Environment-driven intraspecific variation shows coordination of functional traits of deciduous oaks among and within different biological levels

Yutong Lin1,2,3,4, Yuan Lai1,3,4, Songbo Tang1,3,4, Jeannine Cavender-Bares5, Josep Peñuelas6,7, Jordi Sardans6,7, Jianfeng Liu8, Lingling Zhang1,4, Yuanwen Kuang1,3,4()

PDF
Journal of Forestry Research ›› 2024, Vol. 35 ›› Issue (1) : 83. DOI: 10.1007/s11676-024-01721-x

Environment-driven intraspecific variation shows coordination of functional traits of deciduous oaks among and within different biological levels

  • Yutong Lin1,2,3,4, Yuan Lai1,3,4, Songbo Tang1,3,4, Jeannine Cavender-Bares5, Josep Peñuelas6,7, Jordi Sardans6,7, Jianfeng Liu8, Lingling Zhang1,4, Yuanwen Kuang1,3,4()
Author information +
History +

Abstract

Deciduous oaks (Quercus spp.) are distributed from subalpine to tropical regions in the northern hemisphere and have important roles as carbon sinks and in climate change mitigation. Determining variations in plant functional traits at multiple biological levels and linking them to environmental variables across geographical ranges is important for forecasting range-shifts of broadly-distributed species under climate change. We sampled leaves of five deciduous Quercus spp. covering approximately 20° of latitude (~ 21° N − 41° N) and 20 longitude (~ 99° E − 119° E) across China and measured 12 plant functional traits at different biological levels. The traits varied distinctively, either within each biological level or among different levels driven by climatic and edaphic variables. Traits at the organ level were significantly correlated with those at the cellular and tissue levels, while traits at the whole-plant level only correlated with those at the tissue level. The Quercus species responded to changing environments by regulating stomatal size, leaf thickness and the palisade mesophyll thickness to leaf thickness ratios with contrasting degree of effect to adjust the whole-plant functioning, i.e., intrinsic water use efficiency (iWUE), carbon supply and nitrogen availability. The results suggest that these deciduous Quercus spp. will maintain vigour by increasing iWUE when subjected to large temperature changes and insufficient moisture, and by accumulating leaf non-structural carbohydrates under drought conditions. The findings provide new insights into the inherent variation and trait coordination of widely distributed tree species in the context of climate change.

Keywords

Climate gradient / Intraspecific variation / Plant functional traits / Deciduous Quercus species / Whole-plant function

Cite this article

Download citation ▾
Yutong Lin, Yuan Lai, Songbo Tang, Jeannine Cavender-Bares, Josep Peñuelas, Jordi Sardans, Jianfeng Liu, Lingling Zhang, Yuanwen Kuang. Environment-driven intraspecific variation shows coordination of functional traits of deciduous oaks among and within different biological levels. Journal of Forestry Research, 2024, 35(1): 83 https://doi.org/10.1007/s11676-024-01721-x

