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:

Accurate phenology analyses require bud traits and energy budgets

Abstract

Spring phenology is mainly driven by temperature in extratropical ecosystems. Recent evidence highlighted the key role of micrometeorology and bud temperature on delaying or advancing leaf unfolding. Yet, phenology studies, either using ground-based or remote sensing observations, always substitute plant tissue temperature by air temperature. In fact, temperatures differ substantially between plant tissues and the air because plants absorb and lose energy. Here, we build on recent observations and well-established energy balance theories to discuss how solar radiation, wind and bud traits might affect our interpretation of spring phenology sensitivity to warming. We show that air temperature might be an imprecise and biased predictor of bud temperature. Better characterizing the plants’ phenological response to warming will require new observations of bud traits and temperature for accurately quantifying their energy budget. As consistent micrometeorology datasets are still scarce, new approaches coupling energy budget modelling and plant traits could help to improve phenology analyses across scales.

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

Access options

Buy this article

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

Fig. 1: Energy budget of buds and bud traits.
Fig. 2: Simulated differences in temperature between buds and the air (ΔT) from energy balance.
Fig. 3: Spatial variability in bud temperature.
Fig. 4: Potential changes in TbudTair over Europe.
Fig. 5: Impact of ground albedo on simulated bud temperature.
Fig. 6: Impact of bud size on simulated bud temperature.

Similar content being viewed by others

Data availability

FLUXNET2015 data are available at https://fluxnet.fluxdata.org/data/fluxnet2015-dataset/. CRU–JRA data are available at https://catalogue.ceda.ac.uk/uuid/13f3635174794bb98cf8ac4b0ee8f4ed. ERA5 soil temperature data are available at https://cds.climate.copernicus.eu/cdsapp#!/dataset/reanalysis-era5-land. PEP725 phenology data are available at http://www.pep725.eu/.

Code availability

The R code of the model of energy budgets and datasets used to generate the figures and analysis of this manuscript are available from Github at https://github.com/mpeaucelle/Tbud. A version of the git repository is archived on Zenodo at https://zenodo.org/record/5897267 corresponding to tag v.2.0.

References

  1. Peñuelas, J. & Filella, I. Phenology. Responses to a warming world. Science 294, 793–795 (2001).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  3. Ramos-Jiliberto, R., Moisset de Espanés, P., Franco-Cisterna, M., Petanidou, T. & Vázquez, D. P. Phenology determines the robustness of plant-pollinator networks. Sci. Rep. 8, 14873 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  5. Chmielewski, F.-M. in Phenology: An Integrative Environmental Science 2nd edn (ed. Schwartz M. D.) 539–561 (Springer, 2013).

  6. Morellato, L. P. C. et al. Linking plant phenology to conservation biology. Biol. Conserv. 195, 60–72 (2016).

    Article  Google Scholar 

  7. Katelaris, C. H. & Beggs, P. J. Climate change: allergens and allergic diseases. Intern. Med. J. 48, 129–134 (2018).

    Article  PubMed  Google Scholar 

  8. Schwartz, M. D. (ed.) Phenology: An Integrative Environmental Science 2nd edn (Springer, 2013).

  9. Cleland, E. E., Chuine, I., Menzel, A., Mooney, H. A. & Schwartz, M. D. Shifting plant phenology in response to global change. Trends Ecol. Evol. 22, 357–365 (2007).

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  11. Jeong, S.-J., Ho, C.-H., Gim, H.-J. & Brown, M. E. Phenology shifts at start vs. end of growing season in temperate vegetation over the Northern Hemisphere for the period 1982-2008. Glob. Change Biol. 17, 2385–2399 (2011).

    Article  Google Scholar 

  12. 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).

    Article  Google Scholar 

  13. Vitasse, Y. et al. Leaf phenology sensitivity to temperature in European trees: do within-species populations exhibit similar responses. Agric. For. Meteorol. 149, 735–744 (2009).

    Article  Google Scholar 

  14. Wang, S. et al. Temporal trends and spatial variability of vegetation phenology over the Northern Hemisphere during 1982-2012. PLoS ONE 11, e0157134 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. 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 

  16. Huang, M. et al. Velocity of change in vegetation productivity over northern high latitudes. Nat. Ecol. Evol. 1, 1649–1654 (2017).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Zohner, C. M., Mo, L., Pugh, T. A. M., Bastin, J.-F. & Crowther, T. W. Interactive climate factors restrict future increases in spring productivity of temperate and boreal trees. Glob. Change Biol. https://doi.org/10.1111/gcb.15098 (2020).

  19. 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).

