in

Acquisitive plants exhibit stronger phenological shifts in response to warming: insights from meta-analysis and long-term monitoring


Abstract

As climate warming accelerates, shifts in plant phenology are reshaping the functioning and stability of terrestrial ecosystems. While the roles of climatic drivers in shaping phenological responses to warming are well established, the influence of intrinsic plant functional traits remains poorly understood. Here, we combine two complementary approaches through a meta-analysis of 124 field warming experiments and an analysis of long-term phenological monitoring networks (CPON and USA‑NPN) to evaluate phenological responses to warming across a spectrum of resource-use strategies in seasonally cold biomes. Our meta-analysis demonstrates that resource-acquisitive plants, characterized by higher nutrient concentrations and thinner leaves, show significantly stronger phenological responses to experimental warming. This pattern is observed consistently across both leaf-out in spring and senescence in autumn. These results from meta-analysis are further supported by two long-term observational datasets, which also show more pronounced phenological shifts in acquisitive species under long-term warming. Our findings present a trait-climate integration framework that extends beyond conventional environmental drivers, providing a mechanistic foundation to enhance the accuracy of forecasts for plant responses to climate change.

Data availability

The data generated in this study have been deposited in Figshare at https://doi.org/10.6084/m9.figshare.29917052. Plant traits data were obtained from TRY Plant Trait Database (https://www.try-db.org/), climate data from WorldClim (https://www.worldclim.org/) and Climate Research Unit (https://crudata.uea.ac.uk/cru/data/hrg/cru_ts_4.08/). The long-term ground phenological data of USA National Phenology Network (USA-NPN) are available from the website: https://www.usanpn.org/ results/data. The phenological data from China Phenological Observation Network (CPON) were provided by the Meteorological Information Center of the China Meteorological Administration. Source data are provided with this paper.

Code availability

Codes for analysis are available in the Figshare repository (https://doi.org/10.6084/m9.figshare.29917052).

References

  1. Piao, S. et al. Net carbon dioxide losses of northern ecosystems in response to autumn warming. Nature 451, 49–52 (2008).

    Google Scholar 

  2. Manlick, P. J., Perryman, N. L., Koltz, A. M., Cook, J. A. & Newsome, S. D. Climate warming restructures food webs and carbon flow in high-latitude ecosystems. Nat. Clim. Chang. 14, 184–189 (2024).

    Google Scholar 

  3. Xi, Y., Zhang, W., Wei, F., Fang, Z. & Fensholt, R. Boreal tree species diversity increases with global warming but is reversed by extremes. Nat. Plants 10, 1473–1483 (2024).

    Google Scholar 

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

    Google Scholar 

  5. Oleksyn, J. et al. A fingerprint of climate change across pine forests of Sweden. Ecol. Lett. 23, 1739–1746 (2020).

    Google Scholar 

  6. Reich, P. B., Rich, R. L., Lu, X., Wang, Y.-P. & Oleksyn, J. Biogeographic variation in evergreen conifer needle longevity and impacts on boreal forest carbon cycle projections. Proc. Natl. Acad. Sci. USA 111, 13703–13708 (2014).

    Google Scholar 

  7. Elmore, A. J., Nelson, D. M. & Craine, J. M. Earlier springs are causing reduced nitrogen availability in North American eastern deciduous forests. Nat. Plants 2, 16133 (2016).

    Google Scholar 

  8. Chuine, I. Why does phenology drive species distribution?. Philos. Trans. R. Soc. B: Biol. Sci. 365, 3149–3160 (2010).

    Google Scholar 

  9. Fridley, J. D. Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485, 359–362 (2012).

    Google Scholar 

  10. Yang, X. et al. Plant phenology response to nitrogen addition decreases community biomass stability in an alpine meadow. New Phytol. nph.70132, (2025).

  11. Shen, M. et al. Plant phenology changes and drivers on the Qinghai–Tibetan Plateau. Nat. Rev. Earth Environ. 3, 633–651 (2022).

    Google Scholar 

  12. Fu, Y. H. et al. Declining global warming effects on the phenology of spring leaf unfolding. Nature 526, 104–107 (2015).

    Google Scholar 

  13. Möhl, P., Von Büren, R. S. & Hiltbrunner, E. Growth of alpine grassland will start and stop earlier under climate warming. Nat. Commun. 13, 7398 (2022).

    Google Scholar 

  14. Meng, L. et al. Photoperiod decelerates the advance of spring phenology of six deciduous tree species under climate warming. Glob. Chang. Biol. 27, 2914–2927 (2021).

