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Response of leaf morphological traits of relict-endemic Symplocos species (S. coccinea and S. speciosa) to elevation and abiotic fluctuations

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Abstract

Abiotic fluctuations in montane ecosystems trigger changes in the hydric functional traits of tree species. These variations are better recognized in tree species inhabiting montane humid ravine slopes with different elevation, as is the case of many areas across the Mexican Neotropical montane forests. Little is known about the response of tree towards elevation gradients and abiotic changes. In this study, we analyzed the leaf morphological variation of two rare and Mexican endemic Symplocos species (S. coccinea and S. speciosa) occurring eastern Mexico on sites with different microclimate and elevation but similar floristic composition. We quantified how the abiotic factors (i.e. canopy openness, soil temperature, soil moisture, and litter depth) and site elevation influence the leaf traits of these tree species. Symplocos coccinea (with toothed leaf margins) is adapted to high humid conditions and high canopy coverage, while S. speciosa (with almost entire leaf margins) is resilient to environments with moisture deficit and high temperatures. Process-based research with fine-spatial scales at montane ecosystems are needed to understand the resilience and morphological variations of montane tree species under climate change worldwide. In this study, we confirmed that the Symplocos leaf morphological traits (i.e. leaf length, leaf width, leaf shape index, leaf base angle and vein density) are strongly influenced by abiotic conditions (i.e. canopy openness, litterfall depth, soil moisture and soil temperature).

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References

  • Abe N, Yamada T (2008) Variation in allometry and tree architecture among Symplocos species in a Japanese warm-temperate forest. J Plant Res 121(2):155–162

    Article  Google Scholar 

  • Alcántara-Ayala O, Luna-Vega I, Velázquez A (2002) Altitudinal distribution patterns of Mexican cloud forests based upon preferential characteristic genera. Plant Ecol 161(2):167–174

    Article  Google Scholar 

  • Alcántara-Ayala O, Oyama K, Ríos-Muñoz CA, Rivas G, Ramírez-Barahona S (2020) Morphological variation of leaf traits in the Ternstroemia lineata species complex (Ericales: Penthaphylacaceae) in response to geographic and climatic variation. PeerJ 1:e8307. https://doi.org/10.7717/peerj.8307

    Article  Google Scholar 

  • Aldrich M, Billington C, Edwards M, Laidlaw R (1997) A global directory of tropical montane cloud forests. IUCN-WCMC, Cambridge

    Google Scholar 

  • Arlot S, Celisse A (2010) A survey of cross-validation procedures for model selection. Stat Surv 4:40–79. https://doi.org/10.1214/09-SS054

    Article  Google Scholar 

  • Blackman CJ, Brodribb TJ, Jordan GJ (2010) Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytol 188(4):1113–1123. https://doi.org/10.1111/j.1469-8137.2010.03439.x

    Article  PubMed  Google Scholar 

  • Borcard D, Gillet F, Legendre P (2018) Numerical ecology with R. Springer, New York

    Book  Google Scholar 

  • Callis-Duehl K, Vittoz P, Defossez E, Rasmann S (2017) Community-level relaxation of plant defenses against herbivores at high elevation. Plant Ecol 218(3):291–304. https://doi.org/10.1007/s11258-016-0688-4

    Article  Google Scholar 

  • Dang-Le AT, Edelin C, Le-Cong K (2013) Ontogenetic variations in leaf morphology of the tropical rain forest species Dipterocarpus alatus Roxb. ex G. Don. Trees 27(3):773–786

    Article  Google Scholar 

  • FAO-UNESCO (1988) Soil map of the World. Revised legend. World Soil Resources Report 60, FAO-UNESCO, Rome

    Google Scholar 

  • Flores-Franco G, Jiménez-Ramírez J, Mora-Jarvio M (2017) Distribution and diversity of Fagaceae in Hidalgo, Mexico. Bot Sci 95(4):660–721

    Article  Google Scholar 

  • García-Gómez EI (2019) Caracterización anatómica y arquitectónica foliar de dos especies de Ternstroemia mutis ex L. f. (Ternstroemiaceae) distribuidas en los bosques templados humedos de México. Tesis de licenciatura. Universidad Nacional Autónoma de México, Mexico.

