UNIVERSIDADE FEDERAL DE PERNAMBUCO

Douglas Henrique Alves de Melo

EFEITO DA FRAGMENTAÇÃO DE HABITATS SOBRE BORBOLETAS FRUGÍVORAS (: ) NA FLORESTA ATLÂNTICA NORDESTINA

RECIFE 2014 UNIVERSIDADE FEDERAL DE PERNAMBUCO

Douglas Henrique Alves de Melo

EFEITO DA FRAGMENTAÇÃO DE HABITATS SOBRE BORBOLETAS FRUGÍVORAS (LEPIDOPTERA: NYMPHALIDAE) NA FLORESTA ATLÂNTICA NORDESTINA

Dissertação apresentada ao Programa de Pós- graduação em Biologia , Centro de Ciências Biológicas da Universidade Federal de Pernambuco, como requisito parcial da obtenção do título de Mestre em Biologia Animal.

Orientadora: Inara Roberta Leal Coorientador: André Victor Lucci Freitas

RECIFE 2014

Catalogação na fonte Elaine Barroso CRB 1728

Melo, Douglas Henrique Alves de Efeito da fragmentação de habitats sobre borboletas frugívoras (Lepidoptera: Nymphalidae) na Floresta Atlântica Nordestina/ Recife: O Autor, 2014.

90 folhas : il., fig., tab. Orientadora: Inara Roberta Leal Coorientador: André Victor Lucci Freitas Dissertação (mestrado) – Universidade Federal de Pernambuco, Centro de Ciências Biológicas, Biologia Animal, 2014. Inclui bibliografia e anexo

1. Borboleta 2. Floresta Atlântica I. Leal, Roberta Inara (orientadora) II. Freitas, André Victor Lucci (coorientador) III. Título

595.789 CDD (22.ed.) UFPE/CCB- 2014- 230

Douglas Henrique Alves de Melo

EFEITO DA FRAGMENTAÇÃO DE HABITATS SOBRE BORBOLETAS FRUGÍVORAS (LEPIDOPTERA: NYMPHALIDAE) NA FLORESTA ATLÂNTICA NORDESTINA

Dissertação apresentada ao Programa de Pós- graduação em Biologia Animal, Centro de Ciências Biológicas da Universidade Federal de Pernambuco, como requisito parcial da obtenção do título de Mestre em Biologia Animal.

Orientadora: Inara Roberta Leal Coorientador: André Victor Lucci Freitas

Aprovada em: 31/07/2014

BANCA EXAMINADORA

______Profa. Dra. Luciana Iannuzzi Departamento de Zoologia - UFPE

______Profa. Dra. Cleide Maria Ribeiro de Albuquerque Departamento de Zoologia – UFPE

______Prof. Dr. Wendel José Teles Pontes Departamento de Zoologia - UFPE

Aos meus avós, Manuel e Celina (in memorian), Dedico. AGRADECIMENTOS

Ao longo da minha formação, conheci pessoas que muito me ajudaram, desde a graduação até o término deste trabalho. Convivi com pessoas maravilhosas, de professores, biólogos, técnicos aos colegas diários, com os quais aprendi muito e fiz muitas amizades. É certo que vou levar para o resto da minha vida não somente os ensinamentos, orientações ou elogios, mas também as críticas e “puxões de orelha”, pois todas essas coisas serviram de aprendizado e contribuíram para o meu amadurecimento acadêmico, pessoal e profissional. Sou grato a todos.

Primeiramente, a Deus, o Senhor da minha vida, a quem sou grato por toda inspiração e pela realização de mais uma etapa.

A toda minha família por ter apoiado, incentivado e investido durante toda minha vida. Serei sempre agradecido ao meu pai Gabriel, minha mãe Solange e meu irmão David. Não tenho palavras para expressar o quando vocês são importantes para mim.

Sou muito grato a minha fiel companheira e namorada Michele Regina por estar sempre do meu lado me apoiando, incentivando e por sempre ter uma palavra de ânimo nos momentos em que mais preciso. Obrigado por sempre acreditar em mim.

Agradeço a Profa. Dra. Inara Roberta Leal pela orientação, paciência e ensinamentos durante todos esses anos que foram fundamentais para a realização com sucesso deste trabalho. Foi um prazer desenvolver esse trabalho com uma profissional competente como você.

Um agradecimento ao pessoal da Unicamp, em especial:

Ao Prof. Dr. André Victor Lucci Freitas pela oportunidade que me deu ainda aluno da graduação em estagiar no Museu de Zoologia do Instituto de Biologia da Unicamp, que junto com Cristiano Agra, Lucas Kaminski, Eduardo Barbosa, Danilo Muniz e Poliana Felix obtive diversos treinamentos, estes essenciais para maior conhecimento e aprendizagem sobre as borboletas. Agradeço novamente ao Prof. André pelo apoio e coorientação deste trabalho e pela participação do Cristiano nas análises dos dados, sem o qual esta obra não teria o mesmo resultado. A Noemy Seraphim pela identificação das . Obrigado pela sua dedicação em analisar cada exemplar com atenção e pela paciência nas horas em que ficávamos extraindo as genitálias dos indivíduos. Sua ajuda foi diferencial neste trabalho. Aos borboleteiros Cristiano, Tina e Jessie pela estadia nos dias que fiquei em Campinas para identificar as espécies e analisar os dados deste trabalho. Obrigado pela amizade e confiança de vocês, pelo futebol com a rapaziada, pela companhia nas vezes que saímos juntos com o Prof. André para almoçar e jantar, sem contar com os ótimos churrascos. Foram bons momentos, ótimas conversas e também muito aprendizado. Muito obrigado!

Sou especialmente grato à Profa. Dra. Luciana Iannuzzi por sempre estar à disposição para tirar dúvidas e orientar no que for preciso. Mesmo em pouco tempo que nos conhecemos, além de sua gentileza e de procurar sempre encurtar a relação professor-aluno, proporcionando um laço familiar e amigável, percebi o exemplo de profissional que você é. Obrigado pelo carinho, pela força e por cada dica que me deste.

Ao Bruno Filgueiras pela parceria no trabalho de campo, por todos os bons momentos que passamos em Serra Grande, pelas conversas no alojamento, caminhadas nas matas e ideias trocadas. Também sou grato pela sua ajuda em algumas análises deste trabalho. Espero que essa amizade dure por muito tempo.

A Usina Serra Grande, Alagoas, por permitir a realização deste trabalho nos fragmentos e por disponibilizar um alojamento para pesquisas. A importante ajuda nos momentos de campo do amigo Pierre por nos guiar em meio às florestas.

Ao Programa de Pós-Graduação em Biologia Animal pela oportunidade de realizar esta pesquisa. Ao coordenador André Esteves por sua dedicação e por sempre ajudar os alunos no que for preciso. A toda a equipe de professores e colegas do mestrado e doutorado, em especial a Iris Arruda, André Lira, Manolo e Bruno Filgueiras pela amizade, pelas conversas, momentos de distração e bobagens, enfim, por todos os bons momentos que passamos juntos. Ao Laboratório de Taxonomia e Ecologia de Insetos (LABTEI) pelo acolhimento junto à equipe e a todos os colegas de trabalho, os quais me proporcionaram ótimas trocas de experiências, sem contar nas amizades formadas.

A Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE) pela bolsa concedida durante os dois anos do mestrado.

Cabe ainda agradecer algumas pessoas da época da graduação como o Prof. Dr. Argus Vasconcelos de Almeida da Universidade Federal Rural de Pernambuco que me ajudou desde o início do curso e acompanhou toda a minha trajetória até aqui. À bióloga Luci Duarte por apoiar e acreditar no meu potencial. Saudades de nossas coletas no Brejo dos Cavalos. A toda equipe de professores, biólogos e técnicos da entomologia UFRPE e aos amigos da graduação por, mesmo de longe, me acompanharem e incentivarem nessa longa jornada.

Agradeço a todos que direta ou indiretamente contribuíram para a execução deste trabalho e me ajudaram a concluir mais uma etapa da minha vida.

RESUMO

O processo de ocupação do Brasil levou a Floresta Atlântica a uma drástica perda e fragmentação de sua área original, sendo a região Nordeste o setor mais criticamente ameaçado. Diversos estudos mostram que a perda e fragmentação florestal altera a estrutura da comunidade de borboletas, mas nenhum deles foi realizado no Nordeste do Brasil. O objetivo deste estudo foi entender como esta guilda responde ao tipo de hábitat (fragmentos, borda e interior da floresta controle), bem como à área e ao grau de isolamento dos fragmentos em uma área altamente fragmentada da Floresta Atlântica Nordestina. Foram selecionados oito fragmentos florestais com áreas de 8 a 126 ha, além de bordas (50 m da margem) e interiores (> 200 m da margem) do maior remanescente (3.500 ha) da Floresta Atlântica Nordestina, utilizado como controle. Após 18.000 armadilhas/horas de amostragem, foram registrados 833 indivíduos pertencentes a 63 espécies de quatro subfamílias de Nymphalidae. A subfamília mais rica foi Satyrinae (39 espécies), seguida por Charaxinae (12), (10) e Nymphalinae (2). A subfamília mais abundante foi também Satyrinae com 73% dos indivíduos, seguida por Nymphalinae, Biblidinae e Charaxinae. As Curvas de Rarefação mostraram que não há diferenças significativas na riqueza de espécies entre borda da floresta, interior da floresta e fragmentos. Os resultados dos Modelos Lineares Generalizados Mistos também não evidenciaram diferença na riqueza entre os habitats, contudo, indicaram a área dos fragmentos e a combinação de área e o grau de isolamento dos fragmentos como preditores da riqueza observada e estimada e do número de indivíduos coletados, respectivamente. Foram registradas diferenças significativas na composição de espécies entre os hábitats através do Escalonamento Multidimensionais Não-Métricas e das Analises de Similaridade. Adicionalmente, as Análises de Correspondência Canônica indicaram que área e o grau de isolamento dos fragmentos explicaram 34% da variação na composição de espécies de borboletas. A distância entre as unidades amostrais também explicou uma parcela da similaridade na composição de espécies. Esses resultados indicam que a composição de espécies de borboletas frugívoras é mais influenciada pela perda e fragmentação de habitats que a riqueza de espécies. Por fim, vale ressaltar o registro de Morpho menelaus eberti, uma espécie de borboleta ameaçada de extinção neste setor de Floresta Atlântica.

Palavras-chave: conservação, composição de espécies, métricas de fragmentação, Centro de Endemismo Pernambuco ABSTRACT

The occupation of Brazil led to a drastic loss and fragmentation of the Atlantic Forest, being the Northeast region the most critically threatened sector. Several studies have shown that forest loss and fragmentation alter the structure of the community, but the Atlantic Forest from Northeast Brazil have been totally neglected. The aim of this study was understand how this guild responds to habitat type (fragments, edge and interior of control forest), as well as fragment area and patch isolation in a highly fragmented area of Northeastern Atlantic Forest. We selected 8 fragments ranging in size from 8 to 126 ha, as well as in the edge (50 m from forest border) and interior (> 200 m from forest border) of the largest area (3,550 ha) in this sector of Atlantic Forest. After 18,000 traps/hours of sampling, 833 individuals belonging to 63 species from four subfamily of Nymphalidae were recorded. The richest subfamily was Satyrinae (39 species), followed by Charaxinae (12), Biblidinae (10) and Nymphalinae (2). The most abundant subfamily was also Satyrinae with 73% of individuals, followed by Nymphalinae, Biblidinae and Charaxinae. Rarefaction curves showed no significant differences in the species richness among forest edge, forest interior and fragments. The results of Generalized Linear Mixed Models also showed no difference in richness between habitats, however, indicated fragment area as the best predictor of observed and estimated richness and the combination of fragment area and patch isolation as the best model to explain the number of individuals. Significant differences were recorded in the species composition among the habitats through of Non-metric Multidimensional Scaling and Analysis of Similarity. Additionally, the Canonical Correspondence analysis indicated the fragmented area and patch isolation explain 34% of the variation in species composition of fruit-feeding . The distance between survey units also explain the species composition similarity. These results together indicate that the species composition is more influenced by loss and fragmentation of habitat than species richness. Finally, it is worth mentioning the record of Morpho menelaus eberti, a species of butterfly endangered in this sector of Atlantic forest.

