly basis, except during the gaps described in Section 1 (Figure 8). Station L5, 2 nm west of the Eddystone reef (Figure 3), is less strongly stratified in summer than E1 (Armstrong et al., 1970, 1972, 1974;

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Figure 4 Map of the English Channel showing the Marine Biological Association surveys in 1899–1900, the grid of English Channel stations used for the International Council for the Exploration of the Sea surveys from 1903 to 1909 (the ‘‘E’’ stations), and the line of three stations sampled by the MBA in 1921–1938.

Southward, 1984), but it is almost completely free of estuarine influence, and its close proximity to Plymouth means that regular sampling is possible. This site was favoured historically because, being close to the Eddystone lighthouse, it could be easily and reliably located. It has been used mostly for sampling phytoplankton, zooplankton, and planktonic fish stages. The earliest records for zooplankton and studies of fish larvae date back to the end of the nineteenth century, although not all data are from this particular site (Cunningham, 1892b; Holt and Scott, 1898; Browne, 1903; Gough, 1905, 1907; HeVord, 1910; Bygrave, 1911; Clark, 1914, 1920; Allen, 1917). Regular quantitative sampling of mesozooplankton and planktonic fish larvae began in 1924, at weekly intervals, 2 nm east of the Eddystone reef at Station A (Russell, 1925, 1930b, 1933, 1935a). Sampling was relocated later to L5 to maximize ship time, as L5 was en route to E1 (Figure 3, Table 1; Southward, 1970; Southward and Boalch, 1986). On occasion, in bad weather, some of the weekly samples had to be taken at L4. The ICES work in 1902–1909 was carried out over a network of 22 stations extending through the eastern and western basins of the English Channel out into the nearby Celtic Sea (Figure 4; Gough, 1905; Matthews, 1905). From 1921 to 1938, a reduced version of this grid running through the line of stations southwest from Plymouth to Ushant, was sampled by Harvey and Atkins, and later Cooper; (Southward, 1996). Cooper (1961)

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Figure 5 The various station grids used for MBA surveys in the western Channel in the second half of the twentieth century. (A) in 1959 (dotted line) and in 1960 (solid line); (B) in 1961 (solid line) and 1962 (dotted line), with extra stations in 1964 (triangles); (C) from 1965; (D) reduction to 16 stations from 1967, with revised station 9 from 1974 (open circle); (E) in 1979 (solid line) and 1980 (broken line); (F) the stations used for 1981 to 1983 (data from Armstrong and Butler, 1962; Armstrong et al., 1970, 1972, 1974; Boalch, 1987).

investigated a grid of stations across the mouth of the western Channel and across the Celtic Sea on cruises in 1950. A smaller Channel grid was established in 1959 following concerns that station E1 was not typical of conditions in the western Channel (Cooper, 1958b). This was a grid of 42 stations

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Figure 6 Computer-integrated satellite monthly surface temperatures in the Celtic Sea and western English Channel in June (top) and January (bottom). In summer, the water column on the northern side of the western English Channel and in the Celtic

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covering an area of 30  45 nm around E1 (Armstrong and Butler, 1962). Chemical and physical conditions varied considerably from station to station, so in 1961 this grid was extended to cover the mouth of the English Channel; it was modified again in 1964, 1967, 1974, 1979–1980, and 1981– 1983 (Figure 5; see Armstrong et al., 1970, 1972, 1974). Findings from this work are included in Sections 2.1, 2.2, and 2.3.

2.1. Temperature and salinity Early analyses of temperature data for E1 did not detect inter-annual changes (Atkins and Jenkins, 1952; Cooper, 1958a). This apparent absence of variability may have been a result of using the integral mean for the whole water column at this strongly stratified station (Figure 7). A later analysis of the records over a longer period, using surface values only, found a rise of 0.5 8C between 1921 and 1959 (Figure 9; Southward, 1960). A somewhat smaller rise was found for surface temperatures taken in Plymouth Sound for the Plymouth Medical OYcer of Health (Cooper, 1958a). Subsequent analyses of temperatures for the period from 1900 until 1970 showed an increasing trend up to 1961, followed by a period of cooling (Southward and Butler, 1972). A comprehensive analysis of these data was carried out by Maddock and Swann (1977) in conjunction with a study of both sea and air temperature and rainfall over a wider area. These authors concluded that although long-term temperature trends appeared small when compared with seasonal cycles, such changes could be highly significant and related to reported changes in species distributions (Russell et al., 1971; Southward et al., 1975, 1988a,b). Good correlation of temperature trends was found when comparing the Plymouth data with observations in Guernsey and in the northern Bay of Biscay (Figure 9; Southward et al., 1988a). Annual and seasonal variations of salinity at E1 and the Seven Stones light vessel have been described and discussed by Pingree (1980). Seasonal changes in salinity reflect the total freshwater flux from river run-oV, precipitation minus evaporation, and water movement. Water movement has

Sea is stratified, as shown by high surface values (red). In the southern part of the western English Channel, also oV the northern tip of west Cornwall, the water is mixed and cooler at the surface. In winter, temperatures are more uniform, except for the Bristol Channel, the Bay of St. Malo, and Lyme Bay, which are colder. (Advanced Very High Resolution Radiometer [AVHRR] images received by the Natural Environment Research Council Satellite Receiving Station at the University of Dundee, processed by the Natural Environment Research Council Remote Data Sensing Analysis group, Plymouth Marine Laboratory.)

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Figure 7 Satellite image. The region surrounding the serial sampling station, E1, showing surface temperature in July. The highest temperature, dark red, indicates full stratification of the water column. (Advanced Very High Resolution Radiometer

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Figure 8 Quantitative long-term data for the western English Channel held by the Marine Biological Association, Plymouth Marine Laboratory, and the Sir Alister Hardy Foundation for Ocean Science (SAHFOS CPR). Black bars indicate data held as computer files, grey bars are lost data and white denotes gaps in the series.

relatively more eVect on salinity change than on temperature change, and therefore salinity more readily reflects circulation changes. The historical data set of salinity measurements has allowed quantitative estimates to be made of the mean flow through the English Channel from west to east, and a value of 0.14 Sverdrup (Sv) was determined (1 Sv ¼ 106 m3 s1). In the winter, the mean flow provides a significant warming contribution to the monthly heat budget (20% in the eastern English Channel). The causes of interannual variability of temperature and salinity in the western English Channel have been linked to several climatic factors. Records from 1924–1974 show cyclical patterns synchronised with the 11year sunspot index (Southward et al., 1975). This relationship was not apparent in later years (Southward, 1980), although overall trends in the

[AVHRR] image received by the National Environment Research Council Satellite Receiving Station at the University of Dundee, processed by the National Environment Research Council Remote Data Sensing Analysis group, Plymouth Marine Laboratory.)

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Table 1 Sampling methods for zooplankton in the Marine Biological Association long-term data series Stations (see Figure 3) Tow speed and time for double oblique tow to 40 m depth Tow stabilization Net mesh Net aperture dimension Counting techniques

Pre-1958 Post-1958 Pre-1958 1958–1978 1978 onward Post-1958 Pre-1962 Post-1962 Pre-1981 Post-1981 Post-1985 All years

A (Russell, 1933) L5 30 minutes at 2 knots 20 minutes at 4 knots 20 minutes at 2 knots Scripps depressor (Southward, 1970) stramin, irregular holes 0.8 mm terylene, regular holes 0.7 mm 2 m diameter, round 1 m diameter, round 0.9 m2, square (Southward, 1984) Samples preserved in 5% formaldehyde; successively larger subsamples taken with Stempel pipettes or by dipping ladle; counts adjusted to nominal 4000 m3 water filtered (Russell, 1976; Southward and Boalch, 1986)

English Channel and Bay of Biscay indicated a general climatic forcing (Southward et al., 1988a). More recent studies have shown that the strength of the NAO also influences temperature (Alheit and Hagen, 1997; Sims et al., 2001). There are likely to be opposing tendencies between the North Atlantic Oscillation (NAO) and salinity change because positive winter NAO is associated with both an increase in rainfall and an increase in westerly wind strength, which will transport saltier surface water into the region.

2.2. Currents and circulation It has always been assumed from drift-bottle data (Carruthers, 1930) that there is a flow through the English Channel from west to east, although current meter observations from light vessels showed diVering seasonal trends (Carruthers et al., 1950, 1951). The situation is, in fact, more complicated than it appears from these investigations. From inspection of salinity and temperature charts, Matthews (1914) deduced that there was a counterclockwise (cyclonic) swirl in the Celtic Sea, partly extending across the mouth of the English Channel. Harvey (1929) attempted to employ geopotential topographies to calculate water flow in the Celtic Sea without the benefit of computers or even mechanical calculators, assuming a level of no motion. He showed a flow to the north across the mouth of the English Channel and generally northwest across the Celtic Sea. To some extent,

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Figure 9 Annual mean sea surface temperature trends in the western English Channel compared with the Bay of Biscay. Top, Marine Biological Association data for E1, corrected for missing years by calculated annual mean diVerences from nearby stations (the Seven Stones light vessel, Plymouth Sound, and along a line from Plymouth to Guernsey); middle, integrated data from square 508 to 51 8N, 48 to 5 8W (Hadley Centre for Climate Research); bottom, integrated data for Bay of Biscay square, 458 to 50 8N, 58 to 10 8W (Hadley Centre for Climate Research). The heavy lines are 5-year smoothed values. There is an overall similarity in the trends; the Bay of Biscay area is warmer than the western English Channel and the warm period in the 1940–1950s was more pronounced in Biscay. The Marine Biological Association data, from mostly single monthly observations, show wider extremes than the data for square 50–51, which is averaged from many observations each month by merchant ships and other vessels.

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zooplankton distribution seemed to be related to this pattern of water flow, and it was suggested that latitudinal variation in the position of the swirl might influence the movement of northwestern and southwestern plankton indicators from the Celtic Sea into the Channel (Southward, 1962). Cooper (1960, 1961) used geopotential topographies and temperature salinity diagrams from cruises in 1950 to suggest a counterclockwise current pattern in the Celtic Sea in the spring and illustrated ‘‘streamlines’’ of flow into the western Channel from the southwest in August. None of these early investigations employed moored current meters. An extended programme of in situ current measurements coupled with modelling studies for the South West Approaches was begun in 1973, with moorings for continuous measurement of currents and temperature being deployed at E1 and E2 in 1974 (Pingree and GriYths, 1977). The programme was jointly undertaken by the MBA and the National Institute of Oceanography, and these studies established the tidal environment and examined the circulation in the region (Pingree, 1980). Mean northerly to northwesterly currents to the west of the mouth of the English Channel (i.e. Rennell’s Current) were found to be less than 3 cm s1. However, there was little evidence for the south-going component of the swirl on the western side of the Celtic Sea that was deduced by Matthews (1914). Data from drogued Argos drifting data buoys (Pingree et al., 1999) showed a significant northerly coastal current from near the Isles of Scilly to Lundy Island. In addition to northerly flow near the Isles of Scilly, a clockwise circulation was measured around these islands. This circulation is induced by the local rotary tidal streams (Pingree and Mardell, 1986), and similar tidal eVects force a local northward flow around Lands End (Pingree and Maddock, 1985). Measured flows were directed southwestward along the south coast of Ireland and then northwest in a strengthening Valencia coastal current. However, any overall continuity of flow will tend to be lost across St. George’s Channel (Cooper, 1961), with exchange of water in and out of the Irish Sea. Residual flows on the Celtic shelf are weak, but the mean transport is poleward along the continental slope margin in the West European Continental Slope Current. Some residual current vectors, derived from several sources, and an idealized summary diagram are given by Pingree and Mardell (1981) and Pingree and Le Cann (1989). Continental slope currents were measured and modelled, and later studies (Garcia-Soto et al., 2002; Pingree, 2002) linked negative winter NAO conditions with increased continental slope flow and warmer than average temperatures along the slopes and outer shelf, particularly for the winter conditions of 1995–1996. Negative winter NAO conditions are associated with southerly or southeasterly winds in the region and so will tend to add a wind-driven component to a slope current forced by density and dynamic height gradients.

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To understand the large variability in the measured currents, modelling studies were developed to deduce wind-induced circulation in the western English Channel (Pingree and GriYths, 1980). These numerical simulations were for vertically integrated currents or transports driven by a steady uniform wind stress. The models could not simulate important measured diVerences between surface and bottom currents or events in some embayed situations, where the surface currents and bottom currents can be opposed. A southwest wind forces eastward flow along the English Coast in Eddystone Bay and Lyme Bay. A flow is also driven along the north Cornwall Coast and the Irish Coast toward the Irish Sea. However, with a southwest wind stress, the model shows that there is little net transport of water through the Irish Sea and that coastal flows from there are returned southward through the St. George’s Channel and southward in the deeper central water regions of the northern Celtic Sea. The model showed the importance of wind acting over a wide shelf region (including the North Sea) in forcing transports and establishing flow origin or distant influence of local conditions. For example, for a given wind strength, southerly winds are most eVective in driving a net transport of water from the English Channel through the Straits of Dover and into the southern North Sea, whereas westerly winds are least eVective. Water driven along the English Channel coast by westerly and west-south-westerly wind fields has previously had a more northern origin or influence, whereas southerly winds tend to collect water in the entrance to the Channel that has originated from the Armorican Shelf region. This interpretation has considerable significance for the concept of plankton indicator species derived from northwestern and southwestern sources (Southward, 1962, 1980).

2.3. Nutrients The nature of the nutrient data collected oV Plymouth reflects the development of quantitative measurement techniques in marine chemistry and the evolution of the ‘‘agricultural’’ hypothesis that production in the sea was controlled chiefly by inorganic nitrate and phosphate. The earliest phosphate measurements were made in 1916 in Plymouth Sound (Matthews, 1917a,b). Regular inorganic phosphate measurement began at E1 in 1924 when quick and reliable techniques were developed (Atkins, 1923, 1925, 1926a, 1928, 1930), with further modifications taking place in the 1950s (Murphy and Riley, 1962). During the 1920s, a combination of changes in phosphate and pH measurements was used as a proxy for primary production, with the first estimate being 1.4 kg of diatoms per square metre integrated through the 72-m water column at E1 between March and July (Atkins, 1923; but see p.20 of this chapter). Nitrate was sampled sporadically

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Table 2 Hydrographic and chemical sampling and analysis methods employed at E1 (1902–2000) Parameter

Year ranges

Method

Inorganic phosphate

Pre-1938 Tin (II) chloride method (Atkins, 1923) 1948–ca. 1965 Tin (II) chloride method (Harvey, 1948) ca. 1965–1987 Ascorbic acid method (Butler et al., 1979; Murphy and Riley, 1962) Dissolved organic 1950s–1962 Harvey’s method (Harvey, 1955) phosphorus ca. 1962–1987 Photocombustion technique (Armstrong and Tibbitts, 1968) Nitrate Pre-1938 Reduced strychnine method (Cooper, 1932) 1966–1987 Cadmium copper reduction to nitrite (Butler et al., 1979; Wood et al., 1967) Dissolved organic 1962–1987 Photocombustion technique (Armstrong and nitrogen Tibbitts, 1968) Sea surface To 1987 Insulated water bottle, then Lumby sampler temperature and bathythermograph Post-1995 Electronic thermometers fitted on research vessels or conductivity–temperature–depth probe (CTD) Subsurface sea To 1987 Reversing water bottles with thermometers temperature profile and bathythermograph Post-1995 CTD

from 1925 (Harvey, 1926) but was not routinely measured until 1974, when a more reliable method was developed (Wood et al., 1967; Butler et al., 1979). Measurement methods changed several times throughout the series as new and more reliable techniques were developed (Table 2; Figures 10–12; see Joint et al., 1997). With the introduction of the photocombustion technique (Armstrong and Tibbitts, 1968), dissolved organic nutrients could be quantified, greatly enhancing understanding of nutrient dynamics (Figure 13; Butler et al., 1979). The measurements of inorganic phosphate made by Atkins from 1924 to 1930 were diYcult to relate to those of later years, which were carried out by diVerent analysts with modified methods. Joint et al. (1997) have shown that Cooper (1938a) overestimated the correction needed for salt error in Atkins’s analyses. Figure 10A gives the corrected winter maxima, showing the decline from 1929 to 1938 and the return of higher maxima from 1972 to 1984. Figure 10B shows integrated primary production from 1964 to 1984 for comparison with the phosphate values. In eVect, there were slight increases in winter phosphate and primary production after the onset of the cold spell that began in 1962. Seasonal changes in nutrients at E1 are shown in Figure 11, averaged for long periods, and Figure 12 gives examples of nutrient distribution over a

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Figure 10 Nutrients and phytoplankton production. (A) the winter maximum of dissolved reactive (‘‘inorganic’’) phosphate at E1, 1924–1984, sampling was not possible from 1939 to 1947; (B) integrated annual carbon fixation at E1, 1964–1984, as grams of 14C fixed per metre square surface per annum (unpublished compilation of data).

wider area in the western English Channel and Celtic Sea. Analysis of dissolved inorganic nutrients shows they vary inversely with the inorganic form, so that the total quantity in solution remains fairly constant (Butler et al., 1979). The relative seasonal changes in nitrate and dissolved organic nitrogen, averaged for 1969–1977, are shown in Figure 13. Seminal early publications resulting from nutrient research at station E1 include that of Harvey (1927), who demonstrated that the winter ratio of nitrate to phosphate in the English Channel was very similar to that in deep water in the Atlantic. Later, a ratio of 15:1 was proposed as the constant, and it was suggested that ‘‘the anomaly of the nitrate-phosphate ratio’’ (Cooper, 1938a,b,c) be defined as the amount by which the nitrate:phosphate ratio diVered from 15. This ratio is very close to the now widely accepted Redfield ratio of 16:1 (Redfield et al., 1963). Jordan and Joint (1998) reexamined the historical E1 data, highlighting the high degree of variability in nitrate:phosphate ratios, particularly during midsummer, when, in a significant number of years, the values of phosphate increased for short periods of time while nitrate concentrations remained low. Although these changes were discussed in relation to phytoplankton

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Figure 11 Long period mean seasonal distributions by depth at station E1 of dissolved inorganic nutrients: (A) phosphate averaged for 30 years, (B) silicate averaged for 24 years; and (C) nitrate averaged for 10 years. All as microgram-atoms per litre, reproduced, with permission, from Pingree, R. D., Maddock, L. and Butler, E. I. (1977a). The influence of biological activity and physical stability in determining the chemical distributions of inorganic phosphate, silicate and nitrate. Journal of the Marine Biological Association of the United Kingdom 57, 1065–1073; Figure 2.

assimilation and nutrient regeneration, no clear explanation has been determined. Much eVort was made to understand nutrient dynamics in the context of hydrography and biological activity (Pingree et al., 1977a). Early work by Atkins (1926b) recognized the relationship between the spring diatom bloom

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Figure 12 Examples of autumn and winter values of dissolved reactive (‘‘inorganic’’) phosphate from cruises and the Channel Grid as microgram-atoms P per litre. (A) surface values, 18–25/2/1959; (B) the same dates, bottom values showing the water column is well-mixed; (C) values at 10 m, 25–28/10/1965; (D) values at 10 m, 7– 9/12/1965. (Reproduced, with permission, from Southward, A. J. (1962). The distribution of some plankton animals in the English Channel and approaches. II. Surveys with the Gulf III high-speed sampler, 1958–1960. Journal of the Marine Biological Association of the United Kingdom 42, 275–375; Figure 10 and from Armstrong, F. A. J., Butler, E. I. and Boalch, G. T. (1974). Hydrographic and nutrient chemistry surveys in the western English Channel during 1965 and 1966. Journal of the Marine Biological Association of the United Kingdom 54, 895–914; Figures 5 and 15).

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Figure 13 Seasonal changes in inorganic nitrate and dissolved organic nitrogen at station E1, 1969–1977, as monthly mean microgram-atoms nitrogen per litre for the whole water column (reproduced, with permission, from Butler, E. I., Knox, S. and Liddicoat, M. I. (1979). The relationship between inorganic and organic nutrients in seawater. Journal of the Marine Biological Association of the United Kingdom 59, 239–250; Figure 2).

and silica content in seawater, and this work was later further developed by Atkins and Jenkins (1956). Once the seasonal cycle of phytoplankton was understood (see Section 2.4), the characteristic hydrographic conditions promoting bloom onset could be predicted using an analysis of temperature and nutrient vertical distributions from E1 (Pingree and Pennycuick, 1975). The distinctive nutrient signals from each period of the plankton cycle could be determined, together with the degree to which phytoplankton composition (dinoflagellate/diatom) mediates nutrient signals (Figure 14–16; see Pingree et al., 1977a,b). 2.4. Phytoplankton and productivity In his book and his articles on the history of biological oceanography, Mills (1989, 1990, 2001) has discussed in detail the development of nutrient analyses and the measurement of primary productivity at Kiel and at Plymouth. Other historical treatments are covered in the volume edited by Williams et al. (2002). There is no doubt that both the MBA director, Allen, and Garstang, who headed the Lowestoft laboratory from 1903 to 1907, were

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Figure 14 Position of serial stations used for estimation of primary productivity in the western English Channel. (reproduced, with permission, from Maddock, L., Boalch, G. T. and Harbour, D. S. (1981). Populations of phytoplankton in the western English Channel between 1964 and 1974. Journal of the Marine Biological Association of the United Kingdom 61, 565–583; Figure 1). Note that station 2 is the same as E1 and that station 4 is the same as E2; station 7 is 20 nautical miles north of E3.

strongly influenced by the work of V. Hensen and K. Brandt in attempting to assess the problem of production in the sea. In spite of developing nets capable of quantitative measurement, these researches were handicapped by a lack of reliable analytical methods and by the need to concentrate work at sea on fisheries. The removal of the applied fishery work to the government fishery department in 1910 (Mills, 1989; Southward, 1996), and increased financial support from the Development Commission after 1919, enabled new analytical chemical methods to be applied to regular samples obtained by a reliable steamboat (see Section 2.3). The MBA also pioneered culturing of phytoplankton (Allen and Nelson, 1910). Culturing of enriched water samples (Allen, 1919) was developed as an aid to estimating production, allowing quantification of the smallest organisms, which are not retained by phytoplankton nets but can be collected by centrifuging water samples—the nanoplankton of Lohmann (1911) and Gran (1912). This approach was further extended by Parke in the 1950s and 1960s (Marine Biological Association, 1952), but the results remained unpublished at her death. Phytoplankton samples from tow-nets had been analysed for species presence since the 1890s. Early records were semiquantitative (Cleve, 1900; Gough, 1905, 1907; Bullen, 1908; Bygrave, 1911), and included frequent

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Figure 15 Phytoplankton production in the western English Channel for the three stations shown in Figure 14, as monthly mean rate of carbon fixation (grams carbon per metre square per day) averaged for 1964 to 1974. The broken lines show results with values for 1966 omitted (after Boalch, 1987). The scale is the same for each station, with zero baseline.

samples from Plymouth Sound and the Plymouth fishing grounds, as well as less frequently visited stations in the western Channel. Little was published between 1911 and the 1964 Channel Grid project (see following). The most important work to come from this early period was a complete study of the seasonal changes in phytoplankton (Lebour, 1917). This was later followed by a study of phytoplankton dynamics in conjunction with zooplankton, hydrography, and nutrient measurements at L4 (Harvey et al., 1935). The seasonal cycle these workers described is the basis for many reviews and accounts in textbooks (Tait, 1972; Mills, 1989). This innovative, multidisciplinary study showed that zooplankton grazers limited the spring bloom of diatoms, whereas the autumn bloom appeared to be controlled

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Figure 16 Vertical distribution of chlorophyll a from March to October, station E1, 1975–1976, as milligrams per cubic metre. The lower panel shows details of sampling. (Reproduced, with permission, from Holligan, P. M. and Harbour, D. S. (1977). The vertical distribution and succession of phytoplankton in the western English Channel in 1975 and 1976. Journal of the Marine Biological Association of the United Kingdom 57, 1075–1093; Figure 3.)

primarily by light. The results provided a basis for the emerging study of marine productivity measurements. Similar studies were carried out in 1939, and additional measurements were taken in the Western Approaches; findings indicated a high productivity related to vertical mixing of surface with deep oceanic water (Mare, 1940). At this time, chlorophyll measurements were also beginning to be used to estimate phytoplankton biomass (Harvey, 1934a,b; Atkins and Parke, 1951; Atkins and Jenkins, 1953). Characterization of marine optical properties was another important area for early work. It was quickly recognized that attenuation of light in sea water was caused by a combination of absorption and scattering (Atkins, 1926c), with the latter occurring in a predominately forward direction (Atkins and Poole, 1940, 1952). Optical properties of the sea were related to phytoplankton seasonality and depth distribution, and the role of plankton pigments in mediating transmission of blue wavelength light was identified (Atkins and Poole, 1958). The majority of this work was carried out at E1,

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although inshore waters were also investigated (L4, L5). This important work provided the foundation for subsequent marine optics research. After the establishment of the Channel Grid in 1961, phytoplankton studies (counts, measurements of primary production by the 14C method) were added in 1964 to ongoing chemical and physical analyses (Boalch et al., 1969). The number of stations was reduced from 42 to 16 in 1967. Intensive studies were not feasible at all stations, so three stations (2 otherwise known as E1, 4 otherwise known as E2 and 7) were selected for detailed study because of their contrasting hydrography: stratified, mixed, and frontal, respectively (Figures 14 and 15; Boalch et al., 1978; Pingree, 1978; Boalch, 1987). Clear seasonal cycles were found in phytoplankton population structure, and diVerences between stations were related to hydrography. It was not possible to determine long-term trends with these data (Maddock et al., 1981), but productivity varied greatly from year to year, with the timing of maximum growth depending on hydrographic and meteorological conditions (Boalch et al., 1978). Total primary production increased somewhat after 1966 (Boalch, 1987; Figure 10b), which corresponded with measurements of zooplankton biomass at L5 (Russell et al., 1971). This also reflected changes in inorganic nutrient levels (Armstrong et al., 1974) and temperature (Southward and Butler, 1972). Coastal sampling of phytoplankton showed comparable trends, pinpointing two periods when changes were most marked: 1968–1970 and 1983–1985 (Maddock et al., 1989). These patterns could be related to changes in climate and were comparable to those found in other marine taxa (Russell et al., 1971; Southward, 1974a, 1980, 1983, 1984; Southward et al., 1995). Complete characterization of the seasonal succession of phytoplankton using continuous vertical chlorophyll a measurements was an important step and provided the foundation for further work relating biological activity to nutrient chemistry and hydrography (Figures 16 and 17; Pingree et al., 1976; Holligan and Harbour, 1977). Three distinct periods were defined: a nearsurface spring bloom (<4 mg chl m3 at 0–15 m in April); a summer subsurface bloom in the thermocline (2–4 mg chl m3 at 20–25 m in May–September, fueled by regenerated NH4); and a near-surface autumn bloom (<2 mg chl m3 at 0–15 m in late September to October). The spring bloom was dominated by diatoms, which were abundant in the subsurface bloom until May, when dinoflagellates and flagellates began to replace them, in a process completed by midsummer. In the autumn bloom, diatoms again became important. The spring bloom of diatoms usually develops faster than herbivore biomass can increase; consequently, much of the plant biomass falls to the bottom mixed layer and sea floor, later to provide at least a part of the regenerated nitrogen used by the microalgae of the summer phytoplankton. Once this cycle was characterized, it could be related to the diVering physical stability of the water column and temperature (Figures 6 and 7)

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Figure 17 Ocean colour studies to derive phytoplankton distribution and abundance in the Southwest Approaches and Western English Channel were well advanced at the MBA in the early 1980s. The ocean colour data for this CZCS satellite image of 22 June 1981 were processed to show the distribution and abundance of phytoplankton in relation to the physical environment for early summer condtions (Pingree, 1974; Pingree et al., 1982). The delayed seasonal chlorophyll a maximum along the continental slope margin (typically 2 mg m3 in June) and increases in chlorophyll a levels for summer blooms along the Ushant Front off Brittany (yellow) are evident. Low values (blue) in the nutrient depleted surface water of the stratified Celtic Sea and Western English Channel are typically 0.5 mg m3. Sediment loading (red) is obscuring the chlorophyll in some coastal regions.

encountered in the region, and the importance of frontal boundaries as sites of phytoplankton blooms was demonstrated (Pingree et al., 1976, 1978; Pingree and GriYths, 1978). Hydrographic conditions across the English Channel vary from stratified near the English coast, through a transitional region in the center of the Channel, to the Ushant frontal boundary, with a vertically well-mixed zone near the French coast (Pingree, 1978; Le Fe`vre, 1986). These conditions, particularly the degree of vertical stability of the water column, appear to play an important role in the development of dinoflagellate blooms (Holligan and Harbour, 1977; Pingree et al., 1977b; Holligan et al., 1980). Measurements of phytoplankton (Figure 18) and primary production (Figure 15) made at E1 and other Channel grid stations from 1964 to 1984 were part of a Europe-wide investigation into the sardine fishery, organized by the North Atlantic Treaty Organization (NATO) and the International Biological Program (IBP). This period covered marked changes in the

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Figure 18 A century of phytoplankton studies. (A) the diatom Odontella (Biddulphia) sinensis (Greville) Grunow that colonised European waters at the turn of the nineteenth and twentieth centuries. (B) The centric diatom Coscinodiscus wailesii Gran et Angst that replaced Biddulphia as the dominant winter diatom after 1977. (C) The dinoflagellate Gyrodinium aureolum of Hulburt that invaded European waters in the 1950s, abundant, at frontal systems in the western Channel and the cause of certain ‘‘red tides.’’ (D) Fine plankton net in use from Busy Bee in 1899. (E) A similar phytoplankton net in use from Sarsia in 1979, 80 years later. Scales bars for A and B, 100 mm; C, 50 mm (photos A, B and C by G. T. Boalch; D from Marine Biological Association archives, and E by A. J. Southward).

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western English Channel ecosystem. The changes in production and winter phosphate values lagged behind changes in mesozooplankton species and abundance. Nevertheless, during the mid-1970s, and early 1980s, the winter phosphate levels regained the values found before 1930 (after correction according to Joint et al., 1997), and primary production showed a slight increase. The observations indicate the complexity of interactions in the Channel ecosystem and the diYculty of separating the biological and chemical factors used in models. The introduction of remotely sensed information has greatly aided our understanding of spatial patterns in phytoplankton density in the western English Channel, putting in situ measurements in context. Infrared and visible images of the E1 region and South Western Approaches (Figure 6) have been provided for the MBA by the University of Dundee since 1975 and, more recently, by the NERC Remote Sensing Data Analytical Service (RSDAS) in Plymouth. Ocean colour studies were enhanced with the introduction of the Coastal Zone Colour Scanner (CZCS) imagery in 1979–1986 and with Sea Viewing Wide Field-of-view Sensor (SeaWiFS) coverage from 1997. Data were not used for validation but, rather, for planning measurement cruises from Plymouth and observing near-real-time development of plankton blooms in the region. Figure 17 gives an example of the early summer situation in the Celtic Sea and western English Channel. There have been many MBA publications that used the Dundee satellite imagery, both for local studies and for the extended programme to the shelf break and Bay of Biscay. Studies that used the imagery coupled with in situ measurements include Pingree et al. (1982) and Garcia-Soto and Pingree (1998). These authors defined the seasonal distribution and abundance of chlorophyll a at the shelf break and in adjacent shelf and ocean margin environments. Further studies have involved monitoring coccolithophore blooms; a large bloom passing through E1 in June 1992 that aVected the Isles of Scilly was studied using simultaneous in situ measurements from a ship and an aircraft (Sinha and Pingree, 1994; Garcia-Soto et al., 1995). Additional remote-sensing data (altimeter) for sea level and climate change studies were introduced in 1992 in addition to data from the ERS1/2 and TOPEX/Poseidon satellite sensors. The MBA holds an archive of several thousand images from 1975 to 2004, including SeaWiFS data from 1997.

2.5. Zooplankton, larval stages of fish, and pelagic fish Methods used by the MBA for sampling mesozooplankton and planktonic stages of fish are outlined in Southward (1970) and Southward and Boalch (1986). Thirty zooplankton species have been regularly recorded (Table 3; Figures 19, 21–23), corresponding to those observed between 1924 and

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Table 3 List of zooplankton species used as indicators of water conditions in the western English Channel at stations A, L5, and E1, with latest available genus namesa Group

Species

Water body association

Medusae and siphonphores

Aglantha digitalis (O.F. Mu¨ller) Lirope tetraphylla Chamisso and Eysenhardt Muggiaea atlantica Cunningham Nanomia sp. ‘floats’ Tomopteris helgolandica Greef Parasagitta setosa (J. Mu¨ller) Parasagitta elegans (Verrill) Parasagitta friderici (Ritter-Zahony) Calanus helgolandicus Claus Candacia armata Boeck Subeucalanus subcrassus (Giesbrecht) Pareuchaeta hebes (Giesbrecht) Centropages typicus Krøyer Podon spp. Evadne nordmanii Loven Euthemisto gracilipes (Norman) Nyctiphanes couchii (Bell) Meganyctiphanes norvegica (M. Sars) Limacina retroversa (Fleming) Bivalve larvae Clione limacine (Phipps) larvae of Luidia sarsi Duben and Koren Echinoderm larvae and postlarvae Salpa fusiformis Cuvier

Northwestern Southwestern

Polychaetes Chaetognaths Copepods

Cladocerans Amphipods Euphausids Molluscs Echinoderms Tunicates

Doliolidae Appendicularia

Southwestern Northwestern Northwestern Channel Northwestern Southwestern Western Western Southern Western/southwestern Western Northwestern Western Northwestern Northwestern Coastal Western Northwestern Coastal Western/southwestern oceanic South western

a

The list was originally drawn up by Russell (1935a). It has been reviewed and modified by Southward (1962).

1930 (Russell, 1933, 1935a, 1936), with later amendments (Digby, 1950; Southward, 1962). These indicator species were chosen because they were reasonably common in samples, not able to reproduce rapidly, distinctive, and deemed typical of particular water masses. Attention was initially concentrated on the west-to-east longitudinal distribution of zooplankton, from oceanic, through to ‘‘Western,’’ and then to Channel species (Russell, 1935a, 1936). Further sampling led to the detection of relationships between zooplankton and latitude, season, and climate (Southward, 1962), confirmed

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Figure 19 Mesozooplankton sampling. (A) the 2-m net (‘‘ringtrawl’’) in its last configuration, fitted with a terylene mesh; Sarsia, 1972; (B) the 0.9-m square net used for the L5 series from 1975; (C) a modified Kiel multiple closing net, fitted with telemetering of depth, temperature and flow rate, arranged for horizontal tows in 1978 and 1979 (photos by A. J. Southward).

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Figure 20 Sampling oV Plymouth. (A) and (B) W. Garstang testing nets from the steam yacht Busy Bee in 1899, a vertical quantitative net (A) and a horizontal closing net (B). Both of these nets were used for sampling at the ICES stations, 1903–1909. (C) Alister Hardy, helped by W. J. Creese (mate of Salpa) testing a plankton apparatus in 1937; (D) F. S. Russell in the laboratory of Salpa sorting a catch taken by the 2-m net, 1937; (E) conductivity–temperature–depth probe with rosette of

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by later analyses (Southward, 1980; Southward et al., 1995). The original indicator species included north–south species pairings, so factors explaining their occurrence were expanded to include eVects of changing sea temperature (Southward, 1962, 1963, 1980; Russell et al., 1971; Russell, 1973). There has been some criticism of the reliance of the MBA time series on data only from stations L4, L5, and E1, all of which are on the north side of the western Channel. However, there have been several investigations of zooplankton distribution over the whole western Channel and approaches, beginning with Russell (1936). A survey of pilchard and mackerel spawning over the Celtic Sea in 1937–1939 provided further evidence of the distribution of zooplankton indicator species, as well as that of larval fish (Corbin, 1947, 1950). Follow-up surveys of the western Channel and Celtic Sea were made in 1969 and 1979 and were related to the time series at L5 (Southward, 1962, 1980), but removal of ocean-going vessels from local control in 1982 prevented later cruises that had been planned. A survey of pilchard spawning in the Celtic Sea was made in 1975 (Southward and Bary, 1980), and other zooplankton observations were made as part of the hydrographic surveys of the western Channel in 1969 and 1970 and as part of an investigation of pilchard spawning oV Plymouth during the same years (Southward and Demir, 1974). These surveys showed that E1 and L5 plankton records are reasonably representative of the stratified water on the northern side of the western Channel (Southward, 1962), but they confirmed that conditions are diVerent in the southern half of the western Channel, where water is less stratified, and where there is usually only a single peak of phytoplankton (Figure 15). Good agreement has been shown between the pilchard egg counts at L5 and those sampled by the CPR over the western Channel (Coombs and Halliday, 2004). The routine mesozooplankton samples taken weekly oV the Eddystone reef (stations A and L5) have shown dramatic changes in abundance and species composition (Figure 23). Between 1930 and 1936 there was a decline in the chaetognath Parasagitta elegans and associated cold-water plankton (Figures 21 and 22). From 1936 to 1965, these species were replaced by Parasagitta setosa and a warm-water assemblage; this shift in community composition was accompanied by a decline in the abundance of fish larvae and decapod larvae (Figures 21–23) and also reduced catches of cold-water demersal fish (Corbin, 1948, 1949, 1950; Southward, 1962, 1963, 1983, 1984;

Niskin bottles ready to lower from Squilla, 2002; (F) recovering vertical plankton net (WP2) from Sepia at station L4, May 2001. Photos: A, B, C, and D from the Marine Biological Association archives; E, N. Hardman-Mountford; F, T. Smith.

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Figure 21 Examples of mesozooplankton ‘‘indicator’’ species of the western English Channel: (A) the siphonophore, Muggiaea atlantica, a southwestern indicator, abundant in warmer periods; (B) an assemblage of northwestern indicators, including the arrow worm Parasagitta elegans, the medusa Aglantha digitalis, larvae of the starfish Luidia sarsi, the siphonophore Nanomia sp., and euphausids, all abundant in cooler periods; (C) the copepod Pareuchaeta hebes, a western and southwestern indicator; (D) the southwestern warm-water copepod Subeucalanus subcrassus. Scale bars A, C, and D, 1 mm; B, 10 mm (photos by A. J. Southward).

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Figure 22 More mesozooplankton from the serial station L5: (A) eggs of pilchard (Sardina pilchardus) showing the large perivitelline space and the refringent outer membrane that permits easy identification; (B) larvae of flatfish, after absorption of the yolk sac: top, dab (Limanda limanda); middle, brill (Scophthalmus rhombus); bottom, lemon sole (Microstomus kitt); (C) the copepod, Calanus helgolandicus. Scale bars 1 mm (photos by A. J. Southward).

Russell, 1973; Southward and Boalch, 1986, 1994). Further declines were apparent in C. helgolandicus and in euphausids leading to a reduction in the diversity of intermediate trophic levels. Nonclupeid larval fish (Figure 22) were reduced to very low levels from 1930 to 1965. During the period 1926– 1936, herring (Clupea harengus), one of the most commercially important local species (see Figure 2), was replaced by pilchard (Sardina pilchardus) (Cushing, 1961; Russell et al., 1971; Southward et al., 1988a). At the time, these changes (later known as the ‘‘Russell Cycle’’; Cushing and Dickson, 1976) were attributed to reduced Atlantic flow into the English Channel (Kemp, 1938). This was assumed to cause a reduced influx of ‘‘new’’ inorganic nutrients, with the concurrent eVects of decreased primary production and reduced phytoplankton abundance leading to decreases of biomass in all higher trophic levels (Russell, 1933, 1935a; Kemp, 1938). Work in subsequent periods indicated that inorganic nutrient availability was not the

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Figure 23 Examples of long-term data on mesozooplankton abundance at stations A and L5 as monthly means per net haul, corrected to 4000 m3 water filtered. (A) eggs of pilchard (Sardina pilchardus), a warm-water form; (B) the copepod

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primary factor driving these changes, as nutrient levels changed after, not before, the community change (Figure 10; Boalch et al., 1978; Southward, 1980; Southward and Boalch, 1986; Southward et al., 1988a). In eVect, the change in nutrients was a symptom of the change in the community. After corrections to Atkins’s data (Joint et al., 1997), the decline that occurred after 1929 was determined to be smaller than was perceived in the 1930s and afterward (Southward, 1980), but was still a real decline (Figure 10). Events in the 1930s included the end of the local herring fishery and a big increase in pilchard (S. pilchardus). The fishery landings of pilchard in southwest England reflect technological trends and market restraints rather than population abundance, but the planktonic eggs (Figures 22–24) provide a proxy estimate (Southward, 1974b; Southward et al., 1988a,b; Hawkins et al., 2003). Egg abundance oV Plymouth has changed in response to climate events, but it has lagged behind temperature trends by several years. Pilchard eggs were at a low level in the 1920s and then increased remarkably in the 1930s, with a peak from 1940 to 1960 (Figures 23 and 24). There was a low period from 1972 to 1985, following the return to cooler conditions, and then an increase in recent, warm years. Similar trends in pelagic fish were found on a wider regional scale, with large herring catches on the west coast of Sweden and in the northern Bay of Biscay coinciding with those at Plymouth, and also corresponding with severe winters in western Europe and the negative phase of the NAO (Alheit and Hagen, 1997). It is interesting that the herring fishery oV Plymouth did not revive in the cold spell after 1962, possibly because of a lack of source populations that might have recruited to Plymouth. There was a widespread decline in herring populations in other areas in the 1970s, as a result of overexploitation, that eventually led to a moratorium on North Sea catches (Hawkins et al., 2003). The pelagic fish populations oV California have shown considerable fluctuations related both to fishing intensity and climate (Smith and Moser, 2003), but more species of fish are involved in changes there, and it is diYcult to make comparisons with the English Channel. However, as oV California, the species of pelagic fish oV Devon and Cornwall have fluctuated over a long timescale, with the variation driven by changes in the environment. Historical and recent records indicate that herring and pilchard have alternated in abundance as far back as the fifteenth century, with herring being dominant in cooler periods and pilchard taking over in warmer periods, and with mackerel having an intermediate position. In the past,

Calanus helgolandicus, more common in cooler periods; (C) the arrow worms Parasagitta elegans (cold-water northern form) and Parasagitta setosa (intermediate and warm-water species common in the English Channel and North Sea); (D) larval stages of decapod crustaceans (Marine Biological Association database).

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Figure 24 Changing stability of the ecosystem in the western English Channel. Comparison of (A) the annual abundance of pilchard eggs (sum of monthly means) oV Plymouth (stations A and L5) and (B) the percentage of the annual total spawned in spring/summer (April to July) and in autumn (August to December; Marine Biological Association database).

these alternations occurred comparatively smoothly. The abrupt change in the 1930s can be seen, with benefit of hindsight, as a climatically mediated shift intensified by overfishing, leading to recruitment failure (Southward, 1963; Southward et al., 1988a,b). The time-series work showed the large extent of interannual and longerterm variation in abundance of zooplankton. To help explain this variation, a series of biochemical investigations was begun by Corner and his associates into the nutrition and metabolism of the largest plankton herbivore oV Plymouth, C. helgolandicus (Corner, 1961; Cowey and Corner, 1963a; Corner et al., 1965, 1967, 1972, 1974, 1976; Corner and Newell, 1967; Butler et al., 1969, 1970; Sargent et al., 1977; O’Hara et al., 1978, 1979; Gatten et al., 1980). This species is an important component of the diet of many pelagic

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fish and of invertebrate plankton such as Parasagitta. Although it is a warmer-water species compared to its northern congener, Calanus finmarchicus (Beaugrand et al., 2002), C. helgolandicus has tended to be most abundant at L5 in the western English Channel during the cooler climate phases, before 1930 and between 1966 and 1985 (Figures 22 and 23). Attention was given to the amino acids and lipids of C. helgolandicus after it fed on phytoplankton (Cowey and Corner, 1962, 1963b; Gatten et al., 1979; Neal et al., 1986) and to the recycling of lipids and the excretion of various forms of nitrogen and phosphorus (Conover and Corner, 1968; Volkman et al., 1980; Prahl et al., 1984a,b 1985). In looking at seasonal changes in metabolism, it was found that C. helgolandicus could eVectively survive the winter by adopting a carnivorous diet (Corner et al., 1976; Gatten et al., 1979). These later studies corrected earlier excessively high estimates of ammonia excretion and underlined the importance of calanoid faecal pellets in sedimentation of organic matter to the sea bed. Reviews of this work (Corner and Cowey, 1968; Corner and Davies, 1971; Corner and O’Hara, 1986) conclude that in some aspects, notably amino acids and lipids, the dietary requirements of planktonic crustaceans may resemble those of vertebrates, and no single algal food can meet all their nutritional needs. However, their metabolism appears to be able to adjust chain length and degree of unsaturation of lipids, thus making up for some of the dietary deficiencies. The warm-water plankton community that appeared in 1930–1931 persisted oV Plymouth until the early 1960s, then declined after 1962 (see Figure 23). From this point, there was an increasing abundance of Calanus helgolandicus, euphausids, and larvae of demersal fish (Russell, 1973). Coldwater species characterized by Parasagitta elegans returned, reaching a peak in 1979, by which time there was reduced spawning of pilchard oV Plymouth (Southward, 1974a,b 1980, 1995). In addition, after 1961, pilchard peak spawning time switched from spring and autumn to mostly autumn, coinciding with the shift to cooler conditions (Figure 24). After 1985, the balance began to switch back again from cold-water species to warm-water species, including increased spawning of pilchard (Southward et al., 1988a,b 1995). One fact that emerges from the zooplankton data is the existence of alternating periods of stability interspersed with episodes of rapid change. A good example is found in the relative seasonal intensity of spawning of pilchard oV Plymouth. If the percentage of the annual sum of pilchard eggs found in spring and summer is compared with that of autumn spawning, there was indeed a long period of relative stability from 1936 to 1960, whereas from 1962 to 1999 the system was prone to oscillation (Figure 24). A further facet of the change in the ecosystem oV Plymouth was that, after 1931, the seawater from the regular stations (E1 and L5) became less satisfactory for the rearing of invertebrate larvae. It had been found as

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Figure 25 Intertidal studies. (A) mixed barnacles at mid-tide level at St. Ives, Cornwall, spring 1975, photographed in water with the operculum open. The adult barnacles belong to three species as follows: Ba, Semibalanus balanoides; M,

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early as 1889 that the Plymouth Laboratory seawater, pumped up from Plymouth Sound in front of the laboratory and recirculated for long periods, although perfectly adequate for keeping fish and many adult invertebrates in apparent good health, was unsuitable for rearing delicate planktonic stages (Southward and Roberts, 1987). Investigators had to use a supply of ‘‘outside’’ water, collected from the open Channel beyond Plymouth Breakwater. Subsequently, in the 1930s to 1970s, this outside water itself gave poor results. Experimental work (Wilson, 1951; Wilson and Armstrong, 1958, 1961) showed that there was some essential factor in water from the P. elegans community that was lacking at the stations near Plymouth where the P. setosa community had replaced the Parasagitta elegans community. For example, to cultivate in vitro the larvae of echinoderms, including those of the common sea urchin, Echinus esculentus, it was necessary to use seawater collected farther to the west. In the 1950s and 1960s, this collection involved a long journey to the western Celtic Sea south of Ireland, a location where there was a cold-water plankton community that included Aglantha digitalis, P. elegans, and larvae of Luidia sarsi (Figure 21; A. J. S., personal observations; F. A. J. Armstrong, D. P. Wilson, personal communication; Southward, 1980). Despite much chemical analysis, the essential factor in this water was never identified, and it has often been referred to, wrongly, as ‘‘Atlantic Water.’’ In general this water that was beneficial to larval rearing showed slightly elevated winter concentrations of inorganic phosphate when compared to the water close to Plymouth.

2.6. Intertidal observations The first MBA records of selected intertidal organisms on rocky shores were surveys at five sites around Plymouth in 1934 (Moore, 1936). Subsequently, from 1951 to 1987, annual records were taken at these stations, primarily to assess the relative abundance of barnacle species (Figures 25–27) that appeared to be coupled to change in sea temperature (Southward and Crisp, 1954, 1956). A mixed population of three species is shown in Figure 25A. For special studies, one station was selected as showing maximum fluctuation of species (Cellar Beach; Figure 26A), and observations on recruitment and mortality over several years were also made there

Chthamalus montagui; S, Chthamalus stellatus; and the white juvenile barnacles are all recently settled S. balanoides; scale bar, 2 mm. (B) counting barnacles in the field; (C) square decimeter quadrat; (D) the large, warm-water barnacle, Balanus perforatus, that has extended its range to the eastern English Channel, with juveniles that have recently settled on it; scale bar, 2 mm; (E) counting limpets on a large quadrat (photos: A and C by A. J. Southward; B by E. C. Southward; D and E by R. Leaper).

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Figure 26 Changes in annual abundance of intertidal barnacles. (A) at Cellar Beach, South Devon, annual mean number per square centimetre, all tide levels combined, of Chthamalus species (triangles) and Semibalanus balanoides (circles). (B) mean annual abundance of the same species at eight stations along the north

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Figure 27 Sites around southwest England surveyed each year for abundance of intertidal barnacles and other rocky shore organisms, 1954–1987. Eight on the north coast: H, Hartland Quay; B, Bude; T, Trevone; N, Newquay; C, Chapel Porth; S, St. Ives; Cc, Cape Cornwall; Sn, Sennen Cove. Eight on the south coast: P, Porthleven; L, Lizard Point; Lo, Looe; W, Wembury, Church Reef; Pr, Prawle Point; Br, Brixham; Ly, Lyme Regis; Pt, Portland Bill (data from Marine Biological Association database).

(Pannacciulli, 1995). When funding decreased in the 1980s, the number of stations was reduced to three, and then to just the the Cellar Beach site (Southward, 1991). There is a further intertidal series, taken over a wider geographical area in the southwest of England, based on the study done in 1931–1934 by Fischer-Piette (1936) and including a larger number of intertidal organisms than just cirripedes. This series was expanded and continued from 1954 to 1987 at sites around the southwest peninsula (Crisp and Southward, 1958; Southward, 1967; Southward et al., 1995), and a single station (Porthleven) has been continued into recent years. The stations most frequently surveyed are shown in Figure 27, and integrated results for the north coast and south coast stations are given in Figure 26B. There is no

coast of Southwest England and eight stations along the south coast, separated into three tide levels, high water neaps, mid-tide level, and low water neaps; Chthamalus shown with thick lines, Semibalanus with thinner lines (data from Marine Biological Association database).

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doubt that the changes in abundance of barnacles were widespread, not local, and further emphasize the importance of climatic factors. There are further series monitoring intertidal organism abundance that span more than 20 years: observations from 1980 by S. J. Hawkins, focusing primarily on Patella spp. (Southward et al., 1995); a trochid series (1978–1985) investigated by J. R. Lewis and M. A. Kendall, continued in part by N. Mieskowska and M. A. Kendall and additional cirripede series from 1996 by S. J. Hawkins and R. Leaper (unpublished data). Striking changes in barnacle abundance can be seen in the data (Figure 26). Chthamalus spp., with a ‘‘southern’’ or warm-water distribution dominated shores in the 1950s (Southward, 1991) except shortly for a minor cold spell around 1955, and the Chthamalus species reached a marked peak in abundance following the very warm years of 1958–1959. In the 1960s and 1970s, Semibalanus balanoides, the ‘‘northern’’ coldwater species, became more prevalent, increasing rapidly after the cold winter of 1962–1963, which severely aVected Chthamalus populations (Southward, 1967). Since the late 1980s, Chthamalus have increased again, though the population was only slowly regaining the levels recorded during the 1950s when the widescale survey of southwest England stopped in 1987. The continuation of the Cellar Beach counts has shown that the numbers of Chthamalus have now regained the density found in the late 1950s, although S. balanoides is still present. The replacement of S. balanoides by Chthamalus spp. in warmer periods is thought to be mediated by competition. Higher temperatures cause increased mortality of S. balanoides juveniles during the early summer, providing space that can be filled by Chthamalus, which, in warmer years, is able to produce more and earlier broods of larvae that settle in late summer and autumn (Southward and Crisp, 1954, 1956; Burrows, 1988; Burrows et al., 1992). During these studies it was established that good survival after settlement of the high-water species, Chthamalus montagui, depended on exposure to air (Burrows, 1988). The ratio of the barnacle species (the two Chthamalus species compared with S. balanoides) has been used as an index and shows good correspondence with sea temperature, notably with a 2-year time lag (Southward, 1967; Southward et al., 1995). This time lag represents the average interval between reproduction in successive generations. The relationship between events in the Channel and further oVshore (the best correspondence is found with Bay of Biscay sea surface temperature) indicates a general forcing function from the ocean. Most sites showed this pattern, but local factors such as topography and currents, as well as chance events, also appear to have a strong influence, such as at Hartland Point and Peveril Point, where barnacle recruitment is always low. An extension of the range of another warm water barnacle Balanus perforatus has been recorded since 1987 (Herbert et al., 2003). This species (Figure 25D) has recolonized sites in the Isle of Wight where it was killed by

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the cold winter of 1962–1963, and in the past 6 years in the eastern English Channel, it has spread eastward for 120 km on the English side and 170 km on the French side. In west Cornwall in 1960, a school party led by N. Tregenza came on a warm-water hermit crab (Clibanarius erthyropus) in tide pools (Carlisle and Tregenza, 1961). A follow-up programme was instigated by the MBA to monitor the survival of this species, and it was discovered at several sites in north and south Cornwall and one location in southwest Devon (Wembury). The species was greatly set back in Cornwall by the ‘‘Torrey Canyon’’ oil spill clean-up operations of 1967 but survived for a while in Mount’s Bay (Southward and Southward, 1977). Clibanarius was deduced to have colonized Cornwall and south Devon during the final phase of the warm period in 1958–1959, when currents were favourable to dispersal of larvae from Brittany. The species declined during the cold period from 1962 to 1980 and was not recorded after 1985 (Southward and Southward, 1988). EVects of climate change have also been seen in limpets (Figure 25E), though gaps in these data have prevented detailed correlation analysis (Southward et al., 1995). The most rapid decline in Patella depressa (a warm-water species) followed the cold winter of 1962–1963 (Crisp, 1964). It had been abundant in southwest England and south Wales before this, but during the cooler period from 1962 to 1980, it was displaced by P. vulgata. From the mid-1980s, Patella depressa increased in abundance again. Changes in limpet abundance are not as clear as those of the barnacles, probably as a result of life history diVerences (Southward et al., 1995). For instance, there is an extensive juvenile phase in diVerent habitats (rock pools in the case of P. depressa, damp places in the case of P. vulgata) that can obscure signals generated by climate. Changes in trochid (Osilinus lineatus and Gibbula umbilicalis) population structure and distribution have also been recorded (Kendall and Mieskowska, unpublished data), with large extensions in the English Channel beyond the limits found in the 1950s recorded by Crisp and Southward (1958). Breeding populations of Osilinus have recently been found at Osmington Mills. Gibbula umbilicalis has been found as far east as Elmer, near Bognor Regis, on newly constructed sea defences. Although no regular surveys have been carried out on intertidal macroalgal distribution, several changes have been recorded that can be attributed to the eVect of temperature change. Before 1940, the cold-water brown alga Alaria esculenta occurred on the south coast of Devon and was recorded from Plymouth breakwater (Parke, 1952; Widdowson, 1971). Alaria is no longer found on the shore east of Porthleven in Cornwall (or possibly Dodman Point), but it still persists in the subtidal on the wave-beaten Eddystone reef (as seen in MBA records since 1956). In 1946, the warm-water species Laminaria ochroleuca was found in Plymouth Sound

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(Parke, 1948), and it has been recorded as far eastward as Salcombe and westward to the Isles of Scilly. The significance of long-term intertidal records became apparent in the wake of the 1967 ‘‘Torrey Canyon’’ oil spill and the subsequent excessive application of toxic dispersants. Long-term studies of recovery were made at one of the worst-aVected sites, Porthleven (Southward and Southward, 1978; Hawkins et al., 1983; Hawkins and Southward, 1992). The long-term data were vital to separate pollution-induced changes from natural eVects (Smith, 1968; Southward and Southward, 1978; Hawkins and Southward, 1992). Recovery at dispersant-treated sites occurred as a series of damped oscillations (periodic collapses in populations of destabilized key species such as green algae, fucoid algae, limpets, and barnacles) until normal levels of small-scale patchiness were reached after 10–15 years (Hawkins et al., 1983, 2002). In contrast, areas where dispersants had not been applied recovered after 2–3 years (Southward and Southward, 1978). During the mid-1980s, the antifoulant tributyltin (TBT) was discovered to have toxic eVects on a variety of nontarget organisms, especially gastropod molluscs (Bryan et al., 1987, 1993; Gibbs et al., 1987, 1991; Langstone et al., 1990; Spence et al., 1990; Bryan and Gibbs, 1991). In the United Kingdom, the dogwhelk Nucella lapillus proved to be highly sensitive to TBT pollution, decreasing in abundance throughout the English Channel, with some local extinctions. The diatom Skeletonema costatum, which has been shown to be particularly sensitive to TBT (Walsh et al., 1985), disappeared from inshore waters around Plymouth in the 1980s (Boalch, 1987) but has now begun to return again (G. T. B., unpublished data). In 1987, TBT was banned in the United Kingdom on vessels less than 25 m in length. Sites monitored near Plymouth (1986–2000) show that recovery was initially rapid but has leveled out in recent years (Hawkins et al., 2002), indicating there is still some contamination from large ships or from sediments that contain particulate TBT (Evans et al., 1991).

2.7. Demersal fish The demersal fish assemblage oV Plymouth has been sampled at intervals between 1913 and 2003 (Figure 28), and several publications have used the data (Southward, 1963; Southward and Boalch, 1992, 1994; Sims et al., 2001, 2004; Hawkins et al., 2003; Genner et al., 2004). A total of 92 species have been recorded within 784 otter trawls (mean duration, 52 min) during 24 individual years spanning the 90-year period. Trawls were undertaken at 30–50-m depth at 130 fishing ‘‘marks’’ over an area covering 42  19 km. The abundance of individual species was assessed and lengths recorded. Throughout the series, five vessels were used, ranging in overall length

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Figure 28 The Plymouth inshore fishing grounds surveyed for demersal fish abundance from 1913 to 1986. Samples were spread out over 130 fishing ‘‘marks’’ inside this grid, but square N12, which corresponds to the plankton station L4, was most frequently sampled (Marine Biological Association database).

from 19 to 39 m. However, the trawl gears used were of comparable dimensions, and trawling was carried out at similar speeds during the time series. An important aspect of this continuity in method has been the usage of the same vessel (Squilla) and net, and most of the same crew, from 1976 to 2003. This Standard Haul time series was complemented by a high-temporal-resolution trawl series undertaken with Sarsia between 1953 and 1972. Over 1550 trawls, each of 2.4 h mean duration, were made in four trawling areas oV Plymouth: the inshore stations, Looe Grounds (508160 N, 048240 W) and Middle Grounds, including L4 (50815.50 N, 048130 W), and the deeper water grounds, Eddystone (inner) Channel Grounds (50808.50 N, 048150 W), and Eddystone (outer) Channel Grounds (508020 N, 048200 W). The inshore areas were trawled during both the Sarsia and Standard Haul series, but the deeper water grounds were sampled only during the Sarsia series. Additional samples trawled by Sarsia from 1964 to 1977 provided data on the abundance and size of cod, whereas records of smaller gadoids were provided by extra trawl hauls from Squilla, using a fine-mesh cover to the end of the trawl net. The long-term data sets indicate both short- and long-term trends in the responses of fish and squid to both fluctuations in climate and changes

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associated with commercial exploitation of stocks. Interannual changes in the timing of migration of veined squid (Loligo forbesi) were linked to climate-forced changes in sea bottom temperature, with migration occurring earlier in warmer years when the NAO was more positive (Sims et al., 2001). The timing of squid abundance advanced by 120–150 days in the warmest years compared with the coldest. The annual migration of squid through the English Channel represents a clear example of temperature-dependent movement, which is in turn mediated by climatic changes associated with the NAO (Sims et al., 2001). In contrast, the spawning migration of flounder (Platichthys flesus) from their overwintering estuarine habitat to spawning grounds at sea started earlier in cooler years (Sims et al., 2004). Flounder migrated to sea some 1–2 months earlier in years that were up to 2 8C cooler. They arrived on the spawning grounds over a shorter time period (2–6 days) when colder than normal conditions prevailed in the estuary, compared to their arrival in warmer years (12–15 days), indicating a more synchronous, populationlevel early migration when it was cold. Migration was earlier when the largest temperature diVerences occurred between Plymouth Sound and oVshore (E1) environments, diVerences that were related significantly to cold, negative phases of the NAO. Therefore, flounder migration phenology appears to be driven by short-term, climate-induced changes in the thermal resources of their overwintering habitat (Sims et al., 2004). These studies indicate that climate-forced fluctuations in sea temperatures aVect the timing and location of a peak population abundance of fish and cephalopods, which, in turn, may have implications for fishery management. Long-term data on the annual abundance of fish oV Plymouth clearly show major changes in the composition of the demersal fish assemblage (Figures 29 and 30). Analyses show that these long-term changes are driven in part by climate-linked trends in sea temperature as well as by intensity of commercial fishing. As noted earlier, the southwest region has been subjected to marked biological changes over the last century (Russell et al., 1971; Southward, 1980; Southward et al., 1995) that is related to climate warming in the 1930s–1950s and in the years since 1985, with relatively cooler periods occuring in the 1900s and 1970s. These changes resulted in increasing observations of rare warm-water fish in warmer periods, as shown in Figure 31 (Russell, 1953). By the early 1950s, there had been a relative increase in warm-water demersal fish in trawl hauls (Southward, 1963; Southward and Boalch, 1992). This trend was reversed after 1962, and cold-water species made a comeback at the expense of some of the warmwater species (Southward and Boalch, 1992). After 1985, there was a resumption of the warming trend, with increases in warm-water fish, a trend that has been observed at other locations in southwest England (Stebbing

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Figure 29 Changes in similarity of the demersal fish populations of Plymouth from 1913 and 2001, ordinated using multi-dimensional scaling (MDS) of the annual frequencies of occurrence. The closer the points (years), the greater the similarity in community composition. Data from Genner et al. (2001).

et al., 2002). The continued eVect of rising sea temperatures from 1985 to the present day appears to have caused an increased abundance of a subset of dominant (common) species with a southern geographical distribution (e.g. dragonet, Callionymus lyra; Genner et al., 2004). This subset of species has increased in relative population abundance rapidly and opportunistically in response to warming, although the reverse has not occurred—equivalent numbers of taxa have not undergone concomitant declines. One explanation for this trend is that the abundances of many species within the community are limited by temperature-dependent resources, and on warming, the habitats can support a greater abundance of individuals of those species. A fish assemblage in the Bristol Channel has also been demonstrated to contain a subset of dominant species whose abundance was strongly linked to temperature, indicating the potential applicability of long-term observations on a demersal fish community made in the western English Channel to other U.K. regions (Genner et al., 2004). The dominant species in the subset, however, have no direct commercial importance in the region. Changes of some species in the assemblage in the last 25 years show that major ecosystem-level eVects caused by fishing have occurred (Genner et al., 2001). Mean fish length has declined, as has mean maximum length and mean length of maturity for the assemblage. This indicates a species-level shift to taxa that grow to, or mature at, smaller sizes. These declines are most

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Figure 30 Demersal fish. (A) preliminary sorting of trawl catch on deck of Sarsia, 1963; (B) adult cod, about 450 mm total length; (C) changes in individual total length of cod, measured in trawl hauls 1919–2003, n ¼ 358; linear regression, r2 ¼ 0.24, P < .0001; (D) larvae of cod (Gadus morrhua) hatched from planktonic eggs, after absorption of yolk sac. Photographs: A and D, A. J. Southward; B, D. W. Sims.

striking in commercially exploited species, notably skates and rays (Hawkins et al., 2003). Catches of blonde ray (Raja brachyura), for instance, have declined by 88% between 1919–1922 and 1983–2002. Taken with other criteria, evidence is consistent with patterns expected from the selective, unsustainable harvesting of large, commercially valuable species (Genner et al., 2001). The data for certain gadoids show very interesting trends. Cod, Gadus morhua, is one of the species that declined in total length, from a mean of 80 cm in 1919 to 30 cm in 2001 (Figure 30). This cold-water species was scarce oV Plymouth in the 1950s, but after the cold winters of 1961–1962 and 1962– 1963, which signalled the start of a period of declining temperature, numbers of young cod appeared in the catches of the research vessels. By 1977, mature cod were much commoner than in the earlier years of survey. In 1980, samples of fish eggs taken at L5 with the 2-metre diameter mesozooplankton net in early April contained viable cod eggs (up to 15% of total fish

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Figure 31 Examples of rare fish of warm-water distribution caught in the western English Channel, 1949–1972 (based on Russell, F. S. (1953). The English Channel. Transactions of the Devonshire Association for the Advancement of Science, Literature and Art 85, 1–17, with recent changes in nomenclature). (A) Alosa finta; (B) Polyprion americanum; (C) Naucrates ductor; (D) Seriola dumerili; (E) Apogon coccineus; (F) Pagrus pagrus; (G) Lepidopus caudata; (H) Scomber japonicus; (I) Sarda sarda; (J) Euthynnus pelamis; (K) Balistes capriscus; (L) Lagocephalus lagocephalus.

eggs), showing that cod had reached a local density great enough to allow spawning (A.J.S. and P.R.D., personal observation, Figure 30D). Surprisingly, the trawl records show that this species maintained its numbers during the warm period that followed the cold spell (Genner et al., 2004). This survival of cod oV Plymouth is counterintuitive, as the species would have been expected to disappear from the western English Channel when the

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temperatures rise. Another cold-water gadoid Trisopterus esmarkii, a smaller species, appeared oV Plymouth in the late 1970s (Southward and Mattacola, 1980), and its eggs and larvae were detected in small numbers in 1980 and 1981; unlike cod, however, it appears to have vanished in recent years. The complexity of the relationships between competing fish species and their environment has been discussed by Skud (1982) and by Smith and Moser (2003). It is possible that removal of competitors by fishing, and improvement in nutrition following an increase in trash species caused by overexploitation of commercial species, has allowed species such as cod to survive the change in environment in the western English Channel.

