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Modelling the evolutionary effects of a coastal marine reserve on different ecological guilds of fish

Published online by Cambridge University Press:  01 September 2010

Tanja Miethe ,
Jonathan W. Pitchford  and
Calvin Dytham
Tanja Miethe*
Affiliation:
Department of Biology, University of York, PO Box 373, YO10 5YW, UK York Centre for Complex Systems Analysis, University of York, PO Box 373, YO10 5YW, UK
Jonathan W. Pitchford
Affiliation:
Department of Biology, University of York, PO Box 373, YO10 5YW, UK York Centre for Complex Systems Analysis, University of York, PO Box 373, YO10 5YW, UK
Calvin Dytham
Affiliation:
Department of Biology, University of York, PO Box 373, YO10 5YW, UK
*
Correspondence should be addressed to: T. Miethe, Max Planck Institute for Demographic Research, Konrad-Zuse-Strasse 1, 18057 Rostock, Germany email: [email protected]
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Abstract

Marine reserves are used as a management tool to ensure sustainability of fish stocks. Using an individual-based model, we compare the evolutionary effect of a reserve located on a nursery ground, spawning ground, feeding ground, or in a year-round habitat for sedentary species. We model the evolution of life-history traits, specifically size at maturation and site fidelity. Within species, individuals will differ in the time spent within a reserve depending on their patterns of movement and migration. We predict that the evolutionary effect of fishing depends not only on the survival probability but also on the life-history stages primarily affected by high harvest mortality. Protection against evolution to small maturation size is most effective where a reserve protects a sedentary population or protects the feeding grounds of a population. We also find that protection of the feeding ground of an anadromous stock such as Atlantic salmon may lead to local adaptation enhanced by evolution of higher site fidelity, similar to protection of a sedentary species.

Keywords

fisheries-induced evolutionhomingmarine protected areaoverfishingsize selectivityspillover
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 91 , Special Issue 6: Fish Ecology , September 2011 , pp. 1369 - 1380
Copyright
Copyright © Marine Biological Association of the United Kingdom 2010

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References

REFERENCES

Abella, A.J., Caddy, J.F. and Serena, F. (1997) Do natural mortality and availability decline with age? An alternative yield paradigm for juvenile fisheries, illustrated by the hake Merluccius merluccius fishery in the Mediterranean. Aquatic Living Resources 10, 257–269.CrossRefGoogle Scholar
Able, K.W. (2005) A re-examination of fish estuarine dependence: evidence for connectivity between estuarine and ocean habitats. Estuarine, Coastal and Shelf Science 64, 5–17.CrossRefGoogle Scholar
Agardy, T., Bridgewater, P., Crosby, M.P., Day, J., Dayton, P.K., Kenchington, R., Laffoley, D., Mcconney, P., Murray, P.A., Parks, J.E. and Peau, L. (2003) Dangerous targets? Unresolved issues and ideological clashes around marine protected areas. Aquatic Conservation: Marine and Freshwater Ecosystems 13, 1–15.CrossRefGoogle Scholar
Andersen, K.H. and Brander, K. (2009) Expected rate of fisheries-induced evolution is slow. Proceedings of the National Academy of Sciences of the United States of America 106, 11657–11660.CrossRefGoogle ScholarPubMed
Anderson, C.N.K., Hsieh, C.H., Sandin, S.A., Hewitt, R., Hollowed, A., Beddington, J., May, R.M. and Sugihara, G. (2008) Why fishing magnifies fluctuations in fish abundance. Nature 452, 835–839.CrossRefGoogle ScholarPubMed