Key-words: conservation, fragmentation metrics, Pernambuco Center of Endemism, species composition LISTA DE FIGURAS

Figure 1. Map of the Serra Grande landscape, Alagoas, northeastern Brazil (A), showing the forest remnants in this sector of Atlantic forest (B). Forest fragments sampled are represented by dark shaded polygons. Blank spaces represent uniform matrix of sugar-cane monoculture ...... 61 Figure 2. Expected species richness according to the abundance-based richness estimators of frugivorous butterflies recorded in the Serra Grande landscape, Alagoas, northeastern Brazil. (A) Jacknife 1; (B) Chao 1 ...... 62 Figure 3. Species rarefaction curve for the fruit-feeding butterfly assemblages in fragments (dashed line), forest edges (grey line) and forest interiors (black line) in the Serra Grande landscape, Alagoas, northeastern Brazil. Thinner dashed lines are the confidence limits of the habitats ...... 63 Figure 4. Rank-abundance distribution (Whittaker plots) of fruit-feeding butterfly species in fragments (triangles), forest edges (open circles) and forest interiors (dark shaded circles) in the Serra Grande landscape, Alagoas, northeastern Brazil ...... 64 Figure 5. Ordination by NMDS method of fragments (triangles), forest edges (open circles) and forest interiors (dark-shaded circles) of the Serra Grande landscape, Alagoas, northeastern Brazil ...... 65 Figure 6. Biplot of the first and second axes of the Canonical Correspondence of fragments based on fruit-feeding butterfly species composition in the Serra Grande landscape, Alagoas, northeastern Brazil. Numbers are fragments and black circles represent the species ...... 66 LISTA DE TABELAS

Table 1. Abundance of fruit-feeding butterflies sampled in Atlantic forest fragments at Usina Serra Grande, Alagoas, northeastern Brazil ...... 55 Table 2. Results of the Generalized Linear Mixed Models for the effects of habitat type, fragment area and forest cover on number of individuals and observed and estimated fruit-feeding butterflies species richness sampled in Atlantic forest fragments at Usina Serra Grande, Alagoas, northeastern Brazil. AREA = Fragment Area; FC = Forest Cover ...... 58 Table 3. Distribution of abundance by subfamily in the three habitats sampled in Atlantic forest fragments at Usina Serra Grande, Alagoas, northeastern Brazil...... 59 SUMÁRIO

1. APRESENTAÇÃO ...... 12 2. INTRODUÇÃO GERAL ...... 13 2.1. Fragmentação florestal e a conservação da fauna ...... 13 2.2. A Floresta Atlântica Nordestina ...... 15 2.3. Uso de borboletas como ferramentas para diagnóstico ambiental ...... 16 3. BIBLIOGRAFIA CITADA ...... 19 4. CAPÍTULO 1: Effect of habitat loss and fragmentation on fruit-feeding butterflies in the Northeastern Atlantic Forest ...... 27 Abstract ...... 29 Introdution ...... 31 Material and Methods ...... 33 Results ...... 38 Discussion ...... 40 Acknowledgments ...... 45 References ...... 45 5. CAPÍTULO 2: Recent records of Morpho menelaus eberti (Weber) (Lepidoptera: Nymphalidae), an endangered species of Northeast Brazil ...... 67 Additional key words ...... 68 Text...... 68 Acknowledgments ...... 70 Literature cited ...... 71 6. CONSIDERAÇÕES FINAIS ...... 73 7. ANEXOS ...... 75

1. APRESENTAÇÃO

Diante da necessidade de selecionar áreas com elevada diversidade biológica e como o tempo, dinheiro e especialistas para fazer tal seleção são escassos, os indicadores biológicos destacam-se como agentes decodificadores das modificações no ambiente. Os insetos podem fornecer informações relevantes na definição de áreas fragmentadas com longa história de influência antrópica que sejam prioritárias para a conservação (MCGEOCH, 1998). As borboletas frugívoras por possuírem alta diversidade ecológica, fácil método de coleta, fidelidade de microhabitat e responderem a distúrbios ambientais, são considerados excelentes bioindicadores (UEHARA- PRADO et al., 2009). A utilização desses insetos como bioindicadores em uma área extremamente ameaçada com alta diversidade biológica e com baixo número de áreas protegidas, como é o Centro de Endemismo Pernambuco (considerada um hotspot dentro de um dos mais importantes hotspots, a Floresta Atlântica Brasileira, TABARELLI et al., 2006), pode ajudar a diagnosticar as áreas mais relevantes para a conservação. Muitos estudos sobre perda e fragmentação de florestas tropicais têm utilizado as borboletas frugívoras como bioindicadores (SHAHABUDDIN & TERBORGH, 1999; FERMON et al., 2000; HAMER et al., 2003; VEDDELER et al., 2005; BENEDICK et al., 2006, BARLOW et al., 2007), mas poucos têm focado neste grupo na Floresta Atlântica Brasileira (UEHARA-PRADO et al., 2007; RIBEIRO et al., 2008, 2012) e nenhum na Floresta Atlântica Nordestina (ou Centro de Endemismo Pernambuco). Com base nisto, o presente estudo teve como objetivo caracterizar a guilda de borboletas frugívoras quanto à riqueza, abundância e composição de espécies em uma paisagem antiga (criada há mais de 200 anos) e altamente fragmentada da Floresta Atlântica Nordestina e entender como este grupo se comporta frente à modificação de hábitat. No primeiro capítulo, investiguei como a riqueza, composição de espécies e distribuição de indivíduos da comunidade de borboletas frugívoras responde ao tipo de hábitat (fragmentos, borda e interior da floresta controle), métricas da mancha (área do fragmento) e métricas da paisagem (cobertura florestal ao redor dos fragmentos). No segundo capítulo, relatei os recentes registros de uma espécie ameaçada de extinção, característica das florestas nordestinas.

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2. INTRODUÇÃO GERAL

2.1. Fragmentação florestal e a conservação da fauna

Através da expansão de suas populações e do consequente uso dos recursos naturais, o homem tem alterado as paisagens naturais transformando áreas de cobertura vegetal contínua em remanescentes florestais pequenos, isolados e imersos em matrizes de diferentes composições. Este processo é conhecido como fragmentação de habitats, cujas consequências estão entre as principais causas da perda de biodiversidade no mundo (WHITMORE, 1997). Essas matrizes, na grande maioria dos casos, estão relacionadas com atividades humanas (pastos, plantações e áreas urbanas) e são ambientes hostis a biodiversidade (TABARELLI et al., 2004). Entre um terço e metade da superfície terrestre já foi transformada pela atividade humana (VITOUSEK et al., 1997). Como consequência, muitas espécies tiveram suas populações drasticamente reduzidas, de maneira que, em alguns casos, chegaram a se extinguir localmente (DIRZO & RAVEN, 2003). Em florestas tropicais, estes processos têm ocorrido em taxas sem precedentes, com as alterações de habitats em função de atividades antrópicas sendo milhares de vezes mais altas que a taxa procedente da dinâmica natural destas florestas (LAURANCE & PERES, 2006). As paisagens originadas pela fragmentação de habitats são influenciadas por uma série de fatores extrínsecos, tais como perda de área, isolamento dos remanescentes, efeito de matriz, aumento da incidência de fogo, aumento do corte de madeira e da caça, fatores estes que conduzem a alterações na composição das comunidades (LAURANCE et al., 2002; FAHRIG, 2003). Contudo, os efeitos principais dessa conversão da paisagem contínua em fragmentada estão associados à criação das bordas (D’ANGELO et al., 2004; TABARELLI & GASCON, 2005). As áreas de borda podem ser definidas como áreas limites entre dois tipos distintos de habitats (RIES et al., 2004). Elas apresentam diversas alterações em suas condições abióticas como aumento da intensidade luminosa incidente, da temperatura, mudanças das correntes de vento e ressecamento do solo (MURCIA, 1995). A intensidade dessas alterações está bastante ligada à natureza da matriz onde o fragmento está inserido e termina por influenciar a distribuição e a composição de espécies nestas áreas. Diante das severas mudanças abióticas e bióticas causadas pela perda e fragmentação de habitats, padrões de organização biológica podem ser completamente alterados em pequenos fragmentos e áreas de borda, desde organismos até o ecossistema 13

(WIRTH et al., 2008). No caso das florestas tropicais, já foi observado, por exemplo, (1) redução no número e no tamanho de populações de especialistas (eventualmente, até extinções locais), paralelo ao aumento daquelas adaptadas às perturbações em diferentes escalas espaciais (WIRTH et al., 2007; DOHM et al., 2011; LEAL et al., 2012); (2) mudanças na composição taxonômica, funcional e filogenética das assembleias na escala local e de paisagem (HELMUS et al., 2010; SANTOS et al., 2010; FILGUEIRAS et al., 2011; LEAL et al., 2012); (3) redução na riqueza de espécies e na diversidade funcional e filogenética das assembleias nas escalas local e de paisagem (SANTOS et al., 2008; LOPES et al., 2009; HELMUS et al., 2010; SANTOS et al., 2010; FILGUEIRAS et al., 2011; LEAL et al., 2012); (4) aumento de similaridade taxonômica entre assembleias nas escalas de paisagem e regional (LÔBO et al., 2011); (5) alteração, inclusive colapso, de interações entre espécies na escala local (THOMPSON, 2002; GIRÃO et al., 2007); e (6) mudanças nos padrões de fluxo e armazenamento de nutrientes (DANTAS DE PAULA et al., 2011) em resposta a perda e fragmentação de habitats. A Floresta Atlântica é uma das maiores áreas de florestas tropicais do Globo, ocupando o segundo lugar em extensão nas Américas (POR, 1992). Originalmente, a Floresta Atlântica e seus ecossistemas associados cobriam uma área de aproximadamente 1,3 milhões de km², o equivalente a cerca de 15% do território brasileiro, compreendendo 17 Estados, desde a costa leste de Natal, Rio Grande do Norte à Torres/Osório no Rio Grande do Sul (SOS MATA ATLÂNTICA & INPE, 2013). Apesar de sua importância, cerca de 90% de sua área original já foi destruída (BROWN & BROWN, 1992; RIBEIRO et al., 2009), sendo o ecossistema mais ameaçado pela ação antrópica (MORELLATO & HADDAD, 2000; MYERS et al., 2000). Na maioria da região, a vegetação remanescente ocorre como pequenos fragmentos isolados por agricultura ou sistemas não florestados (MORELLATO & HADDAD, 2000). Apesar da perda expressiva de habitat, a Floresta Atlântica é considerada um dos ecossistemas mais ricos em biodiversidade, além de se destacar com altíssimos níveis de endemismo; das 21.361 espécies de plantas vasculares, anfíbios, répteis, aves e mamíferos, 8.567 são endêmicas (MYERS et al., 2000). Por causa desta alta diversidade de espécies e de endemismos, associado à alta taxa de perda de habitat, a Floresta Atlântica é considera um dos principais hotspots mundiais, ou seja, uma das prioridades para a conservação de biodiversidade em todo o mundo (MYERS et al., 2000, MITTERMEIER et al., 2004; TABARELLI et al., 2005).

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2.2. A Floresta Atlântica Nordestina

A Floresta Atlântica Nordestina é uma das sub-regiões da Floresta Atlântica. Localizada ao norte do rio São Francisco, é conhecida também como Centro de Endemismo Pernambuco, e inclui toda a área de floresta costeira entre os estados de Alagoas e Rio Grande do Norte (SANTOS et al., 2007). Forma um bloco de floresta tropical espacialmente e biogeograficamente bem delimitado (SANTOS et al., 2007), cobrindo aproximadamente 56.000 km² ou 4,6% de toda região da Floresta Atlântica (LÔBO et al, 2011). Sua biota é influenciada pela região Amazônica, tornando-se, desta forma, uma área muito distinta dos outros setores da Floresta Atlântica (SILVA & TABARELLI, 2000). Quanto aos efeitos da perda e fragmentação de hábitats, a situação da Floresta Atlântica Nordestina não é diferente dos outros setores desta floresta no Brasil. As florestas desta região têm sido substituídas por cana-de-açúcar desde o início da colonização europeia. Atualmente, resta menos de 12% da área original (RIBEIRO et al., 2009). Suas áreas protegidas são pequenas, isoladas, mal protegidas e mal administradas, com alta pressão da caça e de corte de madeira (SILVA & TABARELLI, 2000, 2001). A perda de hábitat e a fragmentação têm sido tão impressionantes que 48% dos fragmentos remanescentes nesta região são <10 ha e poucos maiores que 1.000 ha (RANTA et al., 1998). Milhares desses fragmentos estão inseridos em uma matriz homogênea de plantações de cana de açúcar, oferecendo uma excelente oportunidade para estudo, em longo prazo, dos efeitos da fragmentação de hábitat (LÔBO et al., 2011). Diversos estudos tem mostrado efeito da perda e fragmentação de hábitats sobre a biota da Floresta Atlântica Nordestina. Em plantas, os principais efeitos incluem o aumento de árvores pioneiras (SANTOS et al., 2008; TABARELLI et al., 2010) em detrimento daquelas tolerantes à sombra (OLIVEIRA et al., 2004; SANTOS et al., 2008), emergentes (LAURANCE et al., 2000; OLIVEIRA et al., 2008; SANTOS et al. 2008), com sementes grandes dispersas por vertebrados (SILVA & TABARELLI, 2000, Santos et al., 2008) e com flores grandes polinizadas por vertebrados (LOPES et al., 2009). LÔBO et al. (2011) mostram que com todos esses efeitos agindo em conjunto, a fragmentação florestal pode levar a uma homogeneização da flora taxonômica de árvores em uma paisagem humanamente modificada.

