Abstract

Despite being one of the groups most well studied in Brazil, the butterfly fauna of northeastern Brazil, especially north of the mouth of São Francisco River, is poorly known. The aim of this study was to inventory the butterfly fauna in a remnant of Atlantic Forest in the state of Pernambuco as a contribution to understanding the distribution of these insects. The study was carried out in a 384.7 hectares fragment of Parque Estadual Dois Irmãos, in the metropolitan region of Recife. The butterflies were sampled monthly with insect nets from August 2011 to July 2012 and from January to August 2016. Additional records were obtained from two entomological collections and from two previous visits to the area in July 2003 and August 2006. A total of 273 species was sampled in 464 hours, with an additional 15 species recorded from the Entomological Collections, totaling 288 butterfly species recorded. The richest family was Hesperiidae (108 species), followed by Nymphalidae (80), Lycaenidae (43) Riodinidae (37), Pieridae (16) and Papilionidae (4). The fauna was dominated by generalist species with a broad geographical distribution, many of them commonly found on open areas, forest edges and secondary vegetation. Roeberella lencates (Hewitson, 1875) and Pheles atricolor atricolor (Butler, 1871) (Riodinidae) represent new records for northeastern Brazil.

Keywords:
Atlantic Forest; Conservation; Inventory; northeastern Brazil

Resumo

Apesar de ser um dos grupos mais bem estudados no Brasil, as borboletas da região Nordeste, especialmente ao norte da foz do Rio São Francisco, são ainda pouco conhecidas. O objetivo deste estudo foi realizar um inventário da fauna de borboletas em um fragmento de Floresta Atlântica no estado de Pernambuco, como uma contribuição para compreensão sobre a distribuição desses insetos. O estudo foi realizado em um fragmento de Floresta Atlântica de 384.7 hectares do Parque Estadual Dois Irmãos, localizado na região metropolitana de Recife. As borboletas foram amostradas mensalmente, de agosto de 2011 a julho de 2012 e de janeiro a agosto de 2016, com auxílio de redes entomológicas. Registros adicionais foram obtidos de duas Coleções Entomológicas e de duas coletas prévias em julho de 2003 e agosto de 2006. Um total de 273 espécies foi registrado em 464 horas e 15 espécies adicionais registradas a partir de Coleções Entomológicas, totalizando 288 espécies de borboletas registradas. A família mais rica foi Hesperiidae (108 espécies), seguida por Nymphalidae (80), Lycaenidae (43), Riodinidae (37), Pieridae (16) e Papilionidae (4). A fauna de borboletas foi dominada por espécies generalistas com uma ampla distribuição geográfica, muitas delas encontradas comumente em áreas abertas, bordas de mata e em vegetação secundária. Roeberella lencates (Hewitson, 1875) e Pheles atricolor atricolor (Butler, 1871) (Riodinidae) representam um novo registro para o Nordeste do Brasil.

Palavras-chave:
Conservação; Floresta Atlântica; Inventário; Nordeste Brasileiro

Introduction

Although the butterfly fauna of Brazil is relatively well sampled, there is still a “knowledge gap” in northeastern Brazil (Santos et al. 2008SANTOS, E.C., MIELKE, O.H.H. & CASAGRANDE, M.M. 2008. Inventários de borboletas no Brasil: Estado da arte e modelo de áreas prioritárias para pesquisa com vista à conservação. Nat. Conserv. 6(2):68-90.). The entire region is relatively under-sampled and poorly known, especially in the highly fragmented forests north of the mouth of São Francisco River (Freitas & Marini-Filho 2011FREITAS, A.V.L. & MARINI-FILHO, O.J. 2011. Plano de ação nacional para a conservação dos lepidópteros ameaçados de extinção. Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio)., Iserhard et al. 2017ISERHARD, C.A., UEHARA-PRADO, M., MARINI-FILHO, O.J., DUARTE, M. & FREITAS, A.V.L. 2017. Fauna da Mata Atlântica: Lepidoptera - Borboletas. In Revisões em Zoologia - Fauna da Mata Atlântica (E.L.A. Monteiro & C.E. Conte, orgs). Editora da UFPR, Curitiba, Paraná, p.57-102; 496-499 (color plates).). This region, which is known as the “Pernambuco Center of Endemism” (Brown Jr. 1977BROWN JR., K.S. 1977. Centros de evolução, refúgios quaternários e conservação de patrimônios genéticos na região neotropical: padrões de diferenciação em Ithomiinae (Lepidoptera: Nymphalidae). Acta Amaz. 7(1):75-137., Santos et al. 2007SANTOS, A.M.M., CAVALCANTI, D.R., SILVA, J.M.C. & TABARELLI, M. 2007. Biogeographical relationships among tropical forests in northeastern Brazil. J. Biogeogr. 34(3):437-446.), is the most endangered sector of the Atlantic Forest, with less than 12% of the original vegetation remaining (Ribeiro et al. 2009RIBEIRO, M.C., METZGER, J.P., MARTENSEN, A.C., PONZONI, F.J. & HIROTA, M.M. 2009. The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol. Conserv. 142(6):1141-1153.), almost half as fragments smaller than 10 ha (Ranta et al. 1998RANTA, P., BLOM, T., NIEMELA, J., JOENSUU, E. & SIITIONEN, M. 1998. The fragmented Atlantic rain forest of Brazil: size, shape and distribution of forest fragments. Biodivers. Conserv. 7(3):385-403.).

