Letter | Published:

Declining global warming effects on the phenology of spring leaf unfolding

Nature volume 526, pages 104107 (01 October 2015) | Download Citation



Earlier spring leaf unfolding is a frequently observed response of plants to climate warming1,2,3,4. Many deciduous tree species require chilling for dormancy release, and warming-related reductions in chilling may counteract the advance of leaf unfolding in response to warming5,6. Empirical evidence for this, however, is limited to saplings or twigs in climate-controlled chambers7,8. Using long-term in situ observations of leaf unfolding for seven dominant European tree species at 1,245 sites, here we show that the apparent response of leaf unfolding to climate warming (ST, expressed in days advance of leaf unfolding per °C warming) has significantly decreased from 1980 to 2013 in all monitored tree species. Averaged across all species and sites, ST decreased by 40% from 4.0 ± 1.8 days °C−1 during 1980–1994 to 2.3 ± 1.6 days °C−1 during 1999–2013. The declining ST was also simulated by chilling-based phenology models, albeit with a weaker decline (24–30%) than observed in situ. The reduction in ST is likely to be partly attributable to reduced chilling. Nonetheless, other mechanisms may also have a role, such as ‘photoperiod limitation’ mechanisms that may become ultimately limiting when leaf unfolding dates occur too early in the season. Our results provide empirical evidence for a declining ST, but also suggest that the predicted strong winter warming in the future may further reduce ST and therefore result in a slowdown in the advance of tree spring phenology.

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  1. 1.

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

  2. 2.

    , , , & Increased plant growth in the northern high latitudes from 1981 to 1991. Nature 386, 698–702 (1997)

  3. 3.

    & Responses to a warming world. Science 294, 793–795 (2001)

  4. 4.

    et al. Recent spring phenology shifts in western Central Europe based on multiscale observations. Glob. Ecol. Biogeogr. 23, 1255–1263 (2014)

  5. 5.

    , & Winter and spring warming result in delayed spring phenology on the Tibetan Plateau. Proc. Natl Acad. Sci. USA 107, 22151–22156 (2010)

  6. 6.

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

  7. 7.

    , , & Sensitivity of leaf unfolding to experimental warming in three temperate tree species. Agric. For. Meteorol. 181, 125–132 (2013)

  8. 8.

    et al. Chilling outweighs photoperiod in preventing precocious spring development. Glob. Change Biol. 20, 170–182 (2014)

  9. 9.

    Why does phenology drive species distribution? Phil. Trans. R. Soc. B 365, 3149–3160 (2010)

  10. 10.

    & Common garden comparison of the leaf-out phenology of woody species from different native climates, combined with herbarium records, forecasts long-term change. Ecol. Lett. 17, 1016–1025 (2014)

  11. 11.

    , & Phenology feedbacks on climate change. Science 324, 887–888 (2009)

  12. 12.

    et al. Climate change, phenology, and phenological control of vegetation feedbacks to the climate system. Agric. For. Meteorol. 169, 156–173 (2013)

  13. 13.

    Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds et al.) (Cambridge Univ. Press, 2014)

  14. 14.

    et al. Leaf onset in the northern hemisphere triggered by daytime temperature. Nature Commun. 6, 6911 (2015)

  15. 15.

    & Photoperiod constraints on tree phenology, performance and migration in a warming world. Plant Cell Environ. 38, 1725–1736 (2015)

  16. 16.

    et al. Warming experiments underpredict plant phenological responses to climate change. Nature 485, 494–497 (2012)

  17. 17.

    Ontogenic changes rather than difference in temperature cause understory trees to leaf out earlier. New Phytol. 198, 149–155 (2013)

  18. 18.

    et al. Harmonized European long-term climate data for assessing the effect of changing temporal variability on land-atmosphere CO2 fluxes. J. Clim. 27, 4815–4834 (2014)

  19. 19.

    et al. Responses of spring phenology to climate change. New Phytol. 162, 295–309 (2004)

  20. 20.

    et al. The influence of local spring temperature variance on temperature sensitivity of spring phenology. Glob. Change Biol. 20, 1473–1480 (2014)

  21. 21.

    , & The interaction between freezing tolerance and phenology in temperate deciduous trees. Front. Plant Sci. 5, 541 (2014)

  22. 22.

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

  23. 23.

    & Photoperiod sensitivity of bud burst in 14 temperate forest tree species. Agric. For. Meteorol. 165, 73–81 (2012)

  24. 24.

    & Predicting the timing of budburst in temperate trees. J. Appl. Ecol. 29, 597–604 (1992)

  25. 25.

