Journal of Insect Conservation

, Volume 20, Issue 3, pp 539–548 | Cite as

Fruit-feeding butterflies in edge-dominated habitats: community structure, species persistence and cascade effect

  • Bruno K. C. Filgueiras
  • Douglas H. A. Melo
  • Inara R. Leal
  • Marcelo Tabarelli
  • André Victor L. Freitas
  • Luciana Iannuzzi


As old-growth forests are converted into edge-affected habitats, a substantial proportion of tropical biodiversity is potentially threatened. Here, we examine a comprehensive set of community-level attributes of fruit-feeding butterfly assemblages inhabiting edge-affected habitats in a fragmented Atlantic forest landscape devoted to sugar cane production. We also explored whether the consequences of habitat loss and fragmentation can interact and cause cascading ecosystem changes, with the pervasive simplification of tree assemblages inhabiting edge-dominated habitats, altering fruit-feeding butterfly persistence. Butterflies were sampled in three forest habitats: small fragments, forest edges and patches of forest interior of a primary forest fragment. Assemblage attributes, including taxonomic composition, correlated to some patch (patch size) and landscape (such as forest cover) metrics as well as habitat structure (tree density and richness). Fruit-feeding butterfly assemblages in the forest interior differed from those in small fragments due to an increased abundance of edge-specialist species. On the other hand, several forest-dependent species were missing in both small fragments and forest edges. Our results suggest that edge-affected habitats dominated by pioneer tree species support taxonomically distinct assemblages, including the presence of disturbance-adapted species, and butterfly community structure is highly sensitive to fragmentation- and plant-related variables, such as forest cover and pioneer tree species. In this way, while the establishment of human-modified landscapes probably results in the local extirpation of forest-dependent species, it allows the persistence of disturbance-adapted species. Thus, forest-dependent species conservation and the plant–animal interaction webs they support could be improved by retaining a significant amount of core forest habitat.


Butterflies Edge-affected habitats Fragmentation Nymphalidae Pioneer trees 



We thank Luis Antônio Bezerra and José Clodoaldo Bakker for authorizing our fieldwork at Usina Serra Grande and Conservação Internacional do Brasil (CI Brasil) for providing aerial photographs of Usina Serra Grande. We are also grateful to ‘Coordenação de Aperfeiçoamento de Pessoal de Nível Superior’ (CAPES) for financial support (PNPD process 02488/09-4) and to ‘Conservação Internacional do Brasil’, ‘Centro de Estudos Ambientais do Nordeste’ (CEPAN) and ‘Usina Serra Grande’ for infrastructure and logistic support during fieldwork. IRL and MT thank the ‘Conselho Nacional de Desenvolvimento Científico e Tecnológico’ (CNPq) for research Grants (Grants 302574/2010-7 and 304598/2011-9). BKCF and DHAM acknowledge ‘Programa de Pós Graduação em Biologia Animal’ (PPGBA-UFPE), and DHAM is grateful for post-graduate fellowships from Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE). AVLF thanks ICMBio for the research permits (SISBIO #10802-5), CNPq for research Grants (process #302585/2011-7, 303834/2015-3 and SISBIOTA-Brasil/CNPq #563332/2010-7), FAPESP (BIOTA-FAPESP Program, Grants #2011/50225-3 and #2013/50297-0) and the National Science Foundation (DEB-1256742).

Supplementary material

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Supplementary material 1 (DOC 35 kb)
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Supplementary material 4 (DOC 65 kb)


