Trait variation of a generalist tree species (Eremanthus erythropappus, Asteraceae) in two adjacent mountain habitats: savanna and cloud forest
Erica Rievrs Borges A G , Jamir Prado-Junior B , Lucas Deziderio Santana C , Camila Nardy Delgado A , Diego Raymundo B , José Hugo Campos Ribeiro D , Davi Rodrigo Rossatto E and Fabrício Alvim Carvalho F
+ Author Affiliations
- Author Affiliations
A Graduate Program in Ecology, Federal University of Juiz de Fora, José Lourenço Kelmer, Juiz de Fora, Brazil.
B Biology Institute, Federal University of Uberlandia, Ceara, Uberlandia, Brazil.
C Department of Forest Sciences, Federal University of Lavras, Lavras 3037, Brazil.
D Federal Institute of Southeast Minas Gerais, Coronel Monteiro de Castro, 550, Muriaé, Brazil.
E Department of Biology, Faculty of Agrarian and Veterinarian Sciences, São Paulo State University, UNESP, Professor Paulo Donato Castellane, Jaboticabal, Brazil.
F Department of Botany, Federal University of Juiz de Fora, José Lourenço Kelmer, Juiz de Fora, Brazil.
G Corresponding author. Email: ericarievrsb@gmail.com
Australian Journal of Botany 66(8) 640-646 https://doi.org/10.1071/BT18114
Submitted: 30 May 2018 Accepted: 12 December 2018 Published: 4 February 2019
Abstract
Cloud forests and savannas differ in several environmental aspects, particularly in light irradiance and water availability. Such differences can be selective for specific sets of leaves and architectural strategies to capture light and use water. In the present study we evaluated functional traits variation in a generalist species in two adjacent habitats experiencing an abrupt change in resource availability (light and water availability). We collected several leaf, stem and architectural traits of the tree species Eremanthus erythropappus (DC.) MacLeish in shrubland savanna (habitat facing higher drought stress and wind exposure) and cloud forest (shaded environment). Trees in the shrubland savanna exhibited functional trait values that enhance drought tolerance (i.e. higher wood density and leaf thickness) whereas trees in the cloud forest exhibited functional trait values that enhance light capture (i.e. taller individuals with higher leaf area and specific leaf area). Additionally, the individuals in the shrubland savanna had wider and deeper crowns, pointing that the benefits of a larger canopy area to capture light during the day and humidity from condensation at night exceed the higher risk of mechanical damage by falling debris due to high wind exposure. For all traits, variation among the individuals was lower than variation among habitats. Our results indicate the strong role of the environment as a driver of intraspecific variation and that architectural traits (usually poorly studied compared with other traits) should be included as an important parameter of variation in functional analyses when evaluating the effect of environmental conditions on tree performance.
Additional keywords: functional traits, environmental gradient, resource availability.
References
Alves LF, Santos FAM (2002) Tree allometry and crown shape of four tree species in Atlantic rain forest, south-east Brazil. Journal of Tropical Ecology 18, 245–260.| Tree allometry and crown shape of four tree species in Atlantic rain forest, south-east Brazil.Crossref | GoogleScholarGoogle Scholar |
Barros Fde V, Goulart MF, Telles SB, Lovato MB, Valladares F, de Lemos-Filho JP (2012) Phenotypic plasticity to light of two congeneric trees from contrasting habitats: Brazilian Atlantic forest versus cerrado (savanna). Plant Biology 14, 208–215.
| Phenotypic plasticity to light of two congeneric trees from contrasting habitats: Brazilian Atlantic forest versus cerrado (savanna).Crossref | GoogleScholarGoogle Scholar | 21972934PubMed |
Bates D, Mäechler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67,
| Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |
Bell LW, Williams AH, Ryan MH, Ewing MA (2007) Water relations and adaptations to increasing water deficit in three perennial legumes, Medicago sativa, Dorycnium hirsutum and Dorycnium rectum. Plant and Soil 290, 231–243.
| Water relations and adaptations to increasing water deficit in three perennial legumes, Medicago sativa, Dorycnium hirsutum and Dorycnium rectum.Crossref | GoogleScholarGoogle Scholar |
Benites VM, Schaefer CEGR, Simas FNB, Santos HG (2007) Soils associated with rock outcrops in the Brazilian mountain ranges Mantiqueira and Espinhaço. Revista Brasileira de Botanica. Brazilian Journal of Botany 30, 569–577.
