unesp 2004 dissertacao... · enfunando os papos, saem da penumbra, aos pulos, os sapos. a luz os...
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unesp UNIVERSIDADE ESTADUAL PAULISTA
Instituto de Biociências de Rio Claro Departamento de Zoologia
BIOLOGIA REPRODUTIVA DE Scinax fuscomarginatus EM UM
FRAGMENTO DE CERRADO NO SUDESTE DO BRASIL
LUÍS FELIPE DE TOLEDO RAMOS PEREIRA
Dissertação apresentada ao Instituto de Biociências da Universidade Estadual Paulista “Julio de Mesquita Filho”, Campus de Rio Claro, para a obtenção do título de Mestre em Ciências Biológicas (Área de Zoologia).
Rio Claro
Estado de São Paulo – Brasil
Abril de 2004
unesp UNIVERSIDADE ESTADUAL PAULISTA
Instituto de Biociências de Rio Claro Departamento de Zoologia
BIOLOGIA REPRODUTIVA DE Scinax fuscomarginatus EM UM
FRAGMENTO DE CERRADO NO SUDESTE DO BRASIL
LUÍS FELIPE DE TOLEDO RAMOS PEREIRA
Orientador: Prof. Dr. DENIS OTÁVIO VIEIRA DE ANDRADE
Co-orientador: Prof. Dr. CÉLIO FERNANDO BAPTISTA HADDAD
Dissertação apresentada ao Instituto de Biociências da Universidade Estadual Paulista “Julio de Mesquita Filho”, Campus de Rio Claro, para a obtenção do título de Mestre em Ciências Biológicas (Área de Zoologia).
Rio Claro
Estado de São Paulo – Brasil
Abril de 2004
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Enfunando os papos, Saem da penumbra, Aos pulos, os sapos. A luz os deslumbra.
Em ronco que aterra,
Berra o sapo-boi: — "Meu pai foi à guerra!"
— "Não foi!" — "Foi!" — "Não foi!".
O sapo-tanoeiro, Parnasiano aguado,
Diz: — "Meu cancioneiro É bem martelado.
Vede como primo
Em comer os hiatos! Que arte! E nunca rimo
Os termos cognatos!
O meu verso é bom Frumento sem joio
Faço rimas com Consoantes de apoio.
Vai por cinqüenta anos Que lhes dei a norma:
Reduzi sem danos A formas a forma.
Clame a saparia
Em críticas céticas: Não há mais poesia,
Mas há artes poéticas . . ."
Urra o sapo-boi: — "Meu pai foi rei" — "Foi!"
— "Não foi!" — "Foi!" — "Não foi!"
Brada em um assomo O sapo-tanoeiro:
— "A grande arte é como Lavor de joalheiro.
Ou bem de estatuário. Tudo quanto é belo, Tudo quanto é vário, Canta no martelo."
Outros, sapos-pipas
(Um mal em si cabe), Falam pelas tripas:
— "Sei!" — "Não sabe!" — "Sabe!".
Longe dessa grita, Lá onde mais densa
A noite infinita Verte a sombra imensa;
Lá, fugindo ao mundo,
Sem glória, sem fé, No perau profundo
E solitário, é
Que soluças tu, Transido de frio,
Sapo-cururu Da beira do rio
Manuel Bandeira, 1918
OS SAPOS
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AGRADECIMENTOS
Ao prof. Célio Fernando Baptista Haddad a quem devo em muito pelo que hoje sei
sobre anfíbios, pela orientação e amizade, principalmente durante os cafezinhos, momentos
nos quais mais aprendi, tanto sobre Biologia, como sobre política, universidades, ética,
churrasco, fotografia, etc...
Ao prof. Denis Otávio Vieira de Andrade pela orientação, mesmo que tangencial, pela
continuidade dos trabalhos antigos, mas sobretudo pelo companheirismo e resistência, afinal
já se foram mais de seis anos de orientação!
Aos Zoólogos que também contribuíram para minha formação, principalmente os
professores Augusto Abe, Rogério Bastos, Márcio Martins, Ivan Sazima, Ariovaldo Cruz
Neto e Francisco Braga.
Ao pessoal dos laboratórios de Herpetologia de Rio Claro: Juliana, Cynthia, Luís,
Moisés, Anne e Flávio, Luciana Lugli, Paulo e Marília, Luciana Bolsoni, Paulo “Perereca”,
Marcos, Olívia e João pelo companheirismo e pela ajuda durante toda a realização da
dissertação, desde o auxílio na elaboração do projeto, coleta de dados, análises “multi-
variadas”, discussões científico-herpetológicas e até a redação final dos capítulos.
À galera de Itirapina que foi fundamental para animar aquele Cerrado, especialmente
Elaine e Hilton, Tozetti e Victor, Beto, Cínthia e Ricardo, Jota, Spina e Cia; eventualmente
Márcio Martins, Kelly, Jeanne e Chan também contribuíram para “azeitonar” minhas
madrugadas em Itirapina.
À administração da Estação Ecológica de Itirapina, principalmente a Denise Zancheta
e os funcionários do Instituto Florestal, especialmente Gilson, que por repetidas vezes me deu
uma forcinha nos atoleiros do Cerrado. É claro, não podia deixar de mencionar a marcante
onipresença e simpatia de Dna. Izabel, quase sempre disposta a nos divertir.
iii
Ao pessoal extracurricular de Rio Claro, os quais sempre me acompanharam nas horas
vagas: Milho Xangrilá, Fábio “Longarina” e “TC”, “Prima” e Zé, Akio, Cauré, Ju Zina, Yara
e Bira, Sabrina, Renata Udulutsch, Renata Campanhã e Lye, Sarahinha, João Ennser, Elis
Regina e Talento.
Ao povo de sampa, principalmente Quito, Gus, Raf’s, Amaral, Ivan, Evandro e Bel, os
quais eternamente farão parte de minhas conquistas.
À Débora pela paciência, companheirismo e amor, os quais parecem ser infinitos.
À toda minha família, mas essencialmente aqueles sem os quais tudo ficaria muito
mais difícil: Regina, Cris, Neide, Iza, Jair, Eliza e Raphael.
Por fim, ao Conselho Nacional de Desenvolvimento Científico e Técnico (CNPq) pela
bolsa de estudos concedida (processo no. 130417/2003-3) e a Idea Wild pelos equipamentos
doados.
iv
ÍNDICE
Resumo ................................................................................................................
Abstract ................................................................................................................
Introdução Geral ..................................................................................................
Conhecimento atual sobre Scinax fuscomarginatus ................................
Objetivos ......................................................................................... ........
O Cerrado e a Área de Estudo ..................................................................
Capítulo 1: ACOUSTIC REPERTOIRE AND CALLING SITE OF SCINAX
FUSCOMARGINATUS (ANURA, HYLIDAE) DURING REPRODUCTION ..
Abstract ....................................................................................................
Introduction ..............................................................................................
Methods ...................................................................................................
Results ......................................................................................................
Discussion ................................................................................................
Acknowledgments ...................................................................................
Literature Cited ........................................................................................
Capítulo 2: REPRODUCTIVE BIOLOGY AND CHORUS ORGANIZATION
OF SCINAX FUSCOMARGINATUS (ANURA, HYLIDAE) .............................
Abstract ....................................................................................................
Introduction ..............................................................................................
Methods ...................................................................................................
Results ......................................................................................................
Discussion ................................................................................................
Acknowledgments ...................................................................................
References ................................................................................................
Considerações Finais ...........................................................................................
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1
RESUMO
O estudo da biologia reprodutiva de populações de anfíbios anuros compreende
diversos aspectos de história natural, comportamento e ecologia, tais como: I) a
caracterização do modo reprodutivo; II) a caracterização das diferentes vocalizações
emitidas e de seus contextos de emissão; III) a verificação da ocorrência de seleção
sexual e de segregação de recursos limitados; IV) a descrição de comportamentos
sociais e de características morfológicas dos adultos, formas larvárias, desovas e ovos
da espécie. O presente estudo investigou a biologia reprodutiva de Scinax
fuscomarginatus sob todos os enfoques enumerados acima. As observações foram
realizadas no período vespertino e noturno, entre setembro de 2002 e março de 2004 em
um fragmento conservado de Cerrado na Estação Ecológica de Itirapina, localizada nos
Municípios de Itirapina e Brotas, interior do Estado de São Paulo. A espécie reproduziu
em ambientes lênticos e temporários, sendo o padrão reprodutivo prolongado e a
organização dos agregados reprodutivos em forma de leks. Os machos defenderam
territórios através de interações acústicas, visuais e físicas, sendo que os machos
vencedores foram sempre os residentes. Foi observado comportamento de macho
satélite, embora interceptação de fêmeas ou de casais amplectados por machos satélites
não tenha sido observada. Nos ambientes estudados o número de machos foi sempre
maior que o de fêmeas, gerando baixas razões sexuais operacionais. Foram descritos em
detalhe quatro tipos de vocalizações (canto de anúncio, canto esporádico, canto
territorial e canto de briga) e seus respectivos contextos de emissão. Com exceção do
canto de anúncio, as demais vocalizações apresentadas são inéditas para a espécie. O
amplexo foi axilar e os ovos foram depositados diretamente na água, no fundo de poças
temporárias. Os ovos possuíam duas cápsulas gelatinosas, as quais conferem maior
espaçamento entre os embriões. A população estudada de S. fuscomarginatus
apresentou uma gama de comportamentos sociais elaborados, incluindo organização
espacial entre machos, interações agonísticas (acústicas, visuais e físicas) e um provável
comportamento de corte (canto de corte), características comuns à espécies de padrão
reprodutivo prolongado.
2
ABSTRACT
Studies on the reproductive biology of anuran populations combine diverse
aspects of natural history, behavior, and ecology, such as: I) characterization of the
reproductive mode; II) characterization of the vocalizations produced by the species and
the contexts of emission; III) verification of the occurrence of sexual selection and
segregation of limited resources; IV) description of the social behaviors and
morphologic characteristics of the adults, tadpoles, clutches, and eggs. The present
study investigated the reproductive biology of Scinax fuscomarginatus considering all
features presented above. Observations occurred during the evening and night between
September 2002 and March 2004 in a fragment of Cerrado at the Estação Ecológica de
Itirapina, located at the counties of Itirapina and Brotas, interior of the state of São
Paulo, southeastern Brazil. The species reproduced in lentic and temporary ponds. The
reproductive pattern was prolonged and the mating system was characterized as lek.
