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,
Plymouth, PL1 2PB, UK
Nicholas C. Halliday, Marine Biological Association of the UK, Citadel
Hill, Plymouth, PL1 2PB, UK
Nicholas J. Hardman-Mountford, Plymouth Marine Laboratory, 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,
Plymouth, PL1 2PB, UK
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,
Plymouth, PL1 2PB, UK
Rebecca Leaper, Marine Biological Association of the UK, Citadel Hill,
Plymouth, PL1 2PB, UK
*Current address: School of Ocean Sciences, University of North Wales
Bangor, Menai Bridge, Gwynedd, LL59 5AB, UK
L. A. McEvoy, North Atlantic Fisheries College, Port Arthur, Scalloway,
Shetland, ZE1 0UN,UK
Nova Mieszkowska, Marine Biological Association of the UK, Citadel Hill,
Plymouth, PL1 2PB, UK
Robin D. Pingree, Marine Biological Association of the UK, Citadel Hill,
Plymouth, PL1 2PB, UK
Henrique Queiroga, Departmento de Biologia, Universidade de Aveiro,
Campus 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,
Plymouth, PL1 2PB, UK
Tania Smith, Plymouth Marine Laboratory, Prospect Place, Plymouth, PL1
3DH, UK
Alan J. Southward, Marine Biological Association of the UK, Citadel Hill,
Plymouth, PL1 2PB, UK
Anthony W. Walne, Sir Alister Hardy Foundation for Ocean Science,
Citadel Hill, Plymouth, PL1 2PB, UK
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
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 196
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
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 243
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
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293
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
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83
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,
4 ALAN J. SOUTHWARD ET AL.
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.
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 5
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.
6 ALAN J. SOUTHWARD ET AL.
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.
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 7
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.
8 ALAN J. SOUTHWARD ET AL.
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;
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 9
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.
10 ALAN J. SOUTHWARD ET AL.
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).
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 11
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
12 ALAN J. SOUTHWARD ET AL.
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.)
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 13
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
14 ALAN J. SOUTHWARD ET AL.
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.
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 15
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)
16 ALAN J. SOUTHWARD ET AL.
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.
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 17
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.
18 ALAN J. SOUTHWARD ET AL.
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
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 19
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
20 ALAN J. SOUTHWARD ET AL.
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).
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 21
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.
22 ALAN J. SOUTHWARD ET AL.
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).
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 23
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).
24 ALAN J. SOUTHWARD ET AL.
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.
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 25
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.
26 ALAN J. SOUTHWARD ET AL.
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.)
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 27
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)
28 ALAN J. SOUTHWARD ET AL.
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.
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 29
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).
30 ALAN J. SOUTHWARD ET AL.
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
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 31
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).
32 ALAN J. SOUTHWARD ET AL.
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).
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 33
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
34 ALAN J. SOUTHWARD ET AL.
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.
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 35
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).
36 ALAN J. SOUTHWARD ET AL.
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).
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 37
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
38 ALAN J. SOUTHWARD ET AL.
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).
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 39
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).
40 ALAN J. SOUTHWARD ET AL.
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
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 41
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,
42 ALAN J. SOUTHWARD ET AL.
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).
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 43
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
44 ALAN J. SOUTHWARD ET AL.
(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).
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 45
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
46 ALAN J. SOUTHWARD ET AL.
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
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 47
(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
48 ALAN J. SOUTHWARD ET AL.
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).
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 49
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
50 ALAN J. SOUTHWARD ET AL.
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).
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 51
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.
52 ALAN J. SOUTHWARD ET AL.
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.
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 53
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
54 ALAN J. SOUTHWARD ET AL.
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).
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 55
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.
56 ALAN J. SOUTHWARD ET AL.
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/.
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 57
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
58 ALAN J. SOUTHWARD ET AL.
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.]
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 59
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.)
60 ALAN J. SOUTHWARD ET AL.
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
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 61
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.
62 ALAN J. SOUTHWARD ET AL.
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.
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 63
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
68 ALAN J. SOUTHWARD ET AL.
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.
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 69
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
70 ALAN J. SOUTHWARD ET AL.
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.
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 71
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.
