Efeito da fragmentação de habitats sobre borboletas frugívoras

Transcription

UNIVERSIDADE FEDERAL DE PERNAMBUCO
Douglas Henrique Alves de Melo
EFEITO DA FRAGMENTAÇÃO DE HABITATS SOBRE BORBOLETAS
FRUGÍVORAS (LEPIDOPTERA: NYMPHALIDAE) NA FLORESTA
ATLÂNTICA NORDESTINA
RECIFE
2014
UNIVERSIDADE FEDERAL DE PERNAMBUCO
Dissertação apresentada ao Programa de Pósgraduação 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
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.
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
Dissertação apresentada ao Programa de Pósgraduação em Biologia Animal, Centro de
Ciências Biológicas da Universidade Federal
de Pernambuco, como requisito parcial da
obtenção do título de Mestre em Biologia
Animal.
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 Hermeuptychia. 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), Biblidinae (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 butterfly 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 butterflies. 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 (UEHARAPRADO 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).
14
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.
15
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
16
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 & MARINIFILHO, 2011). Por fim, a sua preservação pode garantir a de muitas espécies associadas
que habitam os mesmos ambientes ou tenham necessidades similares (NEW, 1997).
17
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; UEHARAPRADO et al., 2007; RIBEIRO et al., 2008; DOVER & SETTELE, 2009; UEHARAPRADO 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.
18
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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
1
Programa de Pós-Graduação em Biologia Animal, Universidade Federal de
Pernambuco, Recife, PE, CEP 50670-901, Brazil
2
Departamento de Ecologia, Zoologia e Genética, Universidade Federal de Pelotas,
Pelotas, RS, C.P. 354, CEP 96160-000, Brazil
3
Departamento de Zoologia, Universidade Federal de Pernambuco, Recife, PE, CEP
50670-901, Brazil
4
Departamento de Biologia Animal, Universidade Estadual de Campinas, Campinas,
SP, C.P. 6109, CEP 13083-862, Brazil
5
Departamento de Botânica, Universidade Federal de Pernambuco, Recife, PE, CEP
50670-901, Brazil
6
Corresponding author: E-mail: [email protected] (I.R. Leal).
28
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 fruitfeeding 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.
29
Key-words: area effects, bioindicators, conservation, forest fragmentation, frugivorous
butterflies, Nymphalidae, patch isolation, Pernambuco Center of Endemism, species
composition, species richness.
30
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 fruitfeeding 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 fruitfeeding 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).
37
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 wellpreserved 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 Satyrini 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 fruitfeeding 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.
44
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.
Taxon
Biblidinae
Biblis hyperia (Cramer, 1779)
Callicore astarte (Cramer, 1779)
Catonephele acontius (Linnaeus, 1771)
Ectima thecla thecla (Fabricius, 1796)
Hamadryas amphinome amphinome (Linnaeus, 1767)
Hamadryas arinome (Lucas, 1853)
Hamadryas feronia feronia (Linnaeus, 1758)
Hamadryas iphthime iphthime (Bates, 1864)
Myscelia orsis (Drury, 1782)
Nica flavilla flavilla (Godart, [1824])
Charaxinae
Archaeoprepona amphimachus amphimachus (Fabricius, 1775)
Archaeoprepona demophon thalpius (Hübner, [1814])
Archaeoprepona demophoon antimache (Hübner, [1819])
Fountainea ryphea phidile (Geyer, 1837)
Fountainea sp.
Hypna clytemnestra forbesi Godman & Salvin, [1884]
Memphis acidalia (Hübner, [1819])
Memphis moruus (Fabricius, 1775)
Prepona amydon ferdinandi Fruhstorfer, 1875
Prepona laertes laertes (Hübner, [1811])
Siderone galanthis galanthis (Cramer, 1775)
Zaretis strigosus (Gmelin, 1790)
Coimbra forest
Total
Fragments Total
Interior Edge Coimbra forest
20
27
47
28
75
0
0
0
1
1
0
1
1
11
12
2
1
3
0
3
0
1
1
0
1
0
1
1
0
1
0
0
0
1
1
0
0
0
2
2
1
0
1
3
4
17
23
40
9
49
0
0
0
1
1
19
13
32
38
70
2
2
4
2
6
12
4
16
8
24
0
0
0
6
6
2
1
3
7
10
1
0
1
0
1
0
1
1
0
1
0
3
3
5
8
0
0
0
4
4
1
1
2
0
2
0
0
0
1
1
0
0
0
2
2
1
1
2
3
5
55
Nymphalinae
Colobura dirce dirce (Linnaeus, 1758)
Historis odius dious Lamas, 1995
Satyrinae
Brassolini
Caligo brasiliensis brasiliensis (C. Felder, 1862)
Caligo idomeneus (Linnaeus, 1758)
Caligo illioneus illioneus (Cramer, 1775)
Caligo teucer ssp.
