Programa de Pós-graduação em Diversidade Animal
Universidade Federal da Bahia
Joice Ruggeri Gomes
Descrição e análise comparativa de larvas do
gênero Physalaemus Fitzinger, 1826 (Amphibia,
Anura, Leiuperidae)
Salvador 2011
ii
Joice Ruggeri Gomes
Descrição e análise comparativa de larvas do gênero
Physalaemus
Fitzinger, 1826 (Amphibia, Anura,
Leiuperidae)
Dissertação apresentada ao Instituto de Biologia da Universidade Federal da Bahia para a obtenção do Título de Mestre em Zoologia pelo Programa de Pós-graduação em Diversidade Animal.
Orientador: Luiz Norberto Weber
Coorientador: Marcelo Felgueiras Napoli
Salvador 2011
iii
Sistema de Bibliotecas - UFBA Gomes, Joice Ruggeri.
Descrição e análise comparativa de larvas do gênero Physalaemus Fitzinger, 1826 (Amphibia, Anura, Leiuperidae) / Joice Ruggeri Gomes. - 2011.
136 f. : il.
Inclui Apêndices e anexos.
Orientador: Prof. Dr. Luiz Norberto Weber. Co-orientador: Prof. Dr. Marcelo Felgueiras Napoli.
Dissertação (mestrado) - Universidade Federal da Bahia, Instituto de Biologia, Salvador, 2011.
1. Anuro. 2. Girino. 3. Morfologia. 4. Physalaemus. I. Weber, Luiz Norberto. II. Napoli, Marcelo Felgueiras. III. Universidade Federal da Bahia. Instituto de Biologia. IV. Título.
CDD - 597.8
CDU - 597.8
v Epígrafe
“A mente que se abre a uma nova idéia nunca voltará ao seu tamanho original”
Albert Einstein
vi Agradecimentos
Quero agradecer muito à minha família, que tanto me apóia e incentiva, em especial à
minha mãe, meu pai, minha avó e minha irmã Raquel! Amo muito vocês!
Ao Profº. Dr. Luiz Norberto Weber, meu orientador, agradeço pela amizade, paciência, cuidado, além da fundamental orientação em minha trajetória.
Ao Profº. Dr. Marcelo Felgueiras Napoli, meu co-orientador, por quem tenho muito respeito e confiança.
Ao Profº Dr. Sergio Potsch de Carvalho-e-Silva, por me aceitar no LAR e me incentivar a estudar sapos! Não estaria aqui não fosse por ele!
A todos os professores do Programa da Pós-graduação em Diversidade Animal da UFBA, profissionais competentes que muito contribuíram para a minha formação, e a Marinalva, secretária do programa. Um agradecimento especial aos professores Adolfo Calor e
Angela Zanata pelos “puxões de orelha” bem dados que me fizeram crescer muito como
aluna e pessoa.
À FAPESB pela bolsa concedida!
Aos meus grandes e amigos para toda a vida: Poline, Elisa e Nathy; Anita (Ana Luísa),
Carla (Carlinha, Carlão), Cordeirinho (André), Paula (“grrrell”), Cyro e André (Clone), obrigada por estarem presentes mesmo tão longe!
Aos meus novos amigos (que sejam eternos enquanto dure... e que dure para sempre!):
Bal, Pri, Nai e Lais, obrigada por tornarem essa jornada mais fácil. Com certeza aprendi e
cresci muito com vocês (viu, Pri?!).
Amigos e colegas do AMPHIBIA (Ariane, Deise, Euvaldo, Emanuela, Jocilene, Lucas,
Maria, Milena, Patricia, Rafael, Tamiris, Thais e os novatos Camila e Robson),
obrigada por tudo, mesmo!
Lucas Menezes Silva (Kias) e Ana Carolina Guedes: agradeço a paciência de vocês
perante meu desespero com o tempo. Obrigada pelo capricho dos desenhos!
Quero agradecer aos meus primeiros amigos “sapólogos” que me ensinaram muito e realmente me fizeram sentir em casa – no LAR
Além de todos os amigos e colegas da Pós em Diversidade Animal (Conseguimos, gente!)
Não posso deixar de agradecer também a Sabrina e ao Conradinho por terem me acolhido em Barreiras e me emprestando muito mais do que um quarto! E a Vaneide,
vii
Edu, Vanessa e Luciano e família por terem sido tão prestativos e facilitarem a minha
estadia em Salvador!
Quero agradecer a todas as pessoas que diretamente me ajudaram durante meu percurso:
Sergio, Marcia, Cyro, Fabio e Marcelle Mongin (UFRJ), Marianna Oliveira (UFBA), Rodrigo Salles e Marcelo Gomes (MNRJ), André Tacioli (UNESP – Rio Claro), Diogo Provete (UNESP – São José do Rio Preto) e Pedro Romano (UFV).
Aos curadores das coleções zoológicas da UFBA (Dr. Marcelo Felgueiras Napoli),
UFRJ (Marcia dos Reis Gomes), MNRJ (Dr. José Perez Pombal Junior), UNESP (Dr. Célio F. B. Haddad e Dra. Denise de Cerqueira Rossa Feres) pelo empréstimo de
material.
A todas as pessoas que passaram pela minha vida e me tornaram quem eu sou, obrigada!
viii Índice Apresentação 10 Resumo 11 Abstract 12 Introdução geral 13 - Revisão histórica 13 - Caracterização morfológica 17
Capítulo I. Description of the oral cavity anatomy of the tadpoles in the genus Physalaemus Fitzinger, 1826 (Amphibia, Anura, Leiuperidae) 21
Abstract 22 Introduction 23 Material e methods 23 Results 25 Discussion 32 References 35 Figures 41 Tables 47
Capítulo II. Morphological comparison between tadpoles of the genus Physalaemus Fitzinger, 1826 (Amphibia, Anura, Leiuperidae) 49
Abstract 50 Introduction 51 Material e methods 52 Results 53 Discussion 61 References 67 Figures 75 Tables 82 Appendix 84
Capítulo III. The tadpole of Physalaemus angrensis Weber, Gonzaga and Carvalho-e-Silva, 2005 (Amphibia; Anura; Leiuperidae) 87
Abstract/Resumo 89
ix
Introduction 90
Material and Methods 90
Results 91 Discussion 92 References 95 Figure Legends 99 Figures 100 Tables 102
Capítulo IV. The tadpole Physalaemus albifrons (Spix, 1824) (Anura, Leiuperidae) 104 Conclusões gerais 111 Referências bibliográficas 113 Anexos I 120 Anexos II 124 Anexos III 131
10 Apresentação
Esta dissertação está dividida em Introdução Geral, seguida por quatro capítulos, Conclusões Gerais e Referências Bibliográficas. Na Introdução Geral, são apresentadas considerações gerais referentes aos capítulos que a sucedem, bem como os objetivos da dissertação. Os capítulos são apresentados sob forma de manuscritos e artigos e seguem as normas do periódico aos quais foram ou serão submetidos. As Conclusões Gerais são referentes a todos os capítulos anteriores e as Referências Bibliográficas, ao final, contêm as citações que aparecem apenas na Introdução Geral.
11 Resumo
Na última revisão taxonômica do gênero Physalaemus Fitzinger, 1826, baseada em características morfológicas de espécimes adultos, foi sugerida que as espécies fossem alocadas em sete grupos de espécies (grupo de Physalaemus albifrons, grupo de P. cuvieri, grupo de P. deimaticus, grupo de P. gracilis, grupo de P. henselii, grupo de P. olfersii e grupo de P. signifer). Atualmente o gênero é composto por 45 espécies das quais 27 apresentam suas larvas descritas e para apenas dez são apresentadas descrições da morfologia oral interna. Visando contribuir para a resolução de problemas taxonômicos e sistemáticos, o objetivo principal deste estudo descrever e comparar larvas do gênero
Physalaemus utilizando-se de caracteres da morfologia externa, oral externa e oral interna.
