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Transient dynamics of an altered large marine ecosystem

Nature volume 477, pages 86–89 (2011)Cite this article

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Abstract

Overfishing of large-bodied benthic fishes and their subsequent population collapses on the Scotian Shelf of Canada’s east coast1,2 and elsewhere3,4 resulted in restructuring of entire food webs now dominated by planktivorous, forage fish species and macroinvertebrates. Despite the imposition of strict management measures in force since the early 1990s, the Scotian Shelf ecosystem has not reverted back to its former structure. Here we provide evidence of the transient nature of this ecosystem and its current return path towards benthic fish species domination. The prolonged duration of the altered food web, and its current recovery, was and is being governed by the oscillatory, runaway consumption dynamics of the forage fish complex. These erupting forage species, which reached biomass levels 900% greater than those prevalent during the pre-collapse years of large benthic predators, are now in decline, having outstripped their zooplankton food supply. This dampening, and the associated reduction in the intensity of predation, was accompanied by lagged increases in species abundances at both lower and higher trophic levels, first witnessed in zooplankton and then in large-bodied predators, all consistent with a return towards the earlier ecosystem structure. We conclude that the reversibility of perturbed ecosystems can occur and that this bodes well for other collapsed fisheries.

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Figure 1: Variability of the eastern Scotian Shelf ecosystem.
Figure 2: Physiological changes in forage fish species and resultant food web effects.
Figure 3: Post-perturbation forage fish variability.

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  • 20 October 2011

    In the 'Damped harmonic oscillator calculations' section of the online-only Methods, the equation was corrected in the HTML and the PDF.

References

  1. Frank, K. T., Petrie, B., Choi, J. S. & Leggett, W. C. Trophic cascades in a formerly cod-dominated ecosystem. Science 308, 1621–1623 (2005)

    Article  ADS  CAS  Google Scholar 

  2. Frank, K. T., Petrie, B., Shackell, N. L. & Choi, J. S. Reconciling differences in trophic control in mid-latitude marine ecosystems. Ecol. Lett. 9, 1096–1105 (2006)

    Article  Google Scholar 

  3. Daskalov, G. M., Grishin, A. N., Rodionov, S. & Mihneva, V. Trophic cascades triggered by overfishing reveal possible mechanisms of ecosystem regime shifts. Proc. Natl Acad. Sci. USA 104, 10518–10523 (2007)

    Article  ADS  CAS  Google Scholar 

  4. Casini, M. et al. Multi-level trophic cascades in a heavily exploited open marine ecosystem. Proc. R. Soc. Lond. B 275, 1793–1801 (2008)

    Article  Google Scholar 

  5. Steele, J. H. & Collie, J. S. in The Global Coastal Ocean: Multiscale Interdisciplinary Processes (eds Robinson, A. R. & Brink, K .) vol. 13, chap. 21 (Harvard, 2004)

    Google Scholar 

  6. Strong, D. R. Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73, 747–754 (1992)

    Article  Google Scholar 

  7. Pace, M. L., Cole, J. J., Carpenter, S. R. & Kitchell, J. F. Trophic cascades revealed in diverse ecosystems. Trends Ecol. Evol. 14, 483–488 (1999)

    Article  CAS  Google Scholar 

  8. Jackson, J. B. C. et al. Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–638 (2001)

    Article  CAS  Google Scholar 

  9. Myers, R. A., Baum, J. K., Shepherd, T. D., Powers, S. P. & Peterson, C. H. Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315, 1846–1850 (2007)

    Article  ADS  CAS  Google Scholar 

  10. Persson, L. et al. Culling prey promotes predator recovery—alternative states in a whole-lake experiment. Science 316, 1743–1746 (2007)

    Article  ADS  CAS  Google Scholar 

  11. Terborgh, J. & Estes, J. A. Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature (Island, 2010)

    Google Scholar 

  12. Yodzis, P. Must top predators be culled for the sake of fisheries? Trends Ecol. Evol. 16, 78–84 (2001)

    Article  CAS  Google Scholar 

  13. Bundy, A., Heymans, J. J., Morisette, L. & Savenkoff, C. Seals, cod and forage fish: a comparative exploration of variations in the theme of stock collapse and ecosystem change in four Northwest Atlantic ecosystems. Prog. Oceanogr. 81, 188–206 (2009)

    Article  ADS  Google Scholar 

  14. Myers, R. A. & Worm, B. Extinction, survival or recovery of large predatory fishes. Phil. Trans. R. Soc. B 360, 13–20 (2005)

    Article  Google Scholar 

  15. Shelton, P. A. et al. Fishing under low productivity conditions is further delaying recovery of Northwest Atlantic cod (Gadus morhua). Can. J. Fish. Aquat. Sci. 63, 235–238 (2006)