    Google Scholar 

  15. Wang, H. et al. Divergent phenological responses of soil microorganisms and plants to climate warming. Nat. Geosci. 18, 753–760 (2025).

    Google Scholar 

  16. Peaucelle, M., Peñuelas, J. & Verbeeck, H. Accurate phenology analyses require bud traits and energy budgets. Nat. Plants 8, 915–922 (2022).

    Google Scholar 

  17. Montgomery, R. A., Rice, K. E., Stefanski, A., Rich, R. L. & Reich, P. B. Phenological responses of temperate and boreal trees to warming depend on ambient spring temperatures, leaf habit, and geographic range. Proc. Natl. Acad. Sci. USA 117, 10397–10405 (2020).

    Google Scholar 

  18. Shen, P. et al. Biodiversity buffers the response of spring leaf unfolding to climate warming. Nat. Clim. Chang. 14, 863–868 (2024).

    Google Scholar 

  19. Rauschkolb, R. et al. Spatial variability in herbaceous plant phenology is mostly explained by variability in temperature but also by photoperiod and functional traits. Int J Biometeorol 68, 761–775 (2024).

    Google Scholar 

  20. Joswig, J. S. et al. Climatic and soil factors explain the two-dimensional spectrum of global plant trait variation. Nat. Ecol. Evol. 6, 36–50 (2022).

    Google Scholar 

  21. Reich, P. B., Walters, M. B. & Ellsworth, D. S. From tropics to tundra: global convergence in plant functioning. Proc. Natl. Acad. Sci. USA 94, 13730–13734 (1997).

    Google Scholar 

  22. Wright, I. J. et al. The worldwide leaf economics spectrum. Nature 428, 821–827 (2004).

    Google Scholar 

  23. Quan, Q. et al. Plant height as an indicator for alpine carbon sequestration and ecosystem response to warming. Nat. Plants 10, 890–900 (2024).

    Google Scholar 

  24. Augusto, L. et al. Widespread slow growth of acquisitive tree species. Nature 640, 395–401 (2025).

    Google Scholar 

  25. Yan, P. et al. Plant acquisitive strategies promote resistance and temporal stability of semiarid grasslands. Ecol. Lett. 28, e70110 (2025).

    Google Scholar 

  26. Dorji, T. et al. Plant functional traits mediate reproductive phenology and success in response to experimental warming and snow addition in Tibet. Glob. Chang. Biol. 19, 459–472 (2013).

    Google Scholar 

  27. Bucher, S. F. & Römermann, C. The timing of leaf senescence relates to flowering phenology and functional traits in 17 herbaceous species along elevational gradients. J. Ecol. 109, 1537–1548 (2021).

    Google Scholar 

  28. Chuine, I. A unified model for budburst of trees. J. Theor. Biol. 207, 337–347 (2000).

    Google Scholar 

  29. Herms, D. A. & Mattson, W. J. The dilemma of plants: to grow or defend. Q. Rev. Biol. 67, 283–335 (1992).

    Google Scholar 

  30. de Bello, F. et al. Functional trait effects on ecosystem stability: assembling the jigsaw puzzle. Trends Ecol. Evol. 36, 822–836 (2021).

    Google Scholar 

  31. Ma, Q., Huang, J.-G., Hänninen, H. & Berninger, F. Divergent trends in the risk of spring frost damage to trees in Europe with recent warming. Glob. Chang. Biol. 25, 351–360 (2019).

    Google Scholar 

  32. Guo, Y. et al. Leaf senescence: progression, regulation, and application. Mol. Hortic. 1, 1–25 (2021).

    Google Scholar 

  33. Liu, Q. et al. Extension of the growing season increases vegetation exposure to frost. Nat. Commun. 9, 426 (2018).

    Google Scholar 

  34. Richardson, A. D. et al. Ecosystem warming extends vegetation activity but heightens vulnerability to cold temperatures. Nature 560, 368–371 (2018).

    Google Scholar 

  35. Alexander, J. M. & Levine, J. M. Earlier phenology of a nonnative plant increases impacts on native competitors. Proc. Natl. Acad. Sci. USA 116, 6199–6204 (2019).

    Google Scholar 

  36. Craven, D. et al. Multiple facets of biodiversity drive the diversity–stability relationship. Nat. Ecol. Evol. 2, 1579–1587 (2018).

    Google Scholar 

  37. Májeková, M., de Bello, F., Doležal, J. & Lepš, J. Plant functional traits as determinants of population stability. Ecology 95, 2369–2374 (2014).