No primeiro e segundo capítulos, as larvas de P. albifrons e P. angrensis são descritas. No terceiro capítulo, a morfologia oral interna de 11 espécies é estudada, descrita e comparada. No quarto capítulo, uma análise comparativa da morfologia externa, oral externa e oral interna de 20 larvas é feita. A partir da análise de cluster (UPGMA), utilizando como distância o índice de Gower, obteve-se grau de dissimilaridade de 45% entre os girinos amostrados. Os girinos de P. angrensis, P. camacan, P. signifer e P.
spiniger formaram um grupo distinto, compartilhando muitos carcateres, corroborando o
grupo morfológico proposto (grupo de Physalaemus signifer). Além disso, as larvas de P.
crombiei e P. gracilis são muito semelhantes quanto a todos os aspectos morfológicos. Os
girinos de P. signifer e P. jordanensis são os mais semelhantes quanto à morfologia externa; por outro lado, em relação à morfologia oral interna, P. signifer é muito semelhante à de P. angrensis, e os girinos de P. jordanensis compartilham poucos caracteres com as espécies.
12
Abstract
In the latest taxonomic review of the genus Physalaemus Fitzinger, 1826, based on morphologic characteristics of the adults, it was suggested that all species were allocated into seven different species groups (Physalaemus albifrons group, P. cuvieri group, P.
deimaticus group, P. gracilis group, P. henselii group, P. olfersii group e P. signifer
group). The genus currently comprises 45 species which 27 have the tadpoles described, although only ten with information upon the internal oral morphology. In order to help on resolutions of taxonomic and systematic problems, the main objective of this study is to describe and compare the tadpoles in the genus Physalaemus by using characters of the external morphology, oral morphology and internal oral morphology. In the first and second chapters, the tadpoles of P. albifrons and P. angrensis are described. In the third chapter, the internal oral morphology from 11 tadpoles are studied, described and compared. In the fourth chapter, the comparative analysis of the external morphology, oral morphology and internal oral morphology among 20 tadpoles is provided. The UPGMA based on Gower’s distance showed that tadpoles in the sample have about 45% of dissimilarity. Physalaemus angrensis, P. camacan, P. signifer and P. spiniger, formed a distinct group, sharing many features, which corroborates the morphological group proposed (Physalaemus signifer group). Furthermore, the tadpoles of P. crombiei and P.
gracilis are very similar regarding to all morphological aspects. The tadpoles of P. signifer
and P. jordanensis are the most similar regarding to the external morphology; on the other hand, regarding to the internal oral morphology, P. signifer is very similar to P. angrensis, and the tadpoles of P. jordanensis share very little characters with the other species.
13 Introdução geral
- Revisão histórica
A família Leptodactylidae até recentemente era divida em cinco subfamílias: Ceratophryinae, Cycloramphinae, Eleutherodactylinae, Leptodactylinae e Telmatobiinae, algumas não claramente monofiléticas e algumas que poderiam inclusive ser polifiléticas (Frost et al. 2006). Visando entender as relações sistemáticas e filogenéticas desta e outras famílias, Frost et al. (2006) combinaram caracteres morfológicos e moleculares de adultos e larvas das espécies de anfíbios anuros e estabeleceram uma nova taxonomia para Lissamphibia. Algumas das mudanças relacionadas à família Leptodactylidae Werner, 1896, são: o gênero Eleutherodactylus foi incluído na família Brachycephalidae Günther, 1858; Cycloramphinae foi elevado à categoria de família (Cycloramphidae); inclusão de Batrachylinae, Ceratophryinae e Telmatobiinae na família Ceratophryidae Tschudi, 1838; e a retirada dos gêneros Edalorhina, Engystomops, Eupemphix, Physalaemus, Pleurodema,
Pseudopaludicola e Somuncuria desta família, criando-se uma nova família, a família
Leiuperidae Bonaparte, 1850.
Atualmente, a família Leiuperidae compreende 79 espécies distribuídas em sete gêneros: Physalaemus Fitzinger, 1826 (45 spp.), Edalorhina Jiménez de la Espada, 1870 (2 spp.); Engystomops Jiménez de la Espada, 1872 (9 spp); Eupemphix Steindachner, 1863 (1 sp.); Pleurodema Tschudi, 1838 (15 spp.); Pseudopaludicola Miranda-Ribeiro, 1926 (12 spp.) e Somuncuria Lynch, 1978 (1 sp.) (Frost, 2011). O gênero Physalaemus é constituído por pequenas rãs distribuídas do Norte à Argentina Central, Leste da Bolívia, Paraguai, Uruguai, Brasil, Guianas, baixadas do Sul da Venezuela, Sudeste da Colômbia, e Oeste do Equador (FROST, 2010) e se caracteriza por construir ninho de espuma (Lynch, 1971) – Modo reprodutivo 11 (Haddad & Prado, 2005).
Lynch (1970) revisou os gêneros Physalaemus, Engystomops e Eupemphix e com base em análises de esqueleto e morfologia externa os colocou em sinonímia. Ele organizou as 35 espécies do gênero Physalaemus em quatro grupos de acordo com semelhanças em caracteres morfológicos externos: grupo de espécies de P. biligonigerus, grupo de espécies de P. cuvieri, grupo de espécies de P. pustulosus e grupo de espécie de
P. signifer.
Mesmo a validade desses grupos sendo freqüentemente questionada até 1999, o gênero Physalaemus possuía 38 espécies, sendo 36 pertencentes aos grupos propostos,
14 além de duas espécies que não apresentavam semelhanças morfológicas com as outras espécies, P. deimaticus Sazima & Caramaschi, 1988 e P. rupestris Caramaschi, Carcerelli & Feio, 1991. Nesse mesmo ano, uma nova espécie de Physalaemus é descrita (Feio et al., 1999) para Minas Gerais, Physalaemus maximus, e os autores sugerem que esta espécie, P.
aguirrei Bokermann, 1966, P. olfersii (Lichtenstein and Martens, 1856) e P. soaresi
Izecksohn, 1965 deveriam compor um único grupo devido as similaridades morfológicas e de hábitos. Assim como é sugerido na descrição de P. erythros (Caramaschi et al., 2003) que a espécie junto com P. deimaticus e P. rupestris também deveriam compor um grupo distinto.
Em 2005 Nascimento et al. fizeram uma revisão do gênero Physalaemus e revalidaram os gêneros Engystomops Jiménez-de-la-Espada, 1872, e Eupemphix Steindachner, 1863. As espécies de Physalaemus se distribuíram em sete grupos: grupo de espécie de Physalaemus cuvieri (9 spp.), grupo de espécies de P. signifer (10 spp.), grupo de espécies de P. albifrons (4 spp.), grupo de espécies de P. deimaticus (3 spp.), grupo de espécies de P. gracilis (5 spp.), grupo de espécies de P. henselii (3 spp.) e grupo de espécies de P. olfersii (4 spp.).
Após a revisão de 2005, três novas espécies pertencentes ao grupo de espécies de
Physalaemus signifer foram descritas: Physalaemus camacan Pimenta, Cruz, and Silvano,
2005, para o Sul da Bahia, P. angrensis Weber, Gonzaga, and Carvalho-e-Silva, 2005, para o município de Angra dos Reis, no Rio de Janeiro, e P. irroratus Cruz, Nascimento, and Feio, 2007, para Minas Gerais; e uma espécie do grupo de espécies de P. olfersii: P.
insperatus Cruz, Cassini, and Caramaschi, 2008, para o estado do Paraná. Recentemente,
Cassini et al. (2010) revisaram o grupo de P. olfersii e revalidaram P. lateristriga (Steindachner, 1864), além de descreverem duas espécies do grupo: P. feioi e P. orophilus.
Dentre as 45 espécies descritas para o gênero, 27 apresentam suas larvas descritas:
P. albonotatus (Kehr et al.,2004), P. aguirrei (Pimenta & Cruz 2004), P. atlanticus
(Haddad & Sazima, 2004), P. biligonigerus (Fernández & Fernández, 1921; como
Paludicola fuscomaculata), P. bokermanni (Cardoso & Haddad, 1985), P. caete (Pombal
& Madureira, 1997), P. camacan (Pimenta et al., 2005), P. centralis (Rossa-Feres & Jim, 1993), P. cicada (Vieira & Arzabe, 2008), P. cuqui (Perroti, 1997), P. cuvieri (Heyer et al, 1990), P. erythros (Baêta et al., 2007), P. fernandezae (Cei, 1980), P. gracilis (Langone, 1989), P. henselii (Cei, 1980), P. irroratus (Cruz et al.,, 2007), P. lisei (Both et al., 2006),
P. jordanensis (Gomes et al., 2010), P. maculiventris (Bokermann, 1963), P. marmoratus
(Nomura et al, 2003; como P. fuscomaculatus), P. maximus (Baêta et al., 2007), P.
