Population diversity and the portfolio effect in an exploited species

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One of the most pervasive themes in ecology is that biological diversity stabilizes ecosystem processes and the services they provide to society1, 2, 3, 4, a concept that has become a common argument for biodiversity conservation5. Species-rich communities are thought to produce more temporally stable ecosystem services because of the complementary or independent dynamics among species that perform similar ecosystem functions6. Such variance dampening within communities is referred to as a portfolio effect7 and is analogous to the effects of asset diversity on the stability of financial portfolios8. In ecology, these arguments have focused on the effects of species diversity on ecosystem stability but have not considered the importance of biologically relevant diversity within individual species9. Current rates of population extirpation are probably at least three orders of magnitude higher than species extinction rates10, so there is a pressing need to clarify how population and life history diversity affect the performance of individual species in providing important ecosystem services. Here we use five decades of data from Oncorhynchus nerka (sockeye salmon) in Bristol Bay, Alaska, to provide the first quantification of portfolio effects that derive from population and life history diversity in an important and heavily exploited species. Variability in annual Bristol Bay salmon returns is 2.2 times lower than it would be if the system consisted of a single homogenous population rather than the several hundred discrete populations it currently consists of. Furthermore, if it were a single homogeneous population, such increased variability would lead to ten times more frequent fisheries closures. Portfolio effects are also evident in watershed food webs, where they stabilize and extend predator access to salmon resources. Our results demonstrate the critical importance of maintaining population diversity for stabilizing ecosystem services and securing the economies and livelihoods that depend on them. The reliability of ecosystem services will erode faster than indicated by species loss alone.

At a glance


  1. Bristol Bay sockeye habitat and associated change in variability of returns at different spatial scales and levels of life history aggregation.
    Figure 1: Bristol Bay sockeye habitat and associated change in variability of returns at different spatial scales and levels of life history aggregation.

    a, Map of Bristol Bay, southwest Alaska. Sockeye salmon nursery lakes are shown in solid black. Fishing districts associated with major rivers are highlighted as striped areas. b, Map of the Wood River system showing streams supporting anadromous salmon populations. c, Interannual variability in total returns to sockeye populations and stocks at three spatial scales and two levels of life history aggregation. Grey symbols are for the Wood River, highlighting the watershed for which continuous long-term data on stream populations (1962–2007, n = 8) exist. Black symbols are for rivers (including the Wood River, n = 8) and the Bristol Bay aggregate (1958–2008). Circles show average variabilities for populations and stocks with their observed age composition, and triangles show average variabilities for the dominant age classes at each spatial scale. Error bars, 1s.e. d, Three age classes of reproductively mature male sockeye salmon from the Wood River that have spent one, two or three years at sea, as indicated.

  2. Effect of interannual variability on the probability of fishery closures or capacity-swamping returns.
    Figure 2: Effect of interannual variability on the probability of fishery closures or capacity-swamping returns.

    Probability of total annual return being less than 10,000,000 (solid line) or greater than 60,000,000 (dotted line) as a function of the coefficient of variation in the overall distribution of returns. No fishing is allowed when total returns are less than about 10,000,000. Returns in excess of 60,000,000 swamp the capacity of the fishing fleet and processing industry to capture their allocation of the resource. Stock abundances were assumed to be characterized by log-normal distributions. Current Bristol Bay returns have a CV of about 0.55 and the simplest component of the stock dynamics is about 1.2.

  3. Annual run timing to fishing districts and streams.
    Figure 3: Annual run timing to fishing districts and streams.

    a, Cumulative returns (catch plus escapement) to each of the major fishing districts in Bristol Bay for 2000–2007. The Bristol Bay fishery can currently process about 2,000,000 fish per day; on days with total returns above this level, the industry cannot capture their allocation of the resource. Between 1978 and 2007, the daily catch plus escapement was >2,000,000 fish on about seven days per season, on average. However, if all the fish had arrived at the fishing grounds with exactly the same timing, as determined by the distribution observed in any single fishing district in a given year, the length of the peak fishing season would have been reduced on average by 20% (range, 8–34%). b, Comparison of the dates of occupancy (dot, peak; line, occupancy period) in spawning habitats where sockeye salmon are available to predators and scavengers for 30 populations in the Wood River system (Supplementary Fig. 1).