    Google Scholar 

  38. Zhang, X. et al. Resource-acquisitive species have greater plasticity in leaf functional traits than resource-conservative species in response to nitrogen addition in subtropical China. Sci. Total Environ. 903, 166177 (2023).

    Google Scholar 

  39. Li, H.-L. et al. China’s subtropical deciduous plants are more sensitive to climate change than evergreen plants by flowering phenology. Glob. Chang. Biol. 30, e17168 (2024).

    Google Scholar 

  40. Polley, H. W., Isbell, F. I. & Wilsey, B. J. Plant functional traits improve diversity-based predictions of temporal stability of grassland productivity. Oikos 122, 1275–1282 (2013).

    Google Scholar 

  41. Zohner, C. M. et al. Effect of climate warming on the timing of autumn leaf senescence reverses after the summer solstice. Science 381, eadf5098 (2023).

    Google Scholar 

  42. Bigler, C. & Vitasse, Y. Premature leaf discoloration of European deciduous trees is caused by drought and heat in late spring and cold spells in early fall. Agric. For. Meteorol. 307, 108492 (2021).

    Google Scholar 

  43. Vitasse, Y. et al. Impact of microclimatic conditions and resource availability on spring and autumn phenology of temperate tree seedlings. New Phytol 232, 537–550 (2021).

    Google Scholar 

  44. Wu, X. et al. Canopy structure regulates autumn phenology by mediating the microclimate in temperate forests. Nat. Clim. Chang. 14, 1299–1305 (2024).

    Google Scholar 

  45. Bai, Y. et al. Heating up the roof of the world: tracing the impacts of in-situ warming on carbon cycle in alpine grasslands on the Tibetan Plateau. Natl. Sci. Rev. 12, nwae371 (2024).

    Google Scholar 

  46. 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).

    Google Scholar 

  47. Wang, H. et al. Alpine grassland plants grow earlier and faster but biomass remains unchanged over 35 years of climate change. Ecol. Lett. 23, 701–710 (2020).

    Google Scholar 

  48. Umaña, M. N. et al. Upscaling the effect of traits in response to drought: the relative importance of safety–efficiency and acquisitive–conservation functional axes. Ecol. Lett. 26, 2098–2109 (2023).

    Google Scholar 

  49. Zhang, W. et al. Seasonal stabilization effects slowed the greening of the Northern Hemisphere over the last two decades. Nat Commun 16, 6287 (2025).

    Google Scholar 

  50. Richardson, A. D. et al. Influence of spring and autumn phenological transitions on forest ecosystem productivity. Philos. Trans. R. Soc. B: Biol. Sci. 365, 3227–3246 (2010).

    Google Scholar 

  51. Gallinat, A. S., Primack, R. B. & Wagner, D. L. Autumn, the neglected season in climate change research. Trends Ecol. Evol. 30, 169–176 (2015).

    Google Scholar 

  52. Lubbe, F. C., Klimešová, J. & Henry, H. A. L. Winter belowground: changing winters and the perennating organs of herbaceous plants. Funct. Ecol. 35, 1627–1639 (2021).

    Google Scholar 

  53. Xu, H. et al. Convergent strategies for leaf traits in tree species from divergent habitats. Glob. Chang. Biol. 31, e70108 (2025).

    Google Scholar 

  54. Harris, T. et al. Capital and income breeders among herbs: how relative biomass allocation into a storage organ relates to clonal traits, phenology and environmental gradients. New Phytol 245, 154–168 (2025).

    Google Scholar 

  55. Jiang, B. et al. Complex interactions of ‘water-light-heat’ climatic conditions on spring phenology in the mid-high latitudes of the Northern Hemisphere. Agric. For. Meteorol. 367, 110520 (2025).

    Google Scholar 

  56. Peaucelle, M. et al. Spatial variance of spring phenology in temperate deciduous forests is constrained by background climatic conditions. Nat Commun 10, 5388 (2019).

    Google Scholar 

  57. 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).

    Google Scholar 

  58. Hänninen, H. et al. Experiments are necessary in process-based tree phenology modelling. Trends Plant Sci 24, 199–209 (2019).

    Google Scholar 

  59. Gu, H. et al. Warming-induced increase in carbon uptake is linked to earlier spring phenology in temperate and boreal forests. Nat. Commun. 13, 3698 (2022).