15
riograndensis (Prigioni & García, 2001), P. rupestris (Nascimento et al., 2001), P. santafecinus (Perotti & Céspedez, 1999), P. signifer (Weber & Carvalho-e-Silva, 2001), P. soaresi (Weber et al., 2005), e P. spiniger (Haddad & Pombal, 1998); e somente dez
apresentam informações sobre a morfologia oral interna: P. santafecinus e P. biligonigerus (Perroti & Céspedez, 1999); P.riograndensis (Sandoval, 20002); P. lisei (Both et al., 2006)
P. marmoratus (Nomura et al, 2003); P. fernandezae (Alcade et al., 2006), P. albonotatus, P. centralis e P. cuvieri (Miranda & Ferreira, 2009) e P. jordanensis (Gomes et al., 2010).
A maioria dos anuros possui um ciclo de vida complexo com uma fase larval aquática. As larvas, chamadas de girinos, são especializadas e alimentam-se, na maioria dos casos, de partículas em suspensão e grande parte da anatomia do girino está envolvida para a obtenção e processamento de alimento, principalmente a área bucofaringeana, que é única entre os vertebrados (Viertel & Richter, 1999).
Os girinos apresentam uma grande diversidade de hábitos amplamente refletidos em sua morfologia externa e oral interna, a qual apresenta caracteres com informações úteis na compreensão das relações ecológicas e sistemáticas (Wassersug, 1976; Spirandeli-Cruz, 1991; d’Heursel & de Sá, 1999).
Lataste (1879) foi quem primeiro propôs a divisão dos anuros com base em caracteres larvares. Ele utilizou presença de espiráculo sinistro ou mediano para separar os anfíbios anuros em Laevogyrinidae ou Mediogyrinidae (Apud Wassersug, 1976). Orton (1953)propôs a divisão dos anuros em quatro grandes grupos com base nos caracteres das larvas: Tipo I (Pipidae e Rhinophynidae): espiráculos duplos e sem partes queratinizadas na boca; Tipo II (Microhylidae): espiráculo único e medial e sem partes orais queratinizadas; Tipo III (Ascaphidae e Discoglossidae): espiráculo medial e com partes orais queratinizadas; Tipo IV: girinos com partes orais queratinizadas e espiráculo sinistro. Em 1976, Wassersug pesquisou novos caracteres na morfologia oral interna das larvas de anfíbios anuros para ajudar a compreensão das relações filogenéticas e sugeriu uma terminologia adequada, baseada em larvas do Tipo IV (Orton 1953) entre os estágios 26-39 (Gosner, 1960), que foi sendo aperfeiçoada (Altig & Johnston, 1986, 1989; Johnston & Altig, 1986; Altig & McDiarmid, 1999).
O uso de caracteres larvares em estudos de anuros pode ajudar a resolver problemas taxonômicos (Wogel et al., 2000) e quando relacionam-se com caracteres dos adultos, podem oferecer importante subsídio para o entendimento da sistemática do grupo (Cruz, 1962). Por isso, visando enriquecer o conhecimento sobre larvas de anuros e auxiliar na
16 taxonomia e sistemática dessa ordem, o objetivo deste estudo é descrever e comparar a morfologia externa, oral externa e oral interna dos girinos do gênero Physalaemus.
17 - Caracterização morfológica
Em 2007, Altig fez uma revisão da nomenclatura usada para descrever a morfologia externa das larvas de anuros, assim como as medidas morfométricas utilizadas. Nesse trabalho, o autor ressalta a necessidade de que todas as marcações (“landmark”) sejam as mesmas para todos os espécimes analisados, caso contrário elas irão representar medidas não comparáveis.
As medidas mais comumente encontradas em trabalhos de descrição de girinos, para a morfologia externa, são (Figura 1): Altura do corpo (AC), máxima altura da cauda (ACd), máxima altura da musculatura da cauda (AM), comprimento do corpo (CC), comprimento da cauda (CCd), comprimento total (CT), diâmetro da narina (DN), diâmetro do olho (DO), distância entre os olhos (OO), distância do espiráculo até a ponta do focinho (EF), largura do corpo (LC), distância da narina até a ponta do focinho (NF), distância do olho até a ponte do focinho (OF), além da largura do disco oral (DO).
O disco oral (Figura 2) segue a nomenclatura proposta por Altig (1970) e revisada pelo mesmo autor em 2007. Nas larvas da maioria dos taxa, o disco oral apresenta um lábio superior (UJS) e um lábio inferior (LJS) compostos por fileiras transversais de dentículos (TR) (Altig, 2007). Além da largura do aparato bucal, verifica-se também a fórmula dentária e o tamanho dessas fileiras de dentículos superiores (A-1; A-2) e posteriores (P-1; P-2; P-3); a presença de papila na margem lateral do disco oral (E), assim como de papila marginal (MP) e submarginal (SM) ao redor do disco oral; e a presença de
gap (G) dorsal na papila marginal (MP).
Em larvas típicas de poça, as papilas marginais sobre a borda do disco oral podem ocorrer em três estados: interrompida amplamente na margem dorsal e inteira na margem ventral (estado mais comum), interrompida amplamente na margem dorsal e com interrupções (ou apenas um interrupção) na margem ventral, ou ainda completa, em torno de todo o disco oral.
18 Figura1: vistas dorsal (A) e lateral (B) de um girino típico de poça (Physalaemus soaresi), com as medidas morfométricas comumente utilizadas em descrições de girinos.
Figura 2: Disco oral de um girino típico de poça, com fórmula dentária 2(2)/3. (Fonte: Altig (2007).
19 Segundo Wassersug (1976), a cavidade bucofaringeana pode ser dividida em duas partes principais, uma anterior chamada cavidade oral, e uma posterior chamada cavidade faringeana.
A cavidade oral das larvas de anfíbios anuros é estreita na porção próxima às narinas, fica larga na região mediana e torna a estreitar novamente na porção próxima à faringe e ao esôfago.
Em larvas do tipo IV, o assoalho bucal é constituído por um par de papilas infralabiais localizadas abaixo do lábio inferior, duas ou mais papilas linguais na região onde a língua se desenvolve e papilas do bolso bucal (“buccal pocket”). O centro do assoalho bucal (“buccal floor arena” ou “BFA”) é limitado por pares de fileiras de papilas e/ou por pústulas. O teto bucal pode ser dividido em três regiões bem definidas. A área pré-coanal limitada pelas coanas onde pode haver papilas pré-nasais ou pústulas. A área pós-nasal é limitada pelas coanas, acima, e por uma prega transversal chamada crista mediana (“median ridge”) e também se encontra papilas. A terceira região (“buccal roof arena” ou “BRA”) é dorsal ao BFA e também apresenta fileiras de papilas e/ pústulas; o BRA é limitado posteriormente por uma mucosa secretora chamada zona glandular (ver Figura 3).
20 Figura 3: Morfologia oral interna do girino de Hyla fermoralis: (A) Assoalho bucal; (B) Teto bucal (fonte: Wassersug, 1980). Escala representa 1mm.
21
Capítulo I
Este capítulo apresenta o manuscrito intitulado “Morphological description of the oral cavity of tadpoles of the genus Physalaemus Fitzinger, 1826 (Amphibia, Anura, Leiuperidae)”, que será submetido para publicação no periódico científico ZOOTAXA. Os critérios de redação e formatação seguem as normas deste periódico, as quais se encontram disponíveis no ANEXO I desta dissertação.
22
MORPHOLOGICAL DESCRIPTION OF THE ORAL CAVITY OF TADPOLES OF THE GENUS PHYSALAEMUS FITZINGER, 1826 (AMPHIBIA, ANURA,
LEIUPERIDAE)
JOICE RUGGERI¹ AND LUIZ NORBERTO WEBER²
¹ Departamento de Zoologia, Instituto de Biologia, Universidade Federal da Bahia, Campus Universitário, Rua Barão de Jeremoabo, Ondina, 40170-115 Salvador, Bahia, Brasil. E-mail: joice.ruggeri@gmail.com
2 Instituto de Ciências Ambientais e Desenvolvimento Sustentável, Universidade Federal
da Bahia, Rua Prof. José Seabra, Centro, 47805-100 Barreiras, Bahia, Brasil.
