Species diversity and community structure of fruit-feeding butterflies (Lepidoptera: Nymphalidae) in an eastern amazonian forest

Authors

  • Lucas Pereira Martins Universidade Federal do Maranhão (UFMA) Departamento de Biologia (DEBIO) Laboratório de Ecologia e Sistemática de Insetos Polinizadores e Predadores (LESPP) Universidade Federal de Goiás (UFG) Instituto de Ciências Biológicas (ICB) Departamento de Ecologia (DECOL) Programa de Pós-Graduação em Ecologia e Evolução (PPG‑EcoEvol) Campus II http://orcid.org/0000-0003-3249-1070
  • Elias da Costa Araujo Junior Universidade Federal do Maranhão (UFMA) Departamento de Biologia (DEBIO) Laboratório de Ecologia e Sistemática de Insetos Polinizadores e Predadores (LESPP) Universidade de São Paulo (USP) Museu de Zoologia (MZUSP) http://orcid.org/0000-0003-1764-5086
  • Ananda Regina Pereira Martins Universidade Federal do Maranhão (UFMA) Departamento de Biologia (DEBIO) Laboratório de Ecologia e Sistemática de Insetos Polinizadores e Predadores (LESPP) McGill University, Department of Biology http://orcid.org/0000-0001-8020-0683
  • Marcelo Duarte Universidade de São Paulo (USP) Museu de Zoologia (MZUSP) http://orcid.org/0000-0002-9562-2974
  • Gisele Garcia Azevedo Universidade Federal do Maranhão (UFMA) Departamento de Biologia (DEBIO) Laboratório de Ecologia e Sistemática de Insetos Polinizadores e Predadores (LESPP) http://orcid.org/0000-0001-6184-4280

DOI:

https://doi.org/10.11606/0031-1049.2017.57.38

Keywords:

Biodiversity, Butterfly assemblage, Frugivorous butterflies, Neotropical region, Tropical forest

Abstract

Deforestation has negative impacts on diversity and community patterns of several taxa. In the eastern Amazon, where much deforestation is predicted for the coming years, forests patches may be essential to maintain the local biodiversity. Despite increasing concerns about the conservation of threatened areas, few studies have been performed to analyze the communities of diversified groups, such as insects, in the eastern Amazon. Here, we investigated species diversity and community structure of fruit-feeding butterflies, a well-known bioindicator group, in a threatened remnant of an eastern Amazonian forest located on Maranhão Island, northeastern Brazil. Fruit-feeding butterflies were sampled monthly for one year. Diversity and evenness indices, richness estimators, rarefaction curve, and rank-abundance plot were used to describe community structure in the study area. We captured 529 fruit-feeding butterflies in four subfamilies, 23 genera and 34 species. The three most abundant species, Hamadryas februa, Hamadryas feronia, and Hermeuptychia cf. atalanta are indicators of disturbed habitats and represented more than half of the collected individuals. Richness estimators revealed that between 87 and 94% of the fruit-feeding butterfly species were sampled, suggesting few additional records would be made for the area. Our results indicate that human-caused disturbances have altered local community patterns and provide baseline data for future research in threatened regions of the eastern Amazon.

Downloads

Download data is not yet available.