2.8. Benthos The benthic invertebrates of the English Channel were sampled intermittently from 1899 to 1985 (Figure 8). The longest continuous data sets are those collected by Holme from 1959 to 1985 (Table 4). These data sets have been assessed for quality of the data and for the potential for resurvey (Genner et al., 2001). Holme made a point of reinvestigating historic sites (e.g. Eddystone Grounds; Figures 3, 22) that had been originally surveyed between 1895 and 1898 (Allen, 1899) and again from 1931 to 1932 (Smith, 1932). Three data sets were produced: a survey of seabed species, a brittlestar survey, and death assemblages. There is also an extensive archive of videotapes, videocassettes, and photographic transparencies. The seabed species data set constitutes a qualitative faunal record of Table 4 Benthic surveys of the Plymouth area (updated from Holme, 1983) Survey date

Ground

Sampling gear

Reference

1895–1898 1906 1922–1923 1928–1929 1931 1939 1949–1951 1950 1958–1962 1970–1981 1972–1982

Eddystone grounds Outside Eddystone Plymouth area Inside Eddystone Eddystone gravels Rame mud Plymouth area Plymouth area English Channel W English Channel Lizard-Start Point

Dredge; trawl Dredge; trawl Grab Grab; trawl Conical dredge Corer; grab Camera Grab Anchor-dredge Dredge TV sledge

1997–2002

Fowey-Eddystone

Scallop dredge; anchor dredge

Allen, 1899 Crawshay, 1912 Ford, 1923 Steven, 1930 Smith, 1932 Mare, 1942 Vevers, 1951, 1952 Holme, 1953 Holme, 1961, 1966a Holme, 1984 Wilson et al., 1977; Franklin et al., 1980 Kaiser et al., 1998 Kaiser and Spence, 2002

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echinoderms and molluscs for 324 stations distributed throughout the English Channel. In addition, Holme compiled reference lists of species (MBA archives) from comparable historic MBA surveys as far back as 1895. The brittlestar survey used a diVerent methodology to the seabed species survey (mini-Agassiz trawl and anchor dredge, respectively) and provides a quantitative record of all echinoderms from 329 stations on the south coast of England. Death assemblages were recorded of dead-shell material retained in anchor dredges. Fluctuations in benthos have been related to sea temperature (notably exceptionally cold winters), immigrant species, dinoflagellate blooms, and increasingly, heavy fishing gear (Holme, 1983). Fluctuations in western species (cold-water species) are likely to relate to temperature (e.g. Munida bamYca, an anomuran crustacean; Echinus acutus, a sea urchin; and Dentalium entalis, a scaphopod mollusc), as are fluctuations in Sarnian species (warm-water species), (e.g. Octopus vulgaris, Venus verrucosa, and Dentalium vulgare) (Holme, 1966b). However, the increased use of toothed scallop dredges and of heavy chains on trawls to catch sole were recognized as increasingly important factors in determining benthic communities (Holme, 1983). The Fowey-Eddystone grounds were resampled with scallop dredge and anchor dredge in 1993 (Kaiser et al., 1998). In a more extensive survey in 1998, selected benthic communities were resampled to test hypotheses regarding the resilience of megabenthic species (Glycymeris glycymeris and Paphia rhomboides) to fishing and dredging disturbance (Kaiser and Spence, 2002). Most sites showed temporal changes in bivalve and echinoderm communities, as would be expected over a 40-year period. However, two out of 10 did not, indicating that a few areas of the seabed exist with a similar community composition to that before the general increase in bottom-fishing disturbance. The results reflect the patchy nature of both the benthic communities and the fishery exploitation of the grounds, highlighting the need for further investigation to interpret the spatial and temporal inconsistencies. There was a well-recorded invasion of the Plymouth fishing grounds in the late 1940s by the warm-water Octopus vulgaris (Rees and Lumby, 1954). This did not last, and the MBA aquarium had to revert to the cool-water species Eledone cirrhosa for octopus displays in the 1960s; some experimental physiologists also migrated to warmer climes. There had been a similar change in the species composition of squid collected by trawling. The common local species, Loligo forbesi, is of northern character, but samples brought into the laboratory in the late 1940s for neurophysiological studies contained a fair number of the southern species, Loligo vulgaris. These squid populations are ephemeral compared with fish, with their the whole life history being compressed into 12 months (Holme, 1974).

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3. PML AND THE FORMER IMER 3.1. Series at station L4 Station L4 is situated about 10 nm southwest of Plymouth (Figure 3) in water about 55 m deep and is influenced by seasonally stratified and transitionalmixed waters (Pingree and GriYths, 1978) and by estuarine outflow from Plymouth Sound. A range of physical, chemical, and biological measurements (see Table 5 for methods), notably zooplankton and phytoplankton species’ composition (Figure 32), has been carried out at L4 on an almost weekly basis since 1988, when the long-term records at E1 and L5 were terminated. Table 5 Sampling techniques for L4, on a weekly basis Sample type

Equipment

Methods

Zooplankton

WP2 net (200 mm) WP2 net (50 mm)a

Phytoplankton

Bottle samples

Chlorophyll

Bottle samples

Particulate carbon and nitrogen

Bottle samples

Vertical haul from 50 m to the surface Samples stored in 5% formalin Identification to genera/species level under dissecting microscope, completed within a week of sampling Collected at 10 m depth Samples stored in 2% Lugol’s iodine (Holligan and Harbour, 1977) 10–100 mL of sample is settled and species abundance determined using an inverted microscope. Determined on 90% acetone extracts of GF/F filtered samples, using a Turner Designs fluorometer. 250-mL aliquots are prefiltered through a 200-mm mesh, then filtered onto 25-mm ashed glass fibre filters (GF/F). CN samples are washed with phosphate buVered saline before storage at 25 8C. All analyses use a Carlo-Erba Elemental Analyser Model NA1500. Autoanalyser, Bran and Luebbe AA3, unfiltered and 0.2-mm Nuclepore, Frozen 20 8C (Brewer and Riley, 1965; GrasshoV, 1976; Kirkwood, 1989; Mantoura and Woodward, 1983) CTD haul to 50 m

Nutrientsa Bottle samples nitrate, nitrite, ammonium, phosphate, silicate Temperature CTD fitted with a and salinity fast repetition rate fluorometer and transmissometer) a

Samples collected since May 2002.

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Figure 32 Summary of long-term data held by PML for station L4. Black indicates periods of sampling. Data can be downloaded at http://www.pml.ac.uk/14/.

A variety of studies have been based on particular elements of the L4 programme: appendicularian and copepod population dynamics (Green et al., 1993; Acuna et al., 1995; Lopez-Urrutia et al., 2004), copepod feeding (Bautista and Harris, 1992; Bautista et al., 1992; Irigoien et al., 2000b), copepod egg production (Bautista et al., 1994; Guisande and Harris, 1995; Pond et al., 1996; Laabir et al., 1998; Irigoien et al., 2000a, 2002), and the testing of new in situ techniques (Biegala and Harris, 1999). The L4 sampling has also been compared with the CPR data for the area (John et al., 2001). The complete L4 data set is available online at http://www.pml.ac.uk/14. One of the strengths of the L4 time series is that it also covers microbial elements of the planktonic food web. For example, Rodriguez et al. (2000) describe parallel changes in viruses, bacteria, phytoplankton, and zooplankton at this station. Over the time series, Pseudocalanus has been the most abundant copepod, making up 12% of the total population. Abundance of Calanus helgolandicus at L4 shows a decreasing trend from 1988 to 1995. Similar trends were seen

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in total zooplankton; low spring abundances of Pseudocalanus and Acartia spp. were characteristic of the years of overall low zooplankton abundance (1988–1995), as was a high abundance of cirripede nauplii (International Council for the Exploration of the Sea, 2003). Recovery of zooplankton populations between 1995 and 1999 was mainly caused by increases in two autumn-developing copepods, Euterpina sp. and Oncaea sp., as well as Paracalanus parvus. Seasonal and interannual variability in environmental variables, egg production rates, and abundance of C. helgolandicus at L4 were analysed by Irigoien and Harris (2003). Their results (Figure 33) show a mismatch between the timing of maximum egg production and the timing of the abundance peaks. However, except for the year 1996, there was a significant relation between the initiation of the thermocline and the timing of the maximum female abundance. Advection and egg mortality caused by sinking were suggested as the main factors controlling the timing of the C. helgolandicus abundance peaks at station L4. The seasonal phytoplankton cycle is characterized by a spring diatom and a summer dinoflagellate bloom. The spring bloom assemblage, dominated by diatoms, diVers from year to year (e.g. Chaetoceros socialis was dominant in 1993, whereas Rhizosolenia delicatula was dominant in 1994). The dominance of diatoms within the spring phytoplankton bloom has been related to the NAO (Irigoien et al., 2000b). Spring diatom concentration (both abundance and percentage of diatoms) showed a positive relation with the winter NAO index when the average for the April–May period was considered (Figure 34). In contrast, the average amount of total phytoplankton carbon during the spring was not related to the NAO. Positive NAO conditions in the northeast Atlantic imply increased westerly wind stress and increased precipitation. Stronger mixing (increased winds) and nutrient levels (increased river runoV ) should favour diatoms to the detriment of flagellates. Phytoplankton composition has important consequences for ecosystems in terms of both energy transfer eYciency and nutritional value for upper trophic levels. The dinoflagellate bloom in summer is intense at L4, and since 1969 it has often been dominated by Gyrodinium aureolum, which may comprise more than 95% of phytoplankton carbon at peak production and can form intense blooms at frontal systems (Le Fe`vre, 1986; Pingree et al., 1975, 1976). Note that this dinoflagellate is an immigrant to the English Channel that arrived in the 1950s and that has caused toxic blooms (Boalch, 1987).

3.2. Bio-optics and photosynthesis From the early 1980s, phytoplankton fluorescence and optical measurements have been made opportunistically throughout the western English Channel (Aiken, 1981a, 1985; Aiken and Bellan, 1986a, 1990). From this

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Figure 33 Examples of seasonal and annual changes in abundance of zooplankton at station L4. (A) females of the copepod Calanus helgolandicus (grey) and sea surface temperature (black); (B) female Calanus helgolandicus (grey) and phytoplankton concentration (black); (C) female Calanus helgolandicus (grey) and the dinoflagellate Gyrodinium aureolum (black); (D) female Calanus helgolandicus (grey) and egg production rate of Calanus helgolandicus. [From Irigoien, X. and Harris, R. P. (2003). Interannual variability of Calanus helgolandicus in the English Channel. Fisheries Oceanography 12, 317–326.]

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Figure 34 Correlations between plankton and climate (as winter NAO index) in data from station L4. (From Irigoien et al., 2000b.)

work came significant advances in instrumentation and methodology for quantifying chlorophyll fluorescence (Aiken, 1981b), chlorophyll absorption (Aiken, 1985), bioluminescence (Aiken and Kelly, 1984), and photosynthetically active radiation (PAR) (Aiken and Bellan, 1986a); notable are the development of hemispherical logarithmic PAR and multiband light sensors (Aiken and Bellan, 1986b). Between 1979 and 1984, chlorophyll fluorescence, salinity, temperature, depth, and zooplankton abundance were measured with the Undulating Oceanographic Recorder (UOR) in conjunction with the CPR along the Plymouth–RoscoV ship-of-opportunity route used in the CPR survey (Robinson et al., 1986). The bio-optical work in Plymouth has been important in the validation of satellite ocean colour measurements. Downwelling and upwelling hemispherical irradiance in four wavebands (443, 520, 560, and 620 nm) was recorded on some UOR tows to provide validation of measurements from space made by the CZCS (Holligan et al., 1983). Throughout the late 1990s, profiled optical data were occasionally acquired at L4, E1, and other stations

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in the western English Channel (Zibordi et al., 1998), and from a buoy designed to provide calibration and validation of the SeaWiFS satellite ocean colour sensor in a shelf sea location in temperate waters, far removed from NASA’s principal site oV Hawaii. The Plymouth Marine Bio-optical Data Buoy (PlyMBODy) was originally sited at L4 (Pinkerton and Aiken, 1999; Pinkerton et al., 2003), but after collision with a merchant ship, it was moved to a new site nearby that had similar oceanographic and optical characteristics. PlyMBODy was deployed through the spring to autumn periods of 1998, 1999, and 2000, and supporting optical data were acquired by profiled systems alongside the buoy site. PlyMBODy showed that a small, low-cost data buoy could provide accurate calibration and validation of SeaWiFS, and reported the calibration errors in the SeaWiFS visible channels in the location of the western English Channel. A regular weekly schedule of sampling optical properties and photosynthetic parameters (with Fast Repetitition Rate Fluorometer, FRRF) at L4 was implemented in 2001 and has continued to the present date (Table 5). These data are being used to validate the Medium Resolution Imaging Spectrometer (MERIS) ocean colour sensor on Environment Satellite (ENVISAT). Occasional sorties were made to E1 before 2002, but it was only through the E1 restart in 2002 that regular monthly sampling of optical properties was established there. Aiken et al. (2004) reported the seasonal succession of phytoplankton quantum eYciency (PQE), pigment composition and the optical properties at L4 and E1. These measurements show that there may be a functional link between these properties, indicating that chlorophyll a is synthesized preferentially when plants are in active growth, providing a pigment and optical proxies for PQE and the possibility of detecting photosynthetic parameters in remotely sensed ocean colour spectra.

4. SAHFOS The CPR was invented by Sir Alister Hardy in the 1920s and was used from Discovery and Discovery II in the Southern Ocean (Hardy, 1936). A school of oceanography was set up in 1932 at University College, Hull, to develop this method of sampling plankton over wide regions (Hardy, 1939). In 1956, the group was reconstituted as the Scottish Oceanographic Laboratory in Edinburgh, with links to the Scottish Marine Biological Association. In 1974, they formed the nucleus of the newly established IMER and moved to Plymouth. As noted in Section 1, the CPR survey was threatened with closure during a period of reorganisation in marine science in the United Kingdom during the late 1980s and early 1990s but was reconstituted as SAHFOS with support from the MBA, the UK Ministry of Agriculture

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Figure 35 The Continuous Plankton Recorder (CPR). (A) the late 1930s version, with the silk cassette and formalin tank placed alongside (after Hardy, 1939); (B) a cross section of the CPR, showing how it works (after Hardy, 1939); (C) the recent model CPR showing the box tail ready for deployment from a merchant ship.

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Fisheries and Food (MAFF), and the international community. SAHFOS now occupies part of the Citadel Hill site with the MBA. 4.1. CPR methods The CPR monitoring conducted by SAHFOS in the western English Channel provides a regular broadscale picture of the plankton community complementary to the time series carried out by the MBA and PML. The CPR is a towed body, approximately 1 m long; seawater that enters the nose cone is filtered onto a continuously moving band of silk mesh (Figure 35). Samples are taken at a depth of about 5–10 m (Batten et al., 2003). Organisms captured on the CPR silk (270 mm mesh) are preserved in borax-buVered formalin within the CPR immediately upon collection. Samples are then returned to the laboratory, where they are counted in a four-stage process (Table 6; for more details, see Colebrook, 1960; Warner and Hays, 1994). A list of the taxa identified can be found in Warner and Hays (1994) or at the SAHFOS Web site (http://www.sahfos.org), along with free access to the CPR database. Methods of analysis have remained relatively unchanged since 1958 (Table 7); although a diVerent method for counting phytoplankton was used from 1948 to 1957. The CPR survey routinely identifies 400 species of phytoplankton and zooplankton. The western English Channel was first sampled by the CPR in January 1952, and a total of 4,768 samples were collected and counted up to 2001. Two routes in the English Channel have been sampled most consistently on a monthly basis (Warner and Hays, 1994). The first runs approximately east to west, from Portsmouth through the English Channel and then across Table 6 Methods used to analyze Continuous Plankton Recorder samples Stage 1: Phytoplankton colour

The intensity of the green colouration of filtering silk is assigned to four categories (which can be converted to chlorophyll equivalents). Stage 2: Phytoplankton analysis Phytoplankton are identified from 20 fields centred on the mesh and traversed diagonally from corner to corner under 450 magnification. The number of fields where each taxon is seen is counted (1/8000 of the silk is covered). Stage 3: Zooplankton traverse Small zooplankton (<2 mm) are identified and counted on a stepwise traverse across both the filtering and covering silks under 48 magnification (1/40 of the silk is covered). Stage 4: Zooplankton eyecount All larger zooplankton (>2 mm) are removed from the silk, identified and counted.

Taxon

Recorded from

Comments

Acautharians Branchiostoma lanceolatum (Pallas) Calanus I–IV Calanus glacialis Jaschnov 1955

2004 1946 1958 1961

Recorded with Radiolarians since 1993

Calanus finmarchicus (Gunnerus) and Calanus helgolandicus (Claus) Calanus hyperboreus (Krøyer) Calanus V–VI total Caligoida Candacia armata (Boeck) egg

1958 1946 1946 1946 1997

Caprellids Cavolinia spp. Cephalopod larvae Chaetognaths

1946 1967 1946 1946

Cirripede larvae

1958

Cladocera (total) Clausocalanus sp. Clio spp. Clione limacina (Phipps) Coccolithophores Coelenterates

1948–1957 1946 1946 1946 1993 1946

64

Table 7 Information on taxonomic resolution and available time series for selected taxa from the Continuous Plankton Recorder database. From Batten et al. (2003), Edwards (2000), Continuous Plankton Recorder Survey Team (2004), the CPR database, and unpublished dataa

Juveniles of all Calanus species. Separated from C. finmarchicus based on size alone. Included in Calanus V–VI total. Recorded as separate species from 1958. Included in Calanus V–VI total. C. finmarchicus, C. helgolandicus, and C. glacialis. Nearly all records are Caligus elongatus Nordmann, 1832. Denoted as ‘‘spiny egg’’ in the survey. Eggs of other copepod species are recorded together as ‘‘copepod eggs.’’ For species see Vane (1951).

Recorded as present since 1965. Only recorded as present. Often identified by presence of nematocysts.

ALAN J. SOUTHWARD ET AL.

May include postlarvae. Some identification may be suspect. Recorded separately in traverse and eyecount. For species see Bainbridge (1963). Recorded as present since 1946. These are Balanidae and Verrucidae larvae. For species see Roskell (1975). Includes Evadne spp., Penilia avirostris and Podon spp. For species see Williams and Wallace (1975).

1993

Copepod nauplii Coscinodiscus wailesii Gran and Angst

1958 1977

Cumaceans Cyphonautes larvae Decapod larvae Dictyocysta spp.

1946 1958 1946 1996

Dinoflagellate cysts Dinophysis acuminata (Clapare`de and Lachmann), D. acuta Ehrenberg, D. caudata Saville-Kent, D. norvegica Clapare`de and Lachmann, D. rotundata Clapare`de and Lachmann (¼Phalacroma rotundatum), D. sacculus Stein, D. tripos Gourret Doliolids

1993 2004

Echinoderm larvae Echinoderm post-larvae Euphausiids Evadne spp. Favella serrata (Mo¨bius) Fish eggs Fish larvae (young fish) Foraminiferans Gammarids Gonyaulax spp. Halosphaera spp.

1949–1957, 1978–present 1949 1946 1946 1958 1996 1946 1946 1993 1946 1965 1996

Recorded as present 1948–1957 and since 1974. Individual eggs are counted for both free and sac spawners. Only Candacia armata (Boeck, 1872) eggs are recorded separately. Recorded as present since 1946. Invasive; first recorded in European waters in the English Channel in 1977. Recorded as present since 1946. For species see Lindley (1987). Recorded within total tintinnids previously. For species see Lindley (1975). Recorded as present since 1974. For species see Reid (1978). Previously all Dinophysis species were grouped (recorded as present since 1948, abundance from 1958).

LONG-TERM RESEARCH IN THE ENGLISH CHANNEL

Copepod eggs

For species see Hunt (1968). For species see Rees (1954a). Separated into juveniles and adults from 1968 to 1988. Recorded as present within Cladocera (total ) from 1948 to 1957. Recorded within tintinnids (total) previously.

(Continued )

65

See Coombs (1980) for species recorded. Recorded as present since 1946. For species see Vane (1951). Includes other genera in Gonyaulaceae (e.g. Alexandrium) Recorded as present since 1948. Counting method changed in 1996.

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Table 7 (Continued) Taxon

Recorded from

Comments

Harpacticoids Hyperiids Isopods Lamellibranch larvae Larvaceans

1946 1946 1947 1949 1958

Includes mainly Microsetella spp. For species see Vane (1951) and McHardy (1970).

Lepas nauplii Limacina retroversa (Fleming) Lucifer typus H. Milne-Edwards Mesocalanus (¼Calanus) tenuicornis (Dana) Noctiluca scintillans Macartney Ostracods Parafavella gigantea (Brandt) Parasitic nematode Penilia avirostris

1955 1958 1997 1946 1981 1947 1996 1948 1946

Phaeocystis spp.

1946

Phytoplankton Colour Pinus pollen Podon spp. Polychaete larvae

1946 1997 1958 1958

Polykrikos schwartzii cysts Bu¨tschli (‘‘Umrindetencysts’’)

1993

Recorded as present since 1946. For species see Rees (1954b). Recorded as present since 1946. The following species have been identified: Oikopleura dioica Fol 1872, O. labradoriensis Lohmann 1892, Fritillaria borealis Lohmann 1896 and F. pellucida Busch 1851. For species see Bainbridge and Roskell (1966). Recorded as present since 1946.

For species see Williams (1975). Recorded within total tintinnids previously.

Recorded as present within Cladocera (total) from 1948 to 1957. Recorded as present since 1946. Tomopteris spp. counted separately. Recorded as present since 1975. The unarmoured motile cells are not recorded in CPR samples.

ALAN J. SOUTHWARD ET AL.

Probably introduced into the North Sea by ballast water in early 1990s. Abundance recorded from 1948 to 1957. Only recorded as present since. Measured in four categories.

1958

Ptychocylis spp.

1996

Radiolarians

1993

Rotifer eggs Salps

1984 1949–1957, 1978–present 1982 1962 1993 1958 1983

Scrippsiella spp. Sergestid larvae Silicoflagellates Siphonophores ‘‘Spindelei’’ Stauroneis (Navicula) membranacea (Cleve) F.W. Mills (¼Ephemera planamembranacea) Stellate body Tasmanites (Pachysphaera) spp. Thaliaceans (salps and doliolids)

1962 1996 1958 1946–1960

Tintinnids (total)

1993

Tintinnopsis spp.

1996

Tomopteris spp. Zoothamnium pelagicum Stein

1946 1993

Includes only adult females and adult males. In the NE Atlantic and North Sea these are probably Pseudocalanus acuspes (Giesbrecht), P. elongatus (Boeck) and P. minutus (Krøyer). Recorded within tintinnids (total) previously. For species see Lindley (1975). Recorded as present 1948–1957. Includes Acantharians. From 2004, Acantharians recorded separately. Adults are not identifiable in CPR samples. For species see Hunt (1968). Most records are of Scrippsiella trochoidea (Stein, 1883). For species see Lindley (1987). Recorded as present 1948–1957 and since 1964. Calycophorans only. Eggs of Kuhnia scombri, a monogenean gill parasite of mackerel Scomber scombrus. Hartley (1986). First described from CPR samples in the NW Atlantic in 1962. Land plant hair. Boalch and Guy-Ohlson (1992) Recorded as present since 1946. Salps and doliolids also recorded separately. Recorded as present 1948–1957. For species see Lindley (1975) Recorded within tintinnids (total) previously. For species see Lindley (1975). Recorded separately from Polychaete larvae. Recorded as present since 1964. Counted as number of colonies.

LONG-TERM RESEARCH IN THE ENGLISH CHANNEL

Pseudocalanus spp.

a

67

Procedures for counting zooplankton have generally remained unchanged since 1948, and phytoplankton counting procedures since 1958 (exceptions noted above). Note that dates given here represent the date when the species was looked for, not when it was first seen. In addition, it should be remembered that changes in the area that the survey samples markedly influences the recording of species.

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Figure 36 Sampling by the Continuous Plankton Recorder in the western English Channel and Approaches, grouped into decades between 1950 and 2001. (A) 1950s to 1970s; (B) 1980s to 2001. Each point represents a Continuous Plankton Recorder sample. For purposes of the present analysis, the western English Channel area lies between 2 8W and 5 8W.

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the Bay of Biscay (Figure 36). This route was first towed in April 1957 and remained in operation until May 2000, although other routes now sample this area. Fourteen ships have towed this route, and a total of 2,548 samples have been counted. The second route that has been well sampled runs from north to south across the English Channel from Plymouth to RoscoV (Figure 36). This route was sampled from April 1974 until May 1994 and resumed again in November 2003. A total of 1,778 samples have been counted.

4.2. Consistency issues As with other long-term time series, there are issues regarding consistency through time. The survey has tried to maintain methodological consistency in terms of equipment and counting procedures as far as is possible, although there have been some changes in counting methods (Table 7). There have only been minor modifications to the CPR itself since 1929. These include the attachment of a box tail that was phased in from 1977 to 1980 to increase stability at faster ship speeds (Figure 35C), and an elongated tail end that was introduced in 1985 to carry additional electronic instruments (see Reid et al., 2003 for more details). However, the synoptic coverage of the survey means that there are additional consistency issues encountered, diVerent from those facing long-term time series at a single location. For example, the CPR is voluntarily towed behind ships of opportunity on their normal routes of passage, which ships present their own consistency issues. One issue related to the use of ships of opportunity is that ship speed has generally increased over the period that the CPR Survey has operated (Figure 37A). On particular routes, this increase has been stepped because of ship changes. For the route from Portsmouth to Spain, ship speed remained remarkably constant at 12.5 knots from 1958 to 1985, after which speed increased to 14 knots. The passenger ferries on the Plymouth to RoscoV route are considerably faster than cargo vessels to Spain, with speeds from 1974 to the mid-1980s averaging 16 knots, increasing to 18 knots by 1995, with some routes being towed at speeds greater than 20 knots. Other consistency issues related to using ships of opportunity manifest themselves spatially. Large spatial changes over the years (Figure 36) are often a consequence of the availability of ships willing to tow CPRs, as well as the eVect of vagaries of funding. This produces variations in the mean latitude and longitude of sampling each month in a region such as the western English Channel, which can influence the plankton community observed. In terms of latitude, there has been very little change in the average

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Figure 37 Continuous Plankton Recorder sampling in the western English Channel. (A) The average towing vessel speed per tow along two of the major lines; (B) the proportion of samples per tow collected during daylight hours.

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sampling position, but there have been greater changes in longitude. The average sampling position in the western English Channel area was 4 8W until the mid-1970s, and is now 2.8 8W, following the introduction of the Plymouth–RoscoV route. Still other consistency issues can manifest on various timescales from annual to diel. On an annual scale, the actual number of samples collected has varied considerably: 60 samples were collected each year from 1957 to 1973, whereas 150 samples per year were collected from 1974 to 1994, when the Plymouth to RoscoV route was operating. On a monthly scale, sampling can be reduced or absent in a particular month because of the jamming of the internal cassette that contains the silk, although this is relatively infrequent (success of CPR tows is 95%). Data for a month can also be lost because a ship is out of service or when the sea state is too rough for safe deployment of CPRs, a condition more frequent in winter. On a diel scale, the time of day that sampling is carried out can change as schedules and ships change. As the CPR is a near-surface sampler, this temporal bias needs to be considered when investigating zooplankton species that undergo diel vertical migration. For the western English Channel, the proportion of samples during daylight is quite variable each month (Figure 37B), although there has also been a clear tendency toward collecting a greater proportion of samples during the night in recent years.

4.3. Plankton and mesocale hydrography A study of mesoscale relationships between plankton and hydrography in the region was conducted by Robinson et al. (1986). The distribution of 21 phyto- and 24 zooplankton taxa in relation to temperature (data from the Undulating Oceanographic Recorder) and fronts was described along the Plymouth–RoscoV route (Aiken, 1981a). The CPR samples yielded similar phytoplankton species to those recorded by Maddock et al. (1981). Three areas could be identified according to their planktonic and hydrographic properties: the French coastal area where the water column is mixed throughout the year, the abundance of phytoplankton and zooplankton is low, and the productive season is short; a central area with strong stratification in summer and high zooplankton (particularly copepod) abundance; and British coastal waters where the spring outbreak of phytoplankton is earliest, numbers of phytoplankton are high, zooplankton numbers are low, and there is a long productive season. Part of the variability in plankton distribution could be related to changing position of fronts at the northern and southern ends of the route (Robinson et al., 1986) between neap and spring tides and over the 18-year cycle.

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4.4. Phytoplankton The CPR survey has recorded 104 taxa of phytoplankton in the western English Channel since 1952. Considerable work has been undertaken on the seasonal dynamics of phytoplankton blooms in the region. Peak blooms of diatoms occur in the western English Channel in May and September, whereas blooms of dinoflagellates occur in July (Reid et al., 1987). The seasonal phytoplankton cycle in the western English Channel tends to show a large spring peak with a small autumn peak (Figure 15; Colebrook, 1979; Boalch, 1987). This seasonal cycle is similar to that of the southern North Sea, but the spring bloom occurs earlier in the western English Channel and is more readily exploited by copepods than are blooms oV the continental shelf (Colebrook, 1979). Robinson et al. (1986) report that the seasonal cycle of phytoplankton species is earlier on the English side of the Channel compared to oV the French coast, probably as a consequence of the greater stability of the water column on the northern side (Pingree and Griffiths, 1978; Colebrook, 1979); this was also noted by Boalch and Harbour (1977) and Boalch (1987) (see Figures 14 and 15) and the timing of stratification development (Pingree, 1975). Interannual changes in phytoplankton in the western Channel region have been described by Robinson and Hunt (1986). They analysed a series spanning 1967–1983 and covering the area at which the Portsmouth to Spain and Plymouth to RoscoV routes intersect (498–50 8N and 38–5 8W). Sixteen phytoplankton species were used to identify long-term trends, and these species (together with the zooplankton) fell into four groups of species with similar trends in their annual abundance. The strongest trend was an increase in the dinoflagellates Prorocentrum spp, Ceratium lineatum, Ceratium furca, Ceratium tripos, and Ceratium fusus and the diatoms Thalassiosira spp. and Rhizosolenia shrubsolei. Complex relationships were found between the plankton and environmental factors (salinity, sea surface temperature, radiation, atmospheric pressure patterns, wind speed, and current strength), indicating that long-term changes are mediated through their interaction with the climate (Robinson, 1985; Robinson and Hunt, 1986). More recently, Edwards et al. (2001) found that there has been little change in the phytoplankton colour (see Table 6) in the western English Channel for the period 1981–1995, although there have been substantial increases elsewhere in the northeast Atlantic Ocean. One of the most dramatic changes to the phytoplankton community in the northeast Atlantic appears to have originated in the western English Channel. This was the site of an introduction of the nonindigenous diatom species Coscinodiscus wailesii (Figure 18B), a large centric diatom (175–500 mm) that was originally known only from the north Pacific Ocean. It was first recorded in the north Atlantic Ocean oV Plymouth in January 1977 (Boalch

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and Harbour, 1977), probably having arrived via ballast water or by the importation of oysters from the North Pacific. It was first seen in CPR samples in the spring of the same year oV Plymouth, and it spread over the next decade throughout the English Channel, North Sea, and Irish Sea (Edwards et al., 2001). C. wailesii has established itself in European continental shelf seas, becoming a significant member of the phytoplankton community in spring and autumn. During spring, this species can compose up to 90% of the phytoplankton biomass in some areas (Edwards et al., 2001). Interestingly, although C. wailesii was scarce for several recent years (Figure 38A), it has become abundant again oV Plymouth in the last 2 years (G. T. B., unpublished data). It should be noted that C. wailesii largely replaced another winter diatom, Biddulphia sinensis, which itself was an immigrant about the turn of the nineteenth and twentieth centuries (Figure 18A). 4.5. Zooplankton species routinely identified The CPR survey has recorded 91 taxa of zooplankton in the western English Channel since 1952. The seasonal cycle of copepods in the western English Channel has been described by Robinson et al. (1986). Although the

Figure 38 Examples of Continuous Plankton Recorder data. Changes in mean annual abundance number per 3 cubic metres in the western English Channel of selected taxa. (A) Coscinodiscus wailesii; (B) Acartia spp.; (C) Centropages typicus; (D) Euphausiacea. (A updated after Edwards et al., 2001; B to D updated after Robinson and Hunt, 1986).

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timing of the seasonal cycle may be slightly earlier oV the English than the French coasts, the most marked diVerence is the longer seasonal cycle of zooplankton in the central Channel. Some key species in the region, however, do not have only one peak in their abundance: the seasonal cycle of the important large copepod Calanius helgolandicus is generally bimodal, with peaks in spring and autumn (Planque and Fromentin, 1996). Interannual trends in 20 zooplankton species were reported by Robinson and Hunt (1986). They found that there had been a general decrease in many species, particularly Acartia spp., mainly Acartia clausi, Centropages typicus, and Euphausiacea. This decline has reversed since 1983, although abundance of these species was low during 2001 (Figure 38B–D, updated from Robinson and Hunt, 1986). More recently, a comparison of CPR data for the English Channel, Bay of Biscay, and Celtic Sea between 1979 and 1995 was conducted, exploring factors that influence the relationship between climate and plankton (Beaugrand et al., 2000). The negative phase of the NAO strongly influences the copepod community in the Channel (Acartia spp., Calarius helgolandicus, Centropages typicus, Oithona spp., and ParaPseudocalanus spp.) through a number of mechanisms including turbulence. New insights into the dynamics of the copepod community in the western English Channel have been provided by analyzing changes in the spatial extent of assemblages in the North Atlantic on the basis of diversity. Copepod diversity in the western English Channel is generally higher than in the North Sea but is lower than in the Bay of Biscay to the south (Beaugrand et al., 2000). Seasonally, diversity is highest from May to September in the western English Channel (Beaugrand and Iban˜ez, 2002). The spatial extent of the regime shift that has been reported in the North Sea by Reid et al. (2001) was investigated by Beaugrand and Iban˜ez (2002). They found that the regime shift aVected copepod diversity in the central and northern North Sea, in the Bay of Biscay, and oV the European shelf, but that there was no significant eVect in the western English Channel or southern North Sea. The most dramatic change, however, has been the movement of warm water copepod assemblages northward, with a retraction of cold-water assemblages toward the pole. This has resulted in fewer cold-water species in the western English Channel and in an increase in the generally warm water pseudooceanic temperate species assemblage comprising Rhincalanus nasutus, Eucalanus crassus, Centropages typicus, Candacia armata, and Calanus helgolandicus (Beaugrand et al., 2002).

4.6. Zooplankton and ichthyoplankton not routinely identified Although many taxa in the CPR survey are not routinely identified to species level and are reported as a combined entity, specific studies are sometimes undertaken. These have been published in Bulletins of Marine Ecology

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throughout the history of the survey. Surveys of common species have been made for the following groups: cirripede larvae (Roskell, 1975), Clausocalanus (Williams and Wallace, 1975), Chaetognatha (Bainbridge, 1963), gastropods (Vane, 1961), ostracods (Williams, 1975), the pteropod Pneumodermopsis (Cooper and Forsyth, 1963), thaliaceans (Barnes, 1961), tintinnids (Lindley, 1975), and young fish (Henderson, 1961; Coombs, 1980). A more general account of various taxa in the North Sea was given by Marshall (1948). A detailed analysis of the distribution and seasonal cycle of decapod larvae captured by the CPR throughout the northeast Atlantic Ocean from 1981 to 1983 was conducted by Lindley (1987). The most common taxa in the western English Channel were Atelecyclus rotundatus, Galathea intermedia, Hippolyte varians, Liocarcinus puber, Pandalina brevirostris, Pilumnus hirtellus, Pisidia longicornis, total Polybinae, and Upogebia deltaura. Both the timing of the appearance of decapod larvae and their distribution were highly correlated with water temperature. These taxa are expected to be good indicators of climate change. Coombs (1975) described interannual and seasonal changes of fish larvae selected from the CPR survey. He noted that the northern limit of the distribution of Stomias boa ferox (dragonfish) shifted much further south between 1968 and 1972 and extended into the Channel, compared to 1948– 1967, when larvae were only found over deep water beyond the continental shelf. Other fish also showed a southerly shift in their distributions (e.g. Melanogrammus aeglefinus [haddock], Micromesistius poutassou [blue whiting], Scomber scombrus [mackerel], and Hippoglossoides platessoides [long rough dab]). This shift occurred over the same period that comparable changes in geographical distributions have been reported in other fish and marine invertebrates for indicating an increased boreal influence from about 1965 (Southward, 1967, 1980; Russell et al., 1971; Russell, 1973). Furthermore, the seasonal period during which most Stomias larvae were found in the Western Approaches shifted from March–April (1948–1961) to April– June (1968–1972). This was coincident with a shift in pilchard egg seasonality in the Channel to later in the year (Russell et al., 1971; Southward, 1974b; Southward et al., 1988a). This adds to the evidence already available (Southward, 1980; Southward et al., 1995) that many marine organisms underwent a marked change around 1965–1967.

5. OVERVIEW The importance of long-term records is increasingly being recognized as anthropogenically driven global climate change, together with more direct regional eVects such as fishing and pollution, are identified as major

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influences on marine ecosystems (Hawkins et al., 2003; Edwards and Richardson, 2004; Richardson and Schoeman, 2004). This recognition is coupled with an urgent need to understand the mechanisms by which these influences act on the marine environment. Such an understanding is of primary importance for interpreting changes now underway and for predicting future eVects, thereby enabling eVective management and conservation of marine biodiversity and resources. Furthermore, research emphasis will undoubtedly shift in the future, as diVerent problems become apparent; thus, records of today could help resolve future problems. Records from the western English Channel presented in this review have exceptional significance as a result of a combination of factors. These are: the location of Plymouth at the edge of many species distributions (Boreal– Lusitanian boundary), the choice of long-term monitoring stations reflecting both oceanic and coastal water properties, the wide range of environmental and biological parameters that have been systematically recorded, and the long temporal scale over which these observations extend, dating from before the onset of large-scale fisheries’ exploitation and encompassing several periods of temperature change including periods of warming, cooling, and warming again. There are, however, significant limitations to the data. First, the data are not complete; there are gaps in all datasets, notably during wars, and through the eVects of reorganisation of government-funded science. Second, methods are not consistent throughout the series. This results from a variety of factors, such as the development of new and increasingly sensitive techniques (e.g. measurement of inorganic and organic nutrients) and the use of diVerent equipment (e.g. replacement of stramin mesozooplankton nets with terylene ones; replacement of vessels incurring changes in towing speeds and, in some cases, reductions in net size). Sampling frequency has also varied during the course of the series, and even for the most well-represented sites such as E1 and L5, the data require careful treatment during analysis to account for this (Southward, 1960; Maddock and Swann, 1977). In addition, long-term records are diYcult and costly to maintain and continue. By their very nature, they cannot be funded on a short-term basis, and past hiatuses in funding have caused gaps in data sets during key periods. Major findings from this work include the dramatic changes in ecology of the western English Channel ecosystem. Three periods characterized by large shifts in the abundance of key species have been identified: 1930–1961, 1962– 1979, and 1985 onward. The first era was a period of warming that included the collapse of the herring fishery, whereas the second period of change was a cooling following the cold winters of 1961–1962 and 1962–1963 (Southward, 1980; Southward et al., 1988a). The current period is characterized by warming becoming more rapid and reaching greater maxima than any time in the twentieth century (Hawkins et al., 2003).

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Periods of strong change are separated by relatively stable intervals when the composition of the fauna and species abundances remains fairly constant (see Section 2.5; Southward, 1980; Southward et al., 1995). Steele (1985) has noted that the MBA time series supports his suggestion that marine ecosystems tend to show more marked switches between stable states than do terrestrial systems. This type of biological change needs to be considered by fishery managers, as predictions based on data for one stable system state (or domain) may not apply to an alternative stable state. The changes in the western English Channel have been collectively termed the Russell Cycle (Cushing and Dickson, 1976), although it is now apparent that the changes are not a straightforward periodic shift in species occurring at predictable frequencies and rates. Early workers based their hypotheses on what was eVectively half a cycle and did not have the benefit of the further transitional periods that are now recorded. Hypotheses regarding these shifts have attributed them to a range of causative factors (Southward, 1963, 1980). In earlier years, depleted nutrients were considered the major cause, particularly a decline in inorganic phosphate, which was presumed to have decreased productivity at a regional scale (Russell, 1933; Kemp, 1938; Harvey, 1955). When a longer time series became available, it was seen that fluctuations in nutrients are more of a symptom than a cause of changes in the ecosystem (Southward, 1963; Joint et al., 1997). Competition between similar pelagic fish species, specifically pilchard and herring, was proposed by Cushing (1961) as a possible mechanism for driving changes in the pelagic food web. Although this competition may account for changes in pelagic systems, it does not explain the trends in demersal fish, intertidal organisms, and benthic communities, leaving climatic factors as the most likely underlying cause (Southward, 1963, 1980; Southward et al., 1988a; Southward and Boalch, 1992). Climate change can operate indirectly in many ways; for example, through fluctuations in reproductive output and recruitment and by influencing oceanic circulation patterns. The overarching influence of climate, manifested as temperature change, is evident from the long-term data and has been reinforced by recent studies. Many marine organisms have clear responses to climatic features such as the strength of the NAO (Alheit and Hagen, 1997; Beaugrand et al., 2000; Irigoien et al., 2000a; Sims et al., 2001). It is most likely that interaction between low-amplitude climatic eVects plays a strong role in forcing changes (Genner et al., 2004). Results from the intertidal zone show that time lags between changes in temperature and organism abundance can be related to life histories of individual species (Southward, 1967, 1991, 1995; Southward et al., 1995), and there may well be similar time lags for changes in long-lived fish species. In contrast, short-lived species such as squid (1 year) and plankton (days, weeks, or months) respond more rapidly. Furthermore, interactions between climatic influences and physiological (e.g. growth and

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reproduction) and ecological (e.g. altered physiochemical environment, competition, and predation) factors generate complex patterns of individual species response. The complexity of interactions between organisms and climate leads to some apparent paradoxes. It has been noted (Section 2.7; Genner et al., 2004) that cod are still present oV Plymouth, whereas this cold-water species would have been predicted to decline. Equally puzzling is the apparent disagreement between the data sets on the status of the copepod Calanus helgolandicus. The samples from stations A, L5, and L4 show this species to be most abundant in the cold phases (before 1931 and from 1966 to 1980), yet data from CPR tows down the Channel indicate a positive relationship between C. helgolandicus and the NAO index (Section 4.4). There is a distinct possibility that absolute numbers of C. helgolandicus may be limited by the feeding activity of the pilchard, so that the population is depressed in warm years when pilchard are abundant on the north side of the western English Channel. There may be a comparable relationship oV California between the Pacific sardine and Calanus pacificus (Smith and Moser, 2003). Other significant findings from the Plymouth time series relate to commercial exploitation. The demersal fish records start before the large increases in commercial eVort during the last three decades of the twentieth century, allowing the substantial eVects of commercial fishing to be seen (Section 2.7). This is significant, as climatic influences on fish behaviour, which are masked by eVects of fishing in contemporary data, can be detected in historic records (e.g. influences of NAO strength on the timing of squid and flatfish migration; Sims et al., 2001, 2004). Furthermore, these data represent an entire demersal assemblage and, hence, include both commercially important and noncommercial species. Such a comprehensive data set is rare, because most management studies are directed at monitoring single, high-value species. Extended reanalysis of historic data and resampling of the same area are likely to aid in the interpretation of the wider ecological eVects of fisheries exploitation and lead to hypotheses for subsequent testing. These results will shed light on the long-term dynamics of the communities by identifying the eVect on fish populations of the interplay between climate change and fishing pressure (Genner et al., 2004). The value of long-term research lies not only in the records themselves; significant advances in understanding have come about indirectly from the long-term research programmes. Many widely accepted concepts in marine biology had their origin in Plymouth: cycling of nutrients in the sea (Atkins, 1925; Cooper, 1932, 1937, 1958b; Atkins and Jenkins, 1956), trophic interactions within pelagic food webs (Lebour, 1919, 1920, 1921; Corner and Cowey, 1968; Corner and Davies, 1971; Corner and O’Hara, 1986), diurnal vertical migratory behaviour of plankton (Russell, 1925, 1926a,b,c, 1927a,b, 1928a,b,c, 1930a, 1931a,b, 1934), and the influence of hydrographic

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properties on pelagic systems (Pingree and Pennycuick, 1975; Pingree et al., 1975, 1976, 1977a,b, 1978; Pingree, 1978; Pingree and GriYths, 1978). Furthermore, work initiated during the 1920s in marine optics (Atkins, 1926c; Atkins and Poole, 1952, 1958) provided the foundation for later work aiding the development of algorithms for estimating phytoplankton biomass from contemporary satellite ocean-colour sensors (Moore et al., 1999). More recently, the L4 data series (Figures 32, 33, and 37) is providing the foundation for many related studies such as molecular biology of zooplankton, microbial and virus ecology, and research into release of biogases (carbon dioxide, methane, and dimethyl-sulphide), as well as providing validation for satellite ocean-colour sensors. The current resurgence of interest in long-term change has led to many of the Plymouth programmes being restarted (methods are given in Table 8), although they were temporarily suspended following the terminal breakdown of RV Squilla in autumn 2003. Demersal fish collection and intertidal surveys were restarted by the MBA in January 2001, with support from the Ministry of Agriculture Fisheries and Food (MAFF)/Department of Environment, Food and Rural Affairs (DEFRA) and within the framework of the Marine Biodiversity and Climate Change (MarClim) consortium from English Nature (EN), Crown Estates, DEFRA, Scottish Natural Heritage (SNH), Scottish Executive, Countryside Council for Wales (CCW), Environment Agency (EN), States of Jersey, Worldwide Fund for Nature (WWF) and Joint Nature Conservation Committee (JNCC). The establishment of a Marine Environmental Change Network (MECN) in 2002, coordinated by the MBA, with DEFRA support, has restored full water column measurements at E1 and plankton studies (young fish and mesozooplankton) at L5 and has supported continuation of the programme at L4. Importantly, this programme has helped increase collaboration between the MBA, PML, and SAHFOS. In addition, the Plymouth–RoscoV CPR route is being restarted by SAHFOS in 2004. A key part of the MBA time-series work is the preservation of historic data. This can mean extraction from obsolete electronic formats, field notebooks, and manuscript reports. Infaunal and epifaunal benthos data have been collated from the MBA archives with funding from MAFF/DEFRA and assistance from PML. Other ongoing work involves the use of remotely sensed data to provide a spatial framework within which to interpret in situ measurements. Recent advances in technology mean that these long-term programmes are more valuable than ever before. MBA models have been used to follow a coccolithphore bloom, which moved from Eddystone Bay to the Isles of Scilly and to predict settlement of Mytilus edulis around Devon and Cornwall under real wind and tide conditions. Among future lines of work is the continued development of coupled physical-ecosystem models (e.g.

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Table 8 Sampling methods for E1 and L5, at monthly intervals, on resumption of full series in 2001 Sample type

Equipment

Methods

Double-oblique profile haul to Mesozooplankton 0.9 m2 Young 10 m depth above the seabed and young fish Fish Trawl (YFT) fitted with a 700 mm Depth and temperature profiles recorded using a data recorder Terylene net, partial Volume of water filtered filtering cod-end calculated using flow data and a Scripps recorded by a flowmeter depressor. fitted across the net mouth 2  1-L sample jars containing aliquot of 20% borax-buVered formaldehyde, for dilution by adding sample to give 5% Nutrients Rosette sampler þ 10-L water samples from 60, 40, 30, NO3, NO2, NH4, Niskin 20, 10 m, and surface PO4, SiO2 Autoanalyzer (Bran and Luebbe AA3) Phytoplankton, Rosette sampler 10 m water sample (rosette sampler) zooplankton 53 mm WP2 net 4  vertical hauls to 50 m, (2  and pigments 200 mm WP2 net 200 mm and 2  53 mm) 1  horizontal 10 m WP2 net (53 mm) haul Samples preserved in Lugol’s iodine and also examined live All pigments measured using high-pressure liquid chromatography Temperature, 2  CTDs (SeaBird Vertical profile to 65 m salinity, optical and Valeport) properties Optics rig (transmissometer, multispectral downwelling irradiance, upwelling radiance, attenuation, scattering and back-scattering)

Proudman Oceanographic Laboratory Coastal Ocean Modelling System [POLCOMS]–European Regional Seas Ecosystem Model [ERSEM]), using western English Channel time-series data to explore relationships between surface and subsurface properties to predict future changes in the ecosystem. Understanding the processes regulating marine ecosystems can require sampling over varied temporal scales. Recent technologies such as advanced

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telemetered instruments (e.g. the smart buoy system developed by the Centre for Ecology, Fisheries and Aquatic Science [CEFAS]), can enhance ongoing core research as well as focus sampling strategies by providing real-time data. Importantly, such instruments yield in situ profile data from the water column. These data, together with satellite-derived information, can greatly extend the spatial and temporal coverage of measurements, help capture processes that occur at multiple scales, and illustrate how they operate within the marine environment. Further goals are to determine the major controls structuring this system and, crucially, to determine the strength of those acting in a top-down direction (such as fishing) relative to those driven from the bottom up (climate related, such as currents, water-column stability, temperature, and light, as well as nutrients). Data from the western English Channel include records of all the key biological components within the ecosystem, along with physical and chemical environmental parameters through several periods of significant change. This holistic perspective of the system is crucial for addressing these increasingly important questions and for generation of tangible support for management and conservation policies. It is also essential for the so-called ‘‘ecosystem approach’’ currently in vogue among policy makers for the management of fisheries and marine ecosystems. In conclusion, the unique western English Channel time series started by the MBA and continued through collaboration of the MBA, PML, and SAHFOS in Plymouth are increasingly valuable for the detection of future ecological responses to environmental change. The legacy of observations collected throughout warming and cooling periods during the last century have clearly demonstrated the importance of this work in contributing to our understanding of the coastal marine environment. In the face of current unprecedented rates of change, it is vital that the lessons of the past are learnt and that these programmes are fully supported and maintained for the future.

DATA AVAILABILITY Much MBA data from E1 and the other Channel stations (1902–1987 and later) are available for research purposes on application to the Director of the MBA, but some restrictions may apply. Some raw data is accessible only by visiting Plymouth. It is expected that the biological data will be made more widely available at the end of the MarClim and MECN projects in 2005. Use of unpublished data is encouraged in collaboration with data gatherers and stewards.

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The PML data for L4 is freely available online at http://www.pml.ac.uk/L4. SAHFOS have an open-access data policy, which allows access to CPR data by the international scientific community. Monthly and annual means of the 400 taxa from the CPR database are available after signing a data agreement, although raw sample data and preserved specimens are accessible only by visiting SAHFOS. For more information on the data licensing agreement and the taxa that are routinely counted, see the SAHFOS website at http://www.sahfos.org or contact SAHFOS directly.

ACKNOWLEDGEMENTS The MBA is indebted to all past members of the laboratory staV and ships’ crews who have taken part in the long-term observations and who have collected and handled the data. In the early years (1886–1912), the MBA was supported through the Board of Trade, and then by the Department of Fisheries. From 1913 to 1964, U.K. government support was administered through the Development Commission. From 1965 to 1987, the time series was supported by the Natural Environment Research Council (NERC). Data rescue and analysis was supported by a small grant from NERC to S.J.H. and A.J.S. in 1991. Support for S.J.H. in 1980–1984 came from a NERC fellowship and a small grant. Restoration of the intertidal time series in 1996 was also funded by a small grant from NERC. The sea-going work in 2000–2003 was aided by NERC-funded ship time and by NERC-funded MBA Fellowships to S.J.H. and D.W.S. Data rescue, sampling, and analysis was helped by contracts from the Ministry of Agriculture, Fisheries, and Food (MAFF, later the Department for the Environment, Food and Rural AVairs, DEFRA) and through the Marine Environmental Change Network (MECN), funded by DEFRA. The intertidal series, since 2001, has been supported by the MarClim project, with consortium funding from English Nature, the Crown Estates, the Environment Agency, the Countryside Council for Wales, Scottish Natural Heritage, the Department of the Environment Fisheries and Rural AVairs, the Scottish Executive, the World Wildlife Fund, and the States of Jersey. We are grateful to T.J. Smyth, NERC Remote Sensing Data Analysis Service, PML, for providing satellite images. PML is funded by the U.K. NERC as a NERC Collaborative Research Centre. Additional funding during the period of study has been provided by the European Union, the U.K. Department of the Environment, and DEFRA. The L4 series has been maintained through a combination of diVerent projects, including PML and Core Strategic support, NERC Community Research, Special Topic and Thematic Programme grants, EU

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projects, and a number of University Studentships. More recently partial support has been provided through MECN. The data set has been maintained by Roger Harris through a combination of diVerent projects. Most of the analyses have been carried out by visiting workers and students. As part of the NERC Marine Productivity Thematic Programme the data have been assembled in the format of an atlas (www.pml.ac.uk/L4). The following are thanked for their help in this respect: Derek Harbour, Bob Head, Angel Lopez-Urrutia, Xabier Irigoien, Tania Smith, and the masters and crews of Sepia and Squilla. Also thanked for help at sea or in the laboratory are Jose Luis Acun˜a, Ricardo Anadon, Begon˜a Bautista, Alain Bedo, Delphine Bonnet, Claudia Castellani, Kathryn Cook, Cilla Course, Emilio Fernandez, Edmund Green, Castor Guisande, Dave Lesley, Alistair Lindley, German Medina, Diego Menendez, Diana Menzel, Bettina Meyer-Harms, Carmen Morales, Birgit Obermu¨ller, David Pond, Catherine Rey (Rassat), Dave Robins, Rachel Schreeve, Paul Tranter, Rachael Woodd-Walker, Pennie Woodyer (Lindeque), and Lidia Yebra. SAHFOS is grateful to all past and present members and supporters of the CPR survey, especially the shipping industry that voluntarily tows CPRs on regular routes. The CPR survey has been recently funded by a consortium consisting of the International Oceanographic Commission and agencies in Canada, The Faroes, France, Iceland, Ireland, the Netherlands, Portugal, and the United States. United Kingdom core funding is provided by DEFRA and NERC.

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Aiken, J. and Bellan, I. (1990). Optical oceanography: an assessment of a towed method. In ‘‘Light and life in the sea’’ (P. J. Herring, A. K. Campbell, M. Whitfield and L. Maddock, eds.), pp. 39–57. Cambridge University Press, Cambridge. Aiken, J. and Kelly, J. (1984). A solid state sensor for mapping and profiling stimulated bioluminescance in the marine environment. Continental Shelf Research 3, 455–464. Aiken, J., Fishwick, J., Moore, G. and Pemberton, K. (2004). The annual cycle of phytoplankton photosynthetic quantum eYciency, pigment composition and optical properties in the western English Channel. Journal of the Marine Biological Association of the United Kingdom 84, 301–313. Alheit, J. and Hagen, E. (1997). Long-term climate forcing of European herring and sardine populations. Fisheries Oceanography. 6, 130–139. Allen, E. J. (1899). On the fauna and bottom deposits near the thirty-fathom line from the Eddystone grounds to Start Point. Journal of the Marine Biological Association of the United Kingdom 5, 365–542. Allen, E. J. (1917). Post-larval teleosts collected near Plymouth during the Summer of 1914. Journal of the Marine Biological Association of the United Kingdom 11, 207–250. Allen, E. J. (1919). A contribution to the quantitative study of plankton. Journal of the Marine Biological Association of the United Kingdom 12, 1–8. Allen, E. J. (1922). The progression of life in the sea. Nature 110, 448–453. Allen, E. J. and Nelson, E. W. (1910). On the artificial culture of marine planktonic organisms. Journal of the Marine Biological Association of the United Kingdom 8, 412–474. Armstrong, F. A. and Butler, E. I. (1962). Hydrographic surveys oV Plymouth in 1959 and 1960. Journal of the Marine Biological Association of the United Kingdom 42, 445–463. Armstrong, F. A. and Tibbitts, S. (1968). Photochemical combustion of organic matter in sea water for nitrogen, phosphorus and carbon determination. Journal of the Marine Biological Association of the United Kingdom 48, 143–152. Armstrong, F. A. J., Butler, E. I. and Boalch, G. T. (1970). Hydrographic and nutrient chemistry surveys in the western English Channel during 1961–1962. Journal of the Marine Biological Association of the United Kingdom 50, 883–905. Armstrong, F. A. J., Butler, E. I. and Boalch, G. T. (1972). Hydrographic and nutrient chemistry surveys in the western English Channel during 1963–1964. Journal of the Marine Biological Association of the United Kingdom 52, 915–930. Armstrong, F. A. J., Butler, E. I. and Boalch, G. T. (1974). Hydrographic and nutrient chemistry surveys in the western English Channel during 1965 and 1966. Journal of the Marine Biological Association of the United Kingdom 54, 895–914. Atkins, W. R. G. (1923). The phosphate content of fresh and salt waters in its relationship to the growth of the algal plankton. Journal of the Marine Biological Association of the United Kingdom 13, 119–150. Atkins, W. R. G. (1925). Seasonal changes in the phosphate content of seawater in relation to the growth of the algal plankton during 1923–1924. Journal of the Marine Biological Association of the United Kingdom 13, 700–720. Atkins, W. R. G. (1926a). The phosphate content of seawater in relation to the growth of the algal plankton. Part III. Journal of the Marine Biological Association of the United Kingdom 14, 447–467. Atkins, W. R. G. (1926b). Seasonal changes in the silica content of natural waters in relation to the phytoplankton. Journal of the Marine Biological Association of the United Kingdom 14, 89–99.