E-mail: luiznorbertow@gmail.com.
Abstract
From the 45 species currently described for the genus Physalaemus and allocated into seven morphological groups, 28 have their tadpoles described, which 11 have information on the oral anatomy. The internal and external oral morphology of the tadpoles are reflected by their habits and may contain important information about the ecological relations among the species and understanding these relations may be helpful on the comprehension of systematic and taxonomic problems among anuran groups, including the genus Physalaemus. Herein, is described the internal oral morphology of the tadpoles of
Physalaemus aguirrei, P. atlanticus, P. camacan, P. cicada, P. crombiei, P. gracilis, P. irroratus, P. maximus, P. rupestris, P. signifer and P. soaresi, along with the comparison
among all species in the genus with previously described oral cavity morphology. This study adds information about the tadpoles from the genus Physalaemus that allows corroborating some of the species group proposed for adult specimens.
Keywords: Taxonomy, internal oral morphology, larval anatomy, Physalaemus
23 Introduction
The Neotropical genus Physalaemus Fitzinger, 1826 belongs to the family Leiuperidae, and comprises little frogs widely distributed in Brazil (Frost, 2011; Nascimento et al., 2005).
Forty five species are currently allocated in the genus, 28 with the tadpole described, which only 11 contain information upon the internal oral morphology: P.
santafecinus and P. biligonigerus (Perroti & Céspedez, 1999); P.riograndensis (Sandoval,
20002); P. lisei (Both et al., 2006) P. marmoratus (Nomura et al, 2003); P. fernandezae (Alcade et al., 2006), P. albonotatus, P. centralis and P. cuvieri (Miranda & Ferreira, 2009), P. jordanensis (Gomes et al., 2010) and P. albifrons (Oliveira et al.).
The larvae of Physalaemus are typical pond tadpoles and are assumed to occur in the bottom (Rossa-Feres et al, 2004; Vera Candioti, 2007). According to Wassersug (1976), the oral cavity of the tadpoles is composed by many papillae which arrangement, length, and number differ among genera and species (Wassersug, 1980) and may reflect their microhabitats, probably containing important information about ecological relations among the species that may contribute on the understanding of the systematic of anuran groups (Spirandeli-Cruz, 1991; d’Heursel & de Sá, 1999).
In order to add taxonomic information of tadpoles from the genus Physalaemus, herein is presented the description of the internal oral anatomy of P. aguirrei, P. atlanticus,
P. camacan, P. cicada, P. crombiei, P. gracilis, P. irroratus, P. maximus, P. rupestris, P. signifer and P. soaresi, comparing them to other species of Physalaemus with internal oral
morphology previously described and available in literature.
Material and methods
Specimens analyzed are deposited in zoological collection at: MNRJ (Museu Nacional, Rio de Janeiro), ZUFRJ (Universidade Federal do Rio de Janeiro, Rio de Janeiro), UFBA (Universidade Federal da Bahia, Bahia), DZSJRP (Universidade Estadual Paulista – São José do Rio Preto, São Paulo), and CFBH (Universidade Estadual Paulista – Rio Claro, São Paulo).
24 Tadpoles of the following species of Physalaemus were analyzed and have the internal oral morphology described: P. aguirrei (MNRJ 30591), from Parque Nacional Descobrimento, Prado, Bahia; P. atlanticus (ZUFRJ 7382 and CFBH), both from Picinguaba, Ubatuba, São Paulo; P. camacan (MNRJ 33342), from Reserva Biológica de UMA, UMA, Bahia; P. cicada (UFBA 1001 and UFBA 10012), from Serra do Ramalho, Bahia; P. crombiei (MNRJ 54313), from Reserva Biológica Santa Lúcia, Santa Lúcia, Espitiro Santo; P. gracilis (DZSJRP 956.7), from São José dos Pinhais, Paraná; P.
irroratus (MNRJ 41460), from Fazenda Duas Barras, Santa Maria do Salto, Minas Gerias; P. maximus (MNRJ 46717), from Santa Rita de Ouro Preto, Ouro Preto, Minas Gerais; P. rupestris (MNRJ 25479), from Parque Nacional de Ibitipoca, Lima Duarte, Minas Gerais; P. signifer (ZUFRJ 5121), from Parque Natural Municipal da Taquara, Duque de Caxias,
Rio de Janeiro; and P. soaresi (ZUFRJ 7436), from Floresta Nacional Mário Xavier, Seropédica, Rio de Janeiro.
Tadpole developmental stages were determined according to Gosner (1960). Measurements in millimeters (Table 1) of the buccal roof height (BRH), buccal roof width (BRW), internarial distance median ridge (IND), median ridge height (MRH), median ridge width (MRW), buccal floor height (BFH) and buccal floor width (BFW) were obtained by using an ocular micrometer in a stereo microscope (Olympus SZ40).
The internal oral morphology was studied following the procedure described by Wassersug (1976) and Spirandeli-Cruz (1991). For that, two tadpoles of each species, between the stages of development 33 and 38, were dissected under the stereo microscope and the oral morphological features were stained with 3% Methylene Blue solution. Only one specimen of P. aguirrei and one specimen of P. soaresi were allowed to be dissected. Dissections were made carefully inserting the micro dissecting scissors into the left corner of the mouth between the upper and lower beaks and cutting back to the posterodorsal corner of the pharynx. This cut separated the Meckel’s cartilage from the palatoquadrate bar and that from the ceratohyal. The same procedure was made in the right side. The mouth could then be opened and oral surface exposed. A longitudinal cut was made along the side of the mouth, freeing the roof from the floor. Descriptions follow the terminology proposed by Wassersug (1976).
25 Results
Oral cavity features – Table 2.
Physalaemus aguirrei Bokermann, 1966
Ventral aspect (Fig. 1A): At Stage 37, buccal floor triangular. Presence of two pairs of
infralabial papillae. The anterior pair (not seen in the figure) is thin with flattened apex, much smaller than the posterior and directed upward. The posterior pair is large, long and curved upward, easily discernible from the anterior pair. Tongue anlage elliptical, with four long and tapered lingual papillae in a transverse row. Buccal pockets horizontally oriented. In the buccal floor arena (BFA) there are three papillae on each side of the arena, pointing to the center; the first and last papillae are finger-like and the one in the middle is chela-shaped; and about ten pustulations dispersed on it. Ventral velum round shaped with small projections along its external margin. Dorsal aspect (Fig. 1B): Buccal roof somewhat triangular. Prenarial arena longer than wide, without papillae or pustulations on it. Elliptical choanae, large, oriented 45° from transverse plane. Internarial distance 5% of the roof width. In the postnarial arena, presence of one pair of finger-like papillae pointing to the center. The median ridge is trapezoid, twice wider than long, with few projections in the superior margin. Presence of a pair of chela-shaped lateral ridge papillae. In the buccal roof arena (BRA), about twenty pustulations dispersed, and four finger-like papillae on each side directed to the center of BFA. Dorsal velum withno projections.
Physalaemus atlanticus Haddad & Pombal, 2004
Ventral aspect (Fig. 2A): At Stage 37, buccal floor triangular. Presence of two pairs of
infralabial papillae, both are large in the basis and flattened in the extremity with irregular margins and apices, but the posterior pair is larger and much discernible (the anterior pair can not be seen in the figure). Tongue anlage elliptical, with four tapered lingual papillae in a transverse row, directed upwards; the two in the middle are longer than the ones in the extremities. Buccal pockets horizontally oriented. In the BFA, presence of one bifid, long and tapered papilla on each side and another five long and finger-like papillae on each side, pointing to the center of the arena and few pustulations dispersed. Ventral velum round shaped with small projections. Dorsal aspect (Fig. 2B): Buccal roof somewhat triangular. Prenarial arena longer than wide; there are some short, conical papillae distributed in a
26 transverse row. Elliptical choanae, large, oriented 45° from transverse plane. Internarial distance 8% of the roof width. In the postnarial arena, presence of one pair of long papillae, large in the basis and tapered in the end, directed to the center; and a pair of short and flattened papillae. Presence of a pair of lateral ridge papillae, bifid and large in the basis, with tapered branches. The median ridge in semicircle is about five times wider than long, with few projections in the superior margin. In the BRA about thirty pustulations dispersed in the arena; it is limited by five papillae on each side, directed to the center of BFA; the first papilla on each side is slender but bifid and the others are finger-like papillae. Dorsal velum with no projections.