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2.3. Uso das borboletas como ferramenta para diagnóstico ambiental

O retorno de sistemas modificados pela atividade humana para comunidades complexas de animais e plantas tropicais pode levar muito tempo ou mesmo ser impossível (BROWN, 1997a). Desta forma, a conservação efetiva das áreas remanescentes de habitats naturais tem sido uma tarefa difícil (WIENS, 1997). Apesar de muitos estudos demonstrarem os efeitos negativos da perda e fragmentação de hábitats a biota, poucos foram traduzidos em diretrizes e/ou políticas públicas necessárias para a gestão da floresta tropical em áreas que sofrem severas ameaças (TABARELLI & GASCON, 2005). Respostas negativas para níveis crescentes de perda e fragmentação de hábitat têm sido documentado em árvores (e.g. OLIVEIRA et al., 2004; SANTOS et al., 2008; TABARELLI et al., 2010), vertebrados (e.g. LAURANCE, 1990; CHIARELLO, 1999; GORRESEN & WILLIG, 2004; CUSHMAN, 2006; GIRAUDO et al., 2008; DIXO & METZGER, 2009) e tem sido mostrado por afetar os artrópodes (BOLGER et al., 2000). Entre os insetos, estudos mostram que área e grau de isolamento dos remanescentes são as variáveis que mais afetam a riqueza e composição de espécies de besouros rola-bosta (LARSEN et al., 2008; FILGUEIRAS et al., 2011) e formigas (BIEBER et al., 2006; GOMES et al., 2010; LEAL et al., 2012), apesar da riqueza e densidade de árvores também serem fatores que estruturam comunidades destes dois grupos de organismos (FILGUEIRAS et al., 2011; LEAL et al., 2012). Por outro lado, comunidades de cupins não têm sido influenciadas por quaisquer variáveis explanatórias (OLIVEIRA et al., 2013). Entre os insetos que têm sido sugeridos como indicadores para inventariar e monitorar a diversidade e a integridade de paisagens naturais (BROWN, 1991; KREMEN, 1992; PEARSON & CASSOLA, 1992; HALFFTER & FAVILA, 1993; KREMEN et al., 1993, 1994; LONGINO, 1994; FAVILA & HALFFTER, 1997), as borboletas são conhecidas como um dos grupos mais apropriados para avaliação ambiental (BROWN, 1991; KREMEN et al., 1993; SPARROW et al., 1994; NEW, 1997; BROWN & FREITAS, 2000, 2003), sendo, por isso, objetos de muitos estudos científicos no Brasil (BROWN, 1996). As borboletas juntamente com as mariposas apresentam entre 146.000 (HEPPNER, 1991) e 180.000 (LAMAS, 2008) espécies descritas da ordem Lepidoptera. Ocorrem no Brasil aproximadamente 71 famílias para este táxon, englobando mais de

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26.000 espécies descritas, metade da ocorrência para a Região Neotropical (BROWN & FREITAS, 1999). Nesta região, as borboletas somam quase 8.000 espécies (LAMAS, 2004), ocorrendo cerca de 3.280 no Brasil e 2.200 na Floresta Atlântica (BROWN & FREITAS, 1999). São divididas em duas superfamílias, sendo representadas por seis famílias, Hesperioidea (Hesperiidae) e Papilionoidea (Papilionidae, Pieridae, Nymphalidae, Lycaenidae e Riodinidae). Estudos apontam Hesperiidae, Nymphalidae e Riodinidae como as três famílias mais ricas no país, seguidas por Lycaenidae, Pieridae e Papilionidae (ISERHARD et al., no prelo). Normalmente, as borboletas podem ser separadas em duas guildas, quando considerado o modo de alimentação dos adultos (DEVRIES, 1987): (1) as nectarívoras, que se alimentam de néctar durante a sua vida adulta, compreendendo as espécies das famílias Papilionidae, Pieridae, Lycaenidae, Riodinidae e Hesperiidae e alguns grupos de Nymphalidae. (2) as frugívoras, que incluem as espécies que se alimentam de frutas fermentadas, pertencentes a quatro subfamílias de Nymphalidae: Biblidinae, Charaxinae, Satyrinae e pela tripo Coeini de Nymphalinae (WAHLBERG et al., 2009). Borboletas frugívoras também podem se alimentar de fezes de vertebrados e seiva secretada por algumas espécies de plantas e carniça (DEVRIES, 1987). Várias características tornam as borboletas bons indicadores: são um grupo altamente diverso, mas as espécies apresentam alta fidelidade de habitat, tem ciclos de vida curtos, as espécies são facilmente atraídas, amostradas e identificadas, além do grupo ser bastante conhecido taxonomicamente, ecologicamente e comportamentalmente (BROWN, 1991, 1992, 1993a–c, 1997a, b; BROWN & FREITAS, 1999). Medidas de diversidade e métodos para avaliação do status nas comunidades desses insetos estão bem avançados, e um monitoramento não destrutivo pode ser efetuado com confiança satisfatória (NEW, 1997). Adicionalmente, borboletas são grandes, coloridas (a maioria), de fácil visualização, e possuem um grande apelo popular, tendo sido inclusive utilizadas como “espécies bandeiras” (flagship species) e/ou “espécies guarda-chuvas” (umbrela species) com êxito em programas de monitoramento (POLLARD & YATES, 1993; RAIMUNDO et al., 2003) que contam com o envolvimento da população leiga e populações tradicionais, propiciando o fortalecimento do elo sociedade-conservação (ver Plano de ação nacional para a conservação dos lepidópteros ameaçados de extinção em FREITAS & MARINI- FILHO, 2011). Por fim, a sua preservação pode garantir a de muitas espécies associadas que habitam os mesmos ambientes ou tenham necessidades similares (NEW, 1997).

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A amostragem com borboletas frugívoras apresenta algumas vantagens práticas: elas são facilmente amostradas com armadilhas contento iscas de frutas fermentadas, permitindo que duas ou mais áreas possam ser amostradas simultaneamente com o mesmo esforço amostral. Além disso, com o uso de armadilhas, as borboletas podem ser identificadas no local de captura, posteriormente, marcadas e liberadas, de modo que pode ser avaliada a taxa de recaptura com o mínimo de manipulação (UEHARA et al., 2005). Este grupo compreende entre 50% e 75% da riqueza total de Nymphalidae Neotropicais (DEVRIES, 1987) e sua diversidade esta correlacionada com a diversidade total de borboletas (BROWN & FREITAS, 2000). Estudos mostram que borboletas respondem às características da estrutura da vegetação (RAMOS, 2000; BARLOW et al., 2007), possuem relação estreita com condições microclimáticas (RIBEIRO & FREITAS, 2010; CHECA et al., 2014) e que a riqueza de espécies é positivamente correlacionada com a área do fragmento (VEDDELER et al., 2005; BENEDICK et al., 2006; UEHARA-PRADO et al., 2007). Características como o grau de isolamento (SHAHABUDDIN & TERBORGH, 1999; VEDDELER et al., 2005; BENEDICK et al., 2006) e o tipo de paisagem circundante (RIBEIRO et al., 2012) também podem influenciar a distribuição da comunidade de borboletas frugívoras. Fragmentação de habitat pode afetar a riqueza, a abundância e a diversidade (DEVRIES et al., 1997; FERMON et al., 2000; VEDDELER et al., 2005; BENEDICK et al., 2006, BARLOW et al., 2007), no entanto, mas do que isso, estudos mostram a fragmentação alterando significativamente a composição da comunidade de borboletas (SHAHABUDDIN & TERBORGH, 1999; HAMER et al., 2003; UEHARA- PRADO et al., 2007; RIBEIRO et al., 2008; DOVER & SETTELE, 2009; UEHARA- PRADO et al., 2009). Apesar de existirem muitos estudos enfocando o efeito da perda e fragmentação de florestas tropicais sobre borboletas frugívoras, poucos têm sido realizados na Floresta Atlântica Brasileira e nenhum na Floresta Atlântica Nordestina. Portanto, estudos ainda são necessários para ajudar a compreender quais os fatores determinantes que estão envolvidos na distribuição deste grupo em paisagens altamente fragmentadas.

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TABARELLI, M.; SILVA, J. M. C.; GASCON, C. Forest fragmentation, synergisms and the impoverishment of neotropical forests. Biodiversity and Conservation, v.13, p. 1419-1425, 2004.

TABARELLI, M.; SIQUEIRA, J. A.; SANTOS, A. M. M. A Floresta Atlântica ao norte do Rio São Francisco. In: PORTO, K. C.; ALMEIDA-CORTEZ, J. S.; TABARELLI, M. (orgs). Diversidade biológica e conservação da Floresta Atlântica ao norte do Rio São Francisco. Ministério do Meio Ambiente, Brasília, p. 41-48.

THOMPSON, J. N. Plant-animal interactions: future directions. In: HERRERA, C. M.; PELLMYR, O. (eds). Plant-animal interactions: an evolutionary approach. Blackwell, Oxford, 2002, p. 236-247.

UEHARA-PRADO, M., BROWN, K. S.; FREITAS, A. V. L. Biological traits of frugivorous butterflies in a fragmented and a continuous landscape in the South Brazilian Atlantic Forest. J. Lepid. Soc. v.59, n.2, p.96-106, 2005.

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UEHARA-PRADO, M.; BROWN, K. S.; FREITAS, A. V. L. 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, v.16, p. 43–54, 2007.

UEHARA-PRADO, M.; FERNANDES, J.O.; BELO, A.M.; MACHADO, G.; SANTOS, A.J.; VAZ-DE-MELLO, A.Z.; FREITAS, A.V.L. Selecting terrestrial arthropods as indicators of small-scale disturbance: A first approach in the Brazilian Atlantic Forest. Biological Conservation, v. 142, n. 6, p. 1220-1228, 2009.

VEDDELER, D.; SCHULZE, C. H.; STEFFAN-DEWENTER, I.; BUCHORI, D.; TSCHARNTKE, T. The contribution of tropical secondary forest fragments to the conservation of fruit-feeding butterflies: effects of isolation and age. Biodiversity and Conservation, v.14, p. 3577-3592, 2005.

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26

CAPÍTULO 1

EFFECT OF HABITAT LOSS AND FRAGMENTATION ON FRUIT-FEEDING

BUTTERFLIES IN THE NORTHEASTERN ATLANTIC FOREST

Artigo a ser submetido para o jornal Insect Conservation and Diversity

27

Effect of habitat loss and fragmentation on fruit-feeding butterflies in the

Northeastern Atlantic Forest

Douglas H. A. Melo1, Bruno K. C. Filgueiras1, Cristiano A. Iserhard2, Luciana

Iannuzzi3, André V. L. Freitas4, Inara R. Leal5,6

1Programa de Pós-Graduação em Biologia Animal, Universidade Federal de

Pernambuco, Recife, PE, CEP 50670-901, Brazil

2Departamento de Ecologia, Zoologia e Genética, Universidade Federal de Pelotas,

Pelotas, RS, C.P. 354, CEP 96160-000, Brazil

3Departamento de Zoologia, Universidade Federal de Pernambuco, Recife, PE, CEP

50670-901, Brazil

4Departamento de Biologia Animal, Universidade Estadual de Campinas, Campinas,

SP, C.P. 6109, CEP 13083-862, Brazil

5Departamento de Botânica, Universidade Federal de Pernambuco, Recife, PE, CEP

50670-901, Brazil

6Corresponding author: E-mail: [email protected] (I.R. Leal).

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Abstract

1. Habitat loss and fragmentation has drastically altered the availability and quality of tropical forest habitats, but information on how this change in habitats quality influence fruit-feeding butterfly assemblage is still insufficient.

2. We examine how species richness, abundance and composition of fruit-feeding butterfly assemblages respond to habitat, fragment area and patch isolation in the

Atlantic forest of northeast Brazil.

3. Our study was carried out in three habitat types: interior of eight fragments ranging in size from 8 to 126 ha, as well as eight areas of forest edge (50 m from forest border) and eight of forest interior (> 200 m from forest border) of the largest area (3,550 ha) in this sector of Atlantic forest.

4. The results indicated that habitat type did not explain species richness, but fragment area and fragment area + patch isolation influenced richness and abundance of fruit- feeding butterflies, respectively.

5. Species composition responded to habitat type, fragment area and patch isolation, as well as the distance between survey units.

6. The record of the endangered species Morpho menelaus eberti in Coimbra Forest deserve special attention, because it is one of the few areas where this species still persists in the Northeast Atlantic forest.

7. These findings highlight 1) fruit-feeding butterfly sensibility to habitat loss and fragmentation, 2) species composition as a better variable to access the responses of fruit-feeding butterfly assemblages to anthropogenic disturbance of Atlantic forest and

3) large remnant as refuge for disturbance and habitat fragmentation sensitive species to, being a priority area for conservation.