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Interactions Between Behaviour and Physical Forcing in the Control of Horizontal Transport of Decapod Crustacean Larvae Henrique Queiroga* and Jack Blanton{

*Departmento de Biologia, Universidade de Aveiro, Campus Universita´rio de Santiago, 3810-193 Aveiro, Portugal E-mail: [email protected] { Skidaway Institute of Oceanography, Savannah, Georgia 31411, USA 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Definitions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Larval Stages. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Types of Vertical Migration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Ecological Categories. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Marine Physical Processes and Larval Transport Mechanisms . . . . . . . . . . . . . . . . . . . . . 3.1. Tides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Wind-Induced Currents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Buoyancy-Induced Currents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4. Geostrophic Currents. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5. Cross-shelf Flow and Exchange . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6. Internal Waves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.7. Sea and Land Breezes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.8. Interaction of Migratory Behaviour With Tidal Currents . . . . . . . . . . . . . . . . . . . . . . 3.9. Estuarine Transport . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.10. Transport Regimes Along Continental Margins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.11. Frontal Zones as Sites of Larval Congregation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Cyclic Vertical Migration in the Natural Environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Sampling Methodology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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4.2. Prevalence of Cyclic Vertical Migration According to Taxonomic and Ecological Category . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ontogenetic Migration and the Extent of Vertical Movements . . . . . . . . . . . . . . . . . . . . . Significance of Vertical Migration in Dispersal: Evidence from Field Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.1. Tidal Migrations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2. Diel Migrations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.3. Ontogenetic Migrations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Proximate Factors Controlling Vertical Migration: Environmental Factors and Endogenous Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.1. Tactic and Kinetic Responses by Estuarine and Marine Larvae . . . . . . . . . . . . . . . 7.2. Endogenous Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Behavioural Control of Vertical Migration: Evidence from Laboratory Studies. . . . . . . 8.1. Responses to Environmental Factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.2. Endogenous Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nonrhythmic Vertical Migration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Mechanism for Depth Regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Modifiers of Vertical Migration Pattern: Temperature, Salinity, and Food . . . . . . . . . . . Vertical and Horizontal Swimming Velocities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Measurements of Horizontal Transport . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.1. Tagging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.2. Larval Velocity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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We summarize what is known of the biophysical interactions that control vertical migration and dispersal of decapod larvae, asking the following main questions: How common is vertical migration in decapod crustacean larvae? What is the vertical extent of the migrations? What are the behavioural mechanisms that control vertical migrations? How does vertical migration interact with the physics of the ocean to control the dispersal of larvae? These questions are analysed by first giving a synopsis of the physical processes that are believed to significantly aVect horizontal transport, and then by describing migration patterns according to taxon, to ecological category based on the habitat of adults and larvae, and to stage within the larval series. Some kind of vertical migration has been found in larval stages of virtually all species that have been investigated, irrespective of taxonomic or ecological category. Most vertical migration schedules have a cyclic nature that is related to a major environmental cyclic factor. Tidal (ebb or flood) migration and daily (nocturnal and twilight) migration are the two types of cyclic migration that have been identified. In general, all species show some type of daily migration, with nocturnal migration being the most common, whereas tidal migrations have only been identified in species that use estuaries during part of their life cycle. Moreover, there are several examples indicating that the

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phasing and extent of migration both change throughout ontogeny. Reported ranges of vertical displacement vary between a few metres in estuaries and several tens of metres (sometimes more than 100 m) in shelf and oceanic waters. Vertical movements are controlled by behavioural responses to the main factors of the marine environment. The most important factors in this respect are light, pressure and gravity, but salinity, temperature, turbulence, current and other factors, also influence behaviour. Many of these factors change cyclically, and the larvae respond with cyclic behaviours. The type of response may be endogenous and regulated by an internal clock, as in the case of some tidally synchronised migrations, but in most cases it is a direct response to a change in an environmental variable, as in diel migration. The reaction of the larvae to exogenous cues depends both on the rate of change of the variable and on the absolute amount of change. A series of dispersal types, involving diVerent spatial and temporal scales, have been identified in decapod larvae: retention of the larval series within estuaries; export from estuarine habitats, dispersal over the shelf, and reinvasion of estuaries by the last stage; hatching in shelf waters and immigration to estuaries by late larvae or postlarvae; complete development on the shelf; and hatching in shelf waters, long-range dispersal in the ocean, and return to the shelf by late stages. In all of these cases, vertical migration behaviour and changes of behaviour during the course of larval development have been related to particular physical processes, resulting in conceptual mechanisms that explain dispersal and recruitment. Most decapod larvae are capable of crossing the vertical temperature diVerences normally found across thermoclines in natural systems. This ability may have significant consequences for horizontal transport within shelf waters, because amplitude and phase diVerences of the tidal currents across the thermocline may be reflected in diVerent trajectories of the migrating larvae.

1. INTRODUCTION Decapod crustacean larvae are large and they can be powerful swimmers. Nevertheless, their swimming abilities are generally insuYcient to counteract the action of the horizontal currents that are typical of coastal and estuarine systems (Mileikovsky, 1973; Chia et al., 1984; Young, 1995). A recurrent theme in research into the dispersal of larvae is that their vertical position aVects dispersal pathways through interaction with depth-varying currents (see Sammarco and Heron, 1994, and bibliographies cited therein). Given their comparatively strong swimming capacity, it is also believed that decapod larvae can actively modify their vertical position in the water column and that, by doing so, they can to some extent control the range and

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direction of their horizontal dispersal. Many of the field studies that investigated the depth distribution of decapod larvae (reviewed in Section 6) have found spatial distributions that can best be interpreted as resulting from active vertical migration that is very often of a rhythmic nature. One may ask, however, whether these migrations are real or an artifact of sampling programmes. The phenomena involved in vertical and horizontal dispersal of marine planktonic organisms operate in multiple spatial and temporal scales (Harris, 1980; Pinel-Alloul, 1995). The logistic problems of sampling invertebrate larvae with enough resolution in the three spatial dimensions and along time, especially when having to account simultaneously for scales of variation that might vary by several orders of magnitude, are not easy to solve with present-day technologies. Larvae are small organisms that easily escape detection and that are impossible to track individually, except in a few invertebrate groups (e.g., Svane and Young, 1989). For instance, when trying to understand the mechanism of estuarine invasion by crab megalopae, a common sampling method is the use of fixed-station studies to measure the vertical distribution of the larvae over the water column for a number of tidal cycles. Such studies reveal large numbers of megalopae in samples collected during flood tides, which has been interpreted as night-time evidence for active swimming during night flood tides (see Section 6). However, a similar pattern could also result from predation on the megalopae during the day and at ebb tide. Our belief that the observed pattern results from active swimming is based on laboratory examination of larval behaviour. It has been demonstrated that endogenous rhythms or tactic and kinetic responses to environmental stimuli associated with the tidal and daily cycles elicit swimming responses of crab megalopae that agree with observed field distributions (Section 8). In contrast, it has never been shown that the diVerential predation pressure allocated to the diVerent combinations of the tidal and diel cycles could result in the observed pattern. Therefore, the most parsimonious explanation is that the pattern results from vertical migration from the bottom into the water column during night flood tides. Many other examples of what have been interpreted as active migratory behaviours have been similarly supported by experimental data. However, predation and physical stress are believed to be the major selective pressures for the development of vertical migration. Most species that live in estuaries as adults are known to export their larvae to the sea (Sandifer, 1975; Christy and Stancyk, 1982; Dittel and Epifanio, 1990; Pereira et al., 2000). The export strategy was initially interpreted as an adaptation to promote gene flow and colonization of new habitats (Scheltema, 1975). This opinion has been challenged with the argument that severity of physical and biological conditions in estuaries that favored the evolution of behavioural traits that result in an export to the sea (Anger, 2001).

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Such traits include hatching rhythms synchronised with tidal and diel cycles (Forward, 1987b; Morgan and Christy, 1994), as well as tidallysynchronised vertical migrations that enhance seaward transport (Forward and Tankersley, 2001). The high osmotic and thermal stresses and intense pelagic predation characteristic of the estuarine environment demand special adaptations, and by spending most of their larval development in the sea, larvae would avoid such constraints (Strathmann, 1982, 1993; Morgan, 1995). In support of this theory, exported larvae of decapod Crustacea seem to lack cryptic, anatomical, and chemical defenses against predation by juvenile fish (Morgan, 1987; Hovel and Morgan, 1997). In addition osmotic stress caused by low salinity results in a reduced energy assimilation capacity and in reduced conversion to tissue growth (Anger et al., 1998; Anger, 2003), resulting in death at the D0 moult stage (see Anger, 1983, for definition of moult stages in larval decapods) and at exuviation. Some species do retain their larvae inside the estuary, which can only be accomplished by tidally synchronised vertical migration (Cronin, 1982). Therefore, whatever pressures are at work to select for retention or export of larvae, tidally synchronised vertical migration is the only way that planktonic larvae can use to cope with the strong tidal currents of the estuarine environment. Many zooplankton display diel vertical migration behaviours, as do decapod larvae. The currently accepted view for explaining nocturnal and reversed migration is the predator-avoidance hypothesis (Zaret and SuVern, 1976; Lampert, 1989, 1993). This hypothesis has been supported by studies showing that diel vertical migration is enhanced by the presence of predator fishes (e.g., Dini and Carpenter, 1988; Dawidowicz et al., 1990). Similar results were obtained with the larvae of a brachyuran crab, where it was shown that fish mucus and chemical substances produced by its degradation induce descent (Forward and Rittschof, 2000). This descent reaction is caused by a lowered intensity threshold for negative phototaxis, which is inversely related to mucus concentration. Therefore, as the concentration of chemical substances originating from fish mucus increases, the photonegative reaction is triggered by increasingly lower light intensities, which cause the larvae to move deeper (Forward and Rittschof, 2000). It is not known whether dispersal-related pressures could also select for diel vertical migration, but, as diel vertical migration has the potential to interact with periodic components of the flow field in marine systems (Shanks, 1995; Hill, 1998), dependable dispersal mechanisms are among its likely consequences. In addition to tide- and day-synchronised vertical migrations, decapod larvae are known to change their average depth of distribution throughout ontogenetic development (Section 5). The evidence comes both from the observations of a vertical segregation of the larval stages in the natural environment, which is also supported by experimental studies on behaviour,

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and from a segregation in the horizontal plane. DiVerential distributions of larval stages within the larval series of a species could, in theory, result from purely physical properties such as centre of gravity without the intervention of behaviour, because the mechanic properties of a larva change as it grows older (Chia et al., 1984). Therefore, the larva would react in a changing way to the flow field during development. However, purely physical mechanisms that can account for diVerences in horizontal transport over the diversity of environmental situations encountered by decapod larvae are not known. Because decapod larvae usually hatch from bottom-dwelling females, feed in surface waters, and must subsequently return to the bottom at settlement, ontogenetic migrations are mandatory processes. The adoption of a planktonic larval phase may originate from the need to avoid a benthic environment rich in predators or for feeding reasons (Pechenik, 1999; Strathmann et al., 2002). The change of depth distribution during ontogeny, including the competent stage, might be related to the need to use currents that vary with depth to maximize the probability of transport to a suitable habitat for settlement. It is intuitively easy to accept that the longer the duration of the larval phase, the higher the dispersal potential. In support of this view, Shanks (personal communication 2003) found a positive correlation between larval development time and dispersal distance. Because currents, especially in coastal waters, are not unidirectional, and because there are several mechanisms (Section 3) that can retain larvae in the geographic area where they were released, the predicted relationship between development time and dispersal distance of often breaks down. There is an ongoing debate concerning the existence of marine metapopulations, the connectivity of local populations, and the probability of occurrence of self-recruitment (Gaines and LaVerty, 1995; Botsford et al., 1998; Sponaugle et al., 2002; Strathmann et al., 2002), which is nourished by the basic diYculty of measuring the flux of small larvae in a complex marine environment. Given the extended larval development time of many decapods, which as a rule ranges from weeks to months, it is likely that these species frequently exchange larvae among local populations. To understand the processes aVecting the dispersal and supply of planktonic decapod larvae, it is necessary to know both the biology of the larvae, including characteristics of larval behaviour, development, growth, and mortality, and the physical setting in which they develop. Comprehension of these processes allows predictions of the rates, location, and timing of larval supply and settlement. The prediction of a specific outcome is only possible when the process itself is deterministic. In the case of larval supply and recruitment, prediction calls for a clear understanding of the biological and physical mechanisms involved and of their interactions. The nature of marine physical processes that result in dispersal at a scale relevant to biological populations (i.e., of the order of 1–1000 km) does not

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account for the fate of individual larvae but, rather, for sets of larvae hatched from ensembles of females. Even larvae hatched from individual females can presumably have diVerent dispersal trajectories because of turbulent diVusion processes (Okubo, 1994). Many of the physical processes reviewed here are cyclic or otherwise predictable on a timescale that is relevant for ecological processes and can be measured, provided appropriate observational strategies are implemented. However, these processes interact with each other and with bottom topography and latitude in such a way that particular ‘‘rules’’ apply to each individual geographic and oceanographic context. Hence, it is not surprising to find that better insights have been obtained in areas of relatively simplified circulation such as estuaries and shallow gulfs, and in areas where the physical oceanography has been well described. Larval dispersal and recruitment can be regarded as stochastic at the individual level but deterministic at the population level. Significant understanding of the processes that control the dynamics of marine populations with larval dispersal cannot be reached unless we know both the physics of the particular system where the life cycle of the population is accomplished, and all its relevant spatial and temporal scales, and the biology of the larval phase, including growth and mortality rates, feeding, and behaviour, as well as its interaction with the physics of the systems. In this review, we summarize what is known of the biophysical interactions that control vertical migration and dispersal of decapod larvae. We emphasize coastal benthic species because these are by far the best studied. First, the physical mechanisms that operate in estuaries and coastal areas are described, with reference to examples where these physical processes have been indicated to play a role in the dispersal of the larvae. Next, the type, prevalence, and vertical extent of vertical movements are reported. The significance of the vertical movements for dispersal control is then analysed with the help of selected examples, followed by an account of the proximate factors that control the vertical movements of the larvae. Finally, the factors that may modify vertical migration behaviour and some of the techniques used to measure the extent of the horizontal movements are examined.

2. DEFINITIONS 2.1. Larval stages Decapod crustaceans show a diversity of larval morphologies and development patterns (Figure 1). Classification of development patterns is based on the types of larvae, number of stages, and presence or absence of metamorphic transitions, and it reflects phylogenetic relationships (reviewed by

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Figure 1(a)

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Figure 1(b)

(Continued)

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Gurney, 1942; Williamson, 1982; Anger, 2001). Moreover, the average duration of larval ontogeny can change both across and within development patterns, with some species showing abbreviated development—usually accompanied by lecithotrophy—or even direct development (Anger, 2001). The common characteristic shared by most decapod species that is relevant for dispersal is that their larvae cannot significantly control horizontal dispersal by consistently swimming against horizontal currents. Because larval behaviour changes during development (Section 4), it is convenient to analyse behavioural reactions and dispersal mechanisms according to larval stage. To simplify the analyses, larval stages are classified simply as first stage, intermediate stages, and last stage. First-stage larvae are those just hatched from the egg and include the first zoea of the Pleocyemata. Although the first nauplius of the Dendrobranchiata is also a first stage, we do not know of accounts of its dispersive ecology, and it will not be included in the analysis. The last stage is here understood as the transitional stage between the planktonic larval phase and the benthic juvenile. It includes the various forms of the decapodid stage sensu Kaestner (1980) and Anger (2001). Also included here are the fourth instar of the Nephropoidea and the postlarvae of the Dendrobranchiata, which lack the morphological characteristics that define them as larvae (Anger, 2001), but which disperse in the plankton and are therefore subjected to transport by currents. 2.2. Types of vertical migration Vertical migration of crab larvae falls into two main types: cyclic migration and ontogenetic migration. During cyclic migration, larvae move up and down in the water column in synchrony with one or more environmental

Figure 1 (a) Examples of larval forms of the major infraorders or divisions within the decapod crustaceans. A: first zoea of Parapenaeus longirostris (Dendrobrachiata), B: first zoea of Palaemon elegans (Caridea), C: first zoea of Nephrops norvegicus (Astacidea), D: first zoea of Callianassa tyrrhena (Thalassinidea), E: third phyllosoma of Palinurus elephas (Palinura), F: first zoea of Pisidia longicornis (Anomura), G: first zoea of Anapagurus sp. (Anomura), H: first zoea of Carcinus maenas (Brachyura). Redrawn from dos Santos (1999) except A, which was redrawn from Heldt (1938), and H, drawn from Rice and Ingle (1975). (b) Examples of post larval forms of the major infraorders or divisions within the decapod crustaceans. A: first postlarva of Parapenaeus longirostris (Dendrobranchiata), B: first postlarva of Palaemon elegans (Caridea), C: stage IV of Nephrops norvegicus (Astacidea), D: megalopa of Callianassa tyrrhena (Thalassinidea), E: puerulus of Palinurus elephas (Palinura), F: megalopa of Anapagurus laevis (Anomura), G: megalopa of Carcinus maenas (Brachyura). Redrawn from: A: dos Santos (1999); B: Ho¨glund (1943); C: Santucci (1926a); D: dos Santos (1999); E: Santucci (1926b); F: MacDonald et al. (1957); G: Rice and Ingle (1975).

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cycles. The two most important natural cues that may synchronise migration are the diel cycle and the tidal cycle, although other environmental periodic oscillations, like the current cycle in estuaries, may also have the potential to entrain periodic responses by larvae. Ontogenetic migration occurs when larvae change their average depth of distribution over the course of the larval period, and it may occur over a background of cyclic vertical migration (see examples in Lindley et al., 1994). Ontogenetic migration is an obligatory process in the case of benthic crustaceans because the larvae hatch from eggs carried by the bottom-dwelling females, disperse and feed in the water column, and then must return to the adult habitat for settlement. Diel vertical migration is a well-known phenomenon among zooplanktonic species. According to Forward (1988), there are three types of diel vertical migration: nocturnal migration, characterized by a daily ascent to a minimum depth between sunset and sunrise; reverse migration, when the daily ascent to the minimum depth occurs during the day; and twilight migration, when a minimum depth is reached near sunset, followed by a descent to intermediate depths during the night and a subsequent ascent near sunrise, before the animals regain the depth level usually occupied during day hours. Tidally timed migrations appear to be much less common than diel migrations, but recent studies made across diVerent invertebrate and fish taxa indicate that larvae of most, if not all, species that inhabit estuaries during some part of their existence migrate in synchrony with the tidal cycle as a way to control their horizontal transport (DeCoursey, 1976; Cronin and Forward, 1982; Laprise and Dodson, 1989; Olmi, 1994; Queiroga et al., 1997; Joyeux, 1998; Jager, 1999). There is no standard terminology to classify the types of tidal vertical migration, despite its importance to selective tidal stream transport (Forward and Tankersley, 2001). For simplification, we will define tidal migration here in a way that is similar to that in which diel migration is defined (i.e., according to the phase of the cycle when the animals are closer to the surface): flood migration, when the larvae rise in the water column during the rising tide, and ebb migration, when the larvae ascend in the water column during the receding tide. These categories of vertical migration are not mutually exclusive. Rhythmic migration can, and very often does, occur over a background of ontogenetic migration. Also, estuarine zooplankton very often display tidal, diel, and ontogenetic components in their vertical movements.

2.3. Ecological categories For the present purpose, decapod species are classified into ecological categories according to the combination of habitats where adults and larvae live. The justification for this is that larvae are subjected to diVerent

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Table 1 Ecological categories of decapod crustaceans according to habitat of adults and larvae Ecological category Obligate estuarine species Estuarine species that export their larvae to shelf waters Shelf species that may penetrate estuaries as adults Shelf species that use estuaries as nursery habitats Shelf species Shelf and slope species

Habitat of adults

Habitat of larvae

Estuary Estuary

Estuary Shelf

Shelf, estuary

Shelf

Shelf

Shelf, estuary

Shelf Shelf, slope

Shelf, ocean Shelf, ocean

environmental factors and forcing agents according to the habitat where they hatch, where they develop, and to which they have to return for successful settlement and metamorphosis. Six ecological categories are considered (Table 1): obligate estuarine species, estuarine species that export their larvae to shelf waters, shelf species that may penetrate estuaries as adults, shelf species that use estuaries as nursery habitats, shelf species, and shelf and slope species.

3. MARINE PHYSICAL PROCESSES AND LARVAL TRANSPORT MECHANISMS Invertebrate larvae in the marine environment are dispersed by currents. A number of physical processes with the capacity to transport larvae predictably have been proposed (reviewed by Boehlert and Mundy, 1988; Shanks, 1995; Epifanio and Garvine, 2001). In all these processes, the rate and direction of transport depends critically on the time of occurrence and the depth distribution of the larvae. It is this interaction between larval behaviour and the environmental forcing agents that marine biologists call a ‘‘recruitment mechanism.’’ The aim of this Section is to describe the physical mechanisms operating in estuaries, shelf areas, and the ocean, and to evaluate their role in the dispersal and transport of decapod crustacean larvae. Circulation regimes relevant to larval transport occur over time scales ranging from seconds to months. Here, we focus on time scales ranging from hours to months. The spatial scales included range from 1 m to 1000 km.

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Circulation aVects larval transport through the nonlinear interaction of many processes. Tidal transport advects waters of diVerent density to diVerent places, and the resulting gradients generate currents that are superposed on the tidal currents themselves. Wind-generated transport adjacent to coasts causes vertical motion, with the accompanying readjustment of the density field, which further aVects horizontal motion through a concomitant increase or decrease in sea level. These sea-level changes propagate into estuaries and influence the estuarine circulation. These are but a few examples. Larvae, while making their trip within or between the diVerent compartments of the marine environment, encounter these complexities. The coupling between larval behaviour and the vertical and horizontal gradients in currents results in a complex trajectory for an individual larva. In this section we first define some of the basic processes responsible for the diVerent aspects of ocean circulation that are relevant to the understanding of larval transport mechanisms. A detailed explanation is beyond the scope of this review, and the interested reader should consult additional references. Excellent introductions to interactions between physical and biological processes in the ocean are Bakun (1996) and Mann and Lazier (1996). Later, specific transport mechanisms will be analysed and illustrated with appropriate references.

3.1. Tides The tides forced by the gravitational fields of the moon and sun induce periodic changes in water level (the ‘‘vertical tide’’). Periodic rise and fall of the tide in coastal margins can inundate large intertidal areas, depending on the slope of the landscape. Spatial changes in elevation and phase of the tidal wave induce the currents (the ‘‘horizontal’’ tide). These tidal currents periodically advect water masses from one place to another, as well as provide the energy to mix the water masses. A given tide can be described in terms of the tidal constituents that define the responsible periodic astronomic forces. Two of the most common constituents are the M2 (the semidiurnal lunar constituent) and the S2 (the semidiurnal solar constituent). The interaction of M2 with a period of 12.42 h with S2 with a period of 12.00 h produces the familiar spring–neap cycle with a period of about 14 days. Diurnal constituents such as K1 and O1 govern the degree of diurnal inequality in the tide. It is the relative magnitude of tidal constituents at a given location that governs the characteristics of the tide, such as the spring-neap diVerences in tidal magnitude, the

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diVerences within a day between two consecutive tides, and whether the tidal regime at a location is semidiurnal, diurnal, or mixed.

3.2. Wind-induced currents Winds exert a pressure on the water surface that in turn generates horizontal and vertical circulation. Because of the Earth’s rotation, any water mass set into motion is deflected to the right in the northern hemisphere and to the left in the southern hemisphere. This is known as the Coriolis eVect. In an ocean without density diVerences, and away from the coast, the combined action of the wind and the Coriolis eVect causes a progressive deflection of the current to the right/left in the northern/southern hemisphere as depth increases, down to a level where frictional influence of the wind is dissipated. This spiral-like motion is called the Ekman spiral. The vertically integrated horizontal transport of water within this Ekman layer is 90 degrees to the right/left in the northern/southern hemisphere. In the presence of a shoreline, continuity requires that water lost or gained at the coast causes upwelling of water from greater depth or downwelling of water to greater depth.

3.3. Buoyancy-induced currents When waters of diVerent densities are brought together (e.g., by tidal or wind-generated currents), the lighter water tends to ride over the heavier water. The resulting currents are a direct consequence of the density diVerence of the two water masses. This density diVerence reduces the eVect of gravity, and a continuous supply of the low-density water represents a supply of buoyancy. In the presence of tidal mixing, which is particularly eYcient in shallow water, the buoyancy diVerences tend to decrease. But in estuarine and coastal areas that receive significant volumes of fresh water, buoyancy can be supplied faster than mixing can destroy the density diVerence. Buoyancy-induced currents are a direct result of horizontal gradients of buoyancy.

3.4. Geostrophic currents The spatial diVerence in water pressure along a reference surface is the primary driving force for horizontal currents. The principal balancing forces are friction and the Coriolis force caused by Earth’s rotation. In deep water, frictional boundary layers at the surface and the bottom are only a small

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fraction of the total water depth, so that the primary force balance is between the horizontal pressure gradient and the Coriolis force. Currents resulting from this force balance are in geostrophic equilibrium, and the currents are called geostrophic currents. In shallow continental shelves, where the frictional layers become a significant fraction of the total water depth, this balance no longer holds, except for in a narrow zone of the water column called the geostrophic interior. In fact, these boundary layers can merge in shallow waters close to the coast, thus preventing a geostrophic balance from occurring. This merging will be covered in more detail in the following text.

3.5. Cross-shelf flow and exchange Wind and bottom stress form surface and bottom boundary layers that, given water of suYcient depth, are separated by an interior region in which the flow is in geostrophic balance. The strength of cross-shelf transport (i.e., the Ekman flow) in these boundary layers is governed by the expression t VE ¼ rf where VE is the Ekman transport, t is the shear stress at the surface or bottom boundary, r is water density, and f is the Coriolis parameter. For winds blowing parallel to the coast in the Northern Hemisphere, oVshore surface transport occurs when the coast is to the left, with a compensating shoreward flow in the bottom boundary layer. This produces an upwelling of deep water to replace the water lost in the surface boundary layer. The opposite (i.e., downwelling) occurs when the coast is to the right of the wind component. The circulation regimes on continental shelves are easily altered by the relative strength of vertical mixing and depth (Garrett and Loder, 1981; Csanady, 1982; Blanton et al., 1995), which, in turn, governs the thickness of each boundary layer. The thickness is a function of stress (surface and bottom) and the horizontal density gradient. Density gradients cause the thickness to be diVerent depending on upwelling or downwelling conditions (Trowbridge and Lentz, 1991; Blanton, 1996). Assuming water is less dense along the coast as a result of freshwater discharge, upwelling brings less dense coastal water over the top of denser water, and vertical stratification increases, thus inhibiting vertical mixing. Downwelling, however, advects higher-density water next to lighter water, and vertical mixing caused by the resulting convection diminishes, or even destroys, vertical

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Figure 2 (a) Vertical mixing is very eYcient for downwelling, and horizontal density gradients are enhanced. The surface and bottom boundary layers merge in deeper waters over the shelf, thus creating a wide zone shoreward, where the net current, consisting of a mixture of surface and bottom water, moves into an estuary. The water is usually low in nutrients. Larvae accumulate within this ‘‘pooling zone’’ and are not swept oVshore or onshore but are transported eYciently along the shore. The net flow shoreward is the amount necessary to account for the increase in sea level caused by downwelling. (b) During upwelling, vertical mixing is inhibited, which enhances vertical stratification. The surface and bottom boundary layers merge closer

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stratification, which is replaced by larger, horizontal density gradients. Because of the asymmetry in vertical mixing between upwelling versus downwelling conditions, the thickness of the bottom boundary layer can increase from typical values of 15 m to as large as 50 m (Trowbridge and Lentz, 1991). Shallow and wide continental shelves can have relatively thick surface and bottom boundary layers and a relatively thin or nonexistent geostrophic zone (Blanton et al., 1995). This is because vertical mixing occurs over a relatively small depth, thereby bringing the surface and bottom boundary layers close together and even causing them to merge. Such shelves are found in several regions of the world’s oceans, including the southeastern United States, the North Sea oV the northern European coast, the west coast of Korea, and the Canadian Arctic. Upwelling and downwelling cycles on shallow, wide shelves can drive large mass exchanges with connecting estuaries (Figure 2). Downwelling circulation pumps large volumes of water into estuaries (Blanton et al., 1995), which could be potentially favourable to larval ingress. However, attempts to correlate the settlement of blue crab megalopae with downwelling events (southward wind stress) have had mixed success on the southeastern U.S. coast (Blanton et al., 2001). Similar attempts along the middle portion of the eastern U.S. coast have been more successful (Goodrich et al., 1989; Little and Epifanio, 1991; Jones and Epifanio, 1995). Upwelling and downwelling cycles appear to be the key to understanding the transport and settlement cycle of blue crab in the mid-Atlantic coast of the United States (see Epifanio and Garvine, 2001, and references therein). Earlystage zoeae are entrained in the buoyant outflows of estuaries like Delaware Bay and Chesapeake Bay, where they are ejected onto the continental shelf. Instead of flowing farther southward in the buoyant jet, the summer circulation generated by the prevailing northward wind stress (upwelling favourable) spreads the waters of the jet seaward and northward, which retains the larvae in the midshelf oVshore of the parent estuaries. Subsequent periods of downwelling in late summer and autumn return the later stages of the larvae to a nearby estuary. The transport and recruitment cycle of blue crab larvae has been successfully modelled by Garvine et al. (1997).

to shore, thus narrowing the ‘‘pooling zone.’’ Flow is most eYcient in the along-shore direction but occurs in a narrower zone than in panel (a). The shoreward flowing bottom water does not enter the estuary except as a mixture with the surface water. The out-flowing water is the amount necessary to account for the decrease in sea level caused by upwelling. (c) The only diVerence between this panel and panel (b) is that the estuary has a deep connection with the ocean (as in the Galician Rias). This allows nutrient-rich water to enter the estuary directly.

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3.6. Internal waves The hypothesis that internal waves can transport larvae shoreward on continental shelves has been advanced by Shanks (1983, 1988). As pointed out by Epifanio and Garvine (2001), the particles advance through the wavefronts at a diVerent speed than the phase speed itself. Studies by Franks (1997) have confirmed this by showing that particles pass into and out of the convergent zones of the internal waves. Thus, it seems doubtful that internal waves can provide a significant mechanism for cross-shelf larval transport (Burrage and Garvine, 1987; Epifanio and Garvine, 2001), except, perhaps, in those rare cases where little or no vertical mixing occurs. 3.7. Sea and land breezes Many coasts are subject to sea and land breezes, which are diurnal fluctuations in winds perpendicular to the coast. These are generated by the heating of the land during the day, which induces the heated air to rise. The rising air is replaced by cooler air from the ocean. The opposite occurs at night, when the land cools (Stull, 1988). Studies of currents on the continental shelf can usually resolve some peak in energy of the cross-shelf current at diurnal frequencies, but the peaks can be easily confounded by the presence of diurnal tidal constituents such as K1 and O1. Moreover, it has been theoretically shown that the cross-shelf wind components can, for all practical purposes, be neglected as agents of water-volume exchange when compared with the along-shelf component (Klinck et al., 1981). Although we know of no studies that have clearly related larval transport to the presence or absence of sea breezes, this mechanism has been proposed by Shanks (1995) as a way for cross-shelf transport. This is based on observations that larvae may reside in the neuston layer, where transport should be downwind, during some parts of the day. 3.8. Interaction of migratory behaviour with tidal currents Although the cumulative results of average wind patterns and buoyancy forces impose a long-term average circulation pattern in both estuaries and oceans, larvae probably are not greatly aVected by the ‘‘average’’ circulation on time scales of days. Instead, they are more aVected by the relatively high frequency tidal and wind forces that change on an hourly and daily basis (Queiroga et al., 1997). The horizontal transport of larvae can be enhanced when they traverse horizontal or vertical gradients in currents. These mechanisms are especially relevant over continental shelves, and in estuaries in particular. The well-known example of selective tidal stream transport

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occurs when vertical migratory behaviour interacts with the vertical gradient of tidal currents during ebb and flood flow. Transport is also enhanced when the vertical migratory period is an exact multiple of one of the tidal constituents like S2. The larvae can also influence their net (tidally averaged) movement by moving from side to side in a tidal channel where currents in the shallow water at the edge are slowed by friction, although this mechanism is less well understood. This section discusses these concepts.

3.8.1. Transport for vertical migratory periods that are exact or approximate multiples of tidal constituents The three most important periodic constituents of tides in terms of their contribution to tidal amplitude at a particular location (and, therefore, to the strength of tidal currents) are the M2, S2, and K1 components, which have periods of 12 h 25 min, 12 h 0 min, and 23 h 56 min, respectively (Open University, 1991). Because friction always reduces current velocity near the bottom, an organism migrating vertically in a tidal current may have a very different horizontal speed and trajectory than a non-migratory organism. An obvious interaction of vertical migration behaviour with tidal currents is the selective tidal stream transport of larvae in estuaries (see below), which has long been recognized to aVect retention and export of larvae in these systems (Forward and Tankersley, 2001). In this case, the larvae migrate in synchrony with the main constituent of the tide, the M2 component. Other less recognized cases of interaction of migratory behaviour with tides, which may have equally significant ecological consequences, concern diel migration, which is very common in decapod larvae (Section 4). These cases have been described by Hill in a series of modelling studies (Hill, 1991a,b, 1995, 1998). Their potential for horizontal transport resides in the fact that the period of the diel migration is an exact or approximate multiple of the period of the tidal constituents. One such case is the interaction with the S2 component, which has a period exactly half that of the migration period. Hill (1991a) showed that for a reasonable magnitude of S2, horizontal transport of larvae undergoing diel migration could be as much as 4 km d1. The presence of a strong M2 tidal constituent lowers the horizontal transport velocity. Another case is the interaction with the K1 constituent, which has a period very close, but not equal, to the period of the migration (Hill, 1991b). This interaction has the potential for long-distance transport over extended periods of time and is oVered as an explanation of the observation that penaeid shrimp larvae in the Gulf of Carpentaria, Australia, are transported away from the coast during the March spawning season but toward the shore during the October spawning season (Rothlisberg et al., 1983b; see

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Section 6.2 for a detailed explanation of the mechanism). In the case of strong diurnal tides, the beat period between the tide and the day cycles is 342 days; there is a 171-day period when the larvae are directed in one direction, followed by another 171-day period when the larvae are advected in the opposite direction. As (Hill, 1991a,b) pointed out, it is important to note that vertical migration extends into the bottom boundary layer, where the current is significantly slowed by friction. In many of the cases, decapod larvae do have the capability to move to this layer in shelf and estuarine waters (see Table 4 in Section 5). When vertical migration is confined to regions above the boundary layer, where shear is weaker, the net horizontal movement is substantially reduced. However, thermohaline stratification may also contribute to the modulation of horizontal advection for a vertically migrating larva even if the migration is confined to depths outside the bottom layer (Hill, 1998). This happens because there are diVerences in the phase and amplitude of the tidal current across the thermocline. For instance, for a diel vertical migration on an S2 tidal flow, unidirectional transport can be as high as one diel excursion per tidal cycle, which corresponds to values around 1 km d1. It will be seen later (Section 11) that decapod larvae appear able to cross most natural thermoclines.

3.8.2. Effect of the co-occurrence of flood tide and night Larvae of many species rise in the water column on night-time flood tides during their migration into and up estuaries. For example, studies of the ingress of penaeid shrimp postlarvae (Hughes, 1972; Rothlisberg et al., 1995; Blanton et al., 2001), portunid megalopae (Little and Epifanio, 1991; Olmi, 1994; Queiroga, 1998), and ocypodid megalopae (Little and Epifanio, 1991; DeVries et al., 1994) confirmed that densities of planktonic forms entering an estuary were significantly greater when flood tide occurred during total darkness. Thus, for those larvae using selective tidal stream transport for estuarine ingress, the most eYcient time of ingress into estuaries would be when flood tide coincides with night (Christy and Morgan, 1998). The amplitudes and phases of the M2, S2, and N2 tidal constituents govern the co-occurrence of flood tide and night at any particular site. These constituents combine to produce a diVerence between the ranges of spring and neap tides and the ‘‘age’’ of the tide (i.e., the time lag between the actual occurrence of the spring or neap tide and the occurrence of the specific lunar and solar alignment that causes it). For some locations (e.g., the east coast of the United States), the co-occurrence of darkness and flood currents are optimized at a time near, but not necessarily on, the day of neap tide. For other locations (e.g., the Atlantic coast of Iberian Peninsula), a lack of light

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coinciding with the flood phase is maximized during spring tides in spring and summer, but not during the rest of the year (Figure 3).

3.9. Estuarine transport The net (i.e., tidally averaged) result of the circulation of most estuaries is the transport of fresh water to the sea. Several modes of estuarine net circulation have been recognized that depend on the depth-to-width ratio, volume of fresh water discharged, and tidal range (Pritchard, 1951). As stated above, an actively migrating larva does not depend on the net circulation but, rather, on the instantaneous flow fields to which it is exposed during the course its vertical movements. In the short term, tides establish a periodic oscillation of the flow, which is linked to predictable changes of several variables; namely, current velocity, turbulence, water height, salinity, and temperature, that can be used by larvae to trigger tidally synchronised behaviours, namely: current velocity, turbulence, salinity, water height, and temperature. In estuaries of the temperate zone during the hottest part of the year, because of the higher thermal inertia of the ocean compared with the river and estuarine waters, a decrease in water temperature occurs as seawater enters the estuary during flood, and a corresponding increase occurs during ebb. The reverse, in turn, occurs during the coldest part of the year. Most of these variables also change with depth. Current intensity is always lower close to the seabed because of friction, and salinity is always higher close to the bottom unless turbulence completely mixes the water column. Because of the range of temperature, diVerences found in nature have a smaller eVect on water density than do salinity diVerences. During the hot season, the high-salinity water that flows close to the bottom during flood has a lower temperature than the overlying layer. Conversely, during the cold season, seawater close to the bottom may be warmer than water higher up in the water column.

3.9.1. Selective tidal stream transport Selective tidal stream transport is the main mechanism by which decapod larvae can either be exported seaward or migrate into estuaries (Forward and Tankersley, 2001). Strong vertical shear in the tidal current over the small depth of the estuary, combined with a vertical migration synchronised with the tide, make the trajectory possible. Larvae can have a net landward trajectory if they migrate to the bottom during ebb, followed by a rise to the surface during the flood phase, as crab megalopae do (e.g., Olmi, 1994; Queiroga, 1998), or they can be advected seaward when they migrate to

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Figure 3 Interaction of the tidal cycle with the daily cycle defines the time during the year when flood flow during night is maximized. Note that the total duration of nocturnal flood is, as a rule, greater during neap tides in spring and summer (days 83 to 263), and it is greater during spring tides during the rest of the year. The data to create this figure were obtained from the tide tables for the Portuguese coast that were published by the Instituto Hidrogra´fico, Portugal. The nocturnal period (shaded area) is defined by the daily sunset and sunrise times.

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the surface during ebb, which is the case of the young crab zoeae (e.g., Queiroga et al., 1997; DiBacco et al., 2001). Selective tidal stream transport is also used when the whole larval series is retained in the estuary (Cronin, 1982). As stated above, selective tidal stream transport in estuaries is one of the possible interactions of a vertical migration schedule with the tidal constituents and occurs when larvae migrate in synchrony with the M2 component of the tide.

3.9.2. Lateral migration of larvae Hypothetically, larval transport can be enhanced by a horizontally sheared tidal current. Surface tidal currents are weaker along the shallow edges of the channel but stronger in its deeper parts. In shallow tidal creeks, larvae that migrate to the sides during ebb followed by migration to the middle of the channel during flood will have a net transport landward. A reverse in the phase of lateral migration would be accompanied by net seaward transport. The eVect of lateral shear and secondary circulation on larval transport has not been well documented. Lateral shear in channels with large longitudinal density gradients generates strong lateral density gradients that also aVect circulation patterns in tidal channels. In the case of flood currents, saltier water is confined to the deeper part of the channel, thereby imposing a lateral pressure gradient (Nunes and Simpson, 1985). This force drives a lateral, or secondary, circulation consisting of a surface flow converging toward the center of the channel. At the bottom, the compensating flow diverges away from the center (see figure in Nunes and Simpson, 1985). This transverse circulation could form the basis for the lateral distribution of competent larvae that settle preferably in shallow areas usually located on the sides of estuaries (Figure 4). The most visible manifestation is an axial front that occurs during flood tide. At ebb, the opposite occurs, with saltier water on the sides, and the secondary circulation reverses. Axial fronts, formed over the deeper part of the channel during flood, may provide a favourable environment for larvae (Eggleston et al., 1998). However, little literature exists to confirm the importance of transverse circulation for the transport of larvae.

3.9.3. Tidal current asymmetry Clearly, larvae are at the mercy of the tidal currents when entering estuaries and making their way landward. The astronomic tide generates higher-frequency overtides as they propagate into shallow estuaries and tidal creeks

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Figure 4 EVects of secondary circulation on the advection of larvae into an estuary. Each panel is a cross section of a hypothetical estuary. There must be a suYciently strong axial density (salinity) gradient for the strength of secondary circulation to be significant. Flood current (a) causes secondary circulation, which concentrates larvae along the axis, where landward flow is strongest. Ebb current (b) causes the reverse secondary circulation, which concentrates larvae at the edges of the estuary, where seaward flow is relatively weak. The net result of this process is that the larvae travel landward more than they travel seaward. This mechanism constitutes another example of selected tidal stream transport, but its importance has not been documented.

(Friedrichs and Aubrey, 1988; Parker, 1991; Blanton and Andrade, 2001). The overtides become significant when the ratio of tidal amplitude to mean water depth increases to 1 or greater. The eVect is to generate tidal currents that are distorted, changing from their original signal, which is essentially sinusoidal. Severe distortion, such as that found in shallow tidal creeks, causes maximum flood or ebb to occur close to the time of high water or low water (Dronkers, 1986; Blanton and Andrade, 2001; Blanton et al., 2002), rather

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than midway between high and low water. The relevance of tidal current distortion to larval transport in conjunction with larval behaviour has not been documented.

3.9.4. Wind-generated exchange with the ocean Water-level fluctuations can induce exchanges of large volumes of water between estuary and ocean, thus expediting the transport of larvae. Rising sea level is the most obvious example, but wind-induced fluctuations at frequencies lower than tidal (subtidal) can play the same role (Blanton et al., 1995, 2001). A clear inverse relationship between fluctuations in alongshore wind stress and subtidal water depth is typically found in estuaries. Typical water level fluctuations can be greater than 0.2 m. Thus, a northward/southward wind-stress fluctuation leads directly to a flux seaward/landward through the inlet. The flux strength is related to the cross-sectional area of the inlet throat and the tidal prism. Using the equation of continuity, the flux strength (F ) is dZ F ¼ uAz ¼ Axy dt where u is channel velocity, Az is the cross-sectional area through the inlet, Axy is the horizontal surface area of the estuary’s water surface, and dZ/dt is the rate of change in the water level. Thus, flux through the inlet is proportional to the ratio of the mean horizontal water surface area of the estuary to the mean crosssectional area of the inlet. Both Az and Axy are functions of time, and Axy, particularly in estuaries and tidal channels with large intertidal areas, can vary significantly during a tidal cycle. These systems can induce large fluxes through the above equation because small changes in water level can cause large changes in Axy relative to changes in Az. Sea-level fluctuations that drive the fluxes can be caused by local wind as well as other events occurring at subtidal frequencies. The fluctuations are superimposed on the normal rise and fall of the lunar tides, both of which are accompanied by the transport of ocean water through the inlet to the estuary. Theoretical studies (Klinck et al., 1981) have shown that the Ekman fluxes generated by the alongshore component of wind are mostly responsible for subtidal exchange between ocean and estuary. The exchange is particularly eYcient for inlets that have a deep connection to the ocean. The most easily visualized eVect occurs for wind-generated upwellings, where high volumes of nitrate flow landward in the bottom boundary layer and move directly into an inlet. On the west coast of Spain, for example, the interannual variability in mussel production in the deep rias correlates well with interannual variability of the strength of upwelling (Blanton et al., 1987).

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A good example of decapod larval movement is the ingress of Callinectes sapidus megalopae into Chesapeake Bay. Studies on the influence of winddriven circulation (Goodrich et al., 1989) have shown that maximum megalopae settlements on artificial substrata are associated with positive anomalies of the residual water volume inside the estuary, driven by the wind. The same study also showed that positive volume anomalies are recurrent events in Chesapeake Bay during the recruitment season. Those authors maintain that, although the timing of the wind forces that drive volume exchange in the Bay is unpredictable on timescales of days to weeks, fluctuations in the wind-forcing regime are known to occur in great enough number and strength during the recruitment season to provide a reliable mechanism for supplying megalopae to this and other estuarine systems in the western North Atlantic Ocean. Large-volume exchanges can also be induced as a result of processes occurring at locations remote from the study area. An example is remotely forced continental shelf waves passing through the system (Schwing et al., 1988). Thus, either downwelling-favourable winds or remotely forced shelf waves can induce subtidal increases in inflow that can hypothetically increase the potential for larval ingress.

3.10. Transport regimes along continental margins Large-scale oceanic boundary currents such as the Gulf Stream and the California Current contain flow paths that can potentially transport larvae for several thousands of kilometres. For example, wind-generated flow along the eastern U.S. continental shelf can carry menhaden larvae from their spawning sites oV the middle Atlantic coast to south of Cape Hatteras, a distance of 200–300 km (Hare et al., 1999; Quinlan et al., 1999; Werner et al., 1999). Eddy motions in this and other large-scale boundary currents can set up large circulation patterns that can ‘‘spin oV’’ larval populations laterally, either toward the coast or farther out into the central oceanic gyres. Largescale transport regimes flow along continental margins. These regimes have large-scale currents and counter-currents that can transport larvae over distances of thousands of kilometres. This section covers aspects of the large-scale and eddy-induced motion that can aVect larval transport.

3.10.1. Eastern boundary currents The mean flow in Eastern boundary currents such as the California Current and the boundary current along the Iberian Peninsula is equatorward in summer and poleward in winter—as a result of seasonal changes in

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the wind regime (see, e.g., Hickey, 1989). Moreover, there are subsurface counter-currents that flow poleward along the continental slope. These currents counter the equatorward surface currents that prevail during the spring and summer upwelling season. During winter, this subsurface flow along the continental slope joins the wind-generated flow on the shelf to produce poleward transport over the entire continental margin. For example, the wind regime along the western coast of the Iberian Peninsula is regulated by the seasonal migration of the subtropical front and the Azores high, the center of which moves from 27 8N in winter to 33 8N in the summer (Wooster et al., 1976; Fiu´za et al., 1982; Sousa and Fiu´za, 1989). Therefore, weak westerly winds predominate during winter and stronger northerly winds dominate the summer atmospheric circulation. These winds, the ‘‘Portuguese trade winds,’’ force southward currents in near-surface layers and are favourable to upwelling. Within intermediate layers there is, south of 43 8N, a geostrophic eastward flow, resulting from the meridional pressure gradient with high southern and low northern values oV the Portuguese coast. This onshore flow of the large-scale motion field is diverted to the north when it encounters the slope, running then along the slope and the outer shelf (Frouin et al., 1990; Haynes and Barton, 1990). The southward-directed component of the Portuguese trade winds balances the pressure gradient. Therefore, as the southward wind forcing lessens during the winter, this current rises to the surface. The water column on continental shelves on the eastern flanks of ocean basins typically has a vertical zone of geostrophic currents (the interior flow) bounded by surface and bottom boundary layers. Winds causing upwelling and downwelling transport large volumes across the shelf within both boundary layers. Transport in the boundary layers is driven by the alongshelf component of wind stress. Upwelling-favourable winds, which blow toward the equator in the northern hemisphere, transport large volumes of surface water seaward in the surface boundary layer. This water is replaced by shoreward transport in the bottom boundary layer—water that is usually nutrient-rich and rises to reach the photic zone. The resulting production is distributed in the vicinity of upwelling fronts, and large concentrations of larvae often congregate there (Shanks et al., 2000). The relaxation (or reversal) of upwelling-favourable wind results causes an onshore convergence of the surface layer and a compensating downwelling of water close to the coast. Cross-shelf transport of larvae depends on their vertical position. OVshore transport will result during upwelling if larvae remain in the upper boundary layer, but the transport will be onshore in the bottom layer. The reverse situation occurs during downwelling (Blanton et al., 1995; Olmi, 1995; Queiroga, 1996, 2003). A feature of upwelling circulation is the formation of an upwelling front, separating the colder and denser waters that come to the surface close to the

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shore from the warmer waters oVshore. Because of density diVerences and a lower seawater level close to the shore, the pressure gradient drives an equatorward jet on the oVshore side of the front, both of which lasts for the duration of the upwelling-favourable winds (Mann and Lazier, 1996). This along-shore component of the upwelling circulation has also been reported in the variability of supply of planktonic larvae to littoral populations of invertebrates, including decapod crustaceans (Wing et al., 1995a,b).

3.10.2. Western boundary currents We discuss here the Gulf Stream as an example of a powerful ocean current having potentially large eVects on larval transport. The eVects result from the large-volume transport along its axis, but more important, the fluctuating eddy motion that can advect a large water volume across the continental margin. The Gulf Stream results in the western intensification of the flow generated by the wind-stress field in the North Atlantic Ocean. The first adequate explanation of westward intensification was presented by Stommel (1948), who showed that the variation of Coriolis force with latitude (the beta eVect) was fundamentally responsible for the dynamic of the intensification. The Gulf Stream axis follows the general trend of the continental slope along the southeastern United States. Transport through the Straits of Florida is about 30 Sv (1 Sv ¼ 1 million cubic meters per second), with some evidence of seasonal variation (Niiler and Richardson, 1973; Schott et al., 1988). There is a threefold increase of transport between 29 8N and Cape Hatteras, from 30 Sv to 90 Sv, and its width more than doubles (Leaman et al., 1989). As large as this transport is, the fluctuations in transport around its mean are mainly responsible for the cross-margin flux of material. These fluctuations are a manifestation of the eddies that form (mainly) on the western (cyclonic) side of the current and propagate downstream toward Cape Hatteras (Lee et al., 1991). Eddies occurring at periods ranging from 2 to 14 days are persistent features of the Gulf Stream. They form mainly through density-induced instabilities on the cyclonic side of the Gulf Stream frontal zone and propagate along the outer shelf at speeds of around 0.4 m/s (Bane and Brooks, 1979), causing an exchange of water and momentum and a net flux of nutrients across the outer shelf (Lee et al., 1981). Upwelling induced in the cold core of each eddy causes a high flux of nutrients into the photic zone and triggers high phytoplankton productivity (Yoder et al., 1981). Eddy dimensions increase significantly in two regions along the southeastern U.S. continental shelf (Lee et al., 1991). The first occurs between 27 8 and 29 8N, where the shelf widens and the Blake Plateau begins. The second occurs between 32 8 and 33 8N, just downstream of the Charleston Bump. The significance of these regions is that the mean transport of nitrogen is oVshore, where eddies grow, and onshore, where the eddies lose energy

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downstream of the amplification regions. This is not a ‘‘sum’’ process because the nitrogen transported shoreward is stranded on the continental shelf, as part of the eddy shears apart from the main body of the stream. The Gulf Stream has been postulated to be the primary agent that transports Atlantic bluefish larvae from spawning sites along the southeastern United States to nursery habitats in the northeastern United States (Hare and Cowen, 1996). The Gulf Stream carries the larvae several hundred kilometres northward until spin-oV eddies of warm streamers of water eject the larvae onto the shelf, where they find suitable nursery habitats. However, field data to verify this hypothesis have not been forthcoming (Epifanio and Garvine, 2001).

3.10.3. Coasts with freshwater discharges Many coasts have rivers that discharge large amounts of fresh water, providing a buoyancy force to coastal circulation. Because of the Coriolis eVect, the buoyant plumes tend to be deflected to the right/left in the northern/ southern hemisphere. Winds that also blow in this direction (downwelling favourable) substantially reinforce the strength of coastal transport. Upwelling winds, however, oppose the buoyancy-induced flow, and the plume tends to spread oVshore. The eVects of wind on buoyant plumes have an important eVect on larval transport (Epifanio and Garvine, 2001). The interaction of wind stress, tides, and eVects of stratification (resulting from river discharge and seasonal heating and cooling) with this basic flow regime has a profound eVect on particle transport. These transport processes as they pertain to the continental shelf of the east coast of the United States have been comprehensively reviewed by Epifanio and Garvine (2001).

3.11. Frontal zones as sites of larval congregation 3.11.1. Coastal upwelling frontal zones Upwelling fronts are formed at the convergence separating open ocean water masses from surface coastal waters brought seaward by oVshore advection. The dynamics of this regime are described in Lentz (1992, 1994). The convergent flow pattern concentrates nutrient-rich waters in the photic zone that originate 100 to 200 m below the surface, providing favourable sites for retention of larvae. If the wind relaxes, the pressure field that is part of the balance generated by the wind becomes unbalanced, causing the frontal zone to move onshore in the case of upwelling and oVshore in the case of downwelling. The frontal zone produced during upwelling becomes unstable when winds relax, and larvae congregated there can be swept shoreward as the

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isopycnals associated with the frontal zone become more horizontal. Upwelling-favourable winds seldom persist for more than 1–2 weeks before they relax or blow in the opposite direction. Winds in the opposite direction produce a downwelling of the surface water that flows toward the coast. Downwelling winds that persist set up a favourable regime that can transport surface water shoreward. Upwelling fronts have been explicitly identified as participating in the transport of barnacle larvae toward the California coast (Roughgarden et al., 1991). In this case, the intensity of settlement of the larvae in intertidal habitats increased sharply after the collision of the front with the coast, following the relaxation of upwelling-favourable winds. In summary, the upwelling commonly found along eastern boundary current systems produces a favourable regime for the production of larvae. Fisheries oceanographers are establishing robust relationships between the wind regime and upwelling that should prove useful to managers of fisheries (Bakun, 1973; Wooster et al., 1976; Blanton et al., 1987).

3.11.2. Frontal zones on wide and shallow continental shelves Frontal zones are generated on wide and shallow continental shelves, where tidal mixing energy is just balanced by the buoyancy supply from surface heating (Simpson and Hunter, 1974) or freshwater discharge (Blanton, 1996). These fronts occur along an isobath, where tidal mixing is just suYcient to destroy vertical stratification caused by the supply of buoyancy. Assuming a one-dimensional process, Simpson and Hunter (1974) found that tidal mixing should balance the buoyancy supplied by solar heating at a location on the shelf where H/U3 is constant. Here H is water depth and U is the magnitude of the tidal current. To the extent that the buoyancy supply is seasonal (surface warming or increased freshwater discharge in spring), these frontal zones are also seasonal. The vertical and horizontal density regimes of coastal frontal zones are highly variable. Wind fluctuations can alter the strength of vertical and horizontal stratification within 6 h of a wind shift (Blanton et al., 1989; Blanton, 1996). The rather dramatic and swift changes in the strength of horizontal and vertical density gradients are a result of the asymmetrical eVect of vertical mixing during upwelling and downwelling regimes (see earlier).

3.11.3. River plumes River plumes are relatively small scale frontal zones that provide favourable sites for larvae. Strong inflow at the leading edge of plumes is a common feature of river plumes (O’Donnell et al., 1998). When these plumes are

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coupled with vertical movement of larvae, large concentrations of larvae can congregate along these convergences (Clancy and Epifanio, 1989). Larvae can also be retained in eddy-like features associated with the outflow of the plume onto the continental shelf (Pearcy, 1992; Yanovsky et al., 2001).

3.11.4. Eddies Topographic features such as capes and bottom irregularities can establish cyclonic eddy motions. Eddies formed by capes that protrude into coastal currents form cyclonic circulation zones that intensify the strength of upwelling (Arthur, 1960; Blanton et al., 1981). Examples of such features are found along the Gulf Stream oV Charleston, South Carolina (Singer et al., 1983; Sedberry and Loefer, 2001), the western coast of the Iberian Peninsula (Fiu´za et al., 1998; Peliz and Fiu´za, 1999; Stevens et al., 2000), and Point Conception, California (Jones et al., 1988; Dugdale and Wilkerson, 1989). The upwelling that occurs close to the eddy’s center often carries water into the photic zone, which enhances production and can provide a favourable environment for larvae. Wing et al. (1995a,b) have related the presence of a persistent eddy south of Point Reyes, California, to the recruitment of coastal invertebrates, including crabs. A cyclonic eddy develops on the leeward side of Point Reyes, generated by upwelling-favourable winds during spring and early summer. The cyclonic circulation of the eddy concentrates the larvae of several invertebrate species. South of Point Reyes, settlement is more intense and occurs during downwelling and, to a certain extent, during upwelling as well. North of Point Reyes, settlement is episodic and appears to be limited to relaxation periods of the upwelling-favourable winds. Wing et al. (1995a,b) propose that, during the relaxation periods, the water trapped in the eddy is released and advected northward and onshore, transporting the larvae with it.

4. CYCLIC VERTICAL MIGRATION IN THE NATURAL ENVIRONMENT Because of their prevalence, ubiquity, and predictability, environmental cyclic factors may constitute important selective pressures that shape the evolution of animal behaviour (Enright, 1975b; DeCoursey, 1983; Palmer, 1995; Drickamer et al., 2002). Many marine physical and biological processes, such as tides, wind-driven circulation, and food production, have a periodic nature that is expressed several time scales. The two most

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important periodic factors that may have caused the evolution of behavioural traits involved in the dispersal control of larvae of shallow water species are the tidal and the diel cycles. This section addresses the methods used for the study of cyclic vertical migration, the types of vertical migration that have been identified, and the prevalence of migration across taxa and ecological category.

4.1. Sampling methodology Studies designed to describe the patterns of variation of vertical position in the water column have used various combinations of collecting gear and sampling strategy (Table 2). Pumps are normally used in estuaries and other shallow water bodies, whereas nets have been used in all kinds of environments. Sampling programmes have taken from two depth levels, including the neuston, to several depth levels to increase vertical resolution (e.g., Brookins and Epifanio, 1985; Forbes and Benfield, 1986; Hobbs and Botsford, 1992; Palmer, 1995; Queiroga et al., 1997; Abello´ and Guerao, 1999). Both pumps and nets can be used to sample at several depth levels. Although pumps can only sample from discrete depths, plankton nets can also integrate samples through the entire vertical range of selected depth strata when towed obliquely. Some types of nets, such as the Longhurst-Hardy Plankton Recorder, the MOCNESS net, or the Messhai net, sample continuously along the water column and have been used to resolve the water column into multiple strata. These nets have the potential to provide accurate and quasi-instantaneous estimates of larval density throughout the water column with one single haul. Unfortunately, because of technical and economic constraints, they have rarely been used to address the vertical distribution of decapod larvae (but see Lindley, 1986, and Shanks, 1986, for exceptions). One further limitation of these nets is the relatively small volume of water Table 2 Sampling methods used in field studies to address cyclic vertical migration of decapod larvae; studies used diVerent combinations of the techniques listed Sampling gear

Vertical resolution

Vertical integration

Horizontal/ temporal resolution

Pump

Neuston and single water-column level Neuston and multiple water-column levels Multiple water-column levels

Discrete

Fixed station, time variation Drift station, time variation Grid of stations, space and time variation

Net Multiple net

Continuous

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that they sample, which may constitute a considerable handicap when sampling for rare larval stages. The sampling programmes addressing horizontal resolution can be grouped into three major types: use of one fixed station, use of one drift station, and use of a grid of stations. Fixed-station studies aim at describing the time pattern of change of vertical position and have been the most commonly used strategy to describe cyclic migrations, especially in estuaries and bays (e.g., Cronin, 1982; Provenzano et al., 1983; Booth et al., 1985; Shanks, 1986; DeVries et al., 1994; Olmi, 1994; Queiroga et al., 1997; Queiroga, 1998). When a fixed station is used, sampling is usually made at regular intervals over one or several cycles of the environmental variable of interest. Several physical and chemical parameters, related to the environmental cycle, can be measured simultaneously, so as to allow the test of specific hypotheses concerning the factors that entrain and synchronise the rhythm. Fixed-station studies are easy to conduct, but a limitation is that diVerent water masses and larval aggregates are sampled through time, which may hinder the test of a particular hypothesis. To overcome this problem, drift stations may be used, where the ship follows a marked water mass (Jamieson et al., 1989). A grid of stations is normally not an option when the primary aim of the study is the investigation of cyclic migration. However, one can take advantage of the fact that sampling extends over the diVerent phases of the environmental cycle to make inferences on changes of vertical position according to phase of day (Hobbs et al., 1992) or phase of tide (see Bousfield, 1955, for an example with barnacle larvae).

4.2. Prevalence of cyclic vertical migration according to taxonomic and ecological category Table 3 lists the types of cyclic vertical migration that have been identified in larval stages of decapod crustaceans, according to taxa and ecological category. Cyclic vertical migration appears to be a universal adaptation in larvae of coastal decapod crustaceans. Virtually all larval stages of all species investigated show some kind of rhythmic migratory behaviour. All ecological categories include species belonging to several diVerent taxonomic groups, with two exceptions: obligate estuarine species and shelf species that use estuaries as nurseries. In the first case, only one brachyuran species is included, which prevents any generalization. The second exception includes only penaeid species of the Dendrobranchiata. This division includes all shelf decapod species that use estuaries as nursery grounds for their juveniles. Brachyura is the most studied group because it is the most diverse group of decapods and also because most of their species occur in shallow water, where the majority of sampling programmes have been conducted.

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Table 3 Types of vertical migration identified from field studies and classified by ecological category Types of vertical migration Infraorder or division

Species

Obligate estuarine species Brachyura Rhithropanopeus harrisii

First stage

Middle stages

Flood, nocturnal

Flood, Flood nocturnal

Estuarine species that export their larvae to the shelf Brachyura Callinectes sapidus Ebb, nocturnal, no rhythm (1/3) Carcinus aestuarii

Brachyura

Carcinus maenas

Ebb, nocturnal

Brachyura Brachyura

Ovalipes ocellatus Pinnixa spp.

Nocturnal

Brachyura

Uca spp.

Ebb

Nocturnal

Shelf species that may penetrate estuaries as adults Caridea Palaemon adspersus Ebb, nocturnal Caridea Palaemon elegans Ebb Thalassinidea Callianassa subterranea Nocturnal Nocturnal

References

Cronin and Forward, 1982, 1986

Flood, Williams, 1971; Smyth, 1980; nocturnal Provenzano et al., 1983; Epifanio et al., 1984; Brookins and Epifanio, 1985, 1988; Mense and Wenner, 1989; DeVries et al., 1994; Olmi, 1994 No rhythm Abello´ and Guerao, 1999 (1/1) Flood Queiroga et al., 1997; Queiroga, 1998 Epifanio, 1988 Flood, DeVries et al., 1994 nocturnal DeCoursey, 1976; Brookins Flood, and Epifanio, 1985; DeVries et al., nocturnal 1994; Garrison, 1999 Pereira et al., 2000 Pereira et al., 2000 Lindley, 1986

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Brachyura

No rhythm (1/3)

Last stage

Lophopanopeus spp. Pachygrapsus crassipes Pachygrapsus marmoratus Pirimela denticulata Portumnus latipes

No rhythm Ebb, nocturnal Ebb Ebb

Shelf species that use estuaries as nursery habitats Dendrobranchiata Penaeus indicus Dendrobranchiata Penaeus japonicus Dendrobranchiata Penaeus plebejus Dendrobranchiata Penaeus vannamei Dendrobranchiata Penaeus spp.

Nocturnal

Nocturnal

Shelf species Caridea Caridea Astacidea Palinura

Pandalus montagui Processa canaliculata Homarus americanus Panulirus cygnus

Reverse Nocturnal Nocturnal Nocturnal

Reverse Nocturnal Nocturnal Nocturnal

Palinura Anomura Anomura Anomura Anomura Brachyura

Scyllarus bicuspidatus Pagurus bernhardus Pagurus prideauxii Pisidia longicornis Porcellana platycheles Cancer magister

Nocturnal Reverse Nocturnal

Nocturnal Reverse Nocturnal

Brachyura

Cancer oregonensis

Nocturnal

Nocturnal

DiBacco et al., 2001 DiBacco et al., 2001 Pereira et al., 2000 Pereira et al., 2000 Abello´ and Guerao, 1999

Flood Flood nocturnal Flood nocturnal Flood Nocturnal

Forbes and Benfield, 1986 Forbes and Benefield, 1986; Kuwahara et al., 1987 Young and Carpenter, 1977; Rothlisberg et al., 1995 Mair et al., 1982 Rothlisberg, 1982

Nocturnal No rhythm

Nocturnal Nocturnal Twilight

Twilight

Lindley et al., 1994 Lindley, 1986 Harding et al., 1987 Phillips et al., 1978; Rimmer and Phillips, 1979 Phillips et al., 1981 Lindley et al., 1994 Lindley, 1986 Abello´ and Guerao, 1999 Abello´ and Guerao, 1999 Booth et al., 1985; Jamieson and Phillips, 1988; Jamieson et al., 1989; Hobbs and Botsford, 1992 Jamieson and Phillips, 1988

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(Continued)

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Brachyura Brachyura Brachyura Brachyura Brachyura

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Table 3 (Continued) Types of vertical migration Species

First stage

Middle stages

Brachyura Brachyura Brachyura Brachyura

Cancer spp. Corystes cassivelaunus Ebalia sp. 3 Macropodia sp.

