Abstract
Ongoing global warming is causing phenological shifts that affect photosynthesis and growth rates in temperate woody species. However, the effects of seasonally uneven climate warming—as is occurring in much of Europe, where the winter/spring months are warming twice as fast than the summer/autumn months—on autumn growth cessation (completion of overwintering buds) and leaf senescence, and possible carry-over effects between phenophases, remain under-investigated. We conducted experiments in which we exposed saplings of canopy and understory species to 4 °C warming in winter/spring, summer/autumn, or all year to disentangle how the timing of bud break, bud set completion, and leaf senescence is affected by seasonally uneven warming. All-year warming led to significantly delayed leaf senescence, but advanced bud set completion; summer/autumn warming only delayed leaf senescence; and winter/spring warming advanced both bud set and senescence. The non-parallel effects of warming on bud completion and leaf senescence show that leaf senescence alone is an inadequate proxy for autumn growth cessation in trees and counterintuitively suggest that continued uneven seasonal warming will advance cessation of primary growth in autumn, even when leaf senescence is delayed. Phenological responses to warming treatments (earlier spring onset, later autumn senescence) were more than twice as high in understory species than in canopy species, which can partly be explained by the absence of carry-over effects among phenophases in the former group. This underscores the need to consider differences among plant functional types when forecasting the future behaviour of ecosystems.
Similar content being viewed by others
References
Augspurger CK (2008) Early spring leaf out enhances growth and survival of saplings in a temperate deciduous forest. Oecologia 156:281–286
Augspurger CK, Bartlett EA (2003) Differences in leaf phenology between juvenile and adult trees in a temperate deciduous forest. Tree Physiol 23:517–525
Augspurger CK, Cheeseman JM, Salk CF (2005) Light gains and physiological capacity of understory woody plants during phenological avoidance of canopy shade. Funct Ecol 19:537–546
Bauerle WL, Oen R, Way DA, Qian SS, Stoy PC et al (2012) Photoperiodic regulation of the seasonal pattern of photosynthetic capacity and the implications for carbon cycling. Proc Natl Acad Sci USA 109:8612–8617
Chuine I (2010) Why does phenology drive species distribution? Philos Trans RSoc B 365:3149–3160
Cooke JEK, Eriksson ME, Junttila O (2012) The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant, Cell Environ 35:1707–1728
Delpierre N, Vitasse Y, Chuine I, Guillemot J, Bazot S, Rutishauser T, Rathgeber CBK (2016) Temperate and boreal forest tree phenology: from organ-scale processes to terrestrial ecosystem models. Ann For Sci 73:5–25
Denny EG, Gerst KL, Miller-Rushing AJ, Tierney GL, Crimmins TM et al (2014) Standardized phenology monitoring methods to track plant and animal activity for science and resource management applications. Int J Biometeorol 58:591–601
Fatichi S, Leuzinger S, Körner C (2013) Moving beyond photosynthesis: from carbon source to sink-driven vegetation modeling. New Phytol 201:1086–1095
Fridley JD (2012) Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485:359–362
Fu YH, Campioli M, Vitasse Y, De Boeck HJ, Van den Berge J (2014) Variation in leaf flushing date influences autumnal senescence and next year’s flushing date in two temperate tree species. Proc Natl Acad Sci USA 111:7355–7360
Hänninen H, Tanino K (2011) Tree seasonality in a warming climate. Trends Plant Sci 16:412–416
Heide OM (1974) Growth and dormancy in Norway spruce ecotypes. I. Interaction of photoperiod and temperature. Physiol Plant 30:1–12
Heide OM (1993a) Daylength and thermal time responses of budburst during dormancy release in some northern deciduous trees. Physiol Plant 88:531–540
Heide OM (1993b) Dormancy release in beech buds (Fagus sylvatica) requires both chilling and long days. Physiol Plant 89:187–191
Heide OM (2003) High autumn temperature delays spring bud burst in boreal trees, counterbalancing the effect of climatic warming. Tree Physiol 23:109–114
Herold A (1980) Regulation of photosynthesis by sink activity: the missing link. New Phytol 86:131–144
IPG (2016) Phenological observation guide of the International Phenological Gardens. International Phenological Gardens of Europe, Berlin, Germany. https://www.agrar.hu-berlin.de/en/institut-en/departments/dntw-en/agrarmet-en/phaenologie/ipg/IPG_ObsGuide.pdf Accessed 1 Aug 2016 (WWW document)
Jeong S-J, Ho C-H, Gim H-J, Brown ME (2011) 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
Jeong SJ, Schimel D, Frankenberg C, Drewry DT, Fisher JB (2017) Application of satellite solar-induced chlorophyll fluorescence to understanding large-scale variations in vegetation phenology and function over northern high latitude forests. Remote Sens Environ 190:178–187
Keenan TF, Richardson AD (2015) The timing of autumn senescence is affected by the timing of spring phenology: implications for predictive models. Glob Change Biol 21:2634–2641
Keenan TF, Gray J, Friedl MA, Toomey M, Bohrer G et al (2014) Net carbon uptake has increased through warming-induced changes in temperate forest phenology. Nat Clim Change 4:598–604
Körner C, Basler D, Hoch G, Kollas C, Lenz A, Randin CF, Vitasse Y, Zimmermann NE (2016) Where, why and how? Explaining the low-temperature range limits of temperate tree species. J Ecol 104:1076–1088
Lam E (2004) Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol 5:305–315
