Abstract
Tropical forests have been rapidly converted into human-modified landscapes but the effects of such conversion on community spatial organization have been rarely addressed. In this paper, we examine to what extent the spatial reconfiguration of tropical landscapes alters plant trait distributions and the spatial organization of tree assemblages. A set of 117 tree species and 1422 individuals (≥10 cm DBH) inhabiting a fragmented Atlantic forest landscape in Brazil were assigned into categories of both vegetative and reproductive life-history traits, and matrices of trait frequencies were correlated to four spatial patch metrics via the concepts of trait-convergent, trait-divergent assembly pattern, and measures of functional richness, evenness, and diversity. Life form and seed dispersal syndrome exhibited the highest and significant degrees of trait-convergence related to connectivity and patch size gradients, respectively. Trait divergence based on seed dispersal syndrome and regeneration strategy emerged as well, particularly in response to patch area and connectivity. Finally, some functional diversity (multiple-traits) measures correlated with either a particular patch metric or species richness. Our results suggest that the spatial distribution of life-history traits and strategies exhibited by tree species correlate with spatial patch metrics, supporting the notion that human disturbances result in new environmental gradients able to spatially reorganize and restructure tree assemblages at broad spatial scales into human-modified landscapes.




Similar content being viewed by others
References
Aguiar AV, Tabarelli M (2010) Edge effects and seedling bank depletion: the role played by the early successional palm Attalea oleifera (Arecaceae) in the Atlantic forest. Biotropica 42:158–166
Arroyo-Rodríguez V, Cavender-Bares J, Escobar F, Melo FPL, Tabarelli M, Santos B (2012) Maintenance of tree phylogenetic diversity in a highly fragmented rain forest. J Ecol 100:702–711
Arroyo-Rodríguez V, Ros M, Escobar F, Melo FPL, Santos BA, Tabarelli M, Chazdon R (2013) Plant β-diversity in fragmented rain forests: testing floristic homogenization and differentiation hypotheses. J Ecol 101:1449–1458
Brandani A, Hartshorn GS, Orians GH (1988) Internal heterogeneity of gaps and species richness in a Costa Rican wet forest. J Trop Ecol 4:99–119
Briant G, Gond V, Laurance SGW (2009) Habitat fragmentation and the desiccation of forest canopies: a case study from eastern Amazonia. Biol Conserv 143:2763–2769
Carlucci M, Streit H, Duarte LDS, Pillar VD (2012) Individual-based trait analyses reveal assembly patterns in tree sapling communities. J Veg Sci 23:176–186
Cordeiro NJ, Howe HF (2001) Low recruitment of trees dispersed by animals in African forest fragments. Conserv Biol 15:1733–1741
Cornwell WK, Schwilk DW, Ackerly DD (2006) A trait-based test for habitat filtering: convex hull volume. Ecology 87:1465–1471
Debastiani VJ, Pillar VD (2012) SYNCSA—R tool for analysis of metacommunities based on functional traits and phylogeny of the community components. Bioinformatics Advance Access. http://bioinformatics.oxfordjournals.org
Denslow JS (1987) Tropical rainforest gaps and tree species diversity. Ann Rev Ecol Syst 18:431–451
Denslow JS, Hartshorn GS (1994) Tree-fall gap environments and forest dynamics processes. In: Mcdade LA, Bawa KS, Hespenheide HA, Hartshorn GS (eds) La Selva: ecology and natural history of a Neotropical rain forest. University of Chicago Press, Chicago, pp 120–127
Dohlm C, Leal IR, Tabarelli M, Meyer ST, Wirth R (2011) Leaf-cutting ants proliferate in the Amazon: an expected response to forest edge? J Trop Ecol 27:645–649
