The life-histories of exploited fish species, such as Pacific salmon, are vulnerable to a wide variety of anthropogenic stressors including climate change, selective exploitation and competition with hatchery releases for finite foraging resources. However, these stressors may generate unexpected changes in life-histories due to developmental linkages when species complete their migratory life cycle in different habitats. We used multivariate time-series models to quantify changes in the prevalence of different life-history strategies of sockeye salmon from Bristol Bay, Alaska, over the past half-century—specifically, how they partition their lives between freshwater habitats and the ocean. Climate warming has decreased the time spent by salmon in their natal freshwater habitat, as climate-enhanced growth opportunities have enabled earlier migration to the ocean. Migration from freshwater at a younger age, and increasing competition from wild and hatchery-released salmon, have tended to delay maturation toward the salmon spending an additional year feeding in the ocean. Models evaluating the effects of size-selective fishing on these patterns had only small support. These stressors combine to reduce the size-at-age of fish vulnerable to commercial fisheries and have increasingly favoured a single-age class, potentially affecting the age class complexity that stabilizes this highly reliable resource.
Access optionsAccess options
Subscribe to Journal
Get full journal access for 1 year
only $8.67 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
All Bristol Bay sockeye age composition, Bristol Bay escapement data, Lake Aleknagik ice break-up dates and Lake Aleknagik temperature data used to support the findings of this study can be found in Supplementary Information. Climate indices PDO and NPGO are available online from http://research.jisao.washington.edu/pdo/ and http://www.o3d.org/npgo/, respectively. North Pacific salmon biomass is available from the online supplementary material for ref. 37.
Code for the multivariate autoregressive state-space models used in this study has been deposited at Github (https://github.com/tjcline/MARSStmb).
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Kingsolver, J. G. et al. Complex life cycles and the responses of insects to climate change. Integr. Comp. Biol. 51, 719–732 (2011).
Salice, C. J., Rowe, C. L., Pechmann, J. H. K. & Hopkins, W. A. Multiple stressors and complex life cycles: Insights from a population-level assessment of breeding site contamination and loss in an amphibian. Environ. Toxicol. Chem. 30, 2874–2882 (2011).
Portner, H. O. & Farrell, A. P. Physiology and climate change. Science 322, 690–692 (2008).
Radchuk, V., Turlure, C. & Schtickzelle, N. Each life stage matters: the importance of assessing the response to climate change over the complete life cycle in butterflies. J. Anim. Ecol. 82, 275–285 (2013).
Folt, C. L., Chen, C. Y., Moore, M. V. & Burnaford, J. Synergism and antagonism among multiple stressors. Limnol. Oceanogr. 44, 864–877 (1999).
Hutchings, J. A. & Myers, R. A. The evolution of alternative mating strategies in variable environments. Evol. Ecol. 8, 256–268 (1994).
Wilbur, H. M. & Rudolf, V. H. W. Life-history evolution in uncertain environments: bet hedging in time. Am. Nat. 168, 398–411 (2006).
Hilborn, R., Quinn, T. P., Schindler, D. E. & Rogers, D. E. Biocomplexity and fisheries sustainability. Proc. Natl Acad. Sci. USA 100, 6564–6568 (2003).
Rouyer, T. et al. Shifting dynamic forces in fish stock fluctuations triggered by age truncation? Glob. Change Biol. 17, 3046–3057 (2011).
Vitousek, P. M., Mooney, H. A., Lubchenco, J. & Melillo, J. M. Human domination of Earth’s ecosystems. Science 277, 494–499 (1997).
Halpern, B. S. et al. A global map of human impact on marine ecosystems. Science 319, 948–952 (2008).
Webster, M. S., Marra, P. P., Haig, S. M., Bensch, S. & Holmes, R. T. Links between worlds: unraveling migratory connectivity. Trends Ecol. Evol. 17, 76–83 (2002).
Crain, C. M., Kroeker, K. & Halpern, B. S. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11, 1304–1315 (2008).
Darling, E. S. & Cote, I. M. Quantifying the evidence for ecological synergies. Ecol. Lett. 11, 1278–1286 (2008).
Hodgson, E. E., Essington, T. E. & Halpern, B. S. Density dependence governs when population responses to multiple stressors are magnified or mitigated. Ecology 98, 2673–2683 (2017).