72 ALAN J. SOUTHWARD ET AL.
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
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 73
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).
74 ALAN J. SOUTHWARD ET AL.
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
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 75
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
76 ALAN J. SOUTHWARD ET AL.
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).
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 77
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
78 ALAN J. SOUTHWARD ET AL.
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
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 79
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.
80 ALAN J. SOUTHWARD ET AL.
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)
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 81
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.
82 ALAN J. SOUTHWARD ET AL.
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
LONG-TERM RESEARCH IN THE ENGLISH CHANNEL 83
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.
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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
ADVANCES IN MARINE BIOLOGY VOL. 47 � 2005 Elsevier Ltd.0-12-026148-0 All rights of reproduction in any form reserved
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).
110 HENRIQUE QUEIROGA AND JACK BLANTON
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,
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 111
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
112 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 113
Figure 1(a)
114 HENRIQUE QUEIROGA AND JACK BLANTON
Figure 1(b) (Continued)
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 115
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).
116 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 117
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
118 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 119
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
120 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 121
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
122 HENRIQUE QUEIROGA AND JACK BLANTON
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.
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 123
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
124 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 125
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
126 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 127
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 129
(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.
130 HENRIQUE QUEIROGA AND JACK BLANTON
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).
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 131
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
132 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 133
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
134 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 135
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
136 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 137
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
138 HENRIQUE QUEIROGA AND JACK BLANTON
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.
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 139
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
140
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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
LARVAE
141
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)
Infraorder ordivision Species
Types of vertical migration
ReferencesFirst stageMiddlestages Last stage
142
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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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 143
Table 4 Extent of vertical distribution according to larval stage determined from field studies
Infraorder ordivision Species
Firststage
Middlestages
Laststage
Stationdepth (m) References
Obligate estuarine species
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)
Shelf species that may penetrate estuaries as adults
Thalassinidea Callianassa subterranea 0–25 25–50 >150 Lindley, 1986 (6)Brachyura Liocarcinus spp. 42 27 >80 Lindley et al., 1994 (12)
Shelf species that use estuaries as nursery habitats
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)
144
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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)
Shelf and slope species
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.
HORIZONTALTRANSPORTOFDECAPOD
LARVAE
145
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
146 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 147
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
148 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 149
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
150 HENRIQUE QUEIROGA AND JACK BLANTON
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.
HORIZONTALTRANSPORTOFDECAPOD
LARVAE
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.
152 HENRIQUE QUEIROGA AND JACK BLANTON
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.
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 153
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
154 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 155
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.
156 HENRIQUE QUEIROGA AND JACK BLANTON
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.
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 157
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
158 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 159
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.
160 HENRIQUE QUEIROGA AND JACK BLANTON
(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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 161
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
162 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 163
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
164 HENRIQUE QUEIROGA AND JACK BLANTON
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
Obligate estuarine species
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)
HORIZONTALTRANSPORTOFDECAPOD
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 )
Infraorder ordivision Species E
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
Shelf species that may penetrate estuaries as adults
Brachyura Libiniaemarginata
F Forward, 1977
Shelf species that use estuaries as nursery habitats
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)
HORIZONTALTRANSPORTOFDECAPOD
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
Shelf and slope species
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 )
Infraorder ordivision Species E
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.
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 169
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.,
170 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 171
(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
172 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 173
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
174 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 175
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
176 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 177
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
178 HENRIQUE QUEIROGA AND JACK BLANTON
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.
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 179
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.
180 HENRIQUE QUEIROGA AND JACK BLANTON
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.
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 181
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.
182 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 183
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
184 HENRIQUE QUEIROGA AND JACK BLANTON
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.
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 185
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,
186 HENRIQUE QUEIROGA AND JACK BLANTON
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.
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 187
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).
188 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 189
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,
190 HENRIQUE QUEIROGA AND JACK BLANTON
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 TRANSPORT OF DECAPOD LARVAE 191
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.
192 HENRIQUE QUEIROGA AND JACK BLANTON
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
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 193
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:
194 HENRIQUE QUEIROGA AND JACK BLANTON
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.
HORIZONTAL TRANSPORT OF DECAPOD LARVAE 195
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.
