Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

An earlier start of the thermal growing season enhances tree growth in cold humid areas but not in dry areas

Abstract

Climatic warming alters the onset, duration and cessation of the vegetative season. While previous studies have shown a tight link between thermal conditions and leaf phenology, less is known about the impacts of phenological changes on tree growth. Here, we assessed the relationships between the start of the thermal growing season and tree growth across the extratropical Northern Hemisphere using 3,451 tree-ring chronologies and daily climatic data for 1948–2014. An earlier start of the thermal growing season promoted growth in regions with high ratios of precipitation to temperature but limited growth in cold–dry regions. Path analyses indicated that an earlier start of the thermal growing season enhanced growth primarily by alleviating thermal limitations on wood formation in boreal forests and by lengthening the period of growth in temperate and Mediterranean forests. Semi-arid and dry subalpine forests, however, did not benefit from an earlier onset of growth and a longer growing season, presumably due to associated water loss and/or more frequent early spring frosts. These emergent patterns of how climatic impacts on wood phenology affect tree growth at regional to hemispheric scales hint at how future phenological changes may affect the carbon sequestration capacity of extratropical forest ecosystems.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Responses of tree growth to changes in the onset of the TSOS across the extratropical Northern Hemisphere.
Fig. 2: Path diagrams and path effects for northern Asia, northern and central Europe, the Mediterranean region, the west and east coasts of the United States, the Colorado Plateau and the Tibetan Plateau.

Similar content being viewed by others

Data availability

The reformatted data of the ITRDB were obtained from https://doi.org/10.5061/dryad.kh0qh06. Tree-ring width data from the ITPCAS tree-ring group are available from https://doi.org/10.11888/Terre.tpdc.271925. The Global Meteorological Forcing Dataset of the Terrestrial Hydrology Research Group at Princeton University was obtained from http://hydrology.princeton.edu/data.pgf.php. The NASA Global Land Data Assimilation System v.2 was obtained from https://disc.gsfc.nasa.gov/datasets/GLDAS_CLSM025_D_2.0/summary?keywords=GLDAS2.0. Source data are provided with this paper.

Code availability

Statistical analyses in this study were performed with publicly available packages in R (v.3.6.2, dplR and sem packages) and Python (v.3.8, scipy package) and the figures were produced using Python (matplotlib, cartopy and seaborn packages). The custom code for the analysis of the data are available from https://doi.org/10.11888/Terre.tpdc.271925.

References

  1. Trenberth, K. E. & Jones, P. D. in Climate Change 2007: The Physical Science Basis (eds Solomon, S. et al.) 235–335 (Cambridge Univ. Press, 2007).

  2. Linderholm, H. W. Growing season changes in the last century. Agr. For. Meteorol. 137, 1–14 (2006).

    Article  Google Scholar 

  3. Yang, B. et al. New perspective on spring vegetation phenology and global climate change based on Tibetan Plateau tree-ring data. Proc. Natl Acad. Sci. USA 114, 6966–6971 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Shen, M., Tang, Y., Chen, J. & Yang, W. Specification of thermal growing season in temperate China from 1960 to 2009. Clim. Change 114, 783–798 (2012).

    Article  Google Scholar 

  5. Zhou, B., Zhai, P., Chen, Y. & Yu, R. Projected changes of thermal growing season over Northern Eurasia in a 1.5 °C and 2 °C warming world. Environ. Res. Lett. 13, 35004 (2018).

    Article  Google Scholar 

  6. Barichivich, J., Briffa, K. R., Osborn, T. J., Melvin, T. M. & Caesar, J. Thermal growing season and timing of biospheric carbon uptake across the Northern Hemisphere. Glob. Biogeochem. Cycles 26, B4015 (2012).

    Article  Google Scholar 

  7. Buitenwerf, R., Rose, L. & Higgins, S. I. Three decades of multi-dimensional change in global leaf phenology. Nat. Clim. Change 5, 364–368 (2015).

