Association of functional trait variation of Quercus castanea with temperature and water availability gradients at the landscape level

Keywords: Climate gradient, leaf economic spectrum, plant morpho-physiological variation, Quercus


Background: Phenotypic variability of tree species is often associated to environmental factors. Quercus castanea is a Mexican red oak with a wide geographical and altitudinal distribution along contrasting environments. It is the most abundant oak species in the Cuitzeo basin, which is characterized by highly heterogeneous environmental conditions. 

Hypothesis: We hypothesized that gradients in temperature, precipitation and soil characteristics across the distribution of Q. castanea within the Cuitzeo basin promote variability in functional traits related to the adjustment to differential water availability at a landscape level.

Studied species: Quercus castanea Née (Fagaceae).

Study site and years of study: Cuitzeo basin in Central Mexico. 2015-2016.

Methods: We quantified leaf chlorophyll concentration (CC), leaf area (LA), leaf thickness (LT), leaf mass per area (LMA) and the Huber value (HV) in 10 individuals from 22 populations of Q. castanea throughout the basin.

Results: Despite the relatively small geographical area (4,000 km2), our results revealed significant differentiation among populations in the studied functional traits. The strongest variation found was in LT, which was negatively correlated with precipitation seasonality. This pattern is opposite to previous reports on Mediterranean oaks but similar to tropical oaks and suggests that the combination with other traits such as leaf phenology is important in the response to water availability.

Conclusions:  Significant functional differences exist among populations of Q. castanea separated by a few kilometers in the heterogenous landscape of the Cuitzeo basin. This species shows clearly sclerophyllous leaves, but leaf thickness varies to a considerable degree across populations.


Download data is not yet available.

Author Biographies

Libny Ingrid Lara-De La Cruz, Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México

Estudiante del Doctorado en Ciencias Biológicas, UNAM

Felipe García-Oliva, Universidad Nacional Autónoma de México

Investigador Titular C de T. C.

Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México

Ken Oyama, Universidad Nacional Autónoma de México

Investigador Titular C de T. C.

Escuela Nacional de Estudios Superiores Morelia, Universidad Nacional Autónoma de Morelia, Universidad Nacional Autónoma de México

Antonio González Rodríguez, Universidad Nacional Autónoma de México

Investigador Titular B de T. C.

Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México

Association of functional trait variation of Quercus castanea with temperature and water availability gradients at the landscape level


Aguilar-Romero R, García-Oliva F, Pineda-García F, Torres I, Peña-Vega E, Ghilardi A, Oyama K. 2016. Patterns of distribution of nine Quercus species along an environmental gradient in a fragmented landscape in central Mexico. Botanical Sciences 94:471-482.

Aguilar-Romero R, Pineda-García F, Paz H, González-Rodríguez A, Oyama K. 2017. Differentiation in the water-use strategies among oak species from central Mexico. Tree Physiology 37:915-925.

Alberto FJ, Bouffier L, Louvet JM, Lamy JB, Delzon S, Kremer A. 2011. Adaptive responses for seed and leaf phenology in natural populations of sessile oak along an altitudinal gradient. Journal of Evolutionary Biology 24:1442–1454.

Aranda I, Cano FJ, Gascó A, Cochard H, Nardini A, Mancha JA, López R, Sánchez-Gómez D. 2015. Variation in photosynthetic performance and hydraulic architecture across European beech (Fagus sylvatica L.) populations supports the case for local adaptation to water stress. Tree Physiology 35:34-46.

Auger S, Shipley B. 2013. Inter-specific and intra-specific trait variation along short environmental gradients in an old-growth temperate forest. Journal of Vegetation Science 24:419-428.

Borcard D, Legendre P, Drapeau P. 1992. Partialling out the spatial component of ecological variation. Ecology 73:1045-1055.

Bruschi P. 2010. Geographical variation in morphology of Quercus petraea (Matt.) Liebl. as related to drought stress. Plant Biosystems 14:298-307.

Bussotti F, Bettini D, Grossoni P, Mansuino S, Nibbi R, Soda C, Tani C. 2002. Structural and functional traits of Quercus ilex in response to water availability. Environmental and Experimental Botany 47:11-23.

Cabrera-González A, Medina-Orozco LE, Sánchez-Espinosa F, Alcalá-de Jesús M, Ayala-Gómez JM. 2010. Los suelos de la Cuenca de Cuitzeo. In: Cram S, Israde I, Mendoza M, Sommer I, Galicia.L, eds. Atlas de la Cuenca del Lago Cuitzeo: un análisis de la geografía del lago y su entorno socioambiental. UNAM-UMSNH, pp 44-47.

Callaway RM, DeLucia EH, Schlesinger WH. 1994. Biomass allocation of montane and desert ponderosa pine: an analog for response to climate change. Ecology 75:1474-1481.

