advances in marine biology, vol. 47

Advances in

MARINE BIOLOGY

VOLUME 47

This Page Intentionally Left Blank

Advances inMARINE 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, SouthamptonOceanography 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

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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 Oceanog-

raphy, 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 Oceanog-

raphy, Anavissos 19013, Attiki, Greece

Martin J. Genner, Marine Biological Association of the UK, Citadel Hill,


Nicholas C. Halliday, Marine Biological Association of the UK, Citadel

Hill, Plymouth, PL1 2PB, UK

Nicholas J. Hardman-Mountford, Plymouth Marine Laboratory, Pros-

pect 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,


J. H. Hecq, MARE Centre, Laboratory of Oceanology, Ecohydrodynamics

Unit, University of Liege, B6, 4000 Liege, 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,


Rebecca Leaper, Marine Biological Association of the UK, Citadel Hill,


*Current address: School of Ocean Sciences, University of North Wales

Bangor, Menai Bridge, Gwynedd, LL59 5AB, UK

L. A. McEvoy, North Atlantic Fisheries College, Port Arthur, Scalloway,

Shetland, ZE1 0UN,UK

Nova Mieszkowska, Marine Biological Association of the UK, Citadel Hill,


Robin D. Pingree, Marine Biological Association of the UK, Citadel Hill,


Henrique Queiroga, Departmento de Biologia, Universidade de Aveiro,

Campus Universitario 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,


Tania Smith, Plymouth Marine Laboratory, Prospect Place, Plymouth, PL1

3DH, UK

Alan J. Southward, Marine Biological Association of the UK, Citadel Hill,


Anthony W. Walne, Sir Alister Hardy Foundation for Ocean Science,

Citadel Hill, Plymouth, PL1 2PB, UK

vi CONTRIBUTORS TO VOLUME 47

CONTENTS

CONTRIBUTORS TO VOLUME 47 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . vSERIES CONTENTS FOR LAST TEN YEARS. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ix

Long-Term Oceanographic and Ecological Research inthe 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. Introduction and Historical Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

2. MBA. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

3. PML and the Former IMER . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56

4. SAHFOS. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61

5. Overview . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 76

Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83

References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 84

Interactions Between Behaviour and Physical Forcing inthe Control of Horizontal Transport of Decapod

Crustacean Larvae

Henrique Queiroga and Jack Blanton

1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 109

2. Definitions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 113

3. Marine Physical Processes and Larval Transport Mechanisms . . . . . . . . . . . . . . . . . . . . . . 118

4. Cyclic Vertical Migration in the Natural Environment. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137

5. Ontogenetic Migration and the Extent of Vertical Movements . . . . . . . . . . . . . . . . . . . . . . 143

6. Significance of Vertical Migration in Dispersal: Evidence from Field Studies . . . . . . . . 148

7. Proximate Factors Controlling Vertical Migration: Environmental Factors and

Endogenous Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161

8. Behavioural Control of Vertical Migration: Evidence from Laboratory Studies . . . . . 164

9. Nonrhythmic Vertical Migration. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 186

10. Mechanism for Depth Regulation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187

11. Modifiers of Vertical Migration Pattern: Temperature, Salinity, and Food . . . . . . . . . . 188

12. Vertical and Horizontal Swimming Velocities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 190

13. Measurements of Horizontal Transport. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192


References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 196

Marine Biofouling on Fish Farms and Its Remediation

R. A. Braithwaite and L. A. McEvoy

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 216

2. Nature and Extent of Problem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 218

3. The Fouling Community of Fish-Cage Netting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223

4. Antifouling Technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 231

5. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 241


References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 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. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 254

2. Nature of Copepod Outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256

3. Factors Controlling the Rate of Copepod Outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263

4. Vertical Flux. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 269

5. Role of Copepod Outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 280

6. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 285


References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293

Taxonomic Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 311

Subject Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 317

CONTENTS

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., Pfannkuche, 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, bio-

geography, 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.

Sokolova, M. N. Trophic structure of abyssal macrobenthos. pp. 427–525.

Semina, H. J. An outline of the geographical distribution of oceanic phyto-

plankton. 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 inver-

tebrates. 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 pollu-

tion – 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.

Bergstrom, 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 develop-

ment 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.

x SERIES CONTENTS FOR LAST TEN YEARS

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, histochem-

ical 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 inverte-

brates. 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.

SERIES CONTENTS FOR LAST TEN YEARS xi

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., Muller-Navarra D. and Hagen W.

Fatty acid trophic markers in the pelagic marine environment. pp.

225–340.

xii SERIES CONTENTS FOR LAST TEN YEARS

Long-Term Oceanographic and EcologicalResearch 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,{ DavidW. 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, UKxSchool of Ocean Science, University of Wales Bangor,

Menai Bridge, Anglesey, LL59 5AB, UK

1. Introduction and Historical Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

2. MBA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

2.1. Temperature and salinity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

2.2. Currents and circulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

2.3. Nutrients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19

2.4. Phytoplankton and productivity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24

2.5. Zooplankton, larval stages of fish, and pelagic fish . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31

2.6. Intertidal observations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43

2.7. Demersal fish . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48

2.8. Benthos . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 54

3. PML and the former IMER . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56

3.1. Series at station L4 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56

3.2. Bio-optics and photosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58

ADVANCES IN MARINE BIOLOGY VOL. 47 � 2005 Elsevier Ltd.0-12-026148-0 All rights of reproduction in any form reserved

4. SAHFOS. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61

4.1. CPR methods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63

4.2. Consistency issues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70

4.3. Plankton and mesocale hydrography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72

4.4. Phytoplankton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73

4.5. Zooplankton species routinely identified . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 74

4.6. Zooplankton and ichthyoplankton not routinely identified. . . . . . . . . . . . . . . . . . . . . . . 75

5. Overview . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 76

Data Availability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82


References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 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 expan-

sion of many sampling programmes, is presented, and possible future ap-

proaches 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 ecosys-

tem. 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 abund-

ance 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.

2 ALAN J. SOUTHWARD ET AL.

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 anthro-pogenic disturbances such as fisheries exploitation and pollution. Comparison

of demersal fish hauls over time highlights fisheries eVects not only on com-

mercially 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 inmarine

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 inter-

actions, 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 time-

series 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 high-

resolution 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

LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 3

Figure 1 The Plymouth research vessels that have carried out chemical andphysical work in the western English Channel and sampled plankton, fish, andbenthos 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 to1921; (B) the 115-ft (36-m) North Sea steam trawler Huxley that sampled from 1903to 1909; (C) the 88-ft (27-m) ex-Naval steam drifter/trawler Salpa, that sampled from1921 to 1939; (D) the 90-ft (28-m) motor fishing vessel Sabella, leased from the Navy,


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 theMBA stated that researchers should ‘‘aim at practical results with

regard to the breeding and management of food fishes’’ (Southward, 1996).

Hence, even before theMBA laboratory buildingwas 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 vesselSula that sampled from 1948 to 1972, seen here winning her class at the Brixhamtrawler race in 1971; (F) the 60-ft (19-m) trawler Squilla that sampled from 1973 to2003, seen here from Sarsia on a joint fishing operation in October 1979; (G) thespecially designed 128-ft (39-m) Sarsia that sampled from 1953 to 1981, seen here ona visit to the RoscoV Laboratory in Brittany in 1978; (H) the 42-ft (13-m) fast motorlaunch Sepia that sampled plankton from 1968 to 2004, seen in 1979. There was aconverted trawler, Frederick Russell, 143 ft (44 m), in use by the Marine BiologicalAssociation from 1981 to 1982, as a replacement for Sarsia, but it was converted togeneral oceanographic research in 1982 and was not available for time series work oVPlymouth afterward. Photos from Marine Biological Association archives.


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 re-

search 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.


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

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


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 mon-

itoring the environment was seen as poor science by administrators, com-

pared 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.

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


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 phytoplank-

ton 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;


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 light-

house, it could be easily and reliably located. It has been used mostly for

sampling phytoplankton, zooplankton, and planktonic fish stages. The earli-

est 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)

Figure 4 Map of the English Channel showing the Marine Biological Associationsurveys in 1899–1900, the grid of English Channel stations used for the InternationalCouncil 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.


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 estab-

lished in 1959 following concerns that station E1 was not typical of condi-

tions in the western Channel (Cooper, 1958b). This was a grid of 42 stations

Figure 5 The various station grids used for MBA surveys in the western Channelin the second half of the twentieth century. (A) in 1959 (dotted line) and in 1960 (solidline); (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 revisedstation 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).


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


covering an area of 30 � 45 nm around E1 (Armstrong and Butler, 1962).

Chemical and physical conditions varied considerably from station to sta-

tion, 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 temperat-

ure 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, pre-cipitation minus evaporation, and water movement. Water movement has

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


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


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 s�1). 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 11-

year 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 SatelliteReceiving Station at the University of Dundee, processed by the National Environ-ment Research Council Remote Data Sensing Analysis group, Plymouth MarineLaboratory.)

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


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 complic-

ated than it appears from these investigations. From inspection of salinity

and temperature charts, Matthews (1914) deduced that there was a counter-

clockwise (cyclonic) swirl in the Celtic Sea, partly extending across the

mouth of the English Channel. Harvey (1929) attempted to employ geopo-

tential 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,

Table 1 Sampling methods for zooplankton in the Marine Biological Associationlong-term data series

Stations(see Figure 3)

Pre-1958 A (Russell, 1933)Post-1958 L5

Tow speed and timefor double obliquetow to 40m depth

Pre-1958 30 minutes at 2 knots1958–1978 20 minutes at 4 knots1978onward

20 minutes at 2 knots

Tow stabilization Post-1958 Scripps depressor (Southward, 1970)Net mesh Pre-1962 stramin, irregular holes �0.8mm

Post-1962 terylene, regular holes �0.7mmNet aperturedimension

Pre-1981 2m diameter, roundPost-1981 1m diameter, roundPost-1985 0.9m2, square (Southward, 1984)

Counting techniques All years Samples preserved in 5% formaldehyde;successively larger subsamples taken withStempel pipettes or by dipping ladle;counts adjusted to nominal 4000m3 waterfiltered (Russell, 1976; Southward andBoalch, 1986)


Figure 9 Annual mean sea surface temperature trends in the western EnglishChannel compared with the Bay of Biscay. Top, Marine Biological Association datafor E1, corrected for missing years by calculated annual mean diVerences fromnearby stations (the Seven Stones light vessel, Plymouth Sound, and along a linefrom Plymouth to Guernsey); middle, integrated data from square 508 to 51 8N, 48 to5 8W (Hadley Centre for Climate Research); bottom, integrated data for Bay ofBiscay square, 458 to 50 8N, 58 to 10 8W (Hadley Centre for Climate Research). Theheavy 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 warmperiod in the 1940–1950s was more pronounced in Biscay. The Marine BiologicalAssociation data, from mostly single monthly observations, show wider extremesthan the data for square 50–51, which is averaged from many observations eachmonth by merchant ships and other vessels.


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 dia-

grams 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 invest-

igations 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 Oceano-

graphy, and these studies established the tidal environment and examined

the circulation in the region (Pingree, 1980). Mean northerly to northwes-

terly currents to the west of the mouth of the English Channel (i.e. Rennell’s

Current) were found to be less than 3 cm s�1. 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 ideal-

ized 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, particu-

larly for the winter conditions of 1995–1996. Negative winter NAO condi-

tions 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.


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 Eddys-

tone 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 south-

ward 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 condi-

tions. 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 develop-

ment 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 phos-

phate 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 produc-

tion, 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


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 quan-

tified, 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 in-

creases 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

Table 2 Hydrographic and chemical sampling and analysis methods employed atE1 (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 organicphosphorus

1950s–1962 Harvey’s method (Harvey, 1955)ca. 1962–1987 Photocombustion technique (Armstrong and

Tibbitts, 1968)Nitrate Pre-1938 Reduced strychnine method (Cooper, 1932)

1966–1987 Cadmium copper reduction to nitrite (Butleret al., 1979; Wood et al., 1967)

Dissolved organicnitrogen

1962–1987 Photocombustion technique (Armstrong andTibbitts, 1968)

Sea surfacetemperature

To 1987 Insulated water bottle, then Lumby samplerand bathythermograph

Post-1995 Electronic thermometers fitted on researchvessels or conductivity–temperature–depthprobe (CTD)

Subsurface seatemperature profile

To 1987 Reversing water bottles with thermometersand bathythermograph

Post-1995 CTD


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:phos-

phate 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

Figure 10 Nutrients and phytoplankton production. (A) the winter maximum ofdissolved reactive (‘‘inorganic’’) phosphate at E1, 1924–1984, sampling wasnot 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 (unpublishedcompilation of data).


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

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


Figure 12 Examples of autumn and winter values of dissolved reactive (‘‘in-organic’’) phosphate from cruises and the Channel Grid as microgram-atoms P perlitre. (A) surface values, 18–25/2/1959; (B) the same dates, bottom values showing thewater column is well-mixed; (C) values at 10m, 25–28/10/1965; (D) values at 10 m, 7–9/12/1965. (Reproduced, with permission, from Southward, A. J. (1962). The distri-bution of some plankton animals in the English Channel and approaches. II. Surveyswith the Gulf III high-speed sampler, 1958–1960. Journal of the Marine BiologicalAssociation 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 chemistrysurveys in the western English Channel during 1965 and 1966. Journal of the MarineBiological Association of the United Kingdom 54, 895–914; Figures 5 and 15).


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 compos-

ition (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

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


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 Asso-

ciation, 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

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


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

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


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; find-

ings 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,

Figure 16 Vertical distribution of chlorophyll a from March to October, stationE1, 1975–1976, as milligrams per cubic metre. The lower panel shows details ofsampling. (Reproduced, with permission, from Holligan, P. M. and Harbour, D. S.(1977). The vertical distribution and succession of phytoplankton in the westernEnglish Channel in 1975 and 1976. Journal of the Marine Biological Association ofthe United Kingdom 57, 1075–1093; Figure 3.)


although inshore waters were also investigated (L4, L5). This important

work provided the foundation for subsequent marine optics research.

After the establishment of theChannelGrid in 1961, phytoplankton studies

(counts, measurements of primary production by the 14Cmethod) 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 diVer-ences 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 near-

surface spring bloom (<4mg chl m�3 at 0–15m inApril); a summer subsurface

bloom in the thermocline (2–4 mg chl m�3 at 20–25 m in May–September,

fueled by regeneratedNH4); and a near-surface autumn bloom (<2mg chl m�3

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 diVeringphysical stability of the water column and temperature (Figures 6 and 7)


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 Fevre,

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

Figure 17 Ocean colour studies to derive phytoplankton distribution and abun-dance in the Southwest Approaches andWestern English Channel were well advancedat the MBA in the early 1980s. The ocean colour data for this CZCS satellite image of22 June 1981 were processed to show the distribution and abundance of phytoplank-ton in relation to the physical environment for early summer condtions (Pingree,1974; Pingree et al., 1982). The delayed seasonal chlorophyll a maximum along thecontinental slope margin (typically 2mgm�3 in June) and increases in chlorophyll alevels 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 Seaand Western English Channel are typically 0.5mgm�3. Sediment loading (red) isobscuring the chlorophyll in some coastal regions.


Figure 18 A century of phytoplankton studies. (A) the diatom Odontella (Biddul-phia) sinensis (Greville) Grunow that colonised European waters at the turn of thenineteenth and twentieth centuries. (B) The centric diatom Coscinodiscus wailesiiGran et Angst that replaced Biddulphia as the dominant winter diatom after 1977.(C) The dinoflagellate Gyrodinium aureolum of Hulburt that invaded Europeanwaters in the 1950s, abundant, at frontal systems in the western Channel and thecause 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 barsfor A and B, 100 mm; C, 50 mm (photos A, B and C by G. T. Boalch; D from MarineBiological Association archives, and E by A. J. Southward).


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 intro-

duction 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 measure-

ment 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


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 con-

centrated 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

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

Group Species Water body association

Medusae andsiphonphores

Aglantha digitalis (O.F. Muller) NorthwesternLirope tetraphylla Chamisso andEysenhardt

Southwestern

Muggiaea atlantica Cunningham SouthwesternNanomia sp. ‘floats’ Northwestern

Polychaetes Tomopteris helgolandica Greef NorthwesternChaetognaths Parasagitta setosa (J. Muller) Channel

Parasagitta elegans (Verrill) NorthwesternParasagitta friderici (Ritter-Zahony) Southwestern

Copepods Calanus helgolandicus Claus WesternCandacia armata Boeck WesternSubeucalanus subcrassus(Giesbrecht)

Southern

Pareuchaeta hebes (Giesbrecht) Western/southwesternCentropages typicus Krøyer Western

Cladocerans Podon spp.Evadne nordmanii Loven

Amphipods Euthemisto gracilipes (Norman) NorthwesternEuphausids Nyctiphanes couchii (Bell) Western

Meganyctiphanes norvegica(M. Sars)

Northwestern

Molluscs Limacina retroversa (Fleming) NorthwesternBivalve larvae CoastalClione limacine (Phipps) Western

Echinoderms larvae of Luidia sarsi Duben andKoren

Northwestern

Echinoderm larvae and postlarvae CoastalTunicates Salpa fusiformis Cuvier Western/southwestern

oceanicDoliolidae South westernAppendicularia

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

Southward (1962).


Figure 19 Mesozooplankton sampling. (A) the 2-m net (‘‘ringtrawl’’) in its lastconfiguration, fitted with a terylene mesh; Sarsia, 1972; (B) the 0.9-m square net usedfor the L5 series from 1975; (C) a modified Kiel multiple closing net, fitted withtelemetering of depth, temperature and flow rate, arranged for horizontal tows in1978 and 1979 (photos by A. J. Southward).


Figure 20 Sampling oV Plymouth. (A) and (B) W. Garstang testing nets from thesteam yacht Busy Bee in 1899, a vertical quantitative net (A) and a horizontal closingnet (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 planktonapparatus in 1937; (D) F. S. Russell in the laboratory of Salpa sorting a catch takenby the 2-m net, 1937; (E) conductivity–temperature–depth probe with rosette of


by later analyses (Southward, 1980; Southward et al., 1995). The original

indicator species included north–south species pairings, so factors ex-

plaining 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 distribu-

tion 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 spawn-

ing 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 invest-

igation of pilchard spawning oV Plymouth during the same years (Southward

andDemir, 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 MarineBiological Association archives; E, N. Hardman-Mountford; F, T. Smith.


Figure 21 Examples of mesozooplankton ‘‘indicator’’ species of the westernEnglish Channel: (A) the siphonophore, Muggiaea atlantica, a southwestern indic-ator, abundant in warmer periods; (B) an assemblage of northwestern indicators,including the arrow worm Parasagitta elegans, the medusa Aglantha digitalis, larvaeof the starfish Luidia sarsi, the siphonophore Nanomia sp., and euphausids, allabundant in cooler periods; (C) the copepod Pareuchaeta hebes, a western andsouthwestern indicator; (D) the southwestern warm-water copepod Subeucalanussubcrassus. Scale bars A, C, and D, 1 mm; B, 10 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

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


Figure 23 Examples of long-term data on mesozooplankton abundance at sta-tions 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


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, thechange 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 south-

west 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 overexploita-

tion, that eventually led to a moratorium on North Sea catches (Hawkins

et al., 2003). The pelagic fish populations oV California have shown consid-

erable 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 oVCalifornia, the species of pelagic fish oV Devon and Cornwall have fluctu-

ated over a long timescale, with the variation driven by changes in the

environment. Historical and recent records indicate that herring and pil-

chard 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 Para-sagitta elegans (cold-water northern form) and Parasagitta setosa (intermediate andwarm-water species common in the English Channel and North Sea); (D) larvalstages of decapod crustaceans (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 longer-

term 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 oVPlymouth, 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

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 spawnedin spring/summer (April to July) and in autumn (August to December; MarineBiological Association database).


fish and of invertebrate plankton such as Parasagitta. Although it is a

warmer-water species compared to its northern congener, Calanus finmarch-

icus (Beaugrand et al., 2002), C. helgolandicus has tended to be most abund-

ant 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). Cold-

water 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, coin-

ciding 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


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


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 neces-

sary 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 communi-

cation; 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 allrecently 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 haverecently 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).


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


(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 inter-

tidal 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 intothree tide levels, high water neaps, mid-tide level, and low water neaps; Chthamalusshown with thick lines, Semibalanus with thinner lines (data from Marine BiologicalAssociation database).

Figure 27 Sites around southwest England surveyed each year for abundance ofintertidal barnacles and other rocky shore organisms, 1954–1987. Eight on the northcoast: 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, PrawlePoint; Br, Brixham; Ly, Lyme Regis; Pt, Portland Bill (data from Marine BiologicalAssociation database).


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) invest-

igated 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 dom-

inated 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 byChthamalus spp. in warmer periods is thought

to be mediated by competition. Higher temperatures cause increased mortal-

ity 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 twoChthamalus 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 (South-

ward, 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 correspondenceis 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


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 col-

onized 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 barn-

acles, 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 macro-

algal 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


(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 oscilla-

tions (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


from 19 to 39 m. However, the trawl gears used were of comparable dimen-

sions, 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-tem-

poral-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 pro-

vided 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

Figure 28 The Plymouth inshore fishing grounds surveyed for demersal fishabundance 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, wasmost frequently sampled (Marine Biological Association database).


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 move-

ment, 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, population-

level 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 tempera-

tures 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 sub-

jected 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 warm-

water species (Southward and Boalch, 1992). After 1985, there was a re-

sumption of the warming trend, with increases in warm-water fish, a trend

that has been observed at other locations in southwest England (Stebbing


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 opportunistic-

ally in response to warming, although the reverse has not occurred—equiva-

lent 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 demon-

strated to contain a subset of dominant species whose abundancewas 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

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


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 mesozoo-

plankton net in early April contained viable cod eggs (up to 15% of total fish

Figure 30 Demersal fish. (A) preliminary sorting of trawl catch on deck of Sarsia,1963; (B) adult cod, about 450mm total length; (C) changes in individual total lengthof 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, afterabsorption of yolk sac. Photographs: A and D, A. J. Southward; B, D. W. Sims.


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). Surpris-

ingly, 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

Figure 31 Examples of rare fish of warm-water distribution caught in the westernEnglish Channel, 1949–1972 (based on Russell, F. S. (1953). The English Channel.Transactions of the Devonshire Association for the Advancement of Science, Literatureand Art 85, 1–17, with recent changes in nomenclature). (A) Alosa finta; (B) Polyprionamericanum; (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.


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 intermit-

tently 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 extens-

ive 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 Eddystone grounds Dredge; trawl Allen, 18991906 Outside Eddystone Dredge; trawl Crawshay, 19121922–1923 Plymouth area Grab Ford, 19231928–1929 Inside Eddystone Grab; trawl Steven, 19301931 Eddystone gravels Conical dredge Smith, 19321939 Rame mud Corer; grab Mare, 19421949–1951 Plymouth area Camera Vevers, 1951, 19521950 Plymouth area Grab Holme, 19531958–1962 English Channel Anchor-dredge Holme, 1961, 1966a1970–1981 W English Channel Dredge Holme, 19841972–1982 Lizard-Start Point TV sledge Wilson et al., 1977;

Franklin et al., 19801997–2002 Fowey-Eddystone Scallop dredge;

anchor dredgeKaiser et al., 1998Kaiser and Spence, 2002


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 Denta-

lium 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 hypo-

theses 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 echino-

derm 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, high-

lighting 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 experi-

mental 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).


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 transitional-

mixed 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 (200mm) Vertical haul from 50m to the surfaceWP2 net (50 mm)a Samples stored in 5% formalin

Identification to genera/species levelunder dissecting microscope,completed within a week of sampling

Phytoplankton Bottle samples Collected at 10m depthSamples stored in 2% Lugol’s iodine(Holligan and Harbour, 1977)

10–100mL of sample is settled andspecies abundance determined usingan inverted microscope.

Chlorophyll Bottle samples Determined on 90% acetone extracts ofGF/F filtered samples, using a TurnerDesigns fluorometer.

Particulatecarbonand nitrogen

Bottle samples 250-mL aliquots are prefiltered througha 200-mm mesh, then filtered onto25-mm ashed glass fibre filters (GF/F).

CN samples are washed with phosphatebuVered saline before storage at �25 8C.

All analyses use a Carlo-Erba ElementalAnalyser Model NA1500.

Nutrientsa

nitrate, nitrite,ammonium,phosphate,silicate

Bottle samples 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)

Temperatureand salinity

CTD fitted with afast repetition ratefluorometer andtransmissometer)

CTD haul to 50m

aSamples collected since May 2002.


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 zooplank-

ton 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

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


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 compos-

ition has important consequences for ecosystems in terms of both energy

transfer eYciency and nutritional value for upper trophic levels. The dinoflagel-

late 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 Fevre, 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 measure-

ments have been made opportunistically throughout the western English

Channel (Aiken, 1981a, 1985; Aiken and Bellan, 1986a, 1990). From this


Figure 33 Examples of seasonal and annual changes in abundance of zooplank-ton at station L4. (A) females of the copepod Calanus helgolandicus (grey) and seasurface temperature (black); (B) female Calanus helgolandicus (grey) and phytoplank-ton concentration (black); (C) female Calanus helgolandicus (grey) and the dinoflagel-late Gyrodinium aureolum (black); (D) female Calanus helgolandicus (grey) and eggproduction rate of Calanus helgolandicus. [From Irigoien, X. and Harris, R. P. (2003).Interannual variability of Calanus helgolandicus in the English Channel. FisheriesOceanography 12, 317–326.]


work came significant advances in instrumentation and methodology for

quantifying chlorophyll fluorescence (Aiken, 1981b), chlorophyll absorption

(Aiken, 1985), bioluminescence (Aiken andKelly, 1984), and photosynthetic-

ally active radiation (PAR) (Aiken and Bellan, 1986a); notable are the devel-

opment 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 hemi-

spherical 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

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


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 photosyn-

thetic 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 compos-

ition 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


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) across section of the CPR, showing how it works (after Hardy, 1939); (C) the recentmodel CPR showing the box tail ready for deployment from a merchant ship.


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 Chan-

nel provides a regular broadscale picture of the plankton community com-

plementary 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-buVeredformalin 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 phytoplank-

ton 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 sampledmost 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 filteringsilk is assigned to four categories (which can beconverted to chlorophyll equivalents).

Stage 2: Phytoplankton analysis Phytoplankton are identified from 20 fieldscentred on the mesh and traversed diagonallyfrom corner to corner under �450magnification. The number of fields whereeach taxon is seen is counted (1/8000 of the silkis covered).

Stage 3: Zooplankton traverse Small zooplankton (<2mm) are identified andcounted on a stepwise traverse across both thefiltering and covering silks under �48magnification (1/40 of the silk is covered).

Stage 4: Zooplankton eyecount All larger zooplankton (>2mm) are removedfrom the silk, identified and counted.


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

Taxon Recorded from Comments

Acautharians 2004 Recorded with Radiolarians since 1993Branchiostoma lanceolatum (Pallas) 1946Calanus I–IV 1958 Juveniles of all Calanus species.Calanus glacialis Jaschnov 1955 1961 Separated from C. finmarchicus based on size alone.

Included in Calanus V–VI total.Calanus finmarchicus (Gunnerus) and Calanus

helgolandicus (Claus)1958 Recorded as separate species from 1958. Included in

Calanus V–VI total.Calanus hyperboreus (Krøyer) 1946Calanus V–VI total 1946 C. finmarchicus, C. helgolandicus, and C. glacialis.Caligoida 1946 Nearly all records are Caligus elongatus Nordmann, 1832.Candacia armata (Boeck) egg 1997 Denoted as ‘‘spiny egg’’ in the survey. Eggs of other

copepod species are recorded together as ‘‘copepod eggs.’’Caprellids 1946 For species see Vane (1951).Cavolinia spp. 1967Cephalopod larvae 1946 May include postlarvae. Some identification may be suspect.Chaetognaths 1946 Recorded separately in traverse and eyecount. For

species see Bainbridge (1963).Cirripede larvae 1958 Recorded as present since 1946. These are Balanidae

and Verrucidae larvae. For species see Roskell (1975).Cladocera (total) 1948–1957 Includes Evadne spp., Penilia avirostris and Podon spp.Clausocalanus sp. 1946 For species see Williams and Wallace (1975).Clio spp. 1946Clione limacina (Phipps) 1946Coccolithophores 1993 Recorded as present since 1965.Coelenterates 1946 Only recorded as present. Often identified by presence

of nematocysts.

64

ALAN

J.SOUTHWARD

ETAL.

Copepod eggs 1993 Recorded as present 1948–1957 and since 1974.Individual eggs are counted for both free and sacspawners. Only Candacia armata (Boeck, 1872) eggsare recorded separately.

Copepod nauplii 1958 Recorded as present since 1946.Coscinodiscus wailesii Gran and Angst 1977 Invasive; first recorded in European waters in the

English Channel in 1977.Cumaceans 1946Cyphonautes larvae 1958 Recorded as present since 1946.Decapod larvae 1946 For species see Lindley (1987).Dictyocysta spp. 1996 Recorded within total tintinnids previously. For

species see Lindley (1975).Dinoflagellate cysts 1993 Recorded as present since 1974. For species see Reid (1978).Dinophysis acuminata (Claparede andLachmann), D. acuta Ehrenberg, D. caudataSaville-Kent, D. norvegica Claparede andLachmann, D. rotundata Claparede andLachmann (¼Phalacroma rotundatum),D. sacculus Stein, D. tripos Gourret

2004 Previously all Dinophysis species were grouped(recorded as present since 1948, abundance from 1958).

Doliolids 1949–1957,1978–present

For species see Hunt (1968).

Echinoderm larvae 1949 For species see Rees (1954a).Echinoderm post-larvae 1946Euphausiids 1946 Separated into juveniles and adults from 1968 to 1988.Evadne spp. 1958 Recorded as present within Cladocera (total ) from 1948 to 1957.Favella serrata (Mobius) 1996 Recorded within tintinnids (total) previously.Fish eggs 1946Fish larvae (young fish) 1946 See Coombs (1980) for species recorded.Foraminiferans 1993 Recorded as present since 1946.Gammarids 1946 For species see Vane (1951).Gonyaulax spp. 1965 Includes other genera in Gonyaulaceae (e.g. Alexandrium)Halosphaera spp. 1996 Recorded as present since 1948. Counting method

changed in 1996.

(Continued )

LONG-TERM

RESEARCH

INTHEENGLISH

CHANNEL

65

Table 7 (Continued)

Taxon Recorded from Comments

Harpacticoids 1946 Includes mainly Microsetella spp.Hyperiids 1946 For species see Vane (1951) and McHardy (1970).Isopods 1947Lamellibranch larvae 1949 Recorded as present since 1946. For species see Rees (1954b).Larvaceans 1958 Recorded as present since 1946. The following

species have been identified: Oikopleura dioica Fol1872, O. labradoriensis Lohmann 1892, Fritillariaborealis Lohmann 1896 and F. pellucida Busch 1851.

Lepas nauplii 1955 For species see Bainbridge and Roskell (1966).Limacina retroversa (Fleming) 1958 Recorded as present since 1946.Lucifer typus H. Milne-Edwards 1997Mesocalanus (¼Calanus) tenuicornis (Dana) 1946Noctiluca scintillans Macartney 1981Ostracods 1947 For species see Williams (1975).Parafavella gigantea (Brandt) 1996 Recorded within total tintinnids previously.Parasitic nematode 1948Penilia avirostris 1946 Probably introduced into the North Sea by ballast

water in early 1990s.Phaeocystis spp. 1946 Abundance recorded from 1948 to 1957. Only recorded

as present since.Phytoplankton Colour 1946 Measured in four categories.Pinus pollen 1997Podon spp. 1958 Recorded as present within Cladocera (total) from 1948 to 1957.Polychaete larvae 1958 Recorded as present since 1946. Tomopteris spp. counted

separately.Polykrikos schwartzii cysts Butschli(‘‘Umrindetencysts’’)

1993 Recorded as present since 1975. The unarmouredmotile cells are not recorded in CPR samples.

66

ALAN

J.SOUTHWARD

ETAL.

Pseudocalanus spp. 1958 Includes only adult females and adult males. In theNE Atlantic and North Sea these are probablyPseudocalanus acuspes (Giesbrecht), P.elongatus (Boeck) and P. minutus (Krøyer).

Ptychocylis spp. 1996 Recorded within tintinnids (total) previously. For speciessee Lindley (1975).

Radiolarians 1993 Recorded as present 1948–1957. Includes Acantharians.From 2004, Acantharians recorded separately.

Rotifer eggs 1984 Adults are not identifiable in CPR samples.Salps 1949–1957,

1978–presentFor species see Hunt (1968).

Scrippsiella spp. 1982 Most records are of Scrippsiella trochoidea (Stein, 1883).Sergestid larvae 1962 For species see Lindley (1987).Silicoflagellates 1993 Recorded as present 1948–1957 and since 1964.Siphonophores 1958 Calycophorans only.‘‘Spindelei’’ 1983 Eggs of Kuhnia scombri, a monogenean gill parasite

of mackerel Scomber scombrus.Stauroneis (Navicula) membranacea (Cleve)F.W. Mills (¼Ephemera planamembranacea)

1962 Hartley (1986). First described from CPR samples inthe NW Atlantic in 1962.

Stellate body 1996 Land plant hair.Tasmanites (Pachysphaera) spp. 1958 Boalch and Guy-Ohlson (1992)Thaliaceans (salps and doliolids) 1946–1960 Recorded as present since 1946. Salps and doliolids

also recorded separately.Tintinnids (total) 1993 Recorded as present 1948–1957. For species

see Lindley (1975)Tintinnopsis spp. 1996 Recorded within tintinnids (total) previously. For species

see Lindley (1975).Tomopteris spp. 1946 Recorded separately from Polychaete larvae.Zoothamnium pelagicum Stein 1993 Recorded as present since 1964. Counted as number

of colonies.

aProcedures 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.

LONG-TERM

RESEARCH

INTHEENGLISH

CHANNEL

67

Figure 36 Sampling by the Continuous Plankton Recorder in the western EnglishChannel and Approaches, grouped into decades between 1950 and 2001. (A) 1950s to1970s; (B) 1980s to 2001. Each point represents a Continuous Plankton Recordersample. For purposes of the present analysis, the western English Channel area liesbetween 2 8W and 5 8W.


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


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


sampling position, but there have been greater changes in longitude. The

average sampling position in the western English Channel area was �4 8Wuntil 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 stratifica-

tion 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.


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 oVthe 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 conse-

quence 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 span-

ning 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 trendwas an increase in

the dinoflagellates Prorocentrum spp, Ceratium lineatum, Ceratium furca, Cer-

atium tripos, and Ceratium fusus and the diatoms Thalassiosira spp. and Rhi-

zosolenia shrubsolei. Complex relationships were found between the plankton

and environmental factors (salinity, sea surface temperature, radiation, atmos-

pheric 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 AtlanticOcean.

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


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 thatC. 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 meanannual abundance number per 3 cubic metres in the western English Channel ofselected taxa. (A) Coscinodiscus wailesii; (B) Acartia spp.; (C) Centropages typicus;(D) Euphausiacea. (A updated after Edwards et al., 2001; B to D updated afterRobinson and Hunt, 1986).


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. Somekey 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 abun-

dance 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 Para-

Pseudocalanus 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. Cope-

pod 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 Ibanez, 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 Ibanez (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 assem-

blages 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 nasu-

tus, 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 some-

times undertaken. These have been published in Bulletins of Marine Ecology


throughout the history of the survey. Surveys of common species have

been made for the following groups: cirripede larvae (Roskell, 1975), Clauso-

calanus (Williams and Wallace, 1975), Chaetognatha (Bainbridge, 1963),

gastropods (Vane, 1961), ostracods (Williams, 1975), the pteropodPneumoder-

mopsis (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 byMarshall (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 inter-

media, 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). Further-

more, 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 sea-

sonality 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


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 predict-

ing 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).


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 ecosys-

tems 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 organ-

isms, 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


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 cope-

pod 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 oVCalifornia between the Pacific sardine and Calanus pacificus (Smith and

Moser, 2003).

Other significant findings from the Plymouth time series relate to com-

mercial exploitation. The demersal fish records start before the large in-

creases 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 commer-

cially 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


properties on pelagic systems (Pingree and Pennycuick, 1975; Pingree et al.,

1975, 1976, 1977a,b, 1978; Pingree, 1978; Pingree and GriYths, 1978). Fur-

thermore, 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 re-

cently, 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 break-

down 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 Envir-

onment, Food and Rural Affairs (DEFRA) and within the framework of the

Marine Biodiversity and Climate Change (MarClim) consortium from Eng-

lish Nature (EN), Crown Estates, DEFRA, Scottish Natural Heritage

(SNH), Scottish Executive, Countryside Council for Wales (CCW), Envir-

onment 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 measure-

ments 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.


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 sam-

pling over varied temporal scales. Recent technologies such as advanced

Table 8 Sampling methods for E1 and L5, at monthly intervals, on resumptionof full series in 2001

Sample type Equipment Methods

Mesozooplanktonand young fish

0.9m2 YoungFish Trawl (YFT)fitted with a 700 mmTerylene net, partialfiltering cod-endand a Scrippsdepressor.

Double-oblique profile haul to�10m depth above the seabed

Depth and temperature profilesrecorded using a data recorder

Volume of water filteredcalculated using flow datarecorded by a flowmeterfitted across the net mouth

2 � 1-L sample jars containingaliquot of 20% borax-buVeredformaldehyde, for dilution byadding sample to give 5%

NutrientsNO3, NO2, NH4,PO4, SiO2

Rosette sampler þNiskin

10-L water samples from 60, 40, 30,20, 10 m, and surface

Autoanalyzer (Bran and LuebbeAA3)

Phytoplankton,zooplanktonand pigments

Rosette sampler53 mm WP2 net200 mm WP2 net

10m water sample (rosette sampler)4 � vertical hauls to 50 m, (2 �200 mm and 2 � 53 mm)

1 � horizontal 10m WP2 net(53mm) haul

Samples preservedin Lugol’s iodine and alsoexamined live

All pigments measured usinghigh-pressure liquid chromatography

Temperature,salinity, opticalproperties

2 � CTDs (SeaBirdand Valeport)

Vertical profile to 65 m

Optics rig(transmissometer,multispectraldownwellingirradiance, upwellingradiance, attenuation,scattering andback-scattering)


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.


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 Envir-

onment 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


projects, and a number of University Studentships. More recently partial

support has been provided through MECN. The data set has been main-

tained 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 arethanked for their help in this respect: Derek Harbour, Bob Head, AngelLopez-Urrutia, Xabier Irigoien, Tania Smith, and the masters and crews ofSepia and Squilla. Also thanked for help at sea or in the laboratory are JoseLuis Acuna, Ricardo Anadon, Begona Bautista, Alain Bedo, DelphineBonnet, Claudia Castellani, Kathryn Cook, Cilla Course, Emilio Fernandez,Edmund Green, Castor Guisande, Dave Lesley, Alistair Lindley, GermanMedina, Diego Menendez, Diana Menzel, Bettina Meyer-Harms, CarmenMorales, Birgit Obermuller, David Pond, Catherine Rey (Rassat), DaveRobins, Rachel Schreeve, Paul Tranter, Rachael Woodd-Walker, PennieWoodyer (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.

REFERENCES

Acuna, J. L., Bedo, A. W., Harris, R. P. and Anadon, R. (1995). The seasonalsuccession of appendicularians (Tunicata: Appendicularia) oV Plymouth. Journalof the Marine Biological Association of the United Kingdom 75, 755–758.

Aiken, J. (1981a). The Undulating Oceanographic Recorder mark 2. Journal ofPlankton Research 3, 551–560.

Aiken, J. (1981b). A chlorophyll sensor for automatic, remote operation in themarine environment. Marine Ecology Progress Series 4, 235–239.

Aiken, J. (1985). The Undulating Oceanographic Recorder mark 2. A multiroleoceanographic sampler for mapping and modeling the biophysical marine environ-ment. In ‘‘Mapping Strategies in Chemical Oceanography’’ (A. Zirino, ed.), pp.315–332. Advances in Chemistry Series, 209, American Chemical Society, Wash-ington DC.

Aiken, J. and Bellan, I. (1986a). A simple hemispherical logarithmic light sensor.Proceedings of the Society of Photo-Optical Instrumentation Engineers, SPIE,637, Ocean Optics 8, pp. 211–216.

Aiken, J. and Bellan, I. (1986b). Synoptic optical oceanography with the UndulatingOceanographic Recorder. Proceeding of the Society of Photo-Optical Instrumenta-tion Engineers, SPIE, 637, Ocean Optics 8, pp. 221–229.


Aiken, J. and Bellan, I. (1990). Optical oceanography: an assessment of a towedmethod. In ‘‘Light and life in the sea’’ (P. J. Herring, A. K. Campbell, M. Whitfieldand L. Maddock, eds.), pp. 39–57. Cambridge University Press, Cambridge.

Aiken, J. and Kelly, J. (1984). A solid state sensor for mapping and profilingstimulated bioluminescance in the marine environment. Continental ShelfResearch 3, 455–464.

Aiken, J., Fishwick, J., Moore, G. and Pemberton, K. (2004). The annual cycle ofphytoplankton photosynthetic quantum eYciency, pigment composition andoptical properties in the western English Channel. Journal of the Marine BiologicalAssociation of the United Kingdom 84, 301–313.

Alheit, J. and Hagen, E. (1997). Long-term climate forcing of European herring andsardine populations. Fisheries Oceanography. 6, 130–139.

Allen, E. J. (1899). On the fauna and bottom deposits near the thirty-fathom linefrom the Eddystone grounds to Start Point. Journal of the Marine BiologicalAssociation of the United Kingdom 5, 365–542.

Allen, E. J. (1917). Post-larval teleosts collected near Plymouth during the Summer of1914. 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 ofthe 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 planktonicorganisms. 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 in1959 and 1960. Journal of the Marine Biological Association of the United Kingdom42, 445–463.

Armstrong, F. A. and Tibbitts, S. (1968). Photochemical combustion of organicmatter in sea water for nitrogen, phosphorus and carbon determination. Journalof the Marine Biological Association of the United Kingdom 48, 143–152.

Armstrong, F. A. J., Butler, E. I. and Boalch, G. T. (1970). Hydrographic andnutrient 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 andnutrient 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 andnutrient 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 itsrelationship to the growth of the algal plankton. Journal of the Marine BiologicalAssociation of the United Kingdom 13, 119–150.

Atkins, W. R. G. (1925). Seasonal changes in the phosphate content of seawater inrelation to the growth of the algal plankton during 1923–1924. Journal of theMarine Biological Association of the United Kingdom 13, 700–720.

Atkins, W. R. G. (1926a). The phosphate content of seawater in relation to thegrowth of the algal plankton. Part III. Journal of the Marine Biological Associationof the United Kingdom 14, 447–467.

