Neotropical Entomology

, Volume 43, Issue 1, pp 27–38

Skipper Richness (Hesperiidae) Along Elevational Gradients in Brazilian Atlantic Forest

  • E Carneiro
  • O H H Mielke
  • M M Casagrande
  • K Fiedler
Ecology, Behavior and Bionomics


Hesperiidae are claimed to be a group of elusive butterflies that need major effort for sampling, thus being frequently omitted from tropical butterfly surveys. As no studies have associated species richness patterns of butterflies with environmental gradients of high altitudes in Brazil, we surveyed Hesperiidae ensembles in Serra do Mar along elevational transects (900–1,800 m above sea level) on three mountains. Transects were sampled 11–12 times on each mountain to evaluate how local species richness is influenced by mountain region, vegetation type, and elevational zones. Patterns were also analyzed for the subfamilies, and after disregarding species that exhibit hilltopping behavior. Species richness was evaluated by the observed richness, Jacknife2 estimator and Chao 1 estimator standardized by sample coverage. Overall, 155 species were collected, but extrapolation algorithms suggest a regional richness of about 220 species. Species richness was far higher in forest than in early successional vegetation or grassland. Richness decreased with elevation, and was higher on Anhangava mountain compared with the two others. Patterns were similar between observed and extrapolated Jacknife2 richness, but vegetation type and mountain richness became altered using sample coverage standardization. Hilltopping species were more easily detected than species that do not show this behavior; however, their inclusion did neither affect estimated richness nor modify the shape of the species accumulation curve. This is the first contribution to systematically study highland butterflies in southern Brazil where all records above 1,200 m are altitudinal extensions of the known geographical ranges of skipper species in the region.


Conservation biology elevation inventory richness estimates tropical mountains 

Supplementary material

13744_2013_175_MOESM1_ESM.doc (264 kb)
ESM 1(DOC 264 kb)