Carter JL, White DA. 2009. Plasticity in the Huber value contributes to homeostasis in leaf water relations of a mallee Eucalypt with variation to groundwater depth. Tree Physiology 29:1407-1418.

Cavender-Bares J, Kitajima K, Bazzaz FA. 2004. Multiple trait associations in relation to habitat differentiation among 17 Floridian oak species. Ecological Monographs 74:635-662.

Cavender-Bares J. 2016. Diversity, distribution and ecosystem services of the North American oaks. International Oaks 27:37-49.

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-Peregrin E, Peguero-Pina JJ, Sancho-Knapik D, eds. Oaks Physiologycal Ecology. Exploring the functional diversity of genus Quercus L. Tree Physiology 7,

Cavender-Bares J. 2019. Diversification, adaptation, and community assembly of the American oaks (Quercus), a model clade for integrating ecology and evolution. New Phytologist 221: 669-692.

Chai Y, Zhang X, Yue M, Liu X, Li Q, Shang H, Meng Q, Zhang R. 2015. Leaf traits suggest different ecological strategies for two Quercus species along an altitudinal gradient in the Qinling Mountains. Journal of Forest Research 20:501-513.

Chávez-Vergara B, Merino A, Vázquez-Marrufo G, García-Oliva F. 2014. Organic matter dynamics and microbial activity during decomposition of forest floor under two native neotropical oak species in a temperate deciduous forest in Mexico. Geoderma 235:133-145.

Cochrane A, Hoyle GL, Yates CJ, Neeman T, Nicotra AB. 2016. Variation in plant functional traits across and within four species of Western Australian Banksia (Proteaceae) along a natural climate gradient. Austral Ecology 41:886-896.

Cooper CE, Vogel JG, Muir JP, Moore GW. 2018. Leaf functional trait responses to changes in water status differ among three oak (Quercus) species. Plant Ecology 219:1463-1479.

Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, Steege HT, Morgan HD, Van Der Heijden MGA, Pausas JG, Poorter. 2003. A handbook of protocols for standarised and easy measurement of plant functional traits worldwide. Australian Journal of Botany 51: 335-380.

Correa-Ayram CA, Mendoza ME, Etter A, Pérez-Salicrup DR. 2017. Potential distribution of Mountain Cloud Forest in Michoacán, México: Priorization for conservation in the context of landscape connectivity. Environmental Management 60:86-103.

Croft H, Chen JM, Luo X, Barlett P, Chen B, Staebler RM. 2017. Leaf chlorophyll content as a proxy for leaf photosynthetic capacity. Global Change Biology 23:3513-3524.

Cuervo-Robayo AP, Téllez-Valdés O, Gómez-Albores MA, Venegas-Barrera CS, Manjarrez J, Martínez-Meyer E. 2014. An update of high-resolution monthly climate surfaces for Mexico. International Journal of Climatology 34:2427-2437.

De la Riva EG, Olmo M, AJ, Evans JP. 2016. Leaf mass per area (LMA) and its relationship with leaf structure and anatomy in 34 Mediterranean woody species along a water availability gradient. PLoSONE 11:e0148788.

Dray S, Legendre P, Peres-Neto PR. 2006. Spatial-modelling: a comprehensive framework for principal coordinate analysis of neighbor matrices (PCNM). Ecological Modelling 196:483-493.

ESRI [Environmental Systems Research Institute] (1999) Arcview GIS 3.3. Environmental Systems Re¬search Institute, Redlands.

Fitzpatrick MC, Keller SR. 2015. Ecological genomics meets community-level modelling of biodiversity: Mapping the genomic landscape of current and future environmental adaptation. Ecology Letters 18:1-16.

Flexas J, Díaz-Espejo A, Gago J, Galmés J, Gulías J, Medrano H. 2014. Photosynthetic limitations in Mediterranean plants: A review. Environmental and Experimental Botany 103:12-23.

García-Nogales A, Linares JC, Laureano RG, Seco JI, Merino J. 2016. Range-wide variation in life-history phenotypes: spatiotemporal plasticity across the latitudinal gradient of the evergreen oak Quercus ilex. Journal of Biogeography 43:2366-2379.

Gil-Pelegrín E, Saz MA, Cuadrat JM, Peguero-Pina JJ, Sancho-Knapik D. 2017. Oaks under Mediterranean-type climates: functional response to summer aridity. In: Gil-Peregrin E, Peguero-Pina JJ, Sancho-Knapik D, eds. Oaks Physiologycal Ecology. Exploring the functional diversity of genus Quercus L. Tree Physiology 7,

Hernández-Calderón E, González-Rodríguez A, Méndez-Alonzo R, Vega-Peña E, Oyama K. 2013. Contrasting leaf phenology in two white oaks, Quercus magnoliifolia and Quercus resinosa, along an altitudinal gradient in Mexico. Canadian Journal of Forest Research 43:208-213.