Atkins, W. R. G. (1926b). Seasonal changes in the silica content of natural waters inrelation to the phytoplankton. Journal of the Marine Biological Association of theUnited Kingdom 14, 89–99.


Atkins, W. R. G. (1926c). The distribution of red algae in relation to illumination.Nature 118, 155–156.

Atkins, W. R. G. (1928). Seasonal variations in the phosphate and silicate content ofseawater during 1926 and 1927 in relation to the phytoplankton crop. Journal ofthe Marine Biological Association of the United Kingdom 15, 191–205.

Atkins, W. R. G. (1930). Seasonal variations in the phosphate and silicate content ofseawater in relation to the phytoplankton crop. Part V. November 1927 to April1929, compared with earlier years from 1923. Journal of the Marine BiologicalAssociation of the United Kingdom 16, 821–852.

Atkins, W. R. G. and Jenkins, P. G. (1952). Note on sea temperatures in the EnglishChannel, 1921 to 1949, and Plymouth sunshine and light. Journal of the MarineBiological Association of the United Kingdom 31, 327–333.

Atkins, W. R. G. and Jenkins, P. G. (1953). Seasonal changes in the phytoplanktonduring the year 1951–52 as indicated by spectrophotometric chlorophyllestimations. Journal of the Marine Biological Association of the United Kingdom31, 495–508.

Atkins, W. R. G. and Jenkins, P. G. (1956). Factors aVecting the vernal phytoplank-ton outburst in the English Channel. Nature 177, 1218–1219.

Atkins, W. R. G. and Parke, M. (1951). Seasonal changes in the phytoplankton asindicated by chlorophyll estimations. Journal of the Marine Biological Associationof the United Kingdom 29, 609–618.

Atkins, W. R. G. and Poole, H. H. (1940). A cubical photometer for studyingthe angular distribution of submarine daylight. Journal of the Marine BiologicalAssociation of the United Kingdom 24, 271–281.

Atkins, W. R. G. and Poole, H. H. (1952). An experimental study of the scattering oflight by natural waters. Proceedings of the Royal Society of London, series B. 140,321–338.

Atkins, W. R. G. and Poole, H. H. (1958). Cube photometer measurements ofthe angular distribution of submarine daylight and the total submarine illu-mination. Journal du Conseil International pour l’Exploration de la Mer. 23,327–336.

Bainbridge, V. (1963). Continuous Plankton Records: contribution towards a plank-ton atlas of the north Atlantic and the North Sea. Part VIII: Chaetognatha.Bulletin of Marine Ecology. 6, 40–51.

Bainbridge, V. and Roskell, J. (1966). A re-description of the larvae of Lepasfascicularis Ellis and Solander with observations on the distribution of Lepasnauplii in the north-eastern Atlantic. In ‘‘Some contemporary studies in marinescience’’ (H. Barnes, ed.), pp. 67–81. George Allen and Unwin, London.

Barnes, B. I. (1961). Continuous Plankton Records: contribution towards a planktonatlas of the north-eastern Atlantic and the North Sea. Part IV: Thaliacea. Bulletinsof Marine Ecology. 5, 102–104.

Batten, S. D., Clarke, R. A., Flinkman, J., Hays, G. C., John, E. H., John, A. W. G.,Jonas, T. D., Lindley, J. A., Stevens, D. P. and Walne, A. W. (2003). CPRsampling—the technical background, materials and methods, consistency andcomparability. Progress in Oceanography. 58, 193–215.

Bautista, B. and Harris, R. P. (1992). Copepod gut contents, ingestion rates andgrazing impact on phytoplankton in relation to size structure of zooplankton andphytoplankton during a spring bloom. Marine Ecology Progress Series. 82, 41–50.

Bautista, B., Harris, R. P., Tranter, P. R. G. and Harbour, D. (1992). In situ copepodfeeding and grazing rates during a spring bloom dominated by Phaeocystis sp. inthe English Channel. Journal of Plankton Research. 14, 691–703.


Bautista, B., Harris, R. P., Rodriguez, V. and Guerrero, F. (1994). Temporalvariability in copepod fecundity during two diVerent spring bloom periods incoastal waters oV Plymouth (SW England). Journal of Plankton Research. 16,1367–1377.

Beaugrand, G. and Ibanez, F. (2002). Spatial dependence of calanoid copepodbiodiversity in the north Atlantic Ocean. Marine Ecology Progress Series. 232,197–211.

Beaugrand, G., Ibanez, F. and Reid, P. C. (2000). Spatial, seasonal and long-termfluctuations of plankton in relation to hydroclimatic features in the English Chan-nel, Celtic Sea and Bay of Biscay. Marine Ecology Progress Series. 200, 93–102.

Beaugrand, G., Reid, P. C. and Ibanez, F. (2002). Reorganisation of North Atlanticmarine copepod biodiversity and climate. Science 296, 1692–1694.

Biegala, I. C. and Harris, R. P. (1999). Sources of seasonal variability in mesozoo-plankton aspartate transcarbamylase activity in coastal waters oV Plymouth, UK.Journal of Plankton Research 21, 2085–2103.

Boalch, G. T. (1987). Changes in the phytoplankton of the Western English Channelin recent years. British Phycological Journal 22, 225–235.

Boalch, G. T. and Guy-Ohlson, D. (1992). Tasmanites, the correct name for Pachy-sphaera (Prasinophyceae, Pterospermatacea). Taxon 41, 529–531.

Boalch, G. T. and Harbour, D. S. (1977). Unusual diatom oV the coast of south-westEngland and its eVect on fishing. Nature 269, 687–688.

Boalch, G. T., Armstrong, F. A. J. and Butler, E. I. (1969). NATOProductivity Project.United Kingdom Report, from the Marine Biological Association of the U.K.Technical Report. NATO Subcommittee on Oceanographic Research 47, 96–102.

Boalch, G. T., Harbour, D. S. and Butler, E. I. (1978). Seasonal phytoplanktonproduction in the western English Channel 1964–1974. Journal of the MarineBiological Association of the United Kingdom 58, 943–953.

Brewer, P. G. and Riley, J. P. (1965). The automatic determination of nitrate inseawater. Deep Sea Research. 12, 765–772.

Browne, F. B. (1903). Report on the eggs and larvae of teleostean fishes observed atPlymouth in the Spring of 1902. Journal of the Marine Biological Association of theUnited Kingdom 6, 598–616.

Bryan, G. W. and Gibbs, P. E. (1991). Impact of low concentrations of tributyltin(TBT) on marine organisms: A review. In ‘‘Metal Ecotoxicology: Concepts andApplications’’ (M. C. Newman and A. W. Intosh, eds.), pp. 323–361. LewisPublishers, Ann Arbor, MI.

Bryan, G. W., Gibbs, P. E., Burt, G. R. and Hummerstone, L. G. (1987). The eVectsof tributyltin (TBT) accumulation on adult dog-whelks, Nucella lapillus: long-termfield and laboratory experiments. Journal of the Marine Biological Association ofthe United Kingdom 67, 525–544.

Bryan, G. W., Burt, G. R., Gibbs, P. E. and Pascoe, P. L. (1993). Nassariusreticulatus (Nassariidae; Gastropoda) as an indicator of tributyltin pollutionbefore and after TBT restrictions. Journal of the Marine Biological Association ofthe United Kingdom 73, 913–929.

Bullen, G. E. (1908). Plankton studies in relation to the western mackerel fishery.Journal of the Marine Biological Association of the United Kingdom 8, 269–302.

Burrows, M. T. (1988). The comparative biology of Chthamalus stellatus Poli andChthamalus montagui Southward. Ph.D. thesis, University of Manchester.

Burrows, M. T., Hawkins, S. J. and Southward, A. J. (1992). A comparison ofreproduction in co-occuring chthamalid barnacles, Chthamalus stellatus (Poli)


and Chthamalus montagui Southward. Journal of Experimental Marine Biology andEcology 160, 229–249.

Butler, E. I., Corner, E. D. S. and Marshall, S. M. (1969). On the nutrition andmetabolism of zooplankton. VI. Feeding eYciency of Calanus in terms of nitrogenand phosphorus. Journal of the Marine Biological Association of the UnitedKingdom 49, 977–1001.

Butler, E. I., Corner, E. D. S. and Marshall, S. M. (1970). On the nutrition andmetabolism of zooplankton. VII. Seasonal surveys of nitrogen and phosphorusexcretion by Calanus in the Clyde Sea area. Journal of the Marine BiologicalAssociation of the United Kingdom 50, 52–60.

Butler, E. I., Knox, S. and Liddicoat, M. I. (1979). The relationship between inor-ganic and organic nutrients in seawater. Journal of the Marine BiologicalAssociation of the United Kingdom 59, 239–250.

Bygrave, W. (1911). Report on the plankton of the English Channel in 1906. Report ofthe North Sea Fisheries Investigations Committee, Southern Area, 1906–1908, pp.235–238. His Majesties Stationery OYce, London.

Calderwood, W. L. (1891). The Plymouth mackerel fishery of 1889–90. From datacollected by Mr. Wm. Roach, associate member M.B.A. Journal of the MarineBiological Association of the United Kingdom 2 (NS), 4–14.

Carlisle, D. B. and Tregenza, N. (1961). A hermit crab new to Britain.Nature 190, 931.Carruthers, J. N. (1930). Further investigations upon water movement in the EnglishChannel. Drift bottle experiments in the summers of 1927, 1928 and 1930, withcritical notes. Journal of the Marine Biological Association of the United Kingdom17, 241–275.

Carruthers, J. N., Lawford, A. L. and Veley, V. F. C. (1950). Studies of watermovements at various light vessels in 1938, 1939 and 1940. I. At the Varne lightshipand her successors. Annales biologiques, Copenhague 6, 115–120.

Carruthers, J. N., Lawford, A. L., Veley, V. F. C. and Gruning, J. F. (1951). Studiesof water movements at various light vessels. II. At the Seven Stones light vesselnear the Scilly Isles. Journal of the Marine Biological Association of the UnitedKingdom 29, 587–608.

Clark, R. S. (1914). General report on the larval and post-larval teleosteans inPlymouth waters. Journal of the Marine Biological Association of the UnitedKingdom 10, 327–494.

Clark, R. S. (1920). The pelagic young and early bottom stages of teleosteans. Journalof the Marine Biological Association of the United Kingdom 12, 159–240.

Cleve, P. T. (1900). The plankton of theNorth Sea, English Channel, and the Skaggerakin 1899. Kungliga Svenska Vetenskapsakademiens Handlingar 32(8), 1–53.

Colebrook, J. M. (1960). Continuous Plankton Records: methods of analysis, 1950–1959. Bulletins of Marine Ecology 5, 51–64.

Colebrook, J. M. (1979). Continuous Plankton Records: Seasonal Cycles of Phyto-plankton and Copepods in the North Atlantic Ocean and the North Sea. MarineBiology 51, 23–32.

Conover, R. J. and Corner, E. D. S. (1968). Respiration and nitrogen excretion bysome marine zooplankton in relation to their life cycles. Journal of the MarineBiological Association of the United Kingdom 48, 49–75.

Continuous Plankton Recorder Survey Team (2004). Continuous Plankton Records:Plankton Atlas of the North Atlantic Ocean 1958–1999. II. Biogeographicalcharts. Marine Ecology Progress Series 2004(Suppl.), 11–75.

Coombs, S. H. (1975). Continuous plankton records show fluctuations in larval fishabundance during 1948–72. Nature 258, 134–136.


Coombs, S. H. (1980). Continuous Plankton Records: A plankton atlas of the NorthAtlantic and North Sea. Supplement 5—young fish, 1948–1972. Bulletin of MarineEcology B, 229–281.

Coombs, S. H. and Halliday, N. C. (2004). Occurrence of sardine eggs in the westernEnglish Channel from CPR sampling. First Progress Report SARDYN project,A4.3, 1–6p. Instituto de Investigacao Agraria e dos Pescas, Lisbon.

Cooper, G. A. and Forsyth, D. C. T. (1963). Continuous Plankton Records: Contri-bution towards a plankton atlas of the north Atlantic and the North Sea. Part VII:The seasonal and annual distributions of the pteropod Pneumodermopsiskeferstein. Bulletins of Marine Ecology 6, 31–38.

Cooper, L. H. N. (1932). The determination of nitrite in the sea by means of reducedstrychnine. Journal of the Marine Biological Association of the United Kingdom 18,161–166.

Cooper, L. H. N. (1937). On the ratio of nitrogen to phosphorus in the sea. Journal ofthe Marine Biological Association of the United Kingdom 22, 177–182.

Cooper, L. H. N. (1938a). Phosphate in the English Channel, 1933–1938, witha comparison with earlier years, 1916 and 1923–1932. Journal of the MarineBiological Association of the United Kingdom 23, 181–195.

Cooper, L. H. N. (1938b). Redefinition of the anomaly of the nitrate-phosphate ratio.Journal of the Marine Biological Association of the United Kingdom 23, 179.

Cooper, L. H. N. (1938c). Salt error in determinations of phosphate in sea water.Journal of the Marine Biological Association of the United Kingdom 23, 171–178.

Cooper, L. H. N. (1958a). Sea temperatures in Plymouth Sound. Journal of theMarine Biological Association of the United Kingdom 37, 1–3.

Cooper, L. H. N. (1958b). Consumption of nutrient salts in the English Channel as ameans of measuring production. Rapports et Proces-verbaux des Reunions. ConseilInternational pour l’Exploration de la Mer, Serie B, 144, 35–37.

Cooper, L. H. N. (1960). The water flow into the English Channel from the south-west. Journal of the Marine Biological Association of the United Kingdom 39,173–208.

Cooper, L. H. N. (1961). The oceanography of the Celtic Sea II. Conditions in thespring of 1950. Journal of the Marine Biological Association of the United Kingdom41, 235–270.

Corbin, P. G. (1947). The spawning of mackerel Scomber scombrus L., and pilchardClupea pilchardus Walbaum, in the Celtic Sea in 1937–39 with observations on thezooplankton indicator species Sagitta and Muggiaea. Journal of the MarineBiological Association of the United Kingdom 27, 65–129.

Corbin, P. G. (1948). On the seasonal abundance of young fish. IX. The year1947. Journal of the Marine Biological Association of the United Kingdom 27,718–722.

Corbin, P. G. (1949). The seasonal abundance of young fish. X. The year 1948.Journal of the Marine Biological Association of the United Kingdom 28,707–712.

Corbin, P. G. (1950). Records of pilchard spawning in the English Channel. Journalof the Marine Biological Association of the United Kingdom 29, 91–95.

Corner, E. D. S. (1961). On the nutrition and metabolism of zooplankton.I. Preliminary observations on the feeding of the marine copepod Calanus helgo-landicus (Claus). Journal of the Marine Biological Association of the UnitedKingdom 41, 5–16.

Corner, E. D. S. and Cowey, C. B. (1968). Biochemical studies on the production ofmarine zooplankton. Biological Reviews 43, 393–426.


Corner, E. D. S. and Davies, A. G. (1971). Plankton as a factor in the nitrogen andphosphorus cycles in the sea. Advances in Marine Biology 9, 101–204.

Corner, E. D. S. and Newell, B. S. (1967). On the nutrition and metabolism ofzooplankton. IV. The forms of nitrogen excreted by Calanus. Journal of the MarineBiological Association of the United Kingdom 47, 113–120.

Corner, E. D. S. and O’Hara, S. C. M. (eds.) (1986). The Biological Chemistry ofMarine Copepods. Clarendon Press, Oxford.

Corner, E. D. S., Cowey, C. B. and Marshall, S. M. (1965). On the feeding andmetabolism of zooplankton. III. Nitrogen excretion by Calanus. Journal of theMarine Biological Association of the United Kingdom 45, 429–442.

Corner, E. D. S., Cowey, C. B. and Marshall, S. M. (1967). On the nutrition andmetabolism of zooplankton. V. Feeding eYciency of Calanus finmarchicus. Journalof the Marine Biological Association of the United Kingdom 47, 259–270.

Corner, E. D. S., Head, R. N. and Kilvington, C. C. (1972). On the nutrition andmetabolism of zooplankton. VIII. The grazing of Biddulphia cells by Calanushelgolandicus. Journal of the Marine Biological Association of the United Kingdom52, 847–861.

Corner, E. D. S., Head, R. N. and Kilvington, C. C. (1974). On the nutrition andmetabolism of zooplankon. IX. Studies relating to the nutrition of overwinteringCalanus. Journal of the Marine Biological Association of the United Kingdom 54,319–331.

Corner, E. D. S., Head, R. N., Kilvington, C. C. and Pennycuick, L. (1976). On thenutrition and metabolism of zooplankton. X. Quantitative aspects of Calanushelgolandicus feeding as a carnivore. Journal of the Marine Biological Associationof the United Kingdom 56, 345–358.

Cowey, C. B. and Corner, E. D. S. (1962). The amino acid composition of Calanusfinmarchicus (Claus) in relation to that of its food. Rapports et Proces-Verbaux duConseil International pour L’Exploration de la Mer 153, 124–128.

Cowey, C. B. and Corner, E. D. S. (1963a). On the nutrition and metabolism ofzooplankton. II. The relationship between the marine copepod Calanus helgolan-dicus and particulate material in Plymouth sea water, in terms of amino acidcomposition. Journal of the Marine Biological Association of the United Kingdom43, 495–511.

Cowey, C. B. and Corner, E. D. S. (1963b). Amino acids and some other nitrogenouscompounds in Calanus finmarchicus. Journal of the Marine Biological Associationof the United Kingdom 43, 485–493.

Crawshay, L. R. (1912). On the fauna of the outer western area of the EnglishChannel. Journal of the Marine Biological Association of the United Kingdom 9,292–393.

Crisp, D. J. (1964). The eVects of the severe winter of 1962–63 on marine life inBritain. Journal of Animal Ecology 33, 179–210.

Crisp, D. J. and Southward, A. J. (1958). The distribution of intertidal organismsalong the coasts of the English Channel. Journal of the Marine BiologicalAssociation of the United Kingdom 37, 157–208.

Cunningham, J. T. (1892a). On a species of siphonophore observed at Plymouth.Journal of the Marine Biological Association of the United Kingdom 2, 212–215.

Cunningham, J. T. (1892b). Ichthyological contributions. Journal of the MarineBiological Association of the United Kingdom 2, 325–330.

Cunningham, J. T. (1892c). On some larval stages of fishes. Journal of the MarineBiological Association of the United Kingdom 11, 68–74.


Cunningham, J. T. (1892d). The rates of growth of some sea fishes, and theirdistribution at diVerent ages. Journal of the Marine Biological Association of theUnited Kingdom 11, 95–118.

Cunningham, J. T. (1892e). The reproduction and growth of pilchard. Journal of theMarine Biological Association of the United Kingdom 11, 151–157.

Cunningham, J. T. (1892f ). On the rate of growth of some sea fishes, and the age andsize at which they begin to breed. Journal of the Marine Biological Association ofthe United Kingdom 11, 222–264.

Cushing, D. H. (1961). On the failure of the Plymouth Herring Fishery. Journal of theMarine Biological Association of the United Kingdom 41, 799–816.

Cushing, D. H. and Dickson, R. R. (1976). The biological response in the sea toclimatic changes. Advances in Marine Biology 14, 1–122.

Digby, P. S. B. (1950). The biology of the small planktonic copepods of Plymouth.Journal of the Marine Biological Association of the United Kingdom 29, 393–438.

Duarte, C. M., Cebrian, J. and Marba, N. (1992). Uncertainty of detecting seachange. Nature 356, 190.

Edwards, M. (2000). Temporal and spatial patterns of marine phytoplankton. Ph.D.Thesis, University of Plymouth.

Edwards, M. and Richardson, A. J. (2004). Impact of climate change on marinepelogic phenology and trophic mismatch. Nature 430, 881–884.

Edwards, M., John, A. W. G., Johns, D. G. and Reid, P. C. (2001). Case history andpersistence of the non-indigenous diatom Coscinodiscus wailesii in the north-eastAtlantic. Journal of the Marine Biological Association of the United Kingdom 81,207–211.

Evans, S. M., Hutton, A., Kendall, M. A. and Samosir, A. M. (1991). Recovery inpopulations of dogwhelks Nucella lapillus (L.) suVering from imposex. MarinePollution Bulletin 22, 331–333.

Fischer-Piette, E. (1936). Etudes sur la biogeographie intercotidale des deux rives dela Manche. Journal of the Linnean Society, Zoology 60, 181–272.

Ford, E. (1923). Animal communities of the level sea-bottom in the waters adjacentto Plymouth.

Ford, E. (1933). An account of the herring investigations conducted at Plymouthduring the years from 1924 to 1933. Journal of the Marine Biological Association ofthe United Kingdom 19, 305–384.

Franklin, A., Pickett, G. D., Holme, N. A. and Barrett, R. L. (1980). Surveyingstocks of scallops (Pecten maximus) and queens (Chlamys opercularis) with under-water television. Journal of the Marine Biological Association of the UnitedKingdom 60, 181–191.

Garcia-Soto, C. and Pingree, R. D. (1998). Late autumn distribution and seasonalityof chlorophyll-a at the shelf-break/slope region of the Armorican and Celtic Shelf.Journal of the Marine Biological Association of the United Kingdom 78, 17–33.

Garcia-Soto, C., Fernandez, E., Pingree, R. D. and Harbour, D. S. (1995). Evolutionand structure of a shelf coccolithophore bloom in the western English Channel.Journal of Plankton Research 17, 2011–2036.

Garcia-Soto, C., Pingree, R. D. and Valdes, L. (2002). Navidad development in thesouthern Bay of Biscay: Climate change and swoddy structure from remote sensingand in situ measurements. Journal of Geophysical Research C8, [np] 15 August2002.

Garstang, W. (1898). On the variations, races and migrations of the mackerel.Journal of the Marine Biological Association of the United Kingdom 5, 235–295.


Garstang, W. (1903). Report on trawling and other investigations carried out in thebays on the South–East Coast of Devon during 1901–1902. Journal of the MarineBiological Association of the United Kingdom 6, 436–527.

Gatten, R. R., Corner, E. D. S., Kilvington, C. C. and Sargent, J. R. (1979).A seasonal survey of the lipids in Calanus helgolandicus (Claus) from the EnglishChannel. In ‘‘Cyclic phenomena in marine plants and animals’’ (E. Naylor andR. G. Hartnoll, eds.), pp. 275–284. Pergamon Press, Oxford.

Gatten, R. R., Sargent, J. R., Forsberg, T. E. V., O’Hara, S. C. M. and Corner,E. D. S. (1980). On the nutrition and metabolism of zooplankton. XIII. Utilisationof lipid by Calanus helgolandicus during maturation and reproduction. Journal ofthe Marine Biological Association of the United Kingdom 60, 391–399.

Genner, M. J., Kendall, M. and Sims, D. W. (2001). Archiving and analysis of theMBA bottom trawl and benthic survey data: Unravelling fishing eVorts fromclimate change. Report to theMinistry of Agriculture, Fisheries and Food, London.

Genner, M. J., Sims, D. W., Wearmouth, V. J., Southall, E. J., Southward, A. J.,Henderson, P. A. and Hawkins, S. J. (2004). Regional climate warming driveslong-term community changes of British marine fish. Proceedings of the RoyalSociety of London B 271, 655–661.

Gibbs, P. E., Bryan, G. W., Pascoe, P. L. and Burt, G. R. (1987). The use of the dog-whelk, Nucella lapillus, as an indicator of tributyltin (TBT) contamination. Journalof the Marine Biological Association of the United Kingdom 67, 507–523.

Gibbs, P. E., Bryan, G. W. and Spence, S. (1991). The impact of tributyltin (TBT)pollution on the Nucella lapillus (Gastropoda) populations around the coast ofsouth-east England. Oceanologica Acta, special issue 11, 257–261.

Gough, L. H. (1905). Report on the plankton of the English Channel in 1903. Reportof the North Sea Fisheries Investigations Committee, Southern Area, 1902–1903, pp.325–377. His Majesties Stationery OYce, London.

Gough, L. H. (1907). Report on the plankton of the English Channel in 1904–1905.Report of the North Sea Fisheries Investigations Committee, Southern Area, 1904–1905, pp. 165–268. His Majesties Stationery OYce, London.

Gran, H. H. (1912). Pelagic plant life. In ‘‘The Depths of the Ocean’’ (J. Murray andJ. Hjort, eds.), pp. 307–386. Macmillan, London.

GrasshoV, K. (1976). ‘‘Methods of Seawater Analysis,’’. Verlag Chemie, Weinheim/New York.

Green, E. P., Harris, R. P. and Duncan, A. (1993). The seasonal abundance of thecopepodite stages of Calanus helgolandicus and Pseudocalanus elongatus oV Ply-mouth. Journal of the Marine Biological Association of the United Kingdom 73,109–122.

Guisande, C. and Harris, R. (1995). EVect of total organic content of eggs onhatching success and naupliar survival in the copepod Calanus helgolandicus.Limnology and Oceanography 40, 476–482.

Hardy, A. C. (1936). The continuous plankton recorder. Discovery Reports 11,454–570.

Hardy, A. C. (1939). Ecological investigations with the continuous planktonrecorder: Object, plan and methods. Bulletins of Marine Ecology 1, 1–57.

Hartley, B. (1986). A check-list of the freshwater, brackish and marine diatoms ofthe British Isles and adjacent coastal waters. Journal of the Marine BiologicalAssociation of the United Kingdom 66, 531–610.

Harvey, H. W. (1923). Hydrographic features of the water in the neighbourhood ofPlymouth during the years 1921 and 1922. Journal of the Marine BiologicalAssociation of the United Kingdom 13, 225–235.


Harvey, H. W. (1925). Water movement and sea temperature in the EnglishChannel. Journal of the Marine Biological Association of the United Kingdom13, 659–664.

Harvey, H. W. (1926). Nitrate in the sea. Journal of the Marine Biological Associationof the United Kingdom 14, 71–88.

Harvey, H. W. (1927). ‘‘Biological Chemistry and Physics of Sea Water’’. CambridgeUniversity Press, London.

Harvey, H. W. (1929). Hydrodynamics of the waters south-east of Ireland. Journal duConsiel permanent International pour l’Exploration de la Mer. 4, 80–92.

Harvey, H. W. (1934a). Measurement of phytoplankton population. Journal of theMarine Biological Association of the United Kingdom 19, 761–773.

Harvey, H. W. (1934b). Annual variation of planktonic vegetation, 1933. Journal ofthe Marine Biological Association of the United Kingdom 19, 775–792.

Harvey, H. W. (1948). The estimation of phosphate and of total phosphorus in seawaters. Journal of the Marine Biological Association of the United Kingdom 27,337–359.

Harvey, H. W. (1955). The Chemistry and Fertility of Sea Waters. University Press,Cambridge.

Harvey, H. W., Cooper, L. H. N., Lebour, M. V. and Russell, F. S. (1935). Planktonproduction and its control. Journal of the Marine Biological Association of theUnited Kingdom 20, 407–441.

Hawkins, S. J. and Southward, A. J. (1992). The Torrey Canyon oil spill: Recoveryof rocky shore communities. In ‘‘Restoring the nation’s marine environment’’(G. W. Thayer, ed.), pp. 583–631. Maryland Sea Grant College, College Park,Maryland.

Hawkins, S. J., Southward, A. J. and Barrett, R. L. (1983). Population structureof Patella vulgata L. during succession on rocky shores in southwest England.Oceanologia Acta, 1983 suppl. 103–107.

Hawkins, S. J., Gibbs, P. E., Pope, N. D., Burt, G. R., Chesman, B. S., Bray, S.,Proud, S. V., Spence, S. K., Southward, A. J. and Langston, W. J. (2002). Recov-ery of polluted ecosystems: The case for long-term studies. Marine EnvironmentalResearch 54, 215–222.

Hawkins, S. J., Southward, A. J. and Genner, M. J. (2003). Detection of environ-mental change in a marine ecosystem—evidence from the western English Chan-nel. Science of the Total Environment 310, 245–256.

HeVord, A. E. (1910). Notes on teleostean ova and larvae observed at Plymouth inspring and summer 1909. Journal of the Marine Biological Association of the UnitedKingdom 9, 1–58.

Henderson, G. T. D. (1961). Continuous Plankton Records: Contribution towards aplankton atlas of the north-eastern Atlantic and the North Sea. Part V: Young fish.Bulletins of Marine Ecology 5, 105–111.

Herbert, R. J. H., Hawkins, S. J., Sheader, M. and Southward, A. J. (2003). Rangeextension and reproduction of the barnacle Balanus perforatus in the easternEnglish Channel. Journal of the Marine Biological Association of the UnitedKingdom 83, 73–82.

Holligan, P. M. and Harbour, D. S. (1977). The vertical distribution and successionof phytoplankton in the western English Channel in 1975 and 1976. Journal of theMarine Biological Association of the United Kingdom 57, 1075–1093.

Holligan, P. M., Maddock, L. and Dodge, J. D. (1980). The distribution of dinofla-gellates around the British Isles in July 1977: A multivariate analysis. Journal of theMarine Biological Association of the United Kingdom 60, 851–867.


Holligan, P. M., Viollier, M., Dupouy, C. and Aiken, J. (1983). Satellite studies onthe distributions of chlorophyll and dinoflagellate blooms in the western EnglishChannel. Continental Shelf Research 2, 81–96.

Holme, N. A. (1953). The biomass of the bottom fauna in the English Channel oVPlymouth. Journal of the Marine Biological Association of the United Kingdom 32,1–49.

Holme, N. A. (1961). The bottom fauna of the English Channel. Journal of theMarine Biological Association of the United Kingdom 41, 397–461.

Holme, N. A. (1966a). The bottom fauna of the English Channel. Part II. Journal ofthe Marine Biological Association of the United Kingdom 46, 401–493.

Holme, N. A. (1966b). Distribution of molluscs in the English Channel. Abstract.Malacologia 5, 53.

Holme, N. A. (1974). The biology of Loligo forbesi Steenstrup (Mollusca: Cephalo-poda) in the Plymouth area. Journal of the Marine Biological Association of theUnited Kingdom 54, 481–503.

Holme, N. A. (1983). Fluctuations in the benthos of the western English Channel.Proceedings of the 17th European Marine Biology Symposium Oceanologia Acta1983 suppl. 121–124.

Holme, N. A. (1984). Fluctuations of Ophiothrix fragilis in the western EnglishChannel. Journal of the Marine Biological Association of the United Kingdom 64,351–378.

Holt, W. L. and Scott, S. D. (1898). A record of the teleostean eggs and larvaeobserved at Plymouth in 1897. Journal of the Marine Biological Association of theUnited Kingdom 5, 156–177.

Hunt, H. G. (1968). Continuous Plankton Records: Contribution towards a planktonatlas of the north Atlantic and the North Sea. Part XI: The seasonal and annualdistributions of Thaliacea. Bulletin of Marine Ecology 6, 225–249.

International Council for the Exploration of the Sea (2003). Report of the WorkingGroup on Zooplankton Ecology. ICES, Gijon, Spain, February, 2003. CouncilMeeting paper 2003/C:01.

Irigoien, X. and Harris, R. P. (2003). Interannual variability of Calanus helgolandicusin the English Channel. Fisheries Oceanography 12, 317–326.

Irigoien, X., Harris, R. P., Head, R. N. and Harbour, D. (2000a). North Atlanticoscillation and spring bloom phytoplankton composition in the English Channel.Journal of Plankton Research 22, 2367–2371.

Irigoien, X., Head, R. N., Harris, R. P., Cummings, D., Harbour, D. and Meyer-Harms, B. (2000b). Feeding selectivity and egg production of Calanus helgolandi-cus in the English Channel. Limnology and Oceanography 45, 44–54.

Irigoien, X., Harris, R. P., Verheye, H. M., Joly, P., Runge, J., Starr, M., Pond,D., Campbell, R., Shreeve, R., Ward, P., Smith, A. N., Dam, H. G., Peterson,W., Tirelli, V., Koski, M., Smith, T., Harbour, D. and Davidson, R. (2002).Copepod hatching success in marine ecosystems with high diatom concentra-tions. Nature 419, 387–389.

John, E. H., Batten, S. D., Harris, R. P. and Hays, G. C. (2001). Comparisonbetween zooplankton data collected by the Continuous Plankton Recorder surveyin the English Channel and by WP-2 nets at station L4, Plymouth (UK). Journal ofSea Research 46, 223–232.

Joint, I., Jordan, M. B. and Carr, M. R. (1997). Is phosphate part of the Russellcycle? Journal of the Marine Biological Association of the United Kingdom 77,625–633.


Jordan, M. B. and Joint, I. (1998). Seasonal variation in nitrate:phosphate ratiosin the English Channel 1923–1987. Estuarine, Coastal and Shelf Science 46,157–164.

Kaiser, M. J. and Spence, F. E. (2002). Inconsistent temporal changes in the mega-benthos of the English Channel. Marine Biology 141, 321–331.

Kaiser, M. J., Armstrong, P. J., Dare, P. J. and Flatt, R. P. (1998). Benthiccommunities associated with a heavily-fished scallop ground in the EnglishChannel. Journal of the Marine Biological Association of the United Kingdom78, 1045–1059.

Kemp, S. (1938). Oceanography and the fluctuations in the abundance of marineanimals. Nature 142, 777–779, 817–820.

Kirkwood, D. S. (1989). Simultaneous determination of selected nutrients in seawater. International Council for the Exploration of the Sea, Council MeetingPaper, CM 1989/C : 29.

Laabir, M., Poulet, S. A., Harris, R. P., Pond, D. W., CueV, A., Head, R. N. andIanora, A. M. (1998). Comparative study of the reproduction of Calanus helgo-landicus in well-mixed and seasonally stratified coastal waters of the westernEnglish Channel. Journal of Plankton Research 20, 407–421.

Langstone, W. J., Bryan, G. W., Burt, G. R. and Gibbs, P. E. (1990). Assessingthe impact of tin and TBT in estuaries and coastal regions. Functional Ecology 4,433–443.

Lankester, E. R., Herdman, W. A., Dickson, H. N. and Garstang, W. (1900). A firstreport of the committee appointed to make periodic investigations of the planktonand physical conditions of the English Channel during 1899. Report of the BritishAssociation for the Advancement of Science 69, 444–446.

Lebour, M. V. (1917). The microplankton of Plymouth Sound from the regionbeyond the breakwater. Journal of the Marine Biological Association of the UnitedKingdom 11, 133–182.

Lebour, M. V. (1919). Feeding habits of some young fish. Journal of the MarineBiological Association of the United Kingdom 12, 9–21.

Lebour, M. V. (1920). The food of young fish. No. 3. 1919. Journal of the MarineBiological Association of the United Kingdom 12, 261–324.

Lebour, M. V. (1921). The larval and post-larval stages of the Pilchard, Sprat andHerring from Plymouth district. Journal of the Marine Biological Association of theUnited Kingdom 12, 427–457.

Le Fevre, J. (1986). Aspects of the biology of frontal systems. Advances in MarineBiology 23, 163–299.

Lindley, J. A. (1975). Continuous Plankton Records: A plankton atlas of the northAtlantic and the North Sea. Supplement 3–Tintinnida (Protozoa, Ciliophora) in1965. Bulletin of Marine Ecology 8, 201–213.

Lindley, J. A. (1987). Continuous Plankton Records: The geographical distributionand seasonal cycles of decapod crustacean larvae and pelagic post-larvae in thenorth-eastern Atlantic Ocean and the North Sea, 1981–3. Journal of the MarineBiological Association of the United Kingdom 67, 145–167.

Lohmann, H. (1911). Uber das Nannoplankton und die Zentrifugierung. Inter-national Revue der gesampten Hydrobiology und Hydrographie 4, 1–38.

Lopez-Urrutia, A., Harris, R., Acuna, J. L., Bamstedt, U., Flood, P. R., Fyhn, H. J.,Gorsky, G., Irigoien, X. and Martinussen, M. (2004). A comparison of appendi-cularian seasonal cycles in four contrasting European coastal environments.Limnology & Oceanography 49, 303–307.


Maddock, L. and Swann, C. L. (1977). A statistical analysis of some trends in seatemperature and climate in the Plymouth area in the last 70 years. Journal of theMarine Biological Association of the United Kingdom 57, 317–338.

Maddock, L., Boalch, G. T. and Harbour, D. S. (1981). Populations of phytoplank-ton in the western English Channel between 1964 and 1974. Journal of the MarineBiological Association of the United Kingdom 61, 565–583.

Maddock, L., Harbour, D. S. and Boalch, G. T. (1989). Seasonal and year-to-yearchanges in the phytoplankton from the Plymouth area, 1963–1986. Journal of theMarine Biological Association of the United Kingdom 69, 229–244.

Mantoura, R. F. C. and Woodward, E. M. S. (1983). Optimization of the indophenolblue method for the automated determination of ammonia in estuarine waters.Estuarine, Coastal and Shelf Science 17, 219–224.

Mare, M. F. (1940). Plankton production oV Plymouth and the mouth of the EnglishChannel in 1939. Journal of the Marine Biological Association of the UnitedKingdom 24, 461–482.

Mare, M. F. (1942). A study of a marine benthic community with special reference tothe microorganisms. Journal of the Marine Biological Association of the UnitedKingdom 25, 517–554.

Marine Biological Association (1952). Council Report for 1949–50. Journal of theMarine Biological Association of the United Kingdom 29, 526.

Marshall, N. B. (1948). Continuous plankton records: zooplankton (other thanCopepoda and young fish) in the North Sea 1938–1939. Hull Bulletins of MarineEcology 2, 173–213.

Matthews, D. J. (1905). Report on the physical conditions in the English channel,1902–1903. Report of the North Sea Fisheries Investigations Committee, SouthernArea, 1902–1903, pp. 289–324. His Majesties Stationery OYce, London.

Matthews, D. J. (1906). Report on the physical conditions in the English Channeland adjacent waters in 1906, with a note on the mean conditions for 1903–1909.Report of the North Sea Fisheries Investigations Committee, Southern Area, 1904–1905, pp. 269–282. His Majesties Stationery OYce, London.

Matthews, D. J. (1911). Report on the physical conditions in the English channeland adjacent waters, 1906. Report of the North Sea Fisheries Investigations Com-mittee, Southern Area, 1906–1908, pp. 269–282. His Majesties Stationery OYce,London.

Matthews, D. J. (1914). The salinity and temperature of the Irish Channel and thewaters south of Ireland. Scientific Investigations of the Fisheries Branch, Ireland1913, no. 4. His Majesties Stationery OYce, London.

Matthews, D. J. (1917a). On the amount of phosphoric acid in the sea water oVPlymouth Sound I. Journal of the Marine Biological Association of the UnitedKingdom 11, 122–130.

Matthews, D. J. (1917b). On the amount of phosphoric acid in the sea water oVPlymouth Sound II. Journal of the Marine Biological Association of the UnitedKingdom 11, 251–257.

McHardy, R. A. (1970). Distribution and abundance of hyperiid amphipodsin near-surface waters of the north Atlantic Ocean and North Sea. Ph.D. Thesis.University of Edinburgh.

Mills, E. L. (1989). Biological Oceanography. An Early History, 1870–1960. CornellUniversity Press, Ithaca, NY.

Mills, E. L. (1990). The ocean regarded as a pasture: Kiel, Plymouth and the explan-ation of the marine plankton cycle, 1887 to 1935. Deutsche HydrographischeZeitschrift 1990 (22B), 20–29.


Mills, E. L. (2001). Problem children of analytical chemistry. Elucidating the seasonalcycle of plankton production through nutrient analysis. In ‘‘Understanding theOceans’’ (M. Deacon, T. Rice and C. Summerhayes, eds.), pp. 228–250. UniversityCollege Press, London.

Moore, G. F., Aiken, J. and Lavender, S. J. (1999). The atmospheric correction ofwater colour and the quantitative retrieval of suspended particulate matter inCase II waters: Application to MERIS. International Journal of Remote Sensing20, 1713–1733.

Moore, H. B. (1936). The biology of Balanus balanoides. V Distribution in thePlymouth area. Journal of the Marine Biological Association of the United Kingdom20, 701–716.

Moore, H. B. and Kitching, J. A. (1939). The biology of Chthamalus stellatus (Poli).Journal of the Marine Biological Association of the United Kingdom 23, 521–541.

Murphy, J. and Riley, J. P. (1962). Modified single solution method for thedetermination of phosphate in natural waters. Analytica Chimica Acta 27, 31–36.

Neal, A. C., Prahl, F. G., Eglinton, G., O’Hara, S. C. M. and Corner, E. D. S. (1986).Lipid changes during a plantonic feeding sequence involving unicellular algae,Elminius nauplii and adult Calanus. Journal of the Marine Biological Associationof the United Kingdom 66, 1–13.

O’Hara, S. C. M., Corner, E. D. S. and Kilvington, C. C. (1978). On the nutritionand metabolism of zooplankton. XII. Measurements by radioimmunoassay of thelevels of a steroid in Calanus. Journal of the Marine Biological Association of theUnited Kingdom 58, 597–605.

O’Hara, S. C. M., Gaskell, S. J. and Corner, E. D. S. (1979). On the nutrition andmetabolism of zooplankton. XIII. Further studies of steroids in Calanus. Journal ofthe Marine Biological Association of the United Kingdom 59, 333–340.

O’Reilly, J. E., Maritorena, S., Mitchell, B. G., Siegel, D. A., Carder, K. L., Garver,M. K. and McClain, C. (1998). Ocean colour algorithms for SeaWiFS. Journal ofGeophysical Research 103, 24937–24953.

Orton, J. H. (1916). An account of researches on races of herrings carried out by theMarine Biological Association at Plymouth, 1914–1915. Journal of the MarineBiological Association of the United Kingdom 11, 71–121.

Pannacciulli, F. G. (1995). Population Ecology and Genetics of European Species ofIntertidal Barnacles. Ph.D. Thesis, University of Liverpool.

Parke, M. (1948). Laminaria ochroleuca de la Pylaie growing on the coast of Britain.Nature 162, 295–296.

Parke, M. (1952). Flora of Devon. Volume II. Part I. The Marine Algae. TheDevonshire Association, Devonshire Press, Torquay.

Pingree, R. D. (1974). The turbulent boundary layer on the continental shelf. Nature250, 720–722.

Pingree, R. D. (1975). The advance and retreat of the thermocline on the continentalshelf. Journal of the Marine Biological Association of the United Kingdom 55,965–974.

Pingree, R. D. (1978). Mixing and stabilization of phytoplankton distributions onthe northwest European continental shelf. In ‘‘Spatial Patterns in Plankton Com-munities. Proceedings of the NATO Conference on Marine Biology, Held at Erice,Italy, 13–21 November 1977’’ (J. H. Steele, ed.), pp. 181–220. Plenum, New York.