  • Givnish T (1979) On the adaptive significance of leaf form. In: Solbrig OT (ed) Topics in plant population biology. Macmillan Education, London, pp 375–407

    Google Scholar 

  • Givnish TJ (1984) Leaf and canopy adaptations in tropical forest. Physiol Ecol Plants Wet Trop 12(Sugden 1982):51–84. https://doi.org/10.1007/978-94-009-7299-5

    Article  Google Scholar 

  • Goldsmith GR, Matzke NJ, Dawson TE (2013) The incidence and implications of clouds for cloud forest plant water relations. Ecol Lett 16(3):307–314. https://doi.org/10.1111/ele.12039

    Article  PubMed  Google Scholar 

  • González-Espinosa M, Ramírez-Marcial N, Galindo-Jaimes L (2006) Secondary succession in montane pine-oak forests of Chiapas, Mexico. In: Kappelle M (ed) Ecology and conservation of Neotropical montane oak forests. Springer, New York, pp 209–221

    Chapter  Google Scholar 

  • González-Espinosa M, Meave JA, Lorea-Hernández FG, Ibarra-Manríquez G, Newton AC (2011) The red list of Mexican cloud forest trees. Fauna & Flora International, Cambridge

    Google Scholar 

  • Graham A (1976) Studies in Neotropical paleobotany. II. The Miocene communities of Veracruz, Mexico. Ann Missouri Bot Gard 4:787–842

    Article  Google Scholar 

  • Guerin GR, Wen H, Lowe AJ (2012) Leaf morphology shift linked to climate change. Biol Lett 8(5):882–886. https://doi.org/10.1098/rsbl.2012.0458

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu J, Riveros-Iregui DA (2016) Life in the clouds: are tropical montane cloud forests responding to changes in climate? Oecologia 180(4):1061–1073. https://doi.org/10.1007/s00442-015-3533-x

    Article  PubMed  Google Scholar 

  • Kappelle M (2006) Ecology and conservation of Neotropical montane oak forests. Ecological studies. Springer, Berlin

    Book  Google Scholar 

  • Kelly LM, Almeda F, Fritsch PW (2016) A taxonomic revision of Mexican and Central American Symplocos (Symplocaceae). Phytotaxa 264(1):1–115

    Article  Google Scholar 

  • Körner C (2007) The use of “altitude” in ecological research. Trends Ecol Evol 22(11):569–574. https://doi.org/10.1016/j.tree.2007.09.006

    Article  PubMed  Google Scholar 

  • Körner C (2012) Alpine treelines functional ecology of the global high elevation tree limits. Springer, Basel

    Google Scholar 

  • Körner C, Paulsen J (2004) A world-wide study of high altitude treeline temperatures. J Biogeogr 31(5):713–732. https://doi.org/10.1111/j.1365-2699.2003.01043.x

    Article  Google Scholar 

  • Li Y, Zou D, Shrestha N, Xu X, Wang Q, Jia W, Wang Z (2020) Spatiotemporal variation in leaf size and shape in response to climate. J Plant Ecol 13(1):87–96. https://doi.org/10.1093/jpe/rtz053

    Article  Google Scholar 

  • Luna-Vega I, Alcántara-Ayala O, Espinosa-Organista D, Morrone JJ (1999) Historical relationships of the Mexican cloud forests: a preliminary vicariance model applying Parsimony analysis of endemicity to vascular plant taxa. J Biogeogr 26(6):1299–1305. https://doi.org/10.1046/j.1365-2699.1999.00361.x

