Skip to main content

Advertisement

Log in

Ongoing seasonally uneven climate warming leads to earlier autumn growth cessation in deciduous trees

  • Global change ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5: a
Fig. 6

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

    Article  PubMed  Google Scholar 

  • Augspurger CK, Bartlett EA (2003) Differences in leaf phenology between juvenile and adult trees in a temperate deciduous forest. Tree Physiol 23:517–525

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Chuine I (2010) Why does phenology drive species distribution? Philos Trans RSoc B 365:3149–3160

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Fatichi S, Leuzinger S, Körner C (2013) Moving beyond photosynthesis: from carbon source to sink-driven vegetation modeling. New Phytol 201:1086–1095

    Article  PubMed  CAS  Google Scholar 

  • Fridley JD (2012) Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485:359–362

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hänninen H, Tanino K (2011) Tree seasonality in a warming climate. Trends Plant Sci 16:412–416

    Article  PubMed  CAS  Google Scholar 

  • Heide OM (1974) Growth and dormancy in Norway spruce ecotypes. I. Interaction of photoperiod and temperature. Physiol Plant 30:1–12

    Article  Google Scholar 

  • Heide OM (1993a) Daylength and thermal time responses of budburst during dormancy release in some northern deciduous trees. Physiol Plant 88:531–540

    Article  PubMed  CAS  Google Scholar 

  • Heide OM (1993b) Dormancy release in beech buds (Fagus sylvatica) requires both chilling and long days. Physiol Plant 89:187–191

    Article  Google Scholar 

  • Heide OM (2003) High autumn temperature delays spring bud burst in boreal trees, counterbalancing the effect of climatic warming. Tree Physiol 23:109–114

    Article  Google Scholar 

  • Herold A (1980) Regulation of photosynthesis by sink activity: the missing link. New Phytol 86:131–144

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Lam E (2004) Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol 5:305–315

    Article  PubMed  CAS  Google Scholar 

  • Lang GA, Eearly JD, Martin GC, Darnell RL (1987) Endo-, para-, and ecodormancy: physiological terminology and classification for dormancy research. HortSci 22:371–377

    Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Penuelas J, Filella I (2001) Responses to a warming world. Science 294:793–795

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Vitasse Y (2013) Ontogenic changes rather than difference in temperature cause understory trees to leaf out earlier. New Phytol 198:149–155

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

Download references

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

Authors

Contributions

CMZ designed the study and conducted the experiments and analyses. CMZ and SSR wrote the manuscript.

Corresponding author

Correspondence to Constantin M. Zohner.

Additional information

Communicated by Stephan Hattenschwiler.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (pdf 555 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-019-04339-7

Keywords

Navigation