Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Coupled dynamics of body mass and population growth in response to environmental change


Environmental change has altered the phenology, morphological traits and population dynamics of many species1,2. However, the links underlying these joint responses remain largely unknown owing to a paucity of long-term data and the lack of an appropriate analytical framework3. Here we investigate the link between phenotypic and demographic responses to environmental change using a new methodology and a long-term (1976–2008) data set from a hibernating mammal (the yellow-bellied marmot) inhabiting a dynamic subalpine habitat. We demonstrate how earlier emergence from hibernation and earlier weaning of young has led to a longer growing season and larger body masses before hibernation. The resulting shift in both the phenotype and the relationship between phenotype and fitness components led to a decline in adult mortality, which in turn triggered an abrupt increase in population size in recent years. Direct and trait-mediated effects of environmental change made comparable contributions to the observed marked increase in population growth. Our results help explain how a shift in phenology can cause simultaneous phenotypic and demographic changes, and highlight the need for a theory integrating ecological and evolutionary dynamics in stochastic environments4,5.

This is a preview of subscription content

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Trends in the phenology, mean phenotypic trait and demography for females of the yellow-bellied marmot population.
Figure 2: The relationship between body mass and demographic and trait transition rates.
Figure 3: Trait-based analysis of the population dynamics.
Figure 4: Contributions of the changes in mean mass ( Z 1 to Z 2) and mass-survival relationship ( S 1 to S 2) to the increase in mean survival from <2000 to ≥2000.


  1. 1

    Walther, G. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002)

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. 2

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

    Article  Google Scholar 

  3. 3

    Stenseth, N. & Mysterud, A. Climate, changing phenology, and other life history traits: Nonlinearity and matchñmismatch to the environment. Proc. Natl Acad. Sci. USA 99, 13379–13381 (2002)

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. 4

    Coulson, T., Benton, T. G., Lundberg, P., Dall, S. R. X. & Kendall, B. E. Putting evolutionary biology back in the ecological theatre: a demographic framework mapping genes to communities. Evol. Ecol. Res. 8, 1155–1171 (2006)

    Google Scholar 

  5. 5

    Chevin, L. M., Lande, R. & Mace, G. M. Adaptation, plasticity and extinction in a changing environment: Towards a predictive theory. PLoS Biol. 8, e1000357 (2010)

    Article  PubMed  PubMed Central  Google Scholar 

  6. 6

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

  7. 7

    Karl, T. & Trenberth, K. Modern global climate change. Science 302, 1719–1723 (2003)

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. 8

    Inouye, D. W., Barr, B., Armitage, K. B. & Inouye, B. D. Climate change is affecting altitudinal migrants and hibernating species. Proc. Natl Acad. Sci. USA 97, 1630–1633 (2000)

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. 9

    Thomas, C. & Lennon, J. Birds extend their ranges northwards. Nature 399, 213 (1999)

    ADS  CAS  Article  Google Scholar 

  10. 10

    Pounds, J. A. et al. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439, 161–167 (2006)

    ADS  CAS  Article  PubMed  Google Scholar 

  11. 11

    Jenouvrier, S. et al. Demographic models and IPCC climate projections predict the decline of an emperor penguin population. Proc. Natl Acad. Sci. USA 106, 1844–1847 (2009)

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. 12

    Fisher, R. A. The Genetical Theory of Natural Selection (Oxford Univ. Press, 1958)

    MATH  Google Scholar 

  13. 13

    Bradshaw, W. & Holzapfel, C. Evolutionary response to rapid climate change. Science 312, 1477–1478 (2006)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. 14

    Via, S. et al. Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol. Evol. 10, 212–217 (1995)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. 15

    Reale, D., McAdam, A. G., Boutin, S. & Berteaux, D. Genetic and plastic responses of a northern mammal to climate change. Proc. R. Soc. Lond. B 270, 591–596 (2003)

    Article  Google Scholar 

  16. 16

    Lande, R. Natural selection and random genetic drift in phenotypic evolution. Evolution 30, 314–334 (1976)

    Article  PubMed  PubMed Central  Google Scholar 

  17. 17

    Berthold, P., Helbig, A. J., Mohr, G. & Querner, U. Rapid microevolution of migratory behavior in a wild bird species. Nature 360, 668–670 (1992)

