Morphological differentiation among populations of Quercus elliptica Neé (Fagaceae) along an environmental gradient in Mexico and Central America

Keywords: Ecological niche modeling, enviromental gradients, leaf functional traits, leaf morphology, population differentiation, Quercus

Abstract

Background: Variation in leaf morphology is an important indicator of how plants respond to different environmental conditions. Leaf trait variation is associated with physiological responses of plants to gradients of humidity and temperature. 

Objective: We analyzed the variation in the leaf morphological and functional traits of Quercus elliptica and its relationships with environmental and geographic variables across the distribution of this species to evaluate population differentiation using ecological niche models.

Study species: Quercus elliptica Neé (Fagaceae).

Study sites and dates: Plants were collected in diverse forest types between 350 and 2,400 m in elevation in Mexico and Central America during 2016 and 2017.

Methods: We measured and analyzed the differentiation in morphological and functional traits of 4,017 leaves from 402 trees from 41 populations using univariate and multivariate analyses.

Results: The leaf length and thickness and specific leaf area (SLA) of Q. elliptica were significantly correlated with the seasonality of temperature, precipitation, elevation and aridity. We identified two divergent morphological groups: (1) populations distributed along the Pacific coast with broad and thin elliptical leaves with high SLA values and inhabited humid forests at more than 1,200 m elevation, and (2) populations located along the Gulf of Mexico coast, and in southern Mexico and Central America with thicker, narrower leaves and lower SLA values and inhabited seasonal tropical forests in less than 1,200 m in elevation. 

Conclusions: Climate and geographic barriers and the ecological niche models supported the population differentiation of Q. elliptica.

Downloads

Download data is not yet available.

Author Biographies

Andrés Torres Miranda, Universidad Nacional Autónoma de México

Profesor asociado C, tiempo completo / Professor Full Time

Laboratorio de Biogeografía de la Conservación

Escuela Nacional de Estudios Superiores Unidad Morelia

Pablo Cuevas-Reyes, Universidad Michoacana de San Nicolás de Hidalgo

Facultad de Biología, Universidad Michoacana de San Nicolás de Hidalgo

Ken Oyama, Uniersidad Nacional Autónoma de México

Escuela Nacional de Estudios Superiores Unidad Morelia Uniersidad Nacional Autónoma de México

Morphological differentiation among populations of Quercus elliptica Neé (Fagaceae) along an environmental gradient in Mexico and Central America

References

Literature cited

Albarrán-Lara AL, Mendoza-Cuenca L, Valencia-Avalos S, González-Rodríguez A, Oyama K. 2010. Leaf fluctuating asymmetry increases with hybridization and introgression between Quercus magnoliifolia and Quercus resinosa (Fagaceae) through an altitudinal gradient in Mexico. International Journal of Plant Sciences 171: 310–322. DOI: 10.1086/650317

Albert CH, Thuiller W, Yoccoz NC, Soudant A, Boucher F, Saccone P, Lavorell S. 2010. Intraspecific functional variability: extent, structure and sources of variation. Journal of Ecology 98: 604-613. https://doi.org/10.1111/j.1365-2745.2010.01651.x

Aranda I, Ramírez-Valiente JA, Rodríguez-Calcerrada J. 2014. Características funcionales que influyen en la respuesta a la sequía de las especies del género Quercus: variación inter-e intra-específica. Revista Ecosistemas 23: 27–36. DOI: 10.7818/ECOS.2014.23-2.05

Bacilieri R, Ducousso A, Kremer A. 1995. Genetic, morphological, ecological and phenological differentiation between Quercus petraea (Matt.) Liebl. and Quercus robur L. in a mixed stand of northwest of France. Silvae Genetica 44: 1-10.

