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.

  • Letter
  • Published:

Day length unlikely to constrain climate-driven shifts in leaf-out times of northern woody plants

Nature Climate Change volume 6, pages 1120–1123 (2016)Cite this article

Subjects

This article has been updated

Abstract

The relative roles of temperature and day length in driving spring leaf unfolding are known for few species, limiting our ability to predict phenology under climate warming1,2. Using experimental data, we assess the importance of photoperiod as a leaf-out regulator in 173 woody species from throughout the Northern Hemisphere, and we also infer the influence of winter duration, temperature seasonality, and inter-annual temperature variability. We combine results from climate- and light-controlled chambers with species’ native climate niches inferred from georeferenced occurrences and range maps. Of the 173 species, only 35% relied on spring photoperiod as a leaf-out signal. Contrary to previous suggestions, these species come from lower latitudes, whereas species from high latitudes with long winters leafed out independent of photoperiod. The strong effect of species’ geographic–climatic history on phenological strategies complicates the prediction of community-wide phenological change.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Relationship between species’ spring photoperiodism and the maximum winter duration in their native ranges.
Figure 2: Effect of day length sensitivity on inter-annual variability in leaf-out.

Similar content being viewed by others

Change history

  • 14 November 2016

    In the version of this Letter originally published, the last sentence should have read 'Therefore, photoperiod may be expected to constrain climate-driven shifts in spring leaf unfolding only at lower latitudes'. This error as been corrected in all versions of the Letter.

References

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

    Article  Google Scholar 

  2. Richardson, A. D. et al. Climate change, phenology, and phenological control of vegetation feedbacks to the climate system. Agr. Forest Meteorol. 169, 156–173 (2013).

    Article  Google Scholar 

  3. Saikkonen, K. et al. Climate change-driven species’ range shifts filtered by photoperiodism. Nat. Clim. Change 2, 239–242 (2012).

    Article  Google Scholar 

  4. 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 

  5. Menzel, A. & Fabian, P. Growing season extended in Europe. Nature 397, 659 (1999).

    Article  CAS  Google Scholar 

  6. 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 

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

    Article  Google Scholar 

  8. Heide, O. M. Dormancy release in beech buds (Fagus sylvatica) requires both chilling and long days. Physiol. Plant. 89, 187–191 (1993).

    Article  Google Scholar 

  9. Basler, D. & Koerner, C. Photoperiod sensitivity of bud burst in 14 temperate forest tree species. Agr. Forest Meteorol. 165, 73–81 (2012).

    Article  Google Scholar 

  10. Zohner, C. M. & Renner, S. S. Perception of photoperiod in individual buds of mature trees regulates leaf-out. New Phytol. 208, 1023–1030 (2015).

    Article  Google Scholar 

  11. Heide, O. M. Daylength and thermal time responses of budburst during dormancy release in some northern deciduous trees. Physiol. Plant. 88, 531–540 (1993).

    Article  CAS  Google Scholar 

  12. Laube, J. et al. Chilling outweighs photoperiod in preventing precocious spring development. Glob. Change Biol. 20, 170–182 (2014).

    Article  Google Scholar 

  13. Polgar, C., Gallinat, A. & Primack, R. B. Drivers of leaf-out phenology and their implications for species invasions: insights from Thoreau’s Concord. New Phytol. 202, 106–115 (2014).

    Article  Google Scholar 

  14. Vitasse, Y., Lenz, A. & Körner, C. The interaction between freezing tolerance and phenology in temperate deciduous trees. Front. Plant Sci. 5, 541 (2014).

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

    Article  CAS  Google Scholar 

  16. Wareing, P. F. Growth studies in woody species. V. Photoperiodism in dormant buds of Fagus sylvatica L. Physiol. Plant. 6, 692–706 (1953).

    Article  Google Scholar 

  17. Falusi, M. & Calamassi, R. Bud dormancy in beech (Fagus sylvatica L.). Effect of chilling and photoperiod on dormancy release of beech seedlings. Tree Physiol. 6, 429–438 (1990).

    Article  CAS  Google Scholar 

  18. Caffarra, A. & Donnelly, A. The ecological significance of phenology in four different tree species: effects of light and temperature on bud burst. Int. J. Biometeorol. 55, 711–721 (2011).

    Article  Google Scholar 

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

    Article  Google Scholar 

  20. Ghelardini, L., Santini, A., Black-Samuelsson, S., Myking, T. & Falusi, M. Bud dormancy in elm (Ulmus spp.) clones—a case study of photoperiod and temperature responses. Tree Physiol. 30, 264–274 (2010).

    Article  Google Scholar 

  21. 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  Google Scholar 

  22. Lechowicz, M. J. Why do temperate deciduous trees leaf out at different times? Adaptation and ecology of forest communities. Am. Nat. 124, 821–842 (1984).

    Article  Google Scholar 

  23. Chuine, I. & Beaubien, E. Phenology is a major determinant of temperate tree range. Ecol. Lett. 4, 500–510 (2001).

    Article  Google Scholar 

  24. Chuine, I. Why does phenology drive species distribution? Phil. Trans. R. Soc. B 365, 3149–3160 (2010).

    Article  Google Scholar 

  25. Zohner, C. M. & Renner, S. S. Common garden comparison of the leaf-out phenology of woody species from different native climates, combined with herbarium records forecasts long-term change. Ecol. Lett. 17, 1016–1025 (2014).

    Article  Google Scholar 

  26. Wang, T. et al. The influence of local spring temperature variance on temperature sensitivity of spring phenology. Glob. Change Biol. 20, 1473–1480 (2014).

    Article  Google Scholar 

  27. Vitasse, Y., Porte, A. J., Kremer, A., Michalet, R. & Delzon, S. Responses of canopy duration to temperature changes in four temperate tree species: relative contributions of spring and autumn leaf phenology. Oecologia 161, 187–198 (2009).

    Article  Google Scholar 

  28. Lenz, A., Hoch, G., Vitasse, Y. & Körner, C. Convergence of leaf-out towards minimum risk of freezing damage in temperate trees. Funct. Ecol. 30, 1480–1490 (2016).

    Article  Google Scholar 

  29. Lenoir, J. & Svenning, J.-C. Climate-related range shifts—a global multidimensional synthesis and new research directions. Ecography 38, 15–28 (2015).

    Article  Google Scholar 

  30. Tiffney, B. H. & Manchester, S. R. The influence of physical environment on phytogeographic continuity and phylogeographic hypotheses in the Northern Hemisphere Tertiary. Int. J. Plant Sci. 162, 3–17 (2001).

    Article  Google Scholar 

  31. Vitasse, Y. & Basler, D. Is the use of cuttings a good proxy to explore phenological responses of temperate forests in warming and photoperiod experiments? Tree Physiol. 34, 174–183 (2014).

    Article  Google Scholar 

  32. Siegel, S. & Castellan, N. J. Non-Parametric Statistics for the Behavioral Sciences 213–214 (MacGraw Hill, 1988).

    Google Scholar 

  33. Dismo v1.1-1 (Hijmans, R. J., Phillips, S., Leathwick, J. & Elith, J., 2011); http://cran.r-project.org/web/packages/dismo/index.html

  34. WORLDCLIM v1.3 (Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones P. G. & Jarvis, A., 2004); http://datadryad.org/handle/10255/dryad.12700

  35. 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).

    Article  Google Scholar 

  36. Peel, M. C., Finlayson, B. L. & McMahon, T. A. Updated world map of the Koeppen–Geiger climate classification. Hydrol. Earth Syst. Sci. 11, 1633–1644 (2007).

    Article  Google Scholar 

  37. Breiman, L. Random forest. Mach. Learn. 45, 15–32 (2001).

    Google Scholar 

  38. Cutler, D. R. et al. Random forests for classification in ecology. Ecology 88, 2783–2792 (2007).

    Article  Google Scholar 

  39. de Villemereuil, P., Wells, J. A., Edwards, R. D. & Blomberg, S. P. Bayesian models for comparative analysis integrating phylogenetic uncertainty. BMC Evol. Biol. 12, 102 (2012).

    Article  Google Scholar 

  40. Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877–884 (1999).

    Article  CAS  Google Scholar 

  41. Revell, L. J. Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

    Article  Google Scholar 

  42. Panchen, Z. A. et al. Leaf out times of temperate woody plants are related to phylogeny, deciduousness, growth habit and wood anatomy. New Phytol. 203, 1208–1219 (2014).

    Article  CAS  Google Scholar 

  43. Webb, C. O. & Donoghue, M. J. PHYLOMATIC: tree assembly for applied phylogenetics. Mol. Ecol. Notes 5, 181–183 (2005).

    Article  Google Scholar 

  44. Bremer, B. et al. An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG III. Bot. J. Linnean Soc. 161, 105–121 (2009).

  45. http://www.mobot.org/MOBOT/research/APweb

  46. Bell, C., Soltis, D. E. & Soltis, P. S. The age and diversification of the angiosperms re-revisited. Am. J. Bot. 97, 1296–1303 (2010).

    Article  Google Scholar 

  47. Smith, S. A., Beaulieu, J. M. & Donoghue, M. J. An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants. Proc. Natl Acad. Sci. USA 107, 5897–5902 (2010).

    Article  CAS  Google Scholar 

  48. Stahl, U., Reu, B. & Wirth, C. Predicting species’ range limits from functional traits for the tree flora of North America. Proc. Natl Acad. Sci. USA 111, 13739–13744 (2014).

    Article  CAS  Google Scholar 

  49. Gelman, A. & Hill, J. Data Analysis Using Regression and Multilevel/Hierarchical Models (Cambridge Univ. Press, 2007).

    Google Scholar 

  50. Grafen, A. The phylogenetic regression. Phil. Trans. R. Soc. B 326, 119–157 (1989).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  52. Plummer, M. JAGS: a program for analysis of Bayesian graphical models using Gibbs sampling. In Proc. 3rd Int. Workshop on Distributed Statistical Computing (eds Hornik, K., Leisch, F. & Zeileis, A.) (DSC, 2003).

    Google Scholar 

  53. R2jags v 0.04-03 (Su, Y.-S. & Yajima, M., 2014); http://CRAN.R-project.org/package=R2jags

  54. Gelman, A. & Rubin, D. B. Inference from iterative simulation using multiple sequences. Stat. Sci. 7, 457–472 (1992).

    Article  Google Scholar 

  55. R v3.3.1 (R Core Team, 2015); http://www.R-project.org

Download references

Acknowledgements

We thank V. Sebald and M. Wenn for help with conducting the twig-cutting experiments. B.M.B. acknowledges funding by Aarhus University and the Aarhus University Research Foundation under the AU IDEAS programme (Centre for Biocultural History) and J.-C.S. support from by the European Research Council (ERC-2012-StG-310886-HISTFUNC). The study was part of the KLIMAGRAD project sponsored by the ‘Bayerisches Staatsministerium für Umwelt und Gesundheit’.

Author information

Authors and Affiliations

  1. Department of Biology, Systematic Botany and Mycology, Munich University (LMU), 80638 Munich, Germany

    Constantin M. Zohner & Susanne S. Renner

  2. Department of Bioscience, Section for Ecoinformatics and Biodiversity, Aarhus University, DK-8000 Aarhus C, Denmark

    Blas M. Benito & Jens-Christian Svenning

Authors
  1. Constantin M. Zohner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Blas M. Benito
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jens-Christian Svenning
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Susanne S. Renner
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

C.M.Z. and S.S.R. designed the study. C.M.Z. conducted the experiments and leaf-out observations. C.M.Z. and B.M.B. performed the analyses. C.M.Z. and S.S.R. led the writing with inputs from the other authors.

Corresponding author

Correspondence to Constantin M. Zohner.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 1406 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zohner, C., Benito, B., Svenning, JC. et al. Day length unlikely to constrain climate-driven shifts in leaf-out times of northern woody plants. Nature Clim Change 6, 1120–1123 (2016). https://doi.org/10.1038/nclimate3138

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nclimate3138

This article is cited by

Search

Advanced 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