    , & Modeling the effects of winter environment on dormancy release of Douglas-fir. For. Ecol. Manage. 259, 798–808 (2010)

  26. 26.

    et al. Satellite radar remote sensing of seasonal growing seasons for boreal and sub-alpine evergreen forests. Remote Sens. Environ. 90, 243–258 (2004)

  27. 27.

    et al. Growing season extension and its impact on terrestrial carbon cycle in the Northern Hemisphere over the past 2 decades. Glob. Biogeochem. Cycles 21, GB3018 (2007)

  28. 28.

    , & The impact of growing-season length variability on carbon assimilation and evapotranspiration over 88 years in the eastern US deciduous forest. Int. J. Biometeorol. 42, 139–145 (1999)

  29. 29.

    & Increase of extreme events in a warming world. Proc. Natl Acad. Sci. USA 108, 17905–17909 (2011)

  30. 30.

    et al. Variation in leaf flushing date influences autumnal senescence and next year’s flushing date in two temperate tree species. Proc. Natl Acad. Sci. USA 111, 7355–7360 (2014)

  31. 31.

    The influence of cold in stimulating the growth of plants. Proc. Natl Acad. Sci. USA 6, 434–435 (1920)

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This study was supported by the National Natural Science Foundation of China (41125004 and 31321061), the 111 Project (B14001), and National Youth Top-notch Talent Support Program in China. Y.H.F. is supported by an FWO Pegasus Marie Curie Fellowship. I.A.J., P.C. and J.P. acknowledge support from the European Research Council through Synergy grant ERC-2013-SyG-610028 “IMBALANCE-P” and A.M. acknowledges support through the (FP7/2007-2013)/ERC grant 282250 “E3-Extreme Event Ecology”. I.A.J. acknowledges support from the University of Antwerp Centre of Excellence “GCE”. The authors acknowledge all members of the PEP725 project for providing the phenological data.

Author information


  1. Sino-French Institute for Earth System Science, College of Urban and Environmental Sciences, Peking University, Beijing 100871, China

    • Yongshuo H. Fu
    • , Hongfang Zhao
    • , Shilong Piao
    • , Shushi Peng
    • , Philippe Ciais
    • , Mengtian Huang
    •  & Zhenzhong Zeng
  2. Centre of Excellence PLECO (Plant and Vegetation Ecology), Department of Biology, University of Antwerp, Universiteitsplein 1, B-2610 Wilrijk, Belgium

    • Yongshuo H. Fu
    •  & Ivan A. Janssens
  3. Key Laboratory of Alpine Ecology and Biodiversity, Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing 100085, China

    • Shilong Piao
  4. Center for Excellence in Tibetan Earth Science, Chinese Academy of Sciences, Beijing 100085, China

    • Shilong Piao
  5. Laboratoire des Sciences du Climat et de l’Environnement, CEA CNRS UVSQ, Gif-sur-Yvette 91190, France

    • Marc Peaucelle
    • , Shushi Peng
    •  & Philippe Ciais
  6. School of Resources and Environment, University of Electronic Science and Technology of China, Chengdu 611731, China

    • Guiyun Zhou
  7. Ecoclimatology, Technische Universität München, Freising 85354, Germany

    • Annette Menzel
  8. Technische Universität München, Institute for Advanced Study, Lichtenbergstraße 2a, 85748 Garching, Germany

    • Annette Menzel
  9. CREAF, Cerdanyola del Vallès, Barcelona 08193, Catalonia, Spain

    • Josep Peñuelas
  10. CSIC, Global Ecology Unit CREAF-CSIC-UAB, Cerdanyola del Vallès, Barcelona 08193, Catalonia, Spain

    • Josep Peñuelas
  11. Department of Atmospheric Sciences, University of Illinois, Urbana, Illinois 61801, USA

    • Yang Song
  12. University of Neuchatel, Institute of Geography, Neuchatel 2000, Switzerland

    • Yann Vitasse
  13. WSL Swiss Federal Institute for Forest, Snow and Landscape Research, Neuchatel 2000, Switzerland

    • Yann Vitasse
  14. WSL Institute for Snow and Avalanche Research SLF, Group Mountain Ecosystems, Davos 7260, Switzerland.

    • Yann Vitasse


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Y.H.F. and H.Z. contributed equally to this work. S.Pi., Y.H.F. and I.A.J. designed the research; H.Z., Y.H.F., M.P., S.Pe. and G.Z. performed the analysis; Y.H.F., S.Pi. and I.A.J. drafted the paper; and Y.H.F., S.Pi., I.A.J., H.Z., M.P., S.Pe., G.Z., P.C., M.H., A.M., J.P., Y.S., Y.V. and Z.Z. contributed to the interpretation of the results and to the writing of the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Shilong Piao.

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