  1. Ackery PR, De Jong R, Vane-Wright RJ (1999) The butterflies Hedyloidea, Hesperioidea and Papilionoidea. In: Kristensen NP (ed) Band/Volume IV Arthropoda: Insecta. Lepidoptera moths and butterflies: evolution, systematics, and biogeography, Volume 1. In: Fischer M (ed). Handbuch der Zoologie. Handbook of Zoology. Walter de Gruyter, Berlin, pp 263–300Google Scholar
  2. Amorin FW, Ávila RS Jr, Camargo AJA, Vieira AL, Oliveira PE (2009) A hawkmoth crossroads? Species richness, seasonality and biogeographical affinities of Sphingidae in Brazilian Cerrado. J Biogeogr 36:662–674CrossRefGoogle Scholar
  3. Axmacher JC, Brehm G, Hemp A, Tünte H, Lyaruu HVM, Müller-Hohenstein K, Fiedler K (2009) Determinants of diversity in afrotropical herbivorous insects (Lepidoptera: Geometridae): plant diversity, vegetation structure or abiotic factors? J Biogeogr 36:337–349CrossRefGoogle Scholar
  4. Azevedo AA, Silveira FA, Aguiar CML, Pereira VS (2008) Fauna de abelhas (Hymenoptera, Apoidea) nos campos rupestres da Cadeia do Espinhaço (Minas Gerais e Bahia: Brasil): riqueza de espécies, padrões de distribuição e ameaças para conservação. Megadiversidade 4:126–157Google Scholar
  5. Basset Y, Eastwood R, Sam L, Lohman DJ, Novotny V, Treuer T, Miller SE, Weiblen GD, Pierce NE, Bunyavejchewin S, Sakchoowong W, Kongnoo P, Osorio-Arenas MA (2011) Comparison of rainforest assemblages across three biogeographical regions using standardized protocols. J Res Lepid 44:17–28Google Scholar
  6. Baz A (1987) Abundancia y riqueza de las comunidades forestales de mariposas (Lepidoptera Rhopalocera) y su relación con la altitud en el Sistema Ibérico meridonal. Graellsia 43:179–192Google Scholar
  7. Bouliner T, Nichols JD, Sauer JR, Hines JE, Pollock KH (1998) Estimating species richness: the importance of heterogeneity in species detectability. Ecology 79:1018–1028CrossRefGoogle Scholar
  8. Brehm G (2007) Contrasting patterns of vertical stratification in two moth families in a Costa Rican lowland rain forest. Basic App Ecol 8:44–54CrossRefGoogle Scholar
  9. Brehm G, Süssenbach D, Fiedler K (2003) Unique elevational diversity patterns of geometrid moths in an Andean Montane forest. Ecography 26:456–466CrossRefGoogle Scholar
  10. Brose U, Martinez ND (2004) Estimating the richness of species with variable mobility. Oikos 105:292–300CrossRefGoogle Scholar
  11. Brose U, Martinez ND, Williams RJ (2003) Estimating species richness: sensitivity to sample coverage and insensitivity to spatial patterns. Ecology 84:2364–2377CrossRefGoogle Scholar
  12. Brown KS Jr (1992) Borboletas da Serra do Japi: Diversidade, hábitats, 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. Unicamp/FAPESP, Campinas, pp 142–187Google Scholar
  13. Brown KS Jr, Freitas AVL (2000a) Atlantic forest butterflies: indicators for landscape conservation. Biotropica 32:934–956Google Scholar
  14. Brown KS Jr, Freitas AVL (2000b) Diversidade de Lepidoptera em Santa Teresa, Espírito Santo. Bol Mus Biol Mello Leitão 11/12:71–118Google Scholar
  15. Caldas A, Robbins RK (2003) Modified Pollard transects for assessing tropical butterfly abundance and diversity. Biol Conserv 110:211–219CrossRefGoogle Scholar
  16. Chao A, Jost L (2012) Coverage-based rarefaction: standardizing samples by completeness rather than by size. Ecology 93:2533–2547PubMedCrossRefGoogle Scholar
  17. Colwell RK (2013) Estimates: statistical estimation of species richness and shared species from samples. Version 9. Available from
  18. Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity throughout extrapolation. Phil Trans R Soc London B 345:101–118CrossRefGoogle Scholar
  19. Colwell RK, Lees DC (2000) The mid-domain effect: geometric constraints on the geography of species richness. Trends Ecol Evol 15:70–76PubMedCrossRefGoogle Scholar
  20. Colwell RK, Mao CX, Chang J (2004) Interpolating, extrapolating and comparing incidence-based species accumulation curves. Ecology 85:2717–2727CrossRefGoogle Scholar
  21. Darrault RO, Schlindwein C (2002) Esfingídeos (Lepidoptera, Sphingidae) no Tabuleiro Paraibano, nordeste do Brasil: abundância, riqueza e relação com plantas esfingófilas. Rev Bras Zool 19:429–443CrossRefGoogle Scholar