| Soils associated with rock outcrops in the Brazilian mountain ranges Mantiqueira and Espinhaço.Crossref | GoogleScholarGoogle Scholar |
Bruijnzeel LA, Kappelle M, Mulligan M, Scatena FN (2011) ‘Tropical montane cloud forests: state of knowledge and sustainability perspectives in a changing world.’ (Eds LA Bruijnzeel, FN Scatena, LS Hamilton) (Cambridge University Press: Cambridge, UK)
Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Hinojosa JA, Hoffmann WA, Franco AC (2004) Processes preventing nocturnal equilibration between leaf and soil water potential in tropical savanna woody species. Tree Physiology 24, 1119–1127.
Cassiani M, Katul GG, Albertson JD (2008) The effects of canopy leaf area index on airflow across forest edges: large-eddy simulation and analytical results. Boundary-Layer Meteorology 126, 433–460.
| The effects of canopy leaf area index on airflow across forest edges: large-eddy simulation and analytical results.Crossref | GoogleScholarGoogle Scholar |
Dias HCT, Fernandes Filho EI, Schaefer CEGR, Fontes LEF, Ventorim LB (2002) Geoambientes do Parque Estadual do Ibitipoca, município de Lima Duarte-MG. Revista Árvore 26, 777–786.
| Geoambientes do Parque Estadual do Ibitipoca, município de Lima Duarte-MG.Crossref | GoogleScholarGoogle Scholar |
Ferreira GA, Prado-Junior JA, Schiavini I, Melo C (2013) Plastic responses in tree architecture and specific leaf area of Xylopia aromatica (Annonaceae): adaptations to environments with different light intensities. Revista Brasileira de Botanica. Brazilian Journal of Botany 36, 279–283.
| Plastic responses in tree architecture and specific leaf area of Xylopia aromatica (Annonaceae): adaptations to environments with different light intensities.Crossref | GoogleScholarGoogle Scholar |
Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology 21, 394–407.
| Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments.Crossref | GoogleScholarGoogle Scholar |
Goldsmith GR, Matzke NJ, Dawson TE (2013) The incidence and implications of clouds for cloud forest plant water relations. Ecology Letters 16, 307–314.
| The incidence and implications of clouds for cloud forest plant water relations.Crossref | GoogleScholarGoogle Scholar | 23216898PubMed |
Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA (2001) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126, 457–461.
| Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure.Crossref | GoogleScholarGoogle Scholar | 28547229PubMed |
Hulshof CM, Swenson NG, Weiser MD (2015) Tree height-diameter allometry across the United States. Ecology and Evolution 5, 1193–1204.
| Tree height-diameter allometry across the United States.Crossref | GoogleScholarGoogle Scholar | 25859325PubMed |
Iida Y, Poorter L, Sterck F, Kassim AR, Potts MD, Kubo T, Kohyama TS (2014) Linking size-dependent growth and mortality with architectural traits across 145 co-occurring tropical tree species. Ecology 95, 353–363.
| Linking size-dependent growth and mortality with architectural traits across 145 co-occurring tropical tree species.Crossref | GoogleScholarGoogle Scholar | 24669729PubMed |
Kohyama AT Hotta M 1990
Lichtenthaler HK, Buschmann C, Döll M, Fietz HJ, Bach T, Kozel U, Meier D, Rahmsdorf U (1981) Photosynthetic activity, chloroplast ultrastructure, and leaf characteristics of high-light and low-light plants and of sun and shade leaves. Photosynthesis Research 2, 115–141.
| Photosynthetic activity, chloroplast ultrastructure, and leaf characteristics of high-light and low-light plants and of sun and shade leaves.Crossref | GoogleScholarGoogle Scholar | 24470202PubMed |
Lohbeck M, Poorter L, Martínez-Ramos M, Rodriguez-Velázquez J, van Breugel M, Bongers F (2014) Changing drivers of species dominance during tropical forest succession. Functional Ecology 28, 1052–1058.
| Changing drivers of species dominance during tropical forest succession.Crossref | GoogleScholarGoogle Scholar |
Long W, Zang R, Schamp BS, Ding Y (2011) Within- and among-species variation in specific leaf area drive community assembly in a tropical cloud forest. Oecologia 167, 1103–1113.