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Key-words: area effects, bioindicators, conservation, forest fragmentation, frugivorous butterflies, Nymphalidae, patch isolation, Pernambuco Center of Endemism, species composition, species richness.

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Introduction

Habitat loss and fragmentation has drastically altered the availability and quality of tropical forest habitats, particularly the permanent elimination of old-growth stands with negative impacts on tropical biodiversity persistence in human-modified landscapes (Foley et al., 2005; Hansen et al., 2013; Laurance et al., 2014). Increasing rates of such conversion has urge scientists to find out the major forces controlling biological dynamic in this emerging and novel environments for the sake of both biodiversity persistence and provision of ecological services (see Melo et al., 2013).

Particularly in the case of tropical forests, the conservation value of human-modified landscapes is still in debate (e.g. Dent & Wright, 2009; Melo et al., 2012), but we already know that biodiversity persistence is correlated with attributes such as patch area, shape, connectivity, surrounding matrix, age, and historic use (Didham et al.,

1996; Kruess & Tscharntke, 2000; Fahrig, 2003; Ewers & Didham, 2006; Filgueiras et al., 2011; Ribeiro et al., 2012; Ribeiro & Freitas, 2012). Patch area and shape are particularly important as they usually correlate strictly with proportion of remaining forest habitat exposed to edge effects: the abiotic and biotic processes at the edge, which result in a detectable difference in composition, structure, or function near the edge, as compared with the ecosystem on either side of the edge (Harper et al., 2005).

Studies have shown effect of habitat loss and fragmentation on a wide variety of taxa. In tree assemblage, for instance, shifts in the functional composition along forest edge and small fragments have been described (Oliveira et al., 2004; Tabarelli et al.,

2008) where shade-tolerant species (Oliveira et al., 2004; Santos et al., 2008), emergent and canopy trees (Laurance et al., 2000; Oliveira et al., 2008; Santos et al., 2008), trees pollinated by vertebrates (Lopes et al., 2009), and large-seeded trees dispersed by medium to large-bodied vertebrate (Melo et al., 2006) are impoverished. In contrast,

31 many other species, such as fast-growing pioneer trees (Laurance et al., 2006; Santos et al., 2008) and lianas (Laurance et al., 2001), can increase in edge-dominated habitats.

Therefore, tree assemblage experiences a process of biotic homogenization driven by the proliferation of some r-strategists in fragmentation-related habitats (Tabarelli et al.,

2008; Lôbo et al., 2011).

Detrimental responses to increasing levels of forest loss and fragmentation have also been documented in vertebrate (Laurance, 1990; Chiarello, 1999; Gorresen &

Willig, 2004; Cushman, 2006; Giraudo et al., 2008; Dixo & Metzger, 2009) and have been shown to affect arthropods (Bolger et al., 2000). Among insects, studies show that the fragment area and isolation are the best explanatory variables for shifts in species richness and functional composition of dung beetles (Larsen et al., 2008; Filgueiras et al., 2011) and ants (Gomes et al., 2010; Leal et al., 2012), although tree density and richness are also important drivers for these changes (Filgueiras et al., 2011; Leal et al.,

2012). On the other hand, termite assemblages were not influenced by patch and landscape metrics, which suggests that they are particularly resilient in relation to fragmentation (Oliveira et al., 2013).

Butterflies also are influenced by human disturbance, being the fragmentation, degradation and destruction of natural landscapes, the main causes of assemblage change and impoverishment (New, 1995, 1997). More specifically, studies show that fruit-feeding butterflies respond to fragment area (Veddeler et al., 2005; Benedick et al.,

2006; Uehara-Prado et al., 2007), degree of isolation (Shahabuddin & Terborgh, 1999;

Veddeler et al., 2005; Benedick et al., 2006) and surrounding landscape (Ribeiro et al.,

2012), as well as characteristics of vegetation structure (Ramos, 2000; Barlow et al.,

2007; Ribeiro & Freitas, 2012) and microclimate conditions (Ribeiro & Freitas, 2010;

Checa et al., 2014). Species richness, abundance and diversity of fruit-feeding

32 butterflies can be affected by habitat fragmentation (DeVries et al., 1997; Fermon et al.,

2000; Veddeler et al., 2005; Benedick et al., 2006; Barlow et al., 2007), but more importantly, alteration in species composition have been frequently documented

(Shahabuddin & Terborgh, 1999; Hamer et al., 2003; Uehara-Prado et al., 2007; Ribeiro et al., 2008; Dover & Settele, 2009; Uehara-Prado et al., 2009).

Here we selected an aging (>200-yr old), and hyper-fragmented landscape of

Atlantic forest to examine how species richness, abundance and composition of fruit- feeding butterfly assemblages respond to habitat type (small fragments, forest edge and forest interior of the largest fragment), patch metrics (fragment area) and landscape metrics (forest cover around fragments). We use fruit-feeding butterflies (i.e. species of

Biblidinae, Charaxinae, Satyrinae and by tribe Coeini of Nymphalinae (sensu Wahlberg et al., 2009) because they can be easily captured in traps baited with standardized mixtures of fermented fruits, allowing simultaneous sampling in several areas with similar effort. Furthermore, the richness of this group is highly correlated with the richness total of the butterflies in a given area (Brown & Freitas, 2000). We expected that forest edge as well as smaller and more isolated fragments support lower species richness and abundance and a different species composition than forest interior.

Material and Methods

Study area

The study was conducted at Usina Serra Grande, a private sugar company located in the State of Alagoas, northeastern Brazil (8°30’S, 35°50’W). The landscape of the Usina Serra Grande (667 km²) has been fragmented during the last 200 years and currently has about 9% of forest cover (Santos et al., 2008), assigned to a unique biogeographic unit of the Atlantic forest region (i.e. the Pernambuco Center of

33

Endemism, Santos et al., 2007). Remaining vegetation consist of 109 forest fragments

(ranging in size from 1.67 to 3,500 ha) immersed in an old (over 60 years), homogeneous, stable and inhospitable matrix of sugarcane monoculture (Santos et al.,

2008). Serra Grande fragments include the Coimbra forest – the largest (3,500 ha) and best preserved patch of Atlantic forest in northeastern Brazil (Santos et al., 2008).

Coimbra still supports ecological groups that are believed to inhabit more continuous and undisturbed tracts of Atlantic forest, such as large-seeded trees and frugivorous vertebrates (e.g. Girão et al., 2007; Santos et al., 2008; Lopes et al., 2009). All these characteristics make of the Serra Grande landscape particularly suitable for assessing the long-term effects of habitat loss and fragmentation.

Serra Grande landscape is located on the low-elevation plains (300-400 m a.s.l.) of the Borborema Plateau, a mountain chain stretching north and south along the northeastern coast of Brazil. The prevailing soils of the study area are latosols and podzolic (IBGE, 1985). The temperature varies between 16 and 40ºC, with annual average of 26ºC and average annual rainfall of ca 2,000 mm (data provided by Usina

Serra Grande), with 3-months dry station (< 60 mm per mouth) lasting from November to January and the months from April to August being the rainiest (IBGE, 1985). The vegetation of the site consists of lower mountain rainforest (Veloso et al., 1991), with three well defined arboreal strata (4-6 m, 15-20 m and 25-30 m) (IBGE, 1985). The families best represented in the area are: Leguminosae, Lauraceae, Sapotaceae,

Chrysobalanaceae e Lecythidaceae (for trees ≥ 10 cm diameter at breast height – DBH;

Oliveira et al., 2008).

We conducted our surveys in three different habitat types: 1) eight small forest fragments, ranging from 8 to 126 ha (hereafter fragments), 2) the interior of the largest fragment of Serra Grande (the Coimbra forest with 3,550 ha) used here as control area

34

(hereafter forest interior), and 3) the edge of the same large fragment (hereafter forest edge) (Fig. 1). We estimated fragment area and amount of forest cover retained in the surrounding landscape as a measure of patch isolation (hereafter patch isolation)

(Gorresen & Willig, 2004) and therefore availability of source populations. It was defined as the percentage of forest within 1-km of the fragment perimeter. The area of fragments and the patch isolation were quantified using two GIS packages (ArcView

3.2 and Erdas Imagine 8.4) on the basis of: 1) three Landsat and Spot images (years

1989, 1998, 2003) and 2) a set of 160 aerial photos (1:8000) taken from helicopter overflights commissioned in April 2003 (provided by Conservation International do

Brasil).

Fruit-feeding butterfly surveys

Butterflies were surveyed following the method described in Uehara-Prado et al.

(2005, 2007). The sampling was carried from November of 2012 to January of 2013, period corresponding to the dry season, in all three habitat types (see above). In each month, the traps remained open in site during four consecutive days. Each one of the eight fragments received one sample unit (hereafter SU) consisting of five portable traps in its interior, totaling 40 traps in eight SUs. In the control area eight SUs were installed in forest edge (50 m from forest border) and eight in the interior (> 200 m from forest border), totaling 80 traps in 16 SUs. The traps stayed arranged in a linear transect, separated from each other by a distance of 30 m, uspended among 1 to 1.5 m of soil.

The traps were revised every 48 h, when the baits were replaced.

Each trap consists of cylindrical tubes made with netting (110 cm of high x 35 cm of diameter) and an internal cone (30 cm high and 22 cm wide at the opening) at the bottom for prevent butterflies to escape. The lower part is open and attached to a

35 plywood platform by a distance of 4 cm for allow entry of butterflies. A mixture of banana and sugar cane juice fermented by 48 h was used as attractive bait. The baits were placed inside of the traps in plastic pots with a perforated cover to prevent the drowning butterflies in liquid, of serve as food for other insects and reduce evaporation

(Hughes et al., 1998).

All the individuals were captured, sacrificed by constriction in the thorax, placed in entomological envelopes for subsequent assembly and identification. Voucher specimens of all recorded species were deposited in the entomological collections of the

Universidade Federal de Pernambuco, Recife, PE, and Universidade Estadual de

Campinas, Campinas, SP, in Brazil.

Statistical analysis

We assessed the completeness of each sample by calculating the number of observed species as a percentage of the total richness, which was estimated based on the average of two abundance-based nonparametric estimators, Chao 1 and Jacknife 1

(Colwell, 2005). Method of individual-based rarefaction was used to compare species richness among habitats (Gotelli & Graves, 1996), an useful comparison of species richness when samples have different sizes. Patterns of species dominance were compared between habitats using species rank-abundance plots. Method of rarefaction and species-abundance models was calculated with the software Past (Hammer et al.,

2001).

Generalized Linear Mixed Models (GLMM) were used to detect the effects of habitat type, fragment area and patch isolation on the observed and estimated fruit- feeding butterfly species richness and on the abundance. The performance of GLMM was assessed using Akaike’s Information Criterion (AIC). We used three measures

36 associated with the AIC to determine the optimal model given the data: the ΔAIC ranks alternative models according to their AIC values; the AIC for each model (rescaled based on the best model) and wAICc – chance for the model to be selected, which varies from 0 to 1 (Burnham & Anderson, 1998).

To test hypothesis that the taxonomic composition is different between the three habitats (forest edge, forest interior and fragments), a non-metric multidimensional scaling (NMDS) ordination was performed, based on a Bray-Curtis dissimilarity matrix of species composition (Clarke & Gorley, 2001). To support this hypothesis the

ANOSIM tests (Clarke & Gorley, 2001) was performed to examine the relationships between habitat types on the species similarity. These analyses were done using

PRIMER software (Clarke & Gorley, 2001).

We also performed a Canonical Correspondence analysis (CCA) to investigate whether explanatory variables explained fruit-feeding butterfly species composition using abundance data. In the stepwise forward selection we included only those environmental variables that proved significant (P < 0.05) in the final ordination.

Explanatory variables were tested for independency with Pearson Correlation. Data on fragment area were log10-transformed prior to analysis in order to meet the assumptions of normality. Normality and homoscedasticity of the residuals were checked with

Lilliefors and Levene tests, respectively. Finally, to check spatial independence in taxonomic similarity between the habitats studied was performed the Mantel test.

GLMM, CCA and Mantel analyses were carried out using R 2.11.1 (R Development

Core Team, 2011).

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Results

After 18000 trap-hours of sampling, 833 individuals were captured, comprising

63 species of fruit-feeding butterflies belonging to all four subfamilies (Table 1). Of this total, 608 individuals of 50 species were captured in fragments and 225 individuals of

43 species in Coimbra Forest (being 128 individuals of 34 species in the edge and 97 individuals of 26 species in the interior). The subfamily with higher number of species was Satyrinae (39 species), followed by Charaxinae (12), Biblidinae (10) and

Nymphalinae (2) (Table 1). The distribution of species richness by subfamily in all sampled habitats follows this same order, differing only in abundance. Comparing among habitat types, the fragments shared 19 species with the interior, and 25 with the forest edge, and the forest edge shared 17 species with the interior. According to the richness estimators, the species richness in the community (all three habitat types pooled) should vary from 73 to 87 (Chao 1 = 80,00 ± 7,03; Jacknife 1 = 79,29 ± 4,03)

(Fig. 2). The number of singletons (considering all habitat types pooled) was 12 in fragments, 18 in forest edge and 12 in forest interior.