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214 HENRIQUE QUEIROGA AND JACK BLANTON
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
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 243
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
ADVANCES IN MARINE BIOLOGY VOL. 47 � 2005 Elsevier Ltd.0-12-026148-0 All rights of reproduction in any form reserved
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
218 R. A. BRAITHWAITE AND L. A. MCEVOY
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.
MARINE BIOFOULING ON FISH FARMS AND ITS REMEDIATION 219
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),
220 R. A. BRAITHWAITE AND L. A. MCEVOY
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
MARINE BIOFOULING ON FISH FARMS AND ITS REMEDIATION 221
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.
222 R. A. BRAITHWAITE AND L. A. MCEVOY
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
MARINE BIOFOULING ON FISH FARMS AND ITS REMEDIATION 223
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
224 R. A. BRAITHWAITE AND L. A. MCEVOY
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).
MARINE BIOFOULING ON FISH FARMS AND ITS REMEDIATION 225
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
226 R. A. BRAITHWAITE AND L. A. MCEVOY
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
MARINE BIOFOULING ON FISH FARMS AND ITS REMEDIATION 227
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).
230 R. A. BRAITHWAITE AND L. A. MCEVOY
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
MARINE BIOFOULING ON FISH FARMS AND ITS REMEDIATION 231
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
232 R. A. BRAITHWAITE AND L. A. MCEVOY
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
MARINE BIOFOULING ON FISH FARMS AND ITS REMEDIATION 233
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,
234 R. A. BRAITHWAITE AND L. A. MCEVOY
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
MARINE BIOFOULING ON FISH FARMS AND ITS REMEDIATION 235
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.
236 R. A. BRAITHWAITE AND L. A. MCEVOY
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).
MARINE BIOFOULING ON FISH FARMS AND ITS REMEDIATION 237
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’’
238 R. A. BRAITHWAITE AND L. A. MCEVOY
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
MARINE BIOFOULING ON FISH FARMS AND ITS REMEDIATION 239
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
240 R. A. BRAITHWAITE AND L. A. MCEVOY
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.
MARINE BIOFOULING ON FISH FARMS AND ITS REMEDIATION 241
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
242 R. A. BRAITHWAITE AND L. A. MCEVOY
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.
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252 R. A. BRAITHWAITE AND L. A. MCEVOY
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
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293
ADVANCES IN MARINE BIOLOGY VOL. 47 � 2005 Elsevier Ltd.0-12-026148-0 All rights of reproduction in any form reserved
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
256 C. FRANGOULIS ET AL.
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).
ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES 257
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,
258 C. FRANGOULIS ET AL.
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).
ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES 259
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).
262 C. FRANGOULIS ET AL.
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.
ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES 263
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
264 C. FRANGOULIS ET AL.
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).
ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES 265
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
266 C. FRANGOULIS ET AL.
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
ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES 267
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
268 C. FRANGOULIS ET AL.
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
ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES 269
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:
270 C. FRANGOULIS ET AL.
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
ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES 271
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;
272 C. FRANGOULIS ET AL.
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.
ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES 273
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
276 C. FRANGOULIS ET AL.
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
ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES 277
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
278 C. FRANGOULIS ET AL.
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.
ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES 279
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
280 C. FRANGOULIS ET AL.
(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
ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES 281
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
282 C. FRANGOULIS ET AL.
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
ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES 283
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,
284 C. FRANGOULIS ET AL.
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,
ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES 285
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.
286 C. FRANGOULIS ET AL.
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.
ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES 287
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
288 C. FRANGOULIS ET AL.
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
ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES 289
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
290 C. FRANGOULIS ET AL.
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
292 C. FRANGOULIS ET AL.
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.