Apostolaki, P., Milner-Gulland, E.J., McAllister, M.K. and Kirkwood, G.P. (2002) Modelling the effects of establishing a marine reserve for mobile fish species. Canadian Journal of Fisheries and Aquatic Sciences 59, 405–415.CrossRefGoogle Scholar
Arnold, G.P. and Metcalfe, J.D. (1996) Seasonal migrations of plaice (Pleuronectes platessa) through the Dover Strait. Marine Biology 127, 151–160.CrossRefGoogle Scholar
Ashley, M.V., Willson, M.F., Pergams, O.R.W, O'Dowd, D.J., Gende, S.M. and Brown, J.S. (2003) Evolutionarily enlightened management. Biological Conservation 111, 115–123.CrossRefGoogle Scholar
Barot, S., Heino, M., Morgan, M.J. and Dieckmann, U. (2005) Maturation of Newfoundland American plaice (Hippoglossoides platessoides): long-term trends in maturation reaction norms despite low fishing mortality? ICES Journal of Marine Science 62, 56–64.CrossRefGoogle Scholar
Baskett, M.L., Levin, S.A., Gaines, S.D. and Dushoff, J. (2005) Marine reserve design and the evolution of size at maturation in harvested fish. Ecological Applications 15, 882–901.CrossRefGoogle Scholar
Baskett, M.L., Micheli, F. and Levin, S.A. (2007a) Designing marine reserves for interacting species: insights from theory. Biological Conservation 137, 163–179.CrossRefGoogle Scholar
Baskett, M.L., Weitz, J.S. and Levin, S.A. (2007b) The evolution of dispersal in reserve networks. American Naturalist 170, 59–78.CrossRefGoogle ScholarPubMed
Beck, M.W., Heck, K.L., Able, K.W., Childers, D.L., Eggleston, D.B., Gillanders, B.M., Halpern, B., Hays, C.G., Hoshino, K., Minello, T.J., Orth, R.J., Sheridan, P.F. and Weinstein, M.R. (2001) The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. BioScience 51, 633–641.CrossRefGoogle Scholar
Beets, J. and Friedlander, A. (1999) Evaluation of a conservation strategy: A spawning aggregation closure for red hind, Epinephelus guttatus, in the US Virgin Islands. Environmental Biology of Fishes 55, 91–98.CrossRefGoogle Scholar
Bergstad, O.A., Jørgensen, T., Knutsen, J.A. and Berge, J.A. (2008) Site fidelity of Atlantic cod Gadus morhua L. as deduced from telemetry and stable isotope studies. Journal of Fish Biology 72, 131–142.CrossRefGoogle Scholar
Beverton, R.J.H. and Holt, S.J. (1957) On the dynamics of exploited fish populations. Caldwell, NJ: Blackburn Press.Google Scholar
Biro, P.A. and Post, J.R. (2008) Rapid depletion of genotypes with fast growth and bold personality traits from harvested fish populations. Proceedings of the National Academy of Sciences of the United States of America 105, 2919–2922.CrossRefGoogle ScholarPubMed
Botsford, L.W., Micheli, F. and Hastings, A. (2003) Principles for the design of marine reserves. Ecological Applications 13, S25–S31.CrossRefGoogle Scholar
Botsford, L.W., Brumbaugh, D.R., Grimes, C., Kellner, J.B., Largier, J., O'Farrell, M.R., Ralston, S., Soulanille, E. and Wespestad, V. (2009) Connectivity, sustainability, and yield: bridging the gap between conventional fisheries management and marine protected areas. Reviews in Fish Biology and Fisheries 19, 69–95.CrossRefGoogle Scholar
Bradbury, I.R., Laurel, B.J., Robichaud, D., Rose, G.A., Snelgrove, P.V.R., Gregory, R.S., Cote, D. and Windle, M.J.S. (2008) Discrete spatial dynamics in a marine broadcast spawner: re-evaluating scales of connectivity and habitat associations in Atlantic cod (Gadus morhua L.) in coastal Newfoundland. Fisheries Research 91, 299–309.CrossRefGoogle Scholar
Burke, J.S., Kenworthy, W.J. and Wood, L.L. (2009) Ontogenetic patterns of concentration indicate lagoon nurseries are essential to common grunts stocks in a Puerto Rican bay. Estuarine, Coastal and Shelf Science 81, 533–543.CrossRefGoogle Scholar
Coleman, F.C., Baker, P. and Koenig, C.C. (2004) A review of Gulf of Mexico marine protected areas: successes, failures, and lessons learned. Fisheries 29, 10–21.CrossRefGoogle Scholar
