PREDAÇÃO E DEFESA EM ANUROS: REVISÃO, DESCRIÇÃO E EVOLUÇÃO LUÍS FELIPE TOLEDO Tese apresentada ao Instituto de Biociências da Universidade Estadual Paulista “Julio de Mesquita Filho”, Campus de Rio Claro,para a obtenção do título de Doutor em Ciências Biológicas (Área de Concentração:Zoologia) Rio Claro Estado de São Paulo – Brasil Agosto de 2007 PREDAÇÃO E DEFESA EM ANUROS: REVISÃO, DESCRIÇÃO E EVOLUÇÃO LUÍS FELIPE TOLEDO Orientador: Prof. Dr. CÉLIO FERNANDO BAPTISTA HADDAD Tese apresentada ao Instituto de Biociências da Universidade Estadual Paulista “Julio de Mesquita Filho”, Campus de Rio Claro,para a obtenção do título de Doutor em Ciências Biológicas (Área de Concentração:Zoologia) Rio Claro Estado de São Paulo – Brasil Agosto de 2007 i FEAR OF THE DARK Tammy Akeo Adapted by Sombra In the night, the “cururu frog” runs Looking back, jump after jump, Hoping not to see anything. Its eyes tremble in fear as it slows Searching the dark for its predators. The frog watches the dark just as the predator watches the frog. The eyes of the predator dance as the frog moves, Carefully watching each and every motion. The frog scans the black around him, Quickly analyzing all that it sees. The frog is safe as long as its eyes don’t see the predator’s. Nothing catches the frog eyes, and it lets out a sigh of relief. Then the frog hears it, the sound of breathing, Slow and steady it turns around Wide-eyed with fear And looks into the eyes that have watched it. A smile spreads across his face realizing the game is over. The frog eyes, wide with terror, stare back at his finally. His eyes gazed deep into the frog To a place no one is allowed. Now cornered, the frog turns to the predator with begging eyes, Longing to be somewhere else, anywhere but here. And now, if you where the cururu, what should you do? ii AGRADECIMENTOS Ao prof. Célio Fernando Baptista Haddad a quem devo em muito pelo que hoje sei sobre anfíbios, pelo suporte, orientação e amizade, principalmente durante os infinitos cafezinhos que tomamos... Aos pesquisadores, herpetólogos e colegas de laboratório que contribuíram constantemente (trazendo bichos, conversando, sugerindo, etc...) para minha formação, seja no campo, em laboratório ou no bar; principalmente: André Pardal Antunes, Anne d’Heursel e Flávio Baldisseri, Ariovaldo Cruz Neto, Carlos Jared e Martinha, Cinthia Brasileiro, Cynthia Prado, Daniel Loebmann, Denis Andrade, Dina, Fausto Nomura, Ingrid, Itamar Martins, Ivan Sazima, João Kiwi Giovanelli, João Portuga Alexandrino e Maria Guimarães, Julian Faivovich, Juliana Zina, Kelly Zamudio e Harry Greene, Lorena Guimarães, Luís Giasson, Márcio Martins, Marcos Grid-Papp, Olívia Araújo, Otávio Marques, Paulo Perereca Garcia, Ricardo Ribeiro, Ricardo Sawaya, Rodrigo Lingnau, Rogério Bastos, Tiago Gomes, Tiago Vasconcelos e Vanessa. Ao pessoal extracurricular que sempre me acompanhou nas horas vagas: Milho Xangrilá, Fábio Longarina e TC, Prima, Lye, Akio, Cauré, Yara, Sabrina, Ariane, Du Murakami, Indra Rani e Olívia, Totó, Gaúcho e Jose, Tozetti, Cynthia e Zara, Leandrão e Priscila, Joana e Luís, Tati Tiemi, Ana Têta, Bomba, Paul, Ganso, Júlia, Natália, Michel, Thaís Kubick, Alê, Érika, Poli, Ju, Fer, Gabi, Vagninho, Toninho, Vanessa e Daniel, Marquinhos, Dirceu e a toda a galera do Sujinho’s e de todas as noitadas inimagináveis. A todos os alunos das UNESPs de Rio Claro e Jaboticabal pelo que me ensinaram nas minhas aulas, especialmente com suas dúvidas capciosas. Aos meus sócios da Fauna Pro, BH e Denis, e outros parceiros, principalmente Marina e Sueli, que sempre tornaram o campo inusitado e possibilitaram diversas viagens pelo Brasil, fundamental para minha tese. Ao povo de sampa, principalmente Alexsandra, Quito, Gus, Raf’s, Amaral, Ivan, Limão, Evandro e Bel, os quais eternamente farão parte de minhas conquistas. À Olívia por tudo que me ensinou, pelo companheirismo e amor, os quais parecem ser infinitos. Por todas as nossas passagens. A toda minha família, mas essencialmente aqueles sem os quais tudo ficaria muito mais difícil: Regina, Cris, Neide, Iza, Jair, Eliza e Raphael. Por fim, à CAPES pela bolsa concedida. iii ÍNDICE Resumo ................................................................................................................ Abstract ................................................................................................................ Introdução Geral .................................................................................................. Material e métodos .............................................................................................. Resultados ............................................................................................................ CAPÍTULO 1: Anuran egg predators and the evolution of reproductive modes CAPÍTULO 2: Predation of juvenile and adult anurans by invertebrates: current knowledge and perspectives …................................................................ CAPÍTULO 3: Anurans as prey: an exploratory analysis and size relationships between predators and their prey ………………………………………………. CAPÍTULO 4: When frogs scream! A review of anuran defensive vocalizations …………………………………………………………...………. CAPÍTULO 5: Behavioral defenses of anurans: an overview …………………. CAPÍTULO 6: Colors and mimicry as defensive strategies of anurans .………. Considerações Finais ........................................................................................... 001 002 003 006 010 017 051 065 101 151 207 237 1 RESUMO GERAL Até a presente tese, a informação sobre predação e estratégias defensivas em anuros estava fragmentada e desconexa na literatura científica. Na ausência de uma revisão sobre o tema, algumas especulações foram geradas baseadas nas impressões pessoais de diversos pesquisadores. Por exemplo, existem muitos ou poucos relatos de anuros sendo apresados? Um determinado comportamento defensivo já foi descrito em algum lugar, ou é inédito? Qual a relação entre os predadores e os mecanismos de defesa dos anuros? Essas e outras perguntas estavam em aberto. Mesmo em livros texto, os quais geralmente revisam os assuntos abordados de forma abrangente, nota-se o parco conhecimento sobre o tema, sendo estes sempre os menores capítulos dos livros e de conteúdo razoavelmente superficial. Todavia, muita informação já foi gerada e muita ainda está por vir. É nesse sentido que idealizamos e realizamos o presente estudo, visando reunir grande parte do conhecimento atual e gerar novas previsões e hipóteses testáveis. Assim, relacionamos os predadores atuais e naturais dos anfíbios anuros (incluindo as desovas e pós-metamórficos) e revisamos as principais estratégias defensivas dos adultos (pós-metamórficos). Muitos dados apresentados são inéditos e outros compilados da literatura, mas ambos analisados de maneira integrada e sempre dando enfoque evolutivo nas discussões apresentadas. Consideramos este estudo um ponto inicial para compreendermos mais profundamente as estratégias defensivas dos anuros e sua relação com os predadores naturais. 2 ABSTRACT Until the present moment, the information about defensive strategies and predation upon anurans was fragmented and disconnected in the scientific literature. In the absence of an overview of the subject, some speculations have been raised based on personal points of view of several scientists. For example, are there many or few reports of predation upon anurans? A specific defensive behavior has already been described or not? How is the relationship between the defensive strategies and predator mechanisms? These and odder questions were hard to answer. Even in text books, where the subjects are treated in a broad way we can notice the poor knowledge of the subject and these are always the shorter and superficial chapters. However, many information is already available and many is about to come. Therefore, we idealized and did the present thesis, aiming to joint a large part of the current knowledge and promoting some previsions and testable hypotheses. So, we related the actual and natural predators of anurans (including eggs and post-metamorphics) and reviewed the main defensive strategies of the adults (post-metamorphics). A great amount of the data presented is novel and other set of data were found in the available literature, but both were analyzed simultaneously with an evolutive approach. We consider this thesis a starting point of a deeper comprehension of the anurans’ defensive strategies and their relationship with natural predators. 