Author Biographies

  • Lucas Pereira Martins, Universidade Federal do Maranhão (UFMA) Departamento de Biologia (DEBIO) Laboratório de Ecologia e Sistemática de Insetos Polinizadores e Predadores (LESPP) Universidade Federal de Goiás (UFG) Instituto de Ciências Biológicas (ICB) Departamento de Ecologia (DECOL) Programa de Pós-Graduação em Ecologia e Evolução (PPG‑EcoEvol) Campus II
    Avenida dos Portugueses, 1.966, Vila Bacanga, CEP 65080‑805, São Luís, MA, Brasil.
    Avenida Esperança, 1.533, Campus Samambaia, CEP 74690‑900, Goiânia, GO, Brasil.
  • Elias da Costa Araujo Junior, Universidade Federal do Maranhão (UFMA) Departamento de Biologia (DEBIO) Laboratório de Ecologia e Sistemática de Insetos Polinizadores e Predadores (LESPP) Universidade de São Paulo (USP) Museu de Zoologia (MZUSP)
    Avenida dos Portugueses, 1.966, Vila Bacanga, CEP 65080‑805, São Luís, MA, Brasil.
    Avenida Nazaré, 481, Ipiranga, CEP 04263‑000, São Paulo, SP, Brasil.
  • Ananda Regina Pereira Martins, Universidade Federal do Maranhão (UFMA) Departamento de Biologia (DEBIO) Laboratório de Ecologia e Sistemática de Insetos Polinizadores e Predadores (LESPP) McGill University, Department of Biology
    Avenida dos Portugueses, 1.966, Vila Bacanga, CEP 65080‑805, São Luís, MA, Brasil.
    Montreal, Quebec, Canada H3A 2K6, Canada.
  • Marcelo Duarte, Universidade de São Paulo (USP) Museu de Zoologia (MZUSP)
    Avenida Nazaré, 481, Ipiranga, CEP 04263‑000, São Paulo, SP, Brasil.
  • Gisele Garcia Azevedo, Universidade Federal do Maranhão (UFMA) Departamento de Biologia (DEBIO) Laboratório de Ecologia e Sistemática de Insetos Polinizadores e Predadores (LESPP)
    Avenida dos Portugueses, 1.966, Vila Bacanga, CEP 65080‑805, São Luís, MA, Brasil.

References

Barlow, J.; Overal, W.L.; Araujo, I.S.; Gardner, T.A. & Peres, C.A. 2007. The value of primary, secondary and plantations forests for fruit-feeding butterflies in the Brazilian Amazon. Journal of Applied Ecology, 44:1001‑1012.

Benedick, S.; Hill, J.K.; Mustaffa, N.; Chey, V.K.; Maryati, M.; Searle, J.B.; Schilthuizen, M. & Hamer, K.C. 2006. Impacts of rain forest fragmentation on butterflies in northern Borneo: species richness, turnover and the value of small fragments. Journal of Applied Ecology, 43:967‑977.

Brooks, T.M.; Mittermeier, R.A.; Mittermeier, C.G.; da Fonseca G.A.B.; Rylands, A.B.; Konstant, W.R.; Flick, P.; Pilgrim, J.; Oldfield, S.; Magin, G. & Hilton-Taylor, C. 2002. Habitat loss and extinction in the hotspots of biodiversity. Conservation Biology, 16:909‑923.

Brown Jr., K.S. 1992. Borboletas da Serra do Japi: diversidade, habitats, recursos alimentares e variação temporal. In: Morellato, L.P.C. História Natural da Serra do Japi: ecologia e preservação de uma área florestal no sudeste do Brasil. Campinas, Editora da UNICAMP. p. 142‑186.

Brown Jr., K.S. & Freitas, A.V.L. 2000. Atlantic Forest butterflies: indicators for landscape conservation. Biotropica, 32:934‑956.

Cajaiba, R.L.; Périco, E.; Dalzochio, M.S.; da Silva, W.B.; Bastos, R.; Cabral, J.A. & Santos, M. 2017. Does the composition of Scarabaeidae (Coleoptera) communities reflect the extent of land use changes in the Brazilian Amazon? Ecological Indicators, 74:285‑294.

Colwell, R.K. & Coddington, J.A. 1994. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society B, 345:101‑118.

Cosmo, L.G.; Barbosa, E.P. & Freitas, A.V.L. 2014. Biology and morphology of the immature stages of Hermeuptychia atalanta (Lepidoptera: Nymphalidae: Satyrinae). Annales de la Société entomologique de France (N.S.), 50:82‑88.

Devries, P.J. 1987. The butterflies of Costa Rica and their natural history. Papilionidae, Pieridae, Nymphalidae. New Jersey, Princeton University Press.

Devries, P.J. & Walla, T.R. 2001. Species diversity and community structure in neotropical fruit-feeding butterflies. Biological Journal of the Linnean Society, 74:1‑15.