  1. Barlow J, Gardner TA, Araujo IS et al (2007a) Quantifying the biodiversity value of tropical primary, secondary and plantation forests. Proc Natl Acad Sci USA 104:18555–18560CrossRefPubMedPubMedCentralGoogle Scholar
  2. Barlow J, Overal WL, Araujo IS, Gardner TA, Peres CA (2007b) The value of primary, secondary and plantation forests for fruit feeding butterflies in the Brazilian Amazon. J Appl Ecol 44:1001–1012CrossRefGoogle Scholar
  3. Benchimol M, Peres C (2013) Anthropogenic modulators of species-area relationships in Neotropical primates: a continental-scale analysis of fragmented forest landscapes. Divers Distrib 19:1339–1352CrossRefGoogle Scholar
  4. Benedick S, Hill JK, Mustaffa N, Chey VK, Maryati M, Searle JB, Schilthuizen M, Hamer KC (2006) Impacts of rain forest fragmentation on butterflies in northern Borneo: species richness, turnover and the value of small fragments. J Appl Ecol 43:967–977CrossRefGoogle Scholar
  5. Bobo KS, Walter M, Fermon H, Njokagbor J, Mühlenberg M (2006) From forest to farmland: butterfly diversity and habitat associations along a gradient of forest conversion in Southwestern Cameroon. J Insect Conserv 10:29–42CrossRefGoogle Scholar
  6. Bonebrake TC, Ponisio LC, Boggs CL, Ehrlich PR (2010) More than just indicators: a review of tropical butterfly ecology and conservation. Biol Conserv 143:1831–1841CrossRefGoogle Scholar
  7. Brook BW, Bradshaw CJA, Koh LP, Sodhi NS (2006) Momentum drives the crash: mass extinction in the tropics. Biotropica 38:302–305CrossRefGoogle Scholar
  8. Brown KS (1992) Borboletas da Serra do Japi: diversidade, habitats, recursos alimentares e variação temporal. In: Morellato LPC (ed) História Natural da Serra do Japi: Ecologia e Preservação de uma Área Florestal no Sudeste do Brasil. Editora Unicamp, Campinas, pp 142–186Google Scholar
  9. Brown KS, Hutchings RW (1997) Disturbance, fragmentation, and the dynamics of diversity in Amazonian butterflies. In: Laurance WF, Bierregaard ROJR (eds) Tropical forest remnants. University of Chicago Press, Chicago, pp 91–110Google Scholar
  10. Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, PlymouthGoogle Scholar
  11. Collier N, Gardner M, Adams M, Mcmahon CR, Benkendorff K, Mackay DA (2010) Contemporary habitat loss reduces genetic diversity in an ecologically specialized butterfly. J Biogeogr 37:1277–1287CrossRefGoogle Scholar
  12. Colwell RK (2013) Estimates: statistical estimation of species richness and shared species from samples, Version 9·1.0 User’s GUIDE and application. Accessed 12 Oct 2015
  13. DeVries PJ (1987) The butterflies of Costa Rica and their natural history. Vol I. Papilionidae, Pieridae, and Nymphalidae. Princeton University Press, New JerseyGoogle Scholar
  14. Estrada A, Anzures A, Coates-Estrada R (1999) Tropical rain forest fragmentation, howler monkeys (Alouatta palliata), and dung beetles at Los Tuxtlas, Mexico. Am J Primatol 48:253–262CrossRefPubMedGoogle Scholar
  15. Ewers RM, Didham RK (2007) Continuous response functions for quantifying the strength of edge effects. Conserv Biol 21(4):926–936CrossRefPubMedGoogle Scholar
  16. Filgueiras BKC, Iannuzzi L, Leal IR (2011) Habitat fragmentation alters the structure of dung beetle communities in the Atlantic Forest. Biol Conserv 144:362–369CrossRefGoogle Scholar
  17. Filgueiras BKC, Tabarelli M, Leal IR, Vaz-de-Mello F, Iannuzzi L (2015) Dung beetle persistence in human modified landscapes: combining species indicators with anthropogenic land use and fragmentation-related effects. Ecol Indic 55:65–73CrossRefGoogle Scholar
  18. Freitas AVL, Iserhard CA, Santos JP, Carreira JYO, Ribeiro DB, Melo DHA, Rosa AHB, Marini-Filho OJ, Accacio GM, Uehara-Prado M (2014) Studies with butterfly bait traps: an overview. Rev Colomb Entomol 40:209–218Google Scholar
  19. Gardner TA, Barlow J, Parry LW, Peres CA (2007) Predicting the uncertain future of tropical forest species in a data vacuum. Biotropica 39:25–30CrossRefGoogle Scholar
  20. Gardner TA, Barlow J, Chazdon R, Ewers RM, Harvey CA, Peres CA, Sodhi NS (2009) Prospects for tropical forest biodiversity in a human-modified world. Ecol Lett 12:561–582CrossRefPubMedGoogle Scholar
  21. Gorresen PM, Willig MR (2004) Landscape responses of bats to habitat fragmentation in Atlantic forest of Paraguay. J Mamm 85:688–697CrossRefGoogle Scholar