3 INTRODUÇÃO Anfíbios anuros são apresados por uma série de animais, desde pequenos invertebrados (e.g., Toledo, 2003) a vertebrados de grande porte (e.g., Martins et al., 1993; Canale & Lingnau, 2003), provavelmente em decorrência de sua grande abundância na natureza, tamanho relativamente pequeno e pele macia (Duellman & Trueb, 1994). Sendo assim, ao longo de sua história evolutiva, a intensa pressão seletiva causada pela predação, deve estar intimamente relacionada ao surgimento de uma grande diversidade de estratégias defensivas, observadas nas espécies atuais (e.g., Edmunds, 1974; Ryan, 1985; Hödl & Amézquita, 2001). Tais adaptações podem ser categorizadas como ecológicas, morfológicas, morfofisiológicas e/ou comportamentais. Como estratégias defensivas ecológicas, destacam-se a utilização de abrigos durante o repouso (e.g., Stewart & Rand, 1991; Michael, 1997) ou durante a atividade (e.g., vocalização: Hartmann, 2004) e o fato de que muitas espécies investem em uma prole numerosa e possuem modos reprodutivos que podem conferir proteção contra predação (e.g., Heyer, 1969; Haddad & Sawaya, 2000). Quanto à morfologia, considera-se que o padrão de coloração dos indivíduos atua como elemento defensivo primário ou secundário e ocorre de diferentes maneiras. A mais difundida entre os anuros é a camuflagem (Hödl & Amézquita, 2001), a qual pode imitar o padrão de cores e formas do hábitat em que a espécie ocorre, ou atribui aos indivíduos um padrão diruptivo (Duellman & Trueb, 1994). Existem também padrões de coloração que podem confundir os predadores ao dar-lhes a impressão de que a presa é maior do que seu tamanho real (referências em Duellman & Trueb, 1994). Ademais, o polimorfismo (e.g., Hoffman & Blouin, 2000; Bourne, 2001), o mimetismo e/ou o aposematismo (e.g., Symula et al., 2001; Vences et al., 2003) também atuam como estratégias defensivas contra predadores visualmente orientados (Duellman & Trueb, 1994). Além do padrão de coloração, algumas características morfológicas também podem atuar como causadoras de padrões diruptivos ou de camuflagem. Diversas espécies possuem estruturas dérmicas (e.g., chifres, pregas tarsais e apêndices calcâneos) que modificam o contorno do corpo dificultando sua localização por predadores (Sazima, 1978; Duellman & Trueb, 1994). 4 Dentre os recursos defensivos morfofisiológicos, o mais difundido é a presença de glândulas epidérmicas (revisão em Toledo & Jared, 1995), as quais podem secretar, por exemplo, substâncias adesivas (Manzanilla et al., 1998; Kwet & Solé, 2002), odoríferas (Sazima, 1974; Waye & Shewchuk, 1995; Grant, 2001; Kizirian et al., 2003) e/ou tóxicas, de irritantes (Jazen, 1962; Powell & Lieb, 2002) a letais (Rabor, 1952; Daly & Meyers, 1967; Tokuyama & Daly, 1983). Em alguns casos, essas secreções revelaram-se eficazes contra diversos predadores, tais como anfíbios (Formanowicz Jr. & Brodie Jr., 1979), répteis (Brodie Jr., 1978; Manzanilla et al., 1998), aves (Brodie Jr. & Nussbaum, 1987) e mamíferos (Brodie Jr. & Formanowicz Jr., 1981; Pearl & Hayes, 2002). Contudo, em muitas outras situações, as toxinas secretadas parecem não conferir proteção aos anuros, sendo estes apresados por insetos, peixes, anfíbios, répteis e aves (ver Cardoso & Sazima, 1976; Haddad & Bastos, 1997; Cochran & Cochran, 2003). Ademais, alguns predadores apresentam estratégias comportamentais e fisiológicas especializadas para a dieta de anuros potencialmente venenosos (ver Frazer, 1973). Todos os mecanismos defensivos mencionados acima podem ou devem ser executados através de comportamentos simples ou elaborados. Alguns comportamentos estão associados à morfologia, como direcionar as glândulas e/ou regiões com coloração aposemática em direção ao possível predador (Hanson & Vial, 1956; Sazima & Caramaschi, 1986; Torr, 1991; Williams et al., 2000), ou realizar posturas em que padrões diruptivos se acentuem (Sazima, 1978; Rocha et al., 1998; Garcia, 1999). Caracteres morfológicos como espinhos e dentes, além de suas funções normais (e.g., estímulo sexual e alimentação, respectivamente), também podem ser utilizados contra predadores em potencial (Vaz-Ferreira & Gehrau, 1975; Hartmann et al., 2003). Algumas das estratégias defensivas são comuns a muitas espécies, como tanatose (Zamprogno et al., 1998; Abbadié-Bisogno et al., 2001; Gramapurohit et al., 2001), inflar o corpo (Hödl & Amézquita, 2001) e emitir gritos de agonia (Sazima, 1975; Hödl & Gollmann, 1986; Azevedo-Ramos, 1995; Williams et al., 2000). Outras estratégias talvez sejam comuns a todas as espécies de anuros, como, por exemplo, o comportamento de fuga (Duellman & Trueb, 1994; Williams et al., 2000). Por outro lado, existem estratégias que são conhecidas apenas para algumas espécies (ver Channing & Howell, 2003; Hartmann et al., 2003). 5 Além de variar de maneira interespecífica, alguns comportamentos defensivos podem variar de maneira intraespecífica. Neste último caso podem variar ao longo da distribuição geográfica da espécie (Bjager, 1980; Williams et al., 2000) ou conforme a lateralidade dos indivíduos (Robins et al., 1998). Alguns comportamentos estão relacionados ao posicionamento das glândulas secretoras de veneno (Sazima & Caramaschi, 1986; Williams et al., 2000), outros estão relacionados à filogenia dos taxa envolvidos (Summers & Colugh, 2001; Hödl & Amézquita, 2001) e outros consistem de convergências etológicas entre espécies ecologicamente semelhantes (Sazima, 1975; Garcia, 1999). A execução de comportamentos defensivos pode estar ainda relacionada a condições momentâneas, como condições fisiológicas (Gomes et al., 2002), durante o cuidado parental (Vaz-Ferreira & Gehrau, 1975; Giaretta & Cardoso, 1995; Toledo et al., 2004) ou durante as agregações reprodutivas (Tuttle et al., 1982). Algumas das estratégias defensivas possuem nomes específicos, como tanatose (Hartmann et al., 2003; McCallum et al., 2003), comportamento de fuga (McCallum et al., 2003) ou mordidas (Giaretta & Cardoso, 1995; Hartmann et al., 2003). Todavia, muitos dos comportamentos defensivos registrados ainda não possuem nomes específicos, havendo necessidade de realizar uma descrição sucinta toda vez que nos referimos a estes. Este é, por exemplo, o caso do comportamento de esticar as pernas traseiras para trás e manter o corpo achatado rente ao solo (e.g., Sazima, 1975; Garcia, 1999), o comportamento de entrelaçar as pernas e erguê-las, mantendo as costas em contato com o solo (Channing & Howell, 2003), ou o comportamento manter a porção anterior do corpo em contato com o solo e erguer a porção posterior do corpo (Sazima & Caramaschi, 1988; Kizirian, 2003). Ademais, poucos são os estudos que avaliaram a eficácia das estratégias defensivas utilizadas pelos anuros (Sazima, 1974; Formanowicz & Brodie, 1979; Manzanilla et al., 1998; Rödel & Braun, 1999; Pearl & Hayes, 2002) e quase nada se conhece sobre a evolução dos diferentes comportamentos defensivos (e.g., Williams et al., 2000). Neste contexto, o presente estudo realiza uma revisão dos comportamentos defensivos conhecidos para diferentes famílias de anuros; descreve comportamentos inéditos; sugere nomes categóricos (em Inglês a princípio) apropriados a cada um dos comportamentos abordados; realiza um mapeamento dos comportamentos sobre árvores filogenéticas atuais (e.g., Faivovich et al., 2005; Frost et al., 2006; Grant et al., 2006) 6 para inferir sobre a origem dos comportamentos defensivos (e.g., origem filogenética vs. convergência ecológica); e levanta hipóteses sobre a real eficiência dos comportamentos na presença de predadores em potencial. MATERIAL & MÉTODOS Área de Estudo Para a realização do presente estudo, além de informações extraídas da literatura, de relatos de inúmeros pesquisadores (mencionados nos respectivos capítulos) e de animais vivos encaminhados ao laboratório de herpetologia, foram realizadas diversas coletas em campo, de acordo com a disponibilidade de recursos financeiros e tempo. Os 56 municípios visitados (em 14 Estados) estão listados a seguir. Entre parênteses estão algumas localidades específicas. ALAGOAS: Passo de Camarajibe; AMAZONAS: Manaus e Presidente Figueiredo; BAHIA: Caraíva, Feira de Santana, Ilhéus, Una, Uruçuca, Salvador (capital e praia do forte) e Sooretama; ESPÍRITO SANTO: Anchieta, Aracruz, Conceição da Barra e Jaquaré; GOIÁS: Alto Paraíso (Vale da Lua e Chapada dos Veadeiros) e São João D’Aliança; MINAS GERAIS: Camanducaia (Monte Verde), Grão Mogol, Pirapora, São Roque de Minas (Serra da Canastra), Santana do Riacho (Serra do Cipó) e São Tomé das Letras; MATO GROSSO DO SUL: Três Lagoas; PARÁ: Belém; PARANÁ: São José dos Pinhais e Tijucas do Sul; PERNAMBUCO: Fernando de Noronha e Tamandaré; RIO GRANDE DO SUL: São Francisco de Paula; SANTA CATARINA: Angelina, Itapema, Lages, Mafra, Rancho Queimado e Treviso; SERGIPE: Itabaiana; SÃO PAULO: Apiaí e Iporanga (PETAR), Barra do Turvo (PEJ), Bertioga, Botucatu, Campinas (Barão Geraldo), Campos do Jordão, Cananéia (PEIC), Cotia, Iguape (PEJ), Itirapina (EEI), Pilar do Sul, Piracicaba, Ribeirão Branco, Rio Claro (FEENA, MSJ e Itapé), Santa Rita do Passa Quatro, São Luiz do Paraitinga (PESM-NSV), São Sebastião (Maresias), Sorocaba, Ubatuba (PEIA e PESM-NP). 