    Article  Google Scholar 

  8. Gonsamo, A., Chen, J. M. & Ooi, Y. W. Peak season plant activity shift towards spring is reflected by increasing carbon uptake by extratropical ecosystems. Glob. Change Biol. 24, 2117–2128 (2018).

    Article  Google Scholar 

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

    Article  Google Scholar 

  10. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  12. Barichivich, J. et al. Large-scale variations in the vegetation growing season and annual cycle of atmospheric CO2 at high northern latitudes from 1950 to 2011. Glob. Change Biol. 19, 3167–3183 (2013).

    Article  Google Scholar 

  13. Peñuelas, J., Rutishauser, T. & Filella, I. Phenology feedbacks on climate change. Science 324, 887–888 (2009).

    Article  PubMed  Google Scholar 

  14. Piao, S. et al. Weakening temperature control on the interannual variations of spring carbon uptake across northern lands. Nat. Clim. Change 7, 359–363 (2017).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  16. Bonan, G. B. Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320, 1444–1449 (2008).

    Article  CAS  PubMed  Google Scholar 

  17. Piao, S. et al. Plant phenology and global climate change: current progresses and challenges. Glob. Change Biol. 25, 1922–1940 (2019).

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  19. Park, T. et al. Changes in timing of seasonal peak photosynthetic activity in northern ecosystems. Glob. Change Biol. 25, 2382–2395 (2019).

    Article  Google Scholar 

  20. Xu, C., Liu, H., Williams, A. P., Yin, Y. & Wu, X. Trends toward an earlier peak of the growing season in Northern Hemisphere mid-latitudes. Glob. Change Biol. 22, 2852–2860 (2016).

    Article  Google Scholar 

  21. Wang, X. et al. No trends in spring and autumn phenology during the global warming hiatus. Nat. Commun. 10, 2389 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  22. Piao, S., Friedlingstein, P., Ciais, P., Viovy, N. & Demarty, J. Growing season extension and its impact on terrestrial carbon cycle in the Northern Hemisphere over the past 2 decades. Glob. Biogeochem. Cycles 21, B3018 (2007).

    Article  Google Scholar 

  23. Buermann, W., Bikash, P. R., Jung, M., Burn, D. H. & Reichstein, M. Earlier springs decrease peak summer productivity in North American boreal forests. Environ. Res. Lett. 8, 24027 (2013).

    Article  Google Scholar 

  24. Buermann, W. et al. Widespread seasonal compensation effects of spring warming on northern plant productivity. Nature 562, 110–114 (2018).

    Article  CAS  PubMed  Google Scholar 

  25. Lian, X. et al. Summer soil drying exacerbated by earlier spring greening of northern vegetation. Sci. Adv. 6, eaax0255 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  27. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Pan, Y. et al. A large and persistent carbon sink in the world’s forests. Science 333, 988–993 (2011).

    Article  CAS  PubMed  Google Scholar 

  29. Delpierre, N. et al. Temperate and boreal forest tree phenology: from organ-scale processes to terrestrial ecosystem models. Ann. For. Sci. 73, 5–25 (2016).

    Article  Google Scholar 

  30. Huang, J. et al. Photoperiod and temperature as dominant environmental drivers triggering secondary growth resumption in Northern Hemisphere conifers. Proc. Natl Acad. Sci. USA 117, 20645–20652 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Li, X. et al. Critical minimum temperature limits xylogenesis and maintains treelines on the southeastern Tibetan Plateau. Sci. Bull. 62, 804–812 (2017).

    Article  Google Scholar 

  32. Rossi, S. et al. Critical temperatures for xylogenesis in conifers of cold climates. Glob. Ecol. Biogeogr. 17, 696–707 (2008).

    Article  Google Scholar 

  33. Lenz, A., Vitasse, Y., Hoch, G. & Körner, C. Growth and carbon relations of temperate deciduous tree species at their upper elevation range limit. J. Ecol. 102, 1537–1548 (2014).