    Article  Google Scholar 

  • Luna-Vega I, Alcántara-Ayala O, Contreras-Medina R, Ponce-Vargas R (2006) Biogeography, current knowledge and conservation of threatened vascular plants characteristic of Mexican temperate forests. Biodivers Conserv 15(12):3773–3799. https://doi.org/10.1007/s10531-005-5401-1

    Article  Google Scholar 

  • Markesteijn L, Poorter L, Bongers F (2007) Light-dependent leaf trait variation in 43 tropical dry forest tree species. Am J Bot 94(4):515–525. https://doi.org/10.3732/ajb.94.4.515

    Article  PubMed  Google Scholar 

  • Midolo G, De Frenne P, Hölzel N, Wellstein C (2019) Global patterns of intraspecific leaf trait responses to elevation. Glob Change Biol 25(7):2485–2498. https://doi.org/10.1111/gcb.14646

    Article  Google Scholar 

  • Milla R, Reich PB (2011) Multi-trait interactions, not phylogeny, fine-tune leaf size reduction with increasing altitude. Ann Bot 107(3):455–465. https://doi.org/10.1093/aob/mcq261

    Article  PubMed  PubMed Central  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2016) vegan: community ecology package. R package version 2.4-3. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Oliveira RS, Eller CB, Bittencourt PRL, Mulligan M (2014) The hydroclimatic and ecophysiological basis of cloud forest distributions under current and projected climates. Ann Bot 113(6):909–920. https://doi.org/10.1093/aob/mcu060

    Article  PubMed  PubMed Central  Google Scholar 

  • Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen–Geiger climate classification. Hydrol Earth Syst Sci 11(5):1633–1644. https://doi.org/10.5194/hess-11-1633-2007

    Article  Google Scholar 

  • Pfennigwerth AA, Bailey JK, Schweitzer JA (2017) Trait variation along elevation gradients in a dominant woody shrub is population-specific and driven by plasticity. AoB PLANTS. https://doi.org/10.1093/aobpla/plx027

    Article  PubMed  PubMed Central  Google Scholar 

  • Rahbek C, Borregaard MK, Antonelli A, Colwell RK, Holt BG, Nogues-Bravo D, Rasmussen CMØ, Richardson K, Rosing MT, Whittaker RJ, Fjeldså J (2019) Building mountain biodiversity: geological and evolutionary processes. Science 365(6458):1114–1119. https://doi.org/10.1126/science.aax0151

    Article  CAS  PubMed  Google Scholar 

  • Read QD, Moorhead LC, Swenson NG, Bailey JK, Sanders NJ (2014) Convergent effects of elevation on functional leaf traits within and among species. Funct Ecol 28(1):37–45. https://doi.org/10.1111/1365-2435.12162

    Article  Google Scholar 

  • Rodríguez-Ramírez EC, Sánchez-González A, Ángeles-Pérez G (2016) Relationship between vegetation structure and microenvironment in Fagus grandifolia subsp. mexicana forest relicts in Mexico. J Plant Ecol 11(2):237–247. https://doi.org/10.1093/jpe/rtw138

    Article  Google Scholar 

  • Rodríguez-Ramírez EC, Vázquez-García JA, García-González I, Alcántara-Ayala O, Luna-Vega I (2020a) Drought effects on the plasticity in vessel traits of two endemic Magnolia species in the tropical montane cloud forests of eastern Mexico. J Plant Ecol 13(3):331–340. https://doi.org/10.1093/jpe/rtaa019

    Article  Google Scholar 

  • Rodríguez-Ramírez EC, Valdez-Nieto JA, Vázquez-García JA, Dieringer G, Luna-Vega I (2020b) Plastic responses of Magnolia schiedeana Schltdl., a relict-endangered Mexican cloud forest tree, to climatic events: evidences from leaf venation and wood vessel anatomy. Forests 11(7):737. https://doi.org/10.3390/f11070737

    Article  Google Scholar 

  • 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. Int J Plant Sci 167(1):11–18. https://doi.org/10.1086/497995

    Article  Google Scholar 

  • Rzedowski J, de Rzedowski GC (1995) Flora del Bajío y de regiones adyacentes. Familia Geraniaceae. Fascículo 40. Instituto de Ecología A.C., Centro Regional del Bajío.

