Letter | Published:

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

Nature volume 466, pages 482485 (22 July 2010) | Download Citation

Abstract

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.

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References

  1. 1.

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

  2. 2.

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

  3. 3.

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

  4. 4.

    , , , & Putting evolutionary biology back in the ecological theatre: a demographic framework mapping genes to communities. Evol. Ecol. Res. 8, 1155–1171 (2006)

  5. 5.

    , & Adaptation, plasticity and extinction in a changing environment: Towards a predictive theory. PLoS Biol. 8, e1000357 (2010)

  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.

    & Modern global climate change. Science 302, 1719–1723 (2003)

  8. 8.

    , , & Climate change is affecting altitudinal migrants and hibernating species. Proc. Natl Acad. Sci. USA 97, 1630–1633 (2000)

  9. 9.

    & Birds extend their ranges northwards. Nature 399, 213 (1999)

  10. 10.

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

  11. 11.

    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)

  12. 12.

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

  13. 13.

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

  14. 14.

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

  15. 15.

    , , & Genetic and plastic responses of a northern mammal to climate change. Proc. R. Soc. Lond. B 270, 591–596 (2003)

  16. 16.

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

  17. 17.

    , , & Rapid microevolution of migratory behavior in a wild bird species. Nature 360, 668–670 (1992)

  18. 18.

    , , , & Climate change and evolution: disentangling environmental and genetic responses. Mol. Ecol. 17, 167–178 (2008)

  19. 19.

    & Structured-Population Models in Marine, Terrestrial, and Freshwater Systems (Chapman & Hall, 1997)

  20. 20.

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

  21. 21.

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

  22. 22.

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

  23. 23.

    , , , & The evolutionary demography of ecological change: linking trait variation and population growth. Science 315, 1571–1574 (2007)

  24. 24.

    , & Seasonal changes in weights of marmots. Am. Midl. Nat. 96, 36–51 (1976)

  25. 25.

    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)

  26. 26.

    , , , & Capture–recapture studies for multiple strata including non-Markovian transitions. Biometrics 49, 1173–1187 (1993)

  27. 27.

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

  28. 28.

    , & Size-specific sensitivity: Applying a new structured population model. Ecology 81, 694–708 (2000)

  29. 29.

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

  30. 30.

    , & Bioenergetic prediction of climate change impacts on northern mammals. Integr. Comp. Biol. 44, 152 (2004)

  31. 31.

    & Marmota flaviventris. Mamm. Species 135, 1–8 (1980)

  32. 32.

    , & 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)

  33. 33.

    & Energetics of yellow-bellied marmot populations. Ecology 59, 78–88 (1978)

  34. 34.

    , & Socioecology of marmots: female reproductive strategies. Ecology 57, 552–560 (1976)

  35. 35.

    , & Energy allocation by yellow-bellied marmots. Physiol. Zool. 62, 429–448 (1989)

  36. 36.

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

  37. 37.

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

  38. 38.

    , , , & Influence of local demography on asymptotic and transient dynamics of a yellow-bellied marmot metapopulation. Am. Nat. 173, 517–530 (2009)

  39. 39.

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

  40. 40.

    & Demography of yellow-bellied marmot populations. Ecology 55, 1233–1245 (1974)

  41. 41.

    , & A 32-year demography of yellow-bellied marmots (Marmota flaviventris). J. Zool. (Lond.) 246, 337–346 (1998)

  42. 42.

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

  43. 43.

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

  44. 44.

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

  45. 45.

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

  46. 46.

    & Mixed Effects Models in S and S-PLUS (Springer, 2000)

  47. 47.

    & Program MARK: survival estimation from populations of marked animals. Bird Study 46, 120–139 (1999)

  48. 48.

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

  49. 49.

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

  50. 50.

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

  51. 51.

    & Model Selection and Inference: A Practical Information-Theoretic Approach 2nd edn (Springer, 2002)

  52. 52.

    , , , & Evolution of complex flowering strategies: an age- and size-structured integral projection model. Proc. R. Soc. Lond. B 270, 1829 (2003)

  53. 53.

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

  54. 54.

    R: A language and environment for statistical computing〉 (2008)

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Acknowledgements

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.

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Affiliations

  1. Department of Life Sciences, Imperial College London, Ascot, Berkshire SL5 7PY, UK

    • Arpat Ozgul
    •  & Tim Coulson
  2. Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK

    • Dylan Z. Childs
  3. Department of Wildlife Ecology and Conservation, University of Florida, Gainesville, Florida 32611, USA

    • Madan K. Oli
  4. Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, Kansas 66045, USA

    • Kenneth B. Armitage
  5. Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California 90095, USA

    • Daniel T. Blumstein
    •  & Lucretia E. Olson
  6. Department of Biology, Stanford University, Stanford, California 94305, USA

    • Shripad Tuljapurkar

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Contributions

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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Arpat Ozgul.

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https://doi.org/10.1038/nature09210

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