Eryphanis automedon (Cramer, 1775)
Opsiphanes cassiae crameri C. Felder & R. Felder, 1862
Opsiphanes invirae remoliatus Fruhstorfer, 1907
Opsiphanes quiteria (Linnaeus, 1758)
Morphini
Morpho helenor anakreon Fruhstorfer, 1910
Morpho menelaus eberti Weber, 1963
Satyrini
Chloreuptychia arnaca (Fabricius, 1776)
Chloreuptychia chlorimene (Hübner, [1819])
Chloreuptychia herseis (Godart, [1824])
Cissia myncea (Cramer, 1780)
Cissia palladia (Butler, 1867)
Cissia terrestris (Butler, 1867)
Erichthodes antonina (C. Felder & R. Felder, 1867)
Euptychoides sp.
Hermeuptychia atalanta (Butler, 1867)
Hermeuptychia fallax (C. Felder & R. Felder, 1862)
Hermeuptychia gisella (Hayward, 1957)
17
17
0
41
4
3
1
0
0
0
0
0
0
5
5
0
32
0
3
1
0
1
4
1
0
0
0
0
15
15
0
73
2
0
0
0
0
1
0
1
0
3
2
1
68
1
1
2
2
1
15
4
0
9
0
4
32
32
0
114
6
3
1
0
0
1
0
1
0
8
7
1
100
1
4
3
2
2
19
5
0
9
0
4
45
39
6
497
26
3
0
5
2
8
1
6
1
9
9
0
462
0
0
11
17
21
44
1
70
26
1
11
77
71
6
611
32
6
1
5
2
9
1
7
1
17
16
1
562
1
4
14
19
23
63
6
70
35
1
15
56
Hermeuptychia hermes (Fabricius, 1775)
Hermeuptychia sp.
Magneuyptychia libye (Linnaeus, 1767)
Pareuptychia sp.1
Pareuptychia sp.2
Paryphthimoides poltys (Prittwitz, 1865)
Paryphthimoides sp.
Paryphthimoides sylvina (C. Felder & R. Felder, 1867)
Pseudodebis sp.
Taygetis echo echo (Cramer, 1775)
Taygetis laches laches (Fabricius, 1793)
Taygetis rufomarginata Staudinger, 1888
Taygetis sosis Hopffer, 1874
Taygetis sp.
Taygetis virgilia (Cramer, 1776)
Yphthimoides manasses (C. Felder & R. Felder, 1867)
Yphthimoides renata (Stoll, 1780)
Zischkaia saundersii (Butler, 1867)
Total individuals
0
0
0
2
1
0
0
0
5
1
3
0
8
1
0
0
1
0
97
1
1
0
13
0
0
1
0
0
0
8
1
2
0
2
0
0
0
128
1
1
0
15
1
0
1
0
5
1
11
1
10
1
2
0
1
0
225
3
0
4
110
2
6
1
1
0
0
57
1
12
1
5
7
47
3
608
4
1
4
125
3
6
2
1
5
1
68
2
22
2
7
7
48
3
833
57
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
AREA
AREA + FC
FC
0.00
4.35
11.57
138.41
142.76
149.99
4
5
4
0.9
0.1
0
AREA
AREA + FC
FC
0.00
3.57
8.52
155.61
159.18
164.14
4
5
4
0.85
0.14
0.01
Observed richness
Estimated richness*
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).
a
Δ AICc relative difference to the value of AICc of the best model.
b
c
AICc the model distance to the real model.
K (number of estimated parameters).
d
wi (AICc weight) which is the chance for the model to be selected.
58
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
97
128
497
Total
59
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.
60
Fig. 1
61
Fig. 2
62
60
Species richness
50
40
30
20
10
0
1
101
201
301
401
Cumulative abundance
501
601
Fig. 3
63
Species abundance
1000
100
10
1
1
11
21
31
41
51
61
Species richness
Fig. 4
64
Fig. 5
65
Fig. 6
66
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 animals 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
68
“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
69
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).
70
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.
71
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]
72
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.
74
7. ANEXOS
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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
79
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.
<http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)17524598/homepage/ForAuthors.html> 2nd April 2014.
Tables
Tables must be self-explanatory and accompanied by legends. Each Table must be
presented on a separate sheet with their pertaining Table legend. Tables should be
created using the table function in MS Word.
