Leaf morphological traits: ecological function, geographic distribution and drivers

doi:10.17521/cjpe.2020.0405

Abstract

Abstract:

Leaf is one of the important organs of plants that facilitates the exchange of water and air with the surrounding environment. The morphological variation of leaves directly affect the physiological and biochemical processes of plants, which also reflects the adaptive strategies of plants to obtain resources. By focusing on several leaf morphological traits, including leaf size, leaf shape, leaf margin (with or without teeth) and leaf type (i.e. single vs. compound leaf), here, we reviewed the relevant research progresses in this field. We summarized the ecological functions of leaf morphological traits, identified their geographical distribution patterns, and explored the underlying environmental drivers, potential ecological interactions, and their effects on ecosystem functioning. We found that the current studies exploring the distribution and determinants of leaf size and leaf margin states mainly focused on single or specific taxon in local regions. Studies have also explored the genetic mechanisms of leaf morphology development. Leaf traits trade off with other functional traits, and their spatial variation is driven by both temperature and water availability. Leaf morphological traits, especially leaf size, influence water and nutrient cycling, reflect the response of communities to climate change, and can be scaled up to predict ecosystem primary productivity. Further studies should pay attention to combine new approaches to obtain unbiased data with high coverage, to explore the long-term adaptive evolution of leaf morphology, and to generalize the scaling in leaf morphology and its effect on ecosystem functioning. Leaf provides an important perspective to understand how plants respond and adapt to environmental changes. Studying leaf morphological traits provides insight into species fitness, community dynamics and ecosystem functioning, and also improves our understanding of the research progresses made in related fields, including plant community ecology and functional biogeography.

Key words: plant traits, leaf size, leaf shape, leaf type, function, environment

LI Yao-Qi, WANG Zhi-Heng. Leaf morphological traits: ecological function, geographic distribution and drivers[J]. Chin J Plant Ecol, 2021, 45(10): 1154-1172.

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URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2020.0405

https://www.plant-ecology.com/EN/Y2021/V45/I10/1154

Figures/Tables 3

Fig. 1 Leaves with varied morphology. A, Convallaria majalis, single leaf with entire margin, leaf blade elliptic to ovate-lanceolate. B, Fagus longipetiolata, single leaf with serrate margin, blade ovate to ovate-oblong. C, Capsella bursa-pastoris, basal leaves rosulate, leaf blade oblong or oblanceolate; cauline leaves amplexicaul, narrowly oblong, lanceolate, or linear, margin entire or dentate. D, Acer truncatum, single leaf, usually 5-lobed. E, Tribulus terrestris, even-pinnately compound leaf, leaflet blades oblong to obliquely oblong, margin entire. F, Metasequoia glyptostroboides, linear leaves, pinnately aligned. Hand painted by CAI Qiong (A-C, F), MAI Yi-Hui (D), and LUO Xiao-Tu (E). Leaf morphology description was obtained from eflora (http://www.efloras.org/flora_page.aspx?flora_id=2).

Fig. 2 Geographic patterns of leaf length for woody plants in China and in New World (i.e. North and South America). Modified from the appendices S1.1a & S6.1a in Li et al. (2020a). NA, not available.

Fig. 3 Percentage of species with entire-margined leaves increased with mean annual temperature in broad-leaved forests of east Asia. From left to right, the percentage of species with entire leaves increased while those with teethed leaves decreased. Fitted regression line was showed in white with R2 = 0.98. Modified from Fig. 2 & 3 in Wolfe et al. (1979).

References 165

[1]	Abrams MD (1994). Genotypic and phenotypic variation as stress adaptations in temperate tree species: a review of several case studies. Tree Physiology, 14, 833-842. PMID
[2]	Ackerly DD (2004). Adaptation, niche conservatism, and convergence: comparative studies of leaf evolution in the California chaparral. The American Naturalist, 163, 654-671. PMID
[3]	Ackerly DD, Dudley SA, Sultan SE, Schmitt J, Coleman JS, Linder CR, Sandquist DR, Geber MA, Evans AS, Dawson TE, Lechowicz MJ (2000). The evolution of plant ecophysiological traits: recent advances and future directions. Bioscience, 50, 979-995. DOI URL
[4]	Ackerly DD, Knight CA, Weiss SB, Barton K, Starmer KP (2002). Leaf size, specific leaf area and microhabitat distribution of chaparral woody plants: contrasting patterns in species level and community level analyses. Oecologia, 130, 449-457. DOI PMID
[5]	Adams JM, Green WA, Zhang Y (2008). Leaf margins and temperature in the North American flora: recalibrating the paleoclimatic thermometer. Global and Planetary Change, 60, 523-534. DOI URL
[6]	Ali S, Khan N, Xie LN (2020). Molecular and hormonal regulation of leaf morphogenesis in Arabidopsis. International Journal of Molecular Sciences, 21, 6132. DOI: 10.3390/ijms21145132. DOI URL
[7]	Bailey IW, Sinnott EW (1915). A botanical index or cretaceous and tertiary climate. Science, 41, 831-834. PMID
[8]	Bailey IW, Sinnott EW (1916). The climatic distribution of certain types of Angiosperm leaves. American Journal of Botany, 3, 24-39. DOI URL
[9]	Baker-Brosh KF, Peet RK (1997). The ecological significance of lobed and toothed leaves in temperate forest trees. Ecology, 78, 1250-1255.
