Abstract
Intraspecific trait variability plays a fundamental role in community structure and dynamics; however, few studies have evaluated its relative importance to the overall response of communities to environmental pressures. Since fire is considered a key factor in Neotropical savannas, we investigated to what extent the functional effects of fire in a Brazilian savanna occurs via intra- or interspecific trait variability. We sampled 12 traits in communities subjected to three fire regimes in the last 12 years: annual, biennial, and protected. To evaluate fire’s relative effects, we fitted a general linear mixed models with species as random and fire as fixed factors, using: (1) all species in the communities (i.e., considering intra- and interspecific variabilities); (2) 18 species common to all fire regimes (i.e., intraspecific variability only); and (3) all species with their overall average trait values (i.e., interspecific variability only). We assessed the relative role of intra- or interspecific variability by comparing the significance of each trait in the three analyses. We also compared the within and between fire variabilities with a variance component analysis. Five traits presented larger intraspecific than interspecific variability, and the main effect of fire occurred at the intraspecific level. These results confirm that it is important to consider intraspecific variability to fully understand fire-prone communities. Moreover, trait variability was larger within than among fire regimes. Thus, fire may act more as an external filter, preventing some of the species from the regional pool from colonizing the cerrado, than as an internal factor structuring the already filtered cerrado communities.
Similar content being viewed by others
References
Albert CH, Thuiller W, Yoccoz NG, Soudant A, Boucher F, Saccone P, Lavorel S (2010) Intraspecific functional variability: extent, structure and sources of variation. J Ecol 98:604–613. doi:10.1016/j.ppees.2011.11.004
Allen SE (1989) Chemical analysis of ecological materials. Blackwell, Oxford
Berling DJ, Osborn CP (2006) The origin of the savanna biome. Glob Change Biol 12:2023–2031. doi:10.1111/j.1365-2486.2006.01239.x
Bolnick DI, Amarasekare P, Araújo MS, Bürger R, Levine JM, Novak M, Rudolf VHW, Schreiber SJ, Urban MC, Vasseur DA (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26:183–192. doi:10.1016/j.tree.2011.01.009
Chapin FS III, Autumn K, Pugnaire F (1993) Evolution of suites of traits in response to environmental stress. Am Nat 142:S78–S92
Cianciaruso MV, Silva IA, Batalha MA, Gaston KJ, Petchey OL (2012) The influence of fire on phylogenetic and functional structure of woody savannas: moving from species to individuals. Perspect Plant Ecol Evol Syst. doi: 10.1016/j.ppees.2011.11.004
Coley PD, Bryant JP, Chapin FS III (1985) Resource availability and plant antiherbivore defense. Science 230:895–899
Conservation International (1999) Ações prioritárias para a conservação do Cerrado e do Pantanal. Conservation International, Brasília
Cornelissen JHC, Lavorel S, Garniel E, Díaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardized and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380. doi:10.1071/BT02124
Coutinho LM (1990) Fire in the ecology of the Brazilian Cerrado. In: Goldammer JG (ed) Fire in the tropical biota: ecosystem processes and global challenges. Ecological Studies. Springer, Berlin, pp 82–105
Craine JM (2009) Resource strategies of wild plants. Princeton University Press, New Jersey
Dantas VL, Batalha MA (2011) Vegetation structure: fine scale relationships with soil in a cerrado site. Flora 206:341–346. doi:10.1016/j.flora.2010.11.003
de Bello F, Lavorel S, Albert CH, Thuiller W, Grigulis K, Dolezal J, Janecek S, Leps J (2010) Quantifying the relevance of intraspecific trait variability for functional diversity. Methods Ecol Evol 2:163–174. doi:10.1111/j.2041-210X.2010.00071.x
França H, Ramos-Neto MB, Setzer A (2007) O fogo no Parque Nacional das Emas. Biodiversidade. Ministério do Meio Ambiente, Brasília
