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.
This is a preview of subscription content
Subscribe to Nature+
Get immediate online access to the entire Nature family of 50+ journals
Subscribe to Journal
Get full journal access for 1 year
only $9.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Peñuelas, J. & Filella, I. Responses to a warming world. Science 294, 793–795 (2001).
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).
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).
Menzel, A. & Fabian, P. Growing season extended in Europe. Nature 397, 659 (1999).
Menzel, A. et al. European phenological response to climate change matches the warming pattern. Glob. Change Biol. 12, 1969–1976 (2006).
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).
Laube, J. et al. Chilling outweighs photoperiod in preventing precocious spring development. Glob. Change Biol. 20, 170–182 (2014).
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).
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).
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).
Vitasse, Y. et al. Assessing the effects of climate change on the phenology of European temperate trees. Agric. For. Meteorol. 151, 969–980 (2011).
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).
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).
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).
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).
Ghelardini, L. et al. Genetic architecture of spring and autumn phenology in Salix. BMC Plant Biology 14, 31 (2014).
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).
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).
Fridley, J. D. Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485, 359–362 (2012).
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).
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).
Ehlers, J. & Gibbard, P. L. The extent and chronology of Cenozoic global glaciation. Quat. Int. 164–165, 6–20 (2007).
Jansson, R. Global patterns in endemism explained by past climatic change. Proc. R. Soc. B 270, 583–590 (2003).
Sandel, B. et al. The influence of Late Quaternary climate-change velocity on species endemism. Science 334, 660–664 (2011).
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).
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).
Willis, C. G. et al. Favorable climate change response explains non-native species’ success in Thoreau’s woods. PLoS ONE 5, e8878 (2010).
Wolkovich, E. M. & Cleland, E. E. Phenological niches and the future of invaded ecosystems with climate change. AoB Plants 6, plu013 (2014).
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).
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).
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).
Ricklefs, R. E. Community diversity: relative roles of local and regional processes. Science 235, 167–171 (1987).
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).
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
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
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).
USDA, NRCS The PLANTS Database (National Plant Data Center, 2016); http://plants.usda.gov
European Invasive Alien Species Gateway (DAISIE, 2016); http://www.europe-aliens.org/
Mack, R. N. et al. Biotic invasions: causes, epidemiology, global consequences, and control. Ecol. Appl. 10, 689–710 (2000).
Fridley, J. D. Of Asian forests and European fields: Eastern U.S. plant invasions in a global floristic context. PLoS ONE 3, e3630 (2008).
Weber, E. & Gut, D. Assessing the risk of potentially invasive plant species in central Europe. J. Nat. Conserv. 12, 171–179 (2004).
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
Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877–884 (1999).
Revell, L. J. Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).
Fridley, J. D. & Craddock, A. Contrasting growth phenology of native and invasive forest shrubs mediated by genome size. New Phytol. 207, 659–668 (2015).
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).
Cressie, N. Spatial prediction and ordinary kriging. Math. Geol. 20, 405–421 (1988).
Pebesma, E. J. Multivariable geostatistics in S: the gstat package. Comput. Geosci. 30, 683–691 (2004).
R Core Team R: A language and environment for statistical computing (R Foundation for Statistical Computing, 2017); http://www.R-project.org
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.
The authors declare no competing financial interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
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
International Journal of Biometeorology (2021)
Biological Invasions (2020)
Biological Invasions (2020)
Ongoing seasonally uneven climate warming leads to earlier autumn growth cessation in deciduous trees
Light energy partitioning, photosynthetic efficiency and biomass allocation in invasive Prunus serotina and native Quercus petraea in relation to light environment, competition and allelopathy
Journal of Plant Research (2018)