Rarefaction curves showed that richness was similar in all three habitat types

(Fig. 3). Analyzing each habitat type, in the Coimbra forest, all SU had their richness within the expected, according to the confidence interval, but one SU from the edge presented a lower richness. Among the fragments, only half of them presented the richness within the expected (data not shown). GLMM did not indicate an effect of habitat type on butterfly richness and abundance, corroborating results of rarefactions curves. On the other hand, GLMM revealed that fragment area was the best model predicting the richness of fruit-feeding butterflies observed and estimated, and that the combination of area and patch isolation was the best model for number of individuals

(Table 2).

38

The species-abundance distribution represented by the Whittaker plots (Fig. 4) shows the preponderance of less abundant species (n ≤ 8 individuals) in all three habitat types (70%, 85% and 88% in fragments, forest edges and in the interior, respectively).

The five most abundant species (represented by more than 60 individuals) were

Pareuptychia sp.1, Euptychoides sp., Taygetis laches laches and Cissia terrestris

(Satyrinae) and Colobura dirce dirce (Nymphalinae), representing 48% of all captured individuals. No species was captured in all SUs, but C. dirce dirce was the most frequent in all three habitat types, being recorded in 21 out of 24 SUs.

Butterfly abundance was much higher in the fragments (almost three times the total sampled in Coimbra forest); within the Coimbra forest, butterfly abundance was clearly higher in the forest edge. The relative abundance of the different taxonomic groups was unequal in the three habitat types: in Coimbra forest, the forest edge showed a clear dominance of Satyrinae compared with the interior (proportions of other subfamilies were much equivalent). In the fragments, the Satyrinae were even more preponderant in relation to Coimbra forest, and in this case, all other groups were less represented (Table 3).

The NMDS showed that the three habitat types are organized in three separated groups: forest interior and forest edge and fragments (Fig. 5). The ordination was well supported by low stress levels of 0.19. This is supported by ANOSIM revealed significant correlation between habitat type and degree of taxonomic similarity between communities. There was a small effect between forest edge and the fragments (R =

0.352, p = 0.001), a stronger effect between the forest edge and forest interior (R =

0.449, p = 0.001) and an even more significant effect between forest interior and fragments (R = 0.685, p = 0.002). In addition, CCA showed that fragment area and patch isolation significantly explained 34% of the variation in species composition of

39 fruit-feeding butterflies (Fig. 6). Finally, Mantel test indicated that the spatial distribution of SU also influenced butterfly species distribution and consequently similarity patterns (R = 0.3407, p = 0.004).

Discussion

Our study investigated how habitat type, and patch and landscape metrics influence species richness and composition of fruit-feeding butterfly assemblages in a fragmented landscape of Atlantic forest. Our results indicated that habitat type did not explain species richness, but fragment area and fragment area + patch isolation influenced richness and abundance of fruit-feeding butterflies, respectively. Species composition responded to habitat type, fragment area and patch isolation, as well as the distance between SU. These findings highlight 1) fruit-feeding butterfly sensibility to habit loss and fragmentation (correlated with habitat type and patch/landscape metrics) and 2) species composition as a better variable to access the responses of butterfly assemblages to anthropogenic disturbance of Atlantic forest.

Despite the rarefaction curve did not reach an indication of asymptote, we do not expect a substantial increase in species richness. This result is supported by other studies in other sectors of Atlantic forest, where similar number of fruit-feeding butterfly species have been collected (e.g. 70 in Uehara-Prado et al., 2007 and 73 in

Ribeiro et al., 2012). Through this comparison, it may be observed that even in a sector highly fragmented, such as the Northeastern Atlantic Forest, the studied landscape presents a fruit-feeding butterfly fauna very rich and diverse, comparable to the well- preserved areas.

Species richness was not different between forest edge, interior and small fragments, but fragment area presented a significant influence on this variable. In fact,

40 this pattern has been already observed in previous studies. For example, Uehara-Prado et al. (2007) observed similar species richness in fragmented and continuous landscapes, but area effects have been documented influencing the richness of fruit-feeding butterflies assemblage (Veddeler et al., 2005; Benedick et al., 2006; Uehara-Prado et al.,

2007). We found no effect of isolation on species richness of fruit-feeding butterflies in this study, but fragment area and isolation played an important role on the number of individuals. Similarly, Veddeler et al. (2005) not verified effect of isolation (up to 1,7 km) on fruit-feeding butterflies in Indonesia. Shahabuddin & Terborgh (1999) in turn suggested that fragments located within 1 km of their habitat source may not experience a reduction in colonization of butterflies. On the other hand, fragments located more than 1 km of large islands may be subject to reduction effects of colonization. These results suggest that habitats with different condition did not suffer a reduction in species number, except when habitat loss and isolation are severe.

Rather than species loss, different habitats presented different species composition, as demonstrated by NMDS and ANOSIM tests. Previous studies have shown that fruit-feeding butterflies do not suffer detectable changes in the process of forest fragmentation on species richness and diversity, but change their species composition considerably. For example, Shahabuddin & Terborgh (1999) found that species composition varied significantly between continental sites and small islands in

Venezuela. Hamer et al. (2003) found little difference in diversity in natural and logged forests of northern Borneo, but observed marked differences in species composition.

Ribeiro et al. (2008) showed high variability in species composition between small fragments of Atlantic forest in São Paulo, Brazil. Uehara-Prado et al. (2007) observed certain ‘resistance and tenacity’ of fruit-feeding butterflies facing habitat modification, which also found no significant changes in species richness between continuous forest

41 and fragments, however found notable differences in species composition between these two habitats in São Paulo, Brazil. These data support the idea of significant interspecific differences in butterfly responses to fragmentation, i.e, adverse effects of fruit-feeding butterflies that can be associated with the dispersal ability, host plant and behavior, reflecting changes in species composition of butterfly assemblages (Shahabuddin &

Terborgh, 1999; Uehara-Prado et al., 2007).

The general patterns of abundance presented that most abundant species in small fragments were not found or occurring very rarely in forest interior. These results are linked with the tribe, presenting higher number of individuals in both habitats, however their composition are totally different indicating specific subset of species related to each habitat. The increasing on populations of Satyrini species after forest fragmentation or other types of disturbance has also been reported in previous studies

(Daily & Ehrlich, 1995; Shahabuddin & Terborgh, 1999; Ribeiro et al., 2012). On the other hand, some studies found lower densities or even absence of large satyrines, like

Taygetis genus, on fragments. This fact strongly suggest an association of these groups with more preserved environments (Shahabuddin & Terborgh, 1999; Ramos, 2000;

Uehara-Prado et al., 2007). In general, the presence of small satyrines in fragments shows suitable conditions for the development and establishment of these species.

Generally, Satyrini associated to this kind of habitat feed on grasses in the larval stage

(Beccaloni et al., 2008), that occurs in high densities in disturbed forests, demonstrating that sun lover butterfly species are much more associated with habitat fragmentation and opened areas.

In some studies in tropical forests (e.g. DeVries et al., 1997; Barlow et al., 2007;

Uehara-Prado et al., 2007), fragmentation-related habitats (e.g. small fragments and forest edges) have higher abundance of fruit-feeding butterflies than well preserved

42 environments (e.g. forest interior). In the present study, the patterns found are similar, in which fragments were more abundant, followed by forest edge and forest interior. As shown above, this occurs because in fragmentation-related habitats light level increases, which promote a proliferation in pioneer plant species in detriment of other species more characteristic of mature forest (Oliveira et al., 2004; Santos et al., 2008), favoring an increase in resource (host plant) for larvae of sun lover species. Forest fragmentation changes the community structure in terms of abundance and composition, replacing species susceptible to environmental disturbances by other more resistant to sunny and perturbed environments, able to explore the surrounding matrix (Ribeiro et al., 2012).

Thus, forest fragmentation results in changes in taxonomic identities between habitats, our results support this idea through similarity analysis, showing that although the species richness did not change in fragmentation-related habitats and in forest interior, the taxonomic composition is different.

Although the NMDS shows dissimilarity among habitats, this does not mean that small fragments are not important for butterfly conservation, and these fragments deserve attention, even presenting an indication of disturbance. This is consistent with the rarefaction curve showing no significant differences in richness between edge and interior and fragments. Moreover, the species were not evenly distributed among fragments. Ribeiro et al. (2008) working in small forest fragments, identified low alpha diversity in each trap and high beta diversity within fragments and among fragments.

This means that butterflies are not randomly distributed inside forest fragments.

Likewise, Benedick et al. (2006) evaluated the impacts of habitat fragmentation on fruit- feeding butterflies in a tropical forest in Borneo, also found high beta diversity among fragments of the landscape. This suggests the importance of forest fragments to the preservation of butterfly fauna, since these habitats maintain populations of several

43 species, due to the heterogeneity of these habitats (Veddeler et al., 2005; Benedick et al., 2006; Ribeiro et al., 2008).

This study shows that fruit-feeding butterflies respond to the effects of habitat loss and fragmentation. All habitats are equally rich, but the species associated to each habitat are not necessarily the same. There is a turnover of disturbance-sensitive species by other able to survive in open and sunny environments. These data reinforce the importance of using fruit-feeding butterflies as indicators of environmental disturbance.

Although small fragments are also important for the preservation of fruit-feeding butterflies, this does not lessen the importance that should be given to large fragments, like the Coimbra forest. Along the samplings there were the records of the endangered species Morpho menelaus eberti, an endangered Brazilian butterfly species from the northeastern Atlantic forest (Machado et al., 2008; Freitas & Brown, 2008; Freitas &

Marini-Filho, 2011). Although a single female has been captured in the forest edge, several other male individuals were observed flying in Coimbra forest, with some individuals seen in nearby fragments (Melo et al., in prep.). The presence of this butterfly in the region, undoubtedly, deserves attention, because it is one of the few areas where this species still persists in the Northeast Atlantic forest. This fact makes clear the importance of Coimbra forest has as refuge for many species that not survive in disturbed and fragmented sites. Habitats like the Coimbra forest deserves special attention and management measures should be taken urgently: 1) in order to protect important and endangered species of Brazilian fauna, and 2) to preserve forests with high levels of endemism, such as the Pernambuco Center of Endemism, also the most threatened of the Brazilian Atlantic Forest.

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Acknowledgments

We thank to Luis Antônio Bezerra and José Clodoaldo Bakker for authorizing our fieldwork at the Usina Serra Grande and Noemy Seraphim Pereira for help in identifying species of the genus Hermeuptychia. We are also grateful to ‘Coordenação de Aperfeiçoamento de Pessoal de Nível Superior’ for financial support (process

02488/09-4) and for ‘Conservação Internacional do Brasil’ (CI Brasil), ‘Centro de

Estudos Ambientais do Nordeste’ (CEPAN) and ‘Usina Serra Grande’ for infrastructure and logistic support during field work. DHAM and BKCF acknowledge the ‘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). IRL thanks the ‘Conselho Nacional de Desenvolvimento

Científico e Tecnológico’ (CNPq) for research grants (process 302574/2010-7). AVLF thanks the ICMBio for the research permits (SISBIO nº 10802-5), CNPq for research grants (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).

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 (11/50225-3).

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Table 1. Abundance of fruit-feeding butterflies sampled in Atlantic forest fragments at Usina Serra Grande, Alagoas, northeastern Brazil.