Pingree, R. D. (1980). Physical oceanography of the Celtic Sea and the EnglishChannel. In ‘‘The Northwest European Shelf Seas: The Sea-bed and the Sea inMotion’’ (F. T. Banner, B. Collins and K. S. Massie, eds.), pp. 415–465. Elsevier,Amsterdam.


Pingree, R. D. (2002). Ocean structure and climate (Eastern North Atlantic): in situmeasurement and remote sensing (altimeter). Journal of the Marine BiologicalAssociation of the United Kingdom 82, 681–707.

Pingree, R. D. and GriYths, D. K. (1977). The bottom mixed layer on the continentalshelf. Estuarine, Coastal and Shelf Science 5, 399–413.

Pingree, R. D. and GriYths, D. K. (1978). Tidal fronts on the shelf seas around theBritish Isles. Journal of Geophysical Research, Oceans and Atmospheres 83,4615–4622.

Pingree, R. D. and GriYths, D. K. (1980). Currents driven by a steady uniform windstress on the shelf seas around the British Isles. Oceanologia Acta 3, 227–236.

Pingree, R. D. and Le Cann, B. (1989). Celtic and Armorican slope and shelf residualcurrents. Progress in Oceanography 23, 303–338.

Pingree, R. D. and Maddock, L. (1985). Rotary currents and residual circulationaround banks and islands. Deep Sea Research 32, 929–947.

Pingree, R. D. and Mardell, G. T. (1986). Coastal tidal jets and tidal fringedevelopment around the Isles of Scilly. Estuarine, Coastal and Shelf Science 23,581–594.

Pingree, R. D. and Pennycuick, L. (1975). Transfer of heat, fresh water and nutrientsthrough the seasonal thermocline. Journal of the Marine Biological Association ofthe United Kingdom 55, 261–274.

Pingree, R. D., Pugh, P. R., Holligan, P. M. and Forster, G. R. (1975). Summerphytoplankton blooms and red tides along tidal fronts in the approaches to theEnglish Channel. Nature 258, 672–677.

Pingree, R. D., Holligan, P. M., Mardell, G. T. and Head, R. N. (1976). The influenceof physical stability on spring, summer and autumn phytoplankton blooms in theCeltic Sea. Journal of the Marine Biological Association of the United Kingdom 56,845–873.

Pingree, R. D., Maddock, L. and Butler, E. I. (1977a). The influence of biologicalactivity and physical stability in determining the chemical distributions of inor-ganic phosphate, silicate and nitrate. Journal of the Marine Biological Associationof the United Kingdom 57, 1065–1073.

Pingree, R. D., Holligan, P. M. and Head, R. N. (1977b). Survival of dinoflagellateblooms in the western English Channel. Nature 265, 266–268.

Pingree, R. D., Holligan, P. M. and Mardell, G. T. (1978). The eVects of verticalstability on phytoplankton distributions in the summer on the northwest Europeanshelf. Deep-Sea Research 25, 1011–1028.

Pingree, R. D., Holligan, P. M. and Mardell, G. T. (1979). Phytoplankton growthand cyclonic eddies. Nature 278, 245–247.

Pingree, R. D., Mardell, G. T., Holligan, P. M., GriYths, D. K. and Smithers, J.(1982). Celtic Sea and Armorican current structure and the vertical distributions oftemperature and chlorophyll. Continental Shelf Research 1, 99–116.

Pingree, R. D., Sinha, B. and GriYths, C. R. (1999). Seasonality of the Europeanslope current (Goban Spur) and ocean margin exchange. Continental ShelfResearch 19, 929–975.

Pinkerton, M. H. and Aiken, J. (1999). Calibration and validation of remotely-sensedobservations of ocean colour from a moored databuoy. Journal of Atmospheric andOceanographic Technology 16, 915–923.

Pinkerton, M. H., Lavender, S. and Aiken, J. (2003). Validation of SeaWiFS oceancolour satellite data using a moored databuoy. Journal of Geophysical Research108, C5.


Planque, B. and Fromentin, J.-M. (1996). Calanus and environment in theeastern North Atlantic. I. Spatial and temporal patterns of C. finmarchicus andC. helgolandicus. Marine Ecology Progress Series 134, 101–109.

Pond, D., Harris, R., Head, R. and Harbour, D. (1996). Environmental and nutri-tional factors determining seasonal variability in the fecundity and egg viability ofCalanus helgolandicus in coastal waters oV Plymouth, UK. Marine EcologyProgress Series 143, 45–63.

Prahl, F. G., Eglinton, G., Corner, E. D. S. and O’Hara, S. C. M. (1984a). Copepodfecal pellets as a source of dihydrophytol in marine sediments. Science 224,1235–1237.

Prahl, F. G., Eglinton, G., Corner, E. D. S., O’Hara, S. C. M. and Forsberg, T. E. V.(1984b). Changes in plant lipids during passage through the gut of Calanus. Journalof the Marine Biological Association of the United Kingdom 64, 317–334.

Prahl, F. G., Eglinton, G., Corner, E. D. S. and O’Hara, S. C. M. (1985). Faecallipids released by fish feeding on zooplankton. Journal of the Marine BiologicalAssociation of the United Kingdom 65, 547–560.

Redfield, A. C., Ketchup, B. H. and Richards, F. A. (1963). The influence oforganisms on the composition of seawater. In ‘‘The Sea’’ (M. N. Hill, E. D.Goldberg, C. O. D. Iselin and W. H. Munk, eds.), pp. 26–77. Wiley Interscience,London.

Rees, C. B. (1954a). Continuous Plankton Records: The distribution of echino-derm and other larvae in the North Sea, 1947–1951. Bulletin of Marine Ecology4, 47–67.

Rees, C. B. (1954b). Continuous Plankton Records: The distribution of lamelli-branch larvae in the North Sea, 1950–1951. Bulletin of Marine Ecology 4, 21–46.

Rees, W. J. and Lumby, J. R. (1954). The abundance of Octopus in the EnglishChannel. Journal of the Marine Biological Association of the United Kingdom 33,515–536.

Reid, P. C. (1978). Dinoflagellate cysts in the plankton. New Phytologist 80, 219–229.Reid, P. C., Robinson, G. A. and Hunt, H. G. (1987). Spatial and temporal patternsof marine blooms in the northeastern Atlantic and North Sea from the ContinuousPlankton Recorder survey. Rapports et Proces-verbaux des Reunions. CommissionInternationale pour l’Exploration de la Mer. 187, 27–37.

Reid, P. C., Borges, M. F. and Svendsen, E. (2001). A regime shift in the North Seacirca 1988 linked to changes in the North Sea horse mackerel fishery. FisheriesResearch 50, 163–171.

Reid, P. C., Colebrook, J. M., Matthews, J. B. L. and Aiken, J. The ContinuousPlankton Recorder Survey Team (2003). The Continuous Plankton Recorder:Concepts and history, from Plankton Indicators to undulating recorders. Progressin Oceanography 58, 117–173.

Richardson, A. J. and Schoeman, D. S. (2004). Climate impact on plankton ecosys-tems in the northeast Atlantic. Science 305, 1609–1612.

Ridge, R. J. (1889). The mackerel fishery in the West of England. Journal of theMarine Biological Association of the United Kingdom 1 (NS), 72–73.

Robinson, G. A. (1985). Continuous plankton records; plankton, climate andfisheries of the western English Channel. ICES Council Meeting Papers, CM1985/L : 41.

Robinson, G. A. and Hunt, H. G. (1986). Continuous plankton records: Annualfluctuations of the plankton in the western English Channel, 1958–83. Journal ofthe Marine Biological Association of the United Kingdom 66, 791–802.


Robinson, G. A., Aiken, J. and Hunt, H. G. (1986). Synoptic surveys of thewestern English Channel. The relationships between plankton and hydrog-raphy. Journal of the Marine Biological Association of the United Kingdom66, 201–218.

Rodriguez, F., Fernandez, E., Head, R. N., Harbour, D. S., Bratbak, G., Heldal, M.and Harris, R. P. (2000). Temporal variability of viruses, bacteria, phytoplanktonand zooplankton in the western English Channel oV Plymouth. Journal of theMarine Biological Association of the United Kingdom 80, 575–586.

Roskell, J. (1975). Continuous Plankton Records: A plankton atlas of the NorthAtlantic and North Sea. Supplement 2—the oceanic cirripede larvae, 1955–1972.Bulletin of Marine Ecology 8, 185–199.

Rozwadowski, H. M. (2003). The Sea Knows No Boundaries. A Century of MarineScience Under ICES. International Council for the Exploration of the Sea inAssociation with the University of Washington Press, Seattle.

Russell, F. S. (1925). The vertical distribution of marine macroplankton. An obser-vation on diurnal changes. Journal of the Marine Biological Association of theUnited Kingdom 13, 769–809.

Russell, F. S. (1926a). The vertical distribution of marine macroplankton II. Thepelagic young of teleostean fishes in the daytime in the Plymouth area, with a noteon the eggs of certain species. Journal of the Marine Biological Association of theUnited Kingdom 14, 101–160.

Russell, F. S. (1926b). The vertical distribution of marine macroplankton III. Diurnalobservations on the pelagic young of teleostean fishes in the Plymouth area. Journal ofthe Marine Biological Association of the United Kingdom 14, 387–414.

Russell, F. S. (1926c). The vertical distribution of marine macroplankton IV. Theapparent importance of light intensity as a controlling factor in the behaviour ofcertain species in the Plymouth area. Journal of the Marine Biological Associationof the United Kingdom 14, 415–440.

Russell, F. S. (1927a). The vertical distribution of marine macroplankton V. The distri-bution of animals caught in the ring-trawl in the daytime in the Plymouth area.Journal of the Marine Biological Association of the United Kingdom 14, 557–608.

Russell, F. S. (1927b). The vertical distribution of plankton in the sea. BiologicalReviews 11, 213–262.

Russell, F. S. (1928a). The vertical distribution of marine macroplankton VI. Furtherobservations on diurnal changes. Journal of the Marine Biological Association ofthe United Kingdom 15, 81–103.

Russell, F. S. (1928b). The vertical distribution of marine macroplankton VII.Observations on Calanus finmarchicus. Journal of the Marine Biological Associationof the United Kingdom 15, 429–454.

Russell, F. S. (1928c). The vertical distribution of marine macroplankton VIII.Further observations on the diurnal behaviour of the pelagic young of teleosteanfishes in the Plymouth area. Journal of the Marine Biological Association of theUnited Kingdom 15, 829–850.

Russell, F. S. (1930a). The vertical distribution of marine macroplankton IX.The distribution of the pelagic young of teleostean fishes in the daytime in thePlymouth area. Journal of the Marine Biological Association of the United Kingdom16, 639–676.

Russell, F. S. (1930b). The seasonal abundance and distribution of the pelagic youngof teleostean fishes caught in the ring-trawl in the oV-shore waters in the Plymoutharea. Journal of the Marine Biological Association of the United Kingdom 16,707–722.


Russell, F. S. (1931a). The vertical distribution of marine macroplankton X. Noteson the behaviour of Sagitta in the Plymouth area. Journal of the Marine BiologicalAssociation of the United Kingdom 17, 391–414.

Russell, F. S. (1931b). The vertical distribution of marine macroplankton XI. Furtherobservations on diurnal changes. Journal of the Marine Biological Association ofthe United Kingdom 17, 767–784.

Russell, F. S. (1933). The seasonal distribution of macroplankton as shown bycatches in the 2-metre stramin ring-trawl in oV-shore waters oV Plymouth. Journalof the Marine Biological Association of the United Kingdom 19, 73–81.

Russell, F. S. (1934). The vertical distribution of marine macroplankton XII. Someobservations on the vertical distribution of Calanus finmarchicus in relation to lightintensity. Journal of the Marine Biological Association of the United Kingdom 19,569–584.

Russell, F. S. (1935a). On the value of certain plankton animals as indicators of watermovements in the English Channel and North Sea. Journal of the Marine BiologicalAssociation of the United Kingdom 20, 309–331.

Russell, F. S. (1935b). The seasonal abundance and distribution of the pelagic youngof teleostean fishes caught in the ring-trawl in oV-shore waters in the Plymoutharea. Part II. Journal of the Marine Biological Association of the United Kingdom20, 147–179.

Russell, F. S. (1936). Observations on the distribution of plankton animal indicatorsmade on Col. E. T. Peel’s yacht ‘‘St. George’’ in the mouth of the English Channel,July, 1935. Journal of the Marine Biological Association of the United Kingdom 20,507–522.

Russell, F. S. (1953). The English Channel. Transactions of the Devonshire Associ-ation for the Advancement of Science, Literature and Art 85, 1–17.

Russell, F. S. (1973). A summary of the observations on the occurrence of planktonicstages of fish oV Plymouth 1924–1972. Journal of the Marine Biological Associationof the United Kingdom 53, 347–355.

Russell, F. S. (1976). The Eggs and Planktonic Stages of British Marine Fishes.Academic Press, London.

Russell, F. S., Southward, A. J., Boalch, G. T. and Butler, E. I. (1971). Changes inbiological conditions in the English Channel oV Plymouth during the last halfcentury. Nature 234, 468–470.

Sargent, J. R., Gatten, R. R., Corner, E. D. S. and Kilvington, C. C. (1977). On thenutrition and metabolism of zooplankton. XI. Lipids in Calanus helgolandicusgrazing Biddulphia sinensis. Journal of the Marine Biological Association of theUnited Kingdom 57, 525–533.

Sims, D. W., Genner, M. J., Southward, A. J. and Hawkins, S. J. (2001). Timing ofsquid migration reflects North Atlantic climate variability. Proceedings of theRoyal Society of London B 268, 2607–2611.

Sims, D. W., Wearmouth, V. J., Genner, M. J., Southward, A. J. and Hawkins, S. J.(2004). Low-temperature driven early spawning migration of a temperate marinefish. Journal of Animal Ecology 73, 333–341.

Sinha, B. and Pingree, R. (1994). A high resolution study of the spatial and spectralcharacteristics of a coccolithophore bloom using aerial remote sensing.Proceedings of Environmental Research Institute of Michigan (ERIM) 3, 763–774.

Skud, B. E. (1982). Dominance in fishes: The relation between environment andabundance. Science 216, 144–158.

Smith, J. E. (1932). The shell gravel and the infauna of the Eddystone Grounds.Journal of the Marine Biological Association of the United Kingdom 18, 243–278.


Smith, J. E. (1968). Torrey Canyon pollution and marine life: A report by thePlymouth Laboratory. University Press, Cambridge.

Smith, P. E. and Moser, H. G. (2003). Long term trends and variability in the larvaeof the Pacific Sardine and associated fish species of the California Current Region.Deep Sea Research II 50, 2514–2536.

Southward, A. J. (1960). On changes of sea temperature in the English Channel.Journal of the Marine Biological Association of the United Kingdom 39, 449–458.

Southward, A. J. (1962). The distribution of some plankton animals in the EnglishChannel 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.

Southward, A. J. (1963). The distribution of some plankton animals in the EnglishChannel and Approaches. III. Theories about long-term biological changes,including fish. Journal of the Marine Biological Association of the United Kingdom43, 1–29.

Southward, A. J. (1967). Recent changes in abundance of intertidal barnacles inSouth-West England: A possible eVect of climatic deterioration. Journal of theMarine Biological Association of the United Kingdom 47, 81–95.

Southward, A. J. (1970). Improved methods of sampling post-larval young fish andmacroplankton. Journal of the Marine Biological Association of the UnitedKingdom 50, 689–712.

Southward, A. J. (1974a). Changes in the plankton community of the western EnglishChannel. Nature 249, 180–181.

Southward, A. J. (1974b). Long-term changes in abundance of the eggs of theCornish pilchard (Sardina pilchardus Walbaum). Journal of the Marine BiologicalAssociation of the United Kingdom 54, 641–649.

Southward, A. J. (1980). The western English Channel—an inconstant ecosystem?Nature 285, 361–366.

Southward, A. J. (1983). Fluctuations in the ecosystem of the Western Channel: Asummary of studies in progress. Proceedings of the 17th European Marine BiologySymposium Oceanologia Acta 1983 suppl. 187–189.

Southward, A. J. (1984). Fluctuations in the ‘‘indicator’’ chaetognaths Sagitta ele-gans and Sagitta setosa in the Western Channel. Oceanologia Acta 7, 229–239.

Southward, A. J. (1991). 40 years of changes in species composition and populationdensity of barnacles on a rocky shore near Plymouth. Journal of the MarineBiological Association of the United Kingdom 71, 495–513.

Southward, A. J. (1995). The importance of long time-series in understandingthe variability of natural systems. Helgolander Meeresuntersuchungen 49,329–333.

Southward, A. J. (1996). The Marine Biological Association and Fishery Research,1884–1924: Scientific and political conflicts that changed the course of marineresearch in the United Kindom. Buckland Occasional Papers 2, 61–80.

Southward, A. J. and Bary, B. M. (1980). Observations on the vertical distribution ofeggs and larvae of mackerel and other teleosts in the Celtic Sea and on thesampling performance of diVerent nets in relation to stock evaluation. Journal ofthe Marine Biological Association of the United Kingdom 60, 295–311.

Southward, A. J. and Boalch, G. T. (1986). Aspects of long term changes in theecosystem of the western English Channel in relation to fish populations. In‘‘International Symposium on Long Term Changes in Marine Fish Populations’’(T. Wyatt and M. G. Larraneta, eds.), pp. 415–446. Instituto InvestigacionesMarinas, Vigo.


Southward, A. J. and Boalch, G. T. (1992). The marine resources of Devon’s coastalwaters. In ‘‘The New Maritime History of Devon. Volume 1: From earlytimes to the late eighteenth century’’ (M. DuVy, S. Fisher, B. Greenhill, D. J.Starkey and J. Youings, eds.), pp. 51–61. Conway Maritime Press, London.

Southward, A. J. and Boalch, G. T. (1994). The eVect of changing climate on marinelife: Past events and future predictions. Exeter Maritime Studies. 9, 101–143.

Southward, A. J. and Butler, E. I. (1972). A note on further changes of sea tempera-ture in the Plymouth area. Journal of the Marine Biological Association of theUnited Kingdom 52, 931–937.

Southward, A. J. and Crisp, D. J. (1954). Recent changes in the distribution of theintertidal barnacles Chthamalus stellatus Poli and Balanus balanoides L. in theBritish Isles. Journal of Animal Ecology. 23, 163–177.

Southward, A. J. and Crisp, D. J. (1956). Fluctuations in the distribution andabundance of intertidal barnacles. Journal of the Marine Biological Association ofthe United Kingdom 35, 211–229.

Southward, A. J. and Demir, N. (1974). Seasonal changes in dimensions and viabilityof the developing eggs of the Cornish pilchard (Sardina pilchardus Walbaum) oVPlymouth. In ‘‘The Early Life History of Fish’’ (J. H. Blaxter, ed.), pp. 53–68.Springer, Heidelberg.

Southward, A. J. and Mattacola, A. D. (1980). Occurrence of Norway Pout, Trisop-terus esmarki (Nilsson) and blue whiting (Micromesistius poutassou (Risso), in thewestern English Channel oV Plymouth. Journal of the Marine BiologicalAssociation of the United Kingdom 60, 39–44.

Southward, A. J. and Roberts, E. K. (1987). One hundred years of marine research atPlymouth. Journal of the Marine Biological Association of the United Kingdom 68,423–445.

Southward, A. J. and Southward, E. C. (1977). Distribution and ecology of thehermit crab Clibanarius erythropus in the Western Channel. Journal of the MarineBiological Association of the United Kingdom 57, 441–452.

Southward, A. J. and Southward, E. C. (1978). Recolonization of rocky shores inCornwall after use of toxic dispersants to clean up the Torrey Canyon spill. Journalof the Fisheries Research Board of Canada 35, 682–705.

Southward, A. J. and Southward, E. C. (1988). Disappearance of the warm waterhermit crab Clibanarius erythropus from south west Britain. Journal of the MarineBiological Association of the United Kingdom 68, 409–412.

Southward, A. J., Butler, E. I. and Pennycuick, L. (1975). Recent cyclic changes inclimate and in abundance of marine life. Nature 253, 714–717.

Southward, A. J., Boalch, G. T. and Maddock, L. (1988a). Fluctuations in theherring and pilchard fisheries of Devon and Cornwall linked to change in climatesince the 16th century. Journal of the Marine Biological Association of the UnitedKingdom 68, 423–445.

Southward, A. J., Boalch, G. T. and Maddock, L. (1988b). Climatic change and theherring and pilchard fisheries of Devon and Cornwall. In ‘‘Devon’s coastline andcoastal waters’’ (D. Starkey, ed.), pp. 33–57. University Press, Exeter.

Southward, A. J., Hawkins, S. J. and Burrows, M. T. (1995). Seventy years’ observa-tions of changes in distribution and abundance of zooplankton and intertidalorganisms in the western English Channel in relation to rising sea temperature.Journal of Thermal Biology. 20, 127–155.

Spence, S. K., Bryan, G. W., Gibbs, P. E., Masters, D., Morris, L. and Hawkins, S. J.(1990). EVects of TBT contamination on Nucella populations. Functional Ecology.4, 425–432.


Stebbing, A. R. D., Turk, S. M. T., Wheeler, A. and Clarke, K. R. (2002). Immigra-tion of southern fish species to south-west England linked to warming of the NorthAtlantic (1960–2001). Journal of the Marine Biological Association of the UnitedKingdom 82, 177–180.

Steele, J. H. (1985). A comparison of terrestrial and marine ecological systems.Nature 313, 355–358.

Steven, G. A. (1930). Bottom fauna and the food of fishes. Journal of the MarineBiological Association of the United Kingdom 16, 677–706.

Steven, G. A. (1948). Contributions to the biology of the mackerel, Scomber scom-brus L. Mackerel migrations in the English Channel and Celtic Sea. Journal of theMarine Biological Association of the United Kingdom 28, 517–539.

Steven, G. A. (1949). Contributions to the biology of the mackerel, Scomber scom-brus (L.) II. A study of the fishery in the south-west of England, with specialreference to spawning, feeding, and ‘‘fishermens signs.’’ Journal of the MarineBiological Association of the United Kingdom 28, 555–576.

Steven, G. A. (1952). Contributions to the biology of the mackerel, Scomberscombrus (L.) III. Age and growth. Journal of the Marine Biological Associationof the United Kingdom 30, 549–568.

Steven, G. A. and Corbin, P. G. (1939). Mackerel investigation at Plymouth. Prelim-inary report. Rapport et proces-verbaux des reunions. Conseil permanent inter-national pour l’Exploration de la Mer. 111(app. 2), 15–18.

Tait, R. V. (1972). Elements of Marine Ecology. Butterworth, London.Vane, F. R. (1951). The distribution and ecology of some north Atlantic planktonicAmphipoda. M.Sc. thesis. University of Liverpool.

Vane, F. R. (1961). Continuous Plankton Records: Contribution towards a planktonatlas of the north-eastern Atlantic and the North Sea. Part III: Gastropoda.Bulletins of Marine Ecology 5, 98–101.

Vevers, H. G. (1951). Photography of the sea floor. Journal of the Marine BiologicalAssociation United Kingdom 30, 101–111.

Vevers, H.G. (1952). A photographic survey of certain areas of sea floor near Plymouth.Journal of the Marine Biological Association United Kingdom 31, 215–221.

Volkman, J.K., Corner, E.D. S. andEglinton,G. (1980). Transformation of biolipids inthe marine food web and underlying bottom sediments. In ‘‘Organic Matter Biogeo-chemistry at the Marine Sediment Water Interface’’ (R. Daumas, ed.), pp. 185–197.Colloques Internationaux duCentreNational de laRecherche Scientifique,Marseille.

Walsh, G. E., McLaughlan, L. L., Lores, E. M., Louie, M. K. and Deans, C. H.(1985). EVects of organotins on growth and survival of two marine diatoms,Skeletonema costatum and Thalassiosira pseudonana. Chemosphere 14, 383–392.

Warner, A. J. and Hays, G. C. (1994). Sampling by the Continuous PlanktonRecorder survey. Progress in Oceanography 34, 237–256.

Widdowson, T. B. (1971). A taxonomic revision of the genus Alaria Greville. Syesis4, 11–49.

Williams, P. J. le B., Thomas, D. N. and Reynolds, C. S. (eds.) (2002). In ‘‘Phytoplank-ton productivity. Carbon assimilation in marine and freshwater systems.’’ BlackwellScience, Oxford.

Williams, R. (1975). The Continuous Plankton Recorder Survey: A plankton atlas ofthe North Atlantic and North Sea: Supplement 4—the Ostracoda in 1963. Bulletinof Marine Ecology 8, 215–228.

Williams,R. andWallace,M.A. (1975). Continuous plankton records: A plankton atlasof theNorthAtlantic andNorth Sea. Supplement 1—the genusClausocalanus (Crust-acea: Copepoda, Calanoida) in 1965. Bulletin of Marine Ecology 8, 167–184.


Wilson, D. P. (1951). A biological diVerence between natural sea waters. Journal ofthe Marine Biological Association of the United Kingdom 30, 1–19.

Wilson, D. P. and Armstrong, F. A. J. (1958). Biological diVerences between seawaters: Experiments in 1954 and 1955. Journal of the Marine Biological Associationof the United Kingdom 37, 331–348.

Wilson, D. P. and Armstrong, F. A. J. (1961). Biological diVerences between seawaters: Experiments in 1960. Journal of the Marine Biological Association of theUnited Kingdom 41, 663–681.

Wilson, J. B., Holme, N. A. and Barrett, R. L. (1977). Population dispersal in thebrittle-star Ophiocomina nigra Abildgaard (Echinodermata: Ophiuroidea). Journalof the Marine Biological Association of the United Kingdom 57, 405–439.

Wood, E. D., Armstrong, F. A. and Richards, F. A. (1967). Determination of nitratein seawater by cadmium-copper reduction to nitrite. Journal of the MarineBiological Association of the United Kingdom 47, 23–31.

Zibordi, G., Alberotanza, L., DoerVer, R., Aiken, J., Wernand, M., Boxall, S.,Santer, R. and Cheileachair, O. N. (1998). Coastal region long-term measurementsfor colour remote sensing development and validation (COLOURS).Third Euro-pean Marine Science and Technology Conference. Project Synopses, Volume II:Strategic Marine Research, pp. 901–906. European Commission, Brussels.


Interactions Between Behaviour andPhysical Forcing in the Control ofHorizontal Transport of Decapod

Crustacean Larvae

Henrique Queiroga* and Jack Blanton{

*Departmento de Biologia, Universidade de Aveiro,

Campus Universitario de Santiago,

3810-193 Aveiro, Portugal

E-mail: [email protected]{Skidaway Institute of Oceanography,

Savannah, Georgia 31411, USA

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 109

2. Definitions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 113

2.1. Larval Stages. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 113

2.2. Types of Vertical Migration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 116

2.3. Ecological Categories. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 117

3. Marine Physical Processes and Larval Transport Mechanisms . . . . . . . . . . . . . . . . . . . . . 118

3.1. Tides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 119

3.2. Wind-Induced Currents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 120

3.3. Buoyancy-Induced Currents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 120

3.4. Geostrophic Currents. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 120

3.5. Cross-shelf Flow and Exchange . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 121

3.6. Internal Waves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 124

3.7. Sea and Land Breezes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 124

3.8. Interaction of Migratory Behaviour With Tidal Currents . . . . . . . . . . . . . . . . . . . . . . 124

3.9. Estuarine Transport . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127

3.10. Transport Regimes Along Continental Margins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132

3.11. Frontal Zones as Sites of Larval Congregation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135

4. Cyclic Vertical Migration in the Natural Environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137

4.1. Sampling Methodology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 138


4.2. Prevalence of Cyclic Vertical Migration According to Taxonomic and

Ecological Category . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 139

5. Ontogenetic Migration and the Extent of Vertical Movements . . . . . . . . . . . . . . . . . . . . . 143

6. Significance of Vertical Migration in Dispersal: Evidence from

Field Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 148

6.1. Tidal Migrations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 149

6.2. Diel Migrations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 154

6.3. Ontogenetic Migrations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 159

7. Proximate Factors Controlling Vertical Migration: Environmental Factors and

Endogenous Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161

7.1. Tactic and Kinetic Responses by Estuarine and Marine Larvae . . . . . . . . . . . . . . . 161

7.2. Endogenous Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 163

8. Behavioural Control of Vertical Migration: Evidence from Laboratory Studies. . . . . . . 164

8.1. Responses to Environmental Factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 170

8.2. Endogenous Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 181

9. Nonrhythmic Vertical Migration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 186

10. Mechanism for Depth Regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187

11. Modifiers of Vertical Migration Pattern: Temperature, Salinity, and Food . . . . . . . . . . . 188

12. Vertical and Horizontal Swimming Velocities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 190

13. Measurements of Horizontal Transport . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192

13.1. Tagging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193

13.2. Larval Velocity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194

Acknowledgements. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 196

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 196

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

108 HENRIQUE QUEIROGA AND JACK BLANTON

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 reinva-

sion 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 diVer-ences 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 deca-

pod 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

HORIZONTAL TRANSPORT OF DECAPOD LARVAE 109

direction of their horizontal dispersal. Many of the field studies that investi-

gated 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 simultan-

eously for scales of variation that might vary by several orders of magnitude,

are not easy to solve with present-day technologies. Larvae are small organ-

isms that easily escape detection and that are impossible to track individu-

ally, 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 inter-

preted 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 exam-

ination 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 ob-

served 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 select-

ive 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).


Such traits include hatching rhythms synchronised with tidal and

diel cycles (Forward, 1987b; Morgan and Christy, 1994), as well as tidally-

synchronised vertical migrations that enhance seaward transport (Forward

and Tankersley, 2001). The high osmotic and thermal stresses and in-

tense 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 Crust-

acea seem to lack cryptic, anatomical, and chemical defenses against preda-

tion 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 accom-

plished 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 deca-

pod larvae. The currently accepted view for explaining nocturnal and re-

versed 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 photonega-

tive 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 migra-

tion, 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,


and from a segregation in the horizontal plane. DiVerential distributions oflarval 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 plank-

tonic larval phase may originate from the need to avoid a benthic environ-

ment 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 mechan-

isms (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 plank-

tonic 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


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 popula-

tions 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 inter-

actions 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 develop-

ment patterns (Figure 1). Classification of development patterns is based on

the types of larvae, number of stages, and presence or absence of meta-

morphic transitions, and it reflects phylogenetic relationships (reviewed by


Figure 1(a)


Figure 1(b) (Continued)


Gurney, 1942; Williamson, 1982; Anger, 2001). Moreover, the average dur-

ation 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 divisionswithin the decapod crustaceans. A: first zoea of Parapenaeus longirostris (Dendro-brachiata), B: first zoea of Palaemon elegans (Caridea), C: first zoea of Nephropsnorvegicus (Astacidea), D: first zoea of Callianassa tyrrhena (Thalassinidea), E: thirdphyllosoma of Palinurus elephas (Palinura), F: first zoea of Pisidia longicornis (Anom-ura), G: first zoea of Anapagurus sp. (Anomura), H: first zoea of Carcinus maenas(Brachyura). Redrawn from dos Santos (1999) except A, which was redrawn fromHeldt (1938), and H, drawn from Rice and Ingle (1975). (b) Examples of post larvalforms of the major infraorders or divisions within the decapod crustaceans. A:first postlarva of Parapenaeus longirostris (Dendrobranchiata), B: first postlarva ofPalaemon elegans (Caridea), C: stage IV of Nephrops norvegicus (Astacidea),D: megalopa of Callianassa tyrrhena (Thalassinidea), E: puerulus of Palinuruselephas (Palinura), F: megalopa of Anapagurus laevis (Anomura), G: megalopaof Carcinus maenas (Brachyura). Redrawn from: A: dos Santos (1999); B: Hoglund(1943); C: Santucci (1926a); D: dos Santos (1999); E: Santucci (1926b); F:MacDonald et al. (1957); G: Rice and Ingle (1975).


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 aminimum

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 select-

ive tidal stream transport (Forward and Tankersley, 2001). For simplifica-

tion, 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. Rhyth-

mic migration can, and very often does, occur over a background of onto-

genetic 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


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 con-

sidered (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 LARVALTRANSPORT 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 crust-

acean 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.

Table 1 Ecological categories of decapod crustaceans according to habitat ofadults and larvae

Ecological categoryHabitat ofadults

Habitat oflarvae

Obligate estuarine species Estuary EstuaryEstuarine species that exporttheir larvae to shelf waters

Estuary Shelf

Shelf species that may penetrateestuaries as adults

Shelf, estuary Shelf

Shelf species that use estuariesas nursery habitats

Shelf Shelf, estuary

Shelf species Shelf Shelf, oceanShelf and slope species Shelf, slope Shelf, ocean


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 super-

posed 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 understand-

ing 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 peri-

odically 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 con-

stituents 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 magni-

tude of tidal constituents at a given location that governs the characteristics

of the tide, such as the spring-neap diVerences in tidal magnitude, the


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 diVer-ence of the two water masses. This density diVerence reduces the eVect ofgravity, 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 diVer-ence. 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


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

VE ¼ �trf

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, oVshoresurface 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 strati-

fication 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


Figure 2 (a) Vertical mixing is very eYcient for downwelling, and horizontaldensity gradients are enhanced. The surface and bottom boundary layers merge indeeper waters over the shelf, thus creating a wide zone shoreward, where the netcurrent, 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 sealevel caused by downwelling. (b) During upwelling, vertical mixing is inhibited, whichenhances vertical stratification. The surface and bottom boundary layers merge closer


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 circula-

tion 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 andGarvine, 2001, and references therein). Early-

stage 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 circula-

tion generated by the prevailing northwardwind 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 down-welling 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-shoredirection but occurs in a narrower zone than in panel (a). The shoreward flowingbottom 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 levelcaused by upwelling. (c) The only diVerence between this panel and panel (b) is thatthe estuary has a deep connection with the ocean (as in the Galician Rias). Thisallows nutrient-rich water to enter the estuary directly.


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 fluctu-

ations 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 mech-

anisms are especially relevant over continental shelves, and in estuaries

in particular. The well-known example of selective tidal stream transport


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 constitu-

ents like S2. The larvae can also influence their net (tidally averaged) move-

ment 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, horizon-

tal transport of larvae undergoing diel migration could be as much as 4 km

d�1. 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


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 migra-

tion extends into the bottom boundary layer, where the current is signifi-

cantly 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 bound-

ary layer, where shear is weaker, the net horizontal movement is substan-

tially 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 migra-

tion 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 d�1. 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


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 circula-

tion 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


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

128

HENRIQ

UEQUEIROGAAND

JACKBLANTON

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 gener-

ates 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, circu-

lation 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-fre-

quency overtides as they propagate into shallow estuaries and tidal creeks


(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

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


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 estuar-

ies. Typical water level fluctuations can be greater than 0.2 m. Thus, a

northward/southward wind-stress fluctuation leads directly to a flux sea-

ward/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

F ¼ uAz ¼ Axy

dZdt

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 rateof change in the water level. Thus, flux through the inlet is proportional to the

ratio of themeanhorizontal water surface area of the estuary to themean cross-

sectional 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 inwater 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 aswell

as other events occurring at subtidal frequencies. The fluctuations are superim-

posed on the normal rise and fall of the lunar tides, both of which are accom-

panied 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 correlateswell with interannual variability of

the strength of upwelling (Blanton et al., 1987).


A good example of decapod larval movement is the ingress of Callinectes

sapidus megalopae into Chesapeake Bay. Studies on the influence of wind-

driven 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. Large-

scale 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 equator-

ward in summer and poleward in winter—as a result of seasonal changes in


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 8Nin the summer (Wooster et al., 1976; Fiuza et al., 1982; Sousa and Fiuza,

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 along-

shelf 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 conver-

gence 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


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 popula-

tions 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 explan-

ation of westward intensification was presented by Stommel (1948), who

showed that the variation of Coriolis force with latitude (the beta eVect) wasfundamentally responsible for the dynamic of the intensification. The Gulf

Stream axis follows the general trend of the continental slope along the south-

eastern United States. Transport through the Straits of Florida is about 30 Sv

(1Sv ¼ 1 million cubic meters per second), with some evidence of seasonal

variation (Niiler andRichardson, 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 itswidthmore thandoubles (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 theGulf Stream frontal zone and propagate along the outer

shelf at speeds of around 0.4m/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


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.

TheGulf 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 north-

ward 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, pro-

viding 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 seawardbyoVshore advection. Thedynamics 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 thewind 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


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.Down-

welling winds that persist set up a favourable regime that can transport surface

water shoreward. Upwelling fronts have been explicitly identified as participat-

ing in the transport of barnacle larvae toward the California coast (Rough-

garden 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

stratificationwithin 6 h of awind 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


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 (Fiuza et al., 1998; Peliz and Fiuza, 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 THENATURAL 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


important periodic factors that may have caused the evolution of behav-

ioural 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 environ-

ments. 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 ob-

liquely. Some types of nets, such as the Longhurst-Hardy Plankton Re-

corder, 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 migra-tion of decapod larvae; studies used diVerent combinations of the techniques listed

Samplinggear

Verticalresolution

Verticalintegration

Horizontal/temporal resolution

Pump Neuston and singlewater-column level

Discrete Fixed station,time variation

Net Neuston and multiplewater-column levels

Drift station,time variation

Multiple net Multiple water-columnlevels

Continuous Grid of stations,space and timevariation


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 environ-

mental 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 diVerentphases 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 totaxonomic 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 eco-

logical 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 juven-

iles. 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.


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

Infraorder ordivision Species

Types of vertical migration

ReferencesFirst stageMiddlestages Last stage

Obligate estuarine species

Brachyura Rhithropanopeusharrisii

Flood,nocturnal

Flood,nocturnal

Flood Cronin and Forward, 1982, 1986

Estuarine species that export their larvae to the shelfBrachyura Callinectes sapidus Ebb,

nocturnal,no rhythm(1/3)

Norhythm(1/3)

Flood,nocturnal

Williams, 1971; Smyth, 1980;Provenzano et al., 1983;Epifanio et al., 1984;Brookins and Epifanio, 1985, 1988;Mense and Wenner, 1989;DeVries et al., 1994; Olmi, 1994

Brachyura Carcinus aestuarii No rhythm(1/1)

Abello and Guerao, 1999

Brachyura Carcinus maenas Ebb, nocturnal Flood Queiroga et al., 1997;Queiroga, 1998

Brachyura Ovalipes ocellatus Nocturnal Nocturnal Epifanio, 1988Brachyura Pinnixa spp. Flood,

nocturnalDeVries et al., 1994

Brachyura Uca spp. Ebb Flood,nocturnal

DeCoursey, 1976; Brookinsand Epifanio, 1985; DeVries et al.,1994; Garrison, 1999

Shelf species that may penetrate estuaries as adults

Caridea Palaemon adspersus Ebb, nocturnal Pereira et al., 2000Caridea Palaemon elegans Ebb Pereira et al., 2000Thalassinidea Callianassa subterranea Nocturnal Nocturnal Lindley, 1986

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Brachyura Lophopanopeus spp. No rhythm DiBacco et al., 2001Brachyura Pachygrapsus crassipes Ebb, nocturnal DiBacco et al., 2001Brachyura Pachygrapsus marmoratus Ebb Pereira et al., 2000Brachyura Pirimela denticulata Ebb Pereira et al., 2000Brachyura Portumnus latipes Nocturnal Abello and Guerao, 1999

Shelf species that use estuaries as nursery habitats

Dendrobranchiata Penaeus indicus Flood Forbes and Benfield, 1986Dendrobranchiata Penaeus japonicus Flood

nocturnalForbes and Benefield, 1986;Kuwahara et al., 1987

Dendrobranchiata Penaeus plebejus Floodnocturnal

Young and Carpenter, 1977;Rothlisberg et al., 1995

Dendrobranchiata Penaeus vannamei Flood Mair et al., 1982Dendrobranchiata Penaeus spp. Nocturnal Nocturnal Nocturnal Rothlisberg, 1982

Shelf species

Caridea Pandalus montagui Reverse Reverse Lindley et al., 1994Caridea Processa canaliculata Nocturnal Nocturnal Nocturnal Lindley, 1986Astacidea Homarus americanus Nocturnal Nocturnal No rhythm Harding et al., 1987Palinura Panulirus cygnus Nocturnal Nocturnal Phillips et al., 1978; Rimmer

and Phillips, 1979Palinura Scyllarus bicuspidatus Nocturnal Nocturnal Phillips et al., 1981Anomura Pagurus bernhardus Reverse Reverse Lindley et al., 1994Anomura Pagurus prideauxii Nocturnal Nocturnal Lindley, 1986Anomura Pisidia longicornis Nocturnal Abello and Guerao, 1999Anomura Porcellana platycheles Nocturnal Abello and Guerao, 1999Brachyura Cancer magister Nocturnal Twilight Booth et al., 1985;

Jamieson and Phillips, 1988;Jamieson et al., 1989;Hobbs and Botsford, 1992

Brachyura Cancer oregonensis Twilight Jamieson and Phillips, 1988

(Continued)

HORIZONTALTRANSPORTOFDECAPOD

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Brachyura Cancer spp. Nocturnal Nocturnal Nocturnal Shanks, 1986Brachyura Corystes cassivelaunus Nocturnal Nocturnal Lindley et al., 1994Brachyura Ebalia sp. 3 Nocturnal Abello and Guerao, 1999Brachyura Macropodia sp. No rhythm

(1/1)Abello and Guerao, 1999

Brachyura Randallia ornata Nocturnal Nocturnal Nocturnal Shanks, 1986

Shelf and slope species

Caridea Pontophilus bispinosus Nocturnal Nocturnal Lindley, 1986Astacidea Nephrops norvegicus Nocturnal Nocturnal Lindley et al., 1994Anomura Munida rugosa Nocturnal Nocturnal Lindley et al., 1994Brachyura Atelecyclus rotundatus Nocturnal Nocturnal Nocturnal Lindley, 1986Brachyura Goneplax rhomboides Nocturnal Abello and Guerao, 1999Brachyura Inachus sp. Nocturnal Abello and Guerao, 1999Brachyura Liocarcinus depurator Nocturnal Abello and Guerao, 1999Brachyura Maja crispata Nocturnal Abello and Guerao, 1999Brachyura Atelecyclus sp. Nocturnal Abello and Guerao, 1999Brachyura Liocarcinus spp. Nocturnal Nocturnal Nocturnal Lindley, 1986

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.