Devries, P.J.; Murray, D. & Lande, R. 1997. Species diversity in vertical, horizontal, and temporal dimensions of a fruit-feeding butterfly community in an Ecuadorian rainforest. Biological Journal of the Linnean Society, 62:343‑364.

Fermon, H.; Waltert, M.; Vane-Wright, R. & Muhlenberg, M. 2005. Forest use and vertical stratification in fruit-feeding butterflies of Sulawesi, Indonesia: impacts for conservation. Biodiversity and Conservation, 14:333‑350.

Freitas, A.V.L.; Iserhard, C.A.; Santos, J.P.; Carreira, J.Y.O.; Ribeiro, D.B.; Melo, D.H.A.; Rosa, A.H.B.; Marini-Filho, O.J.; Accacio, G.M. & Uehara-Prado, M. 2014. Studies with butterfly bait traps: an overview. Revista Colombiana de Entomología, 40:209‑218.

Garwood, K.; Lehman, R.; Carter, W. & Carter, G. 2009. Butterflies of Southern Amazonia. A photographic checklist of common species. McAllen, Tx., RiCalé Publishing.

Jonsson, M.; Dangles, O.; Malmqvist, B. & Guérold, F. 2002. Simulating species loss following perturbation: assessing the effects on process rates. Proceedings of the Royal Society of London B, 269:1047‑1052.

Jost, L. 2006. Entropy and diversity. Oikos, 113:363‑375.

Kindt, R. & Coe, R. 2015. Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. Nairobi, World Agroforestry Centre (ICRAF).

Larsen, T.H.; Williams, N.M. & Kremen, C. 2005. Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecology Letters, 8:538‑547.

Laurance, W.F.; Albernaz, A.K.M.; Fearnside, P.M.; Vasconcelos, H.L. & Ferreira, L.V. 2004. Deforestation in Amazonia. Science, 304:1109.

Magurran, A.E. 2004. Measuring biological diversity. Oxford, Blackwell.

Martins, L.P.; Araujo Junior, E.C.; Martins, A.R.P; Colins, M.S.; Almeida, G.C.F & Azevedo, G.G. 2017. Butterflies of Amazon and Cerrado remnants of Maranhão, Northeast Brazil. Biota Neotropica, 17:1‑11.

Martins, M.B. & Oliveira, T.G. 2011. Amazônia maranhense: Diversidade e conservação. Belém, Museu Paraense Emílio Goeldi.

Melo, A.S. 2008. O que ganhamos “confundindo” riqueza de espécies e equabilidade em um índice de diversidade? Biota Neotropica, 8:21‑27.

Novotny, V. & Basset, Y. 2000. Rare species in communities of tropical insect herbivores: pondering the mystery of singletons. Oikos, 89:564‑572.

Oksanen, J.; Blanchet, F.G.; Friendly, M.; Kindt, R.; Legendre, P.; Mcglinn, D.; Minchin, P.R.; O’Hara, R.B.; Simpson, G.L.; Solymos, P.; Stevens, M.H.H.; Szoecs, E. & Wagner, H. 2017. Vegan: Community Ecology Package. Available at: https://CRAN.R-project.org/package=vegan. Access in: 01/05/2017.

Pimm, S.L.; Jenkins, C.N.; Abell, R.; Brooks, T.M.; Gittleman, J.L.; Joppa, L.N.; Raven, P.H.; Roberts, C.M. & Sexton, J.O. 2014. The biodiversity of species and their rates of extinction, distribution and protection. Science, 344:987‑997.

Purvis, A. & Hector, A. 2000. Getting the measure of biodiversity. Nature, 405:212‑219.

R Development Core Team. 2017. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at: www.r-project.org. Access in: 01/05/2017.

Ramos, F.A. 2000. Nymphalid butterfly communities in an Amazonian forest fragment. Journal of Research on the Lepidoptera, 35:29‑41.

Ribeiro, D.B.; Batista, R.; Prado, P.I.; Brown Jr., K.S. & Freitas, A.V.L. 2012. The importance of small scales to the fruit-feeding butterfly assemblages in a fragmented landscape. Biodiversity and Conservation, 21:811‑827.