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ROLE OF COPEPOD OUTFLUXES IN THE CARBON AND NITROGEN CYCLES 309
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TAXONOMIC INDEX
Acartia clausi, 260, 266, 274, 275
populations of, 74, 74
Acartia spp., 57–8
Acartia tonsa, 260, 266, 274
eggs of, 262
Aglantha digitalis, 32, 36, 43
Alaria esculenta, 47–8
Alosa finta, 53
Amphora coffeaeformis, 224–5
Anapagurus laevis, 114–6
Anapagurus sp., 114–6
Anomalocera patersoni, 274, 279
Antithamnion sp., 231
Apogon coccineus, 53
Ascidiella aspersa, 216, 226, 229
Atelecyclus rotundatus, 75, 142, 145, 146
Atelecyclus sp., 142
Balanus amphitrite, 227
Balanus perforatus, 42–3, 46–7
Balanus sp., 229
Balistes capriscus, 53
Biddulphia sinensis, 30, 73
Biddulphia spp., 30, 228
Botrylloides sp., 229
Branchiostoma lanceolatum, 64
Brongniartella australis, 228
Bryopsis sp., 228
Bugula neritina, 229
Cafeteria sp., 275
Calanus finmarchicus, 41, 64, 260,
261, 274
faecal pellet production in, 266–7
Calanus glacialis, 64, 260
Calanus helgolandicus, 32, 64, 75,
261, 266
abundance of, 57–8
diet/metabolism of, 41
faecal pellet size of, 267
as indicator species, 37, 37, 38–9
as pelagic fish food, 40–1
seasonal variability in, 58, 59, 73–4, 79
at station L4, 57, 59
zooplankton and, 73–4
Calanus hyperboreus, 64, 260
Calanus pacificus, 79, 260
Calanus tenuicornis, 66
Caligus elongatus, 64
Callianassa subterranea, 140, 144, 146
Callianassa tyrrhena, 116
Callinectes sapidus, 140, 144, 166
barokinesis of, 171
current orientation and, 180, 182
decapod larvae dispersal and, 132
diel rhythms and, 186
export/reinvasion by, 150, 152, 153
light stimulus and, 174, 176–7
megalopae of, 180, 182, 185–6
salinity and, 178
turbulence and, 181
Callionymus lyra, 51
Campylodiscus sp., 228
Cancer gracilis, 168
Cancer irroratus, 168, 174, 241
geotaxis and, 170
Cancer magister, 141, 166
megalopae of, 146–7, 189
migration of, 143, 153, 189
zoea of, 170
Cancer oregonensis, 141
megalopae of, 147
migration of, 143
Cancer spp., 142, 145
larvae of, 155
Candacia armata, 32, 64
Caprella sp., 229
Carassius carassius, 240–1
Carcinus aestuarii, 140
Carcinus maenas, 116, 140, 144, 171
endogenous rhythms of, 182–4, 185
export/reinvasion by, 143, 146–7, 150,
152, 166
megalopae of, 160, 180, 182, 184,
185–6, 194
tides and, 153
vertical distribution and, 150
wind-driven transport of, 160–1
zoea of, 160
Cavolinia spp., 64
Centropages hamatus, 275
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
This Page Intentionally Left Blank
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
at station L4, 57, 59
zooplankton and, 73–4
Callinectes sapidus
current orientation and, 180, 182
in decapod larvae dispersal, 132
diel rhythms and, 186
estuary exportreinvasion by, 150, 152, 153
light stimulus and, 176–7
megalopae of, 180, 182, 185–6
salinity and, 178
Callionymus lyra (dragonet)
warming and, 51
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
sea temperature and, 55
Dentalium vulgare
sea temperature and, 55
Diatom blooms, 21, 28 see also
Dinoflagellate blooms; Flagellate blooms
Biddulphia sinensisin, 73
Coscinodiscus wailesii in, 30, 73, 74
light effect on, 26–7
NAO and, 58
nutrient vertical distribution and,
24, 27
seasonality of, 25, 26, 58, 72
silicate concentration and, 22, 24
temperature and, 24
types of, 28
zooplankton grazers and, 26–7
Diatoms
in fish farm biofouling, 224–5
Diel cycles, 72
Callinectes sapidus and, 186
decapod larvae cycles and, 110–11, 117,
125, 126, 143, 149
decapod larvae dispersal and, 110–11, 117,
137–8, 149
decapod larvae migrations and, 154–5,
156, 157–9
Penaeus spp. migration and, 157–9
Plebejus penaeus migration and, 153
vertical migrations and, 279, 289
Dinoflagellate blooms, 28, 29, 54, 55 see also
Diatom blooms; Flagellate blooms
Ceratium spp. and, 73
Gyrodinium aureolum and, 58
Prorocentrum spp. and, 73
seasonality of, 25, 26, 58, 72–3
Diseases, in fish farms, 3, 57
amoebic gill disease, 220, 239
from antibiotic use, 221
DO concentration and, 221
Hysterothylacium aduncum in, 220
phytoplankton poisoning, 220
Renibacterium salmoninarum and, 221
sea louse, 220
stress shock, 220
Dissolved matter (DM)
in copepod outfluxes, 255–6, 280–2
Dissolved organic carbon (DOC), 258, 263,
276, 289
Dissolved organic nitrogen (DON), 20, 22,
23, 24, 276
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)
sea temperature and, 55
Echinus esculentus (sea urchin)
cold-water plankton and larvae, 43
culturing of, 43
Ecosystem models
bay simulations and, 19
continuous measurement in, 18
high-resolution data, 3
long-term time series, 3
stimulus response and, 169, 170–80
wind-induced currents and, 18
Ectocarpus spp.
