Declining global warming effects on the phenology of spring leaf unfolding

Journal name:
Nature
Volume:
526,
Pages:
104–107
Date published:
DOI:
doi:10.1038/nature15402
Received
Accepted
Published online

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.

At a glance

Figures

  1. Changes of apparent temperature sensitivity of leaf unfolding (ST) over time.
    Figure 1: Changes of apparent temperature sensitivity of leaf unfolding (ST) over time.

    a, Species-specific ST and s.d. (in brackets) across all sites in three periods and its difference between 1999–2013 and 1980–1994. The ST was determined using the preseason fixed at the time period 1980–2013 and using ordinary least squares linear regression. The colour scale indicates the magnitude of ST. AG, alder (Alnus glutinosa); BP, silver birch (Betula pendula); AH, horse chestnut (Aesculus hippocastanum); FS, beech (Fagus sylvatica); TC, lime (Tilia cordata); QR, oak (Quercus robur); FE, ash (Fraxinus excelsior). The number of sites for each species are in brackets below the species name. b, The distribution of ST across all species and sites in two different periods and the mean ST and s.d. (in brackets). The asterisk indicates a significant difference of ST between the two periods at P < 0.05. c, Temporal change of ST for individual species and for combined totals for all species across all sites with a 15-year moving window from 1980 to 2013. The black line indicates the average across all species, and the grey area indicates one s.d. either side of the mean. The dotted line indicates the linear regression.

  2. Changes of chilling and spring temperature variation between 1980-1994 and 1999-2013.
    Figure 2: Changes of chilling and spring temperature variation between 1980–1994 and 1999–2013.

    a, b, Species-specific Tstd (the standard deviation of mean spring temperature) (a) and chilling accumulation (b) across all sites over two periods, 1980–1994 and 1999–2013. The Tstd was calculated as the s.d. of mean spring temperature during the preseason over these two periods. The preseason was defined as the period before leaf unfolding for which the correlation coefficient between leaf unfolding and temperature was highest. The chilling accumulation was calculated as chilling days when daily temperature was between 0 °C and 5 °C from 1 November to the average date of leaf unfolding. The asterisks indicate significant differences at P < 0.05.

  3. Changes of modelled apparent temperature sensitivity of leaf unfolding.
    Figure 3: Changes of modelled apparent temperature sensitivity of leaf unfolding.

    ac, As in Fig. 1a, the panels show the modelled species-specific ST, including the s.d. (in brackets), across all sites during three periods and its difference between 1999–2013 and 1980–1994 for the sequential model (a), parallel model (b) and unified model (c). df, As in Fig. 1c, the panels show the modelled temporal change of ST for individual species and for combined totals for all species across all sites with a 15-year moving window from 1980 to 2013 for the sequential model (d), parallel model (e) and unified model (f). g, The model performance. The ST was determined using the preseason fixed at the time period 1980–2013 and using ordinary least squares linear regression. The colour scale indicates the magnitude of ST. r.m.s.e., root mean square error; AG, alder (Alnus glutinosa); BP, silver birch (Betula pendula); AH, horse chestnut (Aesculus hippocastanum); FS, beech (Fagus sylvatica); TC, lime (Tilia cordata); QR, oak (Quercus robur); FE, ash (Fraxinus excelsior). The number of sites for each species are in brackets under the species name.

  4. The distribution of the sites.
    Extended Data Fig. 1: The distribution of the sites.

    The data were obtained from the Pan European Phenology network (http://www.pep725.eu/).

  5. The distribution of preseason length for individual species and for combined totals for all species.
    Extended Data Fig. 2: The distribution of preseason length for individual species and for combined totals for all species.

    The optimal preseason was defined as the period before leaf unfolding for which the correlation coefficient between leaf unfolding and temperature was highest. The numbers in the brackets are the mean dates of leaf unfolding across all sites.