References

[1]
Adams MA, Buckley TN, Turnbull TL (2020) Diminishing CO2-driven gains in water-use efficiency of global forests. Nat Clim Change 10:466–471. https://doi.org/10.1038/s41558-020-0747-7
[2]
Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30(3):258–270. https://doi.org/10.1111/j.1365-3040.2007.01641.x
[3]
Anderson DR (2008) Model based inference in the life sciences: a primer on evidence. Springer, New York
[4]
Azuma W, Ishii HR, Masaki T (2019) Height-related variations of leaf traits reflect strategies for maintaining photosynthetic and hydraulic homeostasis in mature and old Pinus densiflora trees. Oecologia 189:317–328. https://doi.org/10.1007/s00442-018-4325-x
[5]
Badano E, Guerra-Coss FA, Sanchez-Montes de Oca EJ, Briones-Herrera CI, Gelviz-Gelvez SM, Información M (2019) Climate change effects on early stages of Quercus ariifolia (Fagaceae), an endemic oak from seasonally dry forests of Mexico. Acta Bot Mex 126:1466. https://doi.org/10.21829/abm126.2019.1466
[6]
Baillie AL, Fleming AJ (2020) The developmental relationship between stomata and mesophyll airspace. New Phytol 225(3):1120–1126. https://doi.org/10.1111/nph.16341
[7]
Blonder B, Moulton DE, Blois J, Enquist BJ, Graae BJ, Macias-Fauria M, McGill B, Nogue S, Ordonez A, Sandel B, Svenning JC (2017) Predictability in community dynamics. Ecol Lett 20(3):293–306. https://doi.org/10.1111/ele.12736
[8]
Cavender-Bares J, Ramírez-Valiente JA (2017) Physiological evidence from common garden experiments for local adaptation and adaptive plasticity to climate in American live oaks (Quercus Section Virentes): implications for conservation under global change. In: Gil-Pelegrín E, Peguero-Pina J, Sancho-Knapik D (eds). Oaks Physiological Ecology. Exploring the Functional Diversity of Genus Quercus L.. Tree Physiol 7: 107?135. Springer, Cham. https://doi.org/10.1007/978-3-319-69099-5_4
[9]
Cavender-Bares J, Sack L, Savage J (2007) Atmospheric and soil drought reduce nocturnal conductance in live oaks. Tree Physiol 27(4):611–620. https://doi.org/10.1093/treephys/27.4.611
[10]
Cristiano PM, Diaz Villa MVE, De Diego MS, Lacoretz MV, Madanes N, Goldstein G (2020) Carbon assimilation, water consumption and water use efficiency under different land use types in subtropical ecosystems: from native forests to pine plantations. Agric For Meteorol 291:108094. https://doi.org/10.1016/j.agrformet.2020.108094
[11]
Dai YJ, Shen ZG, Liu Y, Wang LL, Hannaway D, Lu HF (2009) Effects of shade treatments on the photosynthetic capacity, chlorophyll fluorescence, and chlorophyll content of Tetrastigma hemsleyanum Diels et Gilg. Environ Exp Bot 65(2–3):177–182. https://doi.org/10.1016/j.envexpbot.2008.12.008
[12]
David TS, Henriques MO, Kurz-Besson C, Nunes J, Valente F, Vaz M, Pereira JS, Siegwolf R, Chaves MM, Gazarini LC, David JS (2007) Water-use strategies in two co-occurring Mediterranean evergreen oaks: surviving the summer drought. Tree Physiol 27(6):793–803. https://doi.org/10.1093/treephys/27.6.793
[13]
Ehleringer JR, Cerling TE (1995) Atmospheric CO2 and the ratio of intercellular to ambient CO2 concentrations in plants. Tree Physiol 15(2):105–111. https://doi.org/10.1093/treephys/15.2.105
[14]
Eustaquio GP, José JPP, Domingo SK (2017) Oaks and people: a long journey together. In: Eustaquio GP, José JPP, Domingo SK (eds) Oaks physiological ecology. Exploring the functional diversity of genus Quercus L. pp 1?11. Springer, Cham, Switzerland
[15]
Fang JY, Wang ZH, Tang ZY (2011) Atlas of woody plants in china: distribution and climate. Higher Education Press, Beijing, and Springer-Verlag, Berlin. https://doi.org/10.1007/978-3-642-15017-3
