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Delayed phenology and reduced fitness associated with climate change in a wild hibernator


The most commonly reported ecological effects of climate change are shifts in phenologies, in particular of warmer spring temperatures leading to earlier timing of key events1,2. Among animals, however, these reports have been heavily biased towards avian phenologies, whereas we still know comparatively little about other seasonal adaptations, such as mammalian hibernation. Here we show a significant delay (0.47 days per year, over a 20-year period) in the hibernation emergence date of adult females in a wild population of Columbian ground squirrels in Alberta, Canada. This finding was related to the climatic conditions at our study location: owing to within-individual phenotypic plasticity, females emerged later during years of lower spring temperature and delayed snowmelt. Although there has not been a significant annual trend in spring temperature, the date of snowmelt has become progressively later owing to an increasing prevalence of late-season snowstorms. Importantly, years of later emergence were also associated with decreased individual fitness. There has consequently been a decline in mean fitness (that is, population growth rate) across the past two decades. Our results show that plastic responses to climate change may be driven by climatic trends other than increasing temperature, and may be associated with declines in individual fitness and, hence, population viability.

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Figure 1: Variation in emergence date from hibernation and two environmental predictors of emergence (spring temperature and date of snowmelt) for adult female Columbian ground squirrels during the past 20 years.
Figure 2: Influence of mean emergence date from hibernation on, and the annual trend in, mean annual fitness of adult female Columbian ground squirrels over the past 20 years.


  1. Parmesan, C. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637–669 (2006)

    Article  Google Scholar 

  2. Thackeray, S. J. et al. Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Glob. Change Biol. 16, 3304–3313 (2010)

    Article  ADS  Google Scholar 

  3. Both, C., van Asch, M., Bijlsma, R. G., van den Burg, A. B. & Visser, M. E. Climate change and unequal phenoloical changes across four trophic levels: constraints or adaptations? J. Anim. Ecol. 78, 73–83 (2009)

    Article  Google Scholar 

  4. Intergovernmental Panel on Climate Change. The Physical Science Basis: Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (Cambridge Univ. Press, 2007)

  5. Visser, M. E. Keeping up with a warming world: assessing the rate of adaptation to climate change. Proc. R. Soc. B. 275, 649–659 (2008)

    Article  Google Scholar 

  6. Ozgul, A. et al. Coupled dynamics of body mass and population growth in response to environmental change. Nature 466, 482–485 (2010)

    Article  ADS  CAS  Google Scholar 

  7. Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003)

    Article  ADS  CAS  Google Scholar 

  8. Root, T. L. et al. Fingerprints of global warming on wild animals and plants. Nature 421, 57–60 (2003)

    Article  ADS  CAS  Google Scholar 

  9. Møller, A. P., Rubolini, D. & Lehikoinen, E. Populations of migratory bird species that did not show a phenological response to climate change are declining. Proc. Natl Acad. Sci. USA 105, 16195–16200 (2008)

    Article  ADS  Google Scholar 

  10. Both, C., Bouwhuis, S., Lessells, C. M. & Visser, M. E. Climate change and population declines in a long-distance migratory bird. Nature 441, 81–83 (2006)

    Article  ADS  CAS  Google Scholar 

  11. Saino, N. et al. Climate warming, ecological mismatch at arrival and population decline in migratory birds. Proc. R. Soc. B. 278, 835–842 (2011)

    Article  Google Scholar 

  12. Geiser, F. & Ruf, T. Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol. Zool. 68, 935–966 (1995)

    Article  Google Scholar 

  13. Humphries, M. M., Thomas, D. W. & Kramer, D. L. The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiol. Biochem. Zool. 76, 165–179 (2003)

    Article  Google Scholar 

  14. Michener, G. R. Spring emergence schedules and vernal behaviour of Richardson’s ground squirrels: why do males emerge from hibernation before females? Behav. Ecol. Sociobiol. 14, 29–38 (1983)

    Article  Google Scholar 

  15. Dobson, F. S., Badry, M. J. & Geddes, C. Seasonal activity and body mass of Columbian ground squirrels. Can. J. Zool. 70, 1364–1368 (1992)

    Article  Google Scholar 

  16. Michener, G. R. Effects of climatic conditions on the annual activity and hibernation cycle of Richardson’s ground squirrels and Columbian ground squirrels. Can. J. Zool. 55, 693–703 (1977)