  1. MacArthur, R. H. Fluctuations of animal populations, and a measure of community stability. Ecology 36, 533536 (1955)
  2. Elton, C. S. The Ecology of Invasions by Animals and Plants (Chapman & Hall, 1958)
  3. Hooper, D. U. et al. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 75, 335 (2005)
  4. Chapin, F. S. et al. Consequences of changing biodiversity. Nature 405, 234242 (2000)
  5. Duffy, J. E. Why biodiversity is important to the functioning of real-world ecosystems. Front. Ecol. Environ 7, 437444 (2009)
  6. Tilman, D. Biodiversity: population versus ecosystem stability. Ecology 77, 350363 (1996)
  7. Figge, F. Bio-folio: applying portfolio theory to biodiversity. Biodivers. Conserv. 13, 827849 (2004)
  8. Markowitz, H. Portfolio selection. J. Finance 7, 7791 (1952)
  9. Luck, G. W., Daily, G. C. & Ehrlich, P. R. Population diversity and ecosystem services. Trends Ecol. Evol. 18, 331336 (2003)
  10. Hughes, J. B., Daily, G. C. & Ehrlich, P. R. Population diversity: its extent and extinction. Science 278, 689692 (1997)
  11. Hilborn, R., Quinn, T. P., Schindler, D. E. & Rogers, D. E. Biocomplexity and fisheries sustainability. Proc. Natl Acad. Sci. USA 100, 65646568 (2003)
  12. Hutchinson, W. F. The dangers of ignoring stock complexity in fishery management: the case of the North Sea cod. Biol. Lett. 4, 693695 (2008)
  13. Quinn, T. P. The Behavior and Ecology of Pacific Salmon and Trout (Univ. Washington Press, 2005)
  14. Doak, D. F. et al. The statistical inevitability of stability-diversity relationships in community ecology. Am. Nat. 151, 264276 (1998)
  15. Mantua, N. J. & Hare, S. R. The Pacific decadal oscillation. J. Oceanogr. 58, 3544 (2002)
  16. Schindler, D. E. et al. Climate change, ecosystem impacts, and management for Pacific salmon. Fisheries 33, 502506 (2008)
  17. Gende, S. M., Edwards, R. T., Willson, M. F. & Wipfli, M. S. Pacific salmon in aquatic and terrestrial ecosystems. Bioscience 52, 917928 (2002)
  18. Naiman, R. J., Bilby, R. E., Schindler, D. E. & Helfield, J. M. Pacific salmon, nutrients, and the dynamics of freshwater and riparian ecosystems. Ecosystems (NY, Print) 5, 399417 (2002)
  19. Schindler, D. E., Leavitt, P. R., Brock, C. S., Johnson, S. P. & Quay, P. D. Marine-derived nutrients, commercial fisheries, and production of salmon and lake algae in Alaska. Ecology 86, 32253231 (2005)
  20. Helfield, J. M. & Naiman, R. J. Keystone interactions: salmon and bear in riparian forests of Alaska. Ecosystems (NY, Print) 9, 167180 (2006)
  21. Payne, L. X. & Moore, J. M. Mobile scavengers create hotspots of freshwater productivity. Oikos 115, 6980 (2006)
  22. Olsen, E. M. et al. Small-scale biocomplexity in coastal Atlantic cod supporting a Darwinian perspective on fisheries management. Evol. Appl. 1, 524533 (2008)
  23. Dixson, D. L. et al. Coral reef fish smell leaves to find island homes. Proc. R. Soc. Lond. B 275, 28312839 (2008)
  24. Rooker, J. R. et al. Natal homing and connectivity in Atlantic bluefin tuna populations. Science 322, 742744 (2008)
  25. Gustafson, R. G. et al. Pacific salmon extinctions: quantifying lost and remaining diversity. Conserv. Biol. 21, 10091020 (2007)
  26. Lindley, S. T. et al. What Caused the Sacramento River Fall Chinook Stock Collapse? Pre-publication report (Pacific Fishery Management Council, 2009); available at left fencehttp://swr.nmfs.noaa.gov/media/salmondeclinereport.pdfright fence.
  27. Moore, J. W., McClure, M., Rogers, L. A. & Schindler, D. E. Synchronization and portfolio performance of threatened salmon. Conserv. Lett. doi:10.1111/j.1755-263X.2010.00119.x. (in the press)
  28. Folke, C. et al. Regime shifts, resilience, and biodiversity in ecosystem management. Annu. Rev. Ecol. Syst. 35, 557581 (2004)
  29. West, F. W. & Fair, L. F. Abundance, Age, Sex, and Size Statistics for Pacific Salmon in Bristol Bay, 2003. Fishery Data Series No. 06–47 (Alaska Department of Fish and Game, 2006)
  30. Rogers, L. A. & Schindler, D. E. Asynchrony in population dynamics in sockeye salmon of southwest Alaska. Oikos 117, 15781586 (2008)
  31. Pyper, B. J. & Peterman, R. M. Comparison of methods to account for autocorrelation in correlation analyses of fish data. Can. J. Fish. Aquat. Sci. 55, 21272140 (1998)

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Author information


  1. School of Aquatic and Fishery Sciences, University of Washington, Box 355020, Seattle, Washington 98195-5020, USA

    • Daniel E. Schindler,
    • Ray Hilborn,
    • Brandon Chasco,
    • Christopher P. Boatright,
    • Thomas P. Quinn &
    • Lauren A. Rogers
  2. The Gordon and Betty Moore Foundation, 1661 Page Mill Road, Palo Alto, California 94304, USA

    • Michael S. Webster


D.E.S. designed and coordinated the project; R.H., B.C. and L.A.R contributed to the analyses; M.S.W. helped design the project; and all authors contributed to the writing.

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The authors declare no competing financial interests.

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Supplementary information

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  1. Supplementary Information (273K)

    This file contains Supplementary Information comprising: Value of sockeye salmon resources in Bristol Bay and Variance scaling in data, Supplementary Figures 1-3 with legends and References.

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