7 Coleta de dados A cada encontro com anfíbios anuros na natureza foram registrados dados gerais, como: I) a localidade e data; II) bioma e microambiente ocupado; III) período da observação (diurno ou noturno); IV) temperatura do ar; V) espécie; VI) comprimento rostro-cloacal (CRC: medido com paquímetro de 0,05 mm de precisão); VII) sexo e classe de idade do indivíduo (juvenil ou adulto) (ver ficha de campo). Com relação ao comportamento foram registrados: I) a atividade do anuro no momento do encontro; II) a reação do anuro à aproximação do pesquisador; III) a reação durante a tentativa ou captura efetiva do indivíduo; e IV) a reação do indivíduo capturado a estímulos provocados pelo pesquisador. Estes estímulos variaram de caso a caso sendo os mais comuns a: sacudida, pressão nas pernas, toques na cabeça no corpo ou próximos à boca, virar o anuro de barriga para cima, realizar movimentos bruscos com as mãos ou objetos em direção aos indivíduos, embora sem tocá-los. Essas formas de estímulo já foram utilizadas anteriormente e costumam gerar bons resultados (e.g., Hödl & Gollmann, 1986; Toledo et al., 2005). Nenhum desses estímulos causou injúrias aos anuros, os quais foram libertados (na maioria dos casos) em ambiente natural após a estimulação. Em seguida foram observados por mais cerca de três minutos, período em que ainda podem desempenhar comportamentos defensivos (Bajger, 1980). Foram também provocados encontros em laboratório entre os anuros e serpentes não peçonhentas, predadores em potencial. Para tanto, serpentes encontradas nos ambientes estudados foram apresentadas aos anuros dentro de viveiros, sendo registrados os comportamentos realizados pelos anuros frente ao encontro, ataque (quando houver) e subjugação (quando houver). Foram também registradas as reações das serpentes frente ao repertório defensivo apresentado pelos anuros. Os experimentos foram realizados no laboratório de Herpetologia e Jacarezário, vinculados ao Departamento de Zoologia da UNESP em Rio Claro, nos quais já são mantidas diversas espécies de serpentes que se alimentam de anuros em ambiente natural (e.g., Chironius spp. e Liophis spp.). Somente foram coletados, transportados, anestesiados, fixados e depositados na coleção de anuros CFBH do Departamento de Zoologia da UNESP de Rio Claro, os indivíduos que necessitaram de confirmação de identificação. Autorizações de captura e 8 transporte de anfíbios e répteis foram concedidas pelo Centro de Conservação e Manejo de Répteis e Anfíbios do IBAMA (processo número: 02010.001495/04-32). Durante a aproximação ou manipulação dos anuros, tanto por parte do pesquisador como por parte de predadores, podem ser emitidas vocalizações, tais como cantos de soltura (que aparentemente não possuem caráter defensivo), gritos de agonia e gritos de alarme. Nestes casos as vocalizações serão gravadas com gravador cassete Marantz PMD222 e microfone externo direcional Audiotecnica AT835b. As análises de som foram realizadas através do programa Raven 1.2.1 configurado a 16 bits de resolução, 44,1 kHz de freqüência de amostragem e “FFT” e “frame length” a 256. As vocalizações serão descritas e as terminologias utilizadas seguirão as adotadas por Duellman & Trueb (1994). C ol et or es : L . F . T . & _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ _; D at a: _ __ _ / _ __ _ / _ __ _ L oc al id ad e: _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ T em p. a r: _ __ __ __ _ ºC E sp éc ie : _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ _ S ex o/ I da de : _ __ __ __ _ C R C : _ __ __ __ __ __ m m ; P es o: __ __ __ __ _g ; M ic ro am bi en te :_ __ __ __ __ __ __ __ __ __ __ _ A ti vi da de : _ __ __ __ __ __ __ C ol or aç ão : A po sm tc C am uf ld o ut ro : _ __ __ __ __ __ _ R ea çã o à ap ro xi m aç ão : Im óv el F ug a o ut ro :_ __ __ __ __ __ __ __ __ __ __ __ __ __ _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ R ea çã o ao m an us ei o: _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ T es te p ar a T an at os e: n ão s im – T ip o: I (q q je it o) I I (f ec ha di nh o) O lh o: F ec ha do a be rt o – O B S : _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ T es te p ar a G ri to A go ni a: n ão s im – B oc a a be rt a f ec ha da . T es te p ar a __ __ __ __ __ __ __ _: n ão s im : _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ T oq ue s em _ __ __ __ __ __ __ __ ( pa rt e do c or po ): R ea çã o: _ __ __ __ __ __ __ __ __ __ __ _ T ip o de S ec re çã o: O do r G ru de nt a T óx ic a M uc os a o ut ra : _ __ __ __ __ __ __ O B S : _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ C ol et or es : L . F . T . & _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ _; D at a: _ __ _ / _ __ _ / _ __ _ L oc al id ad e: _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ T em p. a r: _ __ __ __ _ ºC E sp éc ie : _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ _ S ex o/ I da de : _ __ __ __ _ C R C : _ __ __ __ __ __ m m ; P es o: __ __ __ __ _g ; M ic ro am bi en te :_ __ __ __ __ __ __ __ __ __ __ _ A ti vi da de : _ __ __ __ __ __ __ C ol or aç ão : A po sm tc C am uf ld o ut ro : _ __ __ __ __ __ _ R ea çã o à ap ro xi m aç ão : Im óv el F ug a o ut ro :_ __ __ __ __ __ __ __ __ __ __ __ __ __ _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ R ea çã o ao m an us ei o: _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ T es te p ar a T an at os e: n ão s im – T ip o: I (q q je it o) I I (f ec ha di nh o) O lh o: F ec ha do a be rt o – O B S : _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ T es te p ar a G ri to A go ni a: n ão s im – B oc a a be rt a f ec ha da . T es te p ar a __ __ __ __ __ __ __ _: n ão s im : _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ T oq ue s em _ __ __ __ __ __ __ __ ( pa rt e do c or po ): R ea çã o: _ __ __ __ __ __ __ __ __ __ __ _ T ip o de S ec re çã o: O do r G ru de nt a T óx ic a M uc os a o ut ra : _ __ __ __ __ __ __ O B S : _ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ __ 10 RESULTADOS Os resultados da presente tese estão organizados em capítulos que já foram ou estão sendo preparados para publicação em revistas especializadas. Cada capítulo dará origem a um artigo. Assim, esta tese resultou nos seguintes capítulos/artigos: 1. Toledo, L. F. Araújo, O. G. S., Vonesh, J. & Haddad, C. F. B. Anuran egg predators and the evolution of reproductive modes. South American Journal of Herpetology, submitted. 2. Toledo, L. F. 2005. Predation of juvenile and adult anurans by invertebrates: current knowledge and perspectives. Herpetological Review, 36(4): 395-400. 3. Toledo, L. F., Silva, R. R. & Haddad, C. F. B. 2007. Anurans as prey: an exploratory analysis and size relationships between predators and their prey. Journal of Zoology, 271: 170-177. 4. Toledo, L. F. & Haddad, C. F. B. When frogs scream! A review of anuran defensive vocalizations. Herpetological Journal, submitted. 5. Toledo, L. F., Sazima, I. & Haddad, C. F. B. Behavioral defenses of anurans: an overview. In preparation. 6. Toledo, L. F. & Haddad, C. F. B. Colors and mimicry as defensive strategies of anurans. Journal of Zoology, submitted. 11 LITERATURA CITADA Abbadié-Bisogno, K., Oliver-López, L. & Ramírez-Bautista, A. 2001. Bufo occidentalis (Pine Toad). Death feigning. Herpetological Review 32(4): 247. Azevedo-Ramos, C. 1995. Defensive behaviors of the Neotropical treefrog Hyla geographica (Anura, Hylidae). Revista Brasileira de Biologia 55(1): 45-47. Bjager, J. 1980. Diversity of defensive responses in populations of fire toads (Bombina bombina and Bombina variegata). Herpetologica 36(2): 133-137. Bourne, G. R. 2001. Color pattern, predator avoidance, and foraging behavior in the golden frog Colostethus beebei (Anura: Dendrobatidae). Herpetological Review 32(4): 225-228. Brodie Jr., E. D. 1978. The antipredator functions of Dendrobates auratus (Amphibia, Anura, Dendrobatidae) skin secretion in regard to a snake predator (Thamnophis). Journal of Herpetology 12(2): 264-265. Brodie Jr., E. D. & Formanowicz Jr., D. R. 1981. Palability and antipredator behavior of the treefrog Hyla versicolor to the shrew Blarina brevicauda. Journal of Herpetology 15(2): 235-236. Brodie Jr., E. D. & Nussbaum, R. A. 1987. Antipredator responses of Rana tigerina to a crow. Herpetological Review 18(1): 8-9. Canale, G. & Lingau, R. 2003. Hyla biobeba. Predation. Herpetological Review 34(2): 136. Cardoso, A. J. & Sazima, I. 1976. Batracofagia na fase adulta e larvária da rã-pimenta, Leptodactylus labyrinthicus (Spix, 1824) - Anura, Leptodactylidae. Ciência e Cultura 29(10): 1130-1132. Channing, A. & Howell, K. 2003. Phlyctimantis keithae (wot-wot). Defensive bahavior. Herpetological Review 34(1): 51-52. Cochran, P. A. & Cochran, J. A. 2003. Pseudacris crucifer (Spring Beeper). Predation. Herpetological Review 34(4): 360. Daly, J. W. & Meyers, C. W. 1967. Toxicity of Panamanian poison frogs (Dendrobates): some biological and chemical aspects. Science 156: 970-973. Duellman, W. E. & Trueb, L. 1994. Biology of amphibians. Baltimore: John Hopkins University Press, Baltimore and London. 2ed. 670p. 12 Edmunds, M. 1974. The evolution of predator-prey systems. Pp. 226-287. In: Defense in animals: a survey of antipredator defenses. Longman. Faivovich, J., C. F. B. Haddad, P. C. A. Garcia, D. R. Frost, J. A. Campbell, and W. C. Wheeler. 