[10]	Boyce CK (2005). Patterns of segregation and convergence in the evolution of fern and seed plant leaf morphologies. Paleobiology, 31, 117-140. DOI URL
[11]	Boyce CK (2009). Seeing the forest with the leaves-Clues to canopy placement from leaf fossil size and venation characteristics. Geobiology, 7, 192-199. DOI PMID
[12]	Brown VK, Lawton JH (1991). Herbivory and the evolution of leaf size and shape. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences, 333, 265-272.
[13]	Canny MJ (1990). Fine veins of dicotyledon leaves as sites for enrichment of solutes of the xylem sap. New Phytologist, 115, 511-516. DOI PMID
[14]	Chapin FS, Autumn K, Pugnaire F (1993). Evolution of suites of traits in response to environmental stress. The American Naturalist, 142, S78-S92.
[15]	Chen JM, Mo G, Pisek J, Liu J, Deng F, Ishizawa M, Chan D (2012). Effects of foliage clumping on the estimation of global terrestrial gross primary productivity. Global Biogeochemical Cycles, 26, GB1019. DOI: 10.1029/ 2010GB003996. DOI
[16]	Chen W, Su T, Adams JM, Jacques FMB, Ferguson DK, Zhou ZK (2014). Large-scale dataset from China gives new insights into leaf margin-temperature relationships. Palaeogeography, Palaeoclimatology, Palaeoecology, 402, 73-80. DOI URL
[17]	Conesa MÀ, Muir CD, Molins A, Galmés J (2020). Stomatal anatomy coordinates leaf size with Rubisco kinetics in the Balearic Limonium. AoB PLANTS, 12, plz050. DOI: 10.1093/aobpla/plz050. DOI
[18]	Corner EJ (1949). The durian theory or the origin of the modern tree. Annals of Botany, 13, 367-414. DOI URL
[19]	Cristofori V, Rouphael Y, Gyves EMD, Bignami C (2007). A simple model for estimating leaf area of hazelnut from linear measurements. Scientia Horticulturae, 113, 221-225. DOI URL
[20]	Dolph GE, Dilcher DL (1980). Variation in leaf size with respect to climate in the tropics of the Western Hemisphere. Bulletin of the Torrey Botanical Club, 107, 154-162. DOI URL
[21]	Dunn RE, Strömberg CAE, Madden RH, Kohn MJ, Carlini AA (2015). Linked canopy, climate, and faunal change in the Cenozoic of Patagonia. Science, 347, 258-261. DOI URL
[22]	Durán SM, Martin RE, Díaz S, Maitner BS, Malhi Y, Salinas N, Shenkin A, Silman MR, Wieczynski DJ, Asner GP, Bentley LP, Savage VM, Enquist BJ (2019). Informing trait-based ecology by assessing remotely sensed functional diversity across a broad tropical temperature gradient. Science Advances, 5, eaaw8114. DOI: 10.1126/sciadv. aaw8114. DOI URL
[23]	Duursma RA, Falster DS, Valladares F, Sterck FJ, Pearcy RW, Lusk CH, Sendall KM, Nordenstahl M, Houter NC, Atwell BJ, Kelly N, Kelly JWG, Liberloo M, Tissue DT, Medlyn BE, Ellsworth DS (2012). Light interception efficiency explained by two simple variables: a test using a diversity of small- to medium-sized woody plants. New Phytologist, 193, 397-408. DOI PMID
[24]	Eisenring M, Unsicker SB, Lindroth RL (2021). Spatial, genetic and biotic factors shape within-crown leaf trait variation and herbivore performance in a foundation tree species. Functional Ecology, 35, 54-66. DOI URL
[25]	Ellis B, Daly DC, Hickey LJ, Johnson KR, Mitchell JD, Wilf P, Wing SL (2009). Manual of Leaf Architecture. Cornell University Press, Ithaca, USA.
[26]	Enquist BJ, Kerkhoff AJ, Stark SC, Swenson NG, McCarthy MC, Price CA (2007). A general integrative model for scaling plant growth, carbon flux, and functional trait spectra. Nature, 449, 218-222. DOI URL
[27]	Falster DS, Westoby M (2003). Leaf size and angle vary widely across species: What consequences for light interception? New Phytologist, 158, 509-525. DOI URL
[28]	Fan X, Yan X, Qian C, Bachir DG, Yin X, Sun P, Ma XF (2020). Leaf size variations in a dominant desert shrub, Reaumuria soongarica, adapted to heterogeneous environments. Ecology and Evolution, 10, 10076-10094. DOI URL
[29]	Feild TS, Sage TL, Czerniak C, Iles WJD (2005). Hydathodal leaf teeth of Chloranthus japonicus (Chloranthaceae) prevent guttation-induced flooding of the mesophyll. Plant, Cell & Environment, 28, 1179-1190.
[30]	Fonseca CR, Overton JM, Collins B, Westoby M (2000). Shifts in trait-combinations along rainfall and phosphorus gradients. Journal of Ecology, 88, 964-977. DOI URL
[31]	Franks PJ, Farquhar GD (2007). The mechanical diversity of stomata and its significance in gas-exchange control. Plant Physiology, 143, 78-87. PMID
[32]	Fu QS, Huang XH, Shen SK, Deng T, Sun H (2021). Bibliometric analysis of the status quo of plant functional traits research based on databases across the Web of Science. Chinese Journal of Applied and Environmental Biology, 27, 228-240.
	[ 付全升, 黄先寒, 申仕康, 邓涛, 孙航 (2021). 基于数据库的植物功能性状研究现状文献计量学分析. 应用与环境生物学报, 27, 228-240.]