Hernández-Calderón E, Méndez-Alonso R, Martínez-Cruz J, González-Rodríguez A, Oyama K. 2014. Altitudinal changes in tree leaf and stem functional diversity in a semi-tropical mountain. Journal of Vegetation Science 25:955–966.

Herrera-Arroyo ML, Sork VL, González-Rodríguez A, Rocha-Ramírez V, Vega E, Oyama K. 2013. Seed-mediated connectivity among fragmented populations of Quercus castanea (Fagaceae) in a Mexican Landscape. American Journal of Botany 100:1663-1671.

Kawecki TJ, Ebert D. 2004. Conceptual issues in local adaptation. Ecology Letters 7: 1225-1241.

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 Phytologist 193:730-744.

Lavorel S, Díaz S, Cornelisse JHC, Urcelay C. 2007. Plant functional types: are we getting any closer to the Holy Grail? In: Canadell J, Pitelka LF, Pataki D, eds. Terrestrial ecosystems in a changing world. Springer-Verlag, Berlin, pp 149-164.

Leal-Nares OA, Mendoza ME, Carranza-González E. 2010. Análisis y modelamiento espacial de información climática de la cuenca de Cuitzeo, México. Investigaciones Geográficas 72:49-67.

Lind BM, Friedline CJ, Wegrzyn JL, Maloney PE, Vogler DR, Neale DB, Eckert AJ. 2017. Water availability drives signatures of local adaptation in whitebark pine (Pinus albicaulis Engelm.) across fine spatial scales of the Lake Tahoe Basin, USA. Molecular Ecology 26:3168-3185.

Llanderal-Mendoza J, Gugger PF, Oyama K, Uribe-Salas D, González-Rodríguez A. 2017. Climatic determinants of acorn size and germination percentage of Quercus rugosa (Fagaceae) along a latitudinal gradient in Mexico. Botanical Science 95:37-45.

Lohbeck M, Poorter L, Lebrija-Trejos E, Martínez-Ramos M, Meave JA, Paz H, Pérez-García EA, Romero-Pérez IE, Tauro A, Bongers F. 2013. Successional changes in functional composition contrast for dry and wet tropical forest. Ecology 94:1211-1216.

López E, Bocco G, Mendoza M, Velázquez A, Aguirre-Rivera JR. 2006. Peasant emigration and land-use change at the watershed level: A GIS-based approach in Central Mexico. Agricultural Systems 90:62-78.

Manel S, Gugerli F, Thuiller W, Alvarez N, Legendre P, Holdereger R, Gielly L, Taberlet P, IntraBioDiv Consortium. 2012. Broad-scale adaptive genetic variation in alpine plants is driven by temperature and precipitation. Molecular Ecology 21:3729-3738.

Markwell J, Osterman JC, Mitchell JL. 1995. Calibration of the Minolta SPAD-502 leaf chlorophyll meter. Photosynthesis Research 46:467-472.

McKnow AD, Guy RD, Klápste J, Geraldes A, Friedmann M, Cronk QCB, El-Kassaby YA, Mansfield SD, Douglas CJ. 2014. Geographical and environmental gradients shape phenotypic trait variation and genetic structure in Populus trichocarpa. New Phytologist 201:1263-1276.

Meireles JE, Beulke A, Borkowski DS, Romero-Severson J, Cavender-Bares J. 2017. Balancing selection maintains diversity in a cold tolerance gene in broadly distributed live oaks. Genome 60:762-769.

Mendoza ME, Bocco G, Bravo M, López-Granados E, Osterkamp WR. 2006. Predicting water-sur¬face fluctuation of continental lakes: ARS and GIS based approach in central Mexico. Water Resources Management 20:291-311.

Mendoza ME, López-Granados E, Geneletti D, Pérez-Salicrup DR, Salinas V. 2011. Analyzing land cover and land use change processes at watershed level: A multitemporal study in the Lake Cuitzeo Watershed, Mexico (1975-2003). Applied Geography 31:237-250.

Niinemets Ü. 2001. Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82: 453-469.

Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. 2015. Vegan: Community Ecology Package. R package version 2.2-1.

Oyama K, Herrera-Arroyo ML, Rocha-Ramírez V, Benítez-Malvido J, Ruiz-Sánchez E, González-Rodríguez A. 2017. Gene flow interruption in a recently human-modified landscape: The value of isolated trees for the maintenance of genetic diversity in a Mexican endemic red oak. Forest Ecology and Management 390:27–35.