2005. Systematic review of the frog family Hylidae, with special reference to Hylinae: phylogenetic analysis and taxonomic revision. Bulletin of the American Museum of Natural History 294: 1-240. Formanowicz Jr., D. R. & Brodie Jr., E. D. 1979. Palatability and antipredator behavior of selected Rana to Shrew Blarina. The American Midland Naturalist 101(2): 456- 458. Frazer, J. F. D. 1973. Amphibians. VI + 122pp. Wykeham Publ. Ltd. Londres. Frost, D. R., Grant, T., Faivovich, J., Bain, R. H., Haas, A., Haddad, C. F. B., Sá, R. O., Channing, A., Wilkinson, M., Donnellan, S. C., Raxworthy, C. J., Campbell, J. A., Blotto, B. L., Moler, P., Drews, R. C., Nussbaum, R. A., Lynch, J. D., Green, D. M. & Wheeler, W. C. 2006. Amphibian tree of life. Bulletin of the American Museum of Natural History 297: 1-371. Garcia, P. C. A. 1999. Scytrophrys sawayae (NCN). Defensive behavior. Herpetological Review 30(4): 224. Giaretta, A. A. & Cardoso, A. 1995. Reproductive behavior of Cycloramphus dubius Miranda-Ribeiro (Amphibia, Anura, Leptodactylidae). Revista Brasileira de Zoologia 12(2): 229-232. Gomes, F. B., Bevier, C. & Navas, C. A. 2002. Environmental and physiological factors influence antipredator behavior in Scinax hiemalis (Anura: Hylidae). Copeia 2002(4): 994-1005. Gramapurohit, N. P., Shanbhag, B. A. & Saidapur, S. K. 2001. Rana curtipes (Bicolored Frog). Death feigning. Herpetological Review 32(2): 103. Grant, J. B. 2001. Rana palustris (Pickerel Frog). Production of odor. Herpetological Review 32(2): 183. Grant, T., D. R. Frost, J. P. Caldwell, R. Gagliardo, C. F. B. Haddad, P. J. R. Kok, D. B. Means, B. P. Nooman, W. E. Schargel, and W. C. Wheeler. 2006. Phylogenetic systematics of dart-poison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae). Bulletin of the American Museum of Natural History 299: 1-262. 13 Haddad, C. F. B. & Bastos, R. P. 1997. Predation on the toad Bufo crucifer during reproduction (Anura; Bufonidae). Amphibia-Reptilia 18: 295-298. Haddad, C. F. B. & Sawaya, R. J. 2000. Reproductive modes of Atlantic Forest hylid frogs: a general overview and the description of a new mode. Biotropica 32(4b): 862–871. Hanson, J. A. & Vial, J. L. 1956. Defensive behavior and effects of toxins in Bufo alvarius. Herpetologica 1956(12): 141-149. Hartmann, M. T. 2004. Biologia reprodutiva de uma comunidade de anfíbios anuros na Mata Atlântica. Tese de doutorado em Zoologia [não publicada] – Universidade Estadual Paulista, Rio Claro, São Paulo. Hartmann, M. T., Hartmann, P. A., Prado, C. P. A. & Garcia, P. C. A. 2003. Cycloramphus boraceiensis (Flattened waterfall frog) Defensive behavior. Herpetological Review 34(1): 50. Heyer, W. R. 1969. The adaptive ecology of the species groups of the genus Leptodactylus (Amphibia, Leptodactylidae). Evolution 23: 421-428. Hödl, W. & Amézquita, A. 2001. Visual signaling in anuran amphibians. In: Anuran communication: 121-141. M. J. Ryan (Ed.). Smithsonian Institution Press, Washington. Hödl, W. & Gollmann, G. 1986. Distress calls in Neotropical frogs. Amphibia-Reptilia 7: 11-21. Hoffman, E. A. & Blouin, M. S. 2000. A review of colour and pattern polymorphisms in anurans. Biological Journal of the Linnean Society 70: 633-665. Jazen, D. H. 1962. Injury caused by toxic secretions of Phrynohyas spilomma Cope. Copeia 1962(3): 651. Kizirian, D., Coloma, L. A. & Paredes-Recalde, A. 2003. A new treefrog (Hylidae: Hyla) from southern Ecuador and a description of its antipredator behavior. Herpetologica 59(3): 339-349. Kwet, A. & Solé, M. 2002. Elachistocleis erythrogaster (Red-bellied oval frog). Defensive behavior. Herpetological Review 33: 46. Manzanilla, J., La Marca, E., Villareal, O. & Sanchez, D. 1998. Phrynohyas venulosa (Veined treefrog, “Rana lechosa”). Antipredador device. Herpetological Review 29(1): 39-40. 14 Martins, M., Sazima, I. & Egler, S. G. 1993. Predators of the nest building gladiator frog, Hyla faber, in southeastern Brazil. Amphibia-Reptilia 14: 307-309. McCallum, M. L., Klotz, T. L., Trauth, S. E. 2003. Rana sylvatica (Wood frog). Death feigning. Herpetological Review 34(1): 54-55. Michael, S. F. 1997. Vocalization and diurnal retreat defense in the Puerto Rican Frog Eleuterodactylus cochranae. Journal of Herpetology 31(3): 453-456. Pearl, C. A. & Hayes, M. P. 2002. Predation by oregon sppoted frogs (Rana pretiosa) on western toads (Bufo boreas) in Oregon. The American Midland Naturalist 147(1): 145-152. Powell, R. L. & Lieb, C. S. 2002. Hyla arenicolor (canyon tree frog). Toxic skin secretions. Herpetological Review 34(3): 230. Rabor, D. S. 1952. Preliminary notes on the giant toad, Bufo marinus (Linn.), in the Philippine Islands. Copeia 1952(4): 281-282. Robins, A., G. Lippolist, A. Bisazza, G. Vallortigara & L. J. Rogers (1998). Lateralized agonistic responses and hindlimb use in toads. Animal Behaviour 56: 875-881. Rocha, C. F. D., Sluys, M. V., Bergallo, H. G., Alves, A. S. & Vrcibradic, D. 1998. Zachenus parvulus (Leaf frog). Defensive bahavior and color pattern. Herpetological Review 29(4): 232-233. Rödel, M. O. & Braun, U. 1999. Associations between anurans and ants in a West African Savanna (Anura: Microhylidae, Hyperoliidae, and Hymenoptera: Formicidae). Biotropica 31(1): 178-183. Ryan, M. J. 1985. Costs of reproduction: predation. In: The Túngara Frog: a study in sexual selection and communication. The University of Chicago Press, Chicago and London, Pp. 163-185. Sazima, I. 1974. Experimental predation on the leaf-frog Phyllomedusa rohdei by the water snake Liophis miliaris. Journal of Herpetology 8(4): 376-377. Sazima, I. 1975. Distress call in newly metamorphosed smith frog, Hyla faber Wied. Herpetologica 31(4): 471-472. Sazima, I. 1978. Convergent defensive behavior of two leaf-litter frog of southeastern Brazil. Biotropica 10(2): 158. 15 Sazima, I. & Caramaschi, U. 1986. Descrição de Physalaemus deimaticus, sp. n., e observações sobre comportamento deimático em P. nattereri (Steindn.) - Anura, Leptodactylidae. Revista de Biologia 13(1-4): 91–101. Stewart, M. M. & A. S. Rand (1991). Vocalizations and the defensive retreat sites by male and female frogs, Eleutherodactylus coqui. Copeia 1991: 1013-1024. Summers, K. & Clough, M. E. 2001. The evolution of coloration and toxicity in the poison frog family (Dendrobatidae). PNAS 98(11): 6227-6232. Symula, R., Schulte, R. & Summers, K. 2001. Molecular phylogenetic evidence for a mimetic radiation in Peruvian poison frogs supports a Müllerian mimicry. Proc. R. Soc. Lond. B 268: 2415-2421. Tokuyama, T. & Daly, J. W. 1983. Steroidal alkaloids (batrachotoxins and 4 - hydroxybatrachotoxins), "indole alkaloids" (calycanthine and chimonanthine) and a piperidinyldipyridin 39(1): 41–47. Toledo, L. F. 2003. Predation on seven South American anuran species by water bugs (Belostomatidae). Phyllomedusa 2(2): 105-108. Toledo, L. F., L. D. Guimarães, L. P. Lima, R. P. Bastos & C. F. B. Haddad (2004). Notes on courtship, egg-laying site, and defensive behavior of Epipedobates flavopictus (Anura: Dendrobatidae) from two mountain ranges of central and southeastern Brazil. Phyllomedusa 3: 145-147. Toledo, L. F., Tozetti, A. & Zina, J. 2005. Leptodactylus labyrinthicus (Pepper Frog): Defensive Repertoire. Herpetological Bulletin 90: 29-31. Toledo, R. C. & Jared, C. 1995. Cutaneous granular glands and amphibian venoms. Comparative Biochemistry and Physiology 111A(1): 1-29. Torr, G. A. 1991. Uperoleia laevigata (NCN). Behavior. Herpetological Review 22(4): 129-130. Tuttle, M. D., Taft, L. K. & Ryan, M. J. 1982. Evasive behaviour of a response to bat predation. Animal Behaviour 30: 393-397. Vaz-Ferreira, R. & Gehrau, A. 1975. Comportamiento epimeletico de la rana comun, Leptodactylus ocellatus (L.) (Amphibia, Leptodactylidae) I. Atencion de la cria y actividades alimentares y agressivas relacionadas. Physis, seccion B 34(88): 1-14. 16 Vences, M., J. Kosuch, R. Boistel, C. F. B. Haddad, E. La Marca, S. Lötters & M. Veith (2003). Convergent evolution of aposematic coloration in Neotropical poison frogs: a molecular phylogenetic perspective. Org. Divers. Evol. 3: 215-226. Waye, H. L. & Shewchuk, C. H. 1995. Scaphiopus intermontanus (great basin spadefoot). Production of odor. Herpetological Review 26(2): 98-99. Williams, C. R., Brodie, E. D., Tyler, M. J. & Walker, S. J. 2000. Antipredator mechanisms of Australian frogs. Journal of Herpetology 34(3): 431-443. Zamprogno, C., Zamprogno, M. G. F. & Teixeira, R. L. 1998. Bufo paracnemis (sapo- boi). Death feigning. Herpetological Review 29(2): 96-97. CAPÍTULO 1 PREDADORES DOS OVOS DE ANUROS E A EVOLUÇÃO DOS MODOS REPRODUTIVOS Luís Felipe Toledo, Olívia Gabriela S. Araújo, James R. Vonesh & Célio F. B. Haddad Harry Greene, 1997 17 CAPÍTULO 1 ANURAN EGG PREDATORS AND THE EVOLUTION OF REPRODUCTIVE MODES Luís Felipe Toledo1, Olívia Gabriela S. Araújo1, James R. Vonesh2 & Célio F. B. Haddad1 1Departamento de Zoologia, Instituto de Biociências, Unesp, Rio Claro, São Paulo, Caixa Postal 199, CEP 13506-970, Brazil. E-mail: toledolf2@yahoo.com 2Department of Biology, Virginia Commonwealth University, 1000 West Cary Street, P.O. Box 842012, Richmond, VA 23284-2012, USA. 18 ABSTRACT While anurans face stage-specific predators throughout ontogeny, embryonic stages may be particularly vulnerable due to their more limited suite of anti-predator responses. Some authors have suggested that the evolution of more terrestrial reproductive strategies in anurans (e.g., arboreal or terrestrial eggs, direct development) is an adaptive response to selection by aquatic egg predators. Thus, if current predation is indicative of the selective pressures that shaped these life history strategies, we would predict that the eggs of species with aquatic reproductive strategies would experience greater predation than those of species with more derived reproductive strategies. Here we review published studies of egg predation in anurans to evaluate whether there is evidence that aquatic eggs are more vulnerable to predation. Furthermore, we listed the actual anuran egg predators, found the main predators, and evaluated the effectiveness of some egg laying sites. Eggs deposited in the water and not in foam nests were the most preyed. The family Brachycephalidae was much less preyed than expected, and it could reflect ineffective field observations and/or positive effectiveness of their reproductive strategy: laying eggs with a patchy distribution on the forest floor, in cryptic places, and out of the water. Therefore, we present a review that supports the hypothesis of selective pressures in favour of the egg-laying out of the water. 