[33]	Gallagher RV, Falster DS, Maitner BS, Salguero-Gómez R, Vandvik V, Pearse WD, Schneider FD, Kattge J, Poelen JH, Madin JS, Ankenbrand MJ, Penone C, Feng X, Adams VM, Alroy J, et al. (2020). Open Science principles for accelerating trait-based science across the Tree of Life. Nature Ecology & Evolution, 4, 294-303.
[34]	Gates DM (1980). Biophysical Ecology. Springer, New York, USA.
[35]	Geng Y, Ma W, Wang L, Baumann F, Kühn P, Scholten T, He JS (2017). Linking above- and belowground traits to soil and climate variables: an integrated database on China’s grassland species. Ecology, 98, 1471-1471.
[36]	Givnish T (1984). Leaf and Canopy Adaptations in Tropical Forests. Springer, Dordrecht, the Netherlands. 51-84.
[37]	Givnish TJ (1978a). Ecological aspects of plant morphology: leaf form in relation to environment. Acta Biotheoretica, 27, 83-142.
[38]	Givnish TJ (1978b). On the Adaptive Significance of Compound Leaves, With Particular Reference to Tropical Trees. Cambridge University Press, Cambridge, UK.
[39]	Givnish TJ, Vermeij GJ (1976). Sizes and shapes of liane leaves. The American Naturalist, 110, 743-778. DOI URL
[40]	Glukhov AZ, Strelnikov II (2014). Lamina shape variability in species of the genus Ficus L. in different ecological conditions. Contemporary Problems of Ecology, 7, 210-220. DOI URL
[41]	Gower ST, Kucharik CJ, Norman JM (1999). Direct and indirect estimation of leaf area index, fAPAR, and net primary production of terrestrial ecosystems. Remote Sensing of Environment, 70, 29-51. DOI URL
[42]	Greenwood DR (1992). Taphonomic constraints on foliar physiognomic interpretations of late Cretaceous and Tertiary Paleoclimates. Review of Palaeobotany and Palynology, 71, 149-190. DOI URL
[43]	Greenwood DR (2005). Leaf margin analysis: taphonomic constraints. Palaios, 20, 498-505. DOI URL
[44]	Greenwood DR, Wilf P, Wing SL, Christophel DC (2004). Paleotemperature estimation using leaf-margin analysis: Is Australia different? Palaios, 19, 129-142. DOI URL
[45]	Gregory-Wodzicki KM (2000). Relationships between leaf morphology and climate, Bolivia: implications for estimating paleoclimate from fossil floras. Paleobiology, 26, 668-688. DOI URL
[46]	Guerin GR, Wen H, Lowe AJ (2012). Leaf morphology shift linked to climate change. Biology Letters, 8, 882-886. DOI PMID
[47]	He L, Liu Y, He H, Liu Y, Qi J, Zhang X, Li Y, Mao Y, Zhou S, Zheng X, Bai Q, Zhao B, Wang D, Wen J, Mysore KS, et al. (2020). A molecular framework underlying the compound leaf pattern of Medicago truncatula. Nature Plants, 6, 511-521. DOI URL
[48]	He N, Liu C, Tian M, Li M, Yang H, Yu G, Guo D, Smith MD, Yu Q, Hou J (2018). Variation in leaf anatomical traits from tropical to cold-temperate forests and linkage to ecosystem functions. Functional Ecology, 32, 10-19. DOI URL
[49]	Heberling JM, Mason NWH (2018). Are endemics functionally distinct? Leaf traits of native and exotic woody species in a New Zealand forest. PLOS ONE, 13, e0196746. DOI: 10.1371/journal.pone.0196746. DOI URL
[50]	Hickey LJ (1973). Classification of the architecture of dicotyledonous leaves. American Journal of Botany, 17-33.
[51]	Higuchi Y, Kawakita A (2019). Leaf shape deters plant processing by an herbivorous weevil. Nature Plants, 5, 959-964. DOI PMID
[52]	Hirokazu T (2005). Leaf shape: genetic controls and environmental factors. International Journal of Developmental Biology, 49, 547-555. PMID
[53]	Hodgson JG, Santini BA, Montserrat Marti G, Royo Pla F, Jones G, Bogaard A, Charles M, Font X, Ater M, Taleb A, Poschlod P, Hmimsa Y, Palmer C, Wilson PJ, Band SR, et al. (2017). Trade-offs between seed and leaf size (seed-phytomer-leaf theory): functional glue linking regenerative with life history strategies … and taxonomy with ecology? Annals of Botany, 120, 633-652. DOI PMID
[54]	Huang Y, Lechowicz MJ, Price CA, Li L, Wang Y, Zhou D (2016). The underlying basis for the trade-off between leaf size and leafing intensity. Functional Ecology, 30, 199-205. DOI URL
[55]	Huff PM, Wilf P, Azumah EJ (2003). Digital future for paleoclimate estimation from fossil leaves? Preliminary results. Palaios, 18, 266-274. DOI URL
[56]	Jacobs BF (1999). Estimation of rainfall variables from leaf characters in tropical Africa. Palaeogeography, Palaeoclimatology, Palaeoecology, 145, 231-250. DOI URL
[57]	Jahdi R, Arabi M, Bussotti F (2020). Effect of environmental gradients on leaf morphological traits in the Fandoghlo forest region (NW Iran). iForest, 13, 523-530. DOI URL
[58]	Jetz W, Cavender-Bares J, Pavlick R, Schimel D, Davis FW, Asner GP, Guralnick R, Kattge J, Latimer AM, Moorcroft P, Schaepman ME, Schildhauer MP, Schneider FD, Schrodt F, Stahl U, Ustin SL (2016). Monitoring plant functional diversity from space. Nature Plants, 2, 16024. DOI: 10.1038/nplants.2016.24. DOI URL
[59]	Jin MR, Yuan H, Huang DZ (2020). Sdudy on digital classification of plants based on characteristics of leaf shape and leaf vein. Forestry and Ecological Sciences, 35, 112-118.