[16]
Farquhar GD, Oleary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9(2):121–137. https://doi.org/10.1071/PP9820121
[17]
Gitelson AA, Gritz Y, Merzlyak MN (2003) Relationships between leaf chlorophyll content and spectral reflectance and algorithms for non-destructive chlorophyll assessment in higher plant leaves. J Plant Physiol 160(3):271–282. https://doi.org/10.1078/0176-1617-00887
[18]
Hao Z, Kuang YW, Kang M (2015) Untangling the influence of phylogeny, soil and climate on leaf element concentrations in a biodiversity hotspot. Funct Ecol 29(2):165–176. https://doi.org/10.1111/1365-2435.12344
[19]
Harris I, Osborn TJ, Jones P, Lister D (2020) Version 4 of the CRU TS monthly high-resolution gridded multivariate climate dataset. Sci Data 7:109. https://doi.org/10.1038/s41597-020-0453-3
[20]
He NP, Liu CC, Piao SL, Sack L, Xu L, Luo YQ, He JS, Han XG, Zhou GS, Zhou XH, Lin Y, Yu Q, Liu SR, Sun W, Niu SL, Li SG, Zhang JH, Yu GR (2019) Ecosystem traits linking functional traits to macroecology. Trends Ecol Evol 34:200–210. https://doi.org/10.1016/j.tree.2018.11.004
[21]
He WQ, Liu H, Qi Y, Liu F, Zhu XR (2020) Patterns in nonstructural carbohydrate contents at the tree organ level in response to drought duration. Glob Change Biol 26(6):3627–3638. https://doi.org/10.1111/gcb.15078
[22]
Hovenden MJ, Leuzinger S, Newton PCD, Fletcher A, Fatichi S, Lüscher A, Reich PB, Andresen LC, Beier C, Blumenthal DM, Chiariello NR, Dukes JS, Kellner J, Hofmockel K, Niklaus PA, Song J, Wan S, Classen AT, Langley JA (2019) Globally consistent influences of seasonal precipitation limit grassland biomass response to elevated CO2. Nat Plants 5:167–173. https://doi.org/10.1038/s41477-018-0356-x
[23]
Koehler K, Center A, Cavender-Bares J (2012) Evidence for a freezing tolerance-growth rate trade-off in the live oaks (Quercus series Virentes) across the tropical-temperate divide. New Phytol 193(3):730–744. https://doi.org/10.1111/j.1469-8137.2011.03992.x
[24]
Kremer A, Abbott AG, Carlson JE, Manos PS, Plomion C, Sisco P, Staton ME, Ueno S, Vendramin GG (2012) Genomics of fagaceae. Tree Genet Genomes 8:583–610. https://doi.org/10.1007/s11295-012-0498-3
[25]
Kuglitsch FG, Reichstein M, Beer C, Carrara A, Ceulemans R, Granier A, Janssens IA, Koestner B, Lindroth A, Loustau D, Matteucci G, Montagnani L, Moors EJ, Papale D, Pilegaard K, Rambal S, Rebmann C, Schulze ED, Seufert G, Verbeeck H, Vesala T, Aubinet M, Bernhofer C, Foken T, Grünwald T, Heinesch B, Kutsch W, Laurila T, Longdoz B, Miglietta F, Sanz MJ, Valentini R (2008) Characterisation of ecosystem water-use efficiency of European forests from eddy covariance measurements. Biogeosci Discu 5:4481–4519. https://doi.org/10.5194/bgd-5-4481-2008
[26]
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) LmerTest package tests in linear mixed effects models. J Stat Softw 82(13):1–26. https://doi.org/10.18637/jss.v082.i13
[27]
Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Adv Ecol Res 34:283–362. https://doi.org/10.1016/S0065-2504(03)34004-8
[28]
Lawson T, Vialet-Chabrand S (2019) Speedy stomata, photosynthesis and plant water use efficiency. New Phytol 221(1):93–98. https://doi.org/10.1111/nph.15330
[29]
Liang XY, He PC, Liu H, Zhu SD, Uyehara IK, Hou H, Wu GL, Zhang H, You ZT, Xiao Y, Ye Q (2019) Precipitation has dominant influences on the variation of plant hydraulics of the native Castanopsis fargesii (Fagaceae) in subtropical China. Agric For Meteorol 271:83–91. https://doi.org/10.1016/j.agrformet.2019.02.043
[30]