  6. Changes of apparent temperature sensitivity of leaf unfolding between 1980-1994 and 1999-2013.
    Extended Data Fig. 3: Changes of apparent temperature sensitivity of leaf unfolding between 1980–1994 and 1999–2013.

    ac, Same as Fig. 1, but the ST was calculated based on the preseason that was determined either in the time period 1980–1994 (b) or in 1999–2013 (c). The differences in preseason lengths are provided for individual species and for combined totals for all species (a), and the figures above bars are the mean absolute preseason difference between two periods. For b and c, species-specific ST and its s.d. (in brackets) across all sites in three periods and its difference between 1999–2013 and 1980–1994. The colour scale indicates the magnitude of ST. The number of sites for each species are in brackets under the species name. d, e, The distribution of the proportion and corresponding days (e) of the encroachment of phenology dates into the preseason temperature that the preseason was determined on the period 1980–2013. The proportion was defined as the difference of the mean leaf unfolding dates (diff MSOS) between the period 1999–2013 and 1980–2013 (which is the end date of the preseason temperature that was used to calculate the ST) divided by the preseason length in days. The mean values and s.d. (in brackets) are provided for individual species and for combined totals for all species.

  7. The distribution of partial correlation coefficients between preseason temperature and leaf unfolding dates over the time period 1980-2013.
    Extended Data Fig. 4: The distribution of partial correlation coefficients between preseason temperature and leaf unfolding dates over the time period 1980–2013.

    The mean (and s.d.) of the correlation coefficients across all species and sites are provided. The percentages of negative correlations and statistically significant negative correlations (Neg(Sig)) are also provided.

  8. Changes of apparent temperature sensitivity of leaf unfolding determined by different methods.
    Extended Data Fig. 5: Changes of apparent temperature sensitivity of leaf unfolding determined by different methods.

    ac, The ST were analysed in two 10-year periods (a), were calculated using the reduced major axis (RMA) regression (b), or were calculated based on another climate forcing data set (CRU-NCEP v5, c). Species-specific ST and s.d. (in brackets) across all sites in three periods and the difference between the two study periods are provided. The colour scale indicates the magnitude of ST. The number under the species name is the number of sites. The histograms show the distribution of ST across all species and sites in two different periods and the mean ST and s.d. (in brackets). The asterisk indicates a significant difference of ST between the two periods at P < 0.05.

  9. Changes of apparent temperature sensitivity of leaf unfolding over time.
    Extended Data Fig. 6: Changes of apparent temperature sensitivity of leaf unfolding over time.

    Same as Fig. 1c, but temporal change of ST with 10-year moving windows from 1980 to 2013. The ST was calculated using simple linear regression. The black line indicates the average across all species, and the grey area indicates one s.d. either side of the mean. The dotted line indicates the linear regression.

  10. The differences in climatology over the preseason.
    Extended Data Fig. 7: The differences in climatology over the preseason.

    The fluctuations in mean daily temperature (left) and diurnal variation temperature (TmaxTmin, right) over the preseason across all sites during the time period 1980–1994 and 1999–2013 in three MAT groups, that is, (top panels) 6–8 °C, (middle panels) 8–10 °C and (bottom panels) 10–12 °C. The preseason was determined over the period 1980–2013.

  11. Spatial difference in apparent temperature sensitivity of leaf unfolding reduction.
    Extended Data Fig. 8: Spatial difference in apparent temperature sensitivity of leaf unfolding reduction.

    The difference of ST for each species and across all species studied between two time periods, 1999–2014 and 1980–1994, at different latitudes (bin: 0.5 °) and chilling conditions (bin: two chilling days). The colour scales indicate the differences of ST between the two periods.