  • Sack L, Frole K (2006) Leaf structural diversity is related to hidraulic capacity in tropical rain forest trees. Ecology 87:483–491

    Article  Google Scholar 

  • 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. Nat Commun 3(1). https://doi.org/10.1038/ncomms1835

  • Viechtbauer W (2010) Conducting meta-analyses in R with the metafor. J Stat Softw 36(3):1–48

    Article  Google Scholar 

  • Wickham H (2016) ggplot2: elegant graphics for data analysis. In: Gentleman K, Hornik R, Parmigiani G (eds) 2nd edition, Springer, Houston

  • Williams-Linera G (1999) Leaf dynamics in a tropical cloud forest: phenology, herbivory, and life span. Selbyana 20(1):98–105

    Google Scholar 

  • Williams-Linera G, Devall MS, Alvarez-Aquino C (2000) A relict population of Fagus grandifolia var. mexicana at the Acatlán Volcano, Mexico: structure, litterfall, phenology and dendroecology. J Biogeogr 27(6):1297–1309. https://doi.org/10.1046/j.1365-2699.2000.00500.x

    Article  Google Scholar 

  • World Conservation Monitoring Centre (1998) Symplocos coccinea. The IUCN Red List of Threatened Species 1998: T30845A9582491. https://doi.org/10.2305/IUCN.UK.1998.RLTS.T30845A9582491

  • 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(6354):917–921. https://doi.org/10.1126/science.aal4760

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Yan H, Li B, Han Y, Song B (2018) Spatial distribution patterns of Symplocos congeners in a subtropical evergreen broad-leaf forest of southern China. J For Res 29(3):773–784. https://doi.org/10.1007/s11676-017-0451-2

    Article  CAS  Google Scholar 

  • Zhao W-L, Chen Y-J, Brodribb TJ, Cao K-F (2016) Weak co-ordination between vein and stomatal densities in 105 angiosperm tree species along altitudinal gradients in southwest China. Funct Plant Biol 43(12):1126–1133. https://doi.org/10.1071/FP16012

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors thank Alicia Rojas-Leal who helped with laboratory assistance.

Funding

This research was funded by the DGAPA PAPIIT IN223218 and IN220621 projects. The first author acknowledges the financial support granted by the postdoctoral fellowship CONACYT 2019–2020.

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Authors and Affiliations

  1. Laboratorio de Biogeografía y Sistemática, Facultad de Ciencias, Universidad Nacional Autónoma de México, Mexico City, Mexico

    Ernesto Chanes Rodríguez-Ramírez, María del Refugio Martínez-Mejía & Isolda Luna-Vega

  2. Division of Forest Biodiversity, Korea National Arboretum, Pocheon, 11186, Korea

    Balkrishna Ghimire

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  1. Ernesto Chanes Rodríguez-Ramírez
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  2. María del Refugio Martínez-Mejía
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  3. Balkrishna Ghimire
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  4. Isolda Luna-Vega
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Contributions

ECR-R and MDRM-M: Conceptualization, Methodology, Investigation, Supervision, Writing – review & editing. BG: Writing – review & editing. IL-V: Conceptualization, Investigation, Supervision, Writing – review & editing.

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Correspondence to Isolda Luna-Vega.

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Communicated by George Yan.

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Rodríguez-Ramírez, E.C., Martínez-Mejía, M.d.R., Ghimire, B. et al. Response of leaf morphological traits of relict-endemic Symplocos species (S. coccinea and S. speciosa) to elevation and abiotic fluctuations. Plant Ecol 222, 693–704 (2021). https://doi.org/10.1007/s11258-021-01138-0

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