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Ecosystems

, Volume 12, Issue 4, pp 548–561 | Cite as

Synergistic Effects of Climate and Fishing in a Marine Ecosystem

  • Richard R. KirbyEmail author
  • Gregory Beaugrand
  • John A. Lindley
Article

Abstract

Current climate change and overfishing are affecting the productivity and structure of marine ecosystems. This situation is unprecedented for the marine biosphere and it is essential to understand the mechanisms and pathways by which ecosystems respond. We report that climate change and overfishing are likely to be responsible for a rapid restructuring of a highly productive marine ecosystem with effects throughout the pelagos and the benthos. In the mid-1980s, climate change, consequent modifications in the North Sea plankton, and fishing, all reduced North Sea cod recruitment. In this region, production of many benthic species respond positively and immediately to temperature. Analysis of a long-term, spatially extensive biological (plankton and cod) and physical (sea surface temperature) dataset suggests that synchronous changes in cod numbers and sea temperature have established an extensive trophic cascade favoring lower trophic level groups over economic fisheries. A proliferation of jellyfish that we detect may signal the climax of these changes. This modified North Sea ecology may provide a clear indication of the synergistic consequences of coincident climate change and overfishing. The extent of the ecosystem restructuring that has occurred in the North Sea suggests we are unlikely to reverse current climate and human-induced effects through ecosystem resource management in the short term. Rather, we should understand and adapt to new ecological regimes. This implies that fisheries management policies will have to be fully integrated with the ecological consequences of climate change to prevent a similar collapse in an exploited marine ecosystem elsewhere.

Keywords

climate change cod fisheries management plankton temperature trophic cascade 

Notes

Acknowledgments

We thank the owners, masters, and crews of the ships that tow the Continuous Plankton Recorder on a voluntary basis. R.R.K. is a Royal Society Research Fellow. We also thank three anonymous reviewers for useful comments.