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol 148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1
[31]
Lin YT, Kuang LH, Tang SB, Mou ZJ, Phillips OL, Lambers H, Liu ZF, Sardans J, Pe?uelas J, Lai Y, Lin MX, Chen DX, Kuang YW (2021) Leaf traits from stomata to morphology are associated with climatic and edaphic variables for dominant tropical forest evergreen oaks. J Plant Ecol 14(6):1115–1127. https://doi.org/10.1093/jpe/rtab060
[32]
Liu CC, He NP, Zhang JH, Li Y, Wang Q, Sack L, Yu GR (2018a) Variation of stomatal traits from cold temperate to tropical forests and association with water use efficiency. Funct Ecol 32(1):20–28. https://doi.org/10.1111/1365-2435.12973
[33]
Liu CC, Li Y, Xu L, Chen Z, He NP (2019) Variation in leaf morphological, stomatal, and anatomical traits and their relationships in temperate and subtropical forests. Sci Rep 9:5803. https://doi.org/10.1038/s41598-019-42335-2
[34]
Liu G (1996) Soil physical and chemical analysis and description of soil profiles. Standards Press of China, Beijing
[35]
Liu JF, Deng YP, Wang X, Ni Y, Wang Q, Xiao WF, Lei JP, Jiang ZP, Li MH (2018b) The concentrations of non-structural carbohydrates, N, and P in Quercus variablis does not decline toward its northernmost distribution range along a 1500 km transect in China. Front Plant Sci 9:1444. https://doi.org/10.3389/fpls.2018.01444
[36]
Lohbeck M, Poorter L, Lebrija-Trejos E, Nez-Ramos MM, Meave JA, Paz H, Perez-Garcia EA, Romero-Perez IE, Tauro A, Bongers F (2013) Successional changes in functional composition contrast for dry and wet tropical forest. Ecology 94(6):1211–1216. https://doi.org/10.2307/23436136
[37]
Luo DD, Wang CK, Jin Y, Li ZM, Wang ZG (2023) Different hydraulic strategies under drought stress between Fraxinus mandshurica and Larix gmelinii seedlings. J For Res 34:99–111. https://doi.org/10.1007/s11676-021-01438-1
[38]
Martínez-Sancho E, Dorado-Li?án I, Gutiérrez Merino E, Matiu M, Helle G, Heinrich I, Menzel A (2018) Increased water-use efficiency translates into contrasting growth patterns of Scots pine and sessile oak at their southern distribution limits. Glob Change Biol 24(3):1012–1028. https://doi.org/10.1111/gcb.13937
[39]
Mason RE, Craine JM, Lany NK, Jonard M, Ollinger SV, Groffman PM, Fulweiler RW, Angerer J, Read QD, Reich PB, Templer PH, Elmore AJ (2022) Evidence, causes, and consequences of declining nitrogen availability in terrestrial ecosystems. Science 376(6590):eabh3767. https://doi.org/10.1126/science.abh3767
[40]
McLauchlan KK, Gerhart LM, Battles JJ, Craine JM, Elmore AJ, Higuera PE, Mack MC, McNeil BE, Nelson DM, Pederson N, Perakis SS (2017) Centennial-scale reductions in nitrogen availability in temperate forests of the United States. Sci Rep 7:7856. https://doi.org/10.1038/s41598-017-08170-z
[41]
Mitchell PJ, O’Grady AP, Tissue DT, White DA, OtteNSChlaeger ML, Pinkard EA (2013) Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality. New Phytol 197(3):862–872. https://doi.org/10.1111/nph.12064
[42]
Mo QF, Chen YQ, Yu SQ, Fan YX, Peng ZT, Wang WJ, Li ZA, Wang FM (2020) Leaf nonstructural carbohydrate concentrations of understory woody species regulated by soil phosphorus availability in a tropical forest. Ecol Evol 10(15):8429–8438. https://doi.org/10.1002/ece3.6549
[43]
Münchinger I, Hajek P, Akdogan B, Caicoya AT, Kunert N (2023) Leaf thermal tolerance and sensitivity of temperate tree species are correlated with leaf physiological and functional drought resistance traits. J For Res 34:63–76. https://doi.org/10.1007/s11676-022-01594-y
[44]