Palumbi, S. R. Evolution - humans as the world’s greatest evolutionary force. Science 293, 1786–1790 (2001).
Darimont, C. T. et al. Human predators outpace other agents of trait change in the wild. Proc. Natl Acad. Sci. USA 106, 952–954 (2009).
Ohlberger, J. et al. Pathogen-induced rapid evolution in a vertebrate life-history trait. Proc. R. Soc. Lond. Biol. Sci. 278, 35–41 (2011).
Olsen, E. M. et al. Maturation trends indicative of rapid evolution preceded the collapse of northern cod. Nature 428, 932–935 (2004).
Kuparinen, A. & Merila, J. Detecting and managing fisheries-induced evolution. Trends Ecol. Evol. 22, 652–659 (2007).
Biro, P. A. & Post, J. R. Rapid depletion of genotypes with fast growth and bold personality traits from harvested fish populations. Proc. Natl Acad. Sci. USA 105, 2919–2922 (2008).
Bradshaw, W. E. & Holzapfel, C. M. Evolutionary response to rapid climate change. Science 312, 1477–1478 (2006).
Hoffmann, A. A. & Sgro, C. M. Climate change and evolutionary adaptation. Nature 470, 479–485 (2011).
Edwards, M. & Richardson, A. J. Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430, 881–884 (2004).
Araki, H., Cooper, B. & Blouin, M. S. Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318, 100–103 (2007).
Ruggerone, G. T., Zimmermann, M., Myers, K. W., Nielsen, J. L. & Rogers, D. E. Competition between Asian pink salmon (Oncorhynchus gorbuscha) and Alaskan sockeye salmon (Oncorhynchus nerka) in the North Pacific Ocean. Fish. Oceanogr. 12, 209–219 (2003).
Amoroso, R. O., Tillotson, M. D. & Hilborn, R. Measuring the net biological impact of fisheries enhancement: pink salmon hatcheries can increase yield, but with apparent costs to wild populations. Can. J. Fish. Aquat. Sci. 74, 1233–1242 (2017).
Nehlsen, W., Williams, J. E. & Lichatowich, J. A. Pacific salmon at the crossroads – stocks at risk from California, Oregon, Idaho, and Washington. Fisheries 16, 4–21 (1991).
Kareiva, P., Marvier, M. & McClure, M. Recovery and management options for spring/summer chinook salmon in the Columbia River basin. Science 290, 977–979 (2000).
Environmental Protection Agency. An Assessment of Potential Mining Impacts on Salmon Ecosystems of Bristol Bay, Alaska (USEPA, 2014).
Quinn, T. P., Doctor, K., Kendall, N. & Rich, H. B. Diadromy and the life history of sockeye salmon: nature, nurture, and the hand of man. Am. Fish. Soc. Symp. 2, 245–259 (2009).
Schindler, D. E., Rogers, D. E., Scheuerell, M. D. & Abrey, C. A. Effects of changing climate on zooplankton and juvenile sockeye salmon growth in southwestern Alaska. Ecology 86, 198–209 (2005).
Carter, J. L. & Schindler, D. E. Responses of zooplankton populations to four decades of climate warming in lakes of southwestern Alaska. Ecosystems 15, 1010–1026 (2012).
Rich, H. B., Quinn, T. P., Scheuerell, M. D. & Schindler, D. E. Climate and intraspecific competition control the growth and life history of juvenile sockeye salmon (Oncorhynchus nerka) in Iliamna Lake, Alaska. Can. J. Fish. Aquat. Sci. 66, 238–246 (2009).
Mantua, N. J., Hare, S. R., Zhang, Y., Wallace, J. M. & Francis, R. C. A Pacific interdecadal climate oscillation with impacts on salmon production. Bull. Am. Meteorol. Soc. 78, 1069–079 (1997).
Di Lorenzo, E. et al. North Pacific gyre oscillation links ocean climate and ecosystem change. Geophys. Res. Lett. 35, L08607 (2008).
Ruggerone, G. T. & Irvine, J. R. Numbers and biomass of natural- and hatchery-origin pink salmon, chum salmon, and sockeye salmon in the North Pacific Ocean, 1925-2015. Mar. Coast. Fish. 10, 152–168 (2018).
