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Warming experiments underpredict plant phenological responses to climate change

Nature volume 485, pages 494–497 (2012)Cite this article

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Abstract

Warming experiments are increasingly relied on to estimate plant responses to global climate change1,2. For experiments to provide meaningful predictions of future responses, they should reflect the empirical record of responses to temperature variability and recent warming, including advances in the timing of flowering and leafing3,4,5. We compared phenology (the timing of recurring life history events) in observational studies and warming experiments spanning four continents and 1,634 plant species using a common measure of temperature sensitivity (change in days per degree Celsius). We show that warming experiments underpredict advances in the timing of flowering and leafing by 8.5-fold and 4.0-fold, respectively, compared with long-term observations. For species that were common to both study types, the experimental results did not match the observational data in sign or magnitude. The observational data also showed that species that flower earliest in the spring have the highest temperature sensitivities, but this trend was not reflected in the experimental data. These significant mismatches seem to be unrelated to the study length or to the degree of manipulated warming in experiments. The discrepancy between experiments and observations, however, could arise from complex interactions among multiple drivers in the observational data, or it could arise from remediable artefacts in the experiments that result in lower irradiance and drier soils, thus dampening the phenological responses to manipulated warming. Our results introduce uncertainty into ecosystem models that are informed solely by experiments and suggest that responses to climate change that are predicted using such models should be re-evaluated.

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Figure 1: Map of the experimental and observational sites.
Figure 2: Estimates of the flowering and leafing sensitivities.
Figure 3: Relationship between sensitivities to temperature calculated from interannual variation and from long-term trends.
Figure 4: Sensitivity to temperature decreases throughout the growing season.

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Acknowledgements

This work was conducted as part of the Forecasting Phenology Working Group supported by the National Center for Ecological Analysis & Synthesis (EF-0553768), with additional support from National Science Foundation grants DBI-0905806, IOS-0639794, DEB-0922080 and the Natural Sciences and Engineering Research Council of Canada CREATE Training Program. Special thanks to the many data managers, including G. Aldridge, P. Huth, D. Inouye, G. Johansson, A. Miller-Rushing, J. O’Keefe, R. Primack, S. Smiley, T. Sparks and J. Thompson. We thank M. Ayres, L. Kueppers, D. Moore and M. O’Connor for comments on earlier drafts.

Author information

Authors and Affiliations

  1. Division of Biological Sciences, University of California San Diego, 9500 Gilman Drive 0116, La Jolla, California 92093, USA,

    E. M. Wolkovich & E. E. Cleland

  2. NASA Goddard Institute for Space Studies, New York, 10025, New York, USA

    B. I. Cook

  3. Ocean and Climate Physics, Lamont-Doherty Earth Observatory, Palisades, 10964-8000, New York, USA

    B. I. Cook

  4. Department of Ecology & Evolutionary Biology, University of Connecticut, Storrs, 06269-3043, Connecticut, USA

    J. M. Allen

  5. USA National Phenology Network, 1955 East Sixth Street, Tucson, 85721, Arizona, USA

    T. M. Crimmins

  6. US Geological Survey, 1955 East Sixth Street, Tucson, 85719, Arizona, USA

    J. L. Betancourt

  7. Department of Biological Sciences, North Dakota State University, Fargo, 58108, North Dakota, USA

    S. E. Travers

  8. National Center for Ecological Analysis and Synthesis, 735 State Street, Suite 300, Santa Barbara, California 93101, USA ,

    S. Pau & J. Regetz

  9. Department of Biology, McGill University, 1205 Avenue Docteur Penfield, Montreal, Quebec H3A 1B1, Canada,

    T. J. Davies

  10. Biodiversity Research Centre, University of British Columbia, 6270 University Boulevard, Vancouver, British Columbia V6T 1Z4, Canada ,

    N. J. B. Kraft

  11. Department of Biology, University of Maryland, College Park, 20742, Maryland, USA

    N. J. B. Kraft

  12. National Center for Atmospheric Research, PO Box 3000, Boulder, 80307, Colorado, USA

    T. R. Ault

  13. Swedish University of Agricultural Sciences, Swedish National Phenology Network, Asa, Unit for Field-based Forest Research, SE-36030 Lammhult, Sweden ,

    K. Bolmgren

  14. Theoretical Population Ecology and Evolution, Lund University, SE-22362 Lund, Sweden ,

    K. Bolmgren

  15. Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, 93106, California, USA

    S. J. Mazer

  16. US Geological Survey, Denver Federal Center, MS 412, Denver, Colorado 80225, USA ,

    G. J. McCabe

  17. School of Biology and Ecology & Sustainability Solutions Initiative, University of Maine, Orono, 04469, Maine, USA

    B. J. McGill

  18. Integrative Biology, University of Texas, 1 University Station C0930, Austin, 78712, Texas, USA

    C. Parmesan

  19. Marine Sciences Institute, A425 Portland Square, Drake Circus, University of Plymouth, Plymouth, Devon PL4 8AA, UK ,

    C. Parmesan

  20. Department of Ecology and Evolution, University of Lausanne, 1015 Lausanne, Switzerland,

    N. Salamin

  21. Swiss Institute of Bioinformatics, Quartier Sorge, 1015 Lausanne, Switzerland ,

    N. Salamin

  22. Department of Geography, Bolton 410, PO Box 413, University of Wisconsin-Milwaukee, Milwaukee, 53201-0413, Wisconsin, USA

    M. D. Schwartz

Authors
  1. E. M. Wolkovich
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  2. B. I. Cook
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  17. N. Salamin
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  18. M. D. Schwartz
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  19. E. E. Cleland
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Contributions

E.M.W. conceived the idea, performed analyses and wrote the paper. B.I.C. performed analyses. E.E.C. and N.J.B.K. assisted with analyses. E.M.W., E.E.C., J.M.A., T.M.C., S.E.T. and S.P. developed the STONE database. E.M.W., B.I.C. and J.R. contributed extensively to development of the NECTAR database. All authors (including J.L.B., T.J.D., T.R.A., K.B., S.J.M., G.J.M., B.J.M., C.P., N.S. and M.D.S.) contributed to the editing of the manuscript and to data management of the observational data sets.

Corresponding author

Correspondence to E. M. Wolkovich.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Text including Supplementary Data, Supplementary Methods and Supplementary Results. Also included are Supplementary Tables 1-6, Supplementary Figures 1-9 and additional references. (PDF 712 kb)

Supplementary Data

This file contains the raw sensitivities that are shown in Figure S2c, which are from the PEP725 database and which are discussed in the Supplementary Data, Methods and Results. (ZIP 3239 kb)

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Wolkovich, E., Cook, B., Allen, J. et al. Warming experiments underpredict plant phenological responses to climate change. Nature 485, 494–497 (2012). https://doi.org/10.1038/nature11014

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