| Within- and among-species variation in specific leaf area drive community assembly in a tropical cloud forest.Crossref | GoogleScholarGoogle Scholar | 21695546PubMed |
Martinelli G (2007) Mountain biodiversity in Brazil. Revista Brasileira de Botanica. Brazilian Journal of Botany 30, 587–597.
| Mountain biodiversity in Brazil.Crossref | GoogleScholarGoogle Scholar |
Mendivelso HA, Camarero JJ, Royo Obregón O, Gutiérrez E, Toledo M (2013) Differential growth responses to water balance of coexisting deciduous tree species are linked to wood density in a Bolivian tropical dry forest. PLoS One 8,
| Differential growth responses to water balance of coexisting deciduous tree species are linked to wood density in a Bolivian tropical dry forest.Crossref | GoogleScholarGoogle Scholar | 24116001PubMed |
Ogawa H, Idani G, Moore J, Pintea L, Hernandez-Aguilar A (2007) Sleeping parties and nest distribution of chimpanzees in the Savanna woodland, Ugalla, Tanzania. International Journal of Primatology 28, 1397–1412.
| Sleeping parties and nest distribution of chimpanzees in the Savanna woodland, Ugalla, Tanzania.Crossref | GoogleScholarGoogle Scholar |
Oguchi R, Hikosaka K, Hirose T (2003) Does the photosynthetic light-acclimation need change in leaf anatomy? Plant, Cell & Environment 26, 505–512.
| Does the photosynthetic light-acclimation need change in leaf anatomy?Crossref | GoogleScholarGoogle Scholar |
Oliveira RS, Dawson TE, Burgess SS (2005) Evidence for direct water absorption by the shoot of the desiccation-tolerant plant Vellozia flavicans in the savannas of central Brazil. Journal of Tropical Ecology 21, 585–588.
| Evidence for direct water absorption by the shoot of the desiccation-tolerant plant Vellozia flavicans in the savannas of central Brazil.Crossref | GoogleScholarGoogle Scholar |
Oliveira-Filho AT (2006) ‘Catálogo das Árvores Nativas de Minas Gerais: mapeamento e inventário da flora nativa e dos reflorestamentos de Minas Gerais.’ (Editora UFLA: Lavras)
Oliveira-Filho AT (2009) Classificação das fitofisionomias da América do Sul cisandina tropical e subtropical : proposta de um novo sistema – prático e flexível – ou uma injeção a mais de caos? Rodriguésia 60, 237–258.
| Classificação das fitofisionomias da América do Sul cisandina tropical e subtropical : proposta de um novo sistema – prático e flexível – ou uma injeção a mais de caos?Crossref | GoogleScholarGoogle Scholar |
Oliveira-Filho AT, Fontes MAL (2000) Patterns of floristic differentiation among Atlantic forests in southeastern Brazil and the influence of climate. Biotropica 32, 793–810.
| Patterns of floristic differentiation among Atlantic forests in southeastern Brazil and the influence of climate.Crossref | GoogleScholarGoogle Scholar |
Oliveira-Filho AT, Fontes MAL, Viana PL, Valente ASM, Salimena FRG, Ferreira FM (2013) O mosaico de fitofisionomias do Parque Estadual do Ibitipoca. In ‘Flora do Parq. Estadual do Ibitipoca e seu entorno’. (Eds R Forzza, L Menini Neto, F Salimena, D Zappi) pp. 53–94. (Editora UFJF: Juiz de Fora)
Pavoine S, Vela E, Gachet S, De Bélair G, Bonsall MB (2011) Linking patterns in phylogeny, traits, abiotic variables and space: a novel approach to linking environmental filtering and plant community assembly. Journal of Ecology 99, 165–175.
| Linking patterns in phylogeny, traits, abiotic variables and space: a novel approach to linking environmental filtering and plant community assembly.Crossref | GoogleScholarGoogle Scholar |
Pearcy RW (2007) Responses of plants to heterogeneous light environments. In ‘Functional plant ecology’. (Ed. FV Francisco Pugnaire) pp. 213–257. (CRC Press: Boca Raton, FL, USA)
Pérez-Harguindeguy N, Diaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, 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 K, Morgan HD, ter Steege H, van der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti MV, Conti G, Staver AC, Aquino S, Cornelissen JHC (2013) New handbook for standardized measurement of plant functional traits worldwide. Australian Journal of Botany 61, 167–234.