in fish farm biofouling, 227, 230–1
Eddystone reef, 8, 9
Edinburgh Oceanographic Laboratory, 7
Ekman flow, 121, 122, 123, 148
winds from, 155, 156
Eledone cirrhosa
cool-water octopus, 55
Endogenous rhythms
Carcinus maenas and, 182–4, 185
competitive advantages of, 163–4
in decapod larvae dispersal, 110, 163–4,
181–6
Penaeus duodarum and, 184
English Channel, long-term research, 2–3
benthos in, 54–5
CPR analysis in, 63–70
CPR method consistency and, 70, 71, 72
currents/circulation and, 16–9
data limitations in, 77
data reexamination in, 79
demersal fish and, 48–54
drift-bottle data, 16
ecology/species changes and, 77–8
historical background of, 3–9
importance of, 76–7
intertidal observations in, 42–8
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)
at station L4, 56, 61
Feeding dynamics, 3
Fish farm biofouling/remediation
alternate strategies, 216
antifoulant technology, 231–3
aquaculture trends and, 217
beneficial effects of, 221–2
biological control/grazing in,
240–1, 242–3
detrimental effects of, 219–21
diatoms in, 224–5
diseases in fish farms and, 220, 221
economic consequences of, 222
external factors in, 224
fish farm v. ship methods in, 216
fouling process in, 224–5
fouling taxa, 226, 228–31
legislation in, 235
macroalgae and, 227, 230–1
macrofouling and, 225
nontoxic antifoulants,
238–40, 242–3
records on, 216–17
toxic antifouling materials,
233–4, 237
Fisheries
cyclical populations of, 41, 43
exploitation of, 3, 55
herring, 2, 6, 35, 39–40
mackerel, 6, 35, 76
pilchards, 35, 39–40
pollution of, 3
sardines, 29
unsustained harvesting of, 51–2
Fixed-station sampling
in decapod larvae dispersal, 110, 139
estuaries and, 110, 139, 146
limitations of, 139
Flagellate blooms see also Diatom blooms;
Dinoflagellate blooms
types of, 28
Flounder
spawning migration of, 50
Fluorescence
in bio-optics/photosynthesis, 58
Food-web
influences on, 57, 78, 79
planktonic, 57
FRRF. see Fast Repitition Rate Fluorometre
Gadus morrhua (cod)
cooling and, 52–3
TBT and, 238
Gibbula umbilicalis, 47
GLOBEC, 9
Government Development Commission
research expansion, 6
Gulf of Carpentaria
decapod larvae dispersal study and, 157–9
Gulf stream, 134–5
Gyrodinium aureolum
in dinoflagellate blooms, 58
Haddock
distribution changes in, 76
Health and Safety Executive (HSE), 234
Hermit crabs, 47
Herring
competition with pilchard and, 78
fisheries, 2, 6, 35, 37, 39–40
Hippoglossoides platessoides (long rough dab)
distribution changes in, 76
Horizontal transport of decapod
larvae,105–11. see Decapod larvae
behavioural control evidence in, 164, 165–8,
169, 170–86
continental margins in, 132–5
cross shelf flow/exchange in, 121–3
depth regulation mechanisms in, 187–8
diel cycles in, 137–8
diel migrations in, 154–5, 156, 157–9
ecological categories in, 117–18
endogenous rhythms in, 163–4, 181–6
estuarine transport in, 124–7, 128, 130
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
environmental change and, 2
Light
attenuation in water and, 27
measurements of, 27
pigments, in transmission of, 27–8
Limpets, 42, 46, 47
LOIS see Land-Ocean Interaction Study
Loligo forbesi (squid)
migration of, 50
species composition of, 55
Loligo vulgaris (squid)
species composition of, 55
Longhurst-Hardy Plankton Recorder, 138
Low-income food-deficit countries