  20. Zohner, C. M., Benito, B. M., Svenning, J.-C. & Renner, S. S. Day length unlikely to constrain climate-driven shifts in leaf-out times of northern woody plants. Nat. Clim. Change 6, 1120–1123 (2016).

    Article  Google Scholar 

  21. Peñuelas, J. et al. Complex spatiotemporal phenological shifts as a response to rainfall changes. New Phytol. 161, 837–846 (2004).

    Article  PubMed  Google Scholar 

  22. Papagiannopoulou, C. et al. Vegetation anomalies caused by antecedent precipitation in most of the world. Environ. Res. Lett. 12, 74016 (2017).

    Article  Google Scholar 

  23. 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).

    Article  Google Scholar 

  24. Fu, Y. H. et al. Nutrient availability alters the correlation between spring leaf-out and autumn leaf senescence dates. Tree Physiol. 39, 1277–1284 (2019).

    Article  CAS  PubMed  Google Scholar 

  25. Seyednasrollah, B., Swenson, J. J., Domec, J.-C. & Clark, J. S. Leaf phenology paradox: why warming matters most where it is already warm. Remote Sens. Environ. 209, 446–455 (2018).

    Article  Google Scholar 

  26. Chuine, I., Morin, X. & Bugmann, H. Warming, photoperiods, and tree phenology. Science 329, 277–278 (2010).

    Article  PubMed  Google Scholar 

  27. Vitasse, Y. & Basler, D. What role for photoperiod in the bud burst phenology of European beech. Eur. J. For. Res 132, 1–8 (2013).

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  29. Caffarra, A., Donnelly, A. & Chuine, I. Modelling the timing of Betula pubescens budburst. II. Integrating complex effects of photoperiod into process-based models. Clim. Res. 46, 159–170 (2011).

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  31. Fu, Y. H. et al. Daylength helps temperate deciduous trees to leaf-out at the optimal time. Glob. Change Biol. 25, 2410–2418 (2019).

    Article  Google Scholar 

  32. Singh, R. K., Svystun, T., AlDahmash, B., Jönsson, A. M. & Bhalerao, R. P. Photoperiod- and temperature-mediated control of phenology in trees – a molecular perspective. New Phytol. 213, 511–524 (2017).

    Article  CAS  PubMed  Google Scholar 

  33. Flynn, D. F. B. & Wolkovich, E. M. Temperature and photoperiod drive spring phenology across all species in a temperate forest community. New Phytol. 219, 1353–1362 (2018).

    Article  CAS  PubMed  Google Scholar 

  34. Brelsford, C. C., Nybakken, L., Kotilainen, T. K. & Robson, T. M. The influence of spectral composition on spring and autumn phenology in trees. Tree Physiol. 39, 925–950 (2019).

    Article  CAS  PubMed  Google Scholar 

  35. Strømme, C. B. et al. UV-B and temperature enhancement affect spring and autumn phenology in Populus tremula. Plant Cell Environ. 38, 867–877 (2015).

    Article  PubMed  Google Scholar 

  36. Fu, Y. H. et al. Increased heat requirement for leaf flushing in temperate woody species over 1980-2012: effects of chilling, precipitation and insolation. Glob. Change Biol. 21, 2687–2697 (2015).

    Article  Google Scholar 

  37. Huang, Y., Jiang, N., Shen, M. & Guo, L. Effect of preseason diurnal temperature range on the start of vegetation growing season in the Northern Hemisphere. Ecol. Indic. 112, 106161 (2020).

    Article  Google Scholar 

  38. Meng, F. et al. Opposite effects of winter day and night temperature changes on early phenophases. Ecology 100, e02775 (2019).

    Article  PubMed  Google Scholar 

  39. Zhang, S., Isabel, N., Huang, J.-G., Ren, H. & Rossi, S. Responses of bud-break phenology to daily-asymmetric warming: daytime warming intensifies the advancement of bud break. Int. J. Biometeorol. 63, 1631–1640 (2019).

    Article  PubMed  Google Scholar 

  40. Meng, L. et al. Divergent responses of spring phenology to daytime and nighttime warming. Agric. For. Meteorol. 281, 107832 (2020).

    Article  Google Scholar 

  41. Bigler, C. & Vitasse, Y. Daily maximum temperatures induce lagged effects on leaf unfolding in temperate woody species across large elevational gradients. Front. Plant Sci. 10, 398 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  42. Fu, Y. H. et al. Three times greater weight of daytime than of night-time temperature on leaf unfolding phenology in temperate trees. New Phytol. 212, 590–597 (2016).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  44. Vitasse, Y. et al. Impact of microclimatic conditions and resource availability on spring and autumn phenology of temperate tree seedlings. New Phytol. https://doi.org/10.1111/nph.17606 (2021).

