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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.


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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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