19 RESUMO Anuros enfrentam diferentes predadores ao longo de suas fases ontogenéticas, das quais a fase de ovos deve ser particularmente vulnerável devido à sua limitação de respostas defensivas. Alguns autores sugerem que a evolução de desovas fora de corpos d’água (e.g., no solo, em árvores ou por desenvolvimento direto) é uma resposta adaptativa à seleção exercida pelos predadores aquáticos. Assim, se a predação observada atualmente é um indicativo de pressão seletiva que moldou essas estratégias reprodutivas, nós poderíamos prever que ovos depositados em água sejam mais apresados do que aqueles com estratégias reprodutivas alternativas. Assim, nós revisamos os estudos sobre predação de desovas para avaliar se existe evidência que suporte que os ovos depositados na água sejam mais apresados que os ovos depositados fora da água. Além disso, nós listamos os predadores conhecidos de ovos de anuros, identificamos os principais predadores e inferimos sobre o sucesso de determinadas estratégias reprodutivas. Os ovos depositados na água e não em ninho de espuma foram os mais apresados dentre todas as combinações de estratégias. Os ovos de indivíduos da família Brachycephalidae foram menos apresados do que o esperado; isto poderia estar relacionado com um viés de observação em campo, ou realmente condizer com um maior sucesso adquirido pelas estratégias reprodutivas adotadas por este grupo: depositar ovos de maneira distribuída pelo chão das florestas, em locais crípticos e fora da água. Assim, apoiamos a sugestão de uma pressão para a deposição de ovos fora da água. 20 INTRODUCTION The embryonic stage of anuran development may be the life history stage most vulnerable to predation (Hödl, 1986; Chivers et al., 2001). Eggs are externally fertilized, lack shells, and are often deposited in the environment without the benefit of parental care (e.g., only 10% of frogs species have been reported to exhibit parental care; Duellman and Trueb, 1986; Haddad and Prado, 2005). Furthermore, relative to later stages, embryos have a more limited suite of anti-predator defences. It has been suggested that several reproductive modes (currently there are 39 recognized reproductive modes in anurans, the greatest diversity among tetrapods: Haddad and Prado, 2005) have evolved in response to selective pressures exerted by aquatic egg predation (Downie, 1990; Magnusson and Hero, 1991; Martins, 1993; Haddad and Sawaya, 2000; Prado et al., 2002). In leptodactylids there is a trend to lay eggs in foam nests or in terrestrial environments, with the most ancestral strategy, eggs laid directly in the water, restricted to a few groups (e.g., Prado et al., 2002). Similarly, in some hylid and hyperoliid frogs, eggs are laid arboreally, frequently on leaves or wrapped within them (e.g., Duellman and Trueb, 1994; De la Riva, 1999; Prado et al., 2006). This shift toward non-aquatic reproductive modes is primarily found in tropical taxa and has been hypothesized to be driven by the combination of reduced desiccation risk in the humid tropics, a way to escape disturbance by water turbulence, and high levels of aquatic egg predation (e.g., Heyer, 1969; Magnusson and Hero, 1991; Haddad and Prado, 2005). Selection by predators is also thought to have driven the evolution of parental care as well as other defensive traits in several species (e.g., in mantellids: Lehtinen, 1993; leptodactylids: Martins, 2001; and aromobatids: Bourne et al., 2001; Toledo et al., 2004); toxic eggs (review in Gunzburger and Travis, 2005); plasticity in the timing of anuran eggs hatching (Warkentin, 1995; 2000; Chivers et al., 2001); and plasticity in breeding behaviors, e.g., selecting a safer oviposition site (Holomuzki, 1995; Spieler and Linsenmair, 1997; Summers, 1999; Lips, 2001). While the selective pressures of embryonic predators may be a good explanation for the evolution of some specialized reproductive modes and plastic responses to egg predators, the relationship remains equivocal. While the strength of past egg predation 21 is unknown, it is worth noting that egg predation in species with derived reproductive strategies can also be very high (Duellman and Trueb, 1994; Vonesh 2000; 2005). Magnusson and Hero (1991) attempted to demonstrate that aquatic predators have exerted and continue to exert selective pressure on the evolution of terrestrial oviposition strategies in anurans, however a recent reanalysis of these data revealed no significant relationship (Haddad and Prado, 2005). Besides reducing egg predation, non-aquatic oviposition strategies may have other fitness benefits, e.g., secure egg masses to a homogeneous and immobile substrate, which could also improve hatching success (Richards, 1993). Furthermore, laying eggs in foam nests, instead of in gelatinous masses, may have several other functions. For example, foam nests may provide a source of food, sheltering, an adequate temperature, water balance, and oxygen supply (Gorzula, 1977; Downie, 1990; Haddad and Prado, 2005 and references therein). Consequently, it is likely that different selective pressures (including predation) act in the evolution of reproductive modes (Heyer, 1969; Magnusson and Hero, 1991; Prado et al., 2002; Haddad and Prado, 2005). Here we review the scientific literature regarding embryonic predation in anurans to help elucidate general patterns across anurans. We were interested in exploring the following questions; 1) which predator taxa are responsible for most anuran egg predation and 2) how does that vary with anuran reproductive strategy. By reviewing these studies we hope to generate insights on the relation between predation and reproductive modes in anurans and improve discussion about the role of predator pressure on the evolution of the reproductive modes (e.g., Heyer, 1969; Magnusson and Hero, 1991; Prado et al., 2002). MATERIAL AND METHODS We compiled studies that report egg predation by searching in web-based- databases and by performing an exhaustive reading of the most accessible herpetological journals (e.g., Amphibia-Reptilia, Copeia, Herpetologica, Herpetological Journal, Herpetological Review, and Journal of Herpetology). For each study, we recorded the name and taxonomic group of the prey and predator species, the anuran 22 egg laying site, (i.e., aquatic, arboreal, terrestrial, or subterranean); and the spawn type, (i.e., eggs in a gelatinous mass or in foam nests). Specific names of the amphibians (both preys and predators) and number of species in each family follow Frost (2006). The specific names of the non-amphibian predators are the same as presented in the original publications. We did not include studies that failed to report prey and/or predator identities (e.g., Kaiser and Gibson, 2004). Experimental studies were not considered in most of the analysis; in some experimental studies the predator and its prey do not co-exist in nature, so this may produce unrealistic data (see discussion in Gunzburger and Travis, 2005). RESULTS We found 363 reports of anuran egg predation (APPENDIX I), including experimental studies (N = 225) and natural observations in the field (N = 138; Fig. 1). From these data we recognized 23 taxonomic groups of predators (Table1). In observational field studies of naturally occurring egg predation, dipterans larvae were the most common invertebrate (46.8 %) and anuran larvae the most common vertebrate predators (42.1 %) with anuran larvae being the most common predators over all (23.2 %; Fig. 2). About 67 % of the predators are typically terrestrial (e.g., primates, canids, snakes, anurans, spiders, and dipterans) and the remaining 33 % are aquatic (e.g., fishes, tadpoles, salamander larvae, and crustaceans). Approximately 72 % of the preyed eggs were involved with a gelatinous mass (Fig. 3A) and about 59 % were laid in the water (Fig. 3B). About 38 % of the natural observations involved species that lay eggs in aquatic and gelatinous egg masses (AGEM). Almost 20 % of the reports on egg predation were on hylid eggs followed by leptodactylid (ca. 14 %), ranid (ca. 13 %), and hyperoliid (ca. 12 %). The remaining nine anuran families corresponded to about 41 % of the reports (Fig. 4). The number of species in each anuran family was positively correlated with the number of reports of egg predation within the family (linear regression analysis: r2 = 0.33; df = 14; P = 0.026; Fig. 5). The point related to the family Brachycephalidae was an outlier very distant from the 95 % confidence interval (Fig. 5). 