References

  1. Barkai A, McQuaid C. 1988. Predator-prey role reversal in a marine benthic ecosystem. Science 242:62–64.PubMedCrossRefGoogle Scholar
  2. Batten SD, Clark R, Flinkman J, Hays G, John EH, John AWG, Jonas T, Lindley JA, Stevens DP, Walne A. 2003a. CPR sampling: the technical background, materials and methods, consistency and comparability. Prog Oceanogr 58:193–215.CrossRefGoogle Scholar
  3. Batten SD, Walne AW, Edwards M, Groom SB. 2003b. Phytoplankton biomass from continuous plankton recorder data: an assessment of the phytoplankton colour index. J Plankton Res 25:697–702.CrossRefGoogle Scholar
  4. Beaugrand G. 2004. The North Sea regime shift: evidence, causes, mechanisms and consequences. Prog Oceanogr 60:245–262.CrossRefGoogle Scholar
  5. Beaugrand G, Reid PC. 2003. Long-term changes in phytoplankton, zooplankton and salmon linked to climate change. Glob Chang Biol 9:801–817.CrossRefGoogle Scholar
  6. Beaugrand G, Brander KM, Lindley JA, Souisi S, Reid PC. 2003. Plankton effect on cod recruitment in the North Sea. Nature 426:661–664.PubMedCrossRefGoogle Scholar
  7. Beukema JJ, Dekker R. 2005. Decline of recruitment success in cockles and other bivalves in the Wadden Sea: possible role of climate change, predation on postlarvae and fisheries. Mar Ecol Prog Ser 287:149–167.CrossRefGoogle Scholar
  8. Brander KM. 2007. Global fish production and climate change. Proc Natl Acad Sci USA 104:19709–19714.PubMedCrossRefGoogle Scholar
  9. Briggs RP, Armstrong MJ, Dickey-Collas M, Allen M, McQuaid N, Whitmore J. 2002. The application of fecundity estimates to determine the spawning stock biomass of Irish Sea Nephrops norvegicus (L.) using the annual larval production method. ICES J Mar Sci 59:109–119.CrossRefGoogle Scholar
  10. Casini M, Lövgren J, Hjelm J, Cardinale M, Molinero J-C, Kornilovs, G. 2007. Multi-level trophic cascades in a heavily exploited open marine ecosystem. Proc R Soc B 275:1793–1801CrossRefGoogle Scholar
  11. Daan N, Gislason H, Pope JG, Rice JC. 2005. Changes in the North Sea fish community: evidence of indirect effects of fishing? ICES J Mar Sci 62:177–188.CrossRefGoogle Scholar
  12. Daskalov GM, Grishin AN, Rodionov S, Mihneva V. 2007. Trophic cascades triggered by overfishing reveal possible mechanisms of ecosystem regime shifts. Proc Natl Acad Sci USA 104:10518–10523.PubMedCrossRefGoogle Scholar
  13. Drinkwater KF. 2005. The response of Atlantic cod (Gadus morhua) to future climate change. ICES J Mar Sci 63:1327–1337.CrossRefGoogle Scholar
  14. Edwards M, Richardson AJ. 2004. Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430:881–883.PubMedCrossRefGoogle Scholar
  15. Edwards M, Beaugrand G, Reid PC, Rowden AA, Jones MB. 2002. Ocean climate anomalies and the ecology of the North Sea. Mar Ecol Prog Ser 239:1–10.CrossRefGoogle Scholar
  16. Fileman E, Smith T, Harris R. 2007. Grazing by Calanus helgolandicus and Para-Pseudocalanus spp. on phytoplankton and protozooplankton during the spring bloom in the Celtic Sea. J Exp Mar Biol Ecol 348:70–84.CrossRefGoogle Scholar
  17. Frank KT, Petrie B, Choi JS, Leggett WC. 2005. Trophic cascades in a formerly cod-dominated ecosystem. Science 308:1621–1623.PubMedCrossRefGoogle Scholar
  18. Freitas V, Campos J, Fonds M, Van der Veer HW. 2007. Potential impact of temperature change on epibenthic predator-bivalve prey interactions in temperate estuaries. J Therm Biol 32:328–340.CrossRefGoogle Scholar
  19. Grall J, Chauvaud L. 2002. Marine eutrophication and benthos: the need for new approaches and concepts. Glob Chang Biol 8:813–830.CrossRefGoogle Scholar
  20. Heath. MR. 2005. Changes in the structure and function of the North Sea fish foodweb, 1973–2000, and the impacts of fishing and climate. ICES J Mar Sci 62:847–868.CrossRefGoogle Scholar
  21. Heip C, Basford D, Craeymeersch JA, Dewarumez J-M, Dörjes J, De Wilde P, Duineveld G, Eleftheriou A, Herman PMJ, Niermann U, Kingston P, Künitzer A, Rachor E, Rumohr H, Soetaert K, Soltwedel T. 1992. Trends in biomass, density and diversity of North Sea macrofauna. ICES J Mar Sci 49:13–22.CrossRefGoogle Scholar