Physalaemus camacan Pimenta, Cruz & Silvano, 2005
Ventral aspect (Fig. 3A): At Stage 37, buccal floor slightly triangular. Presence of two
pairs of infralabial papillae. The posterior pair is large and has irregular margins and apex, while the anterior pair is short and tapered, with irregular margins. The posterior pair is easily discernible from the anterior pair, which can not be seen in the figure. Tongue anlage oval with four long, conical lingual papillae in a transverse row, with smooth surfaces. Small buccal pockets horizontally oriented. In the BFA, presence of five–six papillae on each side; the second papillae are bifid and the others are finger-like papillae, all point to the center of the arena, except for the last papillae that are directed upward. There are few pustulations dispersed on the arena. Ventral velum round with some projections in the margin. Dorsal aspect (Fig. 3B): Buccal roof slightly triangular. Prenarial arena wider than longer, without papillae or pustulations on it. Choanae elliptical, oriented 45° from transverse plane. Internarial distance 5% the buccal roof length. In the postnarial arena, presence of a pair of tapered papillae, irregular and large in the basis, directed to the center. One chela-shaped lateral ridge papilla on each side. The median ridge is in semicircle, longer than wide, with some irregularities in the margin. The BRA has about 15 pustulations dispersed, limited by four thin and tapered papillae on each side, directed to the center of the arena. Dorsal velum with irregular margin.
Physalaemus cicada Bokermann, 1966
Ventral aspect (Fig. 4A): At Stage 36, buccal floor triangular. Presence of two pairs of
infralabial papillae. The posterior pair is large in the basis, tapered in the apex, and with
27 irregular margins, while the anterior pair (not seen in the figure) is small, thin and tapered, and is directed upward. The posterior pair is easily discernible from the anterior. Tongue anlage elliptical with four small and tapered lingual papillae in a transverse row, directed upward. Buccal pockets horizontally oriented. In the BFA presence of four–five finger-like papillae on each side, pointing to the center of the arena and about 20 pustulations dispersed on it. Ventral velum round shaped with small projections. Dorsal aspect (Fig. 4B): Buccal roof triangular. Prenarial arena longer than wide. Some short, conical papillae are distributed in a transverse row in the prenarial arena. Elliptical choanae, large, oriented 45° from transverse plane. Internarial distance 7% of the roof width. In the postnarial arena, presence of one large finger-like papilla on each side. The median ridge is trapezoid, about three times wider than long, with irregular superior margin. Presence of a pair of lateral ridge papillae, large and chela-shaped. In the BRA about 40 pustulations dispersed on the arena, limited by three to five finger-like papillae on each side, directed to the center of the arena. Dorsal velum with projections.
Physalaemus crombiei Heyer & Wolf, 1989
Ventral aspect (Fig. 5A): At Stage 36, buccal floor triangular, slightly wider than long.
Presence of two pairs of infralabial papillae, the posterior pair is larger and bifid in the distal third portion, with irregular margins and apices; the anterior pair (not seen in the figure) is shorter, tapered and directed upward. Tongue anlage oval with two tapered lingual papillae in a transverse row. Buccal pockets horizontally orientated. In the BFA about 20 pustulations between five to six finger–like papillae on each side. The first pair consists on the smallest papillae in the BFA. All papillae in the BFA are directed to the center. Ventral velum with small projections. Dorsal aspect (Fig. 5B): Buccal roof triangular, longer than wide. Prenarial arena somewhat shaped as the buccal roof. Presence of six short, conical papillae distributed in “M” in the prenarial arena. Elliptical choanae, large, oriented 45° from transverse plane; its upper internal margin filled with few projections. Internarial distance about 10% of the roof width. In the postnarial arena, presence of two large papillae, directed to the center and two tapered papillae in the middle of the arena. Median ridge in semicircle three times wider than long, serrated in the margin. Presence of one chela–shaped lateral ridge papillae on each side serrated in the upper margin, directed to the center. In the BRA about 30 pustulations limited by two to
28 four finger–like papillae on each side, with different sizes and arranged parallel to each other; all directed to the center of BFA. Dorsal velum with no projections.
Physalaemus gracilis (Boulenger, 1883)
Ventral aspect (Fig. 6A): At Stage 37, buccal floor triangular. Presence of two pairs of
infralabial papillae. The anterior pair is more centrally positioned, is smaller, tapered and directed upward, while the posterior pair is large, bifid, with irregular apices. The posterior pair is much discernible from the anterior pair. Tongue anlage oval with four tapered lingual papillae in a transverse row, directed upward. Buccal pockets horizontally oriented. In the BFA presence of five to seven papillae on each side. Some papillae are large and chela-shaped and some are finger-like; there are about 30 pustulations dispersed in the arena. Ventral velum round shaped. Dorsal aspect (Fig. 6B): Buccal roof triangular. Prenarial arena longer than wide, with three short, flattened papillae on it. Elliptical choanae, large, oriented 45° from transverse plane, serrated in the superior margin. Internarial distance 8% of the roof width. In the postnarial arena, presence of two papillae on each side, one shorter thin and flattened papilla and another large finger-like papilla that points to the center. The median ridge is in semicircle, postulated in the superior margin. Presence of a pair of large chela-shaped lateral ridge papillae, with irregular margins. In the BRA five–six papillae on each side; there are three short, thin finger–like lateral roof papillae. Presence of 30 pustulations dispersed on the arena. Dorsal velum with no projections.
Physalaemus irroratus Cruz, Nascimento & Feio, 2007
Ventral aspect (Fig. 7A): At Stage 36, buccal floor triangular. Presence of two pairs of
infralabial papillae. The posterior pair is large in the basis, tapered in the apex, with irregular margin. The anterior pair is tapered, directed upward and can not be seen in the figure. The posterior pair is easily discernible from the anterior. Tongue anlage elliptical with three small and tapered lingual papillae in a transverse row, directed upwards. Buccal pockets horizontally oriented. In the BFA about ten papillae on each side, pointing to the center of the arena, thin and tapered, except for the second papillae, which are chela-shaped. There are few pustulations dispersed on the arena. Ventral velum with small projections. Dorsal aspect (Fig. 7B): Buccal roof somewhat triangular. Prenarial arena
29 longer than wide, with presence of some short, conical papillae arranged in semicircle on it. Elliptical choanae, large, oriented 45° from transverse plane. Internarial distance 7% of the roof width. In the postnarial arena, presence of one finger-like papilla on each side, large in the basis and serrated in the superior margin, directed upward. The median ridge is in semicircle, twice wider than long, with small projections along its superior margin. Presence of a pair of large chela-shaped lateral ridge papillae. In the BRA about 30 pustulations dispersed on it, and four long and tapered papillae arranged parallel to each other on each side, all directed to the center of BFA. Dorsal velum with no projections.
Physalaemus maximus Feio, Pombal & Caramaschi, 1999
Ventral aspect (Fig. 8A): At Stage 36, buccal floor somewhat triangular. Presence of one
short and tapered infralabial papilla on each side, directed upward. Tongue anlage elliptical with four tapered lingual papillae in a transverse row. Buccal pockets horizontally oriented. In the BFA about 20 pustulations and five to seven long, tapered papillae on each side, some pointing to the center and some directed upward, except for the first on each side that may be larger and bifid. Ventral velum with no projections. Dorsal aspect (Fig. 8B): Buccal roof somewhat triangular. Prenarial arena longer than wide, with about some short, conical papillae on it. Elliptical choanae, large, oriented 45° from transverse plane. Internarial distance 8% of the roof width. In the postnarial arena, presence of two large papillae on each side. The posterior pair is larger and has irregular margins and apices; the anterior pair is large in the basis, becoming tapered. The posterior pair is much discernible from the anterior. The median ridge is trapezoid, twice wider than long, with some projections along its margin. Presence of a large and bifid lateral ridge papilla on each side. In the BRA about 40 pustulations dispersed and four–five finger-like papillae on each side directed to the center of BFA. The last papilla on each side may be bifid. Dorsal velum with no projections.