23 Table 1. Anuran egg predator groups, number of predation reports (N = 363), number of predator species (N = 157), and predator habitat (based on the species listed in appendix I). This table includes experimental studies and field observations. Predator Group Number of reports (number of predator species) Predator most typical habitat Invertebrates Hirudinea 6 (5) Aquatic Platyhelminthes 2 (1) Terrestrial Arachnida 3 (2) Terrestrial Gastropoda 1 (1) Terrestrial Crustacea 5 (5) Aquatic Insecta Coleoptera 16 (9) Terrestrial Diptera 33 (10) Terrestrial Hymenoptera 15 (10) Terrestrial Hemiptera 13 (9) Aquatic Odonata 8 (5) Aquatic Orthoptera 1 (1) Terrestrial Tricoptera 2 (2) Terrestrial Vertebrates Pisces 65 (19) Aquatic Urodela Adults 30 (14) Terrestrial Larvae 4 (1) Aquatic Anura Adults 15 (10) Terrestrial Tadpoles 109 (45) Aquatic Reptile Serpentes 9 (7) Terrestrial Testudines 16 (2) Aquatic Aves 1 (1) Mammals Canidae 1 (1) Terrestrial Primates 7 (2) Terrestrial Rodentia 1 (1) Terrestrial 24 Figure 1. Predation on anuran eggs by invertebrates and vertebrates. A) Foam nest of Leptodactylus labyrinthicus being preyed by an ant (Camponotus rufipes); arboreal nests of Dendropsophus ebraccatus being preyed by B) social ants (Azteca sp.) and C) a wasp (Polybia rejecta); and D) an arboreal nest of Hyperolius spinigularis being preyed by another tree frog (Afrixalus fornasini). Pictures of L. F. Toledo (A), J. Touchon (B and C), and J. R. Vonesh (D). 25 0 5 H ir u d in e a P la ty h e lm in th e s A ra c h n id a C ru s ta c e a D ip te ra H e m ip te ra H y m e n o p te ra O d o n a ta O rt h o p te ra T ri c o p te ra P is c e s U ro d e la ( a d u lts ) U ro d e la la rv a e A n u ra ( a d u lts ) A n u ra ( ta d p o le s ) S e rp e n te s A v e s Group of predator 10 15 20 25 C a n id a e P ri m a te s N u m b e r o f p re d a tio n r e p o rt s ( % ) Figure 2. Percentage of preyed clutches (in natural conditions) by different groups of predators (N = 138). Figure 3. Percentage of preyed clutches (in natural conditions) in relation to A) the clutch characteristics and B) the egg laying sites (N = 138). 0 20 40 60 80 F o a m n e s t G e la ti n o u s e g g m a s s N u m b e r o f p re d a ti o n r e p o rt s ( % ) 0 20 40 60 80 S u b te rr a n e a n T e rr e s tr ia l A rb o re a l A q u a ti c 26 0 5 10 15 20 A rt h ro le p ti d a e B ra c h y c e p h a lid a e B u fo n id a e C e n tr o le n id a e D e n d ro b a ti d a e D ic ro g lo s s id a e H y lid a e H y p e ro lii d a e L e iu p e ri d a e L e p to d a c ty lid a e L im n o d y n a s ti d a e M ic ro h y lid a e P e lo b a ti d a e R a n id a e R h a c o p h o ri d a e S c a p h io p o d id a e Anuran families N u m b e r o f p re d a tio n r e p o rt s ( % ) Figure 4. Percentage of preyed clutches over the 16 anuran families based on the 138 natural observations presented in the Appendix I. Figure 5. Liner regression (solid line) between number of species within an anuran family (accordingly to current systematics: Frost, 2006) and number of predation reports for each family. Doted line shows the 95 % of confidence interval. Art: Arthroleptidae, Bra: Brachycephalidae, Buf: Bufonidae, Cen: Centrolenidae, Den: Dendrobatidae, Dic: Dicroglossidae, Hyl: Hylidae, Hyp: Hyperoliidae, Lei: Leiuperidae, Lep: Leptodactylidae, Lim: Limnodynastidae, Mic: Microhylidae, Pel: Pelobatidae, Ran: Ranidae, Rha: Rhacophoridae, Sca: Scaphiopodidae. DISCUSSION 27 Our review covered a wide range of anuran taxa and the positive relationship found between species in the anuran families and reports in the families indicates that we collected a good sample of what we may find in nature. Although the majority of the predators listed are typically terrestrial, the aquatic ones probably exert the greatest predation pressure, based on the highest number of predation events observed in natural conditions. Looking across predator taxa and embryonic habitats, the main predators of anuran eggs appear to be anuran larvae. In some cases, reports of egg predation may represent feeding on trophic ovules deposited in the nests to feed tadpoles (e.g., Kam et al., 1996; Prado et al., 2005 and references therein). However, in most of the cases, tadpoles are carnivores that prey upon other species clutches (e.g., Downie, 1990; Shepard and Caldwell, 2005) or even conspecific eggs (e.g., Polis and Meyers, 1985; Hearnden, 1991; Prado et al., 2005). By revising the anuran reproductive modes, different authors considered that the mode represented by aquatic and gelatinous egg masses is the generalized and ancestral, called as reproductive mode 1 (reviews in Duellman and Trueb, 1994; Haddad and Prado, 2005). Hence, the other modes (e.g., in foam nests or out of the aquatic environment) have been differentiated from mode 1. Furthermore, it has been suggested that the differentiation of modes was caused by different selective pressures, including an attempt to reduce the predation risk (Downie, 1990; Magnusson and Hero, 1991; Martins, 1993; Haddad and Sawaya, 2000; Prado et al., 2002; Haddad and Prado, 2005). The same scenario may be suggested from our results: the reproductive mode 1 (sensu Haddad and Prado, 2005) accumulated the greater number of reports of predation. It could be a sign of the greater predation pressure on eggs of this mode, resulting in a greater number of observations and, consequently, publications. Therefore, laying eggs out of natural water bodies, i.e., in arboreal, subterranean, terrestrial, or even in constructed nests in the margins of water bodies, may notably prevent egg predation. On the other hand, one could state that our findings are circumstantial because aquatic and gelatinous egg masses (AGEM) are easier to be observed in nature. Although, it could be true when comparing with the probability of finding subterranean eggs, but it could not be when comparing with arboreal eggs and aquatic foam nests. In the first case, most of the clutches are laid on the vegetation associated to the margins of the water bodies. The difficulty in finding them is similar to the difficulty in finding 28 aquatic eggs (person. obs.). In the second case, the foam nests are even easier to find than AGEM (person. obs.). However, a stronger criticism that may arise is that the reproductive mode 1 is the most widespread among the anurans, probably because it is the ancestral mode (Haddad and Prado, 2005), and hence it is the most observed in nature. This fact could produce a larger number of reports of predation of eggs placed in AGEM. The outlier point of the family Brachycephalidae in Fig. 5 may rely on an adaptive hypothesis. Most, if not all of brachycephalid species, lay their eggs on the ground, generally under fallen leaves in the forest floor (Duellman and Trueb, 1994). This strategy makes difficult for researches to observe predation events. However, it could also effectively prevent eggs from predation as the eggs are laid in cryptic places in an unpredicted random patchy distribution on the forest floor. Actually, the lack of predation reports in this family could be a combination of all these factors. The same short number of predation reports in relation to the number of species in the family was observed to adult individuals (Toledo et al., 2007). Hence, if there is an effective defence involved in terrestrial nesting and in a random patchy distribution pattern of clutches and adults brachycephalids, it would, in part, explain the evolutionary success of the family, expressed in the huge number of species (see also Toledo et al., 2007). Tadpoles and post-metamorphic anurans also face several different predators (reviews in Gunzburger and Travis, 2005; Toledo, 2005; Toledo et al., 2007). However, they can avoid predators by many behavioural and physiological adaptations (Duellman and Trueb, 1994). On the other hand, the defensive mechanisms of eggs are limited. By reviewing the egg predation literature we were able to recognize basically four defensive strategies for anuran eggs: 1) eggs can be unpalatable (review in Gunzburger and Travis, 2005) or difficult to be preyed upon (Grubb, 1972; Orians and Janzen, 1974); 2) eggs may be laid in cryptic sites (including egg crypsis) (e.g., Heyer, 1969); 3) eggs can be placed out of the water or in foam nests (e.g., Heyer, 1969); and 4) embryos may immaturely hatch in the presence of the predator (e.g., Warkentin, 1995; 2000). All these strategies may occur lonely or jointly. From this point we lack some other beta-analysis involving the reports of egg predation and experiments to address further questions, such as: in which scale are the specialized reproductive modes effective against predation? Are there specializations 29 among predators to prey eggs of species with specialized reproductive modes? Although we can not answer entirely these questions, our review improved the knowledge on the subject and provides substantial material to continue studying the relation of reproductive modes and predation. ACKNOWLEDGEMENTS Cynthia P. A. Prado made valuable comments during early versions of the manuscript; Kelly Zamudio and Harry Greene helped with the patterns of North American anuran egg laying sites and characteristics; and Justin Touchon provided unpublished data and pictures. FAPESP (BIOTA proc. no. 01/13341-3) and CNPq supported the Herpetology lab, Departamento de Zoologia, Unesp, Rio Claro, State of São Paulo, Brazil. 