Bruschi P, Vendramin G, Bussotti FG, Grossoni P. 2003. Morphological and molecular diversity among Italian populations of Quecus petraea (Fagaceae). Annals of Botany 91: 707-716. DOI: https://doi.org/10.1093/aob/mcg075

Chevin LM, Lande R, Mace GM. 2010. Adaptation, plasticity and extinction in a changing environment: towards a predictive theory. PLoS Biology 8: e1000357. DOI https://doi.org/10.1371/journal.pbio.1000357

Fajardo A, Piper FI. 2011 Intraspecific trait variation and covariation in a widespread tree species (Nothofagus pumilio) in southern Chile. New Phytologist 189: 259-271. DOI: 10.1111/j.1469-8137.2010.03468.x

Franiel I, Więski K. 2005. Leaf features of silver birch (Betula pendula Roth). Variability within and between two populations (uncontaminated vs Pb-contaminated and Zn-contaminated site). Trees 19: 81–88. DOI: 10.1007/s00468-004-0366-3

Frenne P, Graae BJ, Rodríguez-Sánchez F, Kolb A, Chabrerie O, Decocq G, de Kort H, Schrijver A, Diekmann M, Eriksson O, Gruwez R, Hermy M, Lenoir J, Plue J, Coomes DA, Verheyen K. 2013. Latitudinal gradients as natural laboratories to infer species' responses to temperature. Journal of Ecology 101: 784–795. DOI: https://doi.org/10.1111/1365-2745.12074

Futuyma DJ .1998. Evolutionary Biology. 3rd ed. Sinauer Associates, Sunderland, MA.

González-Rodríguez A, Oyama K. 2005 Leaf morphometric variation in Quercus affinis and Q. laurina (Fagaceae), two hybridizing Mexican red oaks. Botanical Journal of the Linnean Society 147:427–435. DOI: 10.1111/j.1095-8339.2004.00394.x

González-Rodríguez A, Arias DM, Valencia 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: https://doi.org/10.3732/ajb.91.3.401

González-Villareal ML. 1986. Contribución al conocimiento del género Quercus (Fagaceae) en el Estado de Jalisco. Flora de Jalisco. Instituto de Botánica, Universidad de Guadalajara, Jalisco.

Gouveia AC, Freitas H. 2009 Modulation of leaf attributes and water use efficiency in Quercus suber along a rainfall gradient. Trees 23: 267–275. DO https://doi.org/10.1007/s00468-008-0274-z

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: 10.1002/joc.1276

Kichenin E, Wardle DA, Peltzer DA, Morse CW, Freschet GT. 2013. Contrasting effects of plant inter‐ and intraspecific variation on community‐level trait measures along an environmental gradient. Functional Ecology 27: 1254–1261. DOI: 10.1111/1365-2435.12116

Kremer A, Dupouey JL, Deans JD, Cottrell J, Csaikl U, Finkeldey R, Espinel S, Jensen J, Kleinschmit J, Van Dam B, Ducousso A, Forrest I, López de Heredia U, Lowe AJ, Tutkova M, Munro RC, Steinhoff S, Badeau V. 2002. Leaf morphological differentiation between Quercus robur and Quercus petraea is stable across western European mixed oak stands. Annals of Forest Science 59: 777-787.

Leigh A, Sevanto S, Ball MC, Close JD, Ellsworth DS, Knight CA, Nicotra AB, Vogel S. 2012. Do thick leaves avoid thermal damage in critically low wind speeds? New Phytologist 194: 477–487. DOI: 10.1111/j.1469-8137.2012.04058.x

Leimu R, Fischer M. 2008. A meta-analysis of local adaptation in plants. PLOS ONE 3 (12): e4010. DOI: https://doi.org/10.1371/journal.pone.0004010

Lohbeck M, Poorter L, Lebrija-Trejos E, Martínez-Ramos M, Meave JA, Paz H, Pérez-García E, Romero-Pérez E, Taura A. & Bongers F. 2013. Successional changes in functional composition contrast for dry and wet tropical forest. Ecology 94: 1211–1216. DOI: https://doi.org/10.1890/12-1850.1