Males defended territories by acoustic, visual, and physical interactions. Winner males
were always the residents. Satellite behavior was observed, although none female or
amplected couple interception was observed. At the studied ponds the number of males
(calling or not) was always higher than the number of females, generating low
operational sex ratios. Four different vocalizations (advertisement, sporadic, territorial
and fighting calls) were described in detail. With the exception of the advertisement
call, the remaining calls are novel for the species. The amplex was axillary and the eggs
were laid directly on the water, in the bottom of temporary ponds. The eggs had two
gelatinous layers, which conferred spacing among the embryos. The studied population
of S. fuscomarginatus showed an elaborated range of social behaviors, including spatial
organization among males at the chorus, agonistic interactions (acoustic, visual, and
physical), and a probable courtship behavior (courtship call). These characteristics are
common in prolonged breeding species.
3
INTRODUÇÃO GERAL
Os estudos com anfíbios anuros na região neotropical e em ambiente natural têm
se dedicado principalmente aos aspectos da biologia reprodutiva das espécies (Martins,
1988; 1993; Haddad & Cardoso, 1992; Freitas et al., 2001; Wogel et al., 2002). Estudos
como estes procuram descrever a temporada de atividade reprodutiva das populações,
geralmente baseada na atividade de vocalização dos machos adultos (Pombal Jr., 1997;
Bernarde & Machado, 2001; Toledo et al., 2003), ou juvenis (Lampert & Linsenmair,
2002) e inferem sobre a influência de fatores abióticos sobre a atividade reprodutiva
(Aichinger, 1987). Alguns desses estudos investigam também os fatores responsáveis
pela seleção sexual, verificando aspectos reprodutivos quantitativos e de relações de
fecundidade (Prado & Uetanabaro, 2000; Bastos & Haddad, 2001).
Ademais, como os anfíbios anuros se destacam por sua alta capacidade de
emissão sonora, muitos estudos em campo já foram realizados sobre esse tema (ver
Ryan, 2001). Com o passar dos anos, diversas funções sociais e diferentes contextos de
emissão dos cantos foram identificados (revisões em Wells, 1988; Haddad, 1995). Por
exemplo, a comunicação sonora entre os anfíbios anuros pode ser utilizada para a
atração de parceiros sexuais (Haddad & Cardoso, 1992; Schwartz, 1994; Brenowitz &
Rose, 1999) ou pode estar relacionada à defesa e delimitação de territórios, podendo
evitar combates físicos entre machos que disputam recursos limitados, como os sítios de
vocalização (Wells, 1988; Bastos & Haddad, 2001) e/ou desova (Martins et al., 1998).
A vocalização ainda pode funcionar como um eficiente meio de segregação reprodutiva
pré-zigótica (Oldham & Gerhardt, 1975; Etges, 1987; Cardoso & Viellard, 1990;
Bourne & York, 2001). A vocalização é, portanto, um eficiente mecanismo de
comunicação entre os anfíbios anuros (Ryan, 2001). Apesar disso, o conhecimento
4
sobre os diversos aspectos relativos à comunicação acústica, incluindo as características
estruturais do repertório acústico das espécies de anuros neotropicais, é ainda escasso.
Outro parâmetro freqüentemente investigado durante a atividade reprodutiva dos
anfíbios anuros é a territorialidade dos machos, incluindo diversos estágios de
interações agressivas, gerada pela disputa de recursos limitados, como sítios de
vocalização, sítios de desova, e/ou parceiras sexuais (Wells, 1977a; 1978; Cardoso &
Haddad, 1984; Martins et al., 1998; Bastos & Haddad, 1995; 2002; Guimarães &
Bastos, 2003). Em conjunto, os estudos sobre biologia reprodutiva dos anuros
neotropicais indicam que os acasalamentos não ocorrem ao acaso, podendo ser
definidos por seleção de machos pelas fêmeas, ou como resultado das interações
acústicas e agressivas entre machos (Arak, 1983, Ryan, 1985; Olson et al., 1986;
Wagner & Sullivan, 1992; Brenowitz & Rose, 1999). Assim, processos de seleção
sexual podem estar atuando no sentido de favorecer o dimorfismo sexual na maioria das
espécies de anuros (Shine, 1979).
O dimorfismo sexual é causado pela diferença entre a soma de todas as pressões
seletivas que afetam características dos machos e a soma de todas as pressões que
afetam características das fêmeas (Ralls, 1976). Em relação ao tamanho e massa
corpórea, as principais pressões para o dimorfismo sexual mencionadas na literatura
são: I) pressão para incremento de fecundidade das fêmeas em virtude do aumento do
tamanho corpóreo (Crump, 1974; Shine, 1979); II) pressão para aumento do tamanho
corpóreo dos machos em virtude de interações agressivas (Davies & Halliday, 1977;
Shine, 1979; Katsikaros & Shine, 1997); III) maior taxa de mortalidade dos machos, não
permitindo que atinjam a mesma idade e, conseqüentemente, o mesmo tamanho das
fêmeas (Shine, 1979; Monnet & Cherry, 2002); ou IV) diferentes taxas de crescimento
entre machos e fêmeas (Halliday & Verrell, 1988).
5
Muitas espécies do gênero Scinax Wagler 1830 possuem dimorfismo sexual e
possuem padrões reprodutivos variados (Lutz, 1973; Haddad et al., 1990; Heyer et al.,
1990; Bourne, 1992; Bevier, 1997; Toledo et al., 2003). Quanto ao sítio de desova,
algumas espécies ovipõem em ambientes lóticos (e.g., S. albicans e S. trapicheiroi:
Carvalho e Silva & Carvalho e Silva, 1994) ou em ninhos de espuma (e.g., S. rizibilis:
Haddad et al., 1990). Entretanto, na maioria das espécies as fêmeas depositam os ovos
em ambientes aquáticos lênticos, nos quais os girinos se desenvolvem (Lutz, 1973;
Bastos & Haddad, 1999). Este modo reprodutivo foi considerado como sendo o modo
basal no cenário evolutivo proposto por Duellman (1985). Quanto à temporada
reprodutiva (sensu Wells, 1977b), são conhecidas tanto espécies de padrão reprodutivo
explosivo [e.g., S. fuscovarius: Bertoluci, 1998; Toledo et al., 2003; S. ruber: Bourne,
1992; Bevier, 1997; Scinax sp. (aff. similis): Toledo et al., 2003], quanto de padrão
reprodutivo prolongado (e.g., S. albicans: Carvalho e Silva & Carvalho e Silva, 1994; S.
boulengeri: Bevier, 1997; S. rizibilis: Bastos & Haddad, 1999; S. centralis e S.
fuscomarginatus: Bernarde & Kokubum, 1999; Bastos et al., 2003a).
Conhecimento Atual Sobre Scinax fuscomarginatus
Scinax fuscomarginatus é um hilídeo de pequeno porte, com pouco mais de 2 cm
de comprimento rostro-cloacal (Lutz, 1973). É uma espécie típica de áreas abertas,
como o Cerrado e Pantanal (Araujo & Colli, 1998), distribuindo-se pelo leste da
Bolívia, por todo território paraguaio e nordeste da Argentina. No Brasil a espécie pode
ser encontrada desde a região sul ao planalto central e do leste da região sudeste ao
extremo oeste da região pantaneira (Frost, 2002) (Figura 1).
6
Figura 1. Mapa da América do Sul indicando (em cinza) a distribuição geográfica aproximada de Scinax fuscomarginatus (segundo Frost, 2002).
Dentre as espécies do gênero, S. fuscomarginatus caracteriza-se por machos que
se agregam em torno de poças permanentes ou temporárias para a reprodução,
utilizando a vegetação marginal como sítio de vocalização (Lutz, 1973; Rossa-Feres &
Jim, 2001; Bastos et al., 2003a). Quanto ao repertorio acústico, apenas o canto de
anuncio é conhecido (Pombal Jr. et al., 1995; Bastos et al., 2003a; 2003b), sendo que
variações na sua estrutura foram reconhecidas quando diferentes populações foram
estudadas (Bueno, 2001; Bueno et al., 2002).
Relações de esforço reprodutivo dos machos já foram brevemente discutidas
(Prado & Haddad, 2003). Sabe-se que a desova é depositada diretamente em corpos
d’água lênticos (Bastos et al., 2003a). Foram descritos o desenvolvimento larval e os
girinos desta espécie, outrora tratada como Hyla parkeri (Vizoto, 1967) e Ololygon
7
fuscomarginata (Altig & Johnston, 1986). Ademais, são encontrados na literatura curtos
relatos sobre predação de adultos por sanguessugas (Brandão & Garda, 2000) e sobre a
gama de comportamentos defensivos apresentados por machos adultos (Toledo, no
prelo).
Objetivos
Esta dissertação é apresentada em dois capítulos, redigidos em inglês e editados
no formato de periódicos especializados. Os capítulos possuem objetivos distintos,
sendo que o primeiro deles visou: (I) descrever o repertório acústico de Scinax
fuscomarginatus; (II) identificar os possíveis contextos de emissão de cada uma das
vocalizações reconhecidas; (III) determinar a temporada de vocalização; (IV) identificar
e descrever os sítios de vocalização utilizados; e (V) realizar comparações com outras
populações a fim de propiciar uma melhor compreensão sobre os padrões de
vocalização desta espécie.
O segundo capítulo é dedicado a: (I) descrição da organização espacial e
temporal dos indivíduos presentes nos agregados reprodutivos; (II) caracterização dos
comportamentos associados à biologia reprodutiva, como comportamento de formação
de casais, interações agressivas entre machos e comportamento de macho satélite; (III)
verificação de aspectos quantitativos tais como relações de fecundidade, esforço
reprodutivo e dimorfismo sexual; e (IV) caracterização da desova e sua caracterização
em ambiente natural.