Table 3 (Continued)


Types of vertical migration

ReferencesFirst stageMiddlestages Last stage

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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 OFVERTICAL 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 avail-

able 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 max-

imum abundance values according to development stage, except for studies

1 and 12, in which average depth of distribution is reported. The data in


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


Firststage

Middlestages

Laststage

Stationdepth (m) References


Brachyura Rhithropanopeusharrisii

1.8 1.9–2.1 2.0 4 Cronin, 1982 (1)

Estuarine species that export their larvae to shelf waters

Brachyura Callinectes sapidus 0–10 0–10 20–35 Epifanio, 1988 (2)Brachyura Callinectes sapidus 0–2 25 25 Epifanio et al., 1984 (3)Brachyura Callinectes sapidus Neuston 10–20 Johnson, 1985 (4)Brachyura Carcinus maenas 0–30 0–30 0–60 20–200 Queiroga, 1996 (5)Brachyura Ovalipes ocellatus 20–35 0–15 0–15 20–35 Epifanio, 1988 (2)Brachyura Uca spp. 20 10–20 Johnson, 1985 (4)


Thalassinidea Callianassa subterranea 0–25 25–50 >150 Lindley, 1986 (6)Brachyura Liocarcinus spp. 42 27 >80 Lindley et al., 1994 (12)


Dendrobranchiata Penaeus spp. 0–20 0–20 0–20 20–30 Rothlisberg, 1982

Shelf species

Caridea Crangon allmani 15–29 >80 Lindley et al., 1994 (12)Caridea Pandalus montagui 11 11–13 14 >80 Lindley et al., 1994 (12)

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Caridea Pontophilus bispinosus 0–50 >150 Lindley, 1986 (6)Caridea Processa canaliculata 0–25 0–50 0–100 >150 Lindley, 1986 (6)Astacidea Homarus americanus 0–10 0–20 Neuston 60 Harding et al., 1987 (7)Palinura Panulirus cygnus 6–25 50–500 Palmer, 1995 (8)Palinura Panulirus cygnus 0–60 0–120 200–>1000 Forward, 1976 (9)Palinura Panulirus spp. 0–50 0–50 75–250 Yeung and McGowan,

1991 (10)Anomura Pagurus bernhardus 12 14–15 >80 Lindley et al., 1994 (12)Anomura Pagurus prideauxii 0–50 0–100 >150 Lindley, 1986 (6)Brachyura Cancer spp. 10 10 25 70 Shanks, 1986 (11)


Astacidea Nephrops norvegicus 22 15 >80 Lindley et al., 1994 (12)Anomura Munida rugosa 29 15 >80 Lindley et al., 1994 (12)Brachyura Atelecyclus rotundatus 0–50 50–100 >150 Lindley, 1986 (6)Brachyura Hyas coarctatus 30 23 >80 Lindley et al., 1994 (12)

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., Rhithro-

panopeus harrisii, Callinectes sapidus, Callianassa subterraneana, Processa

canaliculata, Homarus americanus, Panulirus cygnus, and Pagurus pri-

deauxii). 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


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 mul-

tiple 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 disper-

sal 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 behav-

iour 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


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 develop-

ment 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 devel-

opment. 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 appro-

priate habitats for settlement, larvae must possess a repertoire of behavioural

responses to environmental factors. These responses are expressed diVerentiallyin different larval instars that encounter particular combinations of environ-

mental 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 andMundy, 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; re-

sidual tidal currents; internal waves; and density-driven flow. For these pro-

cesses 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


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 coloniza-

tion 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 synchron-

ised with the tidal and diel cycles, as well as tidal-synchronised vertical

migrations. The high osmotic and thermal stresses and intense pelagic pre-

dation characteristic of the estuarine environment demand special adapta-

tions; 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 reinva-

sion 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 resting-

on-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 post-

larvae during estuarine upstream migration (Penn, 1975; shrimp: Brookins

and Epifanio, 1985; Forbes and Benfield, 1986; Calderon Perez and Poli,

1987; crab: Christy andMorgan, 1998; Olmi, 1994; Queiroga, 1998). Decapod


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 trans-

port, 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 signifi-

cantly more abundant during night ebb tides, resulting from synchronous


Figure 5 Retention of the complete larval phase inside estuaries through tidallysynchronised vertical migration. Inset graph represents a change in the verticalposition of larval stages during the tidal and daily cycles (only one of all possiblecombinations of phase relationship between the two cycles is represented). Thehighest position along the water column is reached during flood. The xanthidRhithropanopeus harrisii is representative of this type of behaviour. HWS ¼ high-water slack; LWS ¼ low-water slack.


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151

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


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 concen-

trated 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, indicat-

ing a net upstream flux. Highest densities occurred during night floods, when

the megalopae aggregated close to the surface. Abundance and depth distribu-

tion 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 estua-

rine 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 showa 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.


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 (For-

ward, 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 apredictable 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), abun-

dance 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 estuar-

ies 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


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 predict-

able onshore/oVshore patterns of larval distributions, which would be regu-

lated 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), some-

times 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 inter-

preted 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 trans-

ported 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 trans-

port, based on wind fields estimated from atmospheric pressure distribu-

tions, 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 diVerentyears (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


Figure 7 Schematic representation of sea (a) and land (b) breezes. Panel (c) rep-resents typical variation of wind intensity. Putative onshore transport of crab mega-lopae occurs when they enter the neuston layer at sunset, when the sea breeze is closeto its maximum intensity.


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 ofCarpentaria (Australia) and the K1 tidal constituent (period ¼ 23.93 h). Verticaldistribution of postlarvae along the day is represented in panel (a) for situations 182days apart, which correspond to opposite phase relationships between the day andthe tide cycles: in Days 0 and 365, postlarvae reach the highest position in the watercolumn 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 ofthe beat period between the day and the tide cycles (which equals 365.4 d). Transportis consistently into one direction during one part of the year, and into the oppositedirection during the other part. The 15-day oscillation of the advective potentialcorresponds to the spring–neap cycle of tidal amplitude. Time was arbitrarily set atDay 0 in both panels.


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 Carpen-

taria 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 north-

ward 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 Carpen-

taria 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


can account for the observed diVerences in recruitment times in the two

nursery areas of the Gulf. During March, the larvae will be advected north-

ward, 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 byphysical 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 back-

ground 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


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 mega-

lopae 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

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


(Hagen et al., 1993) showed that megalopae occurred in a surface layer

that approaches the coast during relaxation of northerly, upwelling-

favourable 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 themajority 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 observa-

tions 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 inver-

tebrates. The environmental factors to which animals respond can be classi-

fied 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


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 move-

ments. 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


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 diVerentsalinities. 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. How-

ever, 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 in-

ternal 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. Bio-

logical 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 free-

running 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


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 labora-

tory 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 themovements 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 (Duchene 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


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

Infraorder ordivision Species E

ndogenous

Light

Pressure

Gravity

Salinity

Turbulence

Current

Tem

perature

Chem

icals

References


Brachyura Eurypanopeusdepressus

F F F Sulkin et al., 1983

Brachyura Neopanopaeussayi

F, I F, I F, I Forward et al., 1989;Forward, 1989a

Brachyura Panopeusherbstii

F, I F, I F, I, L Sulkin, 1973, 1975;Forward, 1977

Brachyura Rhithro-panopeusharrisii

F, I F, I, L F, I, L F, I, L F, I F, I Forward, 1974, 1985, 1989a,b;Forward andCostlow, 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

(Continued)


LARVAE

165

Estuarine species that export their larvae to the shelf

Brachyura Callinectessapidus

L F, I, L F, L F F, I, L F, L L F, I L Naylor and Isaac, 1973;Forward, 1977;Sulkin et al., 1979, 1980;Sulkin and van Heukelem,1982; McConnaughey and Sulkin,1984; Luckenbachand Orth, 1992; Forward and Rittschof,1994; Tankersley and Forward, 1994;Forward et al., 1995, 1997;Tankersley et al., 1995, 1997;Welch and Forward, 2001

Brachyura Carcinusmaenas

F, L F, L F, L Rice, 1964; Knight-Jones andQasim, 1967; Zeng and Naylor,1996a,b; Duchene andQueiroga, 2001.

Brachyura Pachygrapsuscrassipes

L L L Shanks, 1985

Brachyura Sesarmacinereum

F Forward, 1977

Brachyura Uca pugilator F Forward, 1977

Table 5 (Continued )


ndogenous

Light

Pressure

Gravity

Salinity

Turbulence

Current

Tem

perature

Chem

icals

References

166

HENRIQ

UEQUEIROGAAND

JACKBLANTON

Brachyura Uca spp. L L L L L Forward and Rittschof,1994; Tankersley andForward, 1994; Tankersleyet al., 1995


Brachyura Libiniaemarginata

F Forward, 1977


DendrobranchiataPenaeusbrevirostris

L L L Mair et al., 1982

Dendro-branchiata

Penaeuscaliforniensis

L L L Mair et al., 1982

Dendro-branchiata

Penaeusduodarum

L L Hughes, 1969; Hughes, 1972

Dendro-branchiata

Penaeusjaponicus

L Forbes and Benfield, 1986

Dendro-branchiata

Penaeusstylirostris

L L L L Mair et al., 1982

Dendro-branchiata

Penaeusvannamei

L L L L Mair et al., 1982

Shelf species

Astacidea Homarusamericanus

F, I, L F, I, L F, I, L L Ennis, 1975a, 1986;Boudreau et al., 1992

Palinura Panulirus cygnus F Ritz, 1972Anomura Galathea sp. L Knight-Jones and Qasim, 1967Anomura Pagurus

beringanusF Forward, 1987a

Anomura Pagurusgranosimanus

F Forward, 1987a

(Continued)


LARVAE

167

Anomura Paguruslongicarpus

F, I Roberts, 1971

Brachyura Cancer gracilis F Forward, 1987aBrachyura Cancer irroratus F, I F, I F, I F, I Bigford, 1977, 1979Brachyura Cancer magister F, I F, I F, I Jacoby, 1982Brachyura Ebalia tuberosa F F F Schembri, 1982Brachyura Hemigrapsus

oregonensisF Forward, 1987a

Brachyura Hyas araneus F Knight-Jones and Qasim, 1967Brachyura Leptodius

floridanusF, I, L F, I, L F, I Sulkin, 1973, 1975; Wheeler

and Epifanio, 1978Brachyura Liocarcinus

holsatusL Naylor and Isaac, 1973

Brachyura Lophopanopeusbellus

F Forward, 1987

Brachyura Scyra acutifrons F Forward, 1987


Brachyura Geryonquinquedens

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.

Table 5 (Continued )


ndogenous

Light

Pressure

Gravity

Salinity

Turbulence

Current

Tem

perature

Chem

icals

References

168

HENRIQ

UEQUEIROGAAND

JACKBLANTON

review, but good descriptions can be found in Forward (1989b), Forward

and Wellins (1989), Tankersley et al. (1995), Zeng and Naylor (1996a), and

Duchene 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 comple-

ments 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 quan-

tification 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 reac-

tions to light used directional light as a stimulus. As noted by Forward

(1988), directional light does not occur in the natural underwater environ-

ment. 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.


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 depthlevels, 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 interpret-

ation 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 univer-

sal 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.,


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. Mega-

lopae usually display positive geotaxis (L. floridanus and Panopeus herbstii,

Sulkin, 1973; Cancer irroratus, Bigford, 1979), although Pachygrapsus cras-

sipes (Shanks, 1985) andCallinectes sapidus (Sulkin and vanHeukelem, 1982)

megalopae are geonegative. All megalopae show high barokinesis (C. maenas

andMacropipus sp., Rice, 1964;Carcinus maenas andMacropipus 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 investi-

gated 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 s�1 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 s�1. Slow

rates of pressure decrease evoked a descent response in all zoeal stages, with

threshold rates ranging from 0.40 to 0.53 mbar s�1. 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 � 10�2 mbar s�1, whereas Uca spp. megalopae

responded only to rates above 4.9 � 10�2 mbar s�1. 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 mega-

lopae of these species encounter in many of the estuaries where they occur


(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 increas-

ing 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 s�1 (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 ofEbalia 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 7-

day-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

zoeaewere negatively buoyant and that stages I and IIwere geopositive, but not


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

showedhigh 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, al-

though 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 andCassidy, 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 refer-

ences 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 photo-

positive 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 environ-

ment, 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 direc-

tional 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


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 accordingto 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


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 � 10�7

W m�2, 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 � 10�7

W m�2 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 down-

ward-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 develop-

ment proceeds. These reactions agree with the field observation that younger

zoeae are above the 1 � 10�7 W m�2 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 con-

trol of ascent during dusk and descent during dawn. The larval stage investi-

gated 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 distribu-

tion. Before sunset, larvae remained near the 1 � 10�7 W m�2 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 oc-

curred varied over four orders of magnitude, the amount of absolute de-

crease 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 � 10�3 W s�1, which is close to the fastest

rate of change of light intensity around sunset, determined to be�4.0� 10�3

W s�1. The ascent was not controlled by positive phototaxis, because the

larvae did not move directly toward the overhead light source, but appeared


to be directed by negative geotaxis. Moreover, when an inverse light field

was used, where the light source was placed below the experimental cham-

ber, 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 � 10�7 W m�2 (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 � 10�7 W m�2), through rates of

increase that varied over two orders of magnitude. The downward move-

ment was initiated as light increased slightly above the threshold level of

1.87� 10�7 Wm�2. 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 � 10�7 W m�2 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. Down-

ward 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. More-

over, estuarine water inhibited the swimming by megalopae of C. sapidus

that were collected in estuaries at light levels normally encountered in


estuarine and marine waters during the day. On the contrary, at intensity

levels typical of the night period, swimming was not suppressed. The sup-

pression of swimming at high light levels did not occur in oVshore waters.

These diVerences were not caused by salinity or temperature diVerences butby 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 predator-

avoidance mechanism.

Light intensity was also shown to modify the response to other environ-

mental 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 photo-

kinetic 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 s�1 for C. sapidus and 1.0 � 1012

photons m2 s�1 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 � 10�3 ppt s�1. Neopanope sayi larvae responded to lower rates of

change, and the threshold increased from 2.8 � 10�4 ppt s�1 for the first

to 7.0 � 10�4 ppt s�1 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


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. Neopa-

nope 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. Mega-

lopae 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 �10�4 ppt s�1, than for Uca spp., at 1.33 � 10�3 ppt s�1. 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 � 10�4 to 1.32 � 10�3 ppt s�1, 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 investi-

gated 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. californien-

sis, P. brevirostris) preferred lagoon water when given a choice between


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 pro-

gramme, 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, bra-

chyuran, and astacid species. Penaeus duodarum postlarvae show positive

rheotaxis and can swim against slow currents on the order of 5 cm s�1

(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 to-

gether 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.


Megalopae of Callinectes sapidus can orient in relation to currents and

make headway into currents less than 4.8 cm s�1 (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 s�1, 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 s�1 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 s�2 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 hy-

potheses 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.


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 semidiur-

nal 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 third-

stage 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 orienta-

tion 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.


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 rhythmwith a free-running period of 24.63 h.Megalopaewere

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 relation-

ship of the expected day and tidal phases. The mismatch between the en-

dogenous 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 ofC. sapidusmegalopae 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 diVerencescould 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 evi-

denced 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 thatsynchronise endogenous vertical migration and of its ecological significance.


Field-caught zoeae fromWales 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 ofthe 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

(Duchene 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 non-

ovigerous 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 ampli-

tude, 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 atmos-

pheric 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


would therefore be of little use for dispersal and recruitment. Not surpris-

ingly, C. maenas first zoeae hatched from Swedish females did not demon-

strate 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 meso-

tidal 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 wereidentified 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 circa-

tidal 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 mega-

lopae 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 (swim-

ming 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


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 down-

stream 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 swim-

ming 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 condi-

tions 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 sub-

strata. 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.


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 oVshore-and estuarine-collected megalopae, whether a circatidal rhythm could be

entrained by salinity changes typical of estuarine systems, and whether aqua-

tic vegetation could induce settlement and metamorphosis. Megalopae col-

lected 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 thatC. sapidus

megalopae enter estuaries with a solar day rhythm of activity and that this

rhythm is not expressed under natural conditions because light inhibits swim-

ming 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 reduc-

tion during high river runoV periods, the increase in hydrostatic pressure that

results from increased sea level driven bywind 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 Louisi-

ana 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,


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 shallowwaters

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 recruit-

ment to estuarine habitats of P. aztecus (Rogers et al., 1993).

10. MECHANISM FOR DEPTH REGULATION

Sulkin (1984) proposed amodel for depth regulationof 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 environ-

mental cues and level of locomotory activity. Thenegative feedbackmechanism

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 thismodel with the crabRhithropanopeus 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 andWellins (1989) andForward

(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.


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

Figure 10 Light-dependent negative feedback model for depth regulation ofdecapod crustacean larvae. The upper and lower depth limits that a larva reachesduring the course of vertical movements, before corrective behavioural responsesreverse 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 thelevel of light adaptation. In darkness or with low light levels (a), the distance a larvamoves up before a corrective response is larger than the distance it moves down beforeresponding, and the larva ascends in the water column. The reverse occurs with highlight levels (b).


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 30min. In these columns, the temperature change occurred over a distance

of only 0.10m. These conditions seldom, if ever, occur in nature, even in highly

stratified estuarine systems. Temperature diVerences over 10 8C did signifi-

cantly 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 experi-

mental 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 penetrat-

ing 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 aslarge 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


swimmers). The ability to swim across seasonal thermoclines may have con-

siderable 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 trajectoryfrom 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 mechan-

isms may be responsible for the advection of zooplankton on shelf waters

(Mackas, 1992; Mackas et al., 1997; Smith et al., 2001). Haloclines do aVectthe 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 larvaemigrated at the level of the thermocline. Such a pattern ofmigration

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 deca-

pods, 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,


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 s�1,

with most observations falling in the range of 0.5–2 cm s�1. A larva traveling

at a velocity of 0.5 cm s�1 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 eVectdecreases 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 behav-

iour—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 s�1 in early stages (phyllosoma

I–III) to 0.54 cm s�1 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


horizontal swimming speeds are 7.7–10 cm s�1 in the puerulus of Panulirus

argus and average 18 cm s�1 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 andKeller, 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,

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


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 ob-

servation 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 tech-

niques 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 settle-

ment 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 com-

pares the concentrations of trace elements found in wild larvae to those


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 origin-

ated 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 propor-

tion ofP. crassipes zoea I from diVerent origins that was exchanged across thelagoon 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 con-

centration. 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:

ut ¼

Xn

z�1

uzt � DDzt

Xn

z�1

DDzt

;

where u is the longitudinal component of velocity (positive during ebb and

negative during flood), DD is the height of each stratum, andPn

z�1 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:


ult ¼

Xn

z¼1

uzt � DDzt � Czt

Xn

z¼1

DDzt � Czt

;

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 onlarval velocity for a typical situation in which current velocity decreases with depth.Arrows represent current velocity, larval flux, or larval velocity; horizontal barsrepresent 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 distributedwith depth, and depth-integrated current velocity equals depth-integrated larvalvelocity. In (b) the same number of larvae are concentrated close to the surface,where the current is stronger. Therefore, depth-integrated current velocity is smallerthan depth-integrated larval velocity. If the larvae were concentrated close to thebottom, current velocity would be greater than larval velocity.


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 diVer-ence 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 Joao Almeida (Universidade de Aveiro,

Portugal) and Nacho Gonzalez (Centro Andaluz de Ciencia y Tecnologıa,

Marinas, Spain) compiled the data and prepared the figure on the phase

relationships of the tidal and the diel cycles. PerMoksnes (KristinebergMarine

Research Station, Sweden) andAugusto Flores (Universidade Estadual de Sao

Paulo, Brazil) contributed suggestions that helped shape several aspects of the

text. Antonina dos Santos (Instituto Nacional de Investigac,ao 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 Deca-

pod Fisheries: Assessment and Management Options—which was funded by

the European Community under the Fifth Framework Programme (contract

QLK5-CT1999-01272). The Fundac,ao para a Ciencia e Tecnologia, Portugal,

supported a stay of Henrique Queiroga at the Skidaway Institute of Oceanog-

raphy 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.

REFERENCES

Abello, P. and Guerao, G. (1999). Temporal variability in the vertical and mesoscalespatial distribution of crab megalopae (Crustacea: Decapoda) in the NorthwesternMediterranean. Estuarine, Coastal and Shelf Science 49, 129–139.

Aldrich, D. V., Wood, C. E. and Baxter, K. N. (1968). An ecological interpretation oflow temperature response in Penaeus aztecus and P. setiferus postlarvae. Bulletinof Marine Science 18, 61–71.

Almeida, M. J. and Queiroga, H. (2003). Physical forcing of onshore transport ofcrab megalopae in the northern Portuguese upwelling system. Estuarine, Coastaland Shelf Science 57, 1091–1102.


Anastasia, J. R., Morgan, S. G. and Fisher, N. S. (1998). Tagging crustacean larvae:Assimilation and retention of trace elements. Limnology and Oceanography 43,362–368.

Anger, K. (1983). Moult cycle and morphogenesis inHyas araneus larvae (Decapoda,Majidae), reared in the laboratory. Helgolander Meeresuntersuchungen 36,285–302.

Anger, K. (2001). ‘‘The Biology of Decapod Crustacean Larvae’’. A. A. BalkemaPublishers, Rotterdam.

Anger, K. (2003). Salinity as a key parameter in the larval biology of decapodcrustaceans. Invertebrate Reproduction and Development 43, 29–45.

Anger, K., Spivak, E. and Luppi, T. (1998). EVects of reduced salinities on develop-ment and bioenergetics of early larval shore crab, Carcinus maenas. Journal ofExperimental Marine Biology and Ecology 220, 287–304.

Arthur, R. S. (1960). On the calculation of vertical motion in eastern boundarycurrents from determinations of horizontal motion. Journal of GeophysicalResearch 70, 2799–2803.

Atkinson, A., Ward, P., Williams, R. and Poulet, S. A. (1992). Feeding rates and dielvertical migration of copepods near South Georgia: Comparison of shelf andoceanic sites. Marine Biology 114, 49–56.

Bakun, A. (1973). Coastal upwelling indices, west coast of North America,1946–1971. NOAA Technical Report NMFS SSRF-671, U.S. Department ofCommerce

Bakun, A. (1996). ‘‘Patterns in the Ocean: Ocean Processes and Marine PopulationDynamics’’. California Sea Grant College System, La Jolla.

Bane, J. and Brooks, D. (1979). Gulf stream meanders along the continentalmargin from the Florida Straits to Cape Hatteras. Geophysical Research Letters 6,280–282.

Bentley, E. and Sulkin, S. D. (1977). The ontogeny of barokinesis during the zoealdevelopment of the xanthid crab Rhithropanopeus harrisii (Gould). MarineBehaviour and Physiology 4, 275–282.

Bigford, T. E. (1977). EVects of oil on behavioural responses to light, pressureand gravity in larvae of the rock crab Cancer irroratus. Marine Biology 43,137–148.

Bigford, T. E. (1979). Ontogeny of light and gravity responses in rock crab larvae(Cancer irroratus). Marine Biology 52, 69–76.

Blanton, J. O. (1996). Reinforcement of gravitational circulation by wind. Coastaland Estuarine Studies 53, 47–58.

Blanton, J. O. and Andrade, F. (2001). Distortion of tidal currents and the lateraltransfer of salt in a shallow coastal plain estuary (O Estuario do Mira, Portugal).Estuaries 24, 467–480.

Blanton, J. O., Atkinson, L. P., Pietrafesa, L. J. and Lee, T. N. (1981). The intrusionof Gulf Stream water across the continental shelf due to topographically inducedupwelling. Deep-Sea Research 28, 393–405.

Blanton, J. O., Tenore, K. R., Castillejo, F., Atkinson, L. P., Schwing, F. B. andLavin, A. (1987). The relationship of upwelling to mussel production in the rias onthe western coast of Spain. Journal of Marine Research 45, 497–511.

Blanton, J. O., Oey, L.-Y., Amft, J. and Lee, T. (1989). Advection of momentum andbuoyancy in a coastal frontal zone. Journal of Physical Oceanography 19, 98–115.

Blanton, J. O., Wenner, E. L., Werner, F. and Knott, D. (1995). EVects of wind-generated coastal currents on the transport of blue crab megalopae on a shallowcontinental shelf. Bulletin of Marine Science 57, 739–752.


Blanton, J. O., Verity, P., Amft, J., Wenner, E., Barans, C., Knott, D., Stender, B. andWilde, S. (2001). ‘‘Key Factors Influencing Transport of White Shrimp Postlarvae inSoutheastern U.S. Estuaries’’. Georgia Seagrant Programme, Athens, Georgia.

Blanton, J. O., Lin, G. and Elston, S. (2002). Tidal current asymmetry in shallowestuaries and tidal creeks. Continental Shelf Research 22, 1731–1743.

Boehlert, G. W. and Mundy, B. C. (1988). Roles of behavioural and physical factorsin larval and juvenile fish recruitment to estuarine nursery areas. American Fisher-ies Society Symposium 3, 51–67.

Booth, J. D., Phillips, A. C. and Jamieson, G. S. (1985). Fine scale spatial distribu-tion of Cancer magister megalopae and its relevance to sampling methodology.Alaska Sea Grant Report 85, 273–286.

Botsford, L. W., Moloney, C. L., Largier, J. L. and Hastings, A. (1998). Metapopu-lation dynamics of meroplanktonic invertebrates: the Dungeness crab (Cancermagister) as an example. Canadian Special Publication of Fisheries and AquaticSciences 125, 295–306.

Boudreau, B., Simard, Y. and Bourget, E. (1992). Influence of a thermocline onvertical distribution and settlement of post-larvae of the American lobsterHomarus americanus Milne-Edwards. Journal of Experimental Marine Biologyand Ecology 162, 35–49.

Bousfield, E. L. (1955). Ecological control of the occurrence of barnacles in theMiramichi estuary. Bulletin of the Natural History Museum of Canada, BiologySeries 46, 1–65.

Brookins, K. G. and Epifanio, C. E. (1985). Abundance of brachyuran larvae in asmall coastal inlet over six consecutive tidal cycles. Estuaries 8, 60–67.

Burrage, D. and Garvine, R. (1987). Supertidal frequency internal waves on thecontinental shelf south of New England. Journal of Physical Oceanography 17,808–819.

Calderon Perez, J. A. and Poli, C. R. (1987). A (physical) approach to the postlarvalPenaeus in migration mechanism in a Mexican coastal lagoon (Crustacea:Decapoda: Penaeidae). Annales de l’Instituto de Ciencias Marinas y Limnologicas,Universidad Nacional Autonoma de Mexico 14, 147–156.

Caley, M. J., Carr, M. H., Hixon, M. A., Hughes, T. P., Jones, G. P. and Menge,B. A. (1996). Recruitment and the local dynamics of open marine populations.Annual Review of Ecology and Systematics 27, 477–500.

Calinski, M. D. and Lyons, W. G. (1983). Swimming behaviour of the puerulus of thespiny lobster Panulirus argus (Latreille, 1804) (Crustacea: Palinuridae). Journal ofCrustacean Biology 3, 329–335.

Chia, F.-S., Buckland-Nicks, J. and Young, C. M. (1984). Locomotion of marineinvertebrate larvae: A review. Canadian Journal of Zoology 62, 1205–1222.

Christy, J. H. and Morgan, G. (1998). Estuarine immigration by crab postlarvae:Mechanisms, reliability and adaptive significance. Marine Ecology Progress Series174, 51–65.

Christy, J. H. and Stancyk, S. E. (1982). Timing of larval production and fluxof invertebrate larvae in a well-mixed estuary. In ‘‘Estuarine Comparisons’’ (V. S.Kennedy, ed.), pp. 489–503. Academic Press, New York.

Clancy, M. and Epifanio, C. E. (1989). Distribution of crab larvae in relation to tidalfronts in Delaware Bay, USA. Marine Ecology Progress Series 57, 77–82.

Cobb, J. S., Wang, D., Campbell, D. B. and Rooney, P. (1989). Speed and directionof swimming by postlarvae of the American lobster. Transactions of the AmericanFisheries Society 118, 82–86.


Cobb, J. S., Booth, J. D. and Clancy, M. (1997). Recruitment strategies in lobstersand crabs: a comparison. Marine Freshwater Research 48, 797–806.

Creutzberg, F. (1961). The orientation of migrating elvers (Anguilla vulgaris Turt) intidal areas. Netherlands Journal of Sea Research 1, 257–338.

Creutzberg, F. (1975). Orientation in space: Animals. Invertebrates. In ‘‘MarineEcology’’ (O. Kinne, ed.), pp. 555–656. J. Wiley, London.

Crisp, D. J. (1974). Factors influencing the settlement of marine invertebrate larvae.In ‘‘Chemoreception in Marine Organisms’’ (P. T. Grant and A. M. Mackie, eds.),pp. 177–265. Academic Press, London.

Cronin, T. W. (1982). Estuarine retention of larvae of the crab Rhithropanopeusharrisii. Estuarine, Coastal and Shelf Science 15, 207–220.

Cronin, T. W. and Forward, R. B., Jr. (1979). Tidal vertical migration: An endoge-neous rhythm in estuarine crab larvae. Science 205, 1020–1022.

Cronin, T. W. and Forward, R. B., Jr. (1982). Tidally timed behaviour: EVects onlarval distributions in estuaries. In ‘‘Estuarine Comparisons’’ (V. S. Kennedy, ed.),pp. 505–520. Academic Press, New York.

Cronin, T. W. and Forward, R. B., Jr. (1983). Vertical migration rhythms of newlyhatched larvae of the estuarine crab, Rhithropanopeus harrisii. Biological Bulletin165, 139–153.

Cronin, T. W. and Forward R. B., Jr. (1986). Vertical migration cycles of crab larvaeand their role in larval dispersal. Bulletin of Marine Science 39(2) pp. 192–201.

Csanady, G. (1982). ‘‘Circulation in the Coastal Ocean’’. D. Reidel, Dordrecht, TheNetherlands.

Dawidowicz, P., Pijanowska, J. and Ciechomsky, K. (1990). Vertical migration ofChaoborus larvae is induced by the presence of fish. Limnology and Oceanography35, 1631–1637.

DeCoursey, P. (1976). Vertical migration of larval Uca in a shallow estuary. Ameri-can Zoologist 16, 244.

DeCoursey, P. (1983). Biological timming. In ‘‘Behaviour and Ecology’’ (F. J. Vernbergand W. B. Vernberg, eds.), pp. 107–162. Academic Press, New York.

DeVries, M. C., Tankersley, R. A., Forward, R. B., Jr., Kirby-Smith, W. W. andLuettich, R. A., Jr. (1994). Abundance of estuarine crab larvae is associated withtidal hydrologic variables. Marine Biology 118, 403–413.

DiBacco, C. and Chadwick, D. B. (2001). Assessing the dispersal and exchange ofbrachyuran larvae between regions of San Diego Bay, California and nearshorecoastal habitats using elemental fingerprinting. Journal ofMarine Research 59, 53–78.

DiBacco, C. and Levin, L. A. (2000). Development and application of elementalfingerprinting to track the dispersal of marine invertebrate larvae. Limnology andOceanography 45, 871–880.

DiBacco, C., Sutton, D. andMcConnico, L. (2001). Vertical migration behaviour andhorizontal distribution of brachyuran larvae in a low-inflow estuary: Implicationsfor bay-ocean exchange. Marine Ecology Progress Series 217, 191–206.

Dini, M. L. and Carpenter, S. R. (1988). Variability in Daphnia behaviour followingfish community manipulation. Journal of Plankton Research 10, 621–635.

Dittel, A. I. and Epifanio, C. E. (1990). Seasonal and tidal abundance of crab larvaein a tropical mangrove system, Gulf of Nicoya, Costa Rica. Marine EcologyProgress Series 65, 25–34.

Dittel, A. I., Epifanio, C. E. and Lizano, O. (1991). Flux of crab larvae in a mangrovecreek in the Gulf of Nicoya, Costa Rica. Estuarine, Coastal and Shelf Science 32,129–140.


dos Santos, A. (1999).‘‘Larvas de crustaceos decapodes da costa continental portu-guesa’’. PhD thesis, Universidade de Lisboa.

Drickamer, L. C., Vessey, S. H. and Jakob, E. M. (2002). ‘‘Animal Behaviour:Mechanisms, Ecology, Evolution’’. McGraw Hill, New York.

Dronkers, J. (1986). Tidal asymmetry and estuarine morphology. NetherlandsJournal of Sea Research 20, 117–131.

Duchene, J.-C. and Queiroga, H. (2001). Use of an intelligent CCD camera for thestudy of endogenous vertical migration rhythms in first zoeae of the crab Carcinusmaenas. Marine Biology 139, 901–909.

Dugdale, R. and Wilkerson, F. (1989). New production in the upwelling center atPoint Conception, California: Temporal and spatial patterns. Deep-Sea Research36, 985–1007.

Eggleston, D. B., Armstrong, D. A., Elis, W. E. and Patton, W. S. (1998). Estuarinefronts as conduits for larval transport: Hydrodynamics and spatial distribution ofDungeness crab postlarvae. Marine Ecology Progress Series 164, 73–82.

Ennis, G. P. (1975a). Behavioural responses to changes in hydrostatic pressure andlight during larval development of the lobster Homarus americanus. Journal of theFisheries Research Board of Canada 32, 271–281.

Ennis,G. P. (1975b).Observations onhatching and larval release in the lobsterHomarusgammarus. Journal of the Fisheries Research Board of Canada 32, 2210–2213.

Ennis, G. P. (1986). Swimming ability of larval american lobsters, Homarus amer-icanus, in flowing water. Canadian Journal of Fisheries and Aquatic Sciences 43,2177–2183.

Enright, J. T. (1975a). The circadian tape recorder and its entrainment. In ‘‘Physio-logical Adaptation to the Environment’’ (F. V. Vernberg, ed.), pp. 465–476. IntextEducational Publications, New York.

Enright, J. T. (1975b). Orientation in time: endogenous clocks. In ‘‘Marine Ecology’’(O. Kinne, ed.), pp. 917–944. Wiley, London.

Epifanio, C. E. (1988). Dispersal strategies of two species of swimming crab on thecontinental shelf adjacent to Delaware Bay. Marine Ecology Progress Series 49,243–248.

Epifanio, C. E. andGarvine,W.W. (2001). Larval transport on the Atlantic continentalshelf of North America: a review. Estuarine, Coastal and Shelf Science 52, 51–77.

Epifanio, C. E., Valenti, C. C. and Pembroke, A. E. (1984). Dispersal and recruit-ment of blue crab larvae in Delaware Bay, USA. Estuarine Coastal and ShelfScience 18, 1–12.

Falkenhaug, T., Tande, K. S. and Semenova, T. (1997). Diel, seasonal and ontogen-etic variations in the vertical distributions of four marine copepods. MarineEcology Progress Series 149, 105–119.

Fiuza, A. F. G., Macedo, M. E. and Guerreiro, M. R. (1982). Climatological spaceand time variation of the Portuguese coastal upwelling. Oceanologica Acta 5,31–40.

Fiuza, A., Hamann, M., Ambar, I., Del-Rio, G., Gonzalez, N. and Cabanas, J.(1998). Water masses and their circulation oV western Iberia during May 1993.Deep-Sea Research 45, 1127–1160.

Forbes, A. T. and Benfield, M. C. (1986). Tidal behaviour of post-larval penaeidprawns (Crustacea: Decapoda: Penaeidae) in a Southeast African estuary. Journalof Experimental Marine Biology and Ecology 120, 23–34.

Forward, R. B., Jr. (1974). Negative phototaxis in crustacean larvae: Possiblefunctional significance. Journal of Experimental Marine Biology and Ecology 16,11–17.


Forward, R. B., Jr. (1976). A shadow response in a larval crustacean. BiologicalBulletin 151, 126–140.

Forward, R. B., Jr. (1977). Occurrence of a shadow response among brachyuranlarvae. Marine Biology 39, 331–341.

Forward, R. B., Jr. (1985). Behavioural responses of larvae of the crab Rhithropano-peus harrisii (Brachyura: Xanthidae) during diel vertical migration.Marine Biology90, 9–18.

Forward, R. B., Jr. (1986). A reconsideratrion of the shadow response of a larvalcrustacean. Marine Behaviour and Physiology 12, 99–113.

Forward, R. B., Jr. (1987a). Comparative study of crustacean larval photoresponses.Marine Biology 94, 589–595.

Forward, R. B., Jr. (1987b). Larval release rhythms of decapod crustaceans: anoverview. Bulletin of Marine Science 41, 165–176.

Forward, R. B., Jr. (1988). Diel vertical migration: Zooplankton photobiology andbehaviour. Oceanography and Marine Biology Annual Review 26, 361–393.

Forward, R. B., Jr. (1989a). Behavioural responses of crustacean larvae to rates ofsalinity change. Biological Bulletin 176, 229–238.

Forward, R. B., Jr. (1989b). Depth regulation of larval marine decapod crustaceans:Test of an hypothesis. Marine Biology 102, 195–201.

Forward, R. B., Jr. and Costlow, J. D., Jr. (1974). The ontogeny of phototaxis bylarvae of the crab Rhithropanopeus harrisii. Marine Biology 26, 27–33.

Forward, R. B., Jr. and Cronin, T. W. (1980). Tidal rhythms of activity and photo-taxis of an estuarine crab larva. Biological Bulletin 158, 295–303.

Forward, R. B., Jr. and Rittschof, D. (1994). Photoresponses of crab megalopae inoVshore and estuarine waters: implications for transport. Journal of ExperimentalMarine Biology and Ecology 182, 183–192.

Forward, R. B., Jr. and Rittschof, D. (2000). Alteration of photoresponses involvedin diel vertical migration of a crab larva by fish mucus and degradation products ofmucopolysaccharides. Journal of Experimental Marine Biology and Ecology 245,277–292.

Forward, R. B., Jr. and Tankersley, R. A. (2001). Selective tidal-stream transport ofmarine animals. Oceanography and Marine Biology: An Annual Review 39,305–353.

Forward, R. B., Jr. and Wellins, C. A. (1989). Behavioural responses of alarval crustacean to hydrostatic pressure: Rhithropanopeus harrisii (Brachyura:Xathidae). Marine Biology 101, 159–172.

Forward, R. B., Jr., Cronin, T. W. and Stearns, D. E. (1984). Control of diel verticalmigration: photoresponses of a larval crustacean. Limnology and Oceanography 29,146–154.

Forward, R. B., Jr., Wellins, C. A. and Buswell, C. U. (1989). Behavioural responsesof larvae of the crab Neopanope sayi to hydrostatic pressure. Marine EcologyProgress Series 57, 267–277.

Forward, R. B., Jr., Tankersley, R. A., DeVries, M. C. and Rittschof, D. (1995).Sensory physiology and behaviour of blue crab (Callinectes sapidus) postlarvaeduring horizontal transport. Marine and Freshwater Behaviour and Physiology 26,233–248.

Forward, R. B., Jr., Swanson, J., Tankersley, R. A. and Welch, J. M. (1997).Endogenous swimming rhythms of blue crab, Callinectes sapidus, megalopae:EVects of oVshore and estuarine cues. Marine Biology 127, 621–628.

Franks, P. (1997). Spatial patterns in dense algal blooms. Limnology and Oceanog-raphy 42, 1297–1305.


Friedrichs, C. and Aubrey, D. (1988). Non-linear tidal distortion in shallowwell-mixed estuaries: A synthesis. Estuarine, Coastal and Shelf Science 27,521–545.

Frouin, R., Fiuza, A. F. G., Ambar, I. and Boyd, T. J. (1990). Observation of apoleward surface current oV the coast of Portugal and Spain during winter. Journalof Geophysical Research 95, 679–691.

Gaines, S. D. and LaVerty, K. D. (1995). Modelling the dynamics of marinespecies: The importance of incorporating larval dispersal. In ‘‘Ecology ofMarine Invertebrate Larvae’’ (L. McEdward, ed.), pp. 389–412. CRC Press,Boca Raton.

Garrett, C. and Loder, J. (1981). Dynamical aspects of shallow sea fronts. Philosoph-ical Transactions of the Royal Society of London 302, 563–581.

Garrison, L. P. (1999). Vertical migration behaviour and larval transport in bra-chyuran crabs. Marine Ecology Progress Series 176, 103–113.

Garvine, R. W., Epifanio, C. E., Epifanio, C. C. and Wong, K. C. (1997). Transportand recruitment of blue crab larvae: A model with advection and mortality.Estuarine, Coastal and Shelf Science 45, 99–111.

Gherardi, F. (1995). Hermit crab larval behaviour: Depth regulation in Discorsopa-gurus schmitti (Stevens). Journal of Experimental Marine Biology and Ecology 192,107–123.

Gherardi, F. and Cassidy, P. (1994). Macrobenthic associates of bioherms of thepolychaete Sabellaria cementarium from northern Puget Sound. Canadian Journalof Zoology 72, 514–525.

Goodrich, D. M., Van Montfrans, J. and Orth, R. J. (1989). Blue crab megalopalinflux to Chesapeake Bay: Evidence for a wind-driven mechanism. Estuarine,Coastal and Shelf Science 29, 247–260.

Gurney, R. (1942). ‘‘Larvae of Decapod Crustacea’’. Ray Society, London.Hagen, E., Feistel, R. and Mittelstaedt, E. (1993). A case study of meso-scale motionpatterns oV the Portuguese west coast. ICES Hydrography Commitee ThemeSession O.

Harden Jones, F. R., Greer Walker, M. and Arnold, G. P. (1984). Tactics of fishmovement in relation to migration strategy and water circulation. In ‘‘Mechanismsof Migration in Fishes’’ (J. D. McCleave, G. P. Arnold, J. J. Dodson and W. H.Neill, eds.), pp. 185–207. Plenum Press, New York.

Harding, G. C., Pringle, J. D., Vass, W. P., Pearre, S., Jr. and Smith, S. J. (1987).Vertical distribution and daily movements of larval lobsters Homarus americanusover Browns Bank, Nova Scotia. Marine Ecology Progress Series 41, 29–41.

Hare, J. and Cowen, R. (1996). Transport mechanisms of larval and pelagic juvenilebluefish Pomotomus saltatrix from South Atlantic Bight spawning grounds toMiddle Altantic Bight nursery habitats. Limnology and Oceanography 41,1264–1280.

Hare, J., Quinlan, J., Werner, F., Blanton, B., Govani, J., Forward, R., Jr., Settle, L.and Hoss, D. (1999). Influence of vertical distribution on the outcome oflarval transport during winter in the Carolina capes region: Results of athree-dimensional hydrodynamic model. Fisheries Oceanography 8(Suppl. 2),7–76.

Harris, G. P. (1980). Temporal and spatial scales in phytoplankton ecology:Mechanisms, methods, models and management. Canadian Journal of Fisheriesand Aquatic Sciences 37, 877–900.


Harris, R. P. (1988). Interactions between diel vertical migratory behaviour of marinezooplankton and the subsurface chlorophyll maximum. Bulletin of Marine Science43, 663–674.

Hasek, B. and Rabalais, N. (2001). A comparison of molt stages of blue crabmegalopae, Callinectes sapidus (Rathbun), sampled with artificial collectors andplankton nets. Journal of Experimental Marine Biology and Ecology 265, 15–27.

