Abstract
The climate warming that has occurred over the past decades may benefit plant growth and development because it reduces the severity of frost events. However, these rising temperatures may also lead to diminished frost hardiness in plants due to their insufficient hardening. Despite climate warming exerting such dual effects on frost damage, how this might change the frost damage of woody plants remains unknown. Here, we conducted a laboratory experiment that used the relative electrolyte leakage method to derive species-specific model parameters for frost hardiness and a damage model. Then we simulated the daily frost hardiness and damage of five typical temperate tree species (Ulmus pumila, Robinia pseudoacacia, Fraxinus chinensis, Salix babylonica, and Armeniaca vulgaris), from 1980 to 2015, in Beijing, China. The root mean square error (RMSE) between observed and predicted frost damage ranged from 3.58% to 7.65%. According to our simulation results, frost hardiness has declined over this 36-year period due to insufficient cold hardening of plants in autumn coupled with rapid dehardening in spring; however, the percentage of frost damage incurred by the five species showed a declining trend because of the reduced frequency and intensity of frost events. Thus, decreased frost severity may, to a large extent, offset the negative effects of diminished frost hardiness such that the frost risk faced by temperate forests may well remain constant or decline with continued climate warming.
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References
Augspurger CK (2013) Reconstructing patterns of temperature, phenology, and frost damage over 124 years: spring damage risk is increasing. Ecology 94:41–50. https://doi.org/10.1890/12-0200.1
Bennie J, Kubin E, Wiltshire A, Huntley B, Baxter R (2010) Predicting spatial and temporal patterns of bud-burst and spring frost risk in north-West Europe: the implications of local adaptation to climate. Glob Chang Biol 16:1503–1514. https://doi.org/10.1111/j.1365-2486.2009.02095.x
Chmielewski FM, Gotz KP, Weber KC, Moryson S (2018) Climate change and spring frost damages for sweet cherries in Germany. Int J Biometeorol 62:217–228. https://doi.org/10.1007/s00484-017-1443-9
Chuine I (2000) A unified model for budburst of trees. J Theor Biol 207:337–347. https://doi.org/10.1006/jtbi.2000.2178
Chuine I (2010) Why does phenology drive species distribution? Philos T R Soc B 365:3149–3160. https://doi.org/10.1098/rstb.2010.0142
Chuine I, Beaubien EG (2001) Phenology is a major determinant of tree species range. Ecol Lett 4:500–510. https://doi.org/10.1046/j.1461-0248.2001.00261.x
Chuine I, Cour P, Rousseau DD (1998) Fitting models predicting dates of flowering of temperate-zone trees using simulated annealing. Plant Cell Environ 21:455–466. https://doi.org/10.1046/j.1365-3040.1998.00299.x
Delpierre N, Dufrene E, Soudani K, Ulrich E, Cecchini S, Boe J, Francois C (2009) Modelling interannual and spatial variability of leaf senescence for three deciduous tree species in France. Agric For Meteorol 149:938–948. https://doi.org/10.1016/j.agrformet.2008.11.014
Easterling D (2002) Recent changes in frost days and the frost-free season in the United States. B Am Meteorol Soc 83:1327–1332
Ge QS, Wang HJ, Dai JH (2014a) Simulating changes in the leaf unfolding time of 20 plant species in China over the twenty-first century. Int J Biometeorol 58:473–484. https://doi.org/10.1007/s00484-013-0671-x
Ge QS, Wang HJ, Zheng JY, This R, Dai JH (2014b) A 170 year spring phenology index of plants in eastern China. J Geophys Res-Biogeo 119:301–311. https://doi.org/10.1002/2013JG002565
Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annual Rev Plant Physiol Plant Mol Biol 41:187–223. https://doi.org/10.1146/annurev.pp.41.060190.001155