Conover, D.O. (2000) Darwinian fisheries science. Marine Ecology Progress Series 208, 303–307.Google Scholar
Conover, D.O., Munch, S.B. and Arnott, S.A. (2009) Reversal of evolutionary downsizing caused by selective harvest of large fish. Proceedings of the Royal Society B—Biological Sciences 276, 2015–2020.CrossRefGoogle ScholarPubMed
De Mitcheson, Y.S., Cornish, A., Domeier, M., Colin, P.L., Russell, M. and Lindeman, K.C. (2008) A global baseline for spawning aggregations of reef fishes. Conservation Biology 22, 1233–1244.CrossRefGoogle Scholar
Dunlop, E.S., Baskett, M.L., Heino, M. and Dieckmann, U. (2009) Propensity of marine reserves to reduce the evolutionary impacts of fishing in a migratory species. Evolutionary Applications 2, 371–393.CrossRefGoogle Scholar
Dytham, C. (2003) How landscapes affect the evolution of dispersal behaviour in reef fishes: results from an individual-based model. Journal of Fish Biology 63, 213–225.CrossRefGoogle Scholar
Dytham, C. and Travis, J.M.J. (2006) Evolving dispersal and age at death. Oikos 113, 530–538.CrossRefGoogle Scholar
Elliott, M., Whitfield, A.K., Potter, I.C., Blaber, S.J.M., Cyrus, D.P., Nordlie, F.G. and Harrison, T.D. (2007) The guild approach to categorizing estuarine fish assemblages: a global review. Fish and Fisheries 8, 241–268.CrossRefGoogle Scholar
Enberg, K., Dunlop, E.S., Jørgensen, C., Heino, M. and Dieckmann, U. (2009) Implications of fisheries-induced evolution for stock rebuilding and recovery. Evolutionary Applications 2, 394–414.CrossRefGoogle ScholarPubMed
Franco, A., Elliott, M., Franzoi, P. and Torricelli, P. (2008) Life strategies of fishes in European estuaries: the functional guild approach. Marine Ecology Progress Series 354, 219–228.CrossRefGoogle Scholar
Frank, K.T., Petrie, B., Choi, J.S. and Leggett, W.C. (2005) Trophic cascades in a formerly cod-dominated ecosystem. Science 308, 1621–1623.CrossRefGoogle Scholar
Fraser, D.J. and Bernatchez, L. (2005) Adaptive migratory divergence among sympatric brook charr populations. Evolution 59, 611–624.Google ScholarPubMed
Gårdmark, A., Dieckmann, U. and Lundberg, P. (2003) Life-history evolution in harvested populations: the role of natural predation. Evolutionary Ecology Research 5, 239–257.Google Scholar
Gerber, L.R., Heppell, S.S., Ballantyne, F. and Sala, E. (2005) The role of dispersal and demography in determining the efficacy of marine reserves. Canadian Journal of Fisheries and Aquatic Sciences 62, 863–871.CrossRefGoogle Scholar
Godø, O.R. (2003) Fluctuation in stock properties of Northeast Arctic cod related to long-term environmental changes. Fish and Fisheries 4, 121–137.CrossRefGoogle Scholar
Graham, R.T., Carcamo, R., Rhodes, K.L., Roberts, C.M. and Requena, N. (2008) Historical and contemporary evidence of a mutton snapper (Lutjanus analis Cuvier, 1828) spawning aggregation fishery in decline. Coral Reefs 27, 311–319.CrossRefGoogle Scholar
Haedrich, R.L. and Barnes, S.M. (1997) Changes over time of the size structure in an exploited shelf fish community. Fisheries Research 31, 229–239.CrossRefGoogle Scholar
Hart, P.J.B. and Reynolds, J.D. (eds) (2002) Handbook of fish biology and fisheries. Oxford: Blackwell Science Ltd.Google Scholar
Hauser, L. and Carvalho, G.R. (2008) Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish and Fisheries 9, 333–362.CrossRefGoogle Scholar
Heino, M. (1998) Management of evolving fish stocks. Canadian Journal of Fisheries and Aquatic Sciences 55, 1971–1982.CrossRefGoogle Scholar
Hilborn, R., Branch, T.A., Ernst, B., Magnussson, A., Minte-Vera, C.V., Scheuerell, M.D. and Valero, J.L. (2003) State of the world's fisheries. Annual Review of Environment and Resources 28, 359–399.CrossRefGoogle Scholar
Hoff, G.R. (2008) A nursery site of the Alaska skate (Bathyraja parmifera) in the eastern Bering Sea. Fishery Bulletin 106, 233–244.Google Scholar