Physalaemus rupestris Caramaschi, Carcerelli & Feio, 1991
Ventral aspect (Fig. 9A): At Stage 36, buccal floor triangular. Presence of one pair of
infralabial papillae, large in the basis and tapered, directed upward. Tongue anlage elliptical with four long and tapered lingual papillae in a transverse row, directed upwards; the papillae found in the extremities are smaller and flattened. Buccal pockets horizontally
30 oriented. Presence of few pustulations dispersed on the BFA. There are four long, finger-like papillae on each side, pointing to the center of the arena, and about ten papillae closer to the velum, directed upwards. Ventral velum with small projections. Dorsal aspect (Fig. 9B): Buccal roof somewhat triangular. Prenarial arena longer than wide, with two short, flattened papillae. Elliptical choanae, large, oriented 45° from transverse plane. Internarial distance 9% of the roof width. In the postnarial arena, presence of two papillae on each side. The posterior pair is a large finger-like papilla with irregular margin that points to the center and the anterior pair is a smaller and tapered. The posterior pair is discernible from the anterior. There is one lateral ridge papilla on each side, large in the basis and chela-shaped. The median ridge is triangular, about two times wider than long. In the BRA 30 pustulations in the arena and about six finger-like papillae on each side, arranged parallel to each other and directed to the center of BRA. Dorsal velum with no projections.
Physalaemus signifer (Girard, 1853)
Ventral aspect (Fig. 10A): At Stage 37, buccal floor triangular, as long as wide. Presence
of one pair of large infralabial papillae, with irregular margins. Tongue anlage elliptical with two small and conical lingual papillae in a transverse row. Absence of prepocket papillae. Buccal pockets horizontally oriented. In the BFA about 20 pustulations dispersed and five papillae on each side, pointing to the center of the arena. The first papilla on each side may be chela-shaped and the others are shorter, slender and tapered. Ventral velum with small projections. Dorsal aspect (Fig. 10B): Buccal roof somewhat triangular. Prenarial arena longer than wide, with no pustulations or papillae on it. Elliptical choana, large, oriented 45° from transverse plane. Internarial distance 7% of the roof width. In the postnarial arena, presence of two pairs of papillae. One pair is large and bifid and the other pair is finger-like with irregular margins, and points to the center. Presence of one large, bifid lateral ridge papillae on each side. The median ridge is in semicircle, about two times wider than long. In the BRA 20 pustulations dispersed on the arena and about one-two slender and tapered papillae on each side directed to the center of BFA. Dorsal velum with no projections.
Physalaemus soaresi Izeckson, 1965
31
Ventral aspect (Fig. 11A): At Stage 33, buccal floor triangular. Presence of two pairs of
infralabial papilla. The posterior pair is a large finger-like papillae; the anterior pair is short and tapered, directed upward. Tongue anlage oval with three long and tapered lingual papillae in a transverse row, directed upwards. Buccal pockets horizontally oriented. In the BFA there are few pustulation dispersed and about two–three papillae on each side, parallel to each other. The sencond papillae are chela-shaped and the others are finger-like and long. Ventral velum with small projections. Dorsal aspect (Fig. 11B): Buccal roof somewhat triangular. Prenarial arena longer than wide, with three short, flattened papillae on the midline. Elliptical choanae, large, oriented 45° from transverse plane. Internarial distance 6% of the roof width. In the postnarial arena, presence of one long finger-like papilla on each side, directed upward. The median ridge is trapezoid, four times wider than long, with some projections in the superior margin. Presence of a pair of lateral ridge papillae, large and bifid in the basis with irregular margins. In the BRA there are few pustulations dispersed and four long and tapered papillae on each side arranged parallel to each other and directed to the center of BFA. Dorsal velum with no projections.
Discussion
According to Spirandeli-Cruz (1991), tadpoles between Stages 35–38 have few or none intraspecific differences regarding to the buccopharyngeal morphology because the structures are already developed and although the tadpoles of P. soaresi are at Stage 33, it was noticed that the traits are already comparable to those from tadpoles between Stages 35–38.
The median ridge gathered the tadpoles into morphological groups that corroborate the groups proposed by Nascimento et al. (2005), like the P. singifer group which median ridge is semicircular and the P. olfersii group, which median ridge is trapezoid. The number of lingual papillae on the tongue anlage was also a trait shared by species of the same morphological group, but it divided the P. signifier group: P. atlanticus, P. camacan, and P. morerirae have four lingual papillae while P. angrensis, P. crombiei, and P.
signifier, have two and P. irroratus, have three.
In the Physalaemus albifrons group all four species have their tadpole described.
Physalaemus albifrons, P. biligonigerus, P. marmoratus, and P. santafecinus share some
characters like, for example, the number of infralabial papillae (four infralabial papillae) in
32 the buccal floor, and the median ridge in semicircle in the buccal roof (Perotti & Céspedez, 1999; Sandoval & Alvarez, 2001; Nomura et al., 2003; Oliveira et al., 2010). The BFA in
P. albifrons and in P. santafecinus are similar in number, location and shape of the papillae
(Oliveira et al., 2010; Perotti & Céspedez, 1999). The lateral ridge papilla is bifurcated in
P. albifrons, P. biligonigerus and in P. marmoratus (Sandoval, 2002;Nomura et al., 2003;
Oliveira et al., 2010). The BRA papillae may vary from three to four in P. albifrons and P.
marmoratus and from five to six in P. santafecinus (Perotti & Céspedez, 1999; Nomura et al., 2003; Oliveira et al., 2010).
The tadpoles of P. albonotatus, P. centralis, P. cuvieri, and P. cicada belong to the
P. cuvieri group (Nascimento et al. 2005). Miranda and Ferreira (2009) described the
presence of four infralabial papillae in the buccal floor of P. albonotatus, P. centralis and
P. cuvieri which are also present in the tadpole of P. cicada. Like P. albonotatus, P. cicada
presents five papillae on the BFA, but the first also have few lateral roof pappilae (Miranda and Ferreira, 2009) not seen in the buccal floor of P. cicada. According to original descriptions, P. albonotatus and P. cuvieri have two papillae on the postnarial arena as well as P. cicada, differing from P. centralis that have six.
In the Physalaemus deimaticus group, only P. rupestris have the tadpole described and this study provided the description of the internal oral anatomy. This tadpole shares some traits with tadpoles of the P. henselii group, which comprises two species with tadpoles described: P. fernandezae (Alcade et al., 2006) and P. riograndensis (Sandoval, 2002). Physalaemus riograndensis have a triangular median ridge, similar to P. rupestris and differing from P. fernandezae that have a semicircular median ridge. The BFA of P.
rupestris and P. fernandezae are limited by six papillae on each side, differing from P. riograndensis that have only four papillae (Sandoval, 2002; Alcade et al., 2006). Different
from P. rupestris, P. fernandezae and P. riograndensis have about four papillae on each side of the BRA (five-six in P. rupestris) and one lingual papilla on the tongue anlage (four in P. rupestris).
In the P. olfersii group, the tadpoles of P. aguirrei, P. maximus and P. soaresi have a trapezoid median ridge. The tadpoles of P. aguirrei and P. soaresi have four infralabial papillae, differing from P. maximus that have two. On the other hand, P. aguirrei and P.
maximus present four labial papillae while P. soaresi have three. The prenarial arena of P. maximus and P. soaresi are filled with pustulations, differing from P. aguirrei, that have
neither pustulations nor papillae on the prenarial arena.