Coimbra forest Total Taxon Fragments Total Interior Edge Coimbra forest Biblidinae 20 27 47 28 75 Biblis hyperia (Cramer, 1779) 0 0 0 1 1 astarte (Cramer, 1779) 0 1 1 11 12 Catonephele acontius (Linnaeus, 1771) 2 1 3 0 3 Ectima thecla thecla (Fabricius, 1796) 0 1 1 0 1 amphinome amphinome (Linnaeus, 1767) 0 1 1 0 1 Hamadryas arinome (Lucas, 1853) 0 0 0 1 1 Hamadryas feronia feronia (Linnaeus, 1758) 0 0 0 2 2 Hamadryas iphthime iphthime (Bates, 1864) 1 0 1 3 4 orsis (Drury, 1782) 17 23 40 9 49 Nica flavilla flavilla (Godart, [1824]) 0 0 0 1 1 Charaxinae 19 13 32 38 70 Archaeoprepona amphimachus amphimachus (Fabricius, 1775) 2 2 4 2 6 Archaeoprepona demophon thalpius (Hübner, [1814]) 12 4 16 8 24 Archaeoprepona demophoon antimache (Hübner, [1819]) 0 0 0 6 6 Fountainea ryphea phidile (Geyer, 1837) 2 1 3 7 10 Fountainea sp. 1 0 1 0 1 Hypna clytemnestra forbesi Godman & Salvin, [1884] 0 1 1 0 1 Memphis acidalia (Hübner, [1819]) 0 3 3 5 8 Memphis moruus (Fabricius, 1775) 0 0 0 4 4 Prepona amydon ferdinandi Fruhstorfer, 1875 1 1 2 0 2 Prepona laertes laertes (Hübner, [1811]) 0 0 0 1 1 Siderone galanthis galanthis (Cramer, 1775) 0 0 0 2 2 Zaretis strigosus (Gmelin, 1790) 1 1 2 3 5

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Nymphalinae 17 15 32 45 77 Colobura dirce dirce (Linnaeus, 1758) 17 15 32 39 71 Historis odius dious Lamas, 1995 0 0 0 6 6 Satyrinae 41 73 114 497 611 Brassolini 4 2 6 26 32 Caligo brasiliensis brasiliensis (C. Felder, 1862) 3 0 3 3 6 Caligo idomeneus (Linnaeus, 1758) 1 0 1 0 1 Caligo illioneus illioneus (Cramer, 1775) 0 0 0 5 5 Caligo teucer ssp. 0 0 0 2 2 automedon (Cramer, 1775) 0 1 1 8 9 Opsiphanes cassiae crameri C. Felder & R. Felder, 1862 0 0 0 1 1 Opsiphanes invirae remoliatus Fruhstorfer, 1907 0 1 1 6 7 Opsiphanes quiteria (Linnaeus, 1758) 0 0 0 1 1 Morphini 5 3 8 9 17 Morpho helenor anakreon Fruhstorfer, 1910 5 2 7 9 16 Morpho menelaus eberti Weber, 1963 0 1 1 0 1 Satyrini 32 68 100 462 562 Chloreuptychia arnaca (Fabricius, 1776) 0 1 1 0 1 Chloreuptychia chlorimene (Hübner, [1819]) 3 1 4 0 4 Chloreuptychia herseis (Godart, [1824]) 1 2 3 11 14 Cissia myncea (Cramer, 1780) 0 2 2 17 19 Cissia palladia (Butler, 1867) 1 1 2 21 23 Cissia terrestris (Butler, 1867) 4 15 19 44 63 Erichthodes antonina (C. Felder & R. Felder, 1867) 1 4 5 1 6 Euptychoides sp. 0 0 0 70 70 Hermeuptychia atalanta (Butler, 1867) 0 9 9 26 35 Hermeuptychia fallax (C. Felder & R. Felder, 1862) 0 0 0 1 1 Hermeuptychia gisella (Hayward, 1957) 0 4 4 11 15

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Hermeuptychia hermes (Fabricius, 1775) 0 1 1 3 4 Hermeuptychia sp. 0 1 1 0 1 Magneuyptychia libye (Linnaeus, 1767) 0 0 0 4 4 Pareuptychia sp.1 2 13 15 110 125 Pareuptychia sp.2 1 0 1 2 3 Paryphthimoides poltys (Prittwitz, 1865) 0 0 0 6 6 Paryphthimoides sp. 0 1 1 1 2 Paryphthimoides sylvina (C. Felder & R. Felder, 1867) 0 0 0 1 1 Pseudodebis sp. 5 0 5 0 5 Taygetis echo echo (Cramer, 1775) 1 0 1 0 1 Taygetis laches laches (Fabricius, 1793) 3 8 11 57 68 Taygetis rufomarginata Staudinger, 1888 0 1 1 1 2 Taygetis sosis Hopffer, 1874 8 2 10 12 22 Taygetis sp. 1 0 1 1 2 Taygetis virgilia (Cramer, 1776) 0 2 2 5 7 Yphthimoides manasses (C. Felder & R. Felder, 1867) 0 0 0 7 7 Yphthimoides renata (Stoll, 1780) 1 0 1 47 48 Zischkaia saundersii (Butler, 1867) 0 0 0 3 3 Total individuals 97 128 225 608 833

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Table 2. Results of the Generalized Linear Mixed Models for the effects of habitat type, fragment area and forest cover on number of individuals and observed and estimated fruit-feeding butterflies species richness sampled in Atlantic forest fragments at Usina

Serra Grande, Alagoas, northeastern Brazil. AREA = Fragment Area; FC = Forest

Cover.

Response variables Models Δ AICca AICcb Kc wid Observed richness

AREA 0.00 138.41 4 0.9

AREA + FC 4.35 142.76 5 0.1

FC 11.57 149.99 4 0

Estimated richness* AREA 0.00 155.61 4 0.85 AREA + FC 3.57 159.18 5 0.14

FC 8.52 164.14 4 0.01

Number of individuals

AREA + FC 0.00 222.05 5 0.68

AREA 1.56 223.61 4 0.31

FC 10.87 232.92 4 0

* Estimated species richness based on the average of two abundance-based richness estimadors (Jacknife 1 and Chao 1). aΔ AICc relative difference to the value of AICc of the best model. bAICc the model distance to the real model. cK (number of estimated parameters). dwi (AICc weight) which is the chance for the model to be selected.

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Table 3. Distribution of abundance by subfamily in the three habitats sampled in

Atlantic forest fragments at Usina Serra Grande, Alagoas, northeastern Brazil.

Subfamily Forest interior Forest edge Fragments

Biblidinae 20 27 28 Charaxinae 19 13 38 Nymphalinae 17 15 45 Satyrinae 41 73 497 Brassolini 4 2 26 Morphini 5 3 9 Satyrini 32 68 462 Total 97 128 497

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Figure legends

Figure 1. Map of the Serra Grande landscape, Alagoas, northeastern Brazil (A), showing the forest remnants in this sector of Atlantic forest (B). Forest fragments sampled are represented by dark shaded polygons. Blank spaces represent uniform matrix of sugar-cane monoculture.

Figure 2. Expected species richness according to the abundance-based richness estimators of frugivorous butterflies recorded in the Serra Grande landscape, Alagoas, northeastern Brazil. (A) Jacknife 1; (B) Chao 1.

Figure 3. Species rarefaction curve for the fruit-feeding butterfly assemblages in fragments (dashed line), forest edges (grey line) and forest interiors (black line) in the

Serra Grande landscape, Alagoas, northeastern Brazil. Thinner dashed lines are the confidence limits of the habitats.

Figure 4. Rank-abundance distribution (Whittaker plots) of fruit-feeding butterfly species in fragments (triangles), forest edges (open circles) and forest interiors (dark shaded circles) in the Serra Grande landscape, Alagoas, northeastern Brazil.

Figure 5. Ordination by NMDS method of fragments (triangles), forest edges (open circles) and forest interiors (dark-shaded circles) of the Serra Grande landscape,

Alagoas, northeastern Brazil.

Figure 6. Biplot of the first and second axes of the Canonical Correspondence of fragments based on fruit-feeding butterfly species composition in the Serra Grande landscape, Alagoas, northeastern Brazil. Numbers are fragments and black circles represent the species.

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Fig. 1

61

Fig. 2

62

60

50

40

30

20 Species richness Species

10

0 1 101 201 301 401 501 601 Cumulative abundance

Fig. 3

63

1000

100

10 Species abundance Species

1 1 11 21 31 41 51 61 Species richness

Fig. 4

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Fig. 5

65

Fig. 6

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CAPÍTULO 2

RECENT RECORDS OF MORPHO MENELAUS EBERTI (WEBER)

(LEPIDOPTERA: NYMPHALIDAE), AN ENDANGERED SPECIES OF

NORTHEAST BRAZIL

Artigo a ser submetido para o jornal Journal of the Lepidopterists’ Society

67

RECENT RECORDS OF MORPHO MENELAUS EBERTI (WEBER)

(LEPIDOPTERA: NYMPHALIDAE), AN ENDANGERED SPECIES OF

NORTHEAST BRAZIL

Additional key words: conservation, Northeastern Atlantic Forest, Morphini, Alagoas

The Atlantic Forest is a highly endangered ecosystem, concentrating a large portion of the threatened species of and plants in Brazil (Machado et al. 2008,

Martinelli & Moraes 2013). For butterflies in special, 47 out of the 55 threatened species are Atlantic Forest endemics (Machado et al. 2008, Freitas & Marini-Filho

2011), and although this could be argued as the result of a greater knowledge of this ecosystem, it is also a consequence of five centuries of occupation and conversion of almost 90% of the Atlantic Forest (Brown & Brown 1992, Ribeiro et al. 2009). The situation is more critical in the Pernambuco Center of Endemism (sensu Brown 1977), i.e. the coastal forest in the north of São Francisco River, where less than 12% of the

Atlantic forest still persist (Ribeiro et al. 2009). This portion of the Atlantic Forest is home of several threatened species of plants and animals, including three butterflies, namely Scada karschina delicata Talbot 1932, Morpho epistrophus nikolajewna Weber,

1951, and Morpho menelaus eberti Weber, 1963 (Machado et al. 2008, Freitas & Brown

2008a,b,c).

The bright blue M. menelaus eberti, once common in the humid forests of the

Pernambuco Center of Endemism (in the states of Pernambuco and Paraíba, with one individual known from Bahia) in altitudes from 0 to 600m (Blandin 2007, Kesselring pers. com.), now is rare and localized. Several sites where the species has been recorded in the past are now converted to anthropic habitats, and the species reach the status of

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“endangered” due to habitat loss (Machado et al. 2008, Freitas & Brown Jr 2008a,

Freitas & Marini-Filho 2011). As for example, the species is not anymore present in the municipality of São Lourenço da Mata, its type locality in Pernambuco (AVLF pers. obs.), as well as in several other places where it has been recorded in the past, that are now completely disturbed or deforested.

The species has not been recorded for almost two decades, until being spotted at the RPPN Frei Caneca, in Jaqueira, Pernambuco (8°43'37.92"S, 35°50'22.74"W), on

February 2004 (AVLF pers. obs.) and on February 2006 (Olaf H. H. Mielke pers. com.), a new locality for the species already mentioned in Freitas & Marini-Filho (2011).

Recently, the species has been recorded in Coimbra Forest (8°59'53"S, 35°50'29"W), a

3,500 ha forest fragment which is part of the “Usina Serra Grande”, in the municipalities of Ibateguara and São José da Lage, in the state of Alagoas. This forest fragment is the largest and best preserved forest remnant of Atlantic Forest in the

Pernambuco Center of Endemism (Santos et al. 2008). Two individuals were captured in this site: one male, captured with entomological net on 7 February 2012 in a trail in forest interior; one female (attracted by a trap baited with a mixture of banana and sugar cane juice), 13 December 2012, captured in the forest edge, both deposited at the Museu de Zoologia, Unicamp, Campinas, São Paulo, Brazil. In addition to the two above individuals, numerous additional males of M. meneaus eberti were observed flying in the edge and interior of Coimbra Forest, with some encounters in three other nearby smaller fragments (DHAM and BKCF pers. obs.).

This is a very important record not only for adding information about the area of occurrence of this subspecies, but also because this is the first record of M. menelaus eberti in the state of Alagoas. The discovery of new localities for threatened butterfly species is among the actions scheduled by the ‘National action plan for conservation of

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Brazilian Lepidoptera threatened of extinction’ (a recent document containing revised and updated information on Brazilian endangered species; Freitas & Marini-Filho

2011), and this was an specific action cited for M. menelaus eberti. This information is extremely valuable not only for the conservation of this species in particular, but also to plan the future of the remaining Atlantic Forest in the entire Pernambuco Center of

Endemism.

ACKNOWLEDGEMENTS

We thank to Luis Antônio Bezerra and José Clodoaldo Bakker for authorizing our fieldwork at the Usina Serra Grande. We are also grateful to ‘Coordenação de

Aperfeiçoamento de Pessoal de Nível Superior’ for financial support (process

02488/09-4) and for ‘Conservação Internacional do Brasil’ (CI Brasil), ‘Centro de

Estudos Ambientais do Nordeste’ (CEPAN) and ‘Usina Serra Grande’ for infrastructure and logistic support during field work. DHAM and BKCF acknowledges the 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). IRL thanks the ‘Conselho Nacional de Desenvolvimento

Científico e Tecnológico’ (CNPq) for research grants (process 302574/2010-7). AVLF thanks the ICMBio for the research permits (SISBIO nº 10802-5), 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). 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

(11/50225-3).

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LITERATURE CITED

Blandin, P. 2007. The systematics of the genus Morpho, Fabricius, 1807 (Lepidoptera

Nymphalidae, Morphinae). Canterbury, Hillside Books. 277 pp.

Brown Jr, K. S. 1977. Centros de evolução, refugios quaternarios e conservação de patrimónios genéticos na região neotropical: padrões de diferenciação em Ithomiinae

(Lepidoptera: Nymphalidae). Acta Amazonica 7:75-137.

Brown Jr, K. S. & G. G. Brown. 1992. Habitat alteration and species loss in Brazilian forests. pp. 119–142. In Whitmore T. C. & J. Sayer (eds.), Tropical deforestation and species extinction. Chapman & Hall, London.