  45. Azeez, A. et al. EARLY BUD-BREAK 1 and EARLY BUD-BREAK 3 control resumption of poplar growth after winter dormancy. Nat. Commun. 12, 1123 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Hamer, P. The heat balance of apple buds and blossoms. Part I. Heat transfer in the outdoor environment. Agric. For. Meteorol. 35, 339–352 (1985).

    Article  Google Scholar 

  47. Landsberg, J. J., Butler, D. R. & Thorpe, M. R. Apple bud and blossom temperatures. J. Horticultural Sci. 49, 227–239 (1974).

    Article  Google Scholar 

  48. Grace, J. The temperature of buds may be higher than you thought. N. Phytol. 170, 1–3 (2006).

    Article  Google Scholar 

  49. Muir, C. D. tealeaves: an R package for modelling leaf temperature using energy budgets. AoB Plants 11, plz054 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  50. Knohl, A., Schulze, E.-D., Kolle, O. & Buchmann, N. Large carbon uptake by an unmanaged 250-year-old deciduous forest in Central Germany. Agric. For. Meteorol. 118, 151–167 (2003).

    Article  Google Scholar 

  51. Zellweger, F. et al. Forest microclimate dynamics drive plant responses to warming. Science 368, 772–775 (2020).

    Article  CAS  PubMed  Google Scholar 

  52. Bailey, B. N., Stoll, R., Pardyjak, E. R. & Miller, N. E. A new three-dimensional energy balance model for complex plant canopy geometries: Model development and improved validation strategies. Agric. For. Meteorol. 218-219, 146–160 (2016).

    Article  Google Scholar 

  53. Michaletz, S. T. & Johnson, E. A. A heat transfer model of crown scorch in forest fires. Can. J. For. Res. 36, 2839–2851 (2006).

    Article  Google Scholar 

  54. Sanchez‐Lorenzo, A. et al. Reassessment and update of long‐term trends in downward surface shortwave radiation over Europe (1939–2012). J. Geophys. Res. Atmos. 120, 9555–9569 (2015).

  55. Pfeifroth, U., Sanchez‐Lorenzo, A., Manara, V., Trentmann, J. & Hollmann, R. Trends and variability of surface solar radiation in Europe based on surface‐ and satellite-based data records. J. Geophys. Res. Atmos. 123, 1735–1754 (2018).

    Article  Google Scholar 

  56. 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).

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. 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. Change Biol. 25, 351–360 (2019).

    Article  Google Scholar 

  59. Zohner, C. M. et al. Late-spring frost risk between 1959 and 2017 decreased in North America but increased in Europe and Asia. Proc. Natl Acad. Sci. USA https://doi.org/10.1073/pnas.1920816117 (2020).

  60. Xiao, L. et al. Estimating spring frost and its impact on yield across winter wheat in China. Agric. For. Meteorol. 260–261, 154–164 (2018).

    Article  Google Scholar 

  61. Unterberger, C. et al. Spring frost risk for regional apple production under a warmer climate. PLoS ONE 13, e0200201 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Leolini, L. et al. Late spring frost impacts on future grapevine distribution in Europe. Field Crops Res. 222, 197–208 (2018).

    Article  Google Scholar 

  63. Greco, S. et al. Late spring frost in mediterranean beech forests: extended crown dieback and short-term effects on moth communities. Forests 9, 388 (2018).

    Article  Google Scholar 

  64. Augspurger, C. K. Spring 2007 warmth and frost: phenology, damage and refoliation in a temperate deciduous forest. Funct. Ecol. 23, 1031–1039 (2009).

    Article  Google Scholar 

  65. Dong, N., Prentice, I. C., Harrison, S. P., Song, Q. H. & Zhang, Y. P. Biophysical homoeostasis of leaf temperature: a neglected process for vegetation and land-surface modelling. Glob. Ecol. Biogeogr. 26, 998–1007 (2017).

    Article  Google Scholar 

  66. Jones, H. G. Plants and Microclimate. A Quantitative Approach to Environmental Plant Physiology (Cambridge Univ. Press, 2013).

  67. University Of East Anglia Climatic Research Unit (CRU) & Harris, I. C. CRU JRA v1.1: a forcings dataset of gridded land surface blend of Climatic Research Unit (CRU) and Japanese reanalysis (JRA) data; Jan.1901–Dec.2017, 2019; https://catalogue.ceda.ac.uk/uuid/13f3635174794bb98cf8ac4b0ee8f4ed

  68. Dupleix, A., Sousa Meneses, D., de, Hughes, M. & Marchal, R. Mid-infrared absorption properties of green wood. Wood Sci. Technol. 47, 1231–1241 (2013).