  22. Dennis RLH, Shreeve TG, Isaac NJB, Roy DB, Hardy PB, Fox R, Asher J (2006) The effects of visual appearance on bias in butterfly recording and monitoring. Biol Conserv 128:486–492CrossRefGoogle Scholar
  23. DeVries PJ, Austin GT, Martin NH (2009) Estimating species diversity in a guild of Neotropical skippers (Lepidoptera: Hesperiidae) with artificial lures is a sampling problem. Insect Conserv Diver 2:125–134CrossRefGoogle Scholar
  24. Dolibaina DR, Mielke OHH, Casagrande MM (2011) Borboletas (Papilionoidea e Hesperioidea) de Guarapuava e arredores, Paraná, Brasil: um inventário com base em 63 anos de registros. Biota Neotrop 11:341–354CrossRefGoogle Scholar
  25. Emery EO, Brown KS Jr, Pinheiro CEG (2006) As Borboletas (Lepidoptera: Papilionoidea) do Distrito Federal, Brasil. Rev Bras Entomol 50:85–92CrossRefGoogle Scholar
  26. Emmel TC, Austin GT (1990) The tropical rainforest fauna of Rondonia, Brazil: species diversity and conservation. Trop Lepid 1:1–12Google Scholar
  27. Ferro VG, Romanowski HP (2012) Diversity and composition of tiger moths (Lepidoptera: Arctiidae) in an area of Atlantic Forest in southern Brazil: is the fauna more diverse in the grassland or in the forest? Zoologia 29:7–18CrossRefGoogle Scholar
  28. Fiedler K, Truxa C (2012) Species richness measures fail in resolving diversity patterns of speciose forest moth assemblages. Biodiv Conserv 21:2499–2508CrossRefGoogle Scholar
  29. Fleischman E, Austin GT, Weiss AD (1998) An empirical test of Rapoport’s rule: elevational gradients in montane butterfly communities. Ecology 79:2482–2493Google Scholar
  30. Francini RB, Duarte M, Mielke OHH, Caldas A, Freitas AVL (2011) Butterflies (Lepidoptera, Papilionoidea e Hesperioidea) of the “Baixada Santista” region, coastal São Paulo, Southern Brazil. Rev Bras Entomol 55:55–68CrossRefGoogle Scholar
  31. Garcia RJF, Longhi-Wagner HM, Pirani JR, Meirelles ST (2009) A contribution to phylogeography of Brazilian campos: an analysis based on Poaceae. Rev Bras Bot 34:703–713Google Scholar
  32. Gaston KJ (1996) Species richness: measure and measurement. In: Gaston KJ (ed) Biodiversity: a biology by numbers and difference. Blackwell, Oxford, pp 77–113Google Scholar
  33. Gaston KJ (2000) Global patterns of biodiversity. Nature 405:220–227PubMedCrossRefGoogle Scholar
  34. Giulietti AM, Menezes NL, Pirani JR, Meguro M, Wanderley MGL (1987) Flora da Serra do Cipó, Minas Gerais: caracterização e lista de espécies. Bol Bot Univ São Paulo 9:1–151Google Scholar
  35. Gómez-Nucamendi OL, Jones RW, Morón-Ríos A (1999) The Sphingidae (Heterocera) of the “El Ocote” reserve, Chiapas, Mexico. J Lepid Soc 53:153–158Google Scholar
  36. Gotelli N, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391CrossRefGoogle Scholar
  37. Hawkins BA, Albuquerque FS, Araújo MB, Beck J, Bini LM, Cabrero-Sañudo FJ, Castro-Praga I, Diniz-Filho JAF, Ferrer-Castán D, Field R, Gómez JF, Hortal J, Kerr JT, Kitching IJ, León-Cortés JL, Lobo JM, Montoya D, Moreno JC, Olalla-Tárraga MÁ, Pausas JG, Qian H, Rahbek C, Rodríguez MÁ, Sanders NJ, Williams P (2007) A global evaluation of metabolic theory as an explanation for terrestrial species richness gradients. Ecology 88:1877–1888PubMedCrossRefGoogle Scholar
  38. Hsieh TC, Ma KH, Chao A (2013) iNEXT online: interpolation and extrapolation (Version 1.0) [Software]. Available from
  39. Iserhard CA, Romanowski HP (2004) Lista de espécies de borboletas (Lepidoptera, Papilionoidea e Hesperioidea) da região do vale do rio Maquiné, Rio Grande do Sul, Brasil. Rev Bras Zool 21:649–662CrossRefGoogle Scholar
  40. Lamas G (1994) Butterflies of the Explorer’s Inn Reserve. In: Foster RB, Carr JL, Forsyth AB (eds) The Tambopata-Candamo reserved zone of southeastern Peru: a biological assessment. Rapid Assessment Program Working Papers 6:1–184, pp 62–63, 162–177Google Scholar
  41. Lien VV, Yuan D (2003) The differences of butterfly (Lepidoptera, Papilionoidea) communities in habitats with various degrees of disturbance and altitudes in tropical forests of Vietnam. Biodivers Conserv 12:1099–1111CrossRefGoogle Scholar
  42. Maack R (1968) Geografia Física do Estado do Paraná. Universidade Federal do Paraná. Instituto de Biologia e Pesquisa Tecnológica, Curitiba, p 350Google Scholar