Freitas, A. V. L. & O. J. Marini-Filho. 2011. Plano de Ação Nacional para a

Conservação dos Lepidópteros Ameaçados de Extinção. Instituto Chico Mendes de

Conservação da Biodiversidade (ICMBio), Brasília. 124 pp.

Freitas, A. V. L. & K. S. Brown Jr. 2008a. Grasseia menelaus eberti (Fischer, 1962). pp. 413. In Machado, A. B. M., G. M. M. Drummond & A. P. Paglia (eds.), Livro vermelho da fauna brasileira ameaçada de extinção. Ministério do Meio Ambiente,

Brasília, Fundação Biodiversitas, Belo Horizonte.

Freitas, A. V. L. & K. S. Brown Jr. 2008b. Pessonia epistrophus nikolajewna (Weber,

1951). pp. 424. In Machado, A. B. M., G. M. M. Drummond & A. P. Paglia (eds.),

Livro vermelho da fauna brasileira ameaçada de extinção. Ministério do Meio

Ambiente, Brasília, Fundação Biodiversitas, Belo Horizonte.

Freitas, A. V. L. & K. S. Brown Jr. 2008c. Scada karschina delicata Talbot, 1932. pp.

427. In Machado, A. B. M., G. M. M. Drummond & A. P. Paglia (eds.), Livro vermelho da fauna brasileira ameaçada de extinção. Ministério do Meio Ambiente, Brasília,

Fundação Biodiversitas, Belo Horizonte.

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Machado, A. B. M., G. M. M. Drummond & A. P. Paglia. 2008. Livro vermelho da fauna brasileira ameaçada de extinção. Ministério do Meio Ambiente, Brasília,

Fundação Biodiversitas, Belo Horizonte. 1420 pp.

Martinelli, G. & M. A. Moraes. 2013. Livro Vermelho da Flora do Brasil. Andrea

Jakobsson, Rio de Janeiro. 1100 pp.

Paluch, M., O. H. H. Mielke, C. E. B. Nobre, M. M. Casagrande, D. H. A. Melo & A.

V. L. Freitas. 2011. Butterflies (Lepidoptera: Papilionoidea and Hesperioidea) of the

Parque Ecológico João Vasconcelos Sobrinho, Caruaru, Pernambuco, Brazil. Biota

Neotropica 11:229-238.

Ribeiro M. C., J. P. Metzger, A. C. Martensen, F. Ponzoni & M. M. Hirota. 2009.

Brazilian Atlantic forest: how much is left and how is the remaining forest distributed?

Implications for conservation. Biological Conservation 142:1141–1153.

Santos, B. A., C. A. Peres, M. A. Oliveira, A. Grillo, C. P. Alves-Costa, & M. Tabarelli.

2008. Drastic erosion in functional attributes of tree assemblages in Atlantic Forest fragments of Northeastern Brazil. Biological Conservation 141:249–260.

DOUGLAS HENRIQUE ALVES MELO, BRUNO KAROL CORDEIRO

FILGUEIRAS, Programa de Pós-Graduação em Biologia Animal, Universidade

Federal de Pernambuco, CEP 50670-901 Recife, Pernambuco, Brazil; e-mail: [email protected], INARA ROBERTA LEAL, Departamento de Botânica,

Universidade Federal de Pernambuco, CEP 50670-901, Recife, Pernambuco, Brazil, and ANDRÉ VICTOR LUCCI FREITAS, Departamento de Biologia Animal and

Museu de Zoologia, Instituto de Biologia, Universidade Estadual de Campinas, C.P.

6109, CEP 13083-862, Campinas, São Paulo, Brazil; e-mail: [email protected]

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6. CONSIDERAÇÕES FINAIS

Os dados deste estudo revelam que tipo de hábitat não afeta a riqueza de borboletas frugívoras, a menos que haja uma grande perda e isolamento de habitats. Desta forma, borda de floresta, interior de floresta e fragmentos não apresentam diferenças significativas no número de espécies presente em uma paisagem. No entanto, mesmo que os hábitats apresentem riquezas similares, isso não significa ausência de efeito da perda e fragmentação florestal, pois diferenças na composição de espécies são observadas entre borda de floresta, interior de floresta e fragmentos. Fatores como área e grau de isolamento dos fragmentos também influenciam a composição de espécies de borboletas frugívoras, assim como a distância entre as áreas amostradas. Uma gama de trabalhos avaliando os efeitos de perturbações antrópicas sobre a comunidade de borboletas frugívoras tem chegado a resultados similares aos deste. Esses trabalhos mostram que ambientes com diferentes níveis de perturbação apresentam semelhanças na riqueza de espécies e na diversidade, mas a composição é alterada consideravelmente. As modificações na composição de espécies registrada neste estudo podem ser sintetizadas como uma substituição de espécies sensíveis por outras capazes de sobreviver em áreas abertas, ensolaradas e ambientes degradados Isto foi visto claramente na tribo Satyrini, onde a maioria das espécies dominantes em fragmentos e borda de floresta não estiveram presentes ou tiveram suas populações reduzidas substancialmente no interior de floresta. Essas modificações na composição de espécies de borboletas são devidas a alterações na composição da vegetação, onde ocorre uma proliferação de plantas pioneiras (e.g. gramíneas, principal planta hospedeira para a maioria dos satiríneos amantes do sol) em detrimento de grupos mais especializados, como as plantas emergentes, espécies tolerantes à sombra, e grupos polinizados e dispersos por vertebrados. Assim, a composição de espécie é a melhor variável para avaliar a resposta da estrutura da comunidade de borboletas frugívoras à perturbação antrópica na Floresta Atlântica. Mudanças na estrutura da assembleia de árvores seja ela natural ou antrópica podem ter sérias consequências na estrutura da comunidade de borboletas frugívoras. Em uma área tão ameaçada como a Floresta Atlântica Nordestina, tornam-se ainda mais urgentes estratégias que visem o monitoramento ambiental para a preservação dos sistemas naturais da Usina Serra Grande. A presença de elementos indicadores como a

73 ameaçada Morpho menelaus eberti em Coimbra reforça ainda mais esta ideia, pois, mesmo sendo altamente fragmentada, esta paisagem torna-se uma das poucas onde é possível encontrar essa espécie voando na Floresta Atlântica Nordestina. Além disso, é uma das regiões com os maiores fragmentos no Centro de Endemismo Pernambuco restante nos dias de hoje. Diante destes resultados, percebe-se a importância do uso de borboletas frugívoras como uma ótima ferramenta de estudo para diagnosticar a qualidade e a integridade das paisagens naturais. Entre as respostas deste grupo observadas aqui, destacam-se: (1) a sensibilidade das borboletas frugívoras a níveis de perturbação, tais como perda e fragmentação de hábitat, (2) a composição de espécies como a variável que melhor explica as variações da comunidade de borboletas frugívoras à perturbação antrópica na Floresta Atlântica. Tais características, bem como a presença de espécie ameaçada em Coimbra, ressalta (3) a importância de grandes remanescentes como refúgio para espécies sensíveis em setores altamente fragmentados.

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7. ANEXOS

75

INSECT CONSERVATION AND DIVERSITY

AUTHOR GUIDELINES

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Editorial policy Papers submitted to Insect Conservation & Diversity should be original research papers on aspects pertaining mainly to aspects of insect conservation and diversity. Papers concerning other arthropods will also be considered. Reviews, Mini-Reviews, short communications detailing innovative techniques or methodological approaches, and thought provoking forum-type articles on any aspect of insect conservation ranging from policy matters to conjecture based on a solid science base are welcomed.

Papers should be in clear concise English and written in the passive voice. They must not have been published or accepted for publication by any other journal, or be under consideration for publication in another journal. Submission of a manuscript to Insect Conservation and Diversity implies that all persons listed as authors qualify for authorship, and that all who qualify have been listed. Papers will be subjected to peer- review by at least two independent referees, to ensure that articles are both rigorous and readable. Ethical considerations will be taken into account in considering the acceptability of papers, and the editors' decision on this, as on other aspects, will be final.

Insect Conservation and Diversity is a member of and subscribes to the principles of the Committee on Publication Ethics.

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It is the responsibility of the corresponding author to review this policy with all authors and to collectively list in the manuscript (under the Acknowledgment section) and in the online submission system ALL pertinent commercial and other relationships.

Ethical Guidelines The journal expects authors to abide by the guidelines of those statutory bodies, or, discipline that are specific to the country of origin, or, execution of the research.

Pre-submission English Language Editing Authors for whom English is a second language are asked to consult a native English speaker before submission of their manuscript. Alternatively, authors may choose to

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All services are paid for and arranged by the author, and use of one of these services does not guarantee acceptance or preference for publication.

Manuscript Submission All material must be submitted electronically via the Insect Conservation and Diversity Manuscript Central site at: http://mc.manuscriptcentral.com/icdiv

Manuscripts which do not conform to ALL the standards outlined here will be returned to the author(s) with a request that they are edited to meet these standards.

All authors listed in the manuscript must be listed on the electronic system, with a working email address provided for each, as part of the submission process.

For submission assistance or questions please contact the Editorial Office or for technical support contact ScholarOne directly ([email protected]).

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Manuscript that do not adhere to the instructions will not be accepted for further processing. Authors may examine recent issues for details of acceptable style and format.

All manuscripts must be submitted as A4 Microsoft Word documents with wide margins. Lines must be double spaced, and must be numbered consecutively throughout the entire manuscript. Pages should also be numbered. Section and sub-section headings should not be numbered.

All manuscript submissions must include a Title, Running title, Abstract, Keywords and Author details. Only Forum, Policy, Comment/Debate and Short Communications may exclude Keywords and Abstract.

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All original articles should include the above, followed by an Introduction, Materials and Methods, Results, Discussion, Acknowledgements, References, Tables and Figures. Each table should be presented on a separate sheet. Figure legends should also be grouped together on a separate sheet.

Original articles should not exceed 6000 words of text (12 printed pages) without references, though longer articles with merit may be accepted – please contact the Editor-in-Chief before making such a submission.

Short communications should be limited to 1500 words of text without references and have a combined Results and Discussion section. They should also include no more than one figure and one table.

Scientific names of genus, species and subspecies should be italicised. The full name must be used when first mentioned in the manuscript, with the abbreviation used thereafter. The taxonomic affiliation and authority should also be given at the first mention of a species.

Abbreviations must be explained in the text. Authors are asked to use the International System of Units (SI).

Please contact the Editor-in-Chief or Editorial Office with any queries.

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78 explained in the text. Authors must however, clearly state what statistical approaches were used in their analyses (supported where relevant by adequate references) in the Materials and Methods section. Where statistics are presented in the text, we ask that the authors follow the presentation guidelines provided below.

After an analysis of variance, further simultaneous testing of treatment means should not be done, except for specific comparisons planned prior to the experiment. Simple measures of variability (e.g. SE, LSD, CI) should always accompany means. The same data should not be given in both tables and figures.

We would also request that authors ensure a match between the tests used and figures provided in the text. For example, where non-parametric tests are used (e.g. Kruskal- Wallis ANOVA), it is inappropriate to present the mean and standard error of the analysed data. Instead the median and an indicator of variation about the median (e.g. inter-quartiles) should be provided.

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Only articles which have been published or accepted for publication may be included in the reference list. In the text, unpublished studies should be referred to as such, or as personal communication with the author’s surname and initials. It is the author’s responsibility to obtain permission from their colleagues to include their work as personal communication.

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As part of the sentence: Fox (2013), or Stork & Hammond (2013), or Didham et al., (2013).

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If the reference would require the same author abbreviation but different years: Leather et al. (2008, 2011) or (Leather et al., 2008, 2011). a. Journal articles Fuller, R.J., Oliver, T.H. & Leather, S.R. (2008) Forest management effects on carabid beetle communities in coniferous and broadleaved forests: implications for conservation. Insect Conservation and Diversity, 1, 242-252. b. From books, or other non-serial publications Samways, M.J. (2005) Insect Diversity Conservation. Cambridge University Press, Cambridge, UK. c. From reference book contributions

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Hunter, M.D. (1994) The search for pattern in pest outbreaks. Individuals, Populations and Patterns in Ecology (ed. by Foottit, R.G. & Adler, P.H.), pp. 443-448. Intercept, Andover, UK. d. Work which has been accepted for publications Leather, S.R. (In press) Editorial. Insect Conservation and Diversity. e. From websites Insect Conservation and Diversity (2014) Insect Conservation and Diversity Author Guidelines. 2nd April 2014.

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JOURNAL OF THE LEPIDOPTERISTS’ SOCIETY

INSTRUCTIONS TO AUTHORS

The Journal of the Lepidopterists’ Society is a quarterly publication by the Lepidopterists’ Society. Contributions to the Journal may address any aspect of Lepidoptera study, including systematics, natural history, behavior, ecology, distribution, biogeography, and evolution. Categories are Articles, Profiles, General Notes, Technical Comments, Obituaries, Feature Photographs, and Cover Illustrations. Obituaries must be authorized by the president of the Society

Send Journal submissions to the editor at: Summerville, 2507 University Ave., 131 Olin Hall, Drake University, Des Moines, Iowa 50311-4505, USA (or electronically to: [email protected]. Contributors should recommend one or two reviewers upon submission of their manuscript. Short manuscripts concerning new state records, book reviews, new book releases, current events and notices should be sent to the News, James Adams, School of Sciences and Math, 650 College Dr., Dalton State College, Dalton, GA 30720-3778, e-mail: [email protected]. Specific instructions for electronic submissions appear below.