  22. Gotelli NJ, Colwell RK (2001) Estimating species richness. In: Magurran AE, McGill BJ (eds) Biological diversity: frontiers in measurement and assessment. Oxford University Press, Oxford, pp 39–54Google Scholar
  23. Grillo A, Oliveira MA, Tabarelli M (2006) Arvores. In: Porto KC, Almeida-Cortez JS, Tabarelli M (eds) Diversidade biológica e conservação da floresta Atlântica ao norte do Rio São Francisco. Ministério do Meio Ambiente-Governo do Brasil, Brasília, Brasil, pp 191–216Google Scholar
  24. Hawes J, Barlow J, Gardner TA, Peres CA (2008) The value of forest strips for understorey birds in an Amazonian plantation landscape. Biol Conserv 141:2262–2278CrossRefGoogle Scholar
  25. Horner-Devine MC, Daily GC, Ehrlich PR, Boggs CL (2003) Countryside biogeography of tropical butterflies. Conserv Biol 17:168–177CrossRefGoogle Scholar
  26. IBGE (1985) Atlas Nacional do Brasil: Região Nordeste. Instituto Brasileiro de Geografia e Estatística, Rio de JaneiroGoogle Scholar
  27. Koh LP, Dunn RR, Sodhi NS, Colwell RK, Proctor HC, Smith VS (2004) Species coextinctions and the biodiversity crisis. Science 305:1632–1634CrossRefPubMedGoogle Scholar
  28. Laurance WF, Ferreira LV, Rankin-de-Merona JM, Laurance SG (1998) Rain forest fragmentation and the dynamics of Amazonian tree communities. Ecology 79:2032–2040CrossRefGoogle Scholar
  29. Laurance WF, Delamonica P, Laurance SG, Vasconcelos HL, Lovejoy TE (2000) Rainforest fragmentation kills big trees. Nature 404:836–836CrossRefPubMedGoogle Scholar
  30. Laurance WF, Lovejoy LE, Vasconcelos HL, Bruna EM, Didham RK, Stouffer PC, Gascon C, Bierregaard Jr RO, Laurance SG, Sampaio E (2002) Ecosystem decay of Amazonian forest fragments: a 22-year investigation. Conserv Biol 16:605–618CrossRefGoogle Scholar
  31. Leal IR, Filgueiras BKC, Gomes JP, Iannuzzi I, Andersen A (2012) Effects of habitat fragmentation on ant richness and functional composition in Brazilian Atlantic Forest. Biodivers Conserv 21:1687–1701CrossRefGoogle Scholar
  32. 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 46:516–528CrossRefGoogle Scholar
  33. Leidner AK, Haddad NM, Lovejoy TE (2010) Does tropical forest fragmentation increase long-term variability of butterfly communities? PLoS ONE 5(3):e9534CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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 142:1154–1165CrossRefGoogle Scholar
  35. Melo FPL, Dirzo R, Tabarelli M (2006) Biased seed rain in forest edges: evidence from the Brazilian Atlantic forest. Biol Conserv 132:50–60CrossRefGoogle Scholar
  36. Melo FPL, Arroyo-Rodríguez V, Fahrig L, Martínez-Ramos LM, Tabarelli M (2013) On the hope for biodiversity-friendly tropical landscapes. Trends Ecol Evol 28:462–468CrossRefPubMedGoogle Scholar
  37. Mendes G, Arroyo-Rodríguez V, Almeida VR, Pinto SRR, Pillar VD, Tabarelli M (2016) Plant trait distribution and the spatial reorganization of tree assemblages ina fragmented tropical forest landscape. Plant Ecol 217:31–42CrossRefGoogle Scholar
  38. Michalski F, Nishi I, Peres CA (2007) Disturbance-mediated drift in tree functional groups in Amazonian forest fragments. Biotropica 39:691–701CrossRefGoogle Scholar
  39. Morellato LPC, Talora DC, Takahasi A, Bencke CC, Romera EC, Zipparro VB (2000) Phenology of Atlantic rain forest trees: a comparative study. Biotropica 32:811–823CrossRefGoogle Scholar
  40. Norden N, Chazdon RL, Chao A, Jiang YH, Vílchez-Alvarado B (2009) Resilience of tropical rain forests: tree community reassembly in secondary forests. Ecol Lett 12:385–394CrossRefPubMedGoogle Scholar
  41. Nyafwono M, Valtonen A, Nyeko P, Roininen H (2014) Butterfly community composition across a successional gradient in a human-disturbed Afro-tropical rain forest. Biotropica 46:210–218CrossRefGoogle Scholar
  42. Oliveira MA, Grillo AS, Tabarelli M (2004) Forest edge in the Brazilian Atlantic forest: drastic changes in tree species assemblages. Oryx 38:389–394CrossRefGoogle Scholar
  43. Pardini R (2004) Effects of forest fragmentation on small mammals in an Atlantic Forest landscape. Biodivers Conserv 13:2567–2586CrossRefGoogle Scholar
  44. Pimentel DS, Tabarelli M (2004) Seed dispersal of the palm Attalea oleifera in a remnant of the Brazilian Atlantic forest. Biotropica 36:74–84CrossRefGoogle Scholar
  45. R Development Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing.