Research on the butterfly fauna in northeastern Brazil started in the 19th century with Bates (1867)BATES, H.M. 1867. On a collection of butterflies formed by Thomas Belt, ESQ., in the interior of the province of Maranham, Brazil. Trans. Entomol. Soc. London 15(7):535-546. and continued in the next century (e.g. D’Almeida 1935D’ALMEIDA, R. F. 1935. Lista dos lepidópteros capturados pelo Dr. R.V. Ihering no Nordeste do Brasil. Rev. Entomol. 5(3):326-328., Cardoso 1949CARDOSO, A. 1949. Lepidópteros de Alagoas. Rev. Entomol. 20(1-3):427-436., Silva 1967SILVA, A.G. 1967. Catálogo dos Lepidoptera Cearenses. Revi. Inst. Ceará 91-112., Kesselring & Ebert 1982KESSELRING, J. & EBERT, H. 1979 [1982]. Relação das borboletas encontradas na “Mata do Buraquinho”, João Pessoa, estado da Paraíba, Brasil. Rev. Nordest. Biol. 2(1):105-108.). Research activity on butterflies in the region has recently blossomed, with papers on threatened species (Kerpel et al. 2014KERPEL, S., ZACCA, T., NOBRE, C.E.B., JUNIOR, A.F., XAVIER, M. & FONSECA, A. 2014. Borboletas do Semiárido, conhecimento atual e contribuições do PPBio. In Artrópodes do Semi-Árido: biodiversidade e conservação (F. Bravo & A.R. Calor, eds). Printmídia, Feira de Santana, p.245-275., Melo et al. 2014MELO, D.H.A., FILGUEIRAS, B.K.C., LEAL, I.R. & FREITAS, A.V.L. 2014. Recent records of Morpho menelaus eberti (Fischer) (Lepidoptera: Nymphalidae), an endangered butterfly in Northeast Brazil. Trop. Lepid. Res. 24(2):102-104.) and the natural history of poorly-known species (Cardoso 2005CARDOSO, M.Z. 2005. New localities for Heliconius besckei Ménétriés and Heliconius sara (Fabricius) (Lepidoptera, Nymphalidae) in Bahia, Brazil. Neotrop. Entomol. 34(6):1007-1008., Freitas & Brown Jr. 2005FREITAS, A.V.L. & BROWN JR., K.S. 2005. Immature stages of Napeogenes sulphurina Bates, 1862 (Lepidoptera, Nymphalidae, Ithomiinae) from Northeastern Brazil. J. Lepid. Soc. 59(1):35-37., Nobre & Schlindwein 2011NOBRE, C.E.B. & SCHLINDWEIN, C. 2011. New records for species of Theope (Lepidoptera, Riodinidae) for the state of Pernambuco and northeastern Brazil, with notes on their natural history. Rev. Bras. Entomol. 55(2):275-278., 2012NOBRE, C.E.B. & SCHLINDWEIN, C. 2012. New records of Heraclides a. astyalus (Godart) (Lepidoptera: Papilionini) on the northern São Francisco river, Brazil. CheckList 8(5):927-928., Callaghan & Nobre 2014CALLAGHAN, C.J. & NOBRE, C.E.B. 2014. A new species of Pheles Herrich-Schaeffer from Northeast Brazil (Lepidoptera, Riodinidae). Zootaxa 3780(3):558-566., Dolibaina et al. 2014DOLIBAINA, D.R., DIAS, F.M.S., MIELKE, O.H.H. & CASAGRANDE, M.M. 2014. A new species of Eurybia (Lepidoptera: Riodinidae: Eurybiini) from northeastern Brazil. Fla. Entomol. 97(3):1208-1212., Nobre & Robbins 2014NOBRE, C.E.B. & ROBBINS, R.K. 2014. Arawacus euptychia (Lepidoptera: Lycaenidae: Eumaeini) is no longer an obscure species. J. Res. Lepid. 47:73-78.). Although several partial lists are now available (e.g. Duarte Jr. et al. 2001DUARTE JÚNIOR, J.A., ROBERTO, F.A.S., FRANÇA, B.R.A. & MAGGI, B. 2001. Levantamento Preliminar dos Lepidoptera (Papilionoidea e Hesperioidea) do Parque Estadual Dunas, Natal, Rio Grande do Norte, Brasil. Entomol. Vectores 8(3):365-369., Vasconcelos et al. 2009VASCONCELOS, R.N., BARBOSA, E.C.C. & PERES, M.C.L. 2009. Borboletas do Parque Metropolitano de Pituaçu, Salvador, Bahia, Brasil. Sitientibus. Ser. Cienc. Biol. 9(2/3):158-164., Zacca et al. 2011ZACCA, T., BRAVO, F. & XAVIER, M.X. 2011. Butterflies (Lepidoptera:Papilionoidea and Hesperioidea) from Serra da Jibóia, Bahia State, Brazil. EntomoBrasilis 4(3):139-143., Zacca & Bravo 2012ZACCA, T. & BRAVO, F. 2012. Borboletas (Lepidoptera: Papilionoidea e Hesperioidea) da porção norte da Chapada Diamantina, Bahia, Brasil. Biota Neotrop. 12(1): 117-126. http://www.biotaneotropica.org.br/v12n2/en/abstract?inventory+bn00212022012
http://www.biotaneotropica.org.br/v12n2/... , Kerpel et al. 2014KERPEL, S.M., FERREIRA JR, A. & FREITAS, A.V.L. 2014. New record of the endangered Brazilian swallowtail Heraclides himeros baia (Rothschild & Jordan, 1906). J. Lepid. Soc. 68(2):145-146.), very few comprehensive inventories have been published for northeastern Brazil. Examples of recently published well-sampled lists for the region includes those of Nobre et al. (2008NOBRE, C.E.B., SCHLINDWEIN, C. & MIELKE, O.H.H. 2008. The butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Catimbau National Park, Pernambuco, Brazil. Zootaxa 1751:35-45., 2012)NOBRE, C.E.B., IANNUZZI, L. & SCHLINDWEIN, C. 2012. Seasonality of Fruit-Feeding Butterflies (Lepidoptera, Nymphalidae) in a Brazilian Semiarid Area. ISRN Zoology 2012:1-8. and Lima & Zacca (2014)LIMA, J.N.R. & ZACCA, T. 2014. Lista de espécies de borboletas (Lepidoptera: Hesperioidea e Papilionoidea) de uma área de semiárido na região nordeste do Brasil. EntomoBrasilis 7(1):33-40. for areas of semi-arid “Caatinga” and the inventories for an altitudinal and coastal Atlantic Forest (Paluch et al. 2011PALUCH, M., MIELKE, O.H.H., NOBRE, C.E.B., CASAGRANDE, M.M., MELO, D.H.A. & FREITAS, A.V.L. 2011. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Parque Ecológico João Vasconcelos Sobrinho, Caruaru, Pernambuco, Brazil. Biota Neotrop. 11(4):229-238. http://www.biotaneotropica.org.br/v11n4/pt/abstract?inventory+bn01911042011.
http://www.biotaneotropica.org.br/v11n4/... and 2016PALUCH, M., MIELKE, O.H.H., LINHARES, L.M. & SILVA, D.C. 2016. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Private Reserve of Natural Heritage Fazenda Lontra/Saudade, Itanagra, Northern Coast of Bahia, Brazil. Biota Neotrop. 16(1): e20140085. http://dx.doi.org/10.1590/1676-0611-BN-2014-0085.
http://dx.doi.org/10.1590/1676-0611-BN-2... , respectively).

