Abstract
Global warming delays the autumn date of foliar senescence (DFS) in recent decades, with positive implications for growing season length and therefore global carbon storage. However, warming-associated drought, leading to water limitation, may conversely stimulate earlier DFS. Using ground observations since 1940s and 34 years of satellite greenness data (1982‒2015) over the Northern Hemisphere (>30° N), we show the increased impact of drought on DFS. Earlier DFS is linked to decreased precipitation under warming and weaker drought resistance associated with various plant functional traits. For example, isohydric plants with strict regulation of water status may drop leaves fast during droughts. We derive an improved set of phenology models based on this influence and project earlier DFS by the end of the century, particularly at high latitudes (>50° N). Our results limit uncertainties in the later end of plant growth with warming, aiding estimation of carbon uptake of terrestrial ecosystems.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Data availability
All data used in this study are included in the article and the Supplementary Information. The specific link for each dataset can be found in Supplementary Table 1.
Code availability
All the data analyses and modelling were performed using MATLAB. The codes for Tsen calculation and the eight phenology models as well as the satellite LUD and DFS data used in our study are available at https://doi.org/10.5281/zenodo.6892387. Other codes and relevant data are available upon request to the corresponding authors.
References
Richardson, A. D. et al. Terrestrial biosphere models need better representation of vegetation phenology: results from the North American Carbon Program Site Synthesis. Glob. Change Biol. 18, 566–584 (2012).
Keenan, T. F. et al. Net carbon uptake has increased through warming-induced changes in temperate forest phenology. Nat. Clim. Change 4, 598–604 (2014).
Piao, S. L. et al. Leaf onset in the northern hemisphere triggered by daytime temperature. Nat. Commun. 6, 6911 (2015).
Penuelas, J., Rutishauser, T. & Filella, I. Phenology feedbacks on climate change. Science 324, 887–888 (2009).
Garonna, I. et al. Strong contribution of autumn phenology to changes in satellite-derived growing season length estimates across Europe (1982–2011). Glob. Change Biol. 20, 3457–3470 (2014).
Piao, S. L. et al. Net carbon dioxide losses of northern ecosystems in response to autumn warming. Nature 451, 49–52 (2008).
Zhao, Y. et al. ABA receptor PYL9 promotes drought resistance and leaf senescence. Proc. Natl Acad. Sci. USA 113, 1949–1954 (2016).
Keskitalo, J., Bergquist, G., Gardestrom, P. & Jansson, S. A cellular timetable of autumn senescence. Plant Physiol. 139, 1635–1648 (2005).
Liu, Q. et al. Delayed autumn phenology in the Northern Hemisphere is related to change in both climate and spring phenology. Glob. Change Biol. 22, 3702–3711 (2016).
Wu, C. Y. et al. Contrasting responses of autumn-leaf senescence to daytime and night-time warming. Nat. Clim. Change 8, 1092–1096 (2018).
Zani, D., Crowther, T. W., Mo, L., Renner, S. S. & Zohner, C. M. Increased growing-season productivity drives earlier autumn leaf senescence in temperate trees. Science 370, 1066–1071 (2020).
Zhang, Y., Parazoo, N. C., Williams, A. P., Zhou, S. & Gentine, P. Large and projected strengthening moisture limitation on end-of-season photosynthesis. Proc. Natl Acad. Sci. USA 117, 9216–9222 (2020).
Grossiord, C. et al. Plant responses to rising vapor pressure deficit. New Phytol. 226, 1550–1566 (2020).
Ciais, P. et al. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529–533 (2005).
Keenan, T. F. & Richardson, A. D. The timing of autumn senescence is affected by the timing of spring phenology: implications for predictive models. Glob. Change Biol. 21, 2634–2641 (2015).
Liu, L. B. et al. Soil moisture dominates dryness stress on ecosystem production globally. Nat. Commun. 11, 4892 (2020).
Delpierre, N. et al. Modelling interannual and spatial variability of leaf senescence for three deciduous tree species in France. Agric. For. Meteorol. 149, 938–948 (2009).
Piao, S. L. et al. Weakening temperature control on the interannual variations of spring carbon uptake across northern lands. Nat. Clim. Change 7, 359–363 (2017).
Fu, Y. S. H. et al. Declining global warming effects on the phenology of spring leaf unfolding. Nature 526, 104–107 (2015).