Please number Tables consecutively in the order in which they occur within the
manuscript text.
Figures and Preparation of Artwork
Figures should be self-explanatory and accompanied by legends. Figure legends should
be presented grouped, as a list included in the main text of the manuscript following the
References and Tables. Figures should then be uploaded on separate sheets in the
document, or separately during the submission process.
Please number Figures consecutively in the order in which they occur within the
manuscript text.
Prepare your figures according to the publisher's Electronic Artwork Guidelines.
All figures must be provided as high quality images, in TIFF or EPS format.
Although low quality images (GIF/JPG) are adequate for review purposes, print
publication requires high quality images (TIFF/EPS) to prevent the final product being
blurred or fuzzy.
If you submit your figures as GIF/JPG, the Editorial Office will request that the highquality electronic figures of the figures are provided once your paper has been accepted.
Lineart. Create EPS files for images containing lineart. EPS files should be saved with
fonts embedded (and with a TIFF preview if possible). The following packages can be
used to create EPS files: Adobe Illustrator 7.0 and above, Deneba Canvas 6.0 and
above, CorelDRAW 7.0 and above, SigmaPlot 8.01 and above. Other programs may
also be able to create EPS files - use the SAVE AS or EXPORT functions. EPS files can
be produced from other applications [e.g. PowerPoint, Excel (see Electronic Artwork
Guidelines)] BUT results can be unpredictable (e.g. fonts and shading not converted
correctly, lines missing, dotted lines becoming solid).
Half-tones/photographs. Create TIFF files images containing half-tones/photographs.
For scanned images, the scanning resolution (at final image size, see above for a guide
80
to sizes) should be as follows to ensure adequate reproduction: lineart, >800 d.p.i.; halftones, >300 d.p.i. Figures containing both halftone and line images, >600 d.p.i. The
following programs can be used to create TIFF files: Adobe Photoshop 4.0 and above,
Adobe Illustrator 9.0 and GraphPad Prism 3. Other programs may also be able to create
TIFF files - use the SAVE AS or EXPORT functions.
Black and white images should be supplied as 'grayscale'; colour images should be
supplied as CMYK.
Multipart figures should be supplied in the final layout in one file, labelled as (a), (b)
etc.
Supply figures at final size widths if possible: 80 mm (single column) or 165 mm
(double column).
Use sans serif, true-type fonts for labels if possible, preferably Arial or Helvetica, or
Times (New) Roman if serif font is required.
Ensure all lines and lettering are clear.
Supporting Information/Supplementary Material
'Supporting Information' important to the findings of a paper which cannot be included
in the printed copy due to space or format constraints is made available on the
Publisher's website when a paper is published.
Supporting Information should be succinct, not normally exceeding 1500 words, and no
more than 5 tables and figures. It should be designed to allow for complete
understanding of the manuscript.
In addition to text, figures and tables, Supporting Information can include data files (e.g.
extensive species lists and tables of information) and video files (the most common
video file types are supported, providing they do not exceed 50MB). Authors wishing to
submit large files are advised to contact the Editor-in-Chief. This Information should
enhance a reader’s understanding of the paper, but is not essential to the understanding
of the paper. All Supporting Information should be self-explanatory.
All such material must accompany manuscripts when they are originally submitted and
will be reviewed with the main paper. Supporting Information provided with a
manuscript submission will not be edited or altered during the Production process, and a
proof will not be supplied.
The arrangements for depositing the material on the web will be made by the Publisher
after the manuscript has been accepted for publication.
Colour Work Agreement forms
It is the policy of Insect Conservation and Diversity for authors to pay the full cost for
the reproduction of their colour artwork.
Therefore, please note that if there is colour artwork in your manuscript when it is
accepted for publication, Blackwell Publishing require you to complete and return a
81
Colour Work Agreement form before your paper can be published. This form can be
downloaded as a PDF* (portable document format) file from the internet. If you are
unable to access the internet, or are unable to download the form, please contact the
Production Editor at [email protected] and they will be able to email or fax a form to
you.
* To read PDF files, you must have an appropriate software application installed on
your computer. One such example is Acrobat Reader, available as a free download from
the following web address:
http://www.adobe.com/products/acrobat/readstep2.html
Please note this links to an external website. The journal accepts no responsibility for
the content of external sites.
Once completed, please return the form to Customer Services at the address below:
Customer Services (OPI)
John Wiley & Sons Ltd, European Distribution Centre
New Era Estate
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Any article received by Wiley Blackwell with colour work will not be published until
the form has been returned.
