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Warming experiments underpredict plant phenological responses to climate change


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

    Google Scholar 

  2. Morin, X., Roy, J., Sonie, L. & Chuine, I. Changes in leaf phenology of three European oak species in response to experimental climate change. New Phytol. 186, 900–910 (2010)

    Article  Google Scholar 

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

    Article  ADS  Google Scholar 

  4. Schwartz, M. D., Ahas, R. & Aasa, A. Onset of spring starting earlier across the Northern Hemisphere. Glob. Change Biol. 12, 343–351 (2006)

    Article  ADS  Google Scholar 

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

    Article  ADS  Google Scholar 

  6. Cleland, E. E., Chuine, I., Menzel, A., Mooney, H. A. & Schwartz, M. D. Shifting plant phenology in response to global change. Trends Ecol. Evol. 22, 357–365 (2007)

    Article  Google Scholar 

  7. Chapin, F. S. & Shaver, G. R. Physiological and growth responses of arctic plants to a field experiment simulating climatic change. Ecology 77, 822–840 (1996)

    Article  Google Scholar 

  8. Amano, T., Smithers, R. J., Sparks, T. H. & Sutherland, W. J. A 250-year index of first flowering dates and its response to temperature changes. Proc. R. Soc. Lond. B 277, 2451–2457 (2010)

    Article  Google Scholar 

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

    Article  CAS  ADS  Google Scholar 

  10. Dunne, J. A., Harte, J. & Taylor, K. J. Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol. Monogr. 73, 69–86 (2003)

    Article  Google Scholar 

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

    Article  CAS  ADS  Google Scholar 

  12. Chuine, I., Morin, X. & Bugmann, H. Warming, photoperiods, and tree phenology. Science 329, 277–278 (2010)

    Article  ADS  Google Scholar 

  13. Dunne, J. A., Saleska, S. R., Fischer, M. L. & Harte, J. Integrating experimental and gradient methods in ecological climate change research. Ecology 85, 904–916 (2004)

    Article  Google Scholar 

  14. Rohde, A., Bastien, C. & Boerjan, W. Temperature signals contribute to the timing of photoperiodic growth cessation and bud set in poplar. Tree Physiol. 31, 472–482 (2011)

    Article  Google Scholar 

  15. Trenberth, K. E. & Josey, S. A. Observations: Surface and Atmospheric Climate Change 235–336 (IPCC, 2007)

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

    Article  Google Scholar 

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

    Google Scholar 

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

    ADS  Google Scholar 

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

    Article  ADS  Google Scholar 

  20. Molau, U. 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)

    Article  ADS  Google Scholar 

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

    Article  Google Scholar 

  22. Rathcke, B. & Lacey, E. P. Phenological patterns of terrestrial plants. Annu. Rev. Ecol. Syst. 16, 179–214 (1985)

    Article  Google Scholar 

  23. Aikawa, S., Kobayashi, M. J., Satake, A., Shimizu, K. K. & Kudoh, H. Robust control of the seasonal expression of the Arabidopsis FLC gene in a fluctuating environment. Proc. Natl Acad. Sci. USA 107, 11632–11637 (2010)

    Article  CAS  ADS  Google Scholar 

  24. Chapin, F. S., Matson, P. A. & Mooney, H. A. Principles of Terrestrial Ecosystem Ecology (Springer, 2002)

    Google Scholar 

  25. Körner, C. & Basler, D. Phenology under global warming. Science 327, 1461–1462 (2010)

    Article  ADS  Google Scholar 

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

    Article  CAS  ADS  Google Scholar 

  27. Williams, J. W. & Jackson, S. T. Novel climates, no-analog communities, and ecological surprises. Front. Ecol. Environ. 59, 475–482 (2007)

    Article  Google Scholar 

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

    Article  CAS  ADS  Google Scholar 

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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.

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Authors and Affiliations



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.

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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).

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