The purpose of the present study was to inventory the butterfly species found in “Parque Estadual Dois Irmãos”, a forest fragment in the metropolitan region of Recife, Pernambuco, northeastern Brazil, and to compare the results with those of previous inventories in the same region. These baseline results will also serve as a point of comparison for future inventories as ecological succession proceeds in this park.

Material and Methods

1. Study area

Parque Estadual Dois Irmãos (PEDI) (08º 00’ 48” S, 34º 56’ 42.9” W) is a state park in Recife, Pernambuco, northeastern Brazil (Figure 1). PEDI was created by State Law nº 11.622 of December 29, 1998 with ca. 384.7 ha, and has recently expanded (state decree nº 40.547 of March 28, 2014) with the inclusion of adjacent forest (the “Fazenda Brejo dos Macacos”), now totaling 1,157.72 ha. This coastal Atlantic Forest consists of a mix of successional regenerating stages. The present study was carried out in the 384.7 ha area now called “Mata de Dois Irmãos”. This area is the original part of the Park, including a 14 ha zoo. The climate is tropical monsoon (Am of Köppen), hot and humid, with a monthly average temperature of 25.8ºC. Rainfall, with an annual precipitation up to 2,400 mm, is seasonal, with a wet season from March to August and a dry season from September to February (Coutinho et al. 1998COUTINHO, R.Q., LIMA-FILHO, M.F., SOUZA-NETO, J.B. & SILVA, E.P. 1998. Características climáticas, geológicas, geomorfológicas, e geotécnicas da Reserva Ecológica de Dois Irmãos. In Reserva ecológica de Dois Irmãos: estudos em um remanescente de Mata Atlântica em área urbana (Recife - Pernambuco - Brasil) (I.C. Machado, A.V. Lopes & K.C. Pôrto , orgs). Secretaria de Ciências, Tecnologia e Meio Ambiente - SECTMA, Ed. Universitária da UFPE, Recife, p.21-49., Alvares et al. 2014ALVARES, C.A., STAPE, J.L., SENTELHAS, P.C., GONÇALVES, J.L.M. & SPAROVEK, G. 2014. Köppen’s climate classification map for Brazil. Meteorol. Z. 22(6):711-728.). The predominant soils are dystrophic red-yellow latosols (Coutinho et al. 1998COUTINHO, R.Q., LIMA-FILHO, M.F., SOUZA-NETO, J.B. & SILVA, E.P. 1998. Características climáticas, geológicas, geomorfológicas, e geotécnicas da Reserva Ecológica de Dois Irmãos. In Reserva ecológica de Dois Irmãos: estudos em um remanescente de Mata Atlântica em área urbana (Recife - Pernambuco - Brasil) (I.C. Machado, A.V. Lopes & K.C. Pôrto , orgs). Secretaria de Ciências, Tecnologia e Meio Ambiente - SECTMA, Ed. Universitária da UFPE, Recife, p.21-49.), and the vegetation is classified as ombrophilic dense lowland forest (Veloso et al. 1991VELOSO, H.P., RANGEL-FILHO, A.L. & LIMA, J.C.A. 1991. Classificação da vegetação brasileira adaptada a um sistema universal. IBGE, Rio de Janeiro, Brazil.).

