Abstract
Spring leaf phenology has been intensively studied in temperate deciduous broad-leaved tree species, but the phenology of evergreen broad-leaved tree species has seldom been focused on. Evaluation of the difference in spring leaf phenology between coexisting deciduous and evergreen species is essential to predict their responses to climate change. In this study, spring leaf phenology was investigated for the 12 deciduous and 12 evergreen broad-leaved species coexisting in a warm-temperate forest in Japan, based on the predictions that selection pressure for earlier leaf production in spring results in less intraspecific variation in phenology at a given timing (SDmax) and a shorter duration of leaf expansion in deciduous than in evergreen species. In contrast to this prediction, SDmax did not differ between deciduous and evergreen species and was not related to leaf area or LMA. On the other hand, the duration of leaf expansion was longer in evergreen than in deciduous species, and was positively correlated with LMA. The leaves of greater LMA required longer periods of leaf expansion, probably due to a higher cost of and/or more conservative leaf development in the face of herbivory. As a consequence, the timing of full leaf expansion was delayed not only by later budburst (approximately two weeks) but also by a longer duration of leaf expansion (approximately two weeks) in evergreen than in deciduous broad-leaved species, which would probably influence the productivity of newly emerging leaves in spring.
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References
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
Barrett SC, Eckert CG (1990) Variation and evolution of mating systems in seed plants. In: Kawano S (ed) Biological Approaches and Evolutionary Trends in Plants. Academic Press, London, pp 229–254
Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335
Crawley M, Akhteruzzaman M (1988) Individual variation in the phenology of oak trees and its consequences for herbivorous insects Functional Ecology:409–415
Dantec CF, Ducasse H, Capdevielle X, Fabreguettes O, Delzon S, Desprez-Loustau ML (2015) Escape of spring frost and disease through phenological variations in oak populations along elevation gradients. J Ecol 103:1044–1056
Delpierre N, Guillemot J, Dufrêne E, Cecchini S, Nicolas M (2017) Tree phenological ranks repeat from year to year and correlate with growth in temperate deciduous forests. Agric For Meteorol 234:1–10
Denéchère R et al. (2019) The within-population variability of leaf spring and autumn phenology is influenced by temperature in temperate deciduous trees International Journal of Biometeorology:1–11
Flynn D, Wolkovich E (2018) Temperature and photoperiod drive spring phenology across all species in a temperate forest community. New Phytol 219:1353–1362
Grubb PJ, Thompson CL, Harper GH (2014) Why do some evergreen species keep their leaves for a second winter, while others lose them? Forests 5:2594–2612
Koike T (1990) Autumn coloring, photosynthetic performance and leaf development of deciduous broad-leaved trees in relation to forest succession Tree Physiology 7:21–32
Körner C, Basler D (2010) Phenology under global warming Science 327:1461–1462
Kursar TA, Coley PD (1992) Delayed greening in tropical leaves: an antiherbivore defense? Biotropica 24:256–262
Lenz A, Hoch G, Körner C, Vitasse Y (2016) Convergence of leaf-out towards minimum risk of freezing damage in temperate trees. Funct Ecol 30:1480–1490
Menzel A et al (2006) European phenological response to climate change matches the warming pattern. Glob Change Biol 12:1969–1976
Miyazawa S, Satomi S, Terashima I (1998) Slow leaf development of evergreen broad-leaved tree species in Japanese warm temperate forests. Ann Bot 82:859–869
Miyazawa S-I, Terashima I (2001) Slow development of leaf photosynthesis in an evergreen broad-leaved tree, Castanopsis sieboldii: relationships between leaf anatomical characteristics and photosynthetic rate. Plant, Cell Environ 24:279–291
Miyazawa Y, Kikuzawa K (2005) Winter photosynthesis by saplings of evergreen broad-leaved trees in a deciduous temperate forest. New Phytol 165:857–866
Moles AT, Westoby M (2000) Do small leaves expand faster than large leaves, and do shorter expansion times reduce herbivore damage? Oikos 90:517–524
Muffler L, Beierkuhnlein C, Aas G, Jentsch A, Schweiger AH, Zohner C, Kreyling J (2016) Distribution ranges and spring phenology explain late frost sensitivity in 170 woody plants from the Northern Hemisphere. Global Ecol Biogeography 25:1061–1071