8
O Cerrado e a Área de Estudo
O Cerrado é um importante ecossistema que cobre cerca de 23 %
(aproximadamente 2 milhões de km2) do território brasileiro, estendendo-se das
margens da Floresta Amazônica até áreas fragmentadas nos Estados de São Paulo e
Paraná (Ratter et al., 1997). Apesar do Cerrado ser bastante extenso em território
nacional, a herpetofauna deste bioma ainda é muito pouco conhecida, tanto do ponto de
vista taxonômico, quanto ecológico (Araujo & Colli, 1998; Colli et al., 2003). Além de
pouco conhecida, o Cerrado está sendo continuamente ameaçado, principalmente por
atividades agropecuárias. Estas atividades afetaram severamente o Cerrado nos últimos
30 anos, restando atualmente menos de 60 % da sua cobertura original (Ratter et al.,
1997). No Estado de São Paulo, por exemplo, o cerrado já ocupou cerca de 14 % do
território, mas atualmente ocupa apenas 1 % (248,8 mil km2), e apenas 18 % da área
remanescente está protegida por 32 unidades de conservação e de reserva legal (Fiori &
Fioravanti, 2001). Essas reservas, todavia, constituem-se basicamente de fragmentos do
ecossistema original. Sendo assim, estudos biológicos nos fragmentos restantes são de
extrema urgência, principalmente nas áreas mais afetadas como as do Estado de São
Paulo (Martins, 2001).
A Estação Ecológica de Itirapina pertence ao Instituto Florestal do Estado São
Paulo e localiza-se a aproximadamente 230 km do Município de São Paulo, nos
municípios de Itirapina e Brotas (Figura 2) e compreende uma das últimas áreas
preservadas de Cerrado do Estado. A área da reserva é de cerca de 2.300 ha de
vegetação natural de cerrado pouco perturbada, incluindo várias fisionomias, como
campo limpo, campo sujo, campos cerrados, áreas brejosas e matas de galeria (Martins,
9
2001) (Figura 3). O clima da região caracteriza-se por um inverno frio e seco e um
verão quente e chuvoso.
Figura 2. Estação Ecológica de Itirapina (EEc), localizada entre áreas de plantio de Eucaliptus spp. e Pinus spp. (Ripasa e Eex = Estação Experimental de Itirapina), próxima à cidade de Itirapina, interior do Estado de São Paulo, sudeste do Brasil.
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Figura 3. Foto aérea da Estação Ecológica de Itirapina e suas principais fisionomias: CL = campo limpo; CS = campo sujo; CC = campo cerrado; MG = mata de galeria.
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19
Chapter 1
ACOUSTIC REPERTOIRE AND CALLING SITE OF
SCINAX FUSCOMARGINATUS (ANURA, HYLIDAE)
DURING REPRODUCTION
LUÍS FELIPE TOLEDO and CÉLIO FERNANDO BAPTISTA HADDAD
20
JOURNAL OF HERPETOLOGY
ACOUSTIC REPERTOIRE AND CALLING SITE OF SCINAX
FUSCOMARGINATUS (ANURA, HYLIDAE) DURING REPRODUCTION
Luís Felipe Toledo1 and Célio Fernando Baptista Haddad1
1Departamento de Zoologia, Instituto de Biociências, Universidade Estadual Paulista,
Caixa Postal 199, CEP 13506-970, Rio Claro, São Paulo State, Brasil. E-mail:
Corresponding author: LFT: [email protected]
Running title: acoustic repertoire and calling site of S. fuscomarginatus
21
ABSTRACT.—Vocalizations produced by anuran amphibians are considered an
interespecific pre-zygotic segregation mechanism fundamental for intraspecific
communication. Calling helps on the spatial organization of males at breeding sites,
promotes the attraction of new individuals to the chorus, and attracts mature females for
reproduction. In the present study, we describe four distinct vocalizations
(advertisement, sporadic, territorial, and fighting calls) emitted by males of Scinax
fuscomarginatus. We also characterize their contexts of emission for each of these calls.
With the exception of the advertisement call, the remaining descriptions are novel. We
also described the calling sites, the calling season, and the extension of calling activity
in single nights. Field work was made in a fragment of Cerrado biome (Estação
Ecológica de Itirapina), Municipalities of Itirapina and Brotas, state of São Paulo,
southeastern Brazil. At this ecological station, S. fuscomarginatus exhibited a complex
acoustic repertoire, social interactions, and prolonged reproductive pattern. Males made
use of three different strategies to avoid acoustic overlap, which may hinder
disadvantageous female attraction. The advertisement call presented structural
differences when compared to another population of state of São Paulo, but not to with
populations from central Brazil.
22
INTRODUCTION
Anuran amphibians are distinguished by their capacity of sound production,
generally by air flow throughout its vocal cords (Duellman and Trueb, 1994, but see
exception in Souza and Haddad, 2003). Vocalizations have many social functions and
are produced in different contexts (reviews in Wells, 1988; Haddad, 1995). Acoustic
communication between anurans can be used to attract mates (e.g., Haddad and
Cardoso, 1992; Schwartz, 1994; Brenowitz and Rose, 1999). Also, vocalizations may be
related to defense of territory, avoiding physical encounters between males that compete
for a limited resource, such as calling sites (e.g., Wells, 1988; Bastos and Haddad, 2002)
and/or egg laying sites (e.g., Martins et al., 1998).
Calling however, can also attract (Ryan et al., 1982) or prevent potential
predators (Sazima, 1975), and works as an efficient inhibitor of pre-zygotic segregation
(Oldham and Gerhardt, 1975; Etges, 1987; Cardoso and Viellard, 1990; Bourne and
York, 2001). Calling activity is, therefore, a primary communication mechanism for
anuran amphibians (Ryan, 2001).
The structural characteristics of the acoustic repertoire of Neotropical anuran
species remain poorly investigated. For Scinax fuscomarginatus, only the description of
the advertisement call is available (see Pombal Jr. et al., 1995; Bastos et al., 2003a;
2003b). This call, however, may vary among different populations (Bueno, 2001; Bueno
et al., 2002). Regarding the calling season, there is one study that males vocalized for a
short period (Pombal Jr., 1997) and another that males called for over three months
(Bernarde and Kokubum, 1999).
The present study describes the acoustic repertoire and the calling sites of Scinax
fuscomarginatus, and tries to identify the possible contexts in which different
vocalizations were emitted, and determines the calling season for this species.
23
050
100150200250300350400
Oct Nov Dec Jan Feb Mar Apr
Rai
nfal
l (m
m)
0
5
10
15
20
25
Days of rain
A
25
50
75
100
Oct Nov Dec Jan Feb Mar Apr
Rel
ativ
e hu
mid
ity (%
)
10
15
20
25
30 Temperature (ºC
)
B
MATERIALS AND METHODS
Study area.—Field work was done at the Estação Ecológica de Itirapina (EEI) located at
the Municipalities of Itirapina and Brotas, state of São Paulo, Brazil. The EEI is under
the administration of the Instituto Florestal de São Paulo and it is one of the last areas of
pristine Cerrado at this state. The reserve has 2,300 ha of area including typical
phytophysiognomies such as “campo limpo”, “campo sujo”, “campo cerrado”, swamps,
and gallery forests (Martins, 2001). The climate of EEI is characterized by a cold and
dry winter, and a hot and rainy summer, with the highest temperatures, days of rain, and
rainfall in January (Fig. 1). Its sandy soil needs a large water volume prior to the
formation of temporary ponds (person. obs.).
Fig. 1. (A) Total monthly rainfall (bars) and total monthly days of rain (line); and (B) mean monthly relative humidity (bars) and mean monthly temperature (line) at the Estação Ecológica de Itirapina, state of São Paulo, Brazil, between October 2002 and April 2003.
Observations were conducted in two temporary ponds, named “Lagoa do Trem”
and “Lagoa da Ponte”. The first is rectangular and with approximately 250 m2 in the
portion studied (Fig. 2). The Lagoa da Ponte has a rounded shape, with approximately
500 m2 of area and 40 m in diameter. The vegetation of both ponds is similar, with
24
predominance of small herbaceous shrubby vegetation, which the most common is
Andropogon lateralis (Poaceae). These plants grow both in the central part and on the
edges of the ponds, forming small islands of vegetation on the interior of the ponds (Fig.
2).
Fig. 2. Studied portion of Lagoa do Trem, Estação Ecológica de Itirapina, state of São Paulo, Brazil. The arrows indicate the islands of vegetation formed by clumps of Andropogon lateralis.
Data collection and analysis.—Observations were made between September 2002 and
March 2004. During the rainy season field expeditions were made with duration of 4 to
10 consecutive nights. The observation periods begun just before sunset and ended
when the calling activity of the species had decreased considerably, or when stopped.
We did not considered the time adjustments established by the daylight saving time.
For the observations were used white-light flashlights, avoiding that the central
focus of the flashlight illuminated the animals directly. For the observation of individual
behavior and intraspecific interactions we used the sampling methods of ad libitum,
focal-animal, all occurrences of some behaviors, and sequences (see Altmann, 1974;
Lehner, 1996).
25
The individuals observed in the field were weighted with field weighting scales
with 0.005 g of precision, and measured (SVL = snout-vent length) with a 0.05 mm
precision caliper. We also registered the hour of the observation, the individual activity,
sex, presence or absence of mature ovules (when females), and nearest distance between
conspecifics. For individual recognition, the animals were toe-clipped following the
table presented by Powell and Knesel (1992). After that, they were released at the same
place where they were collected. Acoustic census of males in calling activity were made
hourly from the beginning to the end of the calling activity.
Vocalizations were recorded with a Marantz cassette recorder, model PMD222,
with an external directional microphone Audiotecnica, model AT835b, positioned ca.
50 cm from the calling male. We used BASF® cassette tapes model CEII Chrome
Extra, at 4.75 cm/s of speed. The sound analyses were made in a Macintosh® computer,
using the Canary 1.2.4 software, configured with 16 bits of resolution, 22 kHz of
frequency sampling, FFT and frame length of 256 samples.
The terminologies used for the vocalization analyses follow those adopted by
Duellman and Trueb (1994): vocalization was assumed to be any sort of sound emission
made by the vocal apparatus of the animal, where calls and notes are categories of
vocalizations. Notes were treated as sound emissions characterized by discrete temporal
unities that compose the call. The call was considered to be the sound emission formed
by one (simple call) or more (compost call) stereotyped notes, which can be multipulsed
or not. Pulses were considered as sub unities of notes, not always distinguishable.
