{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,25]],"date-time":"2026-01-25T08:41:50Z","timestamp":1769330510218,"version":"3.49.0"},"reference-count":51,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2019,10,9]],"date-time":"2019-10-09T00:00:00Z","timestamp":1570579200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Symmetry"],"abstract":"<jats:p>Leaf surface area (A) and leaf shape have been demonstrated to be closely correlated with photosynthetic rates. The scaling relationship between leaf biomass (both dry weight and fresh weight) and A has been widely studied. However, few studies have focused on the scaling relationship between leaf shape and A. Here, using more than 3600 leaves from 12 Rosaceae species, we examined the relationships of the leaf-shape indices including the left to right side leaf surface area ratio (AR), the ratio of leaf perimeter to leaf surface area (RPA), and the ratio of leaf width to length (RWL) versus A. We also tested whether there is a scaling relationship between leaf dry weight and A, and between PRA and A. There was no significant correlation between AR and A for each of the 12 species. Leaf area was also found to be independent of RWL because leaf width remained proportional to leaf length across the 12 species. However, there was a negative correlation between RPA and A. The scaling relationship between RPA and A held for each species, and the estimated scaling exponent of RPA versus A approached \u22121\/2; the scaling relationship between leaf dry weight and A also held for each species, and 11 out of the 12 estimated scaling exponents of leaf dry weight versus A were greater than unity. Our results indicated that leaf surface area has a strong scaling relationship with leaf perimeter and also with leaf dry weight but has no relationship with leaf symmetry or RWL. Additionally, our results showed that leaf dry weight per unit area, which is usually associated with the photosynthetic capacity of plants, increases with an increasing A because the scaling exponent of leaf dry weight versus A is greater than unity. This suggests that a large leaf surface area requires more dry mass input to support the physical structure of the leaf.<\/jats:p>","DOI":"10.3390\/sym11101255","type":"journal-article","created":{"date-parts":[[2019,10,9]],"date-time":"2019-10-09T03:22:57Z","timestamp":1570591377000},"page":"1255","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":27,"title":["Scaling Relationships between Leaf Shape and Area of 12 Rosaceae Species"],"prefix":"10.3390","volume":"11","author":[{"given":"Xiaojing","family":"Yu","sequence":"first","affiliation":[{"name":"Bamboo Research Institute, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Cang","family":"Hui","sequence":"additional","affiliation":[{"name":"Centre for Invasion Biology, Department of Mathematical Sciences, Stellenbosch University, Matieland 7602, South Africa"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hardev S.","family":"Sandhu","sequence":"additional","affiliation":[{"name":"Everglades Research and Education Center, University of Florida, 3200 E. Palm Beach Road, Belle Glade, FL 33430, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhiyi","family":"Lin","sequence":"additional","affiliation":[{"name":"Bamboo Research Institute, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4696-0130","authenticated-orcid":false,"given":"Peijian","family":"Shi","sequence":"additional","affiliation":[{"name":"Bamboo Research Institute, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China"},{"name":"Tropical Silviculture and Forest Ecology, University of G\u00f6ttingen, B\u00fcsgenweg 1, 37077 G\u00f6ttingen, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2019,10,9]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"79","DOI":"10.3897\/phytokeys.113.30330","article-title":"Similarity analysis between species of the genus Quercus L. (Fagaceae) in southern Italy based on the fractal dimension","volume":"113","author":"Musarella","year":"2018","journal-title":"PhytoKeys"},{"key":"ref_2","first-page":"30","article-title":"Fractal dimension of the leaf vascular system of three Relbunium species (Rubiaceae)","volume":"8","year":"2010","journal-title":"Braz. J. Biol. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/S1369-5266(00)00135-7","article-title":"Vascular patterning and leaf shape","volume":"4","author":"Dengler","year":"2001","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"702","DOI":"10.1145\/1073204.1073251","article-title":"Modeling and visualization of leaf venation patterns","volume":"24","author":"Runions","year":"2005","journal-title":"ACM Trans. Graphics"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1046\/j.1365-2435.1999.00368.x","article-title":"A theoretical approach to linking the composition and morphology with the function of leaves","volume":"13","author":"Roderick","year":"1999","journal-title":"Funct. Ecol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1890","DOI":"10.1104\/pp.107.101352","article-title":"Leaf maximum photosynthetic rate and venation are linked by hydraulics","volume":"144","author":"Brodribb","year":"2007","journal-title":"Plant Physiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1071\/FP11057","article-title":"The evolution and functional significance of leaf shape in the angiosperms","volume":"38","author":"Nicotra","year":"2011","journal-title":"Funct. Plant Biol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0378-1127(94)90070-1","article-title":"Leaf weight per area and leaf size of 85 Estonian woody species in relation to shade tolerance and light availability","volume":"70","author":"Niinemets","year":"1994","journal-title":"For. Ecol. Manag."