LIFDC), 217, 241
Mackerel
fisheries, 6, 76
Macroalgae, 47–8
MAFF, 80
MarClim see Marine Biodiversity and
Climate Change Consortium
Marine Biodiversity and Climate Change
Consortium (MarClim), 80
Marine Biological Association of the United
Kingdom (MBA), 2–3, 80, 82
ICES stations and, 9–10, 11, 12
imaging and, 14, 31
IMER merger with, 7–8
Marine Environmental Change Network
(MECN), 80
Marine optics research
light attenuation in, 27
measurements of light in, 27
pigments/light transmission in, 27–8
MBA see Marine Biological Association
of the United Kingdom
Mean tide level (MTL), 42–3
MECN see Marine Environmental
Change Network
Megalopae
of Callinectes sapidus, 180, 182, 185–6
of Carcinus maenas, 160, 180, 182, 185–6
definition of, 185
in estuaries, 110, 123, 126, 129, 132, 176–7
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)
distribution changes in, 76
MERIS ocean colour sensor on
ENVISAT, 61
Mesoscale hydrography in long-term
research, 76
Mesozooplankton
copepods and, 255–6
global importance, 255–6
productivity and, 38–9
sampling of, 33, 36, 37, 38
seasonality, 29, 31
Messhai nets, 138
Micromesistius poutassou (blue whiting)
distribution changes in, 76
MOCNESS nets, 138
Moulting
in copepod excretion, 262, 284–5, 286
decapod larvae and, 111, 155
in megalopae, 148
moulting rate in copepods and,
267–8, 284–5
MTL see Mean tide level
Munida bamffica
sea temperature and, 55
Mytilus edulis (blue mussel)
marine biofouling/remediation and,
216, 226
Nanoplankton, 25
NAO see North Atlantic Oscillation
National Institute of Oceanography, 18
NATO see North Atlantic Treaty
Organization
Natural Environment Research Council
(NERC)
IMER and, 7
Natural product antifoulant (NPA), 232
Neoparamoeba pemaquidensis
amoebic gill disease pathogen, 220, 239
NERC see Natural Environment
Research Council
Nets
Messhai, 138
MOCNESS, 138
Neuston, 148
sampling, 16, 30, 33, 34–5, 56, 81
Neuston layer, 137–8
wind effects on, 155
zoea in, 153
Neuston nets, 148
Nitrates, inorganic
as nutrient, 19–20, 22, 24
Nitrogen
in copepod outfluxes, 256–7, 282–92
as NH4 in copepod excretion,
256–7, 269
uptake by phytoplankton, 290
Nitrogen, dissolved organic
as nutrient, 20, 22, 23, 24
NLB see Nonleaching biocide
Nonleaching biocide (NLB), 232
North Atlantic Oscillation (NAO), 2–3
climate and, 78–9
currents/circulation relationship
to, 18
diatom blooms and, 58
plankton blooms and, 58, 60
temperature/salinity relationship to, 16
water temperature/salinity in, 16
wind-driven component of, 18–9
North Atlantic Treaty Organization (NATO)
sardine fisheries and, 29
NPA see Natural product antifoulant
Nucella lapillus (dogwhelk)
TBT and, 48
Nutrient
copepod excretion role in, 280–1
Nutrient signals, 25, 26
phytoplankton composition and, 24, 27
Nutrients
carbon as, 20, 21, 26
dissolved organic nitrogen as, 20, 22,
23, 24, 276
dissolved organic phosphorus as,
20–1, 23, 286
inorganic nitrates as, 19–20, 22, 24
inorganic phosphates as, 19–21,
22, 23
nitrate-phosphate ratio, 21
regeneration in copepod outfluxes,
289–90
silicates as, 22
324 SUBJECT INDEX
Octopus vulgaris
sea temperature and, 55
Ontogenetic influences
in decapod larvae, 112, 116
in decapod larvae dispersal, 117, 159–61
vertical distribution in decapods and,
143–8
Osilinus lineatus, 47
