Abstract
Over the past 10 million years, tropical savanna environments have selected for small growth forms within woody plant lineages. The result has been the evolution of subshrubs (geoxyles), presumably as an adaptation to frequent fire. To evaluate the traits associated with the shift from tree to subshrub growth forms, we compared seed biomass, germination, survival, resprouting, biomass allocation, and photosynthesis between congeneric trees and subshrubs, and quantified phylogenetic conservatism. Despite large differences in adult morphology between trees and subshrub species, the differences are modest in seedlings, and most of the variation in traits was explained by genus, indicating considerable phylogenic conservatism. Regardless, tree seedlings invested more heavily in aboveground growth, compared to subshrubs, which is consistent with the adult strategy of savanna trees, which depend on a large resistant-fire stem. Subshrub seedlings also invest in greater non-structural carbohydrate reserves, likely as an adaptation to the high fire frequencies typical of tropical savannas. The modest differences as seedlings suggest that selective pressures during early development may not have contributed substantially to the evolution of the subshrub growth form and that the distinct allocation and life history must arise later in life. This is consistent with the interpretation that the subshrub growth form arose as a life-history strategy in which maturity is reached at a small stem size, allowing them to reproduce despite repeated fire-induced topkill. The convergent evolution of subshrubs within multiple tree lineages reaffirms the importance of fire in the origin and diversification of the flora of mesic savannas.
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References
Aarssen LW (2015) Body size and fitness in plants: revisiting the selection consequences of competition. Perspect Plant Ecol Evol Syst 17:236–242. doi:10.1016/j.ppees.2015.02.004
Amaral LIV, Gaspar M, Costa PMF, Aidar MPM, Buckeridge MS (2007) Novo método enzimático rápido e sensível de extração e dosagem de amido em materiais vegetais. Hoehnea 34:425–431. doi:10.1590/S2236-89062007000400001
Archibald S, Lehmann CER, Gómez-Dans JL, Bradstock RA (2013) Defining pyromes and global syndromes of fire regimes. Proc Natl Acad Sci 110:6442–6447. doi:10.1073/pnas.1211466110
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–51. doi:10.18637/jss.v067.i01
Bellingham PJ, Sparrow AD (2000) Resprouting as a life history strategy in woody plant communities. Oikos 89:409–416. doi:10.1034/j.1600-0706.2000.890224.x
Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745. doi:10.1111/j.0014-3820.2003.tb00285.x
Bond WJ (2016) Ancient grasslands at risk. Science 351:120–122. doi:10.1126/science.aad5132
Bond WJ, van Wilgen BW (1996) Fire and plants, 1st edn. Chapman & Hall, London
Chamberlain S (2016) brranching: Fetch ‘Phylogenies’ from Many Sources. R package version 0.2.0. http://CRAN.R-project.org/package=brranching
Crisp MD, Cook LG (2012) Phylogenetic niche conservatism: what are the underlying evolutionary and ecological causes? New Phytol 196:681–694. doi:10.1111/j.1469-8137.2012.04298.x
Dantas VL, Pausas JG (2013) The lanky and the corky: fire-escape strategies in savanna woody species. J Ecol 101:1265–1272. doi:10.1111/1365-2745.12118
Davies PJ (2010) Plant hormones: biosynthesis, signal transduction, Action!, 3rd edn. Springer, Dordrecht
de Bello F et al (2015) On the need for phylogenetic ‘corrections’ in functional trait-based approaches. Folia Geobot 50:349–357. doi:10.1007/s12224-015-9228-6
Díaz S et al (2016) The global spectrum of plant form and function. Nature 529:167–171. doi:10.1038/nature16489
Eiten G (1972) The cerrado vegetation of Brazil. Bot Rev 38:201–341
Eiten G (1991) What is a herb? : With examples from the tropical “Savanna” of Brazil and the humid temperate zone of Poland. Veröffentlichungen des Geobotanischen Institutes der Eidg. Tech. Hochschule, Stiftung Rübel, in Zürich 106:288–304