Niinemets ü (2015) Is there a species spectrum within the world-wide leaf economics spectrum? Major variations in leaf functional traits in the Mediterranean sclerophyll Quercus ilex. New Phytol 205(1):79–96. https://doi.org/10.1111/nph.13001
[45]
Niu SL, Xing X, Zhang Z, Xia JY, Zhou XH, Song B, Li LH, Wan SQ (2011) Water-use efficiency in response to climate change: from leaf to ecosystem in a temperate steppe. Glob Change Biol 17(2):1073–1082. https://doi.org/10.1111/j.1365-2486.2010.02280.x
[46]
O’Brien MJ, Leuzinger S, Philipson CD, Tay J, Hector A (2014) Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels. Nat Clim Change 4:710–714. https://doi.org/10.1038/nclimate2281
[47]
Pantin F, Fanciullino AL, Massonnet C, Dauzat M, Simonneau T, Muller B (2013) Buffering growth variations against water deficits through timely carbon usage. Front Plant Sci 4:483. https://doi.org/10.3389/fpls.2013.00483
[48]
Pecl GT, Araujo MB, Bell JD, Blanchard J, Bonebrake TC, Chen IC, Clark TD, Colwell RK, Danielsen F, Eveng?rd B, Falconi L, Ferrier S, Frusher S, Garcia RA, Griffis RB, Hobday AJ, Janion-Scheepers C, Jarzyna MA, Jennings S, Lenoir J, Linnetved HI, Martin VY, McCormack PC, McDonald J, Mitchell NJ, Mustonen T, Pandolfi JM, Pettorelli N, Popova E, Robinson SA, Scheffers BR, Shaw JD, Sorte CJB, Strugnell JM, Sunday JM, Tuanmu MN, Vergés A, Villanueva C, Wernberg T, Wapstra E, Williams SE (2017) Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being. Science 355(6332):eaai9214. https://doi.org/10.1126/science.aai9214
[49]
Peguero-Pina JJ, Sisó S, Sancho-Knapik D, Díaz-Espejo A, Flexas J, Galmés J, Gil-Pelegrín E (2016) Leaf morphological and physiological adaptations of a deciduous oak (Quercus faginea Lam.) to the Mediterranean climate: a comparison with a closely related temperate species (Quercus robur L.). Tree Physiol 36(3):287–299. https://doi.org/10.1093/treephys/tpv107
[50]
Poorter H, Niinemets ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182(3):565–588. https://doi.org/10.1111/j.1469-8137.2009.02830.x
[51]
Qian H, Jin Y (2016) An updated megaphylogeny of plants, a tool for generating plant phylogenies and an analysis of phylogenetic community structure. J Plant Ecol 9(2):233–239. https://doi.org/10.1093/jpe/rtv047
[52]
R Core Team 2019 R: A Language and Environment for Statistical Computing (Vienna: R Foundation for Statistical Computing). https://www.R-project.org/
[53]
Ramírez-Preciado RP, Gasca-Pineda J, Arteaga MC (2019) Effects of global warming on the potential distribution ranges of six Quercus species (Fagaceae). Flora 251:32–38. https://doi.org/10.1016/j.flora.2018.12.006
[54]
Ramírez-Valiente JA, Cavender-Bares J (2017) Evolutionary trade-offs between drought resistance mechanisms across a precipitation gradient in a seasonally dry tropical oak (Quercus oleoides). Tree Physiol 37(7):889–901. https://doi.org/10.1093/treephys/tpx040
[55]
Ramírez-Valiente JA, Center A, Sparks JP, Sparks KL, Etterson JR, Longwell T, Pilz G, Cavender-Bares J (2017) Population-level differentiation in growth rates and leaf traits in seedlings of the neotropical live oak Quercus oleoides grown under natural and manipulated precipitation regimes. Front Plant Sci 8:585. https://doi.org/10.3389/fpls.2017.00585
[56]
Rigling A, Bigler C, Eilmann B, Feldmeyer-Christe E, Gimmi U, Ginzler C, Graf U, Mayer P, Vacchiano G, Weber P, Wohlgemuth T, Zweifel R, Dobbertin M (2013) Driving factors of a vegetation shift from scots pine to pubescent oak in dry alpine forests. Glob Change Biol 19(1):229–240. https://doi.org/10.1111/gcb.12038
[57]