Gurvich DE, Enrico L, Cingolani AM (2005) Linking plant functional traits with post-fire sprouting vigour in woody species in central Argentina. Austral Ecol 30:789–796. doi:10.1111/j.1442-9993.2005.01522.x
He T, Pausas JG, Belcher CM, Schwilk DW, Lamont BB (2012) Fire-adapted traits of Pinus arose in the fiery Cretaceous. New Phytol 194:751–759. doi:10.1111/j.1469-8137.2012.04079.x
Higgins SI, Bond WJ, February EC, Bronn A, Euston-Brown DIW, Enslin B, Govender N, Rademan L, O’Regan S, Potgieter ALF (2007) Effects of four decades of fire manipulation on woody vegetation structure in savanna. Ecology 88:1119–1125. doi:10.1890/06-1664
Hoffmann WA, Franco AC (2003) Comparative growth analysis of tropical forest and savanna woody plants using phylogenetically independent contrasts. J Ecol 91:475–484. doi:10.1046/j.1365-2745.2003.00777.x
Jackson JF, Adams DC, Jackson UB (1999) Allometry of constitutive defense: a model and a comparative test with tree bark and fire regime. Am Nat 153:614–632. doi:10.1086/303201
Jung V, Violle C, Mondy C, Hoffmann L, Muller S (2010) Intraspecific variability and trait-based community assembly. J Ecol 98:1134–1140. doi:10.1111/j.1365-2745.2010.01687.x
Keeley JE, Zedler PH (1998) Evolution of life histories in Pinus. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 219–250
Keeley JE, Pausas JG, Rundel PW, Bond WJ, Bradstock RA (2011) Fire as an evolutionary pressure shaping plant traits. Trends Plant Sci 16:406–411. doi:10.1016/j.tplants.2011.04.002
Keeley JE, Bond WJ, Bradstock RA, Pausas JG, Rundel PW (2012) Fire in Mediterranean ecosystems: ecology, evolution and management. Cambridge University Press, Cambridge
Kersch-Becker MF, Lewinsohn TM (2012) Bottom-up multitrophic effects in resprouting plants. Ecology 93:9–16. doi:10.1890/11-0756.1
Köppen W (1931) Grundriss der Klimakunde. Gruyter, Berlin
Kraft NJB, Ackerly DD (2010) Functional trait and phylogenetic tests of community assembly across spatial scales in an Amazonian forest. Ecol Monogr 80:401–422. doi:10.1890/09-1672.1
Lopes CT, Vasconcelos HL (2011) Fire increases insect herbivory in a neotropical savanna. Biotropica 43:612–618. doi:10.1111/j.1744-7429.2011.00757.x
McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185
McLaughlin SB, Wimmer R (1999) Calcium physiology and terrestrial ecosystem processes. New Phytol 142:373–417. doi:10.1046/j.1469-8137.1999.00420.x
Messier J, McGill BJ, Lechowicz MJ (2010) How do traits vary across ecological scales? A case for trait-based ecology. Ecol Lett 13:838–848. doi:10.1111/j.1461-0248.2010.01476.x
Miranda HS, Sato MN, Neto WN, Aire FS (2009) The fire factor. In: Cochrane MA (ed) Tropical fire ecology: climate change, land use, and ecosystem dynamics. Springer, New York, pp 427–450
Moreira B, Tavsanoglu Ç, Pausas JG (2012a) Local versus regional intraspecific variability in regeneration traits. Oecologia 168:671–677. doi:10.1007/s00442-011-2127-5
Moreira B, Tormo J, Pausas JG (2012b) To resprout or not to resprout: factors driving intraspecific variability in resprouting. Oikos. doi:10.1111/j.1600-0706.2011.20258.x
Moretti M, Legg C (2009) Combining plant and animal traits to assess community functional responses to disturbance. Ecography 32:299–309. doi:10.1111/j.1600-0587.2008.05524.x
Müller-Dombois D, Ellenberg H (1974) Aims and methods of vegetation ecology. Wiley, New York
Pausas JG, Keeley JE (2009) A burning story: the role of fire in the history of life. Bioscience 59:593–601. doi:10.1525/bio.2009.59.7.10
Pausas JG, Verdú M (2008) Fire reduces morphospace occupation in plant communities. Ecology 89:2181–2186. doi:10.1890/07-1737.1
Pausas JG, Verdú M (2010) The jungle of methods for evaluating phenotypic and phylogenetic structure of communities. Bioscience 60:614–625. doi:10.1525/bio.2010.60.8.7
Pausas JG, Bradstock RA, Keith DA, Keeley JE, The GCTE (Global Changes of Terrestrial Ecosystems) Fire Network (2004) Plant functional traits in relation to fire in crown-fire ecosystems. Ecology 85:1085–1100. doi:10.1890/02-4094
Pausas JG, Alessio G, Moreira B, Corcobado G (2012) Fires enhance flammability in Ulex parviflorus. New Phytol 193:18–23. doi:10.1111/j.1469-8137.2011.03945.x