He Z, Du J, Chen L, Zhu X, Lin P, Zhao M, Fang S (2018) Impacts of recent climate extremes on spring phenology in arid-mountain ecosystems in China. Agric For Meteorol 260-261:31–40. https://doi.org/10.1016/j.agrformet.2018.05.022
IPCC (2018) Summary for policymakers. In: Global warming of 1.5° C. an IPCC special report on the impacts of global warming of 1.5 °C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. World Meteorological Organization, Geneva, pp 1–32. https://www.ipcc.ch/sr15/chapter/spm/
Keenan TF, Richardson AD (2015) The timing of autumn senescence is affected by the timing of spring phenology: implications for predictive models. Glob Chang Biol 21:2634–2641. https://doi.org/10.1111/gcb.12890
Kollas C, Körner C, Randin CF (2014) Spring frost and growing season length co-control the cold range limits of broad-leaved trees. J Biogeogr 41:773–783. https://doi.org/10.1111/jbi.12238
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. https://doi.org/10.1111/1365-2745.12574
Kreyling J, Schmid S, Aas G (2015) Cold tolerance of tree species is related to the climate of their native ranges. J Biogeogr 42:156–166. https://doi.org/10.1111/jbi.12411
Larcher W (2003) Physiological plant ecology. Springer, Berlin
Leinonen I (1996) A simulation model for the annual frost hardiness and freeze damage of scots pine. Ann Bot-London 78:687–693. https://doi.org/10.1006/anbo.1996.0178
Leinonen I, Repo T, Hänninen H (1996) Testing of frost hardiness models for Pinus sylvestris in natural conditions and in elevated temperature. Silva Fennica 30(2–3):159–168. https://doi.org/10.14214/sf.a9228
Leinonen I, Repo T, Hänninen H (1997) Changing environmental effects on frost hardiness of scots pine during dehardening. Ann Bot-London 79:133–138. https://doi.org/10.1006/anbo.1996.0321
Lenz A, Hoch G, Vitasse Y, Korner C (2013) European deciduous trees exhibit similar safety margins against damage by spring freeze events along elevational gradients. New Phytol 200:1166–1175. https://doi.org/10.1111/nph.12452
Lim CC, Arora R, Townsend EC (1998) Comparing Gompertz and Richards functions to estimate freezing injury in Rhododendron using electrolyte leakage. J Am Soc Hortic Sci 123:246–252. https://doi.org/10.21273/JASHS.123.2.246
Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136. https://doi.org/10.1146/annurev.arplant.57.032905.105316
Linkosalo T, Carter TR, Häkkinen R, Hari P (2000) Predicting spring phenology and frost damage risk of Betula spp. under climatic warming: a comparison of two models. Tree Physiol 20:1175–1182. https://doi.org/10.1093/treephys/20.17.1175
Ma QQ, Huang JG, Hänninen H, Berninger F (2018) Divergent trends in the risk of spring frost damage to trees in Europe with recent warming. Glob Chang Biol 25:351–360. https://doi.org/10.1111/gcb.14479
Mayoral C, Strimbeck R, Sánchez-González M, Calama R, Pardos M (2015) Dynamics of frost tolerance during regeneration in a mixed (pine–oak–juniper) Mediterranean forest. Trees 29:1893–1906. https://doi.org/10.1007/s00468-015-1270-8
Menzel A, Helm R, Zang C (2015) Patterns of late spring frost leaf damage and recovery in a European beech (Fagus sylvatica L.) stand in South-Eastern Germany based on repeated digital photographs. Front Plant Sci 6:1–13. https://doi.org/10.3389/Fpls.2015.00110
Morin X, Chuine I (2014) Will tree species experience increased frost damage due to climate change because of changes in leaf phenology? Can J For Res 44:1555–1565. https://doi.org/10.1139/cjfr-2014-0282
Morin X, Augspurger C, Chuine I (2007) Process-based modeling of species’ distributions: what limits temperate tree species’ range boundaries? Ecology 88:2280–2291. https://doi.org/10.1890/06-1591.1
Pardee GL, Inouye DW, Irwin RE (2017) Direct and indirect effects of episodic frost on plant growth and reproduction in subalpine wildflowers. Glob Chang Biol 24:848–857. https://doi.org/10.1111/gcb.13865