    Article  CAS  Google Scholar 

  69. Howard, R. & Stull, R. IR radiation from trees to a ski run: a case study. J. Appl. Meteorol. Climatol. 52, 1525–1539 (2013).

    Article  Google Scholar 

  70. Monteith, J. L. & Unsworth, M. H. Principles of Environmental Physics. Plants, Animals, and the Atmosphere 4th edn (Elsevier/Academic Press, 2013).

  71. Bergman, T. L., Incropera, F. P. & Lavine, A. S. Fundamentals of Heat and Mass Transfer (J. Wiley & Sons, 2011).

  72. Jacobs, A., Heusinkveld, B. G. & Kessel, G. Simulating of leaf wetness duration within a potato canopy. NJAS Wagening. J. Life Sci. 53, 151–166 (2005).

    Article  Google Scholar 

  73. Gerlein-Safdi, C. et al. Dew deposition suppresses transpiration and carbon uptake in leaves. Agric. For. Meteorol. 259, 305–316 (2018).

    Article  Google Scholar 

  74. Muñoz Sabater, J. Copernicus Climate Change Service: ERA5-Land hourly data from 1981 to present, 2019; https://cds.climate.copernicus.eu/cdsapp#!/dataset/reanalysis-era5-land

  75. Kusch, E. & Davy, R. KrigR – A tool for downloading and statistically downscaling climate reanalysis data. Environ. Res. Lett. 17, 024005 (2022).

    Article  Google Scholar 

  76. R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2018); https://www.R-project.org/

Download references

Acknowledgements

We acknowledge C. Muir and R. Marchin Prokopavicius for their constructive feedback on our work. The project was funded by Fonds Wetenschappelijk Onderzoek (FWO; grant No. G018319N to M.P.), H2020 Marie Skłodowska-Curie Actions (LEAF-2-TBM, grant No. 891369 to M.P.), the European Research Council Synergy (grant No. ERC-SyG-2013-610028 IMBALANCE-P to J.P.), the Spanish Government (grant No. PID2019-110521GB-I00 to J.P.), the Fundación Ramon Areces (grant No. ELEMENTAL-CLIMATE to J.P.), the Catalan Government (grant No. SGR 2017-1005 to J.P.) and the European Research Council (grant No. 637643 TREECLIMBERS to H.V.).

Author information

Authors and Affiliations

Authors

Contributions

M.P. designed the study, performed the analysis and wrote the first version of the manuscript. J.P. and H.V. substantially contributed to the interpretation of the results and the revisions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Marc Peaucelle.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Plants thanks Klaus-Peter Götz 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 Distribution of sites with more than 20 years of leaf unfolding records over 1990-2015.

Sites including data for Common alder (Alnus glutinosa), horse chestnut (Aesculus hippocastanum), silver birch (Betula pendula), European beech (Fagus sylvatica), European ash (Fraxinus excelsior) and pedunculate oak (Quercus robur) from the PEP database.

Extended Data Fig. 2 Weight of each component of the bud energy budget in simulating bud temperature.

Response of the bud-air temperature difference (ΔT) is a complex nonlinear response to Rabs (red), H (orange) and LWbud (Blue). For more clarity, energy components were divided by 500, 100, 500 and 10 for Rabs, H, LWbud and E, respectively. Each point corresponds to the mean ΔT simulated for six species across Europe (n = 1059 sites) under idealized conditions using field observation of budburst and global meteorological data. All sites and species were pooled together. Solar absorptivity to shortwave radiation is set to 0.8. The error bars represent the spatial and species variability (±1SD around the mean, n = 5050). Panels b, c, d and e represent the weight of Rabs, LWbud, H and E in explaining ΔT variability, by showing the relationships of their respective partial residuals in the multiple linear regression ΔT=Rabs + H+LWbud+E (R² = 0.85) using global yearly averages. We observe that H, Rabs and LWbud account for most of the variability in ΔT. Red full lines represent the slope coefficient in the linear regression. Dashed lines represent the standard error associated to each coefficient.

Supplementary information

Supplementary Information

List of variables and parameters of the energy budget model.

Reporting Summary

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Peaucelle, M., Peñuelas, J. & Verbeeck, H. Accurate phenology analyses require bud traits and energy budgets. Nat. Plants 8, 915–922 (2022). https://doi.org/10.1038/s41477-022-01209-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-022-01209-8

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