	[ 金梦然, 袁航, 黄大庄 (2020). 基于叶形和叶脉特征的植物数字化分类研究. 林业与生态科学, 35, 112-118.]
[60]	Jordan GJ (1997). Uncertainty in palaeoclimatic reconstructions based on leaf physiognomy. Australian Journal of Botany, 45, 527-547. DOI URL
[61]	Jordan GJ (2011). A critical framework for the assessment of biological palaeoproxies: predicting past climate and levels of atmospheric CO₂ from fossil leaves. New Phytologist, 192, 29-44. DOI URL
[62]	Kattge J, Diaz S, Lavorel S, Prentice C, Leadley P, Boenisch G, Garnier E, Westoby M, Reich PB, Wright IJ, Cornelissen JHC, Violle C, Harrison SP, van Bodegom PM, Reichstein M, et al. (2011). TRY-A global database of plant traits. Global Change Biology, 17, 2905-2935.
[63]	Kawai K, Okada N (2016). How are leaf mechanical properties and water-use traits coordinated by vein traits? A case study in Fagaceae. Functional Ecology, 30, 527-536. DOI URL
[64]	Kleiman D, Aarssen LW (2007). The leaf size/number trade-off in trees. Journal of Ecology, 95, 376-382. DOI URL
[65]	Koch G, Rolland G, Dauzat M, Bédiée A, Baldazzi V, Bertin N, Guédon Y, Granier C (2018). Are compound leaves more complex than simple ones? A multi-scale analysis. Annals of Botany, 122, 1173-1185. DOI URL
[66]	Kowalski EA (2002). Mean annual temperature estimation based on leaf morphology: a test from tropical South America. Palaeogeography, Palaeoclimatology, Palaeo- ecology, 188, 141-165.
[67]	Leigh A, Sevanto S, Close JD, Nicotra AB (2017). The influence of leaf size and shape on leaf thermal dynamics: Does theory hold up under natural conditions? Plant, Cell & Environment, 40, 237-248.
[68]	Li FL, Bao WK (2014). Elevational trends in leaf size of Campylotropis polyantha in the arid Minjiang River valley, SW China. Journal of Arid Environments, 108, 1-9. DOI URL
[69]	Li XY, Ralf MX, Shahid K, Zheng YC, Li YH, Xing Q (2019). Development of plant leaf margin: advances in research. Chinese Agricultural Science Bulletin, 35, 50-56.
	[ 李晓屿, Ralf Müller-Xing, Shahid Khan, 郑玉彩, 李玉花, 邢倩 (2019). 植物叶缘锯齿发育的研究进展. 中国农学通报, 35, 50-56.]
[70]	Li YQ, Reich PB, Schmid B, Shrestha N, Feng X, Lyu T, Maitner BS, Xu XT, Li YC, Zou DT, Tan ZH, Su XY, Tang ZY, Guo QH, Feng XJ, et al. (2020a). Leaf size of woody dicots predicts ecosystem primary productivity. Ecology Letters, 23, 1003-1013. DOI URL
[71]	Li YQ, Wang ZH, Xu XT, Han WX, Wang QG, Zou DT (2016). Leaf margin analysis of Chinese woody plants and the constraints on its application to palaeoclimatic reconstruction. Global Ecology and Biogeography, 25, 1401-1415. DOI URL
[72]	Li YQ, Zou DT, Shrestha N, Xu XT, Wang QG, Jia W, Wang ZH (2020b). Spatiotemporal variation in leaf size and shape in response to climate. Journal of Plant Ecology, 13, 87-96. DOI URL
[73]	Little SA, Kembel SW, Wilf P (2010). Paleotemperature proxies from leaf fossils reinterpreted in light of evolutionary history. PLOS ONE, 5, e15161. DOI: 10.1371/journal. pone.0015161. DOI URL
[74]	Liu H, Liu G, Xing W (2021). Functional traits of submerged macrophytes in eutrophic shallow lakes affect their ecological functions. Science of the Total Environment, 760, 143332. DOI: 10.1016/j.scitotenv.2020.143332. DOI URL
[75]	Liu WS, Zheng L, Qi DH (2020). Variation in leaf traits at different altitudes reflects the adaptive strategy of plants to environmental changes. Ecology and Evolution, 10, 8166-8175. DOI URL
[76]	Lusk CH, Grierson ERP, Laughlin DC (2019). Large leaves in warm, moist environments confer an advantage in seedling light interception efficiency. New Phytologist, 223, 1319- 1327. DOI URL
[77]	Ma X, Mahecha MD, Migliavacca M, van der Plas F, Benavides R, Ratcliffe S, Kattge J, Richter R, Musavi T, Baeten L, Barnoaiea I, Bohn FJ, Bouriaud O, Bussotti F, Coppi A, et al. (2019). Inferring plant functional diversity from space: the potential of Sentinel-2. Remote Sensing of Environment, 233, 111368. DOI: 10.1016/j.rse.2019.111368. DOI URL
[78]	Maitner BS, Boyle B, Casler N, Condit R, Donoghue J, Durán SM, Guaderrama D, Hinchliff CE, Jørgensen PM, Kraft NJB, McGill B, Merow C, Morueta-Holme N, Peet RK, Sandel B, et al. (2018). The bien R package: a tool to access the Botanical Information and Ecology Network (BIEN) database. Methods in Ecology and Evolution, 9, 373-379.