Hatfield, S. E. (1983). Intermolt staging and distribution of dungeness crab, Cancermagister, megalopae. Fisheries Bulletin, California Department of Fish and Game172, 85–96.

Haynes, R. and Barton, E. D. (1990). A poleward flow along the Atlantic coast of theIberian Peninsula. Journal of Geophysical Research 95, 11425–11441.

Heldt, J. H. (1938). La reproduction chez les Crustaces Decapodes de la famille desPeneides. Annales de l’Institut d’Oceanographie 18, 31–206.

Herrnkind, W. F. (1968). The breeding of Uca pugilator (Bosc) and mass rearing ofthe larvae with comments on the behaviour of the larval and early crab stages(Brachyura, Ocypodidae). Crustaceana 1968 Supplement 2, 214–224.

Hickey, B. M. (1989). Patterns and processes of circulation over the Washingtoncontinental shelf and slope. In ‘‘Coastal Oceanography of Washington andOregon’’ (M. R. Landry and B. M. Hickey, eds.), pp. 41–115. Elsevier, Amster-dam.

Hill, A. E. (1991a). A mechanism for horizontal zooplankton transport by verticalmigration in tidal currents. Marine Biology 111, 485–492.

Hill, A. E. (1991b). Vertical migration in tidal currents. Marine Ecology ProgressSeries 75, 39–54.

Hill, A. E. (1995). The kinematic principles coverning horizontal transport inducedby vertical migration in tidal flows. Journal of the Marine Biological Association ofthe United Kingdom 75, 3–13.

Hill, A. E. (1998). Diel vertical migration in stratified tidal flows: Implications forplankton dispersal. Journal of Marine Research 56, 1069–1096.

Hobbs, R. C. and Botsford, L. W. (1992). Diel vertical migration and timing ofmetamorphosis of larvae of the Dungeness crab Cancer magister. Marine Biology112, 417–428.

Hobbs, R. C., Botsford, L. W. and Thomas, A. (1992). Influence of hydrographicconditions and wind forcing on the distribution and abundance of Dungeness crab,Cancer magister larvae. Canadian Journal of Fisheries and Aquatic Sciences 49,1379–1388.

Hoglund, H. (1943). On the biology and development of Leander squilla (L.) formatypica de Man. Svenska Hydrografisk-Biologiska Kommissionens Skrifter, Ny serieBiologi. 2, 1–58.

Hovel, K. A. and Morgan, S. G. (1997). Planktivory as a selective force for repro-ductive synchrony and larval migration. Marine Ecology Progress Series 157,79–95.

Hughes, D. A. (1969). Responses to salinity changes as a tidal transport mechanismof pink shrimp Penaeus duodarum. Biological Bulletin 136, 43–53.

Hughes, D. A. (1972). On the endogenous control of tide-associated displacements ofpink shrimp, Penaeus duodarum Burkenroad. Biological Bulletin 142, 271–280.

Jackson, G. A. and Strathmann, R. R. (1981). Larval mortality from oVshore mixingas a link between pre-competent and competent periods of development. AmericanNaturalist 118, 16–26.


Jacoby, C. A. (1982). Behavioural responses of the larvae of Cancer magisterDana (1852) to light, pressure and gravity. Marine Behaviour and Physiology 8,267–283.

Jager, Z. (1999). Selective tidal stream transport of the flounder (Platichthys flesus L.)in the Dolard (Ems estuary). Estuarine, Coastal and Shelf Science 49, 347–362.

Jamieson, G. S. and Phillips, A. C. (1988). Occurrence of Cancer crab (C. magisterand C. oregonensis) megalopae oV the west coast of Vancouver Island, BritishColumbia. Fishery Bulletin US 86, 525–542.

Jamieson, G. S. and Phillips, A. C. (1993). Megalopal spatial distribution and stockseparation in Dungeness crab (Cancer magister). Canadian Journal of Fisheries andAquatic Sciences 50, 416–429.

Jamieson, G. S., Phillips, A. C. and Huggett, W. S. (1989). EVects of ocean variabilityon the abundance of Dungeness crab (Cancer magister) megalopae. CanadianSpecial Publications on Fisheries and Aquatic Sciences 108, pp. 305–325.

Johnson, D. F. (1985). The distribution of brachyuran crustacean megalopae in thewaters of the York River, lower Chesapeake Bay and adjacent shelf: Implicationsfor recruitment. Estuarine, Coastal and Shelf Science 20, 693–705.

Jones, B., Atkinson, L., Blasco, D., Brink, K. and Smith, S. (1988). The asymmetricdistribution of chlorophyll associated with a coastal upwelling center. ContinentalShelf Research 8, 1155–1170.

Jones, M. B. and Epifanio, C. E. (1995). Settlement of crab megalopae in southernDelaware Bay: A time series analysis. Bulletin of Marine Science 57, 918.

Joyeux, J.-C. (1998). Spatial and temporal entry patterns of fish larvae into NorthCarolina estuaries: Comparisons between one pelagic and two demersal species.Estuarine, Coastal and Shelf Science 47, 731–752.

Kaestner, A. (1980).‘‘Invertebrate Zoology. Vol III. Crustacea’’. Krieger, New York.Katz, C. H., Cobb, J. S. and Spaulding, M. (1994). Larval behaviour, hydrodynamictransport and potential oVshore-to-inshore recruitment in the American lobsterHomarus americanus. Marine Ecology Progress Series 103, 265–273.

Kelly, P., Sulkin, S. D. and van Heukelem, W. F. (1982). A dispersal model for larvaeof the deep sea red crab Geryon quinquedens based upon behavioural regulation ofvertical migration in the hatching stage. Marine Biology 72, 35–43.

Kingsford, M. J., Leis, J. M., Shanks, A. L., Lindeman, K. C., Morgan, S. G. andPineda, J. (2002). Sensory environments, larval abilities and local self-recruitment.Bulletin of Marine Science 70, 309–340.

Klinck, J., O’Brien, J. and Svendsen, H. (1981). A simple model of fjord and coastalcirculation interaction. Journal of Physical Oceanography 11, 1612–1626.

Knight-Jones, E. W. and Morgan, E. (1966). Responses of marine animals to changesin hydrostatic pressure. Oceanography and Marine Biology Annual Review 4,267–299.

Knight-Jones, E. W. and Qasim, S. Z. (1967). Responses of Crustacea to changes inhydrostatic pressure. In ‘‘Proceedings of the Symposium on Crustacea. MarineBiological Association, India. III’’, pp. 1132–1150.

Knowlton, N. and Keller, B. D. (1986). Larvae which fall short of their potential:Highly localized recruitment in an alpheid shrimp with extended larval recruit-ment. Bulletin of Marine Science 39, 213–223.

Kuwahara, A., Wada, Y. and Hamanaka, Y. (1987). Distribution and transport of aprawn Penaeus japonicus postlarvae. Nippon Suisan Gakkaisho 53, 1561–1566.

Lampert, W. (1989). The adaptive significance of diel vertical migration of zooplank-ton. Functional Ecology 3, 21–27.


Lampert, W. (1993). Ultimate causes of diel vertical migration of zooplankton: Newevidence for the predator-avoidance hypothesis. In ‘‘Diel Vertical Migration ofZooplankton. Proceedings of an International Symposium Held at Lelystad, TheNetherlands’’ (J. Ringelberg, ed.), pp. 79–88. E. Schweizerbart’sche Verlagsbuch-handlung, Stuttgart.

Laprise, R. and Dodson, J. J. (1989). Ontogeny and importance of tidal verticalmigrations in the retention of larval smelt Osmerus mordax in a well-mixed estuary.Marine Ecology Progress Series 55, 101–111.

Latz, M. and Forward, R. B., Jr. (1977). The eVect of salinity upon phototaxis andgeotaxis in a larval crustacean. Biological Bulletin 153, 163–179.

Leaman, K., Johns, E. and Rossby, T. (1989). The average distribution of volumetransport and potential vorticity with temperature at three sections across the GulfStream. Journal of Physical Oceanography 19, 36–51.

Lee, T., Atkinson, L. and Legiskis, R. (1981). Observations of a Gulf Stream frontaleddy on the Georgia continental shelf, April 1977. Deep-Sea Research 28A,347–378.

Lee, T., Yoder, J. and Atkinson, L. (1991). Gulf Stream frontal eddy influence onproductivity of the southeast U.S. continental shelf. Journal of Physical Oceanog-raphy 96, 22191–22205.

Lentz, S. (1992). The surface boundary layer in coastal upwelling regions. Journal ofPhysical Oceanography 22, 1517–1539.

Lentz, S. (1994). Current dynamics over the northern California inner shelf. Journalof Physical Oceanography 24, 2461–2478.

Levin, L. A. (1990). A review of methods for labeling and tracking marine inverte-brate larvae. Ophelia 32, 115–144.

Levin, L. A., Huggett, D., Myers, P., Bridges, T. and Weaver, J. (1993). Rare-earthtagging methods for the study of larval dispersal by marine-invertebrates. Limnol-ogy and Oceanography 38, 346–360.

Lindley, J. A. (1986). Vertical distributions of decapod crustacean larvae and pelagicpost-larvae over Great Sole Bank (Celtic Sea) in June 1983. Marine Biology 90,545–549.

Lindley, J. A. (1987). Continuous plankton records: The geographical distributionand seasonal cycles of decapod crustacean larvae and pelagic post-larvae in theNorth-Eastern Atlantic Ocean and the North Sea, 1981–3. Journal of the MarineBiological Association of the United Kingdom 67, 145–167.

Lindley, J. A., Williams, R. and Conway, D. V. P. (1994). Variability in dry weightand vertical distributions of decapod larvae in the Irish Sea and North Sea duringthe spring. Marine Biology 120, 385–395.

Lipcius, R. N., Olmi, E. J., III and Van Montfrans, J. (1990). Planktonic availability,molt stage and settlement of blue crab postlarvae. Marine Ecology Progress Series58, 235–242.

Little, K. T. and Epifanio, C. E. (1991). Mechanism for the reinvasion of an estuaryby two species of brachyuran megalopae. Marine Ecology Progress Series 68,235–242.

Lough, R. G. (1976). Larval dynamics of the Dungeness crab, Cancer magister, oVthe central Oregon coast, 1970–71. Fishery Bulletin US 74, 353–375.

Luckenbach, M. W. and Orth, R. J. (1992). Swimming velocities and behaviour ofblue crab (Callinectes sapidus Rathbun) megalopae in still and flowing water.Estuaries 15, 186–192.

Mackas, D. L. (1992). Seasonal cycles of zooplankton oV southwestern British Colum-bia: 1979–89. Canadian Journal of Fisheries and Aquatic Sciences 49, 903–921.


Mackas, D. L., Kieser, R., Saunders, M., Yelland, D. R., Brown, R. M. and Moore,D. F. (1997). Aggregation of euphausiids and Pacific hake (Merluccius productus)along the outer continental shelf oV Vancouver Island. Canadian Journal of Fish-eries and Aquatic Sciences 54, 2080–2096.

Mair, J. M., Watkins, J. L. and Williamson, D. I. (1982). Factors aVectingthe immigration of postlarval penaeid shrimp into a Mexican lagoon system.Oceanologica Acta 5(2) no. sp., 339–345.

Mann, K. H. and Lazier, J. R. N. (1996).‘‘Dynamics of Marine Ecosystems: Bio-logical-Physical Interactions in the Oceans’’. Blackwell Scientific, Boston.

McConauhga, J. R. (1988). Export and reinvasion of larvae as regulators of estuarinedecapod populations. American Fisheries Society Symposium 3, 90–103.

McConnaughey, R. A. and Sulkin, S. D. (1984). Measuring the eVects ofthermoclines on the vetical migration of larvae of Callinectes sapidus (Brachyura,Portunidae) in the laboratory. Marine Biology 81, 139–145.

Macdonald, J. D., Pike, R. B. and Williamson, D. I. (1957). Larvae of the Britishspecies of Diogenes, Pagurus, Anapagurus and Lithodes (Crustacea, Decapoda).Proceedings of the Zoological Society of London 128, 209–257.

Mense, D. J. and Wenner, E. L. (1989). Distribution and abundance of early lifehistory stages of the blue crab, Callinectes sapidus, in tidal marsh creeks nearCharleston, South Carolina. Estuaries 12, 157–168.

Metaxas, A. (2001). Behaviour in flow: Perspectives on the distribution and disper-sion of meroplanktonic larvae in the water column. Canadian Journal of Fisheriesand Aquatic Sciences 58, 86–98.

Metcalf, K. S. and Lipcius, R. N. (1992). Relationship of habitat and spatial scalewith physiological state and settlement of blue crab postlarvae in Chesapeake Bay.Marine Ecology Progress Series 82, 143–150.

Metcalf, K. S., van Montfrans, J., Lipcius, R. N. and Orth, R. J. (1995). Settlementindices for blue crab megalopae in the York River, Virginia: Temporal relation-ships and statistical eYciency. Bulletin of Marine Science 57, 781–792.

Mileikovsky, S. A. (1973). Speed of active movement of pelagic larvae of marinebottom invertebrates and their ability to regulate their vertical position. MarineBiology 23, 11–17.

Morgan, S. G. (1987). Morphological and behavioural antipredatory adaptations ofdecapod zoeae. Oecologia 73, 393–400.

Morgan, S. G. (1995). Life and death in the plankton: Larval mortality and adapta-tion. In ‘‘Ecology of Marine Invertebrate Larvae’’ (L. McEdward, ed.),pp. 279–321. CRC Press, Boca Raton, FL.

Morgan, S. G. and Christy, J. H. (1994). Plasticity, constraint and optimality inreproductive timing. Ecology 75, 2185–2203.

Morgan, S. G., Zimmer-Faust, R. K., Heck, K. L., Jr. and Coen, L. D. (1996).Population regulation of blue crabs Callinectes sapidus in the northern Gulf ofMexico: Postlarval supply. Marine Ecology Progress Series 133, 73–88.

Moser, S. M. and Macintosh, D. J. (2001). Diurnal and lunar patterns of larvalrecruitment of brachyura into a mangrove estuary system in Ranong Province,Thailand. Marine Biology 138, 827–841.

Naylor, E. and Isaac, J. (1973). Behavioural significance of pressure responses inmegalopa larvae of Callinectes sapidus and Macropipus sp. Marine Behaviour andPhysiology 1, 341–350.

Niiler, P. and Richardson, W. (1973). Seasonal variability of the Florida Current.Journal of Marine Research 31, 144–167.


Nunes, R. and Simpson, J. (1985). Axial convergence in a well-mixed estuary.Estuarine, Coastal and Shelf Science 20, 637–649.

O’Donnell, J., Marmorino, G. and Trump, C. (1998). Convergence and downwellingat a river plume front. Journal of Physical Oceanography 28, 1481–1495.

Okubo, A. (1994). The role of diVusion and related physical processes in dispersaland recruitment of marine populations. In ‘‘The Bio-Physics of Marine LarvalDispersal’’ (P. W. Sammarco and M. L. Heron, eds.), pp. 5–32. AmericanGeophysical Union, Washington, DC.

Olmi, E. J., III (1994). Vertical migration of blue crab Callinectes sapidus megalopae:Implications for transport in estuaries. Marine Ecology Progress Series 113, 39–54.

Olmi, E. J., III (1995). Ingress of blue crab megalopae in the York River, Virginia,1987–1989. Bulletin of Marine Science 57, 753–780.

Open University (1991).‘‘Waves, Tides and Shallow Water Processes’’. Pergamon,Oxford.

Orensanz, J. M. and Jamieson, G. S. (1998). The assessment and management ofspatially structures stocks: an overview of the North Pacific Symposium on Inver-tebrate Stock Assessment and Management. Canadian Special Publication onFisheries and Aquatic Sciences 125, pp. 441–459.

Ott, F. S. and Forward, R. B., Jr. (1976). The eVect of temperature on phototaxis andgeotaxis by larvae of the crab Rhithropanopeus harrisii (Gould). Journal of Experi-mental Marine Biology and Ecology 23, 97–107.

Palmer, J. D. (1995). ‘‘The Biological Rhythms and Clocks of Intertidal Animals.’’Oxford University Press, Oxford.

Parker, B. (1991). The relative importance of the various non-linear mechanisms in awide range of tidal interactions (review). In ‘‘Tidal Hydrodynamics’’ (B. Parker,ed.), pp. 237–268. Wiley, New York.

Paula, J., Dray, T. and Queiroga, H. (2001). Interaction of oVshore and inshoreprocesses controling settlement of brachyuran megalopae in Saco mangrovecreek, Inhaca Island (South Mozambique). Marine Ecology Progress Series 215,251–260.

Pearce, A. F. and Phillips, B. F. (1994). Oceanic processes, puerulus sttlement andrecruitment of the western rock lobster Panulirus cygnus. In ‘‘The Bio-Physics ofMarine Larval Dispersal’’ (P. W. Sammarco and M. L. Heron, eds.), pp. 279–303.American Geophysical Union, Wasington, DC.

Pearcy, W. (1992).‘‘Ocean Ecology of Pacific Northwest Salmonids’’. University ofWashington Press, Seattle.

Pechenik, J. A. (1999). On the advantages and disadvantages of larval stages in benthicmarine invertebrate life cycles.Marine Ecology Progress Series 177, 269–297.

Peliz, A. and Fiuza, A. (1999). Temporal and spatial variability of CZCS-derivedphytoplankton pigment concentrations oV the western Iberian Peninsula. Inter-national Journal of Remote Sensing 20, 1363–1403.

Penn, J. W. (1975). The influence of tidal cycles on the distributional pathwayof Penaeus latisulcatus Kishinouye in Shark Bay, Western Australia. AustralianJournal of Marine and Freshwater Research 26, 93–102.

Pereira, F., Pereira, R. and Queiroga, H. (2000). Flux of decapod larvae and juvenilesat a station in the lower Canal de Mira (Ria de Aveiro, Portugal) during one lunarmonth. Invertebrate Reproduction and Development 38, 183–206.

Phillips, B. F. (1981). The circulation of the Southeastern Indian Ocean and theplanktonic life cycle of the western rock lobster. Oceanography and Marine BiologyAnnual Review 19, 11–39.


Phillips, B. F. and McWilliam, P. S. (1986). The pelagic phase of rock lobsterdevelopment. Canadian Journal of Fisheries and Aquatic Sciences 43, 2153–2163.

Phillips, B. F. and Olsen, L. (1975). Swimming behaviour of the puerulus larvae ofthe western rock lobster. Australian Journal of Marine and Freshwater Research 26,415–417.

Phillips, B. F. and Pearce, A. F. (1997). Spiny lobster recruitment oV WesternAustralia. Bulletin of Marine Science 61, 21–41.

Phillips, B. F., Rimmer, D. W. and Reid, D. D. (1978). Ecological investigations ofthe late-stage phyllosoma and puerulus larvae of the western rock lobster Panuliruslongipes cygnus. Marine Biology 48, 347–357.

Phillips, B. F., Brown, P. A., Rimmer, D. W. and Reid, D. D. (1979). Distributionand dispersal of the phyllosoma larvae of the Western Rock Lobster, Panuliruscygnus, in the South-eastern Indian Ocean. Australian Journal of Marine andFreshwater Research 30, 773–783.

Phillips, B. F., Brown, P. A., Rimmer, D. W. and Braine, S. J. (1981). Description,distribution and abundance of late larval stages of the Scyllaridae (Slipper lobsters)in the South-east Indian Ocean. Australian Journal of Marine and FreshwaterResearch 32, 417–437.

Pinel-Alloul, B. (1995). Spatial heterogeneity as a multiscale characteristic of zoo-plankton community. Hydrobiologia 300/301, 17–42.

Pollock, D. E. (1995). Evolution of life-history patterns in three genera of spinylobsters. Bulletin of Marine Science 57, 516–526.

Pringle, J. D. (1986). California spiny lobster (Panulirus interruptus) larval retentionand recruitment: A review and synthesis. Canadian Journal of Fisheries and AquaticSciences 43, 2142–2152.

Pritchard, D. W. (1951). The physical hydrography of estuaries and some applica-tions to biological problems. In ‘‘Transactions of the 16th North American Wild-life Conference’’, American wildlife Institute, Washinton, DC. pp. 368–376.

Provenzano, A. J., McConaugha, J. R., Phillips, K. B., Johnson, D. F. and Clark, J.(1983). Vertical distribution of first stage larvae of the blue crab, Callinectessapidus, at the mouth of Chesapeake Bay. Estuarine Coastal and Shelf Science16, 489–499.

Queiroga, H. (1996). Distribution and drift of the crab Carcinus maenas (L.) (Dec-apoda, Portunidae) larvae over the continental shelf oV northern Portugal in April1991. Journal of Plankton Research 18, 1981–2000.

Queiroga, H. (1998). Vertical migration and selective tidal stream transport in themegalopa of the crab Carcinus maenas. Hydrobiologia 375/376, 137–149.

Queiroga, H. (2003). Wind forcing of crab megalopae recruitment to an estuary (Riade Aveiro) in the northern Portuguese upwelling system. Invertebrate Reproductionand Development 43, 47–54.

Queiroga, H., Costlow, J. D., Jr. and Moreira, M. H. (1994). Larval abundancepatterns of Carcinus maenas (Decapoda, Brachyura) in Canal de Mira (Ria deAveiro, Portugal). Marine Ecology Progress Series 111, 63–72.

Queiroga, H., Costlow, J. D., Jr. and Moreira, M. H. (1997). Vertical migration ofthe crab Carcinus maenas first zoea in an estuary: Implications for tidal streamtransport. Marine Ecology Progress Series 149, 121–132.

Queiroga, H., Moksnes, P.-O. and Meireles, S. (2002). Vertical migration behaviourin the larvae of the shore crab, Carcinus maenas (L.), from a microtidal system(Gullmarsfjord, Sweden). Marine Ecology Progress Series 237, 195–207.

Quinlan, J. A., Blanton, B. O., Miller, T. J. and Werner, F. E. (1999). From spawninggrounds to the estuary: Using linked individual-based and hydrodynamic models


to interpret patterns and processes in the oceanic phase of Atlantic menhadenBrevoortia tyrannus life history. Fisheries Oceanography 8(Suppl. 2), 224–246.

Rabalais, N. N., Burditt, Jr, F. R., Coen, L. D., Cole, B. E., Eleuterius, C., Heck,K. L., Jr., McTigue, T. A., Morgan, S. G., Perry, H. M., Truesdale, F. M.,Zimmer-Faust, R. and Zimmerman, R. J. (1995). Settlement of Callinectes sapidusmegalopae on artificial collectors in four Gulf of Mexico estuaries. Bulletin ofMarine Science 57, 855–876.

Rice, A. L. (1964). Observations on the eVects of changes of hydrostatic pressure onthe behaviour of some marine animals. Journal of the Marine Biological Associationof the United Kingdom 44, 163–175.

Rice, A. L. (1966). The orientation of the pressure responses of some marine crust-acea. In ‘‘Proceedings of the Symposium on Crustacea. Marine Biological Associ-ation of India’’, pp. 1124–1131.

Rice, A. L. and Ingle, R. W. (1975). The larval development of Carcinus maenas (L.)and C. mediterraneus Czerniavsky (Crustacea, Brachyura, Portunidae) reared inthe laboratory. Bulletin of the British Museum of Natural History (Zool.) 28,103–119.

Richards, S. A., Possingham, H. P. and Noye, B. J. (1995). Larval dispersion along astraight coast with tidal currents: Complex distribution patterns from a simplemodel. Marine Ecology Progress Series 122, 59–71.

Rimmer, D. W. and Phillips, B. F. (1979). Diurnal migration and vertical distributionof phyllosoma larvae of the western rock lobster Panulirus cygnus. Marine Biology54, 109–124.

Ritz, D. A. (1972). Behavioural responses to light of the newly hatched phyllosomalarvae of Panulirus longipes cygnus George (Crustacea: Decapoda: Palinuridae).Journal of Experimental Marine Biology and Ecology 10, 105–114.

Roberts, M. H., Jr. (1971). Larval development of Pagurus longicarpus Say reared inthe laboratory. III. Behavioural responses to salinity discontinuities. BiologicalBulletin 140, 489–501.

Rogers, B. D., Shaw, R. F., Herke, W. H. and Blanchet, R. H. (1993). Recruitment ofpost-larval and juvenile brown shrimp (Penaeus aztecus Ives) from oVshore toestuarine waters of the northwestern Gulf of Mexico. Estuarine Coastal and ShelfScience 36, 377–394.

Rothlisberg, P. C. (1982). Vertical migration and its eVect on dispersal of penaeidshrimp larvae in the Gulf of Carpentaria, Australia. Fishery Bulletin US 80,541–554.

Rothlisberg, P. C. and Miller, C. B. (1983). Factors aVecting the distribution,abundance and survival of Pandalus jordani (Decapoda, Pandalidae) larvae oVthe Oregon coast. Fishery Bulletin US 81, 455–472.

Rothlisberg, P. C., Church, J. A. and Forbes, A. M. G. (1983a). Modelling theadvection of vertically migrating shrimp larvae. Journal of Marine Research 41,511–538.

Rothlisberg, P. C., Church, J. A. and Forbes, A. M. G. (1983b). Modelling theadvection of vertically migrating shrimp larvae. Journal of Marine Research 41,511–538.

Rothlisberg, P. C., Church, J. A. and Fandry, C. B. (1995). A mechanism for near-shore concentration and estuarine recruitment of post-larval Peneus plebejus Hess(Decapoda, Peneidae). Estuarine Coastal and Shelf Science 40, 115–138.

Roughgarden, J., Pennington, J. T., Stoner, D., Alexander, S. and Miller, K. (1991).Collisions of upwelling fronts with the intertidal zone: The cause of recruitmentpulses in barnacle populations of central California. Acta Oecologica 12, 35–51.


Rumrill, S. S. (1990). Natural mortality of marine invertebrate larvae. Ophelia 32,163–198.

Sammarco, P. W. and Heron, M. L. (eds.) (1994). ‘‘The Bio-Physics of Marine LarvalDispersal’’. American Geophysical Union, Washington, DC.

Sandifer, P. A. (1975). The role of pelagic larvae in recruitment to populations ofadult decapod crustaceans in the York River estuary and adjacent lower Chesa-peake Bay. Estuarine Coastal and Shelf Science 3, 269–279.

Santucci, R. (1926a). Lo sviluppo e l’ecologia post-embrionali dello ‘‘Scampo’’(Nephrops norvegicus (L.) ) nel Tirreno e nei mari nordici.Memoria Reale ComitatoTalassografico Italiano 125, 1–30.

Santucci, R. (1926b). Lo stadio natante e la prima forma post-natante dell’Aragosta(Palinurus vulgaris Latr.) del Mediterraneo. Memoria Reale Comitato Talassogra-fico Italiano 127, 1–11.

Scheltema, R. S. (1975). Relationship of larval dispersal, gene-flow and naturalselection to geographic variation of benthic invertebrates in estuaries andalong coastal regions. In ‘‘Estuarine Research’’ (L. E. Cronin, ed.), pp. 373–391.Academic Press, New York.

Scheltema, R. S. (1986). On dispersal and planktonic larvae of benthic invertebrates:An ecletic overview and summary of problems. Bulletin of Marine Science 39,290–322.

Schembri, P. J. (1982). Locomotion, feeding, grooming and the behavioural re-sponses to gravity, light and hydrostatic pressure in the stage I zoea larvaeof Ebalia tuberosa (Crustacea, Decapoda, Leucosiidae). Marine Biology 72,125–134.

Schone, H. (1975). Orientation in space: Animals. General introduction. In ‘‘MarineEcology’’ (O. Kinne, ed.), pp. 499–554. Wiley, London.

Schott, F., T, N.-L. and ZantoV, R. (1988). Variability of structure and transport ofthe Florida Current in the period range of days to seasonal. Journal of PhysicalOceanography 18, 1209–1230.

Schwing, F., Oey, L.-Y. and Blanton, J. (1988). Evidence for non-local forcing alongthe southeastern United States during a transitional wind regime. Journal ofGeophysical Research 93, 8221–8228.

Scrope-Howe, S. and Jones, D. A. (1986). The vertical distribution of zooplankton inthe western Irish Sea. Estuarine, Coastal and Shelf Science 22, 785–802.

Sedberry, G. and Loefer, J. (2001). Satellite telemetry tracking of swordfish, Xiphiasgladius, oV the eastern United States. Marine Biology 139, 355–360.

Serfling, S. A. and Ford, R. F. (1975). Ecological studies of the puerulus larval stageof the California spiny lobster, Panulirus interruptus. Fishery Bull. U. S. Nat.Ocean. Atmos. Admin. 73, 360–377.

Shanks, A. L. (1983). Surface slicks associated with tidally forced internal waves maytransport pelagic larvae of benthic invertebrates and fishes shoreward. MarineEcology Progress Series 13, 311–315.

Shanks, A. L. (1985). Behavioural basis of internal-wave-induced shoreward trans-port of megalopae of the crab Pachygrapsus crassipes. Marine Ecology ProgressSeries 24, 289–295.

Shanks, A. L. (1986). Vertical migration and cross-shelf dispersal of larval Cancerspp. and Randallia ornata (Crustacea: Brachyura) oV the coast of southernCalifornia. Marine Biology 92, 189–199.

Shanks, A. L. (1995). Mechanisms of cross-shelf dispersal of larval invertebratesand fish. In ‘‘Ecology of Marine Invertebrate Larvae’’ (L. McEdward, ed.),pp. 323–367. CRC Press, Boca Raton, FL.


Shanks, A. L. (1988). Further support for the hypothesis that internal waves cancause shoreward transport of larval invertebrates and fishes. Fisheries Bulletin 86,703–714.

Shanks, A. L., Largier, J. and Brink, L. (2000). Demonstration of the onshoretransport of larval invertebrates by the shoreward movement of an upwellingfront. Limnology and Oceanography 45, 230–236.

Shanks, A. L., Grantham, B. A. and Carr, M. H. (2003). Propagule dispersaldistance and the size and spacing of marine reserves. Ecological Applications13(Suppl. 1), S159–S169.

Simpson, J. and Hunter, J. (1974). Fronts in the Irish Sea. Nature 250, 404–408.Singer, J., Atkinson, L., Blanton, J. and Yoder, J. (1983). Cape Romain and theCharleston Bump: Historical and recent hydrographic observations. Journal ofGeophisical Research 88, 4685–4697.

Smith, C. L., Hill, A. E., Foreman, M. G. G. and Pena, M. A. (2001). Horizontaltransport of marine organisms from interactions between diel vertical migrationand tidal currents oV the west coast of Vancouver. Canadian Journal of Fisheriesand Aquatic Sciences 58, 736–748.

Smyth, P. O. (1980). Callinectes (Decapoda: Portunidae) larvae in the middleAtlantic Bight, 1975–77. Fishery Bulletin 78, 251–265.

Sousa, F. M. and Fiuza, A. F. G. (1989). Recurrence of upwelling filamentsoV northern Portugal as revealed by satellite imagery. In ‘‘4th AVHRR DataUsers’ Meeting’’ (G. Bridge and M. Pooley, eds.), pp. 219–223. EUMETSAT,Darmstadt.

Sponaugle, S., Cowen, R. K., Sanks, A., Morgan, S. G., Leis, J. M., Pineda, J.,Boehlert, G. W., Kingsford, M. J., Lindeman, K. C., Grimes, C. and Munro, J. L.(2002). Predicting self-recruitment in marine populations: Biophysical correlatesand mechanisms. Buletin of Marrine Science 70, 341–375.

Stevens, I., Hamann, M., Johnson, J. and Fiuza, A. F. G. (2000). Comparisonsbetween a fine resolution model and observations in the Iberian shelf-slope region.Journal of Marine Systems 26, 53–74.

Stommel, H. (1948). The westward intensification of wind-driven ocean currents.Transactions of the American Geophysical Union 29, 202–206.

Strathmann, R. R. (1982). Selection for retention or export of larvae in estuaries.In ‘‘Estuarine Comparisons’’ (V. S. Kennedy, ed.), pp. 521–536. Academic Press,New York.

Strathmann, R. R. (1993). Hypotheses on the origins of marine larvae. Annual Reviewof Ecology and Systematics 24, 89–117.

Strathmann, R. R., Hughes, T. P., Kuris, A. M., Lindeman, K. C., Morgan, S. G. P.J. M. and Warner, R. R. (2002). Evolution of local recruitment and its conse-quences for marine populations. Bulletin of Marine Sciences 70, 377–396.

Stull R. B. (ed.) (1988). ‘‘An Introduction to Boundary Layer Meteorology’’. KluwerAcademic Press, Dordrecht.

Sulkin, S. D. (1973). Depth regulation of crab larvae in the absence of light. Journalof Experimental Marine Biology and Ecology 13, 73–82.

Sulkin, S. D. (1975). The influence of light in the depth regulation of crab larvae.Biological Bulletin 148, 333–343.

Sulkin, S. D. (1984). Behavioural basis of depth regulation in the larvae ofbrachyuran crabs. Marine Ecology Progress Series 15, 181–205.

Sulkin, S. D. (1986). Application of laboratory studies of larval behaviour to fisheriesproblems. Canadian Journal of Fisheries and Aquatic Sciences 43, 2184–2188.


Sulkin, S. D. and van Heukelem, W. (1982). Larval recruitment in the crabCallinectes sapidus Rathbun: An amendment to the concept of larval retentionin estuaries. In ‘‘Estuarine Comparisons’’ (V. S. Kennedy, ed.), pp. 459–475.Academic Press, New York.

Sulkin, S. D., Phillips, I. and van Heukelem, W. (1979). On the locomotory rhythm ofbrachyuran crab larvae and its significance in vertical migration. Marine EcologyProgress Series 1, 331–335.

Sulkin, S. D., van Heukelem, W., Kelly, P. and van Heukelem, L. (1980). Thebehavioural basis of larval recruitment in the crab Callinectes sapidus Rathbun:A laboratory investigation of ontogenic changes in geotaxis and barokinesis.Biological Bulletin 159, 402–417.

Sulkin, S. D., van Heukelem, W. F. and Kelly, P. (1983). Behavioural basis of depthregulation in hatching and post-larval stages of the mud crab Eurypanopeusdepressus. Marine Ecology Progress Series 11, 157–164.

Svane, I. B. and Young, C. M. (1989). The ecology and behaviour of ascidian larvae.Oceanography and Marine Biology: An Annual Review 27, 45–90.

Swearer, S. E., Shima, J. S., Hellberg, M. E., Thorrold, S. R., Jones, G. P., Robertson,D. R.,Morgan, S.G., Selkoe, K. A., Ruiz, G.M. andWarner, R. R. (2002). Evidenceof self-recruitment in demersal marine populations. Bulletin of Marine Science 70,251–271.

Tankersley, R. A. and Forward, R. B., Jr. (1994). Endogenous swimming rhythms inestuarine crab megalopae: Implications for flood-tide transport. Marine Biology118, 415–423.

Tankersley, R. A., McKelvey, L. M. and Forward, R. B., Jr. (1995). Responses ofestuarine crab megalopae to pressure, salinity and light: Implications for flood-tidetransport. Marine Biology 122, 391–400.

Thorrold, S. R., Jones, G. P., Hellberg, M. E., Burton, R. S., Swearer, S. E., Neigel,J. E., Morgan, S. G. and Warner, R. R. (2002). Quantifying larval retention andconnectivity in marine populations with artificial and natural markers. Bulletin ofMarine Science 70, 291–308.

Thorson, G. (1964). Light as an ecological factor in the dispersal and settlement oflarvae of marine bottom invertebrates. Ophelia 1, 167–208.

Trowbridge, J. and Lentz, S. (1991). Asymmetric behaviour of an oceanic bottomboundary layer above a sloping bottom. Journal of Physical Oceanography 21,1171–1185.

Udekem d’Acoz, C. d’ (1999). ‘‘Inventaire et distribution des crustaces decapodes del’Atlantique nord-orientale, de la Mediterranee et des eaux douces continentalesadjacentes au nord de 25 8N’’. Museum National d’Histoire Naturelle, Service duPatrimoine Naturel, Paris.

van Montfrans, J., Peery, C. A. and Orth, R. J. (1990). Daily, monthly and annualsettlement patterns by Callinectes sapidus and Neopanope sayi megalopae onartificial collectors deployed in the York River, Virginia: 1985–1988. Bulletin ofMarine Science 46, 214–229.

vanMontfrans, J., Epifanio, C. E., Knott, D.M., Lipcius, R. N.,Mense, D. J., Metcalf,K. S., Olmi, E. J.,, III, Orth, R. J., Posey,M.H.,Wenner, E. L. andWest, T. L. (1995).Settlement of blue crab postlarvae in western North Atlantic estuaries. Bulletin ofMarine Science 57, 834–854.

Warner, R. R. and Cowen, R. C. (2001). Local retention of production in marinepopulations: Evidence, mechanisms and consequences. Bulletin of Marine Science70, 245–249.


Welch, J. M. and Forward, R. B., Jr. (2001). Flood tide transport of blue crab,Callinectes sapidus, postlarvae: Behavioural responses to salinity and turbulence.Marine Biology 139, 911–918.

Welch, J. M., Forward, R. B., Jr. and Howd, P. A. (1999). Behavioural responses ofblue crab Callinectes sapidus larvae to turbulence: implications for selective tidalstream transport. Marine Ecology Progress Series 179, 135–143.

Werner, F. E., Blanton, B. O., Quinlan, J. A. and Luettich, R. A. (1999). Physicaloceanography of the North Carolina continental shelf during the fall and winterseasons: Implications to the transport of larval menhaden. Fisheries Oceanography8, 7–21.

Wheeler, D. E. and Epifanio, C. E. (1978). Behavioural response to hydro-static pressure in larvae of two species of xanthid crabs. Marine Biology 46,167–174.

Williams, A. B. (1971). A ten-year study of meroplankton in North Carolina estuar-ies: Annual occurrence of some brachyuran development stages. Chesapeake Sci-ence 12, 53–61.

Williamson, D. I. (1982). Larval morphology and diversity. In ‘‘Embryology,Morphology and Genetics’’ (L. G. Abele, ed.), pp. 43–110. Academic Press, NewYork.

Wing, S. R., Botsford, L. W., Largier, J. L. and Morgan, L. E. (1995a). Spatialstructure of relaxation events and crab settlement in the northern Californiaupwelling system. Marine Ecology Progress Series 128, 199–211.

Wing, S. R., Largier, J. L., Botsford, L. W. and Quinn, J. F. (1995b). Settlement andtransport of benthic invertebrates in an intermittent upwelling region. Limnologyand Oceanography 40, 316–329.

Wooster, W. S., Bakun, A. and McLain, D. R. (1976). The seasonal upwelling cyclealong the eastern boundary of the North Atlantic. Journal of Marine Research 34,131–141.

Yanovsky, A., Hickey, B. and Munchow, A. (2001). The impact of variable inflow onthe dynamics of a coastal buoyant plume. Journal of Geophysical Research 106,19809–19824.

Yeung, C. and McGowan, M. F. (1991). DiVerences in inshore-oVshore and verticaldistribution of phyllosoma larvae of Panulirus, Scyllarus and Scyllarides in theFlorida Keys in May–June, 1989. Bulletin of Marine Science 49, 699–714.

Yoder, J., Atkinson, L., Lee, T., Kim, H. and McClain, C. (1981). Role of GulfStream frontal eddies in forming phytoplankton patches on the outer southeasternshelf. Limnology and Oceanography 26, 1103–1110.

Young, C. M. (1995). Behaviour and locomotion during the dispersal phase of larvallife. In ‘‘Ecology of Marine Invertebrate Larvae’’ (L. McEdward, ed.), pp. 249–277.CRC Press, Boca Raton, FL.

Young, C. M. and Chia, F.-S. (1987). Abundance and distribution of pelagic larvaeas influenced by predation, behaviour, and hydrographic factors. In ‘‘Reproduc-tion of marine invertebrates’’ (A. C. Giese, J. S. Pearse and V. V. Pearse, eds.),pp. 385–463. Blackwell Scientific, Palo Alto, CA. The Boxwood Press, PacificGrove, CA.

Young, P. C. and Carpenter, S. M. (1977). Recruitment of postlarval penaeid prawnsto nursery areas in Moreton Bay, Queensland. Australian Journal of Marine andFreshwater Research 28, 745–773.

Zaret, T. M. and SuVern, J. S. (1976). Vertical migration in zooplankton as apredator avoidance mechanism. Limnology and Oceanography 21, 804–813.


Zeng, C. and Naylor, E. (1996a). Endogenous tidal rhythms of vertical migration infield collected zoea-1 larvae of the shore crab Carcinus maenas: Implications forebb tide oVshore dispersal. Marine Ecology Progress Series 132, 71–82.

Zeng, C. and Naylor, E. (1996b). Heritability of circatidal vertical migration rhythmsin zoea larvae of the crab Carcinus maenas (L.). Journal of Experimental MarineBiology and Ecology 202, 239–257.

Zeng, C. and Naylor, E. (1996c). Occurrence in coastal waters and endogenous tidalswimming rhythms of late megalopae of the shore crab Carcinus maenas: Implica-tions for onshore recruitment. Marine Ecology Progress Series 136, 69–79.

Zeng, C. and Naylor, E. (1996d). Synchronization of endogenous tidal verticalmigration 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 moultingrhythms in early juvenile shore crabs Carcinus maenas: Adaptations to a highintertidal habitat. Marine Biology 128, 299–305.


Marine Biofouling on Fish Farms andIts 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 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 216

2. Nature and Extent of Problem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 218

2.1. Detrimental eVects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 219

2.2. Beneficial eVects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 221

2.3. Economic consequences . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 222

3. The Fouling Community of Fish-Cage Netting. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223

3.1. Mediation by physical, chemical, and biological factors . . . . . . . . . . . . . . . . . . . . . . . . 223

3.2. Community development. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224

3.3. Fouling taxa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 226

4. Antifouling Technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 231

4.1. Toxic antifouling paints and materials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 233

4.2. Legislation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235

4.3. Nontoxic ‘‘alternative’’ antifoulants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 238

4.4. Biological control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 240

5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 241


References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 243

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


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 particu-

lar importance, because of their cosmopolitan distribution and opportunistic

nature, include the blue mussel Mytilus edulis and the ascidian Ciona intesti-

nalis. 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 ‘‘foul-

release’’ 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 mari-

ners, 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 oiland 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

216 R. A. BRAITHWAITE AND L. A. MCEVOY

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 mar-

iculture 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 linerepresents production; broken line represents value (data provided by the Food andAgricultural Organisation of the United Nations).

