Variability in leaf morphological traits of an endemic Mexican oak (Quercus mexicana Bonpl.) along an environmental gradient

  • Vanessa Sánchez-Acevedo Escuela Nacional de Estudios de Superiores, Unidad Morelia, Universidad Nacional Autónoma de México, Morelia
  • Andrés Torres-Miranda Escuela Nacional de Estudios de Superiores, Unidad Morelia, Universidad Nacional Autónoma de México, Morelia
  • Claudia Gutiérrez-Arellano Escuela Nacional de Estudios de Superiores, Unidad Morelia, Universidad Nacional Autónoma de México, Morelia
  • Karen Beatriz Hernández-Esquivel Escuela Nacional de Estudios de Superiores, Unidad Morelia, Universidad Nacional Autónoma de México, Morelia
  • Ken Oyama Escuela Nacional de Estudios de Superiores, Unidad Morelia, Universidad Nacional Autónoma de México, Morelia
keywords: climate change, drought tolerance, endemic oaks, leaf variation, morfo-functional traits, Sierra Madre Oriental


Background: Phenotypic and functional traits of plant populations vary with environmental conditions at local and regional scales. The analysis of these traits along environmental gradients provides information on the differential response of populations to climate changes.

Objective: We analyzed the leaf morphological variation of an endemic oak to identify the degree of population differentiation along an environmental gradient.

Study species: Quercus mexicana Bonpl. (Fagaceae).

Study site and dates: Samples were collected from 39 populations in the Sierra Madre Oriental and east of the Trans-Mexican Volcanic Belt from 2014 to 2016.

Methods: We measured eight macromorphological traits in 5,507 leaves and three micromorphological traits in 228 leaves. We performed univariate and multivariate statistical analyses to assess the morphological differentiation among populations, and the relationship between variation in leaf traits and environmental variables related to temperature and water availability.

Results: Populations of Q. mexicana showed leaf morphological differentiation along its distribution. Significant linear correlations were found between leaf traits and environmental variables. Smaller and thicker leaves with lower density of trichomes and smaller stomata were found in populations located in more arid regions. In contrast, larger and thinner leaves with higher trichome density and larger stomata occurred in more humid places.

Conclusions: Populations of Q. mexicana are adapted to a wide range of climatic conditions. Considering the predictive future climatic changes for the region (i.e., warmer and drier conditions), Q. mexicana populations with traits better adapted to a more humid and cooler environments could be negatively affected.


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Author Biography

Ken Oyama, Escuela Nacional de Estudios de Superiores, Unidad Morelia, Universidad Nacional Autónoma de México, Morelia

Investigador Titular C, SNI nivel 3

Variability in leaf morphological traits of an endemic Mexican oak (<em>Quercus mexicana</em> Bonpl.) along an environmental gradient


Agrawal AA, Conner JK, Stinchcombe JR. 2004. Evolution of plant resistance and tolerance to frost damage. Ecology Letters 7: 1199-1208. DOI:

Albarrán-Lara AL, Petit RJ, Kremer A, Caron H, Peñaloza-Ramírez JM, Gugger PF, Dávila-Aranda PD, Oyama K. 2019. Low genetic differentiation between two morphologically and ecologically distinct giant-leaved Mexican oaks. Plant Systematics and Evolution 305: 89-101. DOI:

Albert CH, Thuiller W, Yoccoz NG, Douzet R, Aubert S, Lavorel S. 2010. A multi-trait approach reveals the structure and the relative importance of intra- vs. interspecific variability in plant traits. Functional Ecology 24: 1192-120. DOI:

Aranda I, Ramírez-Valiente J, Rodríguez-Calcerrada J. 2014. Integridad funcional en la respuesta a sequía de las especies del género Quercus sp. Ecosistemas 23: 27-36.

Benz BW, Martin CE. 2006. Foliar trichomes, boundary layers, and gas exchange in 12 species of epiphytic Tillandsia (Bromeliaceae). Journal of Plant Physiology 163: 648-656. DOI:

Casson S, Gray JE. 2008. Influence of environmental factors on stomatal development. New Phytologist 178: 9-23. DOI:

Cuervo-Robayo AP, Ureta C, Gómez-Albores MA, Meneses-Mosquera AK, Téllez-Valdés O, Martínez-Meyer E. 2020. One hundred years of climate change in Mexico. PLoS ONE 15: e0209808. DOI:

de la Riva EG, Olmo M, Poorter H, Ubera JL, Villar R. 2016. Leaf mass per area (LMA) and its relationship with leaf structure and anatomy in 34 Mediterranean woody species along a water availability gradient. Plos One 11: e0148788. DOI:

Dunbar-Co S, Sporck MJ, Sack L. 2009. Leaf trait diversification and design in seven rare taxa of the Hawaiian Plantago. International Journal of Plant Sciences 170: 61-75. DOI:

González-Rodríguez A, Arias DM, Valencia-Á. S, Oyama K. 2004. Morphological and RAPD analysis of hybridization between Quercus affinis and Q. laurina (Fagaceae), two Mexican red oaks. American Journal of Botany 91: 401-409. DOI:

Gouveia AC, Freitas H. 2009. Modulation of leaf attributes and water use efficiency in Quercus suber along a rainfall gradient. Trees 23: 267-275. DOI:

Graham A. 1993. Historical factors and biodiversity in Mexico. In: Ramammoorthy TP, Bye R, Fa J, eds. Biological Diversity of Mexico: Origins and Distribution. New York: Oxford University Press, pp. 109-127. ISBN: 0-19-506674-X

Harzé M, Mahy G, Monty A. 2016. Functional traits are more variable at the intra-than inter-population level: a study of four calcareous dry-grassland plant species. Tuexenia 36: 321-336.