Seastedt, T. R. & Knapp, A. K. Consequences of nonequilibrium resource availability across multiple time scales: the transient maxima hypothesis. Am. Nat. 141, 621–633 (1993).
Korner, C. Paradigm shift in plant growth control. Curr. Opin. Plant Biol. 25, 107–114 (2015).
Huxman, T. E. et al. Convergence across biomes to a common rain-use efficiency. Nature 429, 651–654 (2004).
McDowell, N. et al. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought. New Phytol. 178, 719–739 (2008).
Nolan, R. H. et al. Differences in osmotic adjustment, foliar abscisic acid dynamics, and stomatal regulation between an isohydric and anisohydric woody angiosperm during drought. Plant Cell Environ. 40, 3122–3134 (2017).
Fan, Y., Miguez-Macho, G., Jobbágy, E. G., Jackson, R. B. & Otero-Casal, C. Hydrologic regulation of plant rooting depth. Proc. Natl Acad. Sci. USA 114, 10572–10577 (2017).
Choat, B. et al. Triggers of tree mortality under drought. Nature 558, 531–539 (2018).
Giardina, F. et al. Tall Amazonian forests are less sensitive to precipitation variability. Nat. Geosci. 11, 405–409 (2018).
Kannenberg, S. A., Driscoll, A. W., Szejner, P., Anderegg, W. R. L. & Ehleringer, J. R. Rapid increases in shrubland and forest intrinsic water-use efficiency during an ongoing megadrought. Proc. Natl Acad. Sci. USA https://doi.org/10.1073/pnas.2118052118 (2021).
Liu, Q. et al. Extension of the growing season increases vegetation exposure to frost. Nat. Commun. https://doi.org/10.1038/s41467-017-02690-y (2018).
Schuur, E. A. G. et al. Climate change and the permafrost carbon feedback. Nature 520, 171–179 (2015).
Samaniego, L. et al. Anthropogenic warming exacerbates European soil moisture droughts. Nat. Clim. Change 8, 421–426 (2018).
Templ, B. et al. Pan European Phenological database (PEP725): a single point of access for European data. Int. J. Biometeorol. 62, 1109–1113 (2018).
Shen, M. et al. Increasing altitudinal gradient of spring vegetation phenology during the last decade on the Qinghai-Tibetan Plateau. Agric. For. Meteorol. 189, 71–80 (2014).
Zhang, X. Y. Reconstruction of a complete global time series of daily vegetation index trajectory from long-term AVHRR data. Remote Sens. Environ. 156, 457–472 (2015).
Chen, J. et al. A simple method for reconstructing a high-quality NDVI time-series data set based on the Savitzky–Golay filter. Remote Sens. Environ. 91, 332–344 (2004).
White, M. A. et al. Intercomparison, interpretation, and assessment of spring phenology in North America estimated from remote sensing for 1982–2006. Glob. Change Biol. 15, 2335–2359 (2009).
Zhang, X. et al. Monitoring vegetation phenology using MODIS. Remote Sens. Environ. 84, 471–475 (2003).
Gonsamo, A., Chen, J. M., Price, D. T., Kurz, W. A. & Wu, C. Y. Land surface phenology from optical satellite measurement and CO2 eddy covariance technique. J. Geophys. Res. 117, G03032 (2012).
Muñoz, S. ERA5-Land Monthly Averaged Data from 1981 to Present (C3S CDS, date accessed:10-8-2021); https://doi.org/10.24381/cds.68d2bb30
Abatzoglou, J. T., Dobrowski, S. Z., Parks, S. A. & Hegewisch, K. C. TerraClimate, a high-resolution global dataset of monthly climate and climatic water balance from 1958–2015. Sci. Data 5, 170191 (2018).
Müller, W. A. et al. A Higher-resolution version of the Max Planck Institute Earth System Model (MPI-ESM1.2-HR). J. Adv. Model. Earth Syst. 10, 1383–1413 (2018).
Vicente-Serrano, S. M. et al. Response of vegetation to drought time-scales across global land biomes. Proc. Natl Acad. Sci. USA 110, 52–57 (2013).
Allen, R. G., Smith, M., Pereira, L. S. & Perrier, A. An update for the calculation of reference evapotranspiration. ICID Bull. 43, 64–92 (1994).
Gampe, D. et al. Increasing impact of warm droughts on northern ecosystem productivity over recent decades. Nat. Clim. Change https://doi.org/10.1038/s41558-021-01112-8 (2021).