Nocturnal Nocturnal

Nocturnal Nocturnal

Brachyura

Randallia ornata

Nocturnal

Nocturnal

Nocturnal Nocturnal Nocturnal Nocturnal

Nocturnal Nocturnal Nocturnal Nocturnal

Shelf and slope species Caridea Pontophilus bispinosus Astacidea Nephrops norvegicus Anomura Munida rugosa Brachyura Atelecyclus rotundatus Brachyura Goneplax rhomboides Brachyura Inachus sp. Brachyura Liocarcinus depurator Brachyura Maja crispata Brachyura Atelecyclus sp. Brachyura Liocarcinus spp.

Nocturnal

Nocturnal

Last stage Nocturnal Nocturnal No rhythm (1/1) Nocturnal

Nocturnal Nocturnal Nocturnal Nocturnal Nocturnal Nocturnal Nocturnal

References Shanks, 1986 Lindley et al., 1994 Abello´ and Guerao, 1999 Abello´ and Guerao, 1999 Shanks, 1986 Lindley, 1986 Lindley et al., 1994 Lindley et al., 1994 Lindley, 1986 Abello´ and Guerao, Abello´ and Guerao, Abello´ and Guerao, Abello´ and Guerao, Abello´ and Guerao, Lindley, 1986

1999 1999 1999 1999 1999

See Table 2 for definition of ecological category. Empty cells indicate that data are not available. Numbers in brackets indicate number of studies when no rhythm was detected, over total number of studies. Studies included in the table used diVerent combinations of sampling techniques, and some did not test for statistical significance, but all studies sampled at least two depth levels across all phases of the relevant natural cycle.

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Infraorder or division

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Without exception, larval stages of species that occur in estuaries during at least part of their life cycle (obligate estuarine species, estuarine species that export their larvae to shelf waters, shelf species that may penetrate estuaries as adults, and shelf species that use estuaries as nursery habitats) perform some type of tidal migration (Table 3). In obligate estuarine species, all stages perform flood migration. An ontogenetic shift from ebb migration in the first stage to flood migration in the last occurs in estuarine species that export larvae to the coast. The same occurs in coastal species that penetrate estuaries as adults. In shelf species that use estuaries as nursery habitats, the last stage shows flood migration. These patterns of migration are related to the need to use estuarine tidal currents to remain within, enhance export from, or reinvade estuaries by the diVerent larval stages (see below). Tidal migrations were never detected in shelf or shelf and slope species. It is possible that tidal migrations do not serve any useful ecological role in such species, but this aspect has never been investigated. In support of this contention, Queiroga et al. (2002) did not find evidence for tidal migrations in larvae of Carcinus maenas (an estuarine crab species that exports larvae to the shelf) from the Skagerrak, Sweden, where the tidal range is very small and variations of sea level caused by winds or changes of atmospheric pressure are of larger amplitude than those caused by the tide. Diel rhythms were detected in all ecological categories (Table 3), with the most common type being nocturnal migration. Reverse and twilight migration patterns were detected only in shelf species (reverse: Pandalus montagui and Pagurus bernhardus; twilight: Cancer magister and Cancer oregonensis).

5. ONTOGENETIC MIGRATION AND THE EXTENT OF VERTICAL MOVEMENTS Ontogenetic migration occurs when larvae change their average depth of distribution during the larval period. This is an obligatory process in the case of benthic crustaceans because the larvae hatch from eggs carried by bottom-dwelling females, feed in surface waters, and must return to the adult benthic habitat. Moreover, gradual changes in depth distribution may occur during the competent stage. This chapter will examine the available records of ontogenetic migration during the larval phase, as well as the vertical range of distribution of the larval stages. Ontogenetic migrations have been described in larvae that develop in estuarine, shelf, and oceanic waters and across all ecological categories considered in this review. Table 4 reports the depth of occurrence of maximum abundance values according to development stage, except for studies 1 and 12, in which average depth of distribution is reported. The data in

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Table 4 Extent of vertical distribution according to larval stage determined from field studies Infraorder or division

Species

Obligate estuarine species Brachyura Rhithropanopeus harrisii

Middle stages

Last stage

Station depth (m)

References

1.8

1.9–2.1

2.0

4

Cronin, 1982 (1)

25 Neuston 0–60 0–15 20

20–35 25 10–20 20–200 20–35 10–20

Epifanio, 1988 (2) Epifanio et al., 1984 (3) Johnson, 1985 (4) Queiroga, 1996 (5) Epifanio, 1988 (2) Johnson, 1985 (4)

27

>150 >80

Lindley, 1986 (6) Lindley et al., 1994 (12)

Estuarine species that export their larvae to shelf waters Brachyura Callinectes sapidus 0–10 Brachyura Callinectes sapidus 0–2 Brachyura Callinectes sapidus Brachyura Carcinus maenas 0–30 Brachyura Ovalipes ocellatus 20–35 Brachyura Uca spp.

0–10 0–30 0–15

Shelf species that may penetrate estuaries as adults Thalassinidea Callianassa subterranea Brachyura Liocarcinus spp.

0–25 42

25–50

Shelf species that use estuaries as nursery habitats Dendrobranchiata Penaeus spp.

0–20

0–20

0–20

20–30

Rothlisberg, 1982

Shelf species Caridea Caridea

11

15–29 11–13

14

>80 >80

Lindley et al., 1994 (12) Lindley et al., 1994 (12)

Crangon allmani Pandalus montagui

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First stage

0–50 0–50 0–20

0–60 0–50

0–120 0–50

>150 >150 60 50–500 200–>1000 75–250

Pagurus bernhardus Pagurus prideauxii Cancer spp.

12 0–50 10

14–15 0–100 10

>80 >150 70

Lindley, 1986 (6) Lindley, 1986 (6) Harding et al., 1987 (7) Palmer, 1995 (8) Forward, 1976 (9) Yeung and McGowan, 1991 (10) Lindley et al., 1994 (12) Lindley, 1986 (6) Shanks, 1986 (11)

Nephrops norvegicus Munida rugosa Atelecyclus rotundatus Hyas coarctatus

22 29

15 15 0–50 23

>80 >80 >150 >80

Lindley et al., 1994 (12) Lindley et al., 1994 (12) Lindley, 1986 (6) Lindley et al., 1994 (12)

Pontophilus bispinosus Processa canaliculata Homarus americanus Panulirus cygnus Panulirus cygnus Panulirus spp.

Anomura Anomura Brachyura Shelf and slope species Astacidea Anomura Brachyura Brachyura

30

0–100 Neuston 6–25

25

50–100

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0–25 0–10

Caridea Caridea Astacidea Palinura Palinura Palinura

See Table 2 for definition of ecological category. Values in table represent depth (m) of peak densities of larval stages, except in studies 1 and 12 where average values are reported. Empty cells indicate that data are not available. (1) One fixed station sampled during 2–4 days in four diVerent periods; four discrete depth strata. (2) Three stations sampled during the day in five diVerent periods; three to four discrete depth strata including neuston. (3) One fixed station sampled during one tidal cycle during the day; three discrete depth strata including neuston. (4) Twenty-one stations sampled during the day in seven diVerent periods; four discrete depth strata including neuston. (5) Seventy-eight stations sampled once over 9 days; one to five continuous depth strata. (6) Five stations sampled once in 1 day; twenty continuous depth strata. (7) One fixed station sampled during 15 consecutive days; nine discrete depth strata. (8) Twenty-four stations sampled during the night over 20 days; four to five discrete depth strata including neuston. (9) Five fixed stations sampled during 24–36 h in each of five diVerent dates; five discrete depth strata including neuston. (10) Two hundred seventy-six stations sampled once over 10 days; eight continuous depth strata. (11) One station sampled once before sunrise; five discrete depth strata including neuston. (12) Ten stations sampled once around midday and midnight; 16 continuous depth strata.

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Table 4 confirm that ontogenetic shifts in vertical position are a rule in decapod species. Usually, the first stage is closer to the surface, and intermediate stages occur over a more extended vertical range (e.g., Rhithropanopeus harrisii, Callinectes sapidus, Callianassa subterraneana, Processa canaliculata, Homarus americanus, Panulirus cygnus, and Pagurus prideauxii). Examples concern diVerent taxonomic groups and all ecological categories, except shelf and slope species, for which the available data do not support this generalization. The last stage sometimes occurs in the neuston or close to the surface (Callinectus sapidus, Homarus americanus, Panolirus cygnus), and other times in deeper waters or close to the bottom (Callinectes sapidus, Processa canaliculata, Atelecyclus rotundatus). This variability in the depth distribution of the last stage across taxonomic group and ecological category is not surprising, because it is a transitional stage that must disperse in the plankton but that must also move to the bottom to settle. As a general rule, when the studies were conducted in estuaries or in shallow shelf stations adjacent to estuarine inlets, the vertical range of the migration covered a considerable proportion of the water column, even in species such as in Rhithropanopeus harrisii, Callinectes sapidus, and Ovalipes ocellatus that spend the entire zoeal period in the plankton. When sampling was conducted in deeper stations, migration was confined to the upper strata. Examples include most of the studies in which station depth exceeded 70 m. The data in Table 4 clearly indicate that decapod larvae rarely exceed a depth of 100 m. Table 4 is obviously biased because it includes few data on the last stage of shelf and shelf and slope species, which must obviously migrate to the deep waters where adults live. Nonetheless, the available data highlight the point that entirely planktonic forms remain in a surface layer that is subjected to strong advection driven by wind and density diVerences. Moreover, in much of the shelf and in deeper waters, the larvae do not appear to reach close to the bottom, although pratical diYculties in sampling the bottom layer may constitute another sort of bias in Table 4. The last stages of brachyuran crabs present diVerences concerning their vertical position in the water column, as well as those of palinurids and astacids. The pre-settlement stages of brachyuran crabs (megalopa stage) of palinurid lobsters (puerulus stage) and of astacid lobsters (stage IV larvae) often demonstrate different migration patterns than the earlier larval stages. Available reports indicate that megalopae of some crab species undergo vertical migration movements that take them to the neuston layer while dispersing at night in shelf waters (Smyth, 1980; Cancer magister, Shanks, 1986; Jamieson and Phillips, 1988; McConauhga, 1988; Callinectes sapidus, Hobbs and Botsford, 1992), during the dispersal phase in shelf waters. All these reports were based on plankton sampling programmes that included the use of traditional plankton nets plus neuston nets. Other crab megalopae

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seem to move to deeper waters, culminating in a gradual descent during the larval development phase (Atelecyclus rotundatus, Lindley, 1986; Carcinus maenas, Queiroga, 1996). These two last studies were conducted with multiple plankton nets that, in theory, would allow a better representation of changes of concentration accross the water column than traditional nets. However, these two studies did not use neuston nets, so they could have underestimated the abundance of the larvae at the surface. Other megalopae are reported to be entirely neustonic (Pachygrapsus crassipes, Shanks, 1985), based on direct observations of swimming, by SCUBA divers during the day, although evidence of this behaviour from observations made along daily cycles is not available. Therefore, the available evidence will only allow the conclusion that crab megalopae may show diVerent behaviours in shelf waters, depending on the species concerned. Palinurid pueruli and astacid stage IV larvae, however, are powerful swimmers that appear to migrate to the neuston layer immediately after molting. It is reported that these larvae actively swim over large distances across the shelf into shallow habitats, and that this behaviour is an important component of their dispersal strategy (Homarus americanus, Ennis, 1975b; Panulirus cygnus, Phillips and Olsen, 1975; Panulirus interuptus, Serfling and Ford, 1975; Panulirus argus, Calinski and Lyons, 1983; Cobb et al., 1989; Katz et al., 1994). These larvae are not reported to undergo daily migrations, remaining in the neuston layer during the swimming phase (Harding et al., 1987). A final consideration is that there may be a change in the behaviour of crab megalopae (and of other last-stage larvae) within the moult cycle of this stage, which can be assessed from a sequence of morphological modifications of the integument and setae of selected appendages (Hatfield, 1983; Metcalf and Lipcius, 1992; Hasek and Rabalais, 2001). Jamieson and Phillips (1988) found that Cancer magister and C. oregonensis megalopae found in inshore waters were in a more advanced stage of development than megalopae collected further oVshore, indicating that some transport during the megalopal phase brought the megalopae closer to the coast. During a field study that encompassed a large area from the coast of Washington state to northern California during 5 diVerent years (Hobbs and Botsford, 1992), sampling in one of the years was conducted several weeks earlier in the larval season than in the remaining years. A diVerence was found in the proportion of megalopae in the neuston layer during the night, with fewer megalopae moving to surface waters when the sampling was conducted early in the season. This diVerence was attributed to a less developed migration behaviour exhibited by young megalopae. In the estuarine portunid Callinectes sapidus, moult stage progressed from less to more developed in larvae collected from the plankton, on artificial settlement habitats, and from the benthos, indicating the approach to settlement, metamorphosis, and a benthic existence (Lipcius et al., 1990; Morgan et al., 1996). In a study

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concerning another estuarine portunid, Carcinus maenas (Zeng et al., 1997), it was found that megalopae collected from oVshore waters took more time to metamorphose to the first juvenile stage than megalopae collected at the water’s edge, when maintained in similar laboratory conditions. Collectively, these studies show that megalopae are in a more advanced stage of development within the moult cycle as they approach the settlement habitat and establish a connection between dispersal processes and the physiological state of brachyuran megalopae.

6. SIGNIFICANCE OF VERTICAL MIGRATION IN DISPERSAL: EVIDENCE FROM FIELD STUDIES During the dispersive phase in the plankton, decapod larvae are exposed to various environmental factors and forcing mechanisms. This is especially true of larvae that move between diVerent habitats during their ontogenetic development. It is also true for larvae of species that have extended geographical ranges and therefore encounter diVerent combinations and magnitudes of the physical processes involved in dispersal. Thus, to locate successfully the appropriate habitats for settlement, larvae must possess a repertoire of behavioural responses to environmental factors. These responses are expressed diVerentially in different larval instars that encounter particular combinations of environmental factors. In the case of littoral fish and invertebrate species that develop in shelf waters and that must subsequently return to the systems where adult populations occur, the return migration often involves two separate steps that are constrained by diVerent environmental factors: transport of the larvae from the shelf toward the coast and passage through inlets and upstream movement until an appropriate environment is found (Boehlert and Mundy, 1988; Shanks, 1995). Because the environmental processes that dominate neritic waters, and inshore waters diVer, diVerent larval behavioural traits are required in each phase. Shanks (1995) identified the following physical processes that transport larvae across the shelf: wind-generated superficial currents, including sea breezes and Langmuir circulation; wind-drift currents and Ekman transport; onshore convergence following relaxation of upwelling-favourable winds; residual tidal currents; internal waves; and density-driven flow. For these processes to function, it is necessary that larvae occupy particular positions in the water column while they remain in shelf waters. Closer inshore, especially in bays and estuaries, circulation tends to be dominated by tides, and a shift to a tidally synchronised behaviour is necessary to make use of the tidal currents. This section will examine the interactions of the several types of vertical migration and the physics of the systems in a few selected cases, to illustrate

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the ecological significance of the various forms of vertical movements for the dispersal and recruitment mechanisms. The specific behavioural adaptations involved in the control of the vertical movements will be addressed in Section 8.

6.1. Tidal migrations Tidal vertical migrations have been identified in all species that spend some portion of their life cycle in estuarine systems (Table 3). Most species that live in estuaries as adults are known to export their larvae to the sea. Some, however, retain their larvae within the parental habitat. The export strategy was initially interpreted as an adaptation to promote gene flow and colonization of new habitats (Scheltema, 1975). This opinion has been challenged by the argument that it is the severity of physical and biological conditions in estuaries that favoured the evolution of behavioural traits resulting in an export to the sea (Anger, 2001), which include hatching rhythms synchronised with the tidal and diel cycles, as well as tidal-synchronised vertical migrations. The high osmotic and thermal stresses and intense pelagic predation characteristic of the estuarine environment demand special adaptations; by spending most of their larval development in the sea, larvae would avoid such constraints (Strathmann, 1982, 1993; Morgan, 1987, 1995; Hovel and Morgan, 1997; Anger et al., 1998). The evolution of tidal migration resulting in retention, export, or reinvasion is shaped by the constraints imposed by the estuarine circulation; as the larvae are planktonic forms with limited swimming capacity (Mileikovsky, 1973; Chia et al., 1984; Young, 1995), vertical migration in synchrony with the tidal cycle is the only way available to cope with the deterministic nature of tidal currents in these systems. Tidal currents in estuaries are always slower near the bottom because of friction. During migration, the larvae are exposed to tidal currents of diVering intensity. By moving upward during a certain phase of the tide and deeper during the opposite phase, the larvae experience a net transport in a particular direction. This type of behaviour is called selective tidal stream transport (STST, reviewed by Forward and Tankersley, 2001), a term that was coined by Harden Jones et al. (1984) to describe vertical migration behaviour of adult plaice during directional migration in a background of tidal currents. As originally defined, STST implied a restingon-the-bottom period during the phase of the tide when the direction of the current opposes the direction of horizontal migration. This behaviour is identical to that displayed by crab megalopae and shrimp larvae and postlarvae during estuarine upstream migration (Penn, 1975; shrimp: Brookins and Epifanio, 1985; Forbes and Benfield, 1986; Calderon Perez and Poli, 1987; crab: Christy and Morgan, 1998; Olmi, 1994; Queiroga, 1998). Decapod

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zoeae are mostly entirely planktonic forms that do not gather on the bottom (but see Schembri, 1982 and DiBacco et al., 2001). Accordingly, vertical migration of zoeal larvae, either associated with downstream transport in estuarine decapods that export their larvae to the sea (Queiroga et al., 1997) or with retention inside the estuary (Cronin and Forward, 1979), does not involve settlement to the bottom (Forward and Tankersley, 2001). However, these larvae also use the diVerential intensity of tidal currents along the vertical shear gradient, and this mechanism can be considered a generalization of the STST hypothesis (Queiroga et al., 1997; Forward and Tankersley, 2001). Rhithropanopeus harrisii is a xanthid that completes its entire life cycle inside estuaries (Figure 5). In a field study that used pumps to sample along the water column of Newport River estuary (North Carolina) at a fixed station over several 2–5 day periods, it was observed that all four zoeal stages and the megalopa stage were found inside the estuary, with decreasing abundances (abundance of the megalopae was lower than that of the first zoeae by a factor of 30). All of the species’ zoeae migrated around the level of no net motion in synchrony with the tidal cycle, experiencing no net transport, although the timing of vertical migration varied among study periods. Usually, zoeae rose to a minimum depth soon after low tide, descended just before high tide, and remained deep during the duration of ebb tide (Cronin, 1982; Cronin and Forward, 1982). Therefore, all zoeae exhibited the flood type of vertical migration. Cross-spectral analysis showed that the mean depth of distribution of the zoeae was associated most often with the current cycle, although associations with the salinity and diel cycle were also observed. Data for the megalopa stage were less conclusive, but a significant association between position in the water column and the salinity cycle was also detected (Cronin, 1982). The estuarine phase of the mechanisms of export and reinvasion has been studied most thoroughly in portunid crabs Carcinus maenas and Callinectes sapidus. Both are typical examples of portunid brachyurans that form large populations in estuaries and export their larvae to the shelf, where most of the development takes place (Figure 6). Queiroga et al. (1994, 1997) and Queiroga (1998) have studied the vertical distribution of the first zoeae and megalopa of Carcinus maenas in the Ria de Aveiro, northwest Portugal. Their study used a very intensive sampling programme at fixed stations that included 23 sampling periods of 25 h each, spread over 2 lunar months. Pumps were used to resolve the distribution along the vertical dimension of the estuary. Overall, the megalopa was about 100 times less abundant than the first zoeae, and density of intermediate zoeal stages inside the estuary was lower than that of the megalopa, indicating that virtually all first zoeae were exported from the estuary (Queiroga et al., 1994). First zoeae were significantly more abundant during night ebb tides, resulting from synchronous

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Figure 5 Retention of the complete larval phase inside estuaries through tidally synchronised vertical migration. Inset graph represents a change in the vertical position of larval stages during the tidal and daily cycles (only one of all possible combinations of phase relationship between the two cycles is represented). The highest position along the water column is reached during flood. The xanthid Rhithropanopeus harrisii is representative of this type of behaviour. HWS ¼ highwater slack; LWS ¼ low-water slack.

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Figure 6 Export of the first zoea from estuaries (a) followed by reinvasion by the megalopa (b). Inset graphs represent change in vertical position of larval stages during the tidal and daily cycles (only one of all possible combinations of phase relationship between the two cycles is represented). The highest position along the water column is reached during ebb in the export phase (a) and during flood in the reinvasion phase (b). The portunid Carcinus maenas is a representative of this type of behaviour. HWS ¼ high-water slack; LWS ¼ low-water slack.

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release of larvae by the females. Megalopae were more common during night floods. Pooled data from all sampling occasions represented along normalized tidal cycles showed that the species’ first zoea was significantly closer to the surface during ebb than during flood (Queiroga et al., 1997), exhibiting ebb migration. The vertical migrations had virtually identical pattern in winter and spring, with average vertical position of the zoeae spanning 0.6 of the height of the water column in the course of the vertical displacements. Conversely, the vertical position of the megalopa during flood was significantly higher than during ebb (Queiroga, 1998), indicating flood migration, but there was no indicating that the megalopae aggregated preferably in the neuston layer. The occurrence and vertical distribution of Callinectes sapidus first-stage larvae in the Chesapeake Bay, eastern United States, was described by Provenzano et al. (1983). Their study used horizontally towed plankton nets at several depth levels along four periods of 30 h each. Peak abundance occurred consistently following the night-time slack after ebb, mostly at night, presumably also a result of synchronous larval release. Over 60% of the first zoeae was concentrated in the neuston layer during night-time ebb tides. Vertical distribution of megalopae was analysed by Olmi (1994) in the Chesapeake Bay, using vertical arrays of passive nets deployed from a pier at a shallow station and horizontal plankton tows at a deeper station. Several tide cycles were covered in three diVerent years. Similar to the findings for Carcinus maenas, megalopae of Callinectes sapidus were more abundant during flood than during ebb, indicating a net upstream flux. Highest densities occurred during night floods, when the megalopae aggregated close to the surface. Abundance and depth distribution were not aVected by current speed, wind speed, water temperature, or salinity. The eVect of tides on the synchronization of behaviour of decapod larvae entering the estuary may also operate on shelf waters adjacent to the estuarine inlets, because all eVects of the environmental factors associated with the rising tide described above also operate in these locations. A mechanism for the concentration of Penaeus plebejus larvae outside inlets has been proposed by Rothlisberg et al. (1995). Postlarvae of this species in oVshore waters show a diel migration pattern, resting on the bottom during the day. As they eventually become entrained by coastal currents to shallower waters, they change from a diel migratory pattern to a tidal one, when they are more active in the water column during flood. The authors suggest that the mechanism that initiates movement of the postlarvae into the estuary is a response to pressure changes. When pressure change at the bottom during the tidal cycle becomes a significant fraction of the total pressure, postlarvae would change from a diurnal vertical migration pattern to a tidal pattern. Behavioural traits underlying this mechanism were never tested, but this mechanism could be an eVective way of concentrating competent larvae close to estuaries and of initiating upstream transport in this and other groups of decapods.

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Downstream flux of first zoeae of crab species showing adaptations for seaward transport occur with a regular periodicity, regulated by hatching rhythms that are synchronised to occur during night-time ebb tides (Forward, 1987). Because the beat period between the tidal and diel cycles has the same duration as the semilunar cycle, these export events tend to recur at fortnightly intervals (see Section 3; Christy and Stancyk, 1982; Dittel and Epifanio, 1990; reviewed by Pereira et al., 2000). Although tides also oVer a predictable and reliable mechanism for upstream transport inside estuaries, and their phase relationship with the day/night cycle also cycles with a semilunar period (Christy and Morgan, 1998; Pereira et al., 2000), abundance of brachyuran megalopae and settlement events inside individual estuaries tend to be highly episodic during each species’ reproductive season. Data collected with the use of artificial settlement substrata (Metcalf et al., 1995) over extended periods usually show settlement events that last a few days, separated by longer periods when the abundance of settling megalopae can be several orders of magnitude lower (Lipcius et al., 1990; Rabalais et al., 1995; van Montfrans et al., 1995; Almeida and Queiroga, 2003). The estuaries had tidal regimes that changed in relation to tidal amplitude, tidal periodicity, and phasing of day/night cycles, and individual records did not show any periodicity in the settlement process. This lack of periodicity is most probably a consequence of the availability of competent larvae in the plankton of shelf waters adjacent to the estuaries, which depends on past advection history (Richards et al., 1995), as well as on seasonal hatching, temperature-dependent growth rates, and predation. When records obtained over several estuaries with semidiurnal tidal regimes were standardized, pooled, and analysed for periodicity of settlement, a clear period of about 15 days emerged, during which higher settlement intensity was coincident with spring tides (van Montfrans et al., 1995). Clear semilunar periods were also identified from a series of brachyuran megalopae that included several species, thereby dampening the eVect of the absence of larvae of a particular species at particular moments (Moser and Macintosh, 2001; Paula et al., 2001). Here again, highest settlement was associated with high-amplitude tides. Taken together, these studies indicate that the tidal cycle can synchronise immigration of crab megalopae into estuaries through the behavioural adaptations described in Section 8.

6.2. Diel migrations Tidal migrations have never been identified in decapod larvae collected in shelf and oceanic waters (Table 3). It is possible for larvae hatched from estuarine species to retain an endogenous tidal component in their vertical migration behaviour (Zeng and Naylor, 1996c), and this component could

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well interact with along-shelf tidal flows to advect the larvae along the coast. However, this possibility has never been investigated. It is not known to what degree larvae from shelf and slope species have evolved some kind of tidal behaviour. Most likely, the selective pressures would be much weaker than for estuarine species (Queiroga et al., 2002). Diel migrations, however, are very common in all species categories (Table 3). It has been proposed that these migrations could result in predictable onshore/oVshore patterns of larval distributions, which would be regulated by the interaction of a neustonic distribution during part of the day as well as by the system of sea/land breezes (Shanks, 1995). A common pattern of horizontal distribution observed in shelf waters is that young larval stages are concentrated inshore, close to the adults’ habitat, whereas intermediate stages are normally found oVshore (Jackson and Strathmann, 1981), sometimes beyond the shelf break. Very often the competent stage shows a bimodal distribution, with concentration maxima in oVshore as well as in inshore waters (Lough, 1976; Rothlisberg and Miller, 1983; Pringle, 1986; Lindley, 1987; Queiroga, 1996). This bimodal distribution is normally interpreted as a consequence of moulting from the previous stage, which occurs oVshore, followed by a diVerential onshore transport of the competent stage originated by a change of behaviour. If first and intermediate larval stages show a nocturnal pattern of vertical migration (Table 3), their occurrence in surface waters during the night could result in a night-time oVshore net movement under the influence of the land breeze. Conversely, net onshore transport of crab megalopa could result from their presence in the neuston in species showing twilight migration such as Cancer larvae (Jamieson and Phillips, 1988). When entering the neuston layer at sunset, the larvae would be carried onshore by the strong sea breeze that is still blowing. When they re-enter the neuston around sunrise, the larvae would be transported seaward by the land breeze (Figure 7). Because the land breeze is of less intense than the sea breeze, the net transport would be onshore (Shanks, 1995). Onshore transport of crab megalopae has also been reported to result from the interaction of vertical migration and onshore transport caused by geostrophic winds. Hobbs et al. (1992) calculated wind-driven Ekman transport, based on wind fields estimated from atmospheric pressure distributions, and related nearshore density of Cancer magister megalopae with two diVerent vertical migration scenarios. Their data included observations on megalopal distribution over a stretch of coast 700 km long for 4 diVerent years (see also Hobbs and Botsford, 1992). The vertical migration scenarios were a subsurface uniform depth distribution within the Ekman layer (no migration) and 12 h in the neuston during the night followed by 12 h in subsurface waters. The uncertainty of the Coriolis deflection of the neuston layer was accounted for by testing deviations of 38 and 158 to the right of the

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Figure 7 Schematic representation of sea (a) and land (b) breezes. Panel (c) represents typical variation of wind intensity. Putative onshore transport of crab megalopae occurs when they enter the neuston layer at sunset, when the sea breeze is close to its maximum intensity.

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wind. The best fit between onshore transport and nearshore density of megalopae was obtained when megalopae were simulated as remaining in subsurface waters during the day and in the neuston layer during the night, assuming that transport in the neuston layer would be down the wind and at 3% of the wind speed. A very elegant study on the interaction between diel vertical migration and the tidal cycle (Figure 8) was provided by Rothlisberg (1982) and Rothlisberg et al. (1983a). Four species of Penaeus occur in the Gulf of Carpentaria, northeast Australia (P. esculentus, P. vanamei, P. stilirostris,

Figure 8 Interaction between diel migration of Penaeus postlarvae in the Gulf of Carpentaria (Australia) and the K1 tidal constituent (period ¼ 23.93 h). Vertical distribution of postlarvae along the day is represented in panel (a) for situations 182 days apart, which correspond to opposite phase relationships between the day and the tide cycles: in Days 0 and 365, postlarvae reach the highest position in the water column during ebb; in Day 182, the highest position is reached during flood. Panel (b) represents the change in the relative advective potential throughout the duration of the beat period between the day and the tide cycles (which equals 365.4 d). Transport is consistently into one direction during one part of the year, and into the opposite direction during the other part. The 15-day oscillation of the advective potential corresponds to the spring–neap cycle of tidal amplitude. Time was arbitrarily set at Day 0 in both panels.

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and P. brevirostris). In a study designed to understand the patterns of vertical migration (Rothlisberg, 1982), which did not discriminate among the four species, it was found that larvae and postlarvae had a clearly defined nocturnal migration pattern. Because bottom depths of the Gulf of Carpentaria do not generally exceed 60 m, the larvae were very close to the bottom during the day. Reproduction of the four species occurs twice during the year, with hatching taking place between March and May and between October and December, but the nursery areas located on the northeastern and southeastern Gulf only receive the larvae that hatch in one of the seasons. The northeastern area receives recruits originated in the March to May period and the southeastern area those spawned in the October to December period. To investigate why these two nursery areas do not receive recruits originating from the two annual spawning events, a numerical model that included wind- and tidally driven circulation was developed (Rothlisberg et al., 1983a). This model also included several scenarios of vertical migration; namely, a diurnal phase spent very close to the bottom, a diurnal phase spent at intermediate depths, and no migration with the larvae either at the surface or the bottom. All simulations developed for the month of March that included some kind of nocturnal migration resulted in northward transport of the postlarvae for both the northeast and southeast nursery areas, whereas those for the month of October all resulted in a southward path. Larvae that did not migrate remained in the vicinity of the simulated points of release. Seasonal wind diVerences could not account for the results. To explain this result, the tide regime at the Gulf of Carpentaria has to be considered. Tides here are of the mixed, predominantly diurnal, type and are dominated by the K1 luni–solar diurnal constituent. This tidal constituent has a period of 23.93 h, which is close, but not equal, to the day period. Supposing a situation in which the nocturnal migration of the larvae is (almost) in synchrony with the tidal cycle, the larvae will be transported in a certain direction, because they will consistently be close to the shallow bottom during a particular phase of the tide, where the tidal current speed is low. However, as time goes by, the migration cycle and the tide cycle will slowly shift out of phase. As this happens, the unidirectional transport decreases progressively, until it reverses and reaches a maximum in the opposite direction when the two cycles are in opposite phases. Because of the small diVerence between the periods of the K1 tide and of the day, the beat period between the two cycles, that is, the period that spans the time when both cycles are in phase, through the time when they are out of phase, then to the time when they return to phase, is 365.4 d (Hill, 1995). This means that, during half of the year, the tidal transport will take place predominantly in one direction, but it will occur in the opposite direction during the other half. Thus, a diel migration over a background of a tidal migration can result in a horizontal advection that changes seasonally and

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can account for the observed diVerences in recruitment times in the two nursery areas of the Gulf. During March, the larvae will be advected northward, away from the southeastern area but into the northeastern one, resulting in peak recruitment in the northeast but no recruitment in the southeast, and the reverse will occur during October.

6.3. Ontogenetic migrations Changes in behaviour during larval development have been described clearly in laboratory studies. These changes can result in diVerential transport by physical processes, even if individual stages do not migrate. As seen earlier (Section 5), behavioural changes throughout ontogeny can also be inferred from field studies, when diVerent stages show dissimilar ranges of depth or horizontal distributions (see references in Tables 3 and 4). This section will examine two cases in which a diVerential depth distribution among stages has been related to diVerential advection processes. Spiny lobsters have an unusual, long larval phase comprising several phyllosoma stages and a puerulus decapodid (Pollock, 1995; Anger, 2001). Panulirus cygnus occurs along the west coast of Australia. It has a larval phase composed of nine phyllosoma stages that lasts between 9 and 12 months (Phillips, 1981); during this time, larvae can be carried long distances into the Indian Ocean (Phillips, 1981; Phillips and McWilliam, 1986; Figure 9). The phyllosoma larvae have been found to perform nocturnal migrations, where the maximum depth of distribution during the day appears to be dependent on underwater light intensity (Phillips et al., 1978; Rimmer and Phillips, 1979). The nocturnal migration occurs over a background of an ontogenetic migration, with older phyllosoma stages moving deeper during the day than young and intermediate larvae, as an apparent consequence of an increased photonegative response (Rimmer and Phillips, 1979). Surface flow in the area of distribution of the species is driven primarily by wind and has an oVshore direction during spring and summer (Phillips, 1981; Phillips and McWilliam, 1986). This flow carries young P. cygnus phyllosoma westward away from the continental shelf and at least 1500 km oVshore, with the greater abundances being found between 375 and 1000 km from the coast of western Australia (Phillips et al., 1979; Phillips, 1981). As the phyllosomae develop, they will spend more time in deeper waters. Excluding the surface layer, subjected to the eVects of the wind, the geostrophic flow in the upper 300 m of the Indian Ocean in the area of distribution of P. cygnus larvae is eastward, towards the Australian coast. It is presumed that this geostrophic flow, which can be enhanced by strong onshore currents associated with meanders of the Leewin current (Pearce and Phillips, 1994), carries the late larvae back to near the shelf

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Figure 9 Schematic representation of circulation in the upper Indian Ocean, (based on data from Phillips, 1981 and Philips and Mac William, 1986) and vertical distribution of Panulirus cygnus phyllosoma. Both early- and late-stage phyllosoma show nocturnal migration, but whereas migration of early late-stage phyllosoma is restricted to the top 60 m of the ocean, maximum densities of these older stages can be found below 120 m during the day.

edge (Phillips, 1981; Phillips and McWilliam, 1986; Phillips and Pearce, 1997). The last phyllosoma then metamorphoses to the puerulus stage, which is believed to swim across the continental shelf in the search of fitting settlement habitats (Phillips and Olsen, 1975; Phillips et al., 1978; Phillips and Pearce, 1997). Carcinus maenas is a portunid crab native to European coastal waters that has been introduced elsewhere in the world (Grosholz and Ruiz, 1995; Udekem d’Acoz, 1999). A series of studies conducted on the Portuguese northwest coast appear to show a relation between the depth distribution of the megalopae and their onshore wind-driven transport. Carcinus maenas larvae are restricted to the first 60 m of shelf waters. The first and second zoeae were found to be more common in the top 30 m, but from the third zooeal onward, the larvae were gradually deeper, with megalopae being equally distributed between the 0–30- and 30–60-m depth levels (Queiroga, 1996). Intermediate zoeal stages had a unimodal horizontal distribution, being concentrated on the middle shelf, but the distribution of the megalopae was bimodal, with maxima of abundance on the middle shelf and close to the shore (Queiroga, 1996). This horizontal distribution indicates that some process transported the megalopae shoreward, but not the zoeae. The same study and other hydrographic measurements taken concurrently

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(Hagen et al., 1993) showed that megalopae occurred in a surface layer that approaches the coast during relaxation of northerly, upwellingfavourable winds. This hypothesis was further tested in subsequent studies that showed that the abundance of megalopae inside estuaries followed the relaxation of the northerly winds or the increase of southerly winds (Almeida and Queiroga, 2003; Queiroga, 2003). The zoeal stages are not transported onshore presumably because, having a shallower distribution, they are more likely to be transported close down wind within the surface Ekman layer.

7. PROXIMATE FACTORS CONTROLLING VERTICAL MIGRATION: ENVIRONMENTAL FACTORS AND ENDOGENOUS RHYTHMS Like the majority of invertebrate larvae, decapod larvae are negatively buoyant (Chia et al., 1984; Sulkin, 1984; Young, 1995; Metaxas, 2001). Thus, their maintenance in the water column is only possible through active swimming. All field studies on vertical distribution of decapod larvae (Table 3) show defined patterns of vertical distribution that change with species, larval stage, and sampling time relative to particular environmental cycles. These observations imply that larvae are able to regulate their swimming activity to reach or maintain a certain position in the water column. It is generally agreed that vertical position has paramount consequences on feeding, predation exposure, and dispersal by currents (reviewed by Rice, 1964; Thorson, 1964; Scheltema, 1986; Young and Chia, 1987; Rumrill, 1990).

7.1. Tactic and kinetic responses by estuarine and marine larvae The regulation of vertical position by a planktonic organism depends on its capacity to orient and determine its position in relation to a set of spatial coordinates. Discussions of general orientation mechanisms in marine animals can be found in Schone (1975), and in Creutzberg (1975) for invertebrates. The environmental factors to which animals respond can be classified as scalars or vectors. A scalar (e.g., pressure) can change through space or time but does not contain any directional information. A vector (e.g., light) can also vary in magnitude, but also contains directional information of change (e.g., light). The behavioural responses of free-living animals to environmental stimuli can broadly be classified into kineses and taxes. A kinesis (e.g., barokinesis), or kinetic response, is a nonoriented response to a scalar. The animal just increases or decreases locomotor activity as a

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function of the stimulus intensity, until it eventually moves away from or close to the source, usually following a winding route. Kineses are either high or low depending on whether the intensification of the stimulus induces an increase or a decrease in activity. Taxes (e.g., phototaxis), or tactic responses, are directional reactions to vectorial cues. Taxes are termed positive or negative according to whether the response is directed toward the stimulus source or in the opposite direction. In the marine environment, there are only four physical factors with vectorial properties (Crisp, 1974; Young, 1995): gravity, light, light polarity, and current. Light, light polarity, and gravity are oriented vertically and can potentially be used to direct behavioural responses during vertical movements. Current direction cannot usually be used by planktonic larvae as an orienting cue because they reside in a water parcel that is moving with the larva. Settling stages could, in principle, respond by oriented swimming with or against the current because they frequently touch and probe the bottom, which would provide them with an environmental background for feeling current direction and strength. Settling stages of penaeid larvae do exhibit rheotactic behaviours (Hughes, 1969), but to our knowledge, rheotactic behaviour during settlement has not been described in other decapod groups. The principal scalar factors to which marine animals respond are light intensity, pressure, temperature, salt concentration, and other dissolved substances. In theory, larvae could respond with an oriented behaviour to scalar quantities, provided they could probe simultaneously several points in space to detect the spatial direction of change. For instance, pressure could be used to determine the vertical direction if the larvae could measure pressure in several points and detect the direction of the pressure gradient, but since larvae are usually small and their sense organs only detect order of magnitude diVerences, the probability that a larva might sense dissimilarities between two sensorial organs is low. Nonetheless, directional responses induced by changes in scalar quantities have evolved frequently among larvae of benthic invertebrates. Such responses depend on the interaction of the response to the scalar stimulus with the response to one of the vectors, either light or gravity. For example, crab megalopae react to a pressure increase by active upward swimming (Knight-Jones and Qasim, 1967; Forward et al., 1995). In this case, the orientation of movement is directed by gravity, although the response had invoked by of a scalar quantity (Crisp, 1974). When studying the eVects of a scalar quantity on behaviour, one must to consider two diVerent aspects of change of the variable. One is the rate of change; decapod larvae can only sense and react to rates of change above a certain threshold. The second is the absolute amount of change; once the rate threshold has been reached, larvae do not react before reaching an absolute threshold. Rate thresholds and absolute thresholds have been

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found to change with species and larval stage (Forward et al., 1989; Forward, 1989a; Tankersley et al., 1995). Gravity, pressure, and light are the most relevant factors for controlling vertical movements of larvae (Crisp, 1974). Gravity is a ubiquitous factor and is essentially invariant with depth and time. Pressure is also ubiquitous and varies in a predictable manner with depth, if one excludes small changes caused by density diVerences associated with water masses diVerent salinities. Light is more variable because its intensity, composition, and angular distribution change with depth, although its direction is always vertical. Thorson (1964) originally suggested that light would be the most important factor involved in depth regulation by marine larvae. However, Sulkin (1984) expressed the opinion that, given the vital importance of the maintenance of appropriate position in the water column for the survival of marine larvae, it would be expected that selective pressures operate to select a combination of behavioural traits that are based on responses not only to light but also to more conservative stimuli (i.e., gravity and pressure).

7.2. Endogenous rhythms Decapod larvae can also modify their vertical distribution in the water column through responses to endogenous cycles of activity. A biological rhythm occurs when animal activity patterns can be directly related to environmental features that occur with regular frequencies (Drickamer et al., 2002). Biological rhythms are regulated by biological clocks, which are internal timing mechanisms that involve a self-sustaining physiological pacemaker and an environmental cyclic synchroniser. Because of the internal physiological mechanism, biological rhythms also persist in artificial constant conditions; hence the term endogenous rhythm, which is frequently used as a synonym. Biological rhythms have evolved to prepare animals for changes in their environment that will occur in a predictable manner. Biological rhythms give animals that display them a competitive advantage over animals that must rely solely on the environmental factors associated with natural cycles. A rhythm can be considered endogenous if its phase relationship with the relevant natural cycle can be altered by an artificial cycle of the same environmental factor, and this resynchronised rhythmic behaviour persists autonomously for several cycles under constant conditions (i.e., under the absence of the natural and artificial cycles). Also the period of the freerunning rhythm, under constant conditions must be similar, but not equal, to that of the natural cycle (Enright, 1975a). In fact, if the period is exactly equal to that of the natural cycle, the possibility cannot be excluded that

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conditions are not absolutely constant for the test animals, and that some subtle stimulus associated with natural environmental cycles and not felt by the researcher, is experienced by the organisms. From this last stipulation derives the term ‘‘circa’’ (or approximately), indicating that a rhythmic activity that, in the natural environment, is expressed with a period equal to that of, for example, the tide or day cycles, shows under constant laboratory conditions a circatidal or circadian period. Good reviews of the types of biological rhythms expressed by marine animals and of their physiological mechanisms and environmental synchronisers can be found in Enright (1975b), De Coursey (1983), and Palmer (1995).

8. BEHAVIOURAL CONTROL OF VERTICAL MIGRATION: EVIDENCE FROM LABORATORY STUDIES Behavioural responses by decapod larvae to environmental factors and endogenous rhythms have been the objects of considerable research since the 1970s (summarized in Table 5). Many of these studies have been conducted in laboratory conditions in an attempt to isolate the eVects of the diVerent variables that modify larval behaviour. Such isolation of factors is frequently impossible to accomplish in field studies (Sulkin, 1986). Depending on the need to isolate the eVect of individual factors or to describe the eVect of the interaction between scalar and vector stimuli, experimental approaches have considered one isolated factor or two factors simultaneously. Normally, the larvae are placed in standard conditions and left to acclimate for a period of time, after which they are stimulated and their reaction recorded. The study of endogenous rhythms of activity is conducted under constant conditions. Very often, the larvae are illuminated with infrared light, which has been shown to be invisible to them (Forward and Costlow, 1974). In this way, behaviour can be observed without the disturbance that a visible light would cause. The study of larval behaviour often involves the use of an actograph (i.e., a device that records movements). An actograph consists of a chamber in which test organisms are placed, and a method that detects and records their position over time. The methods that have been used to record the movements of larvae consist of three types: video recordings followed by visual analysis of the images (Cronin and Forward, 1982, 1986; Forward et al., 1997); video recordings followed by automatic analysis of the images (Ducheˆne and Queiroga, 2001); and the use of paired infrared light–emitting diodes and receptors, which automatically record the position of an organism by interruption of the infrared beams (Zeng and Naylor, 1996a,c). A detailed account of the methodologies used in laboratory studies of decapod larval behaviour is outside the scope of this

F, I

F, I

F, I

F, I

F F, I

F, I, L

F, I F, I, L F, I, L F, I, L F, I

F, I

Chemicals

Temperature

Current

F

Turbulence

Gravity

F

Salinity

Pressure

Obligate estuarine species Brachyura Eurypanopeus depressus Brachyura Neopanopaeus sayi Brachyura Panopeus herbstii RhithroBrachyura panopeus harrisii

Light

Species

Endogenous

Infraorder or division

References

Sulkin et al., 1983 Forward et al., 1989; Forward, 1989a Sulkin, 1973, 1975; Forward, 1977 Forward, 1974, 1985, 1989a,b; Forward and Costlow, 1974; Ott and Forward, 1976; Bentley and Sulkin, 1977; Latz and Forward, 1977; Wheeler and Epifanio, 1978; Cronin and Forward, 1979, 1982, 1983, 1986; Forward et al., 1989; DiBacco and Levin, 2000

165

(Continued)

HORIZONTAL TRANSPORT OF DECAPOD LARVAE

Table 5 Laboratory studies on the influence of endogenous and several environmental factors on swimming and vertical migration activity of larval decapod crustaceans

166

Estuarine species that export their larvae to the shelf Brachyura Callinectes L F, I, L F, L sapidus

Carcinus maenas

Brachyura

Pachygrapsus crassipes Sesarma cinereum Uca pugilator

Brachyura Brachyura

F, L F, L

L

F

F, L

L

L

F, I L

Chemicals

Temperature

Current

Turbulence

Salinity F, I, L F, L L

References

Naylor and Isaac, 1973; Forward, 1977; Sulkin et al., 1979, 1980; Sulkin and van Heukelem, 1982; McConnaughey and Sulkin, 1984; Luckenbach and Orth, 1992; Forward and Rittschof, 1994; Tankersley and Forward, 1994; Forward et al., 1995, 1997; Tankersley et al., 1995, 1997; Welch and Forward, 2001 Rice, 1964; Knight-Jones and Qasim, 1967; Zeng and Naylor, 1996a,b; Ducheˆne and Queiroga, 2001. Shanks, 1985

F

Forward, 1977

F

Forward, 1977

HENRIQUE QUEIROGA AND JACK BLANTON

Brachyura

Gravity

Pressure

Species

Light

Infraorder or division

Endogenous

Table 5 (Continued )

Uca spp.

L

L

L

L

L

Shelf species that may penetrate estuaries as adults Brachyura Libinia F emarginata Shelf species that use estuaries as nursery habitats Dendrobranchiata Penaeus brevirostris DendroPenaeus branchiata californiensis DendroPenaeus L branchiata duodarum DendroPenaeus L branchiata japonicus L Penaeus Dendrostylirostris branchiata DendroPenaeus L branchiata vannamei Shelf species Astacidea Palinura Anomura Anomura Anomura

F, I, L F, I, L

Forward and Rittschof, 1994; Tankersley and Forward, 1994; Tankersley et al., 1995 Forward, 1977

L

L

L

Mair et al., 1982

L

L

L

Mair et al., 1982

L

Hughes, 1969; Hughes, 1972 Forbes and Benfield, 1986

L

L

L

Mair et al., 1982

L

L

L

Mair et al., 1982

F

Ennis, 1975a, 1986; Boudreau et al., 1992 Ritz, 1972 Knight-Jones and Qasim, 1967 Forward, 1987a

F

Forward, 1987a

F L

F, I, L L

(Continued)

167

Homarus americanus Panulirus cygnus Galathea sp. Pagurus beringanus Pagurus granosimanus

HORIZONTAL TRANSPORT OF DECAPOD LARVAE

Brachyura

168

Anomura Brachyura Brachyura Brachyura Brachyura Brachyura

Brachyura Brachyura Brachyura

Pagurus longicarpus Cancer gracilis Cancer irroratus Cancer magister Ebalia tuberosa Hemigrapsus oregonensis Hyas araneus Leptodius floridanus Liocarcinus holsatus Lophopanopeus bellus Scyra acutifrons

Shelf and slope species Brachyura Geryon quinquedens

F F, I F, I F F

F, I F, I F

Chemicals

Temperature

Current

Turbulence

Salinity

Gravity

Pressure

F, I

References

Roberts, 1971 Forward, 1987a F, I Bigford, 1977, 1979 Jacoby, 1982 Schembri, 1982 Forward, 1987a

F, I F, I F

F F, I, L F, I, L F, I

Knight-Jones and Qasim, 1967 Sulkin, 1973, 1975; Wheeler and Epifanio, 1978 Naylor and Isaac, 1973

L F

Forward, 1987

F

Forward, 1987 F

F

F

Kelly et al., 1982

See Table 2 for definition of ecological category. Chemicals include water of diVerent origin (e.g., estuarine and sea water). F ¼ first stage; I ¼ intermediate stages; L ¼ last stage. Empty cells indicate that data are not available.

HENRIQUE QUEIROGA AND JACK BLANTON

Brachyura Brachyura

Species

Light

Infraorder or division

Endogenous

Table 5 (Continued )

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review, but good descriptions can be found in Forward (1989b), Forward and Wellins (1989), Tankersley et al. (1995), Zeng and Naylor (1996a), and Ducheˆne and Queiroga (2001). Sulkin (1984, 1986) proposed a conceptual model for laboratory study of depth regulation by brachyuran larvae consisting of three components. The first component is the natural buoyancy of the larva. Active reactions will have diVerent results depending on whether a larva floats, sinks, or is neutrally buoyant. The second component is orientation. Orientation of the body usually depends on the reaction of larvae to the vertical vectors of gravity and light and will determine whether locomotor activity complements or compensates for the eVects of buoyancy. The third component is the level of locomotor activity. The speed and the frequency of locomotion vary in response to the intensity of the scalar factors, which may change with depth. Therefore, the intensity of the reaction of a larva to these factors determines to what extent the eVects of buoyancy are modified by the swimming activity of the larva. On the basis of this model, the vertical distribution of a larva depends on the dynamic balance between these components, which can be independently subjected to rigorous quantification in the laboratory. Therefore, changes of vertical distribution in the natural environment can be predicted from species- and stage-specific measurable reactions to the diVerent factors. It must be said, however, that even though they are a powerful aid to the study of the control of vertical movements, predictions of behaviour in the field based on laboratory studies rely on realistic simulations of the type, rates, and amounts of change of the variables under study, a condition that may be diYcult to meet. The most significant advances permitting in-depth understanding of the control of vertical position and predictions about behaviours in the natural environment came from studies in which the types, rates, and absolute amounts of change of environmental variables were carefully controlled with electronic sensors and were constrained to remain within ecologically significant boundaries (see examples in the following sections). For instance, many of the former studies of pressure eVects on swimming activity and vertical migration were done with the use of unrealistic step increases and decreases, to which the larvae are never subjected, and without considering rates of change of the variable. (e.g., Rice, 1966; Knight-Jones and Qasim, 1967; Naylor and Isaac, 1973; Ennis, 1975a; Wheeler and Epifanio, 1978). Similarly, most of the studies on reactions to light used directional light as a stimulus. As noted by Forward (1988), directional light does not occur in the natural underwater environment. Despite their limitations, the former studies are still useful in that they show a common behavioural basis exhibited by decapod larvae, where particular patterns displayed by diVerent larval stages and ecological categories can be related to particular ecological needs.

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8.1. Responses to environmental factors Studies on the behavioural reaction of decapod larvae to external stimuli (summarized in Table 5) have dealt mostly with brachyuran decapods. This bias derives from the ease of obtaining and rearing the larvae of this group in laboratory conditions. Nonetheless, the species investigated belong to all ecological categories considered in this review and occur at diVerent depth levels, allowing some generalizations to be drawn (see also Sulkin, 1984).

8.1.1. Pressure and gravity Pressure and gravity are the two most ubiquitous and conservative variables of the marine environment (Crisp, 1974), and they form the basis of the negative feedback model for depth regulation of crab larvae (Sulkin, 1984). Similar models have not been developed for other decapod groups, but scattered evidence available for nonbrachyurans also supports this model. Therefore, as they provide a clear conceptual background for the interpretation of depth regulatory traits exhibited by decapod larvae, responses to pressure and gravity will be analysed together in this section. The first data and reviews on the eVect of pressure and gravity of decapod larvae and other marine animals, were by Rice (1964, 1966) and Knight-Jones and Morgan (1966). The first zoea of almost all studied brachyuran crabs shows negative geotaxis (Sulkin, 1973; Ott and Forward, 1976; Latz and Forward, 1977; Bigford, 1979; Sulkin et al., 1980, 1983; Kelly et al., 1982; Schembri, 1982) and, usually, high barokinesis (Sulkin, 1973; Sulkin et al., 1980, 1985; Schembri, 1982; Forward et al., 1989). This behaviour appears to be universal among the first stage of brachyuran crabs, and as a consequence, newly hatched larvae swim to the surface. Thermal and haline stratification that naturally occur in the larvae’s habitat do not seem to be strong enough to obstruct this migration when the larvae either occur in estuaries (Sulkin et al., 1983; McConnaughey and Sulkin, 1984) or in coastal waters (Kelly et al., 1982). Intermediate zoeal stages exhibit more variable responses. In some species there is an inversion of the geotactic signal in the older zoeae, which become more positively geotactic (Rhithropanopeus harrisii, Ott and Forward, 1976; Callinectes sapidus, Sulkin et al., 1980; Cancer magister, Jacoby, 1982; Geryon quinquedens, Kelly et al., 1982), but not in others (Panopeus herbstii and Leptodius floridanus, Sulkin, 1973; Cancer irroratus, Bigford, 1979). Several patterns of barokinesis have been described. Cancer magister, R. harrisii, and Neopanopae sayi display high barokinesis in advanced zoeal stages (Wheeler and Epifanio, 1978; Jacoby, 1982; Forward et al.,

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1989), and Leptodius floridanus responds neutrally to pressure change in the last zooeal stage (Sulkin, 1973; Wheeler and Epifanio, 1978). In C. sapidus, there is a reversal of the barokinetic response in older zoeae, which show low barokinesis (Sulkin et al., 1980). The passage to the megalopa phase is always accompanied by profound modifications of the behavioural responses relative to the zoeal phase. Megalopae usually display positive geotaxis (L. floridanus and Panopeus herbstii, Sulkin, 1973; Cancer irroratus, Bigford, 1979), although Pachygrapsus crassipes (Shanks, 1985) and Callinectes sapidus (Sulkin and van Heukelem, 1982) megalopae are geonegative. All megalopae show high barokinesis (C. maenas and Macropipus sp., Rice, 1964; Carcinus maenas and Macropipus sp., Naylor and Isaac, 1973; Eurypanopeus depressus, Sulkin et al., 1983; Pachygrapsus crassipes, Shanks, 1985). Collectively, the studies cited above show that the later zoeal stages of brachyuran crabs, display behaviours that result in the larvae having a lower position in the water column than in earlier stages, with increasingly positive geotaxis and neutral or low barokinesis. The passage to the megalopal stage is associated with a clear shift in behaviour that causes movement toward the surface or the bottom, depending on the species. The eVects of pressure rates of change on larval behaviour were investigated in the crabs Rhithropanopeus harrisii, Callinectes sapidus, and Uca spp. Forward and Wellins (1989) tested the responses of Rhitropanopeus harrisii zoeae to rates of pressure change in the absence of light. Rates of pressure increase above 0.175 mbar s1 evoked an ascent reaction induced by high barokinesis and negative geotaxis in stage I–III zoeae. Threshold rates needed to induce similar responses in stage IV were 1.19 mbar s1. Slow rates of pressure decrease evoked a descent response in all zoeal stages, with threshold rates ranging from 0.40 to 0.53 mbar s1. Because larval sinking and descent swimming rates expose the larvae to pressure changes above these threshold levels, the authors concluded that larvae can move rapidly enough to produce changes in pressure that evoke compensatory, depth regulatory, behavioural responses. The responses of Callinectes sapidus and Uca spp. to pressure, salinity, and light were studied by Tankersley et al. (1995) to test the hypothesis that salinity and pressure increase during flood could trigger an ascent in the water column during the night. Larvae of both genera moved upward on an increase in pressure. The rate thresholds were diVerent. In C. sapidus, the lowest rate of pressure increase that produced a significant ascent was 2.8  102 mbar s1, whereas Uca spp. megalopae responded only to rates above 4.9  102 mbar s1. Absolute thresholds were similar for both genera. They depended on rate of pressure increase and were greater for the lowest rates, varying between 2 and 6 mbar. These threshold levels are below the typical rates of pressure change that megalopae of these species encounter in many of the estuaries where they occur

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(DeVries et al., 1994), which led the authors to conclude that pressure changes could not be responsible for the control of swimming during night-time flood tides in both species. Responses to pressure have been studied in the non-brachyurans Penaeus Japonicus and Homarus americanus. In Penaeus japonicus, pressure increases stimulated postlarvae to swim from the bottom to the water column, which was interpreted as aiding in tide transport into estuaries during flood (Forbes and Benfield, 1986). Homarus americanus stage I larvae showed positive barokinesis and swam to the surface on pressure increases to a maximum of 1370 mbar. Below 690 mbar, the positive response increased with increasing rate of pressure change, and at 1379 mbar all larvae were at the surface. Older stages were less responsive to pressure increase but, nevertheless, responded positively. The minimum rate evoking a response by stage I larvae appeared to be 1.15 mbar s1 (Ennis, 1975a). Ennis (1975a) also reported that stage I to stage III larvae released below the sea surface swam upward. Newly moulted stage IV larvae also swam upward when released below the surface, but older stage IV larvae released near the bottom remained there, looking for shelter. Because fewer larvae swam to the surface with increasing natural light intensities, the upward swimming behaviour is probably induced by negative geotaxis, and not by positive phototaxis. Species in which the zoeal stages do not fit the above paradigm of a surface distribution are characterized by unusual habits during the larval or juvenile phases. For example, newly hatched first-stage zoeae of Ebalia tuberosa exhibit positive phototaxis to directional light, negative geotaxis, and high barokinesis. These behaviours induce upward swimming and result in a position close to the surface, but there is a change in behaviour during the following days, so that 7day-old stage I larvae are photonegative and geopositive and stop responding to pressure increase (Schembri, 1982). These adaptations are related to the specialized semibenthic habits of the larvae of Ebalia, which feed on detritus deposited on the bottom (Schembri, 1982). Another example concerns the hermit crab Discorsopagurus schmitti. This species has the unusual habit of protecting its soft abdomen exclusively inside empty tubes of the polychaete Sabellaria cementarium, which forms bioherms in the shallow subtidal zone of rocky shores. Because of the rarity of occurrence of this particular type of habitat, one interesting question to pose concerns the mechanisms by which the competent megalopae find the correct habitat, especially considering the relatively long larval phase (up to 70 days) and considering that megalopae and juveniles will preferentially select empty gastropod shells over polychaete tubes when both are presented in choice experiments. The hypothesis advanced is that larval stages of D. schmitti should demonstrate behavioural traits that would result in retention near the parental habitat by assuming a low position in the water column (Gherardi, 1995). Results of experiments showed that all zoeae were negatively buoyant and that stages I and II were geopositive, but not

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stages III and IV. The positive geotaxis of first and second zoeal stages is contrary to the usual rule in decapod crustaceans. However, stages I and II showed high barokinesis in response to discrete pressure increases, and pressure increase appeared to augment the number of positive responses to light, which would promote ascent in the water column by late–stage larvae. Moreover, the presence of a current close to the bottom appeared to increase the height of vertical swimming excursions made by the stage I–III larvae. Therefore, although some behaviours displayed by the early zoeae indicate that they would remain close to the bottom, Sabellaria bioherms are a high-energy environment dominated by strong swell and tidal currents (Gherardi and Cassidy, 1994), and it is hard to see how these behaviours alone would promote retention close to this habitat.