[79]	Malhado A, Whittaker RJ, Malhi Y, Ladle RJ, Ter Steege H, Phillips O, Aragão L, Baker TR, Arroyo L, Almeida S (2010). Are compound leaves an adaptation to seasonal drought or to rapid growth? Evidence from the Amazon rain forest. Global Ecology and Biogeography, 19, 852- 862. DOI URL
[80]	Malhado ACM, Malhi Y, Whittaker RJ, Ladle RJ ter Steege H, Phillips OL, Butt N, Aragao L, Quesada CA, Araujo- Murakami A, Arroyo L, Peacock J, Lopez-Gonzalez G, Baker TR, Anderson LO, et al. (2009). Spatial trends in leaf size of Amazonian rainforest trees. Biogeosciences, 6, 1563-1576. DOI URL
[81]	Mathakutha R, Steyn C le Roux PC, Blom IJ, Chown SL, Daru BH, Ripley BS, Louw A, Greve M (2019). Invasive species differ in key functional traits from native and non- invasive alien plant species. Journal of Vegetation Science, 30, 994-1006. DOI
[82]	McDonald PG, Fonseca CR, Overton JM, Westoby M (2003). Leaf-size divergence along rainfall and soil-nutrient gradients: Is the method of size reduction common among clades? Functional Ecology, 17, 50-57. DOI URL
[83]	Mebrahtu T, Hanover JW, Layne DR, Flore JA (1991). Leaf temperature effects on net photosynthesis, dark respiration, and photorespiration of seedlings of black locust families with contrasting growth-rates. Canadian Journal of Forest Research, 21, 1616-1621. DOI URL
[84]	Messier J, McGill BJ, Enquist BJ, Lechowicz MJ (2017). Trait variation and integration across scales: Is the leaf economic spectrum present at local scales? Ecography, 40, 685-697. DOI URL
[85]	Michaletz ST, Weiser MD, McDowell NG, Zhou J, Kaspari M, Helliker BR, Enquist BJ (2016). The energetic and carbon economic origins of leaf thermoregulation. Nature Plants, 2, 16129. DOI: 10.1038/nplants.2016.129. DOI PMID
[86]	Milla R, Reich PB (2007). The scaling of leaf area and mass: the cost of light interception increases with leaf size. Proceedings of the Royal Society B: Biological Sciences, 274, 2109-2115. DOI URL
[87]	Milla R, Reich PB (2011). Multi-trait interactions, not phylogeny, fine-tune leaf size reduction with increasing altitude. Annals of Botany, 107, 455-465. DOI URL
[88]	Moles AT, Perkins SE, Laffan SW, Flores-Moreno H, Awasthy M, Tindall ML, Sack L, Pitman A, Kattge J, Aarssen LW, Anand M, Bahn M, Blonder B, Cavender-Bares J, Cornelissen JHC, et al. (2014). Which is a better predictor of plant traits: temperature or precipitation? Journal of Vegetation Science, 25, 1167-1180. DOI URL
[89]	Nardini A, Unapuu-Pikas E, Savi T (2014). When smaller is better: leaf hydraulic conductance and drought vulnerability correlate to leaf size and venation density across four Coffea arabica genotypes. Functional Plant Biology, 41, 972-982. DOI PMID
[90]	Nicotra AB, Leigh A, Boyce CK, Jones CS, Niklas KJ, Royer DL, Tsukaya H (2011). The evolution and functional significance of leaf shape in the angiosperms. Functional Plant Biology, 38, 535-552. DOI URL
[91]	Niinemets Ü (1998). Are compound-leaved woody species inherently shade-intolerant? An analysis of species ecological requirements and foliar support costs. Plant Ecology, 134, 1-11. DOI URL
[92]	Niinemets Ü (2001). Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology, 82, 453-469. DOI URL
[93]	Niinemets Ü, Portsmuth A, Tena D, Tobias M, Matesanz S, Valladares F (2007). Do we underestimate the importance of leaf size in plant economics? Disproportional scaling of support costs within the spectrum of leaf physiognomy. Annals of Botany, 100, 283-303. PMID
[94]	Niinemets Ü, Portsmuth A, Tobias M (2006). Leaf size modifies support biomass distribution among stems, petioles and mid-ribs in temperate plants. New Phytologist, 171, 91-104. PMID
[95]	Niinemets Ü, Sparrow A, Cescatti A (2005). Light capture efficiency decreases with increasing tree age and size in the southern hemisphere gymnosperm Agathis australis. Trees, 19, 177-190. DOI URL
[96]	Niklas KJ, Cobb ED, Niinemets Ü, Reich PB, Sellin A, Shipley B, Wright IJ (2007). “Diminishing returns” in the scaling of functional leaf traits across and within species groups. Proceedings of the National Academy of Sciences of the United States of America, 104, 8891-8896. PMID
[97]	Nobel PS (2009). Physicochemical and Environmental Plant Physiology. 4th ed. Academic Press, San Diego, USA. 318-363.