MARINE BIOFOULING ON FISH FARMS AND ITS REMEDIATION 217

aquaculture and currently dominate global production. As a consequence,

most studies have been undertaken in Asia, particularly in China. Unfortu-

nately, 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 macro-

algal 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 m�2 have been recorded following

only 21 days of immersion (Dubost et al., 1996). Measurements of 2.2 kg

m�2 (Cronin et al., 1999), 4.5 kg m�2 (Lee et al., 1985), and 7.8 kg m�2

(Hodson et al., 2000) have also been reported, as have dry mass measure-

ments of 0.82 kg m�2 (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


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), caus-

ing 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;

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

Country Author(s)

n/aa Huguenin and Huguenin (1982)b

Australia 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)

Canada Enright et al. (1983, 1993)c; Cote et al. (1993, 1994)c;Enright (1993); Claereboudt et al. (1994)c

Chile Romo et al. (2001)d

France Dubost et al. (1996)b; Nehr et al. (1996); Gonzalez (1998)e

Ireland Deady et al. (1995)Malaysia Chua and Teng (1977); Cheah and Chua (1979)Norway Kvenseth (1996); Solberg et al. (2002);

Kvenseth and Andreassen (2003)Palau Hasse (1974)c

Scotland His et al. (1996)c

Singapore Lee et al. (1985)UK Milne (1970, 1975a,b); Ross et al. (2002)c

USA Hidu et al. (1981); Ahlgren (1998)c; Parsons et al. (2002)c

Venezuela Lodeiros and Himmelman (1996, 2000)c

aConcerned with several countries.bRecorded in a freshwater/low salinity environment.cAssociated with shellfish farming.dAssociated with seaweed farming.eRecorded from a land-based system.


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 eutrophi-

cation (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’’ organ-

isms. 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 impli-

cations 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),


partly because of the need for specialist staV to carry out highly labour-

intensive 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 shell-

fish, 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, detrimen-

tal 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


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 indir-

ectly 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 phyto-

plankton 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 expen-

sive 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 conse-

quences 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 pro-

duced 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.


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 three-

dimensional surface structure (Kohler et al., 1999). Fouling of surfaces by

abiotic and biotic substances has molecular, microbial, and macro-

organismal levels of organisation (Rittschof, 2000), with the composition

of the fouling community depending primarily on qualitative and quantita-

tive 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 proper-

ties, 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 macro-

algal fouling (Hodson et al., 2000). Furthermore, fouling does not, necessar-

ily, 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


to their light requirements, although it has been shown that, conversely,

invertebrate fouling can increase with depth (Cronin et al., 1999). Accord-

ingly, 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 signifi-

cantly 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 macro-

molecules 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 microfoul-

ers, 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 cm�2 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 m�2 week�1 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


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 resist-

ance to a treated surface as it gradually loses its toxicity (Harris and Forbes,

1946). Accordingly, diVerent genera have demonstrated diVerential re-

sistance 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 diVer-ence (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 heteroge-

neous 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).


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 foul-

ing fish cage netting following only 2 months of immersion, and representa-

tives 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 con-

trast, 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 aquacul-

ture industry cannot be accurately made; fouling significance is linked to

abundance and not merely presence.

The blue musselMytilus edulis (Figure 2), and sea squirts, particularlyCiona

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 aquacul-

ture 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


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 ap-

pears 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 photo-

synthetic 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, macro-

algae 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 byMytilus edulis andCiona 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


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

Number ofTaxa Recorded

Number ofidentified Genera

Number ofidentified Species

Genera/SpeciesRecorded MoreThan Oncea

AlgaeBacillariophyceae 20 18 4 Biddulphia sp.

Campylodiscus sp.Fragilaria sp.

Cyanophyceae 4 4 1 Oscillatoria sp.Chrysophyceae 1 1 0Chlorophyceae 17 14 4 Bryopsis sp.

Cladophora sp.Enteromorpha sp. (5)Ulothrix sp.Ulva nematoideaUlva spp. (3)

Phaeophyceae 10 9 7 Ectocarpus siliculosusEctocarpus sp. (4)Scytosiphon lomentaria

Rhodophyceae 24 15 18 Brongniartella australisCeramium tasmanicumGracilaria sp.Polysiphonia abscissa

Protozoa 4 4 1 Vorticella sp.Porifera 4 3 4Cnidaria 1 1 1ScyphozoaHydrozoa 6 3 5 Obelia australis (3)

Tubularia larynx (4)Anthozoa 5 5 5

228

R.A.BRAITHWAITEAND

L.A.M

CEVOY

PlatyhelminthesTurbellaria 1 1 1

Bryozoa 7 5 5 Bugula neritina (3)Scrupocellaria bertholetti (3)

AnnelidaPolychaeta 10 9 6

CrustaceaCirripedia 6 2 5 Balanus sp.Malacostraca 21 18 13 Caprella sp.

ArthropodaPycnogonida 1 1 1

MolluscaProsobranch 9 6 7 Littorina spp.Gastropoda Thais spp.Opisthobranch 7 4 7 Dendronotus frondosusGastropodaBivalvia 24 16 17 Hiatella arctica

Hiatella spp.Modiolus sp.Mytilus edulis (9)Perna viridisPinctada sp.

Echinodermata 1 1 0HemichordataAscidiacea 11 9 7 Ascidiella aspersa (3)

Botrylloides sp.Ciona intestinalis (4)Molgula ficus

aRecorded twice unless otherwise indicated in brackets.

MARINEBIO

FOULING

ON

FISH

FARMSAND

ITSREMEDIATIO

N229

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

Figure 2 Biofouling of finfish cage netting: (A) waterline fouling by the green algalgenus Enteromorpha at a Scottish salmon farm, which has developed on a copper-based coating that gives a the red colour to the netting; (B) heavy fouling of a netimmersed at a sea trout farm on the Danish east coast, where the mussels have severelyobstructed the free flow of water through material; the mussels average 5–10 mm inlength, and the mesh is approximately 20 mm from knot to knot (photograph courtesyG. Nicholl).


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 Sarcotha-

lia crispata (Romo et al., 2001). In pond systems, the genera GiVordia (now

Hincksia) and Ectocarpus have been recorded as important fouling organ-

isms (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 inverte-

brates 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 algalbiofouling may be the deposition of calcium carbonate (CaCO3), which can

constitute 56% of the fouling dry weight (Heath et al., 1996). Thus, eVortshave also been made to control calcification by using phosphonate inhibi-

tors. 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 formula-

tions, 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


manipulation of the pheromonal cues that help determine fouling are also

being investigated (Clare and Matsumura, 2000; Holmstrom 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 anti-

foulants (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


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 immer-

sion, 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 on-

growing 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 devel-

opment, 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


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 eVectiveagainst a wide range of organisms (Houghton, 1984), and it has been sug-

gested that leaching rates for copper of 22 mg cm�2 day�1 and 16 mg cm�2

day�1 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 aquacul-

ture industry include, for example, Aquasafe W and Flexgard VI-II Water-

base 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 copper-

nickel 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,


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 antifoul-

ing paints under the Pest Control Products Act (PCP), combines net anti-

foulants 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 registra-

tion 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, presum-

ably, 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


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 Healthand Safety Executive for use in UK aquaculture

Product Name Ingredient(s) Marketing Company

VC 17M-EP Coppera International Coatings LtdAmercoat 70ESP Copper Metaa Ameron BVVC 17M Copper Metaa International Coatings LtdAqua-Guard Cuprous Oxide Steen-Hansen Maling ASAqua-Net Cuprous Oxide Steen-Hansen Maling ASAquasafe W Cuprous Oxide GJOCO A/SBoatguard Cuprous Oxide International Coatings LtdBottomkote Cuprous Oxidea International Coatings LtdCarmypaint SV-881 Cuprous Oxide Carmyco S.A.

Paints-Varnishes-AdhesivesCopper Net Cuprous Oxide Steen-Hansen Maling ASFlexgard VI-IIWaterbase Preservative

Cuprous Oxide Aquatess Ltd(manufactured by FlexabarAquatech Corporation)

Hempel’s NetAntifouling 715GB

Cuprous Oxide Hempel Paints Ltd

Net-Guard Cuprous Oxide Steen-Hansen Maling ASNetrex AF Cuprous Oxide Tulloch EnterprisesFlexgard VI Cuprous Oxide and

ChlorothalonilaFlexabar AquatechCorporation

Hempel’s AntifoulingRennot 7150

Cuprous Oxide andDichlofluanidb

Hempel Paints Ltd

aApproval for sale and advertisement has expired. Product retains short-term approval for

storage and use.bApproval for advertisement, sale, supply and storage has expired. Product approved short

term, for disposal purposes only.


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. Triorganotin-

containing 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 volun-

tary ban on its use by the National Farmers Union for Scotland in the

autumn of 1986 (Balls, 1987). Likewise, according to ORTEPA (the Orga-

notin 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 indus-

try, between 1977 and 1983, $147 million (Alzieu, 2000). It was also demon-

strated 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).


The toxicity of copper to marine organisms is well documented (Mance,

1987). For example, concentrations as low as 2.5 mg L�1, lower than

some environmentally recorded levels, have been shown to aVect, signifi-cantly, germination in Baltic Sea Fucus vesiculosus (Andersson and

Kautsky, 1996). Likewise, 2.5 mg L�1 can adversely aVect bivalve molluscs

(Mance, 1987). The UK environmental quality standard (EQS) for dissolved

copper in sea water is 5 mg L�1 (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 L�1 (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 copper-

containing 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 antifoul-

ing 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 sub-

stances 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’’


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 m�1 (Andersson et al., 1999) and are commonly quoted

as ameasure 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 perform-

ance (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 ofmaterial 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 concen-

trate 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 formula-

tion 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 alterna-

tives 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 cur-

rently work with slower craft and, thus, it would appear likely that they are


also unsuitable for use in stationary aquaculture facilities. They are also

relatively expensive, and their eYcacy has not been satisfactorily proven

(Kohler 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.). Simi-

larly, 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, develop-

ing 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 con-

trol’’; 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


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 Oreo-

chromis 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 technolo-

gical 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. Consider-

ation 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 prob-

lem to today’s aquaculturist. Maintenance is almost continually necessi-

tated, 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.


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 de-

veloping 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 indus-

try, 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 cur-

rent technology are needed, particularly in light of the relative expense of

foul-release systems. Research into systems that work under low hydro-

dynamic 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


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 Competi-

tive and Sustainable Growth Programme (GRD2-2000-30252). We would

also like to thank Sue Marrs and Alan Southward as well as three an-

onymous referees for their helpful comments on an earlier version of the

manuscript.

REFERENCES

Ahlgren, M. O. (1998). Consumption and assimilation of salmon net pen foulingdebris by the red sea cucumber Parastichopus califomicus: Implications for poly-culture. Journal of the World Aquaculture Society 29, 133–139.

Alberte, R. S., Snyder, S., Zahuranec, B. J. and Whetstone, M. (1992). Biofoulingresearch needs for the United States navy: Program history and goals. Biofouling.6, 91–95.

Alzieu, C. (1996). Biological eVects of tributyltin on marine organisms. In ‘‘Tributyltin:Case Study of an Environmental Contaminant’’ (S. J. de Mora, ed.), pp. 167–211.Cambridge University Press, Cambridge.

Alzieu, C. (2000). Environmental impact of TBT: The French experience. Science ofthe Total Environment 258, 99–102.

Anonymous (1999). Intersleek 700: A new fouling control innovation fromInternational. The Naval Architect, pp. 42.

Andersen, R. J., Luu, H. A., Chen, D. Z. X., Holmes, C. F. B., Kent, M. L., LeBlanc,F., Taylor, F. J. R. and Williams, D. E. (1993). Chemical and biological evidencelinks microcystins to salmon netpen liver disease. Toxicon 31, 1315–1323.

Anderson, C. (2002). TBT-Free in 2003: What are the options? Proceedings of theConference on Ship Design and Operation for Environmental Sustainability, April2002. pp. 17–19. Royal Institute of Naval Architects, London.


Andersson, S. and Kautsky, L. (1996). Copper eVects on reproductive stages of BalticSea Fucus vesiculosus. Marine Biology 125, 171–176.

Andersson, M., Berntsson, K., Jonsson, P. and Gatenholm, P. (1999). Microtexturedsurfaces: Towards macrofouling resistant coatings. Biofouling 14, 167–178.

Angel, D. L. and Spanier, E. (2002). An application of artificial reefs to reduceorganic enrichment caused by net-cage fish farming: Preliminary results. ICESJournal of Marine Science 59, S324–S329.

Balls, P. W. (1987). Tributyltin (TBT) in the waters of a Scottish sea loch arising fromthe use of antifoulant treated netting by salmon farmers. Aquaculture 65, 227–237.

Barton, J. R. (1997). Environment, sustainability and regulation in commercialaquaculture: The case of Chilean salmonid production. Geoforum 28, 313–328.

Basheer, C., Tan, K. S. and Lee, H. K. (2002). Organotin and Irgarol-1051 contamin-ation in Singapore coastal waters. Marine Pollution Bulletin 44, 697–703.

Bech, M. (2002). A survey of imposex in muricids from 1996 to 2000 and identifica-tion of optimal indicators of tributyltin contamination along the east coast ofPhuket Island, Thailand. Marine Pollution Bulletin 44, 887–896.

Bell, G. M. and Chadwick, J. (1994). Regulatory controls on biocides in the UnitedKingdom and restrictions on the use of triorganotin-containing antifoulingproducts. International Biodeterioration and Biodegradation 34, 375–386.

Bennett, R. F. (1996). Industrial manufacture and applications of tributyltincompounds. In ‘‘Tributyltin: Case Study of an Environmental Contaminant’’(S. J. de Mora, ed.), pp. 21–61. Cambridge University Press, Cambridge.

Benson, P. H., Brining, D. L. and Perrin, D. W. (1973). Marine fouling and itsprevention. Marine Technology January, 30–37.

Berk, S. G., Mitchell, R., Bobbie, R. J., Nickels, J. S. and White, D. C. (2001).Microfouling on metal surfaces exposed to seawater. International Biodeteriorationand Biodegradation 48, 167–175.

Beveridge, M. (1996). Cage Aquaculture. The University Press, Cambridge.Bingaman, W. W. and Willingham, G. L. (1994). The changing regulatory environ-ment: EPA registration of a new marine antifoulant active ingredient. InternationalBiodeterioration and Biodegradation 34, 387–399.

Black, E., Gowen, R., Rosenthal, H., Roth, E., Stechy, D. and Taylor, F. J. R.(1997). The costs of eutrophication from salmon farming: Implications forpolicy—a comment. Journal of Environmental Management 50, 105–109.

Blair, A., Campbell, R. and Grant, P. T. (1982). A submersible fish cage that can berotated on the surface to remove biofouling and for other purposes. Aquaculture29, 177–184.

Brandini, F. P., da Silva, E. T., Pellizzari, F. M., Fonseca, A. L. O. and Fernandes,L. F. (2001). Production and biomass accumulation of periphytic diatoms growingon glass slides during a 1-year cycle in a subtropical estuarine environment (Bay ofParanagua, Southern Brazil). Marine Biology 138, 163–171.

Burridge, L. E., Haya, K., Zitko, V. and Waddy, S. (1999). The lethality of Salmosan(azamethiphos) to American lobster (Homarus americanus) larvae, postlarvae, andadults. Ecotoxicology and Environmental Safety 43, 165–169.

Burridge, L. E., Haya, K., Page, F. H., Waddy, S. L., Zitko, V. and Wade, J. (2000a).The lethality of the cypermethrin formulation Excis� to larval and post-larvalstages of the American lobster (Homarus americanus). Aquaculture 182, 37–47.

Burridge, L. E., Haya, K., Waddy, S. L. and Wade, J. (2000b). The lethality of anti-sea lice formulations Salmosan� (azamethiphos) and Excis� (cypermethrin) tostage IV and adult lobsters (Homarus americanus) during repeated short-termexposures. Aquaculture 182, 27–35.


Callow, M. E. (1990). Ship fouling: Problems and solutions. Chemistry and Industry5, 123–127.

Callow, M. E. (1996). Ship-fouling: The problem and method of control. Biodeter-ioration Abstracts 10, 411–421.

Callow, M. E. and Callow, J. A. (1998). Attachment of zoospores of the fouling algaEnteromorpha in the presence of zosteric acid. Biofouling 13, 87–95.

Callow, M. E. and Callow, J. A. (2002). Marine biofouling: A sticky problem.Biologist 49, 10–14.

Callow, M. E., Jennings, A. R., Brennan, A. B., Seegert, C. E., Gibson, A., Wilson,L., Feinberg, A., Baney, R. and Callow, J. A. (2002). Microtopographic cues forsettlement of zoospores of the green fouling alga Enteromorpha. Biofouling 18,237–245.

Champ, M. A. (2000). A review of organotin regulatory strategies, pending actions,related costs and benefits. Science of the Total Environment 258, 21–71.

Cheah, S. H. and Chua, T. E. (1979). A preliminary study of the tropicalmarine fouling organisms on floating net cages. Malayan Nature Journal 33,39–48.

Chua, T. and Teng, S. K. (1977). Floating fish pens for rearing fishes in coastalwaters, reservoirs and mining pools in Malaysia. Fisheries Bulletin of the Ministryof Agriculture of Malaysia 20, 1–36.

Claereboudt, M. R., Bureau, D., Cote, J. and Himmelman, J. H. (1994). Foulingdevelopment and its eVect on the growth of juvenile giant scallops (Placopectenmagellanicus) in suspended culture. Aquaculture 121, 327–342.

Clare, A. S. (1995). Natural ways to banish barnacles. New Scientist. 145, 38–41.Clare, A. S. (1996). Marine natural product antifoulants: Status and potential.Biofouling 9, 211–229.

Clare, A. S. (1998). Towards nontoxic antifouling. Journal of Marine Biotechnology6, 3–6.

Clare, A. S. and Matsumura, K. (2000). Nature and perception of barnacle settle-ment pheremones. Biofouling 15, 57–71.

Clare, A. S., Rittschof, D., Gerhart, D. J. and Maki, J. S. (1992). Molecular ap-proaches to nontoxic antifouling. Invertebrate Reproduction and Development 22,67–76.

Clarkson, N. and Evans, L. V. (1995). Further studies investigating a potentialnon-leaching biocide using the marine fouling diatom Amphora coVeaeformis.Biofouling 9, 17–30.

Cote, J., Himmelman, J. H., Claereboudt, M. and Bonardelli, J. C. (1993). Influenceof density and depth on the growth of juvenile sea scallops (Placopecten magella-nicus) in suspended culture. Canadian Journal of Fisheries and Aquatic Sciences 50,1857–1869.

Cote, J., Himmelman, J. H. and Claereboudt, M. R. (1994). Separating eVects oflimited food and space on growth of the giant scallop Placopecten magellanicus insuspended culture. Marine Ecology Progress Series 106, 85–91.

Cowling, M. J., Hodgkiess, T., Parr, A. C. S., Smith, M. J. and Marrs, S. J. (2000).An alternative approach to antifouling based on analogues of natural processes.Science of the Total Environment 258, 129–137.

Cronin, E. R., Cheshire, A. C., Clarke, S. M. and Melville, A. J. (1999). An investi-gation into the composition, biomass and oxygen budget of the fouling communityon a tuna aquaculture farm. Biofouling 13, 279–299.

Daniel, G. F. and Chamberlain, A. H. L. (1981). Copper immobilisation in foulingdiatoms. Botanica Marina 24, 229–243.


Davies, I. M., Bailey, S. K. and Harding, M. J. C. (1998). Tributyltin inputs to theNorth Sea from shipping activities, and potential risk of biological eVects. ICESJournal of Marine Science 55, 34–43.

Davis, A. and Williamson, P. (1996). Marine biofouling: A sticky problem. NERCNews April, 25–27.

de la Court, F. H. (1988). The minimum leaching rate of some toxins from antifoul-ing paints required to prevent settlement of fouling organisms. In ‘‘Proceedings ofthe 7th International Biodeterioration Symposium’’ (D. R. Houghton, R. N. Smithand H. O. W. Eggins, eds.), pp. 6–11. September 1987, Cambridge. ElsevierApplied Science, London.

de Mora, S. J. (1996). The tributyltin debate: Ocean transportation versus seafoodharvesting. In ‘‘Tributyltin: Case Study of an Environmental Contaminant’’ (S. J.de Mora, ed.), pp. 1–20. Cambridge University Press, Cambridge.

de Nys, R., Steinberg, P. D., Willemsen, P., Dworjanyn, S. A., Gabelish, C. L. andKing, R. J. (1995). Broad-spectrum eVects of secondary metabolites from the redalga Delisea pulchra in antifouling assays. Biofouling 8, 259–271.

de Sousa, G., Delescluse, C., Pralavorio, M., Perichaud, M., Avon, M., Lafaurie,M. and Rahmani, R. (1998). Toxic eVects of several types of antifoulingpaints in human and rat hepatic or epidermal cells. Toxicology Letters 96/97,41–46.

Deady, S., Varian, S. J. A. and Fives, J. M. (1995). The use of cleaner-fish to controlsea lice on two Irish salmon (Salmo salar) farms with particular reference to wrassebehavior in salmon cages. Aquaculture 131, 73–90.

Delort, E., Watanabe, N., Etoh, H., Sakata, K. and Ceccaldi, H. J. (2000). Analysisof initial fouling process in coastal environment: EVects of settlement, attachment,and metamorphosis promoters. Marine Biotechnology 2, 224–230.

Dempsey, M. J. (1981). Colonisation of antifouling paints by marine bacteria.Botanica Marina 24, 185–191.

Donovan, D. A., Bingham, B. L., From, M., Fleisch, A. F. and Loomis, E. S. (2003).EVects of barnacle encrustation on the swimming behaviour, energetics, morpho-metry, and drag coeYcient of the scallop Chlamys hastata. Journal of the MarineBiological Association of the United Kingdom 83, 813–819.

Douglas-Helders, G. M., Tan, C., Carson, J. and Nowak, B. F. (2003). EVectsof copper-based antifouling treatment on the presence of Neoparamoebapemaquidensis Page, 1987 on nets and gills of reared Atlantic salmon (Salmosalar). Aquaculture 221, 13–22.

Dubost, N., Masson, G. and Moreteau, J. C. (1996). Temperate freshwater foulingon floating net cages: Method of evaluation, model and composition. Aquaculture143, 303–318.

Eckman, J. E., Thistle, D., Burnett, W. C., Paterson, G. L. J., Robertson, C. Y. andLambshead, P. J. D. (2001). Performance of cages as large animal-exclusiondevices in the deep sea. Journal of Marine Research 59, 79–95.

Enright, C. (1993). Control of fouling in bivalve aquaculture. World Aquaculture 24,44–46.

Enright, C., Krailo, D., Staples, L., Smith, M., Vaughan, C., Ward, P., Gaul, P. andBorgese, G. (1983). Biological control of fouling algae in oyster aquaculture.Journal of Shellfish Research 3, 41–44.

Enright, C., Elner, R. W., Griswold, A. and Borgese, E. M. (1993). Evaluation ofcrabs as control agents for biofouling in suspended culture of European oysters.World Aquaculture 24, 49–51.


Ernst, W., Jackman, P., Doe, K., Page, F., Julien, G., Mackay, K. and Sutherland, T.(2001). Dispersion and toxicity to non-target aquatic organisms of pesticides used totreat sea lice on salmon in net pen enclosures.Marine Pollution Bulletin 42, 433–444.

Evans, C. J. and Smith, P. J. (1975). Organotin-based antifouling systems. Journal ofthe Oil and Colour Chemists’ Association 58, 160–168.

Evans, L. V. (1981). Marine algae and fouling—a review, with particular reference toship-fouling. Botanica Marina 24, 167–171.

Evans, L. V. and Christie, A. O. (1970). Studies on the ship-fouling algaEnteromorpha: I. Aspects of the fine-structure and biochemistry of swimmingand newly settled zoospores. Annals of Botany 34, 451–466.

Evans, L. V. and Clarkson, N. (1993). Antifouling strategies in the marine environ-ment. Journal of Applied Bacteriology 74, S119–S124.

Evans, S. M. (1999). TBT or not TBT?: That is question. Biofouling 14, 117–129.Evans, S. M. (2000). Response to the letter from Nichols. Marine Pollution Bulletin40, 713–715.

Evans, S. M., Leksono, T. and McKinnell, P. D. (1995). Tributyltin pollution: Adiminishing problem following legislation limiting the use of TBT-based anti-fouling paints. Marine Pollution Bulletin 30, 14–21.

Finlay, J. A., Callow, M. E., Schultz, M. P., Swain, G. W. and Callow, J. A. (2002).Adhesion strength of settled spores of the green alga Enteromorpha. Biofouling 18,251–256.

Folke, C., Kautsky, N. and Troell, M. (1997). Salmon farming in context: Responseto Black et al. Journal of Environmental Management 50, 95–103.

Food and Agriculture Organisation of the United Nations (2002). The State ofWorld Fisheries and Aquaculture (SOFIA), p. 150. FAO, Rome.

Fletcher, R. L. (1988). Brief review of the role of marine algae in biodeterioration.International Biodeterioration 24, 141–152.

Fletcher, R. L. (1995). Epiphytism and fouling in Gracilaria cultivation—an over-view. Journal of Applied Phycology 7, 325–333.

Furtado, S. E. J. and Fletcher, R. L. (1987). Test procedures for marine antifoulingpaints. In ‘‘Preservatives in the Food, Pharmaceutical and Environmental Indus-tries’’ (R. G. Board, M. C. Allwood and J. G. Banks, eds.), pp. 145–163. BlackwellScientific Publications, Oxford.

Gonzalez, L. (1998). The life cycle of Hysterothylacium aduncum (Nematoda:Anisakidae) in Chilean marine farms. Aquaculture 162, 173–186.

Gosling, E. (1992). The mussel Mytilus: Ecology, physiology, genetics and culture. In‘‘Developments in Aquaculture and Fisheries Science’’ (E. Gosling, ed.), pp. 1–20.Elsevier, Amsterdam.

Granmo, A., Ekelund, R., Sneli, J. A., Berggren, M. and Svavarsson, J. (2002).EVects of antifouling paint components (TBTO, copper and triazine) on theearly development of embryos in cod (Gadus morhua L.). Marine Pollution Bulletin44, 1142–1148.

Gucinski, H., Baier, R. E., Meyer, A. E., Fornalik, M. S. and King, R. W. (1984).Surface microlayer properties aVecting drag phenomena in seawater. In ‘‘Proceed-ings of the 6th International Congress onMarine Corrosion and Fouling’’, August,pp. 5–18. Athens, Greece.

Gunn, N., Woods, D. C., Blunn, G., Fletcher, R. L. and Jones, E. B. G. (1987).Problems associated with marine microbial fouling. In ‘‘Microbial Problems in theOVshore Oil Industry’’ (E. C. Hill, J. L. Shennan and R. J. Watkinson, eds.),pp. 175–200. Wiley, London.


Hall, L. W. and Anderson, R. D. (1999). A deterministic ecological risk assessmentfor copper in European saltwater environments. Marine Pollution Bulletin 38,207–218.

Harris, J. E. and Forbes, W. A. D. (1946). Under-water paints and the fouling ofships, with reference to the work of the marine corrosion sub-committee of theIron and Steel Institute and the Admiralty corrosion committee, Paper 9. Instituteof Naval Architects, London.

Haslbeck, E. G., Kavanagh, C. J., Shin, H. W., Banta, W. C., Song, P. and Loeb,G. I. (1996). Minimum eVective release rate of antifoulants (2): Measurement ofthe eVect of TBT and zosteric acid on hard fouling. Biofouling 10, 175–186.

Hasse, J. (1974). Utilisation of rabbit fishes (Signidae) in tropical oyster culture. TheProgressive Fish-Culturist 36, 160–162.

Hattori, T. and Shizuri, Y. (1996). A screening method for antifouling substancesusing spores of the fouling macroalga Ulva conglobata Kjellman. Fisheries Science62, 955–958.

Hayden, H. S., Blomster, J., Maggs, C. A., Silva, P. C., Stanhope, M. J. andWaaland, J. R. (2003). Linnaeus was right all along: Ulva and Enteromorphaare not distinct genera. European Journal of Phycology 38, 277–294.

Heath, C. R., Leadbeater, B. S. C. and Callow, M. E. (1996). The control ofcalcification of antifouling paints in hard waters using a phosphonate inhibitor.Biofouling 9, 317–325.

Hellio, C., de la Broise, D., Dufosse, L., Le Gal, Y. and Bourgougnon, N. (2001).Inhibition of marine bacteria by extracts of macroalgae: Potential use for environ-mentally friendly antifouling paints. Marine Environmental Research 52, 231–247.

Hendey, N. I. (1951). Littoral diatoms of Chichester harbour with special reference tofouling. Journal of the Royal Microscopical Society 71, 1–86.

Henrikson, A. A. and Pawlik, J. R. (1995). A new antifouling assay method: Resultsfrom field experiments using extracts of four marine organisms. Journal ofExperimental Marine Biology and Ecology 194, 157–165.

Hidu, H., Conary, C. C. and Chapman, S. R. (1981). Suspended culture of oysters:Biological fouling control. Aquaculture 22, 189–192.

His, E., Beiras, R., Quiniou, F., Parr, A. C. S., Smith, M. J., Cowling, M. J. andHodgkiess, T. (1996). The non-toxic eVects of a novel antifouling material onoyster culture. Water Research 30, 2822–2825.

Hodson, S. L. and Burke, C. (1994). Microfouling of salmon-cage netting: A prelim-inary investigation. Biofouling 8, 93–105.

Hodson, S. L., Burke, C. M. and Lewis, T. E. (1995). In situ quantification of fish-cage fouling by underwater photography and image analysis. Biofouling 9,145–151.

Hodson, S. L., Lewis, T. E. and Burke, C. M. (1997). Biofouling of fish-cage netting:EYcacy and problems of in situ cleaning. Aquaculture 152, 77–90.

Hodson, S. L., Burke, C. M. and Bissett, A. P. (2000). Biofouling of fish-cage netting:The Ycacy of a silicone coating and the eVect of netting colour. Aquaculture 184,277–290.

Holm, E. R., Nedved, B. T., Phillips, N., Deangelis, K. L., Hadfield, M. G. andSmith, C. M. (2000). Temporal and spatial variation in the fouling of siliconecoatings in Pearl Harbour, Hawaii. Biofouling 15, 95–107.

Holmstrom, C., Steinberg, P., Christov, V., Christie, G. and Kjelleberg, S. (2000).Bacteria immobilised in gels: Improved methodologies for antifouling and biocon-trol applications. Biofouling 15, 109–117.


Houghton, D. R. (1984). Toxicity testing of candidate antifouling paint testing. In‘‘Proceedings of the Symposium on Marine Biodeterioration’’ (J. D. Costlow andR. C. Tipper, eds.), pp. 255–258. Naval Institute Press, Annapolis, MD.

Houghton, D. R., Pearman, I. and Tierney, D. (1973). The eVect of water velocity onthe settlement of swarmers of the green alga Enteromorpha sp. In ‘‘Proceedings ofthe 3rd International Congress on Marine Corrosion and Fouling’’, October 1972.Gaithersberg, MD.

Howard, K. T. and Kingwell, S. J. (1975). Marine fish farming: Development ofholding facilities (with particular reference to work by the white fish authority onthe Scottish West coast). Oceanology International 75, 183–190.

Huguenin, J. E. and Huguenin, S. S. (1982). Biofouling resistant shellfish trays.Journal of Shellfish Research 2, 41–46.

Huse, I., Bjordal, A., Ferno, A. and Furevik, D. (1990). The eVect of shading in penrearing of Atlantic salmon (Salmo salar). Aquacultural Engineering 9, 235–244.

Ingram, B. A., Gooley, G. J., Mckinnon, L. J. and de Silva, S. S. (2000). Aquacul-ture-agriculture systems integration: An Australian prospective. Fisheries Manage-ment and Ecology 7, 33–43.

Judge, M. L. and Craig, S. F. (1997). Positive flow dependence in the initial coloniza-tion of a fouling community: Results from in situ water current manipulations.Journal of Experimental Marine Biology and Ecology 210, 209–222.

Kavanagh, C. J., Schultz, M. P., Swain, G. W., Stein, J., Truby, K. and Wood, C. D.(2001). Variation in adhesion strength of Balanus eburneus, Crassostrea virginicaand Hydroides dianthus to fouling-release coatings. Biofouling 17, 155–167.

Kuwa, M. (1984). Fouling organisms on floating cage of wire netting and the removalby Oplegnathus sp cultured with other marine fish. Bulletin of the Japanese Societyof Scientific Fisheries 50, 1635–1640.

Kvenseth, P. G. (1996). Large-scale use of wrasse to control sea lice and net fouling insalmon farms in Norway. In ‘‘Wrasse: Biology and Use in Aquaculture’’ (M. D. J.Sayer, J. W. Treasurer and M. J. Costello, eds.), pp. 196–203. Fishing News Books,Oxford.

Kvenseth, P. G. and Andreassen, J. (2003). Wrasse, sea lice and economy. In‘‘Cleanerfish’’ (A. M. Hjelme, ed.), pp. 27–30. Norsk Fiskeoppdrett A/S, Norway.

Kohler, J., Hansen, P. D. and Wahl, M. (1999). Colonisation patterns at the substra-tum-water interface: How does surface microtopography influence recruitmentpatterns of sessile organisms? Biofouling 14, 237–248.

Lai, H., Kessler, A. O. and Khoo, L. E. (1993). Biofouling and its possible modes ofcontrol at fish farms in Penang, Malaysia. Asian Fisheries Science 6, 99–116.

Lee, H. B., Lim, L. C. and Cheong, L. (1985). Observations on the use of antifoulingpaint in netcage fish farming in Singapore. Singapore Journal of Primary Industries13, 1–12.

Lesser, M. P., Shumway, S. E., Cucci, T. and Smith, J. (1992). Impact of foulingorganisms on mussel rope culture-interspecific competition for food among sus-pension-feeding invertebrates. Journal of Experimental Marine Biology andEcology 165, 91–102.

Lewis, A. G. and Metaxas, A. (1991). Concentrations of total dissolved copper in andnear a copper-treated salmon net pen. Aquaculture 99, 269–276.

Lewthwaite, J. C., Molland, A. F. and Thomas, K. W. (1985). An investigation intothe variation of ship skin frictional resistance with fouling. Transactions of the TheRoyal Institution of Naval Architects 127, 269–285.

Li, S. (1994). Fish culture in cages and pens. ‘‘Freshwater Fish Culture in China:Principles and Practice,’’ pp. 305–346. Elsevier, Amsterdam.


Lodeiros, C. J. and Himmelman, J. H. (1996). Influence of fouling on the growth andsurvival of the tropical scallop Euvola (Pecten) ziczac (L. 1758) in suspendedculture. Aquaculture Research 27, 749–756.

Lodeiros, C. J. M. and Himmelman, J. H. (2000). Identification of factors afectinggrowth and survival of the tropical scallop Euvola (Pecten) ziczac in the Golfo DeCariaco, Venezuela. Aquaculture 182, 91–114.

Lovegrove, T. (1979a). Anti-fouling paint in farm ponds. Fish Farming International9, 13–15, 39.

Lovegrove, T. (1979b). Control of fouling in farm cages. Fish Farming International6, 35–37.

Mallet, A. L. and Carver, C. E. (1991). An assessment of strategies for growingmussels in suspended culture. Journal of Shellfish Research 10, 471–477.

Mance, G. (1987). ‘‘Pollution Threat of Heavy Metals in Aquatic Environments’’.Elsevier Applied Science, New York.

Matthiessen, P., Reed, J. and Johnson, M. (1999). Sources and potential eVects ofcopper and zinc concentrations in the estuarine waters of Essex and SuVolk,United Kingdom. Marine Pollution Bulletin 38, 908–920.

Mckenzie, J. D. and Grigolava, I. V. (1996). The echinoderm surface and its role inpreventing microfouling. Biofouling 10, 261–272.

Meadows, P. S. and Campbell, J. I. (1995). ‘‘An Introduction to Marine Science’’.Blackie Academic and Professional, Glasgow.

Milne, P. H. (1970). Fish farming: A guide to the design and construction of netenclosures. Marine Research 1, 1–31.

Milne, P. H. (1975a). Fouling of marine cages—part one. Fish Farming International2, 15–19.

Milne, P. H. (1975b). Fouling of marine cages—part two: Further trials in Scottishlochs. Fish Farming International 2, 18–21.

Milne, P. H. (1991). Ablation and after: The law and the profits. In ‘‘Polymers in aMarine Environment’’ (R. Button, P. Yakimuik and K. Williams, eds.),pp. 139–145. London Marine Management (Holdings) Ltd, London.

Moring, J. R. and Moring, K. A. (1975). Succession of net biofouling material andits role in the diet of pen-cultured Chinook salmon. The Progressive Fish-Culturist37, 27–30.

Nehr, O., Blancheton, J. P. and Alliot, E. (1996). Development of an intensive culturesystem for sea bass (Dicentrarchus labrax) larvae in sea enclosures. Aquaculture142, 43–58.

Neushul, M., Foster, M. S., Coon, D. A., Woessner, J. W. and Harge, W. W. (1976).An in situ study of recruitment, growth and survival of subtidal marine algae:Techniques and preliminary results. Journal of Phycology. 12, 397–408.

Newkirk, G. (1996). Sustainable coastal production systems: A model for integratingaquaculture and fisheries under community management. Ocean and CoastalManagement 32, 69–83.

Norberg, J. (1999). Periphyton fouling as a marginal energy source in tropical tilapiacage farming. Aquaculture Research 30, 427–430.

Okamura, H., Watanabe, T., Aoyama, I. and Hasobe, M. (2002). Toxicity evaluationof new antifouling compounds using suspension-cultured fish cells. Chemosphere46, 945–951.

Paclibare, J. O., Evelyn, T. P. T., Albright, L. J. and Prosperiporta, L. (1994).Clearing of the kidney-disease bacterium Renibacterium salmoninarum fromseawater by the blue mussel Mytilus edulis, and the status of the mussel as areservoir of the bacterium. Diseases of Aquatic Organisms 18, 129–133.


Pantastico, J. B. and Baldia, J. P. (1981). An assessment of algal growth in net cagesin Laguna Lake. Fisheries Research Journal of the Philippines 6, 19–25.

Parsons, G. J., Shumway, S. E., Kuenstner, S. and Gryska, A. (2002). Polyculture ofsea scallops (Placopecten magellanicus) suspended from salmon cages. AquacultureInternational 10, 65–77.

Phillippi, A. L., O’Conner, N. J., Lewis, A. F. and Kim, Y. K. (2001). Surfaceflocking as a possible anti-biofoulant. Aquaculture 195, 225–238.

Prilutzky, A., Birkan, V. and Appelbaum, S. (1995). A self-cleaning device for outletscreens in fish rearing tanks. Aquacultural Engineering 14, 281–288.

Ranke, J. and JastorV, B. (2000). Multidimensional risk analysis of antifoulingbiocides. Environmental Science and Pollution Research 7, 105–114.

Reise, K., Gollasch, S. and WolV, W. J. (1999). Introduced marine species of theNorth Sea coasts. Helgolander Meeresuntersuchungen 52, 219–234.

Rittschof, D. (2000). Natural product antifoulants: One perspective on the challengesrelated to coatings development. Biofouling 15, 119–127.

Robinson, M. G., Hall, B. D. and Voltolina, D. (1985). Slime films on antifoulingpaints; short-term indicators of long-term eVectiveness. Journal of CoatingsTechnology 57, 35–41.

Romo, H., Alveal, K. and Werlinger, C. (2001). Growth of the commercial carra-geenophyte Sarcothalia crispata (Rhodophyta, Gigartinales) on suspended culturein central Chile. Journal of Applied Phycology 13, 229–234.

Ross, K. A., Thrope, J. P., Norton, T. A. and Brand, A. R. (2002). Fouling in scallopcultivation: Help or hinderence? Journal of Shellfish Research 21, 539–547.

Scott, C., Fletcher, R. L. andBremer,G. B. (1996). Observations on themechanisms ofattachment of some marine fouling blue-green algae. Biofouling 10, 161–173.

Shim,W. J., Kahng, S. H., Hong, S. H., Kim, N. S., Kim, S. K. and Shim, J. H. (2000).Imposex in the rock shell, Thais clavigera, as evidence of organotin contaminationin the marine environment of Korea. Marine Environmental Research 49, 435–451.

Short, J. W. and Thrower, F. P. (1986). Accumulation of butyltins in muscle tissue ofchinook salmon reared in sea pens treated with tri-n-butyltin. Marine PollutionBulletin 17, 542–545.

Short, J. W. and Thrower, F. P. (1987). Toxicity of tri-n-butyltin to Chinook salmon,Oncorhynchus tshawytscha, adapted to seawater. Aquaculture 61, 193–200.

Singer, I. L., Kohl, J. G. and Patterson, M. (2000). Mechanical aspects of siliconecoatings for hard foulant control. Biofouling 6, 301–309.

Solberg, C. B., Saethre, L. and Julshamn, K. (2002). The eVect of copper-treated netpens on farmed salmon (Salmo salar) and other marine organisms and sediments.Marine Pollution Bulletin 45, 126–132.

Southward, A. J. (1995). Occurrence in the English Channel of a warm-watercirripede Solidobalanus fallax. Journal of the Marine Biological Association of theUnited Kingdom 75, 199–210.

Stachowitsch, M., Kikinger, R., Herler, J., Zolda, P. and Geutebruck, E. (2002).OVshore oil platforms and fouling communities in the southern Arabian Gulf(Abu Dhabi). Marine Pollution Bulletin 44, 853–860.

Stein, J., Truby, K., Wood, C. D., Stein, J., Gardner, M., Swain, G., Kavanagh, C.,Kovach, B., Schultz, M., Wiebe, D., Holm, E., Montemarano, J., Wendt, D.,Smith, C. and Meyer, A. (2003a). Silicone foul release coatings: EVect of theinteraction of oil and coating functionalities on the magnitude of macrofoulingattachment strengths. Biofouling 19, 71–82.

Stein, J., Truby, K., Wood, C. D., Takemori, M., Vallance, M., Swain, G., Kavanagh,C., Kovach, B., Schultz, M., Wiebe, D., Holm, E., Montemarano, J., Wendt, D.,


Smith, C. and Meyer, A. (2003b). Structure-property relationships of siliconebiofouling-release coatings: EVect of silicone network architecture on pseudobar-nacle attachment strengths. Biofouling 19, 87–94.

Strandenes, S. P. (2000). The second order eVects on commercial shipping of restric-tions on the use of TBT. Science of the Total Environment 258, 111–117.

Tan, C. K. F., Nowak, B. F. and Hodson, S. L. (2002). Biofouling as a reservoir ofNeoparamoeba pemaquidensis (Page, 1970), the causative agent of amoebic gilldisease in Atlantic salmon. Aquaculture 210, 49–58.