Muller O, Hikosaka K, Hirose T (2005) Seasonal changes in light and temperate affect the balance between light harvesting and light utilisation components of photosynthesis in an evergreen understory shrub. Oecologia 143:501–508
Murray M, Cannell M, Smith R (1989) Date of budburst of fifteen tree species in Britain following climatic warming. J Appl Ecol 26:693–700
Nitta I, Ohsawa M (1997) Leaf dynamics and shoot phenology of eleven warm-temperate evergreen broad-leaved trees near their northern limit in central Japan. Plant Ecol 130:71–88
Ohsawa M (1995) Latitudinal comparison of altitudinal changes in forest structure, leaf-type, and species richness in humid monsoon. Asia Vegetatio 121:3–10
Osada N (2017) Relationships between the timing of budburst, plant traits, and distribution of 24 coexisting woody species in a warm-temperate forest in Japan. Am J Bot 104:550–558
Osada N, Hiura T (2019) Intraspecific differences in spring leaf phenology in relation to tree size in temperate deciduous trees. Tree Physiol 39:782–791
Osada N, Sugiura S, Kawamura K, Cho M, Takeda H (2003) Community-level flowering phenology and fruit set: comparative study of 25 woody species in a secondary forest in Japan. Ecol Res 18:711–723
Panchen ZA 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
Parmesan C (2006) Ecological and evolutionary responses to recent climate change Annual Review of Ecology. Evolution and Systematics 37:637–669
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42
Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60
Sestak Z, Ticha I, Catsky J, Solarova J, Pospisilova J, Hodanova D (1985) Integration of photosynthetic characteristics during leaf development. In: Sestak Z (ed) Photosynthesis during leaf development. Junk Publishers, Dordrecht, Boston, Dr. W, pp 263–286
Sugiura S (2011) Structure and dynamics of the parasitoid community shared by two herbivore species on different host plants Arthropod-Plant. Interactions 5:29–38
Sun S (2003) Leaf expansion rate, final leaf size and leaf expansion period are not necessarily correlated. Oikos 100:200–201
Vitasse Y, Fran√ßois C, Delpierre N, Dufr√™ne E, Kremer A, Chuine I, Delzon S (2011) Assessing the effects of climate change on the phenology of European temperate trees. Agric For Meteorol 151:969–980
Vitasse Y, Lenz A, Hoch G, Körner C (2014) Earlier leaf-out rather than difference in freezing resistance puts juvenile trees at greater risk of damage than adult trees. J Ecol 102:981–988
Warman L, Moles AT, Edwards W (2011) Not so simple after all: searching for ecological advantages of compound leaves. Oikos 120:813–821
Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24:2098–2100
Webb CO, Donoghue MJ (2005) Phylomatic: tree assembly for applied phylogenetics. Mol Ecol Notes 5:181–183
Wesołowski T, Rowiński P (2006) Timing of bud burst and tree-leaf development in a multispecies temperate forest. For Ecol Manage 237:387–393
Woodward F, Lomas M, Kelly C (2004) Global climate and the distribution of plant biomes Philosophical Transactions of the Royal Society of London. B: Biological Sciences 359:1465–1476
Zanne AE et al (2014) Three keys to the radiation of angiosperms into freezing environments. Nature 506:89–92
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 Nature. Clim Change 6:1120–1123
Acknowledgements
I appreciate Dr. Delpierre and an anonymous reviewer for their helpful comments. This study was partly supported by grants from the Fujiwara Natural History Public Interest Incorporated Foundation and JSPS grant (15K07465 and 19K06130).
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Communicated by Lesley Rigg.
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11258_2020_1052_MOESM1_ESM.eps
Seasonal changes in the phenological stage and standard deviation of the phenological stage (SD) of the 24 species in 2012. Dots and lines indicate the phonological stage and SD, respectively. The maximum value of SD was defined as SDmax for each species and year Supplementary file1 (EPS 2134 kb)
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Osada, N. Intraspecific variation in spring leaf phenology and duration of leaf expansion in relation to leaf habit and leaf size of temperate tree species. Plant Ecol 221, 939–950 (2020). https://doi.org/10.1007/s11258-020-01052-x
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DOI: https://doi.org/10.1007/s11258-020-01052-x