  43. Machado AMB, Drummond GM, Paglia AP (2008) Livro vermelho da fauna brasileira ameaçada de extinção. MMA, Fundação Biodiversitas, Brazil, p 1420Google Scholar
  44. Magurran AE (2004) Ecological diversity and its measurement. Blackwell, Oxford, 256pGoogle Scholar
  45. Mallet-Rodriguez F, Parrini R, Pimentel LMS, Bessa R (2010) Altitudinal distribution of birds in a mountainous region in southeastern Brazil. Zoologia 27:503–522Google Scholar
  46. Marchiori MO, Romanowski HP (2006) Borboletas (Lepidoptera, Papilionoidea e Hesperioidea) do Parque Estadual do Espinilho e entorno, Rio Grande do Sul, Brasil. Rev Bras Zool 24:1029–1037CrossRefGoogle Scholar
  47. Martinelli G (2007) Mountain diversity in Brazil. Rev Bras Bot 30:587–597CrossRefGoogle Scholar
  48. May RM (1988) How many species on earth? Science 241:1441–1449PubMedCrossRefGoogle Scholar
  49. Mielke OHH (1968) Contribuição ao estudo faunístico dos “Hesperiidae” brasileiros I. Resultados de uma excursão à Foz do Iguaçú, Paraná, Brasil, com notas taxonômicas (Lepidoptera). Atas Soc Biol Rio de Janeiro 12:73–78Google Scholar
  50. Mielke CGC (1995) Papilionoidea e Hesperioidea (Lepidoptera) de Curitiba e seus arredores, Paraná, Brasil, com notas taxonômicas sobre Hesperiidae. Rev Bras Zool 11:759–776CrossRefGoogle Scholar
  51. Mielke OHH (2004) Hesperiidae. In: Lamas G (ed) Checklist: part 4a. Hesperioidea–Papilionoidea. In: Heppner JB (ed) Atlas of Neotropical Lepidoptera. Volume 5A. Association of Tropical Lepidoptera, Gainsville, pp 3–11, 25–86Google Scholar
  52. Mielke OHH (2005) Catalogue of the American Hesperioidea. Vols 1–6. Sociedade Brasileira de Zoologia, Curitiba, p 1536Google Scholar
  53. Mielke OHH, Casagrande MM (1997) Papilionoidea e Hesperioidea (Lepidoptera) do Parque Estadual do Morro do Diabo, Teodoro Sampaio, São Paulo, Brasil. Rev Bras Zool 14:967–1001CrossRefGoogle Scholar
  54. Mielke OHH, Emery E, Pinheiro CEG (2008) As borboletas Hesperiidae (Lepidoptera, Hesperioidea) do Distrito Federal, Brasil. Rev Bras Entomol 52:283–288CrossRefGoogle Scholar
  55. Mielke OHH, Carneiro E, Casagrande MM (2012a) Hesperiidae (Lepidoptera, Hesperioidea) from Ponta Grossa, Paraná, Brazil: 70 years of records with special reference to faunal composition of Vila Velha State Park. Rev Bras Entomol 56:59–66CrossRefGoogle Scholar
  56. Mielke OHH, Carneiro E, Casagrande MM (2012b) Os Hesperiidae (Lepidoptera, Hesperioidea) da RPPN Klagesi, Santo Antônio do Tauá, Pará, Brasil: nova contribuição para o conhecimento da biodiversidade da área de endemismo Belém. Acta Amazon 42:251–258CrossRefGoogle Scholar
  57. Nogués-Bravo D, Araújo MB, Romdal T, Rahbeck C (2008) Scale effects and human impact on the elevational species richness gradients. Nature 453:216–220PubMedCrossRefGoogle Scholar
  58. Orozco S, Muriel SB, Palacio J (2009) Diversidad de lepidópteros diurnos en um área de bosque seco tropical del Occidente Atioqueño. Actual Biol 31:31–41Google Scholar
  59. Palmer MW (1990) The estimation of species richness by extrapolation. Ecology 71:1195–1198CrossRefGoogle Scholar
  60. Palmer MW (1991) Estimating species richness: the second order Jacknife reconsidered. Ecology 72:1512–1513CrossRefGoogle Scholar
  61. Pinheiro CEG, Malinov IC, Andrade TO, Maravalhas JB, de Andrade MBM, de Deus LPA, Pedrosa LGP, Zanatta GV (2008) As borboletas (Lepidoptera, Papilionoidea) do campus universitário Darcy Ribeiro (Distrito Federal, Brasil). Biota Neotrop 8:139–144CrossRefGoogle Scholar
  62. Prieto C, Dahners HW (2006) Eumaeini (Lepidoptera: Lycaenidae) del cerro San Antonio: dinámica de la riqueza y comportamiento de “Hilltopping”. Rev Colomb Entomol 32:179–190Google Scholar
  63. Rahbek C (2005) The role of spatial scale and the perception of large-scale species-richness patterns. Ecol Lett 8:224–239CrossRefGoogle Scholar
  64. Robbins RK, Lamas G, Mielke OHH, Harvey DJ, Casagrande MM (1996) Taxonomic composition and ecological structure of the species-rich butterfly community at Pakitza, Parque Nacional del Manu, Perú. In: Wilson DE, Sandoval A (eds) Manu. The Biodiversity of Southeastern Peru. La Biodiversidad del Sureste del Perú. Editorial Horizonte, Lima, pp 217–252Google Scholar