Abiotic factors that could interfere in the activity of the anurans were registered
(time, air and water temperatures, measured with a 0.5 ºC precision mercury
thermometer, and rain occurrence). Additional climatic data (relative humidity,
temperature, rainfall, and days of rain per month) were obtained at the meteorological
26
station of the Fazenda Seriema, located ca. 15 km from the study site. Meteorological
factors were correlated with the number of calling males which attended the chorus in
the same day or with the mean monthly activity of the species at EEI. The calling sites
were characterized by measuring height and distance of the calling site from the nearest
pond margin; perimeter, height, and form of the occupied vegetation clump; and its
distance to the nearest vegetation clump.
For the analysis of statistical correlations and influences, after verified the
homogeneity of variance premises and data normality, we used the r coefficient of
Pearson and linear regression analysis, respectively. Significant values were considered
when P < 0.05 (Zar, 1999).
27
RESULTS
The calling season of Scinax fuscomarginatus at the EEI was extended from
December to March for two consecutive reproductive seasons (2002-2003 and 2003-
2004). The calling season began after the formation of lentic and temporary aquatic
environments. The Lagoa do Trem was formed before the Lagoa da Ponte, hence the
presence of calling males on these habitats occurred in distinct periods (Fig. 3).
The number of calling males remained relatively high for two to three weeks
after the start of the calling activity, and decreased rapidly after that (Fig. 3). The
number of calling males was positively correlated with the monthly rainfall (r = 0.755;
P = 0.05), days of rain per month (r = 0.868; P = 0.033), and mean monthly air
temperature (r = 0.763; P = 0.046), but not with the relative humidity (r = -0.012; P =
0.958).
Males were recaptured always at the same pond where they were captured and
marked, generally in successive nights, using exactly the same calling site. The
individuals remained in the chorus for three consecutive nights in average (SD = 2.27;
range = 1–8 consecutive nights; N = 22). One calling male was recaptured 15 days after
its first capture.
28
0
3
6
9
12
15
18
21
12/1
6/20
02
1/4/
2003
1/6/
2003
1/14
/200
3
2/6/
2003
2/8/
2003
2/10
/200
3
2/12
/200
3
2/14
/200
3
3/8/
2003
3/15
/200
3
Field trips
Num
ber
of c
allin
g m
ales
Lagoa do Trem
Lagoa da Ponte
Fig. 3. Scinax fuscomarginatus calling season in two temporary ponds (Lagoa do Trem and Lagoa da Ponte) at the Estação Ecológica de Itirapina, state of São Paulo, Brazil, between December 2002 and March 2003.
We observed males calling between 0 and 150 cm above the ground or from the
water surface (Fig. 4A), mainly above the border vegetation of the temporary ponds.
However, some calling males were also found as far as 2.3 m from the pond (Fig. 4B).
During calling, males perched on branches of the emerging vegetation, with their heads
usually oriented vertically and upwards (Fig. 5), but also adopting different positions
(Table 1). Males could be oriented to the central part of the pond, to its margins, or even
oriented parallel to the nearest margin (Table 1).
29
Fig. 4. Characterization of the calling sites explored by males of Scinax fuscomarginatus at the Estação Ecológica de Itirapina. A) Height of the calling site, and B) distance of the calling site in relation to the nearest pond margin. The negative values represents measurements toward the central part of the pond; N = 58 in both cases.
Fig. 5. Adult male of Scinax fuscomarginatus during calling activity on emerging vegetation at the Lagoa do Trem, Estação Ecológica de Itirapina, state of São Paulo, southeastern Brazil.
0
10
20
30
40
50
60
-150
0 to
-100
1-1
000
to -5
01
-500
to -1
0 to
50
51 to
100
101
to 1
50
151
to 2
00
> 20
0
Margin distance (cm)
Males observed (%
)
0
5
10
15
20
250
to 1
011
to 2
021
to 3
0
31 to
40
41 to
50
51 to
60
61 to
70
71 to
80
81 to
90
91 to
100
> 10
0
Calling site height (cm)
Mal
es o
bser
ved
(%)
A) B)
30
Table 1. Position of males of Scinax fuscomarginatus during calling activity at Estação Ecológica de Itirapina, state of São Paulo, Brazil. Numbers in parenthesis indicate the total number of observations.
Calling male position Observations (%) In relation to the margins (57) Oriented to the center of the pond 33.9 Oriented to the margin 38.7 Parallel to the margin 27.4 In relation to the ground (61) Parallel 21.2 Perpendicular Head upwards
27.3
Head downwards 21.2 Total 48.5 Diagonal Head upwards
16.7
Head downwards 13.6 Total 30.3
Males also called from small gramineous clumps in the middle of the ponds. In
94.7% of the observations (total N = 62), only one male was observed occupying a
single clump in the middle of the pond. On the remaining clumps (N = 5) satellite males
were observed. There was no significant correlation between the physical characteristics
of the anurans and any of the four analyzed physical characteristics of the clumps (Table
2).
Table 2. Pearson coefficient (r) and significance (P) for the correlation between physical characteristics of adult calling males of Scinax fuscomarginatus and four structural parameters of their calling site at the Estação Ecológica de Itirapina, state of São Paulo, southeastern Brazil (N = 17).
Calling male
Clump perimeter
Clump height
Clump volume
Distance to the nearest clump
SVL r
P 0.1622 0.534
0.4731 0.0551
0.2252 0.385
0.1692 0.516
Mass r
P 0.1897 0.466
0.4241 0.0898
0.1184 0.651
0.3398 0.182
31
Four distinct vocalizations emitted by males of Scinax fuscomarginatus were
recognized. All vocalizations were simple and formed by one multipulsed note, but
showed distinct physical structures (Table 3) and were emitted in different social
contexts.
Advertisement call (Fig. 6A).—The single note that forms this call has the mean
dominant frequency (3.82 ± 0.22 kHz) lower than the remaining calls described for this
species. It is emitted with variable intervals, between 0.58 and 19.59 s, frequently higher
than the duration of the note (540.1 ± 61.92 ms). Advertisement calls in antiphony were
also registered (Fig. 7). The intervals between pulses of the same call did not showed
great variation (see Table 3), generating a significant and positive regression between
the number of pulses per call and the duration of the call (r2 = 0.58; P < 0.0001; Fig. 8).
Sporadic call (Fig. 6B).—Formed by one note that has frequency amplitude
similar to those of the advertisement and territorial calls. However, the sporadic call has
the highest interval between pulses (4.3 ± 4.9 ms), the lowest number of pulses per call
(from 21 to 48), and the shortest duration of the call (304.5 ± 55.4 ms). There are two
bands of dominant frequency in this vocalization; the first band has mean frequency of
4.0 kHz and the second of 4.6 kHz. This call was emitted most frequently by males
during the beginning and during the end of the calling activity, when the density of
calling males was lower (Fig. 9).
Territorial call (Fig. 6C).—Formed by a single note with dominant frequency
amplitude similar to the amplitudes of the other calls (between 2.09 and 5.32 kHz). This
was the longest call (718.9 ± 71.5 ms) recorded and the one with the highest number of
pulses (from 111 to 150 pulses per call). It shows temporal variation across its emission.
It is possible to analyze territorial call notes in two different parts; the initial and central
32
portion of the note have the duration of the pulses and the interval of pulses higher than
the final portion of the note (Table 3).
Fighting call (Fig. 6D).—Emitted with a lower intensity than the calls described
above. Among them, it is the call that presents the lowest duration (85.0 ± 8.0 ms) and
the lowest duration of the pulses (always less than 1 ms). It is the call that has the
highest pulse repetition rate, which were always higher than 200 per call, without
distinguishable intervals among them. The fighting call has the minimum frequency (1.8
kHz) lower than the other calls (territorial: 2.09 kHz; advertisement: 2.4 kHz; sporadic:
2.8 kHz) and the mean frequency amplitude (4.1 kHz) higher than the other calls
(sporadic: 2.4 kHz; advertisement: 3.16 kHz; territorial: 3.2 kHz). The fighting calls
were emitted by males during physical interactions (see Chapter 2). Fighting calls were
repeatedly emitted, but without regular repetition rate over the whole combat by both
males (see Chapter 2).
33
Table 3.
34
Fig. 6. Sonogram (above) and ocilogram (below) of (A) advertisement call (air temperature = 19.5 ºC), (B) sporadic call (air temperature = 23 ºC), (C) territorial call (air temperature = 24 ºC), and (D) fighting call (air temperature = 24 ºC) emitted by males of Scinax fuscomarginatus. Recordings made between February 2003 and January 2004, at the Estação Ecológica de Itirapina, state of São Paulo, Brazil.
D) C)
Freq
uenc
y (k
Hz)
Time (ms) Time (ms)
Freq
uenc
y (k
Hz)
08
06
04
02
08
06
04
02
0 100 200 300 400 500 600 700 800 900
Freq
uenc
y (k
Hz)
A) B)
Time (ms) Time (ms)
Freq
uenc
y (k
Hz)
08
06
04
02
08
06
04
02
0 100 200 300 400 500 600 700 800 0 50 100 150 200 250 300 350 400 450
0 20 40 60 80 100 120 140 160
35
Fig. 7. Antiphony of the advertisement call of Scinax fuscomarginatus. Letters “A” and “B” represents calls emitted by two males during vocal interaction. Recordings were made in January 2004 (air temperature = 21 ºC), at the Estação Ecológica de Itirapina, state of São Paulo, Brazil.
40
60
80
100
120
140
300 400 500 600 700
Duration of the note (ms)
Num
ber
of p
ulse
s/no
te
Fig. 8. Linear regression between number of pulses per note/call and duration of the note/call (N = 102) of the Scinax fuscomarginatus advertisement call at the Estação Ecológica de Itirapina, state of São Paulo, Brazil.