Horwood, J.W., Nichols, J.H. and Milligan, S. (1998) Evaluation of closed areas for fish stock conservation. Journal of Applied Ecology 35, 893–903.CrossRefGoogle Scholar
Hsieh, C.H., Reiss, C.S., Hunter, J.R., Beddington, J.R., May, R.M. and Sugihara, G. (2006) Fishing elevates variability in the abundance of exploited species. Nature 443, 859–862.CrossRefGoogle ScholarPubMed
Hu, L.M. and Wroblewski, J.S. (2009) Conserving a subpopulation of the northern Atlantic cod metapopulation with a marine protected area. Aquatic Conservation: Marine and Freshwater Ecosystems 19, 178–193.CrossRefGoogle Scholar
Hutchings, J.A. and Fraser, D.J. (2008) The nature of fisheries- and farming-induced evolution. Molecular Ecology 17, 294–313.CrossRefGoogle ScholarPubMed
Jennings, S., Greenstreet, S.P.R. and Reynolds, J.D. (1999) Structural change in an exploited fish community: a consequence of differential fishing effects on species with contrasting life histories. Journal of Animal Ecology 68, 617–627.CrossRefGoogle Scholar
Jennings, S., Kaiser, M.J. and Reynolds, J.D. (2001) Marine fisheries ecology. Oxford: Blackwell Publishing.Google Scholar
Jørgensen, T. (1990) Long-term changes in age at sexual maturity of Northeast Arctic Cod (Gadus morhua L). Journal du Conseil International pour l'Exploration de la Mer 46, 235–248.CrossRefGoogle Scholar
Jørgensen, C., Enberg, K., Dunlop, E.S., Arlinghaus, R., Boukal, D.S., Brander, K., Ernande, B., Gårdmark, A., Johnston, F., Matsumuru, S., Pardoe, H., Rabb, K., Silva, A., Vainikka, A., Dieckmann, U., Heino, M. and Rijnsdorp, A.D. (2007) Ecology—managing evolving fish stocks. Science 318, 1247–1248.CrossRefGoogle ScholarPubMed
Klemetsen, A., Amundsen, P.A., Dempson, J.B., Jonsson, B., Jonsson, N., O'Connell, M.F. and Mortensen, E. (2003) Atlantic salmon Salmo salar L., brown trout Salmo trutta L. and Arctic charr Salvelinus alpinus (L.): a review of aspects of their life histories. Ecology of Freshwater Fish 12, 1–59.CrossRefGoogle Scholar
Knutsen, H., Jorde, P.E., André, C. and Stenseth, N.C. (2003) Fine-scaled geographical population structuring in a highly mobile marine species: the Atlantic cod. Molecular Ecology 12, 385–394.CrossRefGoogle Scholar
Kuparinen, A. and Merilä, J. (2007) Detecting and managing fisheries-induced evolution. Trends in Ecology and Evolution 22, 652–659.CrossRefGoogle ScholarPubMed
Law, R. (2000) Fishing, selection, and phenotypic evolution. ICES Journal of Marine Science 57, 659–668.CrossRefGoogle Scholar
Law, R. (2007) Fisheries-induced evolution: present status and future directions. Marine Ecology Progress Series 335, 271–277.CrossRefGoogle Scholar
Law, R. and Grey, D.R. (1989) Evolution of yields from populations with age-specific cropping. Evolutionary Ecology 3, 343–359.CrossRefGoogle Scholar
Limburg, K.E., Walther, Y., Hong, B., Olson, C. and Stora, J. (2008) Prehistoric versus modern Baltic Sea cod fisheries: selectivity across the millennia. Proceedings of the Royal Society B—Biological Sciences 275, 2659–2665.CrossRefGoogle ScholarPubMed
Loher, T. (2008) Homing and summer feeding site fidelity of Pacific halibut (Hippoglossus stenolepis) in the Gulf of Alaska, established using satellite-transmitting archival tags. Fisheries Research 92, 63–69.CrossRefGoogle Scholar
Longhurst, A. (2002) Murphy's law revisited: longevity as a factor in recruitment to fish populations. Fisheries Research 56, 125–131.CrossRefGoogle Scholar
Mangel, M. (2000) Trade-offs between fish habitat and fishing mortality and the role of reserves. Bulletin of Marine Science 66, 663–674.Google Scholar
Marshall, C.T. and McAdam, B.J. (2007) Integrated perspectives on genetic and environmental effects on maturation can reduce potential for errors of inference. Marine Ecology Progress Series 335, 301–310.CrossRefGoogle Scholar