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R ep or ts ( N = 3 63 ) of a nu ra ns t ha t ha d th ei r eg gs p re ye d (N = 1 07 s pp ), e gg l ay in g si te ( aq ua ti c: Q ; ar bo re al : R ; te rr es tr ia l: T ; or su bt er ra ne an : S ), c lu tc h ty pe ( ge la ti no us m as s: G ; fo am n es ts : F ), a nd t he r es pe ct iv e pr ed at or s (N = 1 57 s pp ). A n as te ri sk ‘ *’ a ft er a nu ra n sp ec ie s na m es in di ca te s ex pe ri m en ta l s tu di es . A nu ra n sp ec ie s (p re y) Sp aw n ty pe P re da to r sp ec ie s P re da to r gr ou p So ur ce A R T H R O L E PT ID A E ( 1 sp .) A rt h ro le p ti s sy lv a ti ca Q / G A m b ys to m a o p a cu m U ro de la W al te rs ,1 97 5 A rt h ro le p ti s sy lv a ti ca Q / G G er ri s b u en o i H em ip te ra E at on a nd P as zk ow sk i, 19 99 A rt h ro le p ti s sy lv a ti ca Q / G G er ri s p in g re en si s H em ip te ra E at on a nd P as zk ow sk i, 19 99 A rt h ro le p ti s sy lv a ti ca Q / G L im n ep h il u s sp . T ri co pt er a S te in ,1 98 5 B O M B IN A T O R ID A E ( 1 sp .) B o m b in a v a ri eg a te * Q / G R a n a t em p o ra ri a T ad po le H eu ss er ,1 97 0 B R A C H Y C E P H A L ID A E ( 3 sp p. ) E lu th er o d a ct yl u s co q u i T / G M eg a se li a s ca la ri s D ip te ra V il la a nd T ow ns en d, 1 98 3 E le u th er o d a ct yl u s g u en th er i T / G E ch in a n th er a c ep h a lo st ri a ta S er pe nt es M ou ra -L ei te e t a l. , 2 00 3 E le u th er o d a ct yl u s sp . T / G R h a d in a ea l a ch ry m a n s Se rp en te s Q ui ja no a nd R oj as , 1 99 5 E le u th er o d a ct yl u s sp . T / G R h a d in a ea b il in ea ta S er pe nt es S az im a et a l. , 1 99 2 E le u th er o d a ct yl u s sp . T / G L ep to ti la c a ss in ii A ve s P ou li n et a l. , 2 00 1 B U FO N ID A E ( 8 sp p. ) A n a xy ru s a m er ic a n u s* Q / G A m b ys to m a o p a cu m U ro de la W al te rs ,1 97 5 A n a xy ru s a m er ic a n u s* Q / G N o to p h th a lm u s vi ri d es ce n s U ro de la W al te rs ,1 97 5 A n a xy ru s a m er ic a n u s* Q / G A rt h ro le p ti s sy lv a ti ca T ad po le P et ra nk a et a l. , 1 99 4 A n a xy ru s b o re a s* Q / G A m b ys to m a g ra ci le U ro de la L ic ht ,1 96 9 A n a xy ru s b o re a s* Q / G G a st er o st eu s a cu le a tu s P is ce s L ic ht ,1 96 9 A n a xy ru s b o re a s* Q / G H a em o p si s sp . H ir ud in ea L ic ht , 1 96 9 A n a xy ru s b o re a s* Q / G S a lm o c la rk ii P is ce s L ic ht ,1 96 9 B u fo b u fo * Q / G A es h n a sp . O do na ta H en ri ck so n, 19 90 B u fo b u fo * Q / G C o ri xa d en ti p es H em ip te ra H en ri ck so n, 1 99 0 B u fo b u fo * Q / G C ym a ti a b o n sd o rf fi H em ip te ra H en ri ck so n, 1 99 0 B u fo b u fo * Q / G D ys ti cu s la p p o n ic u s C ol eo pt er a H en ri ck so n, 1 99 0 B u fo b u fo * Q / G G la en o co ri st a p ro p in q u a H em ip te ra H en ri ck so n, 1 99 0 B u fo b u fo * Q / G L eu co rr h in ia d u b ia O do na ta H en ri ck so n, 19 90 B u fo b u fo * Q / G N o to n ec ta g la u ca H em ip te ra H en ri ck so n, 1 99 0 39 B u fo b u fo * Q / G R h a n tu s ex o le tu s C ol eo pt er a H en ri ck so n, 1 99 0 B u fo b u fo * Q / G L is so tr it o n h el ve ti cu s U ro de la D en to n an d B ee be e, 1 99 1 B u fo b u fo * Q / G L is so tr it o n v u lg a ri s U ro de la D en to n an d B ee be e, 1 99 1 B u fo b u fo * Q / G L is so tr it o n v u lg a ri s U ro de la H en ri ck so n, 19 90 B u fo b u fo * Q / G R a n a t em p o ra ri a T ad po le H eu ss er ,1 97 0 B u fo t er re st ri s Q / G ( in si de ov ar iu m ) B u fo t er re st ri s T ad po le B ab bi tt ,1 99 5 C h a u n u s m a ri n u s* Q / G L a cc o tr ep h es sp . H em ip te ra C ro ss la nd a nd A lf or d, 1 99 8 C h a u n u s m a ri n u s* Q / G C yb is te r sp . C ol eo pt er a C ro ss la nd a nd A lf or d, 1 99 8 C h a u n u s m a ri n u s* Q / G C yb is te r g o d ef fr o yi C ol eo pt er a C ro ss la nd a nd A lf or d, 1 99 8 C h a u n u s m a ri n u s* Q / G H yd a ti cu s vi tt a tu s C ol eo pt er a C ro ss la nd a nd A lf or d, 1 99 8 C h a u n u s m a ri n u s* Q / G S a n d ra co tt u s b a ke w el li C ol eo pt er a C ro ss la nd a nd A lf or d, 1 99 8 C h a u n u s m a ri n u s* Q / G L et h o ce ru s in su la n u s H em ip te ra C ro ss la nd a nd A lf or d, 1 99 8 C h a u n u s m a ri n u s* Q / G M a cr o b a tr a ch iu m sp . C ru st ac ea C ro ss la nd a nd A lf or d, 1 99 8 C h a u n u s m a ri n u s* Q / G H o lt h u is a n a sp . C ru st ac ea C ro ss la nd a nd A lf or d, 1 99 8 C h a u n u s m a ri n u s* Q / G C h er a x q u a d ri ca ri n a tu s C ru st ac ea C ro ss la nd a nd A lf or d, 1 99 8 C h a u n u s m a ri n u s* Q / G A u st ro p ep le a l es so n i G as tr op od a C ro ss la nd a nd A lf or d, 1 99 8 C h a u n u s m a ri n u s* Q / G C ra te ro ce p h a lu s st er cu sm u sc a ru m P is ce s C ro ss la nd a nd A lf or d, 1 99 8 C h a u n u s m a ri n u s Q / G C h a u n u s m a ri n u s T ad po le H ea rn de n, 19 91 C h a u n u s m a ri n u s* Q / G L it o ri a b ic o lo r A nu ra C ro ss la nd a nd A lf or d, 1 99 8 C h a u n u s m a ri n u s* Q / G L it o ri a r u b el la A nu ra C ro ss la nd a nd A lf or d, 1 99 8 C h a u n u s m a ri n u s* Q / G L it o ri a i n fr a fr en a ta A nu ra C ro ss la nd a nd A lf or d, 1 99 8 C h a u n u s m a ri n u s* Q / G L it o ri a a lb o g u tt a ta T ad po le C ro ss la nd ,1 99 8 C h a u n u s m a ri n u s* Q / G L it o ri a a lb o g u tt a ta A nu ra C ro ss la nd a nd A lf or d, 1 99 8 C h a u n u s m a ri n u s* Q / G L im n o d yn a st es o rn a tu s T ad po le C ro ss la nd ,1 99 8 C h a u n u s m a ri n u s* Q / G L im n o d yn a st es o rn a tu s A nu ra C ro ss la nd a nd A lf or d, 1 99 8 C ra n o p si s va ll ic ep s* Q / G G a m b u si a a ff in is P is ce s G ru bb ,1 97 2 C ra n o p si s va ll ic ep s* Q / G Ic ta lu ra s m el a s P is ce s L ic ht ,1 96 8 C ra n o p si s va ll ic ep s* Q / G L ep o m is c yn el lu s P is ce s L ic ht ,1 96 8 C ra n o p si s va ll ic ep s* Q / G L ep o m is m eg a lo ti s P is ce s L ic ht ,1 96 8 C ra n o p si s va ll ic ep s* Q / G N ot id en ti fi ed m ou se R od en ti a L ic ht , 1 96 8 40 E p id a le a c a la m it a Q / G L is so tr it o n b o sc a i U ro de la T ej ed o, 19 91 E p id a le a c a la m it a Q / G T ri tu ru s p yg m a eu s U ro de la T ej ed o, 19 91 E p id a le a c a la m it a Q / G B u fo b u fo T ad po le B an ks a nd B ee be e, 1 98 7 E p id a le a c a la m it a Q / G E p id a le a c a la m it a T ad po le B an ks a nd B ee be e, 1 98 7 E p id a le a c a la m it a * Q / G P el o b a te s cu lt ri p es T ad po le T ej ed o, 19 91 E p id a le a c a la m it a Q / G P el o b a te s cu lt ri p es T ad po le T ej ed o, 19 91 E p id a le a c a la m it a * Q / G P el o d yt es p u n ct a tu s T ad po le T ej ed o, 19 91 E p id a le a c a la m it a Q / G P el o d yt es p u n ct a tu s T ad po le T ej ed o, 19 91 E p id a le a c a la m it a * Q / G R a n a d a lm a ti n a T ad po le H eu ss er ,2 00 1 E p id a le a c a la m it a * Q / G R a n a t em p o ra ri a T ad po le H eu ss er ,1 97 0 E p id a le a c a la m it a Q / G R a n a t em p o ra ri a T ad po le B an ks a nd B ee be e, 1 98 7 E p id a le a c a la m it a * Q / G L is so tr it o n h el ve ti cu s U ro de la D en to n an d B ee be e, 1 99 1 E p id a le a c a la m it a * Q / G L is so tr it o n v u lg a ri s U ro de la D en to n an d B ee be e, 1 99 1 R h in el la m a rg a ri ti fe ra Q / G L ep to d a ct yl u s p en ta d a ct yl u s T ad po le W el ls ,1 97 9 C E N T R O L E N ID A E ( 5 sp p. ) C en tr o le n e p ro so b le p o n R / G S ib o n a rg u s S er pe nt es R ya n an d L ip s, 2 00 4 C en tr o le n e p ro so b le p o n R / G C u p ie n n u s sp . A ra ch ni d H ay es , 1 98 3 C o ch ra n el la g ra n u lo sa R / G S es a rm a r o b er ti C ru st ac ea H ay es , 1 98 3 H ya li n o b a tr a ch iu m c o ly m b ip h yl lu m R / G N ot id en ti fi ed H ym en op te ra M cD ia rm id , 1 97 8; V il la e t a l. , 1 98 2 H ya li n o b a tr a ch iu m c o ly m b ip h yl lu m R / G P o ly b ia s p. H ym en op te ra D ra ke a nd R an ve st el , 2 00 5 H ya li n o b a tr a ch iu m f le is ch m a n n i R / G C u p ie n n u s sp . A ra ch ni d H ay es , 1 98 3 H ya li n o b a tr a ch iu m f le is ch m a n n i R / G P a ro ec a n th u s ti b ia li s O rt ho pt er a H ay es , 1 98 3 H ya li n o b a tr a ch iu m f le is ch m a n n i R / G D ro so p h il a sp . D ip te ra V il la , 1 97 7 H ya li n o b a tr a ch iu m f le is ch m a n n i R / G Z yg o th ri ch a sp . D ip te ra V il la , 1 97 8; 1 98 0; V il la a nd T ow ns en d, 1 98 3 H ya li n o b a tr a ch iu m p u lv er a tu m R / G D ro so p h il a sp . D ip te ra V il la , 1 97 7 D E N D R O B A T ID A E ( 2 sp p. ) O o p h a g a p u m il io Q / G O o p h a g a p u m il io T ad po le W ey go ld t, 19 80 ; B ru st , 1 99 3 R a n it o m ey a v en tr im a cu la ta Q / G R a n it o m ey a v en tr im a cu la ta T ad po le S um m er s, 1 99 9 D IC R O G L O SS ID A E ( 2 sp .) H o p lo b a tr a ch u s o cc ip it a li s Q / G H o p lo b a tr a ch u s o cc ip it a li s T ad po le S pi el er a nd L in se nm ai r, 1 99 7 H o p lo b a tr a ch u s ti g er in u s Q / G H ir u d a b ir m a n ic a H ir ud in ea M cC an n, 1 93 2 H Y L ID A E ( 32 s pp .) 