Pivello VR, Coutinho LM (1992) Transfer of macro-nutrients to the atmosphere during experimental burnings in an open cerrado (Brazilian savanna). J Trop Ecol 8:487–497. doi:10.1017/S0266467400006829
R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Ramos-Neto MB, Pivello VR (2000) Lightning fires in a Brazilian savanna National Park: rethinking management strategies. Environ Manag 26:675–684. doi:10.1007/s002670010124
Rasband W (2004) ImageJ: Image process and analysis in Java. National Institutes of Health, Bethesda
Ruggiero P, Batalha MA, Pivello VR, Meirelles ST (2002) Vegetation-soil relationship in cerrado (Brazilian savanna) and semideciduous forest, Southeastern Brazil. Plant Ecol 160:1–16. doi:10.1023/A:1015819219386
Saura-Mas S, Lloret F (2007) Leaf and shoot water content and leaf dry matter content of mediterranean woody species with different post-fire regenerative strategies. Ann Bot 99:545–554. doi:10.1093/aob/mcl284
Silva DM, Batalha MA (2008) Soil–vegetation relationships in cerrados under different fire frequencies. Plant Soil 311:87–96. doi:10.1007/s11104-008-9660-y
Silva IA, Batalha MA (2010) Woody plant species co-occurrence in Brazilian savannas under different fire frequencies. Acta Oecol 36:85–91. doi:10.1016/j.actao.2009.10.004
Simon MF, Gretherc R, Queiroz LP, Skemae C, Penningtone RT, Hughes CE (2009) Recent assembly of the Cerrado, a Neotropical plant diversity hotspot, by in situ evolution of adaptations to fire. Proc Natl Acad Sci USA 48:20359–20364. doi:10.1073/pnas.0903410106
Unesco, United Nations Educational, Scientific, and Cultural Organization (2001) Cerrado protected areas: Chapada dos Veadeiros and Emas National Parks. http://whc.unesco.org/en/list/1035. Accessed on 14-May-2012
Verdú M, Pausas JG (2007) Fire drives phylogenetic clustering in Mediterranean Basin woody plant communities. J Ecol 95:1316–1323. doi:10.1111/j.1365-2745.2007.01300.x
Violle C, Enquist BJ, McGill BJ, Jiang L, Albert CH, Hulshof C, Jung V, Messier J (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27:244–252. doi:10.1016/j.tree.2011.11.014
Ward D, Spiegel M, Saltz D (1997) Gazelle herbivory and interpopulation differences in calcium oxalate content of leaves of a desert lily. J Chem Ecol 23:333–346. doi:10.1023/B:JOEC.0000006363.34360.9d
Weiher E, Keddy PA (1995) The assembly of experimental wetland plant communities. Oikos 73:323–335
Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol Syst 33:125–159. doi:10.1146/annurev.ecolsys.33.010802.150452
Wilson JB (1999) Assembly rules in plant communities. In: Weiher E, Keddy P (eds) Ecological assembly rules: perspectives, advances retreats. Cambridge University Press, Cambridge, pp 130–164
Wright IJ, Reich PB, Cornelisen JHC, Falster DS, Groom PK, Hikosaka K, Lee W, Lusk CH, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Warton DI, Westoby M (2005) Modulation of leaf economic traits and trait relationships by climate. Glob Ecol Biogeogr 14:411–421. doi:10.1111/j.1466-822x.2005.00172.x
Acknowledgments
We are grateful to Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support and scholarships granted to the authors; to Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA). for research permission; to Emas National Park staff. for logistical assistance; to P.K. Amorim, S.P. Campos, C.A. Casali, I.A. Silva, A.V.F. Jardim, M.O. Maia, L.T. Manica, F.Q. Martins, D.M. Silva, and L. Sims for helping us in fieldwork; and to Charlotte Reemts for kindly revising the English. J.G.P. acknowledges the support from the VIRRA project (CGL2009-12048/BOS; the Spanish Government). The study complies with the current laws of Brazil.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Jon Keeley.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Dantas, V.d.L., Pausas, J.G., Batalha, M.A. et al. The role of fire in structuring trait variability in Neotropical savannas. Oecologia 171, 487–494 (2013). https://doi.org/10.1007/s00442-012-2431-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-012-2431-8