Time (s)
Freq
uenc
y (k
Hz)
08
06
04
02
0,5 1 1,5 2 2,5 3 3,5 4 4,5
A B A B A B A B A B
36
We found a negative correlation between body mass and SVL in relation to the
advertisement call dominant frequency (r = -0.83; r2 = 0.68; P = 0.0005; and r = -0.82;
r2 = 0.57; P = 0.0006, respectively) (Fig. 8). SVL and body mass were not correlated to
the number of pulses per note, duration of the call, and calling rate (P > 0.05 for all
cases). There was also no correlation between air temperature and the dominant
frequency, number of pulses per call, duration of the call, or vocalization rate (P > 0.05
for all cases).
Fig. 8. Linear regression (lines) between mass and dominant frequency (A), and between SVL and dominant frequency (B) of the advertisement call of Scinax fuscomarginatus at the Estação Ecológica de Itirapina, municipalities of Itirapina and Brotas, state of São Paulo, Brazil; N = 13.
The calling activity of S. fuscomarginatus began one or two hours before the
sunset and continued for up to eight hours after the sunset. The number of calling males
emitting advertisement calls increased for about one hour after the sunset, when the
peak of calling activity was reached. After that, the number of calling individuals
decreased gradually. The territorial call was emitted at higher rates in the beginning of
the calling activity, and it was emitted again only during male interactions (see chapter
3
3.25
3.5
3.75
4
4.25
4.5
0.6 0.7 0.8 0.9
Mass (g)
Dom
inan
t fre
quen
cy (
kHz)
3
3.25
3.5
3.75
4
4.25
4.5
21 22 23 24 25 26
SVL (mm)
Dom
inant frequency (kHz)
A) B)
37
2) (Fig. 9). The calling rate (number of calls per minute) varied across the night, and it
was positively correlated with the number of calling males present at the chorus (r =
0.82; P = 0.047) (Table 4). In four occasions males were heard calling between 1100
and 1300 h, calling rarely and generally emitting sporadic calls rather than
advertisement calls.
Fig. 9. Calling activity pattern of Scinax fuscomarginatus at the Estação Ecológica de Itirapina, Municipalities of Itirapina and Brotas, state of São Paulo, Brazil. Mean values (bars) and standard deviation (lines) of seven nights for the advertisement call, and results for one night for the remaining vocalizations. The number of males refers to calling individuals observed in an area of approximately 250 m2.
Table 4. Number of calling males of Scinax fuscomarginatus in an area of approximately 250 m2, mean number of advertisement, territorial, and sporadic calls emitted by six males heard from a steady position over one night (January 10, 2004) at the Estação Ecológica de Itirapina. The sampling interval was two minutes, and the data were corrected for one minute sampling. The values are expressed as mean ± standard deviation (range).
Vocalization rate (calls/minute)
Hours in relation to the sunset Advertisement Territorial Sporadic
Number of calling
males -1 7.67 ± 1.76 (6 to 9) 3.3 ± 1.2 (2 to 4.3) 0.16 ± 0.29 (0 to 1.5) 03 0 17.83 ± 2.47 (15 to 19) 0.0 0.0 08 1 14 ± 0.5 (13.5 to 14.5) 0.0 0.0 10 2 9.67 ± 2.08 (8 to 12) 0.0 0.0 07 3 7.83 ± 1.76 (6 to 9.5) 0.0 0.0 04 4 7.5 ± 3.77 (3.5 to 11) 0.78 ± 0.51 (0.3 to 1.3) 0.83 ± 1.44 (0 to 2.5) 03
0
3
6
9
12
15
18
-2 -1 0 1 2 3 4 5
Hours in relation to the sunset
Num
ber
of m
ales
AdvertisementTerritorialSporadic
38
DISCUSSION
Although the correlation between temperature, days of rain, and rainfall with the
number of calling males, the presence of ponds was the limiting factor for the beginning
of the calling season of Scinax fuscomarginatus at EEI. Males that called at Lagoa da
Ponte only began the calling activity when the pond was present, approximately one
month after the beginning of the calling activity at Lagoa do Trem (Fig. 3). Scinax
fuscomarginatus presented a prolonged breeding pattern (sensu Wells, 1977) at EEI (see
also Chapter 2).
The fact that individuals were not recaptured out of the pond where they were
first captured, indicate reproductive site phylopatry for S. fuscomarginatus, at least
during the calling season. The fidelity to the calling site and the permanence of males at
the breeding site for consecutive days can increase the chances of mating by the males
(Murphy, 1994) and decrease the number of agonistic interactions, since the calling
territories do not need to be established again over the nights.
The calling site of S. fuscomarginatus at EEI was similar to sites observed in
other studies. This species uses calling perches at the margins of temporary lentic ponds
(Rossa-Feres and Jim, 2001; Bastos et al., 2003) or permanent ponds (Pombal Jr. et al.,
1995; Bernarde and Kokubum, 1999; Bastos et al., 2003). Males prefer calling sites
between 0 and 50 cm high in dense or sparse shrubby vegetation (Pombal Jr. et al.,
1995; Rossa-Feres and Jim, 2001). The males’ positioning at the chorus during
vocalizations seems to be random (Rossa-Feres and Jim, 2001), and may depend on the
vegetation architecture used as perch. Likewise, the lack of correlation between the
analyzed structural characteristics of the vegetation and the physical characteristics of
39
the calling males suggests that the calling site choice is influenced by other factors. It is
possible that factors, such as male density of the same or of different species, interfere
in the calling site choice (see Schwartz and Wells, 1984; Etges, 1987).
Scinax fuscomarginatus presented a complex acoustic repertoire, with at least
four different vocalizations. This is characteristic of species with prolonged breeding
pattern (Wells, 1977; Bastos and Haddad, 1995; Guimarães and Bastos, 2003) and with
complex social behavior (Martins and Haddad, 1988; Bastos and Haddad, 1999).
The advertisement call can have several functions: (I) attraction of other males to
the chorus; (II) female attraction; (III) and/or regulation of the spatial distribution
among males present at the core (Haddad, 1995; Ryan, 2001). The dominant frequency
and call duration of S. fuscomarginatus of EEI were slightly smaller when compared to
another population from the state of São Paulo, southeastern Brazil (see Pombal Jr. et
al., 1995). However, it was not different from one population from the state of Goiás,
central Brazil (see Bastos et al., 2003a). The description presented by Bokermann
(1967) for the advertisement call of one species in the Municipality of Rio de Janeiro,
treated as Hyla fuscomarginata, refers to the advertisement call of Scinax alter (see
Izeckshon and Carvalho e Silva, 2001 for the occurrence of S. alter and the absence of
S. fuscomarginatus in the municipality of Rio de Janeiro).
Therefore, besides taxonomic misunderstandings, the differences observed
among the different studies may reflect populational divergences, already described for
S. fuscomarginatus (see Bueno, 2001; Bueno et al., 2002) and other anuran species (e.g.,
Cardoso and Haddad, 1984; Heyer and Reid, 2003). However, the acoustic differences
observed could be an artifact generated, or attenuated if the differences really exists, due
to different calling analysis methodology (e.g., different softwares), or due to different
recording equipment used (e.g., different microphones, recording tapes, or recorders)
40
(Balmires et al., 1997; Bastos et al., 2003a). Moreover, in our study always more than
10 individuals were present at the chorus during the recordings, while on the recordings
made by Pombal Jr. et al. (1995) only two individuals were calling. Hence, there are
differences in the social circumstances on which the recordings were made, which may
result in acoustic variation (see Wells, 1988).
The territorial call seemed to maintain the spatial segregation among males
present at the breeding site, as reported for other anuran species (e.g., Brenowitz and
Rose, 1999). This call was emitted in the beginning of the calling activity, and could
indicate the delimitation of a territory to be occupied and defended throughout the night.
Further emissions of territorial calls were heard only when males invaded other
territories, generally finishing by the intruder departure (see Chapter 2). These
observations reveal the efficiency of this kind of vocalization, which can prevent fight
during agonistic interactions (Wells, 1988; Chapter 2). Fighting may cause serious
injuries to anurans including death and have elevated energy costs (Kluge, 1981;
Martins and Haddad, 1988). Escalated aggressive behavior, also observed in S.
fuscomarginatus (Chapter 2), is a mechanism widespread among anuran amphibians,
especially in hylids (e.g., Brenowitz, 1989; Bastos and Haddad, 1995; Martins et al.,
1998).
We were unable to identify any social context associated to the emission of the
sporadic call. However, since these calls were always emitted at the beginning of the
calling activity, at the end of it, and during the day, allied to the fact that its physical
structure is similar to the advertisement call, we suggest that the sporadic call is am
attempt of the males to produce advertisement calls, which is hindered by an adequate
state of the vocal chords (Haddad, 1987). The sporadic calls produced in the beginning
of the night would be a consequence of the quiescent state of the vocal chords after
41
many hours of inactivity. At the end of the calling activity the sporadic calls were
emitted only when few individuals were still calling. Therefore, the production of
sporadic calls at that moment could be done by males that were not calling for an hour
or a few hours, time enough to make the vocal chords quiescent. Similar callings were
reported to Hyla minuta (Haddad, 1987) and H. faber (Martins and Haddad, 1988), but
in the second case they were named as “initial call”, because they were heard just in the
beginning of the calling period.
Although the social context of the emission of fighting calls is clear (see also
Chapter 2), it was not possible to demonstrate its function. There are reports that this
call is associated to the escalated aggressive behavior observed during agonistic
interactions (e.g., Bastos and Haddad, 1995; Martins et al., 1998), however there are no
demonstrations for such speculation and its function remain unclear.
The correlation observed between SVL and body mass vs. advertisement call
dominant frequency reinforces the indication that there is a negative correlation between
size and mass vs. calling frequency in anurans (Robertson, 1986; Given, 1987; Sullivan,
1982; 1992; Guimarães and Bastos, 2003). This correlation is originated by the
difference of the laryngeal components of individuals of different sizes (Martin, 1972).
Hence, it is possible that many of the calling site intruders evaluate the opponent’s
condition by its advertisement call frequency (Robertson, 1986) and leave before any
physical or even acoustic interaction (Martins et al., 1998; Chapter 2).