  12. Changes in chilling accumulation and modelled correlation between chilling and apparent temperature sensitivity of leaf unfolding.
    Extended Data Fig. 9: Changes in chilling accumulation and modelled correlation between chilling and apparent temperature sensitivity of leaf unfolding.

    a, Chilling accumulation for individual species and for combined totals for all species with 15-year moving windows from 1980 to 2013. The chilling accumulation was calculated as chilling days when daily temperature was between 0 °C and 5 °C from 1 November to the average date of leaf unfolding. The black line indicates the average across all species, and the grey area indicates one s.d. either side of the mean. The dotted line indicates the linear regression. b, Same as Fig. 2b, but chilling accumulation was calculated as chilling days when daily temperature was below 5 °C from 1 November to the average date of leaf unfolding. The asterisks indicate significant differences at P < 0.05. c, The modelled (unified model) ST under different artificial winter warming conditions. The temperature in winter, defined as the period from the 1 November to 31 January, was warmed by +1 °C to +5 °C over the period 1980–2013. The points with most chilling days indicate the real winter temperatures, and each of the other points indicate one winter warming treatment. The lines indicate simple linear regressions.

  13. Changes in apparent temperature sensitivity of leaf unfolding between years with more or less chilling.
    Extended Data Fig. 10: Changes in apparent temperature sensitivity of leaf unfolding between years with more or less chilling.

    a, b, ST for years with less chilling (a) and more chilling (b) with a 20-year moving window for 1980–2013. For each 20-year series, we divided the 20 years into two groups based on the mean chilling accumulation (chilling was accumulated when daily temperature within the temperature range between 0 °C and 5 °C from 1 November to the day of leaf unfolding). The 10 years with chilling higher than the overall mean were defined as more chilling, and the other 10 years were defined as less chilling. The black lines indicate the average across all species, and the grey area indicates one s.d. either side of the mean. The dotted lines are the linear regressions. c, Chilling accumulation for years with less chilling (red line) and more chilling (blue line) with a 20-year moving window for 1980–2013. d, The mean radiation sum over the preseason for years with less chilling (red line) and more chilling (blue line) with a 20-year moving window for 1980–2013. The preseason was determined over the period 1980–2013.

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Author information

Affiliations

  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

Contributions

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 financial interests

The authors declare no competing financial interests.

Corresponding author

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Extended data figures and tables

Extended Data Figures

  1. Extended Data Figure 1: The distribution of the sites. (144 KB)

    The data were obtained from the Pan European Phenology network (http://www.pep725.eu/).

  2. Extended Data Figure 2: The distribution of preseason length for individual species and for combined totals for all species. (106 KB)

    The optimal preseason was defined as the period before leaf unfolding for which the correlation coefficient between leaf unfolding and temperature was highest. The numbers in the brackets are the mean dates of leaf unfolding across all sites.

  3. Extended Data Figure 3: Changes of apparent temperature sensitivity of leaf unfolding between 1980–1994 and 1999–2013. (673 KB)

    ac, Same as Fig. 1, but the ST was calculated based on the preseason that was determined either in the time period 1980–1994 (b) or in 1999–2013 (c). The differences in preseason lengths are provided for individual species and for combined totals for all species (a), and the figures above bars are the mean absolute preseason difference between two periods. For b and c, species-specific ST and its s.d. (in brackets) across all sites in three periods and its difference between 1999–2013 and 1980–1994. The colour scale indicates the magnitude of ST. The number of sites for each species are in brackets under the species name. d, e, The distribution of the proportion and corresponding days (e) of the encroachment of phenology dates into the preseason temperature that the preseason was determined on the period 1980–2013. The proportion was defined as the difference of the mean leaf unfolding dates (diff MSOS) between the period 1999–2013 and 1980–2013 (which is the end date of the preseason temperature that was used to calculate the ST) divided by the preseason length in days. The mean values and s.d. (in brackets) are provided for individual species and for combined totals for all species.

  4. Extended Data Figure 4: The distribution of partial correlation coefficients between preseason temperature and leaf unfolding dates over the time period 1980–2013. (58 KB)

    The mean (and s.d.) of the correlation coefficients across all species and sites are provided. The percentages of negative correlations and statistically significant negative correlations (Neg(Sig)) are also provided.