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"785","DOI":"10.2307\/1313100","article-title":"Leaf form and photosynthesis: Do leaf structure and orientation interact to regulate internal light and carbon dioxide?","volume":"47","author":"Smith","year":"1997","journal-title":"BioScience"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1046\/j.1469-8137.1999.00466.x","article-title":"Research review: Components of leaf dry mass per area-thickness and density-alter leaf photosynthetic capacity in reverse directions in woody plants","volume":"144","author":"Niinemets","year":"1999","journal-title":"New Phytol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1890\/0012-9658(2001)082[0453:GSCCOL]2.0.CO;2","article-title":"Global-scale climatic controls of leaf dry mass per area, density, and thinness in trees and shrubs","volume":"82","author":"Niinemets","year":"2001","journal-title":"Ecology"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1893","DOI":"10.1890\/12-1602.1","article-title":"Leaf traits within communities: Context may affect the mapping of traits to function","volume":"94","author":"Funk","year":"2013","journal-title":"Ecology"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1111\/1365-2745.12184","article-title":"Trade-off between light interception efficiency and light use efficiency: Implications for species coexistence in one-sided light competition","volume":"102","author":"Onoda","year":"2014","journal-title":"J. Ecol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"135","DOI":"10.5735\/085.052.0201","article-title":"Leaf mass per area (LMA) as a possible predictor of adaptive strategies in two species of Sesleria (Poaceae): Analysis of morphological, anatomical and physiological leaf traits","volume":"52","author":"Puglielli","year":"2015","journal-title":"Ann. Bot. Fenn."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Yu, X.J., Shi, P.J., Hui, C., Miao, L.F., Liu, C.L., Zhang, Q.Y., and Feng, C.N. (2019). Effects of salt stress on the seaf shape and scaling of Pyrus betulifolia Bunge. Symmetry, 11.","DOI":"10.3390\/sym11080991"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1083","DOI":"10.1002\/j.1537-2197.1986.tb08555.x","article-title":"Temporal and spatial patterns of specific leaf weight in successional northern hardwood tree species","volume":"73","author":"Jurik","year":"1986","journal-title":"Am. J. Bot."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"8891","DOI":"10.1073\/pnas.0701135104","article-title":"\u201cDiminishing returns\u201d in the scaling of functional leaf traits across and within species groups","volume":"104","author":"Niklas","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Bernard, E.E., and Kare, M.R. (1962). Structural, Hydraulic, and \u2018Economic\u2019 Aspects of Leaf Venation and Shape. Biological Prototypes and Synthetic Systems, Plenum Press.","DOI":"10.1007\/978-1-4684-1716-6"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1078\/1433-8319-00049","article-title":"A reassessment of the strategies of plants which cope with shortages of resources","volume":"1","author":"Grubb","year":"1998","journal-title":"Perspect. Plant Ecol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"821","DOI":"10.1038\/nature02403","article-title":"The worldwide leaf economics spectrum","volume":"428","author":"Wright","year":"2004","journal-title":"Nature"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Pan, S., Liu, C., Zhang, W.P., Xu, S.S., Wang, N., Lin, Y., Gao, J., and Wang, Y. (2013). The scaling relationships between leaf mass and leaf area of vascular plant species change with altitude. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0076872"},{"key":"ref_22","first-page":"e00793","article-title":"The scaling relationships of leaf biomass vs. leaf surface area of 12 bamboo species","volume":"20","author":"Huang","year":"2019","journal-title":"Glob. Ecol. Conserv."},{"key":"ref_23","first-page":"1909","article-title":"Shape analysis of symmetric structures: Quantifying variation among individuals and asymmetry","volume":"56","author":"Klingenberg","year":"2002","journal-title":"Evolution"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Wang, P., Ratkowsky, D.A., Xiao, X., Yu, X.J., Su, J.L., Zhang, L.F., and Shi, P.J. (2018). Taylor\u2019s power law for leaf bilateral symmetry. Forests, 9.","DOI":"10.3390\/f9080500"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1111\/j.1469-8137.2010.03476.x","article-title":"Structural and hydraulic correlates of heterophylly in Ginkgo biloba","volume":"189","author":"Leigh","year":"2011","journal-title":"New Phytol."},{"key":"ref_26","unstructured":"Editorial Board of Flora of China, Chinese Academy of Sciences (1993). Flora of China, Science Press."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1381","DOI":"10.3732\/ajb.1100106","article-title":"Differences in the scaling of area and mass of Ginkgo biloba (Ginkgoaceae) leaves and their relevance to the study of specific leaf area","volume":"98","author":"Niklas","year":"2011","journal-title":"Am. J. Bot."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1111\/j.1469-8137.2009.02830.x","article-title":"Causes and consequences of variation in leaf mass per area (LMA): A meta-analysis","volume":"182","author":"Poorter","year":"2009","journal-title":"New Phytol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"856","DOI":"10.3389\/fpls.2015.00856","article-title":"Capturing spiral radial growth of conifers using the superellipse to model tree-ring geometric shape","volume":"6","author":"Shi","year":"2015","journal-title":"Front. Plant Sci."