Sheffield, J., Wood, E. F. & Roderick, M. L. Little change in global drought over the past 60 years. Nature 491, 435–438 (2012).
Peng, J., Wu, C. Y., Zhang, X. Y., Wang, X. Y. & Gonsamo, A. Satellite detection of cumulative and lagged effects of drought on autumn leaf senescence over the Northern Hemisphere. Glob. Change Biol. 25, 2174–2188 (2019).
Harris, I., Jones, P. D., Osborn, T. J. & Lister, D. H. Updated high-resolution grids of monthly climatic observations—the CRU TS3.10 Dataset. Int. J. Climatol. 34, 623–642 (2014).
Beaudoing, H., Rodell, M. & NASA/GSFC/HSL. GLDAS Noah Land Surface Model L4 3 Hourly 0.25 × 0.25 Degree Version 2.0 (GES DISC, 2015); https://doi.org/10.5067/342OHQM9AK6Q
Beaudoing, H., Rodell, M. & NASA/GSFC/HSL. GLDAS Noah Land Surface Model L4 3 Hourly 0.25 ×0.25 Degree Version 2.1 (GES DISC, 2016); https://doi.org/10.5067/E7TYRXPJKWOQ
Zheng, Y. et al. Improved estimate of global gross primary production for reproducing its long-term variation, 1982–2017. Earth Syst. Sci. Data 12, 2725–2746 (2020).
Zhang, K. et al. Vegetation greening and climate change promote multidecadal rises of global land evapotranspiration. Sci. Rep. https://doi.org/10.1038/srep15956 (2015).
Li, Y. et al. Estimating global ecosystem isohydry/anisohydry using active and passive microwave satellite data. J. Geophys. Res. 122, 3306–3321 (2017).
Moesinger, L. et al. The global long-term microwave Vegetation Optical Depth Climate Archive (VODCA). Earth Syst. Sci. Data 12, 177–196 (2020).
Gupta, H. V., Kling, H., Yilmaz, K. K. & Martinez, G. F. Decomposition of the mean squared error and NSE performance criteria: implications for improving hydrological modelling. J. Hydrol. 377, 80–91 (2009).
Botta, A., Viovy, N., Ciais, P., Friedlingstein, P. & Monfray, P. A global prognostic scheme of leaf onset using satellite data. Glob. Change Biol. 6, 709–725 (2000).
Acknowledgements
This work was funded by the Strategic Priority Research Programme of the Chinese Academy of Sciences (XDA19040103), the National Natural Science Foundation of China (42125101) and the CAS Interdisciplinary Innovation Team (JCTD-2020-05). J.P. and P.C. were funded by European Research Council Synergy grant ERC-SyG-2013-610028 IMBALANCE-P. J.P. was also financially supported by the Fundación Ramon Areces grant ELEMENTAL-CLIMATE, the Spanish Government grant PID2019-110521GB-I00 and the Catalan Government grant SGR 2017-1005.
Author information
Authors and Affiliations
Contributions
C.W., J.P. and Q.G. designed the research. C.W. and J.P. wrote the first draft of the manuscript. J.P. performed data analyses and remote-sensing model simulations. X.W. and H.H. contributed to model simulation. P.C., J.P. and S.B. substantially revised the manuscript with intensive suggestions. H.W., A.B., R.J., X.Z., W.Y., E.L., R.L., W.J. and Y.F. contributed to the writing of the manuscript.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing interests.
Peer review
Peer review information
Nature Climate Change thanks Ainong Li, Constantin Zohner and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Supplementary Information
Supplementary Figs. 1–14 and Tables 1 and 2.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Wu, C., Peng, J., Ciais, P. et al. Increased drought effects on the phenology of autumn leaf senescence. Nat. Clim. Chang. 12, 943–949 (2022). https://doi.org/10.1038/s41558-022-01464-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41558-022-01464-9
This article is cited by
-
Higher vegetation sensitivity to meteorological drought in autumn than spring across European biomes
Communications Earth & Environment (2023)
-
Autumn canopy senescence has slowed down with global warming since the 1980s in the Northern Hemisphere
Communications Earth & Environment (2023)
-
Widespread and complex drought effects on vegetation physiology inferred from space
Nature Communications (2023)
-
Response of water-use efficiency to phenology in the natural forest and grassland of the Loess Plateau in China
Science China Earth Sciences (2023)
-
The effects of climate change on the timing of peak fall foliage in Acadia National Park
Landscape Ecology (2023)