    Article  Google Scholar 

  34. Zeng, Q., Rossi, S., Yang, B., Qin, C. & Li, G. Environmental drivers for cambial reactivation of Qilian junipers (Juniperus przewalskii) in a semi-arid region of northwestern China. Atmosphere 11, 232 (2020).

    Article  Google Scholar 

  35. Ren, P. et al. Growth rate rather than growing season length determines wood biomass in dry environments. Agr. For. Meteorol. 271, 46–53 (2019).

    Article  Google Scholar 

  36. Sanginés De Cárcer, P. et al. Vapor-pressure deficit and extreme climatic variables limit tree growth. Glob. Change Biol. 24, 1108–1122 (2017).

    Article  Google Scholar 

  37. Zhang, J. et al. Drought limits wood production of Juniperus przewalskii even as growing seasons lengthens in a cold and arid environment. Catena 196, 104936 (2021).

    Article  Google Scholar 

  38. Huang, J., Deslauriers, A. & Rossi, S. Xylem formation can be modeled statistically as a function of primary growth and cambium activity. New Phytol. 203, 831–841 (2014).

    Article  CAS  PubMed  Google Scholar 

  39. Rossi, S., Morin, H. & Deslauriers, A. Causes and correlations in cambium phenology: towards an integrated framework of xylogenesis. J. Exp. Bot. 63, 2117–2126 (2012).

    Article  CAS  PubMed  Google Scholar 

  40. Rossi, S., Girard, M. J. & Morin, H. Lengthening of the duration of xylogenesis engenders disproportionate increases in xylem production. Glob. Change Biol. 20, 2261–2271 (2014).

    Article  Google Scholar 

  41. Cuny, H. E. et al. Woody biomass production lags stem-girth increase by over one month in coniferous forests. Nat. Plants 1, 15160 (2015).

    Article  CAS  PubMed  Google Scholar 

  42. Pasho, E., Camarero, J. J. & Vicente-Serrano, S. M. Climatic impacts and drought control of radial growth and seasonal wood formation in Pinus halepensis. Trees 26, 1875–1886 (2012).

    Article  Google Scholar 

  43. 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).

    Article  CAS  Google Scholar 

  44. Chen, L. et al. Leaf senescence exhibits stronger climatic responses during warm than during cold autumns. Nat. Clim. Change 10, 777–780 (2020).

    Article  CAS  Google Scholar 

  45. Körner, C. Paradigm shift in plant growth control. Curr. Opin. Plant Biol. 25, 107–114 (2015).

    Article  PubMed  Google Scholar 

  46. Muller, B. et al. Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. J. Exp. Bot. 62, 1715–1729 (2011).

    Article  CAS  PubMed  Google Scholar 

  47. Charney, N. D. et al. Observed forest sensitivity to climate implies large changes in 21st century North American forest growth. Ecol. Lett. 19, 1119–1128 (2016).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  49. Deslauriers, A. & Morin, H. Intra-annual tracheid production in balsam fir stems and the effect of meteorological variables. Trees 19, 402–408 (2005).

    Article  Google Scholar 

  50. Piao, S. et al. Characteristics, drivers and feedbacks of global greening. Nat. Rev. Earth Environ. 1, 14–27 (2020).

    Article  Google Scholar 

  51. Huang, M. et al. Air temperature optima of vegetation productivity across global biomes. Nat. Ecol. Evol. 3, 772–779 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  52. Keenan, T. F. & Riley, W. J. Greening of the land surface in the world’s cold regions consistent with recent warming. Nat. Clim. Change 8, 825–828 (2018).

    Article  CAS  Google Scholar 

  53. Camarero, J. J., Olano, J. M. & Parras, A. Plastic bimodal xylogenesis in conifers from continental Mediterranean climates. New Phytol. 185, 471–480 (2010).

    Article  PubMed  Google Scholar 

  54. Fu, Y. H. et al. Unexpected role of winter precipitation in determining heat requirement for spring vegetation green-up at northern middle and high latitudes. Glob. Change Biol. 20, 3743–3755 (2014).

    Article  Google Scholar 

  55. Wu, X. et al. Uneven winter snow influence on tree growth across temperate China. Glob. Change Biol. 25, 144–154 (2018).