41 A cr is c re p it a n s* Q / G G a m b u si a a ff in is P is ce s G ru bb ,1 97 2 A g a ly ch n is a n n a e* R / G M eg a se li a s ca la ri s D ip te ra V il la a nd T ow ns en d, 1 98 3 A g a ly ch n is c a ll id ry a s R / G D ro so p h il a s p. D ip te ra V il la , 1 97 7 A g a ly ch n is c a ll id ry a s R / G N ot id en ti fi ed H ym en op te ra V il la et a l. , 1 98 2 A g a ly ch n is c a ll id ry a s R / G A g el a ia sp . H ym en op te ra W ar ke nt in ,2 00 0 A g a ly ch n is c a ll id ry a s R / G P o ly b ia r ej ec ta H ym en op te ra W ar ke nt in , 2 00 0 A g a ly ch n is c a ll id ry a s R / G L ep to d ei ra s ep te n tr io n a li s S er pe nt es W ar ke nt in , 1 99 5; 2 00 0 A g a ly ch n is c a ll id ry a s R / G S ib o n a rg u s S er pe nt es R ya n an d L ip s, 2 00 4 A g a ly ch n is c a ll id ry a s* R / G K in o st er n o n l eu co st o m u m T es tu di ne s R ob er ts , 1 99 4 A g a ly ch n is c a ll id ry a s* R / G R h in o cl em m ys f u n er ea T es tu di ne s R ob er ts , 1 99 4 A g a ly ch n is c a ll id ry a s* R / G L ep to d a ct yl u s p en ta d a ct yl u s T ad po le R ob er ts ,1 99 4 A g a ly ch n is c a ll id ry a s* R / G A g a ly ch n is c a ll id ry a s T ad po le R ob er ts ,1 99 4 A g a ly ch n is c a ll id ry a s* R / G A g a ly ch n is c a lc a ri fe r T ad po le R ob er ts ,1 99 4 A g a ly ch n is c a ll id ry a s* R / G D en d ro p so p h u s eb ra cc a tu s T ad po le R ob er ts ,1 99 4 A g a ly ch n is c a ll id ry a s* R / G R iv u lu s is th m en si s P is ce s R ob er ts ,1 99 4 A g a ly ch n is c a ll id ry a s* R / G R h a m d ia g u a te m a le n si s P is ce s R ob er ts ,1 99 4 A g a ly ch n is c a ll id ry a s* R / G A . fa sc ia tu s P is ce s R ob er ts ,1 99 4 A g a ly ch n is c a ll id ry a s* R / G P h o li s g il li P is ce s R ob er ts ,1 99 4 A g a ly ch n is s a lt a to r R / G P o ly b ia cf .r ej ec ta H ym en op te ra W ar ke nt in , 2 00 0 A g a ly ch n is s a lt a to r* R / G K in o st er n o n l eu co st o m u m T es tu di ne s R ob er ts , 1 99 4 A g a ly ch n is s a lt a to r* R / G R h in o cl em m ys f u n er ea T es tu di ne s R ob er ts , 1 99 4 A g a ly ch n is s a lt a to r* R / G L ep to d a ct yl u s p en ta d a ct yl u s T ad po le R ob er ts ,1 99 4 A g a ly ch n is s a lt a to r* R / G A g a ly ch n is c a ll id ry a s T ad po le R ob er ts ,1 99 4 A g a ly ch n is s a lt a to r* R / G A g a ly ch n is c a lc a ri fe r T ad po le R ob er ts ,1 99 4 A g a ly ch n is s a lt a to r* R / G D en d ro p so p h u s eb ra cc a tu s T ad po le R ob er ts ,1 99 4 A g a ly ch n is s a lt a to r* R / G R iv u lu s is th m en si s P is ce s R ob er ts ,1 99 4 A g a ly ch n is s a lt a to r* R / G R h a m d ia g u a te m a le n si s P is ce s R ob er ts ,1 99 4 A g a ly ch n is s a lt a to r* R / G A st ya n a x fa sc ia tu s P is ce s R ob er ts ,1 99 4 A g a ly ch n is s a lt a to r* R / G P h o li s g il li P is ce s R ob er ts ,1 99 4 D en d ro p so p h u s eb ra cc a tu s R / G D ro so p h il a sp . D ip te ra V il la ,1 97 7 D en d ro p so p h u s eb ra cc a tu s R / G A g el a ia sp . H ym en op te ra W ar ke nt in , 2 00 0 D en d ro p so p h u s eb ra cc a tu s R / G A zt ec a sp . H ym en op te ra J. T ou ch on , u np ub l. da ta 42 D en d ro p so p h u s eb ra cc a tu s R / G P o ly b ia r ej ec ta H ym en op te ra J. T ou ch on , u np ub l. da ta D en d ro p so p h u s eb ra cc a tu s* R / G K in o st er n o n l eu co st o m u m T es tu di ne s R ob er ts , 1 99 4 D en d ro p so p h u s eb ra cc a tu s* R / G R h in o cl em m ys f u n er ea T es tu di ne s R ob er ts , 1 99 4 D en d ro p so p h u s eb ra cc a tu s* R / G L ep to d a ct yl u s p en ta d a ct yl u s T ad po le R ob er ts ,1 99 4 D en d ro p so p h u s eb ra cc a tu s* R / G A g a ly ch n is c a ll id ry a s T ad po le R ob er ts ,1 99 4 D en d ro p so p h u s eb ra cc a tu s* R / G A g a ly ch n is c a lc a ri fe r T ad po le R ob er ts ,1 99 4 D en d ro p so p h u s eb ra cc a tu s* R / G D en d ro p so p h u s eb ra cc a tu s T ad po le R ob er ts ,1 99 4 D en d ro p so p h u s eb ra cc a tu s* R / G R iv u lu s is th m en si s P is ce s R ob er ts ,1 99 4 D en d ro p so p h u s eb ra cc a tu s* R / G R h a m d ia g u a te m a le n si s P is ce s R ob er ts ,1 99 4 D en d ro p so p h u s eb ra cc a tu s* R / G A st ya n a x fa sc ia tu s P is ce s R ob er ts ,1 99 4 D en d ro p so p h u s eb ra cc a tu s* R / G P h o li s g il li P is ce s R ob er ts ,1 99 4 D en d ro p so p h u s m in u tu s Q / G L ep to d a ct yl u s la b yr in th ic u s T ad po le S he pa rd a nd C al dw el l, 20 05 D en d ro p so p h u s p h le b o d es * Q / G K in o st er n o n l eu co st o m u m T es tu di ne s R ob er ts , 1 99 4 D en d ro p so p h u s p h le b o d es * Q / G R h in o cl em m ys f u n er ea T es tu di ne s R ob er ts , 1 99 4 D en d ro p so p h u s p h le b o d es * Q / G L ep to d a ct yl u s p en ta d a ct yl u s T ad po le R ob er ts ,1 99 4 D en d ro p so p h u s p h le b o d es * Q / G A g a ly ch n is c a ll id ry a s T ad po le R ob er ts ,1 99 4 D en d ro p so p h u s p h le b o d es * Q / G A g a ly ch n is c a lc a ri fe r T ad po le R ob er ts ,1 99 4 D en d ro p so p h u s p h le b o d es * Q / G D en d ro p so p h u s eb ra cc a tu s T ad po le R ob er ts ,1 99 4 D en d ro p so p h u s p h le b o d es * Q / G R iv u lu s is th m en si s P is ce s R ob er ts ,1 99 4 D en d ro p so p h u s p h le b o d es * Q / G R h a m d ia g u a te m a le n si s P is ce s R ob er ts ,1 99 4 D en d ro p so p h u s p h le b o d es * Q / G A . fa sc ia tu s P is ce s R ob er ts ,1 99 4 D en d ro p so p h u s p h le b o d es * Q / G P h o li s g il li P is ce s R ob er ts ,1 99 4 D en d rp o so p h u s ru b ic u n d u lu s Q / G L ep to d a ct yl u s la b yr in th ic u s T ad po le S he pa rd a nd C al dw el l, 20 05 H yl a a rb o re a Q / G R a n a t em p o ra ri a T ad po le H eu ss er ,1 97 0 H yl a c h ry so sc el is * Q / G G a m b u si a a ff in is P is ce s G ru bb ,1 97 2 H yl a c h ry so sc el is * Q / G Il yb iu s sp . C ol eo pt er a R es et ar it s, 1 99 8 H yl a c h ry so sc el is * Q / G P a ch id ip la x lo n g ip in n is O do na te R es et ar it s, 19 98 H yl a v es ic o lo r* Q / G A m b ys to m a m a cu la tu m U ro de la W al te rs ,1 97 5 H yl a v es ic o lo r* Q / G N o to p h th a lm u s vi ri d es ce n s U ro de la W al te rs ,1 97 5 H yp si b o a s b o a n s* Q / G N ot id en tif ie d C ol eo pt er a M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s b o a n s* Q / G A ll o b a te s m a rc h es ia n u s T ad po le M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s b o a n s* Q / G H yp si b o a s b o a n s T ad po le M ag nu ss on a nd H er o, 1 99 1 43 H yp si b o a s b o a n s* Q / G H yp si b o a s g eo g ra fi cu s T ad po le M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s b o a n s* Q / G L ep to d a ct yl u s kn u d se n i T ad po le M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s b o a n s* Q / G L ep to d a ct yl u s p en ta d a ct yl u s T ad po le M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s b o a n s* Q / G O st eo ce p h a lu s ta u ri n u s T ad po le M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s b o a n s* Q / G P h yl lo m ed u sa v a il la n ti T ad po le M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s b o a n s* Q / G O d o n a te n a ia d s O do na ta M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s b o a n s* Q / G A eq u id en s te tr a m er u s P is ce s M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s b o a n s* Q / G P yr rh u li n a s p. P is ce s M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s g eo g ra fi cu s* Q / G N ot id en tif ie d C ol eo pt er a M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s g eo g ra fi cu s* Q / G N ot id en tif ie d C ol eo pt er a M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s g eo g ra fi cu s* Q / G A ll o b a te s fe m o ra li s T ad po le M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s g eo g ra fi cu s* Q / G A ll o b a te s m a rc h es ia n u s T ad po le M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s g eo g ra fi cu s* Q / G H yp si b o a s b o a n s T ad po le M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s g eo g ra fi cu s* Q / G H yp si b o a s g eo g ra fi cu s T ad po le M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s g eo g ra fi cu s* Q / G H yp si b o a s g ra n o su s T ad po le M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s g eo g ra fi cu s* Q / G L ep to d a ct yl u s kn u d se n i T ad po le M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s g eo g ra fi cu s* Q / G L ep to d a ct yl u s p en ta d a ct yl u s T ad po le M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s g eo g ra fi cu s* Q / G L ep to d a ct yl u s rh o d o m ys ta x T ad po le M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s g eo g ra fi cu s* Q / G O st eo ce p h a lu s ta u ri n u s T ad po le M ag nu ss on a nd H er o, 1 99 1 H yp si b o a s g eo g ra fi cu s* Q / G P h yl lo m ed u sa b ic o lo u r T ad po le M ag nu ss o