33
Physalaemus lisei (Both et al., 2006), P. jordanensis (Gomes et al., 2010) and P. gracilis belong to the P. gracilis group. The tadpoles of P. jordanensis have six infralabial
papillae on each side and P. lisei have three multiple-brancnhing papillae on each side, differing from P. gracilis that have two papillae on each side. Physalaemus lisei have five lingual papillae (Both et al., 2006), differing from P. jordanensis and P. gracilis. Like the tadpoles in the P. olfersii group, the median ridge is trapezoid in P. jordanensis and in P.
lisei; it is in semicircle in P. gracilis. Both P. gracilis and P. jordanensis have lots of
pustulations on the the buccal floor and buccal roof arenas, but they differ as the number of papillae on those arenas. Physalaemus lisei have four papillae on each side of both BRA and BFA, differing from P. gracilis that have four-five papillae on each side of the BRA and five-seven on each side of the BFA, and from P. jordanensis that have eight papillae on each side of the BRA and six on each side of the BFA. The tadpole of P. gracilis has few lateral roof papillae close to the ventral velum like P. albonotatus, differing from other tadpoles from its morphological group.
The tadpoles of P. angrensis (unpublished data), P. atlanticus, P. camacan, P.
crombiei, P. irroratus and P. signifer belong to the P. signifer group and share the
semicircular median ridge. Physalaemus angrensis and P. signifer have a pair of large infralabial papillae, while the other tadpoles have four large tadpoles except for the P.
atlanticus, which two papillae are large and two are slender. The lingual papillae can vary
among species: P. irroratus have three small and tapered papillae on the tongue anlage; P.
angrensis, P. crombiei and P. signifer have two lingual papillae, in P. angrensis and P. crombiei they are tapered, in P. signifer they are flattened; P. atlanticus and P. camacan
have four tapered lingual papillae. The papillary on the BRA in tadpoles of the P. signifer group vary from five to seven on each side, except for P. irroratus that has about ten on each side. In the postnarial arena the tadpoles may have two or four papillae; P. angrensis,
P. camacan and P. irroratus have two papillae that differ as the shape, which are larger in P. camacan and P. irroratus, and P. atlanticus, P. crombiei and P. signifer have two pairs
of papillae, one much larger than the other.
It was described the presence of prepocket papillae for the tadpoles of P. centralis,
P. cuvieri, P. jordanensis, and P. lisei (Miranda and Ferreira, 2009; Gomes et al., 2010;
Both at al., 2006) but in the present study those papillae were not observed. However, according to Wassersug and Heyer (1988), the actual number of prepocket papilla is difficult to assess because of the continuation of the prepocket papillary field with the BFA and do not show any meaningful patterns of variation.
34 Miranda and Ferreira (2009) inferred that the presence of three-four labial papillae should be a diagnostic character for the P. cuvieri group, once tadpoles from other species group with the oral anatomy available, have one or two labial papillae. This study does not corroborate such inference due to some tadpoles in the P. signifer group which also present three or four lingual papillae.
Acknowledgments
We thank Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB) for financial support. We acknowledge Universidade Federal da Bahia (UFBA), Universidade Federal do Rio de Janeiro (UFRJ), Universidade Estadual Paulista (UNESP) and Museu Nacional (MNRJ), for the loan of specimens. We also thank Ana Carolina Guedes for the drawnings.
35 References
Alcade, L., Natale, G.S. & Cajade, R. (2006) The tadpole of Physalaemus fernandezae (Anura: Leptodactylidae). Herpetological Journal, 16, 203-211.
Altig, R. (1970) A key to the tadpoles of the continental United States and Canada.
Herpetologica, 26, 180-207.
Altig, R. & McDiarmid, R.W. (1999) Body plan development and morphology. In: McDiarmid, R.W. and Altig, R. (Eds), Tadpoles, The Biology of Anuran Larvae. The University of Chicago Press, Chicago and London, pp. 24-51.
Baêta, D., Lourenço, A.C.C., Pezzuti, T.L. & Pires, M.R.S. (2007) The tadpole, advertisement call, and geographic distribution of Physalaemus maximus Feio, Pombal & Caramaschi, 1999 (Amphibia, Anura, Leiuperidae). Arquivos do Museu Nacional,
Rio de Janeiro, 65, 27-32
Bokermann, W.C.A. (1963) Girinos de anfíbios brasileiros 2 (Amphibia, Salientia). Revista
Brasileira de Biologia, 23, 349-353.
Both, C., Kwet, A. & Solé, M. (2006) The tadpole of Physalaemus lisei Braun & Braun, 1977 (Anura, Leptodactylidae) from southern Brazil. Alytes, 24, 109-116.
Cardoso, A.J. & Haddad, C.F.B. (1985) Nova espécie de Physalaemus do grupo signiferus (Amphibia, Anura, Leptodactylidae). Revista Brasileira de Biologia, 45, 33-37.
Cei, J.M. (1980) Amphibians of Argentina. Monitore Zoologico Italiano (NS) Monografia, 2, 1-609.
Cruz, C.A.G., Nascimento, L.B. & Feio, R.N. (2007) A new species of the genus
Physalaemus Fitzinger, 1826 (Anura, Leiuperidae) from Southeastern Brazil. Amphibia-Reptilia, 28, 457-465.
36 D’Heursel, A. & de Sá, R.O. (1999) Comparing the tadpoles of Hyla geographica and
Hyla semilineata. Journal of Herpetology, 33, 353-361.
Fernández, K. & Fernández, M. (1921) Sobre la biologia y reproducción de algunos batracios argentinos I. Cystignathidae. Anales de la Sociedad Científica Argentina, 91, 97-139.
Frost, D.R. (2011) Amphibian Species of the World: an online reference. Version 5.4. American Museum of Natural History, New York, USA. Available from http://
http://research.amnh.org/vz/herpetology/amphibia/ (accessed April 1, 2011)
Gomes, F.B.R., Provete, D.B. & Martins, I.A. (2010) The tadpole of Physalaemus
jordanensis Bokermann, 1967 (Anura, Leiuperidae) from Campos do Jordão, Serra da
Mantiqueira, Southeastern Brazil. Zootaxa, 2327, 65-68.
Gosner, K. L. (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16, 183-190.
Haddad, C.F.B. & Pombal Jr, J.P. (1998) Redescription of Physalaemus spiniger (Anura: Leptodactylidae) and description of two new reproductive modes. Journal of
Herpetology, 32:557-565.
Haddad, C.F.B. & Sazima, I. (2004) A new species of Physalaemus (Amphibia; Leptodactylidae) from the Atlantic forest in southeastern Brazil. Zootaxa, 479, 1-12.
Heyer, W.R., Rand, A.S., Cruz, C.A.G., Peixoto, O.L. & Nelson, C.E. (1990) Frogs of Boracéia. Arquivos de Zoologia, Museu de Zoologia da Universidade de São Paulo, 31, 231-410.
Kehr, A.I., Schaefer, E.F. & Duré, M.I. (2004) The tadpole of Physalaemus albonotatus (Anura: Leptodactylidae). Journal of Herpetology, 38, 145-148.
37 Langone, J.A. (1989) Descripcion de la larva de Physalaemus gracilis (Boulenger, 1883) (Amphibia, Anura, Leptodactylidae). Comumunicaciones Zooogicas. del Museo de
Historia Natural de Montevideo, 12:1-11.
Lynch J.D. (1971) Evolutionary Relationships, Osteology, and Zoogeography of Leptodactyloid Frogs. Miscellaneous Publication. Museum of Natural History
University of Kansas, 53, 1–238.
Miranda, N.E.O. & Ferreira, A. (2009) Internal buccal morphology of the tadpoles of the genera Eupemphix, Physalaemus and Leptodactylus. Biota Neotropica, 9, 165-176.
Nascimento, L.B., Carvalho Jr., R.R.; Wogel, H.; Fernandes, D.S. & Feio, R.N. (2001) Reprodução e descrição do girino de Physalaemus rupestris Caramaschi, Carcerelli & Feio, 1991 (Amphibia, Anura, Leptodactylidae). Boletim do Museu Nacional, Nova
Série, Série Zoologia, 450, 1-10.
Nascimento, L.B., Caramaschi, U. & Cruz, C.A.G. (2005) Taxonomic review of the species groups of the genus Physalaemus Fitzinger, 1826 with revalidation of the genera Engystomops Jiménez-de-la-Espada, 1872 and Eupemphix Steindachner, 1863 (Amphibia, Anura, Leptodactylidae). Arquivos do Museu Nacional, Rio de Janeiro, 63, 297-320.
Nomura, F., Rossa-Feres, D.C. & Prado, V.H.M. (2003) The tadpole of Physalaemus
fuscomaculatus (Anura: Leptodactylidae), with a description of internal oral
morphology. Zootaxa, 370,1-8.