Panulirus cygnus
nocturnal migrations of, 159
ontogenetic dispersal in, 117, 159–61
phyllosoma stages in, 159
PAR see Photosynthetically active radiation
Parasagitta elegans
as indicator species, 35–6, 38–9
population cycles of, 41, 43
Parasagitta setosa
as indicator species, 35–6, 38–9
Particulate matter (PM)
in copepod outfluxes, 255–6, 280–2
Patella spp., 42, 46
depressa, 47
PDMS see Polydimethylsiloxan
Pelagic fish
Calanus helgolandicus as food
for, 40–1
environmental change and, 2, 39
fishing intensity and, 39
Penaeus duodarum
endogenous rhythms of, 184
Penaeus plebejus
estuary export/reinvasion by, 153
Penaeus spp.
diel migration pattern of, 157–9
Gulf of Carpentaria study and, 157
plebejus, diel migration pattern
of, 153
Peritrophic membrane
in copepod faecal pellets, 258, 272, 286
roles of, 258
Phosphates, inorganic
as nutrient, 19–21, 22, 23
in pollution, 9
seasonal variations in, 20, 21, 22, 23
Phosphorus
copepod excretion and, 257, 269, 286
Phosphorus, dissolved organic
as nutrient, 20–1, 23, 286
Photosynthetically active radiation (PAR)
in bio-optics/photosynthesis, 60
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.
in dinoflagellate blooms, 73
Proudman Oceanographic Laboratory
Coastal Ocean Modelling System
(POLCOMS), 80
Pseudocalanus spp.
at station L4, 57–8
Quantitative long-term data, 15
Quantitative measurement techniques 14C
uptake analysis in, 21, 28
in marine chemistry, 19
sampling for, 25, 34
Raja brachyura (blond ray)
decline of, 51–2
Rate of change hypothesis
in zooplankton, 174, 176
Remote Sensing Data Analytical
Service (RSDAS)
imaging and, 14, 31
Research vessels, 4, 5–6
Rhithropanopeus harrisii
depth regulation of, 174–5, 187
in estuaries, 148, 151, 170,
173–8
phototaxis in, 175
response to stimuli in, 173–7
tidal migrations of, 181–2, 185
water column migration and, 150, 151,
152, 182
RSDAS see Remote Sensing Data
Analytical Service
Russell Cycle, 37, 78
SAHFOS. see Sir Alister Hardy Foundation
for Ocean Science
Salinity
autoanalytical techniques
and, 7
changes in, 177–9
circulation and, 13, 15
decapod larvae dispersal and,
110–11, 189–90, 266
in estuaries, 127
photataxis changes with, 178
rainfall/windstrength and, 16
run-off and, 13, 15
seasonal trends and, 13, 15
Sv unit and, 15
water temperature in English channel and,
12, 13–19
water temperature/NAO and, 16
Sampling programs, 5–6, 34–5
continuous measurement in, 18
drift-bottle method in, 16
drifting buoys in, 18
fixed-station sampling, 110, 139, 146
long-term data summary of, 57
nets used in, 16, 30, 33, 34–5, 56, 81
for quantitative measurement, 25, 34
sampling methods of, 16
station E1 and, 61, 81
station L4 and, 8–9, 56–8, 59, 60, 61, 80
stations L1/E5 and, 8–9, 80–1
stations off Plymouth and, 7–9
stations/South West England and, 45–6
time-series measurement in, 40–1
tow-net method in, 15, 25, 30
for zooplankton, 16
Sardina pilchardus (pilchard), 37, 38–40
cyclical populations of, 41, 43
Sardines
fisheries of, 29
Scomber scombrus (mackerel)
distribution changes in, 76
Scottish Oceanographic Laboratory
relationship to SAFHO/SIMER, 61
Sea Viewing Wide Field-of-view Sensor
(SeaWiFS), 29, 31
validation by buoys, 61
Selective tidal stream transport (STST) in
decapod larvae dispersal, 149–50
Semibalanus spp.