    ADS  Article  Google Scholar 

  18. 18

    Gienapp, P., Teplitsky, C., Alho, J. S., Mills, J. A. & Merila, J. Climate change and evolution: disentangling environmental and genetic responses. Mol. Ecol. 17, 167–178 (2008)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. 19

    Tuljapurkar, S. & Caswell, H. Structured-Population Models in Marine, Terrestrial, and Freshwater Systems (Chapman & Hall, 1997)

    Book  Google Scholar 

  20. 20

    Sæther, B.-E. et al. Population dynamical consequences of climate change for a small temperate songbird. Science 287, 854–856 (2000)

    ADS  Article  PubMed  PubMed Central  Google Scholar 

  21. 21

    Coulson, T. & Tuljapurkar, S. The dynamics of a quantitative trait in an age-structured population living in a variable environment. Am. Nat. 172, 599–612 (2008)

    Article  PubMed  PubMed Central  Google Scholar 

  22. 22

    Ozgul, A. et al. The dynamics of phenotypic change and the shrinking sheep of St. Kilda. Science 325, 464–467 (2009)

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23

    Pelletier, F., Clutton-Brock, T., Pemberton, J., Tuljapurkar, S. & Coulson, T. The evolutionary demography of ecological change: linking trait variation and population growth. Science 315, 1571–1574 (2007)

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. 24

    Armitage, K. B., Downhower, J. F. & Svendsen, G. E. Seasonal changes in weights of marmots. Am. Midl. Nat. 96, 36–51 (1976)

    Article  Google Scholar 

  25. 25

    Armitage, K. B. in Wild Mammals of North America: Biology, Management, and Conservation 2nd edn (eds Feldhamer, G. A., Thompson, B. C. & Chapman, J. A.) 188–210 (Johns Hopkins Univ. Press, 2003)

    Google Scholar 

  26. 26

    Brownie, C., Hines, J. E., Nichols, J. D., Pollock, K. H. & Hestbeck, J. B. Capture–recapture studies for multiple strata including non-Markovian transitions. Biometrics 49, 1173–1187 (1993)

    Article  Google Scholar 

  27. 27

    Wood, S. N. Generalized Additive Models: An Introduction with R. (Chapman & Hall, 2006)

    Book  Google Scholar 

  28. 28

    Easterling, M. R., Ellner, S. P. & Dixon, P. M. Size-specific sensitivity: Applying a new structured population model. Ecology 81, 694–708 (2000)

    Article  Google Scholar 

  29. 29

    Ellner, S. P. & Rees, M. Integral projection models for species with complex demography. Am. Nat. 167, 410–428 (2006)

    Article  PubMed  PubMed Central  Google Scholar 

  30. 30

    Humphries, M., Umbanhowar, J. & McCann, K. Bioenergetic prediction of climate change impacts on northern mammals. Integr. Comp. Biol. 44, 152 (2004)

    Article  PubMed  PubMed Central  Google Scholar 

  31. 31

    Frase, B. A. & Hoffmann, R. S. Marmota flaviventris . Mamm. Species 135, 1–8 (1980)

    Article  Google Scholar 

  32. 32

    Armitage, K. B., Melcher, J. C. & Ward, J. M. Oxygen consumption and body temperature in yellow-bellied marmot populations from montane-mesic and lowland-xeric environments. J. Comp. Physiol. B 160, 491–502 (1990)

    Article  Google Scholar 

  33. 33

    Kilgore, D. L. & Armitage, K. B. Energetics of yellow-bellied marmot populations. Ecology 59, 78–88 (1978)

    Article  Google Scholar 

  34. 34

    Andersen, D., Armitage, K. & Hoffmann, R. Socioecology of marmots: female reproductive strategies. Ecology 57, 552–560 (1976)

    Article  Google Scholar 

  35. 35

    Melcher, J., Armitage, K. & Porter, W. Energy allocation by yellow-bellied marmots. Physiol. Zool. 62, 429–448 (1989)

    Article  Google Scholar 

  36. 36

    Armitage, K. B. Sociality as a life-history tactic of ground-squirrels. Oecologia 48, 36–49 (1981)

    ADS  Article  PubMed  PubMed Central  Google Scholar 

  37. 37

    Armitage, K. B. Reproductive strategies of yellow-bellied marmots: energy conservation and differences between the sexes. J. Mamm. 79, 385–393 (1998)