Ribeiro, D.B.; Prado, P.I.; Brown Jr., K.S. & Freitas, A.V.L. 2010. Temporal diversity patterns and phenology in fruit-feeding butterflies in the Atlantic Forest. Biotropica, 42:710‑716.

Ricklefs, R.E. & Lovette, I.J. 1999. The roles of island area per se and habitat diversity in the species-area relationships of four Lesser Antillean faunal groups. Journal of Animal Ecology, 68:1142‑1160.

Rydon, A.H.B. 1964. Notes on the use of butterfly traps in East Africa. Journal of the Lepidopterists’ Society, 18:51‑58.

Santos, E.C.; Mielke, O.H.H. & Casagrande, M.M. 2008. Butterfly inventories in Brazil: the state of the art and the priority-areas model for research aiming at conservation. Natureza & Conservação, 6:178‑200.

Santos, J.P.; Iserhard, C.A.; Teixeira, M.O.; & Romanowski, H.P. 2011. Fruit-feeding butterflies guide of subtropical Atlantic Forest and Araucaria Moist Forest in State of Rio Grande do Sul, Brazil. Biota Neotropica, 11:253‑274.

Schmidt, F.A.; Ribas, C.R. & Schoereder, J.H. 2013. How predictable is the response of ant assemblages to natural forest recovery? Implications for their use as bioindicators. Ecological Indicators, 24:158‑166.

Silva, J.M.C.; Rylands, A.B. & Fonseca, G.A.B. 2005. O destino das áreas de endemismo da Amazônia. Megadiversidade, 1:124‑131.

Silva, P.G. & Di Mare, R.A. 2012. Escarabeíneoscopro-necrófagos (Coleoptera, Scarabaeidae, Scarabaeinae) de fragmentos de Mata Atlântica em Silveira Martins, Rio Grande do Sul, Brazil. Iheringia Série Zoologia, 102:197‑205.

Tonhasca Jr., A.; Blackmer, J.L. & Albuquerque, G.S. 2002. Abundance and diversity of euglossine bees in the fragmented landscape of the Brazilian Atlantic Forest. Biotropica, 34:416‑422.

Tulloch, A.I.T.; Barnes, M.D.; Ringma, J.; Fuller, R.A. & Watson, J.E.M. 2016. Understanding the importance of small patches of habitat for conservation. Journal of Applied Ecology, 53:418‑429.

Uehara-Prado, M.; Brown Jr., K.S. & Freitas, A.V.L. 2007. Species richness, composition and abundance of fruit-feeding butterflies in the Brazilian Atlantic Forest: comparison between a fragmented and a continuous landscape. Global Ecology and Biogeography, 16:43‑54.

Vedeller, D.; Schulze, C.H.; Steffan-Dewenter, I.; Buchori, D. & Tscharntke, T. 2005. The contribution of tropical secondary forest fragments to the conservation of fruit-feeding butterflies: effects of isolation and age. Biodiversity and Conservation, 14:3577‑3592.

Vieira, I.C.G.; Toledo, P.M.; Silva, J.M.C. & Higuchi, H. 2008. Deforestations and threats to the biodiversity of Amazonia. Brazilian Journal of Biology, 68:949‑956.

Wahlberg, N.; Leneveu, J.; Kodandaramaiah, U.; Peña, C.; Nylin, S.; Freitas, A.V.L. & Brower, A.V.Z. 2009. Nymphalid butterflies diversify following near demise at the Cretaceous/Tertiary boundary. Proceedings of the Royal Society B, 276:4295‑4302.

Downloads

Published

2017-12-20

Issue

Section

Original Article

How to Cite

Martins, L. P., Araujo Junior, E. da C., Martins, A. R. P., Duarte, M., & Azevedo, G. G. (2017). Species diversity and community structure of fruit-feeding butterflies (Lepidoptera: Nymphalidae) in an eastern amazonian forest. Papéis Avulsos De Zoologia, 57(38), 481-489. https://doi.org/10.11606/0031-1049.2017.57.38