Henn JJ, Buzzard V, Enquist BJ, Halbritter AH, Klanderud K, Maitner BS, Michaletz ST, Pötsch C, Seltzer L, Telford RJ, Yang Y, Zhang L, Vandvik V. 2018. Intraspecific trait variation and phenotypic plasticity mediate alpine plant species response to climate change. Frontiers in Plant Science 9: 1548. DOI:

Hernández CM, Carrasco AG. 2004. Climatología. In: Luna-Vega I, Morrone J, Espinosa-Organista D, eds. Biodiversidad de la Sierra Madre Oriental. México: Universidad Nacional Autónoma de México (UNAM), Facultad de Ciencias, pp. 63-108. ISBN: 970-32-1526-2

Hetherington AM, Woodward FI. 2003. The role of stomata in sensing and driving environmental change. Nature 424: 901-908. DOI:

Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 1965-1978. DOI:

Iwata H. Ukai Y. 2002. SHAPE: a computer program package for quantitative evaluation of biological shapes based on elliptic Fourier descriptors. Journal of Heredity 93: 384-385. DOI:

Körner C, Basler D, Hoch G, Kollas C, Lenz A, Randin CF, Vitasse Y, Zimmermann NE. 2016. Where, why and how? Explaining the low-temperature range limits of temperate tree species. Journal of Ecology 104: 1076-1088. DOI:

Laforest-Lapointe I, Martínez-Vilalta J, Retana J. 2014. Intraspecific variability in functional traits matters: case study of Scots pine. Oecologia 175: 1337-1348. DOI:

Lara-De La Cruz LI, García-Oliva F, Oyama K, González-Rodríguez A. 2020. Association of functional trait variation of Quercus castanea with temperature and water availability gradients at the landscape level. Botanical Sciences 98: 16-27. DOI:

Lawson T, Blatt MR. 2014. Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiology 164: 1556-1570.

Lee TD, Reich PB, Bolstad PV. 2005. Acclimation of leaf respiration to temperature is rapid and related to specific leaf area, soluble sugars and leaf nitrogen across three temperate deciduous tree species. Functional Ecology 19: 640-647.

Lozano-García S, Vázquez-Selem L. 2005. A high elevation Holocene pollen record from Iztaccihuatl volcano, Central Mexico. The Holocene 15: 329-338. DOI:

Martínez-Blancas A, Martorell C. 2020. Changes in niche differentiation and environmental filtering over a hydric stress gradient. Journal of Plant Ecology 13: 185-194. DOI:

Maya-García R, Torres-Miranda CA, Cuevas-Reyes P, Oyama K. 2020. Morphological differentiation among populations of Quercus elliptica Neé (Fagaceae) along an environmental gradient in Mexico and Central America. Botanical Sciences 98: 50-65. DOI:

Meier IC, Leuschner C. 2008. Leaf size and leaf area index in Fagus sylvatica forests: Competing effects of precipitation, temperature, and nitrogen availability. Ecosystems 11: 655-669.

Metcalfe DB, Meir P, Aragão LE, Lobo-do-Vale R, Galbraith D, Fisher RA, Chaves MM, Maroco JP, da Costa ACL, de Almeida SS, Braga AP, Goncalves PHL, de Athaydes J, da Costa M, Portela TT, de Oliveira AAR, Malhi Y, Williams M. 2010. Shifts in plant respiration and carbon use efficiency at a large-scale drought experiment in the eastern Amazon. New Phytologist 187: 608-621. DOI:

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: 1-8. DOI:

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, CavenderBares J, Hans J, Cornelissen C, Cornwell WC, Díaz S, Dickie JB, Freschet GT, Griffiths JG, Gutierrez AG, Hemmings FA, Hickler T, Hitchcock TD, Keighery M, Kleyer M, Kurokawa H, Leishman MR, Liu K, Niinemets U, Onipchenko V, Onoda Y, Peñuelas J, Pillar VD, Reich PB, Shiodera S, Siefert A, SosinskiJr EE, Soudzilovskaia NA, Swaine EK, Swenson NG, van Bodegom PM, Warman L, Weiher E, Wright IJ, Zhang H, Zobel M, Bonser SP. 2014. Which is a better predictor of plant traits: temperature or precipitation? Journal of Vegetation Science 25: 1167-1180. DOI:

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:[0453:GSCCOL]2.0.CO;2

Nóbrega CM, Pereira JS. 1992. Gradients of anatomy and morphology of leaves in the crowns of cork oak. Scientia gerundensis 18: 53.