Peguero-Pina JJ, Sisó S, Fernández-Marín B, Flexas J, Galmés J, García-Plazaola JI, Niinemets Ü, Sancho-Knapik D, Gil-Peregrin E. 2016. Leaf functional plasticity decreases the water consumption without further consequences for carbon uptake in Quercus coccifera L. under Mediterranean conditions. Tree Physiology 36:356-367.

Peres-Neto PR, Legendre P, Dray S, Borcard D. 2006. Variation partitioning of species data matrices: Estimation and comparison of fractions. Ecology 87:2614-2625.

Petit RJ, Carlson J, Curtu AL, Loustau ML, Plomion C, González-Rodríguez A, Sork V, Ducousso A. 2013. Fagaceae trees as models to integrate ecology, evolution and genomics. New Phytologist 197:369-371.

Ramírez-Valiente JA, Sánchez-Gómez D, Aranda I, Valladares F. 2010. Phenotypic plasticity and local adaptation in leaf ecophysiological traits of 13 contrasting cork oak populations under different water availabilities. Tree Physiology 30:618–627.

Ramírez-Valiente JA, Valladares F, Delgado A, Nicotra AB, Aranda I. 2015. Understanding the importance of intra-population functional variability and phenotypic plasticity in Quercus suber. Tree Genetics & Genomes 11:35.

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. Frontiers in Plant Science 8:585.

Ramos-Ortiz S, Oyama K, Rodríguez-Correa H, González-Rodríguez A. 2015. Geographic structure of genetic and phenotypic variation in the hybrid zone between Quercus affinis and Q. laurina in Mexico. Plant Species Biology 31:219-232.

Rasband WS. 2010. ImageJ. Bethesda, MD, USA. National Institutes of Health.

Rosbakh S, Römermann C, Poschlod P. 2015. Specific leaf area correlates with temperature: new evidence of trait variation at the population, species and community levels. Alpine Botany 125:79–86.

Sáenz-Romero C, Lamy JB, Ducousso A, Musch B, Ehrenmann F, Delzon S, Caver S, Chalupka W, Dağdaş S, Hansen JK, Lee SJ, Liesebach M, Rau HM, Psomas A, Schneck V, Steiner W, Zimmermann NE, Kremer A. 2017. Adaptive and plastic responses of Quercus petraea populations to climate across Europe. Global Change Biology 23: 2831-2847.

Schondube JE, Macgregor-Fors I, Morales-Pérez L, Mendoza M, López E. 2010. Ecología espacial de aves en la Cuenca de Cuitzeo. In: Cram S, Galicia L, Israde-Alcantara I, eds. Atlas de la Cuenca de Lago Cuitzeo: Análisis de la geografía del lago y su entorno socioambiental. 102–107. Universidad Nacional Autónoma de México-Universidad Michoacana de San Nicolás de Hidalgo, México, D.F., México.

Souto C, Premoli A, Reich P. 2009. Complex bioclimatic and soil gradients shape leaf trait variation in Embothrium coccineum (Proteaceae) among austral forest in Patagonia. Revista Chilena de Historia Natural 82:209-222.

Trelease W. 1924. The american oaks. Memoirs National Academy of Sciences 20:1-255.

Tyree MT, Dixon MA. 1986. Water stress induced cavitation and embolism in some woody plants. Physiologia Plantarum 66: 397-405.

Tyree MT, Ewers FW. 1991. The hydraulic architecture of trees and other woody plants. New Phytologist 119:345-360.

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.

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

Valencia-Cuevas L, Mussali-Galante P, Piñero D, Castillo-Mendoza E, Rangel-Altamirano G, Tovar-Sánchez E. 2015. Hybridization of Quercus castanea (Fagaceae) across a red oak species gradient in Mexico. Plant Systematics and Evolution 301:1085-1097.

Valladares F, Sánchez- Gómez D. 2006. Ecophysiological traits associated with drought in Mediterranean tree seedlings: individual responses versus interspecific trends in eleven species. Plant Biology 8:688-697.

Van den Wollenberg AL. 1977. Redundancy analysis: an alternative for canonical analysis. Psychometrika 42:207–219.

Westoby M, Falser DS, Moles AT, Vesk PA, Wright IJ. 2002. Plant ecological strategies: some leading dimensions of variation between species. Annual Review of Ecology and Systematics 33:125-159.

Wilson PJ, Thompson K, Hodgson JG. 1999. Specific leaf area and leaf dry matter content as alternative predictors of plant strategies. New Phytologist 143:155-162.

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, Lamont BB, Lee T, Lee W, Lusk C, Midgle J, Navas ML, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklas EJ, Villar R. 2004. The worldwide leaf economics spectrum. Nature 428:621-827.

How to Cite
Lara-De La Cruz, L. I., 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(1), 16-27.