    Article  Google Scholar 

  56. Wang, X. et al. Disentangling the mechanisms behind winter snow impact on vegetation activity in northern ecosystems. Glob. Change Biol. 24, 1651–1662 (2018).

    Article  Google Scholar 

  57. Adams, H. D. et al. Experimental drought and heat can delay phenological development and reduce foliar and shoot growth in semiarid trees. Glob. Change Biol. 21, 4210–4220 (2015).

    Article  Google Scholar 

  58. He, W., Liu, H., Qi, Y., Liu, F. & Zhu, X. Patterns in nonstructural carbohydrate contents at the tree organ level in response to drought duration. Glob. Change Biol. 26, 3627–3638 (2020).

    Article  Google Scholar 

  59. Williams, A. P. et al. Temperature as a potent driver of regional forest drought stress and tree mortality. Nat. Clim. Change 3, 292–297 (2012).

    Article  Google Scholar 

  60. Vitasse, Y. et al. Contrasting resistance and resilience to extreme drought and late spring frost in five major European tree species. Glob. Change Biol. 25, 3781–3792 (2019).

    Article  Google Scholar 

  61. Zhao, S. et al. The International Tree-Ring Data Bank (ITRDB) revisited: data availability and global ecological representativity. J. Biogeogr. 46, 355–368 (2019).

    Article  Google Scholar 

  62. Babst, F., Poulter, B., Bodesheim, P., Mahecha, M. D. & Frank, D. C. Improved tree-ring archives will support earth-system science. Nat. Ecol. Evol. 1, 8 (2017).

    Article  PubMed  Google Scholar 

  63. Elmore, A. J., Guinn, S. M., Minsley, B. J. & Richardson, A. D. Landscape controls on the timing of spring, autumn, and growing season length in mid-Atlantic forests. Glob. Change Biol. 18, 656–674 (2012).

    Article  Google Scholar 

  64. Kannenberg, S. A. et al. Drought legacies are dependent on water table depth, wood anatomy and drought timing across the eastern US. Ecol. Lett. 22, 119–127 (2018).

    Article  PubMed  Google Scholar 

  65. Rossi, S., Deslauriers, A., Anfodillo, T. & Carraro, V. Evidence of threshold temperatures for xylogenesis in conifers at high altitudes. Oecologia 152, 1–12 (2007).

    Article  PubMed  Google Scholar 

  66. Gao, S. et al. Dynamic responses of tree-ring growth to multiple dimensions of drought. Glob. Change Biol. 24, 5380–5390 (2018).

    Article  Google Scholar 

  67. Peltier, D. M. P. & Ogle, K. Tree growth sensitivity to climate is temporally variable. Ecol. Lett. 23, 1561–1572 (2020).

    Article  PubMed  Google Scholar 

  68. Wilmking, M. et al. Global assessment of relationships between climate and tree growth. Glob. Change Biol. 26, 3212–3220 (2020).

    Article  Google Scholar 

  69. Seftigen, K., Frank, D. C., Björklund, J., Babst, F. & Poulter, B. The climatic drivers of normalized difference vegetation index and tree-ring-based estimates of forest productivity are spatially coherent but temporally decoupled in Northern Hemispheric forests. Glob. Ecol. Biogeogr. 27, 1352–1365 (2018).

    Article  Google Scholar 

  70. Bunn, A. G. A dendrochronology program library in R (dplR). Dendrochronologia 26, 115–124 (2008).

    Article  Google Scholar 

  71. R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019); https://www.R-project.org/

  72. Sheffield, J., Goteti, G. & Wood, E. F. Development of a 50-year high-resolution global dataset of meteorological forcings for land surface modeling. J. Clim. 19, 3088–3111 (2006).

    Article  Google Scholar 

  73. Frich, P. L. et al. Observed coherent changes in climatic extremes during the second half of the twentieth century. Clim. Res. 19, 193–212 (2002).