Perotti, M. G. (1997) The tadpole of Physalaemus cuqui Lobo, 1993 (Amphibia, Anura, Leptodactylidae). Amphibia-Reptilia, 18, 427-432.
Perotti, M.G. & Céspedez, J.A. (1999) The tadpole of Physalaemus santafecinus, with comments on the buccoharyngeal morphology. Journal of Herpetology, 33, 312-315.
38 Pimenta, B.V.S. & Cruz, C.A.G. (2004) The tadpole and advertisement call of
Physalaemus aguirrei Bokermann, 1966 (Anura, Leptodactylidae). Amphibia-Reptilia,
25, 197-204.
Pimenta, B.V.S., Cruz, C.A.G. & Silvano, D.L. (2005) A new species of the genus
Physalaemus Fitzinger, 1826 (Anura, Leptodactylidae) from the Atlantic Rain Forest of
southern Bahia, Brazil. Amphibia-Reptilia, 26, 201-210.
Pombal Jr., J.P. & Madureira, C.A. (1997) A new species of Physalaemus (Anura, Leptodactylidae) from the Atlantic rain forest of northeastern Brazil. Alytes, 15, 105- 112.
Prigioni, C.M. & García, J.E. (2001) Descripción de la larva de Physalaemus
riograndensis Milstead, 1960 (Anura: Leptodactylidae). Acta Zoológica Platense, 1,
1-5.
Rossa-Feres, D.C. & Jim J.S. (1993) Tadpole of Physalaemus centralis (Anura, Leptodactylidae). Copeia, 2, 566-569.
Rossa-Feres, D.C., Jim, J.S. & Fonseca, M.G. (2004) Diets of tadpoles form a temporary pond in southeastern Brazil (Amphibia: Anura). Revista Brasileira de Zoologia, 21, 4, 745 – 754.
Sandoval, M. T. & Alvarez B. B. (2001) Microanatomía del disco oral y cavidad bucal de larvas de anuros. Reunión de comunicaciones científicas de la UNNE, Corrientes, Argentina.
Sandoval, M. T. (2002) Descripción del disco oral y cavidad bucofaríngea de larvas de dos especies de anuros de la familia Leptodactylidae. Reunión de comunicaciones
científicas de la UNN, Corrientes, Argentian.
Spirandeli-Cruz, E.F. (1991). Estudo comparativo da morfologia oral interna de larvas de
anfíbios anuros que ocorrem na região de Botucatu, São Paulo (Amphibia, Anura).
39 Tese (Doutorado em Zoologia), Instituto de Biociências da Universidade de São Paulo, São Paulo, 237p.
Vera Candioti, M.F. (2007) Anatomy of anuran tadpoles from lentic water bodies: systematic relevance and correlation with feeding habits. Zootaxa, 1600, 1-175.
Vieira, W.L.S. & Arzabe, C. (2008) Descrição do girino de Physalaemus cicada (Anura: Leiuperidae). Iheringia, Série Zoológica, Porto Alegre, 98, 266-269.
Wassersug, R.J. (1976) Oral morphology of anuran larvae: terminology and general description. Occasional Papers of the Museum of Natural History, University of
Kansas, 48, 1-23.
Wassersug, R.J. (1980) Internal oral features of larvae from eight anuran families: Functional, systematic, evolutionary, and ecological considerations. Occasional Papers
of the Museum of Natural History, University of Kansas, 68, 1-146.
Weber, L.N. & Carvalho-e-Silva, S.P. (2001) Descrição da larva de Physalaemus signifer (Girard, 1853) (Amphibia, Anura, Leptodactylidae) e informações sobre a reprodução e a distribuição geográfica da espécie. Boletim do Museu Nacional, Nova Série, Série
Zoologia, 462, 1-6.
Weber, L.N., Carvalho-e-Silva, S.P. & Gozaga, L.P. (2005) The tadpole of Physalaemus
soaresi Izecksohn, 1965 (Anura: Leptodactylidae), with comments on taxonomy,
reproductive behavior, and vocalizations. Zootaxa, 1072, 35-42.
40
FIGURE LEGENDS
Figure 1: (A) Floor and (B) roof of Physalaemus aguirrei, at Stage 37. Scale = 1 mm. Figure 2: (A) Floor and (B) roof of Physalaemus atlanticus, at Stage 37. Scale = 1 mm. Figure 3: (A) Floor and (B) roof of Physalaemus camacan, at Stage 37. Scale = 1 mm. Figure 4: (A) Floor and (B) roof of Physalaemus cicada, at Stage 36. Scale = 1 mm. Figure 5: (A) Floor and (B) roof of Physalaemus crombiei, at Stage 36. Scale = 1 mm. Figure 6: (A) Floor and (B) roof of Physalaemus gracilis, at Stage 37. Scale = 1 mm. Figure 7: (A) Floor and (B) roof of Physalaemus irroratus, at Stage 36. Scale = 1 mm. Figure 8: (A) Floor and (B) roof of Physalaemus maximus, at Stage 36. Scale = 1 mm. Figure 9: (A) Floor and (B) roof of Physalaemus rupestris, at Stage 36. Scale = 1 mm. Figure 10: (A) Floor and (B) roof of Physalaemus signifer, at Stage 37. Scale = 1 mm. Figure 11: (A) Floor and (B) roof of Physalaemus soaresi, at Stage 33. Scale = 1 mm.
Table 1: Mean and Standard Deviation of the internal oral features of the tadpoles of
Physalaemus aguirrei, P. atlanticus, P. camacan, P. cicada, P. crombiei, P. gracilis, P. irroratus, P. maximus, P. rupestris, P. signifer and P. soaresi, Stage 33 – 39 (Gosner,
1960) in millimeter (mm). BRH = Buccal Roof Height; BRW = Buccal Roof Width; IND
= Internarial Distance Median Ridge; MRH = Median Ridge Height; MRW = Median
Ridge Width; BFH = Buccal Floor Height; BFW = Buccal Floor Width.
Table 2: Comparison of the oral cavity between the tadpoles of Physalaemus in the Stages 33* – 37. Abbreviations stand for: BRA = Buccal Roof Papillae; BFA = Buccal Floor Papillae.
41
A B
Figure 1.
A B
Figure 2.
42 A B Figure 3. A B Figure 4.
43 A B Figure 5. A B Figure 6.
44
A B
Figure 7.
45 A B Figure 8. A B Figure 9.
46 A B Figure 10. A B Figure 11.
47 Table 1. Species BHR BRW IND MRH MRW BFH BFW P. aguirrei 3.96 3.3 0.17 0.4 0.17 2.64 2.64 P. angrensis 3.14 (±0.23) 2.64 0.33 0.33 0.08 (±0.02) 2.31 (±0.23) 2.48 (±0.23) P. atlanticus 3.8 (±0.23) 2.89 (±0.25) 0.23 0.5 0.23 2.39 (±0.12) 2.89 (±0.12) P. camacan 3.3 3.3 0.17 0.33 0.17 2.31 2,81 (±0.23) P. cicada 2.97 2.56 (±0.35) 0.17 0.45 (±0.07) 0.17 1.98 2.31 P. crombiei 2.86 (±0.24) 2.52 (±0.24) 0.18 (±0.12) 0.25 (±0.12) 0.07 2.4 (±0.35) 2.99 (±0.43) P. gracilis 3.47 (±0.23) 3.63 0.3 (±0.05) 0.46 (±0.05) 0.2 (±0.05) 2.97 3.3 P. irroratus 3.14 (±0.23) 2.48 (±0.23) 0.17 0.4 0.2 (±0.05) 2.23 (±0.12) 2.64 P. maximus 4.29 3.8 (±0.23) 0.33 0.66 0.28 (±0.07) 3.3 3.8 (±0.23) P. rupestris 3.63 3.14 (±0.23) 0.28 (±0.07) 0.61 (±0.07) 0.25 (±0.12) 2.89 (±0.12) 3.63 P. signifer 3.63 (±0.47) 2.97 0.21 (±0.02) 0.36 (±0.05) 0.18 (±0.02) 2.31 2.31 P. soaresi 3.3 2.97 0.17 0.53 0.13 2.48 2.64