Martínez-Cabrera D, Zavala-Chávez F y Terrazas T. 2011. Estudio morfométrico de Quercus sartorii y Q. xalapensis (Fagaceae). Revista Mexicana de Biodiversidad 82: 551–568. DOI: http://dx.doi.org/10.22201/ib.20078706e.2011.2.459

McAssey EV, Corbi J, Burke JM. 2016. Range-wide phenotypic and genetic differentiation in wild sunflower. BMC Plant Biology 16: 249. DOI: 10.1186/s12870-016-0937-7

McLean EH, Prober SM, Stock WD, Steane DA, Potts BM, Vaillancourt RE, Byrne M. 2014. Plasticity of functional traits varies clinally along a rainfall gradient in Eucalyptus tricarpa. Plant Cell Environment 37: 1440–1451. DOI: 10.1111/pce.12251

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. DOI: 10.1007/s10021-008-9135-2

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, 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, IJ Wright, 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: https://doi.org/10.1111/jvs.12190

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: https://doi.org/10.1071/FP11057

Niinemets U. 2001. Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82: 453–469. DOI: https://doi.org/10.1890/0012-9658(2001)082[0453:GSCCOL]2.0.CO;2

Ogaya R, Peñuelas J. 2003. Comparative field study of Quercus ilex and Phillyrea latifolia: photosynthetic response to experimental drought conditions. Environmental and Experimental Botany 50: 137-148. DOI: 10.1016/S0098-8472(02)00019-4

Paine CET, Baratolo C, Chave J, Hérailt B. 2011. Funtional traits of individual trees reveal ecological constraints on community assembly in tropical rain forest. Oikos 120: 720-727. DOI: https://doi.org/10.1111/j.1600-0706.2010.19110.x

Pearse IS, Hipp AL. 2012. Global patterns of leaf defenses in oak species. Evolution 66: 2272–2286. DOI: https://doi.org/10.1111/j.1558-5646.2012.01591.x

Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell W., Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, de Vos AC, Buchmann N, Funes G., Quétier F, Hodgson JG, Thompson, Morgan HD, Steege H, van der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti MV, Conti G, Staver AC, Aquino S y Cornelissen JHC. 2013. New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany, 61: 167-234. DOI: https://doi.org/10.1071/BT12225

Phillips SJ, Dudík M. 2008. Modeling of species distributions with Maxent: New extensions and a comprehensive evaluation. Ecography 31: 161–175. DOI: https://doi.org/10.1111/j.0906-7590.2008.5203.x

Ponton S, Dupoguey J, Dreyer E. 2004. Leaf morphology as species indicator in seedlings of Quercus robur L. and Q. petrea (Matt.) Liebl: Modulation by irradiance and growth flush. Annals of Forest Science, 61, 73–80. DOI: 10.1051/forest:2003086

R Core Team. 2013. R: A Languaje and Environment for Statistical Computing Available, http//www.r.project.org.

Ramírez-Valiente JA, Valladares F, Delgado A, Nicotra AB, Aranda I. 2015 Understanding the importance of intrapopulation functional variability and phenotypic plasticity in Quercus suber. Tree Genetics Genomes 11: 35. DOI 10.1007/s11295-015-0856-z

Rodríguez I, Rangel S. 2007. Arquitectura foliar de diez especies de encino (Quercus, Fagaceae) de México. Acta Botánica Mexicana 81: 9-34. DOI: https://doi.org/10.21829/abm81.2007.1049

Romero-Rangel S, Rojas-Zenteno E, de Lourdes M., Aguilar-Enríquez M. 2002. El género Quercus (Fagaceae) en el Estado de México. Annals of the Missouri Botanical Garden 89: 551-593.

