Abstract
Evaluating the interactions between cold requirements for leaf coloration and environmental cues is crucial for understanding the mechanisms of leaf senescence and accurately predicting autumn phenology. Based on remote sensing-derived and ground-observed leaf coloration dates for deciduous broadleaf forests during 1981–2014, we determined location-specific cold requirements for autumn leaf coloration and assessed their spatiotemporal changes. Then, we revealed the major environmental cues of cold requirements and their spatial differentiation. Results show that cold requirements have nonsignificant trends during the past decades at 57.9% of pixels. The interannual variation of cold requirements was mainly influenced by growing-season accumulated temperature (GDDgs) at 35.8% of pixels and accumulated growing season index (AGSI) at 23.2% of pixels, but less affected by leaf unfolding and low precipitation index (LPI). The increase in GDDgs or AGSI may decrease cold requirements, and vice versa. The spatial differentiations of the effects of GDDgs and AGSI depend highly on local summer temperature among climatic classifications with similar humidity conditions. Specifically, the effects of GDDgs on cold requirements concentrated in humid regions with warmer summers, while that of AGSI mainly occurred in humid and winter dry regions with cooler summers. Higher summer temperatures would strengthen the effects of GDDgs and reduce the effects of AGSI on cold requirements. These findings deepen the understanding of the influences of environmental factors on leaf senescence progress and suggest that the shifts of factors affecting cold requirements under global warming may enlarge the uncertainty in predicting autumn leaf coloration dates.
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References
Aikio S, Taulavuori K, Hurskainen S, Taulavuori E, Tuomi J (2019) Contributions of day length, temperature and individual variability on the rate and timing of leaf senescence in the common lilac Syringa vulgaris. Tree Physiol 39(6):961–970
Archetti M, Richardson AD, O'Keefe J, Delpierre N (2013) Predicting climate change impacts on the amount and duration of autumn colors in a New England forest. PLoS One 8(3):e57373
Barr AG et al (2004) Inter-annual variability in the leaf area index of a boreal aspen-hazelnut forest in relation to net ecosystem production. Agric For Meteorol 126(3-4):237–255
Barreto-Munoz A (2013) Multi-sensor vegetation index and land surface phenology earth science data records in support of global change studies: data quality challenges and data explorer system. Dissertations & Theses - Gradworks 19(1):138–154
Beil I, Kreyling J, Meyer C, Lemcke N, Malyshev AV (2021) Late to bed, late to rise-Warmer autumn temperatures delay spring phenology by delaying dormancy. Glob Chang Biol 27(22):5806–5817
Bolton D (1980) The computation of equivalent potential temperature. Mon Weather Rev 108(7):1046–1053
Busetto L et al (2010) Remote sensing of larch phenological cycle and analysis of relationships with climate in the Alpine region. Glob Chang Biol 16:2504–2517
Chen Y, Lang W, Chen X (2022) Process-based simulation of autumn phenology of trees and the regional differentiation attribution in northern China. Chin J Plant Ecol 46(7):753–765
Delpierre N et al (2009) Modelling interannual and spatial variability of leaf senescence for three deciduous tree species in France. Agric For Meteorol 149(6-7):938–948
Dragoni D et al (2011) Evidence of increased net ecosystem productivity associated with a longer vegetated season in a deciduous forest in south-central Indiana, USA. Glob Chang Biol 17(2):886–897
Dufrêne E et al (2005) Modelling carbon and water cycles in a beech forest. Ecol Model 185(2-4):407–436
Estrella N, Menzel A (2006) Responses of leaf colouring in four deciduous tree species to climate and weather in Germany. Clin Res 32(3):253–267