    Article  Google Scholar 

  16. Savenkoff, C. et al. Effects of fishing and predation in a heavily exploited ecosystem: comparing periods before and after the collapse of groundfish in the southern Gulf of St. Lawrence (Canada). Ecol. Modell. 204, 115–128 (2007)

    Article  Google Scholar 

  17. Fauchald, P. Predator–prey reversal: a possible mechanism for ecosystem hysteresis in the North Sea? Ecology 91, 2191–2197 (2010)

    Article  Google Scholar 

  18. Petrie, B., Frank, K. T., Shackell, N. L. & Leggett, W. C. Structure and stability in exploited marine fish communities: quantifying critical transitions. Fish. Oceanogr. 18, 83–101 (2009)

    Article  Google Scholar 

  19. Petrie, B. Does the North Atlantic Oscillation affect hydrographic properties on the Canadian Atlantic continental shelf? Atm.-Ocean 45, 141–151 (2007)

    Article  Google Scholar 

  20. Fisher, J. A. D., Frank, K. T., Petrie, B., Leggett, W. C. & Shackell, N. L. Temporal dynamics within a contemporary latitudinal diversity gradient. Ecol. Lett. 11, 883–897 (2008)

    Article  Google Scholar 

  21. Forsyth, D. M. & Caley, P. Testing the irruptive paradigm of large-herbivore dynamics. Ecology 87, 297–303 (2006)

    Article  Google Scholar 

  22. Peterson, R. O., Page, R. E. & Dodge, K. M. Wolves, moose, and the allometry of population cycles. Science 224, 1350–1352 (1984)

    Article  ADS  CAS  Google Scholar 

  23. Frank, K. T., Shackell, N. L. & Simon, J. E. An evaluation of the Emerald/Western Bank juvenile haddock closed area. ICES J. Mar. Sci. 57, 1023–1034 (2000)

    Article  Google Scholar 

  24. Anderson, S. C., Lotze, H. K. & Shackell, N. L. Evaluating the knowledge base for expanding low-trophic-level fisheries in Atlantic Canada. Can. J. Fish. Aquat. Sci. 65, 2553–2571 (2008)

    Article  Google Scholar 

  25. Richardson, A. J., Bakun, A., Hays, G. C. & Gibbons, M. J. The jellyfish joyride: causes, consequences and management responses to a more gelatinous future. Trends Ecol. Evol. 24, 312–322 (2009)

    Article  Google Scholar 

  26. Shackell, N. L., Frank, K. T., Fisher, J. A. D., Petrie, B. & Leggett, W. C. Decline in top predator body size and changing climate alter trophic structure in an oceanic ecosystem. Proc. R. Soc. B 277, 1353–1360 (2010)

    Article  Google Scholar 

  27. Fisher, J. A. D., Frank, K. T. & Leggett, W. C. Breaking Bergmann’s rule: truncation of Northwest Atlantic marine fish body sizes. Ecology 91, 2499–2505 (2010)

    Article  Google Scholar 

  28. Murawski, S. A. Rebuilding depleted fish stocks: the good, the bad, and mostly, the ugly. ICES J. Mar. Sci. 67, 1830–1840 (2010)

    Article  Google Scholar 

  29. Rodionov, S. N. A sequential algorithm for testing climate regime shifts. Geophys. Res. Lett. 31, L09204 (2004)

    Article  ADS  Google Scholar 

  30. Rooney, N., McCann, K., Gellner, G. & Moore, J. C. Structural asymmetry and the stability of diverse food webs. Nature 442, 265–269 (2006)

    Article  ADS  CAS  Google Scholar 

  31. Doubleday, W. G. Studies No. 2, Manual on Groundfish Surveys in the Northwest Atlantic (NAFO Scientific Council Studies, 1981)

    Google Scholar 

  32. Doubleday, W. G. & Rivard, D. Bottom trawl surveys. Can. Spec. Pub. Fish. Aquat. Sci. 58, 1–273 (1981)

    Google Scholar 

  33. Chadwick, E. M. P. et al. History of annual multi-species trawl surveys on the Atlantic coast of Canada. AZMP Bull. 6, 25–42 (2007)

    Google Scholar 

  34. Shackell, N. L. & Frank, K. T. Marine fish diversity on the Scotian Shelf, Canada. Aquat. Conserv.: Mar. Freshwat. Ecosyst. 13, 305–321 (2003)

    Article  Google Scholar 

  35. Mayo, R. K., Gifford, V. M. & Jearld, A. Age validation of redfish, Sebastes marinus (L.), from the Gulf of Maine-Georges Bank Region. J. Northwest Atl. Fish. Sci. 2, 13–19 (1981)

    Article  Google Scholar 

  36. Fowler, G. W. & Stobo, W. T. Status of 4VW American plaice and yellowtail flounder. DFO Can. Sci. Advis. Sec. Res. Doc. 2000, 1–86 (2000)