Rossatto DR, Hoffmann WA, Ramos Silva LC, Haridasan M, Sternberg LSL, Franco AC. 2013. Seasonal variation in leaf traits between congeneric savanna and forest trees in Central Brazil: Implications for forest expansion into savanna. Trees 27: 1139–1150. DOI 10.1007/s00468-013-0864-2

Rundle H and Nosil P. 2005. Ecological speciation. Ecology Letters 8: 336-352. DOI: https://doi.org/10.1111/j.1461-0248.2004.00715.x

Sakaguchi S, Qui YX, Liu YH, Qi XS, Klim SH, Han J, Takeuch Y, Worth JR, Yamasaki M, Sakurai S, Isagi Y. 2012. Climate oscillation during the Quaternary associated with landscape heterogeneity promoted allopatric lineage divergence of a temperate tree Kalopanax septemlobus (Araliaceae) in East Asia. Molecular Ecology 21: 3823–3838. DOI: https://doi.org/10.1111/j.1365-294X.2012.05652.x

Salgado-Negrete B, Pérez F, Markesteijn L, Jiménez-Castillo M, Armesto JJ. 2013. Diverging drought-tolerance strategies explain tree species distribution along a fog-dependent moisture gradient in a temperate rain forest. Oecologia 173: 625-635. DOI 10.1007/s00442-013-2650-7

Sambatti JB, Rice KJ. 2006. Local adaptation, patterns of selection, and gene flow in the Californian serpentine sunflower (Helianthus exilis). Evolution 60: 696–710. DOI: https://doi.org/10.1111/j.0014-3820.2006.tb01149.x

Schlichting CD, Levin DA.1986. Phenotypic plasticity: an evolving plant

character. Biological Journal of the Linnean Society 29: 37-47.

Sterck F, Markesteijn L, Schieving F, Poorter L. 2011. Functional traits determine trade-offs and niches in a tropical forest community. Proceedings of the National Academy of Sciences USA 10851: 20627-20632. DOI: https://doi.org/10.1073/pnas.1106950108

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.

Tovar-Sánchez E, Oyama K. 2004. Natural hybridization and hybrid zones between Quercus crassifolia and Quercus crassipes (Fagaceae) in Mexico:

Morphological and molecular evidence. American Journal of Botany 91: 1352-1363. DOI: https://doi.org/10.3732/ajb.91.9.1352

Trabucco A, Zomer RJ. 2009. Global aridity index (global‐aridity) and global potential evapo‐transpiration (global‐pet) geospatial database. CGIAR Consortium for Spatial Information. Published online, available from CGIAR‐CSI GeoPortal at http://www.cgiar‐csi.org/

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: https://doi.org/10.1016/j.foreco.2008.08.002

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

Valencia-A S, Gómez CM, Becerra LF. 200. Catálogo de Encinos del Estado de Guerrero, México. Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, INIFAP, México D.F.

Valladares F, Niinemets U. 2008. Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology, Evolution and Systematics 39: 237–257. DOI: https://doi.org/10.1146/annurev.ecolsys.39.110707.173506

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: https://doi.org/10.1111/ele.12348

Violle C, Enquist BJ, McGill BJ, Jiang LIN, Albert CH, Hulshof C, Jung V, Messier J. 2012. The return of the variance: intraspecific variability in community ecology. Trends Ecology and Evolution 27: 244–252. DOI: 10.1016/j.tree.2011.11.014

Viscosi V, Antonecchia G, Lepais O, Fortini P, Gerber S, Loy A. 2012. Leaf shape and size differentiation in white oaks: assessment of allometric relationships among three sympatric species and their hybrids. International Journal of Plant Sciences 173: 875–884. DOI: 10.1086/667234

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, Midgley JJ, Navas ML, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R. 2004. The worldwide leaf economics spectrum. Nature 428: 821–827.

Zomer RJ, Trabucco A, Bossio DA, Verchot LV. 2008. Climate change mitigation: a spatial analysis of global land suitability for clean development mechanism afforestation and reforestation. Agriculture, Ecosystems and Environment 126: 67–80. DOI: doi:10.1016/j.agee.2008.01.014

Published
2020-03-10
How to Cite
Maya-García, R., Torres-Miranda, C. A., 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(1), 50-65. https://doi.org/10.17129/botsci.2395
Section
ECOLOGY / ECOLOGÍA