Ewers RM, Didham RK (2006) Confound factors in the detection of species responses to habitat fragmentation. Biol Rev 81:117–142
Ferraz G, Russell GJ, Stouffer PC, Bierregaard RO Jr, Pimm SL, Lovejoy TE (2003) Rates of species loss from Amazonian forest fragments. Proc Natl Acad Sci USA 100:14069–14073
Filgueiras BKC, Iannuzzi L, Leal IR (2011) Habitat fragmentation alters the structure of dung beetle communities in the Atlantic Forest. Biol Conserv 144:362–369
Forman RTT (1995) Some general principles of landscape and regional ecology. Landsc Ecol 10:133–142
Galetti M, Guevara R, Côrtes MC, Fadini R, Von Matter S, Leite AB, Labecca F, Ribeiro T, Carvalho CS, Collevatti RG, Pires MM, Guimarães PR Jr, Brancalion PH, Ribeiro MC, Jordano P (2013) Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340:1086–1090
Gibson L, Lynam AJ, Bradshaw CJA, He F, Bickford DP, Woodruff DS, Bumrungsri S, Laurance WF (2013) Near-complete extinction of native small mammal fauna 25 years after forest fragmentation. Science 341:1508–1510
Girão LC, Lopes AV, Tabarelli M, Bruna EM (2007) Changes in tree reproductive traits reduce functional diversity in a fragmented Atlantic forest landscape. PLoS One 2:e908
González-Zamora A, Arroyo-Rodríguez V, Escobar F, Rös M, Oyama K, Ibarra-Manríquez G, Stoner KE, Chapman CA (2014) Contagious deposition of seeds in spider monkeys’ sleeping trees limits effective seed dispersal in fragmented landscapes. PLoS One 9:e89346
Grime JP (2006) Trait convergence and trait divergence in herbaceous plant communities: mechanisms and consequences. J Veg Sci 17:255–260
Harper JL (1977) Population biology of plants. Academic Press, London
Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton
Ibánez I, Katz DSW, Peltier D, Wolf SM, Barrie BTC (2014) Assessing the integrated effects of landscape fragmentation on plants and plant communities: the challenge of multiprocess–multiresponse dynamics. J Ecol 102:882–895
Joner F (2012) Padrões de organização em comunidades de plantas herbáceas. PhD thesis, Graduate Program in Ecology, UFRGS, Porto Alegre
Laliberté E, Lengendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305
Laurance WF, Yensen E (1991) Predicting impacts of edge effects in fragmented habitats. Biol Conserv 55:77–92
Laurance WF, Delamônica P, Laurance SG, Vasconcelos HL, Lovejoy TE (2000) Rainforest fragmentation kills big trees. Nature 404:836
Laurance WF, Lovejoy TE, Vasconcelos HL, Bruna EM, Didham RK, Stouffer PC, Gascon C, Bierregaard RO, Laurance SG, Sampaio E (2002) Ecosystem decay of Amazonian forest fragments: a 22-year investigation. Conserv Biol 16:605–618
Laurance WF, Nascimento HEM, Laurance SG, Andrade AC, Fearnside PM, Ribeiro JEL, Capretz RL (2006a) Rain forest fragmentation and the proliferation of successional trees. Ecology 87:469–482
Laurance WF, Nascimento HEM, Laurance SG, Andrade AC, Ribeiro JELS, Giraldo GP, Lovejoy TE, Condit R, Chave J, Harms KE, D’Ângelo S (2006b) Rapid decay of tree-community composition in Amazonian forest fragments. Proc Natl Acad Sci USA 103:19010–19014
Laurance WF, Camargo JLC, Luizão RCC, Laurance SG, Pimm SL, Bruna EM, Stouffer PC, Williamson GB, Benítez-Malvido J, Vasconcelos HL, Van Houtan KS, Zartman CE, Boyle SA, Didham RK, Andrade A, Lovejoy TE (2011) The fate of Amazonian forest fragments: a 32-year investigation. Biol Conserv 144:56–67
Laurance WF, Clements GR, Sloan S, O’Connell CS, Mueller ND, Goosem M, Venter O, Edwards DP, Phalan B, Balmford A, Van Der Ree R, Arrea IB (2014) A global strategy for road building. Nature 513:229–233