    Google Scholar 

  37. Bundy, A. Mass balance models of the eastern Scotian Shelf before and after the cod collapse and other ecosystem changes. Can. Tech. Rep. Fish. Aquat. Sci. 2520, 1–192 (2004)

    Google Scholar 

  38. Richardson, A. J. et al. Using continuous plankton recorder data. Prog. Oceanogr. 68, 27–74 (2006)

    Article  ADS  Google Scholar 

  39. Smith, S. J. Analysis of data from bottom trawl surveys. NAFO Sci. Coun. Studies 28, 25–53 (1996)

    Google Scholar 

  40. Benoît, H., Swain, D. & Chouinard, G. Using the long-term bottom-trawl survey of the Southern Gulf of St. Lawrence to understand marine fish populations and community change. AZMP Bull. 8, 19–27 (2008)

    Google Scholar 

  41. Choi, J. S., Frank, K. T., Petrie, B. D. & Leggett, W. C. Integrated assessment of a large marine ecosystem: a case study of the devolution of the Eastern Scotian Shelf, Canada. Oceanogr. Mar. Biol. Ann. Rev 42, 47–67 (2005)

    Google Scholar 

  42. Litzow, M. A., Urban, J. D. & Laurel, B. J. Increased spatial variance accompanies reorganization of two continental shelf ecosystems. Ecol. Apps 18, 1331–1337 (2008)

    Article  Google Scholar 

  43. Harrison, G. et al. Optical, chemical, and biological oceanographic conditions in the Maritimes Region in 2008. DFO Can. Sci. Advis. Sec. Res. Doc. 2009, 1–55 (2009)

    Google Scholar 

  44. Mills, E. L. & Fournier, R. O. Fish production and the marine ecosystems of the Scotian Shelf, eastern Canada. Mar. Biol. 54, 101–108 (1979)

    Article  Google Scholar 

  45. Tremblay, M. J. & Roff, J. C. Production estimates for Scotian Shelf copepods based on mass specific P/B ratios. Can. J. Fish. Aquat. Sci. 40, 749–753 (1983)

    Article  Google Scholar 

  46. Cochlan, W. Seasonal study of uptake and regeneration of nitrogen on the Scotian Shelf. Cont. Shelf Res. 5, 555–577 (1986)

    Article  ADS  Google Scholar 

  47. Fournier, R., Marra, J., Bohrer, R. & van Det, M. Plankton dynamics and nutrient enrichment of the Scotian Shelf. J. Fish. Res. Bd Can. 34, 1004–1018 (1977)

    Article  CAS  Google Scholar 

  48. Mousseau, L., Fortier, L. & Legendre, L. Annual production of fish larvae and their prey in relation to size-fractionated primary production (Scotian Shelf, NW Atlantic). ICES J. Mar. Sci. 55, 44–57 (1998)

    Article  Google Scholar 

  49. Cauffopé, G. & Heymans, S. Energy contents and conversion factors for sea lion’s prey. UBC Fish. Centre Res. Rep 13, 225–237 (2005)

    Google Scholar 

  50. Myers, R. A., Mertz, G. & Fowlow, P. S. Maximum population growth rates and recovery times for Atlantic cod, Gadus morhua . Fish. Bull. 95, 762–772 (1997)

    Google Scholar 

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Acknowledgements

We thank the Department of Fisheries and Oceans staff who collected and maintained the multi-trophic level and biogeochemical monitoring data, J. Black for assistance with computing and database issues, and A. Bundy and D. R. Strong for helpful criticisms. Symbols for Fig. 2b are courtesy of the Integration and Application Network (http://www.ian.umces.edu/symbols). This research was supported by Fisheries and Oceans Canada and Discovery grants from the Natural Sciences and Engineering Research Council of Canada (to K.T.F. and W.C.L.).

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Authors and Affiliations

  1. Ocean Sciences Division, Bedford Institute of Oceanography, P.O. Box 1006, Dartmouth, Nova Scotia B2Y 4A2, Canada

    Kenneth T. Frank & Brian Petrie

  2. Department of Biology, Queen’s University, Kingston, Ontario K7L 3N6, Canada

    Jonathan A. D. Fisher & William C. Leggett

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  1. Kenneth T. Frank
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Contributions

K.T.F. developed the overall concept of paper reported here. B.P and K.T.F. developed the initial hypothesis and assembled the relevant data. Most analyses were performed by B.P. with assistance from J.A.D.F. and K.T.F. All authors contributed to the interpretations and synthesis of the analytical results.

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Correspondence to Kenneth T. Frank.

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Frank, K., Petrie, B., Fisher, J. et al. Transient dynamics of an altered large marine ecosystem. Nature 477, 86–89 (2011). https://doi.org/10.1038/nature10285

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