Pérez-Estrada LB, Cano-Santana Z, Oyama K. 2000. Variation in leaf trichomes of Wigandia urens: environmental factors and physiological consequences. Tree Physiology 20: 629-632. DOI:

Pérez-Mojica E, Valencia-Á. S. 2017. Estudio preliminar del género Quercus (Fagaceae) en Tamaulipas, México. Acta Botanica Mexicana 120: 59-111. DOI:

Pollock LJ, Morris WK, Vesk PA. 2012. The role of functional traits in species distributions revealed through a hierarchical model. Ecography 35: 716-725. DOI:

R Core Team. 2016. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

Richardson AD, Ashton PMS, Berlyn GP, McGroddy ME, Cameron IR. 2001. Within-crown foliar plasticity of western hemlock, Tsuga heterophylla, in relation to stand age. Annals of Botany 88: 1007-1015. DOI:

Riordan EC, Gugger PF, Ortego J, Smith C, Gaddis K, Thompson P, Sork VL. 2016. Association of genetic and phenotypic variability with geography and climate in three southern California oaks. American Journal of Botany 103: 73-85. DOI:

Rodríguez-Gómez F, Oyama K, Ochoa-Orozco M, Mendoza-Cuenca L, Gaytán-Legaria R, & González-Rodríguez A. 2018. Phylogeography and climate-associated morphological variation in the endemic white oak Quercus deserticola (Fagaceae) along the Trans-Mexican Volcanic Belt. Botany 96: 121-133. DOI:

Sack L, Frole K. 2006. Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees. Ecology 87: 483-491. DOI:

Schilmiller AL, Last RL, Pichersky E. 2008. Harnessing plant trichome biochemistry for the production of useful compounds. The Plant Journal 54: 702-711. DOI:

Stahl U, Reu B, Wirth C. 2014. Predicting species’ range limits from functional traits for the tree flora of North America. Proceedings of the National Academy of Sciences USA 111: 13739-13744. DOI:

Tang CQ, Ohsawa M. 1999. Altitudinal distribution of evergreen broad-leaved trees and their leaf-size pattern on a humid subtropical mountain, Mt. Emei, Sichuan, China. Plant Ecology 145: 221-233. DOI:

Toledo VM. 1982. Pleistocene changes of vegetation in tropical México. In: Prance GT, ed. Biological Diversification in the Tropics. Nueva York: Columbia University Press, pp. 93-111. ISBN: 0-231-04876-9

Tovar-Sánchez E, Mussali-Galante P, Esteban-Jiménez R, Piñero D, Arias DM, Dorado O, Oyama K. 2008. Chloroplast DNA polymorphism reveals geographic structure and introgression in the Quercus crassifolia × Quercus crassipes hybrid complex in Mexico. Botany 86: 228-239. DOI:

Trabucco A, Zomer RJ. 2009. Global Aridity Index (Global-Aridity) and Global Potential Evapotranspiration (Global-pet) Geospatial Database. CGIAR Consortium for Spatial Information. CGIAR-CSI GeoPortal online. DOI:

Uribe-Salas D, Sáenz-Romero C, González-Rodríguez A, Téllez-Valdéz O, Oyama K. 2008. Foliar morphological variation in the white oak Quercus rugosa Née (Fagaceae) along a latitudinal gradient in Mexico: Potential implications for management and conservation. Forest Ecology and Management 256: 2121-2126. DOI:

Valencia-Á. S. 2004. Diversidad del género Quercus (Fagaceae) en México. Boletín de la Sociedad Botánica de México 75: 33-53. DOI:

Valladares F, Matesanz S, Guilhaumon F, Araújo MB, Balaguer L, Benito?Garzón M, Cornwel W, Gianoli E, van Kleunen M, Naya DE, Nicotra AB, Poorter H, Zavala MA. 2014. The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecology Letters 17: 1351-1364. DOI:

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:

Ward JH, Hook ME. 1963. Application of a hierarchical grouping procedure to a problem of grouping profiles. Educational and Psychological Measurement 23: 69-81. DOI:

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, Wang H, Wilf P. 2017. Global climatic drivers of leaf size. Science 357: 917. DOI:

Yan W, Zhong Y, Shangguan Z. 2017. Contrasting responses of leaf stomatal characteristics to climate change: a considerable challenge to predict carbon and water cycles. Global Change Biology 23: 3781-3793. DOI:

Zhu Y, Kang H, Xie Q, Wang Z, Yin S, Liu C. 2012. Pattern of leaf vein density and climate relationship of Quercus variabilis populations remains unchanged with environmental changes. Trees 26: 597-607. DOI:

How to Cite
Sánchez-Acevedo, V., Torres-Miranda, A., Gutiérrez-Arellano, C., Hernández-Esquivel, K. B., & Oyama, K. (2022). Variability in leaf morphological traits of an endemic Mexican oak (Quercus mexicana Bonpl.) along an environmental gradient. Botanical Sciences, 100(3), 579-599.