  65. Roderjan CV, Kuniyoshi YS, Galvão F (1992) As regiões fitogeográficas do Paraná. Acta For Bras 1:3–7Google Scholar
  66. Safford HD (2007) Brazilian Paramos IV. Phytogeography of the campos de altitude. J Biogeogr 34:1701–1722CrossRefGoogle Scholar
  67. Sanchez-Rodriguez JF, Baz A (1995) The effects of elevation on the butterfly communities of a Mediterranean Mountain, Sierra de Javalambre, Central Spain. J Lepid Soc 49:192–207Google Scholar
  68. Santos EC, Mielke OHH, Casagrande MM (2008) Butterflies inventories in Brazil: the state of art and the priority areas models for research aiming at conservation. Nat Conservação 6:176–198Google Scholar
  69. Shields O (1967) Hilltopping. J Res Lepid 6:69–178Google Scholar
  70. Sparrow HR, Sisk TD, Ehrlich PR, Murphy DD (1994) Techniques and guidelines for monitoring Neotropical butterflies. Conserv Biol 8:800–809CrossRefGoogle Scholar
  71. Specht A, Corseuil E (2002) Diversidade de noctuídeos (Lepidoptera, Noctuidae) em Salvador do Sul, Rio Grande do Sul, Brasil. Rev Bras Zool 19:281–298CrossRefGoogle Scholar
  72. Spitzer K, Novotny V, Tonner M, Lepŝ J (1993) Habitat preferences, distribution and seasonality of the butterflies (Lepidoptera, Papilionoidea) in a montane tropical rain forest, Vietnam. J Biogeogr 20:109–121CrossRefGoogle Scholar
  73. Stattersfield AJ, Crosby MJ, Long AJ, Wege DC (1998) Endemic bird areas of the world: priorities for biodiversity conservation. BirdLife International, Cambridge, p 815Google Scholar
  74. Summerville KS, Crist TO (2005) Temporal patterns of species accumulation in a survey of Lepidoptera in a beech-maple forest. Biodivers Conserv 14:3393–3406CrossRefGoogle Scholar
  75. Tews J, Brose U, Grimm V, Tielbörger K, Wichmann MC, Schwager M, Jeltsch F (2004) Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J Biogeogr 31:79–92CrossRefGoogle Scholar
  76. Tobar DL, Rangel JOC, Andrade MG (2002) Diversidad de mariposas (Lepidoptera: Rhopalocera) en la parte alta de la cuenca del rio El Roble (Quindío-Colombia). Caldasia 24:393–409Google Scholar
  77. Uehara-Prado M, Brown KS Jr, Freitas AVL (2007) Species richness, composition and abundance of fruit-feeding butterflies in the Atlantic Forest: comparisons between a fragmented and a continuous landscape. Global Ecol Biogeogr 16:43–54CrossRefGoogle Scholar
  78. Veloso HP, Filho ALRR, Lima JCA (1991) Classificação da vegetação brasileira adaptada a um sistema universal. IBGE, Rio de Janeiro, p 123Google Scholar
  79. Vu LV, Vu CQ (2011) Diversity pattern of butterfly communities (Lepidoptera Papilionoidea) in different habitat types in a tropical rain forest of Southern Vietnam. ISRN Zool 2011:1–8CrossRefGoogle Scholar
  80. Wahlberg N, Brower AVZ, Nylin S (2005) Phylogenetic relationships and historical biogeography of tribes and genera in the subfamily Nymphalinae (Lepidoptera: Nymphalidae). Biol J Linn Soc 86:227–251CrossRefGoogle Scholar
  81. Warren AD, Ogawa JR, Brower AZ (2008) Phylogenetic relationships of subfamilies and circumscription of tribes in the family Hesperiidae (Lepidoptera, Hesperiidae). Cladistics 24:1–35CrossRefGoogle Scholar
  82. Wei SG, Li L, Walther BA, Ye WH, Huang ZL, Cao HL, Lian JY, Wang ZG, Chen YY (2010) Comparative performance of species-richness estimators using data from a subtropical forest tree community. Ecol Res 25:93–101CrossRefGoogle Scholar
  83. Willig MR, Kaufman DM, Stevens RD (2003) Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis. Annu Rev Eco Evol Syst 34:273–309CrossRefGoogle Scholar
  84. Zikán JF (1928) Die Macro-Lepidoptera des Itatiaya (Südabhang bei Campo-Bello). Ent Rdsch 45:7–8, 10–11, 13–14, 19–20, 22–23, 26, 32, 35–36, 38–39, 46Google Scholar
  85. Zikán JF, Zikán W (1968) Inseto-fauna do Itatiaia e da Mantiqueira. III Lepidoptera. Pesqui Agropecu Bras 3:45–109Google Scholar

Copyright information

© Sociedade Entomológica do Brasil 2013

Authors and Affiliations

  • E Carneiro
    • 1
  • O H H Mielke
    • 1
  • M M Casagrande
    • 1
  • K Fiedler
    • 2
  1. 1.Lab de Estudos de Lepidoptera Neotropical, Depto de ZoologiaUniv Federal do ParanáCuritibaBrasil
  2. 2.Dept of Tropical Ecology and Animal Biodiversity, Fac of Life SciencesUniv of ViennaViennaAustria

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