  5. Extended Data Figure 5: Changes of apparent temperature sensitivity of leaf unfolding determined by different methods. (645 KB)

    ac, The ST were analysed in two 10-year periods (a), were calculated using the reduced major axis (RMA) regression (b), or were calculated based on another climate forcing data set (CRU-NCEP v5, c). Species-specific ST and s.d. (in brackets) across all sites in three periods and the difference between the two study periods are provided. The colour scale indicates the magnitude of ST. The number under the species name is the number of sites. The histograms show the distribution of ST across all species and sites in two different periods and the mean ST and s.d. (in brackets). The asterisk indicates a significant difference of ST between the two periods at P < 0.05.

  6. Extended Data Figure 6: Changes of apparent temperature sensitivity of leaf unfolding over time. (322 KB)

    Same as Fig. 1c, but temporal change of ST with 10-year moving windows from 1980 to 2013. The ST was calculated using simple linear regression. The black line indicates the average across all species, and the grey area indicates one s.d. either side of the mean. The dotted line indicates the linear regression.

  7. Extended Data Figure 7: The differences in climatology over the preseason. (384 KB)

    The fluctuations in mean daily temperature (left) and diurnal variation temperature (TmaxTmin, right) over the preseason across all sites during the time period 1980–1994 and 1999–2013 in three MAT groups, that is, (top panels) 6–8 °C, (middle panels) 8–10 °C and (bottom panels) 10–12 °C. The preseason was determined over the period 1980–2013.

  8. Extended Data Figure 8: Spatial difference in apparent temperature sensitivity of leaf unfolding reduction. (413 KB)

    The difference of ST for each species and across all species studied between two time periods, 1999–2014 and 1980–1994, at different latitudes (bin: 0.5 °) and chilling conditions (bin: two chilling days). The colour scales indicate the differences of ST between the two periods.

  9. Extended Data Figure 9: Changes in chilling accumulation and modelled correlation between chilling and apparent temperature sensitivity of leaf unfolding. (220 KB)

    a, Chilling accumulation for individual species and for combined totals for all species with 15-year moving windows from 1980 to 2013. The chilling accumulation was calculated as chilling days when daily temperature was between 0 °C and 5 °C from 1 November to the average date of leaf unfolding. The black line indicates the average across all species, and the grey area indicates one s.d. either side of the mean. The dotted line indicates the linear regression. b, Same as Fig. 2b, but chilling accumulation was calculated as chilling days when daily temperature was below 5 °C from 1 November to the average date of leaf unfolding. The asterisks indicate significant differences at P < 0.05. c, The modelled (unified model) ST under different artificial winter warming conditions. The temperature in winter, defined as the period from the 1 November to 31 January, was warmed by +1 °C to +5 °C over the period 1980–2013. The points with most chilling days indicate the real winter temperatures, and each of the other points indicate one winter warming treatment. The lines indicate simple linear regressions.

  10. Extended Data Figure 10: Changes in apparent temperature sensitivity of leaf unfolding between years with more or less chilling. (314 KB)

    a, b, ST for years with less chilling (a) and more chilling (b) with a 20-year moving window for 1980–2013. For each 20-year series, we divided the 20 years into two groups based on the mean chilling accumulation (chilling was accumulated when daily temperature within the temperature range between 0 °C and 5 °C from 1 November to the day of leaf unfolding). The 10 years with chilling higher than the overall mean were defined as more chilling, and the other 10 years were defined as less chilling. The black lines indicate the average across all species, and the grey area indicates one s.d. either side of the mean. The dotted lines are the linear regressions. c, Chilling accumulation for years with less chilling (red line) and more chilling (blue line) with a 20-year moving window for 1980–2013. d, The mean radiation sum over the preseason for years with less chilling (red line) and more chilling (blue line) with a 20-year moving window for 1980–2013. The preseason was determined over the period 1980–2013.

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