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Shi, P.J., Ratkowsky, D.A., Li, Y., Zhang, L.F., Lin, S.Y., and Gielis, J. (2018). A general leaf area geometric formula exists for plants-evidence from the simplified Gielis equation. Forests, 9.","DOI":"10.3390\/f9110714"},{"key":"ref_31","unstructured":"R Core Team (2015). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing. Available online: http:\/\/www.R-project.org."},{"key":"ref_32","first-page":"e00666","article-title":"Lamina shape does not correlate with lamina surface area: An analysis based on the simplified Gielis equation","volume":"19","author":"Su","year":"2019","journal-title":"Glob. Ecol. Conserv."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2109","DOI":"10.1098\/rspb.2007.0417","article-title":"The scaling of leaf area and mass: The cost of light interception increases with leaf size","volume":"274","author":"Milla","year":"2007","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"ref_34","unstructured":"Montgomery, E.G. (1911). Correlation Studies in Corn, Agricultural Experimental Station. Annual Report No. 24."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Shi, P.J., Liu, M.D., Yu, X.J., Gielis, J., and Ratkowsky, D.A. (2019). Proportional relationship between leaf area and the product of leaf length and width of four types of special leaf shapes. Forests, 10.","DOI":"10.3390\/f10020178"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"476","DOI":"10.1002\/ajpa.21090","article-title":"Used and misuse of the reduced major axis for line-fitting","volume":"140","author":"Smith","year":"2009","journal-title":"Am. J. Phys. Anthropol."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Hsu, J.C. (1996). Multiple Comparisons: Theory and Methods, Chapman and Hall\/CRC.","DOI":"10.1201\/b15074"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"583","DOI":"10.3389\/fpls.2018.00583","article-title":"Why does not the leaf weight-area allometry of bamboos follow the 3\/2-power law?","volume":"9","author":"Lin","year":"2018","journal-title":"Front. Plant Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1073","DOI":"10.1007\/s00468-019-01843-4","article-title":"Leaf area-length allometry and its implications in leaf-shape evolution","volume":"33","author":"Shi","year":"2019","journal-title":"Trees"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1093\/oxfordjournals.aob.a084366","article-title":"Leaf area and absolute water content","volume":"34","author":"Hughes","year":"1970","journal-title":"Ann. Bot."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1007\/BF00317710","article-title":"Leaf specific mass confounds leaf density and thickness","volume":"88","author":"Witkowski","year":"1991","journal-title":"Oecologia"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1146\/annurev.pp.28.060177.002035","article-title":"Comparative photosynthesis of sun and shade plants","volume":"28","author":"Boardman","year":"1977","journal-title":"Annu. Rev. Plant Physiol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1139\/x82-006","article-title":"Autumnal nutrient transfers by retranslocation, leaching, and litter fall in a chestnut oak forest in southern Illinois","volume":"12","author":"Ostman","year":"1982","journal-title":"Can. J. For. Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/0169-5347(89)90103-1","article-title":"Ecological significance of above-ground architectural patterns in woody plants: A question of cost-benefit relationships","volume":"4","year":"1989","journal-title":"Trends Ecol. Evol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1006\/anbo.1997.0519","article-title":"Crown spread patterns for five deciduous broad-leaved woody species ecological significance of the retention patterns of larger branches","volume":"80","author":"Sumida","year":"1997","journal-title":"Ann. Bot."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1093\/aob\/mcf042","article-title":"Spatial arrangement of branches in relation to slope and neighbourhood competition","volume":"89","author":"Sumida","year":"2002","journal-title":"Ann. Bot."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1139\/x79-001","article-title":"Crown stratification by species in even-aged mixed stands of Douglas-fir-western hemlock","volume":"9","author":"Wierman","year":"1979","journal-title":"Can. J. For. Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"275","DOI":"10.2307\/3545019","article-title":"Tree architectures adapted to efficient light utilization: Is there a basis for latitudinal gradients?","volume":"65","author":"Kuuluvainen","year":"1992","journal-title":"Oikos"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1139\/x88-003","article-title":"Development of cherrybark oak and sweet gum in mixed, even-aged bottomland stands in central Mississippi, U.S.A","volume":"18","author":"Clatterbuck","year":"1988","journal-title":"Can. J. For. Res."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1007\/BF02348474","article-title":"The crown shape of an evergreen oak, Quercus glauca, in a hardwood community","volume":"2","author":"Sumida","year":"1997","journal-title":"J. For. Res."},{"key":"ref_51","unstructured":"Wu, J. (2007). Landscape Ecology: Pattern, Process, Scale and Hierarchy, Higher Education Press. [2nd ed.]."}],"container-title":["Symmetry"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-8994\/11\/10\/1255\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:28:30Z","timestamp":1760189310000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-8994\/11\/10\/1255"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,10,9]]},"references-count":51,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2019,10]]}},"alternative-id":["sym11101255"],"URL":"https:\/\/doi.org\/10.3390\/sym11101255","relation":{},"ISSN":["2073-8994"],"issn-type":[{"value":"2073-8994","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,10,9]]}}}