balanoides, 46
cold-water species of, 46
Silicate
in diatom blooms, 22, 24
as nutrient, 22
Sir Alister Hardy Foundation for Ocean
Science (SAHFOS), 2, 3
CPR surveys and, 9, 61, 80, 82
relationship to Scottish Oceanographic
Laboratory, 61
Squid, veined
migration of, 50
species composition of, 55
St. George’s Channel, 18
Straits of Dover
currents/circulation in, 19
STST see Selective tidal stream transport
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
sea temperature and, 55
Vertical fates
of copepod outfluxes, 254, 287–90
Vertical flux (VF)
equation for, 269–70
sedimentation rate and, 269–70
sinking speed, 270–2
Vertical flux, passive
biodegradation/microorganisms influenced,
278–9, 288
in copepod excretion, 270–2, 274–5
coprophagy in, 277–8
coprorhexy/coprochaly in, 276–7
molecular diffusion/physical degradation
and, 273–6
Stokes’ equation and, 270, 272
stratification/turbulent diffusion
and, 273
vertical advection and, 272–3
Vertical migrations
diel cycles and, 279, 289
field studies in, 148–61
horizontal transport of decapod larvae and,
116–17, 137–43
of megalopae, 146–7
modifiers of decapod larvae dispersal,
188–90
nonrhythmic, 186–7
positioning in decapod larvae dispersal,
108–10
water column and, 146, 161,
162, 171
of zoea, 150
Viruses, 3, 25, 57
Water column, 3, 9
copepod outfluxes and, 292
DOC in, 269–70, 282–3, 289
DON in, 24
horizontal transport in decapod larvae and,
110, 116, 117, 121, 126–7, 133, 138
larval velocity in, 194–5
light influence in, 177, 188
MECN research on, 80
PM in, 292
position importance in transport
and, 161
Rhithropanopeus harrisii migration and,
150, 151, 152, 182
SMART buoy data on, 81
surface temperature, 12, 13
temperature influence in, 187–8
tidal influence in, 182, 185
turbulence influence in, 180
vertical flux in, 269–70
vertical migrations in decapod larvae
and, 146, 161, 163, 171
vertical position in, 161, 163, 171
vertical stability in, 29, 72, 76
Water temperature, 3
autoanalytical techniques
and, 7
column, 13, 14, 16, 187–8
estuaries and, 127
geotaxis changes with, 179
long term trends and, 13
rainfall/windstrength and, 16
salinity in English channel and,
12, 13–19
salinity of NAO and, 16
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
autoanalytical techniques
and, 7
Wind effects
continental margins and, 132–5
cross-shelf, 121, 122, 123–4
on current/scirculation, 19, 58
diurnal fluctuations, 124
Ekman flow and, 121, 122, 123,
148, 155, 156
Langmuir circulation and, 148
on NAO, 18–19
on neuston layer, 155
on salinity, 16
sea/land breezes, 124, 148
on water temperature, 18
wind-generated exchange
in, 131–2
Wind-driven component
cross-shelf, 121, 122, 123–4
in NAO, 18–19
Zoea, 116, 123, 129, 146
of Carcinus maenas, 160
definition of, 185
depth regulation of, 173–5
in neuston layer, 153
night ebb tides and, 150, 152
pressure/gravity and, 170–1
semilunar export of, 154
vertical migration of, 150
Zooplankton see also Mesozooplankton
Acartia clausi and, 74
biomass indicators in, 21, 28, 32, 35,
36, 37, 38
Calanus helgolandicus and, 73–4
Centropages typicus and, 74
environmental change and, 2
preferendum hypothesis/light intensity
and, 174, 176
rate of change hypothesis in, 174, 176
sampling methods for, 16
seasonality of, 73–5
surveys of, 10, 73–6
zooplankton grazers and, 26
Zostera marina (eelgrass)
in fish farm biofouling, 232
328 SUBJECT INDEX