McDowall, R.M. (2008) Diadromy, history and ecology: a question of scale. Hydrobiologia 602, 5–14.CrossRefGoogle Scholar
McQuinn, I.H. (1997) Metapopulations and the Atlantic herring. Reviews in Fish Biology and Fisheries 7, 297–329.CrossRefGoogle Scholar
Miethe, T., Pitchford, J. and Dytham, C. (2009) An individual-based model for reviewing marine reserves in the light of fisheries-induced evolution in mobility and size at maturation. Journal of Northwest Atlantic Fisheries Science 41, 151–162.Google Scholar
Miethe, T., Dytham, C., Dieckmann, U. and Pitchford, J. (2010) Marine reserves and the evolutionary effects of fishing on size at maturation. ICES Journal of Marine Science 67, 412–425.CrossRefGoogle Scholar
Morris, C.J. and Green, J.M. (2002) Biological characteristics of a resident population of Atlantic cod (Gadus morhua L.) in southern Labrador. ICES Journal of Marine Science 59, 666–678.CrossRefGoogle Scholar
Myers, R.A. and Worm, B. (2003) Rapid worldwide depletion of predatory communities. Nature 423, 280–283.CrossRefGoogle ScholarPubMed
Olsen, E.M., Lilly, G.R., Heino, M., Morgan, M.J., Brattey, J. and Dieckmann, U. (2005) Assessing changes in age and size at maturation in collapsing populations of Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 62, 811–823.CrossRefGoogle Scholar
Pampoulie, C., Ruzzante, D.E., Chosson, V., Jorundsdottir, T.D., Taylor, L., Thorsteinsson, V., Danielsdottir, A.K. and Marteinsdottir, G. (2006) The genetic structure of Atlantic cod (Gadus morhua) around Iceland: insight from microsatellites, the Pan I locus, and tagging experiments. Canadian Journal of Fisheries and Aquatic Sciences 63, 2660–2674.CrossRefGoogle Scholar
Pastoors, M.A., Rijnsdorp, A.D. and van Beek, F.A. (2000) Effects of a partially closed area in the North Sea (‘plaice box’) on stock development of plaice. ICES Journal of Marine Science 57, 1014–1022.CrossRefGoogle Scholar
Pauly, D., Christensen, V., Dalsgaard, J., Froese, R. and Torres, F. (1998) Fishing down the foodwebs. Science 279, 860–863.CrossRefGoogle Scholar
Pauly, D., Watson, R. and Alder, J. (2005) Global trends in world fisheries: impacts on marine ecosystems and food security. Philosophical Transactions of the Royal Society B—Biological Sciences 360, 5–12.CrossRefGoogle ScholarPubMed
Petursdottir, G., Begg, G.A. and Marteinsdottir, G. (2006) Discrimination between Icelandic cod (Gadus morhua L.) populations from adjacent spawning areas based on otolith growth and shape. Fisheries Research 80, 182–189.CrossRefGoogle Scholar
Quinn, T.P. and Myers, K.W. (2004) Anadromy and the marine migrations of Pacific salmon and trout: Rounsefell revisited. Reviews in Fish Biology and Fisheries 14, 421–442.CrossRefGoogle Scholar
Quinn, T.P., Hodgson, S., Flynn, L., Hilborn, R. and Rogers, D.E. (2007) Directional selection by fisheries and the timing of sockeye salmon (Oncorhynchus nerka) migrations. Ecological Applications 17, 731–739.CrossRefGoogle ScholarPubMed
Ray, G.C. (2005) Connectivities of estuarine fishes to the coastal realm. Estuarine, Coastal and Shelf Science 64, 18–32.CrossRefGoogle Scholar
Reynolds, J.D., Mace, G.M., Redford, K.H. and Robinson, J.G. (eds) (2001) Conservation of exploited species. Cambridge: Cambridge University Press.Google Scholar
Roberts, C.M. (1997) Ecological advice for the global fisheries crisis. Trends in Ecology and Evolution 12, 35–38.CrossRefGoogle ScholarPubMed
Roberts, C.M., Hawkins, J.P. and Gell, F.R. (2005) The role of marine reserves in achieving sustainable fisheries. Philosophical Transactions of the Royal Society B—Biological Sciences 360, 123–132.CrossRefGoogle ScholarPubMed