    Article  Google Scholar 

  17. Lane, J. E. et al. A quantitative genetic analysis of hibernation emergence date in a wild population of Columbian ground squirrels. J. Evol. Biol. 24, 1949–1959 (2011)

    Article  CAS  Google Scholar 

  18. Nussey, D. H., Wilson, A. J. & Brommer, J. E. The evolutionary ecology of individual phenotypic plasticity in wild populations. J. Evol. Biol. 20, 831–844 (2007)

    Article  CAS  Google Scholar 

  19. Christensen, J. H. et al. in The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds Solomon, S. et al.) 847–940 (Cambridge Univ. Press, 2007)

  20. Murie, J. O. & Harris, M. A. Annual variation of spring emergence and breeding in Columbian ground squirrels (Spermophilus columbianus). J. Mamm. 63, 431–439 (1982)

    Article  Google Scholar 

  21. Qvarnström, A. Brommer, J. E. & Gustafsson, L. Testing the genetics underlying the co-evolution of mate choice and ornament in the wild. Nature 441, 84–86 (2006)

    Article  ADS  Google Scholar 

  22. Wiggett, D. R. & Boag, D. A. Intercolony natal dispersal in the Columbian ground squirrel. Can. J. Zool. 67, 42–50 (1989)

    Article  Google Scholar 

  23. Murie, J. O., Boag, D. A. & Kivett, V. K. Litter size in Columbian ground squirrels (Spermophilus columbianus). J. Mamm. 61, 237–244 (1980)

    Article  Google Scholar 

  24. Dobson, F. S. & Murie, J. O. Interpretation of intraspecific life history patterns: evidence from Columbian ground squirrels. Am. Nat. 129, 382–397 (1987)

    Article  Google Scholar 

  25. Boag, D. A. & Murie, J. O. Weight in relation to sex, age and season in Columbian ground squirrels (Sciuridae: Rodentia). Can. J. Zool. 59, 999–1004 (1981)

    Article  Google Scholar 

  26. Charmantier, A. et al. Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320, 800–803 (2008)

    Article  ADS  CAS  Google Scholar 

  27. van de Pol, M. & Wright, J. A simple method for distinguishing within- versus between-subject effects using mixed models. Anim. Behav. 77, 753–758 (2009)

    Article  Google Scholar 

  28. Lande, R. & Arnold, S. J. The measurement of selection on correlated characters. Evolution 37, 1210–1226 (1983)

    Article  Google Scholar 

  29. Whiteman, C. D. Mountain Meteorology: Fundamentals and Applications. (Oxford University Press, 2000)

    Google Scholar 

  30. Bates, D. M., Maechler, M. & Dai, B. lme4: Linear mixed-effects models using S4 classes. (2008)

  31. Sæther, B.-E., Ringsby, T. H., Bakke, O. & Solberg, E. J. Spatial and temporal variation in demography of a house sparrow metapopulation. J. Anim. Ecol. 68, 628–637 (1999)

    Article  Google Scholar 

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We thank the volunteers and assistants who helped with fieldwork, and the University of Calgary for providing accommodation at the Biogeosciences Institute (E. Johnson and J. Buchanan-Mappin). D. Stralberg, S. Boutin and E. Bayne provided comments and assistance that improved an earlier version of this paper, and M. Low wrote the R script to calculate the spring temperature climate window. Funding was provided by the Natural Sciences and Engineering Research Council of Canada (NSERC) (J.O.M. and S. Boutin (University of Alberta)), National Science Foundation (DEB-0089473) (F.S.D.), the Royal Society of London (J.E.L. and L.E.B.K) and Agence Nationale de la Recherche of France (ANR-08-JCJC-0041-01) (A.C., F.S.D. and J.E.L.) and the Alberta Conservation Association (J.E.L.). All protocols were approved by the Life and Environmental Sciences Animal Care Committee at the University of Calgary as well as the Animal Care and Use Committee at the University of Alberta (1992 to 1998) or the Institutional Animal Care and Use Committee at Auburn University (1999 to 2011).

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J.E.L., L.E.B.K., A.C. and F.S.D. developed the concept of the paper, and F.S.D. and J.O.M. collected the field data. J.E.L. performed all analyses and wrote the paper, and all other authors provided intellectual insight and detailed comments. All authors obtained funding.

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Correspondence to Jeffrey E. Lane.

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The authors declare no competing financial interests.

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Lane, J., Kruuk, L., Charmantier, A. et al. Delayed phenology and reduced fitness associated with climate change in a wild hibernator. Nature 489, 554–557 (2012).

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