| New handbook for standardized measurement of plant functional traits worldwide.Crossref | GoogleScholarGoogle Scholar |
Pita P, Pardos JA (2001) Growth, leaf morphology, water use and tissue water relations of Eucalyptus globulus clones in response to water deficit. Tree Physiology 21, 599–607.
| Growth, leaf morphology, water use and tissue water relations of Eucalyptus globulus clones in response to water deficit.Crossref | GoogleScholarGoogle Scholar | 11390304PubMed |
Poorter L (1999) Growth responses of 15 rainforest tree species to a light gradient : the relative importance of morphological and physiological traits. Functional Ecology 13, 396–410.
Poorter L, Bongers F, Sterck F, Wöll H (2003) Architecture of 53 rain forest tree species differing in adult stature and shade tolerance. Ecology 84, 602–608.
| Architecture of 53 rain forest tree species differing in adult stature and shade tolerance.Crossref | GoogleScholarGoogle Scholar |
Poorter L, Bongers L, Bongers F (2006) Architecture of 54 moist-forest tree species: traits, trade-offs, and functional groups. Ecology 87, 1289–1301.
| Architecture of 54 moist-forest tree species: traits, trade-offs, and functional groups.Crossref | GoogleScholarGoogle Scholar | 16761607PubMed |
Pounds J, Fogden M, Campbell J (1999) Biological response to climate change on a tropical mountain. Nature 398, 611–615.
| Biological response to climate change on a tropical mountain.Crossref | GoogleScholarGoogle Scholar |
Prado-Junior JA, Schiavini I, Vale VS, Raymundo D, Lopes SF, Poorter L (2016) Functional traits shape size-dependent growth and mortality rates of dry forest tree species. Journal of Plant Ecology 10, 1–12.
| Functional traits shape size-dependent growth and mortality rates of dry forest tree species.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2017) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at: http://www.R-project.org/ (accessed 6 May 2017)
Ratnam J, Bond WJ, Fensham RJ, Hoffmann WA, Archibald S, Lehmann CER, Anderson MT, Higgins SI, Sankaran M (2011) When is a ‘forest’ a savanna, and why does it matter? Global Ecology and Biogeography 20, 653–660.
| When is a ‘forest’ a savanna, and why does it matter?Crossref | GoogleScholarGoogle Scholar |
Ratter JA, Ribeiro JF, Bridgewater S (1997) The Brazilian cerrado vegetation and threats to its biodiversity. Annals of Botany 80, 223–230.
| The Brazilian cerrado vegetation and threats to its biodiversity.Crossref | GoogleScholarGoogle Scholar |
Reich PB (2014) The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto. Journal of Ecology 102, 275–301.
| The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto.Crossref | GoogleScholarGoogle Scholar |
Ribeiro JHC, Fonseca CR, Carvalho FA (2017) The woody vegetation of quartzite soils in a mountain landscape in the Atlantic forest domain (south-eastern Brazil): structure, diversity and implications for conservation. Edinburgh Journal of Botany 74, 15–32.
| The woody vegetation of quartzite soils in a mountain landscape in the Atlantic forest domain (south-eastern Brazil): structure, diversity and implications for conservation.Crossref | GoogleScholarGoogle Scholar |
Rossatto DR, Hoffmann WA, de Carvalho Ramos Silva L, 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.
| Seasonal variation in leaf traits between congeneric savanna and forest trees in central Brazil: Implications for forest expansion into savanna.Crossref | GoogleScholarGoogle Scholar |
Scheiter S, Langan L, Higgins SI (2013) Next-generation dynamic global vegetation models: learning from community ecology. New Phytologisthytologist 198, 957–969.
| Next-generation dynamic global vegetation models: learning from community ecology.Crossref | GoogleScholarGoogle Scholar |
Scolforo JR, Araujo EG, Mello JM, Morais V, Altoe T, Ferraz-Filho AC, Scolforo H (2014) Spatial analysis of the natural regeneration of candeia (Eremanthus erythropappus (DC.) MacLeish) as influenced by non-candeia tree layer composition. Australian Journal of Basic and Applied Sciences 8, 211–219.