Vocalizations in anurans, especially advertisement calls, are related to the
reproductive success of the calling individual, since they attract mature females and
repel competitive males in the vicinity (Haddad, 1995; Bastos and Haddad, 2002). In
this context, three strategies were used by males of Scinax fuscomarginatus at EEI: (I)
calling males divided the physical environment, showing preference for distances much
42
larger than the distance in which agonistic interactions were observed (see Chapter 2);
(II) nearby males emitted advertisement calls in antiphony; and (III) males increased
their calling rate when a higher number of males were present at the chorus. The first
strategy avoids interception of attracted females by opportunistic males (e.g., Haddad,
1991). The first and second strategies reduce the probability of signal overlap among
calling males (Dyson and Passmore, 1992; Bastos and Haddad, 1999). The third
strategy increases the advertisement call overlaps most of the time; however, it also
increases the amount of acoustic information available for females (Bastos and Haddad,
1995) and increases the chances of emitting calls during some short silent periods of the
chorus. Hence, these three strategies increase the chances of calling males of attracting
females (Wells and Schwartz, 1984; Wells, 1988), and at least the first and the second
strategies reduce the competition among conspecifics (Wollerman, 1999).
ACKNOWLEDGMENTS.—We are grateful to Denis O. V. Andrade, Marcos G. Papp, and
Luís O. M. Giasson for the discussion and suggestions on early versions of the
manuscript; Débora Y. Campos, Bruna Franco, and João Giovanelli for helping on field
activities; Denise Zancheta for the access permission to the Estação Ecológica de
Itirapina; IBAMA and IF for the licenses conceded (license n. 026/02 – RAN–IBAMA,
proc. n. 02001.002893/02-61 and autos n. 41.012/02 – COTEC letter 471/2002,
respectively); IDEA WILD for equipment donation; CNPq (proc. n. 130417/2003-3) for
the Masters’ scholarship and FAPESP (proc. n. 01/13341-3) and CNPq for granting the
Herpetology lab.
43
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49
Chapter 2
REPRODUCTIVE BIOLOGY AND CHORUS ORGANIZATION IN SCINAX
FUSCOMARGINATUS (ANURA, HYLIDAE)
LUÍS FELIPE TOLEDO and CÉLIO FERNANDO BAPTISTA HADDAD
50
AMPHIBIA–REPTILIA
REPRODUCTIVE BIOLOGY AND CHORUS ORGANIZATION IN
Scinax fuscomarginatus (ANURA, HYLIDAE)
Luís Felipe Toledo1 and Célio Fernando Baptista Haddad1
1Departamento de Zoologia, Instituto de Biociências, Universidade Estadual Paulista,
Caixa Postal 199, CEP 13506-970, Rio Claro, Brasil. E-mail: [email protected]
Corresponding author: LFT: [email protected]
Running title: Reproductive biology of S. fuscomarginatus
51
Abastract
Reproduction is one of the most studied aspects of the natural history of
Neotropical anurans. Likewise, the present study investigated the reproductive biology
of Scinax fuscomarginatus in one of the last Cerrado fragments of the state of São
Paulo. Naturalistic observations were made between September 2002 and March 2004
at Estação Ecológica de Itirapina (EEI), state of São Paulo, southeastern Brazil.
Reproduction occurred in lentic and temporary water bodies. The species exhibited a
prolonged breeding pattern and a lek mating system. Males were smaller than females
and defended territories by means of acoustic, visual, and physical interactions. Winner
males were residents, but they did not differ in size and mass from the intruders males.
Satellite behavior was observed, but none female or amplected couple interception was
registered. The number of males at the chorus was always higher than the number of
females, generating low operational sex ratios. Scinax fuscomarginatus presented the
generalized reproductive mode in which the eggs are laid in the water and the tadpoles
are aquatic. The amplex was axillary and the eggs were deposited at the bottom of
temporary ponds. Oocytes, egg-masses, and eggs were described. Egg size,
pigmentation, and shape seems to be associated to the biotic and abiotic characteristics
of the microhabitat of deposition and are thought to afford protection against ultraviolet
radiation, predation, and permitting egg respiration in hypoxic environments.
52
Introduction
Studies with anurans in natural environment in the Neotropics have focused
mainly on the reproductive biology of the species (e.g., Martins, 1988; 1993; Haddad
and Cardoso, 1992; Freitas et al., 2001; Wogel et al., 2002; Guimarães and Bastos,
2003). These studies usually describe the reproductive season of the populations,
generally based on the calling activity of adult males (e.g., Pombal Jr., 1997; Bernarde
and Machado, 2001) and juveniles (Lampert and Linsenmair, 2002), and comment
about the abiotic factors that might influence the patterns of reproductive activity
(Aichinger, 1987). Some detailed studies investigated factors that might be involved in
sexual selection, verifying quantitative reproductive aspects and size-fecundity
relationships (e.g., Prado et al., 2000; Bastos and Haddad, 2001).
Territoriality of males is another commonly studied aspect of the reproductive
biology of anurans, including agonistic interactions for limited resources, such as
calling sites, egg laying sites, and/or females (Wells, 1977a; 1978; Cardoso and Haddad,
1984; Martins et al., 1998; Bastos and Haddad, 1995; 2002). Studies on reproductive
biology conducted on Neotropical anurans show that mates are not formed by chance,
being defined through female selection, or as a result of the aggressive interactions
among males (Arak, 1983, Ryan, 1985; Olson et al., 1986; Wagner and Sullivan, 1992;
Brenowitz and Rose, 1999). Therefore, sexual selection may be a causal factor to the
size sexual dimorphism found in the majority of the anuran species (Shine, 1979).
Sexual dimorphism is caused by the difference between the sum of all selective
pressures that affects males’ characteristics and the sum of all selective pressures that
affects females’ characteristics (Ralls, 1976). In relation to length and mass, the main
explanations leading to sexual dimorphism are: (I) selective pressure for the fecundity
53
increment of the female, that results in body size enlargement (Crump, 1974; Shine,
1979); (II) selective pressure for the increase of male body size as a consequence of
aggressive interactions (Davies and Halliday, 1977; Shine, 1979; Katsikaros and Shine,
1997); (III) higher mortality rate of males, not permitting them to reach the same age
and, consequently, the same size of females (Shine, 1979; Monnet and Cherry, 2002);
and (IV) different growing rates between the sexes (Halliday and Verrell, 1988).
Most species in the genus Scinax Wagler 1830 exhibit sexual dimorphism in
size, where females are generally larger than males (Lutz, 1973; Heyer et al., 1990). The
genus is also characterized by having diverse reproductive patterns (Haddad et al., 1990;
Bourne, 1992; Bevier, 1997; Toledo et al., 2003). Scinax rizibilis lays eggs on foam
nests (Haddad et al., 1990), and few other species of Scinax lay eggs in lotic water
bodies (e.g., S. albicans and S. trapicheiroi: Carvalho e Silva and Carvalho e Silva,
1994). However, in the majority of the species, females lay their eggs in lentic aquatic
environments where the tadpoles grow (Lutz, 1973: Haddad et al., 1990; Bourne, 1992;
Bevier, 1997; Toledo et al., 2003), the basal reproductive mode proposed by Duellman
(1985). In regard to the reproductive pattern (sensu Wells, 1977a), there are Scinax
species with the explosive reproductive pattern [e.g., S. fuscovarius: Bertoluci, 1998;
Toledo et al., 2003; S. ruber: Bourne, 1992; Bevier, 1997; Scinax sp. (aff. similis):
Toledo et al., 2003] and species that exhibit the prolonged reproductive pattern (e.g., S.
albicans: Carvalho e Silva & Carvalho e Silva, 1994; S. boulengeri: Bevier, 1997; S.
rizibilis: Bastos and Haddad, 1999; S. centralis and S. fuscomarginatus: Bernarde and
Kokubum, 1999; Bastos et al., 2003).
Scinax fuscomarginatus is characterized by males that join around permanent or
temporary ponds for reproduction, using the boundary vegetation as calling sites (see
Chapter 1; Lutz, 1973; Bernarde and Kokubum, 1999; Rossa-Feres and Jim, 2001;
54
Bastos et al., 2003). Only the advertisement call of this species is currently known
(references in Chapter 1) and its reproductive effort relationships have been discussed
before (Prado and Haddad, 2003). It is also known that S. fuscomarginatus lay their
eggs directly on lentic water bodies (Bastos et al., 2003), and that its larval development
has been described previously (as Hyla parkeri in Vizoto, 1967; and as Ololygon
fuscomarginata in Altig and Johnston, 1986). Finally, there are anecdotal reports about
adult predation by leeches (Brandão and Garda, 2000) and about the variety of
defensive behaviors presented by adult males (Toledo, in press).
Herein, we studied the reproductive biology of S. fuscomarginatus through the:
(I) description of the spatial and temporal organization of the individuals at the breeding
site; (II) characterization of the behaviors associated to reproductive biology, such as:
pair formation; aggressive interactions among males; and satellite males behavior; (III)
verification of quantitative aspects of reproduction, such as: fecundity, reproductive
effort of females, and sexual dimorphism; and (IV) characterization of the egg-masses
and its arrangements.
55
Methods
Study area
The present study was carried out at the Estação Ecológica de Itirapina (EEI),
located on the municipalities of Itirapina and Brotas, central São Paulo State,
southeastern Brazil. The EEI has approximately 230 km2 of natural vegetation,
including at least five distinct Cerrado physiognomies (Martins, 2001). On the
physiognomies of “campo sujo” and “campo limpo” it is common the formation of
lentic and temporary ponds, with the water temperature varying from 20 to 45 ºC (pers.
obs.). These water bodies are formed essentially during the summer (between
November and March) and make possible the reproduction of several anuran species,
including Scinax fuscomarginatus (Toledo, 2003).
Data collection
Field trips, lasting from four to 10 consecutive days, were made between
September 2002 and March 2004. Observations began one hour before the sunset and
finished when the calling activity decreased considerably. During the observations, head
flashlights were used, avoiding that the central focus of illumination reached directly the
animals. The following sampling methods were used for individual and intraspecific
behavior observations: “ad libitum”, “focal-animal”, “all occurrences of some
behaviors”, and “sequences” (Altmann, 1974; Lehner, 1996).