Johnson, S. P. & Schindler, D. E. Trophic ecology of pacific salmon (Oncorhynchus spp.) in the ocean: a synthesis of stable isotope research. Ecol. Res. 24, 855–863 (2009).
Myers, K., Aydin, K., Walker, R., Fowler, S. & Dahlberg, M. Known Ocean Ranges of Stocks of Pacific Salmon and Steelhead as Shown by Tagging Experiments, 1956-1995 (University of Washington, School of Fisheries, Fisheries Research Institute, 1996).
Morita, K. & Fukuwaka, M. A. Does size matter most? The effect of growth history on probabilistic reaction norm for salmon maturation. Evolution 60, 1516–1521 (2006).
Schindler, D. E. et al. Climate change, ecosystem impacts, and management for pacific salmon. Fisheries 33, 502–506 (2008).
Abdul-Aziz, O. I., Mantua, N. J. & Myers, K. W. Potential Climate Change impacts on thermal habitats of Pacific salmon (Oncorhynchus spp.) in the North Pacific Ocean and adjacent seas. Can. J. Fish. Aquat. Sci. 68, 1660–1680 (2011).
Kendall, N. W., Hard, J. J. & Quinn, T. P. Quantifying six decades of fishery selection for size and age at maturity in sockeye salmon. Evol. Appl. 2, 523–536 (2009).
Smith, B. D. Trends in wild adult steelhead (Oncorhynchus mykiss) abundance for snowmelt-driven watersheds of British Columbia in relation to freshwater discharge. Can. J. Fish. Aquat. Sci. 57, 285–297 (2000).
Ruggerone, G. T. & Connors, B. M. Productivity and life history of sockeye salmon in relation to competition with pink and sockeye salmon in the North Pacific Ocean. Can. J. Fish. Aquat. Sci. 72, 818–833 (2015).
Sharpe, D. M. T. & Hendry, A. P. Life history change in commercially exploited fish stocks: an analysis of trends across studies. Evol. Appl. 2, 260–275 (2009).
Kendall, N. W., Dieckmann, U., Heino, M., Punt, A. E. & Quinn, T. P. Evolution of age and length at maturation of Alaskan salmon under size-selective harvest. Evol. Appl. 7, 313–322 (2014).
Schindler, D. E. et al. Population diversity and the portfolio effect in an exploited species. Nature 465, 609–612 (2010).
White, J. W., Botsford, L. W., Hastings, A. & Holland, M. D. Stochastic models reveal conditions for cyclic dominance in sockeye salmon populations. Ecol. Monogr. 84, 69–90 (2014).
Cunningham, C. J. et al. A general model for salmon run reconstruction that accounts for interception and differences in availability to harvest. Can. J. Fish. Aquat. Sci. 75, 439–451 (2017).
Holmes, E. E., Ward, E. J. & Wills, K. MARSS: multivariate autoregressive state-space models for analyzing time-series data. R. J. 4, 11–19 (2012).
Harvey, A. C. Forecasting. Structural Time Series Models and the Kalman Filter (Cambridge University Press, 1989).
Cowpertwait, P. S. P. & Metcalfe, A. V. Introductory Time Series with R (Springer, 2009).
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation of Statistical Computing, 2018).
We thank the many graduate students, postdocs, faculty and research scientists who have worked for the University of Washington’s Alaska Salmon Program for help in collecting and organizing these data, particularly J. Carter. Thank you to the Alaska Department of Fish and Game for the brood table data for sockeye salmon returning to Bristol Bay. We thank T. Walsworth for helpful comments throughout the project. Funding was provided by the National Science Foundation (NSF) through a graduate research fellowship to T.J.C. Ongoing monitoring of Bristol Bay lakes has been supported by NSF and the Gordon and Betty Moore Foundation.
Supplementary Fig. 1, Supplementary Tables 1–4, Supplementary References
Returns of sockeye salmon to Bristol Bay since brood year 1963 aggregated by river system, freshwater age, and ocean age. Returns are in thousands of fish and ages are in years
The escapement of sockeye salmon to the 9 river systems in Bristol Bay since 1963. Escapement numbers are in thousands. Escapement is counted near the mouth of each river by the Alaska Department of Fish and Game
Average summer surface (0–20 m) watertemperature (ºC) and day of spring ice off for Lake Aleknagik, AK
About this article
Nature Ecology & Evolution (2019)