Forsythe WC, Rykiel EJ, Stahl RS, Wu HI, Schoolfield RM (1995) A model comparison for daylength as a function of latitude and day of year. Ecol Model 80(1):87–95
Fracheboud Y et al (2009) The control of autumn senescence in European Aspen. Plant Physiol 149(4):1982–1991
Fu Y et al (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(20):7355–7360
Fu Y et al (2015) Increased heat requirement for leaf flushing in temperate woody species over 1980-2012: effects of chilling, precipitation and insolation. Glob Chang Biol 21(7):2687–2697
Fu Y et al (2019) Nutrient availability alters the correlation between spring leaf-out and autumn leaf senescence dates. Tree Physiol 39(8):1277–1284
Ge Q, Wang H, Rutishauser T, Dai J (2015) Phenological response to climate change in China: a meta-analysis. Glob Chang Biol 21(1):265–274
Gunderson CA, O'Hara KH, Campion CM, Walker AV, Edwards NT (2010) Thermal plasticity of photosynthesis: the role of acclimation in forest responses to a warming climate. Glob Chang Biol 16(8):2272–2286
Hänninen H (1990) Modelling bud dormancy release in trees from cool and temperate regions. Acta For
Hollinger DY, Aber J, Dail B (2004) Spatial and temporal variability in forest-atmosphere CO2 exchange (vol 10, pg 1689, 2004). Glob Chang Biol 10(11):1961–1961
Huang M et al (2019) Air temperature optima of vegetation productivity across global biomes. Nat Ecol Evol 3(5):772–779
Jeong SJ, Medvigy D (2014) Macroscale prediction of autumn leaf coloration throughout the continental United States. Glob Ecol Biogeogr 23(11):1245–1254
Jeong SJ, Medvigy D, Shevliakova E, Malyshev S (2013) Predicting changes in temperate forest budburst using continental-scale observations and models. Geophys Res Lett 40(2):359–364
Jolly WM, Nemani R, Running SW (2005) A generalized, bioclimatic index to predict foliar phenology in response to climate. Glob Chang Biol 11(4):619–632
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(7):2634–2641
Keenan TF et al (2014) Net carbon uptake has increased through warming-induced changes in temperate forest phenology. Nat Clim Chang 4(7):598–604
Körner C (2013) Growth controls photosynthesis—Mostly. Nova Acta Leopoldina NF114 Nr 391:273–283
Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006) World map of the Koppen-Geiger climate classification updated. Meteorol Z 15(3):259–263
Kramer K (1994) Selecting a model to predict the onset of growth of Fagus sylvatica. J Appl Ecol 31(1):172–181
Krinner G et al (2005) A dynamic global vegetation model for studies of the coupled atmosphere-biosphere system. Glob Biogeochem Cycles 19(1):44
Lang W, Chen X, Liang L, Ren S, Qian S (2019a) Geographic and climatic attributions of autumn land surface phenology spatial patterns in the temperate deciduous broadleaf forest of China. Remote Sens 11(13):1546
Lang W, Chen X, Qian S, Liu G, Piao S (2019b) A new process-based model for predicting autumn phenology: how is leaf senescence controlled by photoperiod and temperature coupling? Agric For Meteorol 268:124–135
Leopold AC, Kriedemann PE (1975) Plant growth and development. McGraw-Hill, New York, NY, London, etc
Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136
Liu Q et al (2016) Delayed autumn phenology in the Northern Hemisphere is related to change in both climate and spring phenology. Glob Chang Biol 22(11):3702–3711
Liu G, Chen X, Zhang Q, Lang W, Delpierre N (2018) Antagonistic effects of growing season and autumn temperatures on the timing of leaf coloration in winter deciduous trees. Glob Chang Biol 24(8):3537–3545
Liu G, Chen XQ, Fu YS, Delpierre N (2019) Modelling leaf coloration dates over temperate China by considering effects of leafy season climate. Ecol Model 394:34–43
Liu F, Wang X, Wang C, Zhang Q (2021) Environmental and biotic controls on the interannual variations in CO2 fluxes of a continental monsoon temperate forest. Agric For Meteorol 296:108232
Lu, X. and Keenan, T.F., 2022. No evidence for a negative effect of growing season photosynthesis on leaf senescence timing. Glob Chang Biol, 28(9), 3083-3093.