Individuals were weighted with 0.05 g of precision and the snout-vent length
(SVL) was measured with a caliper to the nearest 0.05 mm. The following parameters
were registered: air temperature, observation time, distance to the nearest conspecific
56
individual, distance and height of each individual from the pond, sex, and presence or
absence of ovules in the females. For individual recognition, the animals were toe-
clipped following Powell and Knesel (1992), and released exactly at the same place
from where they were captured.
The operational sex ratios followed Emlen and Oring (1977): OSR = (number of
females at the pond) / (number of males at the pond + number of females at the pond).
The eggs were collected from clutches deposited by pairs maintained in plastic bags;
eggs were conserved in 5 % formalin between 48 and 72 hours after spawning. The eggs
were counted, measured, and classified according to the Gosner’s table (Gosner, 1960).
Statistical analysis
The homogeneity of variances and normality of the data set were verified. For
comparisons between mass and SVL of winner vs. loser males involved in agonistic
interactions, or between calling/dominant vs. silent/satellite males, we used a paired t
test. We used a t-Student test to compare distances among males present at the
reproductive aggregation. The comparison among male mass and size vs. female mass
and size was made with an U-test of Mann-Whitney. In all cases, significant values
were considered when P < 0.05 (Zar, 1999).
57
Results
The reproductive season of Scinax fuscomarginatus at Estação Ecológica de
Itirapina, based on the calling activity of males, lasted approximately three and a half
months, from December 2002 to March 2003, and from December 2003 to March 2004.
These periods coincided with the rainy and hot season of the year, as well as with the
presence of temporary lentic ponds (see Chapter 1). In the beginning of the reproductive
season, only males were observed at the reproductive aggregation. Females were found
only approximately 20 days after the beginning of the calling season. The first aquatic
larvae were found ca. 30 days after the beginning of the calling season in the same
ponds where the naturalistic observations took place. Metamorphic individuals were
found 40 and 50 days after the beginning of the calling season, holding on branches of
vegetation above the water or swimming in the ponds. Adult females after oviposition
were significantly larger, but not heavier, than adult males (table 1).
Table 1. Comparison of snout-vent length (SVL) and body mass between adult males and females of Scinax fuscomarginatus at Estação Ecológica de Itirapina, municipalities of Itirapina and Brotas, São Paulo State. Values expressed as mean ± standard deviation (range; N).
Males Females (after oviposition)
P U
SVL (mm) 22.21 ± 0.77 (20.0 – 24.0; 52)
23.17 ± 0.30 (23 – 23.7; 5)
0.003 251.2
Mass (g) 0.56 ± 0.07 (0.35 – 0.75; 51)
0.58 ± 0.06 (0.5 – 0.65; 5)
0.429 170.5
Males of S. fuscomarginatus used the edge vegetation of temporary ponds as
calling sites (see Chapter 1). Despite the apparently erratic distribution of the calling
sites around the temporary ponds (see fig. 2 in Chapter 1), 52% of the calling males
were found separated by 100 to 300 cm from each other. For distances equal or inferior
58
to 30 cm, direct interactions between males were observed (fig. 1). Hence, The calling
territory has approximately 60 cm in diameter. Inside the territory of a resident male
two sorts of interactions were identified: (I) while the dominant male was calling, one or
two other males assumed a submission posture, remaining silently as satellite males; or
(II) the resident male defended its calling site by means of aggressive behaviors, and if
the intruder did not respect the aggressive signs the interaction could end in physical
combats (fig. 2).
Figure 1. Distance between Scinax fuscomarginatus nearest males at Estação Ecológica de Itirapina during the calling activity. White bars represent distances where satellite males or agonistic interactions were observed; grey bars represent the distances when solitary males were observed calling without occurrence of agonistic interactions (N = 56).
0
5
10
15
20
25
10 20 30 40 50 60 70 80 90 100 200 300 400 >400
Distance between males (cm)
Obs
erva
tions
(%)
59
Figure 2. Schematic summary of the agonistic interactions between adult males of Scinax fuscomarginatus at Estação Ecológica de Itirapina, São Paulo state, southeastern Brazil.
When its territory was invaded, the resident male turned towards the intruder and
started to emit territorial calls (calls described in Chapter 1). If the intruder did not
assume a submission posture, as satellite male, both males initiated an acoustic
confront. First, the intruder could emit few advertisement calls (described in Chapter 1),
but soon began to emit territorial calls. Males called intensively, although silent periods
of up to 30 seconds occurred, the acoustic confront restarted when one of the males
called again. During the calling contest, both resident (N = 1) and intruder (N = 1),
could perform rapid extension and contraction of arms and legs.
Loser male moves away (n = 5)
Intruder assumes submission posture (satellite behavior)
with its vocal sac deflated and with its belly touching the
substrate (n = 5)
Both males call, advertisement and/or territorial calls (n = 4)
Resident male emit advertisement call (n = 7)
Males interact physically emitting
fighting calls (n = 2)
Resident male emitting advertisement calls
Silent intruder male invades resident’s territory (n = 8)
Resident male emit territorial calls (n = 8)
60
If the intruder did not move away, the resident male approached the intruder
giving short distance hops, starting the physical combat. During the combat, males gave
chest-to-chest hugs, with the heads oriented to the same direction, and both males
emitted fighting calls (see chapter 1). In two fights observed the loser male moved away
just after the combat. These combats lasted for 15 and 70 seconds.
Winner males were always the residents. These males were not significantly larger
(t = 1.23; df = 5; P = 0.273) nor heavier (t = 1.17; df = 5; P = 0.296) than intruders or
satellite males (table 2). Females were not observed defending territories or involved in
agonistic interactions.
Table 2. Mass and snout-vent length (SVL) of Scinax fuscomarginatus males (winners or dominants and losers or satellites) of the agonistic encounters observed at the Estação Ecológica de Itirapina, state of São Paulo, Brazil. Values of SVL and mass are expressed as mean ± standard deviation (range; N). In only one combat the males were captured, measured, and weighted.
Encounters without combat Encounters with combat SVL (mm) Mass (g) SVL (mm) Mass (g)
Winners or dominants
22.2 ± 0.74 (21.0 – 23.0; 5)
0.57 ± 0.06 (0.5 – 0.65; 5)
21.9 0.6
Losers or satellites
22.4 ± 1.48 (20.0 – 24.0; 7)
0.55 ± 0.08 (0.45 – 0.7; 7)
21.8 0.6
Satellite male behavior was observed in few occasions, on which one male
(dominant male) emitted advertisement calls, and one (N = 5) or two other males (N =
1) remained in submission posture, with the head and belly touching the substrate, and
with the vocal sac deflated (satellite males). On three occasions, the dominant males
were removed by the observer and after two to four minutes after the removal of the
dominant male, the satellite males began to emit advertisement calls. Satellite males
were observed independently of chorus density and approximation of females to groups
of dominant and satellite males was not observed.
61
Throughout the study, only nine females were observed, five of which were
captured. The operational sex ratio obtained for nights with presence of females were
0.083 in average (SD = 0.053; range = 0.025 – 0.143; N = 6 nights). Two females with
ovules in different stages of development were captured near to the temporary ponds in
January 2003; only females with mature ovules were found in the breeding site moving
toward calling males (fig. 3A). Gravid females were also observed motionless for up to
four minutes in front of calling males, head oriented toward them (fig. 3B). After that,
females were observed moving toward the nearest male, or in the direction of other
males in the vicinity. When the male perceived the presence of a female, he moved to
her, emitting courtship calls with short duration and low energy intensity (not recorded)
(N = 1). When the male was less than 10 cm from the female, he jumped on the
female’s dorsum, and amplected her axillary (fig. 3C).
During the amplexus the male remained with his ventral region totally in contact
with the dorsal surface of the female. With his arms, the male performed arrhythmic
contractions on the female’s flanks, in a rate of six to eight per minute. Pair formation
occurred after 0159 h, in average, after the sunset (range = 0105 h – 0225 h; N = 4).
Between 0230 h and 4h after the amplexus, the female moved down from the vegetation
branches to the pond’s water level (mean = 0315 h; N = 4). Afterward, the female with
the amplected male jumped into the water and remained fluctuating on the water surface
or resting on the emerging branches of the aquatic vegetation for approximately five
minutes (fig. 3D). Subsequently, the pair dived and remained submerged for 20 seconds
at most, before return to water surface. These dives were repeated from four to six
times, when oviposition occurred, 0530 h, in average, after the sunset (range = 0445 h –
0605 h; N = 4). Then, still inside the water, the male released the female and the
62
individuals rapidly moved to the edge of the ponds, hiding on the closest vegetation
clump (N = 3).
Figure 3. Pair formation and egg-laying sequence of Scinax fuscomarginatus at Estação Ecológica de Itirapina, São Paulo state, southeastern Brazil. A) Calling male; B) female oriented toward a calling male; C) axillary amplected pair; D) amplected pair resting at the vegetation on the water surface of a temporary pond (indicated by an arrow).
Gravid females had a mean of 346 ovules in their ovaries (SD = 33.5; range =
316 – 382; N = 4), with approximately 0.82 mm in diameter (SD = 0.07; range = 0.74 –
0.93 mm; N = 12). Ovules were black on the animal pole and beige on the vegetative
pole (fig. 4A). The egg-mass is formed by a single and circular layer of eggs, whose
coloration and diameter was similar to those of the ovules. Eggs had two concentric
gelatinous capsules (absent in the ovules). Eggs at stage 13 had a mean diameter of 0.98
mm (SD = 0.07; range = 0.86 – 1.08 mm; N = 18). The inner gelatinous capsule had a
mean diameter of 1.17 mm (SD = 0.04; range = 1.13 – 1.19 mm; N = 6) while the outer
AA
DD CC
BB
63
capsule had a mean diameter of 2.65 mm (SD = 0.34; range = 2.22 – 3.33 mm; N = 8)
(fig. 4B). When submerged in water, the eggs remained with the animal pole upwards.
Figure 4. A) Mature ovules in the ovaries; and B) fertilized egg of Scinax fuscomarginatus of the Estação Ecológica de Itirapina, São Paulo state, Brazil. The arrows show the external limits of the inner (I) and outer (O) gelatinous capsules.