    Google Scholar 

  60. Li, D., Belitz, M., Campbell, L. & Guralnick, R. Extreme weather events have strong but different impacts on plant and insect phenology. Nat. Clim. Chang. 15, 321–328 (2025).

    Google Scholar 

  61. Ge, Q., Wang, H., Rutishauser, T. & Dai, J. Phenological response to climate change in China: a meta-analysis. Glob. Chang. Biol. 21, 265–274 (2015).

    Google Scholar 

  62. USA National Phenology Network. Plant individual phenometrics data, 2009–2024. USA-NPN https://doi.org/10.5066/F78S4N1V (2024).

  63. Leys, C., Ley, C., Klein, O., Bernard, P. & Licata, L. Detecting outliers: do not use standard deviation around the mean, use absolute deviation around the median. J. Exp. Soc. Psychol. 49, 764–766 (2013).

    Google Scholar 

  64. Kattge, J. et al. TRY – a global database of plant traits. Glob. Chang. Biol. 17, 2905–2935 (2011).

    Google Scholar 

  65. Kembel, S. W. et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464 (2010).

    Google Scholar 

  66. Lu, C. et al. Diminishing warming effects on plant phenology over time. New Phytol 245, 523–533 (2025).

    Google Scholar 

  67. Adams, D. C., Gurevitch, J. & Rosenberg, M. S. Resampling tests for meta-analysis of ecological data. Ecology 78, 1277–1283 (1997).

    Google Scholar 

  68. Viechtbauer, W. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36, 1–48 (2010).

    Google Scholar 

  69. Jin, Y. & Qian, H. V. PhyloMaker: an R package that can generate very large phylogenies for vascular plants. Ecography 42, 1353–1359 (2019).

    Google Scholar 

  70. Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

    Google Scholar 

  71. Blomberg, S. P., Garland, T. & Ives, A. R. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717–745 (2003).

    Google Scholar 

  72. Lê, S., Josse, J. & Husson, F. FactoMineR: an R package for multivariate analysis. J. Stat. Softw. 25, 1–18 (2008).

    Google Scholar 

  73. Butler, E. E. et al. Mapping local and global variability in plant trait distributions. Proc. Natl. Acad. Sci. USA 114, E10937–E10946 (2017).

    Google Scholar 

  74. R. Core Team. R: A language and environment for statistical computing (R Foundation for Statistical Computing, 2025).

  75. Xiong, K. Dataset and R code for ‘Acquisitive plants exhibit stronger phenological shifts in response to warming: insights from meta-analysis and long-term monitoring’. figshare https://doi.org/10.6084/m9.figshare.29917052 (2025).

Download references

Acknowledgements

This research was supported by the National Natural Science Foundation of China (Grant Nos. 32422055 (H.L.), 32130065 (H.L.) and 42125101 (C.W.)) and the National R&D Program of China (Grant No. 2023YFF0806800 (H.L.)). H.L. also acknowledges support from the Shanghai Rising-Star Program (Grant No. 23QA1402900) and Fundamental and Interdisciplinary Disciplines Breakthrough Plan of the Ministry of Education of China (JYB2025XDXM904). We would like to express our gratitude to all the authors of the published papers included in our meta-analysis, as well as to the contributors of the two long-term phenological datasets. We also thank the contributors of the TRY database, as well as the authors who provided the spatial distribution data of the traits used in Fig. 4.

Author information

Authors and Affiliations

Authors

Contributions

H.L. and C.W. conceived the study. K.X., H.Z., and H.L. conducted the analysis with inputs from C.L. and X.W. P.R., P.C., J.P., and C.W. provided significant revisions. K.X., C.W., and H.L. wrote the manuscript, with contributions from all co-authors.

Corresponding authors

Correspondence to
Chaoyang Wu or Huiying Liu.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Communications thanks the anonymous reviewers for their contribution to the peer review of this work. A peer review file is available.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information (download PDF )

Reporting Summary (download PDF )

Transparent Peer Review file (download PDF )

Source data

Source Data (download XLSX )

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and permissions

About this article

Cite this article

Xiong, K., Reich, P.B., Ciais, P. et al. Acquisitive plants exhibit stronger phenological shifts in response to warming: insights from meta-analysis and long-term monitoring.
Nat Commun (2026). https://doi.org/10.1038/s41467-026-70474-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41467-026-70474-4


Source: Ecology - nature.com

Championing fusion’s promising underdog

Ecoepidemiological determinants of Borrelia infection in sigmodontine rodents from the Delta and Parana Islands ecoregion, Argentina

Back to Top