8.1.2. Light Caution is necessary when interpreting studies on reaction to light. Most decapod larvae react to directional light by positive phototaxis (see references in Table 5). This behaviour is similar to that displayed by most zooplanktonic organisms when they are tested in the laboratory under similar conditions (reviewed by Forward, 1988). If zooplankton are photopositive to high light intensities, then it could be predicted that they would accumulate close to the surface during the day, which is usually not the case. However, directional light does not occur in the natural marine environment, and when experiments are conducted with a light field that simulates the environment’s natural angular light distribution, most studies showed that zooplanktonic organisms are photonegative to high light intensities and photopositive to low light intensities (Forward, 1988). For example, light-adapted zoeae of the crab Rhithropanopeus harrisii showed positive phototaxis to high-intensity and negative phototaxis to low-intensity directional light. Dark-adapted larvae showed positive phototaxis throughout the range of light intensities. On the contrary, when stimulated with a natural light field, light-adapted zoeae showed negative phototaxis through the entire range of light intensities (Forward and Wellins, 1989). The results obtained with R. harrisii larvae indicate that responses in a natural light field are a better indicator of behaviour in nature (Forward et al., 1984). Most of the older studies identified in Table 5 did not realistically simulate natural light conditions. An interesting aspect of the reaction of Rhithropanopeus harrisii to light is that, when illuminated with a simulated ‘‘natural’’ light field from below and not from above, light-adapted larvae show negative phototaxis to high light intensities (Forward, 1986) and swim upward. This reaction indicates that, somehow, the sign of phototaxis, the level of photokinesis, and the

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reaction to gravity interact in some yet unclear way. Nevertheless, the studies made with directional light are consistent in that most show positive phototaxis, which is triggered by high photokinesis, throughout the larval series, including the megalopa. Examples include Uca pugilator (Herrnkind, 1968), Rhithropanopeus harrisii (Forward and Costlow, 1974), Leptodius floridanus and Panopeus herbstii (Sulkin, 1975), Callinectes irroratus (Bigford, 1979), and Callinectes sapidus (Sulkin et al., 1980). Collectively, these studies indicate that the kinetic reaction to light may interact with the reaction to other scalar or orientating cues and modify vertical swimming behaviour in brachyuran decapods. According to Forward (1988), two main hypotheses were developed to explain the control by light of the nocturnal type of vertical diel migration behaviour. The Preferendum Hypothesis states that zooplankton follows a particular preferred light intensity, which changes depth with the changing position of the sun above the horizon. Zooplankton would ascend during sunset and descend during sunrise in the course of nocturnal migration, following the preferred or optimum light level. According to the Rate of Change Hypothesis, the factor that triggers vertical movements is the rate and direction of change in light intensity from the ambient light level to which zooplankton are exposed. The ascent during sunset would result from a rapid decrease in light intensity evoking upward movement, and the descent at sunrise would result from the rapid increase in intensity. During night and day, the rates of change would be too low to be detected, and zooplankton would remain at the depth they would have reached during the migration. Hypotheses explaining the reverse type of vertical migration have not been developed (Forward, 1988). These two hypotheses could apply to the initial ascent and final descent observed during twilight migration. The midnight sinking and the subsequent ascent before sunrise are diYcult to explain as responses to light, and they could result from activity rhythms (Forward, 1988). Most field studies on vertical migration of zooplankton indicate that populations do not seem to consistently follow a particular light intensity level. Instead, the populations appear to be distributed over a wide range of intensity levels. As a consequence, these studies do not support the Preferendum Hypothesis. The available data from a few laboratory studies appear to confirm the Rate of Change Hypothesis, because ascent and descent responses by each species are not triggered by an absolute light level, but depend on the rate of change in intensity, which diVers according to the level of light adaptation (Forward, 1988). The mechanism of depth regulation during the diel cycle has best been studied in the zoeae of R. harrisii. In addition to a tidal-related rhythm of vertical migration, Rhithropanopeus harrisii larvae also display the nocturnal type of vertical migration (Cronin and Forward, 1986). Forward et al. (1984) examined the vertical distribution of R. harrisii larvae in the field

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in connection with light intensity distribution. They also determined the absolute thresholds for phototaxis and the responses to intensity changes. After dark adaptation, and when stimulated with a directional light source, stage I and IV zoeae show negative phototaxis at low light intensity and a pronounced positive phototaxis at high light intensities. The lowest intensity to produce negative as well as positive phototaxis was around 1  107 W m2, and did not change with development stage. This light level is therefore considered to be the lowest threshold for photosensitivity. The field data showed that, as zoeal development proceeded, the mean vertical distribution of the larvae during the day approached the depth of 1  107 W m2 light intensity. Dark-adapted larvae showed negative geotaxis in darkness and, when illuminated above the threshold level with a light source that simulated natural underwater light distribution, reacted with a downward-directed response induced by negative phototaxis. All zoeae showed the response, but the light levels necessary to produce it decreased gradually from stage I to stage IV, which demonstrates a higher sensitivity as development proceeds. These reactions agree with the field observation that younger zoeae are above the 1  107 W m2 level and approach it as development proceeds. Further observations indicated that the descent during negative phototaxis resulted from passive sinking, and not directional downward swimming. Therefore, the authors concluded that light levels above the lower threshold appear to act as a barrier to upward migration during the day, because the mean larval depth occurred near here. The mechanism controlling the depth regulation is negative geotaxis in darkness, which changes to negative phototaxis and a sinking response when a particular light level is encountered. In a subsequent study, Forward (1985) investigated the behavioural control of ascent during dusk and descent during dawn. The larval stage investigated was the fourth zoea, which has been shown to have the most pronounced diel migratory pattern. Again, the experimental design involved the use of a light field that simulated the natural underwater light distribution. Before sunset, larvae remained near the 1  107 W m2 level and were adapted to the light intensity to which they showed the most pronounced ascent behaviour on light decrease. The cue for the ascent reaction was the relative rate of intensity decrease, not an absolute light level or an absolute amount of intensity change, because intensities at which the response occurred varied over four orders of magnitude, the amount of absolute decrease also varied by four orders of magnitude, and both depended on the level of light adaptation. The minimum rate of change in light intensity that evoked the ascent was 8.6  103 W s1, which is close to the fastest rate of change of light intensity around sunset, determined to be 4.0  103 W s1. The ascent was not controlled by positive phototaxis, because the larvae did not move directly toward the overhead light source, but appeared

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to be directed by negative geotaxis. Moreover, when an inverse light field was used, where the light source was placed below the experimental chamber, the larvae did not move toward the light, but away from it. During the night, the larvae are dark adapted, and the light intensities are below the lower sensitivity threshold of 1  107 W m2 (Forward et al., 1984). In these conditions, the larvae would tend to move upward because they are negatively geotactic (Forward et al., 1984). The cue that triggers their descent at sunrise is the absolute level of light intensity, not the rate of intensity increase, because the absolute intensity that evoked a response was almost constant (at an average level of 1.87  107 W m2), through rates of increase that varied over two orders of magnitude. The downward movement was initiated as light increased slightly above the threshold level of 1.87  107 W m2. The descent reaction was not a sinking reaction, because the larvae moved down slower than anesthetised larvae sank. It also was not a positive geotaxis, because when stimulated with the reverse light field, the larvae moved up following an intensity increase. Thus, the behaviour that underlies the downward response at sunrise must be a negative phototaxis. Finally, during the day larvae remain close to the depth of the 1  107 W m2 level that is just above the lower threshold of sensitivity (Forward et al., 1984). They would have a tendency to ascend, but as they encounter light levels slightly above this value, they will descend by negative phototaxis. Given the reactions to light exhibited by R. harrisii larvae, Forward (1985, 1988) argues that the control of nocturnal vertical migration may be best explained by a synthesis of the Preferendum and Rate of Change hypotheses, and that both hypotheses apply to diVerent phases of the migration. Downward response during sunset and depth maintenance during the day are associated with a preferred light level. At sunset, the upward movement is triggered by the rate of change of light intensity. In brachyuran species that live in estuaries as adults and export their larvae to the sea, the megalopa is the stage that reinvades the estuary. These larvae are commonly found in estuarine waters during the flood and at night, independent of species (Epifanio et al., 1984; Brookins and Epifanio, 1985; Little and Epifanio, 1991; Olmi, 1994; Queiroga, 1998). However, in oVshore waters, megalopae do not show such consistent patterns of vertical and temporal distribution. To study this problem, Forward and Rittschof (1994) compared the photoresponses of Callinectus sapidus and Uca spp. megalopae in estuarine water to those exhibited in oVshore water, under a light field that simulates natural underwater light distribution. They found that megalopae of both genera collected oVshore swam more actively in oVshore water than in estuarine water, independent of light intensity. Moreover, estuarine water inhibited the swimming by megalopae of C. sapidus that were collected in estuaries at light levels normally encountered in

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estuarine and marine waters during the day. On the contrary, at intensity levels typical of the night period, swimming was not suppressed. The suppression of swimming at high light levels did not occur in oVshore waters. These diVerences were not caused by salinity or temperature diVerences but by some chemical cue associated with land drainage or with the flora and fauna of estuarine water. The behaviour induced by estuarine water was reversible, indicating that it did not result from ontogenetic changes. The results indicate that suppression of swimming by high light levels in estuarine waters is responsible for the absence of megalopae of the two genera in estuarine waters during the day, which could help act as a predatoravoidance mechanism. Light intensity was also shown to modify the response to other environmental factors associated with flood tide in estuaries. When illuminated with a light field that simulated natural underwater light distribution, megalopae of Callinectes sapidus and Uca spp. were negatively phototactic or photokinetic and responded to an increase in light intensity by remaining near the bottom. When stimulated with a pressure increase above threshold levels, the larvae responded by swimming up, but the magnitude of the response decreased with increasing light levels, until the response was inhibited at intensities above 1.0  1014 photons m2 s1 for C. sapidus and 1.0  1012 photons m2 s1 for Uca spp., respectively (Tankersley et al., 1995). These responses imply that megalopae of both genera will be inhibited from swimming in the water column by daytime light intensities. Collectively, inhibitions of swimming in estuarine waters and of pressure response by high light levels are responsible for the commonness of brachyuran megalopae in estuaries during night floods.

8.1.3. Salinity Forward (1989a) studied the responses of first and fourth zoeae of the xanthids Rhithropanopeus harrisii and Neopanope sayi to salinity changes. Zoeae of both species responded to a salinity increase with an ascent. The threshold rates were the same for both stages of R. harrisii and were equal to 1.1  103 ppt s1. Neopanope sayi larvae responded to lower rates of change, and the threshold increased from 2.8  104 ppt s1 for the first to 7.0  104 ppt s1 to the fourth stage. At the respective threshold rates of salinity increase, the minimum absolute change needed to evoke an ascent varied between 0.09 and 0.11 ppt in stage I zoeae and between 0.21 and 0.59 ppt in stage IV zoeae of both species (Forward, 1989a). A salinity decrease did not evoke a descent in the water column. This last result was interpreted as a consequence of a putative diVerence in the rate and absolute thresholds for an increase and a decrease in salinity, with the thresholds for an increase

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in salinity being lower than for a decrease. The diVerences in sensitivity encountered in the two species were attributed to the habitat in which the larvae develop. Rhithropanopeus harrisii remains inside estuaries, where rates of salinity change may be pronounced for the whole larval period. Neopanope sayi, in contrast, lives in estuaries as adults, but its larvae develop in the sea, where rates of salinity change are much lower. Considering the salinity gradients that larvae of both species may encounter in nature and their swimming and sinking rates, it was concluded that larvae of both species can respond to natural salinity increases in their environment (Forward, 1989a). In brachyuran megalopae, the responses to rates of salinity change were investigated in Callinectes sapidus and Uca spp. (Tankersley et al., 1995), which are both estuarine species that export their larvae to the sea. Megalopae of both species ascended in the water column on a salinity increase. The rate threshold was an order of magnitude lower for C. sapidus, at 5.53  104 ppt s1, than for Uca spp., at 1.33  103 ppt s1. The absolute thresholds were similar, ranging between 0.3 and 0.4 ppt for C. sapidus and between 0.3 and 0.5 ppt for Uca spp. On the basis of rates of salinity increase in a tidal estuary of North Carolina (Northwest Atlantic), which were found to range from 2.64  104 to 1.32  103 ppt s1, it was concluded that only the megalopae of C. sapidus could respond to natural rates of salinity increase during flood tide by upward swimming. Salinity not only can trigger kinetic responses by crab larvae but also can reverse the sign of the taxes. For instance, Rhithropanopeus harrisii zoeae change phototaxis from positive to negative on salinity decrease (Latz and Forward, 1977). In this species, as well as in Neopanope sayi, an increase in salinity causes a concurrent increase in swimming activity (Forward, 1989a). These two species are obligate estuarine species that retain all of their larvae inside estuaries. These responses are interpreted as adaptations to avoid downward transport. Assuming a downward position in the water column by negative phototaxis triggered by a salinity decrease during ebb, the larvae will be exposed to lower current velocities during this phase of the tide. Conversely, an increase in swimming activity after a rise in salinity during flood will cause upward swimming by high halokinesis (see below) and a consequent enhanced upstream transport. The absolute threshold salinity diVerences that these larvae can detect vary between 0.1 and 0.3 ppt (Forward, 1989a). The influence of salinity on distribution of dispersive stages was investigated in penaeid species that use estuaries as nursery grounds (Mair et al., 1982). When oVered waters of diVerent salinity simultaneously, postlarvae of four penaeid species (Penaeus californiensis, P. brevirostris, P. vannamei, and P. stylirostris) selected lower salinity. Two of the species (P. californiensis, P. brevirostris) preferred lagoon water when given a choice between

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waters of estuarine and sea origin of the same salinity. The larvae did not consistently swim with or against currents, and salinity, water origin, light, and endogenous rhythms did not have a detectable eVect on direction of swimming. The selection of water of lower salinity or of water with a lagoon origin could be used to help concentrate larvae at the river mouth but could hardly be the main mechanism for upstream movement, for the postlarvae would not be able to swim against the current. In a field sampling programme, the authors detected large numbers of postlarvae at the surface during flood, possibly triggered by a reaction to the rising tide. This flood tide transport was identified as the mechanism responsible for upstream migration of the species investigated (Mair et al., 1982).

8.1.4. Temperature High temperatures have been shown to reverse the geotatic behaviour in Rhithropanopeus harrisii zoeae from a negative to a positive response (Ott and Forward, 1976). This behaviour could also aid in larval retention. In spring and summer, the usual pattern of change in estuaries during the tidal cycle is a temperature increase during ebb and a decrease during flood tide. A lower position in the water column caused by positive geotaxis during ebb tide would reduce seaward transport.

8.1.5. Current Swimming behaviour in flowing waters has been studied in penaeid, brachyuran, and astacid species. Penaeus duodarum postlarvae show positive rheotaxis and can swim against slow currents on the order of 5 cm s1 (Hughes, 1969). This behaviour would not result in unidirectional upstream transport in estuaries, because estuarine currents are normally of much higher intensity and also because a constant positive signal in rheotatic behaviour would result in position maintenance, and not in unidirectional transport, as the direction of the current changes with phase of the tide (Forward and Tankersley, 2001). However, a decrease in salinity from 33 to 30 ppt will make the postlarvae sink to the bottom. The larvae also avoid penetrating water of lesser salinity (Hughes, 1969). These behaviours together would promote upward transport toward estuarine nursery habitats: During ebb, the decrease in salinity would confine the postlarvae to the bottom, where they would be able to maintain position, whereas during flood they would swim in the water column and, being unable to withstand slow currents, be carried by the tide.

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Megalopae of Callinectes sapidus can orient in relation to currents and make headway into currents less than 4.8 cm s1 (Luckenbach and Orth, 1992), but this response appears to be variable, with only a small proportion of the animals acting in this way. At velocities higher than 6.3 cm s1, the larvae are transported downstream. Orientation of Homarus americanus larvae to currents is variable during the younger stages, but stage IV is positively rheotactic. Stage IV larvae are also the most powerful swimmers, being able to sustain swimming against currents of 9 cm s1 for periods of up to 30 min (Ennis, 1986). The ecological significance of positive rheotaxis is not clear, because these larvae occur in the surface layer of shelf waters, where they have no visual cues or fixed substrata to aid in the detection of current direction.

8.1.6. Turbulence Turbulence controls swimming in crab megalopae during selective tidal stream transport in estuaries. Welch et al. (1999) showed that increases of turbulent kinetic energy (TKE) in a flow tank triggered swimming of Callinectes sapidus megalopae. The number of megalopae swimming higher in the water increased with increases of TKE and decreased with a drop of TKE. Moreover, a threshold at 1.1 cm2 s2 was detected, above which increases in TKE did not increase swimming, because megalopae were maximally stimulated to swim. In a subsequent experiment, Welch and Forward (2001) investigated the simultaneous eVects of salinity and turbulence changes that megalopae undergo during ebb and flow tides in the estuary to elucidate further the behavioural reactions involved in selective tidal stream transport. The hypotheses tested were: that an increase in salinity during flood would evoke swimming from the bottom to the water column (Latz and Forward, 1977; Tankersley et al., 1995); that swimming was maintained during the whole duration of flood by high levels of turbulence; that megalopae would stop swimming and drop to the bottom during slack after high water because of decreased turbulence levels; and that during the ensuing ebb tide, the salinity drop would override the eVect of turbulence and megalopae would remain on the bottom. Callinectes sapidus megalopae behaved as predicted during the simulated flood. During ebb, a considerable proportion of the megalopae was swimming high in the flow tank. This response was considered to be an artifact of the flow tank, in which shear stress is concentrated in much smaller spatial dimensions relative to nature and would thus sweep more megalopae from the bottom than expected. Even so, the percentage of megalopae swimming during ebb was significantly smaller than during flood, supporting the proposed model.

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8.2. Endogenous rhythms 8.2.1. Tidal migrations As highlighted in Table 3, tidal rhythms in activity and vertical migration have been identified only in species that use estuaries during some part of their life cycles. Therefore, it is not surprising that endogenous rhythms with circatidal periodicity have been identified and studied only in such species. The examples cited herein concern obligate estuarine species, estuarine species that export their larvae to the shelf and shelf species that use estuaries as nursery grounds. For a review on tidal rhythms and the nature of their biological clocks, see Palmer (1995). Rhithropanopeus harrisii is the best known case of an obligate estuarine species. Cronin and Forward (1979) showed that laboratory-reared first zoeae of this species maintained in constant conditions displayed a vertical migration rhythm with a period of 24.6 h. The larvae ascended in the water column during the expected laboratory night and descended during the day. These larvae did not show any sign of a circatidal rhythm. However, field-caught zoeae had a circatidal rhythm of vertical migration with a 12.3-h period, during which the highest position in the water column was reached during flood. The rhythm expressed by zoeae collected during neap tides had a smaller amplitude than that exhibited by zoeae collected during spring tides, indicating a weaker synchronizing influence of neap tides. In a subsequent study (Cronin and Forward, 1983), first zoeae derived from estuaries with semidiurnal tides and with aperiodic tides were investigated for tidal endogenous rhythmicity. Larvae that were collected in estuaries with semidiurnal tides had clear circatidal rhythms of vertical migration. These rhythms had larger amplitudes than those exhibited by larvae that hatched in the laboratory from ovigerous females collected from estuaries with semidiurnal tides. In contrast, neither larvae collected in estuaries with aperiodic tides nor larvae hatched in the laboratory from ovigerous females collected in estuaries with aperiodic tides displayed any kind of rhythmicity. These results indicate that the eYciency of the synchronizing agents is higher when they operate on the larvae rather than on the embryos. Endogenous rhythmicity of swimming speed was investigated in the thirdstage zoeae of Rhithropanopeus harrisii collected in the field (DiBacco and Levin, 2000). The study found an endogenous rhythm in which the larvae swam faster during expected flood tides than during ebb. Because increase in swimming activity results in upward movement because of the basic orientation of brachyuran zoeae (Sulkin, 1984), the authors concluded that this behaviour could be the basis of the tidal rhythm in vertical migrations by zoeae of the species.

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The rhythms identified in the first zoea of R. harrisii have a clear ecological meaning in that, by assuming a higher position in the water column during flood, they will use the higher intensity currents closer to the surface to avoid downstream transport. Tankersley and Forward (1994) investigated the endogenous control of swimming activity in the megalopae of Callinectes sapidus and of Uca spp. Both are estuarine species that export their larvae to shelf waters. Megalopae of both genera are abundant in estuarine waters during night-time flood tides, and this pattern could be controlled by an endogenous clock. Furthermore, the megalopae of both genera appear to diVer in their behaviour in shelf waters. The C. sapidus megalopae are more abundant in the neuston during the night (Smyth, 1980; McConauhga, 1988), whereas Uca spp. larvae move deeper during development, with the megalopae very often being found close to the bottom in shelf and estuarine waters. The results showed that field-collected megalopae of the two genera had diVerent rhythmic endogenous behaviours (Tankersley and Forward, 1994). Callinectes sapidus had a circadian rhythm with a free-running period of 24.63 h. Megalopae were more active during expected daytime hours. In contrast, Uca spp. megalopae had a circatidal rhythm with a period of 12.28 h, where maximum activity occurred near the expected times of high tide regardless of the phase relationship of the expected day and tidal phases. The mismatch between the endogenous diel rhythm displayed by C. sapidus and their tide-synchronised occurrence in the field show that this internal rhythm cannot be involved in the control of flood-tide transport of C. sapidus megalopae in estuaries, giving further substance to the evidence that selective tidal stream transport in this species is controlled by environmental factors associated with the tidal cycle. In contrast, the rhythm displayed by Uca spp. may be involved in selective tidal stream transport. Peaks of activity in the laboratory occurred around expected high tide, whereas in the field maximum larval abundance was recorded during the last half of the flood (DeVries et al., 1994). The diVerences could be attributable to manipulation of the individuals in the laboratory experiments, or to some factor associated with the tidal cycle that modulates the behaviour. That environmental factors can modulate the rhythm is evidenced by the small numbers of Uca spp. megalopae that are found during daytime flood-tides in estuaries (Brookins and Epifanio, 1985; DeVries et al., 1994; Little and Epifanio, 1991), which is a consequence of the inhibition of swimming activity by high light levels (Forward and Rittschof, 1994; Tankersley et al., 1995). Biological rhythms of activity and vertical migration have been studied in the first zoea and in the megalopa of Carcinus maenas, which is also an estuarine species that exports larvae to the shelf. This species provides one of the most complete and informative case studies of the diVerent factors that synchronise endogenous vertical migration and of its ecological significance.

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Field-caught zoeae from Wales showed an endogenous rhythm with a period of approximately 12.4 h. Peaks of abundance in the top of the experimental chamber consistently occurred immediately after expected high tides. The rhythm had the same characteristics in larvae collected in diVerent stages of the neap–spring cycle and in locations with diVerent hydrological conditions (Zeng and Naylor, 1996a). In Wales, C. maenas occurs mainly on rocky shores, whereas in Portugal the largest populations occur inside estuaries. Nevertheless, the first zoeae hatched in the laboratory from Portuguese females also displayed an endogenous rhythm of circatidal periodicity (Ducheˆne and Queiroga, 2001). The persistence of this behaviour in crabs from these diVerent types of environment indicates that an endogenous rhythm resulting in a higher position in the water column may prevent stranding up the shore (Zeng and Naylor, 1996a), and also to enhance seaward dispersal (Queiroga et al., 1997). The factor that synchronises migration appears to be the hatching process itself (Zeng and Naylor, 1996d). In a study designed to test several factors as potential synchronisers, newly hatched larvae were kept in the laboratory for several months away from tidal influences. It was found that temperature variations, handling procedurtes, the starting times of experiments relative to the light cycle, and the starting times of experiments relative to hatching did not influence the phasing or the periodicity of the rhythm. In contrast, peaks of abundance of the larvae in the top of the chamber consistently occurred, across several experimental conditions, soon after every 12.4-h interval from the time of hatching, indicating that this factor is the synchronizing agent. The heritability of the circatidal migrations in C. maenas larvae from Wales was investigated in larvae that hatched in the laboratory from nonovigerous females that were brought to the laboratory and kept in constant conditions for periods of from several months to up to 1 year. The embryos produced by these females were never exposed to tidal influences, and yet the larvae displayed a remarkable endogenous rhythm of vertical migration that cycled with a period of 12.4 h. This result indicates that the periodicity of the rhythm is genetically inherited (Zeng and Naylor, 1996b). Rhythmicity of first zoeae of C. maenas from the Skagerrak, Sweden, was investigated by Queiroga et al. (2002). Tides in the Skagerrak are semidiurnal but, contrary to the situation in Wales and in Portugal, are of very small amplitude, with an average tidal range of 0.3 m. Moreover, variations of sea level caused by winds and atmospheric pressure are of larger amplitude than tidal variations. In such conditions, currents and changes of hydrostatic pressure associated with variations of sea water level are unpredictable, because they are not related to a cyclic environmental phenomenon, but rather to atmospheric pressure, which is an essentially stochastic factor. Therefore, the selective pressures that could lead to the development of such behaviours do not exist in this system, and vertical migration in phase with local tides

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would therefore be of little use for dispersal and recruitment. Not surprisingly, C. maenas first zoeae hatched from Swedish females did not demonstrate an endogenous rhythm of vertical migration of circatidal periodicity. A field sampling programme also failed to demonstrate any pattern related to the tide (Queiroga et al., 2002). The lack of tidal rhythmicity in the Carcinus maenas larvae from the microtidal environment of Sweden, as opposed to what was found in mesotidal areas of Portugal and the British Isles, raises the question of population isolation. If the behaviour is genetically inherited (Zeng and Naylor, 1996b), then one possible explanation for the lack of tidal rhythm in Swedish larvae is that populations from the Skagerrak and from the British Isles are reproductively isolated, or at least that larvae originated in tidal areas of the North Sea do not reach the Skagerrak (Queiroga et al., 2002). An alternative explanation is that the tidal clock is present within individual larvae but the lack of a natural synchronizing agent that would entrain the rhythm results in an ansynchronous behaviour exhibited by the ensemble of larvae that were collectively subjected to experimentation (Palmer, 1995). This is the only known case in which diVerent larval dispersal strategies were identified in the same species, and it suggests that this can occur in species with an extended geographical distribution, such as C. maenas. The endogenous rhythmicity of the megalopa of Careinus maenas was also studied by Zeng and Naylor (1996c). This study found that field-collected megalopae displayed an endogenous rhythm of vertical migration of circatidal periodicity, where the ascent phase of the migration occurred during the expected ebb phase of the tide. This is the same phasing exhibited by field-collected first zoeae, and it is at odds with the behaviour detected in field studies, either in Wales (Zeng and Naylor, 1996c) or in Portugal (Queiroga et al., 1994; Queiroga, 1998), which consistently showed this stage to be more abundant and to occur higher in the water column during flood. This mismatch between the phasing of the endogenous rhythm and the field distributions means that the endogenous behaviour cannot be involved in selective tidal stream transport (Queiroga, 1998). However, this behaviour could be useful in avoiding premature stranding of megalopae in shallow zones, allowing them to oscillate between the intertidal and nearshore waters until a suitable substratum is found (Zeng and Naylor, 1996c). The endogenous rhythmicity of penaeid larvae was studied by Hughes (1972). Postlarvae of Penaeus duodarum showed an endogenous rhythm of swimming activity, in which they were positively rheotatic (i.e., swimming against the current) during flood and negatively rheotatic (swimming with the current), during ebb. This mechanism would cause transport of postlarvae toward the sea, which would be in opposition to field evidence. Therefore, this internal biological rhythm cannot be directly responsible for

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the regulation of upstream transport by the species. Hughes suggested, following Creutzberg (1961), that this tide-related endogenous behaviour may help improve the eYcacy of the tide transport mechanism. If postlarvae are in the water column during ebb tide, swimming slowly in the downstream direction, they will not sense the end of ebb because they would essentially be confined to a water mass that is subjected to little change in physical properties. If a change from swimming with the current to swimming against the current occurs by endogenous control at the transition from ebb to flood phases, the chance that postlarvae will sense the salinity increase during flood is higher, and they will most readily increase activity and react by swimming closer to the surface, where currents are stronger (Hughes, 1969). No rhythm in swimming activity related to the day cycle was detected. Therefore, the high numbers of postlarvae found in the water column during the night should result from a direct reaction to light intensity. The comparative analysis of the endogenous rhythms shown by the first and last stages of these diVerent species allows some further considerations. Cronin and Forward (1983) could not demonstrate the synchroniser agent responsible for the entrainment of the circatidal rhythm of the first zoeae of Rhithropanopeus harrisii hatched in the laboratory. It may well be that this behaviour is genetically inherited (Zeng and Naylor, 1996b) and that the hatching process itself that synchronises the rhythm (Zeng and Naylor, 1996d), as in Carcinus maenas. The other interesting observation is that, in the above cases, all zoeae (first and third zoeae of Rhithropanopeus harrisii and first zoeae of Carcinus maenas) that displayed circatidal rhythmicity in laboratory-constant conditions had rhythms whose amplitude and phasing relative to the expected natural tidal cycle matched the behaviour of zoeae in nature. In contrast, a mismatch between the amplitude and phasing of the rhythm expressed in the laboratory and the behaviour in the field was detected in the megalopae of two of the three species that were investigated (in C. maenas and Callinectes sapidus, but not in Uca spp.). Zoeae are entirely planktonic forms that are transported within a parcel of water that is flowing up and down the estuary, but that may not change its physical–chemical properties with time. Even if they perform vertical migrations, zoeae will encounter similar conditions throughout the water column in many instances. The only way that these larvae may have both to choose the right phase of the tide for upward or downward migration and to react to a change in water direction might be by an endogenous rhythm synchronised with the tide. Megalopae, however, have to probe the bottom frequently in search of suitable settlement substrata. By doing so, they will be able to sense changes of physical variables associated with the tidal cycle, such as pressure, salinity, or temperature, and use them to control their behaviour in relation to tidal flow.

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8.2.2. Diel migrations There are very few cases in which an endogenous control of a diel rhythm of vertical migration has been demonstrated in decapod crustacean larvae, in agreement with the view that diel rhythms are usually controlled by a direct response to changing light levels (Forward, 1988). Callinectes sapidus megalopae have a circadian rhythm with a free-running period of 24.63 h, in which activity maxima coincide with expected daytime (Tankersley and Forward, 1994). This endogenous swimming rhythm was further investigated (Forward et al., 1997) to determine whether it occurred both in oVshoreand estuarine-collected megalopae, whether a circatidal rhythm could be entrained by salinity changes typical of estuarine systems, and whether aquatic vegetation could induce settlement and metamorphosis. Megalopae collected at sea and in several estuaries all had a circadian activity rhythm in which they swam during the expected day phase in the field. Moreover, salinity changes did not induce a circatidal rhythm, and submerged vegetation did not suppress the rhythm. Therefore, the authors concluded that C. sapidus megalopae enter estuaries with a solar day rhythm of activity and that this rhythm is not expressed under natural conditions because light inhibits swimming in estuarine waters (Forward and Rittschof, 1994).

9. NONRHYTHMIC VERTICAL MIGRATION Aperiodic changes of environmental variables in the marine environment are frequently associated with weather events. Examples are the salinity reduction during high river runoV periods, the increase in hydrostatic pressure that results from increased sea level driven by wind events, and the cooling of surface waters during the passage of cold fronts. The behavioural responses of the larvae to these unpredictable but recurrent events contribute to the variability of larvae in space and time and may aVect dispersal and recruitment. Vertical migration behaviour in response to aperiodic changes of salinity and temperature has been proposed as the mechanism of invasion of estuaries by postlarvae of the penaeid shrimp Penaeus aztecus in the Louisiana area of the Gulf of Mexico (Rogers et al., 1993). Tides in this area are diurnal and of small amplitude, and salinity and temperature changes in estuaries are more associated with the passage of cold fronts than with the periodic rise and fall of the tide. During the passage of cold fronts, cold northerly winds drive strong outflows of reduced salinity from the estuaries and lower the water temperature considerably. Salinity decrease evokes descent of penaeid postlarvae to the bottom (Hughes, 1969; Mair et al., 1982; Forbes and Benfield, 1986). This behaviour is enhanced by the drop in temperature,

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which has been shown to cause inactivity, descent onto the bottom, and burrowing in this species (Aldrich et al., 1968). After the passage of the cold front, the water level gradient relaxes and, as a consequence, the shallow waters are warmed by mixing with inner warmer and saltier shelf waters and by the return of warmer southerly winds. In these conditions, the postlarvae swim freely in the water column and can be carried into the estuary and upstream by the inflow current. This sequence of events, which can be further modulated by periodic vertical migration related to the diel cycle, results in pulses of recruitment to estuarine habitats of P. aztecus (Rogers et al., 1993).

10. MECHANISM FOR DEPTH REGULATION Sulkin (1984) proposed a model for depth regulation of crustacean larvae that is called the negative feedback model. According to this model, the vertical position of the negatively buoyant larva depends on its orientation to environmental cues and level of locomotory activity. The negative feedback mechanism maintains the larva at a particular depth. As the larva descends, the increase in pressure will induce an activity increase and negative geotaxis, which will cause an ascent. When the larva ascends, the pressure decrease induces a decreased locomotory activity, and the larva sinks passively. For this model to operate, it is necessary that the upward swimming and sinking velocities of larvae be fast enough that the rates of pressure change actually felt by the larvae are above their response thresholds. Forward and Wellins (1989) used this model with the crab Rhithropanopeus harrisii as the test species, therefore supporting the model. A useful model for depth regulation should also consider the vertical distance the larvae move before the corrective responses occur. A larva at a particular depth ascends or descends a certain distance before the corrective behavioural response reverses the direction of movement. These upper and lower depth limits form a window, within which depth is regulated (Forward, 1989b). Forward and Wellins (1989) and Forward (1989b) showed that the limits and symmetry of this window depend on the level of light adaptation. In darkness or with low light levels, the distance R. harrisii zoeae move up before a corrective response occurs is larger than the distance zoeae move down before responding. The reverse occurs with high light levels. This new model was termed the light-dependent negative feedback model for depth regulation (Forward, 1989b; Figure 10). This model does not require that depth be maintained at a particular absolute value. Studies on the pressure responses of decapod larvae never demonstrated an ability of the larvae to detect absolute pressure levels (e.g., Rice, 1964; Knight-Jones and Morgan, 1966) but, rather, that they respond to rates of change of this variable.

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Figure 10 Light-dependent negative feedback model for depth regulation of decapod crustacean larvae. The upper and lower depth limits that a larva reaches during the course of vertical movements, before corrective behavioural responses reverse the direction of movement, form a window within which depth is regulated. The limits of this window (represented by the box) are asymmetrical and depend on the level of light adaptation. In darkness or with low light levels (a), the distance a larva moves up before a corrective response is larger than the distance it moves down before responding, and the larva ascends in the water column. The reverse occurs with high light levels (b).

Because larvae undergo diel and tidal vertical migrations in response to internal clocks and to environmental variables, these factors can override depth regulation and lead to vertical migration. Therefore this model applies to moments when larvae remain at relatively constant depths, such as during the day or night (Forward, 1989b).

11. MODIFIERS OF VERTICAL MIGRATION PATTERN: TEMPERATURE, SALINITY, AND FOOD Compared to other invertebrate larvae, decapod larvae are relatively strong swimmers. Their vertical swimming speeds are of the order of centimetres per second, which means that they are capable of swimming through a water column of some tens of metres in 2–3 h (Mileikovsky, 1973; Chia et al., 1984). An important question concerning the vertical movements of these larvae is whether thermohaline stratification can constitute an impediment

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to vertical movements, thereby aVecting the vertical position of the larvae. This question has been addressed rarely. The few observations available indicate that naturally occurring thermal stratification does not seem to constitute a physical barrier to vertical migration. In laboratory experiments, first zoeae of Callinectes sapidus (McConnaughey and Sulkin, 1984), Geryon quinquedens (Kelly et al., 1982), and Eurypanopeus depressus (Sulkin et al., 1983) were able to swim upward through thermoclines of 10 8C established in test columns 0.45 m high in less than 30 min. In these columns, the temperature change occurred over a distance of only 0.10 m. These conditions seldom, if ever, occur in nature, even in highly stratified estuarine systems. Temperature diVerences over 10 8C did significantly reduce the vertical movements of C. sapidus in these experiments (McConnaughey and Sulkin, 1984). Crab megalopae seem also capable of moving over important temperature diVerences. Jamieson and Phillips (1993) report daily migrations of Cancer magister megalopae over several tens of metres in the Strait of Georgia, Vancouver Island, that expose them to temperatures above 16 8C at surface and below 10 8C in deeper strata. A diVerent aspect of migration through thermoclines was investigated in stage IV larvae of the lobster Homarus americanus (Boudreau et al., 1992). Here the interest was in seeing whether competent larvae could swim down through sharp decreases in temperature and settle on the bottom. In this case, the gradients were in the range of 58–10 8C and were compressed over vertical distances of 0.20 m. The results showed that gradients of 5 8C could significantly prevent the larvae from descending to the bottom of the experimental column, but again the experimental conditions did not realistically simulate natural conditions. However, decapod larvae generally seem to perceive and react to even small decreases in salinity, consistent with their sensitivity to changes in this parameter (Tankersley et al., 1995). The usual reaction seems to be the avoidance of reduced salinities at the surface. In a controlled experiment, Hughes (1969) concluded that Penaeus duodarum postlarvae avoid penetrating an upper layer of reduced salinity when the diVerence is as small as 1 ppt. In another laboratory experiment, Roberts (1971) detected aggregation of first zoeae of Pagurus longicarpus at the discontinuity when surface salinity was lower than bottom salinity by 5 or 10 ppt, and found that diVerences as large as 15 ppt would completely prevent the larvae from crossing the boundary. A sensitivity to salinity reduction of surface waters seems also to be present in the megalopa of Carcinus maenas from the Ria de Aveiro, Portugal, which were absent from surface waters when their salinity exceeded that of the bottom water by about 1.5 ppt (Queiroga, 1998). From the evidence described above, it appears that thermoclines of the magnitude usually found in nature do not prevent vertical migration of decapod larvae, even in the earlier stages (which contain the weaker

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swimmers). The ability to swim across seasonal thermoclines may have considerable importance for the horizontal dispersal of larvae in shelf systems subjected to tidal currents. As highlighted by Hill (1998; see Section 3), the phase and the velocity of the tidal currents may be diVerent above and below the thermocline, and a larva undergoing diel migration across the thermal boundary may be subjected to a completely diVerent horizontal trajectory from that of a larva that is not migrating, which may result in considerable horizontal unidirectional displacement for the migrating larva. These aspects have never been directly investigated, but studies on zooplankton behaviour and distribution, coupled with physical modeling, show that such mechanisms may be responsible for the advection of zooplankton on shelf waters (Mackas, 1992; Mackas et al., 1997; Smith et al., 2001). Haloclines do aVect the ability of decapod larvae to perform vertical migrations. The avoidance of low-salinity surface water is useful when maintaining competent stages close to the bottom during flood, in a layer of water with stronger upstream velocity, as they are entering stratified estuaries. There are several records indicating that zooplankton in general seem to modify their pattern of diel vertical migration in the sea in the presence of food aggregations (Scrope-Howe and Jones, 1986; Harris, 1988; Atkinson et al., 1992; Falkenhaug et al., 1997). This aspect has been poorly studied in decapod larvae. The only available observations seem to be those by Lindley et al., (1994) on the Irish Sea and the North Sea. These authors have found that larvae from a number of species (Pandalus montagui, Pagurus bernhardus, and Nephrops norvegicus) had a vertical migration pattern that deviated from the usual norm of nocturnal migration. Those larvae showed restricted vertical movements and tended to remain close to high concentrations of chlorophyll a that were usually found near the thermocline. In one case (N. norvegicus), the larvae migrated at the level of the thermocline. Such a pattern of migration in a stratified system may have the consequences described above.

12. VERTICAL AND HORIZONTAL SWIMMING VELOCITIES The literature on swimming velocities of invertebrate larvae, including decapods, has been reviewed by Mileikovsky (1973) and by Chia et al. (1984). The studies on the swimming velocities of decapod larvae include frequent observations on upward active swimming, whereas downward velocities are usually measured during passive sinking of anesthetized larvae. Usually, larvae are placed inside small test chambers and stimulated with pressure changes or with light to evoke a swimming response. Mileikovsky and Chia et al.,’s reviews, and other observations not included there (e.g., Sulkin et al., 1979; Calinski and Lyons, 1983; Cobb et al., 1989; Forward and Wellins,

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1989; Forward et al., 1989), indicate that the vertical velocities of larvae belonging to a wide range of taxonomic groups fall within 0.2 to 8.3 cm s1, with most observations falling in the range of 0.5–2 cm s1. A larva traveling at a velocity of 0.5 cm s1 is able to move a vertical distance of 10 m in about 0.5 h and a vertical distance of 100 m in 5.5 h. It would appear that these times are short enough to allow the larvae to move over the entire water column of most estuaries, and over a considerable portion of the water column of the continental shelf, during the course of a tide and a day cycle, respectively. It must be stated that, because of practical diYculties, the demonstration that the larvae can maintain these velocities over extended periods of time and over the appropriate spatial scales is problematic. Swimming activities of the same batch of unfed crab zoeae have been repeatedly measured over periods of several days without signs of decreased velocities (Sulkin et al., 1979; Forward and Cronin, 1980), indicating that these larvae do appear to sustain these velocities for prolonged periods, but the experimental columns were only some tens of centimetres high, and the larvae would reach the surface or the bottom very quickly. However, the reported velocity values might be underestimated because of wall eVects. As highlighted by Chia et al. (1984), the presence of a surface exerts a drag on small animals moving in a fluid, that can be felt over considerable distances. Although decapod larvae are relatively large compared to other invertebrate larvae and the drag eVect decreases with increased size, many of the observations were made in small containers, and none of the studies have taken this error into account. Another diYculty in extrapolating laboratory observations to behaviour in nature concerns the stimuli that are used to evoke the swimming behaviour—usually directional light and step pressure changes—none of which occur in natural waters. The only available measurements of vertical displacement velocities of decapod larvae in the field seem to be those made on phyllosomae of Panulirus longipes by Rimmer and Phillips (1979), from the velocities of ascent during sunset and descent during sunrise of the modal depth of the larvae. The velocities ranged from 0.38 cm s1 in early stages (phyllosoma I–III) to 0.54 cm s1 in late stages (phyllosoma VII–IX), which are within the range of velocities measured in the laboratory. Data on horizontal velocity are much rarer but point to a similar order of magnitude as for vertical swimming (Chia et al., 1984). These values are one to two orders of magnitude lower than instantaneous and, in some cases, net velocities in marine systems (Figure 11). The pueruli of the Panulira and the stage IV larva of the Astacidae constitute exceptions among decapod larvae, being powerful swimmers that are believed to use directional swimming for periods of days to weeks from oVshore waters into coastal habitats (Serfling and Ford, 1975; Cobb et al., 1997; Phillips and Pearce, 1997). Reported

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Figure 11 Horizontal velocities of several types of currents in marine and estuarine environments, and swimming velocities of marine larvae.

horizontal swimming speeds are 7.7–10 cm s1 in the puerulus of Panulirus argus and average 18 cm s1 in stage IV of Homarus americanus.

13. MEASUREMENTS OF HORIZONTAL TRANSPORT The previous sections showed that most decapod larvae undergo extensive dispersal from the source areas. Although circumstantial evidence shows that local recruitment in populations of marine species with extended larval periods can be of greater importance than previously recognized (Warner and Cowen, 2001; Kingsford et al., 2002; Swearer et al., 2002; Thorrold et al., 2002), and isolated examples of local recruitment do exist for decapod species (Knowlton and Keller, 1986), dispersal away from the parental location seems to be the general rule in this group. The probabilities of larval death resulting from inability to find appropriate settlement habitats and of exchange of individuals among local populations in decapods appear therefore to be high, which should have important consequences for population dynamics,

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community structure, and the evolution of life histories (Gaines and LaVerty, 1995; Caley et al., 1996; Orensanz and Jamieson, 1998). A recent review of literature has found a significant positive relationship between the length of the larval period and dispersal distance in a sample of marine invertebrates that included decapods (Shanks et al., 2003). The means to establish trajectories of larvae in the field include direct observation of individual larvae, observation of patches of larvae resulting from mass spawning, assessment of distribution relative to known sources, observation of the progressive spread of introduced species, use of techniques for following water masses or larvae, hydrodynamical modelling and inferences from physical and behavioural mechanisms, and genetics (Levin, 1990; Shanks et al., 2003). However, except for the estuarine environment where, because of well-defined terrestrial borders, fluxes of larvae have been measured (Christy and Stancyk, 1982; Dittel et al., 1991; Pereira et al., 2000), there are no available data on the actual rates at which decapod larvae are transported, and the fraction of larvae exchanged between local populations is unknown.

13.1. Tagging The best method to follow individual larvae from their source to the settlement habitat and to measure mortality during planktonic development would be to mark and recapture the larvae. The methods of larval tagging, including artificial and natural tags, and the diYculties in applying these techniques, have been discussed in several papers (Levin, 1990; Levin et al., 1993; Anastasia et al., 1998; DiBacco and Levin, 2000; Thorrold et al., 2002). One promising technique is to tag the larvae with elements that occur at very low levels in the environment but that are accumulated in the larvae through their food or transmitted from the mother. Tests using selenium as a tracer are very promising. Laboratory experiments with larvae of several crab species show that selenium is rapidly taken up from their food, is assimilated at eYciencies above 60%, is consistently retained at concentrations above background levels for weeks, and does not consistently aVect larval survival. However, the probability of recapture of larvae is very low because of mortality, diVusion, and multidirectional transport, so this method requires that hundreds of thousands or millions of larvae be marked (Anastasia et al., 1998). Another promising approach is elemental fingerprinting. This technique measures the elemental composition of larvae in naturally occurring trace elements, which is related to the concentrations of these elements in the environments in which the larvae hatched and developed. This method compares the concentrations of trace elements found in wild larvae to those

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determined in reference larvae of known origin. Because all larvae from a particular place are naturally tagged, every larva collected potentially constitutes a recapture. DiBacco and Levin (2000) report results of a study that applied elemental fingerprinting to first zoeae of the crab Pachygrapsus crassipes. The study was able to discriminate between first zoeae that originated in San Diego Bay (California) and those from other lagoonal habitats and open shores in the region. Used in conjunction with synoptical field sampling, elemental fingerprinting allowed the quantification of the proportion of P. crassipes zoea I from diVerent origins that was exchanged across the lagoon inlet (DiBacco and Levin, 2000; DiBacco and Chadwick, 2001). Because the trace-elemental signals are likely to change with feeding and moulting, it is not yet possible to generalize the use of elemental fingerprinting to track larval trajectories from hatching to settlement until the uptake and retention of the elements used to identify origins are evaluated (DiBacco and Levin, 2000).

13.2. Larval velocity In estuaries in which the flow is essentially bidirectional because of the action of tides, it is possible to calculate transport rates from carefully planned simultaneous observations of current velocity and larval concentration. Queiroga et al. (1997) and Queiroga (1998) used the concept of larval velocity to determine the influence of vertical migration on horizontal transport of first zoea and megalopae of Carcinus maenas in the Ria de Aveiro, Portugal. The studies involved hourly sampling at a fixed station with a pump, at several levels along the water column during extended periods of time. The influence of the vertical position of the larvae on their net tidal transport was assessed by first calculating the vertically integrated instantaneous current velocity ut: n X

ut ¼

uzt  DDzt

z1

n X

; DDzt

z1

where u is the longitudinal component of velocity (positive during Pebb and negative during flood), DD is the height of each stratum, and nz1 DDzt equals Zt, the instantaneous height of the water column. Subsequently, a vertically integrated instantaneous larval velocity, ult, was calculated and was designated as the instantaneous larval velocity:

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HORIZONTAL TRANSPORT OF DECAPOD LARVAE n X

ult ¼

uzt  DDzt  Czt

z¼1

n X

; DDzt  Czt

z¼1

where the symbols have the meanings explained above. Note that if the larvae are uniformly distributed throughout the water column, the Czt terms in the above equation are all equal and cancel out to produce a value that is equal to ut. The larvae are thus transported at a velocity that equals the vertically integrated current velocity. If the larvae do not distribute evenly with depth, then ult does not equal ut (Figure 12). Because tidal current intensity usually increases with increasing distance from the bottom because of a decrease in bottom friction, changes in vertical position result in instantaneous transport velocities of the larvae that diVer from the depth-integrated current velocity.

Figure 12 Schematic representation of the influence of vertical distribution on larval velocity for a typical situation in which current velocity decreases with depth. Arrows represent current velocity, larval flux, or larval velocity; horizontal bars represent concentration of larvae. The number of larvae is the same in both panels (i.e., the ‘‘sum’’ of the bars is the same). In (a) the larvae are uniformly distributed with depth, and depth-integrated current velocity equals depth-integrated larval velocity. In (b) the same number of larvae are concentrated close to the surface, where the current is stronger. Therefore, depth-integrated current velocity is smaller than depth-integrated larval velocity. If the larvae were concentrated close to the bottom, current velocity would be greater than larval velocity.

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The diVerence between water velocity and larval velocity measures how much the larvae are able to enhance or counteract average downstream transport along the axis of the estuary. The calculations showed that the velocity diVerence averaged over the tidal cycle was positive for the first zoeae, indicating that vertical migration enhanced seaward transport, and that it was negative for the megalopa, showing it moved upstream against the net flux.

ACKNOWLEDGEMENTS We thank several colleagues and friends, as well as several institutions, for their contribution to this work. Maria Joa˜o Almeida (Universidade de Aveiro, Portugal) and Nacho Gonzalez (Centro Andaluz de Ciencia y Tecnologı´a, Marinas, Spain) compiled the data and prepared the figure on the phase relationships of the tidal and the diel cycles. Per Moksnes (Kristineberg Marine Research Station, Sweden) and Augusto Flores (Universidade Estadual de Sa˜o Paulo, Brazil) contributed suggestions that helped shape several aspects of the text. Antonina dos Santos (Instituto Nacional de Investigac,a˜o das Pescas e do Mar, Portugal) prepared the figure illustrating some of the larval stages of decapod crustaceans. The inspiration and partial financial support for this review came from the European concerted action EDFAM—European Decapod Fisheries: Assessment and Management Options—which was funded by the European Community under the Fifth Framework Programme (contract QLK5-CT1999-01272). The Fundac,a˜o para a Cieˆncia e Tecnologia, Portugal, supported a stay of Henrique Queiroga at the Skidaway Institute of Oceanography with a sabbatical grant (grant SFRH/BSAB/294/2002). The main part of the text was written at Skidaway, with the help of the resources and support staV available at their excellent library.

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Zeng, C. and Naylor, E. (1996a). Endogenous tidal rhythms of vertical migration in field collected zoea-1 larvae of the shore crab Carcinus maenas: Implications for ebb tide oVshore dispersal. Marine Ecology Progress Series 132, 71–82. Zeng, C. and Naylor, E. (1996b). Heritability of circatidal vertical migration rhythms in zoea larvae of the crab Carcinus maenas (L.). Journal of Experimental Marine Biology and Ecology 202, 239–257. Zeng, C. and Naylor, E. (1996c). Occurrence in coastal waters and endogenous tidal swimming rhythms of late megalopae of the shore crab Carcinus maenas: Implications for onshore recruitment. Marine Ecology Progress Series 136, 69–79. Zeng, C. and Naylor, E. (1996d). Synchronization of endogenous tidal vertical migration rhythms in laboratory-hatched larvae of the crab Carcinus maenas. Journal of Experimental Marine Biology and Ecology 198, 269–289. Zeng, C., Abello´, P. and Naylor, E. (1997). Endogenous tidal and semilunar moulting rhythms in early juvenile shore crabs Carcinus maenas: Adaptations to a high intertidal habitat. Marine Biology 128, 299–305.

Marine Biofouling on Fish Farms and Its Remediation R. A. Braithwaite*,{ and L. A. McEvoy{

*School of Ocean Sciences, University of North Wales Bangor, Menai Bridge, Gwynedd, LL59 5AB, UK E-mail: [email protected] { North Atlantic Fisheries College, Port Arthur, Scalloway, Shetland, ZE1 0UN,UK

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Nature and Extent of Problem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Detrimental eVects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Beneficial eVects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Economic consequences . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. The Fouling Community of Fish-Cage Netting. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Mediation by physical, chemical, and biological factors . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Community development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Fouling taxa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Antifouling Technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Toxic antifouling paints and materials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Legislation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Nontoxic ‘‘alternative’’ antifoulants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4. Biological control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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The fish farming industry suVers significantly from the eVects of biofouling. The fouling of cages and netting, which is costly to remove, is detrimental to fish health and yield and can cause equipment failure. With rapid expansion of

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the aquaculture industry, coupled with the tightening of legislation on the use of antifouling biocides, the problems of fish farm biofouling are increasing. The nature of the biological communities that develop on fish farm equipment and the antifouling practices that can be employed to reduce it are described here. Particular emphasis is placed on antifouling legislature and the future needs of the industry. The biological communities that develop on fish cages and netting are distinctive, in comparison to those that foul ships. Temperate species of particular importance, because of their cosmopolitan distribution and opportunistic nature, include the blue mussel Mytilus edulis and the ascidian Ciona intestinalis. Antifouling practices include predominantly the use of copper-based antifoulant coatings, in combination with practical fish husbandry and site management practices. The antifouling solutions presently available are not ideal, and it is widely accepted that there is an urgent need for research into combatant technologies. Such alternatives include the adoption of ‘‘foulrelease’’ technologies and ‘‘biological control’’ through the use of polyculture systems. However, none of these have, as yet, been proven satisfactory. In view of current legislative trends and the possible future ‘‘phasing out’’ of available antifouling materials, there is a need to find alternative strategies.

1. INTRODUCTION Marine fouling is a worldwide phenomenon that has always plagued mariners, with written records extending back to the fifth century B.C. (Woods Hole Oceanographic Institution [WHOI], 1952). It occurs in all oceans and at all depths; however, its character and magnitude vary markedly with physical and biological factors (Benson et al., 1973). There are various definitions (Evans and Christie, 1970; Evans, 1981; Callow, 1996; Clare, 1996; Mckenzie and Grigolava, 1996; de Sousa et al., 1998; Tan et al., 2002), but for the context of this review, biofouling can be defined as ‘‘the growth of unwanted organisms on the surfaces of man-made structures immersed in the sea, which has economic consequences’’ (WHOI, 1952). A wide range of structures and materials can be aVected (Benson et al., 1973; Evans, 1981). These may be fixed or floating, intertidal or subtidal, and they can be located in coastal waters or oVshore (Fletcher, 1988). They include oil and gas installations, power plant cooling systems, wharves, boats’ hulls, antifouling paints, fish cages and netting, metal, wood, plastic, and rope (Evans and Clarkson, 1993; Berk et al., 2001; Stachowitsch et al., 2002). In contrast to activities such as shipping, for which reports of associated fouling extend back for thousands of years, intensive fish farming is a relatively young industry. Aquaculture production of fish steadily increased

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after the end of World War II, and in line with decreasing wild fish capture, cage culture has greatly intensified since the 1960s (Beveridge, 1996). For example, earnings from the tuna farming industry within parts of South Australia increased 10-fold during the 8 years before 1998, from $4 million to $40 million annually (Cronin et al., 1999). Aquaculture is one of the fastest growing sectors of the world food economy, and in 2000, production, which was dominated by fish, was 45.7 million tonnes by weight and $56.5 billion by value (Figure 1). Its contribution to global supplies increased from 3.9% in 1970 to 27.3% in 2000, which is an average compounded rate of 9.2% per year (Food and Agriculture Organisation of the United Nations, 2002). It is estimated that fish farming production may actually outstrip capture fisheries production within the first quarter of this century (Beveridge, 1996). As a consequence, fish farm fouling is a growing, global problem. The problems of the fouling of modern synthetic materials used in mariculture are little known or, at least, are rarely documented (Cheah and Chua, 1979). Research into marine fouling of fish cage netting was initiated over 30 years ago (Milne, 1970), yet data are still relatively scant. Much of the information that is available about fouling associated with the industry is anecdotal or of limited value. This is in great contrast to the problems of ship fouling, which have been studied in great depth over many years (WHOI, 1952). Quantitative studies of net fouling are sparse (Cronin et al., 1999). This is particularly true of studies undertaken within the freshwater environment (Dubost et al., 1996) and of Western aquaculture. Developing and ‘‘low-income food-deficit countries’’ (LIFDCs) have a long history of

Figure 1 Trend of world aquaculture industry over the last 50 years: solid line represents production; broken line represents value (data provided by the Food and Agricultural Organisation of the United Nations).

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aquaculture and currently dominate global production. As a consequence, most studies have been undertaken in Asia, particularly in China. Unfortunately, however, reports from such investigations are not often widely available. This review highlights the unique nature and extent of the problem of fouling within the aquaculture industry. Details on antifouling practices, both historical and contemporary, are discussed, and the future of today’s technologies is considered in relation to the industry’s evolving needs and legislation. Consideration has been given to the culture of shellfish as well as finfish and, for reasons of brevity, when these are discussed collectively, the term ‘‘fish’’ is used. Fouling is also a major problem associated with the macroalgal mariculture industry; for example, in Gracilaria cultivation (Fletcher, 1995). Therefore, mention is also given to the problems of this where appropriate. Of note, the macroalgal genus Enteromorpha has now been subsumed by the genus Ulva (Hayden et al., 2003); however, the former name is used throughout, where appropriate, to prevent confusion. With respect to shellfish, only the fouling of associated mariculture equipment is discussed, and not that of direct shell fouling, although it also is a major problem for the industry (Enright, 1993; Lodeiros and Himmelman, 1996), partly because of detrimental ecological repercussions that can result from species introductions through shipment of fouled produce (Reise et al., 1999) and the increased energy costs to fouled organisms (Donovan et al., 2003). The problems of epiphytism in macroalgal cultivation have been discussed elsewhere (Fletcher, 1995).

2. NATURE AND EXTENT OF PROBLEM It has been stated that biofouling presents a serious problem to mariculture worldwide (Hodson et al., 1997, 2000), as documented in Table 1. Nets can visibly foul within 1–2 weeks of immersion (Cheah and Chua, 1979), and fouling intensities of, for example, 1.4 kg m2 have been recorded following only 21 days of immersion (Dubost et al., 1996). Measurements of 2.2 kg m2 (Cronin et al., 1999), 4.5 kg m2 (Lee et al., 1985), and 7.8 kg m2 (Hodson et al., 2000) have also been reported, as have dry mass measurements of 0.82 kg m2 (Lodeiros and Himmelman, 2000). The open area of a mesh, immersed for only 7 days in Tasmania, decreased by 37% as a result of fouling (Hodson et al., 1995). It has been reported that mesh can be blocked by up to 50% as a result of mussel growth (Milne, 1970). Increases in weight can be 200-fold (Milne, 1970; Beveridge, 1996), and it has been calculated that a net being monitored at Port Lincoln, South Australia, had developed

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Table 1 List of publications containing reports of biofouling recorded from marine finfish aquaculture equipment based at sea, unless otherwise indicated Country

Author(s)

n/aa Australia

Huguenin and Huguenin (1982)b Hodson and Burke (1994); Hodson et al. (1995, 1997, 2000); Cronin et al. (1999); Ingram et al. (2000)b; Tan et al. (2002); Douglas-Helders et al. (2003) Enright et al. (1983, 1993)c; Cote et al. (1993, 1994)c; Enright (1993); Claereboudt et al. (1994)c Romo et al. (2001)d Dubost et al. (1996)b; Nehr et al. (1996); Gonzalez (1998)e Deady et al. (1995) Chua and Teng (1977); Cheah and Chua (1979) Kvenseth (1996); Solberg et al. (2002); Kvenseth and Andreassen (2003) Hasse (1974)c His et al. (1996)c Lee et al. (1985) Milne (1970, 1975a,b); Ross et al. (2002)c Hidu et al. (1981); Ahlgren (1998)c; Parsons et al. (2002)c Lodeiros and Himmelman (1996, 2000)c

Canada Chile France Ireland Malaysia Norway Palau Scotland Singapore UK USA Venezuela a

Concerned with several countries. Recorded in a freshwater/low salinity environment. c Associated with shellfish farming. d Associated with seaweed farming. e Recorded from a land-based system. b

a fouling community weighing 6.5 tonnes (Cronin et al., 1999). Similarly, biomass weights of up to 18 tonnes have been recorded fouling a single salmon net in Scotland (D. Goodlad, pers. comm.).

2.1. Detrimental effects Hydrodynamic forces on a fouled net, which can reduce cage volume, constrict net openings (Phillippi et al., 2001), and stress moorings, have been calculated at up to 12.5 times that of a clean net (Milne, 1970). Concurrently, the weight of cages can severely increase (Milne, 1970), causing further structural stress as well as a reduction in cage buoyancy and increased net deformation (Milne, 1970; Beveridge, 1996; Phillippi et al., 2001). Fouling can also cause physical damage to the nets themselves (Beveridge, 1996). Fouling eVectively decreases the specified mesh size by increasing net surface area (Beveridge, 1996), which causes disruption to water flow (Enright, 1993; Lai et al., 1993; Lodeiros and Himmelman, 1996;

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Eckman et al., 2001). As a result, nutrient exchange and waste removal are restricted (Howard and Kingwell, 1975; Cote et al., 1993; Ahlgren, 1998; Eckman et al., 2001), which aVects not only the health of stock but also the surrounding environment; for example, by causing localized eutrophication (Folke et al., 1994). Similarly, supplies of oxygen may be disrupted (Lovegrove, 1979b; Cronin et al., 1999), and anoxic conditions can develop (Lai et al., 1993); this is particularly pertinent in temperate regions during the summer, when the period of most aggressive fouling coincides with high water temperatures that further reduce oxygen levels. In 2002, Atlantic Salmon of Maine, a subsidiary of Fjord Seafood, lost 4,500 fish at their Harbor Scrag Farm, at a cost of $40,000, because of a lack of dissolved oxygen (DO) as a result of net fouling (J. Lewis, pers. comm.). Decreases in DO levels can be further compounded by the respiratory activity of fouling organisms themselves (Cronin et al., 1999). The complex fouling communities that can develop may indirectly cause further stress to stock by aVording habitat to a range of ‘‘harmful’’ organisms. The fouling community may harbour disease, such as ‘‘netpen liver disease’’ (Andersen et al., 1993) or amoebic gill disease (Tan et al., 2002), and parasites; for example, the nematode Hysterothylacium aduncum (Gonzalez, 1998) and the sea louse Lepeophtheirus salmonis (Huse et al., 1990). Worries exist over the potential for the latter species to transfer to wild fish (Beveridge, 1996) in addition to concerns about its eVects on stock. It has also been reported that fouled shellfish cages can harbour potential predators such as echinoderms and decapod crustacea (Ross et al., 2002). Concerns have been raised over the potential for fouling to enhance the incidence of phytoplankton species that are responsible for causing ‘‘shellfish poisoning’’ (Ross et al., 2002). Conversely, others have suggested that the availability of phytoplankton, on which most shellfish feed, may be reduced as a consequence of biofouling (Enright, 1993; Lodeiros and Himmelman, 1996). Fouling can also create health and safety concerns; for example, fouling increases the weight and slipperiness of equipment that is handled and, in the tropics, the frequency of contact with stinging and cutting organisms is raised (Hasse, 1974). Indirect eVects of biofouling development on fish cages and netting include remedial costs; for example, through frequent onshore cleaning and repairs (Hodson et al., 1997), which, in turn, have detrimental environmental implications and can further stress stock through increased disturbance (Paclibare et al., 1994). Hosing, which may be a significant point source input of ship antifouling biocides into the environment (Thomas et al., 2002), along with other remedial measures (Strandenes, 2000), is also a common net cleaning practice (Lee et al., 1985) and is often carried out in situ. Nets can require lifting and cleaning up to every 5–8 days during summer periods. These processes incur great expense (Paclibare et al., 1994; Hodson et al., 1997),

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partly because of the need for specialist staV to carry out highly labourintensive work (Blair et al., 1982; Li, 1994) that can be very time-consuming (Lee et al., 1985) and costly (Dubost et al., 1996). However, nets are more commonly changed every few months (Beveridge, 1996), and sometimes as often as every month (Lai et al., 1993). Fouling, as well as its removal, can increase stock stress and, possibly, associated mortalities (Ahlgren, 1998). For example, suspension-feeding fouling organisms can compete with shellfish, such as scallops, for food resources (Cote et al., 1993; Claereboudt et al., 1994; Lodeiros and Himmelman, 1996). The increase in disease and parasites resulting from the development of fouling adds to concerns over the use of combatant chemicals, such as cypermethrin, azamethiphos, and emamectin benzoate, which are used for their treatment but have, potentially, detrimental environmental eVects (Burridge et al., 1999, 2000a,b; Ernst et al., 2001; Waddy et al., 2002). However, these concerns appear smaller than general perceptions may suggest, as, for example, Marine Harvest Scotland Limited (formerly Marine Harvest McConnell), Scotland’s largest salmon farming operator, did not use any antibiotics in 2002 and made only one treatment the previous year (S. Bracken, pers. comm.). Fouling can also wound finfish, resulting in bacterial and viral infections (Lai et al., 1993). This would, presumably, be most prevalent in bottom-dwelling finfish stock that are in contact with the hard fouling that typically develops below the photic zone; for example, halibut and turbot. Within enclosed cages, resuspension of fouling material following cleaning and general husbandry practices can also add to the problems of fouling (Nehr et al., 1996).