[98]	Okajima Y, Taneda H, Noguchi K, Terashima I (2012). Optimum leaf size predicted by a novel leaf energy balance model incorporating dependencies of photosynthesis on light and temperature. Ecological Research, 27, 333-346. DOI URL
[99]	Ordoñez JC, van Bodegom PM, Witte JPM, Wright IJ, Reich PB, Aerts R (2009). A global study of relationships between leaf traits, climate and soil measures of nutrient fertility. Global Ecology and Biogeography, 18, 137-149. DOI URL
[100]	Parkhurst DF, Loucks OL (1972). Optimal leaf size in relation to environment. Journal of Ecology, 60, 505-537. DOI URL
[101]	Peel JR, Sanchez MCM, Portillo JL, Golubov J (2017). Stomatal density, leaf area and plant size variation of Rhizophora mangle (Malpighiales:Rhizophoraceae) along a salinity gradient in the Mexican Caribbean. Revista de Biologia Tropical, 65, 701-712.
[102]	Peijian S, Kexin Y, Ülo N, Johan G (2021). Can leaf shape be represented by the ratio of leaf width to length? Evidence from nine species of Magnolia and Michelia (Magnoliaceae). Forests, 12, 41. DOI: 10.3390/f12010041. DOI URL
[103]	Peppe DJ, Lemons CR, Royer DL, Wing SL, Wright IJ, Lusk CH, Rhoden CH (2014). Biomechanical and leaf-climate relationships: a comparison of ferns and seed plants. American Journal of Botany, 101, 338-347. DOI URL
[104]	Peppe DJ, Royer DL, Cariglino B, Oliver SY, Newman S, Leight E, Enikolopov G, Fernandez-Burgos M, Herrera F, Adams JM, Correa E, Currano ED, Erickson JM, Hinojosa LF, Hoganson JW, et al. (2011). Sensitivity of leaf size and shape to climate: global patterns and paleoclimatic applications. New Phytologist, 190, 724-739. DOI URL
[105]	Poorter L, Rozendaal DM (2008). Leaf size and leaf display of thirty-eight tropical tree species. Oecologia, 158, 35-46. DOI URL
[106]	Pray TR (1955). Foliar venation of angiosperms. II. Histogenesis of the venation of Liriodendron. American Journal of Botany, 42, 18-27. DOI URL
[107]	Price CA, Wing S, Weitz JS (2012). Scaling and structure of dicotyledonous leaf venation networks. Ecology Letters, 15, 87-95. DOI URL
[108]	Pyakurel A, Wang JR (2014). Leaf morphological and stomatal variations in paper birch populations along environmental gradients in Canada. American Journal of Plant Sciences, 5, 1508-1520. DOI URL
[109]	Reich PB (2012). Key canopy traits drive forest productivity. Proceedings of the Royal Society B: Biological Sciences, 279, 2128-2134. DOI URL
[110]	Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleksyn J, Westoby M, Walters MB (2003). The evolution of plant functional variation: traits, spectra, and strategies. International Journal of Plant Sciences, 164, S143-S164.
[111]	Ren JS, Ji XY, Wang CH, Hu JJ, Nervo SE, Li JH (2020). Variation and genetic parameters of leaf morphological traits of eight families from Populus simonii × P. nigra. Forests, 11, 1319. DOI: 10.3390/f11121319. DOI URL
[112]	Renaguli R, Liu SZ, Liu TQ, Chen BZ, Wang JS (2020). Survey of plant leaf area measurement methods. Anhui Agricultural Science Bulletin, 26, 22-23.
	[ 热娜古丽•热西提,刘生智, 刘同金, 陈炳舟, 王家硕 (2020). 植物叶面积测量方法综述. 安徽农学通报, 26, 22-23.]
[113]	Rollet B (1990). Leaf morphology//Rollet B, Högermannc, Roth I. Stratification of Tropical Forests as Seen in Leaf Structure. Springer, Dordrecht, the Netherlands. 1-75.
[114]	Rouphael Y, Mouneimne AH, Ismail A, Mendoza-De Gyves E, Rivera CM, Colla G (2010). Modeling individual leaf area of rose (Rosa hybrida L.) based on leaf length and width measurement. Photosynthetica, 48, 9-15. DOI URL
[115]	Royer DL, Kooyman RM, Little SA, Wilf P (2009a). Ecology of leaf teeth: a multi-site analysis from an Australian subtropical rainforest. American Journal of Botany, 96, 738-750. DOI URL
[116]	Royer DL, Meyerson LA, Robertson KM, Adams JM (2009b). Phenotypic plasticity of leaf shape along a temperature gradient in Acer rubrum. PLOS ONE, 4, e7653. DOI: 10.1371/journal.pone.0007653. DOI URL
[117]	Royer DL, Peppe DJ, Wheeler EA, Niinemets Ü (2012). Roles of climate and functional traits in controlling toothed vs. untoothed leaf margins. American Journal of Botany, 99, 915-922. DOI PMID
[118]	Royer DL, Wilf P (2006). Why do toothed leaves correlate with cold climates? Gas exchange at leaf margins provides new insights into a classic paleotemperature proxy. International Journal of Plant Sciences, 167, 11-18. DOI URL
[119]	Royer DL, Wilf P, Janesko DA, Kowalski EA, Dilcher DL (2005). Correlations of climate and plant ecology to leaf size and shape: potential proxies for the fossil record. American Journal of Botany, 92, 1141-1151. DOI PMID
[120]	Runions A, Tsiantis M, Prusinkiewicz P (2017). A common developmental program can produce diverse leaf shapes. New Phytologist, 216, 401-418. DOI PMID
[121]	Sack L, Scoffoni C, McKown AD, Frole K, Rawls M, Havran JC, Tran H, Tran T (2012). Developmentally based scaling of leaf venation architecture explains global ecological patterns. Nature Communications, 3, 837. DOI: 10.1038/ ncomms1835. DOI URL
[122]	Salisbury EJ, Oliver FW (1928). On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora. Philosophical Transactions of the Royal Society of London: Series B, 216, 1-65.