2. Sampling and identification

Sampling was carried out monthly from August 2011 to July 2012, following the protocol described in Brown Jr. (1972)BROWN JR., K.S. 1972. Maximizing daily butterfly counts. J. Lepid. Soc. 26(3):183-196., Brown Jr. & Freitas (2000)BROWN JR., K.S. & FREITAS, A.V.L. 2000. Atlantic Forest butterflies: indicators for landscape conservation. Biotropica 32(4b):934-956. and Iserhard et al. (2013)ISERHARD, C.A., BROWN JR., K.S. & FREITAS, A.V.L. 2013. Maximized sampling of butterflies to detect temporal changes in tropical communities. J. Insect. Conserv. 17(3):615-622., with four sampling days each month, totaling 48 field trips. In addition, occasional visits were conducted between January and August 2016, totaling 17 additional field trips. The daily sampling period was from 9:00 to 16:00 hours, with a total sampling effort of 455 hours. Sampling was conducted along pre-existing trails (up to 2 linear km) covering a variety of habitats by one collector using an insect net (with a handle 1 m in length). Special attention was devoted to forest edges, water bodies or their banks, rich soil and flower patches, small clearings, and other heterogeneous environments. Areas with notable concentrations of butterflies were observed until no additional species had been recorded for a period of five to ten minutes. Additional data were obtained from two previous visits by AVLF (July 29, 2003 and August 10, 2006, totaling 9 samplings hours) and from material deposited in the Entomological Collection, Biology Department, Universidade Federal Rural de Pernambuco (UFRPE), and the Entomological Collection, Universidade Federal de Pernambuco (UFPE). Specimens were mounted and deposited in the following Brazilian institutions: 1) Universidade Federal de Pernambuco, Recife, PE; 2) Museu de Zoologia, Universidade Estadual de Campinas, Campinas, SP; and 3) Coleção Entomológica Padre Jesus Santiago Moure, UFPR, Curitiba, PR.

The authors identified species using the literature, the museum collections for which they are responsible, and their taxonomic expertise, which is partly based on years of fieldwork in Brazil and other Neotropical countries. The Discussion is based on these same information sources. The nomenclature in Table 1 follows Lamas (2004)LAMAS, G. 2004. Checklist: Part 4A Hesperioidea - Papilionoidea. In Atlas of Neotropical Lepidoptera (J.B. Heppner, ed.) Association of Tropical Lepidoptera, Gainesville., but higher taxonomic categories for Nymphalidae were updated from Wahlberg et al. (2009)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. Proc. R. Soc. B 276(1677):4295-4302., for Riodinidae from Seraphim et al. (2018)SERAPHIM, N., KAMINSKI, L.A., DeVRIES, P.J., PENZ, C., CALLAGHAN, C., WAHLBERG, N., SILVA-BRANDÃO, K.L. & FREITAS, A.V.L. 2018. Molecular phylogeny and higher systematics of the metalmark butterflies (Lepidoptera: Riodinidae). Syst. Entomol. 43(2):407-425. and Hall (2018)HALL, J.P.W. 2018. A Monograph of the Nymphidiina (Lepidoptera: Riodinidae: Nymphidiini): Phylogeny, Taxonomy, Biology, and Biogeography. Entomological Society of Washington, Washington, DC., for Hesperiidae from Warren et al. (2009)WARREN, A.D., OGAWA, J.R. & BROWER, A.V.Z. 2009. Revised classification of the family Hesperiidae (Lepidoptera: Hesperioidea) based on combined molecular and morphological data. Syst. Entomol. 34(3):467-523.. The higher classification of butterflies was updated from Heikkilä et al. (2012)HEIKKILÄ, M., KAILA, L., MUTANEN, M., PEÑA, C. & WAHLBERG, N. 2012. Cretaceous origin and repeated tertiary diversification of the redefined butterflies. Proc. R. Soc. B 279(1731): 1093-1099.. All families were sampled, except for the Hedylidae.

Results

In total, 288 butterfly species in six families were recorded at PEDI (Table 1). The fieldwork yielded 273 species in 464 sampling hours. An additional 15 species had been previously sampled (vouchers in UFPE and UFRPE, as noted in Table 1). The most species rich family was Hesperiidae with 108 species (37,5%), followed by Nymphalidae with 80 (28%), Lycaenidae with 43 (15%), Riodinidae with 37 (13%), Pieridae with 16 (5,5%) and Papilionidae with 4 (1%).

A number of unusual riodinid species were found. The species Roeberella lencates (Hewitson, 1875) and Pheles atricolor atricolor (Butler, 1871) were recorded for northeastern Brazil for the first time (Table 1). A single individual of R. lencates was captured when resting in a “pitangueira” tree (Eugenia uniflora, Myrtaceae) in an open sunny area known as “Chapéu do Sol”. A single individual of P. atricolor atricolor was found on a trail along a forest edge. It made short flights followed by landing on a leaf. A third riodinid Eurybia gonzagaDolibaina, Dias, Mielke & Casagrande, 2014DOLIBAINA, D.R., DIAS, F.M.S., MIELKE, O.H.H. & CASAGRANDE, M.M. 2014. A new species of Eurybia (Lepidoptera: Riodinidae: Eurybiini) from northeastern Brazil. Fla. Entomol. 97(3):1208-1212. is a recently described endemic for Pernambuco. It was observed frequently in PEDI. This species flies near the ground at dusk. It lands on the underside of leaves.