Matos FS et al (2012) Physiological characterization of leaf senescence of Jatropha curcas L. populations. Biomass Bioenerg 45:57–64
Matsumoto K, Ohta T, Irasawa M, Nakamura T (2003) Climate change and extension of the Ginkgo biloba L. growing season in JaPEP. Glob Chang Biol 9(11):1634–1642
McAdam SAM et al (2022) An abrupt increase in foliage ABA levels on incipient leaf death occurs across vascular plants. Plant Biol 24(7):1262–1271
Menzel A (2003) Plant phenological anomalies in Germany and their relation to air temperature and NAO. Clim Chang 57(3):243–263
Menzel A, Fabian P (1999) Growing season extended in Europe. Nature 397(6721):659–659
Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp Bot 52(360):1383–1400
Pearl R (1928) The rate of living. University of London Press, London
Peñuelas J, Filella I, Comas P (2002) Changed plant and animal life cycles from 1952 to 2000 in the Mediterranean region. Glob Chang Biol 8(6):531–544
Ren S, Chen X, Lang W, Schwartz MD (2018) Climatic controls of the spatial patterns of vegetation phenology in mid-latitude grasslands of the Northern Hemisphere. J Geophys Res Biogeosci 123(8):2323–2336
Richardson AD, Bailey AS, Denny EG, Martin CW, O'Keefe J (2006) Phenology of a northern hardwood forest canopy. Glob Chang Biol 12(7):1174–1188
Richardson AD et al (2010) Influence of spring and autumn phenological transitions on forest ecosystem productivity. Philos Trans R Soc Lond B Biol Sci 365(1555):3227–3246
Richardson AD et al (2012) Terrestrial biosphere models need better representation of vegetation phenology: results from the North American Carbon Program Site Synthesis. Glob Chang Biol 18(2):566–584
Richardson AD et al (2018) Ecosystem warming extends vegetation activity but heightens vulnerability to cold temperatures. Nature 560(7718):368–371
Rosenthal SI, Camm EL (1996) Effects of air temperature, photoperiod and leaf age on foliar senescence of western larch (Larix occidentalis Nutt) in environmentally controlled chambers. Plant, Cell Environ 19(9):1057–1065
Sarmiento G, Monasterio M (1983) Life forms and phenology. In: Bourliere F (ed) Tropical Savannas. Elsevier, Amsterdam, pp 79–104
Scheftic W, Zeng XB, Broxton P, Brunke M (2014) Intercomparison of seven NDVI products over the United States and Mexico. Remote Sens 6(2):1057–1084
Vitasse Y et al (2009) Leaf phenology sensitivity to temperature in European trees: do within-species populations exhibit similar responses? Agric For Meteorol 149(5):735–744
Vitasse Y et al (2011) Assessing the effects of climate change on the phenology of European temperate trees. Agric For Meteorol 151(7):969–980
Weedon GP et al (2014) The WFDEI meteorological forcing data set: WATCH forcing data methodology applied to ERA-Interim reanalysis data. Water Resour Res 50(9):7505–7514
Worrall J (1993) Temperature effects on bud-burst and leaf-fall in subalpine larch. J Sustain For 1(2):1–18
Worrall J (1999) Phenology and the changing seasons. Nature 399(6732):101–101
Wu CY, Gough CM, Chen JM, Gonsamo A (2013) Evidence of autumn phenology control on annual net ecosystem productivity in two temperate deciduous forests. Ecol Eng 60:88–95
**e Y, Wang X, Silander JA Jr (2015) Deciduous forest responses to temperature, precipitation, and drought imply complex climate change impacts. Proc Natl Acad Sci USA 112(44):13585–13590
**e YY, Wang XJ, Wilson AM, Silander JA (2018) Predicting autumn phenology: how deciduous tree species respond to weather stressors. Agric For Meteorol 250:127–137
Yang YT, Guan HD, Shen MG, Liang W, Jiang L (2015) Changes in autumn vegetation dormancy onset date and the climate controls across temperate ecosystems in China from 1982 to 2010. Glob Chang Biol 21(2):652–665
Yin S (2012) Plant geography (in Chinese). Science Press, Bei**g, China
Yu R, Schwartz MD, Donnelly A, Liang L (2016) An observation-based progression modeling approach to spring and autumn deciduous tree phenology. Int J Biometeorol 60(3):335–349
Zani D, Crowther TW, Mo L, Renner SS, Zohner CM (2020) Increased growing-season productivity drives earlier autumn leaf senescence in temperate trees. Science (New York, N.Y.) 370(6520):1066–1071
Zhang GL, Zhang YJ, Dong JW, **ao XM (2013) Green-up dates in the Tibetan plateau have continuously advanced from 1982 to 2011. Proc Natl Acad Sci USA 110(11):4309–4314
Zheng YL, Feng YL, Lei YB, Yang CY (2009) Different photosynthetic responses to night chilling among twelve populations of Jatropha curcas. Photosynthetica 47(4):559–566
Zhou S et al (2017) Dominant role of plant physiology in trend and variability of gross primary productivity in North America. Scientific Rep 7(1):1–10
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This work was supported by the National Natural Science Foundation of China (grant numbers 41771049, 41471033).
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X.C. and W.L. designed the research; W.L. performed the analysis and wrote the draft; all the authors contributed to the interpretation of the results and the writing of the paper.
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Lang, W., Qian, S., Chen, X. et al. Spatiotemporal variation of cold requirements for leaf coloration and its environmental cues over the northern deciduous broadleaved forests. Int J Biometeorol 67, 1409–1421 (2023). https://doi.org/10.1007/s00484-023-02508-1
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DOI: https://doi.org/10.1007/s00484-023-02508-1