Pau S et al (2011) Predicting phenology by integrating ecology, evolution and climate science. Glob Chang Biol 17:3633–3643. https://doi.org/10.1111/j.1365-2486.2011.02515.x
Primack RB, Laube J, Gallinat AS, Menzel A (2015) From observations to experiments in phenology research: investigating climate change impacts on trees and shrubs using dormant twigs. Ann Bot-London 116:889–897. https://doi.org/10.1093/aob/mcv032
Quan JL (2019) Enhanced geographic information system-based mapping of local climate zones in Beijing, China. Sci China Technol Sc 62:2243–2260. https://doi.org/10.1007/s11431-018-9417-6
Repo T (1991) Rehardening potential of scots pine seedlings during dehardening. Silva Fennica 25:13–21. https://doi.org/10.14214/sf.a15591
Sakai A, Weiser CJ (1973) Freezing resistance of trees in North-America with reference to tree regions. Ecology 54:118–126. https://doi.org/10.2307/1934380
Sierra-Almeida A, Cavieres LA, Bravo LA (2018) Warmer temperatures affect the in situ freezing resistance of the Antarctic vascular plants. Front Plant Sci 9:1–13. https://doi.org/10.3389/fpls.2018.01456
Stone JM, Palta JP, Bamberg JB, Weiss LS, Harbage JF (1993) Inheritance of freezing resistance in tuber-bearing Solanum species: evidence for independent genetic control of nonacclimated freezing tolerance and cold acclimation capacity. Proc Natl Acad Sci 90:7869–7873. https://doi.org/10.1073/pnas.90.16.7869
Taiz L, Zeiger E (2006) Plant physiology, fourth edn. Sinauer Associates, Sunderland
Tao ZX, Wang HJ, Dai JH, Alatalo J, Ge QS (2018) Modeling spatiotemporal variations in leaf coloring date of three tree species across China. Agric For Meteorol 249:310–318. https://doi.org/10.1016/j.agrformet.2017.10.034
Tibbits WN, White TL, Hodge GR, Borralho NMG (2006) Genetic variation in frost resistance of Eucalyptus globulus ssp. globulus assessed by artificial freezing in winter. Aust J Bot 54:521–529. https://doi.org/10.1071/BT02061
Tudela V, Santibáñez F (2016) Modelling impact of freezing temperatures on reproductive organs of deciduous fruit trees. Agric For Meteorol 226–227:28–36. https://doi.org/10.1016/j.agrformet.2016.05.002
Vitasse Y, Lenz A, Korner C (2014) The interaction between freezing tolerance and phenology in temperate deciduous trees. Front Plant Sci 5:1–12. https://doi.org/10.3389/Fpls.2014.00541
Vitra A, Lenz A, Vitasse Y (2017) Frost hardening and dehardening potential in temperate trees from winter to budburst. New Phytol 216:113–123. https://doi.org/10.1111/nph.14698
Wan MW, Liu XZ (1979) Method of Chinese phenological observation. Science Press, Beijing
Woldendorp G, Hill MJ, Doran R, Ball MC (2008) Frost in a future climate: modelling interactive effects of warmer temperatures and rising atmospheric [CO2] on the incidence and severity of frost damage in a temperate evergreen (Eucalyptus pauciflora). Glob Chang Biol 14:294–308. https://doi.org/10.1111/j.1365-2486.2007.01499.x
Xu WH, Sun CH, Zuo JQ, Ma ZG, Li WJ, Yang S (2019) Homogenization of monthly ground surface temperature in China during 1961-2016 and performances of GLDAS reanalysis products. J Clim 32:1121–1135. https://doi.org/10.1175/Jcli-D-18-0275.1
Ye DX, Zhang Y (2008) Characteristics of frost changes from 1961 to 2007 over China (in Chinese). J Appl Meteorol Sci 19:661–665. https://doi.org/10.3969/j.issn.1001-7313.2008.06.004
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This work was supported by the National Natural Science Foundation of China [grant numbers 41901014, 41871032].
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Tao, Z., Xu, Y., Ge, Q. et al. Reduced frost hardiness in temperate woody species due to climate warming: a model-based analysis. Climatic Change 165, 35 (2021). https://doi.org/10.1007/s10584-021-03074-4
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DOI: https://doi.org/10.1007/s10584-021-03074-4