Discussion

1. Species richness

The 288 butterfly species recorded at PEDI is considerably lower than at sites in SE Brazil (800+ species, Francini et al. 2011FRANCINI, R.B., DUARTE, M., MIELKE, O.H.H., CALDAS, A. & FREITAS, A.V.L. 2011. Butterflies (Lepidoptera, Papilionoidea and Hesperioidea) of the “Baixada Santista” region, coastal São Paulo, southeastern Brazil. Rev. Bras. Entomol. 55(1):55-68.) and the Amazon Basin (up to 1700 species in Robbins et al. 1996ROBBINS, R.K., LAMAS, G., MIELKE, O.H.H., HARVEY, D.J. & CASAGRANDE, M.M. 1996. Taxonomic composition and ecological structure of the species-rich butterfly community at Pakitza, Parque Nacional del Manu, Perú. In The biodiversity of southeastern Peru (D.E. Wilson & A. Sandoval eds). Smithsonian Institution, Washington, DC, p.217-252. and Brown 2005BROWN JR, K.S. 2005. Geological, evolutionary and ecological bases of the diversification of Neotropical butterflies: implications for conservation. In Tropical rainforests: Past, Present and Future (E. Bermingham, C.W. Dick & C. Moritz , eds). University of Chicago Press, Chicago, p.166-201.), but is similar in richness to other inventories for the Atlantic Forest of northeastern Brazil. Kesselring & Ebert (1982)KESSELRING, J. & EBERT, H. 1979 [1982]. Relação das borboletas encontradas na “Mata do Buraquinho”, João Pessoa, estado da Paraíba, Brasil. Rev. Nordest. Biol. 2(1):105-108. found 291 butterfly species in the urban park “Mata do Buraquinho” in João Pessoa, Paraíba after five years of sampling. Paluch et al. (2011PALUCH, M., MIELKE, O.H.H., NOBRE, C.E.B., CASAGRANDE, M.M., MELO, D.H.A. & FREITAS, A.V.L. 2011. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Parque Ecológico João Vasconcelos Sobrinho, Caruaru, Pernambuco, Brazil. Biota Neotrop. 11(4):229-238. http://www.biotaneotropica.org.br/v11n4/pt/abstract?inventory+bn01911042011.
http://www.biotaneotropica.org.br/v11n4/... , 2016)PALUCH, M., MIELKE, O.H.H., LINHARES, L.M. & SILVA, D.C. 2016. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Private Reserve of Natural Heritage Fazenda Lontra/Saudade, Itanagra, Northern Coast of Bahia, Brazil. Biota Neotrop. 16(1): e20140085. http://dx.doi.org/10.1590/1676-0611-BN-2014-0085.
http://dx.doi.org/10.1590/1676-0611-BN-2... recorded 197 species in a forest area in Caruaru, Pernambuco (216 sampling hours) and 260 species in Itanagra, Bahia (288 sampling hours), respectively. Cardoso (1949)CARDOSO, A. 1949. Lepidópteros de Alagoas. Rev. Entomol. 20(1-3):427-436. recorded 218 butterfly species in the forest of Maceió, Alagoas after many years of sampling. Even though PEDI is located in an urban area of Recife that is close to a large highway, its butterfly fauna is comparable in richness to these other sites in northeastern Brazil.

The richness of Nymphalidae at PEDI was similar to that recorded in Kesselring & Ebert (1982)KESSELRING, J. & EBERT, H. 1979 [1982]. Relação das borboletas encontradas na “Mata do Buraquinho”, João Pessoa, estado da Paraíba, Brasil. Rev. Nordest. Biol. 2(1):105-108. and in other studies in the region (Cardoso 1949CARDOSO, A. 1949. Lepidópteros de Alagoas. Rev. Entomol. 20(1-3):427-436., Paluch et al. 2011PALUCH, M., MIELKE, O.H.H., NOBRE, C.E.B., CASAGRANDE, M.M., MELO, D.H.A. & FREITAS, A.V.L. 2011. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Parque Ecológico João Vasconcelos Sobrinho, Caruaru, Pernambuco, Brazil. Biota Neotrop. 11(4):229-238. http://www.biotaneotropica.org.br/v11n4/pt/abstract?inventory+bn01911042011.
http://www.biotaneotropica.org.br/v11n4/... , 2016PALUCH, M., MIELKE, O.H.H., LINHARES, L.M. & SILVA, D.C. 2016. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Private Reserve of Natural Heritage Fazenda Lontra/Saudade, Itanagra, Northern Coast of Bahia, Brazil. Biota Neotrop. 16(1): e20140085. http://dx.doi.org/10.1590/1676-0611-BN-2014-0085.
http://dx.doi.org/10.1590/1676-0611-BN-2... ). With seven species recorded, the number of Ithomiini is similar to that recorded in João Pessoa, Paraíba, with eight species (Kesselring & Ebert 1982KESSELRING, J. & EBERT, H. 1979 [1982]. Relação das borboletas encontradas na “Mata do Buraquinho”, João Pessoa, estado da Paraíba, Brasil. Rev. Nordest. Biol. 2(1):105-108.) and in Itanagra, Bahia, with seven species (Paluch et al. 2016PALUCH, M., MIELKE, O.H.H., LINHARES, L.M. & SILVA, D.C. 2016. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Private Reserve of Natural Heritage Fazenda Lontra/Saudade, Itanagra, Northern Coast of Bahia, Brazil. Biota Neotrop. 16(1): e20140085. http://dx.doi.org/10.1590/1676-0611-BN-2014-0085.
http://dx.doi.org/10.1590/1676-0611-BN-2... ). In contrast, 11 species of Ithomiini were recorded in Maceió, Alagoas (Cardoso 1949CARDOSO, A. 1949. Lepidópteros de Alagoas. Rev. Entomol. 20(1-3):427-436.), 11 in Areia, Paraíba (see Kerpel et al. 2014KERPEL, S., ZACCA, T., NOBRE, C.E.B., JUNIOR, A.F., XAVIER, M. & FONSECA, A. 2014. Borboletas do Semiárido, conhecimento atual e contribuições do PPBio. In Artrópodes do Semi-Árido: biodiversidade e conservação (F. Bravo & A.R. Calor, eds). Printmídia, Feira de Santana, p.245-275.), 14 in Caruaru, Pernambuco (Paluch et al. 2011PALUCH, M., MIELKE, O.H.H., NOBRE, C.E.B., CASAGRANDE, M.M., MELO, D.H.A. & FREITAS, A.V.L. 2011. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Parque Ecológico João Vasconcelos Sobrinho, Caruaru, Pernambuco, Brazil. Biota Neotrop. 11(4):229-238. http://www.biotaneotropica.org.br/v11n4/pt/abstract?inventory+bn01911042011.
http://www.biotaneotropica.org.br/v11n4/... ), 17 in Usina Serra Grande, São José da Lage, Alagoas and 18 in the RPPN Frei Caneca, Jaqueira, Pernambuco (DHAM, Carlos E. B. Nobre and AVLF unpublished data), all sites in northeastern Brazil. PEDI lacks typical forest species such as Aeria olena ssp., Hypoleria alema oreas Weymer, 1899 and Heterosais edessa (Hewitson, [1855]), species recorded in some sites in the region (DHAM and AVLF pers, obs.). Further expeditions to the large area of “Fazenda Brejo dos Macacos” could add more species of Ithomiini associated with shaded humid forests.