Lang GA, Eearly JD, Martin GC, Darnell RL (1987) Endo-, para-, and ecodormancy: physiological terminology and classification for dormancy research. HortSci 22:371–377
Laube J, Sparks TH, Estrella N, Höfler J, Ankerst DP, Menzel A (2014) Chilling outweighs photoperiod in preventing precocious spring development. Glob Change Biol 20:170–182
Lechowicz MJ (1984) Why do temperate deciduous trees leaf out at different times? Adaptation and ecology of forest communities. Am Nat 124:821–842
Liu Q, Fu YH, Zhu Z, Liu Y, Liu Z et al (2016) Delayed autumn phenology in the Northern Hemisphere is related to change in both climate and spring phenology. Glob Change Biol 22:3702–3711
McKown AD, Guy RD, Quamme LK (2016) Impacts of bud set and lammas phenology on root:shoot biomass partitioning and carbon gain physiology in poplar. Trees 30:2131–2141
Menzel A, Sparks TH, Estrella N, Koch E, Aasa A et al (2006) European phenological response to climate change matches the warming pattern. Glob Change Biol 12:1969–1976
Panchen ZA, Primack RB, Nordt B, Ellwood ER, Stevens A-D et al (2014) Leaf out times of temperate woody plants are related to phylogeny, deciduousness, growth habit and wood anatomy. New Phytol 203:1208–1219
Penuelas J, Filella I (2001) Responses to a warming world. Science 294:793–795
Piao SL, Ciais P, Friedlingstein P, Peylin P, Reichstein M et al (2008) Net carbon dioxide losses of northern ecosystems in response to autumn warming. Nature 451:49–52
Polgar C, Gallinat A, Primack RB (2014) Drivers of leaf-out phenology and their implications for species invasions: insights from Thoreau’s Concord. New Phytol 202:106–115
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org. Accessed 17 Jan 2018
Reich P, Walters M, Ellsworth D (1992) Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecol Monogr 62:365–392
Renner SS, Zohner CM (2018) Climate change and phenological mismatch in trophic interactions among plants, insects, and vertebrates. Annu Rev Ecol Evol Syst 11:165–182
Richardson AD, Keenan TF, Migliavacca M, Ryu Y, Sonnentag O, Toomey M (2013) Climate change, phenology, and phenological control of vegetation feedbacks to the climate system. Agric For Meteorol 169:156–173
Rohde A, Bastien C, Boerjan W (2011) Temperature signals contribute to the timing of photoperiodic growth cessation and bud set in poplar. Tree Physiol 31:472–482
Signarbieux C, Toledano E, Sanginés de Carcer P, Fu YH et al (2017) Asymmetric effects of cooler and warmer winters on beech phenology last beyond spring. Glob Change Biol. https://doi.org/10.1111/gcb.13740
Strømme CB, Julkunen-Tiitto R, Krishna U, Lavola A, Olsen JE, Nybakken L (2015) UV-B and temperature enhancement affect spring and autumn phenology in Populus tremula. Plant, Cell Environ 38:867–877
Tanino KK, Kalcsits L, Silim S, Kendall E, Gray GR (2010) Temperature-driven plasticity in growth cessation and dormancy development in deciduous woody plants: a working hypothesis suggesting how molecular and cellular function is affected by temperature during dormancy induction. Plant Mol Biol 73:49–65
Thackeray SJ, Henrys PA, Hemming D, Bell JR, Botham MS et al (2016) Phenological sensitivity to climate across taxa and trophic levels. Nature 535:241–245
Tylewicz S, Petterle A, Marttila S, Miskolczi P, Azeez A, Singh RK, Immanen J, Mähler N, Hvidsten TR, Eklund DM, Bowmann JL, Helariutta Y, Bhalerao RP (2018) Photoperiodic control of seasonal growth is mediate by ABA acting on cell-cell communication. Science 360:212–215
Vitasse Y (2013) Ontogenic changes rather than difference in temperature cause understory trees to leaf out earlier. New Phytol 198:149–155
Vitasse Y, Hoch G, Randin CF, Lenz A, Kollas C, Scheepens JF, Körner C (2013) Elevational adaptation and plasticity in seedling phenology of temperate deciduous tree species. Oecologia 171:663–678
Vitasse Y, Signarbieux C, Fu YH (2018) Global warming leads to more uniform spring phenology across elevations. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.1717342115
Zohner CM, Renner SS (2014) 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
Zohner CM, Renner SS (2017) Innately shorter vegetation periods in North American species explain native/non-native phenological asymmetries. Nat Ecol Evol. https://doi.org/10.1038/s41559-017-0307-3
Zohner CM, Benito BM, Svenning J-C, Renner SS (2016) Day length unlikely to constrain climate-driven shifts in leaf-out times of northern woody plants. Nat Clim Change 6:1120–1123
Zohner CM, Benito BM, Fridley JD, Svenning J-C, Renner SS (2017) Spring predictability explains different leaf-out strategies in the woody floras of North America, Europe, and East Asia. Ecol Lett 20:452–460
Acknowledgements
We thank V. Sebald, H. Schmitt, and M. Wenn for help with the experiments, two reviewers for their constructive comments, and the Elfriede and Franz Jakob Foundation for supporting research in the Botanical Garden Munich. This work benefitted from the sharing of expertise within the DFG priority program SPP 1991 on Taxon-Omics.
Author information
Authors and Affiliations
Contributions
CMZ designed the study and conducted the experiments and analyses. CMZ and SSR wrote the manuscript.
Corresponding author
Additional information
Communicated by Stephan Hattenschwiler.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zohner, C.M., Renner, S.S. Ongoing seasonally uneven climate warming leads to earlier autumn growth cessation in deciduous trees. Oecologia 189, 549–561 (2019). https://doi.org/10.1007/s00442-019-04339-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-019-04339-7