Sack L, Cowan PD, Jaikumar N, Holbrook NM (2003) The “hydrology” of leaves: co-ordination of structure and function in temperate woody species. Plant Cell Environ 26(8):1343–1356. https://doi.org/10.1046/j.0016-8025.2003.01058.x
[58]
Sardans J, Pe?uelas J, Rodà F (2006) Plasticity of leaf morphological traits, leaf nutrient content, and water capture in the Mediterranean evergreen oak Quercus ilex subsp. ballota in response to fertilization and changes in competitive conditions. écoscience 13(2):258–270. https://doi.org/10.2980/i1195-6860-13-2-258.1
[59]
Schermelleh-Engel K, Moosbrugger H, Müller H (2003) Evaluating the fit of structural equation models: tests of significance and descriptive goodness-of-fit measures. Methods Psychol Res 8(2):23–74
[60]
Soh WK, Yiotis C, Murray M, Parnell AC, Mcelwain JC (2019) Rising CO2 drives divergence in water use efficiency of evergreen and deciduous plants. Sci Adv 5(12):eaax7906. https://doi.org/10.1126/sciadv.aax7906
[61]
Struckman S, Couture JJ, LaMar MD, Dalgleish HJ (2019) The demographic effects of functional traits: an integral projection model approach reveals population-level consequences of reproduction-defence trade-offs. Ecol Lett 22(9):1396–1406. https://doi.org/10.1111/ele.13325
[62]
Sun LK, Zhang BG, Wang B, Zhang GS, Zhang W, Zhang BL, Chang SJ, Chen T, Liu GX (2017) Leaf elemental stoichiometry of Tamarix Lour. species in relation to geographic, climatic, soil, and genetic components in China. Ecol Eng 106:448–457. https://doi.org/10.1016/j.ecoleng.2017.06.018
[63]
Tang SB, Dawson HR, Silva LCR, Pe?uelas J, Sardans J, Lambers H, Zeng FY, Lai Y, Jia YL, Zhou GY, Fang YT, Tu Y, Xi D, Zhang DX, Kuang YW (2022a) Atmospheric factors outweigh species traits and soil properties in explaining spatiotemporal variation in water-use efficiency of tropical and subtropical forest species. Agric For Meteorol 323:109056. https://doi.org/10.1016/j.agrformet.2022.109056
[64]
Tang SB, Lai Y, Tang XL, Phillips OL, Liu JF, Chen DX, Wang SL, Chen LC, Tian XJ, Kuang YW (2021) Multiple environmental factors regulate the large-scale patterns of plant water use efficiency and nitrogen availability across China’s forests. Environ Res Lett 16:034026. https://doi.org/10.1088/1748-9326/abe3bb
[65]
Tang SB, Liu JF, Gilliam FS, Hietz P, Wang ZH, Lu XK, Zeng FY, Wen DZ, Hou EQ, Lai Y, Fang YT, Tu Y, Xi D, Huang ZQ, Zhang DX, Wang R, Kuang YW (2022b) Drivers of foliar 15 N trends in southern China over the last century. Glob Change Biol 28(18):5441–5452. https://doi.org/10.1111/gcb.16285
[66]
Tang ZY, Xu WT, Zhou GY, Bai YF, Li JX, Tang XL, Chen DM, Liu Q, Ma WH, Xiong GM, He HL, He NP, Guo YP, Guo Q, Zhu JL, Han WX, Hu HF, Fang JY, Xie ZQ (2018) Patterns of plant carbon, nitrogen, and phosphorus concentration in relation to productivity in China’s terrestrial ecosystems. Proc Natl Acad Sci USA 115(16):4033–4038. https://doi.org/10.1073/pnas.1700295114
[67]
Tarin T, Nolan RH, Medlyn BE, Cleverly J, Eamus D (2020) Water-use efficiency in a semi-arid woodland with high rainfall variability. Glob Change Biol 26(2):496–508. https://doi.org/10.1111/gcb.14866
[68]
Terashima I, Hanba YT, Tholen D, Niinemets ü (2011) Leaf functional anatomy in relation to photosynthesis. Plant Physiol 155(1):108–116. https://doi.org/10.1104/pp.110.165472
[69]
Teshera-Levye J, Miles B, Terwilliger V, Lovelock CE, Cavender-Bares J (2020) Drivers of habitat partitioning among three Quercus species along a hydrologic gradient. Tree Physiol 40(2):142–157. https://doi.org/10.1093/treephys/tpz112
[70]