[123]	Schellenberger Costa D, Zotz G, Hemp A, Kleyer M (2018). Trait patterns of epiphytes compared to other plant life-forms along a tropical elevation gradient. Functional Ecology, 32, 2073-2084. DOI URL
[124]	Schmerler SB, Clement WL, Beaulieu JM, Chatelet DS, Sack L, Donoghue MJ, Edwards EJ (2012). Evolution of leaf form correlates with tropical-temperate transitions in Viburnum (Adoxaceae). Proceedings of the Royal Society B: Biological Sciences, 279, 3905-3913. DOI URL
[125]	Schneider JV, Habersetzer J, Rabenstein R, Wesenberg J, Wesche K, Zizka G (2017). Water supply and demand remain coordinated during breakdown of the global scaling relationship between leaf size and major vein density. New Phytologist, 214, 473-486. DOI PMID
[126]	Schuepp PH (1993). Leaf boundary layers. New Phytologist, 125, 477-507. DOI PMID
[127]	Scoffoni C, Rawls M, McKown A, Cochard H, Sack L (2011). Decline of leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture. Plant Physiology, 156, 832-843. DOI URL
[128]	Smith DD, Sperry JS, Adler FR (2017). Convergence in leaf size versus twig leaf area scaling: Do plants optimize leaf area partitioning? Annals of Botany, 119, 447-456. DOI URL
[129]	Stowe LG, Brown JL (1981). A geographic perspective on the ecology of compound leaves. Evolution, 35, 818-821. DOI URL
[130]	Su T, Xing YW, Liu YSC, Jacques FM, Chen WY, Huang YJ, Zhou ZK (2010). Leaf margin analysis: a new equation from humid to mesic forests in China. Palaios, 25, 234-238. DOI URL
[131]	Tao Q, Guo DS, Wei BY, Zhang F, Pang CX, Jiang H, Zhang JZ, Wei T, Gu HY, Qu LJ, Qin GJ (2013). The TIE1 transcriptional repressor links TCP transcription factors with TOPLESS/TOPLESS-RELATED corepressors and modulates leaf development in Arabidopsis. Plant Cell, 25, 421-437. DOI URL
[132]	Terashima I, Hikosaka K (1995). Comparative ecophysiology of leaf and canopy photosynthesis. Plant, Cell & Environment, 18, 1111-1128.
[133]	Tian M, Yu G, He N, Hou J (2016). Leaf morphological and anatomical traits from tropical to temperate coniferous forests: mechanisms and influencing factors. Scientific Reports, 6, 19703. DOI: 10.1038/srep19703. DOI URL
[134]	Traiser C, Klotz S, Uhl D, Mosbrugger V (2005). Environmental signals from leaves-A physiognomic analysis of European vegetation. New Phytologist, 166, 465-484. DOI URL
[135]	Turner IM (2001). The Ecology of Trees in the Tropical Rain Forest. Cambridge University Press, Cambridge, UK.
[136]	Vendramini F, Díaz S, Gurvich DE, Wilson PJ, Thompson K, Hodgson JG (2002). Leaf traits as indicators of resource-use strategy in floras with succulent species. New Phytologist, 154, 147-157. DOI URL
[137]	Wang C, He J, Zhao TH, Cao Y, Wang G, Sun B, Yan X, Guo W, Li MH (2019). The smaller the leaf is, the faster the leaf water loses in a temperate forest. Frontiers in Plant Science, 10, 58. DOI: 10.3389/fpls.2019.00058. DOI URL
[138]	Wang H, Harrison SP, Prentice IC, Yang Y, Bai F, Togashi HF, Wang M, Zhou S, Ni J (2018). The China Plant Trait Database: toward a comprehensive regional compilation of functional traits for land plants. Ecology, 99, 500. DOI PMID
[139]	Warman L, Moles AT, Edwards W (2011). Not so simple after all: searching for ecological advantages of compound leaves. Oikos, 120, 813-821. DOI URL
[140]	Webb LJ (1959). A physiognomic classification of Australian rain forests. Journal of Ecology, 47, 551-570. DOI URL
[141]	Werger MJA, Ellenbroek GA (1978). Leaf size and leaf consistence of a riverine forest formation along a climatic gradient. Oecologia, 34, 297-308. DOI PMID
[142]	Whitman T, Aarssen LW (2009). The leaf size/number trade-off in herbaceous angiosperms. Journal of Plant Ecology, 3, 49-58. DOI URL
[143]	Wiemann MC, Manchester SR, Dilcher DL, Hinojosa LF, Wheeler EA (1998). Estimation of temperature and precipitation from morphological characters of dicotyledonous leaves. American Journal of Botany, 85, 1796-1802. PMID
[144]	Wilf P (1997). When are leaves good thermometers? A new case for leaf margin analysis. Paleobiology, 23, 373-390. DOI URL
[145]	Wilf P, Wing SL, Greenwood DR, Greenwood CL (1998). Using fossil leaves as paleoprecipitation indicators: an Eocene example. Geology, 26, 203-206. DOI URL
[146]	Wilf P, Zhang SP, Chikkerur S, Little SA, Wing SL, Serre T (2016). Computer vision cracks the leaf code. Proceedings of the National Academy of Sciences of the United States of America, 113, 3305-3310.