Four amplected pairs were measured and weighted. Male body mass
corresponded to 65.17% of the female body mass after egg-laying (SD = 4.25; range =
62.5 to 71.43%). Male SVL corresponded to 95.76% of the female SVL (SD = 2.45;
range = 93.3 – 99.13%). The mass of ovules represented 37.13% of the mass of the
females after oviposition (SD = 9.72; range = 23.08 – 45.45 %; N = 4). A mean of
86.22% of the eggs were fertilized (SD = 11.19; range = 75.63 – 97.94%; N = 3).
AA BB
I
O
64
Discussion
Scinax fuscomarginatus at the EEI exhibited a series of characteristics that defines
this species as a prolonged breeder (sensu Wells, 1977a): extended reproductive season,
at least three months long; calling as the unique form for female attraction; lack of
active searching for females, lack of attempts to dislodge amplected males; and males
that defend territories (calling sites) by means of acoustical, visual, and physical
aggressive interactions.
The reproductive system of S. fuscomarginatus is here classified as lek, in
concordance with the criteria proposed by Bradbury (1981). Such classification is based
on: (1) there was no parental care; (2) males formed exhibition arenas around temporary
ponds; (3) females moved around the arena having the opportunity for sexual selection,
evaluating acoustic displays produced by males; and (4) the calling site did not grant
any required resource by females, besides the own male. Besides this, the lek system of
reproductive choruses is proposed to occur in species that: (I) have prolonged breeding
patterns, on which females attend the choruses in an asynchronic manner, while males
remain in reproductive activity (calling) during all reproductive season of females; (II)
have low operational sex ratios; and (III) males are incapable to control essential
resources for females (Emlen and Oring, 1977). Since the reproductive aggregations of
Scinax fuscomarginatus fits on these criteria, the reproductive system of this species can
be considered as leks, as reported for other hylid species (e.g., Hyla elegans: Bastos and
Haddad, 1996; H. minuta: Haddad and Cardoso, 1992; Scinax rizibilis: Bastos and
Haddad, 1999; S. ruber: Bourne, 1977).
65
Adult males of S. fuscomarginatus are territorial, defending its calling sites. Use of
calling and apparent visual signalization (rapid movements of the limbs) seemed to be
efficient as an aggressive signalization. Accordingly, few physical combats were
observed during the reproductive seasons. The use of acoustic and visual signs (e.g.,
Pombal Jr. et al., 1994; Haddad and Giaretta, 1999) and the escalated aggressive
behavior (e.g., Martins and Haddad, 1998; Bastos and Haddad 1995; 2002) may be
considered adaptive since physical combats results in elevated energetic costs (see
Robertson, 1986; Bevier, 1997) and may lead to lethal injuries or attract predators
(references on Martins et al., 1998). The scarcity of physical interactions observed can
also be related to the high availability of calling sites at the studied ponds.
The absence of differences in mass and SVL between dominant and satellite males
may be related to the small sample size, and/or to the low precision of the scale used in
the field (see discussion below). Winner males of the territorial interactions were also
the resident males, a recurrent situation among hylids, probably because resident males
show better physical conditions when compared to the intruders (references in Bastos
and Haddad, 2001) or satellite males (see Robertson, 1986; Haddad, 1991; Guimarães
and Bastos, 2003).
Satellite behavior was rare at the studied population and female interception by
satellite males was not observed. Therefore, satellite male behavior of S.
fuscomarginatus could be related to the dynamics of the chorus. They could be waiting
for the availability of calling sites, abandoned by dominant males (Wells, 1977b).
Alternatively, satellite males could be waiting for variations in the physical conditions
of dominant males, as there is considerable energetic costs in calling for consecutive
days (Bevier, 1997), promoting dominance alternation of a calling site (Robertson,
66
1986). However, these alternatives do not exclude the possibility of satellite males be
waiting to intercept females attracted by the dominant males.
Lack of difference between male and female body masses after oviposition could
be a natural situation, could be caused by the small sample size, or due to the low
precision of weighing scale used (de 0.05 g) when compared to the mean mass of adult
individuals of Scinax fuscomarginatus at EEI (ca. 0.57 g for both sexes). However, this
species differed in SVL with females larger than males. This dimorphism could be
related to an increment in female’s fecundity associated to the increment in SVL
(Crump, 1974; Shine, 1979) or could be related to different growing rates between the
sexes (Halliday and Verrell, 1988). The hypothesis of different mortality rates among
the sexes (Shine, 1979; Monnet and Cherry, 2002) is unlikely because S.
fuscomarginatus seems to have an annual life cycle, since there were no recaptures from
one reproductive season to the other. Therefore, all individuals that attended the chorus
should have the same age: ca. one year.
Pair formation behavior was similar to other hylid species, since males did not
wait for a female contact before the amplex (Morris, 1989; Bastos and Haddad 1996;
Haddad and Sawaya, 2000). It has been suggested that this behavior is a strategy to
avoid interception of the females by satellite or neighboring males (Arnold, 1976;
Haddad, 1991; Bourne, 1992). It has also been reported that hylid pairs that form above
vegetation remain practically motionless for a few hours until move down to the water
for oviposition (e.g., Bourne, 1992; Bastos and Haddad, 1996; present study). During
this period, the female could be receiving a stimulus for the oviposition (see Scarlata
and Murphy, 2003), such as the arrhythmic compression of its flanks by the amplected
male (present study). This could also be a strategy for waiting for the males on the
vicinity to stop the calling activity and/or leave the neighborhoods, reducing the chances
67
of pair interception and displacement of the amplected male (Bastos and Haddad, 1996;
1999).
The diameter of the eggs of S. fuscomarginatus is on the lower range of egg sizes
usually reported for anuran amphibians. To our knowledge, they are only larger than the
eggs of Hymenochirus boettgeri (Pipidae: 0.75 mm) and almost equal to the eggs of
Limnaoedus ocularis (Hylidae: 0.95 mm) (references in Duellman and Trueb, 1994).
Nevertheless, the eggs of S. fuscomarginatus have two relatively large gelatinous
external capsules, with the external layer having around 2.65 mm in diameter (for
comparisons see Duellman and Trueb, 1994). These two capsules may provide a better
spacing among individual eggs inside the whole egg-mass. Spacing may facilitate egg
oxygenation, since the eggs that are directly exposed to atmospheric air (i.e., eggs
deposited in foam nests or out of the water) generally have thin capsules (Salthe, 1963)
or only one capsule (pers. obs.).
Based on the egg-masses obtained in plastic bags, it is suggested that the eggs may
remain as a single layer on the bottom of temporary ponds, which reaches high
temperatures during the day. Therefore, egg-mass characteristics (single layer and
presence of two gelatinous capsules) may be adaptive in the habitats occupied by S.
fuscomarginatus, as has been suggested for species that reproduce in hypoxic
environments (see Seymour and Bradford, 1995). Furthermore, the pigmentation on the
upper surface of the eggs (animal pole) may protect them against ultraviolet radiation,
which may affect the development of the embryos (Duellman and Trueb, 1994). The
egg’s coloration also provides camouflage (Duellman and Trueb, 1994); since the
pigmented pole did not contrast with the bottom of the ponds where they were
deposited. This may hinder their localization by visually oriented predators.
68
Acknowledgments. Cynthia P. A. Prado and Denis V. Andrade made helpful
suggestions on previous versions of the manuscript; researches of EEI had contributed
in field activities; Denise Zancheta for the acess permition to the Estação Ecológica de
Itirapina; IBAMA (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais
Renováveis) and IF (Instituto Florestal) for the licences conceded (licence n. 026/02 –
IBAMA/RAN, proc. n. 02001.002893/02-61 and autos n. 41.012/02 –IF/COTEC letter
471/2002, respectivelly); IDEA WILD for equipment donation; CNPq (proc. n.
130417/2003-3) for the Master’s scholarship, and FAPESP (proc. n. 01/13341-3) for
granting the Herpetology lab.
69
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Considerações Finais
• Scinax fuscomarginatus apresentou um padrão reprodutivo prolongado,
reproduzindo-se por mais de três meses consecutivos.
• A população estudada de Scinax fuscomarginatus apresentou dimorfismo sexual
quanto ao comprimento rostro-cloacal, sendo que as fêmeas foram maiores que
os machos.
• Todas as fases do ciclo reprodutivo de S. fuscomarginatus ocorreram em lagoas
temporárias, sendo que as principais fases foram: vocalização dos machos para
atração de fêmeas; formação de casais; desova no fundo das lagoas;
desenvolvimento dos girinos até a metamorfose.
• Os machos emitiram, pelo menos, quatro tipos de vocalizações, com estruturas
físicas distintas: canto de anúncio, canto territorial, canto de briga e canto
esporádico. Foi também identificado, mas não gravado nem analisado, um
quinto tipo de vocalização: o canto de corte.
• A freqüência dominante do canto de anúncio variou com o comprimento rostro-
cloacal e a massa corpórea dos machos, podendo então ser utilizada como
parâmetro para seleção sexual pelas fêmeas, ou para a avaliação das condições
físicas por machos rivais.
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• As características do canto de anúncio da população estudada de S.
fuscomarginatus diferiram quando comparadas à outra população do Estado de
São Paulo, mas não diferiram quando comparadas a uma população do Estado
de Goiás.
• A taxa de vocalização dos machos variou ao longo da noite, acompanhando a
variação de densidade dos machos em atividade de vocalização presentes no
coro.
• Os machos foram territoriais e dividiram o espaço físico das lagoas através de
comunicação acústica, sinalização visual e interações físicas, havendo um
escalonamento de agressividade.
• Foi identificada uma distância preferencial entre os machos vocalizantes nas
lagoas (entre 1 e 3 m) e seus territórios de vocalização possuíam cerca de 60 cm
de diâmetro.
• Apesar da conspícua territorialidade dos machos de S. fuscomarginatus, alguns
indivíduos permitiram a presença de machos satélites, embora nenhuma
interceptação de fêmeas tenha sido observada.
• A desova de S. fuscomarginatus foi depositada no fundo de lagoas. Os ovos
possuíam pigmentação escura no pólo animal, o qual permaneceu orientado para
cima dentro da água. Além disso, os ovos fecundados possuíam duas cápsulas
gelatinosas. Essas características podem ser adaptativas, visto que podem
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conferir proteção contra predadores visualmente orientados e permitir melhor
oxigenação aos embriões.