The richness of Hesperiidae and Lycaenidae in PEDI was similar to that recorded by Kesselring & Ebert (1982)KESSELRING, J. & EBERT, H. 1979 [1982]. Relação das borboletas encontradas na “Mata do Buraquinho”, João Pessoa, estado da Paraíba, Brasil. Rev. Nordest. Biol. 2(1):105-108., but higher than other localities in the region (Cardoso 1949CARDOSO, A. 1949. Lepidópteros de Alagoas. Rev. Entomol. 20(1-3):427-436., Paluch et al. 2011PALUCH, M., MIELKE, O.H.H., NOBRE, C.E.B., CASAGRANDE, M.M., MELO, D.H.A. & FREITAS, A.V.L. 2011. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Parque Ecológico João Vasconcelos Sobrinho, Caruaru, Pernambuco, Brazil. Biota Neotrop. 11(4):229-238. http://www.biotaneotropica.org.br/v11n4/pt/abstract?inventory+bn01911042011.
http://www.biotaneotropica.org.br/v11n4/... , 2016PALUCH, M., MIELKE, O.H.H., LINHARES, L.M. & SILVA, D.C. 2016. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Private Reserve of Natural Heritage Fazenda Lontra/Saudade, Itanagra, Northern Coast of Bahia, Brazil. Biota Neotrop. 16(1): e20140085. http://dx.doi.org/10.1590/1676-0611-BN-2014-0085.
http://dx.doi.org/10.1590/1676-0611-BN-2... ). For Pieridae, the number of recorded species is similar to most inventories conducted in the region (Cardoso 1949CARDOSO, A. 1949. Lepidópteros de Alagoas. Rev. Entomol. 20(1-3):427-436., Kesselring & Ebert 1982KESSELRING, J. & EBERT, H. 1979 [1982]. Relação das borboletas encontradas na “Mata do Buraquinho”, João Pessoa, estado da Paraíba, Brasil. Rev. Nordest. Biol. 2(1):105-108., Paluch et al. 2011PALUCH, M., MIELKE, O.H.H., NOBRE, C.E.B., CASAGRANDE, M.M., MELO, D.H.A. & FREITAS, A.V.L. 2011. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Parque Ecológico João Vasconcelos Sobrinho, Caruaru, Pernambuco, Brazil. Biota Neotrop. 11(4):229-238. http://www.biotaneotropica.org.br/v11n4/pt/abstract?inventory+bn01911042011.
http://www.biotaneotropica.org.br/v11n4/... , 2016PALUCH, M., MIELKE, O.H.H., LINHARES, L.M. & SILVA, D.C. 2016. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Private Reserve of Natural Heritage Fazenda Lontra/Saudade, Itanagra, Northern Coast of Bahia, Brazil. Biota Neotrop. 16(1): e20140085. http://dx.doi.org/10.1590/1676-0611-BN-2014-0085.
http://dx.doi.org/10.1590/1676-0611-BN-2... ). The richness of Papilionidae is low compared to that in southern Atlantic Forest sites (see Brown Jr. & Freitas 2000BROWN JR., K.S. & FREITAS, A.V.L. 2000. Atlantic Forest butterflies: indicators for landscape conservation. Biotropica 32(4b):934-956.), though similar to other well-sampled sites on the Atlantic Forest of northeastern Brazil (Kesselring & Ebert 1982KESSELRING, J. & EBERT, H. 1979 [1982]. Relação das borboletas encontradas na “Mata do Buraquinho”, João Pessoa, estado da Paraíba, Brasil. Rev. Nordest. Biol. 2(1):105-108., Paluch et al. 2011PALUCH, M., MIELKE, O.H.H., NOBRE, C.E.B., CASAGRANDE, M.M., MELO, D.H.A. & FREITAS, A.V.L. 2011. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Parque Ecológico João Vasconcelos Sobrinho, Caruaru, Pernambuco, Brazil. Biota Neotrop. 11(4):229-238. http://www.biotaneotropica.org.br/v11n4/pt/abstract?inventory+bn01911042011.
http://www.biotaneotropica.org.br/v11n4/... , 2016PALUCH, M., MIELKE, O.H.H., LINHARES, L.M. & SILVA, D.C. 2016. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Private Reserve of Natural Heritage Fazenda Lontra/Saudade, Itanagra, Northern Coast of Bahia, Brazil. Biota Neotrop. 16(1): e20140085. http://dx.doi.org/10.1590/1676-0611-BN-2014-0085.
http://dx.doi.org/10.1590/1676-0611-BN-2... ). Finally, the number of Riodinidae species was similar to those in Kesselring & Ebert (1982)KESSELRING, J. & EBERT, H. 1979 [1982]. Relação das borboletas encontradas na “Mata do Buraquinho”, João Pessoa, estado da Paraíba, Brasil. Rev. Nordest. Biol. 2(1):105-108. and Paluch et al. (2016)PALUCH, M., MIELKE, O.H.H., LINHARES, L.M. & SILVA, D.C. 2016. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Private Reserve of Natural Heritage Fazenda Lontra/Saudade, Itanagra, Northern Coast of Bahia, Brazil. Biota Neotrop. 16(1): e20140085. http://dx.doi.org/10.1590/1676-0611-BN-2014-0085.
http://dx.doi.org/10.1590/1676-0611-BN-2... , but was greater than the numbers reported in Cardoso (1949)CARDOSO, A. 1949. Lepidópteros de Alagoas. Rev. Entomol. 20(1-3):427-436. and Paluch et al. (2011)PALUCH, M., MIELKE, O.H.H., NOBRE, C.E.B., CASAGRANDE, M.M., MELO, D.H.A. & FREITAS, A.V.L. 2011. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Parque Ecológico João Vasconcelos Sobrinho, Caruaru, Pernambuco, Brazil. Biota Neotrop. 11(4):229-238. http://www.biotaneotropica.org.br/v11n4/pt/abstract?inventory+bn01911042011.
http://www.biotaneotropica.org.br/v11n4/... .