GENERAL MANUSCRIPT GUIDELINES

Authors should submit manuscripts electronically, via email or by providing a diskette with text laid out in a standard PC or Macintosh-based word processing format. Manuscripts should be entirely double-spaced, using a legible typeface (preferably a serif font like Times New Roman) to allow for easy identification of letters and numbers (e.g., number 1, lower case L, and upper case I). Do not break words with hyphenation at the right margin of the page. Do not use right justification or center. Number pages in the header area in the upper right corner.

If your word processing files include symbols such as μ @ ± â, or special table formats, please submit one hardcopy via regular mail. Special symbols (e.g. male & female symbols) should be avoided because they are likely to be altered when files are read on different machines. When formatting your paper to include symbols for male and female, please include parenthetical identifiers (M#) or (F#) so that we properly place appropriate gender symbols within the text. Upon receipt, the editor will check your files for problems of incompatibility between computer applications or systems. Illustrations can be submitted electronically on a diskette or via email. Please follow instructions below for the size, resolution and file type acceptable for images in your final manuscript.

ARTICLES, PROFILES, AND TECHNICAL COMMENTS

Organize articles, profiles, and technical comments as follows: I. Title followed by author(s)’ names and affiliations, II. Abstract and key words, III. Text divided into appropriate sections as outlined below, IV. Acknowledgments, V. Literature Cited, VI. Tables numbered consecutively with a caption explaining table content, VII. Captions for figures numbered consecutively, and copies of figures numbered to correspond with captions.

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I. Title & Authors. The title page should include the manuscript title, author’s name, affiliation, and full address, including email address. Unless indicated otherwise, it is assumed that the senior author of multiple authored contributions will revise both the manuscript and page proofs. Make title explicit, descriptive, and as short as possible. It is unnecessary to include the word Lepidoptera in the title. List family names and other higher level taxonomic categories in parenthesis.

II. Abstract and key words. The indented word "ABSTRACT." (in capitals, boldface, and followed by a period) precedes a meaningful digest of the manuscript. An abstract in Spanish can follow the English abstract if desired by the author. Up to five key words or terms not in the title should accompany articles (it is unnecessary to include the word Lepidoptera), entitled Additional key words.

III. Text. Write with precision, clarity, and economy. Use the active voice and the first person whenever appropriate. Mark major sections of the manuscript with centered headings using all capitals, but do not use a heading for the introduction. Headings for taxonomic, natural history, and experimental contributions will differ and should follow standard scientific format. Use articles published in the Journal as models. Subheadings within a section are followed by a period and set in boldface. The example below shows a heading and subheading:

RESULTS

Field studies. From 1959 through 1988, 18,255 Biston betularia…

In taxonomic manuscripts, taxon names can be used both as headings and subheadings. They should be centered, italicized, and followed by the author’s name in roman type. Year of publication is optional; if provided, it should be separated from author’s name by a comma. Indicate new taxa and change in status of a taxon in English, spelled fully, and in boldface (e.g., new species, new combination, new synonym). New taxa with author and status appear entirely in boldface. When needed, authors’ initials may be added to elucidate their identity. In the examples below, the genus name appears as a section heading, and species names are subheadings; new status is assigned to one species, and one is being described as new:

MYLON GODMAN & SALVIN, 1894

Mylon orsa Evans, 1953

Mylon exstincta Mabille & Boullet, 1917, new status

Mylon simplex Austin, new species

Descriptions should be clear and concise, employing standard terminology (e.g., head scoli, not head horns) and traditional plural derivations (e.g., larva, larvae; tarsus, tarsi; valva, valvae), and include measurements (mean, range) and number of examined specimens when applicable. Abbreviations such as FW (forewing) and HW (hindwing) can be used to abridge text. Wing venation should be reported using the strandard abbreviation for each wing vein with its number subscripted. For example, a reference

86 to the first cubital vein would read: Cu1. Depending on the circumstances, terminology for descriptions can be used either in the singular or plural forms, but text should be internally consistent.

When appropriate, manuscripts must name a public repository where voucher specimens documenting the identity of organisms can be found. Kinds of reports that require vouchering include descriptions of new taxa, life histories, host associations, immature morphology, and some experimental studies.

In both descriptive and experimental studies, make reference to figures (abbreviated Fig. or Figs.) and tables (Table, not abbreviated) whenever appropriate, and these should be numbered and listed sequentially in the text (i.e., Fig. 1 should be listed in the text before Fig. 2).

Examples of how to list references in text are: Remington (1963), (Fruhstorfer 1913), Vansconcellos-Neto (1986, 1991), DeVries (1991a, b), Vane-Wright and Ackery (1989), (Clarke & Sheppard 1960), Rothschild et al. (1979). Unpublished data should be cited as (unpublished), or (HFG unpublished) to single out one of multiple authors when appropriate. Personal communications should be cited as (J. W. Brown pers. com.). Manuscripts in press should be cited as such both in the text and Literature Cited section, e.g., Epstein (in press). Only those manuscripts accepted for publication should be cited as “in press;” do not cite submitted papers or papers in review as “in press.”

Use the following general guidelines for notations, measurements, symbols, and other items. The first mention of a plant or animal in the text should include the full scientific name with author and family. For measurements, use metric units and abbreviate them correctly (e.g., 15 km, 20 μg). For time, use a 24 h clock (0930 h, not 9:30 AM). For date, use “day month year” format. Spell months fully; use full notation for year. As a recommendation of manuscript style, numerals can be used when indicating day of the month, measurements, statistics, anatomical counts (e.g., 4 setae), standard entomological terminology (e.g., forewing vein M3), and numbers of specimens examined (e.g., 2 specimens), but should be otherwise expressed in their word equivalent between one (1) and nine (9). For the final publication it is desirable to use male and female symbols to condense accounts of examined material; however, gender symbols in your submitted manuscript should be formatted as follows: Male (M#) or Female (F#) (gender letter in Caps/upper case followed by pound sign). The gender symbol will be inserted into the final manuscript during layout and visible in your final proof. Use italics for scientific names only (genus and below). Do not use italics for emphasis (e.g., this species occurs only at elevations above 800 m). Use roman type (not italics) for Latin abbreviations and expressions (i.e., e.g., ca., et. al., sensu strictu, in situ, ad libitum, a priori).

IV. Acknowledgments Section. Under the centered heading ACKNOWLEDGMENTS, in one single paragraph list persons that contributed to the study using either their full name or initials, but remaining consistent throughout the text. Fully spell out names of institutions. List permit granting institutions when applicable. Acknowledge financial support at the end of the paragraph, followed by grant number when applicable.

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V. Literature Cited pages. List references alphabetically under the centered heading LITERATURE CITED. Write authors’ names in plain text (do not use Caps Lock), and use roman type (not italics) for both reference and journal titles, except for scientific names and special notations. Abbreviated journal titles should appear as listed in the international Serials Catalogue: Part I: Catalogue (International Council of Scientific Unions Abstracting Board, 1978), except when they consist of a single word (e.g., Biotropica). Examples are listed below.

Books: Sheppard, P. M. 1959. Natural selection and heredity. 2nd ed. Hutchinson, London. 209 pp.

Book chapters: Janzen, D. H. 1988a. Guanacaste National Park: Tropical ecological and biocultural restoration, pp. 143-192. In Cairns, J. J. (ed.), Rehabilitating damaged ecosystems. Vol. II. CRC Press, Boca Raton, Florida.

Journal articles: Pollard, E. 1977. A method for assessing changes in the abundance of butterflies. Biol. Conserv. 12:115-124.

Multiple authors: Nicolay, S. S. & G. B. Small Jr. 1969. A new subspecies of Pyrrhopyge creon (Hesperiidae) from Panama. J. Lepid. Soc. 23:127-130. Fairchild, W. L., D. C. Eidt, & C. A. A. Weaver. 1987. Effects of fenitrothion insecticide on inhabitants of leaves of the pitcher plant, Sarracenia purpurea L. Canad. Entomol. 119:647-652.

Multiple citations of the same author: Bell, E. L. 1931. Studies in the Pyrrhopyginae, with descriptions of several new species (Lepidoptera, Rhopalocera, Hesperiidae). J. New York Entomol. Soc. 39:417-491. ———. 1933. Studies in the Pyrrhopyginae, with descriptions of new species (Lepidoptera, Rhopalocera, Hesperiidae). J. New York Entomol. Soc. 41:265-295, 481-529.

Manuscripts in press: Janzen, D. H. In press. Ecology of dry forest wildland insects in the Area de Conservación Guanacaste, northwestern Costa Rica. In Frankie, G. W., A. Mata & S. B. Vinson (eds.), Biodiversity conservation in Costa Rica: learning the lessons in seasonal dry forest. Univ. Calif. Press, Berkeley.

Proceedings of meetings: Philbrick, R. N. (ed.) 1967. Proceedings of the Symposium on the biology of the California islands. Santa Barbara Botanic Garden, Santa Barbara, California.

Theses and dissertations: Penz, C. M. 1996. The higher-level phylogeny of the passion-vine butterflies (Nymphalidae, Heliconiinae). Ph.D. Dissertation. University of Texas, Austin, Texas.

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Computer programs: Maddison, W. P. & D. R. Maddison. 2000. MacClade: version 4.0 PPC. Sinauer, Sunderland.

Internet resources: Author (2002) Title of website, database or other resources, Publisher name and location (if indicated), number of pages (if known). Available from: http://xxx.xxx.xxx/ (Date of access).

Anonymous institutional or organizational publications: International Code of Zoological Nomenclature. 1985. 3 rd ed. International Trust for Zoological Nomenclature (BM[NH]). University of California Press, Berkeley, California.

VI. Tables. Number tables consecutively in Arabic numerals. Label them in plain text, i.e. Do not use All Caps (e.g., Table 1.). Each table should have a concise and informative heading. Type each table on a separate sheet and place after the Literature Cited section, with the approximate desired position indicated in the text. Avoid vertical lines and vertical writing.

VII. Figures and Legends. Explanation of Figures. Type figure legends double-spaced, on a separate sheet following the Lit Cited or Tables section. Type EXPLANATION OF FIGURES at top of page as a header centered on the sheet. Use a separate paragraph for each figure legend, numbered consecutively. When multiple images are included in a single full page figure, please number the images consecutively with Arabic numerals (Fig. 1, 2, 3), or alternatively use an Arabic numeral followed by a lower case letter (e.g. Fig. 1a, 1b, 1c). Use the term "Figure" for all images in your paper; do not use the term “plate.” Figure Guidelines. Color illustrations are encouraged; contact editor for submission requirements and cost. We are able to publish color at only a minimal charge (an extra $10 per page). Illustrate only half of symmetrical objects such as adults with wings spread, unless whole illustration is crucial. Bear in mind that your illustrations will be reduced to fit a Journal page (plan to make lettering sufficiently large), and that the figure legend will appear at the bottom of the page below your figure (Journal page: 16.5 cm width, 22.5 cm height). Submit figures electronically. Use tiff format (not jpg) and submit image with all layers flattened at a resolution of 350 ppi (137 pixels per cm). (A one-column illustration should be at least1000 pixels wide, a 2-column illustration should be at least 2200 pixels wide). Color files are to be saved in CMYK mode; B&W files are saved as Grayscale mode.

GENERAL NOTES Organize notes without page breaks as follows: title (all capitals), additional key words, text, literature cited, author name and full address, including email address when available. Do not divide text into sections, but use boldface, indented headings when necessary (for an example, see Cordero 1999, J. Lepid. Soc. 53(4):169-170). Keep figures and tables to a minimum, but use when necessary. Acknowledgments are given in the last paragraph of the text. Title, Additional key words, and Literature Cited follow the same format as articles. General guidelines for notations, measurements, symbols, and other items are also the same as for articles.

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PAGE CHARGES For authors affiliated with institutions, page charges are $50 per Journal page. For authors without institutional support, page charges are $25 per Journal page. For authors who are not members of the Society, page charges are $100 per Journal page. Authors will be charged a full page price for any partially filled pages. Authors unable to pay page charges for any reason should apply to the editor at the time of submission for a reduced rate or free publication. Authors of Tributes and Obituaries are exempt from page charges.

PAGE PROOFS The edited manuscript and galley proofs will be mailed to the author for correction of printer’s errors. Changes to text after final submission will be charged to authors at the rate of $3.00 per line. A purchase order for reprints will accompany proofs.

CORRESPONDENCE Address all matters relating to the Journal to the editor.

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