Tian D, Yan ZB, Ma SH, Ding YH, Luo YK, Chen YH, Du EZ, Han WX, Kovacs ED, Shen HH, Hu HF, Kattge J, Schmid B, Fang JY (2019) Family-level leaf nitrogen and phosphorus stoichiometry of global terrestrial plants. Sci China Life Sci 62:1047–1057. https://doi.org/10.1007/s11427-019-9584-1
[71]
Tian M, Yu GR, He NP, Hou JH (2016) Leaf morphological and anatomical traits from tropical to temperate coniferous forests: mechanisms and influencing factors. Sci Rep 6:19703. https://doi.org/10.1038/srep19703
[72]
Touhami I, Chirino E, Aouinti H, Khorchani AEI, Elaieb MT, Khaldi A, Nasr Z (2020) Decline and dieback of cork oak (Quercus suber L.) forests in the Mediterranean basin: a case study of Kroumirie, Northwest Tunisia. J For Res 31:1461–1477. https://doi.org/10.1007/s11676-019-00974-1
[73]
Wang LQ, Ali A (2021) Climate regulates the functional traits-aboveground biomass relationships at a community-level in forests: a global meta-analysis. Sci Total Environ 761:143238. https://doi.org/10.1016/j.scitotenv.2020.143238
[74]
Wang P, Richter AS, Kleeberg JRW, Geimer S, Grimm B (2020) Post-translational coordination of chlorophyll biosynthesis and breakdown by BCMs maintains chlorophyll homeostasis during leaf development. Nat Commun 11:1254. https://doi.org/10.1038/s41467-020-14992-9
[75]
Wang RL, Yu GR, He NP, Wang QF, Zhao N, Xu ZW (2016) Latitudinal variation of leaf morphological traits from species to communities along a forest transect in eastern China. J Geogr Sci 26:15–26. https://doi.org/10.1007/s11442-016-1251-x
[76]
Wang RZ, Huang WW, Chen L, Ma LN, Guo CY, Liu XQ (2011) Anatomical and physiological plasticity in Leymus chinensis (Poaceae) along large-scale longitudinal gradient in northeast China. PLoS ONE 6(11):e26209. https://doi.org/10.1371/journal.pone.0026209
[77]
Woolfenden HC, Baillie AL, Gray JE, Hobbs JK, Morris RJ, Fleming AJ (2018) Models and mechanisms of stomatal mechanics. Trends Plant Sci 23(9):822–832. https://doi.org/10.1016/j.tplants.2018.06.003
[78]
Wright GC, Rao RCN, Farquhar GD (1994) Water-use efficiency and carbon isotope discrimination in peanut under water deficit conditions. Crop Sci 34(1):92–97. https://doi.org/10.2135/cropsci1994.0011183X003400010016x
[79]
Yan WM, Zhong YQW, Shangguan ZP (2017) Contrasting responses of leaf stomatal characteristics to climate change: a considerable challenge to predict carbon and water cycles. Glob Change Biol 23(9):3781–3793. https://doi.org/10.1111/gcb.13654
[80]
Yu GR, Wang QF, Fang HJ (2014) Theoretical framework and research methods of the basic scientific problems of the coupled carbon-nitrogen-water cycle in terrestrial ecosystems. Quat Sci 34(4):683–698. https://doi.org/10.3969/j.issn.1001-7410.2014.04.01. (in Chinese)
[81]
Zeng ZZ, Piao SL, Li LZX, Zhou LM, Ciais P, Wang T, Li Y, Lian X, Wood EF, Friedlingstein P, Mao JF, Estes LD, Myneni RB, Peng SS, Shi XY, Seneviratne SI, Wang YP (2017) Climate mitigation from vegetation biophysical feedbacks during the past three decades. Nat Clim Change 7:432–436. https://doi.org/10.1038/nclimate3299
[82]
Zhang JH, Zhao N, Liu CC, Yang H, Li ML, Yu GR, Wilcox K, Yu Q, He NP, Niu SL (2018) C:N: P stoichiometry in China’s forests: from organs to ecosystems. Funct Ecol 32(1):50–60. https://doi.org/10.1111/1365-2435.12979
[83]
Zhou SX, Duursma RA, Medlyn BE, Kelly JWG, Prentice IC (2013) How should we model plant responses to drought? An analysis of stomatal and non-stomatal responses to water stress. Agr For Meteorol 182–183:204–214. https://doi.org/10.1016/j.agrformet.2013.05.009
[84]
Zhou ZK (1993) The fossil history of Quercus. Acta Bot Yunnanica 15(1):21–23 (in Chinese)
PDF

Accesses

Citations

Detail

Sections
Recommended

/