2.2. Beneficial effects There are several positive attributes of biofouling that benefit aquaculturists. Most notable is the manipulation of fouling for seeding mussel lines (Mallet and Carver, 1991), which is a method of cultivation that relies exclusively on natural spatfall. Fouling of nets by mussels can reduce the risks posed to salmon by the bacterial pathogen Renibacterium salmoninarum, which can cause kidney disease (Paclibare et al., 1994). Fouling may also reduce the eVects of abrasion on caged fish (Beveridge, 1996), assuming that it was soft fouling. Periphyton fouling development on nets has been investigated as a marginal energy source for the culture of tilapia species (Norberg, 1999), and it has been suggested that fouling can be exploited as an integral component of the sustainable polyculture systems advocated for tilapia cultivation (Newkirk, 1996). Fouling invertebrates may provide supplemental foods for salmon, thereby increasing growth (Moring and Moring, 1975), and it has been stated that fouling debris can provide a food source for the

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cultivation of, for example, commercially important detritivores (Ahlgren, 1998). Similarly, in Canada, fouling by potentially valuable periwinkles and crabs has been encouraged (Hidu et al., 1981; Enright et al., 1983, 1993). It has even been suggested that stimulating biofouling development may indirectly aVord shelter for caged fish from predatory birds (Norberg, 1999), which can be a significant problem (Ingram et al., 2000). Fouling may also decrease flow rates that would otherwise reduce scallop growth (Cote et al., 1993), although controlling these rates would usually be the remit of site selection. Macroalgal fouling in land-based aquaculture systems can also help to increase DO concentrations, while reducing ammonium levels (Newkirk, 1996; Tudor, 1999). It is also possible that increased levels of nutrients, as by-products of invertebrate fouling, may stimulate both phytoplankton production, which in turn benefits filter-feeding aquaculture species such as scallops (Ross et al., 2002), and the aquaculture of seaweeds (Newkirk, 1996).

2.3. Economic consequences It is widely accepted that fouling in the aquaculture industry is an expensive problem (Enright, 1993; Hodson et al., 1997). For example, more than half of the labour time associated with the culture of oysters in Nova Scotia, Canada, is concerned with the removal of fouling (Enright, 1993), and the associated costs account for approximately 20% of the market price (Enright et al., 1993). Significant sums of time and money are clearly spent trying to tackle fouling; for example, through antifouling procedures and maintenance routines. The cost of antifouling a single salmon net alone can be several thousands of pounds. Nevertheless, there are virtually no scientific data available for the broad economic consequences of fish-cage fouling specifically. For fouling as a whole, it has been stated that $260 million were spent worldwide on antifouling coatings in 1993 (Bennett, 1996), whereas the amount of antifouling paint being produced annually has been calculated at 37,500 tonnes, or 25  106 L (Davies et al., 1998). However, it should be noted that it is unclear whether these figures include data on antifouling usage in industries other than shipping, such as fish farming; despite this, shipping activities would, regardless, account for the majority of these values because of the industry’s relatively large size. Estimates of annual, global costs of tackling biofouling vary widely and, again, are typically concerned with ship fouling. For example, Clare (1995) suggested costs of $1,400 million and Milne (1991) calculated at least $2,500 million, whereas Evans (1999) cited an annual figure of $5,700 million.

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3. THE FOULING COMMUNITY OF FISH-CAGE NETTING 3.1. Mediation by physical, chemical, and biological factors All surfaces, including those of mariculture equipment, immersed in sea water undergo a series of discrete, sequential, chemical and biological changes (Gunn et al., 1987). Thus, the development of a fouling community is a stepwise process, with each stage conditioning the surface for the next (Daniel and Chamberlain, 1981; Davis and Williamson, 1996). However, it is worth noting that this ‘‘classical’’ fouling process is a simplified one, and complex interactions between fouling organisms, their environment, and the surface may modify it (Clare et al., 1992); organisms can and will settle in the absence of typical conditioning layers. Not only do settlers modify the surface chemistry for subsequent settlement, they also aVect the threedimensional surface structure (Ko¨hler et al., 1999). Fouling of surfaces by abiotic and biotic substances has molecular, microbial, and macroorganismal levels of organisation (Rittschof, 2000), with the composition of the fouling community depending primarily on qualitative and quantitative aspects of the inoculum (Callow, 1996; Dubost et al., 1996). Net fouling is, therefore, a highly dynamic process that varies temporally with both biological and seasonal succession (Moring and Moring, 1975; Alberte et al., 1992; Lai et al., 1993; Hodson and Burke, 1994; Cronin et al., 1999; Tan et al., 2002). For example, fouling of floating net cages in temperate waters is most aggressive during summer months and increases with length of immersion (Dubost et al., 1996). The substratum material and its properties, such as mesh size and whether a net is knotted or not, are also integral in determining the nature of the fouling community that develops on it (Huguenin and Huguenin, 1982; Beveridge, 1996; Dubost et al., 1996). For example, Milne (1975a) demonstrated that galvanized steel mesh fouled less than net made from synthetic fibre. Likewise, wood, of all the materials used in aquaculture, is unique in being prone to attack by ‘‘boring’’ organisms, including the shipworm Teredo navalis, a teredinid bivalve mollusc found commonly within the North Atlantic (Tuente et al., 2002). In addition, netting colour has been demonstrated to aVect the development of macroalgal fouling (Hodson et al., 2000). Furthermore, fouling does not, necessarily, develop uniformly over a surface (Lewthwaite et al., 1985). Net fouling can be highly variable and change with depth and surface orientation, as well as between adjacent cages (Huguenin and Huguenin, 1982; Cronin et al., 1999; Hodson et al. 1995). It has been documented several times that fouling intensities are greatest nearer the water surface (Moring and Moring, 1975; Claereboudt et al., 1994; Hodson et al., 1995; Dubost et al., 1996; Lodeiros and Himmelman, 2000). This is certainly the case for fouling algae, owing

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to their light requirements, although it has been shown that, conversely, invertebrate fouling can increase with depth (Cronin et al., 1999). Accordingly, much anecdotal evidence also suggests that bivalve fouling is greatest toward the bottom of nets. External factors, such as water flow (Judge and Craig, 1997), nutrient supply, competition, and other environmental variables also modify the colonization and growth processes (Callow, 1996). Grazing can also significantly aVect fouling development (Brandini et al., 2001). In the case of aquaculture, this grazing can stem from stock within the cages when species such as tilapia (Norberg, 1999) or cod (D. Robertson, pers. comm.) are cultured (Neushul et al., 1976). Farm management practices, such as net changing and washing, of course, also aVect the fouling community (Tan et al., 2002). Fouling varies spatially (Holm et al., 2000), as its intensity and diversity naturally follow the distributional pattern of the marine epibenthos from which it is largely derived. It is most intense in coastal or shallow waters, where species diversity is greatest and temperatures, as well as nutrient levels, are higher (Meadows and Campbell, 1995). Concurrently, fouling is more aggressive in tropical regions than in temperate zones, where the nature of the ‘‘fouling potential’’ is diVerent (Cheah and Chua, 1979; Bennett, 1996). It has also been demonstrated that farming practices in freshwater and brackish environments suVer less from fouling than do farms located in fully saline conditions (Beveridge, 1996), though it can still be very severe (Dubost et al., 1996). Fouling variations can also occur over relatively small geographical areas (Huguenin and Huguenin, 1982).

3.2. Community development Marine fouling starts with the adsorption of inorganic material and macromolecules on immersed surfaces, forming an initial conditioning film that is approximately 5 nm in depth (Gunn et al., 1987). This is followed by a primary microbial film formed by the settlement of, among other microfoulers, bacteria, fungi, and blue-green algae (Scott et al., 1996). Bacteria have been recorded on surfaces following only 4 h immersion, and fouling bacterial cell densities of 218 cm2 have been measured (Dempsey, 1981). However, this microfouling ‘‘slime layer’’ comprises mainly diatoms (Evans, 1981; Gunn et al., 1987; Hodson and Burke, 1994), and typical thicknesses of 100–600 mm have been reported (Woods et al., 1988). Fouling diatom production rates of 31  108 cells m2 week1 have been measured in situ (Brandini et al., 2001), and as many as 97 species of diatom, from 27 genera, have been reported fouling toxic surfaces (Hendey, 1951). Accordingly, Moring and Moring (1975) reported the rapid growth of filamentous

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diatoms on salmon nets during summer months. Amphora coVeaeformis is the most commonly reported fouling diatom species (Wigglesworth-Cooksey and Cooksey, 1992) and is one of the few algae that successfully colonizes copper-based antifouling paints (Robinson et al., 1985). As such, the genus Amphora has been recorded fouling salmon cages (Hodson and Burke, 1994). Subsequently, this fouling leads to the development of complex and diverse plant and animal communities (Delort et al., 2000). Macrofouling is often concerned primarily with those species that are sessile, as opposed to the free-living organisms that are often attracted by the resources aVorded, such as habitat and food. However, because the concept of fouling is based on practical considerations (WHOI, 1952) and mobile organisms can also be of economic consequence to the aquaculturist, for the context of this review, such species will also be considered (e.g., decapods). Approximately 2,000 fouling species, including 615 plant species, have been reported, on both toxic and nontoxic surfaces (WHOI, 1952). These included 13 of the 17 recognized invertebrate phyla. Other sources indicate that as many as 4,000–5,000 species are controlled by antifouling paints (Evans and Smith, 1975). All benthic organisms are potential ‘‘foulers’’. However, they will settle in order of their species-specific resistance to a treated surface as it gradually loses its toxicity (Harris and Forbes, 1946). Accordingly, diVerent genera have demonstrated diVerential resistance to antifouling biocides (Woods et al., 1988), and in practice, only relatively few genera are typically found growing on treated surfaces (Furtado and Fletcher, 1987). The macrofouling community that develops on fish-cage netting is very diVerent to that found on ships, as has been documented by several workers (Milne, 1970; Moring and Moring, 1975; Cheah and Chua, 1979; Kuwa, 1984; Lai et al., 1993; Dubost et al., 1996; Cronin et al., 1999). This diVerence (see following Section) is undoubtedly a result, in large part, of the substratum (i.e., typically mesh, coupled with the employment of that material within stationary structures). Factors such as hydrodynamic force will also play an important conditioning role. The surface variables of an antifouled mesh, such as roughness, are not easily controlled. Typical net mesh is not monofilament and, inherently, can have a relatively heterogeneous surface, as well as a high surface-area-to-volume ratio. It is therefore highly prone to fouling (Hodson et al., 1997). Also, because fish farms are anchored close inshore, they are in continuous contact with the relatively aggressive coastal fouling inoculum (WHOI, 1952). Unlike ships, they spend no time out at sea, and because they are stationary the environment for attached fouling organisms remains stable too. On top of this, the fish farm environment is highly conducive to fouling development because of the elevated nutrient and organic loadings that are present (Folke et al., 1994; Black et al., 1997; Cronin et al., 1999; Angel and Spanier, 2002).

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3.3. Fouling taxa Net fouling communities can be highly diverse (Cronin et al., 1999). For example, Cheah and Chua (1979) identified around 34 species fouling fish cage netting following only 2 months of immersion, and representatives of taxa from eight animal phyla and two algal divisions were recorded by Cronin et al. (1999) as fouling nets. Similarly, 39 species were recorded by Claereboudt et al. (1994) as fouling pearl nets. Table 2 provides a summary of the frequency with which taxa have been recorded fouling aquaculture equipment from around the world. In total, 149 genera and 119 species, distributed among 11 phyla and constituting 184 individual taxa, are detailed. These include, predominantly, algae and sessile invertebrates, although a number of mobile animals are also listed. Thirty-six genera, including 17 species, are listed more than once, and of these, only 10 taxa occur more than twice. The information for Table 2 was extracted from publications that provided identifications of fouling organisms to the taxon of genus or species; these publications were limited to only 25 papers. Of these, the majority listed only the most predominant fouling taxa. In contrast, just a few references, for example, Cheah and Chua (1979), provided detailed lists of all fouling. Other publications do not list fouling organisms identified to such taxon levels. In addition, many further references noted the development of fouling as a whole or the presence of certain fouling groups, for example, mussels; however, no identifications to any scientific taxon were reported. Of note, no data on the relative or absolute abundances of the taxa detailed in Table 2 were originally published. As such, attempts at inferring the importance of individual taxa as a fouling threat to the aquaculture industry cannot be accurately made; fouling significance is linked to abundance and not merely presence. The blue mussel Mytilus edulis (Figure 2), and sea squirts, particularly Ciona intestinalis and Ascidiella aspersa, are the most commonly recorded organisms observed fouling temperate mariculture equipment and often dominate the ‘‘climax communities’’ that develop (Milne, 1970, 1975a,b; Moring and Moring, 1975; Lesser et al., 1992; Claereboudt et al., 1994; Paclibare et al., 1994; Hodson et al., 2000). Similarly, during studies on the fouling of tropical floating net cages, tunicates and bivalve mussels, among others, were again predominant fouling organisms (Cheah and Chua, 1979; Cronin et al., 1999; Tan et al., 2002). Table 2 demonstrates that these groups are often present on aquaculture equipment. Such organisms are a particular threat to the aquaculture industry because of their relative size and weight, which disrupt the exchange of materials through the net and cause structural stress, respectively. To judge from the literature, barnacles would not seem likely to pose any significant threat to the fish farmer. This is in contrast to ship fouling, where bamacles are some of the most frequently reported and studied fouling

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organisms; for example, Balanus amphitrite (Clare and Matsumura, 2000). It is possible that epifaunal species with rigid attachment systems such as most barnacles and tubeworms, another common ship-fouling group, are not prevalent on netting because it is a substrate that tends to flex. Netting is not flat or solid and, perhaps, favours organisms such as mussels and tunicates that possess attachment processes that can cope more easily with this (i.e., byssus threads and fleshy basal systems, respectively). However, there is a warm-water barnacle, Solidobalanus fallax, that ranges the eastern Atlantic from southwest England to Angola, whose ‘‘normal’’ habitat is other organisms such as macroalgae, cnidarians, crustaceans, and molluscs. This species is now being recorded with increasing frequency along the English Channel and the Atlantic coasts of France, Spain, and Portugal attached to plastic detritus, plastic-coated crab and lobster pot frames, and synthetic netting, including both woven and knotted monofilament (Southward, 1995; A. J. Southward, pers. comm.). This barnacle, which appears to select ‘‘low-energy’’ surfaces, has the potential to be a pest of fish cages in the warmer waters south of Britain. Macroalgae are not important fish-cage net fouling organisms in the North Atlantic, although they are present (Milne, 1970, 1975a). Despite the genera Enteromorpha and Ectocarpus occurring relatively frequently on aquaculture equipment (Table 2), it is likely that the significance of their presence is relatively minimal. Their growth is restricted, owing to photosynthetic requirements, to the upper illuminated areas of substrata (Milne, 1975a; Pantastico and Baldia, 1981; Cronin et al., 1999; Ingram et al., 2000). For example, for a typical salmon net with a circumference of 80 m and a depth of 20 m, macroalgae may not be able to grow on at least 80% of the net, assuming, generously, a restricted penetration of growth to 5 m depth. In Norwegian fjords, where nets are often 30 m in depth and can reach even greater dimensions, this figure may be considerably greater. Also, macroalgae do not possess the weight or size of, for example, bivalves and, therefore, do not disrupt the flow of materials through nets or stress cages structurally to a relatively great extent. Macroalgae also do not occur at the bottom of nets, where waste material can accumulate and the exchange of water is highly important. Another reason why the genus Enteromorpha does not dominate the fouling communities that develop on fish cage netting may be the lack of fast operating speeds possessed, for example, by ships, which favor algal spore settlement (Houghton et al., 1973). A huge reproductive potential, which is reportedly one of the main reasons for the success of Ectocarpus and Enteromorpha as ship-fouling genera, is also a property possessed by Mytilus edulis and Ciona intestinalis. For example, C. intestinalis is fertile throughout the year and, like Enteromorpha, has, a cosmopolitan temperate distribution, though this is largely a result of introductions (G. Lambert, pers. comm.). Similarly, M. edulis is found throughout temperate

228

Table 2 Numbers of taxa, genera, and species in each group reported from aquaculture equipment Number of identified Species

Number of identified Genera

Algae Bacillariophyceae

20

18

4

Cyanophyceae Chrysophyceae Chlorophyceae

4 1 17

4 1 14

1 0 4

Phaeophyceae

10

9

7

Rhodophyceae

24

15

18

4 4 1

4 3 1

1 4 1

6

3

5

5

5

5

Protozoa Porifera Cnidaria Scyphozoa Hydrozoa Anthozoa

Genera/Species Recorded More Than Oncea Biddulphia sp. Campylodiscus sp. Fragilaria sp. Oscillatoria sp. Bryopsis sp. Cladophora sp. Enteromorpha sp. (5) Ulothrix sp. Ulva nematoidea Ulva spp. (3) Ectocarpus siliculosus Ectocarpus sp. (4) Scytosiphon lomentaria Brongniartella australis Ceramium tasmanicum Gracilaria sp. Polysiphonia abscissa Vorticella sp.

Obelia australis (3) Tubularia larynx (4)

R. A. BRAITHWAITE AND L. A. MCEVOY

Number of Taxa Recorded

Annelida Polychaeta Crustacea Cirripedia Malacostraca Arthropoda Pycnogonida Mollusca Prosobranch Gastropoda Opisthobranch Gastropoda Bivalvia

Echinodermata Hemichordata Ascidiacea

a

1 7

1 5

1 5

10

9

6

6 21

2 18

5 13

1

1

1

9

6

7

7

4

7

24

16

17

1

1

0

11

9

7

Bugula neritina (3) Scrupocellaria bertholetti (3)

Balanus sp. Caprella sp.

Littorina spp. Thais spp. Dendronotus frondosus Hiatella arctica Hiatella spp. Modiolus sp. Mytilus edulis (9) Perna viridis Pinctada sp.

MARINE BIOFOULING ON FISH FARMS AND ITS REMEDIATION

Platyhelminthes Turbellaria Bryozoa

Ascidiella aspersa (3) Botrylloides sp. Ciona intestinalis (4) Molgula ficus

Recorded twice unless otherwise indicated in brackets.

229

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R. A. BRAITHWAITE AND L. A. MCEVOY

Figure 2 Biofouling of finfish cage netting: (A) waterline fouling by the green algal genus Enteromorpha at a Scottish salmon farm, which has developed on a copperbased coating that gives a the red colour to the netting; (B) heavy fouling of a net immersed at a sea trout farm on the Danish east coast, where the mussels have severely obstructed the free flow of water through material; the mussels average 5–10 mm in length, and the mesh is approximately 20 mm from knot to knot (photograph courtesy G. Nicholl).

regions in both the southern and northern hemispheres (Gosling, 1992), and individuals can produce as many as 40 million eggs annually (Thompson, 1979). Algae, nevertheless, can cause serious problems by settling on aquaculture systems (Hattori and Shizuri, 1996) and, as already mentioned, are typically found in the upper, illuminated, regions of nets (Milne, 1975a; Pantastico and Baldia, 1981; Cronin et al., 1999; Ingram et al., 2000). In temperate waters, algae typically constitute the pioneering fouling communities that settle before mussel spawning and subsequent domination (Milne, 1970). For example, the genus Ectocarpus was reported as an early colonizer during sea trials on the west coast of Scotland (Milne, 1970). Similarly, the red algal

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genus Anththamnion dominated the fouling community that developed on nets immersed in Tasmania during regeneration trials (Hodson et al., 1995), and species of the green algal genus Ulva have often been reported fouling netting (Milne, 1970; Cronin et al., 1999). For example, Ulva rigida was the dominant species recorded from silicone-coated salmon cage netting during trials (Hodson et al., 2000), and Ulva nematoidea was an important species recorded fouling ropes used for cultivation of the carrageenophyte Sarcothalia crispata (Romo et al., 2001). In pond systems, the genera GiVordia (now Hincksia) and Ectocarpus have been recorded as important fouling organisms (Lovegrove, 1979a), as has the latter from macroalgal mariculture practices in Chile along with species of the red algal genera Ceramium and Polysiphonia (Romo et al., 2001). Similarly, hydroids, for example, Tubularia larynx, have often been observed fouling mariculture equipment (Milne, 1970, 1975a,b; Claereboudt et al., 1994; Cote et al., 1994; Deady et al., 1995), along with many other species of invertebrates as well as with macroalgae that are typical of fouling communities (Milne, 1970; Lesser et al., 1992; Cronin et al., 1999; Tan et al., 2002).

4. ANTIFOULING TECHNOLOGY Recent research into various technologies for antifouling has had various levels of practical application to the fish farming industry, as it has focused primarily on combatting ship fouling. These technologies have included toxic coatings, osmotic stress, radiation, electric systems (alternating and pulsed currents, anodic dissolution of heavy metals and cathodic exfoliating surfaces), ultrasonics, heat, air bubbles, ultraviolet light, coloured surfaces, chlorine (bulk addition or electrochemically evolved), peeling or moving substrata, and periodic cleaning (Benson et al., 1973). A side eVect of algal biofouling may be the deposition of calcium carbonate (CaCO3), which can constitute 56% of the fouling dry weight (Heath et al., 1996). Thus, eVorts have also been made to control calcification by using phosphonate inhibitors. Much attention is presently being placed on the elucidation of the principles that govern bioadhesion and on understanding the chemistries and physical interactions between adhesive exopolymers and surfaces (Alberte et al., 1992; Callow and Callow, 2002). Accordingly, consideration has been given to the incorporation of enzymes into antifouling formulations, to disrupt the adhesives used by organisms to attach themselves firmly to substrata (Callow, 1990). The inclusion of ‘‘drag-reducing’’ molecules, for example, polyox (polyoxyethylene) has also been investigated (Gucinski et al., 1984). The identification of antifouling mechanisms, which exist for many invertebrate and plant species (Mckenzie and Grigolava, 1996), and

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manipulation of the pheromonal cues that help determine fouling are also being investigated (Clare and Matsumura, 2000; Holmstro¨m et al., 2000). For example, many organisms, such as starfish, remain clear of fouling growths. A great deal of attention has been given to the identification of so-called nontoxic, or at least environmentally benign, natural product antifoulants (NPAs), of which over 90 have been characterized (Clare, 1998). Such studies have included plants (Todd et al., 1993; de Nys et al., 1995) as well as animals (Henrikson and Pawlik, 1995; Hellio et al., 2001), though few bioactive compounds have been commercially successful (Clare, 1996; Rittschof, 2000). One compound that has shown particular promise is zosteric acid, which is derived from the eelgrass Zostera marina (Haslbeck et al., 1996; Callow and Callow, 1998). Other lines of research have included the incorporation of nonleaching biocides (NLBs), where toxins are bound to the surface (Clarkson and Evans, 1995), and the testing of hydrogels and hydrogel-containing surfaces (His et al., 1996; Cowling et al., 2000). At present, because of environmental and political pressures, much work is being focused on the development of biocide-free ‘‘nonstick,’’ or ‘‘foul release,’’ low-surface-energy coatings (Hodson et al., 2000; Holm et al., 2000). Associated work on microtexturing of surfaces has also been pursued (Andersson et al., 1999; Phillippi et al., 2001; Wilkerson et al., 2001; Callow et al., 2002). Fish farmers typically combat net fouling by using a combination of procedures. These include regular net changing and cleaning (Enright, 1993; Beveridge, 1996; Hodson et al., 1997; Tan et al., 2002), adoption of fouling resistant or rotating cage designs (Blair et al., 1982), and chemical control (Enright, 1993; Beveridge, 1996; Hodson et al., 1997). The use of larger mesh sizes, where applicable, can also reduce fouling by limiting the surface area for fouling attachment (Lodeiros and Himmelman, 1996). Fouling can necessitate regular cage washing (Li, 1994), and cleaning of nets commonly employs high-pressure water hosing (Lee et al., 1985; Enright, 1993; Lodeiros and Himmelman, 1996; Cronin et al., 1999). Although manual brushing and scrubbing is tedious and labour intensive (Enright, 1993), enclosures are often cleaned this way, for example, on a daily basis using a broom and ‘‘vacuum cleaner’’ (Nehr et al., 1996). Simple practical measures, for example, providing shade by the use of polyethylene netting covers to inhibit algal growth, have also been investigated (Huse et al., 1990). It has been suggested that fouling may be reduced by culturing scallops at greater depths (Claereboudt et al., 1994; Lodeiros and Himmelman, 1996, 2000) or minimizing the fouling inoculum by carefully planned positioning of sites (Enright, 1993; Claereboudt et al., 1994). Studies on macroalgal mariculture indicate that fouling can be avoided by starting cultures in autumn and maintaining them at greater depths (Romo et al., 2001). In addition, the practicalities of in situ net cleaning, adapted from ship

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hull cleaning procedures (Alberte et al., 1992), have been investigated (Hodson et al., 1997). Air or sun drying is another means of removing fouling organisms (Enright, 1993) and can be facilitated by employing rotating or semisubmersible cage designs, or those that can be lifted easily, such as shellfish nets. However, the cleaning of fouled cages is destructive, time consuming, and awkward (Hodson et al., 1995). In shellfish farming, further methods employed by the farmer have included hot water immersion, freshwater immersion, brine immersion, and even burning (Enright, 1993). Before the advent of modern, nonabsorbent mesh, fish farmers would soak their nets in tannin from the bark of mangrove trees (Rhizophora sp.) (Beveridge, 1996). Thus, the antifouling eYcacy of tannin extracted from Rhizophora mucronata has been evaluated (Lai et al., 1993).

4.1. Toxic antifouling paints and materials The main protective method against fouling, whether it be for ships or nets, involves the use of toxic antifouling paints (Lovegrove, 1979b; Short and Thrower, 1986; Evans and Clarkson, 1993; Douglas-Helders et al., 2003), which work by creating a toxic boundary layer at the surface of the paint as the component biocides leach out (Evans, 1981). Antifoulants are preferred by the aquaculture industry because they are more economical than manual cleaning (Short and Thrower, 1987). These paints are applied to nets typically made from synthetic fibres, including polyamide (PA), more commonly known as nylon (Beveridge, 1996). Nets made of a range of mesh sizes are employed in finfish farming and their use is dependent on stock age and size; for example, salmon smolt are often kept in 13 mm ‘half-mesh’ (square as opposed to full-mesh stretched/diamond-patterned netting) before ongrowing in 25 mm nets. Other common mesh sizes used for salmon culture include 15, 27 and 29 mm but because this measurement is recorded between two adjacent knots the actual aperture size is slightly less and the open area of a net may be only 80 percent of the total area occupied. The benefits of employing antifouling coatings on fish farm nets, to reduce biofouling development, have been demonstrated by Lai et al. (1993). Antifouling paints containing only copper, in the monovalent form of cuprous oxide, is the paint technology used almost exclusively in the fish farming industry today (Lovegrove, 1979a; Lewis and Metaxas, 1991; Enright, 1993; Hodson and Burke, 1994; Beveridge, 1996; Douglas-Helders et al., 2003). These coatings are typically based on a waxy emulsion that provides the flexibility that is required from nets; this is not the case with ship antifouling paints, which are based upon diVerent technologies. In general, ship antifouling paint systems cannot be applied directly in the aquaculture industry because of the nature of the substratum (i.e. the flexibility both innate in nets but also required on

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coating, and incompatibility issues that consequently exist; for example, many boat paints, such as contact leaching/hard free-association paints, are designed specifically to work from and form a hard surface). Paints produced for aquaculture can contain 40% copper by weight, although typical volumes are less. Citing Aqua-Net (Steen-Hansen Maling AS, Norway) as an example, 1 kg of dry net requires treatment with 1 litre of paint, which has a biocidal content of 10%–25%. Cuprous [copper (I)] oxide, Cu2O, of which the cuprous ion (Cuþ) is the toxic component, is a powder under normal ambient conditions and is responsible for the red colour seen in nets that have been treated with copper-based antifoulants. Copper is highly eVective against a wide range of organisms (Houghton, 1984), and it has been suggested that leaching rates for copper of 22 mg cm2 day1 and 16 mg cm2 day1 are required to inhibit algal and barnacle fouling, respectively (de la Court, 1988). The cost of treating a knotless net with antifoulant adds approximately 25% to its cost (Beveridge, 1996). Traditionally, antifouling paints can be either oil-based or water-based, with the latter being favored by Health and Safety guidelines. Water-based compositions registered by the Health and Safety Executive (HSE) for use in the United Kingdom aquaculture industry include, for example, Aquasafe W and Flexgard VI-II Waterbase Preservative, which are manufactured by GJOCO A/S, Norway, and Flexabar Aquatech Corporation, United States, respectively. Usually, nets are soaked in the antifoulant solution for several minutes before being hung up to dry, fully open; for example, a period of 15 min is recommended for Netrex AF, a product of Mobil Oil AS. It is recommended that nets then be immersed as soon as possible and that stock should not be introduced for at least 24 h (Beveridge, 1996). Treatments typically provide 6 months’ adequate protection, after which progressive failure occurs. Therefore, in temperate climates nets are often treated annually and immersed in the spring, before the onset of the main fouling season (Beveridge, 1996). Apart from nylon netting, rigid cages using, for example, 90:10 coppernickel alloy, which exhibits relatively good antifouling properties (Huguenin and Huguenin, 1982; Alberte et al., 1992), and galvanized steel mesh (Milne, 1970, 1975a), are sometimes employed in mariculture practices as well; for example, in the shellfish industry (Huguenin and Huguenin, 1982). Similarly, Aquamesh, produced by Riverdale Mills Corporation of the United States and used largely in the shellfish industry, is a ‘‘galvanized after welding’’ wire mesh coated with polyvinyl chloride that has some antifouling properties. Nonrigid materials, with a similar function, that supposedly minimize fouling include Vexar and Durethene, both of which are meshes made from extruded polyethylene. In addition, cage designs that aid net cleaning by rotating or being semisubmersible, such as the Farmocean oVshore system and Ocean Spar products, are also available (Blair et al., 1982). Other recent cage innovations include the product MarineMesh,

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developed by an Australian company, OneSteel; the smooth metal links, to which organisms can have diYculty adhering, purportedly reduce fouling.

4.2. Legislation It is very apparent that information regarding the regulation and legislation of toxic antifouling products for use in the aquaculture industry is largely unavailable or simply lacking for many countries. This is most likely a result, largely, of the young nature of the industry, coupled with the fact that many nations do not have transparent or well-defined and detailed systems of regulation. This may be particularly pertinent in less well developed parts of the world, such as eastern Asia, where it has been reported that legislation even for ship antifouling products is severely lacking; for example, in Korea (Shim et al., 2000), Singapore (Basheer et al., 2002) and Thailand (Bech, 2002). It has also been suggested that the Chilean salmon farming industry has grown at a rate that has outpaced the capabilities of the authorities to regulate it (Barton, 1997). In addition, where information on antifouling products is available, limited diVerentiation is often apparent between paints available for use in the shipping industry and those allowed for application in aquaculture. For example, the Canadian Pest Management Regulatory Authority (PMRA), which administers the registration of biocidal antifouling paints under the Pest Control Products Act (PCP), combines net antifoulants along with ship antifoulants in its list of currently registered products. This list comprises 61 products, which are all based solely on copper; however, of these products, it is likely that only a few are designed for use in aquaculture. The situation is largely similar in New Zealand. There, on behalf of the New Zealand Food Safety Authority, the Agricultural Compounds and Veterinary Medicines (ACVM) Group, under the ACVM Act (1997), which is a companion measure to various other acts, is responsible for the registration of antifouling paints. A total of 46 products are currently registered, and many of these contain cobiocides in addition to copper. Again, of these paints, only a few are likely to be specific to aquaculture. Also, presumably, those formulations not based solely on copper are designed for ship antifouling purposes and not for application in aquaculture. In the United Kingdom, chemical antifouling treatments are assessed by the Biocides and Pesticides Assessment Unit (BPU), formerly the Pesticides Registration Section (PRS), of the HSE and are given approval for specific uses under the Control of Pesticides Regulations 1986 (COPR). As of October 1998, owing to the European Union Biocidal Products Directive 98/8/EC (BPD), which regulates pesticides not used for agricultural purposes, the HSE has been reviewing copper-based antifouling treatments. Table 3 lists

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the 16 toxic products that are provisionally registered for use in aquaculture at present (i.e., in 2003). BPD regulations were implemented by the HSE in May 2000, and following this transitional period, all antifouling biocides will come under the Biocidal Products Regulations. There are eight organic and organometal booster biocides currently employed in the approximately 400 ship antifouling products registered in the United Kingdom for use during 2003, in addition to a number of copper- and tin-based ingredients. However, despite research into the toxicity of alternative organic antifouling biocides to fish, for example, the toxicity evaluation of Sea-Nine 211, Irgarol 1051, Diuron, and pyrithione compounds to chinook salmon Oncorhynchus tshawytscha, (Okamura et al., 2002), biocides other than copper are little used. Those that are currently employed include chlorothalonil, which is formulated in Flexgard VI, a product of Flexabar Aquatech Corporation, United States. The only other biocide used in currently registered antifouling

Table 3 List of toxic antifouling products currently registered with the Health and Safety Executive for use in UK aquaculture Product Name

Ingredient(s)

Marketing Company

VC 17M-EP Amercoat 70ESP VC 17M Aqua-Guard Aqua-Net Aquasafe W Boatguard Bottomkote Carmypaint SV-881

Coppera Copper Metaa Copper Metaa Cuprous Oxide Cuprous Oxide Cuprous Oxide Cuprous Oxide Cuprous Oxidea Cuprous Oxide

Copper Net Flexgard VI-II Waterbase Preservative

Cuprous Oxide Cuprous Oxide

Hempel’s Net Antifouling 715GB Net-Guard Netrex AF Flexgard VI

Cuprous Oxide

International Coatings Ltd Ameron BV International Coatings Ltd Steen-Hansen Maling AS Steen-Hansen Maling AS GJOCO A/S International Coatings Ltd International Coatings Ltd Carmyco S.A. Paints-Varnishes-Adhesives Steen-Hansen Maling AS Aquatess Ltd (manufactured by Flexabar Aquatech Corporation) Hempel Paints Ltd

Hempel’s Antifouling Rennot 7150

Cuprous Oxide Cuprous Oxide Cuprous Oxide and Chlorothalonila Cuprous Oxide and Dichlofluanidb

Steen-Hansen Maling AS Tulloch Enterprises Flexabar Aquatech Corporation Hempel Paints Ltd

a Approval for sale and advertisement has expired. Product retains short-term approval for storage and use. b Approval for advertisement, sale, supply and storage has expired. Product approved short term, for disposal purposes only.

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products for aquaculture is Dichlofluanid, which is found in Hempel’s Antifouling Rennot 7150, developed by Hempel Paints Limited, Denmark. Both of these products are currently being phased out of the UK market. The former retains approval for supply, storage, and use for a short period, whereas the latter holds approval for disposal purposes only. Similarly, four of the other 14 registered toxic antifoulants for aquaculture use in the United Kingdom are presently being phased out (Table 3). The situation is similar in many other E.U. countries and has been led, partly, by the BPD. For example, in Finland, Netrex AF was only marketed until August 31, 2003, and its use must cease after June 30, 2004. In the past, tributyltin (TBT)-containing coatings were widely used in the fish farming industry (Lee et al., 1985; Short and Thrower, 1986, 1987), and in large parts of Asia, TBT use remains unrestricted for antifouling purposes; for example, in Korea (Shim et al., 2000). Singapore (Basheer et al., 2002), and Thailand (Bech, 2002). However, the ban on the use of TBT-based antifouling formulations, drawn up by the MEPC (Marine Environmental Protection Committee) of the IMO (International Maritime Organisation) during their forty-second meeting in November 1998 (Champ, 2000), has not aVected the UK fish-farming industry. Triorganotincontaining coatings for nets and cages, floats, or other apparatus used in connection with the propagation or cultivation of fish or shellfish in the United Kingdom were prohibited from retail and wholesale in 1987 under the Control of Pollution (Antifouling Paints and Treatments) Regulations 1987 (Waite et al., 1991; Bell and Chadwick, 1994). This followed a voluntary ban on its use by the National Farmers Union for Scotland in the autumn of 1986 (Balls, 1987). Likewise, according to ORTEPA (the Organotin Environmental Programme Association), Germany banned the use of organotin on structures for mariculture in 1990. In addition, it is possible that tin-based antifoulants have not been used in Canada for the past 15–20 years (F. Masi, pers. comm.). In New Zealand, the (then) Ministry of Agriculture and Fisheries banned organotin application to salmon cages in 1988, and this moiety was further banned as a condition of new marine farming licenses around 1990 (S. Metherell, pers. comm.). These measures were taken in response to problems with TBT that were first reported in the mid 1970s, following the harmful eVects observed in Crassostrea gigas oyster populations from Arcachon Bay, oV the French Atlantic coast (Evans et al., 1995; Alzieu, 1996). Problems arising from use of TBT cost the oyster industry, between 1977 and 1983, $147 million (Alzieu, 2000). It was also demonstrated in the late 1980s that organotins were accumulating in the muscle tissue of salmon reared in pens treated with TBT-containing antifoulants and that aquaculture-produced fish purchased from the marketplace of several countries also contained detectable levels of organotins (Short and Thrower, 1986).

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The toxicity of copper to marine organisms is well documented (Mance, 1987). For example, concentrations as low as 2.5 mg L1, lower than some environmentally recorded levels, have been shown to aVect, significantly, germination in Baltic Sea Fucus vesiculosus (Andersson and Kautsky, 1996). Likewise, 2.5 mg L1 can adversely aVect bivalve molluscs (Mance, 1987). The UK environmental quality standard (EQS) for dissolved copper in sea water is 5 mg L1 (Voulvoulis et al., 1999), a value that was exceeded in over 20% of samples measured during a survey of UK estuarine waters in 1992 to 1996 that included the measurement of concentrations up to 80 mg L1 (Matthiessen et al., 1999). This latter value is several-fold higher than that reported to aVect early development in embryos of the Atlantic cod Gadus morhua (Granmo et al., 2002). In New Zealand, copper-containing antifouling formulations have questionably been marketed as the ‘‘environmentally friendly’’ alternative to TBT (de Mora, 1996). Since restrictions on the use of TBT, increases in the use of coppercontaining coatings have been considered responsible for observed increases in the levels of copper in the aquatic environment (Voulvoulis et al., 1999), over which environmental concerns are being raised (Hall and Anderson, 1999; Solberg et al., 2002). For example, antifouling paints provide the largest single source of copper (around 30%) in Swedish coastal waters (Andersson and Kautsky, 1996) and are responsible for the greatest input of copper into UK waters (Matthiessen et al., 1999). It has been reported that the aquaculture industry alone used 180 tonnes of copper for antifouling in 1998, a marked increase from the 47 tonnes used in 1985 (Solberg et al., 2002). However, it seems very likely that global copper consumption, per annum in the aquaculture industry, is considerably greater than these figures indicate. Some investigators believe that there is little ecological risk from present seawater concentrations of copper in Europe (Hall and Anderson, 1999), but this belief is in contrast to reports that suggest copper levels in UK waters may be having an ecological eVect (Matthiessen et al., 1999). A belief exists that copper may be banned from use in antifouling systems because the European Commission is proposing to give copper a R50/R53 classification, which is based on the E.U. directive on the dangerous substances 67/548/EEC. This is a ‘‘risk phrase’’ that means copper is very toxic to aquatic organisms and may cause long-term adverse eVects in the aquatic environment.

4.3. Nontoxic ‘‘alternative’’ antifoulants Fluoropolymer and, to a greater extent, silicone coatings based, commonly, on PDMS (polydimethylsiloxans) provide the major nontoxic alternative to toxic antifoulants and are typically referred to as ‘‘nonstick’’ or ‘‘foul-release’’

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coatings. Such siloxane elastomers function by reducing the adhesion strength of fouling organisms that are, consequently, loosely attached and easily removed (Tsibouklis et al., 2000); they rely on both a low surface energy and a low elastic modulus. Such surface energies are typically (in air) in the range of 20–30 mN m1 (Andersson et al., 1999) and are commonly quoted as a measure of the non-stick nature of a surface. Oils can be incorporated into them to improve their antifouling eYcacy (Stein et al., 2003a), and physical properties can be enhanced through the addition of fillers such as calcium carbonate or silica, although the latter has been reported to reduce performance (Stein et al., 2003b). Concurrently, coating thickness has been shown to affect efficacy and thin coatings are fouled more easily (Singer et al., 2000). Raft-testing of nonstick coatings, through static panel immersion trials as commonly employed for toxic paints, is not the ideal means of material testing because of the need for hydrodynamic shear to enable eYcacy. Therefore, before ship-patch trials, and before, or complementary with, raft-testing with rotor systems, among other experiments, laboratory bioassays that concentrate on measuring the strength of adhesion of classic ship fouling organisms to experimental material is a major preliminary test route used for selecting and developing potentially useful formulations. Zoospores of the genus Enteromorpha and species of barnacle cyprid are commonly employed in such tests (Kavanagh et al., 2001; Finlay et al., 2002). Accordingly, the American Standard for Testing and Materials (ASTM) D5618-94 employs barnacles in shear for testing foul-release surfaces. The first commercially available biocide-free antifouling paint formulation was Intersleek 425, released in 1996 for use on ships (Anonymous, 1999). Some nontoxic antifouling systems have been used in fish farming (Nehr et al., 1996; Hodson et al., 2000). However, the adoption of alternatives to copper-based antifoulants has been limited, as is also the case in the shipping industry (Anderson, 2002), despite the arguments for moving away from the use of copper-based solutions. For example, the occurrence of amoebic gill disease, which is the main disease in the Australian salmonid farming industry, caused by the protozoan Neoparamoeba pemaquidensis, has been shown to increase when nets are treated with copper antifoulant (Douglas-Helders et al., 2003). Also, copper-treated nets are not ideal for bottom-dwelling finfish species, such as halibut, that are in continuous contact with it. The suitability for application of nontoxic coatings, whether it be to ship hulls or nets, is restricted, and they are often easily damaged, thus disrupting the surface properties on which their antifouling capability is intrinsically dependent (Callow and Callow, 2002). In the shipping industry, silicone-based systems are only applied to vessels that operate at speeds suYciently fast enough to produce the hydrodynamic shear necessary to maintain a clean hull; for example, fast ferries. These systems do not currently work with slower craft and, thus, it would appear likely that they are

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also unsuitable for use in stationary aquaculture facilities. They are also relatively expensive, and their eYcacy has not been satisfactorily proven (Ko¨hler et al., 1999). However, because of the tightening of legislation on the use of toxic antifouling products and concerns that copper may be banned for use in antifoulants, emphasis has been placed on the development of such environmentally friendly agents. The interest in developing nontoxic coatings is strengthened by the wish to dispense with the poor environmental reputation that has attached itself to the fish farming industry because of, for example, old concerns over concentrations of antifouling biocides beneath fish farms (Balls, 1987; Lewis and Metaxas, 1991). The use of nonbiocidal solutions also enhances the healthy image of the final product (Hodson and Burke, 1994; Hodson et al., 1997) and can aid farms to acquire ‘‘organic’’ status, for example, in the United Kingdom through certification by The Soil Association following fulfilment of their organic standards. Also, in this climate, with its increasing regulatory controls, it is uneconomical for companies to develop and register new antifouling biocides (Bingaman and Willingham, 1994). Such costs can be in excess of $4 million (Anderson, 2002). For example, the registration of Sea-Nine 211 in the United States by Rohm & Haas took approximately 10 years and cost $10 million (Rittschof, 2000). Thus, from a manufacturer’s perspective, the benefit to developing nontoxic antifouling systems is further enhanced because the vast costs that are incurred with registering toxic coatings do not exist. Foul-release systems that are currently available include Hyperkote AQ and the BioSafe fouling control system, which are marketed by Hyperlast Limited, United Kingdom, and Wattyl Aquaculture, Australia, respectively. International Coatings Limited, United Kingdom, also has a ‘‘foul-release’’ coating that is registered and commercially available for use in the UK aquaculture industry i.e., Intersleek BXA810/ 820, now rebranded as Intersleek 425; (C. Anderson, pers. comm.). Similarly, Poseidon Ocean Sciences Incorporated, United States, who are already commercially developing Frescalin, a metal-free coating additive, are, in conjunction with Innovative Coatings Corporation, United States, developing nontoxic, environmentally safe, antifouling coatings for the marine aquaculture industry (J. Matias, pers. comm.).

4.4. Biological control Antifouling routines in fish farming have included that of ‘‘biological control’’; for example, fouling control through the use of herbivorous fish as grazers (Lee et al., 1985; Enright, 1993; Beveridge, 1996; Kvenseth, 1996). In Norway, experiments with wrasse species, which feed on blue mussel spat, allowed a reduction in salmon net changes of 50% (Kvenseth, 1996). It has

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also been reported that wrasse, used as sea-lice control agents in salmon farms, grazed on algae, crustaceans, and small molluscs on the nets in which they were caged (Deady et al., 1995). Similarly, it has been estimated that the use of wrasse reduced the costs of fouling on four Norwegian salmon pens by NOK 194,000 (approximately equivalent to $28,000) over a 2-year period (Kvenseth and Andreassen, 2003). To remove fouling algae from cages, Li (1994) advised mixing in, with cultured carp, scraping species such as Oreochromis spp. (tilapia), Carassius carassius (crucian carp), Cyprinus carpio (common carp), or Cirrhinus molitorella (mud carp). It has been stated that such methods have considerable potential for solving the problems of biofouling (Huguenin and Huguenin, 1982) and may have major technological and economic implications in future aquaculture practices (Enright et al., 1993). Rabbitfish (siganids) have been noted for their ability to maintain cages free of algal fouling (Newkirk, 1996) and have proven useful in controlling fouling on cages containing grouper and carangids (Chua and Teng, 1977). Siganus canaliculatus and Siganus lineatus have also been successfully used in oyster mariculture (Hasse, 1974). Similarly, knifejaws, Oplegnathus sp., (Kuwa, 1984) and the common carp, Cyprinus carpio (Li, 1994; Prilutzky et al., 1995), have been used to reduce fouling development in aquaculture systems. Beveridge (1996) mentions other workers who have employed tilapia, prawns, mullet, and rohu for similar reasons. Consideration has been given to polyculture systems incorporating the red sea cucumber, Parastichopus californicus, which is a commercially important detritivore that can feed on fouling growth debris (Ahlgren, 1998). Similarly, biological control may be suitable for controlling fouling in shellfish culture (Lodeiros and Himmelman, 1996), and the periwinkle Littorina littorea and the crab Cancer irroratus have potential as fouling control agents (Hidu et al., 1981; Enright et al., 1983).

5. CONCLUSIONS Fouling, despite purveying some benefits, typically poses an expensive problem to today’s aquaculturist. Maintenance is almost continually necessitated, and costly antifouling procedures are integral to farming practices. Yet little information is available on the fouling communities that quickly develop on newly submerged equipment, a reflection of the speed with which the industry has grown over the last half-century. A range of typical fouling organisms have been recorded fouling aquaculture equipment. However, it appears that such communities are distinct from those typical of ship fouling, owing to the fundamental diVerences that exist in respective substrata and the conditions in which they are used.

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Clearly there is an urgent need for eVective, environmentally acceptable antifouling agents and procedures, particularly in light of the rapid growth of the fish farming industry, which looks set to continue, and because of concerns that all toxins, including copper, will be phased out of use. This is compounded by the fact that aquaculture is most prevalent in developing and LIFDCs (Food and Agriculture Organisation of the United Nations, 2002), in which antifouling legislation is lacking the most and aquaculture production rates are the highest; for example, in large parts of Asia, which in 1996 accounted for 91% of the world’s reported tonnage. Conventional methods are, however, far from ideal and do not prevent fouling completely or indefinitely. This lack of protection is compounded in the fish farming industry by the fact that, in contrast to the shipping industry, there are relatively very few antifouling products available. Ship paints typically contain a number of complementary biocides that provide the required broad-spectrum activity required for combating fouling; it is accepted that copper formulated alone is not suYciently eYcacious. Thus, it is not surprising that aquaculture paints based solely on copper do not provide a comprehensive level of protection against fouling. Perhaps some of the organic booster biocides that have recently been adopted in the ship antifouling industry could be successfully applied in aquaculture. For example, Zinc Omadine and Sea-Nine 211 are compounds that appear to have a relatively excellent ecotoxicological profile as well as very good antifouling properties. Despite the potential, this is an avenue that is unlikely to be explored in view of current trends that exhibit a reduction in the numbers of biocides registered for antifouling purposes. A nontoxic coating approach to the problems of aquaculture fouling would be ideal. Led by the shipping industry, research into such technologies has accelerated greatly in recent years. However, it has been stated that the environmentally motivated wish to dispense with the use of antifouling biocides seems unrealistic (Ranke and JastorV, 2000). There is clearly a lack of viable alternative systems that are both environmentally friendly and eYcacious. This not only is the case for much of the shipping industry but also is evident for aquaculture. Because of the nature of substrata used in aquaculture (i.e. netting) and the static nature of farm sites, alternatives to copper-based systems do not yet exist, and it seems unlikely that they will do so in the near future, either. If the aquaculture industry is to adopt a nontoxic coating approach to antifouling, significant developments in current technology are needed, particularly in light of the relative expense of foul-release systems. Research into systems that work under low hydrodynamic shear will be necessary, as these systems do not currently exist. As a consequence, toxic paint coatings remain the predominant preventative technique for tackling marine biofouling, and it is highly likely that the

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next generation of net antifoulants will also contain biocides, as has been envisaged for future ship coatings (Evans, 2000). In summary, it is widely agreed that improved fouling control measures are needed in the aquaculture industry (Enright, 1993). Yet, because of the lack of viable alternatives to currently available copper-based solutions, the adoption of nontoxic alternatives appears unlikely in the near future. In the long term, in view of current legislative trends, control measures will most likely include foul-release technologies and, possibly, biological control systems. However, for this step to take place, there is, undoubtedly, a need for the generation of information, which is presently severely lacking, on the fouling communities that develop on fish farm equipment in addition to research on novel antifouling systems.

ACKNOWLEDGEMENTS This study was supported by a European Union Fifth Framework Competitive and Sustainable Growth Programme (GRD2-2000-30252). We would also like to thank Sue Marrs and Alan Southward as well as three anonymous referees for their helpful comments on an earlier version of the manuscript.

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Comparison of Marine Copepod Outfluxes: Nature, Rate, Fate and Role in the Carbon and Nitrogen Cycles C. Frangoulis,* E. D. Christou* and J. H. Hecq{

*Hellenic Centre for Marine Research, Institute of Oceanography, Anavissos 19013, Attiki, Greece, E-mail: [email protected] { MARE Centre, Laboratory of Oceanology, Ecohydrodynamics Unit, University of Lie`ge, B6, 4000 Lie`ge, Belgium

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Nature of Copepod Outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Nature of excretion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Nature of copepod particulate matter outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Factors Controlling the Rate of Copepod Outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Factors controlling the rate of copepod dissolved matter excretion . . . . . . . . . . . . 3.2. Factors controlling the rate of copepod particulate matter outfluxes . . . . . . . . . . . 3.3. Relationships between the diVerent outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Vertical Flux . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Passive vertical flux. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Vertical migration and active vertical flux . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Role of Copepod Outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. Role of copepod dissolved matter outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Role of copepod particulate matter outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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We compare the nature of copepod outfluxes of nonliving matter, the factors controlling their rate and their fate, and finally their role, particularly their relative importance in the carbon and nitrogen cycle. Copepods release dissolved matter through excretion and respiration and particulate matter through production of faecal pellets, carcasses, moults, and dead eggs. Excretion liberates several organic C, N, and P compounds and inorganic N and P compounds, with inorganic compounds constituting the larger part. The faecal pellets of copepods are covered by a peritrophic membrane and have a highly variable size and content. There is less information on the nature of other copepod particulate products. The weight-specific rates of posthatch mortality, respiration, excretion, and faecal pellet production have similar C or N levels and are higher than those of moulting and egg mortality. In general, most important factors controlling these rates are temperature, body mass, food concentration, food quality, and faunistic composition. Physical and biological factors govern the vertical fate of copepod products by aVecting their sedimentation speed and concentration gradient. The physical factors are sinking speed, advection, stratification, turbulent diVusion, and molecular diVusion. They influence the sedimentation speed and degradation of the copepod products. The biological factors are production, biodegradation (by zooplankton, nekton, and microorganisms) and vertical migration of copepods (diel or seasonal). Physical degradation and biodegradation by zooplankton and nekton are faster than biodegradation by microorganisms. The most important copepod outfluxes are excretion and faecal pellet production. Excretion oVers inorganic nutrients that can be directly used by primary producers. Faecal pellets have a more important role in the vertical transport of elements than the other particulate products. Most investigation has focused on carbon burial in the form of copepod faecal pellets, measured by sediment traps, and on the role of ammonia excretion in nutrient recycling. Full evaluation of the role of copepod products in the transport and recycling of elements and compounds requires a quantification of all copepod products and their diVerent fates, particularly detritiphagy, remineralization, and integration as marine snow.

1. INTRODUCTION A pressing issue for the international community is understanding natural and anthropogenic forcing of the nutrient and carbon biogeochemical cycles. The rapidly increasing anthropogenic pressure and the ‘‘greenhouse eVect’’ have turned eutrophication and global change into key issues in marine research. To cope with these phenomena, a good knowledge of the sources and sinks of both nutrient and carbon cycles is necessary, because they are

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closely linked, as nutrient and light availability drive the biogenic components of the carbon cycle. The oceans are likely to be a major sink for released anthropogenic carbon on a long-term basis (Wollast, 1991). Marine flora incorporate inorganic carbon into organic molecules, constituting 40% of the total organic carbon production of the earth, and 95% of this production is by phytoplankton (Duarte and Cebrian, 1996). The carbon entering the upper ocean can be transferred to deep waters via three pathways; a physical one (the solubility pump; i.e., the transport of inorganic and organic carbon by deep convection) and two biological ones (the carbonate pump and the biological CO2 pump; i.e., active and passive vertical transport of biogenic particles; Sundquist, 1993). The biological CO2 pump largely relies on zooplankton. Despite the small size of zooplankton organisms (mm to mm size scale), their total biomass is estimated to be greater than that of other marine consumers such as zoobenthos and zoonekton (Conover, 1978). Herbivorous zooplankters consume more than 40% of the phytoplankton production (Duarte and Cebrian, 1996, and references therein) and release into the surrounding water a variety of liquid and solid materials that contribute to the dissolved matter (DM) and particulate matter (PM), respectively. DM and PM can accelerate the vertical transport of carbon and nutrients to deep water. An important process accelerating vertical fluxes of phytoplankton organic matter is the compaction and packing of this matter into faecal pellets by herbivorous zooplankton (e.g., Smayda, 1971; Turner, 2002). The intensity of this process varies according to the faecal pellet and zooplankton characteristics as well as environmental factors, so that carbon and nutrients will either be rapidly transported out of the eutrophic zone or be recycled in their production zone (Turner, 2002). These diVerent fates of carbon and nutrients transported through zooplankton products highlight the ‘‘switching’’ role of zooplankton in the cycle of these elements. The fact that zooplankton can drive the carbon and nutrient cycles by recycling or export of their products makes study of the fates of these products necessary. Furthermore, zooplankton outfluxes give information on the fates of pollutants, as zooplankters can transport elements and unassimilated organisms (even still living) through the sinking of their products (Fowler and Fisher, 1983). Pollutants can be concentrated in these products and transferred by ingestion to other organisms (Fowler, 1977). Reviews already exist on zooplankton-dissolved products (Corner and Davies, 1971; Le Borgne, 1986) and on zooplankton faecal pellets (Turner and Ferrante, 1979; Fowler and Knauer, 1986; Fowler, 1991; Noji, 1991; Turner, 2002). The purpose of this review is not to repeat what has been discussed earlier. The information compiled is focused on copepods, dominant mesozooplankters in the world ocean, in terms of both abundance

256

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(55%–95%, Longhurst, 1985) and biomass (up to 80%, Kiørboe, 1998). However, comparison with other groups is attempted, and for processes that are common for all zooplankton and for which available information refers to mixed zooplankton rather than copepods per se, the term ‘‘zooplankton’’ instead of ‘‘copepods’’ is used. The analysis of all PM and DM products is based on their nature, the factors controlling their rate and their fate, and finally their role, particularly in their relative importance in the carbon and nitrogen cycles. Note that this role depends on the variability of the zooplankton biomass for which the reader can refer to other reviews (e.g., Mauchline, 1998). An evaluation of this comparative information in terms of needs and cautions to be taken for future studies is also attempted. This can provide appropriate information on the strategy chosen for experimental work and can help in the modeling of ecosystems by identifying the relative importance of all processes implicated, by improving their parameterization, and by defining the forcing factors.

2. NATURE OF COPEPOD OUTFLUXES Copepods (and other zooplankters) produce DM actively by excretion and respiration (DM passively released from PM is discussed later [Section 4.1]). Respiration produces only CO2, whereas excretion implicates many products, as detailed below. Excretion is considered here to be the actively released liquid forms of remaining end products of metabolism (assimilated material). Indirect release of solutes, such as from phytoplankton, caused by sloppy feeding of copepods, are not a copepod outflux and therefore will not be discussed. Aspects of metabolic pathways and the anatomy related to excretion can be found in Regnault (1987), concerning crustaceans, and in Wright (1995).

2.1. Nature of excretion 2.1.1. Chemical forms of nitrogen excretion Ammonia constitutes from 50% to 90% of the total nitrogen excreted by zooplankton (ammoniotelic animals) (Roger, 1978; Regnault, 1987; Le Borgne, 1986; Le Borgne and Rodier, 1997, and references therein). The form of ammonia excreted by zooplankton, whether unionized ammonia (NH3) or ammonium ions (NHþ 4 ), is not certain (for crustaceans, see Regnault, 1987). In the following, no distinction is made between the two forms, and the chemical symbol NHþ 4 is used for simplicity. The other

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257

nitrogen-containing substances excreted by zooplankton are organic: urea (e.g., Ba˚mstedt, 1985; Miller, 1992; Conover and Gustavson, 1999) and amino acids (e.g., Gardner and PaVenho¨fer, 1982; Regnault and Lagarde`re, 1983; Dam et al., 1993). Uric acid excretion seems to be exceptional (Regnault, 1987, and references therein), and there is no evidence of excretion of soluble proteins (Corner and Newell, 1967). There is an important variability on the proportion of organic nitrogen in total nitrogen excretion, with authors finding high (Johannes and Webb, 1965; Le Borgne, 1973, 1977) or low proportion of organic nitrogen (Corner and Newell, 1967; Corner et al., 1976; Dam et al., 1993). This variability could be explained by the experimental conditions, such as abnormally high animal concentrations, the temperature, and the animal species (Le Borgne, 1986). Another reason is the transformation of excreted organic nitrogen to ammonia by bacterial activity, which could cause an overestimate (20%) of ammonia excretion (Mayzaud, 1973). In addition, nitrogen in the food content positively influences the percentage of ammonia to total nitrogen excreted (Miller, 1992). Finally, the excretion of some substances can occur occasionally, as has been described for amino acid nitrogen, which can be excreted in ‘‘spurt events’’ of 20–60 min (Gardner and PaVenho¨fer, 1982).

2.1.2. Chemical forms of phosphorus excretion In general, more than 50% of the total phosphorus excreted by copepods is in an inorganic form, as orthophosphate (PO4) (Corner and Davies, 1971, and references therein; Roger, 1978, and references therein; Ba˚mstedt, 1985). No information was found on the chemical composition of the excreted organic fractions. In Calanus spp., the variability of the ratio of inorganic to organic phosphorus excreted relates to the food level (Butler et al., 1970). Temperature does not seem to influence this ratio (Le Borgne, 1982).

2.1.3. Chemical forms of carbon excretion Excretion of dissolved organic carbon (DOC) by copepods includes the previously mentioned organic nitrogen compounds (i.e., urea and amino acids) and organic phosphorus excretion, as well as monosaccharides and polysaccharides (Strom et al., 1997). The dissolved organic carbon excreted can be refractory as well as labile (Park et al., 1997). Although experiments characterizing the carbohydrates released by copepod excretion have yet to be performed (Park et al., 1997), it is well known that DOC is also liberated from copepod particulate products (Section 4.1.1.4) and has an important role in the DOC pool (Section 5.1.1.2 and Section 5.2.1.1).

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2.2. Nature of copepod particulate matter outfluxes 2.2.1. Faecal pellets 2.2.1.1. Peritrophic membrane Copepods produce membrane-covered faecal pellets (Gauld, 1957; Yoshikoshi and Ko, 1988). In general, a peritrophic membrane is also found in other crustaceans (shrimps, Caridea: Forster, 1953; and euphausiids: Moore, 1931), whereas it is lacking in ciliates, tintinnids (Stoecker, 1984) and gelatinous zooplankton (salps, pteropods, doliolids: Bruland and Silver, 1981). The peritrophic membrane of copepods (Ferrante and Parker, 1977; Yoshikoshi and Ko, 1988) appears to constist of chitinous microfibrils and a ground substance containing acid mucopolysaccharides and proteins, but its chitinous nature has been doubted by Honjo and Roman (1978). Several hypotheses exist concerning the role of this membrane. First, to protect the delicate midgut epithelium from damage by hard or sharp particles in the food (Yoshikoshi and Ko, 1988). Second, the peritrophic membrane of copepods would also be a means to compact the pellet content to help speedy removal of indigestible remains of food from the water where the animals are feeding (Gauld, 1957). Third, another function could be to prevent the food from passing through the gut too quickly, allowing the regulation of the intestinal transit and the assimilation rate (Reeve, 1963). Finally, the peritrophic membrane could function as a filter, allowing economic and eVective use of secreted enzymes. In any case, whatever the functional significance of the peritrophic membrane, it is not necessarily the same among copepods that have diVerent modes of life. This is shown by the thickness of the membrane: Free-living copepods, which can consume sharp-edged hard diatoms, have thick peritrophic membranes, whereas parasitic ones, which can consume mucus that is secreted by the gills of the marine bivalve host, have much thinner membranes (Yoshikoshi and Ko, 1988). 2.2.1.2. Shape, size, colour, content, and chemical composition Most copepods have cylindrical pellets, as do euphausiids (Gauld, 1957; Fowler and Small, 1972; Martens, 1978; Cade´e et al., 1992; Yoon et al., 2001). DiVerent shapes have been identified for other zooplankters: rectangular (salps), coil and conical (pteropod and heteropod molluscs) (Bruland and Silver, 1981; Yoon et al., 2001), oval (amphipods and ostracods: review by Noji, 1991), spherical, or ovoid (Gowing and Silver, 1985). The size of zooplankton faecal pellets varies from a few micrometers for the ‘‘minipellets’’ of protozoans and small invertebrates (3–50 mm: Gowing and Silver, 1985) to several millimeters for pellets from large crustaceans (Fowler and Small, 1972) and gelatinous zooplankton (Bruland and Silver,

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259

1981). The size of copepod faecal pellets increases with the ingestion rate (Dagg and Walser, 1986; Huskin et al., 2000). The size of the animal also influences positively the size of pellet (PaVenho¨fer and Knowles, 1979; Harris, 1994; Uye and Kaname, 1994); however, this relationship is considered to be weak (Feinberg and Dam, 1998). Food concentration can influence the pellet size, positively (up to a saturation point) (Gaudy, 1974; Ayukai and Nishizawa, 1986; Bathmann and Liebezeit, 1986; Dagg and Walser, 1986; Butler and Dam, 1994; Feinberg and Dam, 1998; Tsuda and Nemoto, 1990; Huskin et al., 2000) or negatively, depending on the food type ingested (Feinberg and Dam, 1998). The quality of food also influences the size of faecal pellets, as shown by diVerent laboratory diets (diatoms, flagellates, dinoflagellates, or ciliates) (Turner, 1977; Hansen et al., 1996a; Feinberg and Dam, 1998) and in field studies (Frangoulis et al., 2001). The colour of faecal pellets will depend on the diet of the animal: olivegreen to brown from diatoms (Feinberg and Dam, 1998; Urban-Rich et al., 1998), bright green from photosynthetic flagellates, pink or orange from heterotrophic dinoflagellates, white from ciliates (Feinberg and Dam, 1998), and red from a carnivorous diet (Urban-Rich et al., 1998). Numerous studies that have examined the faecal pellet content show that it varies from a fluVy, amorphous material, where phytoplankton cells are only occasionally observed, to a sac filled exclusively with intact, and even viable, phytoplankton cells (Porter, 1973; Eppley and Lewis, 1981; Bathmann et al., 1987; references in the review by Turner, 2002). The chemical composition of faecal pellets is complex. Several pigments (Currie, 1962; Bathmann and Liebezeit, 1986; Head and Harris, 1992, 1996; Head and Horne, 1993; Head et al., 1996; Stevens and Head, 1998) as well as lipids, amino acids, hydrocarbons, sugars, sterols, wax esters, pigments, trace elements, radionuclides, and alumino-silicate particles have been found in faecal pellets (reviews by Fowler and Knauer, 1986; Fowler, 1991; Turner, 2002). Herbivorous copepods can produce toxin-containing faecal pellets after ingesting toxic algae (Maneiro et al., 2000; Wexels Riser et al., 2003). Considering that the aim of this study is the role of the carbon and nutrients cycle, we discuss only the C, N, and P content of pellets. The C, N, and P composition (Table 1) depends on food quantity and quality (Johannes and Satomi, 1966; Honjo and Roman, 1978; Anderson, 1994; Urban-Rich et al., 1998), animal size (Small et al., 1983), animal species, animal assimilation eYciency, and pellet compaction (e.g., Gonza´lez and Smetacek, 1994). Some studies make estimations of faecal C vertical flux using such literature values. Caution should be taken using literature values expressed as an amount of the element per pellet (e.g., nanograms C pellet1) or per pellet volume (e.g., nanograms C mm3), as a large range of variation (more than one order of magnitude) is found among these data (Table 1).