Fensham RJ, Fairfax RJ, Butler DW, Bowman DMJS (2003) Effects of fire and drought in a tropical eucalypt savanna colonized by rain forest. J Biogeogr 30:1405–1414. doi:10.1046/j.1365-2699.2003.00934.x
Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand Oaks
Freckleton R et al (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726. doi:10.1086/343873
Gignoux J, Konaté S, Lahoreau G, Le Roux X, Simioni G (2016) Allocation strategies of savanna and forest tree seedlings in response to fire and shading: outcomes of a field experiment. Sci Rep 6:38838. doi:10.1038/srep38838
Gottsberger G, Silberbauer-Gottsberger I (2006) Life in the cerrado, a South American tropical seasonal ecosystem: origin, structure, dynamics and plant use. Reta Verlag, Ulm
Gupta R, Chakrabarty SK (2013) Gibberellic acid in plant. Plant Signal Behav 8:e25504. doi:10.4161/psb.25504
Hedges SB, Kumar S (2009) The timetree of life. Oxford University Press, New York
http://dharmasastra.live.cf.private.springer.com/articles/srep38838#supplementary-information
Hoffmann WA, Franco AC (2003) Comparative growth analysis of tropical forest and savanna woody plants using phylogenetically independent contrasts. J Ecol 91:475–484
Hoffmann WA, Solbrig OT (2003) The role of topkill in the differential response of savanna woody species to fire. For Ecol Manag 180:273–286. doi:10.1016/S0378-1127(02)00566-2
Hoffmann WA, Orthen B, Nascimento PKV (2003) Comparative fire ecology of tropical savanna and forest trees. Funct Ecol 17:720–726. doi:10.1111/j.1365-2435.2003.00796.x
Hoffmann WA, Orthen B, Franco AC (2004) Constraints to seedling success of savanna and forest trees across the savanna-forest boundary. Oecologia 140:252–260. doi:10.1007/s00442-004-1595-2
Hoffmann WA et al (2009) Tree topkill, not mortality, governs the dynamics of savanna-forest boundaries under frequent fire in Central Brazil. Ecology 90:1326–1337. doi:10.1890/08-0741.1
Hoffmann WA et al (2012) Ecological thresholds at the savanna-forest boundary: how plant traits, resources and fire govern the distribution of tropical biomes. Ecol Lett 15:759–768. doi:10.1111/j.1461-0248.2012.01789.x
Johnson PCD (2014) Extension of Nakagawa & Schielzeth’s R 2GLMM to random slopes models. Methods Ecol Evol 5:944–946. doi:10.1111/2041-210x.12225
Lahoreau G, Barot S, Gignoux J, Hoffmann WA, Setterfield SA, Williams PR (2006) Positive effect of seed size on seedling survival in fire-prone savannas of Australia, Brazil and West Africa. J Trop Ecol 22:719–722. doi:10.1017/s026646740600349x
Leishman MR, Wright IJ, Moles AT, Westoby M (2000) The evolutionary ecology of seed size. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities, 2nd edn. CABI Publishing, New York, pp 31–57
Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11:995–1003. doi:10.1111/j.1461-0248.2008.01229.x
Maurin O et al (2014) Savanna fire and the origins of the ‘underground forests’ of Africa. New Phytol 204:201–214. doi:10.1111/nph.12936
Michonneau F, Bolker B, Holder M, Lewis P, O’Meara B (2015) rncl: an interface to the nexus class library. R package version 0.6.0. http://CRAN.R-project.org/package=rncl
Miranda HS, Bustamante MMC, Miranda AC (2002) The fire factor. In: Oliveira PS, Marquis RJ (eds) The cerrados of Brazil: ecology and natural history of a neotropical savanna. Columbia University Press, New York, pp 51–68
Moles AT, Westoby M (2004) What do seedlings die from and what are the implications for evolution of seed size? Oikos 106:193–199. doi:10.1111/j.0030-1299.2004.13101.x
Münkemüller T et al (2012) How to measure and test phylogenetic signal. Methods Ecol Evol 3:743–756. doi:10.1111/j.2041-210X.2012.00196.x
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. doi:10.1111/j.2041-210x.2012.00261.x
Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884. doi:10.1038/44766