    Article  Google Scholar 

  74. Selyaninov, G. T. About climate agricultural estimation (in Russian). Proc. Agric. Meteorol. 20, 165–177 (1928).

    Google Scholar 

  75. Streiner, D. L. Finding our way: an introduction to path analysis. Can. J. Psychiatry 50, 115–122 (2005).

    Article  PubMed  Google Scholar 

  76. Fox, J., Nie, Z. & Byrnes, J. sem: Structural equation models. R package version 3.1-9 https://CRAN.R-project.org/package=sem (2017).

  77. Iturbide, M. et al. An update of IPCC climate reference regions for subcontinental analysis of climate model data: definition and aggregated datasets. Earth Syst. Sci. Data 12, 2959–2970 (2020).

    Article  Google Scholar 

  78. Bagozzi, R. P. & Yi, Y. Specification, evaluation, and interpretation of structural equation models. J. Acad. Mark. Sci. 40, 8–34 (2012).

    Article  Google Scholar 

Download references

Acknowledgements

We acknowledge all contributors to the ITRDB for providing tree-ring data. This study was supported by the Second Tibetan Plateau Scientific Expedition and Research Program (2019QZKK0301), the National Natural Science Foundation of China (41907387, 42030508 and 41988101) and the China Postdoctoral Science Foundation (2019M660813). J.P. was funded by Spanish Government projects PID2019–110521GB-I00, Fundación Ramón Areces project ELEMENTAL-CLIMATE and Catalan government project SGR2017-1005.

Author information

Authors and Affiliations

Authors

Contributions

S.G. and E.L. designed the research. S.G. and R.L. performed the analysis. S.G. drafted the manuscript. E.L., F.B., J.J.C., Y.H.F., S.P., S.R., M.S., T.W. and J.P. contributed ideas, interpreted the results and were involved in the editing and writing of the manuscript.

Corresponding author

Correspondence to Eryuan Liang.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks Bao Yang, Yingying Xie 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.

Extended data

Extended Data Fig. 1 Responses of tree growth to changes in TSOS in the extratropical Northern Hemisphere.

Spatial distributions of simple correlation coefficients (A), partial correlation coefficients (B), significant (p < 0.1) simple correlation coefficients (C) and significant (p < 0.1) partial correlation coefficients (D) of TSOS and RWI. (E) Areas with significant (p < 0.1, dark blue) and nonsignificant (light blue) trends toward earlier TSOS between 1948 and 2016 in the extratropical Northern Hemisphere. (F) Areas with significant (p < 0.05, blue shaded area) trends toward earlier TSOS overlapping tree-ring chronologies with significant (p < 0.1) simple correlation coefficients of TSOS and RWI. The significance of the correlation analyses is estimated by two-tailed Student’s t-test. This figure was generated using the matplotlib and cartopy package in Python.

Source data

Extended Data Fig. 2 Scatter plots of TSOS–RWI relationships in different regions.

TSOS–RWI relationships of tree-ring chronologies with significant (p < 0.1) simple correlations for northern Asia (A), northern Europe (B), central Europe (C), the Mediterranean region (D), the west coast of the US (E), the east coast of the US (F), the Colorado Plateau (G) and the Tibetan Plateau (H). The predicted mean (solid lines) is bounded by the 95% confidence intervals (shaded areas). This figure was generated using the seaborn package, ‘lmplot’ function in Python.

Source data

Supplementary information

Supplementary Information

Supplementary text, Figs. 1–6, Tables 1–3 and references.

Reporting Summary.

Source data

Source Data Fig. 1

Statistical source data for individual data points.

Source Data Fig. 2

Statistical source data.

Source Data Extended Data Fig. 1

Statistical source data for individual data points.

Source Data Extended Data Fig. 2

Source data for individual data points.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gao, S., Liang, E., Liu, R. et al. An earlier start of the thermal growing season enhances tree growth in cold humid areas but not in dry areas. Nat Ecol Evol 6, 397–404 (2022). https://doi.org/10.1038/s41559-022-01668-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-022-01668-4

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing