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Innately shorter vegetation periods in North American species explain native–non-native phenological asymmetries

Abstract

The length of the vegetation period (LVP), which is the time between leaf-out and leaf senescence, affects numerous ecosystem functions, including biogeochemical cycles and interspecific interactions. The evolutionary mechanisms determining LVP, however, are poorly understood, and thus, it is unknown whether innate LVPs differ between eastern North American (ENA), European and East Asian species. Here we monitored LVP in 2014–2015 in 396 Northern Hemisphere woody species grown in a common garden. We found that ENA species, under the same conditions, have three weeks (11%) shorter vegetation periods than their European and East Asian relatives, because their leaves flushed 9 ± 4 and 13 ± 4 days later and senesced 9 ± 4 and 11 ± 4 days earlier. LVPs of species introduced from Eurasia into ENA are therefore longer than those of native species, suggesting that the spread of non-natives might alter seasonal forest productivity in ENA. LVP between naturalized invasive and non-invasive species, however, did not differ, rejecting the common assumption that longer leaf presentation generally fosters invasive success. A likely explanation for the shorter LVP of ENA species is that region’s uniquely high inter-annual temperature variation. These results highlight the footprint of regional climate history, which will affect forest response to climate change.

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Fig. 1: LVP of ENA, European and East Asian species.
Fig. 2: LVP of naturalized non-invasive, invasive and native species in ENA and Europe.

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References

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  3. 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 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  6. 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 

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

    Article  Google Scholar 

  8. 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 

  9. 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 

  10. Zohner, C. M., Benito, B. M., Fridley, J. D., Svenning, J.-C. & Renner, S. S. Spring predictability explains different leaf-out strategies in the woody floras of North America, Europe, and East Asia. Ecol. Lett. 20, 452–460 (2017).

    Article  Google Scholar 

  11. Vitasse, Y. et al. Assessing the effects of climate change on the phenology of European temperate trees. Agric. For. Meteorol. 151, 969–980 (2011).

    Article  Google Scholar 

  12. 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 Phyt. 213, 511–524 (2017).

    Article  CAS  Google Scholar 

  13. Cooke, J. E. K., Eriksson, M. E. & Junttila, O. The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant Cell Environ. 35, 1707–1728 (2012).

    Article  CAS  Google Scholar 

  14. 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 

  15. Panchen, Z. A. et al. Substantial variation in leaf senescence times among 1360 temperate woody plant species: implications for phenology and ecosystem processes. Ann. Bot. 116, 865–873 (2015).

    Article  Google Scholar 

  16. Ghelardini, L. et al. Genetic architecture of spring and autumn phenology in Salix. BMC Plant Biology 14, 31 (2014).

    Article  Google Scholar 

  17. Harrington, R. A., Brown, B. J. & Reich, P. B. Ecophysiology of exotic and native shrubs in southern Wisconsin. 1. Relationship of leaf characteristics, resource availability, and phenology to seasonal patterns of carbon gain. Oecologia 80, 356–367 (1989).

    Article  Google Scholar 

  18. Xu, C. Y., Griffin, K. L. & Schuster, W. Leaf phenology and seasonal variation of photosynthesis of invasive Berberis thunbergii (Japanese barberry) and two co-occurring native understory shrubs in a northeastern United States deciduous forest. Oecologia 154, 11–21 (2007).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  20. Wolkovich, E. M. et al. Temperature-dependent shifts in phenology contribute to the success of exotic species with climate change. Am. J. Bot. 100, 1407–1421 (2013).

    Article  Google Scholar 

  21. Heberling, J. M., Jo, I., Kozhevnikov, A., Lee, H. & Fridley, J. D. Biotic interchange in the Anthropocene: strong asymmetry in East Asian and eastern North American plant invasions. Global Ecol. Biogeogr. 26, 447–458 (2017).

    Article  Google Scholar 

  22. Ehlers, J. & Gibbard, P. L. The extent and chronology of Cenozoic global glaciation. Quat. Int. 164–165, 6–20 (2007).

    Article  Google Scholar 

  23. Jansson, R. Global patterns in endemism explained by past climatic change. Proc. R. Soc. B 270, 583–590 (2003).

    Article  Google Scholar 

  24. Sandel, B. et al. The influence of Late Quaternary climate-change velocity on species endemism. Science 334, 660–664 (2011).

    Article  CAS  Google Scholar 

  25. Dynesius, M. & Jansson, R. Evolutionary consequences of changes in species’ geographical distributions driven by Milankovitch climate oscillations. Proc. Natl Acad. Sci. USA 97, 9115–9120 (2000).

    Article  CAS  Google Scholar 

  26. Park, T. et al. Changes in growing season duration and productivity of northern vegetation inferred from long-term remote sensing data. Environ. Res. Lett. 11, 084001 (2016).

    Article  Google Scholar 

  27. Willis, C. G. et al. Favorable climate change response explains non-native species’ success in Thoreau’s woods. PLoS ONE 5, e8878 (2010).

    Article  Google Scholar 

  28. Wolkovich, E. M. & Cleland, E. E. Phenological niches and the future of invaded ecosystems with climate change. AoB Plants 6, plu013 (2014).

    Article  Google Scholar 

  29. Augspurger, C. K., Cheeseman, J. M. & Salk, C. F. Light gains and physiological capacity of understorey woody plants during phenological avoidance of canopy shade. Funct. Ecol. 19, 537–546 (2005).

    Article  Google Scholar 

  30. Gill, D. S., Amthor, J. S. & Bormann, F. H. Leaf phenology, photosynthesis, and the persistence of saplings and shrubs in a mature northern hardwood forest. Tree Physiol. 18, 281–289 (1998).

    Article  Google Scholar 

  31. Rothstein, D. E. & Zak, D. R. Photosynthetic adaptation and acclimation to exploit seasonal periods of direct irradiance in three temperate, deciduous-forest herbs. Funct. Ecol. 15, 722–731 (2001).

    Article  Google Scholar 

  32. Ricklefs, R. E. Community diversity: relative roles of local and regional processes. Science 235, 167–171 (1987).

    Article  CAS  Google Scholar 

  33. Denny, E. G. et al. Standardized phenology monitoring methods to track plant and animal activity for science and resource management applications. Int. J. Biometeorol. 58, 591–601 (2014).

    Article  Google Scholar 

  34. Phenological Observation Guide of the International Phenological Gardens (International Phenological Gardens of Europe, Berlin, revised from original version from 1960); https://www.agrar.hu-berlin.de/en/institut-en/departments/dntw-en/agrarmet-en/phaenologie/ipg/IPG_ObsGuide.pdf

  35. Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. WorldClim high resolution global climate surfaces v.1.3. (Dryad Digital Repository, 2004); http://datadryad.org/handle/10255/dryad.12700

  36. Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).

    Article  Google Scholar 

  37. USDA, NRCS The PLANTS Database (National Plant Data Center, 2016); http://plants.usda.gov

  38. European Invasive Alien Species Gateway (DAISIE, 2016); http://www.europe-aliens.org/

  39. Mack, R. N. et al. Biotic invasions: causes, epidemiology, global consequences, and control. Ecol. Appl. 10, 689–710 (2000).

    Article  Google Scholar 

  40. Fridley, J. D. Of Asian forests and European fields: Eastern U.S. plant invasions in a global floristic context. PLoS ONE 3, e3630 (2008).

    Article  Google Scholar 

  41. Weber, E. & Gut, D. Assessing the risk of potentially invasive plant species in central Europe. J. Nat. Conserv. 12, 171–179 (2004).

    Article  Google Scholar 

  42. Nehring, S., Kowarik, I., Rabitsch, W. & Essl, F. (eds) Naturschutzfachliche Invasivitäts—Bewertungen für in Deutschland wild lebende gebietsfremde Gefäßpflanzen (Bundesamt für Naturschutz, Bonn, 2013); http://www.bfn.de

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

    Article  CAS  Google Scholar 

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

  45. Fridley, J. D. & Craddock, A. Contrasting growth phenology of native and invasive forest shrubs mediated by genome size. New Phytol. 207, 659–668 (2015).

    Article  CAS  Google Scholar 

  46. 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 

  47. Cressie, N. Spatial prediction and ordinary kriging. Math. Geol. 20, 405–421 (1988).

    Article  Google Scholar 

  48. Pebesma, E. J. Multivariable geostatistics in S: the gstat package. Comput. Geosci. 30, 683–691 (2004).

    Article  Google Scholar 

  49. R Core Team R: A language and environment for statistical computing (R Foundation for Statistical Computing, 2017); http://www.R-project.org

Download references

Acknowledgements

The study was part of the KLIMAGRAD project sponsored by the ‘Bayerisches Staatsministerium für Umwelt und Gesundheit’. We thank S. Petrone for help with the phenological observations and R. Ricklefs for comments on the manuscript.

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C.M.Z. designed the study and performed the analyses. C.M.Z. and S.S.R. co-wrote the paper.

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Correspondence to Constantin M. Zohner.

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Supplementary Information

Supplementary Figures 1–8

Supplementary Table 1

Leaf out and senescence dates at the Munich Botanical Garden in 2014 and 2015 giving each species order, family, maximum attainable growth height, and occurrence status in ENA and EU

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Zohner, C.M., Renner, S.S. Innately shorter vegetation periods in North American species explain native–non-native phenological asymmetries. Nat Ecol Evol 1, 1655–1660 (2017). https://doi.org/10.1038/s41559-017-0307-3

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