2. Taxonomic composition

The relative contribution of each butterfly family in PEDI mirrors the pattern reported in the list of Brazilian butterflies and in all well sampled sites in Brazil. Hesperiidae is the richest family, followed by Nymphalidae (Brown Jr. & Freitas 1999BROWN JR., K.S. & FREITAS, A.V.L. 1999. Lepidoptera. In Biodiversidade do Estado de São Paulo, Brasil: invertebrados terrestres (C.R.F. Brandão & E.M. Cancello, eds). FAPESP, São Paulo, p.225-245., 2000BROWN JR., K.S. & FREITAS, A.V.L. 2000. Atlantic Forest butterflies: indicators for landscape conservation. Biotropica 32(4b):934-956., Francini et al. 2011FRANCINI, R.B., DUARTE, M., MIELKE, O.H.H., CALDAS, A. & FREITAS, A.V.L. 2011. Butterflies (Lepidoptera, Papilionoidea and Hesperioidea) of the “Baixada Santista” region, coastal São Paulo, southeastern Brazil. Rev. Bras. Entomol. 55(1):55-68.). Lycaenidae and Riodinidae are equivalent in richness in PEDI, a pattern similar to that observed in most southern Atlantic Forest sites and in montane forests. However, it diverges from that observed in the lowland forests of Rio de Janeiro and Espírito Santo (Brown Jr. & Freitas 2000BROWN JR., K.S. & FREITAS, A.V.L. 2000. Atlantic Forest butterflies: indicators for landscape conservation. Biotropica 32(4b):934-956., Francini et al. 2011FRANCINI, R.B., DUARTE, M., MIELKE, O.H.H., CALDAS, A. & FREITAS, A.V.L. 2011. Butterflies (Lepidoptera, Papilionoidea and Hesperioidea) of the “Baixada Santista” region, coastal São Paulo, southeastern Brazil. Rev. Bras. Entomol. 55(1):55-68.), where Riodinidae surpasses Lycaenidae. Clearly, additional surveys in other sites in the Pernambuco Center of Endemism and in the forests of Bahia are needed to better document these patterns.

In the Atlantic Forest, Nymphalidae is considered a reliable surrogate of the total butterfly fauna, generally making up 25-29% of the total butterfly fauna (Brown Jr. & Freitas 2000BROWN JR., K.S. & FREITAS, A.V.L. 2000. Atlantic Forest butterflies: indicators for landscape conservation. Biotropica 32(4b):934-956.). Based on this indicator, the fauna of PEDI would be expected to vary between 276 and 320 species, which is consistent with the 288 recorded species.

3. Habitat

The fauna of PEDI is dominated by species commonly found along forest edges, in open habitats and disturbed forests. As an example, all species of Pieridae recorded in the study site are typical of secondary forests and disturbed areas with the possible exception of Leucidia elvina (Godart, 1819). The same is true for Hesperiidae and Papilionidae, except for Parides zacynthus polymetus (Godart, 1819), and the major groups of Nymphalidae. The tribe Ithomiini (Nymphalidae: Danainae) is poorly represented, as noted, with most of those in PEDI associated with open disturbed habitats and forest edges (with the exception of Napeogenes inachia ssp.).