Leal IR, Wirth R, Tabarelli M (2014) The multiple impacts of leaf-cutting ants and their novel ecological role in human-modified Neotropical forests. Biotropica 46:516–528
Lees AC, Peres CA (2008) Conservation value of remnant riparian forest corridors of varying quality for Amazonian birds and mammals. Conserv Biol 22:439–449
Lôbo D, Leão T, Melo FPL, Santos AMM, Tabarelli M (2011) Forest fragmentation drives Atlantic forest of northeastern Brazil to biotic homogenization. Divers Distrib 17:287–296
Lopes AV, Girão LC, Santos BA, Peres CA, Tabarelli M (2009) Long-term erosion of tree reproductive trait diversity in edge-dominated Atlantic forest fragments. Biol Conserv 142:1154–1165
Melo FPL, Dirzo R, Tabarelli M (2006) Biased seed rain in forest edges: evidence from the Brazilian Atlantic forest. Biol Conserv 132:50–60
Melo FPL, Martínez-Salas E, Benítez-Malvido J, Ceballos G (2010) Forest fragmentation reduces recruitment of large-seeded tree species in a semi-deciduous tropical forest of southern Mexico. J Trop Ecol 26:35–43
Metzger JP (1997) Relationships between landscape structure and tree species diversity in tropical forests of South-East Brazil. Landsc Urban Plan 37:29–35
Metzger JP, Martensen AC, Dixo M, Bernacci LC, Ribeiro MC, Teixeira AMG, Pardini R (2009) Time-lag in biological responses to landscape changes in a highly dynamic Atlantic forest region. Biol Conserv 142:1166–1177
Michalski F, Nishi I, Peres CA (2007) Disturbance-mediated drift in tree functional groups in Amazonian forest fragments. Biotropica 39:691–701
Moore RP, Robinson WD, Lovette IJ, Robinson TR (2008) Experimental evidence for extreme dispersal limitation in tropical forest birds. Ecol Lett 11:960–968
Munguía-Rosas MA, Jurado-Dzib SG, Mezeta-Cob CR, Montiel S, Rojas A, Pech-Canché JM (2014) Continuous forest has greater taxonomic, functional and phylogenetic plant diversity than an adjacent naturally fragmented forest. J Trop Ecol 30:323–333
Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol 15:278–285
Oliveira MA, Grillo AS, Tabarelli M (2004) Forest edge in the Brazilian Atlantic forest: drastic changes in tree species assemblages. Oryx 38:389–394
Oliveira MA, Santos AMM, Tabarelli M (2008) Profound impoverishment of the large-tree stand in a hyper-fragmented landscape of the Atlantic forest. For Ecol Manag 256:1910–1917
Orihuela RLZ, Peres CA, Mendes G, Jarencow JA, Tabarelli M (2015) Markedly divergent tree assemblage responses to tropical forest loss and fragmentation across a strong seasonality gradient. PLoS One 10:e0136018
Pacala SW, Tilman D (1994) Limiting similarity in mechanistic and spatial models of plant competition in heterogeneous environment. Am Nat 143:222–257
Paine CET, Baraloto C, Chave J, Hérault B (2011) Functional traits of individual trees reveal ecological constraints on community assembly in tropical rain forests. Oikos 120:720–727
Pakeman RJ (2011) Functional diversity indices reveal the impacts of land use intensification on plant community assembly. J Ecol 99:1143–1151
Peres-Neto PR, Jackson DA (2001) How well do multivariate data sets match? The advantages of a Procrustean superimposition approach over the Mantel test. Oecologia 129:169–178
Pillar VD, Duarte LS, Sosinski EE, Joner F (2009) Discriminating trait-convergence and divergence assembly patterns in ecological community gradients. J Veg Sci 20:334–348
Pillar VD, Blanco CC, Müller SC, Sosinski EE, Joner F, Duarte LDS (2013) Functional redundancy and stability in plant communities. J Veg Sci 24:963–974
Pinto SRR, Santos AMM, Tabarelli M (2009) Seed predation by rodents and safe sites for large-seeded trees in a fragment of the Brazilian Atlantic forest. Braz J Biol 69:763–771