Thomas, K. V., McHugh, M. and Waldock, M. (2002). Antifouling paint boosterbiocides in UK coastal waters: Inputs, occurrence and environmental fate. TheScience of the Total Environmental 293, 117–127.

Thompson, R. J. (1979). Fecundity and reproductive eVort of the blue mussel(Mytilus edulis), the sea urchin (Strongylocentrotus droebachiensis) and the snowcrab (Chionectes opilio) from populations in Nova Scotia and Newfoundland.Journal of the Fisheries Research Board of Canada 36, 955–964.

Todd, J. S., Zimmerman, R. C., Crews, P. and Alberte, R. S. (1993). The antifoulingactivity of natural and synthetic phenolic-acid sulfate esters. Phytochemistry 34,401–404.

Tsibouklis, J., Stone, M., Thorpe, A. A., Graham, P., Nevell, T. G. and Ewen, R. J.(2000). Inhibiting bacterial adhesion onto surfaces: The non-stick coatingapproach. International Journal of Adhesion and Adhesives 20, 91–96.

Tudor, M. (1999). Diurnal changes of dissolved oxygen in fouling land-based tanksfor rearing of sea bass. Aquacultural Engineering 19, 243–258.

Tuente, U., Piepenburg, D. and Spindler, M. (2002). Occurrence and settlement ofthe common shipworm Teredo navalis (Bivalvia: Teredinidae) in Bremerhavenharbours, Northern Germany. Helgoland Marine Research 56, 87–94.

Voulvoulis, N., Scrimshaw, M. D. and Lester, J. N. (1999). Alternative antifoulingbiocides. Applied Organometallic Chemistry 13, 135–143.

Waddy, S. L., Burridge, L. E., Hamilton, M. N., Mercer, S. M., Aiken, D. E. andHaya, K. (2002). Emamectin benzoate induces molting in American lobster,Homarus americanus. Canadian Journal of Fisheries and Aquatic Sciences 59,1096–1099.

Waite, M. E., Waldock, M. J., Thain, J. E., Smith, D. J. and Milton, S. M. (1991).Reductions in TBT concentrations in UK estuaries following legislation in 1986and 1987. Marine Environmental Research 32, 89–111.

Wigglesworth-Cooksey, B. and Cooksey, K. E. (1992). Can diatoms sense surfaces?State of our knowledge. Biofouling 5, 227–238.

Wilkerson, W. R., Seegert, C. A., Feinberg, A. W., Zhao, L. C., Callow, M. E.,Baney, R. and Brennan, A. B. (2001). Bioadhesion studies on microtexturedsiloxane elastomers. Polymer Preprints 42, 147–148.

Woods, D. C., Fletcher, R. L. and Jones, E. B. G. (1988). Microfouling filmcomposition, thickness and surface roughness on ship trial anifouling paints. In‘‘Proceedings of the 7th International Biodeterioration Symposium’’, September6–11 1987, Cambridge. Elsevier Applied Science, London.

Woods Hole Oceanographic Institution (1952). ‘‘Marine Fouling and itsPrevention’’. United States Naval Institute, Annapolis, MD.


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 Liege, B6, 4000 Liege, Belgium

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 254

2. Nature of Copepod Outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256

2.1. Nature of excretion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256

2.2. Nature of copepod particulate matter outfluxes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 258

3. Factors Controlling the Rate of Copepod Outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263

3.1. Factors controlling the rate of copepod dissolved matter excretion . . . . . . . . . . . . 264

3.2. Factors controlling the rate of copepod particulate matter outfluxes . . . . . . . . . . . 266

3.3. Relationships between the diVerent outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 268

4. Vertical Flux . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 269

4.1. Passive vertical flux. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 270

4.2. Vertical migration and active vertical flux . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 279

5. Role of Copepod Outfluxes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 280

5.1. Role of copepod dissolved matter outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 280

5.2. Role of copepod particulate matter outfluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 282

6. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 285


References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293


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 dis-

solved 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 pro-

duction. 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

254 C. FRANGOULIS ET AL.

closely linked, as nutrient and light availability drive the biogenic compon-

ents 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 charac-

teristics 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 nutri-

ents 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 prod-

ucts (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, dom-

inant mesozooplankters in the world ocean, in terms of both abundance

ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES 255

(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 ‘‘zoo-

plankton’’ 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 experi-

mental 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 prod-

ucts, 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 (NHþ4 ), is not certain (for crustaceans, see

Regnault, 1987). In the following, no distinction is made between the two

forms, and the chemical symbol NHþ4 is used for simplicity. The other


nitrogen-containing substances excreted by zooplankton are organic: urea

(e.g., Bamstedt, 1985; Miller, 1992; Conover and Gustavson, 1999) and

amino acids (e.g., Gardner and PaVenhofer, 1982; Regnault and Lagardere,

1983; Dam et al., 1993). Uric acid excretion seems to be exceptional

(Regnault, 1987, and references therein), and there is no evidence of excre-

tion 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 concen-

trations, 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 ex-

cretion (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 PaVenhofer, 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; Bamstedt, 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).


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 eco-

nomic 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; Cadee et al., 1992; Yoon et al.,

2001). DiVerent shapes have been identified for other zooplankters: rectangu-

lar (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,


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 (PaVenhofer and Knowles, 1979;

Harris, 1994; Uye and Kaname, 1994); however, this relationship is con-

sidered 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: olive-

green 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., Gonzalez

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 pellet�1) or per pellet volume (e.g., nanograms C mm�3), as a large range

of variation (more than one order of magnitude) is found among these data

(Table 1).


Table 1 Carbon, nitrogen and phosphorus content of fresh copepod faecal pellets. In studies with mixed copepod species, speciesdescribed are the most dominant

Faecal pellet producer

Food conditions(area, ifnatural foodconditions)

Faecal pellet composition

C N P Weight ratios

% DWngpel�1 pg mm�3 % DW

ngpel�1 pg mm�3 % DW C:N C:P N:P Source

Single copepod speciesAcartia clausi Coccolithophores

culture— 133–276 0.53–1.10* — 13–28 0.05–0.11* — — — — Honjo and

Roman, 1978Acartia clausi Natural food

(Woods Hole,Massachusetts)

— 96–187 0.38–0.75* — 15–38 0.06–0.15* — — — — Honjo andRoman, 1978

Acartia tonsa Thalassiosiraweissflogii culture

— — 0.17–2.50 — — 0.06–0.78 3.2–7.1 — — Butler andDam, 1994

Acartia tonsa Thalassiosiraweissflogii culture

— — 0.28 — — — — — — — Hansen et al.,1996a

Acartia tonsa Rhodomonasbaltica culture

— — 0.39 — — — — — — — Hansen et al.,1996a

Acartia tonsa Thalassiosira sp.and Isochrysisgalbana culture

— — — — — — — 10–16 — — Checkley andEnzeroth, 1985

Calanusfinmarchicus

Natural food(Barents Sea)

— — 0.05 — — 0.01 — 7.0 — — Gonzalez andSmetacek, 1994

Calanusglacialis

Natural food(NE Greenlandshelf)

— 377 0.05* — 22 <0.01* — — — — Daly, 1997

Calanushyperboreus

Natural food (NEGreenland shelf)

— 1450 0.04* — 125 <0.01* — 28.5 — — Daly, 1997

Calanuspacificus

Thalassiosiraweissflogii culture

— — — — — — — 7.5 — — Downs andLorenzen, 1985

Eucalanuspileatus

Rhizosolenia alataculture

— — — — — — — 14.8 — — PaVenhofer andKnowles, 1979

260

C.FRANGOULIS

ETAL.

Metridia longa Natural food (NEGreenland shelf)

— 1140 0.21* — 70 0.01* — — — — Daly, 1997

Pontellameadii

Natural food(GalvestonBay, Texas)

12.0 — — 2.7 — — — 4.8 — — Turner, 1979

Temora stylifera Hymenomonaselongata culture

— 154 0.43* — 18 0.05* — 8.3 — — Abou Debs, 1984

Temora spp. Thalassiosira sp.and Isochrysisgalbana culture

— — — — — — — 8–25 — — Checkley andEnzeroth, 1985

Mixed copepodsPseudocalanus

spp., Temora longicornisThalassiosira

weissflogii culture25.0 — — 3.0 — — — 7–9 — — Morales, 1987

Clausocalanusspp., Euchaetaspp., Orthona spp.,Oncaea mediterranea

Natural food (EastPacific OceanoV California)

29.6 — — 4.8 — — — 6.1 — — Small et al., 1983

Calanus finmarchicus,Oithona similis,Pseudocalanus elongatus,Temora longicornis,

Natural food(Bjornafjorden)

— — 0.06 — — — — — — — Gonzalez et al.,1994

Calanus helgolandicus,Centropages typicus,Euchaeta marina,Euchirella rostrata

Natural food (NWMediterraneanSea)

24.8–26.3 — — 5.3 — — 0.3 4.9–6.0 79.2 17.2 Marty et al., 1994

Mesozooplankton Copepods Natural food(western coastof Mexico)

12.0–27.0 — — — — — — — — — Andrews et al.,1984

Mesozooplankton Copepods Natural food(Irish Sea)

— 56–145 — — 9–19 — — 6.2–10.4 — — Claustre et al.,1992

Mesozooplankton Copepods Natural food(oV Bermuda)

— — 0.01–0.25 — — — — — — — Urban-Richet al., 1998

*Estimated mean values using average volume.

ROLEOFCOPEPOD

OUTFLUXESIN

THECARBON

AND

NITROGEN

CYCLES

261

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 trans-

parent 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 par-

tially crushed by net towing can be recognized by the loss of some append-

ages (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 exo-

skeleton 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 egg�1

(Kiørboe et al., 1985; review by Huntley and Lopez, 1992; Kiørboe and

Sabatini, 1994, and references therein). Nitrogen content is 9 ng N egg�1 for

Acartia tonsa eggs (Kiørboe et al., 1985) and 5 ng N egg�1 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).


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

Process rate

gN gNcop�1 d�1 gC gCcop d

�1 Source

Excretion 0.13–0.23 0.09–0.12(DOC)

Small et al., 1983

0.06–0.36 — Verity, 1985— 0.04–0.08

(DOC)Steinberg et al., 2000

0.01–0.48(generally<0.20)

— Review by Corner and Davies,1971

0.04–0.25 — Checkley et al., 1992, andreferences therein

Respiration — 0.06–0.13 Small et al., 1983— 0.04–0.18 Steinberg et al., 2000

Faecal pelletproduction

0.01–0.02 0.02–0.08 Daly, 1997; Small et al., 1983— 0.01–0.84

(generally<0.24)

Review by Corner et al., 1986;Small and Ellis, 1992

Posthatchmortality

0.03–0.14a 0.03–0.21a Kiørboe and Nielsen, 1994;Roman et al., 2002

Egg mortalityb <0.01 to 1.20b — Checkley et al., 1992, andreferences therein; Campbellet al., 2001

0.01 to 0.68b

(average 0.20)— Review by Mauchline, 1998

— <0.01 to 0.87b

(generally<0.07)

Park and Landry, 1993, andreferences therein; Campbellet al., 2001

— average 0.37b,c Peterson and Dam, 1996Moulting — <0.01–0.02 Vidal, 1980

cop: copepod.

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

bCalculated from female weight-specific egg production rate (references in table) and egg

hatching success (Ianora et al., 1992; Jonasdottir, 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.

cFor herbivorous species, assuming that all assimilated nitrogen is channeled into egg

production in adult females.


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 d�1). 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 d�1 (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 ismore 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 matterexcretion

The three main factors influencing excretion of DM are temperature, indi-

vidual 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 tempera-

ture in marine zooplankton is described by Q10 (Prosser, 1961). The values of


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 PaVenhofer, 1982;Kiørboe et al., 1985; Anderson, 1992; Urabe, 1993), although a negative

relation (for nauplii and copepodite stage II) (PaVenhofer 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 l�1, 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 l�1) (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).


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 onAcartia 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 matteroutfluxes

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; PaVenhofer 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 (PaVenhofer 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 faecalpellet production rate; Centropages typicus females decrease their faecal pel-

let 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). How-

ever, 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 pro-

duction 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 concentra-

tion (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

(PaVenhofer et al., 1995). PaVenhofer (1994) did not find such a relation for

early copepodites (CII) of Eucalanus pileatus, although it was present in


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 Gude, 1999). Posthatch mortal-

ity rates increase with temperature in both sac and broadcast-spawning

copepods (Hirst and Kiøboe, 2002). Mortality in sac spawners is independ-

ent 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 concen-

tration, 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


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 inverte-

brates 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 (Jonasdottir, 1994), and abun-

dance 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; Jonasdottir, 1994; Jonasdottir

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., tempera-

ture, food) or internal factors (e.g., species, body mass, sex). A good positive

relationship was reported between respiration and excretion, in laboratory


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). Statistic-

ally 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 non-

feeding 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, phos-

phorus 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 m�2 d�1). In experimental studies, the vertical flux (VF)

(also called ‘‘sedimentation rate’’ in zooplankton studies) is expressed as the

following depth-integrated flux:

VF ¼Z H

0

@

@zðsCÞdz ¼

Z H

0

@

@zðWaC þWsC � l

@C

@zÞdz ð1Þ


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 con-

centration 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 s�1) 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

18

1

mðrs � rÞgD2 ð2Þ

where rs is the particle density (g cm�3), r is the water density (g cm�3), g is

the acceleration of gravity (cm s�2), D is the sphere diameter (cm), and m the

water molecular viscosity (g cm�1 s�1). For cylindrical and elliptical par-

ticles, Komar et al. (1981) modified the Stokes equation. For cylindrical

particles (as copepod faecal pellets), the equation is:


ws ¼ 0:07901

mðrs � rÞgL2 L

D

� ��1:664

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 withthose of other zooplankton groups

Product Group

Sinking Speed

m d�1 cm s�1 Source

Faecal pellet Copepods 25–250 0.03–0.29 Smayda, 1971; Turner, 1977;Honjo and Roman, 1978; Smallet al., 1979; Bienfang,1980; Yoon et al., 2001

Appendicularians 25–166 0.03–0.19 Gorsky et al., 1984Doliolids 41–405 0.05–0.47 Bruland and Silver, 1981;

Deibel, 1990Euphausiids 15–860 0.03–1.00 Fowler and Small, 1972;

Youngbluth et al., 1989; Cadeeet al., 1992; Yoon et al., 2001

Pteropods 65–1800 0.08–2.08 Bruland and Silver, 1981;Yoon et al., 2001

Heteropods 120–650 0.14–0.75 Yoon et al., 2001Salps 40–2700 0.05–3.13 Bruland and Silver, 1981;

Madin, 1982; Yoon et al.,2001

Carcasses Copepods 35–720 0.04–0.83 Apstein, 1910; Gardiner, 1933;Seiwel and Seiwel, 1938

Amphipods 875 1.01 Apstein, 1910Chaetognaths 435 0.50 Apstein, 1910Cladocerans 120–160 0.14–0.19 Apstein, 1910Euphausiids 1760–3170 2.04–3.67 Mauchline and Fisher, 1969;

Fowler and Small, 1972Ostracods 400 0.46 Apstein, 1910Salps 165–250 0.19–0.29 Apstein, 1910Siphonophores 240 0.28 Apstein, 1910

Eggs Copepods 30 0.03 Kiørboe et al., 1988Euphausiids 130–180 0.15–0.21 Mauchline and Fisher, 1969

Moults Euphausiids 50–1020 0.06–1.18 Mauchline and Fisher, 1969;Nicol and Stolp, 1989, andreferences therein

Feeding nets Larvaceans 120 0.14 Hansen et al., 1996b


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 ofmaterial ingested (Table 4),

whereas food concentration has only a small eVect on pellet density (Feinbergand Dam, 1998). In the study of Feinberg and Dam (1998), pellet density

was measured directly. However, most studies use indirect density estima-

tions 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 cm�3), whereas Stokes’ law under-

estimated 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 par-

ticles (McCave, 1984; Kiørboe, 1997) creating ‘‘marine snow’’ (i.e., floccu-

lent 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 d�1 (<0.01 to 0.10 cm s�1) (higher values can be

found locally or temporally) (Wroblewski, 1977; Jacques and Treguer, 1986;


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 nega-

tively 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 (Gonzalez et al., 1994). When such a

strong stratification occurs, the water density and molecular viscosity in-

crease rapidly with depth (i.e., the sinking speed of particles decreases, see

Equations [2] and [3]), and the vertical turbulent diVusion coeYcient de-

creases (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 degrad-

ation 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 contra-

dictory. 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.


Table 4 Copepod faecal pellet sinking speed and density (fresh faecal pellets)

Faecal pelletproducer

FP sinkingspeed (m d�1)

FP density(g cm�3)

Food conditions (area,if natural food conditions) T 8C S Source

Single copepod speciesAcartia clausi 74–210 — Flagellates culture 15 33.1 Smayda, 1971A. tonsa 80–150 — Coccolith. culture 15 — Honjo and Roman, 1978A. tonsa — 1.15 Diatoms culture — — Butler and Dam, 1994A. tonsa 33 1.13 Diatom 1 culture — — Feinberg and Dam, 1998A. tonsa 32 (high) 1.11 Diatom 2 culture — — Idem

27 (low)A. tonsa 20 (high) 1.10 (high) Flagellate 1 culture — — Idem

28 (low) 1.11 (low)A. tonsa 20 (high) 1.15 Flagellate 2 culture — — Idem

24 (low)A. tonsa 27 (high) 1.14 Heter. Dinofl. culture — — Idem

23 (low)A. tonsa 17 (high) 1.20 Heter. flagel. 1 culture — — Idem

21 (low)A. tonsa 30 (high) 1.12 (high) Heter. flagel. 2 culture — — Idem

68 (low) 1.17 (low)A. tonsa 45 1.13 (high) Ciliates culture — — Idem

1.12 (low)Anomalocerapattersoni

25–220 1.15 Natural food (oV Monaco) 14 — Small et al., 1979; Komaret al., 1981

Calanusfinmarchicus

— 1.19 Natural food (flagellatesa,oV Newfoundland)

— — Urban et al., 1993

C. finmarchicus — 1.11 Natural food (diatomsa,oV Newfoundland)

— — Urban et al., 1993

C. finmarchicus 180–220 — Coccolith. culture 15 — Honjo and Roman, 1978Calanus sp. 70–171 1.17 Diatoms culture 15 29.2 Bienfang, 1980

274

C.FRANGOULIS

ETAL.

Calanus sp. 51–152 1.11 Flagellates culture 15 29.2 Bienfang, 1980Pontella meadii 18–153 — Diatoms culture 22 34.5 Turner, 1977P. meadii 15–125 — Flagellates culture 22 34.5 Turner, 1977Mixed copepodsTemora longicornis,Pseudocalanuselongatus, Acartiaclausi, Centropageshamatus

37–251 1.31–1.45 Natural (SBNS) 25 31.2 Frangoulis et al., 2001

Clausocalanusarcuicornis, A.clausi, C. typicus,Coryceaus typicus

15–150 1.28 Natural (oV Monaco) 14 — Small et al., 1979; Komar et al., 1981

Copepods (>500 mm) 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,

aDominant phytoplankton group.

ROLEOFCOPEPOD

OUTFLUXESIN

THECARBON

AND

NITROGEN

CYCLES

275

Several explanations exist for the discrepancies between the studies cited

above. First, some studies were not experimentally designed to allow estima-

tion 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 concen-

trations of diatoms in their experiment. Other possible explanations are the

nonlinearity of the leaking process and incubation diVerences (i.e., tempera-

ture 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. More-

over, 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 leak-

ing 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 exam-

ined 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


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 elem-

ents (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. Cope-

pods 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; PaVenhofer and Knowles, 1979;

Gonzalez 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 (PaVenhofer 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 ‘‘cop-

rophagous filter’’ that significantly reduces the vertical flux of faecal pellets

(Gonzalez and Smetacek, 1994; Gonzalez 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 pellet-

reworking copepods (e.g., Oithona) and essentially pellet-producing cope-

pods (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


appearance of carcasses is almost identical to that of living individuals, the

ability of predators to distinguish between them should be low. This assump-

tion 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 originat-

ing 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 pro-

duced 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 remineraliza-

tion 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


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 approxi-

mately 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 (Jonasdottir, 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.


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 nutri-

ents (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% (Bamstedt, 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 ex-

cretion 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 require-

ments 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


(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 produc-

tion 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


from copepods migrating vertically. In some areas, the amount of respirat-

ory 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


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., lyso-

cline) (Broecker and Peng, 1982). However, biologically mediated dissol-

ution 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 year�1 (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;

PaVenhofer 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 asubstantial fraction to themaintenance 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;

PaVenhofer 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

(PaVenhofer andKnowles, 1979). Second, the active transport of faecal pellets

and other particulate products by migrant copepods is important in the


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. Sedi-

ment may be transported in copepod pellets in the plume of the Mississippi

River (Turner, 1984, 1987) and in the highly turbid ecosystem of the South-

ern 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 cope-

pods (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,


1977; Fowler, 1977). However, moulting results in less body matter losses

than faecal pellet production and posthatch mortality (Table 2). The down-

ward 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, particu-

larly 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 poly-

chaetes (Marcus, 1984; Marcus and Schmidt-Gegenbach, 1986), hydromedu-

sae (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 excre-

tion includes inorganic compounds (ammonia, orthophosphate) together

with several organic compounds of nitrogen and phosphorus (e.g., Gardner

and PaVenhofer, 1982; Bamstedt, 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; Bamstedt, 1985; Le Borgne, 1986;

Regnault, 1987; Le Borgne and Rodier, 1997); however, there is an import-

ant 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,


moulting, and egg mortality. Copepod faecal pellets are covered by a peri-

trophic 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 gel-

atinous zooplankton (Bruland and Silver, 1981). There are several possible

functions of the peritrophic membrane (e.g., protection of the midgut epi-

thelium) 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; Cadee 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 compos-

ition of faecal pellets is complex (pigments, lipids, amino acids, hydrocar-

bons, 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., Gonzalez 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, sub-

itaneous (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.


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., PaVenhofer 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;

PaVenhofer 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 (Jonasdottir, 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.


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 sedi-mentation 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; Gonzalez et al.,

1994), and turbulent mixing can prolong the residence time of particles in

the mixed layer (Alldredge et al., 1987). Leaking by molecular diVusionreleases carbon and nutrients from pellets and carcasses and depends on

temperature and turbulence and also in the case of faecal pellets food concen-

tration (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 ver-

tical fate of copepod products are production and biodegradation by zoo-

plankton, nekton, and microorganisms. Biodegradation by zooplankton and

nekton is done by detritiphagy (including coprophagy) (e.g., Frankenberg

and Smith, 1967; Gonzalez 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) (Jonasdottir, 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


copepod excretion to the nutrient requirements of phytoplankton is highly

variable spatially and temporally (Corner and Davies, 1971; Bamstedt, 1985;

Le Borgne, 1986; Alcaraz, 1988; Alcaraz et al., 1998). The active flux

of excretory nitrogen during the diel migration of mesozooplankton gener-

ally 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; PaVenhofer 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 bio-

degradation 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 zooplank-

ton (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 regener-

ation using separate zooplankton fractions (such as micro-, meso-, and


macrozooplankton) should be treated with caution because in a natural food

web, the trophic interactions between the fractions can result in a signifi-

cantly 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 phyto-

plankton and zooplankton biomass can influence the export of matter in

an ecosystem. For example, a high match (short time-lag) maintains phyto-

plankton 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 reten-

tion of mesozooplankton particulate products in the water column, corres-

ponds 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 mesozoo-

plankton, 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 sea-

sonal 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 out-

fluxes 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 produc-

tion from faecal pellets. This lack of interest in the particulate nitrogen

production from copepods is the result of two assumptions: (1) the contri-

bution 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


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

N supplied bymesozooplankton(mg N m�3 h�1)

N uptake byphytoplankton(mg N m�3 h�1)

Mesozooplankton Nsupplya/phyto N(%)Study area Depth (m)

Ammoniaexcretion FPP Source

Sargasso Sea 0–200 — — 140–1700 (NH4) 10 (NH4) Dugdale andGoering, 1967

North PacificOcean

— 3–5 6–10 (NH4) 45–50 (NH4) Eppley et al., 1973

OV Peru(coastalupwelling)

0–100 4–20 — 20–290 (NH4) 1–30 (NH4) Smith, 1978a

Newport Riverestuary

1 4–400 — 40–4200 (NH4) 8 (NH4) Smith, 1978b

Ross Sea 0–200 1–2 — 65–100 (NH4) 2 (NH4) Biggs, 1982East-centralPacific Ocean

0–100 12 1 63 (total N) 20 (total N) Small et al., 1983

OV Morocco(upwelling)

0–40 46 — 124 (NH4) 37 (NH4) Head et al., 1996

Mediterranean(Catalan) Seacoastal 0–100 20–33 — 11–20 (total N) 100–285 (total N)frontal 0–100 5–111 — 16–58 (total N) 9–189 (total N) Alcaraz et al.,

1988, 1994oVshore 0–100 1–13 — 3–39 (total N) 5–160 (total N)

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

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

ROLEOFCOPEPOD

OUTFLUXESIN

THECARBON

AND

NITROGEN

CYCLES

291

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 oVeredin 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 discus-

sion (Dam et al., 1993). Among the few studies on faecal pellet flux that

include faecal pellet production values, some authors use direct measure-

ments (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 (Gonzalez 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 particu-

late 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 eVectsof detritiphagy, remineralization, or integration into the marine snow, espe-

cially 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 con-

clusions 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


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 abso-

lute 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 Fran-

kignoulle, 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.

REFERENCES

Abou Debs, C. (1984). Carbon and nitrogen budget of the calanoid copepod Temorastylifera: eVect of food concentration and composition of food. Marine EcologyProgress Series 15, 213–223.

Alcaraz, M. (1988). Summer zooplankton metabolism and its relation to primaryproduction in the Western Mediterranean. Oceanologica Acta (Suppl. 9), 185–191.

Alcaraz, M., Saiz, E., Marrase, C. and Vaque, D. (1988). EVects of turbulence on thedevelopment of phytoplankton biomass and copepod populations in marinemicrocosms. Marine Ecology Progress Series 49, 117–125.

Alcaraz, M., Saiz, E. and Estrada, M. (1994). Excretion of ammonia by zooplanktonand its potential contribution to nitrogen requirements for primary production inthe Catalan Sea (NW Mediterranean). Marine Biology 119, 69–76.

Alcaraz, M., Saiz, E., Fernandez, J. A., Trepat, I., Figueiras, F., Calbet, A. andBautista, B. (1998). Antarctic zooplankton metabolism: Carbon requirements andammonium excretion of salps and crustacean zooplankton in the vicinity of theBransfield Strait during January 1994. Journal of Marine Systems 17, 347–359.

Alldredge, A. L. (1972). Abandoned larvacean houses: A unique food source in thepelagic environment. Science 177, 885–887.

Alldredge, A. L. (1976). Discarded appendicularian houses as sources of food,surface habitat, and particulate organic matter in planktonic environments.Limnology and Oceanography 21, 14–23.


Alldredge, A. L. (1984). The quantitative significance of gelatinous zooplankton aspelagic consumers. In ‘‘Flows of energy andmaterials in marine ecosystems. Theoryand practice’’ (M. J. R. Fasham, ed.), pp. 407–433. Plenum Press, New York.

Alldredge, A. L. (1998). The carbon, nitrogen and mass content of marine snow as afunction of aggregate size. Deep-Sea Research 45, 529–541.

Alldredge, A. L. and Cohen, Y. (1987). Can microscale chemical patches persist inthe sea? Microelectrode study of marine snow, faecal pellets. Science 235, 689–691.

Alldredge, A. L. and Gotschalk, C. C. (1988). In situ settling behaviour of marinesnow. Limnology and Oceanography 33, 339–351.

Alldredge, A. L. and Silver, M. (1988). Characteristics, dynamics and significance ofmarine snow. Progress in Oceanography 20, 41–82.

Alldredge, A. L., Gotschalk, C. C. and MacIntyre, S. (1987). Evidence for sustainedresidence ofmacrocrustacean faecal pellets in surfacewaters oVSouthernCalifornia.Deep-Sea Research 34, 1641–1652.

Anderson, A. (1992). Modelling the influence of food C:N ratio, and respiration ongrowth and nitrogen excretion in marine zooplankton and bacteria. Journal ofPlankton Research 14, 1645–1671.

Anderson, T. R. (1994). Relating C:N ratios in zooplankton food and faecal pelletsusing a biochemical model. Journal of Experimental Marine Biology and Ecology184, 183–199.

Andrews, C. C., Karl, D. M., Small, L. F. and Fowler, S. W. (1984). Metabolicactivity and bioluminescence of oceanic faecal pellets and sediment trap particles.Nature 307, 539–541.

Apstein, C. (1910). Hat ein Organismus in der Tiefe gelebt, in der er gefischt ist?Internationale Revue der Gesamten Hydrobiologie und Hydrographie 3, 17–33.

Atkinson, A., Ward, P. and Murphy, E. J. (1996). Diel periodicity of subantarcticcopepods: Relationships between vertical migration, gut fullness and gut evacu-ation rate. Journal of Plankton Research 18, 1387–1405.

Ayukai, T. andHattori, H. (1992). Production and downward flux of zooplankton faecalpellets in the anticyclonic gyre of Shikoku, Japan. Oceanologica Acta 15, 163–172.

Ayukai, T. and Nishizawa, S. (1986). Defecation rate as possible measure of ingestionrate of Calanus pacificus (Copepoda; Calanoida). Bulletin of the Plankton Societyof Japan 33, 3–10.

Bamstedt, U. (1985). Seasonal excretion rates of macrozooplankton from theSwedish west coast. Limnology and Oceanography 30, 607–617.

Ban, S., Burns, C., Castel, J., Chaudron, Y., Christou, E. D., Escribano, R., Umani,S. F., Gasparini, S., Ruiz, F. G., HoVmeyer, M., Ianora, A., Kang, H.-K., Laabir,M., Lacoste, A., Miralto, A., Ning, X., Poulet, S., Rodriguez, V., Runge, J., Shi, J.,Starr, M., Uye, S. and Wang, Y. (1997). The paradox of diatom-copepod inter-actions. Marine Ecology Progress Series 157, 287–293.

Bathmann, U. V. and Liebezeit, G. (1986). Chlorophyll in copepod faecal pellets:Changes in pellet numbers and pigment content during a declining Baltic springbloom. Marine Ecology 7, 59–73.

Bathmann, U. V., Noji, T. T., Voss, M. and Peinert, R. (1987). Copepod faecalpellets: Abundance, sedimentation and content at a permanent station in Norwe-gian Sea in May/June 1986. Marine Ecology Progress Series 38, 45–51.

Bathmann, U. V., Noji, T. T. and von Bodungen, B. (1991). Sedimentation ofpteropods in the Norwegian Sea in autumn. Deep-Sea Research 38, 1341–1360.

Bautista, B., Harris, R. P., Rodriguez, V. and Guerrero, F. (1994). Temporal vari-ability in copepod fecundity during two diVerent spring bloom periods in coastalwaters oV Plymouth (SW England). Journal of Plankton Research 16, 1367–1377.


Belmonte, G., Miglietta, A., Rubino, F. and Boero, F. (1997). Morphological con-vergence of resting stages of planktonic organisms: A review. Hydrobiologia 355,159–165.

Bianchi, A., Garcin, J., Gorsky, G., Poulicek, M. and Tholosan, O. (1999). Stimula-tion of the potential heterotrophic activity in deep seawater by barotolerantbacteria colonizing faecal pellets produced by migrating zooplankton. Life Sci-ences 322, 1113–1120.

Bidigare, R. R. (1983). Nitrogen excretion by marine zooplankton. In ‘‘Nitrogen inthe Marine Environment’’ (E. J. Carpenter and D. G. Capone, eds.), pp. 385–409.Academic Press, New York.

Bienfang, P. K. (1980). Herbivore diet aVects faecal pellet settling. Canadian Journalof Fisheries and Aquatic Sciences 37, 1352–1357.

Biggs, D. C. (1982). Zooplankton excretion and NHþ4 cycling in near-surface waters

of the Southern Ocean. I. Ross Sea, Austral summer 1977–1978. Polar Biology 1,55–67.

Bochdansky, A. D. and Herndl, G. J. (1992). Ecology of amorphous aggregations(marine snow) in the Northern Adriatic Sea. V. Role of faecal pellets in marinesnow. Marine Ecology Progress Series 89, 297–303.

Bougis, P. (1974). ‘‘Ecologie du plancton marin. II Zooplancton’’. Masson et Cie,Paris.

Broecker, W. S. and Peng, T.-H. (1982). ‘‘Tracers in the sea’’. Lamont-DohertyGeological Observatory, Columbia University, New York.

Bruland, K. W. and Silver, M. W. (1981). Sinking rates of faecal pellets fromgelatinous zooplankton. Marine Biology 63, 295–300.

Butler, M. and Dam, H. G. (1994). Production rates and characteristics of faecalpellets of the copepod Acartia tonsa under simulated phytoplankton bloom condi-tions: Implications for vertical flux. Marine Ecology Progress Series 114, 81–91.

Butler, E. I., Corner, E. D. S. and Marshall, S. M. (1970). On the nutrition andmetabolism of zooplankton. VII. Seasonal survey of nitrogen and phosphorusexcretion by Calanus in the Clyde Sea area. Journal of the Marine BiologicalAssociation of the United Kingdom 50, 525–560.

Cadee, G. C., Gonzalez, H. and Schnack-Schiel, S. B. (1992). Krill diet aVects faecalstring settling. Polar Biology 12, 75–80.

Calbet, A. and Alcaraz, M. (1996). EVects of constant and fluctuating food supply onegg production rates of Acartia grani (Copepoda: Calanoida). Marine EcologyProgress Series 140, 33–39.

Campbell, R. G., Runge, J. A. and Durbin, E. G. (2001). Evidence for food limitationof Calanus finmarchicus production rates on the southern flank of Georges Bankduring April 1997. Deep-Sea Research 48, 531–549.

Carlotti, F., Rey, C., Javanshir, A. and Nival, S. (1997). Laboratory studies on eggand faecal pellet production of Centropages typicus: EVect of age, eVect oftemperature, individual variability. Journal of Plankton Research 19, 1143–1165.

Checkley, D. M. (1980). The egg production of a marine planktonic copepod inrelation to its food supply: Laboratory studies. Limnology and Oceanography 25,430–446.

Checkley, D. M. and Entzeroth, L. C. (1985). Elemental and isotopic fractionation ofcarbon and nitrogen by marine, planktonic copepods and implications to themarine nitrogen cycle. Journal of Plankton Research 7, 553–568.

Checkley, D. M. J., Dagg, M. J. and Uye, S. (1992). Feeding, excretion and eggproduction by individuals and populations of the marine, planktonic copepods,Acartia spp. and Centropages furcatus. Journal of Plankton Research 14, 71–96.


Claustre, H., Poulet, S. A., Williams, R., Ben Mlih, F., Martin-Jezequel, V. andMarty, J. C. (1992). Relationship between the qualitative nature of particles andcopepod faeces in the Irish Sea. Marine Chemistry 40, 231–248.

Conover, R. J. (1978). Transformation of organic matter. In ‘‘Marine Ecology. VolIV Dynamics’’ (O. Kinne, ed.), pp. 221–499. Wiley, New York.

Conover, R. J. and Corner, E. D. S. (1968). Respiration and nitrogen excretion bysome marine zooplankton in relation to their life cycles. Journal of the MarineBiological Association of the United Kingdom 48, 49–75.

Conover, R. J. and Gustavson, K. R. (1999). Source of urea in artic seas. Zooplank-ton metabolism. Marine Ecology Progress Series 179, 41–54.

Conway, D. V. P. (1997). Interactions of inorganic nitrogen in the uptake andassimilation by marine phytoplankton. Marine Biology 39, 221–232.

Conway, D. V. P., McFadzen, I. R. B. and Tranter, P. R. G. (1994). Digestion ofcopepod eggs by larval turbot Scophthalmus maximus and egg viability followinggut passage. Marine Ecology Progress Series 106, 303–309.

Cooper, L. H. N. (1935). The rate of liberation of phosphate in sea water by thebreakdown of plankton organisms. Journal of the Marine Biological Association ofthe United Kingdom 20, 197–200.

Corner, E. D. S. and Davies, A. G. (1971). Plankton as a factor in the nitrogen andphosphorus cycle in the sea. Advances in Marine Biology 9, 101–204.

Corner, E. D. S. and Newell, B. S. (1967). On the nutrition and metabolism ofzooplankton. IV. The forms and nitrogen excreted by Calanus. Journal of theMarine Biological Association of the United Kingdom 47, 113–121.

Corner, E. D. S., Head, R. N. and Kilvington, C. C. (1972). On the nutrition andmetabolism of zooplankton. VIII. The grazing of Biddulphia cells by Calanushelgolandicus. Journal of the Marine Biological Association of the United Kingdom52, 847–861.

Corner, E. D. S., Head, R. N., Kilvington, C. C. and Pennycuick, L. (1976). On thenutrition and metabolism of zooplankton. X. Quantitative aspects of Calanushelgolandicus feeding as a carnivore. Journal of the Marine Biological Associationof the United Kingdom 56, 345–358.

Corner, E. D. S., Head, R. N. and Kilvington, C. C. (1986). Copepod faecal pelletsand the vertical flux of biolipids. In ‘‘The Biological Chemistry of Marine Cope-pods’’ (E. D. S. Corner and S. C. M. O’Hara, eds.), pp. 260–321. Clarendon Press,Oxford.

Currie, R. I. (1962). Pigments in zooplankton faeces. Nature 193, 956–957.Daan, R. (1989). Factors controlling the summer development of copepod popula-tions in the Southern Bight of the North Sea. Netherlands Journal of Sea Research23, 305–322.

Dagg, M. J. and Walser, W. E. J. (1986). The eVect of food concentration on faecalpellet size in marine copepods. Limnology and Oceanography 31, 1066–1071.

Daly, K. L. (1997). Flux of particulate matter through copepods in the NortheastWater Polynya. Journal of Marine Systems 10, 319–342.

Dam, H. G., Miller, C. A. and Jonasdottir, S. H. (1993). The trophic role ofmesozooplankton at 47 8N, 20 8W during the North Atlantic bloom experiment.Deep-Sea Research 40, 197–212.

Dauby, P. (1985). Dynamique et productivite de l’ecosysteme planctonique du golfede Calvi-Corse. PhD Thesis. University of Liege.

Deibel, D. (1990). Still-water sinking velocity of faecal material from the pelagictunicate Dolioletta gegenbauri. Marine Ecology Progress Series 62, 55–60.


Downs, J. N. and Lorenzen, C. J. (1985). Carbon:Pheopigment ratios of zooplanktonfaecal pellets as an index of herbivorous feeding. Limnology and Oceanography 30,1024–1036.

Duarte, C. M. and Cebrian, J. (1996). The fate of marine autotrophic production.Limnology and Oceanography 41, 1758–1766.

Dugdale, R. C. and Goering, J. J. (1967). Uptake of new and regenerated forms ofnitrogen in primary productivity. Limnology and Oceanography 12, 196–206.

Elder, D. L. and Fowler, S. W. (1977). Polychlorinated biphenyls: Penetration intothe deep ocean by zooplankton faecal pellet transport. Science 197, 459–461.

Eppley, R. W. and Lewis, W. M. J. (1981). Photosynthesis in copepods. Science 214,1349–1350.

Eppley, R. W., Renger, E. H., Venrick, E. L. and Mullin, M. M. (1973). A study ofplankton dynamics and nutrient cycling in the central gyre of the North Pacificocean. Limnology and Oceanography 18, 534–551.

Feinberg, L. R. and Dam, H. G. (1998). EVect of diet on dimension, density andsinking rates of faecal pellets of the copepod Acartia tonsa. Marine EcologyProgress Series 175, 87–96.

Fernandez, F. (1977). Efecto de la intensidad de luz natural en la actividad metabo-lica y en la alimentacion de varias especies de copepodos planctonicos. Investiga-cion Pesquera 41, 575–602.

Ferrante, J. G. and Parker, J. I. (1977). Transport of diatom frustules by copepodfaecal pellets to the sediments of Lake Michigan. Limnology and Oceanography 22,92–98.

Flinkman, J., Vuorinen, I. and Christiansen, M. (1994). Calanoid copepod eggssurvive passage through fish digestive tracts. ICES Journal of Marine Science 51,127–129.

Forster, G. R. (1953). Peritrophic membranes in the Caridea (Crustacea Decapoda).Journal of the Marine Biological Association of the United Kingdom 32, 315–318.

Fowler, S. W. (1977). Trace elements in zooplankton particulate products. Nature269, 51–53.

Fowler, S. W. (1991). Biologically mediated removal, transformation, and regener-ation of dissolved elements and compounds. In ‘‘Ocean Margin Processes inGlobal Change’’ (R. F. C. Mantoura, M. Martin and R. Wollast, eds.),pp. 127–143. Wiley, New York.

Fowler, S. W. and Fisher, N. S. (1983). Viability of marine phytoplankton inzooplankton faecal pellets. Deep-Sea Research 30, 963–969.

Fowler, S. W. and Knauer, G. A. (1986). Role of large particles in the transport ofelements and organic compounds through the oceanic water column. Progress inOceanography 16, 147–194.

Fowler, S. W. and Small, L. F. (1972). Sinking rates of euphausiid faecal pellets.Limnology and Oceanography 17, 293–296.

Frangoulis, C., Belkhiria, S., GoVart, A. andHecq, J. H. (2001). Dynamics of copepodfaecal pellets in relation to a Phaeocystis dominated phytoplankton bloom:Characteristics, production and flux. Journal of Plankton Research 23, 75–88.

Frankenberg, D. and Smith, K. L. J. (1967). Coprophagy in marine animals. Limnol-ogy and Oceanography 12, 443–450.

Gamble, J. C. (1978). Copepod grazing during a declining spring phytoplanktonbloom in the Northern North Sea. Marine Biology 49, 303–315.

Gardiner, A. C. (1933). Vertical distribution in Calanus finmarchicus. Journal of theMarine Biological Association of the United Kingdom 18, 575–610.


Gardner, W. S. and PaVenhofer, G. A. (1982). Nitrogen regeneration by the subtrop-ical marine copepod Eucalanus pileatus. Journal of Plankton Research 4, 725–734.

Gaudy, R. (1974). Feeding four species of pelagic copepods under experimentalconditions. Marine Biology 25, 125–141.

Gaudy, R. and Boucher, J. (1983). Relation between respiration, excretion (ammoniaand inorganic phosphorus) and activity of amylase trypsin in diVerent species ofpelagic copepods from an Indian Ocean equatorial area.Marine Biology 75, 37–45.

Gaudy, R., Cervetto, G. and Pagano, M. (2000). Comparison of the metabolism ofAcartia clausi and A. tonsa: Influence of temperature and salinity. Journal ofExperimental Marine Biology and Ecology 247, 51–65.