  46. Ribeiro DB, Freitas AVL (2012) The effect of reduced-impact logging on fruit-feeding butterflies in Central Amazon, Brazil. J Insect Conserv 16:733–744CrossRefGoogle Scholar
  47. Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153CrossRefGoogle Scholar
  48. Ribeiro DB, Prado PI, Brown KSJR, Freitas AVL (2010) Temporal diversity patterns and phenology in fruit-feeding butterflies in the Atlantic forest. Biotropica 42:710–716CrossRefGoogle Scholar
  49. Ribeiro DB, Batista R, Prado PI, Brown KSJR, Freitas AVL (2012) The importance of small scales to the fruit-feeding butterfly assemblages in a fragmented landscape. Biodivers Conserv 21:811–827CrossRefGoogle Scholar
  50. Ribeiro DB, Williams MR, Specht A, Freitas AVL (2015) Vertical and temporal variability in the probability of detection of fruit-feeding butterflies and moths (Lepidoptera) in tropical forest. Aust Entomol. doi: 10.1111/aen.12157 Google Scholar
  51. Sant’Anna CLB, Ribeiro DB, Garcia LC, Freitas AVL (2014) Fruit-feeding butterfly communities are influenced by restoration age in tropical forests. Restor Ecol 22:480–485CrossRefGoogle Scholar
  52. 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 141:249–260CrossRefGoogle Scholar
  53. Silva JMC, Tabarelli M (2000) Tree species impoverishment and the future flora of the Atlantic forest of northeast Brazil. Nature 404:72–74CrossRefGoogle Scholar
  54. Solar RRDC, Barlow J, Ferreira J, Berenguer E, Lees AC, Thomson JR, Louzada J, Maués M, Moura NG, Oliveira VHF, Chaul JCM, Schoereder JH, Vieira ICG, Mac Nally R, Gardner TA (2015) How pervasive is biotic homogenization in human-modified tropical forest landscapes? Ecol Lett 18:1108–1118CrossRefPubMedGoogle Scholar
  55. Tabarelli M, Mantovani W, Peres CA (1999) Effects of habitat fragmentation and plant guild structure in the montane Atlantic forest of southeastern Brazil. Biol Conserv 91:119–127CrossRefGoogle Scholar
  56. Tabarelli M, Lopes AV, Peres CA (2008) Edge-effects drive tropical forest fragments towards an early-successional system. Biotropica 40:657–661CrossRefGoogle Scholar
  57. Tabarelli M, Aguiar AV, Ribeiro MC, Metzger JP, Peres CA (2010) Prospects for biodiversity conservation in the Atlantic forest: lessons for aging human-modified landscapes. Biol Conserv 143:2328–2340CrossRefGoogle Scholar
  58. Tabarelli M, Peres CA, Melo FPL (2012) The ‘few winners and many losers’ paradigm revisited: emerging prospects for tropical forest biodiversity. Biol Conserv 155:136–140CrossRefGoogle Scholar
  59. Thornton DH, Branch LC, Sunquist ME (2011) The relative influence of habitat loss and fragmentation: do tropical mammals meet the temperate paradigm? Ecol Appl 21:2324–2333CrossRefPubMedGoogle Scholar
  60. Turner IM (1996) Species loss in fragments of tropical rain forest: a review of the evidence. J Appl Ecol 33:200–209CrossRefGoogle Scholar
  61. Uehara-Prado M, Brown KSJR, Freitas AVL (2007) Species richness, composition and abundance of fruit-feeding butterflies in the Brazilian Atlantic forest: comparison between a fragmented and a continuous landscape. Global Ecol Biogeogr 16:43–54CrossRefGoogle Scholar
  62. Uehara-Prado M, Fernandes JO, Bello AM, Machado G, Santos AJ, Vaz-de-Mello FZ, Freitas AVL (2009) Selecting terrestrial arthropods as indicators of small-scale disturbance: a first approach in the Brazilian Atlantic Forest. Biol Conserv 142:1220–1228CrossRefGoogle Scholar
  63. Urbas P, Araújo MV Jr, Leal IR, Wirth R (2007) Cutting more from cut forests: edge effects on foraging and herbivory of leaf-cutting ants in Brazil. Biotropica 39:489–495CrossRefGoogle Scholar
  64. Wright SJ, Muller-Landau HC (2006) The future of tropical Forest species. Biotropica 38:287–301CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Bruno K. C. Filgueiras
    • 1
  • Douglas H. A. Melo
    • 1
  • Inara R. Leal
    • 2
  • Marcelo Tabarelli
    • 2
  • André Victor L. Freitas
    • 3
  • Luciana Iannuzzi
    • 4
  1. 1.Programa de Pós-Graduação em Biologia AnimalUniversidade Federal de PernambucoRecifeBrazil
  2. 2.Departamento de BotânicaUniversidade Federal de PernambucoRecifeBrazil
  3. 3.Departamento de Biologia Animal, Instituto de BiologiaUniversidade Estadual de CampinasCampinasBrazil
  4. 4.Departamento de ZoologiaUniversidade Federal de PernambucoRecifeBrazil

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