[147]	Williams LJ, Cavender-Bares J, Paquette A, Messier C, Reich PB (2020). Light mediates the relationship between community diversity and trait plasticity in functionally and phylogenetically diverse tree mixtures. Journal of Ecology, 108, 1617-1634. DOI URL
[148]	Wolfe JA (1979). Temperature Parameters of Humid to Mesic Forests of Eastern Asia and Relation to Forests of Other Regions of the Northern Hemisphere and Australasia: Analysis of Temperature Data from More Than 400 Stations in Eastern Asia. United States Department Printing Office, Washington D.C.
[149]	Wolfe JA (1993). A Method of Obtaining Climatic Parameters from Leaf Assemblages. United States Government Printing Office, Washington D.C.
[150]	Wolfe JA (1995). Paleoclimatic estimates from Tertiary leaf assemblages. Annual Review of Earth and Planetary Sciences, 23, 119-142. DOI URL
[151]	Wolfe JA, Uemura K, Wilf P, Wing SL, Greenwood DR, Greenwood CL (1999). Using fossil leaves as paleoprecipitation indicators: an Eocene example: comment and reply. Geology, 27, 91-92. DOI URL
[152]	Wright IJ, Dong N, Maire V, Prentice IC, Westoby M, Díaz S, Gallagher RV, Jacobs BF, Kooyman R, Law EA, Leishman MR, Niinemets Ü, Reich PB, Sack L, Villar R, et al. (2017). Global climatic drivers of leaf size. Science, 357, 917-921. DOI PMID
[153]	Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, et al. (2004). The worldwide leaf economics spectrum. Nature, 428, 821-827. DOI URL
[154]	Wu B, Liu J, Jiang K, Zhou J, Wang C (2019). Differences in leaf functional traits between simple and compound leaves of Canavalia maritime. Polish Journal of Environmental Studies, 28, 1425-1432. DOI URL
[155]	Xia K, Su T, Liu YS, Xing Y-W, Jacques FMB, Zhou ZK (2009). Quantitative climate reconstructions of the late Miocene Xiaolongtan megaflora from Yunnan, southwest China. Palaeogeography, Palaeoclimatology, Palaeoecology, 276, 80-86. DOI URL
[156]	Xu F, Guo W, Xu W, Wei Y, Wang R (2009). Leaf morphology correlates with water and light availability: What consequences for simple and compound leaves? Progress in Natural Science, 19, 1789-1798. DOI URL
[157]	Yang D, Niklas KJ, Xiang S, Sun S (2010). Size-dependent leaf area ratio in plant twigs: implication for leaf size optimization. Annals of Botany, 105, 71-77. DOI URL
[158]	Yang D, Zhang YJ, Song J, Niu CY, Hao GY (2019a). Compound leaves are associated with high hydraulic conductance and photosynthetic capacity: evidence from trees in Northeast China. Tree Physiology, 39, 729-739. DOI URL
[159]	Yang Y, Zhao J, Zhao P, Wang H, Wang B, Su S, Li M, Wang L, Zhu Q, Pang Z, Peng C (2019b). Trait-based climate change predictions of vegetation sensitivity and distribution in China. Frontiers in Plant Science, 10, 908. DOI: 10.3389/fpls.2019.00908. DOI URL
[160]	Yang Y, Zhu Q, Peng C, Wang H, Xue W, Lin G, Wen Z, Chang J, Wang M, Liu G, Li S (2016). A novel approach for modelling vegetation distributions and analysing vegetation sensitivity through trait-climate relationships in China. Scientific Reports, 6, 24110. DOI: 10.1038/ srep24110. DOI URL
[161]	Yates MJ, Anthony Verboom G, Rebelo AG, Cramer MD (2010). Ecophysiological significance of leaf size variation in Proteaceae from the Cape Floristic Region. Functional Ecology, 24, 485-492. DOI URL
[162]	Zhang D, Peng Y, Li F, Yang G, Wang J, Yu J, Zhou G, Yang Y (2019). Trait identity and functional diversity co-drive response of ecosystem productivity to nitrogen enrichment. Journal of Ecology, 107, 2402-2414. DOI URL
[163]	Zhang JZ, Wei BY, Yuan RR, Wang JH, Ding MX, Chen ZY, Yu H, Qin GJ (2017). The Arabidopsis RING-Type E3 ligase TEAR1 controls leaf development by targeting the TIE1 transcriptional repressor for degradation. The Plant Cell, 29, 243-259. DOI URL
[164]	Zhao WL, Zhang JL, Zhang YJ, Cao KF (2019). Analysis of photosynthesis-water relationship between simple- and compound-leafed leguminous trees. Plant Science Journal, 37, 628-636.
	[ 赵万里, 张教林, 章永江, 曹坤芳 (2019). 豆科复叶和单叶树种的光合-水分关系分析. 植物科学学报, 37, 628-636.]
[165]	Zhu J, Zhang Y, Yang X, Chen N, Li S, Wang P, Jiang L (2020). Warming alters plant phylogenetic and functional community structure. Journal of Ecology, 108, 2406-2415. DOI URL