Gauld, D. T. (1957). A peritrophic membrane in calanoid copepods. Nature 179,325–326.

Genin, A., Gal, G. and Haury, L. (1995). Copepod carcasses in the ocean. II. Nearcoral reefs. Marine Ecology Progress Series 123, 65–71.

Glibert, P. M. (1982). Regional studies of daily, seasonal and size fraction variabilityin ammonium remineralization. Marine Biology 70, 209–222.

Glibert, P. M. (1998). Interactions of top-down and bottom-up control in planktonicnitrogen cycling. Hydrobiologia 363, 1–12.

Glibert, P. M., Miller, C. A., Garside, C., Roman, M. R. and McManus, G. B.(1992). NHþ

4 regeneration and grazing: Interdependent processes in 15NHþ4 size-

fractionated experiments. Marine Ecology Progress Series 82, 65–74.Gonzalez, H. E. and Smetacek, V. (1994). The possible role of the cyclopoid copepodOithona in retarding vertical flux of zooplankton faecal material. Marine EcologyProgress Series 113, 233–246.

Gonzalez, H. E., Gonzalez, S. R. and Brummer, G. J. A. (1994). Short-term sedi-mentation pattern of zooplankton, faeces and microplankton at a permanentstation in the Bjørnafjorden (Norway) during April–May 1992. Marine EcologyProgress Series 105, 31–45.

Gorsky, G., Fisher, N. S. and Fowler, S. W. (1984). Biogenic debris from the pelagictunicate, Oikopleura dioica, and its role in the vertical transport of a transuraniumelement. Estuarine, Coastal and Shelf Science 18, 13–23.

Gowing, M. M. and Silver, M. W. (1985). Minipellets: A new and abundant size classof marine faecal pellets. Journal of Marine Research 43, 395–418.

Gries, T. and Gude, H. (1999). Estimates of the non consumptive mortality ofmesozooplankton by measurement of sedimentation losses. Limnology and Ocean-ography 44, 459–465.

Gulati, R. D., Martinez, C. P. and Siewertsen, K. (1995). Zooplankton as a com-pound mineralising and synthesizing system: Phosphorus excretion. Hydrobiologia315, 25–37.

Hansen, B., Fotel, F. L., Jensen, N. J. andMansen, S. D. (1996a). Bacteria associatedwith a marine planktonic copepod in culture. II. Degradation of faecal pelletsproduced on a diatom, a nanoflagellate or a dinoflagellate diet. Journal of PlanktonResearch 18, 275–288.

Hansen, J. L. S., Kiørboe, T. and Alldredge, A. L. (1996b). Marine snow derivedfrom abandoned larvacean houses: Sinking rates, particle content and mechanismof aggregate formation. Marine Ecology Progress Series 141, 205–215.

Hansen, B. W., Nielsen, T. G. and Levinsen, H. (1999). Plankton communitystructure and carbon cycling on the western coast of Greenland during the strati-fied summer situation. III. Mesozooplankton. Aquatic Microbial Ecology 16,233–249.


Harding, G. C. H., Hargrave, B. T. and Geen, G. H. (1973). Decomposition ofmarine copepods. Phosphorus excretion by zooplankton. Limnology and Oceanog-raphy 18, 670–673.

Hargrave, B. T. and Geen, G. H. (1968). Phosphorus excretion by zooplankton.Limnology and Oceanography 13, 332–343.

Harris, E. (1959). The nitrogen cycle in Long Island Sound. Bulletin of the BinghamOceanographic Collection 17, 31–65.

Harris, R. P. (1994). Zooplankton grazing on the coccolithophore Emiliania huxleiand its role in inorganic carbon flux. Marine Biology 119, 431–439.

Harrison, W. G. (1980). Nutrient regeneration and primary production in the sea. In‘‘Primary Productivity in the Sea’’ (P. G. Falkowski, ed.), pp. 433–460. PlenumPress, New York.

Harrison, W. G., Harris, L. R. and Irwin, B. D. (1996). The kinetics of nitrogenutilization in the oceanic mixed layer: Nitrate and ammonium interactions atnanomolar concentrations. Limnology and Oceanography 41, 16–32.

Haury, L., Fey, C., Gal, G., Hobday, A. and Genin, A. (1995). Copepod carcasses inthe ocean. I. Over seamounts. Marine Ecology Progress Series 123, 57–63.

Haury, L., Fey, C., Newland, C. and Genin, A. (2000). Zooplankton distributionaround four eastern North Pacific seamounts. Progress in Oceanography 45,69–105.

Hays, G. C., Harris, R. P. and Head, R. N. (1997). The vertical nitrogen flux causedby zooplankton diel vertical migration.Marine Ecology Progress Series 160, 57–62.

Head, E. J. H. and Harris, L. R. (1992). Chlorophyll and carotenoid transformationand destruction by Calanus spp. grazing on diatoms. Marine Ecology ProgressSeries 86, 229–238.

Head, E. J. H. and Horne, E. P. W. (1993). Pigment transformation and vertical fluxin an area of convergence in the North Atlantic. Deep-Sea Research 40, 329–346.

Head, E. J. H., Harrison, W. G., Irwin, B. I., Horne, E. P. W. and Li, W. K. W.(1996). Plankton dynamics and carbon flux in an area of upwelling oV the coast ofMorocco. Deep-Sea Research 43, 1713–1738.

Head, E. J. H. and Harris, L. R. (1996). Chlorophyll destruction by Calanus spp.grazing on phytoplankton: Kinetics, eVects of ingestion rate and feeding history,and mechanistic interpretation. Marine Ecology Progress Series 135, 223–235.

Hernandez-Leon, S. and Torres, S. (1997). The relationship between ammonia excre-tion and GDH activity in marine zooplankton. Journal of Plankton Research 19,587–601.

Hirche, H. J. (1997). Life cycle of the copepod Calanus hyperboreus in the GreenlandSea. Marine Biology 128, 607–618.

Hirst, A. G. and Bunker, A. J. (2003). Growth of marine planktonic copepods:Global rates and patterns in relation to chlorophyll a, temperature, and bodyweight. Limnology and Oceanography 48, 1988–2010.

Hirst, A. G. and Kiørboe, T. (2002). Mortality of marine planktonic copepods:global rates and patterns. Marine Ecology Progress Series 230, 195–209.

Hirst, A. G. and Lampitt, R. S. (1998). Towards a global model of in situ weight-specific growth in marine planktonic copepods. Marine Biology 132, 247–257.

Hirst, A. G., RoV, J. C. and Lampitt, R. S. (2003). A synthesis of growth ratesin marine epipelagic invertebrate zooplankton. Advances in Marine Biology 44,1–142.

Honjo, S. and Roman, M. R. (1978). Marine copepod faecal pellets: Production,preservation and sedimentation. Journal of Marine Research 36, 45–57.


Hopcroft, R. R. and RoV, J. C. (1996). Zooplankton growth rates: Diel egg produc-tion in the copepods Oithona, Euterpina and Coryceaus from tropical waters.Journal of Plankton Research 18, 789–803.

Huntley, M. and Lopez, M. D. G. (1992). Temperature dependent production ofmarine copepods: A global synthesis. American Naturalist 140, 201–242.

Huskin, I., Anadon, R., Alvarez-Marques, F. and Harris, R. P. (2000). Ingestion,faecal pellet and egg production rates of Calanus helgolandicus on feeding cocco-lithophorid versus non-coccolithophorid diets. Journal of Experimental MarineBiology and Ecology 248, 239–254.

Hygum, B. H., Petersen, J. W. and Sondergaard, M. (1997). Dissolved organiccarbon released by zooplankton grazing activity—a high-quality substrate poolfor bacteria. Journal of Plankton Research 19, 97–111.

Ianora, A., Mazzocchi, M. G. and Grottoli, R. (1992). Seasonal fluctuations infecundity and hatching success in the planktonic copepod Centropages typicus.Journal of Plankton Research 14, 1483–1494.

Ianora, A., Poulet, S. A. and Miralto, A. (1995). A comparative study of the inhibi-tory eVect of diatoms on the reproductive biology of the copepod Temora stylifera.Marine Biology 121, 533–540.

Ikeda, T. (1985). Metabolic rates of epipelagic marine zooplankton as a function ofbody mass and temperature. Marine Biology 85, 1–12.

Ikeda, T. and Mitchell, A. W. (1982). Oxygen uptake, ammonia excretion andphosphate excretion by krill and other Antarctic zooplankton in relation to theirbody size and chemical composition. Marine Biology 71, 283–298.

Ikeda, T., Kanno, Y., Ozaki, K. and Shinada, A. (2001). Metabolic rates of epipe-lagic marine copepods as a function of body mass and temperature. MarineBiology 139, 587–596.

Jacobsen, T. R. and Azam, F. (1984). Role of bacteria in copepod faecal pelletdecomposition: Colonization, growth rates and mineralisation. Bulletin of MarineScience 35, 495–502.

Jacques, G. and Treguer, P. (1986). Les remontees d’eau cotieres. In ‘‘EcosystemesPelagiques Marins. Collection d’Ecologie 19’’, pp. 3–22. Masson et Cie, Paris.

Johannes, R. E. and Satomi, M. (1966). Composition and nutritive value of faecalpellets of a marine crustacean. Limnology and Oceanography 11, 191–197.

Johannes, R. E. and Webb, K. L. (1965). Release of dissolved amino-acids by marinezooplankton. Science 150, 76–77.

Jonasdottir, S. H. (1994). EVects of food quality on the reproductive success ofAcartia tonsa and Acartia hudsonica: Laboratory observations. Marine Biology121, 67–81.

Jonasdottir, S. H., Fields, D. and Pantoja, S. (1995). Copepod egg production inLong Island Sound, USA, as a function of the chemical composition of seston.Marine Ecology Progress Series 119, 87–98.

Jumars, P. A., Penry, D. L., Baross, J. A., Perry, M. J. and Frost, B. W. (1989).Closing the microbial loop: Dissolved carbon pathway to heterotrophic bacteriafrom incomplete ingestion, digestion and absorption in animals. Deep-Sea Re-search 36, 483–495.

Kang, H. K. and Poulet, S. A. (2000). Reproductive success in Calanus helgolandicusas a function of diet and egg cannibalism. Marine Ecology Progress Series 201,241–250.

Karl, D. M., Knauer, G. A. and Martin, J. H. (1988). Downward flux of particulateorganic matter in the ocean: A particle decomposition paradox. Nature 332,438–440.


Kiørboe, T. (1997). Small-scale turbulence, marine snow formation, and planktivor-ous feeding. Scientia Marina 61, 141–158.

Kiørboe, T. (1998). Population regulation and role of mesozooplankton in shapingmarine pelagic food webs. Hydrobiologia 363, 13–27.

Kiørboe, T. and Nielsen, T. G. (1994). Regulation of zooplankton biomass andproduction in a temperate, coastal ecosystem. 1. Copepods. Limnology and Ocean-ography 39, 493–507.

Kiørboe, T. and Sabatini, M. (1994). Reproductive and life-cycle strategies in egg-carrying cyclopoid and free-spawning calanoid copepods. Journal of PlanktonResearch 16, 1353–1366.

Kiørboe, T., Mohlenberg, F. and Hamburger, K. (1985). Bioenergetics of the plank-tonic copepod Acartia tonsa: Relation between feeding, egg production and respir-ation, and composition of specific dynamic action. Marine Ecology Progress Series26, 85–97.

Kiørboe, T., Mohlenberg, F. and Tiselius, P. (1988). Propagation of planktoniccopepods: Production and mortality of eggs. Hydrobiologia 167/168, 219–225.

Kleppel, G. S., Burkart, C. A. and Houchin, L. (1998). Nutrition and the regulationof egg production in the calanoid copepod Acartia tonsa. Limnology and Oceanog-raphy 43, 1000–1007.

Knauer, G. A., Martin, J. H. and Bruland, K. W. (1979). Fluxes of particulatecarbon, nitrogen, and phosphorus in the upper water column of the northeastPacific. Deep-Sea Research 26, 97–108.

Komar, P. D., Morse, A. P., Small, L. F. and Fowler, S. W. (1981). An analysis ofsinking rates of natural copepod and euphausiid faecal pellets. Limnology andOceanography 26, 172–180.

Krause, M. (1981). Vertical distribution of faecal pellets during FLEX 076. Helgo-lander Wissenschaftliche Meeresuntersuchungen 34, 313–327.

Laabir, M., Poulet, S. A. and Ianora, A. (1995). Measuring production andviability of eggs in Calanus helgolandicus. Journal of Plankton Research 17,1125–1142.

Lampitt, R. S., Noji, T. and von Bodungen, B. (1990). What happens to zooplanktonfaecal pellets? Implications for material flux. Marine Biology 104, 15–23.

Landry, M. R. (1978). Population dynamics and production of a planktonic marinecopepod, Acartia clausi, in a small temperate lagoon on San Juan Island, Wash-ington. Internationale Revue der gesamten Hydrobiologie 63, 77–119.

Le Borgne, R. P. (1973). Etude de la respiration et de l’excretion d’azote et dephosphore des populations zooplanctoniques de l’upwelling mauritanien (mars-avril, 1972). Marine Biology 19, 249–257.

Le Borgne, R. P. (1977). Etude de la production pelagique de la zone equatoriale del’Atlantique a 4 8W. III. Respiration et excretion d’azote et de phosphore duzooplancton. Cahiers d’ORSTOM, Serie Oceanographie 15, 349–362.

Le Borgne, R. P. (1982). Les facteurs de variation de la respiration et de l’excretiond’azote et de phosphore du zooplancton de l’Atlantique intertropical oriental. II.Nature des populations zooplanctoniques et des facteurs du milieu. OceanographieTropicale 17, 187–201.

Le Borgne, R. P. (1986). The release of soluble end products of metabolism. In ‘‘TheBiological Chemistry of Marine Copepods’’ (E. D. S. Corner and S. C. M. O’Hara,eds.), pp. 109–164. Clarendon Press, Oxford.

Le Borgne, R. and Rodier, M. (1997). Net zooplankton and the biological pump:a comparison between the oligotrophic and mesotrophic equatorial Pacific. Deep-Sea Research 44, 2003–2023.


Lee, B. G. and Fisher, N. S. (1992). Decomposition and release of elements fromzooplankton debris. Marine Ecology Progress Series 88, 117–128.

Lee, B. G. and Fisher, N. S. (1994). EVects of sinking and zooplankton grazing on therelease of elements from planktonic debris. Marine Ecology Progress Series 110,299–307.

Legendre, L. and Rassoulzadegan, F. (1995). Plankton and nutrient dynamics inmarine waters. Ophelia 41, 153–172.

Lomas, M. W., Glibert, P. M. and Berg, G. M. (1996). Characterization of nitrogenuptake by natural populations of Aureococcus anophageVerens (Chrysophyceae) asa function of incubation duration, substrate concentration, light and temperature.Journal of Phycology 32, 907–916.

Longhurst, A. R. (1985). The structure and evolution of plankton communities.Progress in Oceanography 15, 1–35.

Longhurst, A. R. and Harrison, W. G. (1988). Vertical nitrogen flux from the oceaniczone by diel migrant zooplankton and nekton. Deep-Sea Research 35, 881–890.

Longhurst, A. R. and Williams, R. (1992). Carbon flux by seasonal vertical migrantcopepods is a small number. Journal of Plankton Research 14, 1495–1509.

Longhurst, A. R., Bedo, A. W., Harrison, W. G., Head, E. J. H. and Sameoto, D. D.(1990). Vertical flux of respiratory carbon by oceanic diel migrant biota. Deep-SeaResearch 37, 685–694.

Lopez, M. D. G. (1991). Moulting and mortality depend on age and stage in naupliarCalanus pacificus: Implication for development time of field cohorts. MarineEcology Progress Series 75, 79–89.

Madin, L. P. (1982). Production, composition and sedimentation of salp faecalpellets in oceanic waters. Marine Biology 67, 39–45.

Maneiro, I., Frangopulos, M., Guisande, C., Fernandez, M., Reguera, B. andRiveiro, I. (2000). Zooplankton as a potential vector of diarrhetic shellfishpoisoning toxins through the food web. Marine Ecology Progress Series 201,155–163.

Marcus, N. H. (1984). Recruitment of copepod nauplii into the plankton: Import-ance of diapause eggs and benthic processes. Marine Ecology Progress Series 15,47–54.

Marcus, N. H. (1996). Ecological and evolutionary significance of resting eggs inmarine copepods: past, present, and future studies. Hydrobiologia 320, 141–152.

Marcus, N. H. and Boero, F. (1998). Minireview: The importance of benthic-pelagiccoupling and forgotten role of life cycles in coastal aquatic systems. Limnology andOceanography 43, 763–768.

Marcus, N. H. and Schmidt-Gegenbach, J. (1986). Recruitment of individuals intothe plankton: The importance of bioturbation. Limnology and Oceanography 31,206–210.

Marcus, N. H., Lutz, R., Burnett, W. and Cable, P. (1994). Age, viability and verticaldistribution of zooplankton resting eggs from an anoxic basin: Evidence of an eggbank. Limnology and Oceanography 39, 154–158.

Marshall, S. M. and Orr, M. A. (1952). On the biology of Calanus finmarchicus, VII.Factors aVecting egg production. Journal of the Marine Biological Association ofthe United Kingdom 30, 527–547.

Marshall, S. M. and Orr, M. A. (1955). On the biology of Calanus finmarchicus, VIII.Food uptake, assimilation and excretion in adult stage V Calanus. Journal of theMarine Biological Association of the United Kingdom 34, 495–529.

Marshall, S. M. and Orr, M. A. (1972). ‘‘The Biology of a Marine Copepod’’.Springer, Edinburgh.


Martens, P. (1978). Faecal pellets. Fiches d’Identification du Zooplankton 162, 1–4.Martens, P. and Krause, M. (1990). The fate of faecal pellets in the North Sea.Helgolander wissenschaftliche Meeresuntersuchungen 49, 9–19.

Martin, J. H. (1968). Phytoplankton-zooplankton relationships in Narragansett Bay.III-Seasonal changes in zooplankton excretion rates in relation to phytoplanktonabundance. Limnology and Oceanography 13, 63–71.

Marty, J. C., Nicolas, E., Miquel, J. C. and Fowler, S. W. (1994). Particulate fluxes oforganic compounds and their relationship to zooplankton faecal pellets in NWMediterranean Sea. Marine Chemistry 46, 387–405.

Mauchline, J. (1998). The biology of calanoid copepods. Advances in Marine Biology33, 1–710.

Mauchline, J. and Fisher, L. R. (1969). The biology of euphausiids. Advances inMarine Biology 7, 1–454.

Mayzaud, P. (1971). Etude du metabolisme de quelques especes du zooplancton et deses consequences ecologiques: Respiration et excretion azotee. PhD Thesis. Uni-versite de Paris, France.

Mayzaud, P. (1973). Respiration and nitrogen excretion of zooplankton: II. Studiesof the metabolic characteristics of starved animals. Marine Biology 21, 19–28.

McCarthy, J. J. (1971). The role of urea in marine zooplankton ecology. PhD Thesis.University of California, San Diego.

McCave, I. N. (1975). Vertical flux of particles in the ocean. Deep-Sea Research 22,491–502.

McCave, I. N. (1984). Size spectra and aggregation of suspended particles in the deepocean. Deep-Sea Research 31, 329–352.

Miller, C. A. (1992). EVects of food quality and quantity on nitrogen excretion by thecopepod Acartia tonsa. PhD Thesis. University of Maryland.

Miller, C. A. and Gilbert, P. M. (1998). Nitrogen excretion by the calanoid copepodAcartia tonsa: Results of mesocosm experiments. Journal of Plankton Research 20,1767–1780.

Miller, C. A., Penry, D. L. and Glibert, P. M. (1995). The impact of trophicinteractions on rates of nitrogen regeneration and grazing in Chesapeake Bay.Limnology and Oceanography 40, 1005–1011.

Miller, C. A., Glibert, P. M., Berg, G. M. and Mulholland, M. R. (1997). EVects ofgrazer and substrate amendments on nutrient and plankton dynamics in estuarineenclosures. Aquatic Microbial Ecology 12, 251–261.

Milliman, J. D., Troy, P. J., Balch, W.M., Adams, A. K., Li, H. andMackenzie, F. T.(1999). Biologically mediated dissolution of calcium carbonate above the chemicallysocline? Deep-Sea Research 46, 1653–1669.

Mochioka, N. and Iwamizu, M. (1996). Diet of anguilloid larvae: Leptocephali feedselectively on larvacean houses and faecal pellets. Marine Biology 125, 447–452.

Møller, E. F. and Nielsen, T. G. (2001). Production of bacterial substrate by marinecopepods: EVect of phytoplankton biomass and cell size. Journal of PlanktonResearch 23, 527–536.

Møller, E. F., Thor, P. and Nielsen, T. G. (2003). Production of DOC by Calanusfinmarchicus, C. glacialis and C. hyperboreus through sloppy feeding and leakagefrom faecal pellets. Marine Ecology Progress Series 262, 185–191.

Moore, H. B. (1931). The specific identification of faecal pellets. Journal of theMarine Biological Association of the United Kingdom 17, 359–365.

Morales, C. E. (1987). Carbon and nitrogen content of copepod faecal pellets: EVectof food concentration and feeding behaviour. Marine Ecology Progress Series 36,107–114.


Morales, C. E., Harris, R. P., Head, R. N. and Tranter, P. R. G. (1993). Copepodgrazing in the oceanic northeast Atlantic during 6 week drifting station: Thecontribution of size classes and vertical migrants. Journal of Plankton Research15, 185–211.

Morris, R. J., Bone, Q., Head, R., Braconnot, J. C. and Nival, P. (1988). Role ofsalps in the flux of organic matter to the bottom of the Ligurian Sea. MarineBiology 97, 237–241.

Nagata, T. and Kirchman, D. C. (1992). Release of macromolecular organic com-plexes by heterotrophic marine flagellates. Marine Ecology Progress Series 83,233–240.

Nejstgaard, J. C., Naustvoll, L. J. and Sazhin, A. (2001). Correcting for underesti-mation of microzooplankton grazing in bottle incubation experiments with meso-zooplankton. Marine Ecology Progress Series 221, 59–75.

Nicol, S. and Stolp, M. (1989). Sinking rates of cast exoskeletons of Antarctic krill(Euphausia superba Dana) and their role in the vertical flux of particulate matterand fluoride in the Southern Ocean. Deep-Sea Research 36, 1753–1762.

Nielsen, T. G., Møller, E. F., Satapoomin, S., Ringuette, M. and Hopcroft, R. R.(2002). Egg hatching rate of the cyclopoid copepod Oithona similis in Arctic andTemperate waters. Marine Ecology Progress Series 236, 301–306.

Nival, P., Malara, G., Charra, R., Palazzoli, I. and Nival, S. (1974). Etude de larespiration et de l’excretion de quelques copepodes planctoniques (Crustacea) dansla zone de remontee d’eau profonde des cotes marocaines. Journal of ExperimentalMarine Biology and Ecology 15, 231–260.

Noji, T. T. (1991). The influence of macrozooplankton on vertical particulate flux.Sarsia 76, 1–9.

Noji, T. T., Estep, K. E., Macintyre, F. and Norrbin, F. (1991). Image analysis offaecal material grazed upon by three species of copepods: Evidence for coprorhexy,coprophagy and coprochaly. Journal of the Marine Biological Association of theUnited Kingdom 71, 465–480.

Ohman, M. D. and Hirche, H. J. (2001). Density-dependent mortality in an oceaniccopepod population. Nature 412, 638–641.

Ohman, M. D. and Wood, S. N. (1995). The inevitability of mortality. ICES Journalof Marine Science 52, 517–522.

Osterberg, C., Carey, A. G. and Curl, H. (1963). Acceleration of sinking rates ofradionulides in the ocean. Nature 200, 1276–1277.

PaVenhofer, G. A. (1994). Variability due to feeding activity of individual copepods.Journal of Plankton Research 16, 617–626.

PaVenhofer, G. A. and Gardner, W. S. (1984). Ammonium release by juveniles andadult females of the subtropical marine copepod Eucalanus pileatus. Journal ofPlankton Research 6, 505–513.

PaVenhofer, G. A. and Knowles, S. C. (1978). Feeding of marine planktonic cope-pods on mixed phytoplankton. Marine Biology 48, 143–152.

PaVenhofer, G. A. and Knowles, S. C. (1979). Ecological implications of faecal pelletsize, production and consumption by copepods. Journal of Marine Research 37,36–47.

PaVenhofer, G. A., Bundy, M. H., Lewis, K. D. and Metz, C. (1995). Rates ofingestion and their variability between individual calanoid copepods—direct ob-servations. Journal of Plankton Research 17, 1573–1585.

Park, C. and Landry, M. R. (1993). Egg production by the subtropical copepodUndinula vulgaris. Marine Biology 117, 415–421.


Park, J. C., Aizaki, M., Fukushima, T. and Otsuki, A. (1997). Production of labileand refractory DOC by zooplankton excretion: An experimental study using largeoutdoor continuous flow through ponds. Canadian Journal of Fisheries and AquaticSciences 54, 434–443.

Peterson, W. T. and Dam, H. G. (1996). Pigment ingestion and egg production ratesof the calanoid copepod Temora longicornis: Implication for gut pigment loss andomnivorous feeding. Journal of Plankton Research 18, 855–861.

Peterson, W. T. and Kimmerer, W. J. (1994). Processes controlling recruitment of themarine calanoid copepod Temora longicornis in Long Island Sound: Egg produc-tion, egg mortality, and cohort survival rates. Limnology and Oceanography 39,1594–1605.

Porter, K. G. (1973). Selective grazing and diVerential digestion of algae by zoo-plankton. Nature 244, 179–180.

Poulet, S. A., Ianora, A., Miralto, A. and Meijer, L. (1994). Do diatoms arrest eggdevelopment in copepods? Marine Ecology Progress Series 111, 79–86.

Poulicek, M., Nisin, O., Loizeau, V., Bourge, I., Toussaint, C. and Voss-Foucart,M. F. (1992). Etude experimentale in situ de la degradation du materiel detritiqueen pleine eau et a l’interface sedimentaire. Bulletin de la Societe Royale de Liege 61,129–142.

Prosser, C. L. (1961). Oxygen: Respiration and metabolism. In ‘‘ComparativeAnimal Physiology’’ (C. L. Prosser and F. A. Brown, eds.), pp. 165–211. W.B. Saunders, Philadelphia.

Redden, A. M. and Daborn, G. R. (1991). Viability of subitaneous copepod eggsfollowing fish predation on egg-carrying calanoids.Marine Ecology Progress Series77, 307–310.

Reeve, M. R. (1963). The filter-feeding of Artemia. III. Faecal pellets and theirassociated membranes. Journal of Experimental Biology 40, 215–221.

Reinfelder, J. R. and Fisher, N. S. (1993). Release rates of trace elements and proteinfrom decomposing planktonic debris. 2. Copepod carcasses and sediment trapparticulate matter. Journal of Marine Research 51, 423–442.

Regnault, M. (1987). Nitrogen excretion in marine and fresh-water crustacea. Bio-logical Reviews of the Cambridge Philosophical Society 62, 1–24.

Regnault, M. and Lagardere, J. P. (1983). EVects of ambient noise on the metaboliclevel of Crangon crangon (Decapoda, Natantia). Marine Ecology Progress Series11, 71–78.

Rey, C., Carlotti, F., Tande, K. and Hygum, B. H. (1999). Egg and faecal pelletproduction of Calanus finmarchicus females from controlled mesocosms and in situpopulations: Influence of age and feeding history. Marine Ecology Progress Series188, 133–148.

Roger, C. (1978). Azote et phosphore chez un crustace macroplanctonique, Mega-nyctiphanes norvegica (M. Sars) (Euphausiacea): Excretion minerale et constitu-tion. Journal of Experimental Marine Biology and Ecology 33, 57–83.

Roman, M. R. and Gauzens, A. L. (1997). Copepod grazing in the equatorial Pacific.Limnology and Oceanography 42, 623–634.

Roman, M. R., Duclow, H. W., Fuhrman, J. A., Garside, C., Glibert, P. M., Malone,T. C. and McManus, G. B. (1988). Production, consumption and nutrient cyclingin a laboratory mesocosm. Marine Ecology Progress Series 42, 39–52.

Roman, M. R., Adolf, H. A., Landry, M. R., Madin, L. P., Steinberg, D. K. andZhang, X. (2002). Estimates of oceanic mesozooplankton production: A compari-son using the Bermuda and Hawaii time-series data. Deep-Sea Research 49,175–192.


Roman, M., Smith, S., Wishner, K., Zhang, X. S. and Gowing, M. (2000). Meso-zooplankton production and grazing in the Arabian Sea. Deep-Sea Research 47,1423–1450.

Sabine, C. L. and Mackenzie, F. T. (1991). Oceanic sinks for anthropogenic CO2.International Journal of Energy and Environmental Economics 1, 119–127.

Sarhan, T., Lafluente, J. G., Vargas, M., Vargas, J. M. and Plaza, F. (2000).Upwelling mechanisms in the northwestern Alboran Sea. Journal of MarineSystems 23, 317–331.

Satomi, M. and Pomeroy, L. R. (1965). Respiration and phosphorus excretion insome marine populations. Ecology 46, 877–881.

Seiwel, H. R. and Seiwel, G. E. (1938). The sinking of decomposing plankton in seawater and its relationship to oxygen consumption and phosphorus liberation.Proceedings of the American Philosophical Society 78, 465–481.

Silver, M. W., Shanks, A. L. and Trent, J. D. (1978). Marine snow: Microplanktonhabitat and source of small-scale patchiness in pelagic populations. Science 201,371–373.

Siokou-Frangou, I., Christou, E. D., Frangopoulu, N. and Mazzocchi, M. G. (1997).Mesozooplankton distribution from Sicily to Cyprus (Eastern Mediterranean). II.Copepod assemblages. Oceanologica Acta 20, 537–548.

Skjoldal, H. R. and Wassmann, P. (1986). Sedimentation of particulate organicmatter and silicium during spring and summer in Lindaspollene, Western Norway.Marine Ecology Progress Series 30, 49–63.

Small, L. F. and Ellis, S. G. (1992). Faecal carbon production by zooplankton inSanta Monica Basin: The eVects of body size and carnivorous feeding. Progress inOceanography 30, 197–221.

Small, L. F. and Fowler, S. W. (1973). Turnover and vertical transport of zinc by theeuphausiid Meganyctiphanes norvegica in the Ligurian Sea. Marine Biology 18,284–290.

Small, L. F., Fowler, S. W. and Unlu, M. Y. (1979). Sinking rates of natural copepodfaecal pellets. Marine Biology 51, 233–241.

Small, L. F., Fowler, S. W., Moore, S. A. and La Rosa, J. (1983). Dissolved andfaecal pellet carbon and nitrogen release by zooplankton in tropical waters. Deep-Sea Research 30, 1199–1220.

Small, L. F., Knauer, G. A. and Tuel, M. D. (1987). The role of sinking faecal pelletsin stratified euphotic zones. Deep-Sea Research 34, 1705–1712.

Small, L. F., Landry, M. R., Eppley, R. W., Azam, F. and Carlucci, A. F. (1989).Role of plankton in the carbon and nitrogen budgets of Santa Monica Basin,California. Marine Ecology Progress Series 56, 57–74.

Smayda, T. J. (1969). Some measurements of the sinking rate of faecal pellets.Limnology and Oceanography 14, 621–625.

Smayda, T. J. (1971). Normal and accelerated sinking of phytoplankton in the sea.Marine Geology 11, 105–122.

Smith, C. R. (1985). Food for the deep sea: Utilization, dispersal and flux of nektonfalls at the Santa Catalina Basin floor. Deep-Sea Research 32, 417–442.

Smith, S. L. (1978a). Nutrient regeneration by zooplankton during a red tide oVPeru, with notes on biomass and species composition of zooplankton. MarineBiology 49, 125–132.

Smith, S. L. (1978b). The role of zooplankton in the nitrogen dynamics of a shallowestuary. Estuarine and Coastal Marine Science 7, 555–565.


Souissi, S., Carlotti, F. and Nival, P. (1997). Food-dependent and temperature-dependent probability function of moulting rate in copepods: Application topopulation dynamics model. Journal of Plankton Research 19, 1331–1346.

Steinberg, D. K. (1995). Diet of copepods (Scopalatum vorax) associated with meso-pelagic detritus (giant larvacean houses) in Monterey Bay, California. MarineBiology 122, 571–584.

Steinberg, D. K., Silver, M., Pilskaln, C. H., Coale, S. L. and Paduan, J. B. (1994).Midwater zooplankton communities on pelagic detritus (giant larvacean houses) inMonterey Bay, California. Limnology and Oceanography 39, 1606–1620.

Steinberg, D. K., Silver, M. W. and Pilskaln, C. H. (1997). Role of mesopelagiczooplankton in the community metabolism of giant larvacean house detritus inMonterey Bay, California, USA. Marine Ecology Progress Series 147, 167–179.

Steinberg, D. K., Carlson, C. A., Bates, N. R., Goldthwait, S. A., Madin, L. P. andMichaels, A. F. (2000). Zooplankton vertical migration and the active transport ofdissolved organic and inorganic carbon in the Sargasso Sea. Deep-Sea Research 47,137–158.

Stephens, G. C. and North, B. B. (1971). Extrusion of carbon accompanying uptakeof amino acids by marine phytoplankters. Limnology and Oceanography 16,752–757.

Stevens, C. J. and Head, E. J. H. (1998). A model of chlorophyll a destruction byCalanus spp. and implications for the estimation of ingestion rates using the gutfluorescence method. Marine Ecology Progress Series 171, 187–198.

Stoecker, D. K. (1984). Particle production by planktonic ciliates. Limnology andOceanography 29, 930–940.

Strom, S. L., Benner, R., Ziegler, S. and Dagg, M. J. (1997). Planktonic grazers are apotentially important source of marine dissolved organic carbon. Limnology andOceanography 42, 1364–1374.

Sundquist, E. T. (1993). The global carbon dioxide budget. Science 259, 934–941.Svensen, C. and Nejstgaard, J. C. (2003). Is sedimentation of copepod faecal pelletsdetermined by cyclopoids? Evidence from enclosed ecosystems. Journal of Plank-ton Research 25, 917–926.

Takahashi, M. and Ikeda, T. (1975). Excretion of ammonia and inorganic phos-phorus by Euphausia pacifica and Metridia pacifica at diVerent concentrations ofphytoplankton. Journal of the Fisheries Research Board of Canada 32, 2189–2195.

Tsuda, A. and Nemoto, T. (1990). The eVect of food concentration on the faecalpellet size of the marine copepod Pseudocalanus newmani. Bulletin of the PlanktonSociety of Japan 37, 83–90.

Turner, J. T. (1977). Sinking rates of faecal pellets from the marine copepod Pontellameadii. Marine Biology 40, 249–259.

Turner, J. T. (1979). Microbial attachment to copepod faecal pellets and its possibleecological significance. Transactions of the American Microscopical Society 98,131–135.

Turner, J. T. (1984). Zooplankton feeding ecology: Contents of faecal pellets of thecopepods Eucalanus pileatus and Paracalanus quasimodo from continental shelfwaters of the Gulf of Mexico. Marine Ecology Progress Series 15, 27–46.

Turner, J. T. (1987). Zooplankton feeding ecology: Contents of faecal pellets of thecopepod Centropages velificatus from waters near the mouth of the MississippiRiver. The Biological Bulletin 173, 377–386.

Turner, J. T. (2002). Zooplankton faecal pellets, marine snow and sinking phyto-plankton blooms. Aquatic Microbial Ecology 27, 57–102.


Turner, J. T. and Ferrante, J. G. (1979). Zooplankton faecal pellets in aquaticecosystems. BioScience 29, 670–677.

Twombly, S. and Tish, N. (2000). Body size regulation in copepod crustaceans.Oecologia 122, 318–326.

Urabe, J. (1993). N and P cycling coupled by grazers activities: Food quality andnutrient release by zooplankton. Ecology 74, 2337–2350.

Urban-Rich, J. (1999). Release of dissolved organic carbon from copepod faecalpellets in the Greenland Sea. Journal of Experimental Marine Biology and Ecology232, 107–124.

Urban-Rich, J. (2001). Seston eVects on faecal pellet carbon concentrations from amixed community of copepods in Balsfjord, Norway, and the Antarctic PolarFront. ICES Journal of Marine Science 58, 700–710.

Urban-Rich, J., Hansell, D. A. and Roman, M. R. (1998). Analysis of copepod faecalpellet carbon using high temperature combustion method. Marine Ecology Pro-gress Series 171, 199–208.

Urban, J. L., Deibel, D. and Scwinghamer, P. (1993). Seasonal variations in thedensities of faecal pellets produced by Oikopleura vanhoeVeni (Larvacea) andCalanus finmarchicus (Copepoda). Marine Biology 117, 607–613.

Uye, S. (1988). Temperature-dependent development and growth of Calanus sinicus(Copepoda: Calanoida) in the laboratory. Hydrobiologia 167/168, 285–293.

Uye, S. and Kaname, K. (1994). Relations between faecal pellet volume and body sizefor major zooplankters of the Inland Sea of Japan. Journal of Oceanography 14,343–358.

Vargas, C. A., Tonnesson, K., Sell, A., Maar, M., Møller, E. F., Zervoudaki, T.,Giannakourou, A., Christou, E. D., Satapoomin, S., Petersen, J. K., Nielsen, T. G.and Tiselius, P. (2002). Importance of copepods versus appendicularians invertical carbon fluxes in a Swedish fjord. Marine Ecology Progress Series 241,125–138.

Verity, P. G. (1985). Ammonia excretion rates of oceanic copepods and implicationsfor estimates of primary production in the Sargasso Sea. Biological Oceanography3, 249–283.

Vidal, J. (1980). Physioecology of zooplankton. II. EVects of phytoplankton concen-tration, temperature and body size on the development and moulting rates ofCalanus pacificus and Pseudocalanus sp. Marine Biology 56, 135–146.

Voss, M. (1991). Content of copepod faecal pellets in relation to food supply in KielBight and its eVect on sedimentation rate. Marine Ecology Progress Series 75,217–225.

Wassmann, P. (1998). Retention versus export food chains: Processes controllingsinking loss from marine pelagic systems. Hydrobiologia 363, 29–57.

Wen, Y. H. and Peters, R. H. (1994). Empirical models of phosphorus and nitrogenexcretion rates by zooplankton. Limnology and Oceanography 39, 1669–1679.

Wexels Riser, C., Wassmann, P., Olli, K. and Arashkevich, E. (2001). Production,retention and export of zooplankton faecal pellets on and oV the Iberian shelf,north-west Spain. Progress in Oceanography 51, 423–442.

Wexels Riser, C., Wassmann, P., Olli, K., Pasternak, A. and Arashkevich, E. (2002).Seasonal variation in production, retention and export of zooplankton faecalpellets in the marginal ice zone and central Barents Sea. Journal of Marine Systems38, 175–188.

Wexels Riser, C., Jansen, S., Bathmann, U. and Wassmann, P. (2003). Grazing ofCalanus helgolandicus on Dinophysis norvegica during bloom conditions in the


North Sea: Evidence from investigations of faecal pellets.Marine Ecology ProgressSeries 256, 301–304.

Wheeler, E. H. J. (1967). Copepod detritus in the deep sea. Limnology and Oceanog-raphy 12, 697–702.

Wollast, R. (1991). The coastal organic carbon cycle: Flux, sources and sinks. In‘‘Ocean Margin Processes in Global Change’’ (R. F. C. Mantoura, J. M. Martinand R. Wollast, eds.), pp. 365–381. Wiley, New York.

Wollast, R. (1998). Evaluation and comparison of the global carbon cycle in thecoastal zone and in the open oceans. In ‘‘The Global Coastal Ocean’’ (K. H. Brinkand A. R. Robinson, eds.), pp. 213–252. Wiley, New York.

Wollast, R. and Chou, L. (2001). The carbon cycle at the ocean margin in theNorthern Gulf of Biscay. Deep-Sea Research 48, 3265–3293.

Wright, P. A. (1995). Nitrogenous excretion: Three end products, many physiologicalroles. Journal of Experimental Biology 198, 273–281.

Wroblewski, J. (1977). A model of phytoplankton plume formation during variableOregon upwelling. Journal of Marine Research 35, 357–394.

Yamaguchi, A., Watanabe, Y., Ishida, H., Harimoto, T., Furusawa, K., Suzuki, S.,Ishizaka, J., Ikeda, T. and Takahashi, M. (2002). Community and trophic struc-tures of pelagic copepods down to greater depths in the western subarctic Pacific(WEST-COSMIC). Deep-Sea Research 49, 1007–1025.

Yoon, W. D., Kim, S. K. and Han, K. N. (2001). Morphology and sinking velocitiesof faecal pellets of copepod, molluscan, euphausiid, and salp taxa in the north-eastern tropical Atlantic. Marine Biology 139, 923–928.

Yoshikoshi, K. and Ko, Y. (1988). Structure and function of the peritrophic mem-branes of copepods. Nippon Suisan Gakkaishi 54, 1077–1082.

Youngbluth, M. J., Bailey, T. G., Davoll, P. J., Jacoby, C. A., Blades-Eckelbarger, P.I. and Griswold, C. A. (1989). Faecal pellet production and diel migratory behav-iour by the euphausiid Meganyctiphanes norvegica eVect benthic-pelagic coupling.Deep-Sea Research 36, 1491–1501.

Zhang, X. and Dam, H. G. (1997). Downward export of carbon by diel migrantmesozooplankton in the central equatorial Pacific. Deep-Sea Research 44,2191–2202.


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

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

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

312 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

TAXONOMIC INDEX 313

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

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

314 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

TAXONOMIC INDEX 315

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

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


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

Carbon14C 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

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

318 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

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

SUBJECT INDEX 319

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

Dentalium entalis


Dentalium vulgare


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

320 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)


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

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

SUBJECT INDEX 321

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)


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

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


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


Haddock


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)


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

322 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

Laminaria ochroleuca

temperature change and, 47–8

Land-Ocean Interaction Study (LOIS), 9

Langmuir circulation

winds/currents and, 148

Larval fish


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)


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

SUBJECT INDEX 323

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)


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)


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


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

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


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

324 SUBJECT INDEX

Octopus vulgaris


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)


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)


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

SUBJECT INDEX 325

Prorocentrum spp.


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

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)


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


St. George’s Channel, 18

Straits of Dover

currents/circulation in, 19

STST see Selective tidal stream transport

326 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


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

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


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

SUBJECT INDEX 327

Water temperature (cont.)

sunspot index and, 15–16

surface, 10, 12–13, 14–15, 16, 17

wind effects on, 18

Water transparency


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

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


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

328 SUBJECT INDEX

advances in marine biology, vol. 47

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