260 Table 1 Carbon, nitrogen and phosphorus content of fresh copepod faecal pellets. In studies with mixed copepod species, species described are the most dominant Faecal pellet composition

Faecal pellet producer Single copepod species Acartia clausi Acartia clausi Acartia tonsa Acartia tonsa Acartia tonsa Acartia tonsa

Calanus hyperboreus Calanus pacificus Eucalanus pileatus

Coccolithophores culture Natural food (Woods Hole, Massachusetts) Thalassiosira weissflogii culture Thalassiosira weissflogii culture Rhodomonas baltica culture Thalassiosira sp. and Isochrysis galbana culture Natural food (Barents Sea) Natural food (NE Greenland shelf) Natural food (NE Greenland shelf) Thalassiosira weissflogii culture Rhizosolenia alata culture

C

N

P

Weight ratios

% DW

ng pel1

—

133–276 0.53–1.10* —

13–28 0.05–0.11* —

—

—

—

—

96–187 0.38–0.75* —

15–38 0.06–0.15* —

—

—

—

—

—

0.17–2.50 —

—

0.06–0.78

3.2–7.1

—

—

—

—

0.28

—

—

—

—

—

—

—

—

—

0.39

—

—

—

—

—

—

—

—

—

—

—

—

—

—

10–16

—

—

—

—

0.05

—

—

0.01

—

7.0

—

—

—

377

0.05*

—

22

<0.01*

—

—

—

—

Gonza´lez and Smetacek, 1994 Daly, 1997

—

1450

0.04*

—

125

<0.01*

—

28.5

—

—

Daly, 1997

—

—

—

—

—

—

—

7.5

—

—

—

—

—

—

—

—

—

14.8

—

—

Downs and Lorenzen, 1985 PaVenho¨fer and Knowles, 1979

pg mm3

ng % DW pel1 pg mm3

% DW C:N

C:P N:P

Source

Honjo and Roman, 1978 Honjo and Roman, 1978 Butler and Dam, 1994 Hansen et al., 1996a Hansen et al., 1996a Checkley and Enzeroth, 1985

C. FRANGOULIS ET AL.

Calanus finmarchicus Calanus glacialis

Food conditions (area, if natural food conditions)

Pontella meadii Temora stylifera Temora spp. Mixed copepods Pseudocalanus spp., Temora longicornis Clausocalanus spp., Euchaeta spp., Orthona spp., Oncaea mediterranea Calanus finmarchicus, Oithona similis, Pseudocalanus elongatus, Temora longicornis, Calanus helgolandicus, Centropages typicus, Euchaeta marina, Euchirella rostrata Mesozooplankton Copepods

Natural food (NE Greenland shelf) Natural food (Galveston Bay, Texas) Hymenomonas elongata culture Thalassiosira sp. and Isochrysis galbana culture

—

1140

0.21*

—

70

0.01*

—

12.0

—

—

2.7

—

—

—

—

154

0.43*

—

18

0.05*

—

—

—

—

—

Thalassiosira weissflogii culture Natural food (East Pacific Ocean oV California)

25.0

—

—

3.0

29.6

—

—

Natural food (Bjornafjorden)

—

—

Natural food (NW Mediterranean Sea)

Natural food (western coast of Mexico) Mesozooplankton Copepods Natural food (Irish Sea) Mesozooplankton Copepods Natural food (oV Bermuda)

—

—

Daly, 1997

4.8

—

—

Turner, 1979

—

8.3

—

—

Abou Debs, 1984

—

—

8–25

—

—

Checkley and Enzeroth, 1985

—

—

—

7–9

—

—

Morales, 1987

4.8

—

—

—

6.1

—

—

Small et al., 1983

0.06

—

—

—

—

—

—

Gonza´lez et al., 1994

24.8–26.3 —

—

5.3

—

—

0.3

12.0–27.0 —

—

—

—

—

—

—

56–145 —

—

9–19 —

—

—

—

—

—

0.01–0.25 —

—

—

—

4.9–6.0

79.2 17.2 Marty et al., 1994

—

—

Andrews et al., 1984

6.2–10.4 —

—

Claustre et al., 1992 Urban-Rich et al., 1998

—

—

—

—

ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES

Metridia longa

*Estimated mean values using average volume.

261

262

C. FRANGOULIS ET AL.

2.2.2. Carcasses and moults Copepod carcasses are distinguished from live animals by their condition, ranging from slight damage or a few missing appendages to empty broken exoskeletons (Haury et al., 1995). Copepod carcasses are also more transparent than copepods collected alive because of a loss of the dorsal muscle and internal tissue (Harding et al., 1973; Genin et al., 1995; Haury et al., 1995). The exoskeleton is often split between the cephalic and thoracic segments (Wheeler, 1967; Harding et al., 1973). Individuals broken or partially crushed by net towing can be recognized by the loss of some appendages (Haury et al., 1995), whereas the remaining appendages are in good condition (i.e., there is no loss of segments from the swimming legs, and tissue is present in the first antennae) (Wheeler, 1967). Although moults have similar appearance to carcasses because the exoskeleton is also split between the cephalon and thoracic segments, they can be distinguished from recently formed carcasses because they do not contain residual tissue at all and the exoskeleton is often complete at least for freshly produced moults. However, highly degraded moults may be diYcult to distinguish from carcasses.

2.2.3. Dead eggs Copepod eggs that do not hatch will be considered as ‘‘dead eggs.’’ This includes unfertilized eggs (oocytes), sterile eggs, and dead eggs sensu stricto. Unfertilized eggs are easily distinguished from fertilized eggs, as only the latter have two or more visible nuclei (Ianora et al., 1992; Poulet et al., 1994). The two types of resting (dormant) eggs, subitaneous (nondiapause) and quiescent, can lead to wrong estimates of egg mortality, as these eggs can hatch after long periods (from a few days up to 40 years: Marcus et al., 1994; Marcus, 1996; Marcus and Boero, 1998), whereas the estimates of egg mortality are carried out over short periods. However, most resting eggs have typical spiny coverings and can be distinguished (Belmonte et al., 1997). The C content of copepod eggs varies between 15 and 6000 ng C egg1 (Kiørboe et al., 1985; review by Huntley and Lopez, 1992; Kiørboe and Sabatini, 1994, and references therein). Nitrogen content is 9 ng N egg1 for Acartia tonsa eggs (Kiørboe et al., 1985) and 5 ng N egg1 for Paracalanus parvus eggs (Checkley, 1980). Egg carbon or nitrogen content is estimated as a proportion of egg volume (Checkley, 1980; Huntley and Lopez 1992; Hansen et al., 1999).

263

ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES

3. FACTORS CONTROLLING THE RATE OF COPEPOD OUTFLUXES The range of rates of copepod outfluxes of dissolved and particulate matter is shown in Table 2. The weight-specific posthatch mortality rate of Table 2 is based on direct estimates from two studies (Kiørboe and Nielsen, 1994;

Table 2 Order of magnitude of copepod weight-specific outflux rates Process rate Process

gN gNcop1 d1

gC gCcop d1

Excretion

0.13–0.23

0.09–0.12 (DOC) — 0.04–0.08 (DOC) —

Small et al., 1983

—

Checkley et al., 1992, and references therein Small et al., 1983 Steinberg et al., 2000 Daly, 1997; Small et al., 1983 Review by Corner et al., 1986; Small and Ellis, 1992

0.06–0.36 — 0.01–0.48 (generally <0.20) 0.04–0.25 Respiration Faecal pellet production

— — 0.01–0.02 —

Posthatch 0.03–0.14a mortality Egg mortality b <0.01 to 1.20 b 0.01 to 0.68b (average 0.20) —

Moulting

— —

0.06–0.13 0.04–0.18 0.02–0.08 0.01–0.84 (generally <0.24) 0.03–0.21a — —

Source

Verity, 1985 Steinberg et al., 2000 Review by Corner and Davies, 1971

Kiørboe and Nielsen, 1994; Roman et al., 2002 Checkley et al., 1992, and references therein; Campbell et al., 2001 Review by Mauchline, 1998

<0.01 to 0.87 b Park and Landry, 1993, and (generally references therein; Campbell <0.07) et al., 2001 average 0.37b,c Peterson and Dam, 1996 <0.01–0.02 Vidal, 1980

cop: copepod. a

Range could be larger and estimated by growth rates, see text for details.

b

Calculated from female weight-specific egg production rate (references in table) and egg hatching success (Ianora et al., 1992; Jo´nasdo´ttir, 1994). Adult copepod females constitute generally less than 10% of the copepod population (Dauby, 1985); therefore, egg mortality rate constitutes, for the whole population, 10 times fewer body losses. c For herbivorous species, assuming that all assimilated nitrogen is channeled into egg production in adult females.

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C. FRANGOULIS ET AL.

Roman et al., 2002), and thus is too limited in range (and environments) to allow us to examine patterns. Growth rates could give a good indication of what weight-specific mortality rates look like in copepods across the globe. In these two studies, mean growth rate, averaged over 1 (Kiørboe and Nielsen, 1994) or 4 (Roman et al., 2002) years, is almost equal to mean weight-specific mortality rate (diVerence less than 0.005 d1). This indicates that we could use the global syntheses of weight-specific growth rates for marine copepods (Hirst and Lampitt, 1998; Hirst and Bunker, 2003; Hirst et al., 2003) and conclude from these syntheses that average weight-specific mortality rate can be expected to be close to 0.14  0.21 d1 (Hirst et al., 2003). The ranges for posthatch mortality, respiration, excretion, and faecal pellet production have the same order of magnitude and are higher than those of moulting and egg mortality (Table 2). A comparison of simultaneous measures of rates of respiration, excretion, and faecal pellet production was made by Small et al. (1983). They concluded that on nitrogen-specific basis, faecal pellet production rate represents a body loss that is more than eight times less that of excretion, whereas on a carbon basis, faecal pellet production rate represents a body loss more than twice less than that lost in respiration. However, the relative importance of these processes in the carbon and nutrient cycle will depend not only on their rate but also on their nature and fate as well as on copepod biomass variability.

3.1. Factors controlling the rate of copepod dissolved matter excretion The three main factors influencing excretion of DM are temperature, individual body mass (size) (Ikeda, 1985), and the amount of food (Le Borgne, 1986). The factors discussed below are from literature on N and P excretion and not on DOC excretion (unless specified), for which less information exists. However, for DOC excretion, common controlling factors with N and P excretion can be expected as for all metabolic processes (e.g., temperature, body mass).

3.1.1. Factors controlling the excretion rate 3.1.1.1. Temperature In all zooplankton, excretion is positively related to water temperature for N, P (Hargrave and Geen, 1968; Nival et al., 1974; Roger, 1978; Ikeda, 1985; Ikeda et al., 2001), and DOC (Steinberg et al., 2000). Most frequently, the relationship between excretion (as for other metabolic rates) and temperature in marine zooplankton is described by Q10 (Prosser, 1961). The values of

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265

Q10 for copepod excretion in the marine environment range from 1.8 to 2.0 for ammonia and from 1.6 to 1.9 for phosphate excretion rates (Ikeda et al., 2001). 3.1.1.2. Body mass (size) There is a positive, nonlinear relationship between the excretion rate per individual and the body mass (Mayzaud, 1973; Nival et al., 1974; Ikeda, 1985; Verity, 1985; Ikeda et al., 2001). 3.1.1.3. Faunistic composition Faunistic composition influences excretion; however, in some cases, this factor can be partly (or even totally) caused by body mass variations. There are diVerences in excretion rates between species (even of the same genus) (e.g., Gaudy et al., 2000), stages, and sexes (e.g., Butler et al., 1970). 3.1.1.4. Food concentration Most studies have positively related excretion to food concentration (Butler et al., 1970; Takahashi and Ikeda, 1975; Gardner and PaVenho¨fer, 1982; Kiørboe et al., 1985; Anderson, 1992; Urabe, 1993), although a negative relation (for nauplii and copepodite stage II) (PaVenho¨fer and Gardner, 1984), or even no relationship (Hernandez-Leon and Torres, 1997), has also been described. Takahashi and Ikeda (1975) found excretion increasing with food concentration (as chl a), but only up to 15 mg chl a l1, and decreasing above this level. 3.1.1.5. Food quality Copepod excretion rate has been linked positively to the food content in P (i.e., negatively to the ratio of C:P) (Gulati et al., 1995) and N (i.e., negatively to the ratio of C:N) (Anderson, 1992). Phosphorus excretion is also negatively related to the food N:P ratio (Urabe, 1993). 3.1.1.6. Biomass or density Biomass or density increase has been described as influencing the copepod excretion positively (Satomi and Pomeroy, 1965; Nival et al., 1974) or negatively (when density exceeded 400 copepods l1) (Hargrave and Geen, 1968). For Satomi and Pomeroy (1965), an increase or decrease can be observed depending on species or the other factors aVecting excretion. 3.1.1.7. Light Artificial light, compared to darkness, has a positive eVect on nitrogen (Mayzaud, 1971) and phosphorus excretion (Fernandez, 1977). However, below a certain threshold of light intensity, no excretion rate increase is observed (review by Le Borgne, 1986).

266

C. FRANGOULIS ET AL.

3.1.1.8. Salinity Salinity aVects excretion in some copepod species (Hargrave and Geen, 1968). However, Gaudy et al. (2000) showed that salinity has no eVect on Acartia clausi, whereas for Acartia tonsa, there is an eVect when increasing the salinity that can be positive or negative, depending on temperature. 3.2. Factors controlling the rate of copepod particulate matter outfluxes 3.2.1. Factors controlling the faecal pellet production rate 3.2.1.1. Body mass Faecal pellet production rate has been described as being positively related to animal mass (Reeve, 1963; PaVenho¨fer and Knowles, 1979). This is related to the positive relationship between the faecal pellet production rate and ingestion rate (Corner et al., 1972; Gaudy, 1974; Gamble, 1978; Huskin et al., 2000; Nejstgaard et al., 2001), with the latter increasing with animal mass (PaVenho¨fer and Knowles, 1978). 3.2.1.2. Copepod faunistic composition There are diVerences in the rate of faecal pellet production among copepod species (Daly, 1997). The age of the animal has been found to aVect faecal pellet production rate; Centropages typicus females decrease their faecal pellet production with age (Carlotti et al., 1997). Female copepods generally produce more pellets than males (Marshall and Orr, 1972), but this may be a result of diVerences in mass. Faecal pellet production rate, expressed in terms of pellet number produced per individual, is higher in copepods (Gamble, 1978; Honjo and Roman, 1978; Ayukai and Hattori, 1992) than in salps (Madin, 1982) and euphausiids (Ayukai and Hattori, 1992). However, these groups show similar levels in terms of N or C produced per dry weight of individual (Small et al., 1983). 3.2.1.3. Food concentration and quality The food concentration was found to influence positively faecal pellet production rate, at least for copepodite V and adult copepods (as discussed below, the only study found on earlier stages indicated no influence of food concentration). A positive curvilinear relationship between food concentration (number of diatom cells) and faecal pellet production rate was reported for Calanus helgolandicus females and stage V copepods (Corner et al., 1972), for Calanus finmarchicus females (Marshall and Orr, 1955), for A. tonsa females (Butler and Dam, 1994), and for Paracalanus aculeatus females (PaVenho¨fer et al., 1995). PaVenho¨fer (1994) did not find such a relation for early copepodites (CII) of Eucalanus pileatus, although it was present in

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267

adults. Food quality in terms of size, type, and age has been reported to influence faecal pellet production of C. finmarchicus females (Marshall and Orr, 1955). The faecal pellet production rate of C. helgolandicus when fed with dinoflagellates shows higher or lower rates than when fed with diatoms, depending on the dinoflagellate species (Huskin et al., 2000; Kang and Poulet, 2000). However, much lower rates are reported when they are fed with coccolithophores (Huskin et al., 2000) or heterotrophic flagellates (Feinberg and Dam, 1998). Feeding history can also influence faecal pellet production rate, as a higher rate was observed in C. finmarchicus females coming from a low food environment than those coming from a high food environment (Rey et al., 1999). 3.2.1.4. Temperature and light Marshall and Orr (1955) and Carlotti et al. (1997) observed an increase in the faecal pellet production rate with temperature for Calanus finmarchicus (between 5 8 and 15 8C) and Centropages typicus (between 15 8 and 20 8C). Marshall and Orr (1955) also observed that faecal pellet production was higher in darkness. Because of the light factor, the diel variation of faecal pellet production rate observed in the North Sea may be explained by the influence of light as assumed by Martens and Krause (1990). 3.2.2. Factors controlling the posthatch mortality rate Posthatch mortality of copepods (and other zooplankters) has numerous causes. These can be internal (developmental stage, senescence, genetic background), external (starvation, predation, parasitism), or a combination of external and internal factors (e.g., eYciency of enzymatic activity is a function of temperature) (reviews by Genin et al., 1995; Ohman and Wood, 1995; Haury et al., 1995, 2000; Gries and Gu¨de, 1999). Posthatch mortality rates increase with temperature in both sac and broadcast-spawning copepods (Hirst and Kiøboe, 2002). Mortality in sac spawners is independent of body weight, whereas in broadcasters it decreases slightly with body weight. The proportion of total adult mortality caused by predation is independent of temperature, on average accounting for around two-thirds to three-quarters of the total (Hirst and Kiørboe, 2002). 3.2.3. Factors controlling the moulting rate In copepods, the moulting rate increases with temperature, food concentration, and growth rate (Marshall and Orr, 1972; Vidal, 1980; Souissi et al., 1997; Hirst and Bunker, 2003) and decreases with body mass (Souissi et al., 1997; Twombly and Tish, 2000) and age (Lopez, 1991). High food

268

C. FRANGOULIS ET AL.

concentration in situ has a much lower eVect on moulting rate than in laboratory observations at the same temperature (Campbell et al., 2001). In the presence of light, compared to darkness, the moulting rate is higher (Marshall and Orr, 1972).

3.2.4. Factors controlling egg mortality rate Egg predation by copepods themselves (egg cannibalism, Kang and Poulet, 2000; Kiørboe et al., 1988; Peterson and Kimmerer, 1994), other invertebrates such as polychaetes (Marcus, 1984; Marcus and Schmidt-Gegenbach, 1986), and fish (Landry, 1978; Redden and Daborn, 1991; Conway et al., 1994) is an important cause of egg mortality. Egg cannibalism represents between 10% and 30% of egg mortality (Kiørboe et al., 1988), whereas predation by fish has been reported to be a major cause of egg mortality (Landry, 1978). Egg mortality in copepods depends also on the food type ingested (diatoms increase and flagellates decrease mortality) (Ban et al., 1997; Ianora et al., 1995), increases with age (Jo´nasdo´ttir, 1994), and abundance of adult females and juveniles (Ohman and Hirche, 2001), but is not correlated with chl a or breeding intensity (Ianora et al., 1992; Laabir et al., 1995). Egg mortality in broadcasters is much greater than in sac spawners, because of egg hatch failure, egg sinking, higher rates of predation, and higher advection losses (Hirst and Kiørboe, 2002). Some authors (Ianora et al., 1992; Laabir et al., 1995) found no correlation between temperature and egg mortality, whereas other authors found a positive relationship (hatching success decreasing) (Uye, 1988) or a negative one (hatching success increasing) (Nielsen et al., 2002). Hirst and Kiørboe (2002), reviewing field measurements on egg mortality, concluded that egg mortality rates increase with temperature in both sac- and broadcast, spawning copepods. The importance of egg mortality as an outflux depends also on the total (dead and living) egg production rate that is aVected by species, temperature, photoperiod, and food concentration and quality (Marshall and Orr, 1952; Kiørboe et al., 1985; Bautista et al., 1994; Jo´nasdo´ttir, 1994; Jo´nasdo´ttir et al., 1995; Calbet and Alcaraz, 1996; Hopcroft and RoV, 1996; Ban et al., 1997; Kleppel et al., 1998; Campbell et al., 2001).

3.3. Relationships between the different outfluxes Many of the processes presented above are interrelated, and this is partly explained by the fact that they depend on common external (e.g., temperature, food) or internal factors (e.g., species, body mass, sex). A good positive relationship was reported between respiration and excretion, in laboratory

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269

experiments, using one predator species and a stable food type (Kiørboe et al., 1985). Also, in situ short time experiments (month or season) have established the same relation during a period dominated by one predator species or by a homogeneous population dominated by one group (Satomi and Pomeroy, 1965; Le Borgne, 1973; Gaudy and Boucher, 1983). Statistically significant relationships between phosphorus and nitrogen excretion were also reported first in laboratory experiments, using one predator species and a stable food type, and second in situ during a short period (month or season) dominated by one predator species or by a homogeneous (essentially one group) population (Le Borgne, 1973; Roger, 1978, and references therein). Wen and Peters (1994) constructed an empirical model using data from published studies and found a strong nonlinear relationship between phosphorus and nitrogen excretion rates, with small biases resulting from taxonomic diVerences. However, their model used mostly data from nonfeeding animals. The ratios of respiration to excretion and of phosphorus to nitrogen excretion (usually expressed as the atomic ratio O:N, O:P, and N:P) vary between species (Gaudy and Boucher, 1983, and references therein), between stages of development, and between type of food ingested (Conover and Corner, 1968; Le Borgne, 1986). Egg production can be related to phosphorus excretion and faecal pellet production. During egg formation, more phosphorus is retained by females, resulting in a reduced excretion of this element (Gaudy and Boucher, 1983). At 20 8C, the total egg production during the lifespan of a C. typicus female is related to their corresponding total cumulated faecal pellet production (Carlotti et al., 1997). Excretion of nitrogen and phosphorus can be related to moulting; excretion increases during moulting as, for example, phosphorus excretion in euphausiids (Ikeda and Mitchell, 1982) and ammonia excretion in decapod crustaceans (Regnault, 1987). Finally, the importance of growth, a key descriptor of copepod outflux rates, because of its relation to mortality, respiration, and moulting (Hirst and Bunker, 2003; Hirst et al., 2003), should be pointed out.

4. VERTICAL FLUX This section examines the factors controlling the vertical flux of copepod products (e.g., mg C m2 d1). In experimental studies, the vertical flux (VF) (also called ‘‘sedimentation rate’’ in zooplankton studies) is expressed as the following depth-integrated flux: Z VF ¼ 0

H

@ ðsCÞdz ¼ @z

Z 0

H

@ @C ðWa C þ Ws C  l˜ Þdz @z @z

ð1Þ

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C. FRANGOULIS ET AL.

where s is the apparent velocity, C is the concentration of the zooplankton product, wa is the vertical component of the water velocity vector, ws is the gravitational settling velocity, l˜ is the vertical turbulent diVusion coeYcient, and H is the water column height. The unit vector along the vertical (z) points downward. In plankton studies, the most commonly used term for the gravitational settling velocity is ‘‘sinking rate’’ and for the apparent velocity ‘‘sinking rate,’’ ‘‘sinking speed,’’ or ‘‘sedimentation speed’’ (physicists usually call it ‘‘deposition velocity’’ or ‘‘fall velocity’’). Hereafter the terms ‘‘sinking speed’’ and ‘‘sedimentation speed’’ are used for the gravitational settling velocity, and the apparent velocity, respectively, to separate the units of velocity and avoid confusion between terms. Sedimentation speed of dissolved matter is controlled only by water hydrodynamics (turbulent diVusion and advection). Hence, the following sections discuss the vertical flux of copepod particulate products. Various physical and biological factors aVect the sedimentation speed and the concentration gradient of zooplankton particulate products in general. Passive vertical flux is distinguished from active vertical flux related to copepod migration.

4.1. Passive vertical flux 4.1.1. Physical factors influencing the passive vertical flux of particulate matter 4.1.1.1. Sinking speed The sinking speed of a particle (ws cm s1) depends on the shape and dimension or dimensions of the particle, the water molecular viscosity, and the diVerence between particle and water densities. Depending on the particle shape, the sinking speed can be calculated from diVerent equations. For example, for spherical particles the sinking speed can be calculated using the Stokes equation: ws ¼

1 1 ðr  rÞgD2 18 m s

ð2Þ

where rs is the particle density (g cm3), r is the water density (g cm3), g is the acceleration of gravity (cm s2), D is the sphere diameter (cm), and m the water molecular viscosity (g cm1 s1). For cylindrical and elliptical particles, Komar et al. (1981) modified the Stokes equation. For cylindrical particles (as copepod faecal pellets), the equation is:

ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES

 1:664 1 2 L ws ¼ 0:0790 ðrs  rÞgL m D

271 ð3Þ

where L is the cylinder length (cm) and D is the cylinder diameter (cm). The sinking speeds of copepod particulate products are compared with those of other zooplankton in Table 3. (a) Faecal pellets. As shown above, the sinking speed of faecal pellets will depend on their shape, size, and density. Pellet width is the most influential parameter in the estimation of sinking speed compared to pellet length and density (Feinberg and Dam, 1998). The relationship to size of faecal pellets

Table 3 Comparison of the sinking speed of copepod particulate products with those of other zooplankton groups Sinking Speed Product

Group

m d1

cm s1

Source

Faecal pellet

Copepods

25–250

0.03–0.29

Appendicularians Doliolids

25–166 41–405

0.03–0.19 0.05–0.47

Euphausiids

15–860

0.03–1.00

Pteropods

65–1800

0.08–2.08

Heteropods Salps

120–650 40–2700

0.14–0.75 0.05–3.13

Copepods

35–720

0.04–0.83

Amphipods Chaetognaths Cladocerans Euphausiids

875 435 120–160 1760–3170

1.01 0.50 0.14–0.19 2.04–3.67

Moults

Ostracods Salps Siphonophores Copepods Euphausiids Euphausiids

400 165–250 240 30 130–180 50–1020

0.46 0.19–0.29 0.28 0.03 0.15–0.21 0.06–1.18

Feeding nets

Larvaceans

120

0.14

Smayda, 1971; Turner, 1977; Honjo and Roman, 1978; Small et al., 1979; Bienfang, 1980; Yoon et al., 2001 Gorsky et al., 1984 Bruland and Silver, 1981; Deibel, 1990 Fowler and Small, 1972; Youngbluth et al., 1989; Cade´e et al., 1992; Yoon et al., 2001 Bruland and Silver, 1981; Yoon et al., 2001 Yoon et al., 2001 Bruland and Silver, 1981; Madin, 1982; Yoon et al., 2001 Apstein, 1910; Gardiner, 1933; Seiwel and Seiwel, 1938 Apstein, 1910 Apstein, 1910 Apstein, 1910 Mauchline and Fisher, 1969; Fowler and Small, 1972 Apstein, 1910 Apstein, 1910 Apstein, 1910 Kiørboe et al., 1988 Mauchline and Fisher, 1969 Mauchline and Fisher, 1969; Nicol and Stolp, 1989, and references therein Hansen et al., 1996b

Carcasses

Eggs

272

C. FRANGOULIS ET AL.

has been shown by several workers (Smayda, 1969; Turner, 1977; Small et al., 1979; Komar et al., 1981; Alldredge et al., 1987; Frangoulis et al., 2001; Yoon et al., 2001). The pellet density depends strongly on the pellet size (inverse nonlinear relationship) and, to a lesser degree, on the type of material ingested (Table 4), whereas food concentration has only a small eVect on pellet density (Feinberg and Dam, 1998). In the study of Feinberg and Dam (1998), pellet density was measured directly. However, most studies use indirect density estimations based on the pellet dimensions and their sinking speed, which are much easier to obtain than direct pellet density measures. Yoon et al. (2001) compared the density estimates using the equations of Komar et al. (1981), Stokes’ law, and Newton’s second law. They concluded that the relationship of Komar et al. gave the highest-density values followed closely by those of Newton’s second law (diVerence 0.03 g cm3), whereas Stokes’ law underestimated the density (when used for nonspherical faecal pellets). They also concluded that the relationship of Komar et al. is appropriate for fresh faecal pellets from copepods feeding on natural food, but may not be representative of other faecal pellets (i.e., not fresh or from organisms feeding on cultured food). The peritrophic membrane of copepods increases the sinking speed by providing a smooth covering that decreases frictional drag (Honjo and Roman, 1978). In addition, the peritrophic membrane probably contributes to compactness because the pellet volume increases when it is removed (Noji et al., 1991). (b) Other particulate products. The sinking speed of other particulate products will depend on the same factors described above (dimension, form, particle density, water density and viscosity). The dimension and density eVects have been shown for euphausiid carcasses and moults (Mauchline and Fisher, 1969; Nicol and Stolp, 1989). It is important to notice that the diVerential sinking speed of particles can cause aggregation, by collision of faster with slower sinking particles (McCave, 1984; Kiørboe, 1997) creating ‘‘marine snow’’ (i.e., flocculent amorphous aggregates >0.5 mm in diameter). The latter is a major source of particulate flux (Fowler and Knauer, 1986; Turner, 2002), and a large part of it consists of zooplankton products (e.g., faecal pellets, moults) (e.g., Silver et al., 1978; Alldredge and Gotschalk, 1988; Bochdansky and Herndl, 1992; Alldredge, 1998). 4.1.1.2. Vertical advection Upwelling events could counteract the sedimentation of particles (Alldredge et al., 1987), as vertical upward velocities of water during upwelling vary generally from 2 to 84 m d1 (<0.01 to 0.10 cm s1) (higher values can be found locally or temporally) (Wroblewski, 1977; Jacques and Tre´guer, 1986;

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273

Sarhan et al., 2000) and thus are of the same range as the sinking speeds of some zooplankton products (Table 3). However, this does not always negatively aVect their downward vertical flux, at least regarding faecal pellets, as faecal pellet production increases during upwelling conditions, enhancing the downward vertical flux (Knauer et al., 1979). 4.1.1.3. Stratification and turbulent diffusion Enhanced vertical stratification occurring at the thermocline can decrease the sedimentation speed of particles (Gonza´lez et al., 1994). When such a strong stratification occurs, the water density and molecular viscosity increase rapidly with depth (i.e., the sinking speed of particles decreases, see Equations [2] and [3]), and the vertical turbulent diVusion coeYcient decreases (see Equation [1]). As a result, particles can accumulate at the thermocline (Krause, 1981; Youngbluth et al., 1989). Turbulence resulting from storms considerably enhances the transfer of particles through the thermocline (Krause, 1981). Storms can prolong the residence time of particles in the mixed layer. Turbulent mixing prolongs the residence time of particles directly through the water movement transfer and indirectly through the physical degradation by breakdown, which, by reducing their size, decreases their sinking speed (for faecal pellets; Alldredge et al., 1987). Finally turbulence can also enhance aggregation of particles (McCave, 1984) and formation of ‘‘marine snow’’ (Kiørboe, 1997). 4.1.1.4. Molecular diffusion and physical degradation by leaking (a) Faecal pellets. Although all workers agree that broken faecal pellets have a higher leaking rate, the information concerning this leaking rate is contradictory. Jumars et al. (1989) suggested from model calculations that most solutes diVuse out of faecal pellets within several minutes. Møller et al. (2003) found that freshly expelled faecal pellets lost more than 20% of their carbon content within the first hour, but the release rate decreased afterward. Urban-Rich (1999) reported an 86% reduction in the faecal pellet DOC pool within 6 h. However, other authors suggested longer time scales. Alldredge and Cohen (1987) found that the peritrophic membrane of faecal pellets is an eYcient diVusion barrier. Lampitt et al. (1990) showed that in 28 h, from less than 5% up to 15% of the pellet C is released as DOC from intact and broken pellets, respectively. Johannes and Satomi (1966) observed that intact faecal pellets, in the absence of bacteria, after 4 days lost 50% of their carbon content by leaking, especially when incubated in the dark. Strom et al. (1997) did not observe a DOC release from intact faecal pellets, whereas broken faecal pellets released DOC on time scales of hours or days, which was immediately taken up by bacteria.

274

Table 4 Copepod faecal pellet sinking speed and density (fresh faecal pellets) Faecal pellet producer Single copepod species Acartia clausi A. tonsa A. tonsa A. tonsa A. tonsa A. tonsa A. tonsa A. tonsa A. tonsa A. tonsa

FP density (g cm3)

Food conditions (area, if natural food conditions)

T 8C

S

Source

74 –210 80–150 — 33 32 (high) 27 (low) 20 (high) 28 (low) 20 (high) 24 (low) 27 (high) 23 (low) 17 (high) 21 (low) 30 (high) 68 (low) 45

— — 1.15 1.13 1.11

Flagellates culture Coccolith. culture Diatoms culture Diatom 1 culture Diatom 2 culture

15 15 — — —

33.1 — — — —

Smayda, 1971 Honjo and Roman, 1978 Butler and Dam, 1994 Feinberg and Dam, 1998 Idem

1.10 (high) 1.11 (low) 1.15

Flagellate 1 culture

—

—

Idem

Flagellate 2 culture

—

—

Idem

1.14

Heter. Dinofl. culture

—

—

Idem

1.20

Heter. flagel. 1 culture

—

—

Idem

Heter. flagel. 2 culture

—

—

Idem

Ciliates culture

—

—

Idem

Natural food (oV Monaco)

14

—

Natural food (flagellatesa, oV Newfoundland) Natural food (diatomsa, oV Newfoundland) Coccolith. culture Diatoms culture

—

—

Small et al., 1979; Komar et al., 1981 Urban et al., 1993

—

—

Urban et al., 1993

15 15

— Honjo and Roman, 1978 29.2 Bienfang, 1980

Anomalocera pattersoni Calanus finmarchicus C. finmarchicus

25–220

1.12 (high) 1.17 (low) 1.13 (high) 1.12 (low) 1.15

—

1.19

—

1.11

C. finmarchicus Calanus sp.

180–220 70–171

— 1.17

A. tonsa

C. FRANGOULIS ET AL.

FP sinking speed (m d1)

51–152 18–153 15–125

1.11 — —

Flagellates culture Diatoms culture Flagellates culture

15 22 22

29.2 34.5 34.5

Bienfang, 1980 Turner, 1977 Turner, 1977

37–251

1.31–1.45

Natural (SBNS)

25

31.2

Frangoulis et al., 2001

15–150

1.28

Natural (oV Monaco)

14

—

Small et al., 1979; Komar et al., 1981

26–159

1.25

Natural (NE Atlantic)

18

—

Yoon et al., 2001

In studies with mixed copepod species, the species described are the most dominant. Coccolith.: Coccolithophores, FP: faecal pellet, Diatom 1: Thalassiosira weissflogii, Diatom 2: Chaetoceros neogracile, Flagellate 1: Rhodomonas lens, Flagellate 2: Tetraselmis sp., Heter. Dinofl.: Heterotrophic dinoflagellate, Heter. flagel., Heterotrophic flagellate, Heterotrophic flagellate 1: Cafeteria sp., Heterotrophic flagellate 2: Oikomonas sp., Low: low food concentration, High: high food concentration (distinction between high and low food concentration is made only when it was significant at P < 0.05), SBNS: Southern Bight of the North Sea, a

Dominant phytoplankton group.

ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES

Calanus sp. Pontella meadii P. meadii Mixed copepods Temora longicornis, Pseudocalanus elongatus, Acartia clausi, Centropages hamatus Clausocalanus arcuicornis, A. clausi, C. typicus, Coryceaus typicus Copepods (>500 mm)

275

276

C. FRANGOULIS ET AL.

Several explanations exist for the discrepancies between the studies cited above. First, some studies were not experimentally designed to allow estimation of leakage during the period immediately following release, as in Møller et al. (2003). Second, food concentration diVerences could also explain the divergence of those studies. Head and Harris (1996) observed no leak of DOC, DON, pigments, or biogenic silica after 4 days from faecal pellets originating from high food conditions, whereas under low food conditions, for the same period, leaking occurred. Møller et al. (2003) suggested that the high leakage rate they found could be associated to the high food concentrations of diatoms in their experiment. Other possible explanations are the nonlinearity of the leaking process and incubation diVerences (i.e., temperature diVerences and the use of a stationary or a spinning incubator allowing simulation of the free-falling of particles). Lee and Fisher (1994) examined the leaking of carbon from faecal pellets and reported that temperature increase and the use of a spinning wheel increases the leaking rate. Moreover, leaking rate is high during the first days and decreases progressively. On nutrients release, Head and Harris (1996) observed 20%–30% of the total nitrogen leaking out of copepod faecal pellets in 2 days. However, this was observed only for pellets produced under low food concentration, whereas no leaking was observed even after 4 days for pellets produced under high food concentration (Head and Harris, 1996). (b) Carcasses. Degradation of copepod carcasses generally starts with a rapid leaking of soluble internal organic compounds during the first 24 h of decomposition (Seiwel and Seiwel, 1938; Harding et al., 1973; Lee and Fisher, 1992, 1994). With a stationary incubator, the leaking rate of carcasses was faster than that of faecal pellets at both low (2 8C) and high temperatures (18 8C). However, with a spinning incubator, at high temperatures the leaking rate of carcasses and faecal pellets were similar (Lee and Fisher, 1994). 4.1.2. Biological factors affecting the passive vertical flux of particulate matter The biological factors that influence the passive vertical flux of copepod (and other zooplankton) products are production and biodegradation. The factors influencing the production rate of copepod products were examined earlier (Section 3). Biodegradation depends on zooplankton itself, nekton, and microorganisms (hereafter biodegradation is considered to include consumption of zooplankton products). 4.1.2.1. Zooplankton and nekton mediated biodegradation (a) Coprorhexy and coprochaly. Copepods aVect the degradation of their own pellets by coprorhexy and coprochaly. Coprorhexy is the fragmentation of faecal pellets without ingestion, whereas coprochaly is the destruction of

ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES

277

the peritrophic membrane (Lampitt et al., 1990; Noji et al., 1991). These processes occur within hours, and thus they are faster than biodegradation by microorganisms, which takes days or weeks (Section 4.1.2.2). Their combined eVect could reduce faecal pellet sinking speed from 25% to 50% (Noji et al., 1991). In addition, they increase the leaking of dissolved elements (Lampitt et al., 1990), as well as the substrate for microorganisms (larger surface area to volume ratio and greater porosity of less dense particles) (Noji et al., 1991). (b) Coprophagy. Coprophagy is the ingestion of faecal material. Copepods have been reported to practice coprophagy on their own faecal pellets (Lampitt et al., 1990). Coprophagy is explained by the nutritive value of faecal pellets, as marine organisms can obtain a substantial fraction of the organic material required for maintenance metabolism by ingesting faecal pellets (Frankenberg and Smith, 1967; PaVenho¨fer and Knowles, 1979; Gonza´lez and Smetacek, 1994). The coprophagy rate will depend on the type of pellets and the type of animal (Frankenberg and Smith, 1967). First, faecal pellet type in terms of size, sinking speed, and carbon–nitrogen content influences this rate. For the same amount of faecal matter produced, several small pellets have more chances of being ingested (than one big faecal pellet), and their slower sinking speed increases this probability (PaVenho¨fer and Knowles, 1979). The coprophagy rate was found to be positively related to the carbon and nitrogen content of faecal pellets (Frankenberg and Smith, 1967). Second, depending on the type of animal, high or low coprophagy rate (or even absence of coprophagy) can be found in copepods (Noji et al., 1991), as in other marine animals (Frankenberg and Smith, 1967). As in the case of coprorhexy and coprochaly, coprophagy will finally reduce the vertical flux of faecal pellets. These losses can be important at times, as copepods, particularly the genus Oithona, may constitute a ‘‘coprophagous filter’’ that significantly reduces the vertical flux of faecal pellets (Gonza´lez and Smetacek, 1994; Gonza´lez et al., 1994). Oncaea seems to play a similar scavenging role: It has been observed to feed on sinking larvacean houses (Alldredge, 1972; Alldredge and Silver, 1988) and is probably also capable of intercepting sinking marine snow and faeces (Skjoldal and Wassmann, 1986). The biomass ratio between such essentially pelletreworking copepods (e.g., Oithona) and essentially pellet-producing copepods (calanoids) may be used to predict relative pellet retention or vertical flux of calanoid faecal pellets (Svensen and Nejstgaard, 2003). (c) Detritiphagy on other particulate products. Carcasses are known as a possible (although insuYcient) food source for copepods (Yamaguchi et al., 2002), euphausiids, fishes, or gelatinous zooplankton (Haury et al., 2000), but they are considered less nutritious than living copepods (Genin et al., 1995). Genin et al. (1995) considered that because the external

278

C. FRANGOULIS ET AL.

appearance of carcasses is almost identical to that of living individuals, the ability of predators to distinguish between them should be low. This assumption could be also expanded to dead eggs because predation on eggs exists (Section 3.2.4). However, for moults this assumption could not be true because they could be easily distinguished from live copepods by their transparency. 4.1.2.2. Biodegradation by microorganisms and remineralization (a) Faecal pellets. Turner (2002) extensively reviewed biodegradation of faecal pellets by microorganisms and concluded that this is mainly brought about by bacteria and protists that show a microbial colonizing succession on faecal pellets, initiated essentially by internal bacteria probably originating from ingestion, and depends on the diets under which the faecal pellets are produced. There is some dispute about the time needed for the degradation of faecal pellets. Some laboratory studies showed that the surface membrane of faecal pellets, produced by animals on cultured diets, is degraded after 3– 11 days at high temperatures (20 8–25 8C), whereas at lower temperatures (5 8C), membranes remain intact for 20–35 days (Honjo and Roman, 1978; Turner, 1979). The same range for membrane degradation time (4–10 days) was found by Alldredge et al. (1987) for faecal pellets from natural diets at 15 8C, whereas for total degradation of the pellets, 8–12 days were necessary. In contrast, other experiments with faecal pellets produced from natural diets (Small and Fowler, 1973), as well as culture studies (Jacobsen and Azam, 1984), have shown pellets to remain intact for several weeks at temperatures as high as 18 8C. Active remineralization of large sinking particles is, in general, low, as these particles are poor habitats for bacterial growth (Karl et al., 1988). Copepod faecal pellets are an exception, as they contain bacteria when they are produced and are also rapidly colonized by bacteria from the water column (see above). Therefore, active remineralization in faecal pellets must be more important than in other biogenic particles. Johannes and Satomi (1966) found that the C, N, and P content of faecal pellets decreases faster with bacterial activity. In addition; Jacobsen and Azam (1984) found that faecal pellet carbon remineralization by bacteria to CO2 amounts to 0.5% of the pellet carbon per day. When microzooplankton is added, this remineralization rate doubles. (b) Carcasses. Degradation of copepod carcasses by microorganisms begins on the exoskeleton and progresses into the organism through the mouth (Harding et al., 1973; Poulicek et al., 1992, and references therein). Degradation increases with temperature, but it is unlikely that the copepod

ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES

279

intestinal flora contributes significantly to degradation (Harding et al., 1973). Carcasses are rapidly covered by bacteria already existing on the living organism, followed by a colonization by external bacteria (Poulicek et al., 1992, and references therein). The degradation rate for copepod carcasses was reported to be 11 days at 4 8C and 3 days at 22 8C (Harding et al., 1973). Poulicek et al. (1992) found biodegradation rate values at 14 8C within this range, with most of the content of the carcasses (lipids and proteins) being degraded within 3 days, whereas for the chitinous structures, 8 days were necessary. Comparable degradation rates were found in Anomalocera pattersoni by Reinfelder and Fisher (1993). The biodegradation rate of carcasses is thus probably faster than that of faecal pellets (see above). Concerning remineralization, a rapid release of phosphate within 24 h following the death of copepods has been reported (Seiwel and Seiwel, 1938). From one-third to one-fourth of the total phosphate is released during the first 12 h, and the total phosphate is released in 6 days (Cooper, 1935). (c) Moults and eggs. No information was found for the time necessary for complete degradation of moults. However, we can assume that approximately 8 days are necessary, as for the chitinous structures of carcasses (Poulicek et al., 1992). Unfertilized eggs usually disintegrate fairly rapidly (<72 h) after being spawned (Jo´nasdo´ttir, 1994; Poulet et al., 1994).

4.2. Vertical migration and active vertical flux The flux of copepod products can be modified by ‘‘active’’ vertical flux because of the diel and seasonal migration of copepods. The larger copepods can undertake diel vertical migrations up to several hundreds of metres (review by Bougis, 1974). They are generally at the surface during the night and in deeper waters during the day. The percentage of the total mesozooplankton biomass (copepod dominated) constituted by diel vertical migrators is generally 10%–40% (Longhurst et al., 1990, and references therein; Zhang and Dam, 1997). Seasonal migrators overwinter at depths from 200 to 1000 m and perhaps deeper, resurfacing in spring to feed on the seasonal algal bloom. The surviving population is a small remnant of the population of the previous autumn (25%) (Longhurst and Williams, 1992, and references therein). The contribution of this process to the total vertical flux is discussed in the following section, separately for each copepod product.

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5. ROLE OF COPEPOD OUTFLUXES 5.1. Role of copepod dissolved matter outfluxes 5.1.1. Role of excretion 5.1.1.1. Role of excretion in the nutrient cycle Excretion by marine organisms is important in nutrient cycles, as it produces readily assimilable inorganic and organic nutrients for primary producers, but zooplankton excretion is particularly important because its rate is higher than those of other marine invertebrates (for nitrogen, Corner and Davies, 1971). Both inorganic and organic copepod excretion play a role in the nutrient cycle. All zooplankton organisms produce mainly inorganic forms of nutrients (Section 2.1) that are taken up by phytoplankton faster than organic forms (Corner and Davies, 1971). Inorganic nitrogen excretion is of primary importance, because ammonia is the preferred nitrogen form for many primary producers (Dugdale and Goering, 1967; Conway, 1977; Harrison et al., 1996; Lomas et al., 1996). The organic nutrients excreted by copepods can be used by bacteria and, in some cases, by phytoplankton, as, for example, urea (McCarthy, 1971), amino acids (Stephens and North, 1971), and organic phosphorus compounds (Corner and Davies, 1971). The potential contribution of inorganic zooplankton excretion to nutrient requirements of phytoplankton is highly variable and lies between 2% and 300% (Ba˚mstedt, 1985; review by Corner and Davies, 1971; review by Alcaraz, 1988; Alcaraz et al., 1998; Le Borgne, 1986). This large variability can be explained by three factors. First, the amount of nutrients excreted is a function of the zooplankton size-fraction. Microplankton and bacterioplankton usually show higher excretion rates of ammonia than do mesozooplankton and macrozooplankton (Smith, 1978a; Glibert, 1982; Hernandez-Leon and Torres, 1997). However, macrozooplankton and mesozooplankton can contribute significantly to the total regeneration of nitrogen (Roman et al., 1988; Glibert et al., 1992; Miller et al., 1995, 1997), whereas specifically mesozooplankton excretion generally provides a more significant proportion of the total ammonia regenerated (Bidigare, 1983; Dam et al., 1993; Miller and Glibert, 1998). Second, there is the spatial variability of the excretion contribution to phytoplankton demand. In some areas, excretion supplies all the requirements in inorganic nitrogen (Verity, 1985) and phosphorus (Martin, 1968; Eppley et al., 1973), whereas in other areas zooplankton regenerates only 2% of the daily ammonia requirements of phytoplankton (Biggs, 1982). Even in the same area, large variations can be found, as in the Catalan Sea

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(western Mediterranean Sea), where the mesozooplankton contribution to the nitrogen requirement of phytoplankton varies from 5% to 285% (Alcaraz et al., 1994). In general, the importance of zooplankton excretion in the regeneration of nutrients is high (>40%) in less productive areas, such as the open ocean, and low (<40%) in highly productive waters, such as those in areas of upwelling and in estuaries (Harrison, 1980; Le Borgne, 1986; Wollast, 1998). Third, there is a temporal variation of the excretory contribution to phytoplankton needs, both seasonal and annual. Seasonal variation has been shown in Narragansett Bay (Rhode Island), with high values in autumn (182% for N and 200% for P) and low values in spring (3% for N and 17% for P) (Martin, 1968). Furthermore, year-to-year variation has also been evident (Harris, 1959). These temporal variations could be explained by the production of the system: When the system is more productive, as during the spring bloom in temperate areas or when upwelling occurs, the contribution is usually lower, and vice versa (review by Le Borgne, 1986). Excretion of nitrogen during the diel migration of copepods can constitute at times an active flux (Hays et al., 1997) similar to or even higher than the passive PON flux (Longhurst and Harrison, 1988, and references therein). However, when several regions are compared, the active flux of excretory nitrogen has generally a median value of 5% of the PON passive vertical flux (ranging from 1% to 140%) (Longhurst and Harrison, 1988, and references therein). 5.1.1.2. Role of excretion in the carbon cycle Because of the close relationship between the carbon and nutrient cycles, copepod nutrient excretion plays an indirect role in the carbon cycle, but it has also a direct eVect on the constitution of the DOC pool (see also Section 5.2.1.1). This pool is one of the largest organic carbon reservoirs on earth (Strom et al., 1997). Evaluation of DOC sources is a major concern when studying the global carbon cycle because DOC makes up greater than 95% of the total organic matter in the ocean itself (Nagata and Kirchman, 1992). However, downward transport of dissolved excretion products out of the euphotic layer is generally considered negligible (McCave, 1975) and is ignored in the carbon/nutrient cycle (Wollast, 1998).

5.1.2. Role of respiration For the same reasons as excretion, respiration is generally not taken into account in the downward export of carbon (Wollast, 1998; Wollast and Chou, 2001). Downward export of carbon by respiration does exist, coming

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from copepods migrating vertically. In some areas, the amount of respiratory carbon transported out from the euphotic zone by migrant copepods can be of the same order of magnitude as that of gravitational particle sinking (Longhurst et al., 1990; Zhang and Dam, 1997). However, on a global scale, carbon export by the respiration of migrant copepods represents 1% of the global sinking flux of particles at 200 m depth (Longhurst and Williams, 1992), so respiration will not be further discussed.

5.2. Role of copepod particulate matter outfluxes 5.2.1. Role of faecal pellets Copepod faecal pellets can transport an important amount of organic and inorganic matter over long distances. Many of them have high sinking speeds and a peritrophic membrane that retains elements to a greater degree than other products that originate from copepods (moults and carcasses), other zooplankton, and other pelagic organisms, including phytoplankton and fish (Fowler and Knauer, 1986). Vertical transport might also occur when copepods eat at the surface at night and then produce faecal pellets after migrating down to deeper layers in the daytime (Morales et al., 1993; Atkinson et al., 1996; Bianchi et al., 1999), but the quantity involved appears to be negligible (Atkinson et al., 1996). The role of transport of matter by faecal pellets is further analysed in the following sections. 5.2.1.1. Role of faecal pellets in the carbon cycle (a) Downward transport of particulate organic carbon (POC). Turner (2002) has brought together a growing body of literature that agrees that the contribution of mesozooplankton faecal pellets to the export of material and sequestration of carbon is generally minor or variable. Turner (2002) indicates that usually these pellets contribute between a few and some 30% of the vertical POC flux, although in some areas or periods they contribute a larger part (>80%) of the POC flux. The emerging view is that it is mainly macrozooplankton faecal pellets, phytoplankton, and marine snow that are involved in the sedimentary carbon flux; their relative contributions are highly variable and depend on multiple interacting factors (review by Turner, 2002) such as the physical and biological factors aVecting the vertical flux of zooplankton products discussed above. (b) Contribution to the DOC pool. The degradation of faecal pellets is a way in which DOC is added to the water column. In conditions of high faecal pellet production and degradation, leaking from faecal pellets may be

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a significant contributor to the DOC pool and to bacterial growth, as an important amount of DOC would be liberated in the water column. DOC released by faecal pellets together with excretion and sloppy feeding could be a pathway of DOC to bacteria as important as that of DOC excretion directly from intact phytoplankton (Strom et al., 1997; Urban-Rich, 1999; Møller and Nielsen, 2001; Møller et al., 2003). This DOC is considered to be a high-quality substrate pool for bacteria (Hygum et al., 1997; Urban-Rich, 1999). (c) Dissolution of CaCO3. The dissolution of CaCO3 consumes CO2 and is only thermodynamically possible at great depths (below 1500 m; i.e., lysocline) (Broecker and Peng, 1982). However, biologically mediated dissolution of CaCO3 was observed at depths above the lysocline, among which was dissolution within copepod faecal pellets and guts (Milliman et al., 1999). Biologically mediated dissolution processes can absorb as much anthropogenic CO2 as 0.05 Gt C year1 (Sabine and Mackenzie, 1991). 5.2.1.2. Role of faecal pellets in the nutrient cycle Few studies exist on the vertical transport of nutrients by faecal pellets (compared to those on the transport of carbon). As discussed previously, faecal pellets have been shown to be mostly recycled at the surface; therefore, they generally contribute to regenerated production. Faecal pellets are reported to contribute little to nitrogen export to the benthos (Knauer et al., 1979; Daly, 1997). Knauer et al. (1979) estimated that faecal pellets constituted up to 5% and 20% of the total particulate organic nitrogen (PON) and particulate organic phosphorus (POP) vertical flux, respectively. However, during upwelling conditions, the same authors estimated that these contributions increased up to 25% and 60% of the total PON and POP vertical flux, respectively. 5.2.1.3. Role of faecal pellets in the nutrition of marine organisms Faecal pellets are known to contribute to the nutrition of many pelagic and benthic organisms (Frankenberg and Smith, 1967; Honjo and Roman, 1978; PaVenho¨fer and Knowles, 1979; Youngbluth et al., 1989; Mochioka and Iwamizu, 1996). They can transport organic matter of high nutritive value toward deeper layers (Fowler and Fisher, 1983). In this way, they can oVer a substantial fraction to the maintenance metabolism (Frankenberg and Smith, 1967) of the pelagos and benthos by means of coprophagy and ingestion of ‘‘marine snow’’ (Frankenberg and Smith, 1967; Honjo and Roman, 1978; PaVenho¨fer and Knowles, 1979; Turner, 1979; Bathmann and Liebezeit, 1986; Youngbluth et al., 1989). Their consumption and nutritive value depend on the pellet size, shape, sinking speed, carbon, and nitrogen contents (PaVenho¨fer and Knowles, 1979). Second, the active transport of faecal pellets and other particulate products by migrant copepods is important in the

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nutrition of marine organisms, as it oVers particulate products with a higher nutritional value than those falling from surface waters. 5.2.1.4. Role of faecal pellets in the transport of toxins, pollutants, and pelagic sediments Because faecal pellets are a means of transport of organic matter, they also transport the associated toxins, pollutants, and pelagic sediments. Toxic phytoplankton (Wexels Riser et al., 2003) and numerous pollutants (see the review of Turner, 2002, for an extensive list) are transported by faecal pellets. These pollutants can be transferred by coprophagy to the benthic (Osterberg et al., 1963; Elder and Fowler, 1977) or pelagic ecosystem (Krause, 1981), and thus be bioaccumulated in higher trophic levels. Sediment may be transported in copepod pellets in the plume of the Mississippi River (Turner, 1984, 1987) and in the highly turbid ecosystem of the Southern Bight of the North Sea (Frangoulis et al., 2001). 5.2.2. Role of posthatch mortality Dead organisms have a similar role to that of faecal pellets in the transport of matter in the carbon and nutrient cycles, in the nutrition of marine organisms (Wheeler, 1967), and in the transport of pollutants (Elder and Fowler, 1977; Fowler, 1977). However, they are less important than faecal pellets in the downward (passive) transport of matter because most carcasses originating from the upper layer of the water column decompose faster than faecal pellets (Smith, 1985; Fowler and Knauer, 1986; Lee and Fisher, 1994). However, the percentage of dead to total copepods increases with depth (Siokou-Frangou et al., 1997), becoming higher than that of living copepods (Wheeler, 1967; Siokou-Frangou et al., 1997; Yamaguchi et al., 2002). Dead copepods have been found at great depths (4000 m), but they seem to result mostly from the local mortality of migrating organisms (Wheeler, 1967), thus constituting an active downward flux. Locally, this flux can have a significant eVect on the downward transport of matter. On the diel scale, it can constitute up to 40% of the gravitational particle sinking (Zhang and Dam, 1997), and on the seasonal scale, it can be similar to the total passive flux of carbon (Hirche, 1997). 5.2.3. Role of moulting Moults play a similar role to that of carcasses and faecal pellets, such as transport of matter in the carbon and nutrient cycles, nutrition of marine organisms (Wheeler, 1967), and transport of pollutants (Elder and Fowler,

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1977; Fowler, 1977). However, moulting results in less body matter losses than faecal pellet production and posthatch mortality (Table 2). The downward transport of matter is also smaller than that of faecal pellets, despite the fact that they can have similar sinking speeds (Table 3). In fact, moults, like carcasses, retain fewer elements than faecal pellets because they degrade faster. This explains why they are rarely found in sediment traps, particularly in deep ones (review by Fowler and Knauer, 1986). Estimations of active flux of moults are lacking (Steinberg et al., 2000). 5.2.4. Role of egg mortality ‘‘Dead’’ eggs have a similar role to that of other particulate products in the nutrition of marine organisms (Section 3.2.4) and the transport of matter as pollutants (Elder and Fowler, 1977; Fowler, 1977), carbon, and nutrients. As a direct downward exporter of matter, eggs are less important than the other copepod particulate products because their sinking speed is less, their degradation is faster than that of other particulate products (Section 4.1.1.1. and Section 4.1.2.2.c), and predation decreases their passive vertical flux. However, egg predation may indirectly lead to outflux from surface waters through pellet production by predators, although a large proportion of eggs are viable after passage through the predator gut. High survival of copepod eggs has been reported for eggs passing through the guts of polychaetes (Marcus, 1984; Marcus and Schmidt-Gegenbach, 1986), hydromedusae (Daan 1989), and fish (Redden and Daborn, 1991; Conway et al., 1994; Flinkman et al., 1994).

6. DISCUSSION Copepods release dissolved matter through excretion and respiration, and particulate matter through faecal pellet production, posthatch mortality, moulting, and egg mortality. Respiration produces only CO2, whereas excretion includes inorganic compounds (ammonia, orthophosphate) together with several organic compounds of nitrogen and phosphorus (e.g., Gardner and PaVenho¨fer, 1982; Ba˚mstedt, 1985; Le Borgne, 1986; Regnault, 1987; Dam et al., 1993). Inorganic excretion constitutes the larger part of the total excretion (e.g., Corner and Davies, 1971; Ba˚mstedt, 1985; Le Borgne, 1986; Regnault, 1987; Le Borgne and Rodier, 1997); however, there is an important variability in the proportion of inorganic matter in the total excretion as a result of several factors, including temperature, species, and food (e.g., Mayzaud, 1973; Le Borgne, 1986; Miller, 1992). However, copepods release particulate matter through faecal pellet production, posthatch mortality,

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moulting, and egg mortality. Copepod faecal pellets are covered by a peritrophic membrane (Gauld, 1957; Yoshikoshi and Ko, 1988). This is also true for other many planktonic crustaceans (e.g., shrimps, euphausiids: Forster, 1953; Moore, 1931), but not for ciliates, tintinnids (Stoecker, 1984), or gelatinous zooplankton (Bruland and Silver, 1981). There are several possible functions of the peritrophic membrane (e.g., protection of the midgut epithelium) that will depend on the animal mode of life (Gauld, 1957; Reeve, 1963; Yoshikoshi and Ko, 1988). Most copepods have cylindrical-shaped pellets (Gauld, 1957; Fowler and Small, 1972; Martens, 1978; Cade´e et al., 1992; Yoon et al., 2001). Their size depends on the ingestion rate (e.g., Huskin et al., 2000), animal size (e.g., Uye and Kaname, 1994), food type (e.g., Feinberg and Dam, 1998), and food concentration (e.g., Dagg and Walser, 1986; Tsuda and Nemoto, 1990; Butler and Dam, 1994; Feinberg and Dam, 1998; Huskin et al., 2000). The colour of faecal pellets will depend on the diet of the animal (Feinberg and Dam, 1998; Urban-Rich et al., 1998). Their content varies from an amorphous material to intact and even viable phytoplankton cells (e.g., review by Turner, 2002). The chemical composition of faecal pellets is complex (pigments, lipids, amino acids, hydrocarbons, sugars, trace elements, radionuclides, etc.) (e.g., review by Turner, 2002). The faecal C, N, and P composition (Table 1) will depend on the food quantity and quality (e.g., Urban-Rich et al., 1998), animal size (Small et al., 1983), animal species, animal assimilation eYciency, and pellet compaction (e.g., Gonza´lez and Smetacek, 1994). In estimations of faecal C, the vertical flux when using literature values, those expressed as an amount of the element per dry weight should be preferred to those expressed per pellet or per pellet volume (Table 1). Copepod carcasses are distinguished from live animals by their condition, ranging from slight damage or a few missing appendages to empty broken exoskeletons (Haury et al., 1995). Although moults have similar appearance, they can be distinguished from recently formed carcasses, as they do not contain any residual tissue and the exoskeleton is often complete, at least for freshly produced moults. Dead eggs include nonfertilized eggs, sterile eggs, and dead eggs sensu stricto. The two types of resting (dormant) eggs, subitaneous (nondiapause) and quiescent, can lead to wrong estimates of egg mortality, as these eggs can hatch after long periods (Marcus, 1996, 1998; Marcus and Boero 1998). The carbon or nitrogen content of eggs can be estimated using the egg volume (Checkley, 1980; Huntley and Lopez 1992; Hansen et al., 1999). The review of the nature of these outfluxes showed that faecal pellets and excretion have been widely studied compared to the other outfluxes. However even for the ‘‘well-studied’’ outfluxes there are still unknowns, such as the chemical composition of the excreted phosphorus organic fractions.