Copyright
If your paper is accepted, the author identified as the formal corresponding author for
the paper will receive an email prompting them to login into Author Services; where via
the Wiley Author Licensing Service (WALS) they will be able to complete the license
agreement on behalf of all authors on the paper.
For authors signing the copyright transfer agreement
If the OnlineOpen option is not selected, the corresponding author will be presented
with the copyright transfer agreement (CTA) to sign. The terms and conditions of the
CTA can be previewed in the samples associated with the Copyright FAQs below:
CTA Terms and Conditions http://authorservices.wiley.com/bauthor/faqs_copyright.asp
For authors choosing OnlineOpen
If the OnlineOpen option is selected, the corresponding author will have a choice of the
following Creative Commons License Open Access Agreements (OAA):
Creative Commons Attribution License OAA
Creative Commons Attribution Non-Commercial License OAA
Creative Commons Attribution Non-Commercial -NoDerivs License OAA
82
To preview the terms and conditions of these open access agreement, please visit the
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Serviceshttp://authorservices.wiley.com/bauthor/faqs_copyright.asp
and
visit
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If you select the OnlineOpen option and your research is funded by The Wellcome Trust
and members of the Research Councils UK (RCUK) you will be given the opportunity
to publish your article under a CC-BY license supporting you in complying with
Wellcome Trust and Research Councils UK requirements. For more information on this
policy and the Journal's compliant self-archiving policy, please visit:
http://www.wiley.com/go/funderstatement.
Proofs
The corresponding author will receive an email alert containing a link to a web site. A
working e-mail address must therefore be provided for the corresponding author. The
proof can be downloaded as a PDF file from this site. Appropriate software, such as
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Acrobat Reader can be downloaded (free of charge) from the following website:
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Please note this links to an external website. The journal accepts no responsibility for
the content of external sites.
This will enable the file to be opened, read on screen and printed out in order for any
corrections to be added. Further instructions will be sent with the proof. Hard copy
proofs will be posted if no e-mail address is available.
Offprints
Free access to the final PDF offprint or your article will be available via Author
Services only. Please therefore sign up for Author Services if you would like to access
your article PDF offprint and enjoy the many other benefits the service offers.
Author Material Archive Policy
Please note that unless specifically requested, Wiley Blackwell will dispose of all
submitted hardcopy or electronic material two months after publication. If you require
the return of any material submitted, please inform the Editorial Office or Production
Editor as soon as possible if you have not yet done so.
Author Services
Online production tracking is now available for your article through Wiley
Blackwell's Author Services.
Author Services enables authors to track articles – once they have been accepted –
through the production process to publication online and in print. Authors can check the
status of their articles online and choose to receive automated emails at key stages of
production so they do not need to contact the production editor to check on progress.
83
Visit http://authorservices.wiley.com/bauthor/ for more details on online production
tracking and for a wealth of resources including FAQs and tips on article preparation,
submission, and more.
Cover Photographs
Photographs which may be suitable as cover for Insect Conservation and Diversity are
welcome by the Editor-in-Chief. It is not necessary that these be related to the submitted
manuscript.
OnlineOpen
OnlineOpen is available to authors of articles who wish to make their article open
access. With OnlineOpen the author, their funding agency, or institution pays a fee to
ensure that the article is made available to non-subscribers upon publication via Wiley
Online Library, as well as deposited in PubMed Central and PMC mirror sites. In
addition to publication online via Wiley Online Library, authors of OnlineOpen articles
are permitted to post the final, published PDF of their article on a website, institutional
repository, or other free public server, immediately on publication.
For the full list of Terms and Conditions, see:
http://wileyonlinelibrary.com/onlineopen#OnlineOpen_Terms
Prior to acceptance, there is no requirement to inform the Editorial Office of your
intention to publish your paper OnlineOpen if you do not wish to. All OnlineOpen
articles are treated in the same manner as any other article submission. They will
undergo the same review process, and be accepted or rejected based on their merit.
If you want your article to be open access please choose the appropriate license
agreement when you log in to Wiley's Author Services system. Click on 'Make my
article OnlineOpen' and choose the appropriate license by clicking on 'Sign license
agreement now' when you log in to Wiley's Author Services system. Authors will also
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Correspondence
All correspondence should be addressed to the Editor-in-Chief:
Professor Simon R. Leather
Editor-in-Chief, Insect Conservation & Diversity
Department of Crop & Environmental Sciences
Harper Adams University
Newport, Shropshire, TF10 8NB
U.K.
You may also contact the Editorial Office with any questions.
84
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.
85
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.
87
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.
88
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.
89
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.
90

Efeito da fragmentação de habitats sobre borboletas frugívoras

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