4. Biogeography

The biogeographic composition of the PEDI fauna shows a large contribution of widely distributed species, as illustrated with the Lycaenidae, Papilionidae and Pieridae. For Lycaenidae for example, many of the species have wide geographic distributions; with 24 of 43 species (56%) occurring from Central America to Brazil. Alternately, some species are primarily Amazonian and penetrate the Atlantic Forest only in the north. Examples are Nesiostrymon hyccara (Hewitson, 1868), Ostrinotes tarena (Hewitson, 1874), and Thereus enenia (Hewitson, 1867). Others are endemic to the Atlantic Forest, such as Panthiades hebraeus (Hewitson, 1867) and Theritas triquetra (Hewitson, 1865). Although none of the Lycaenidae, Pieridae and Papilionidae at PEDI are endemic to the Pernambuco Center of Endemism, this is not true for Riodinidae. For example, the recently described Eurybia gonzaga is known only from Pernambuco (Dolibaina et al. 2014DOLIBAINA, D.R., DIAS, F.M.S., MIELKE, O.H.H. & CASAGRANDE, M.M. 2014. A new species of Eurybia (Lepidoptera: Riodinidae: Eurybiini) from northeastern Brazil. Fla. Entomol. 97(3):1208-1212.). It was also recorded in “RPPN Frei Caneca”, Jaqueira (as type material, see Dolibaina et al. 2014DOLIBAINA, D.R., DIAS, F.M.S., MIELKE, O.H.H. & CASAGRANDE, M.M. 2014. A new species of Eurybia (Lepidoptera: Riodinidae: Eurybiini) from northeastern Brazil. Fla. Entomol. 97(3):1208-1212.), in “Parque Natural Municipal Professor João Vasconcelos Sobrinho”, Caruaru (cited as Eurybia pergaea by Paluch et al. 2011PALUCH, M., MIELKE, O.H.H., NOBRE, C.E.B., CASAGRANDE, M.M., MELO, D.H.A. & FREITAS, A.V.L. 2011. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the Parque Ecológico João Vasconcelos Sobrinho, Caruaru, Pernambuco, Brazil. Biota Neotrop. 11(4):229-238. http://www.biotaneotropica.org.br/v11n4/pt/abstract?inventory+bn01911042011.
http://www.biotaneotropica.org.br/v11n4/... ), and in “Estação Ecológica do Tapacurá”, São Lourenço da Mata (DHAM pers, obs.). All sites are in Pernambuco, indicating that this species is a common faunistic component of this region. The Nymphalidae also present several taxa endemic or predominantly occurring in the Pernambuco Center of Endemism, such as Napeogenes inachia ssp. and Hypothyris ninonia daetina (Danainae: Ithomiini), Pierella hyalinus ssp. and Pierella kesselringi Zacca, Siewert & Paluch, 2016 (Satyrinae: Haeterini), Morpho helenor anakreon Fruhstorfer, 1910 (Satyrinae: Morphini) and Heliconius ethilla flavomaculatus Weymer, 1894 (Heliconinae).

5. Conservation

No threatened butterflies are recorded in PEDI, but there is a historical record (about 50 years ago) of Morpho menelaus eberti Fischer, 1962 (Nymphalidae: Satyrinae: Morphini) in the “Chapéu do Sol”, deposited in the National Museum of Natural History in Paris (Blandin 2007BLANDIN, P. 2007. The systematics of the genus Morpho, Fabricius, 1807 (Lepidoptera Nymphalidae, Morphinae). Hillside Books, Canterbury.). Although habitat loss, years of logging and other urban related disturbances could explain the local extinction of M. melenaus eberti, this butterfly could still persist in the area in low densities. Another threatened morphine that could be present in the area is Morpho epistrophus nikolajewna Weber, 1951. This butterfly has been recorded to the south in Maceió (Cardoso 1949CARDOSO, A. 1949. Lepidópteros de Alagoas. Rev. Entomol. 20(1-3):427-436.), to the north in Igarassu (Carlos E. B. Nobre pers. comm.) and in João Pessoa (Kesselring & Ebert 1982KESSELRING, J. & EBERT, H. 1979 [1982]. Relação das borboletas encontradas na “Mata do Buraquinho”, João Pessoa, estado da Paraíba, Brasil. Rev. Nordest. Biol. 2(1):105-108.), which are Atlantic Forest fragments near urban areas. Further sampling is needed before stating that both species of Morpho Fabricius, 1807 are absent in forested areas around Recife.

The reported results showed that PEDI possesses a relatively rich butterfly community. Considering the degree of threat to the fauna of the Atlantic Forest of northeastern Brazil, PEDI is of enormous importance for conserving butterflies, as it is for vertebrates such as birds and mammals (Machado et al. 1998MACHADO, I.C., LOPES, A.V. & PÔRTO, K.C. 1998. Reserva Ecológica de Dois Irmãos: Estudos em um remanescente de Mata Atlântica em área urbana (Recife - Pernambuco - Brasil). Secretaria de Ciência e Tecnologia e Meio Ambiente - SECTMA - UFPE, Recife.). Conservation strategies should be developed in conjunction with public entities, such as the Environment Secretariat of Recife, and non-governmental organizations such as the “Centro de Pesquisas Ambientais do Nordeste” (CEPAN), and with the local communities surrounding the whole area. Priority actions for PEDI should include the proposition of a sustainable management plan focused on reintroduction of locally extinct species of plants and animals, an effective plan for restoring heavily disturbed areas, and establishment of programs of ecological monitoring and management of the surrounding environments so that the area can persist as an important Atlantic Forest remnant.

Acknowledgements

We are indebted to all the staff of the “Parque Estadual Dois Irmãos” by allowing research in the area. We also thank David Douglas for their assistance in the field activities and Silvino Pinto for the photographs of butterflies provided for consultation. The following people helped with identifications: Curtis Callaghan (Riodinidae) and Noemy Seraphim (Hermeuptychia). We also are grateful to the ICMBio for the research permits (SISBIO nº 10802-5). AVLF thanks the CNPq (process 302585/2011-7), the BR-BoL (MCT/CNPq/FNDCT 50/2010), the FAPESP (grant 2012/50260-6) and the National Science Foundation (DEB-1256742). OHHM thanks the CNPq for the fellowship (process 304639/2014-1). MD thanks CNPq (process 305905/2012-0), FAPESP (process 2012/13898-0) and Pró-Reitoria de Pesquisa da Universidade de São Paulo (Projeto 1). This publication is part of the RedeLep ‘Rede Nacional de Pesquisa e Conservação de Lepidópteros’ SISBIOTA-Brasil/CNPq (563332/2010-7), and of the BIOTA-FAPESP Program (2011/50225-3).

References

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