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290. doi:10.1093/bioinformatics/btg412
Pilon NAL, Durigan G (2017) Growing faster and colonizing first: evolutionary and ecological advantages of the tallest individuals within a cohort. Austral Ecol. doi:10.1111/aec.12479
Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50. doi:10.1111/j.1469-8137.2011.03952.x
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Raunkiaer C (1934) The life forms of plants and statistical plant geography. Clarendon Press, Oxford
Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223. doi:10.1111/j.2041-210X.2011.00169.x
Ribeiro LC, Barbosa ERM, van Langevelde F, Borghetti F (2015) The importance of seed mass for the tolerance to heat shocks of savanna and forest tree species. J Veg Sci 26:1102–1111. doi:10.1111/jvs.12314
Rossatto DR, Franco AC (2017) Expanding our understanding of leaf functional syndromes in savanna systems: the role of plant growth form. Oecologia 183:953–962. doi:10.1007/s00442-017-3815-6
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. doi:10.1007/s00468-013-0864-2
Simon MF, Pennington TR (2012) Evidence for adaptation to fire regimes in the tropical savannas of the Brazilian Cerrado. Int J Plant Sci 173:711–723. doi:10.1086/665973
Simon MF, Grether R, Queiroz LP, Skema C, Pennington 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 106:20359–20364. doi:10.1073/pnas.0903410106
Simon MF, Grether R, de Queiroz LP, Särkinen TE, Dutra VF, Hughes CE (2011) The evolutionary history of Mimosa (Leguminosae): toward a phylogeny of the sensitive plants. Am J Bot 98:1201–1221. doi:10.3732/ajb.1000520
Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Natural 108:499–506. http://www.jstor.org/stable/2459681
Stevens PF (2001 onwards) Angiosperm Phylogeny Website. Version 12, July 2012 [and more or less continuously updated since]
Swenson NG (2014) Comparative methods and phylogenetic signal. In: Swenson NG (ed) Functional and phylogenetic ecology in R. Springer, New York, pp 147–171
Vesk PA, Westoby M (2004) Sprouting ability across diverse disturbances and vegetation types worldwide. J Ecol 92:310–320. doi:10.1111/j.0022-0477.2004.00871.x
Wanntorp H-E et al (1990) Phylogenetic approaches in ecology. Oikos 57:119–132. doi:10.2307/3565745
Warming E (1908) Lagoa Santa: contribuição para a geographia phytobiologica. Imprensa Official do Estado de Minas Geraes, Belo Horizonte
Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24:2098–2100. doi:10.1093/bioinformatics/btn358
White F (1976) The underground forests of Africa: a preliminary review. Gard Bull Singap 29:57–71
Zizka A, Govender N, Higgins SI (2014) How to tell a shrub from a tree: a life-history perspective from a South African savanna. Austral Ecol 39:1–12. doi:10.1111/aec.12142
Acknowledgements
Dr. T. C. R. Williams, MSs. T. B. Moreira and W. S. Carmo provided valuable laboratorial support. V. F. Gomes, J. P. Amaral for the great help in fieldwork. This research was funded by the Brazilian Biodiversity Fund (Funbio), Brazilian Agricultural Research Corporation (Embrapa), Brazilian Research Council (CNPq) and Coordination for the Improvement of Higher Education Personnel (CAPES—Process nº 99999.009939/2014-08).
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ABG conceived, designed and performed the experiments with contributions from all authors; ABG executed the field work; ABG and WAH performed the statistical analysis. ABG, AS, WAH wrote the manuscript and provided editorial advice.
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Communicated by Fernando Valladares.
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Giroldo, A.B., Scariot, A. & Hoffmann, W.A. Trait shifts associated with the subshrub life-history strategy in a tropical savanna. Oecologia 185, 281–291 (2017). https://doi.org/10.1007/s00442-017-3930-4
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DOI: https://doi.org/10.1007/s00442-017-3930-4