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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    et al. Responses of tundra plants to experimental warming: meta-analysis of the international tundra experiment. Ecol. Monogr. 69, 491–511 (1999)

  2. 2.

    , , & Changes in leaf phenology of three European oak species in response to experimental climate change. New Phytol. 186, 900–910 (2010)

  3. 3.

    et al. European phenological response to climate change matches the warming pattern. Glob. Change Biol. 12, 1969–1976 (2006)

  4. 4.

    , & Onset of spring starting earlier across the Northern Hemisphere. Glob. Change Biol. 12, 343–351 (2006)

  5. 5.

    Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob. Change Biol. 13, 1860–1872 (2007)

  6. 6.

    , , , & Shifting plant phenology in response to global change. Trends Ecol. Evol. 22, 357–365 (2007)

  7. 7.

    & Physiological and growth responses of arctic plants to a field experiment simulating climatic change. Ecology 77, 822–840 (1996)

  8. 8.

    , , & A 250-year index of first flowering dates and its response to temperature changes. Proc. R. Soc. Lond. B 277, 2451–2457 (2010)

  9. 9.

    & Shifting dominance within a montane vegetation community: results of a climate-warming experiment. Science 267, 876–880 (1995)

  10. 10.

    , & Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol. Monogr. 73, 69–86 (2003)

  11. 11.

    et al. Divergence of reproductive phenology under climate warming. Proc. Natl Acad. Sci. USA 104, 198–202 (2007)

  12. 12.

    , & Warming, photoperiods, and tree phenology. Science 329, 277–278 (2010)

  13. 13.

    , , & Integrating experimental and gradient methods in ecological climate change research. Ecology 85, 904–916 (2004)

  14. 14.

    , & Temperature signals contribute to the timing of photoperiodic growth cessation and bud set in poplar. Tree Physiol. 31, 472–482 (2011)

  15. 15.

    & Observations: Surface and Atmospheric Climate Change 235–336 (IPCC, 2007)

  16. 16.

    et al. Open-top designs for manipulating field temperature in high-latitude ecosystems. Glob. Change Biol. 3, 20–32 (1997)

  17. 17.

    Theory and performance of an infrared heater for ecosystem warming. Glob. Change Biol. 11, 2041–2056 (2005)

  18. 18.

    et al. Infrared heater arrays for warming ecosystem field plots. Glob. Change Biol. 142, 309–320 (2008)

  19. 19.

    Simulated climate-change: are passive greenhouses a valid microcosm for testing the biological effects of environmental perturbations? Glob. Change Biol. 1, 29–42 (1995)

  20. 20.

    Responses to natural climatic variation and experimental warming in two tundra plant species with contrasting life forms: Cassiope tetragona and Ranunculus nivalis. Glob. Change Biol. 3, 97–107 (1997)

  21. 21.

    Temperature effects of passive greenhouse apparatus in high-latitude climate-change experiments. Funct. Ecol. 9, 340–350 (1995)

  22. 22.

    & Phenological patterns of terrestrial plants. Annu. Rev. Ecol. Syst. 16, 179–214 (1985)

  23. 23.

    , , , & Robust control of the seasonal expression of the Arabidopsis FLC gene in a fluctuating environment. Proc. Natl Acad. Sci. USA 107, 11632–11637 (2010)

  24. 24.

    , & Principles of Terrestrial Ecosystem Ecology (Springer, 2002)

  25. 25.

    & Phenology under global warming. Science 327, 1461–1462 (2010)

  26. 26.

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

  27. 27.

    & Novel climates, no-analog communities, and ecological surprises. Front. Ecol. Environ. 59, 475–482 (2007)

  28. 28.

    et al. Attributing physical and biological impacts to anthropogenic climate change. Nature 453, 353–357 (2008)

Download references

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

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, New York 10025, USA

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

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

    • J. M. Allen
  5. USA National Phenology Network, 1955 East Sixth Street, Tucson, Arizona 85721, USA

    • T. M. Crimmins
  6. US Geological Survey, 1955 East Sixth Street, Tucson, Arizona 85719, USA

    • J. L. Betancourt
  7. Department of Biological Sciences, North Dakota State University, Fargo, North Dakota 58108, 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, Maryland 20742, USA

    • N. J. B. Kraft
  12. National Center for Atmospheric Research, PO Box 3000, Boulder, Colorado 80307, 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, California 93106, 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, Maine 04469, USA

    • B. J. McGill
  18. Integrative Biology, University of Texas, 1 University Station C0930, Austin, Texas 78712, 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, Wisconsin 53201-0413, USA

    • M. D. Schwartz

Authors

  1. Search for E. M. Wolkovich in:

  2. Search for B. I. Cook in:

  3. Search for J. M. Allen in:

  4. Search for T. M. Crimmins in:

  5. Search for J. L. Betancourt in:

  6. Search for S. E. Travers in:

  7. Search for S. Pau in:

  8. Search for J. Regetz in:

  9. Search for T. J. Davies in:

  10. Search for N. J. B. Kraft in:

  11. Search for T. R. Ault in:

  12. Search for K. Bolmgren in:

  13. Search for S. J. Mazer in:

  14. Search for G. J. McCabe in:

  15. Search for B. J. McGill in:

  16. Search for C. Parmesan in:

  17. Search for N. Salamin in:

  18. Search for M. D. Schwartz in:

  19. Search for E. E. Cleland in:

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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to E. M. Wolkovich.

Supplementary information

PDF files

  1. 1.

    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.

Zip files

  1. 1.

    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.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature11014

Further reading

Comments

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.