Robichaud, D. and Rose, G.A. (2001) Multiyear homing of Atlantic cod to a spawning ground. Canadian Journal of Fisheries and Aquatic Sciences 58, 2325–2329.CrossRefGoogle Scholar
Robichaud, D. and Rose, G.A. (2004) Migratory behaviour and range in Atlantic cod: inference from a century of tagging. Fish and Fisheries 5, 185–214.CrossRefGoogle Scholar
Rose, G.A. (1993) Cod spawning on a migration highway in the North-West Atlantic. Nature 366, 458–461.CrossRefGoogle Scholar
Ruzzante, D.E., Taggart, C.T., Lang, S. and Cook, D. (2000a) Mixed-stock analysis of Atlantic cod near the Gulf of St Lawrence based on microsatellite DNA. Ecological Applications 10, 1090–1109.CrossRefGoogle Scholar
Ruzzante, D.E., Wroblewski, J.S., Taggart, C.T., Smedbol, R.K., Cook, D. and Goddard, S.V. (2000b) Bay-scale population structure in coastal Atlantic cod in Labrador and Newfoundland, Canada. Journal of Fish Biology 56, 431–447.Google Scholar
Salvanes, A.G.V., Skjæraasen, J.E. and Nilsen, T. (2004) Sub-populations of coastal cod with different behaviour and life-history strategies. Marine Ecology Progress Series 267, 241–251.CrossRefGoogle Scholar
Solmundsson, J., Palsson, J. and Karlsson, H. (2005) Fidelity of mature Icelandic plaice (Pleuronectes platessa) to spawning and feeding grounds. ICES Journal of Marine Science 62, 189–200.CrossRefGoogle Scholar
Tenhumberg, B., Tyre, A.J., Pople, A.R. and Possingham, H.P. (2004) Do harvest refuges buffer kangaroos against evolutionary responses to selective harvesting? Ecology 85, 2003–2017.CrossRefGoogle Scholar
Thériault, V., Dunlop, E.S., Dieckmann, U., Bernatchez, L. and Dodson, J.J. (2008) The impact of fishing-induced mortality on the evolution of alternative life-history tactics in brook charr. Evolutionary Applications 1, 409–423.CrossRefGoogle ScholarPubMed
Travis, J.M.J. and Dytham, C. (1998) The evolution of dispersal in a metapopulation: a spatially explicit, individual-based model. Proceedings of the Royal Society of London Series B—Biological Sciences 265, 17–23.CrossRefGoogle Scholar
Vilhjalmsson, H. (2002) Capelin (Mallotus villosus) in the Iceland–East Greenland–Jan Mayen ecosystem. ICES Journal of Marine Science 59, 870–883.CrossRefGoogle Scholar
West, C.D., Dytham, C., Righton, D. and Pitchford, J.W. (2009) Preventing overexploitation of migratory fish stocks: the efficacy of marine protected areas in a stochastic environment. ICES Journal of Marine Science 66, 1919–1930.CrossRefGoogle Scholar
Wood, C.C., Bickham, J.W., Nelson, R.J., Foote, C.J. and Patton, J.C. (2008) Recurrent evolution of life history ecotypes in sockeye salmon: implications for conservation and future evolution. Evolutionary Applications 1, 207–221.CrossRefGoogle ScholarPubMed
Woodhead, A.D. (1959) Variations in the activity of the thyroid gland of the cod, Gadus callarias L, in relation to its migrations in the Barents Sea. The ‘dummy run’ of the immature fish. Journal of the Marine Biological Association of the United Kingdom 38, 417–422.CrossRefGoogle Scholar
Worm, B. and Myers, R.A. (2003) Meta-analysis of cod–shrimp interactions reveals top-down control in oceanic food webs. Ecology 84, 162–173.CrossRefGoogle Scholar
Wright, P.J., Neat, F.C., Gibb, F.M., Gibb, I.M. and Thordarson, H. (2006) Evidence for metapopulation structuring in cod from the west of Scotland and North Sea. Journal of Fish Biology 69, 181–199.CrossRefGoogle Scholar
Wroblewski, J., Neis, B. and Gosse, K. (2005) Inshore stocks of Atlantic cod are important for rebuilding the East Coast fishery. Coastal Management 33, 411–432.CrossRefGoogle Scholar
Wroblewski, J.S., Kryger-Hann, L.K., Methven, D.A. and Haedrich, R.L. (2007) The fish fauna of Gilbert Bay, Labrador: a marine protected area in the Canadian subarctic coastal zone. Journal of the Marine Biological Association of the United Kingdom 87, 575–587.CrossRefGoogle Scholar