  22. Hop H, Gjøsæter J, Danielssen DS. 1992. Seasonal feeding ecology of cod (Gadus morhua L.) on the Norwegian Skagerrak coast. ICES J Mar Sci 49:453–461.CrossRefGoogle Scholar
  23. Hughes TP, Bellwood DR, Folke C, Steneck RS, Wilson J. 2005. New Paradigms for supporting the resilience of marine ecosystems. Trends Ecol Evol 20:380–386.PubMedCrossRefGoogle Scholar
  24. Ibañez F, Fromentin JM, Castel J. 1993. Application de la méthode des sommes cumulées à l’analyse des séries chronologiques en océanographie. C R Acad Sci, Sci Vie 316:745–748.Google Scholar
  25. ICES. 2006. Report of the ICES Advisory Committee on Fishery Management, Advisory Committee on the Marine Environment and Advisory Committee on Ecosystems, 2006. ICES Advice. Books 1–10. 6:310 pGoogle Scholar
  26. Kirby RR, Johns DG, Lindley JA. 2006. Fathers in hot water: rising sea temperatures and a Northeastern Atlantic pipefish baby boom. Biol Lett 2:597–600.PubMedCrossRefGoogle Scholar
  27. Kirby RR, Beaugrand G, Lindley JA, Richardson AJ, Edwards M, Reid PC. 2007. Climate effects and benthic-pelagic coupling in the North Sea. Mar Ecol Prog Ser 330:31–38.CrossRefGoogle Scholar
  28. Kirby RR, Beaugrand G, Lindley JA. 2008. Climate-induced effects on the merozooplankton and the benthic-pelagic ecology of the North Sea. Limnol Oceanogr 53:1805–1815.Google Scholar
  29. Lehoërff G, Ibanez F, Poniz P, Fromentin JM. 1995. Hydroclimatic relationships with planktonic time series from 1975 to 1992 in the North Sea off Gravelines, France. Mar Ecol Prog Ser 129:269–281.CrossRefGoogle Scholar
  30. Lilly GR, Parsons DG, Kulka DW. 2000. Was the increase in shrimp biomass on the northeast Newfoundland Shelf a consequence of a release in predation pressure from cod. J Northwest Atlantic Fish Sci 27:45–61.CrossRefGoogle Scholar
  31. Lindley JA, Williams R, Hunt HG. 1993. Anomalous seasonal cycles of decapod crustacean larvae in the North Sea in an exceptionally warm year. J Exp Mar Biol Ecol 172:47–66.CrossRefGoogle Scholar
  32. Lohrer AM, Thrush SF, Hunt L, Hancock N, Lundquist C. 2005. Rapid reworking of subtidal sediments by burrowing spatangoid urchins. J Exp Mar Biol Ecol 321:155–169.CrossRefGoogle Scholar
  33. Lynam CP, Gibbons J, Axelsen B, Sparks CAJ, Coetzee J, Heywood BG, Brierley AS. 2006. Jellyfish overtake fish in a heavily fished ecosystem. Curr Biol 16:492–493.CrossRefGoogle Scholar
  34. MacKenzie BR, Myers RA. 2007. The development of the northern European fishery for north Atlantic bluefin tuna, Thunnus thynnus during 1900–1950. Fish Res 87:229–239.CrossRefGoogle Scholar
  35. Molinero J-C, Casini M, Buecher E. 2008. The influence of the Atlantic and regional climate variability on the long-term changes in gelatinous carnivore populations in the northwestern Mediterranean. Limnol Oceanogr 53:1456–1467.Google Scholar
  36. Montgomery DC. 1991. Introduction to statistical quality control. Second edition. New York: Wiley. 674 p.Google Scholar
  37. Nunes CdAP, Jangoux M. 2004. Reproductive cycle of the spatangoid echinoid Echinocardium cordatum (Echinodermata) in the southwestern North Sea. Invertebr Reprod Dev 45:41–57Google Scholar
  38. Ólafsson EB, Peterson CH, Ambrose WG. 1994. Does recruitment limitation structure populations of macro-invertebrates in marine soft sediments. Oceanogr Mar Biol Annu Rev 32:65–109.Google Scholar
  39. Ottersen G, Stenseth NC, Hurrell JH. 2004. Climatic fluctuations and marine systems: a general introduction to the ecological effects. In: Stenseth NC, Ottersen G, Hurrell JH, Belgrano A, Eds. Marine ecosystems and climate variation. The North Atlantic, a comparative perspective. Chippenham: Oxford University Press. pp 3–14.Google Scholar
  40. Pace ML, Cole JJ, Carpenter SR, Kitchell JF. 1999. Trophic cascades revealed in diverse ecosystems. Trends Ecol Evol 14:483–488.PubMedCrossRefGoogle Scholar
  41. Pauly D, Christensen V, Dalsgaard J, Froese R, Torres F Jr. 1998. Fishing down marine food webs. Science 279:860–863.PubMedCrossRefGoogle Scholar
  42. Perry AL, Low PJ, Ellis JR, Reynolds JD. 2005. Climate change and distribution shifts in marine fishes. Science 308:1912–1915.PubMedCrossRefGoogle Scholar