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The schematic diagram (Figure 1) summarizes the review of the factors aVecting the rate and the vertical fate of copepod outfluxes (these factors are common for all products from zooplankton). For excretion rate, faecal pellet production rate, and moulting rate, the most important controlling factors of the rate are generally temperature (e.g., Marshall and Orr, 1955; Souissi et al., 1997; Ikeda et al., 2001), body mass (e.g., PaVenho¨fer and Knowles, 1979; Souissi et al., 1997; Ikeda et al., 2001), food concentration (e.g., Marshall and Orr, 1955; Takahashi and Ikeda, 1975; Kiørboe et al., 1985; PaVenho¨fer et al., 1995; Campbell et al., 2001), food quality (e.g., Urabe, 1993; Gulati et al., 1995; Kang and Poulet, 2000), and copepod faunistic composition (e.g., Daly, 1997; Gaudy et al., 2000). Egg mortality rate depends on predation (e.g., Marcus and Schmidt-Gegenbach, 1986; Conway et al., 1994; Kang and Poulet, 2000), the food type ingested (Ianora et al., 1995; Ban et al., 1997), animal age (Jo´nasdo´ttir, 1994), and temperature (Hirst and Kiørboe, 2002). For the posthatch mortality rate, factors are internal (developmental stage, senescence, genetic background) or external (temperature, starvation, predation, parasitism) (e.g., Ohman and Wood,

Figure 1 Diagram of the vertical fates of copepod (and other zooplankton) products and the factors controlling them. DM: dissolved matter, T 8: temperature, zoo: zooplankton.

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1995; Hirst and Kiørboe, 2002). Although several of the above relationships are clear (e.g., positive relationship between body mass and excretion), some are not well established (negative, positive or no relationship are found), and others are poorly studied (e.g., few studies concerning the influence of food type on excretion rate). Physical and biological factors govern the vertical fate of all zooplankton products (Figure 1). First, physical factors, such as sinking speed, advection, stratification, turbulent diVusion, and molecular diVusion, influence the sedimentation speed and degradation of the zooplankton products. The sinking speed of a particle depends on the shape and dimensions of the particle, the water molecular viscosity, and the diVerence between particle and water densities (e.g., Komar et al., 1981). Upwelling events can counteract the sedimentation of particles (Alldredge et al., 1987). Stratification can decrease the sedimentation speed of particles (e.g., Krause, 1981; Gonza´lez et al., 1994), and turbulent mixing can prolong the residence time of particles in the mixed layer (Alldredge et al., 1987). Leaking by molecular diVusion releases carbon and nutrients from pellets and carcasses and depends on temperature and turbulence and also in the case of faecal pellets food concentration (e.g., Lampitt et al., 1990; Lee and Fisher, 1994; Head and Harris, 1996; Møller et al., 2003). Second, the biological factors that govern the vertical fate of copepod products are production and biodegradation by zooplankton, nekton, and microorganisms. Biodegradation by zooplankton and nekton is done by detritiphagy (including coprophagy) (e.g., Frankenberg and Smith, 1967; Gonza´lez et al., 1994; Haury et al., 2000; Yamaguchi et al., 2002) and, in the case of copepods, also by coprorhexy and coprochaly (Lampitt et al., 1990; Noji et al., 1991). Biodegradation occurs through the activities of bacteria and protists (e.g., review by Turner, 2002). Physical degradation and biodegradation by zooplankton and nekton are faster than biodegradation by microorganisms. The order of the biodegradation rate of copepod products by microorganisms depends strongly on temperature and in decreasing order of importance, is eggs (<3 days) (Jo´nasdo´ttir, 1994; Poulet et al., 1994), moults (<8 days) (Poulicek et al., 1992), carcasses (3–11 days) (Harding et al., 1973; Poulicek et al., 1992), and faecal pellets (3–50 days) (e.g., Small and Fowler, 1973; Alldredge et al., 1987). Finally, diel (e.g., Longhurst et al., 1990) and seasonal (Longhurst and Williams, 1992) vertical migration of copepods constitutes an active process that will also influence the vertical flux of copepod products. The most important copepod outfluxes are excretion and faecal pellet production. Excretion oVers inorganic nutrients that can be directly used by primary producers (Dugdale and Goering, 1967; Conway, 1977; Harrison et al., 1996; Lomas et al., 1996) and organic nutrients that can be used by bacteria and, in some cases, by phytoplankton (Corner and Davies, 1971; McCarthy, 1971; Stephens and North, 1971). The potential contribution of

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copepod excretion to the nutrient requirements of phytoplankton is highly variable spatially and temporally (Corner and Davies, 1971; Ba˚mstedt, 1985; Le Borgne, 1986; Alcaraz, 1988; Alcaraz et al., 1998). The active flux of excretory nitrogen during the diel migration of mesozooplankton generally makes little contribution compared to the PON passive vertical flux (Longhurst and Harrison, 1988, and references therein). The contribution of copepod DOC excretion to the DOC pool is not well known. This contribution needs more investigation to determine the quantity and composition of the excreted DOC, especially during a bloom situation, when copepods could be a major source of DOC to the water column. Copepod particulate products are important in the transport of matter in the carbon (e.g., Strom et al., 1997; review by Turner 2002) and nutrient (Knauer et al., 1979; Daly, 1997) cycles, in the nutrition of marine organisms (e.g., Frankenberg and Smith, 1967; PaVenho¨fer and Knowles, 1979; Mochioka and Iwamizu, 1996) and in the transport of toxins (Wexels Riser et al., 2003) and pollutants (e.g., Fowler, 1977; review by Turner 2002). On the basis of the literature presented, we believe their relative importance, in decreasing order, to be faecal pellets, carcasses, moults, and eggs. This relative importance can be demonstrated by comparing the biodegradation rates (see above) and sinking speeds (Table 3) of zooplankton particulate products. To summarize this in order of importance, Fowler and Small (1972), referring to euphausiids, stated that ‘‘faecal pellets sink at rates faster than those of eggs and about the same as those of moults. On the other hand, carcasses of the organisms that produce the faecal pellets sink two to four times faster than the fastest pellets. Dead euphausiids disintegrate into smaller pieces in a matter of days, whereas faecal pellets of these animals can remain intact for months. The rapid decomposition of carcasses slows the sinking rate of dead zooplankton.’’ In future studies, a wider research strategy is necessary, as discussed in the next five points. First, other zooplankton groups should be studied, because locally or temporally they can dominate total abundance and biomass of mesozooplankton and macrozooplankton (Alldredge, 1984; Longhurst, 1985) and constitute an important outflux. For example, in some areas and during some seasons, appendicularians, pteropods, and salps occur in high concentrations, and their feeding nets (together with the attached detritus) represent a significant sink of organic matter (Morris et al., 1988; Bathmann et al., 1991; Hansen et al., 1996b; review by Kiørboe, 1998) that can be as high as that of copepod faecal pellets (Vargas et al., 2002). The high particle content provides an important contribution to the nutrition of zooplankton (Alldredge, 1976; Steinberg et al., 1994, 1997; Steinberg, 1995) and anguilloid larvae (Mochioka and Iwamizu, 1996). Second, it should be emphasized that measurements of nutrient regeneration using separate zooplankton fractions (such as micro-, meso-, and

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macrozooplankton) should be treated with caution because in a natural food web, the trophic interactions between the fractions can result in a significantly diVerent nutrient regeneration. Mesozooplankton, through grazing, excretion and ‘‘sloppy feeding,’’ can aVect nutrient regeneration from both phytoplankton (the primary consumers of nitrogen) and the protozoa (the primary regenerators of nitrogen). The net eVect of mesozooplankton on the regeneration of nitrogen will be negative or positive depending on the trophic interactions between the microbial food web and microzooplankton and between microzooplankton and mesozooplankton (Glibert et al., 1992; Miller et al., 1995, 1997; review by Glibert, 1998). Third, the match (time-lag) between the seasonal evolution of phytoplankton and zooplankton biomass can influence the export of matter in an ecosystem. For example, a high match (short time-lag) maintains phytoplankton biomass low, limiting the aggregation of large cells and, thus, their vertical export. This results in rapid recycling of phytoplankton in the water column and low sinking losses. This phenomenon, together with the retention of mesozooplankton particulate products in the water column, corresponds to a retention food chain, as opposed to an export food chain (review by Wassmann, 1998). Another consequence of a high match is that when this match occurs, microzooplankton is probably less grazed on by mesozooplankton, allowing a better recycling of nitrogen by microzooplankton. During this period, the system would be dominated by an herbivorous and retention web (the herbivorous web, including microbial components, as discussed in the review by Legendre and Rassoulzadegan, 1995). Therefore, to establish such indirect eVects of zooplankton, vertical flux studies should examine the carbon-nutrient outflux from zooplankton, the vertical flux of phytoplankton and zooplankton products, the match between the seasonal evolution of phytoplankton and zooplankton biomass, the primary production, and the zooplankton trophic interactions and grazing pressure. A fourth aspect appears when the potential contribution of nitrogen outfluxes of copepods and the nitrogen uptake of phytoplankton are compared (Table 5). This comparison shows that although several studies examined the potential contribution of copepod ammonia excretion to the nitrogen uptake of phytoplankton, few examined simultaneously the nitrogen supply from ammonia excretion and particulate nitrogen production. Table 5 shows that we found only one study (Small et al., 1983), limited to the nitrogen production from faecal pellets. This lack of interest in the particulate nitrogen production from copepods is the result of two assumptions: (1) the contribution of particulate nitrogen to the total nitrogen produced is much lower than that of ammonia excretion, and (2) excretion is an direct contribution to the ammonia pool, whereas previous degradation and remineralization are needed for particulate products. However, the first assumption may not always be true. Because the sum of all copepod PN production has a rate

N supplied by mesozooplankton (mg N m3 h1) FPP

N uptake by phytoplankton (mg N m3 h1)

Mesozooplankton N supplya/phyto N (%)

—

140–1700 (NH4)

10 (NH4)

6–10 (NH4)

45–50 (NH4)

Dugdale and Goering, 1967 Eppley et al., 1973

Study area

Depth (m)

Ammonia excretion

Sargasso Sea

0–200

—

North Pacific Ocean OV Peru (coastal upwelling) Newport River estuary Ross Sea East-central Pacific Ocean OV Morocco (upwelling) Mediterranean (Catalan) Sea coastal frontal

—

3–5

0–100

4–20

—

20–290 (NH4)

1–30 (NH4)

Smith, 1978a

1

4–400

—

40–4200 (NH4)

8 (NH4)

Smith, 1978b

0–200 0–100

1–2 12

— 1

65–100 (NH4) 63 (total N)

2 (NH4) 20 (total N)

Biggs, 1982 Small et al., 1983

0–40

46

—

124 (NH4)

37 (NH4)

Head et al., 1996

0–100 0–100

20–33 5–111

— —

11–20 (total N) 16–58 (total N)

100–285 (total N) 9–189 (total N)

0–100

1–13

—

3–39 (total N)

5–160 (total N)

oVshore

a

Faecal pellet nitrogen production or ammonia excretion nitrogen production, or their sum when data from both were available.

Alcaraz et al., 1988, 1994

291

Values are range (two values) or mean (one value). FPP: faecal pellet production.

Source

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Table 5 Mesozooplankton (dominated by copepods) nitrogen production (from ammonia excretion or faecal pellet production), phytoplankton nitrogen uptake and their ratio

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close to the nitrogen excretion rate (Table 2), the particulate nitrogen may constitute an amount equal or greater than that originating from nitrogen excretion. In some periods or areas, the nitrogen from all PM together could be mostly remineralized in the water column and would be then be as important as excretion in the potential contribution to the uptake of primary producers. Therefore, future studies should examine simultaneously the contribution of excretion and particulate products to the nitrogen oVered in the water column. Finally, concerning carbon export, the emerging view is that it is mainly macrozooplankton faecal pellets, phytoplankton, and marine snow that are involved in the sedimentary carbon flux; their relative contributions are highly variable and depend on multiple interacting factors (review by Turner, 2002). However, there are still open questions about the pellets that stay in the water column: the ‘‘missing faeces.’’ Among these missing faeces, a large part may be microzooplankton faecal pellets that are tiny and thus sink very slowly (Small et al., 1987; Ayukai and Hattori, 1992). The quantity of missing faeces is poorly known because most studies investigating faecal pellet flux have not examined faecal pellet production, and this limits discussion (Dam et al., 1993). Among the few studies on faecal pellet flux that include faecal pellet production values, some authors use direct measurements (Small et al., 1983, 1989; Ayukai and Hattori, 1992; Wexels Riser et al., 2001, 2002), but others are based on indirect estimations (Bathmann and Liebezeit, 1986; Voss, 1991; Roman and Gauzens, 1997; Roman et al., 2000, 2002). Little is also known concerning the fate of the missing faeces, such as the relative roles of coprophagy (Gonza´lez and Smetacek, 1994), remineralization, and integration into marine snow. Future research should include the quantity and fate of the missing faeces and other zooplankton particulate products that remain in the water column. In conclusion, it should be noted that for a long time, most scientific work on carbon burial caused by copepods was limited to faecal pellets, and as measured by sediment traps. The evaluation of the role of copepod particulate products on the transport and recycling of elements and compounds not only requires pellet flux measurements but also should attempt to quantify the production and fate of all products. Little is known of the relative eVects of detritiphagy, remineralization, or integration into the marine snow, especially for copepod particulate products other than faecal pellets. Concerning nutrient recycling by copepods, many workers have examined only ammonia excretion. As discussed previously, in some periods or areas, the nitrogen from PM could be mostly remineralized in the water column and would then be as important as excretion. Furthermore, many workers have come to conclusions only in terms of percentages, without comparing the actual values obtained with those in literature, or only with literature of the same study area, thus often leading to speculative or limited discussion. For example, a

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low contribution of faecal pellet carbon to the total carbon vertical flux could be relative to other sources of particulate matter. In shallow waters, other sources of particulate matter may be more important than in the open sea, thus reducing the relative faecal pellet contribution, whereas the absolute value of faecal pellet vertical flux can be higher than in the open sea. Therefore, to obtain a more constructive discussion, comparison of actual values obtained should be done with literature from other areas than the one studied to determine the importance of a process on a global scale. Also, although shallow coastal areas are sites of high production and carbon fluxes, few sediment trap studies have been carried out.

ACKNOWLEDGEMENTS We thank Alberto Borges, Patrick Dauby, Khalid El Kalay, Michel Frankignoulle, Gilles Lepoint, John Pinnegard, Michel Rixen, Nikos Skliris, Alan Southward, Sandi Toomey, Kristell Van Hove, and two anonymous reviewers for helpful comments, corrections, and advice. Operating grant support from FRFC Belgium to CF is gratefully acknowledged.

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TAXONOMIC INDEX

Acartia clausi, 260, 266, 274, 275 populations of, 74, 74 Acartia spp., 57–8 Acartia tonsa, 260, 266, 274 eggs of, 262 Aglantha digitalis, 32, 36, 43 Alaria esculenta, 47–8 Alosa finta, 53 Amphora coffeaeformis, 224–5 Anapagurus laevis, 114–6 Anapagurus sp., 114–6 Anomalocera patersoni, 274, 279 Antithamnion sp., 231 Apogon coccineus, 53 Ascidiella aspersa, 216, 226, 229 Atelecyclus rotundatus, 75, 142, 145, 146 Atelecyclus sp., 142 Balanus amphitrite, 227 Balanus perforatus, 42–3, 46–7 Balanus sp., 229 Balistes capriscus, 53 Biddulphia sinensis, 30, 73 Biddulphia spp., 30, 228 Botrylloides sp., 229 Branchiostoma lanceolatum, 64 Brongniartella australis, 228 Bryopsis sp., 228 Bugula neritina, 229 Cafeteria sp., 275 Calanus finmarchicus, 41, 64, 260, 261, 274 faecal pellet production in, 266–7 Calanus glacialis, 64, 260 Calanus helgolandicus, 32, 64, 75, 261, 266 abundance of, 57–8 diet/metabolism of, 41 faecal pellet size of, 267 as indicator species, 37, 37, 38–9 as pelagic fish food, 40–1 seasonal variability in, 58, 59, 73–4, 79 at station L4, 57, 59 zooplankton and, 73–4

Calanus hyperboreus, 64, 260 Calanus pacificus, 79, 260 Calanus tenuicornis, 66 Caligus elongatus, 64 Callianassa subterranea, 140, 144, 146 Callianassa tyrrhena, 116 Callinectes sapidus, 140, 144, 166 barokinesis of, 171 current orientation and, 180, 182 decapod larvae dispersal and, 132 diel rhythms and, 186 export/reinvasion by, 150, 152, 153 light stimulus and, 174, 176–7 megalopae of, 180, 182, 185–6 salinity and, 178 turbulence and, 181 Callionymus lyra, 51 Campylodiscus sp., 228 Cancer gracilis, 168 Cancer irroratus, 168, 174, 241 geotaxis and, 170 Cancer magister, 141, 166 megalopae of, 146–7, 189 migration of, 143, 153, 189 zoea of, 170 Cancer oregonensis, 141 megalopae of, 147 migration of, 143 Cancer spp., 142, 145 larvae of, 155 Candacia armata, 32, 64 Caprella sp., 229 Carassius carassius, 240–1 Carcinus aestuarii, 140 Carcinus maenas, 116, 140, 144, 171 endogenous rhythms of, 182–4, 185 export/reinvasion by, 143, 146–7, 150, 152, 166 megalopae of, 160, 180, 182, 184, 185–6, 194 tides and, 153 vertical distribution and, 150 wind-driven transport of, 160–1 zoea of, 160 Cavolinia spp., 64 Centropages hamatus, 275

312 Centropages typicus, 32, 74, 261 CPR data, 74 faecal pellet production, 269 PM outfluxes of, 266–7 Ceramium sp., 231 Ceramium tasmanicum, 228 Ceratium spp., 73 Chaetoceros neogracile, 275 Chaetoceros socialis, 58 Chthamalus montagui, 42–3 Chthamalus spp., 45, 46 Chthamalus stellatus, 42–3 Ciona intestinalis, 226, 227, 229 in marine fouling, 216 Cirrhinus molitorella, 240–1 Cladophora sp., 228 Clausocalanus arcuicornis, 275 Clausocalanus spp., 64, 75, 261 Clibanarius erthyropus, 47 Clio spp., 64 Clione limacina, 32, 64 Clupea harengus, 2, 35, 76 egg abundance of, 39–40 pilchard competition with, 37, 78 population studies of, 6 Corycaeus typicus, 275 Corystes cassivelaunus, 140 Coscinodiscus wailesii, 30, 65, 73, 74 Crangon allmani, 144 Crassostrea gigas, 237 Cyprinus carpio, 240–1 Dendronotus frondosus, 229 Dentalium entalis, 55 Dentalium vulgare, 55 Dictyocysta spp., 65 Dinophysis acuminata, 65 Dinophysis acuta, 65 Dinophysis caudata, 65 Dinophysis norvegica, 65 Dinophysis rotundata, 65 Dinophysis sacculus, 65 Discorsopagurus schmitti, 172 Ebalia sp., 142 Ebalia tuberosa, 168, 172 Echinus acutus, 55 Echinus esculentus culturing of larvae, 43 Ectocarpus siliculosus, 228

TAXONOMIC INDEX

Ectocarpus spp., 228 in marine fouling, 227, 230–1 Eledone cirrhosa, 55 Enteromorpha spp., 218, 228, 239 in marine fouling, 227, 230–1 Eucalanus crassus, 75 Eucalanus pileatus, 260, 266–7 Euchaeta spp., 261 Euchirella rostrata, 261 Eurypanopeus depressus, 165, 171, 189 Euterpina sp., 58 Euthemisto gracilipes, 32 Euthynnus pelamis, 53 Evadne nordmanii, 32 Evadne spp., 65 Favella serrata, 65 Fragilaria sp., 228 Fritillaria borealis, 66 Fritillaria pellucida, 66 Fucus vesiculosis, 238 Gadus morrhua, 48, 49, 52, 224 antifoulants and, 238 spawning/populations of, 52, 79 Galathea intermedia, 75 Galathea sp., 167 Geryon quinquedens, 168 zoeae of, 170, 189 Gibbula umbilicalis, 47 Giffordia sp., 231 Glycymeris glycymeris, 55 Goneplax rhomboides, 142 Gonyaulax spp., 65 Gracilaria sp., 218, 228 Gyrodinium aureolum, 30, 58, 59 Halosphaera spp., 65 Hemigrapsus oregonensis, 168 Hiatella arctica, 229 Hiatella spp., 229 Hippoglossoides platessoides, 76 Hippolyte varians, 75 Homarus americanus, 141, 145, 167, 171 barokinesis in, 172 ontogenetic migration in, 146 orientation in, 180 Hyas araneus, 168

313

TAXONOMIC INDEX

Hyas coarctatus, 145 Hymenomonas elongata, 261 Hysterothylacium aduncum, 220 Inachus sp., 142 Isochrysis galbana, 261 Khunia scombri, 67 Lagocephalus lagocephalus, 53 Laminaria ochroleuca, 47–8 Leocarcinus puber, 75 Lepas nauplii, 66 Lepeophtheirus salmonis, 220 Lepidopus caudata, 53 Leptodius floridanus, 170–1 Libinia emarginata, 167 Limacina retroversa, 32, 66 Limanda limanda, 36 Liocarcinus depurator, 142 Liocarcinus holsatus, 168 Liocarcinus spp., 142, 144 Lirope tetraphylla, 32 Littorina littorea, 241 Littorina spp., 229 Loligo forbesi, 49–50, 55 Loligo vulgaris, 55, 78 Lophopanopeus bellus, 168 Lophopanopeus spp., 141 Lucifer typus, 66 Luidia sarsi, 32, 36, 43 Macropipus sp., 171 Maja crispata, 142 Meganyctiphanes norvegica, 32 Melanogrammus aeglefinus, 76 Mesocalanus tenuicornis. See Calanus tenuicornis Metridia longa, 261 Micromesistius poutassou, 76 Microsetella sp., 65 Microstomus kitt, 36 Modiolus sp., 229 Molgula ficus, 229 Muggiaea atlantica, 32, 36 Munida bamffica, 55 Munida rugosa, 142, 145 Mytilus edulis, 216, 229 abundance of, 227 in marine fouling, 226

Nanomia sp., 32, 36 Neopanopae sayi, 165, 170, 177–8 Neoparamoeba pemaquidensis, 239 Nephrops norvegicus, 114–6, 142, 145 migration in, 190 Naucrates ductor, 53 Noctiluca scintillans, 66 Nucella lapillus, 48 Nyctiphanes couchii, 32 Obelia australis, 228 Octopus vulgaris, 55 Odontella sinensis. See Biddulphia sinensis Oikomonas sp., 275 Oikopleura dioica, 66 Oikopleura labradoriensis, 66 Oithona similis, 261 Oithona spp., 74, 261, 277 Oncaea mediterranea, 261 Oncaea sp., 277 Oreochromis spp., 221, 224, 240–1 Oscillatoria sp., 228 Osilinus lineatus, 47 Ovalipes ocellatus, 140, 144, 146 Pachygrapsus crassipes, 141, 166 elemental fingerprinting of, 194 geotaxis in, 171 migration in, 147 Pachygrapsus marmoratus, 141 Pachysphaera spp., 67 Pagrus pagrus, 53 Pagurus beringanus, 167 Pagurus bernhardus, 141, 145, 190 migration in, 143 Pagurus granosimanus, 167 Pagurus longicarpus, 168, 189 Pagurus prideauxii, 141, 145, 146 Palaemon adspersus, 140 Palaemon elegans, 114–6, 140 Palinurid pueruli, 147 Palinurus elephas, 114–6 Pandalina brevirostris, 75 Pandalus montagui, 141, 143, 144 migration in, 190 Panopeus herbstii, 165, 170 Panulirus cygnus, 141, 145, 160, 167 migration in, 147 ontogenetic migration in, 159 ontogenetic shifts in, 146

314 Paphia rhomboides, 55 Paracalanus aculeatus, 266 Paracalanus parvus, 58, 262 Parafavella gigantea, 66 Parapenaeus longirostris, 114–6 Para-Pseudocalanus spp., 74 Parasagitta elegans, 32, 36, 38–9 as indicator species, 35–6 population cycles of, 41, 43 Parasagitta friderici as indicator species, 32 Parasagitta setosa, 32, 38–9 P. elegans v., 35–6 Parastichopus californicus, 241 Pareuchaeta hebes, 32, 36 Patella depressa, 47 Patella spp., 43, 46, 48 Patella vulgata, 47 Penaeus aztecus, 186 Penaeus brevirostris, 158, 167, 178–9 Penaeus californiensis, 167, 178–9 Penaeus duodarum, 167, 184, 189 Penaeus esculentus, 157 Penaeus indicus, 141 Penaeus japonicus, 167, 171 Penaeus plebejus, 153 Penaeus spp., 144 diel migration of, 153, 157–9, 157 Penaeus stilirostris, 157, 167 Penaeus vannamei, 141, 157, 167 Penilia avirostris, 66 Perna viridis, 229 Phaeocystis spp., 66 Pilumnus hirtellus, 75 Pinctada sp., 229 Pinnixa spp., 140 Pirimela denticulata, 141 Pisidia longicornis, 75, 114–6, 141 Platichthys flesus, 50 Pneumodermopsis spp., 75 Podon spp., 32, 66 Polykrikos schwartzii, 66 Polyprion atlanticum, 53 Polysiphonia abscissa, 228 Polysiphonia sp., 231 Pontella meadii, 261, 275 Pontophilus bispinosus, 142, 145 Porcellana platycheles, 141 Portumnus latipes, 141

TAXONOMIC INDEX

Processa canaliculata, 141, 145, 146 Prorocentrum spp., 73 Pseudocalanus acuspes, 66 Pseudocalanus elongatus, 66, 261, 275 Pseudocalanus minutus, 66 Pseudocalanus spp., 57–8, 66, 74, 261 Ptychocylis spp., 67 Raja brachyura, 51–2 Randallia ornata, 142 Renibacterium salmoninarum, 221 Rhincalanus nasutus, 75 Rhithropanopeus harrisii, 140, 144, 165 depth regulation of, 174–5, 187 in estuaries, 150, 151, 170, 173–8 ontogenetic shift in, 146 phototaxis in, 173, 174, 175 pressure change and, 171 response to stimuli in, 170, 173–7 salinity and, 177–8 tidal migration of, 181–182, 185 water column migration and, 150, 151, 152, 182 zoeae of, 187 Rhizophora mucronata, 233 Rhizosolenia alata, 260 Rhizosolenia delicatula, 58 Rhizosolenia shrubsolei, 73 Rhodomonas baltica, 260 Rhodomonas lens, 275 Sabellaria cementarium, 172–3 Salpa fusiformis, 32 Sarcothalia crispata, 231 Sarda sarda, 53 Sardina pilchardus, 37, 38–39, 40 herring v., 6 spawning/distribution of, 35, 37, 39–40, 41, 43 Scomber japonicus, 53 Scomber scombrus, 5, 67 pilchard v., 6 spawning/distribution of, 35, 39, 76 Scophthalmus rhombus, 36 Scrippsiella trochoidea, 67 Scrupocellaria bertholetti, 229 Scyllarus bicuspidatus, 141 Scyra acutifrons, 168 Scytsiphon lomentaria, 228 Semibalanus balanoides, 42, 45, 46

315

TAXONOMIC INDEX

Seriola dumerili, 53 Sesarma cinereum, 166 Siganus canaliculatus, 241 Siganus lineatus, 241 Skeletonema costatum, 3 TBT sensitivity in, 48 Solidobalanus fallax, 227 Stauroneis membranacea, 67 Stomias boa ferox, 75–6 Subeucalanus subcrassus, 32, 36 Temora longicornis, 261, 275 Temora spp., 261 Temora stylifera, 261 Teredo navalis, 223 Tetraselmis sp., 275 Thais spp., 229 Thalassiosira spp., 73 Thalassiosira weissflogii, 260, 261, 275 Tinntinopsis spp., 67

Tomopteris helgolandica, 32 Tomopteris sp., 66, 67 Trisopterus esmarkii, 54 Tubularia larynx, 228, 231 Uca pugilator, 166 photokinesis of, 174 Uca spp., 140, 144, 167 photoresponse in, 176–8 pressure change and, 171 Ulva nematoidea, 228, 231 Ulva rigida, 231 Ulva spp., 218, 228 Upogebia deltaura, 75 Venus verrucosa, 55 Vorticella sp., 228 Zoothamnium pelagicum, 67 Zostera marina, 232

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SUBJECT INDEX

Acartia clausi in zooplankton, 74 Acartia spp. at station L4, 57–8 Advection, 188 in circulation, 58 passive vertical flux and, 272–3 Amorican Shelf, 19 Amphora coffeaeformis (diatom) in fish farm biofouling, 224–5 Antifoulant technology bioadhesion disruption and, 231–2 biological control/grazing and, 240–1, 242–3 BPD and, 235 BPU and, 235 copper-containing, 233–5 COPR and, 233 electro/chemical/physical, 231–3 netting mesh size in, 233 NLBs and, 232 nontoxic, 238–40, 242–3 NPAs and, 232 PDMS and, 238–9 polyamide and, 233 TBT, 3, 48, 237, 238 toxic materials and, 233–4, 235 ARGOS drifting buoys sampling programs and, 18 Ascidiella aspersa in marine biofouling, 216, 226 Autoanalytical techniques chlorophyll a fluorescence, 7 salinity, 7 temperature, 7 water transparency, 7 AVHRR satellite images, 12, 14 Balanus spp. perforatus, 42–3, 46–7 warm-water species of, 46–7 Barnacles abundance of, 44, 46–7 intertidal fauna, 43–7 sampling sites of, 44–5

species of, 42–3 species ratios and, 46 Benthic fauna environmental change and, 2 Benthos, 148 brittlestar survey technique and, 55 in long-term research, 54–5 megabenthic species of, 55 populations/dredge type and, 55 sea temperature and, 55 surveys of, 54 Biddulphia sinensis in diatom blooms, 73 Biocides/Pesticides Assessment Unit (BPU), 235 Biofouling see Fish farm biofouling/remediation Biogases from plankton, 80 Bioluminescence in bio-optics/photosynthesis, 60 Biomass chlorophyll a fluorescence relationship to, 27, 28, 29 in copepod excretion, 265 copepod outfluxes influence on, 290 indicators in zooplankton, 21, 28, 32, 35, 36, 37, 38 phytoplankton, measurement of, 27 zooplankton species indicators of, 21, 28, 32, 36, 37, 38 Bio-optics/photosynthesis, 60–1 bioluminescence in, 60 chlorophyll absorption in, 60 photosynthetically active radiation in, 60 phytoplankton fluorescence in, 58 Blake plateau, 134 Blond ray decline of, 51–2 Blooms see Diatom blooms; Dinoflagellate blooms; Flagellate blooms Blue whiting distribution changes in, 76

318 BPD see European Union Biocidal Products Directive BPU see Biocides/Pesticides Assessment Unit Brachyura, 111, 116, 139, 146, 150 locomotor activity in, 169 natural buoyancy of, 169 orientation of, 169 Brittlestar survey, 55 Bulletins of Marine Ecology on plankton seasonality, 75 Calanus finmarchicus, 41 Calanus helgolandicus, 57, 64, 75 diet/metabolism of, 41 faecal pellet size of, 267 as indicator species, 37, 38–9 as pelagic fish food, 40–1 seasonal variability, 58, 59, 73–4, 79 at station L4, 57, 59 zooplankton and, 73–4 Callinectes sapidus current orientation and, 180, 182 in decapod larvae dispersal, 132 diel rhythms and, 186 estuary exportreinvasion by, 150, 152, 153 light stimulus and, 176–7 megalopae of, 180, 182, 185–6 salinity and, 178 Callionymus lyra (dragonet) warming and, 51 Carbon 14 C uptake analysis, 21, 28 copepod faecal pellets and, 282–3, 292–3 copepod outfluxes and, 254 as DOC, 257, 258, 263, 276, 281, 289 DOC v. POC, 282 export in copepod outfluxes, 292 as nutrient, 20, 21, 26 Carcinus maenas endogenous rhythms of, 182–4, 185 estuary exportreinvasion by, 150, 152, 153 megalopae of, 160, 180, 182, 185–6 wind-driven transport of, 160–1 zoea of, 160 Celtic Sea currents/circulation in, 16, 18 Ceratium spp. in dinoflagellate blooms, 73 Channel Grid Project, 26 hydrography and, 28 long-term trends in, 26

SUBJECT INDEX

Chlorophyll absorption in bio-optics, 60 measurements of, 27 Chlorophyll a fluorescence autoanalytical techniques and, 7 biomass relationship to, 27, 28, 29 growth phase and, 61 seasonal distribution and, 31 Chthamalus spp. balanoides, 44, 46 montagui, 46 Ciona intestinalis in marine biofouling, 216, 226 Clibanarius erthyropus warm-water hermit crab, 46 Climate see also Water temperature benthos distribution and, 55 blooms and, 28 environmental change and, 2–3 NAO and, 78–9 prediction of, 3 species distribution and, 78 Clupea harengus (herring), 2, 6, 35, 37, 39–40 Coastal Zone Colour Scanner (CZCS), 31 validation by UOR, 60 Cod, 52–3 Continuous Plankton Recorder (CPR) Survey, 62 see also CPR method consistency Edinburgh Oceanographic Laboratory and, 7 lines of tow for, 63, 68, 69, 70 Scottish Marine Biological Association and, 7 station L4 compared to, 57 taxonomic resolution for, 64–7 UOR validation of, 60 Control of Pesticides Regulations (COPR), 235 Copepod excretion see also Copepod faecal pellets; Vertical flux biomass/density in, 265 body mass in, 265, 267 carbon as DOC, 255, 281 carcasses/moults in, 262, 284–5, 286 dead eggs in, 262, 286 DOC v. POC in, 282 egg mortality rate, 267–8, 285 egg production rate, 269 egg types/composition and, 262 faecal pellets in, 254, 258–9, 260–1

SUBJECT INDEX

faunistic composition in, 265, 266 food concentration in, 265, 266 food quality in, 265, 266–7 light in, 265, 267 moulting rate, 267–8, 284–5 nitrogen as NH4, 256–7, 269 nutrient role of, 280–1 phosphorus and, 257, 269, 286 posthatch mortality, 267, 284 salinity in, 266 temperature role in, 264–5, 267 vertical flux, active in, 279 vertical flux equation in, 269–80 vertical flux, passive in, 269–79 Copepod faecal pellets CaCO3 dissolution by, 283 carbon cycle role of, 282–3, 292–3 DOC v. POC and, 282 food quality and, 259 food type and, 259 ingestion rate and, 259 nutrient cycle and, 259, 283–4 peritrophic membrane in, 258, 272, 286 physical/chemical composition of, 258–9, 260–1 toxin transport and, 284, 289 Copepod outfluxes in carbonnitrogen cycles, 253–6 see also Copepod excretion biomass influence in, 290 carbon cycle and, 254 carbon export in, 292 dissolved matter role in, 255–6, 280–2 factors controlling excretion in, 254, 263–9 faecal pellets in, 254, 258–9, 260–1 future studies in, 289–90 nitrogen excretion in, 256–7, 282–92 nutrient regeneration in, 289–90 organic v. inorganic, 254 particulate matter role in, 255–6, 282–5 peritrophic membrane role in, 254 phosphorus excretion in, 257, 269, 286 vertical fates of, 254, 287–90 vertical flux, active in, 279 vertical flux, passive in, 270–9 zooplankton role in, 255–6 Copepod respiration, 254, 256 excretion ratio v., 269 output rate of, 263–4 role of, 281–2

319 Copepods, 32, 36, 37, 38 in blooms, 71–2 diversity and, 74–5 population dynamics of, 56, 57–8 seasonality of, 58 Coscinodiscus wailesii in diatom blooms, 30, 73, 74 CPR see Continuous Plankton Recorder Survey CPR method consistency diel migration and, 72 in long-term research, 70, 71, 72 mechanical difficulties and, 72 sampling frequency and, 72 ship speed and, 70, 71 Cross-shelf flow upwelling in, 120, 122, 123, 134 Culturing phytoplankton, 25 water quality and, 41, 43 Currents/circulation advection and, 58, 190 buoyancy/water density and, 120 cross-shelf flow/exchange in, 121–3, 134 drift-bottle data, 16 environmental factors in, 162, 179–80 geostrophic, 120–1, 132–4 lateral tidal shear in, 129, 130 selective tidal stream in, 127, 128, 129 tidal current asymmetry in, 129–31 tidal mechanisms and, 110–11, 112–13, 117, 119–20 tides/currents and, 120–24, 137–8 wind-induced models of, 19, 120 CZCS see Coastal Zone Colour Scanner Decapod larvae dispersal of, 108–13, 116 ecological categories of, 117–18 growth stages of, 113, 114, 115, 116 moult stage of, 111, 155 ontogeny in, 112, 116 Decapod larvae dispersal behavioural control evidence in, 164, 165–8, 169, 170–86 bimodal distribution in, 155 buoyant freshwater plumes in, 135, 136 Callinectes sapidus in, 132 continental margin/seddies and, 132–5, 137

320 Decapod larvae dispersal (cont.) cross-shelf flow in, 121, 122, 123 depth regulation mechanisms in, 187–8 diel cycles in, 110–11, 117, 137–8, 149 diel migrations in, 154–5, 156, 157–9 endogenous rhythms in, 110, 163–4, 181–6 as export/reinvasion mechanism, 149, 150, 152 fixed-station sampling in, 110, 139, 146 flood tide in, 126–7, 143, 150 food influence in, 190 geostrophic currents in, 120–1, 132–4 Gulf of Carpentaria study and, 157–9 internal waves in, 124 larval velocity measurements in, 194–6 lateral shear in, 129, 130 migratory behaviour/tides in, 124–7, 149–50, 151–2, 153–4 night-time in, 126–7, 150, 159, 176 ontogenetic dispersal in, 117, 159–61 ontogenetic/vertical distribution in, 143–8 orientation capability in, 161–3 phototaxis and, 111, 117 pooling zone, 122 predators and, 110–11 salinity/osmotic stress in, 110–11, 189–90 sampling interpretation in, 110 sampling methodology in, 138–9 sea/land breezes in, 124, 148 STST in, 149–50 swimming velocities in, 190–1 tagging measurements in, 193–4 taxonomic prevalence/vertical movement and, 139, 140–1, 143 thermal stratification in, 189–90 tidal cycles in, 110–11, 117, 119–20, 137–8, 149 vertical migration modifiers in, 188–90 vertical migration/positioning in, 108–90 vertical migrations, nonrhythmic in, 186–7 DEFRA, 80 Demersal fish, 41, 53, 80 blond ray decline and, 51–2 flounder migration and, 50 maturation trends for, 51–2 quantitative surveys of, 6, 48–9 short v. long-term data from, 50–1, 52 squid population and, 50, 55 trends in abundance of, 49–51 Dendrobranchiata, 116, 139

SUBJECT INDEX

Dentalium entalis sea temperature and, 55 Dentalium vulgare sea temperature and, 55 Diatom blooms, 21, 28 see also Dinoflagellate blooms; Flagellate blooms Biddulphia sinensisin, 73 Coscinodiscus wailesii in, 30, 73, 74 light effect on, 26–7 NAO and, 58 nutrient vertical distribution and, 24, 27 seasonality of, 25, 26, 58, 72 silicate concentration and, 22, 24 temperature and, 24 types of, 28 zooplankton grazers and, 26–7 Diatoms in fish farm biofouling, 224–5 Diel cycles, 72 Callinectes sapidus and, 186 decapod larvae cycles and, 110–11, 117, 125, 126, 143, 149 decapod larvae dispersal and, 110–11, 117, 137–8, 149 decapod larvae migrations and, 154–5, 156, 157–9 Penaeus spp. migration and, 157–9 Plebejus penaeus migration and, 153 vertical migrations and, 279, 289 Dinoflagellate blooms, 28, 29, 54, 55 see also Diatom blooms; Flagellate blooms Ceratium spp. and, 73 Gyrodinium aureolum and, 58 Prorocentrum spp. and, 73 seasonality of, 25, 26, 58, 72–3 Diseases, in fish farms, 3, 57 amoebic gill disease, 220, 239 from antibiotic use, 221 DO concentration and, 221 Hysterothylacium aduncum in, 220 phytoplankton poisoning, 220 Renibacterium salmoninarum and, 221 sea louse, 220 stress shock, 220 Dissolved matter (DM) in copepod outfluxes, 255–6, 280–2 Dissolved organic carbon (DOC), 258, 263, 276, 289 Dissolved organic nitrogen (DON), 20, 22, 23, 24, 276

SUBJECT INDEX

Dissolved oxygen (DO) in disease at fish farms, 220, 222 DM see Dissolved matter DO see Dissolved oxygen DOC see Dissolved organic carbon DON see Dissolved organic nitrogen Downwelling cross-shelf flow and, 121, 122, 123 validation by CZCS/UOR, 60–1 Drifting buoys sampling programs and, 18 Echinus acutus (sea urchin) sea temperature and, 55 Echinus esculentus (sea urchin) cold-water plankton and larvae, 43 culturing of, 43 Ecosystem models bay simulations and, 19 continuous measurement in, 18 high-resolution data, 3 long-term time series, 3 stimulus response and, 169, 170–80 wind-induced currents and, 18 Ectocarpus spp. in fish farm biofouling, 227, 230–1 Eddystone reef, 8, 9 Edinburgh Oceanographic Laboratory, 7 Ekman flow, 121, 122, 123, 148 winds from, 155, 156 Eledone cirrhosa cool-water octopus, 55 Endogenous rhythms Carcinus maenas and, 182–4, 185 competitive advantages of, 163–4 in decapod larvae dispersal, 110, 163–4, 181–6 Penaeus duodarum and, 184 English Channel, long-term research, 2–3 benthos in, 54–5 CPR analysis in, 63–70 CPR method consistency and, 70, 71, 72 currents/circulation and, 16–9 data limitations in, 77 data reexamination in, 79 demersal fish and, 48–54 drift-bottle data, 16 ecology/species changes and, 77–8 historical background of, 3–9 importance of, 76–7 intertidal observations in, 42–8

321 MBA and, 9–13 mesoscale hydrography in, 76 mesozooplankton/productivity and, 38–9 NAO in, 78–9 nutrients and, 19–24 physiological/species factors and, 78–9 phytoplankton blooms in, 25, 26, 72–3 phytoplankton/productivity and, 24–31 PML/IMER and, 56–61 Russell cycle in, 37, 78 SAHFOS and, 61–3 temperatures/alinity and, 12, 13–9 zooplankton species in, 73–6 zooplankton/larval/pelagic fish and, 31–43 Enteromorpha spp. in fish farm biofouling, 227, 230–1 Environmental factors benthic fauna and, 2 benthos distribution and, 55 climate and, 2–3 cooling and, 2 current/circulation, 160, 179–80 in estuaries, 111, 127 gravity, 162–3, 170–3 intertidal fauna and, 2, 78 larval fish and, 2 light, 162–3, 173–7 light intensity, 162 light polarity, 162 pelagic fish and, 2, 39 pressure, 162–3, 170–3 salinity, 162, 177–9 temperature, 162, 179 warming and, 2 zooplankton and, 2 ENVISAT MERIS ocean colour sensor on, 61 ERSEM see European Regional Seas Ecosystem Model Estuaries Carcinus maenas export in, 150, 152, 153 decapod larvae transport in, 124–7, 128, 130 environmental conditions of, 127 environmental stresses of, 111 fixed-station sampling in, 110, 139, 146 flux-strength equation in, 131 lateral tidal shear in, 129, 130 megalopae in, 110, 123, 126, 129, 132, 176–7

322 Estuaries (cont.) as nurseries, 139 physical mechanisms in, 118–19, 122, 124 Rhithropanopeus harrisii in, 150, 151, 170, 173–8 salinity in, 127 selective tidal stream in, 127, 128, 129 tidal current asymmetry in, 129–31 water temperature and, 127 wind-generated exchange in, 131–2 European Continental Slope Current, 18 European Regional Seas Ecosystem Model (ERSEM), 80 European Union Biocidal Products Directive (BPD), 235 Fast Repitition Rate Fluorometer (FRRF) at station L4, 56, 61 Feeding dynamics, 3 Fish farm biofouling/remediation alternate strategies, 216 antifoulant technology, 231–3 aquaculture trends and, 217 beneficial effects of, 221–2 biological control/grazing in, 240–1, 242–3 detrimental effects of, 219–21 diatoms in, 224–5 diseases in fish farms and, 220, 221 economic consequences of, 222 external factors in, 224 fish farm v. ship methods in, 216 fouling process in, 224–5 fouling taxa, 226, 228–31 legislation in, 235 macroalgae and, 227, 230–1 macrofouling and, 225 nontoxic antifoulants, 238–40, 242–3 records on, 216–17 toxic antifouling materials, 233–4, 237 Fisheries cyclical populations of, 41, 43 exploitation of, 3, 55 herring, 2, 6, 35, 39–40 mackerel, 6, 35, 76 pilchards, 35, 39–40 pollution of, 3 sardines, 29 unsustained harvesting of, 51–2

SUBJECT INDEX

Fixed-station sampling in decapod larvae dispersal, 110, 139 estuaries and, 110, 139, 146 limitations of, 139 Flagellate blooms see also Diatom blooms; Dinoflagellate blooms types of, 28 Flounder spawning migration of, 50 Fluorescence in bio-optics/photosynthesis, 58 Food-web influences on, 57, 78, 79 planktonic, 57 FRRF. see Fast Repitition Rate Fluorometre Gadus morrhua (cod) cooling and, 52–3 TBT and, 238 Gibbula umbilicalis, 47 GLOBEC, 9 Government Development Commission research expansion, 6 Gulf of Carpentaria decapod larvae dispersal study and, 157–9 Gulf stream, 134–5 Gyrodinium aureolum in dinoflagellate blooms, 58 Haddock distribution changes in, 76 Health and Safety Executive (HSE), 234 Hermit crabs, 47 Herring competition with pilchard and, 78 fisheries, 2, 6, 35, 37, 39–40 Hippoglossoides platessoides (long rough dab) distribution changes in, 76 Horizontal transport of decapod larvae,105–11. see Decapod larvae behavioural control evidence in, 164, 165–8, 169, 170–86 continental margins in, 132–5 cross shelf flow/exchange in, 121–3 depth regulation mechanisms in, 187–8 diel cycles in, 137–8 diel migrations in, 154–5, 156, 157–9 ecological categories in, 117–18 endogenous rhythms in, 163–4, 181–6 estuarine transport in, 124–7, 128, 130

SUBJECT INDEX

flood tide in, 126–7, 143, 150 frontal zones in, 132–5 geostrophic currents in, 120–1, 132–4 internal waves in, 124 larval stages and, 113–16 measurements of, 192–6 migratory behaviour/tides in, 124–7, 149–50, 151–2, 153–4 night-time in, 126–7, 176 ontogenetic migrations in, 159–61 pooling zone, 122 sea/land breezes in, 124 stimulus responses in, 161–3, 170–86 swimming velocities in, 190–2 taxonomic prevalence/vertical movement and, 139, 140–2, 143 tides/currents in, 119–24, 137–8 vertical migration field studies and, 148–61 vertical migration modifiers in, 188–90 vertical migrations in, 116–17, 137–43 vertical migrations, nonrhythmic in, 186–7 water column position importance in, 161 IBP see International Biological Program ICES see International Council for the Exploration of the Sea Ichthyoplankton, 75–6 Bulletins of Marine Ecology, 75 IMER see Institute for Marine Environmental Research Institute for Marine Environmental Research (IMER), 2, 7–8 MBA merger with, 2, 7–8 International Biological Program (IBP) sardine fisheries and, 29 International Council for the Exploration of the Sea (ICES), 5–6 Channel surveys and, 10–13 Plymouth stations and, 7–9 Intertidal fauna barnacles, 43–7 environmental change and, 2, 78 hermit crabs, 47 life cycle factors in, 78–9 limpets, 42, 46, 47 Intertidal flora macroalgae in, 47–8

323 Laminaria ochroleuca temperature change and, 47–8 Land-Ocean Interaction Study (LOIS), 9 Langmuir circulation winds/currents and, 148 Larval fish environmental change and, 2 Light attenuation in water and, 27 measurements of, 27 pigments, in transmission of, 27–8 Limpets, 42, 46, 47 LOIS see Land-Ocean Interaction Study Loligo forbesi (squid) migration of, 50 species composition of, 55 Loligo vulgaris (squid) species composition of, 55 Longhurst-Hardy Plankton Recorder, 138 Low-income food-deficit countries LIFDC), 217, 241 Mackerel fisheries, 6, 76 Macroalgae, 47–8 MAFF, 80 MarClim see Marine Biodiversity and Climate Change Consortium Marine Biodiversity and Climate Change Consortium (MarClim), 80 Marine Biological Association of the United Kingdom (MBA), 2–3, 80, 82 ICES stations and, 9–10, 11, 12 imaging and, 14, 31 IMER merger with, 7–8 Marine Environmental Change Network (MECN), 80 Marine optics research light attenuation in, 27 measurements of light in, 27 pigments/light transmission in, 27–8 MBA see Marine Biological Association of the United Kingdom Mean tide level (MTL), 42–3 MECN see Marine Environmental Change Network Megalopae of Callinectes sapidus, 180, 182, 185–6 of Carcinus maenas, 160, 180, 182, 185–6 definition of, 185 in estuaries, 110, 123, 126, 129, 132, 176–7

324 Megalopae (cont.) flooding and, 180 light stimulus and, 171–2 moults in, 148 night floods and, 153, 177 pressure/gravity and, 171 STST and, 149–50 turbulence and, 180 vertical migration of, 146–7 Melanogrammus aeglefinus (haddock) distribution changes in, 76 MERIS ocean colour sensor on ENVISAT, 61 Mesoscale hydrography in long-term research, 76 Mesozooplankton copepods and, 255–6 global importance, 255–6 productivity and, 38–9 sampling of, 33, 36, 37, 38 seasonality, 29, 31 Messhai nets, 138 Micromesistius poutassou (blue whiting) distribution changes in, 76 MOCNESS nets, 138 Moulting in copepod excretion, 262, 284–5, 286 decapod larvae and, 111, 155 in megalopae, 148 moulting rate in copepods and, 267–8, 284–5 MTL see Mean tide level Munida bamffica sea temperature and, 55 Mytilus edulis (blue mussel) marine biofouling/remediation and, 216, 226 Nanoplankton, 25 NAO see North Atlantic Oscillation National Institute of Oceanography, 18 NATO see North Atlantic Treaty Organization Natural Environment Research Council (NERC) IMER and, 7 Natural product antifoulant (NPA), 232 Neoparamoeba pemaquidensis amoebic gill disease pathogen, 220, 239 NERC see Natural Environment Research Council

SUBJECT INDEX

Nets Messhai, 138 MOCNESS, 138 Neuston, 148 sampling, 16, 30, 33, 34–5, 56, 81 Neuston layer, 137–8 wind effects on, 155 zoea in, 153 Neuston nets, 148 Nitrates, inorganic as nutrient, 19–20, 22, 24 Nitrogen in copepod outfluxes, 256–7, 282–92 as NH4 in copepod excretion, 256–7, 269 uptake by phytoplankton, 290 Nitrogen, dissolved organic as nutrient, 20, 22, 23, 24 NLB see Nonleaching biocide Nonleaching biocide (NLB), 232 North Atlantic Oscillation (NAO), 2–3 climate and, 78–9 currents/circulation relationship to, 18 diatom blooms and, 58 plankton blooms and, 58, 60 temperature/salinity relationship to, 16 water temperature/salinity in, 16 wind-driven component of, 18–9 North Atlantic Treaty Organization (NATO) sardine fisheries and, 29 NPA see Natural product antifoulant Nucella lapillus (dogwhelk) TBT and, 48 Nutrient copepod excretion role in, 280–1 Nutrient signals, 25, 26 phytoplankton composition and, 24, 27 Nutrients carbon as, 20, 21, 26 dissolved organic nitrogen as, 20, 22, 23, 24, 276 dissolved organic phosphorus as, 20–1, 23, 286 inorganic nitrates as, 19–20, 22, 24 inorganic phosphates as, 19–21, 22, 23 nitrate-phosphate ratio, 21 regeneration in copepod outfluxes, 289–90 silicates as, 22

SUBJECT INDEX

Octopus vulgaris sea temperature and, 55 Ontogenetic influences in decapod larvae, 112, 116 in decapod larvae dispersal, 117, 159–61 vertical distribution in decapods and, 143–8 Osilinus lineatus, 47 Panulirus cygnus nocturnal migrations of, 159 ontogenetic dispersal in, 117, 159–61 phyllosoma stages in, 159 PAR see Photosynthetically active radiation Parasagitta elegans as indicator species, 35–6, 38–9 population cycles of, 41, 43 Parasagitta setosa as indicator species, 35–6, 38–9 Particulate matter (PM) in copepod outfluxes, 255–6, 280–2 Patella spp., 42, 46 depressa, 47 PDMS see Polydimethylsiloxan Pelagic fish Calanus helgolandicus as food for, 40–1 environmental change and, 2, 39 fishing intensity and, 39 Penaeus duodarum endogenous rhythms of, 184 Penaeus plebejus estuary export/reinvasion by, 153 Penaeus spp. diel migration pattern of, 157–9 Gulf of Carpentaria study and, 157 plebejus, diel migration pattern of, 153 Peritrophic membrane in copepod faecal pellets, 258, 272, 286 roles of, 258 Phosphates, inorganic as nutrient, 19–21, 22, 23 in pollution, 9 seasonal variations in, 20, 21, 22, 23 Phosphorus copepod excretion and, 257, 269, 286 Phosphorus, dissolved organic as nutrient, 20–1, 23, 286 Photosynthetically active radiation (PAR) in bio-optics/photosynthesis, 60

325 Phototaxis see also Environmental factors in decapod larvae dispersal, 111, 117 in Rhithropanopeus harrisii, 175 Phytoplankton biomass measurement of, 27 blooms of, 25, 26, 72–3 culturing of, 25 depth distribution of, 27 fluorescence in, 58 light attenuation and, 27–8 nitrogen uptake by, 290 nutrient signals and, 24, 27 poisoning in fish farms and, 220 productivity research on, 24–31 seasonality of, 27, 28 surveys of, 10 Phytoplankton quantum efficiency (PQE), 61 Pilchard, 6, 35, 37, 38 competition with herring and, 78 distribution changes of, 76 fisheries of, 39, 40, 41 Plankton nanoplankton and, 25 surveys of, 6, 9, 10 Platichthys flesus (flounder) spawning migration of, 50 PlyMBODy see Plymouth Marine Bio-optical Data Buoy Plymouth Marine Bio-optical Data Buoy (PlyMBODy) validation of SeaWiFS by, 61 Plymouth Marine Laboratory (PML), 2 CPR surveys and, 9, 80, 82 PM see Particulate matter PML see Plymouth Marine Laboratory POLCOMS see Proudman Oceanographic Laboratory Coastal Ocean Modelling System Pollution accute, 3 chronic, 3 crude oil and, 3, 48 phosphate levels of, 9 species destabilization by, 3, 48 TBT and, 3, 48, 237 Polydimethylsiloxan (PDMS), 238–9 PQE. see Phytoplankton quantum efficiency Preferendum hypothesis zooplankton/light intensity and, 174, 176

326 Prorocentrum spp. in dinoflagellate blooms, 73 Proudman Oceanographic Laboratory Coastal Ocean Modelling System (POLCOMS), 80 Pseudocalanus spp. at station L4, 57–8 Quantitative long-term data, 15 Quantitative measurement techniques 14C uptake analysis in, 21, 28 in marine chemistry, 19 sampling for, 25, 34 Raja brachyura (blond ray) decline of, 51–2 Rate of change hypothesis in zooplankton, 174, 176 Remote Sensing Data Analytical Service (RSDAS) imaging and, 14, 31 Research vessels, 4, 5–6 Rhithropanopeus harrisii depth regulation of, 174–5, 187 in estuaries, 148, 151, 170, 173–8 phototaxis in, 175 response to stimuli in, 173–7 tidal migrations of, 181–2, 185 water column migration and, 150, 151, 152, 182 RSDAS see Remote Sensing Data Analytical Service Russell Cycle, 37, 78 SAHFOS. see Sir Alister Hardy Foundation for Ocean Science Salinity autoanalytical techniques and, 7 changes in, 177–9 circulation and, 13, 15 decapod larvae dispersal and, 110–11, 189–90, 266 in estuaries, 127 photataxis changes with, 178 rainfall/windstrength and, 16 run-off and, 13, 15 seasonal trends and, 13, 15 Sv unit and, 15

SUBJECT INDEX

water temperature in English channel and, 12, 13–19 water temperature/NAO and, 16 Sampling programs, 5–6, 34–5 continuous measurement in, 18 drift-bottle method in, 16 drifting buoys in, 18 fixed-station sampling, 110, 139, 146 long-term data summary of, 57 nets used in, 16, 30, 33, 34–5, 56, 81 for quantitative measurement, 25, 34 sampling methods of, 16 station E1 and, 61, 81 station L4 and, 8–9, 56–8, 59, 60, 61, 80 stations L1/E5 and, 8–9, 80–1 stations off Plymouth and, 7–9 stations/South West England and, 45–6 time-series measurement in, 40–1 tow-net method in, 15, 25, 30 for zooplankton, 16 Sardina pilchardus (pilchard), 37, 38–40 cyclical populations of, 41, 43 Sardines fisheries of, 29 Scomber scombrus (mackerel) distribution changes in, 76 Scottish Oceanographic Laboratory relationship to SAFHO/SIMER, 61 Sea Viewing Wide Field-of-view Sensor (SeaWiFS), 29, 31 validation by buoys, 61 Selective tidal stream transport (STST) in decapod larvae dispersal, 149–50 Semibalanus spp. balanoides, 46 cold-water species of, 46 Silicate in diatom blooms, 22, 24 as nutrient, 22 Sir Alister Hardy Foundation for Ocean Science (SAHFOS), 2, 3 CPR surveys and, 9, 61, 80, 82 relationship to Scottish Oceanographic Laboratory, 61 Squid, veined migration of, 50 species composition of, 55 St. George’s Channel, 18 Straits of Dover currents/circulation in, 19 STST see Selective tidal stream transport

SUBJECT INDEX

Sunspot index water temperature and, 15–16 Sv see Sverdrup unit Sverdrup unit (Sv) in salinity, 15 TBT see Tributyl tin Temperature see Water temperature tilapia, 221, 224, 241 TKE see Turbulent kinetic energy Tow-net method in sampling programs, 15, 25, 30 Toxin transport copepod faecal pellets and, 284, 289 Tributyl tin (TBT) Gadus morrhua and, 48 Nucella lapillus and, 48 oysters and, 237 Skeletonema costatum and, 48 species sensitivity to, 3, 48, 236, 237, 238 Trisopterus esmarkii cold-water gadoid, 54 Turbulent kinetic energy (TKE), 180 Undulating Oceanic Recorder (UOR), 60 UOR see Undulating oceanic Recorder Upwelling, 148 cross-shelf flow and, 121, 122, 123, 134 frontal zone, 135–6 validation by CZCS/UOR, 60–1 Venus verrucosa sea temperature and, 55 Vertical fates of copepod outfluxes, 254, 287–90 Vertical flux (VF) equation for, 269–70 sedimentation rate and, 269–70 sinking speed, 270–2 Vertical flux, passive biodegradation/microorganisms influenced, 278–9, 288 in copepod excretion, 270–2, 274–5 coprophagy in, 277–8 coprorhexy/coprochaly in, 276–7 molecular diffusion/physical degradation and, 273–6 Stokes’ equation and, 270, 272 stratification/turbulent diffusion and, 273 vertical advection and, 272–3

327 Vertical migrations diel cycles and, 279, 289 field studies in, 148–61 horizontal transport of decapod larvae and, 116–17, 137–43 of megalopae, 146–7 modifiers of decapod larvae dispersal, 188–90 nonrhythmic, 186–7 positioning in decapod larvae dispersal, 108–10 water column and, 146, 161, 162, 171 of zoea, 150 Viruses, 3, 25, 57 Water column, 3, 9 copepod outfluxes and, 292 DOC in, 269–70, 282–3, 289 DON in, 24 horizontal transport in decapod larvae and, 110, 116, 117, 121, 126–7, 133, 138 larval velocity in, 194–5 light influence in, 177, 188 MECN research on, 80 PM in, 292 position importance in transport and, 161 Rhithropanopeus harrisii migration and, 150, 151, 152, 182 SMART buoy data on, 81 surface temperature, 12, 13 temperature influence in, 187–8 tidal influence in, 182, 185 turbulence influence in, 180 vertical flux in, 269–70 vertical migrations in decapod larvae and, 146, 161, 163, 171 vertical position in, 161, 163, 171 vertical stability in, 29, 72, 76 Water temperature, 3 autoanalytical techniques and, 7 column, 13, 14, 16, 187–8 estuaries and, 127 geotaxis changes with, 179 long term trends and, 13 rainfall/windstrength and, 16 salinity in English channel and, 12, 13–19 salinity of NAO and, 16

328 Water temperature (cont.) sunspot index and, 15–16 surface, 10, 12–13, 14–15, 16, 17 wind effects on, 18 Water transparency autoanalytical techniques and, 7 Wind effects continental margins and, 132–5 cross-shelf, 121, 122, 123–4 on current/scirculation, 19, 58 diurnal fluctuations, 124 Ekman flow and, 121, 122, 123, 148, 155, 156 Langmuir circulation and, 148 on NAO, 18–19 on neuston layer, 155 on salinity, 16 sea/land breezes, 124, 148 on water temperature, 18 wind-generated exchange in, 131–2 Wind-driven component cross-shelf, 121, 122, 123–4 in NAO, 18–19

SUBJECT INDEX

Zoea, 116, 123, 129, 146 of Carcinus maenas, 160 definition of, 185 depth regulation of, 173–5 in neuston layer, 153 night ebb tides and, 150, 152 pressure/gravity and, 170–1 semilunar export of, 154 vertical migration of, 150 Zooplankton see also Mesozooplankton Acartia clausi and, 74 biomass indicators in, 21, 28, 32, 35, 36, 37, 38 Calanus helgolandicus and, 73–4 Centropages typicus and, 74 environmental change and, 2 preferendum hypothesis/light intensity and, 174, 176 rate of change hypothesis in, 174, 176 sampling methods for, 16 seasonality of, 73–5 surveys of, 10, 73–6 zooplankton grazers and, 26 Zostera marina (eelgrass) in fish farm biofouling, 232