Shirima DD, Munishi PKT, Lewis SL, Al B (2011) Carbon storage, structure and composition of miombo woodlands in Tanzania’s Eastern Arc Mountains. African Journal of Ecology 49, 332–342.
| Carbon storage, structure and composition of miombo woodlands in Tanzania’s Eastern Arc Mountains.Crossref | GoogleScholarGoogle Scholar |
Siefert A, Violle C, Chalmandrier L, Albert CH, Taudiere A, Fajardo A, Aarssen LW, Baraloto C, Carlucci MB, Cianciaruso MV, de L. Dantas V, de Bello F, Duarte LDS, Fonseca CR, Freschet GT, Gaucherand S, Gross N, Hikosaka K, Jackson B, Jung V, Kamiyama C, Katabuchi M, Kembel SW, Kichenin E, Kraft NJB, Lagerström A, Le Bagousse-Pinguet Y, Li Y, Mason N, Messier J, Nakashizuka T, Overton JM, Peltzer DA, Pérez-Ramos IM, Pillar VD, Prentice HC, Richardson S, Sasaki T, Schamp BS, Schöb C, Shipley B, Sundqvist M, Sykes MT, Vandewalle M, Wardle DA (2015) A global meta-analysis of the relative extent of intraspecific trait variation in plant communities. Ecology Letters 18, 1406–1419.
| A global meta-analysis of the relative extent of intraspecific trait variation in plant communities.Crossref | GoogleScholarGoogle Scholar | 26415616PubMed |
Sterck FJ, Bongers F (1998) Ontogenetic changes in size, allometry, and mechanical design of tropical rain forest trees. American Journal of Botany 85, 266–272.
| Ontogenetic changes in size, allometry, and mechanical design of tropical rain forest trees.Crossref | GoogleScholarGoogle Scholar |
Sterck F, Martinéz-Ramos M, Dyer-Leal G, Rodríguez-Velazquez J, Poorter L (2003) The consequences of crown traits for the growth and survival of tree saplings in a Mexican lowland rainforest. Functional Ecology 17, 194–200.
| The consequences of crown traits for the growth and survival of tree saplings in a Mexican lowland rainforest.Crossref | GoogleScholarGoogle Scholar |
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 of the United States of America 108, 20627–20632.
| Functional traits determine trade-offs and niches in a tropical forest community.Crossref | GoogleScholarGoogle Scholar | 22106283PubMed |
Streher AS, Sobreiro JFF, Morellato LPC, Silva TSF (2017) Land surface phenology in the tropics: the role of climate and topography in a snow-free mountain. Ecosystems 20, 1436–1453.
| Land surface phenology in the tropics: the role of climate and topography in a snow-free mountain.Crossref | GoogleScholarGoogle Scholar |
Sylvia DM, Fuhrmann JJ, Hartel PG, Zuberer DA, Darmstadt TU, Hall P (1998) ‘Principles and applications of soil microbiology.’ (Prentice Hall: Upper Saddle River: NJ, USA)
Webster GL (1995) The panorama of neotropical cloud forests. In ‘Proceeding of the biodiversity and conservation of neotropical montane forests symposium’. (Eds SP Churchill, H Balslev, E Forero, JL Luteyn) pp. 53–77. (New York Botanical Gardens: New York)
Wellstein C, Poschlod P, Gohlke A, Chelli S, Campetella G, Rosbakh S, Canullo R, Kreyling J, Jentsch A, Beierkuhnlein C (2017) Effects of extreme drought on specific leaf area of grassland species: a meta-analysis of experimental studies in temperate and sub-Mediterranean systems. Global Change Biology 23, 2473–2481.
| Effects of extreme drought on specific leaf area of grassland species: a meta-analysis of experimental studies in temperate and sub-Mediterranean systems.Crossref | GoogleScholarGoogle Scholar | 28208238PubMed |
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 M-L, Niinemets Ü, 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.
| The worldwide leaf economics spectrum.Crossref | GoogleScholarGoogle Scholar | 15103368PubMed |
Živković U, Miljković D, Klisarić NB, Tarasjev A, Avramov S (2015) Seasonal variation of leaf ecophysiological traits of Iris variegata observed in two consecutive years in natural habitats with contrasting light conditions. Archives of Biological Sciences 67, 1227–1236.
| Seasonal variation of leaf ecophysiological traits of Iris variegata observed in two consecutive years in natural habitats with contrasting light conditions.Crossref | GoogleScholarGoogle Scholar |