  43. Pinnegar JK, Polunin NVC, Francour P, Badalamenti F, Chemello R, Harmelin-Vivien M-L, Hereu B, Milazzo M, Zabala M, D’Anna G, Pipitone C. 2000. Trophic cascades in benthic marine ecosystems: lessons for fisheries and protected-area management. Environ Conserv 27:179–200.CrossRefGoogle Scholar
  44. Pörtner HO, Berdal B, Blust R, Brix O, Colosimo A, De Wachter B, Giuliani A, Johansen T, Fischer T, Knust R, Lannig G, Naevdal G, Nedenes A, Nyhammer G, Sartoris FJ, Serendero I, Sirabella P, Thorkildsen S, Zakhartsev M. 2001. Climate induced temperature effects on growth performance, fecundity and recruitment in marine fish: developing a hypothesis for cause and effect relationships in Atlantic cod (Gadus morhua) and common eelpout (Zoarces viviparus). Cont Shelf Res 21:1975–1997.CrossRefGoogle Scholar
  45. Purcell JE. 2005. Climate effects on formation of jellyfish and ctenophore blooms: a review. J Mar Biol Assoc UK 85:461–476.CrossRefGoogle Scholar
  46. Raitsos DE, Reid PC, Lavender SJ, Edwards M, Richardson AJ. 2005. Extending the SeaWIFS chlorophyll dataset back 50 years in the northeast Atlantic. Geophys Res Lett 32:L06603. doi: 10.1029/2005GL022484.CrossRefGoogle Scholar
  47. Rees CB. 1955. Continuous plankton records: the decapod larvae in the North Sea 1950–51. Bull Mar Ecol 4:69–80.Google Scholar
  48. Rees HL, Eggleton JD, Rachor E, Vanden Berghe E. 2007. Structure and dynamics of the North Sea benthos. ICES Cooperative Research Report No 288, 258 pGoogle Scholar
  49. Reid PC, Borges M, Svenden E. 2001. A regime shift in the North Sea circa 1988 linked to changes in the North Sea horse mackerel fishery. Fish Res 50:163–171.CrossRefGoogle Scholar
  50. Reid PC, Colebrook JM, Matthews JBL, Aiken J. 2003. The Continuous Plankton Recorder: concepts and history, from Plankton Indicators to undulating recorders. Prog Oceanogr 58:117–173.CrossRefGoogle Scholar
  51. Rindorf A, Lewy P. 2006. Warm, windy winters drive cod corth and homing of spawners keeps them there. J Anim Ecol 43:445–453.CrossRefGoogle Scholar
  52. Scheffer M, Carpenter S, de Young B. 2005. Cascading effects of overfishing marine ecosystems. Trends Ecol Evol 20:579–581.PubMedCrossRefGoogle Scholar
  53. Schiel DR, Steinbeck JR, Foster MS. 2004. Ten years of induced ocean warming causes comprehensive changes in marine benthic communities. Ecology 85:1833–1839.CrossRefGoogle Scholar
  54. Smith BE, Ligenza TJ, Almeida FP, Link JS. 2007. The trophic ecology of Atlantic cod: insights from tri-monthly, localized scales of sampling. J Fish Biol 71:749–762.CrossRefGoogle Scholar
  55. Wilmers CC. 2007. The anatomy of predator-prey dynamics in a changing climate. J Anim Ecol 76:1037–1044.PubMedCrossRefGoogle Scholar
  56. Winder M, Schindler DE. 2004. Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85:2100–2106.CrossRefGoogle Scholar
  57. Woodruff SD, Diaz HF, Worley SJ. 1988. COADS release 2 data and metadata enhancements for improvements of marine surface flux fields. Phys Chem Earth 25:517–527.Google Scholar
  58. Worm B, Myers RA. 2003. Meta-analysis of cod-shrimp interactions reveals top-down control in oceanic food webs. Ecology 84:162–173.CrossRefGoogle Scholar
  59. Worm B, Barbier EB, Beaumont N, Emmett Duffy J, Folke C, Halpern BS, Jackson JBC, Lotze HK, Micheli F, Palumbi SR, Sala E, Selkoe KA, Stachowicz JJ, Watson R. 2006. Impacts of biodiversity loss on ecosystem services. Science 314:787–790.PubMedCrossRefGoogle Scholar
  60. Zeiss B, Kröncke I. 1997. Long-term macrofaunal studies in a subtidal habitat off Norderney (East-Frisia, Germany) from 1978–1994. I. The late winter samples. Oceanol Acta 20:311–318.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Richard R. Kirby
    • 1
    Email author
  • Gregory Beaugrand
    • 2
  • John A. Lindley
    • 3
  1. 1.School of Biological SciencesUniversity of PlymouthPlymouthUK
  2. 2.Centre National de la Recherche Scientifique, Laboratoire d’Océanologie et de Géosciences’ UMR LOG CNRS 8187Université des Sciences et Technologies de Lille 1Lille 1France
  3. 3.The Sir Alister Hardy Foundation for Ocean Science, The LaboratoryPlymouthUK

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