Podgaiski LR, Joner F, Lavorel S, Moretti M, Ibanez S, Mendonça MS Jr, Pillar VD (2013) Spider trait assembly patterns and resilience under fire-induced vegetation change in south Brazilian Grasslands. PLoS One 8:e60207
Pütz S, Groeneveld J, Alves LF, Metzger JP, Huth A (2011) Fragmentation drives tropical forest fragments to early successional states: a modeling study for Brazilian Atlantic forests. Ecol Model 222:1986–1997
Rao CR (1982) Diversity and dissimilarity coefficients: a unified approach. Theor Popul Biol 21:24–43
Ricotta C, Szeidl L (2009) Diversity partitioning of Rao’s quadratic entropy. Theor Popul Biol 76:299–302
R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
Santos BA, Benítez-Malvido J (2012) Insect herbivory and leaf disease in natural and human disturbed habitats: lessons from early-successional Heliconia herbs. Biotropica 44:53–62
Santos BA, Peres CA, Oliveira MA, Grillo A, Alves-Costa CP, Tabarelli M (2008) Drastic erosion in functional attributes of tree assemblages in Atlantic forest fragments of northeastern Brazil. Biol Conserv 141:249–260
Santo-Silva EE, Almeida WR, Melo FPL, Zickel CS, Tabarelli M (2013) The nature of seedling assemblages in a fragmented tropical landscape: implications for forest regeneration. Biotropica 45:386–394
SAS Institute Inc. (2005) JMP® Version 6.0.0, Cary
Silva JMC, Tabarelli M (2000) Tree species impoverishment and the future flora of the Atlantic forest of northeast Brazil. Nature 404:72–74
Supp SR, Ernest SKM (2014) Species-level and community-level responses to disturbance: a cross-community analysis. Ecology 95:1717–1723
Tabarelli M, Peres CA (2002) Abiotic and vertebrate seed dispersal in the Brazilian Atlantic Forest: implications for forest regeneration. Biol Conserv 106:165–176
Tabarelli M, Mantovani W, Peres CA (1999) Effects of habitat fragmentation on plant guild structure in the montane Atlantic forest of southeastern Brazil. Biol Conserv 91:119–127
Tabarelli M, Lopes AV, Peres CA (2008) Edge-effects drive forest fragments towards an early-successional system. Biotropica 40:657–661
Tabarelli M, Aguiar AV, Girão LC, Peres CA, Lopes AV (2010a) Effects of pioneer trees species hyperabundance on forest fragments in northeastern Brazil. Conserv Biol 24:1654–1663
Tabarelli M, Aguiar AV, Ribeiro MC, Metzger JP, Peres CA (2010b) Prospects for biodiversity conservation in the Atlantic Forest: lessons from aging human-modified landscapes. Biol Conserv 143:2328–2340
Tabarelli M, Peres CA, Melo FPL (2012) The ‘few winners and many losers’ paradigm revisited: emerging prospects for tropical forest biodiversity. Biol Conserv 155:136–140
Tabarelli M, Aguiar Neto AV, Leal IR, Lopes AVF (2013) Serra Grande: Uma floresta de idéias. Editora Universitária da UFPE, Recife
Vellend M (2010) Conceptual synthesis in community ecology. Q Rev Biol 85:183–206
Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301
Acknowledgments
We are very grateful to M. Oliveira and A. Grillo for making their tree databases available to us, and to L. A. Bezerra and J. C. Bakker for authorizing our fieldwork in the Usina Serra Grande landscape. We also thank M. Lohbeck and three anonymous reviewers, who helped us to improve this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Lara Souza.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mendes, G., Arroyo-Rodríguez, V., Almeida, W.R. et al. Plant trait distribution and the spatial reorganization of tree assemblages in a fragmented tropical forest landscape. Plant Ecol 217, 31–42 (2016). https://doi.org/10.1007/s11258-015-0557-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-015-0557-6