    Article  Google Scholar 

  38. 38

    Ozgul, A., Oli, M. K., Armitage, K. B., Blumstein, D. T. & Van Vuren, D. H. Influence of local demography on asymptotic and transient dynamics of a yellow-bellied marmot metapopulation. Am. Nat. 173, 517–530 (2009)

    Article  PubMed  PubMed Central  Google Scholar 

  39. 39

    Armitage, K. B. Social and population dynamics of yellow-bellied marmots: results from long-term research. Annu. Rev. Ecol. Syst. 22, 379–407 (1991)

    Article  Google Scholar 

  40. 40

    Armitage, K. B. & Downhower, J. F. Demography of yellow-bellied marmot populations. Ecology 55, 1233–1245 (1974)

    Article  Google Scholar 

  41. 41

    Schwartz, O. A., Armitage, K. B. & Van Vuren, D. A 32-year demography of yellow-bellied marmots (Marmota flaviventris). J. Zool. (Lond.) 246, 337–346 (1998)

    Article  Google Scholar 

  42. 42

    Frase, B. A. & Armitage, K. B. Yellow-bellied marmots are generalist herbivores. Ethol. Ecol. Evol. 1, 353–366 (1989)

    Article  Google Scholar 

  43. 43

    Woods, B. C. & Armitage, K. B. Effect of food supplementation on juvenile growth and survival in Marmota flaviventris . J. Mamm. 84, 903–914 (2003)

    Article  Google Scholar 

  44. 44

    Armitage, K. B. in Biodiversity in Marmots (eds Le Berre, M., Ramousse, R. & Le Guelte, L.) 223–226 (International Marmot Network, 1996)

    Google Scholar 

  45. 45

    Bates, D. & Maechler, M. lme4: Linear mixed-effects models using S4 classes. R package v. 0.999375-32. (2009)

  46. 46

    Pinheiro, J. C. & Bates, D. M. Mixed Effects Models in S and S-PLUS (Springer, 2000)

    Book  Google Scholar 

  47. 47

    White, G. C. & Burnham, K. P. Program MARK: survival estimation from populations of marked animals. Bird Study 46, 120–139 (1999)

    Article  Google Scholar 

  48. 48

    Laake, J. & Rexstad, E. in Program MARK: A Gentle Introduction (eds Cooch, E. & White, G. C) 〈〉 (2007)

    Google Scholar 

  49. 49

    Schluter, D. Estimating the form of natural selection on a quantitative trait. Evolution 42, 849–861 (1988)

    Article  PubMed  PubMed Central  Google Scholar 

  50. 50

    Kingsolver, J. G. et al. The strength of phenotypic selection in natural populations. Am. Nat. 157, 245–261 (2001)

    CAS  Article  Google Scholar 

  51. 51

    Burnham, K. P. & Anderson, D. R. Model Selection and Inference: A Practical Information-Theoretic Approach 2nd edn (Springer, 2002)

    MATH  Google Scholar 

  52. 52

    Childs, D., Rees, M., Rose, K., Grubb, P. & Ellner, S. Evolution of complex flowering strategies: an age- and size-structured integral projection model. Proc. R. Soc. Lond. B 270, 1829 (2003)

    Article  Google Scholar 

  53. 53

    Caswell, H. Matrix Population Models: Construction, Analysis, and Interpretation (Sinauer, 2001)

    Google Scholar 

  54. 54

    R Project for Statistical Computing R: A language and environment for statistical computing 〈〉 (2008)

Download references


We thank the ‘marmoteers’ who participated in collecting the long-term data, Rocky Mountain Biological Laboratory for providing the field facilities, B. Barr and D. Inouye for providing additional information on climate and plant phenology, and L. M. Chevin, J. A. Hostetler, D. Inouye, N. J. Singh and I. M. Smallegange for comments. This work was funded by NERC, the Wellcome Trust, NSF, NIH and NIA.

Author information




K.B.A. and D.T.B. led the long-term study; K.B.A., D.T.B., L.E.O. and A.O. collected data; A.O. and T.C. conceived the ideas for the paper and its structure; A.O., D.Z.C., T.C., M.K.O. and S.T. designed the analyses; A.O. and D.Z.C. conducted the analyses; A.O. wrote the manuscript; all authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to Arpat Ozgul.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Table S1 and Supplementary Figures S1-S8 with legends. (PDF 559 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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

Download citation

Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing