Fausto Nomura-Relatório Universal Final

HERANA OU AMBIENTE?
PROCESSOS FILOGENTICOS
VS PROCESSOS ECOLGICOS NA DETERMINAO DAS
CARACTERSTICAS MORFOLGICAS EM GIRINOS
Prof. Dr. Fausto Nomura
RELATRIO FINAL de projeto apresentado ao

Ministrio da Cincia e Tecnologia MCT e ao
Conselho Nacional de Desenvolvimento
Cientfico e Tecnolgico CNPq.
Goinia
Dezembro de 2012
2
SUMRIO
Resumo ..................................................................................................................................... 3
Introduo Geral ..................................................................................................................... 4
Referncias Bibliogrficas .......................................................................................... 6
Principais Dificuldades Enfrentadas no Perodo ................................................................. 9
Indicadores ............................................................................................................................. 10
Captulo 1 ............................................................................................................................... 11
Captulo 2 ............................................................................................................................... 41
Captulo 3 ............................................................................................................................... 84
Captulo 4 ............................................................................................................................. 116
Captulo 5 ............................................................................................................................. 138
Captulo 6 ............................................................................................................................. 154
Captulo 7 ............................................................................................................................. 180

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RESUMO
Para a teoria de nicho, comunidades ecolgicas no so formadas por associaes
puramente casuais de espcies e diversos parmetros so utilizados para pesquisar os padres
formados por estas associaes. Em particular, os padres de uso e partilha de recursos pode
ser estudados por meio da morfologia das espcies, devido relao entre a morfologia e a
utilizao dos recursos disponveis no ambiente. Devido a essa relao, por meio de medidas
lineares simples de caracteres externos ou osteolgicos possvel inferir padres e processos
adaptativos que estruturam a partilha de recursos em uma comunidade. Existe uma grande
variedade de formas de girinos, larvas de anfbios anuros, resultando numa classificao
baseado no aspecto morfolgico, no hbito e no comportamento. Entretanto, apesar da
importncia de fatores ecolgicos na classificao destas guildas ecomorfolgicas, tambm
ocorre influncia de componentes filogenticos na evoluo de determinados caracteres
morfolgicos. O grau em que componentes filogenticos e ecolgicos moldam a morfologia
externa de girinos ainda no totalmente compreendida. Esta interao entre ecologia e
filogenia na determinao da forma dos girinos ilustrativa de dois processos envolvidos na
estruturao de comunidades: seleo de espcies em funo de filtros ambientais e
interaes competitivas, que so diretamente relacionados com a similaridade fenotpica e o
relacionamento filogentico de espcies co-ocorrentes. Desta maneira, nosso objetivo
principal analisar a evoluo dos caracteres morfolgicos inter e intra guilda para verificar
quais caracteres so resultantes de processos filogenticos e quais so resultantes de processos
ecolgicos. Para isso, propomos a utilizao da anlise morfomtrica geomtrica, juntamente
com a morfometria tradicional, e a otimizao de caracteres em propostas filogenticas
recentes.
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INTRODUO GERAL
Para a teoria de nicho, comunidades ecolgicas no so formadas por associaes puramente
casuais de espcies (Adler et al. 2007). Ao contrrio, as comunidades ecolgicas apresentam
padres de organizao e os eclogos tm tentado compreender quais processos geram e
mantm as comunidades ecolgicas organizadas (Brooks & McLennan 1993, Levin 1992).
Assim, uma das questes centrais da ecologia de comunidades explicar a origem e
manuteno das combinaes de espcies que coexistem em determinadas situaes
ambientais (Lewinsohn 1990).
Diversos parmetros so utilizados para pesquisar padres em comunidades
biolgicas, incluindo o nmero de espcies e suas abundncias absolutas e relativas, os tipos
de espcies presentes, suas propriedades fenotpicas (McPeek & Miller 1996) e os padres de
uso e partilha de recursos (Pianka 1994). Em teoria, diferenas de nicho limitam o
crescimento populacional de uma determinada espcie mais do que esta mesma espcie inibe
o crescimento de outras, promovendo a coexistncia (Chesson 2000). Neste contexto,
determinados aspectos da morfologia de uma espcie podem estar relacionados ao modo de
utilizao dos recursos disponveis no ambiente (Betz 2006, Emerson 1985), possibilitando,
pela comparao de medidas lineares simples de caracteres externos ou osteolgicos, a
determinao dos padres e processos adaptativos que estruturam a partilha de recursos em
uma comunidade (Nomura 2008, Bock 1994, Ricklefs & Travis 1980).
Existe uma grande variedade de formas de girinos, larvas de anfbios anuros,
representadas por um amplo espectro de tamanhos, formas de corpo, modos de alimentao,
taxas de desenvolvimento e preferncias de hbitat (Orton 1953, Altig & Johnston 1989,
McDiarmid & Altig 1999), resultando em uma grande diversidade morfolgica ainda no
totalmente estudada ou analisada (e.g., Haas 2003, Sokol 1977, 1981, Wassersug 1980,
Wassersug & Rosenberg 1979, Fabrezi & Lavilla, 1993, Larson & de S 1998, McDiarmid &
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Altig 1999, Maglia et al. 2001). A principal sntese morfolgica de girinos explicitamente
definida pelas similaridades entre as diferentes formas (Altig & Johnston 1989, McDiarmid &
Altig 1999), resultando numa classificao em dois grandes grupos: girinos endotrficos
(nutrem-se de fontes parentais durante todo seu desenvolvimento) e girinos exotrficos
(obtm energia atravs da ingesto de alimentos do ambiente externo) (Altig & Johnston
1989). Apenas entre espcies exotrficas de ambientes lnticos e lticos, possvel
reconhecer a existncia de diversas guildas baseadas na morfologia geral de alguns caracteres,
como forma do corpo, posio do olho e configurao e orientao do disco oral (Altig &
Johnston, 1989; McDiarmid & Altig 1999). Entretanto, apesar da importncia de fatores
ecolgicos na determinao da forma corporal de girinos (Altig & Johnston 1989, McDiarmid
& Altig 1999), tambm ocorre influncia de componentes filogenticos na evoluo de
determinados caracteres morfolgicos (Fatorelli & Rocha 2008, McDiarmid & Altig 1999).
Por exemplo, as guildas neustnicas e bentnicas parecem formar um complexo de
equivalentes ecolgicos, reunindo girinos de diversas famlias de anuros, enquanto que a
guilda de raspadores lnticos de suspenso parece resultar de organismos com uma histria
evolutiva em comum, incluindo a maioria dos girinos das espcies do gnero Phyllomedusa
(McDiarmid & Altig 1999).
O grau em que componentes filogenticos e ecolgicos moldam a morfologia externa
de girinos ainda no totalmente compreendida (e.g., Haas 2003, Nomura et al. 2003). Desta
maneira, apesar de girinos filogeneticamente relacionados apresentarem morfologias
semelhantes (Fatorelli & Rocha 2008), no necessariamente as guildas ecomorfolgicas so
resultantes de processos filogenticos. Esta interao entre ecologia e filogenia na
determinao da forma e do comportamento dos girinos ilustrativa de dois processos
envolvidos na estruturao de comunidades ecolgicas: seleo de espcies em funo de
filtros ambientais (Weiher & Keddy 1995, Weiher et al. 1998) e interaes competitivas
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(Elton 1946, MacArthur & Levins 1967, Chesson 1991, Leibold 1998). Estes dois processos
esto diretamente relacionados com a similaridade fenotpica e o relacionamento filogentico
de espcies co-ocorrentes (Tofts & Silvertown 2000, Webb 2000). Se espcies
filogeneticamente relacionadas compartilham caractersticas morfolgicas similares e
apresentam conservatismo de nicho, os filtros ambientais promovem a coexistncia de
espcies aparentadas, resultando em um padro chamado de agrupamento filogentico
(phylogenetic clustering, Cavender-Bares et al. 2004). Entretanto, a excluso competitiva
pode limitar a coexistncia de espcies relacionadas filogeneticamente que partilham recursos
limitantes e gerar um padro oposto ao do agrupamento filogentico, denominado disperso
filogentica (phylogenetic overdispersion, Cianciaruso et al. 2009, Cavender-Bares et al.
2004). Em estudos filogenticos com anfbios anuros, a homoplasia, tanto em estudos com
caracteres larvais ou de adultos, aparenta ser muito comum (Haas 2003). ainda necessrio
demonstrar os aspectos funcionais de estruturas morfolgicas para elucidar os padres de
similaridade morfolgica em girinos (Nomura et al. 2003, McDiarmid & Altig 1999) e o
reconhecimento de covariao entre caractersticas de hbitat e morfolgicas (Conte et al.
2007).
REFERNCIAS BIBLIOGRFICAS
Adler PB, Hillerislambers J, Levine JM (2007) A niche for neutrality. Ecology Letters
10(2):95-104.
Altig R (2007) A primer for the morphology of anuran tadpoles. Herpetological Conservation
and Biology 2(1):71-74.
Altig R, Johnston GF (1989) Guilds of anuran larvae: relationships among developmental
modes, morphologies, and habitats. Herpetologycal Monographs 3:81-109.
Betz O (2006) Ecomorpholoy: Integration of form, function, and ecology in the analysis of
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morphological structures. Mitteilungen der Deutschen Gesellschaft fr Allgemeine fr
Entomologie 15:409-416.
Bock WJ (1994) Concepts and methods in ecomorphology. Journal of Biosciences 19(4):403-
413
Brooks DR, McLennan DA (1993) Historical ecology: examining phylogenetic components
of community evolution. In: Ricklefs RE, Schluter D (Eds.) Species diversity in
ecological communities. University of Chicago Press, Chicago:267-280p.
Cavender-Bares J, Ackerly DD, Baum DA, Bazzaz FA (2004) Phylogenetic overdispersion in
Floridian oak communities. The American Naturalist 163(6):823-843.
Chesson P (2000) Mechanisms of maintenance of species diversity. Annual Review of
Ecology and Systematics 31:343-366.
Cianciaruso MV, Silva IA, Batalha MA (2009) Diversidade filogentica e funcional: novas
abordagens para a ecologia das comunidades. Biota Neotropica, no prelo.
Conte CE, Nomura F, Rossa-Feres DC, DHeursel A, Haddad CFB (2007) The tadpole of
Scinax catharinae (Anura: Hylidae) with description of the internal oral morphology, and a
review of the tadpoles from the Scinax catharinae group. Amphibia-Reptilia 28:177-192.
Elton C (1946) Competition and the structure of ecological communities. Journal of Animal
Ecology 15:5468.
Emerson SB (1985) Skull shape in frogs correlations with diet. Herpetologica 41(2):177-
188.
Fabrezi M, Lavilla EO (1993) Anatom_iia del condrocraneo en larvas de trs especies de
Telmatobius del grupo meridional (Anura: Leptodactylidae). Physis 48:3946.
Fatorelli P, Rocha CFD (2008) O que molda a distribuio das guildas de girinos tropicais?
Quarenta anos de busca por padres. Oecologia Brasiliensis 12(4):733-742
Haas A (2003) Phylogeny of frogs as inferred from primarily larval character (Amphibia:
8
Anura). Cladistics 19(1):23-89.
Larson P, de S RO (1998) Chondrocranial morphology of Leptodactylus larvae
(Leptodactylidae: Leptodactylinae): Its utility in phylogenetic reconstruction. Journal of
Morphology 238:287305.
Leibold M (1998) Similarity and local coexistence of species in regional biotas. Evolutionary
Ecology 12:95100.
Levin SA (1992) The problem of pattern and scale in ecology. Ecology 73(6):1943-1967.
Lewinsohn TM (1990) Concepes alternatives da organizao de comunidades. In: Atas do
Encontro de Ecologia Evolutiva do Brasil, v. nico, 26-35p.
MacArthur R, Levins R (1967) The limiting similarity, convergence and divergence of
coexisting species. American Naturalist 101:377385.
Maglia AM, Pgener LA, Trueb L (2001) Comparative development of anurans: Using
phylogeny to understand ontogeny. American Zoologist 41:538551.
McDiarmid R, Altig R (1999) Tadpoles. The Biology of anurans larvae. The University of
Chicago Press, Chicago:444 pp.
McPeek MA, Miller TE (1996) Evolutionary biology and community ecology. Ecology
77(5):1319-1320.
Nomura F, Rossa-Feres DC, Prado VHM (2003) The tadpole of Physalaemus fuscomaculatus
(Anura: Leptodactylidae), with a description of internal oral morphology. Zootaxa 370:1-
8.
Orton GL (1953) The systematics of vertebrate larvae. Systematic Zoology 2:63-75.
Orton GL (1957) Larval evolution and frog classification. Systematic Zoology 6:79-86.
Pianka E (1994) Evolutionary Ecology. Harper Collins, New York, 512p.
Ricklefs RE, Travis J (1980) A morphological approach to the study of avian community
organization. Auk 97:321-338

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Sokol OM (1977) The free swimming Pipa larvae, with a review of pipid larvae and pipid
phylogeny (Anura: Pipidae). Journal of Morphology 154:357426.
Tofts R, Silvertown J (2000) A phylogenetic approach to community assembly from a local
species pool. Proceedings of the Royal Society of London B 267:363369.
Wassersug R (1980) Internal oral features of larvae from eight anuran families: Functional,
systematic, evolutionary, and ecological considerations. Miscellaneous Publications
Museum of Natural History of University Kansas 68:1146.
Wassersug R, Rosenberg K (1979) Surface anatomy of branchial food traps of tadpoles: A
comparative study. Journal of Morphology 159:393426.
Webb C (2000) Exploring the phylogenetic structure of ecological communities: an example
for rain forest trees. The American Naturalist 156:145155.
Weiher E, Clarke G, Keddy P (1998) Community assembly rules, morphological dispersion,
and the coexistence of plant species. Oikos 81:309322.
Weiher E, Keddy P (1995) The assembly of experimental wetland plant communities. Oikos
73:323335.
PRINCIPAIS DIFICULDADES ENFRENTADAS NO PERODO
As dificuldades encontradas foram relacionadas quantidade de material coletado. Ainda
faltam triar e identificar materiais provenientes da Serra do Cip, MG, Barro Alto, GO, e
Niquelndia, GO. Esses lotes de animais coletados compem a tese de doutoramento da aluna
Nbia Carla Santos Marques (PPG Ecologia & Evoluo/UFG) e o projeto de Iniciao
Cientfica do Muryllo Ferreira de Melo (curso de Ecologia & Anlise Ambiental/UFG). A
necessidade de se assumir uma funo administrativa como coordenador do curso de Ecologia
& Anlise Ambiental tambm contribui para a dificuldade na identificao do material
proveniente destas localidades. Assim, a incorporao dos objetivos deste projeto em

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trabalhos de graduao e ps-graduao tornam plausvel a publicao dos resultados do
projeto, mesmo aps o seu encerramento.
Em funo da parceria com o RAN/ICMBio/GO e com a empresa Anglo American do
Brasil e da contemplao de um subprojeto na rede de pesquisa SISBiota Girinos de anuros
da Mata Atlntica, da Amaznia, do Pantanal e de Zonas de Transio: caracterizao
morfolgica, distribuio espacial e padres de diversidade (Processo FAPESP n 10/52321-
7 e Processo CNPq n 563075/2010-4), a maior parte das atividades de campo neste projeto
foi custeada com recursos de outras fontes, o que justfica o valor devolvido ao CNPq ao final
deste projeto (essencialmente combustvel e aluguel de carro).
INDICADORES
Comps a equipe deste projeto alunos de ps-graduao e de graduao, o que resultou em
uma dissertao de mestrado defendida e um trabalho de concluso de curso. Adicionalmente,
este projeto gerou at o momento dois trabalhos aceitos para publicao [um na revista
Ethology Ecology & Evolution (Qualis B2 IF 0.743) e outro na revista Biota Neotropica
(Qualis B2)], um em reviso (Community Ecology, Qualis A2 IF 1.679) e quatro artigos em
fase final de redao ou inicial de submisso (Hydrobiologia, Qualis A2 IF 1.784;
Biotropica, Qualis A2 IF 2.229; Natureza & Conservao, Qualis B1 IF 1.049; Iheringia.
Qualis B2 IF 0.230).
Os resultados deste projeto so apresentados na forma de captulos, referentes ao
contedo dos artigos descritos acima.

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CAPTULO 1 (Aceito na revista Biota Neotropica)
Diversidade de Anuros (Amphibia) na Reserva Extrativista Lago do Cedro,
Gois
Muryllo Melo1, Fernanda Fava1, Hugo Bonfim Arruda Pinto2, Rogrio Pereira Bastos1, Fausto
Nomura1,3
1
Laboratrio de Herpetologia e Comportamento Animal, Departamento de Ecologia, Instituto
de Cincias Biolgicas, Universidade Federal de Gois, CP 131, CEP 74000-970, Goinia,
GO, Brasil
2
RAN - Centro Nacional de Pesquisa e Conservao de Rpteis e Anfbios, Setor Leste
Universitrio, CEP: 74.605.090, Rua 229, n 95, Goinia/GO, Brasil

3
Laboratrio de Ecologia e Funcionamento de Comunidades, Departamento de Ecologia,
Instituto de Cincias Biolgicas, Universidade Federal de Gois, CP 131, CEP 74000-970,
Goinia, GO, Brasil
RESUMO
O Cerrado uma savana tropical que abriga uma anurofauna muito diversa, com cerca de 150
espcies conhecidas, das quais aproximadamente 32% so endmicas. Apesar desta grande
diversidade, muitas espcies podem estar sendo extintas antes mesmos de serem descritas ou
mesmo conhecidas (Linnean shortfall), o que limita o conhecimento dos padres
biogeogrficos (Wallacean shortfall). Neste trabalho, apresentamos o inventrio da
anurofauna da Reserva Extrativista Lago do Cedro, noroeste do estado de Gois. Ao todo,
registramos 43 espcies de anuros, distribudas em cinco famlias, das quais cinco espcies
so endmicas do Cerrado. A alta riqueza de espcies encontradas pode ser explicada pela
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heterogeneidade de habitats, promovida pelas diferentes fitofisionomias dentro da unidade de
conservao. A riqueza de espcies e a representatividade por famlia so semelhantes ao
encontrado em outras taxocenoses no Cerrado, com a anurofauna local formada por espcies
generalistas e de ampla distribuio. As famlias com maior diversidade de espcies foram
Hylidae e Leptodactylidae, padro frequentemente encontrado nas assembleias neotropicais. A
utilizao dos stios de reproduo pelas espcies de anuros foi similar ao de outros locais
amostrados no complexo biogeogrfico Chaco-Cerrado-Caatinga. A Reserva Extrativista
Lago do Cedro uma importante unidade de conservao do Cerrado, servindo de abrigo para
populaes de anuros, sendo representativa da diversidade de anfbios no bioma, e
apresentando localizao estratgica devido a posio central com relao a reas de
preservao na bacia do Araguaia.
Palavras-Chaves: unidade de conservao, girinos, Cerrado, Anura, bacia do rio Araguaia
ABSTRACT
The Cerrado is a tropical savannah that shelters a high diversified anuran assemblage, with
about 150 known species of which approximately 32% are endemic. Despite this high
diversity, several species are extinguished before they can be described or formally known by
the science (Linnean shortfall), which limits the knowledge about biogeographic patterns or
species distribution (Wallacean shortfall). We present an inventory of the frogs of the
Extractivist Reserve of the Lago do Cedro, northwestern region of the state of Gois. In this
area, we recorded 43 species, distributed in five anuran families, of which five species are
endemic to the Cerrado. The high species richness found can be explained by the habitat
heterogeneity, promoted by different vegetation types within the reserve boundaries. Species
richness and representativeness per family are similar to other assemblages found in the
Cerrado, with a local anuran assemblage formed by generalist and widely distributed species.
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The families Hylidae and Leptodactylidae presented the highest species diversity, which is
common in neotropical assemblages. The use of breeding sites by anuran species was similar
to the habitat use described in other sampled sites in the Chaco-Cerrado-Caatinga
biogeographic domain. The Extractivist Reserve Lago do Cedro is an important conservation
area of the Cerrado, sheltering representative anuran diversity and being strategically
positioned as a connection among other nature reserves within the Araguaia basin.
Keywords: Conservation unit, tadpole, Cerrado, Anura, Araguaia basin
INTRODUO
O Brasil um pas extenso e megadiverso, com 946 espcies de anfbios descritas (SBH
2012), sendo que, somente para o Cerrado, h registros para mais cerca de 150 espcies, das
quais 32% so endmicas (Bastos 2007). Entretanto, estima-se que a anurofauna do Cerrado
seja ainda mais diversa (Colli et al. 2002), uma vez que este tipo de savana neotropical
composta por uma variedade de ambientes que formam um mosaico estrutural de clima, solo
e fitofisionomias, o que promove a manunentao de uma alta diversidade de espcies com
caracteristicas bastante especializadas (Ratter et al. 1997, Oliveira & Marquis 2002).
Apesar de ocupar 23% do territrio brasileiro (Furley 1999), o Cerrado uma das
regies tropicais mais ameaadas no mundo, devido ao alto impacto das diversas atividades
humanas ao qual o bioma vem sendo submetido (Ratter et al.1997). Assim, embora muitas
novas espcies sejam ainda descritas (p.ex., Rhinella cerradensis, Maciel et al. 2007; Scinax
pusillus, Pombal et al. 2011; Ameerega berohoka, Vaz-Silva & Maciel 2011), provvel que
muitas outras sejam extintas antes mesmos de serem descritas ou mesmo conhecidas (Linnean
shortfall, segundo Whittaker 2005). Devido a essas ameaas, e por abrigar elevada
diversidade biolgica, o Cerrado considerado um dos hotspots para o estudo e conservao
da biodiversidade mundial (Myers et al. 2000). Apesar de todos estes fatores, menos de 2% de
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sua rea total protegida por unidades de conservao, parques ou reservas naturais (Brasil
1998).
Este panorama gera uma ausncia de conhecimento sobre aspectos de histria natural,
tamanho e dinmicas populacionais das espcies do bioma (Colli et al. 2002) e limitam o
conhecimento dos padres biogeogrficos (Wallacean shortfall, segundo Whittaker 2005).
Nesse contexto, a forte presso antrpica e o alto grau de endemismo reforam a importncia
de inventrios taxonmicos neste bioma (Bertoluci & Rodrigues 2005, Oda et al. 2009). Alm
do conhecimento de histria natural e ecologia, imprescindveis para compreenso dos
padres de diversidade e os processos que os determinam, inventrios taxonmicos podem
estabelecer princpios de manejo, restaurao e uso sustentvel da diversidade de um bioma.
Neste trabalho, apresentamos a composio de espcies e comentrios sobre biologia,
ecologia e distribuio geogrfica das espcies da anurofauna da Reserva Extrativista Lago do
Cedro (RELC), Aruan, Gois.
MATERIAL E MTODOS
1. rea de estudo
O estudo foi realizado na RELC (510010.15 W, 144140.38S), localizada no entorno do
municpio de Aruan, na regio noroeste do estado de Gois, possuindo aproximadamente
17.337 hectares (Figura 1). A regio localizada na plancie de inundao do Mdio Araguaia,
com altitude media de 250 m (SIMEGO 2012). A temperatura da regio pode chegar a 38 C e
a precipitao mdia anual de 1751 mm (SIMEGO 2012). O clima regional, segundo a
classificao climtica de Kppen-Geiger, do tipo tropical de vero mido e perodo de
estiagem no inverno (Aw) (Latrubesse & Stevaux 2002). A RELC faz parte de um plano para
a implantao do corredor do Araguaia, que pretende ligar o Parque Nacional das Emas,
Gois, at o Tucuru, Par, tornando-a estratgica na conservao de espcies do Cerrado

15
(Klink & Machado 2005).
A bacia do rio Araguaia considerada uma das reas prioritrias para a conservao da
biodiversidade associada a ambientes aquticos do Cerrado (AGMA et al. 2004). A regio
composta, principalmente, por reas rurais, em que a pastagem o uso predominante do solo.
A expanso da fronteira agrcola na regio provocou um intenso e crescente processo de
degradao ambiental, aumentando a fragmentao da paisagem e a ocorrncia de espcies
exticas, principalmente de gramneas, tais como Brachiaria spp. (Villanueva 2009). Alm
disso, a plancie de inundao do rio Araguaia sofre um intenso processo de antropizao
provocado por processos de desmatamento, minerao, eroso e sedimentao dos canais
principais e da plancie de inundao (Latrubesse et al. 2007, Latrubesse & Stevaux 2002).
2. Mtodo de coleta
A amostragem da riqueza e da abundncia de adultos e girinos de anuros foi realizada em
dezembro de 2010 em fevereiro e maro de 2011. A diversidade foi registrada pelos seguintes
mtodos: levantamento em stios de reproduo, coleta de girinos, busca ativa, transectos
aleatrios e armadilhas de interceptao e queda.
O mtodo de levantamento de stios de reproduo foi realizado durante a noite,
percorrendo-se a margem de cada corpo d'gua para a contagem de machos adultos em
atividade de vocalizao (Scott Jr & Woodward 1994). As coletas de girinos foram realizadas
durante o dia em cada corpo dgua, com o auxlio de um pu de tela de arame com malha de
3 mm durante uma hora ou aps completar o permetro. Quando o ambiente apresentava
profundidade superior a 1,5 metros, a coleta foi realizada apenas na rea entre as margens a
at dois metros em direo ao interior do corpo dgua. A tabela 1 descreve os ambientes
amostrados quanto ao tipo de vegetao (interior e exterior do corpo dgua), profundidade e
tamanho.
Utilizamos o mtodo de busca ativa para a localizao das espcies em seus refgios
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diurnos. Este mtodo foi associado transectos aleatrios (Heyer et al. 1994), que eram
percorridos na rea prxima aos locais de instalao das armadilhas de interceptao-e-queda
ou prximo aos corpos dgua amostrados. Nestes transectos, verificvamos cavidades em
rvores, rochas, troncos ou no solo, e tambm na serapilheira e ao longo de vegetao
marginal dos cursos dgua (Heyer et al. 1994). As amostragens por armadilhas de
interceptao-e-queda (pitfall traps) so importantes complementos no inventrio da
anurofauna, pois capturam espcies de hbitos terrestres e fossoriais (Heyer et al. 1994). As
armadilhas de interceptao-e-queda eram formadas por trs barreiras com 5m de
comprimento e 0,4m de altura dispostas em Y, com um balde de 60 l no centro e outros trs
baldes de 60 l posicionados na extremidade de cada barreira de interceptao (Figura 2). No
total, foram instaladas 25 armadilhas em reas de mata mida e cerrado sensu stricto, mas,
devido ao tamanho da equipe e limitaes logsticas, apenas 15 armadilhas eram ativadas por
expedio.
Espcimes testemunhos na fase adulta de cada espcie de anuro encontrada foram
coletados e anestesiados com xilocana a 5%, sendo em seguida fixados em formalina a
10% durante 24 horas e conservados em lcool 70% (Jim 1980). A classificao taxonmica
da fase adulta segue Frost (2009). Todos os girinos coletados foram anestesiados em soluo
de benzocana a 5% e posteriormente fixados e conservados em formalina 10%. A
identificao dos anuros na fase larvria foi feita com base em Rossa-Feres & Nomura
(2006). Para as espcies que no aparecem na chave de identificao, utlizamos a descrio
das larvas disponveis na literatura. Material testemunho est depositado na coleo cientfica
da Universidade Federal de Gois (ZUFG).
3. Anlises dos dados
A expectativa da riqueza local foi estimada com base na abundncia das espcies de anuros
em cada rea amostrada pelo mtodo de rarefao por interpolao baseada na amostra
17
(Gotelli & Colwell 2001), sendo realizadas tanto para adultos como para girinos.
Adicionalmente, calculamos a estimativa de riqueza de espcies pelo estimador no-
paramtrico Jackknife 1, a partir de 5000 aleatorizaes da matriz de abundncia original,
com o auxlio do software Estimates verso 7.5.0 (Colwell 2005).
Realizamos uma anlise de porcentagem de similaridade (SIMPER) para estimar a
contribuio de cada espcie para a variao encontrada na composio na assembleia de
anuros para cada expedio realizada (dezembro, fevereiro e maro). A SIMPER foi gerada a
partir da matriz de distncia Euclidiana (Clarke & Warwick 2001) da abundncia das espcies
em cada rea amostrada, com o auxlio do software Past verso 2.14 (Hammer et al. 2001).
RESULTADOS
1. Diversidade de espcies
Registramos na RELC 43 espcies de anfbios anuros pertencente a 15 gneros, distribudos
em cinco famlias: Bufonidae (duas espcies), Hylidae (22 espcies), Leiuperidae (oito
espcies), Leptodactylidae (nove espcies) e Microhylidae (duas espcies) (Tabela 2, Figuras
3, 4, 5, 6 e 7).
Pela amostragem por stio de reproduo registramos 29 espcies e 1188 indivduos.
As espcies mais abundantes na fase adulta foram Scinax fuscomarginatus e Dendropsophus
rubicundulus com 251 e 217 indivduos respectivamente, e presentes em 21 e 18 corpos
d'gua. Vinte e trs espcies tambm foram encontradas na fase larval, com um total de 806
indivduos, sendo que os hildeos Dendropsophus gr. microcephalus, Dendropsophus sp.1,
Dendropsophus sp.2, Scinax sp.1 (gr. ruber) e Scinax sp.2 (gr. ruber), e os leiuperdeos
Physalaemus marmoratus, Physalaemus sp. e Pseudopaludicola sp.3 foram registrados
somente em fase larval. Scinax sp.2 (gr. ruber) foi a espcie com maior abundancia na fase
larval.
18
Na amostragem por armadilhas de interceptao-e-queda registramos 11 espcies,
sendo que cinco espcies foram registradas somente por este mtodo: Leptodactylus gr.
marmoratus, Leptodactylus sertanejo, Leptodactylus mystaceus, Leptodactylus mystacinus e
Chiasmocleis albopunctata.
Dendropsophus rubicundulus, D. nanus e Pseudopaludicola sp.2 contriburam com
mais de 50% da variao na composio de anuros na fase adulta encontrados na RELC
(Tabela 3). Entretanto, de modo geral, o gnero Dendropsophus o que mais contribuiu para
explicar a variao na composio da assembleia na fase adulta (Tabela 3). Para anuros na
fase larval, duas famlias contriburam com mais de 60% da variao na composio de
espcies nos corpos d'gua amostrados, sendo Hylidae com 37 % e Leiuperidae com 23%.
Entretanto, a contribuio ao nvel genrico foi mais variada quando comparada a fase adulta,
sendo as espcies Scinax sp.2 (gr. ruber), Leptodactylus podicipinus e Dendropsophus sp.1
importantes para a primeira expedio, Scinax sp.1 (gr. ruber) e Physalaemus centralis
importantes para a segunda expedio e D. rubicundulus e Pseudopaludicola sp.2 importantes
para a terceira expedio.
A curva de rarefao da fase adulta (Figura 8) se estabilizou, o que no ocorreu para a
fase larval (Figura 9). A riqueza estimada pelo Jackknife 1 foi de 35,82 espcies para adultos e
de 30,76 para girinos. A curva de rarefao e a riqueza de espcies estimada indicam que, com
o aumento do esforo de amostragem, mais espcies podem ser registradas.
2. Histria natural
Na RELC, todos os stios de reproduo amostrados foram ambientes lnticos. Das espcies
encontradas na regio, 28 (93%) foram registradas em atividade de vocalizao.
2.1. Bufonidae
Os indivduos de R. schneideri foram encontrados no nvel da gua ou parcialmente
submersos, em reas de solo exposto ou escondidos sob serapilheira, troncos ou base da

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vegetao. Encontramos um jovem adulto de R mirandaribeiroi, amostrado em um nico stio
reprodutivo Indivduos de R. schneideri e R. mirandaribeiroi no foram encontrados em
atividade de vocalizao, apesar de serem observados nos stios de reproduo.
2.2. Hylidae
Os hildeos do gnero Hypsiboas (H. albopunctatus, H. raniceps, H. lundii, Hypsiboas
sp. e H. paranaiba) foram registrados em corpos de gua associados borda de ambientes
florestais e vocalizaram em ramos de vegetao arbustiva e arbreas marginais). Destas, H.
albopunctatus e H. raniceps foram mais abundantes e foram tambm utilizaram como stios
de vocalizao, vegetao herbcea.
Dendropsophus minutus, D. nanus e D. rubicundulus vocalizaram em poas de reas
abertas empoleirados em gramneas ou na vegetao herbcea marginal ou sobre vegetao
emergente. Estas espcies foram sempre abundantes e foram observadas vocalizando nas trs
expedies.
As espcies do gnero Scinax utilizaram diversos stios de vocalizao. Os machos de
S. fuscomarginatus utilizaram lagoas temporrias ou permanentes, empoleirando
principalmente nos ramos da vegetao herbcea e gramnea nas margens e na vegetao
emergente no interior dos corpos dgua. Esta espcie foi frequentemente a mais abundante
sendo amplamente distribuda entre os corpos dgua. Scinax fuscovarius, na RELC, estava
presente em corpos dgua temporrios de reas abertas e os machos vocalizaram no cho ou
sobre a vegetao marginal nas margens desses corpos dgua.
Os indivduos de Pseudis bolbodactyla e Lysapsus caraya (encontrados
frequentemente em amplexo) vocalizaram no interior dos corpos dgua. Os machos dessas
espcies vocalizaram associados vegetao flutuante quando presente. Os machos de
Phyllomedusa azurea vocalizaram em ramos da vegetao arbrea associada aos corpos d
gua permanentes.
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2.3. Leiuperidae
Os machos de Eupemphix nattereri vocalizaram na gua, nas bordas de poas
permanentes e temporrias. As espcies Physalaemus cuvieri e P. centralis foram encontradas
vocalizando nas trs expedies. Os machos vocalizaram nas margens de corpos dgua
temporrios e permanentes, sob o substrato, frequentemente encobertos pela base da
vegetao marginal e emergente. Ninhos de espuma foram observados sempre ancorados
vegetao aqutica. A identificao das espcies do gnero Pseudopaludicola problemtica
e motivo de discusses taxonmicas, sendo comuns erros de identificao (Ribeiro-Jnior &
Bertoluci 2009). Assim, consideramos conveniente no determinar um nome s espcies
encontradas. Na RELC, foram observados duas espcies de Pseudopaludicola sendo que os
machos vocalizaram em coro no incio da noite, e o maior perodo de vocalizaes era por
volta de 21h00mim, sempre sob o substrato em reas encharcadas de ambientes permanentes
e temporrios.
2.4. Leptodactylidae
Os leptodactildeos estavam associados a matas e foram encontrados no substrato,
debaixo de troncos ou serapilheira. Poucas espcies (Leptodactylus labyrinthicus, L. fuscus, L.
latrans, L podicipinus, L. pustulatus) foram encontradas vocalizando em rea aberta sob a
vegetao marginal do corpo d'gua. Nestes casos, estas espcies eram encontradas em baixa
abundncia, emitindo as vocalizaes com rara frequncia. Indivduos de Leptodactylus
labyrinthicus foram registrados vocalizando principalmente em reas abertas. Os machos L.
fuscus vocalizaram em ambientes abertos desde ambiente com bastante vegetao at
ambientes com pouca vegetao. Os machos de L. latrans vocalizaram ao nvel dgua em
poas situadas em reas abertas ou na borda da mata.
2.5. Microhylidae
Os microhildeos Chiasmocleis albopunctata (registrados somente em dezembro) e

21
Elachistocleis cesarii vocalizaram aps intensas precipitaes. Os indivduos de C.
albopunctata vocalizaram com o corpo parcialmente submerso e formando grandes agregados
reprodutivos. Os machos de Elachistocleis cesarii utilizam a borda interior e as margens dos
corpos dgua como stios de vocalizao e no foram encontrados em grande nmero por
stio reprodutivo.
DISCUSSO
A alta riqueza de espcies encontradas na RELC pode ser explicada pela heterogeneidade de
habitats (Eterovick & Sazima 2000), promovida pelas diferentes fitofisionomias do Cerrado.
Alguns estudos indicam que processos biticos e abiticos influenciam na estrutura e
diversidade de comunidades de anuros (Parris 2004), o que pode explicar a diversidade de
espcies de anuros da RELC. Dentre os processos biticos podemos citar a competio
(Wilbur 1987) e a predao (Heyer et al. 1975), e entre os fatores abiticos, a sazonalidade
climtica (Rossa-Feres & Jim 1996), o clima (Santos et al. 2007) e o grau de heterogeneidade
ambiental (Eterovick & Sazima 2000). Recentemente, alguns estudos apontaram uma
aparente ausncia de padres gerais relacionados estrutura dessas assembleias, sugerindo
que seriam resultados de presses que foram importantes no passado, mas no esto
influenciando no presente (Eterovick 2003, Gotelli & McCabe 2002).
A riqueza de espcies por famlia de anuros na RELC semelhante ao encontrado em
outras taxocenoses no Cerrado (Tabela 4). As famlias com maior diversidade de espcies
foram Hylidae e Leptodactylidae, com 51% e 21% das espcies registradas, respectivamente.
Este resultado est de acordo com de outros estudos, que apontam uma alta riqueza de
espcies destas famlias em ambientes neotropicais (Duellman 1999, Oda et al. 2009, Ribeiro-
Jnior & Bertoluci 2008). Entretanto, a importncia destas famlias de anuros na composio
da taxocenose pode variar de acordo com fatores locais. Apesar de a famlia Hylidae
22
apresentar o maior nmero de espcies nas taxocenoses de anuros, essa composio pode
variar de 31% (So Desidrio, Valdujo et al. 2009) a 50% das espcies (Apor, Vaz-Silva et al.
2007), enquanto que Leptodactylidae pode representar de 10% (Bodoquena, Uetanabaro et al.
2007) a 31% das espcies (Niquelndia, Oda et al. 2009). Esse padro tambm observado
para outras famlias representativas do Cerrado, como Leiuperidae, que pode representar de
3% (Oda et al. 2009) a 22% das espcies nas taxocenoses (Valdujo et al. 2009), e Bufonidae
pode representar de 3% (Itiquira, Brasileiro et al. 2005; Niquelndia, Oda et al. 2009) a 16%
da composio de espcies nestas taxocenoses (Valdujo et al. 2009).
Os hildeos apresentaram maior abundncia de indivduos e riqueza de espcies tanto
para girinos e adultos de anfbios da RELC. No presente estudo houve um padro semelhante
na ocorrncia temporal e no uso de microambientes entre os hildeos. Esse resultado sugere
que espcies de hildeos podem suportar uma maior sobreposio em recursos temporais ou
espaciais, como j foi encontrado para outras espcies (Menin et al. 2005).
A curva de rarefao dos adultos apresentou uma estabilizao, o que indica que seria
necessrio um esforo muito grande para se amostrar espcies adicionais. Tanto a curva de
rarefao obtida para a fase larvria quanto a riqueza estimada pelo Jackknife 1 indicam que o
nmero de girinos registrados est subestimado, sendo encontrada somente uma frao das
larvas das espcies presentes na RELC. Desta maneira, a riqueza estimada pelo Jackknife 1
pode estar relacionada ao registro de espcies raras ou de reproduo explosiva. O encontro
de oito espcies registradas por outros mtodos de inventariamento refora a necessidade de
mtodos auxiliares (armadilhas de queda, busca ativa e coleta de girinos) como meio de se
aumentar a eficincia de inventrios da anurofauna (Heyer et al. 1994).
Plancies de inundao so importantes para a biota local, pois criam ambientes
lnticos temporrios e possibilitam a troca de matria entre a plancie e o rio principal (Junk et
al. 1989). As maiores precipitaes pluviomtricas ocorrem entre os meses de outubro e

23
maro, perodo cujas guas extravasam do canal principal (picos de vazo) plancie criando
uma paisagem heterognea de ambientes lnticos temporrios, principalmente em reas
abertas (Junk et al. 1989). Periodicamente, esses novos ambientes na RELC secam durante os
meses entre maio e setembro (estao seca), quando diminui a frequncia de chuva (Simego
2012). A anurofauna da RELC, vista sob aspectos da biologia reprodutiva das espcies
encontradas, apresentou utilizao de stios reprodutivos similares ao de trabalhos do
complexo biogeogrfico Chaco-Cerrado-Caatinga, sendo observada uma anurofauna local
formada por espcies generalistas e amplamente distribudas nesse complexo biogeogrfico
(Bastos 2007, Bastos et al. 2003, Oda et al. 2009).
Em resumo, o padro de estruturao de taxocenose de anuros determinado por
multifatores, que podem agir em diferentes escalas, como fatores biticos, competio e
predao (Huston 1994) ou caractersticas dos corpos dgua, que geralmente so importantes
na estruturao das comunidades (Laan & Verboom 1990, Vos & Chardon 1998).
Especialmente para o Cerrado, o padro de variao fitofisionmica e de heterogeneidade
local dos ambientes utilizados pelas espcies de anfbios anuros contribui para a alta
diversidade local de espcies em taxocenoses neste bioma. Adicionalmente, este trabalho
contribui para a elaborao e implementao do plano de manejo de anuros da RELC, uma
vez que fornece informaes bsicas sobre o padro de distribuio das espcies de anfbios
anuros na regio. Nenhuma espcie registrada na RELC est atualmente alocada em alguma
categoria de ameaa (GAA 2012). Entretanto, isso no reduz a importncia da RELC como
abrigo de populaes e conexo com outras assembleias na bacia do Araguaia. Como a regio
altamente modificada com desmatamentos, queimadas e uso de fertilizantes qumicos e
agrotxicos, a regulao da RELC pode ser uma importante ferramenta para a implantao de
um modelo econmico sustentvel na bacia do Araguaia, permitindo o desenvolvimento
econmico da regio com perspectivas de preservao e proteo.

24
AGRADECIMENTOS
Agradeo ao Programa de Iniciao Cientfica PIVIC/ICMBio pela oportunidade de
desenvolver esse projeto. Ao Chefe da Reserva Lago do Cedro, Sr. Leonardo T. S. Cndido
que nos gentilmente permitiu as coletas na reserva e proprietrios das fazendas do entorno
pelo apoio durante o estudo. Ao professor Natan Medeiros Maciel pelo auxilio na
identificao de muitas das espcies. Ao Renan Costa Nunes e a Ms. Luciana Signorelli pela
colaborao no trabalho de campo. Rassa Furtado Souza e Alessandro Ribeiro Morais pela
leitura crtica do manuscrito. Ao ICMBIO RAN pelo apoio logstico e financeiro e ao CNPq
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33
TABELAS
Tabela 1. Caracterizao dos habitats amostrados na RESEX Lago do Cedro. Tipos de

vegetao: (Vhe) herbcea, (Var) arbustiva, (Vg) gramnea, (Vab) arbrea e (Vaq) aqutica.
Bastante: > 75% de cobertura vegetal; reduzida: <50% de cobertura vegetal. NA dados
ausentes.
Vegetao no corpo d'
gua Profundidade Tamanho
Ambiente Tipo de vegetao
mximo
interior marginal mxima (m) (m)
1 Vhe,Var,Vab,Vaq,Vg bastante Bastante 1 150 x 100
2 Vhe,Var,Vab,Vg bastante NA 0,5 150 x 50
3 Vhe,Var,Vab bastante Reduzida 0,3 30 x 20
4 Var,Vab,Vaq reduzida Bastante 0,25 25 x 25
5 Var,Vab bastante Bastante 0,3 15 x 10
6 Var,Vaq, Vg reduzida Reduzida 0,15 2 x 1,5
7 Var,Vab,Vaq bastante Reduzida 1,5 15 x 7
8 Vhe,Var,Vab,Vaq,Vg bastante Bastante 0,2 20 x 15
10 Vhe,Var,Vab,Vaq,Vg bastante Bastante 1 150 x 50
11 Var,Vab,Vg reduzida Reduzida 0,5 150 x 200
12 Var,Vaq,Vg reduzida Bastante 0,4 40 x 128
13 Var,Vab,Vaq,Vg bastante Reduzida 0,20 20 x 100
14 Vhe,Var,Vab, bastante Bastante 2,1 400 x 200
15 Vhe,Var,Vab,Vg reduzida Reduzida 1,2 200 x 200
16 Vhe,Var,Vab, bastante Reduzida 0,2 25 x 5
17 Vhe,Var,Vab,Vaq,Vg reduzida Reduzida 3,2 15 x 60
18 Var,Vg reduzida Reduzida 3,5 50 x 25
19 Vhe,Var,Vg reduzida Bastante 2 100 x 25
20 Vhe,Var,Vab,Vg reduzida Bastante 1,2 150 x 100
21 Vhe,Var,Vg bastante Reduzida 3,2 100 x 100
22 Var,Vab,Vg bastante Bastante 4,2 200 x 200
23 Var,Vab,Vg bastante Reduzida 2,5 200 x 200
24 Vhe,Var,Vab,Vg reduzida Reduzida 2 200 x 25
25 Vhe,Vab,Vaq,Vg reduzida Bastante 0,8 200 x 100
26 Vhe,Var,Vab,Vg bastante Reduzida 2 200 x 50
27 Var,Vab,Vaq,Vg reduzida Bastante 0.5 150 x 50
28 Vhe,Var,Vab,Vaq,Vg bastante Reduzida 1,5 100 x 60
29 Vhe,Var,Vab,Vaq,Vg bastante Reduzida 0,5 100 x 20
30 Vhe,Var,Vab,Vaq,Vg reduzida Bastante 0,2 20 x 30
31 Vhe,Var,Vab,Vaq,Vg bastante Bastante 0,5 50 x 50
32 Vhe,Var,Vab,Vg bastante Bastante 0,5 70 x 30
*Ambiente com degradao mdia. **Ambiente bastante degradado.
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Tabela 2. Espcies de anuros registados na RELC por mtodo de amostragem, tipo de habitat
e distribuio. Mtodo: (1) levantamento por stio de reproduo, (2) coleta de girinos, (3)
armadilha de interceptao-e-queda e (4) busca ativa. Tipo de habitat: G gramnea, VE
vegetao emergente, VHM vegetao herbcea marginal, VHG vegetao herbcea, S
serapilheira, VA vegetao arbustiva, M macrfita, FF formao florestal, PV prximo
vereda, Var vegetao arbrea, CaU campo mido, CS campo sujo. Distribuio: AM
ocorrncia no cerrado e na Amaznia, E endmica do Cerrado, O distribuio ampla em
reas abertas na Amrica do Sul, W espcie amplamente distribuda na Amrica do Sul.
Famila/Espcie Metdo Tipo de habitat Distribuio

BUFONIDAE (2)
Rhinella schneideri (Werner 1984)* 1, 3, 4 G/FF W
Rhinella mirandaribeiroi (Gallardo 1965)* 1 FF W
HYLIDAE (22)
Dendropsophus cruzi (Pombal & Bastos 1998) 1 VE/VHM E
Dendropsophus gr. microcephalus* 2 VE/VHM NE
Dendropsophus minutus (Peters 1982) 1, 2 VHM/CaU/VE W
Dendropsophus nanus (Boulenger 1889) 1, 2 VHM W
Dendropsophus rubicundulus (Reinhardt &
1 VE NE
Ltken 1862)
Dendropsophus sp.1 2 - -
Dendropsophus sp.2 2 - -
Hypsiboas albopunctatus (Spix 1824) 1 VHM W
Hypsiboas lundii (Burrmeister 1856) 1 FF/PV NE
Hypsiboas multifaciatus (Gnther1859) 1 VA AM
Hypsiboas punctatus (Schneider 1799) 1 G W
VA/ VAr/
Hypsiboas raniceps Cope 1862 1, 2 W
FF/PV
Hypsiboas sp. 1, 2 VA -
Lysapsus caraya Gallardo 1964 1 M E
Phyllomedusa azurea Cope 1862 *** 1, 2 VA AM
Pseudis bolbodactyla Lutz 1925 1, 2 M AT
Scinax constrictus Lima, Bastos & Giaretta 2005 1 VHM E
Scinax fuscomarginatus (Lutz 1925) 1, 2 VE/VHM W
Scinax fuscovarius (Lutz 1925) 1, 2 VHM W
Scinax sp.1 (gr. ruber)* 2 - -
Scinax sp.2 (gr. ruber)*, ** 2 - -
Trachycephalus typhonius (Linnaeus, 1758) 1, 4 CS W
LEPTODACTYLIDAE (9)
Leptdactylus sp. (gr. marmoratus)* 3 FF -
Leptodactylus fuscus (Schneider 1799) 1, 3, 4 FF W
35
Leptodactylus labyrinthicus (Spix, 1824) 1, 4 CaU/CS W

Leptodactylus latrans (Steffen, 1815) 1, 3, 4 FF/G W
Leptodactylus mystaceus (Spix 1824)* 3 FF W
Leptodactylus mystacinus (Burmeister 1861)* 3 FF AT
Leptodactylus podicipinus (Cope 1862) 1, 3, 4 FF/CaU O
Leptodactylus pustulatus (Peters 187) 1 S/CaU E
Leptodactylus sertanejo Giaretta & Costa 2007* 3 FF E
LEIUPERIDAE (8)
Eupemphys nattereri Steindachner 1863 1 FF NE
Physalaemus centralis Bokermann 1962 1, 2 FF/CaU NE
Physalaemus cuvieri Fitzinger 1826 1, 2 FF/CS W
Physalaemus marmoratus (Reinhardt & Ltken
2 - NE
1862)*, **
Physalaemus sp.* 2 - -
Pseudopaludicula sp.1 1,2 CaU -
Pseudopaludicula sp.2 1,2 SE -
Pseudopaludicola sp.3* 2 - -
MICROHYLIDAE (2)
1, 2, 3,
Elachistocleis cesarii (Miranda-Ribeiro 1920) FF/VG W
4
Chiasmocleis albopunctata (Boettger 1885)* 3 FF NE
*Espcie que no foi encontrada vocalizando.**Espcie com pouco exemplares amostrados.
***Status de conservao com deficincia de dados (IUCN).
Tabela 3. Porcentagem de similaridade temporal (SIMPER) entre as poas d'gua amostrados
na RELC. Abundncia (Abund), Dendropsophus minutus (Dmin), D. nanus (Dnan),
Dendropsophus sp. 1 (Dsp.1), Dendropsophus sp. 2 (Dsp.2), D. rubicundulus (Drub), ,
Elachistocleis cesari (Elac), Hypsiboas lundii (Hlun), H. raniceps (Hran), Leptodactylus
latrans (Llat), L. podicipinus (Lpod), Lysapus caraya (Lysc), Physalaemus centralis (Pcen),
P. cuvieri (Pcuv), Pseudis bobodactyla (Psbb), Pseudopaludicola sp. 2 (Psp.2), Scinax sp. 1
(Ssp. 1), Scinax gr. ruber, Scinax fuscovarius (Scfv).
% Abund. Mdia Abund. Mdia. Abund. Mdia

Espcie Contribuio Cumulativa 1 2 3
Adultos
Drub 18.1 21.17 0.1 11.7 5.45
Dnan 11.19 34.26 5.3 6.83 1.45
Psp.2 9.365 45.21 2 2.5 3.82
Lysc 7.696 54.22 0.6 6.83 0.0909
Dmin 7.457 62.94 4.3 0.167 2.55
Hlun 5.01 68.8 4 0 0
36
Psbb 3.675 73.1 2.4 1.17 0.455

Llat 3.664 77.39 0.2 2.67 1
Hran 2.817 80.68 0.6 1.92 0.727
Girinos
Ssp.1 17.04 18.55 0 7.64 1.33
Scru 17.03 37.09 12.9 0 1.58
Pcuv 11.55 49.66 5.71 0.571 3.25
Pcen 9.565 60.07 0 3.21 3.42
Dsp.1 5.816 66.41 6.29 0 0
Lpod 5.62 72.52 6.71 0 0
Dsp.2 3.164 75.97 0 0.571 1.33
Scfv 3.087 79.33 0 0.143 7.25
Elac 2.59 82.15 0.857 0.5 2.25
Tabela 4. Nmero total de espcies de anuros em diversas regies do Cerrado. APA rea de
Proteo Ambiental; EE Estao Ecolgica; FE Floresta Estadual; FLONA Floresta
Nacional; PARNA Parque Nacional; PE Parque Estadual; RPPN Reserva Particular de
Proteo da Natureza.
Regio Riqueza Referncia

PE das Furnas do Bom Jesus, SP 27 Arajo et al., 2009
FLONA de Silvnia, GO 29 Bastos et al., 2003
APA de Cafuringa, DF 35 Brando et al., 2006
Morrinhos, GO 26 Borges & Juliano, 2007
EE de Itirapina, SP 28 Brasileiro et al., 2005
Norte da bacia do rio Tocantins, MA, 38 Brasileiro et al., 2008
TO
Hidrolndia, GO 22 Campos & Vaz-Silva, 2010
RPPN Santurio do Caraa. MG 38 Canelas & Bertoluci, 2007
Serra do Cip, MG 43 Eterovick & Sazima, 2003
PARNA das Emas, GO 25 Kopp et al., 2010
Niquelndia, GO 38 Oda et al., 2009; Nomura et al., 2012
EE e FE de Assis, SP 23 Ribeiro-Jr & Bertoluci, 2009
Hidreltrica Ponte de Pedra, MT e MS 33 Silva et al., 2009
Joo Pinheiro, MG 37 Silveira, 2006
PARNA da Serra da Bodoquena, MS 38 Uetanabaro et al., 2007
EE Serra Geral do Tocantins, TO 39 Valdujo et al., 2010
Noroeste do estado de So Paulo 27 Vasconcelos & Rossa-Feres, 2005
Hidreltrica de Espora, GO 32 Vaz-Silva et al., 2009
Sudoeste do estado de Gois, GO 39 Morais et al., 2011
37
FIGURAS
Figura 1. Mapa da localizao da RESEX Lago do Cedro, Aruan, GO. Linha pontilhada
indica o limite municipal de Aruan, GO. Linha contnua indica a divisa entre os estados do
Mato Grosso e Gois.
Figura 2. Armadilha de interceptao-e-queda instalada em rea de cerrado sensu stricto.

38
Figura 3. Espcies de anfibios anuros encontradas na RESEX Lago do Cedro, Aruan, GO.
A) Rhinella schneideri, B) Rhinella mirandaribeiroi, C) Dendropsophus cruzi, D)
Dendropsophus nanus, E) Dendropsophus rubicundulus, F) Hypsiboas punctatus.
A) Hypsiboas raniceps, B) Hypsiboas sp., C) Lysapus caraya, D) Pseudis bolbodactyla, E)
Phyllomedusa azurea, F) Scinax constrictus.

39
A) Scinax fuscomarginatus, B) Trachycephalus typhonius, C) Eupemphys nattereri, D)
Physalaemus centralis, E) Physalaemus cuvieri, F) Pseudopaludicola sp.1.
A) Pseudopaludicola sp.2, B) Leptodacylus fuscus, C) jovem de Leptodacylus labyrinthicus,
D) Leptodacylus mystaceus, E) Leptodacylus mystacinus, F) Leptodacylus pustulatus.

40
A) Chiasmocleis albopunctata, B) Elachistocleis cesarii.
Figura 8. Curva de rarefao das espcies encontradas na fase adulta
Figura 9. Curva de rarefao das espcies encontradas na fase larval

41
CAPTULO 2 (Em avaliao na revista Community Ecology)
Ecomorfologia de Girinos Brasileiros: relao entre ecologia, morfologia e
filogenia
Nbia. C. S. Marques e Fausto Nomura
Programa de Ps-Graduao em Ecologia e Evoluo, Instituto de Cincias Biolgicas,
Universidade Federal de Gois, Goinia, Gois, Brasil
Departamento de Ecologia, Instituto de Cincias Biolgicas, Universidade Federal de
Gois, Goinia, Brasil.
RESUMO
Girinos podem ocorrer em diversos tipos de ambientes e, devido a essa ampla ocupao, h
uma considervel diversidade morfolgica entre os girinos de diferentes espcies. Essas
diferenas morfolgicas podem ser representadas por medidas lineares ou geomtricas e
associadas a fatores ecolgicos para testar hipteses sobre o efeito das presses ambientais no
padro evolutivo dos girinos. Entretanto, necessrio isolar o efeito da histria evolutiva
desses caracteres morfolgicos antes de determinar quais padres so gerados pelo uso ou
compartilhamento de recursos. Assim, o objetivo do trabalho analisar como a escolha de
microambientes de girinos pode ser explicada por interaes ecolgicas (representada pelas
variveis morfomtricas) ou evolutivas (representada pela similaridade filogentica) entre os
girinos de diferentes espcies de anuros. Para isso, analisamos girinos de 101 espcies de
anuros, as quais foram classificadas quanto guilda ecomorfolgica, uso do hbitat, posio
na coluna dgua e tipo de substrato do fundo do corpo dgua. Para medir a similaridade no
uso de recursos espaciais (microambientes), utilizamos a similaridade morfolgica entre os

42
diferentes tipos de girinos, por meio de duas tcnicas distintas: morfometria tradicional e
morfometria geomtrica. Para representar a similaridade filogentica, reconstrumos a
filogenia das espcies de anuros e calculamos a distncia patrstica entre todos os pares
possveis. Posteriormente, usamos as matrizes morfolgicas e a matriz filogentica como
preditoras da varincia encontrada na matriz ecolgica, por meio do mtodo de partio da
varincia, usando uma anlise de redundncia parcial. De modo geral, tanto as interaes
interespecficas (inferida pela similaridade morfolgica) quanto a histria evolutiva (inferida
pela similaridade filogentica) foram importantes para explicar a seleo de microambientes
das larvas de diferentes espcies de anuros. Entretanto, a importncia destes dois fatores
variou em funo do critrio para a medio da similaridade morfolgica. Quando utilizamos
informaes morfolgicas extradas por meio da morfometria tradicional, a quantidade
explicada pela filogenia foi duas vezes maior do que a quantidade explicada pela morfologia
(23% e 10%, respectivamente). Entretanto, as matrizes baseadas em morfologia geomtrica, a
filogenia mais informativa apenas quando comparada a vista dorsal?. Quando utilizamos a
vista lateral, a morfologia geomtrica mostrou-se to informativa quanto a filogenia (11% e
10% de variao explicada, respectivamente). De modo geral, tanto a interao interespecfica
quanto a histria evolutiva das espcies so importante para determinar a escolha de
microambiente dos girinos.
INTRODUO
A origem da adaptao do organismo ao seu ambiente uma questo amplamente discutida na
biologia evolutiva, que busca compreender como os caracteres morfolgicos e ecolgicos de
uma espcie se modificam e evoluem. A ecologia morfolgica, ou ecomorfologia, uma
forma elegante de pensar essa questo, uma vez que investiga as relaes existentes entre a
morfologia (i.e., fentipo) e a ecologia (i.e., variao no uso de recursos), ao nvel de

43
comunidades, populaes, guildas e indivduos (Peres-Neto 1999). Desta maneira, possvel
detectar diferenas morfolgicas entre organismos e associar essas diferenas com presses
ambientais e fatores ecolgicos (Irschik & Losos 1999). Ao nvel de comunidades, essas
diferenas, que podem ser extradas de medidas lineares ou geomtricas de organismos
(Adams & Rohlf 2000; Candioti 2006; Maderbacher et al. 2007, Las-Casas & Azevedo-Jr
2009), nos permite detectar como as presses ecolgicas atuam para determinar a composio
de espcies em assembleias animais.
Girinos ocorrem em diversos tipos de ambientes, como poas permanentes e
temporrias, ambientes artificiais, lagoas, riachos, depresses nos troncos de rvores cadas e
gua acumulada em epfitas (Inger 1985; Starrett 1973; Altig & McDiarmid 1999 a,b). Em
consequncia desta ampla ocupao, existe uma considervel diversidade morfolgica,
decorrente das diferentes adaptaes necessrias para cada tipo de ambiente. Por exemplo,
girinos de ambientes lnticos, apesar de considerados como o tipo mais comum de girinos,
apresentam menor perodo larval e tamanho at a metamorfose do que girinos de ambientes
lticos (Patterson & McLachlan 1989).
Em funo desta grande diversidade de formas, Orton (1953, 1957) reuniu os girinos
em quatro grupos funcionais com base na morfologia oral externa, posio do espirculo e
tipos ecolgicos. Cada grupo estava restrito a uma famlia ou grupo de famlias de Anura,
sugerindo grandes radiaes sequenciais na histria evolutiva dos girinos. Esta proposta
considerada a primeira formalizao do conceito de tipos ecomorfolgicos para girinos (Altig
& McDiarmid 1999). Posteriormente, Altig & Johnston (1989) modificaram e ampliaram essa
formalizao, formando dois grupos ecomorfolgicos de girinos com base na fonte de energia
para o seu desenvolvimento: endotrficos (alimentam-se da fonte parental durante o seu
desenvolvimento, subdivididos em sete guildas), e exotrficos (obtm energia pela ingesto
de alimentos de fontes externas, subdivididos em 15 guildas).

44
Entretanto, o papel da histria evolutiva nas mudanas dos aspectos funcionais de
caracteres morfolgicos no deixa de ser menos importante que os ecolgicos. Muitos
padres de uso e compartilhamento de recursos so melhor explicados com base em
caractersticas de linhagens evolutivas (Brooks & McLennan 1993; Cadle & Greene 1993;
Martins 1994; Vitt et al. 1999; Eterovick & Fernandes 2001; Webb et al. 2002). Neste caso,
deveramos testar hipteses sobre os processos que modelam as comunidades combinando
aspectos ecolgicos com a histria evolutiva das espcies (Brooks & McLennan 1991).
Assim, o ambiente agiria como um filtro que selecionaria linhagens ou caractersticas
morfofuncionais de girinos mais bem adaptados a essas condies ambientais especficas.
O objetivo deste trabalho analisar como as preferncias ecolgicas de girinos de
diferentes guildas (principalmente a escolha de microhbitat) podem ser explicadas por
interaes ecolgicas (medidas por similaridade morfolgicas) ou pelas relaes evolutivas
entre as espcies (medidas por distncia filogentica). Selecionamos girinos de 11 guildas
ecomorfolgicas (de acordo com Altig & McDiarmid 1999) para responder a seguinte
questo: o que modelou a escolha de microhbitat entre esses girinos, um processo de
convergncia adaptativa mediada por interaes interespecficas (correlao com a
morfologia) ou um histria evolutiva em comum (correlao com a filogenia)?
MATERIAL E MTODOS
Para este estudo, analisamos 101 espcies de girinos, classificados de acordo com 11 guildas
ecomorfolgicas e o uso do hbitat (bentnico, neustnico, nectnico, carnvoro, aderente,
gastromyzophorus, nidicola, "suspension feeder", "suspension rasper", macrfago,
arborcola), velocidade da gua (lntico ou ltico), posio na coluna dgua (superfcie, meia
gua, fundo) e associao com substrato do fundo do corpo dgua (pedregoso, folhoso,
detritos, lodoso ou arenoso). A caracterizao de cada espcie, quanto aos atributos

45
ecolgicos, foi obtida a partir de dados publicados em revistas especializadas (Tab. 1) e a
classificao das guildas ecomorfolgicas foi feita de acordo com Altig & McDiarmid
(1999a). Os atributos ecolgicos foram organizados em uma matriz binria nomeada matriz
ecolgica. J para os dados morfolgicos, utilizamos duas tcnicas distintas para a
caracterizao das espcies: a morfometria tradicional e a morfometria geomtrica. Esta
abordagem nos permite testar, adicionalmente, a eficincia relativa dos dois mtodos em
representar informaes ecolgicas a partir da anlise morfomtrica independente de efeitos
filogenticos.
Morfometria tradicional
Utilizamos 14 variveis morfomtricas, que so medidas de profundidade, largura e
comprimento. Essas medidas foram definidas por Altig & McDiarmid (1999b), sendo oito em
vista lateral (Fig. 1A) e seis em vista dorsal (Fig. 1B), para representar a variao morfolgica
de 67 espcies de girinos, a partir de dados obtidos da literatura (Tab. 1). As medidas em vista
lateral so: comprimento total (CT, distncia entre a extremidade anterior do focinho e a
extremidade final da cauda); comprimento do corpo (CC, distncia entre a extremidade
anterior do focinho e o incio da cauda); altura do corpo (AC, maior distncia ventro-dorsal do
corpo); altura da nadadeira dorsal (AND, maior distncia entre as margens dorsais da
nadadeira e da musculatura caudal); altura da musculatura caudal (AMC, maior distncia
ventro-dorsal da musculatura caudal); altura da nadadeira ventral (ANV, maior distncia entre
as margens ventrais da nadadeira e da musculatura caudal); distncia do olho a extremidade
do focinho (DOF, distncia entre a extremidade anterior do focinho e o centro do olho);
distncia da narina a extremidade do focinho (DNF, distncia entre a extremidade anterior do
focinho e o centro da narina). As medidas em vista dorsal so: largura do corpo (LC, maior
distncia entre as laterais do corpo); largura da musculatura caudal (LMC, maior largura da
musculatura caudal, medida na base da cauda junto ao corpo); distncia interocular (DIO,
46
distncia entre os centros dos olhos); distncia internasal (DIN, distncia entre os centros das
narinas); dimetro do olho (Dmo, distncia mxima entre as margens dos olhos); dimetro da
narina (Dmn, distncia mxima entre as margens das narinas). Essas medidas so comumente
usadas nas descries das espcies e foram organizadas em uma matriz retangular nomeada
matriz ecomorfolgica tradicional
Morfometria geomtrica
A morfometria geomtrica um mtodo que descreve a variao da forma do organismo no
levando em considerao o efeito do tamanho, orientao e rotao (Zelditich et al. 2004).
Para representar a forma dos organismos, estabelecemos uma srie de marcos anatmicos
("landmarks"), os quais devem ser reconhecidos em todos os indivduos estudados
independente da espcie e serem homlogos (i.e., terem correspondncia biolgica da posio
de marcos entre formas, Sneath & Sokal 1973). Para esta abordagem, utilizamos 101 espcies
de girinos, dos quais 23 marcos anatmicos foram selecionados em vista lateral (sensu Van
Buskirk 2009, Fig.2A), e 18 marcos anatmicos em vista dorsal (Fig.2B, anexo 1). Os marcos
anatmicos foram definidos de acordo com a classificao de Bookstein (1991), podendo ser:
i) Justaposio de tecidos (i.e. encontro de trs ou mais estruturas); ii) Pontos de mxima
curvatura (e.g. extremidades de processos) e, iii) Pontos extremos (e.g. ponta do focinho).
Pontos de mxima curvatura e pontos extremos so considerados pseudo-marcos pela
inconsistncia de sua definio e deficincia quanto homologia (Monteiro & Reis 1999),
mas foram includos devido ao pequeno nmero de marcos anatmicos verdadeiros em
girinos. Os marcos anatmicos foram obtidos a partir das imagens publicadas nos artigos de
descrio das espcies. Cada marco anatmico gera um sistema de coordenadas no plano
cartesiano, que so utilizadas nas anlises estatsticas posteriores. As matrizes de dimenses
morfolgicas geomtricas resultantes foram separadas, com uma matriz de coordenadas dos
marcos anatmicos em vista lateral, nomeada matriz ecomorfolgica lateral e outra em vista
47
dorsal, nomeada matriz ecomorfolgica dorsal. Cada uma destas matrizes foram
transformadas pelo mtodo de Procrustes (Rohlf 1990). Esse mtodo diminui as diferenas
entre as configuraes dos marcos anatmicos a partir do centroide da forma, que a
distncia mdia entre todos os marcos anatmicos e o centro de gravidade da forma (Zelditch
et al. 2004). Desta maneira, as coordenadas dos marcos anatmicos representam o desvio do
centroide (Zelditich et al. 2004, Van Buskirk 2009). Uma desvantagem do mtodo de
Procrustes que o nmero de coordenadas excede em quatro vezes o nmero de dimenses
do espao de forma (shape space), onde as coordenadas, que agora so invariantes ao
tamanho, orientao e posio, esto localizadas (Zelditch et al. 2004). Sendo ento
necessrio o descarte de quatro coordenadas para o ajuste dos graus de liberdade para a
anlise por mtodos estatsticos convencionais (Zelditch et al. 2004). Desta maneira, aps a
transformao, calculamos as partial warps scores pelo mtodo do thin-plate spline
transformation grid, que uma ferramenta convencional de interpolao da superfcie
(Zelditich et al. 2004). A utilizao das partial warps scores resolve o problema de graus de
liberdade de nosso conjunto de dados sem a necessidade de critrios subjetivos de seleo de
coordenadas.
Como as relaes interespecficas promovem modificaes morfolgicas nas espcies,
os dados ecomorfolgicos extrados pela morfometria tradicional e morfometria geomtrica
foram utilizados como substitutos das relaes interespecficas. Assim, podemos representar
as presses ecolgicas atuantes na determinao da composio de espcies em assembleias
de girinos.
Filogenia
Para testar a hiptese de que as preferncias ecolgicas dos girinos podem ser decorrentes do
conservatismo de nicho, que a tendncia de espcies filogeneticamente prximas
apresentarem requisitos ecolgicos similares, foi construda uma matriz de filogenia dos
48
girinos, calculada a partir da distncia patrstica entre todos os pares possveis de espcies
representados em uma rvore filogentica e nomeada matriz filogentica. Essa rvore
filogentica foi construda com base nas hipteses filogenticas apresentadas em Faivovich
(2002), Faivovich et al. (2004), Faivovich et al. (2005), Frost et al. (2006), Grant et al. (2006),
Pramuk et al. (2008), Faivovich et al. (2009), Wiens (2010) e Frost (2011), pela substituio
simples dos ramos terminais. As espcies que no foram utilizadas em nenhuma das hipteses
filogenticas mencionadas acima foram posicionadas em politomia com as espcies
congenricas, com relao aos grupos de espcies reconhecidos.
Anlises Estatsticas
Para testar quais fatores, interaes interespecficas (inferidas pela similaridade morfolgica)
ou relaes evolutivas (inferida pela similaridade filogentica) afetam as preferncias
ecolgicas dos 101 girinos de anuros, usamos as matrizes ecomorfolgicas tradicional e
geomtrica, e a matriz filogentica como preditoras da varincia encontrada na matriz
ecolgica. As matrizes foram submetidas a algumas transformaes a fim de torn-las
independentes e comparveis para realizar a anlise de partio da varincia. A matriz
ecolgica foi transformada em uma matriz de similaridade, por meio do ndice de similaridade
de Gower (Pavoine et al. 2009). Posteriormente, utilizamos uma anlise de coordenadas
principais (PCoA; Legendre & Legendre 1998) para extrair autovetores e autovalores da
matriz ecolgica e a matriz filogentica. A matriz ecomorfolgica tradicional foi transformada
pela equao alomtrica, a fim de se remover o efeito do tamanho dos atributos
morfomtricos. Posteriormente, os dados transformados da matriz ecomorfolgica tradicional
e das matrizes de partial warps scores geomtrica, foram submetidos a uma anlise de
componentes principais (PCA), a qual reduz as informaes morfolgicas em um espao
multivariado reduzido e diminui o efeito de variveis colineares nas informaes
morfolgicas. Os autovetores obtidos de uma matriz de dados a qual foi feita uma anlise de
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componentes principais (PCA) diretamente comparvel com os autovetores obtidos com a
PCoA (Legendre & Legendre 1998). Assim, possvel comparar diretamente as matrizes de
autovetores ecomorfolgicas tradicional e geomtrica, que foram submetidas PCA, com as
matrizes de autovetores ecolgica e filogentica, submetidas PCoA.
Para testar se h sobreposio das guildas ecomorfolgicas no espao morfolgico, ou
seja, verificar se espcies de diferentes guildas possuem a morfologia externa semelhante, foi
realizada uma Anlise de varincia multivariada (MANOVA) no paramtrica utilizando o
teste post hoc de Bonferroni. A MANOVA permite saber se existe diferena entre os grupos
quando consideramos todas as variveis respostas simultaneamente (Quinn & Keough 2002),
sendo possvel a comparao par a par das guildas, verificando a sobreposio morfolgica de
cada par.
Para testar o efeito de fatores filogenticos, resumido pelo autovetores da PCoA para
a matriz filogentica, e de interaes, resumido pelos autovetores obtidos pelas matrizes
ecomorfolgicas tradicional e geomtrica, submetemos a matriz de autovetores ecolgica ao
mtodo de partio da varincia (Diniz-Filho et al. 1998; Desdevises et al. 2003; Peres-Neto
et al. 2006), usando uma anlise de redundncia parcial (RDA) (Legendre & Legendre 1998).
O mtodo de partio proposto por Diniz-filho et al. (1998) permite a partio da variao
fenotpica em componentes filogenticos e especficos, como a morfologia. Cada matriz
morfolgica foi utilizada apenas uma vez, resultando em trs RDA. Os autovetores da matriz
ecolgica foram utilizados como a matriz resposta e os autovetores da matriz filogentica e
das matrizes ecomorfolgica tradicional e geomtrica como matrizes preditoras. Usamos essa
abordagem para testar a importncia da contribuio de interaes interespecficas (usando as
matrizes ecomorfolgicas como substituto) e da histria evolutiva (usando a matriz
filogentica como substituto) e a contribuio compartilhada dos dois para a seleo de
microambientes em girinos de anfbios anuros. Aps avaliar a contribuio total dos fatores
50
(interaes interespecfica e histria evolutiva), ns testamos a significncia dos dois termos
ao modelo de RDA, usando uma ANOVA permutacional (Oksanen et al. 2005).
Os marcos anatmicos foram marcados com o auxlio dos softwares tpsUtil (Rohlf
2009) e tpsDig2 (Rohlf 2008). As rvores filogenticas foram construdas com o software
Mesquite, v.2.74. As anlises de PCoA e PCA foram feitas utilizando o software Past verso
2.02 (Hammer et al. 2001). Todas as outras anlises foram feitas usando o ambiente R (R
Development Core Team, 2011).
RESULTADOS
Quando utilizamos a informao morfolgica extrada por meio da morfometria tradicional, a
PCoA resumiu 90,7% da variao entre as espcies nos 11 primeiros eixos principais (Tab. 2).
J para a informao filogentica, foram necessrios apenas os cinco primeiros eixos para
explicar 90,9% da variao na relao filogentica entre as espcies estudadas (Tab.2). A
variao ecolgica encontrada foi resumida pelos sete primeiros eixos resultantes da PCA, os
quais explicaram 91,4% da variao total (Tab. 2).
Quando consideramos a matriz de dados baseada na morfometria geomtrica, foram
necessrios os 13 primeiros eixos da PCA para resumir 90,8% da variao total encontrada na
matriz ecomorfolgica lateral e dos oito primeiros eixos para resumir 91,7% da variao total
encontrada na matriz ecomorfolgica dorsal. Como houve variao no nmero de trabalhos
com a descrio de girinos de espcies de anuros que apresentam a vista dorsal e/ou lateral
(101 espcies em vista lateral, 67 espcies em vista dorsal), realizamos duas PCoA para os
atributos ecolgicos e filogenticos, com o nmero correspondente de espcies. Assim, para
comparao com a matriz ecomorfolgica lateral, utilizamos os seis primeiros eixos da PCoA
que explicou 90,9% da variao filogentica total, e os 15 primeiros eixos que correspondeu a
90,1% da variao para ecolgica total (Tab. 2). Para a comparao com a matriz
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ecomorfolgica dorsal, foram necessrios os cinco primeiros eixos da PCoA para explicar
91,7% da variao filogentica total, os 12 primeiros eixos para explicar 90,5% da variao
ecolgica total (Tab.2).
Independente da matriz ecomorfolgica utilizada [tradicional (Fig.3), dorsal (Fig.4) ou
lateral (Fig.5)] observamos que os grupos formados pelas guildas ecomorfolgicas
apresentaram uma alta sobreposio no espao morfolgico, demonstrando que espcies de
diferentes guildas podem apresentar morfologia semelhante. Entre todas as guildas
ecomorfolgicas amostradas, a guilda suspension feeder a que apresenta a morfologia mais
distinta [tradicional (Tab.3), dorsal (Tab.4) e lateral (Tab.5)].
Padres adaptativos de uso de microhbitat
Obtivemos resultados distintos quando utilizamos a matriz ecomorfolgica tradicional ou
geomtrica (dorsal ou lateral) para explicar a escolha de microhbitat por girinos de anuros.
Com a matriz ecomorfolgica tradicional, a contribuio de interaes interespecficas para
explicar a seleo de microambientes foi de 10% (Fig.6). Quando utilizamos as informaes
obtidas por meio da morfometria geomtrica o resultado tambm foi diferente se
consideramos a matriz ecomorfolgica dorsal ou lateral. Nesses casos, a contribuio de
interaes interespecficas foi de 6% para a matriz ecomorfolgica dorsal, e 11% para a lateral
(Fig. 6). Apesar de no ser possvel a comparao estatstica entre os termos de um modelo ou
entre o mesmo termo de diferentes modelos de uma RDA, a matriz ecomorfolgica
tradicional apresentou uma contribuio similar ao da matriz ecomorfolgica lateral, enquanto
houve uma maior variao da contribuio filogentica para explicar a seleo de
microambientes dos girinos, dependendo do tipo de matriz ecomorfolgica utilizada. Quando
utilizamos a matriz ecomorfolgica tradicional, a filogenia explicou 23% da variao,
enquanto que para as matrizes ecomorfolgicas dorsal e lateral a contribuio da filogenia foi
de apenas 9% e 10%, respectivamente (Fig. 6; Tab. 6). Aparentemente, dados geomtricos

52
apresentam melhor performance quando comparados a morfometria tradicional para explicar
a variao no uso de microambientes por girinos de anuros.
DISCUSSO
Larval adaptive radiation and convergent adaptation have produced an abundance of
modification for pond life, stream life, arboreal life, terrestrial life (direct development), for
surface feeding, and for predatory habits, and other specializations of less obvious ecological
significance Orton (1957)
As anlises de redundncia parcial nas matrizes ecomorfolgicas tradicional e dorsal,
mostram que as preferncias ecolgicas dos girinos so explicadas em sua maior parte pela
histria evolutiva das espcies, como predito pela teoria do conservatismo de nicho (Wiens
& Graham 2005; Horner & Bohannan 2006; Cavender-Bares et al. 2009). Na matriz
ecomorfolgica lateral a morfologia explica uma maior parte das preferncias ecolgicas dos
girinos, demonstrando a influncia das interaes interespecficas, como predao e
competio, em moldar a ecologia das espcies. Nossos dados sugerem que tanto o
conservatismo de nicho, quanto as relaes interespecficas, so importantes para determinar a
seleo de microambientes por girinos de espcies de anuros.
A plasticidade fenotpica, que a habilidade de um gentipo produzir diferentes
fentipos de acordo com as mudanas ambientais, bastante comum em girinos, sendo
causada principalmente por interaes predador-presa (Kishida & Nishimura 2004, McIntyre
et al. 2004) e competio (Laurila 2000, Barnett & Richardson 2002, Monello et al. 2006).
Sendo assim, espervamos que a morfologia (i.e. fentipo) tivesse uma participao maior na
explicao da ecologia das espcies. Van Buskirk (2009) ao comparar a adaptao e a inrcia
filogentica em girinos da Austrlia, demonstrou que algumas mudanas morfolgicas nas
espcies representam adaptaes ao hbitat que elas ocupam, sugerindo que a forma do corpo
53
tem mudado em resposta as mudanas no uso do hbitat. Porm, a inrcia filogentica foi
surpreendentemente grande, demonstrando que h uma forte influncia dos caracteres
ancestrais, o que foi interpretado como fentipos que so, em parte, mal adaptados ao seu
ambiente (Van Buskirk 2009). Eterovick & Fernandes (2001) encontraram resultados
semelhantes, sendo o uso do microhbitat da famlia Hylidae influenciado por fatores
ecolgicos, enquanto na famlia Leptodactylidae por fatores filogenticos. Nosso estudo
encontrou resultados similares, sendo a morfologia e a filogenia importantes para explicar a
seleo de microambientes por girinos de anuros. Desta maneira, as espcies retm aspectos
do seu nicho fundamental, que so as condies abiticas na qual a espcie capaz de
sobreviver ao longo do tempo (Wiens & Graham 2005), demonstrando que nem sempre as
mudanas na ecologia das espcies vm acompanhadas de mudanas morfolgicas.
Entretanto, apesar da histria evolutiva apresentar um papel importante na determinao das
caractersticas ecolgicas dos girinos das espcies de anuros, interaes interespecficas, que
promovem modificaes morfolgicas, so necessrias para refinar a adaptao do organismo
ao ambiente o qual ocupa. A morfologia tpica de uma populao deveria ser aquela que
confere o melhor desempenho no hbitat ocupado (Pinto & vila 2004). Porm, deve existir
um retardo de tempo entre a modificao ambiental e o surgimento de novos atributos
morfolgicos, o qual resulta em um refinamento adaptativo. Nomura & Rossa-Feres (dados
no publicados) consideram que a alta contribuio de mecanismos histricos para explicar a
variao em atributos ecolgicos de girinos bentnicos como uma surpresa, uma vez que a
plasticidade fenotpica desta guilda ecomorfolgica alta. Interaes interespecficas, como a
predao e a competio, podem induzir novos padres comportamentais em girinos de
anuros, antes de induzir novidades morfolgicas (Nomura & Rossa-Feres, dados no
publicados).
Nossos resultados demonstram que nem sempre mudanas comportamentais so

54
precedidas por novidades morfolgicas nos girinos de diferentes espcies de anuros, sendo
grande a sobreposio das espcies no espao morfolgico. Essa grande sobreposio mostra
que h formas morfolgicas redundantes que permitem a ocupao de diferentes hbitats.
Porm as solues morfolgicas encontradas para a ocupao dos diferentes microhbitats so
semelhantes entre essas guildas. Esses novos padres comportamentais podem ser moldados
pelas relaes interespecficas, como a predao (e.g., atravs de reduo da atividade ou
evitao espacial; Kats & Dill 1998; Lima & Dill, 1990) ou a competio (e.g. aumentando a
taxa de forrageamento e amplitude de sua dieta; Akre & Johnson 1979, Formanowicz 1982,
Stephens & Krebs 1986, Anholt & Davies 1987, Anholt & Werner 1995, Anholt et al. 1996),
sendo poucos os exemplos de mudanas morfolgicas em resposta a competio (Relyea
2002). A competio e a predao conferem aos organismos a mesma gama de traos
morfolgicos e comportamentais, porm em direes opostas (e.g. predao induz baixa
atividade enquanto competio induz alta atividade; Relyea 2002), sendo um paradigma na
ecologia de comunidades (Vance 1978, Abrams 1982, Werner & Anholt 1993, Holt & Lawton
1994, Leibold 1996). Esse paradigma pode ser o responsvel pela baixa contribuio da
morfologia em moldar a seleo de microambientes em girinos de anuros. Assim, a predao
e a competio atuando em direes opostas podem se anular, no permitindo grandes
mudanas morfolgicas nas espcies (apesar de serem organismos com plasticidade fenotpica
alta), abrindo espao para a inrcia filogentica, que o reflexo da escolha do ancestral.
A histria evolutiva das espcies e a morfologia tm um papel importante em moldar a
ecologia das espcies, mas o sinal morfolgico varia de acordo com a tcnica escolhida,
morfometria tradicional ou morfometria geomtrica. A morfometria tradicional resulta de uma
srie de medidas morfomtricas que se sobrepem ou apresentam o mesmo sentido, o que as
torna redundantes (Bookstein et al. 1985; Rohlf & Marcus 1993; Zelditch et al. 2004;
Mutanen & Pretorius 2007; Maderbacher et al. 2008). J a morfometria geomtrica detecta as
55
diferenas na forma em direo oblqua, bem como em direes horizontal e vertical (Viana et
al. 2006), alm de eliminar todas as variaes dos dados que no so advindos da forma do
organismo, atravs do mtodo de superimposio (Mutanen & Pretorius 2007). Strauss &
Bookstein (1982) afirmaram que o mtodo geomtrico mais eficiente que os mtodos
tradicionais, porque supera as limitaes empregadas por estes mtodos que so baseados em
medidas longitudinais. Como o mtodo geomtrico tem um aspecto tridimensional, ele
consegue detectar melhor algumas variaes do corpo que podem ser visualizadas com
tcnicas multivariadas (Viana et al. 2006). Vrios autores compararam a morfometria
tradicional com a geomtrica em diferentes reas da Biologia (Adams & Rohlf 2000;
Bemvenuti & Rodrigues 2003; Parsons et al. 2003; Viana et al. 2006; Bernal 2007; Mutanen
& Pretorius 2007; Maderbacher et al. 2008) e todos concluram que a morfometria geomtrica
conferiu um melhor resultado para seus dados do que a tradicional. Nos nossos resultados fica
claro que na morfometria tradicional os dados morfolgicos so subestimados, dando um peso
maior para a inrcia filogentica em moldar a ecologia dos indivduos, o que pode criar a falsa
concluso de que as relaes interespecficas no tm grande contribuio para definir
atributos ecolgicos de organismos. A morfometria geomtrica extrai informaes mais
precisas dos organismos, o que melhora a resoluo dos sinais ecomorfolgicos dos dados
obtidos. Utilizando a informao geomtrica, no detectamos uma grande divergncia entre os
termos filogenticos e morfolgicos para explicar o uso de microambientes em girinos,
quando comparado ao resultado da anlise utilizando dados morfomtricos tradicionais.
Desse modo, nosso trabalho demonstra a importncia das interaes interespecficas e
da histria evolutiva das espcies em moldar a escolha do microambiente de girinos. Apesar
de serem organismos com plasticidade fenotpica alta, os girinos de anuros no apresentam
grandes novidades morfolgicas, porm apresentam mudanas comportamentais, podendo ser
em resposta as interaes interespecficas. A histria evolutiva apresenta papel importante na

56
escolha de microambientes, sendo o resultado da escolha das espcies ancestrais, indo de
acordo com a teoria do conservatismo de nicho (Wiens & Graham 2005; Horner & Bohannan
2006; Cavender-Bares et al. 2009). Diferentes resultados foram obtidos de acordo com a
tcnica utilizada para extrair a informao morfolgica (geomtrica ou tradicional), sendo a
morfometria geomtrica mais precisa, no mostrando grandes divergncias entre a morfologia
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71
TABELAS
Tabela 1. Atributos ecolgicos das 101 espcies de girinos. Lo= Ltico, Le= Lntico; Fo= Folhas; P= Pedras; L= Lodo; A= Areia; D= Detritos;
S= Superfcie; Ma= Meia gua; F= Fundo; - = Dados ausentes.
Substra
Uso do Posio
to
Espcies Guilda Ambien Coluna Referncias
do
te d'gua
fundo
Allobates nidicola Nidicola - S/Ma/F Fo Caldwell & Lima 20031, 3
Ameerega braccata Bentnico Lo F P Haddad & Martins 1994 3
Ameerega flavopicta Bentnico Lo F P Haddad & Martins 19943; Costa et al. 2006
Ameerega hahneli Bentnico Lo F P Haddad & Martins 19943
Ameerega picta Bentnico Lo F P Haddad & Martins 19943
Anomaloglossus
Nidicola - S/Ma/F Fo Junc et al. 19941, 3
stepheni
Aplastodiscus
Bentnico Lo/Le F Fo/L Gomes 20093
callypigius
Aplastodiscus eugenioi Bentnico Lo F P/A Carvalho-e-Silva & Carvalho-e-Silva 20051, 2
Aplastodiscus perviridis Bentnico Le F Fo/L Gomes 20092
Atelopus pulcher Gastromyzophorous Lo Ma/F Fo/D Gascon 19892
Bokermannohyla
Bentnico Lo/Le F Fo/L Gomes 20092
circumdata
Bokermannohyla
Bentnico Lo F P Lugli & Haddad 2006a1, 2
itapoty
Bokermannohyla
Bentnico - F D/L Pombal & Haddad 19932
luctuosa
Bokermannohyla oxente Bentnico Lo F P Lugli & Haddad 2006b1, 2
Chiasmocleis
Suspension feeder Le Ma/F D/L Nascimento & Skuk 20061, 2
alagoanus
Chiasmocleis carvalhoi Suspension feeder - Ma/F D/L Wogel et al. 20041, 2
Chiasmocleis cf
Suspension feeder Le Ma/F D/L Gomes 20093
laucosticta
72
Chiasmocleis hudsoni Suspension feeder Lo/Le Ma/F D/L Rodrigues et al. 20081, 2
Dendropsophus
Macrfago - F Fo/L Wild 19922
allenorum
Dendropsophus
Nectnico Le F Fo/D Bokermann 19633; Dias 2008
berthalutzae
Dendropsophus giesleri Nectnico - Ma D/L Santos et al. 19981, 2; Gomes 2009
Dendropsophus microps Carnvoro/Macrfago Lo/Le Ma Fo/L Bokermann 1963; Santos et al. 19982
Dendropsophus minutus Carnvoro/Macrfago Le Ma Fo/L Bokermann 1963; Rossa-Feres & Nomura 20062
Dendropsophus
Carnvoro Le Ma Fo/L Peixoto & Gomes 19991, 2
nahdereri
Dendropsophus nanus Macrfago Le F L Bokermann 19631; Rossa-Feres & Nomura 20062
Dermatonotus muelleri Suspension feeder Le S/Ma D/L Rossa-Feres & Nomura 20062
Elachistocleis bicolor Suspension feeder Le Ma/F Fo/L Candioti 20061; Rossa-Feres & Nomura 20062
Eupemphix nattereri Bentnico Le F D/L Rossa-Feres & Nomura 20062
Hylodes amnicola Bentnico Lo F P/Fo Pombal et al. 20021, 2
Hylodes sazimai Bentnico Lo F P/Fo Haddad & Pombal. 19952
Hylodes uai Bentnico Lo F P/Fo Nascimento et al. 20011, 2
Hypsiboas
Bentnico Lo/Le F Fo/D/L Rossa-Feres & Nomura 20062
albopunctatus
Hypsiboas atlanticus Bentnico Le F Fo/D Nascimento et al. 20091, 2
Hypsiboas caipora Bentnico Lo S P Antunes et al. 20081, 2
Hypsiboas cipoensis Bentnico Le F Fo Eterovick et al. 20021, 3
Hypsiboas freicanecae Nectnico Lo F Fo Carnaval & Peixoto 20041, 2
Hypsiboas
Bentnico Lo F P Bokermann 19633
geographicus
Hypsiboas goianus Bentnico Lo F Fo/D Eterovick et al. 20021, 3
Hypsiboas joaquini Bentnico Lo/Le F D/L Garcia et al. 20031, 2
Hypsiboas lundii Bentnico Lo/Le F Fo/L Rossa-Feres & Nomura 20062
Hypsiboas poaju Bentnico Le F L Garcia et al. 20081, 2
Hypsiboas prasinus Bentnico Le F D/L Gomes 20092
73
Hypsiboas raniceps Bentnico Le F D/L Rossa-Feres & Nomura 20062

Itapotihyla langsdorffii Bentnico Le F Fo/L Pimenta & Canedo 20071, 2
Leptodactylus
Bentnico - F L Orton 19513
albilabris
Leptodactylus elenae Bentnico Le F L Prado & D'Heursel 20061, 2
Leptodactylus fuscus Bentnico Le F D/L Rossa-Feres & Nomura 20062
Leptodactylus
Carnvoro Lo/Le F Fo/D/L Rossa-Feres & Nomura 20062
labyrinthicus
Leptodactylus latrans Bentnico Le Ma/F Fo/D/L Rossa-Feres & Nomura 20062
Leptodactylus
Bentnico - F L Orton 19513
melanonotus
Leptodactylus
Bentnico Le F Fo/L de S et al 2007a1, 3
notoaktites
Leptodactylus
Bentnico Le Ma/F Fo/L Rossa-Feres & Nomura 20062
podicipinus
Leptodactylus
Bentnico Le F Fo/D de S et al 2007b1, 3
pustulatus
Lysapsus limellus Nectnico - Ma Fo Kehr & Basso 19901, 3; Candioti 2006
Megaelosia apuana Bentnico Lo/Le F D/L Pombal et al 20031, 2
Odontophrynus
Bentnico Lo/Le - Fo/L Gomes 20092
americanos
Suspension
Phasmahyla cochranae Lo S P Bokermann 19662; Gomes 2009
rasper/Arborcola
Phasmahyla guttata Arborcola Lo/Le S/Ma P/Fo/L Bokermann 19662
Phyllodytes edelmoi Arborcola Le S/Ma/F Fo Peixoto et al. 20031, 2
Phyllodytes gyrinaethes Arborcola Le S/Ma/F Fo Peixoto et al. 20031, 2
Phyllodytes
Arborcola Le S/Ma/F Fo Caramaschi et al. 19921, 2
melanomystax
Phyllomedusa ayeaye Suspension rasper Le S/Ma P/Fo/L Pezzuti et al. 20091, 2
Phyllomedusa centralis Suspension rasper Lo Ma Fo/L Brando et al. 20091, 2
Phyllomedusa oreades Suspension rasper Lo/Le S/Ma P/Fo/L Brando 20021, 2
74
Physalaemus atlanticus Bentnico Le F P/D/L Haddad & Sazima 20041, 2

Physalaemus camacan Bentnico Le F P/D/L Pimenta et al. 20051, 2
Rossa-Feres & Jim 19931; Rossa-Feres & Nomura
Physalaemus centralis Bentnico Le F L/D
20062
Physalaemus cicada Bentnico Le F L/D Vieira & Arzabe 20081, 2
Physalaemus cuvieri Bentnico Le F L/D Rossa-Feres & Nomura 20062; Gomes 2009*
Physalaemus irroratus Bentnico Le F L/D Cruz et al. 20073
Physalaemus spiniger Bentnico Le F L/D Haddad & Pombal 19981, 2
Pleurodema
Bentnico Le F D/L Rossa-Feres & Nomura 20062
fuscomaculatum
Proceratophrys avelinoi Carnvoro Lo/Le F Fo/D/L de S & Langone 20021, 3
Pseudis paradoxa Nectnico Le Ma/F Fo/D/L Rossa-Feres & Nomura 20063
Rhinella jimi Bentnico Le S/F Fo/D/L Tolledo & Toledo 20101, 2
Rhinella rubecens Bentnico Lo/Le S/F P Eterovick & Sazima 19991, 3
Rhinella schneideri Bentnico Le S/F D/L Rossa-Feres & Nomura 20062
Scinax aff caldarum Nectnico Le Ma Fo/L Gomes 20093
Carvalho-e-Silva & Carvalho-e-Silva 1994; Conte
Scinax albicans Aderente Lo/Le F P/Fo
et al. 20071, 3
Carvalho-e-Silva et al. 1995; Alves & Carvalho-e-
Scinax alter Nectnico Le Ma Fo/D
Silva 2002; Conte et al. 20071, 2
Scinax angrensis Aderente Lo/Le F P Conte et al. 20071, 3
Scinax argyreornatus Bentnico Le F Fo/D
et al. 20071, 3
Scinax Ariadne Bentnico Lo F P/A Bokermann 1967; Conte et al. 20073
Scinax berthae Nectnico Le Ma D/L de S et al. 19971; Conte et al. 20073
Scinax catharinae Bentnico Lo/Le F Fo/L Conte et al. 20071, 2
Carvalho-e-Silva & Carnaval 1997; Alves &
Scinax cuspidatus Nectnico Le Ma Fo/D
Carvalho-e-Silva 20021, 2
Scinax flavoguttatus Bentnico Lo F Fo/D Conte et al. 20071, 3
Scinax fuscomarginatus Nectnico Le Ma D/L Rossa-Feres e Nomura 20062
Scinax fuscovarius Nectnico Le Ma D/L Rossa-Feres e Nomura 20062
75
Scinax hayii Nectnico Le F Fo/L Dias 2008; Gomes 20092

Haddad & Pombal 1987; Conte et al. 20073; Dias
Scinax hiemalis Bentnico Lo F Fo/L
2008
Scinax humilis Bentnico Le F Fo
et al. 20071, 3
Scinax kautskyi Aderente Lo/Le F P Conte et al. 20071, 3
Scinax littoralis Bentnico Lo/Le - Fo/L/A Pombal & Gordo 1991; Conte et al. 20073
Scinax machadoi Nectnico Lo F P Conte et al. 20073
Carvalho-e-Silva 1986; Conte et al 20071; Gomes
Scinax obtriangulatus Bentnico Le S/F Fo/D
20092
Scinax ranki Bentnico Lo/Le F Fo/D Andrade & Cardoso 1987; Conte et al. 20073
Alves & Carvalho-e-Silva 19991; Rossa-Feres &
Scinax similis Nectnico Le S/Ma/F Fo
Nomura 20062
Scinax trapicheiroi Aderente Lo/Le F P/Fo
et al. 20071, 3
Trachycephalus
Nectnico Le Ma/F Fo/L Schiesari & Moreira 19961, 2
coriaceus
Trachycephalus
Nectnico Le Ma/F D/L Rossa-Feres & Nomura 20062
venulosus
1
Referncias das variveis morfomtricas tradicionais.
2
Referncias das imagens de girinos em vista lateral e dorsal extradas para o uso na morfometria geomtrica.
3
Referncias das imagens de girinos somente em vista lateral extradas para o uso na morfometria geomtrica.
76
Tabela 2. Autovalores (Evalues) e o percentual de variao encontrada (%Var.) pela Anlise de componentes principais (PCA) e Anlise de
Coordenadas principais (PCoA) nas matrizes Ecolgica; Filogentica; Morfometria tradicional; Morfometria geomtrica em vista lateral e em
vista dorsal. Nmeros em negrito indicam os eixos usados na anlise de partio (porcentagem de explicao total superior a 90%).
Morfometria Geomtrica Morfometria Tradicional
Vista Lateral Vista Dorsal
Ecolgica Morfolgica Filogentica Ecolgica Morfolgica Filogentica Ecolgica Morfolgica Filogentica
Eixo Evalues %Var. Evalues %Var. Evalues %Var. Evalues %Var. Evalues %Var. Evalues %Var. Evalues % Var. Evalues % Var. Evalues % Var.
1 1.3299 38.422 0.0047428 27.12 1.624 46.457 1.0202 42.65 0.0062194 34.728 0.94928 41.312 1.1465 39.928 8980.35 42.252 1.3094 48.661
2 0.87704 25.338 0.0029288 16.75 0.99376 28.428 0.52634 22.005 0.0039689 22.162 0.75372 32.802 0.69194 24.099 3054.11 14.37 0.79635 29.594
3 0.25837 7.4643 0.0020239 11.57 0.32637 9.3365 0.19114 7.991 0.0021911 12.235 0.23222 10.106 0.31848 11.092 2377.73 11.187 0.20321 7.5516
4 0.15808 4.567 0.0013152 7.52 0.12004 3.4338 0.13121 5.4855 0.001389 7.756 0.090556 3.941 0.11404 3.9718 1619.04 7.6176 0.097945 3.6398
5 0.11408 3.2958 0.0012359 7.07 0.063263 1.8098 0.0775 3.2401 0.0010267 5.733 0.048222 2.0986 0.095926 3.3408 1355.77 6.3789 0.044369 1.6488
6 0.082183 2.3743 0.0008508 4.86 0.052259 1.4949 0.062926 2.6307 0.0007592 4.2394 0.029695 1.2923 0.066596 2.3194 1199.75 5.6448 0.036108 1.3418
7 0.067379 1.9466 0.0006689 3.82 0.040816 1.1676 0.047374 1.9806 0.0004821 2.6917 0.026251 1.1425 0.057323 1.9964 847.751 3.9887 0.027866 1.0355
8 0.047199 1.3636 0.0005117 2.93 0.028761 0.82277 0.027375 1.1445 0.0003974 2.2188 0.021959 0.95564 0.038132 1.328 654.772 3.0807 0.023528 0.87435
9 0.042803 1.2366 0.0004759 2.72 0.02287 0.65423 0.024368 1.0188 0.0002751 1.5361 0.015053 0.65511 0.028324 0.98644 451.071 2.1223 0.011699 0.43476
10 0.036629 1.0582 0.0003388 1.94 0.019407 0.55517 0.022235 0.92957 0.0002195 1.2256 0.012205 0.53115 0.026229 0.9135 260.217 1.2243 0.010991 0.40846
11 0.029564 0.85411 0.0002801 1.6 0.018012 0.51525 0.018284 0.7644 0.0001983 1.1071 0.0095422 0.41527 0.022362 0.77882 192.182 0.90421 0.0093167 0.34622
12 0.024068 0.69533 0.0002673 1.53 0.0124 0.35473 0.016224 0.67826 0.0001709 0.95399 0.0092834 0.40401 0.018511 0.64469 149.678 0.70423 0.0067162 0.24958
13 0.020985 0.60624 0.000242 1.38 0.007231 0.20685 0.015797 0.66042 0.0001117 0.62376 0.0056919 0.24771 0.016065 0.55951 111.618 0.52516 0.0041019 0.15243
14 0.017411 0.503 0.000204 1.1664 0.0048551 0.13889 0.0096731 0.4044 9.00E-05 0.50246 0.0051032 0.22209 0.01484 0.51682 - - 0.0030051 0.11168
15 0.013069 0.37758 0.0001706 0.9757 0.0036215 0.1036 0.008409 0.35155 6.98E-05 0.38949 0.0027781 0.1209 0.0096934 0.3376 - - 0.0028085 0.10437
77
Tabela 3. Anlise de varincia multivariada (MANOVA) no paramtrica entre as diferentes guildas utilizando a Matriz ecomorfolgica
tradicional. Em negrito os resultados estatisticamente significantes (p< 0.05; correo de Bonferroni).
Aderente Arborcola Bentnico Carnvoro Macrfago Nectnico Nidicola Suspension feeder Suspension rasper
Aderente 0 0.0845 0.8664 0.0289 0.1993 0.3429 0.0689 0.0152 0.1706
Arborcola - 0 0.1607 0.093 0.2456 0.1479 0.2027 0.0163 0.0942
Bentnico - - 0 0.9089 0.171 0.0165 0.2819 0.1222 0.4689
Carnvoro - - - 0 0.2491 0.2271 0.0977 0.0907 0.2979
Macrfago - - - - 0 0.3345 0.6676 0.3359 0.4989
Nectnico - - - - - 0 0.1152 0.0233 0.538
Nidicola - - - - - - - 0.8576 0.1933
Suspension feeder - - - - - - - 0 0.0365
Suspension rasper - - - - - - - - 0
Tabela 4. Anlise de varincia multivariada (MANOVA) no paramtrica entre as diferentes guildas utilizando a Matriz ecomorfolgica dorsal.
Em negrito os resultados estatisticamente significantes (p< 0.05; correo de Bonferroni).
Arborcola Bentnico Carnvoro Gastomyzophorus Macrfago Nectnico Suspension feeder Suspension rasper
Arborcola 0 0.0642 0.9007 0.1631 0.2343 0.5887 0.0339 0.2701
Bentnico - 0 0.1268 0.1276 0.0564 0.0704 0.0052 0.2337
Carnvoro - - 0 0.1923 0.2666 0.9116 0.1841 0.3702
Gastomyzophorus - - - 0 0.3445 0.1793 0.3293 0.2459
Macrfago - - - - 0 0.283 0.0464 0.0979
Nectnico - - - - - 0 0.2792 0.8076
Suspension feeder - - - - - - 0 0.0487
Suspension rasper - - - - - - - 0
78
Tabela 5. Anlise de varincia multivariada (MANOVA) no paramtrica entre as diferentes guildas utilizando a Matriz ecomorfolgica lateral. Em
negrito os resultados estatisticamente significantes (p< 0.05; correo de Boferroni).
Aderente Arborcola Bentnico Carnvoro Gastromyzophorus Macrfago Nectnico Nidicola Suspension feeder Suspension rasper
Aderente 0 0.8551 0.7027 0.4102 0.2027 0.0655 0.1828 0.0696 0.004 0.0271
Arborcola - 0 0.0348 0.8976 0.3347 0.9543 0.1211 0.95 0.0163 0.7993
Bentnico - - 0 0.1329 0.053 0.1673 0 0.1381 0 0.0778
Carnvoro - - - 0 0.172 0.763 0.5578 0.4654 0.0033 0.1338
Gastromyzophorus - - - - 0 0.3364 0.057 0.3292 0.1361 0.2519
Macrfago - - - - - 0 0.5553 0.3286 0.0343 0.2025
Nectnico - - - - - - 0 0.1424 0 0.0684
Nidicola - - - - - - - 0 0.0335 0.1981
Suspension feeder - - - - - - - - 0 0.215
Suspension rasper - - - - - - - - - 0
79
Tabela 6. Teste de permutao (ANOVA) para Anlise de Redundncia Parcial (RDA). Var=
Varincia; F= Estatstica F; N.Pe= Nmero de permutaes.
GL Var F N.Pe P
Model: rda(formula = ecomg ~ morfomg + filomg)
Ecomorfolgica lateral 13 0.01 3.958 99 0.01
Filogentica 6 0.003 2.295 99 0.01
Resduos 82 0.016 - - -
Model: rda(formula = ecod ~ morfod + filod)

Ecomorfolgica dorsal 8 0.009 3.834 99 0.01
Filogentica 5 0.004 2.991 99 0.01
Resduos 54 0.017 - - -
Model: rda(formula = ecomt ~ morfomt + filomt)

Ecomorfolgica Tradicional 7 0.006 2.309 99 0.01
Filogentica 5 0.010 4.852 99 0.01
Resduos 53 0.022 - - -
80
FIGURAS
A)
B)
Figura 1. Medidas morfomtricas tradicionais nos girinos A) Vista lateral: CT= Comprimento
total; CC= Comprimento do corpo; ANV= Altura da nadadeira ventral; AND= Altura da
nadadeira dorsal; AC= Altura do corpo; DOF= Distncia olho-focinho; DNF= Distncia
narina-focinho; B) Vista dorsal: LMC= Largura da musculatura caudal; LC= Largura do
corpo; DIO= Distncia interocular; DIN= Distncia internasal; Dmn= Dimetro da narina;
Dmo= Dimetro do olho.
A)
B)
Figura 2. Marcos anatmicos utilizados na Morfometria Geomtrica. A) Vista lateral (sensu

Van Buskirk 2009) e B) Vista dorsal. Em vista lateral o centro da abertura do espirculo no
foi incluso como marco anatmico (marco anatmico nmero 9 em Van Buskirk 2009) por
sua localizao ser muito varivel entre as espcies (sinistro, lateral, ventral lateral, ventral
posterior e ventral central; Altig & McDiarmid, 1999b), tornando difcil sua visualizao e
marcao.
81
3.2
2.4
1.6
0.8
Component 2
-2 -1.5 -1 -0.5 0.5 1 1.5 2 2.5
-0.8
-1.6
-2.4
-3.2
-4
Component 1
Figura 3. Anlise de componentes principais na matriz ecomorfolgica tradicional, as cores

representam as guildas ecomorfolgicas. Preto= Bentnico, Verde= Nectnico, Azul=
Suspension feeder, Vermelho= Arborcola, Rosa= Aderente, Amarelo= Carnvoro, Cinza=
Macrfago, Roxo= Nidicola, Marrom= Suspension rasper.
2.4
1.8
1.2
0.6
Component 2
-4.8 -4 -3.2 -2.4 -1.6 -0.8 0.8 1.6
-0.6
-1.2
-1.8
-2.4
-3
Component 1
Figura 4. Anlise de componentes principais na matriz ecomorfolgica dorsal, as cores

Macrfago, Roxo= Nidicola, Marrom= Suspension rasper, Azul escuro= Gastromyzophorus.
82
1.2
0.6
-4 -3 -2 -1 1 2 3 4
-0.6
Component 2
-1.2
-1.8
-2.4
-3
-3.6
Component 1
Figura 5. Anlise de componentes principais na matriz ecomorfolgica lateral, as cores

Macrfago, Roxo= Nidicola, Marrom= Suspension rasper, Azul escuro= Gastromyzophorus.
Tradicional
Morfologia
Filogenia
Dorsal
Interao
Resduos
Lateral
-20 0 20 40 60 80 100 120
Figura 6. Resultado da Anlise de Redundncia Parcial. Interao (componente b, segundo

Diniz-Filho et al. 1998)= Interao entre os componentes morfolgico (componente a) e o
filogentico (componente c).
83
Anexo 1
No. Descrio
---- --------------------------------------
Ponta do focinho
Ponto de mnima curvatura do lado anterior direito do corpo
Ponto de mnima curvatura do lado anterior esquerdo do corpo
Centro do olho direito
Centro do olho esquerdo
Ponto de mxima curvatura do lado anterior direito do corpo
Ponto de mxima curvatura do lado anterior esquerdo do corpo
Ponto de mxima curvatura do lado posterior direito do corpo
Ponto de mxima curvatura do lado posterior esquerdo do corpo
Ponto em que a nadadeira caudal se une ao lado esquerdo do corpo
Ponto em que a nadadeira caudal se une ao lado direito do corpo
Insero da nadadeira caudal no lado direito do corpo
Insero da nadadeira caudal no lado esquerdo do corpo
Borda da nadadeira caudal no lado direito do corpo a 1/3 de distncia entre #11 e # 18
Borda da nadadeira caudal no lado esquerdo do corpo a 1/3 de distncia entre #10 e #18
Borda da nadadeira caudal no lado direito do corpo a 2/3 de distncia entre #11 e # 18
Borda da nadadeira caudal no lado esquerdo do corpo a 2/3 de distncia entre #10 e # 18
Ponta da cauda
84
CAPTULO 3 (a ser submetido para a revista Natureza & Conservao)
Ecomorphology of benthic tadpoles
Fausto Nomura, Tadeu Siqueira2 & Denise de Cerqueira Rossa-Feres3

1
Departamento de Ecologia, Universidade Federal de Gois, UFG, Cx. Postal 131, St.
Itatiaia, CEP 74001-970, Goinia, GO, Brasil. E-mail: fausto_nomura@yahoo.com.br
(corresponding author)
3
Universidade Estadual Paulista, UNESP, Rua Cristvo Colombo, 2265, Jd. Nazareth, CEP
15054-000, So Jos do Rio Preto, SP, Brazil
ABSTRACT
The relationship among morphology, physiology and ecological performance has been used
to understand individual behavior, trophic interactions and the evolution of morphological
diversity. By combining ecology and evolutionary history, we are capable to test hypothesis
about processes that shape biological assemblages. In this study, we analyze how ecological
preferences of benthic tadpoles can be explained by their ecological interactions (measured
by morphological diversity) and by their phylogenetic relationship. Morphological diversity
was inferred from raw morphological data (RMD) and ecomorphological attributes (EMA),
whereas phylogenetic relationship was inferred from recent phylogenetic hypothesis. We used
a partial redundancy analysis to partition the variation in tadpoles' ecological preferences into
morphological and phylogenetic components. We found that ecological preferences of
tadpoles were better explained by from phylogeny than by morphology. When considering
EMA, the morphological influence remained lesser than the phylogenetic signal, but became
greater than the component shared by phylogenetic and morphological information,

85
indicating that it is easier to segregated phylogenetic signals from morphology when using
ecomorphological attributes. Thus, for studies aiming to investigate behavioral functional
aspects, the use of EMA data appears to be more adequate. Both results indicate that
phylogenetically close species are more prone to share habitat preferences, denoting that
interspecific interactions contribute less than ecological filters to the tadpoles' guild
preferences.
Keywords: Ecological filters, interspecific interactions, patristic distance, partial redundancy
analysis.
INTRODUCTION
In the tropics, tadpoles have different adaptations involved in microhabitat use and feeding
behavior (Hoff et al., 1999), but once most of these anurans lay eggs in lentic and temporary
ponds, as depressions in the trunks of fallen trees, large pools, and water accumulated in
epiphytes or snail shells (Inger, 1985; Starrett, 1973; Duellman & Trueb, 1986; Menin et al.,
2006), the majority of tropical anuran species have benthic tadpoles (Salthe & Mecham, 1974
Diaz Panigua 1989). Higher morphological divergence among tadpoles were generally
detected along high order habitat dimensions, as stream vs. pond, benthic vs. pelagic, and
hydroperiod (Van Buskirk 2009). The adaptive history of tadpoles appears to be linked to the
adaptation into these higher order habitat dimensions, once such adaptive radiations required
the evolution of specific bauplan (Roelants et al. 2011). This can be true because the effect of
stabilizing selection on sets of characters that had functional importance should be greater
than the selective pressures of individual characters (Richardson & Chipman 2003).
The relationship among morphology, physiology and ecological performance has been
used to understand individual behavior, trophic interactions and the evolution of
morphological diversity (Pettersson & Hedenstrm, 2000). In this context, the

86
ecomorphological approach assumes that a particular environment restricts both the
morphology and ecology in parallel. Thus, patterns in the ecology of individuals, populations
or groups of species can be inferred through morphological characters (Mullaney & Gale,
1996). By using this approach, it is possible to detect morphological differences among
species and associate these differences with environmental pressures and biological factors,
as competition and predation (Irschik & Losos, 1999). These differences could be easily
extracted from morphometric data, and allow for the detection of how ecological pressures
are related to shaping functional guilds, community assembling rules, and species interaction
(such as predation and competition).
Functional differences and ecological performance that result in changes in the
exploitation of resources can lead to morphological changes (Breda, 2005). Also, the
evolutionary history has an important role in the determination of evolution of functional
aspects of morphological characters (Altig & McDiarmid, 1999a). Several studies have
demonstrated that many patterns of use and sharing of resources can be more easily explained
based on the characteristics of the evolutionary lineages that comprise the biological
community (Brooks & McLennan, 1993; Cadle & Greene, 1993; Martins, 1994; Vitt et al.,
1999; Eterovick & Fernandes, 2001; Webb et al., 2002). This new approach combines
ecology and the evolutionary history of species and allows us to test hypothesis about the
processes that shaped a community (Brooks & McLennan, 1991). In approach, the
environment act as a filter, selecting lineages or traits of tadpoles better adapted to these
specific habitat conditions (Mouillot et al., 2007).
These two approaches (ecomorphological and phylogenetic) can be combined to infer
the total contribution of biotic interactions and historical processes in determining tadpoles
microhabitat preferences. This could be done by considering the morphological variation
(measured by morphological similarity ecomorphology approach) as a surrogate for biotic

87
interactions and phylogenetic relationships (measured by phylogenetic distance
evolutionary approach) as a surrogate of historical effects. In this study, we aim to analyze
how microhabitat use of benthic tadpoles from temporary ponds can be explained by biotic
and historical components. We attempt to answer what drive the microhabitat choices of
benthic tadpoles, a convergence adaptive process mediated by interspecific interactions
(correlation with morphology) or a common evolutionary history (correlation with
phylogeny).
MATERIAL AND METHODS
We analyzed tadpoles of 22 anuran species, deposited in the scientific amphibian collection
(DZJSRP-Tadpoles) of the Universidade Estadual Paulista, UNESP, So Jos do Rio Preto,
So Paulo State, Brazil. These tadpoles were collected in temporary ponds located in Nova
Aliana, So Jos do Rio Preto and Vitria Brasil, So Paulo State, Brazil. Although the
primary objective here is to evaluate the total contribution of phylogeny and morphology to
the microhabitat distribution of benthic tadpoles, we also included nektonic tadpoles as
comparative tools to the groups obtained for the benthic tadpoles, and also included
suspension feeders and macrophagous tadpoles that are commonly found in benthic
microhabitats (Table 1). The taxonomic classification of tadpoles follows Frost et al. (2006),
Faivovich et al. (2005) and Nascimento et al. (2005).
Data Set
Ecological attributes of the tadpoles related to habitat use was inferred from Provete (2010),
Prado et al. (2009), Laufer & Barreneche (2008), Kolenc et al. (2008), Echeverra et al.
(2007), Eterovick & Barata (2006), Kolenc et al. (2006), Rossa-Feres & Nomura (2006),
Candioti et al. (2004), Peltzer & Lajmanovih (2004), Rossa-Feres et al. (2004), Nomura et al.
(2003), Lajmanovich (2000), and Lavilla (1992). Based on these works, the tadpoles were
88
classified according to the position in the water column (deep and distance to the margin),
association to vegetation (high or low plant cover), and ecomorphological guild (according to
Altig and McDiarmid 1999). These ecological categories were organized in a binary matrix
which was transformed by the mixed-variables coefficient of distance, a generalization of the
Gower's coefficient (Pavoine et al. 2009), in an distance matrix named as tadpoles' ecological
attributes (TEA matrix).
To evaluate the relationship between the ecological attributes with tadpole
morphology, we measured seventeen morphometric dimensions (Altig & McDiarmid 1999b)
for each species: total length; body length; maximum body height; maximum body width; eye
diameter; nostril diameter; interorbital distance; internarial distance; nostril-snout distance;
eye-snout distance; tail length; maximum dorsal fin height; maximum ventral fin height;
maximum tail muscle height; maximum tail muscle width; spiracle length and vent tube
length (Fig. 1). These measurements were taken from tadpoles in developmental stages 26 to
40 (Gosner, 1960), under a Zeiss stereomicroscope with an ocular micrometer at 8.0x
magnification. For Chiasmocleis carvalhoi, Leptodactylus notoaktites and Leptodactylus
elenae, morphometrics data were obtained from Wogel et al. (2004), De S et al. (2007) and
Prado & dHeursel (2006), respectively. We named this data matrix as raw morphological
dimensions (RMD). To separate the size effect of morphometric attributes, we used the
logarithmic transformation.
Subsequently, these morphometric dimensions were transformed in eleven
ecomorphological attributes that represent differential performances of the tadpoles according
to habitat use, adapted from those commonly used to fishes (Gatz, 1979a,b; Watson & Balon,
1984; Balon et al., 1986): body shape; relative tail length; relative dorsal fin height; relative
ventral fin height; relative tail muscle width; relative nostril size; nostril position on the
transverse axis; nostril position on the longitudinal axis; relative eye size; relative spiracle
89
length and relative vent tube size. We named this data matrix as ecomorphological attributes
(EMA matrix).
If we find a strong relationship between TEA matrix and morphology (RMD and
EMA) matrices, it is reasonable to infer, according to the ecomorphological approach, that
the diversification in habitat use is resultant of the intensity of interspecific interactions, such
as competition. Conversely, the tadpole ecological preferences could be resultant of niche
conservatism, which is the tendency for closely related species to be ecologically similar,
and, in such case, the TEA matrix should reflect the phylogenetic relationship of the tadpoles.
If ecological filters are the process acting in the determination of the ecological preferences
of benthic tadpoles, a measure of phylogenetic distance should explain the tadpoles
microhabitat preferences better than the RMD or EMA matrices. To address this hypothesis,
we constructed a phylogenetic matrix (PHY) calculating the patristic distance among all
possible tadpoles pairs, based on the phylogenetic hypothesis presented in Frost et al. (2006)
(Fig. 2), with the Athephastanura clade replaced by the topology presented in Grant et al.
(2006).
Statistical Analysis
To test whether ecological filters or competition determine the TEA preferences of benthic
tadpoles, we use the morphology (RMD and EMA matrices) and phylogeny (PHY matrix) as
predictors of the variance found in ecological attributes of tadpoles (TEA matrix). To test this,
we submitted our data set to the variation partitioning method (Borcard et al. 1992) based on
a redundancy analysis (RDA) (Legendre & Legendre 1998). By using this analysis, we aimed
to infer to which degree the ecological attributes of tadpoles is explained by morphology
(RMD or EMA matrices), by phylogeny (PHY matrix), or by an interaction of both. The
method allows the partitioning of the phenotypic variation, in this case the microhabitat
preferences, into phylogenetic and other specific components, as morphology (Diniz-Filho et

90
al. 1998). This technique starts with a principal coordinate analysis (PCoA; Legendre &
Legendre 1998) on the PHY matrix and, in our case, on the TEA matrix. The PCoA extracts
eigenvalues and eigenvectors directly from distance matrices, with final results being similar
to those obtained with the principal component analysis (PCA) (Diniz-Filho et al. 1998;
Legendre & Legendre 1998). As a matter of fact, to a given data matrix on which a PCA has
been computed, the eigenvectors obtained by PCoA would be directly comparable (Legendre
& Legendre 2003). This property allow us to use the PCA to reduce the morphological
information in principal components (eigenvectors), avoiding colinearity among
morphological traits, and compare these morphological eigenvectors (eRMD and eEMA
matrices) to eigenvectors extracted from PHY and TEA matrices by the PCoA analysis. Thus,
in RDA, the eigenvectors of the TEA matrix (eTEA) composed our response matrix whereas
the eigenvectors of the PHY matrix (ePHY) and of the morphological matrices (eRMD and
eEMA) composed the predictor matrices.
Variation partitioning is more suitable than analyzing the individual contribution of
regressors via their partial correlation coefficients, and the total percentage of variation
explained by the model (R2) is partitioned into unique and common contributions of the set
of predictors (Peres-Neto et al. 2006). In our analysis, we used the sample bias correction
proposed by Peres-Neto et al. (2006) and obtained adjusted R2 values from the varpart
function, available in the vegan library in R-language (Oksanen et al 2005). We used this
approach to test the amount of contribution from interspecific interactions (predicted from
eRMD and eEMA matrices), niche conservatism (predicted from ePHY) and the shared
contribution of both to the microhabitat preferences (eTEA) of benthic tadpoles. After
assessing the total contribution of interespecific interactions and niche conservatism, we
evaluate both terms in the model using an ANOVA like permutation test for RDA to assess
the significance of constraints (Oksanen et al. 2005).

91
The RDA partition indicates which component explains the higher amount of
variation in the ecological attributes of benthic tadpoles, but does not indicates which
mechanism is generating the described pattern. If niche conservatism is the dominant process
in the determination of the assemblages of benthic tadpoles, we expected that closely related
species would be positioned closer to each other in the microhabitat space than to unrelated
species. Conversely, if interspecific interactions are the dominant process, we expected that
closely related species would be positioned further from each other in the microhabitat space
than unrelated species. To detect this effect, we use the RDA to assess how each component
of our models, morphlogical and phylogenetic, were affecting the microhabitat preferences of
benthic tadpoles, by comparing the relative position of species that compose the clades
showed in the figure 1. For the purpose of this analysis, these species were considered
closely related and their relative position compared to congeneric and unrelated species. The
RDA could be considered a special multiple regression that correlates a multiple response
variable Y with a common matrix of predictors X (Peres-Neto et al 2006). In this case, the
percentage of variation of the response matrix explained by the predictor matrix is the
canonical equivalent of the regression coefficient of determination, R2 (Peres-Neto et al
2006).
PCoA and PCA analysis were carried out using the software Past version 2.02
(Hammer et al., 2001). All other analyses were made in R environment (R Development
Core Team, 2010).
RESULTS
According to our PCA, the variation found in the RMD could be resumed in the five first
principal components (96.72%), whereas the variation found in the EMA in the six first
principal components (96.81%). In PCoA, the first nine principal coordinates resumed
92
95.20% of the phylogenetic variance, whereas the 12 first principal coordinates resumed
96.48% of total variance in the TEA (Tab. 2). Comparing the two morphological data sets
(RMD and EMA), the resultant configuration shows some discrepancies between the results.
When we used the EMA data matrix, the species were scattered in the diagram, showing a
large variation in the morphological attributes when compared to the diagram produced by
RMD data matrix (Fig. 3). Furthermore, the species differed not only in distribution but also
in relative position. For example, while in the EMA output the Leptodactylidae species were
separated by species of the remaining families, in the RMD the Leptodactylidae species were
grouped, with the exception of Leptodactylus latrans (Fig. 3).
Variation partitioning analysis using eRMD showed a greater contribution of the
phylogenetic component (component c) and shared morphological and phylogenetic
component (component b) than the morphological component alone (component a) in
explaining the variation in ecological preferences of benthic tadpoles (Fig. 4). However,
when using eEMA, the morphological component was lower than the phylogenetic
component, but larger than the shared morphological and phylogenetic component (Fig. 4).
Both results indicate that phylogenetic and morphological components significantly affect
microhabitat preferences (table 3). Also, the contribution of morphology is larger when it was
represented by eEMA than by eRMD, being easiest to segregate between phylogenetic and
morphological components from microhabitat preferences when using ecomorphological
attributes (Fig. 4).
Since both terms in our model were significant, we analyzed the distribution of the
species included in the selected clades using the phylogenetic and morphological component.
When ePHY was used to explain the variation in the ecological space, L. podicipinus+L.
ocellatus, P. saltica+P. mystacalis+P. Pseudopaludicola sp. and L. notonektites+L. eleneae
clades were clustered, but E. bicolor+D. muelleri, H. raniceps+H. albopunctatus and P.

93
cuvieri+P. centralis clades were not (Fig. 5). Also, H. lundii and H. albopunctatus tadpoles
had convergent habitat preferences in relation to Leiuperidae tadpoles. When we considered
eRMD or eEMA as explanatory matrices in our RDA analysis, the L. podicipinus+L.
ocellatus and P. saltica+P. mystacalis+P. Pseudopaludicola sp. Clades were the only ones
that were clustered, and we find that the ecological preferences among Leiuperidae and
Leptodactylidae are convergent (Fig. 6 and 7).
DISCUSSION
Our study demonstrates that tadpoles' ecological preferences are resultant of phylogenetic
constraints, as predict by the niche conservatism hypothesis (Horner & Bohannan 2006,
Cavender-Bares et al. 2009). Larval external morphology can be used to reveal phylogenetic
patterns in anurans, since it is resultant of historical factors that selected larval characteristics
according to specific microhabitat structure, i.e., current tadpole preference is the result of the
ancestors' microhabitat choices. However, our results also suggest that niche conservatism is
not the only process acting on the definition of the habitat preferences of benthic tadpoles.
Morphological convergence promoted by ecological pressures, also clustered distant taxa in
the same ecomorphological group (Altig & McDiarmid 1999b; Motta & Kotrschal, 1992;
Winemiller et. al., 1995), which is a sign that adaptive processes (biotic or abiotic) were also
important to determinate the current structure of the community. We suggest, then, that niche
conservatism and interespecific interactions are concurrent processes that determinate the
guild structure, once each process could affect different clades and could be generated by the
ecological filters mechanism (Angermeier & Winston, 1998).
The secondary changes resulting from adaptive radiation and convergent evolution
present in tadpole's morphology (Altig & Johnston 1989) are difficult to isolate when inferred
from raw morphological data. Our results suggest that EMA are more representative of
94
ecological effects in tadpoles morphology, while RMD is more affected by the phylogenetic
component. Although morphology is affected by ecology and behavior, ecomorphological
attributes are more representative of interspecific interactions. For example, the family
Hylidae, one of the most diversified among anurans (Duellman & Trueb, 1986; Faivovich et.
al., 2005) and with great morphological and behavioral diversity among adults (Altig &
McDiarmid, 1999b), showed a strong phylogenetic signal in raw morphological characters
when compared to ecomorphological attributes. Even for tadpole species usually classified as
benthic, as Leiuperidae, Leptodactylidae and Microhylidae, EMA indicates a more diversified
morphology than RMD.
We considered the major contribution of historical mechanisms in the definition of
ecological attributes of tadpoles strikingly surprising, considering the high phenotypic
plasticity presented by several tadpoles of anuran species. Tadpoles can change its
morphology to mediate predator-prey interactions (Kishida & Nishimura 2004, McIntyre et
al. 2004), food availability (F. Nomura, unpubl. data), and interactions with competitors
(Laurila 2000, Barnett & Richardson 2002, Monello et al. 2006). We assumed the ability to
phenotypic variation presented by tadpoles as an indicative that interespecific interactions
were a main mechanism in the definition of ecological preferences. Apparently, interespecific
interactions are important to originate new behavioral patterns that do not necessarily induce
morphological novelties. For example, benthic tadpoles of R. schneideri sometimes swim in
the water column, having benthic habit during the day and neustonic habit during the night
when they feed on the water surface, positioned with the ventral side up (Rossa-Feres &
Nomura, 2006). This kind of new behavior for tadpoles does not need any new morphological
adaptation which, in turn, makes more difficult to infer habitat use from morphology.
There is some controversy about the relative importance of larval characters to infer
anuran evolution, especially when the morphology of larvae suggests different relationships
95
from those obtained from the adults morphology (Wassersug 1980; Haas 2000). Our results
show that the relationship between external morphology and phylogeny is higher using RMD,
but this relationship can vary among families. For studies interested in understanding the
functional aspects of tadpoles relationship, the use of EMA data appears to be more adequate.
In conclusion, although interspecific interactions, as competition and predation pressure, are
important to determine the use of microhabitat by tadpoles (Heyer, 1976; Nomura et al.
2011), our results show that the major contribution, at least for benthic tadpoles, comes from
phylogeny. Morphology is an important ecological aspect that, maybe, is not fully
demonstrated in the habitat affinities (Peres-Neto 1999), but illustrated the ecological
conditions selected early in lineage evolutionary history.
ACKNOWLEDGEMENTS
The authors thanks L.M. Bini and M.V. Cianciaruso for helpful comments. Loma for the data
gathering and initial analysis. CNPq by the financial support (FN, proc. N 472125/2010-9).
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TABLES
Table 1. Tadpoles species included in partial Redundancy Analysis.
Species Family Ecomorphological guild
Rhinella schneideri Bufonidae Benthic
Dendropsophus nanus Hylidae Macrophagous
Hypsiboas albopunctatus Hylidae Benthic
H. lundii Hylidae Benthic
H. raniceps Hylidae Benthic
Scinax fuscovarius Hylidae Nektonic
S. fuscomarginatus Hylidae Nektonic
S. similis Hylidae Nektonic
Trachycephalus venulosus Hylidae Benthic
Eupemphix nattereri Leiuperidae Benthic
Physalaemus centralis Leiuperidae Benthic
P. cuvieri Leiuperidae Benthic
P. marmoratus Leiuperidae Benthic
Pseudopaludicola mystacalis Leiuperidae Benthic
P. saltica Leiuperidae Benthic
Pseudopaludicola sp. Leiuperidae Benthic
Leptodactylus elenae Leptodactylidae Benthic
L. fuscus Leptodactylidae Benthic

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L. labyrinthicus Leptodactylidae Carnivorous
L. notoaktites Leptodactylidae Benthic
L. ocellatus Leptodactylidae Benthic
L. podicipinus Leptodactylidae Benthic
Chiasmocleis carvalhoi Microhylidae Suspension-Feeder
Dermatonotus muelleri Microhylidae Suspension-Feeder
Elachistocleis bicolor Microhylidae Suspension-Feeder
Table 2. Eigenvalues (Evalues) and percent variation explained for Principal Components
Analysis (PCA) and Principal Coordinates Analysis (PCoA) applied to tadpoles'
morphological (RMD = Raw Morphological data set; EMA = Ecomorphological Attributes
data set), Phylogenetic (PHY) and ecological attributes (TEA). Bold numbers indicate the
axis used in partition analysis (total percent explanation higher than 95%).
RMD (PCA) EMA(PCA) PHY(PCoA) TEA(PCoA)
Axis Evalues % Var. Evalues % Var. Evalues % var. Evalues % Var.
1 1.533 64.893 0.101 53.301 367.720 43.517 1.559 25.615
2 0.470 19.889 0.028 14.715 199.760 23.640 1.249 20.519
3 0.205 8.697 0.023 12.343 108.300 12.816 0.753 12.370
4 0.050 2.124 0.017 8.933 58.717 6.949 0.574 9.427
5 0.026 1.118 0.011 5.671 27.335 3.235 0.452 7.428
6 0.020 0.862 0.004 1.848 25.003 2.959 0.373 6.124
7 0.017 0.706 0.003 1.410 7.314 0.866 0.256 4.210

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8 0.013 0.566 0.002 1.007 5.720 0.677 0.191 3.133
9 0.010 0.440 0.001 0.443 4.581 0.542 0.138 2.267
10 0.005 0.200 < 0.001 0.262 4.159 0.492 0.125 2.049
11 0.004 0.155 < 0.001 0.067 3.912 0.463 0.106 1.741
12 0.003 0.131 - - 3.828 0.453 0.097 1.599
13 0.002 0.082 - - 3.481 0.412 0.077 1.258
14 0.002 0.069 - - 3.343 0.396 0.063 1.041
15 0.001 0.050 - - 3.178 0.376 0.044 0.729
16 < 0.001 0.018 - - 2.000 0.237 0.030 0.489

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Table 3. Permutation test for partial Redundancy Analysis (RDA). eETA = Eigenvector
matrix of tadpoles' ecological attributes obtained from a Principal Coordinate Analysis;
eRMD = Eigenvector matrix of tadpoles' raw morphological data obtained from a Principal
Component Analysis; eEMA = Eigenvector matrix of tadpoles' ecomorphological attributes
obtained from a Principal Component Analysis; ePHY = Eigenvector matrix of tadpoles'
patristic distance obtained from a Principal Coordinate Analysis; Df = Degrees of freedom;
Var = Variance; F = F statistic; N.Perm = number of maximum permutations.
Df Var F N.Perm P
Model: RDA (eETA = eRMD + ePHY)
eRMD (a) 5 0.089 3.288 99 0.01
ePHY (c) 9 0.101 2.065 99 0.01
Residual (d) 10 0.054 - - -
Model: RDA (eETA = eEMA + ePHY)
eEMA (a) 6 0.099 3.170 99 0.01
ePHY (c) 9 0.099 2.126 99 0.01
Residual (d) 9 0.045 - - -

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FIGURES
Figure 1. Morphometric variables extracted from tadpoles. A = Dorsal view; B = Lateral
view. Scale = 10mm.TL = total length; BL = body length; BH = maximum body height; BW
= maximum body width; ED = eye diameter; ND = nostril diameter; IOD = interorbital
distance; IND = internarial distance; NSD = nostril-snout distance; ESD = eye-snout
distance; TAL = tail length; DFH = maximum dorsal fin height; VFH = maximum ventral fin
height; TMH = maximum tail muscle height; TMW = maximum tail muscle width; SL =
spiracle length; and VTL = vent tube length.

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[A FIGURA FOI SUPRIMIDA PARA ADEQUAR O TAMANHO DO ARQUIVO]
Figure 2. Phylogenetic relationship of anuran species used to infer the patristic distance. The
numbers inside circles correspond to the clades that the relative position of the species were
compared in the RDA analysis.

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Figure 3. Principal Component Analysis of morphological component of benthic tadpoles.
EMA = Ecomorphological attributes data matrix; RMD = Raw morphological data matrix;
Ccar = Chiasmocleis carvalhoi; Dnan = Dendropsophus nanus; Dmue = Dermatonotus
muelleri; Ebic = Elachistocleis bicolor; Enat = Eupemphix nattereri; Halb = Hypsiboas
albopunctatus; Hlun = Hypsiboas lundii; Hran = Hypsiboas raniceps; Lfus = Leptodactylus
fuscus; Llab = Leptodactylus labyrinthicus; Lele = Leptodactylus elenae; Lnot =
Leptodactylus notoaktites; Lpod = Leptodactylus podicipinus; Loce = Leptodactylus
ocellatus; Pcen = Physalaemus centralis; Pcuv = Physalaemus cuvieri; Pmar = Physalaemus
marmoratus; Pmys = Pseudopaludicola mystacalis; Psal = Pseudopaludicola saltica; Psp =
Pseudopaludicola sp.; Rsch = Rhinella schneideri; Sfum = Scinax fuscomarginatus, Sfus =
Scinax fuscovarius; Ssim = Scinax similis; Tven = Trachycephalus venulosus.

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a b c d
EMA
RMD
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%
Figure 4. Total variance partition of ecological attibutes of tadpoles explained by (a)
morphology, (b) morphology + phylogeny, (c) phylogeny, and (d) neither morphology or
phylogeny residuals. EMA = Ecomorphological attributes data matrix; RMD = Raw
morphological data matrix.
Figure 5. RDA analysis of microhabitat preferences of benthic tadpoles when explained by
the phylogenetic relationship among tadpoles. The numbers after species abbreviations
indicates the species that are considered closely related in this analysis (see figure 2). Ccar =
Chiasmocleis carvalhoi; Dnan = Dendropsophus nanus; Dmue = Dermatonotus muelleri;

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Ebic = Elachistocleis bicolor; Enat = Eupemphix nattereri; Halb = Hypsiboas albopunctatus;
Hlun = Hypsiboas lundii; Hran = Hypsiboas raniceps; Lfus = Leptodactylus fuscus; Llab =
Leptodactylus labyrinthicus; Lele = Leptodactylus elenae; Lnot = Leptodactylus notoaktites;
Lpod = Leptodactylus podicipinus; Loce = Leptodactylus ocellatus; Pcen = Physalaemus
centralis; Pcuv = Physalaemus cuvieri; Pmar = Physalaemus marmoratus; Pmys =
Pseudopaludicola mystacalis; Psal = Pseudopaludicola saltica; Psp = Pseudopaludicola sp.;
Rsch = Rhinella schneideri; Sfum = Scinax fuscomarginatus, Sfus = Scinax fuscovarius;
Ssim = Scinax similis; Tven = Trachycephalus venulosus.
Figure 6. RDA analysis of microhabitat preferences of benthic tadpoles when explained by
the raw morphological measurements of benthic tadpoles. The numbers after species
abbreviations indicates the species that are considered closely related in this analysis (see
figure 2). Ccar = Chiasmocleis carvalhoi; Dnan = Dendropsophus nanus; Dmue =

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Dermatonotus muelleri; Ebic = Elachistocleis bicolor; Enat = Eupemphix nattereri; Halb =
Hypsiboas albopunctatus; Hlun = Hypsiboas lundii; Hran = Hypsiboas raniceps; Lfus =
Leptodactylus fuscus; Llab = Leptodactylus labyrinthicus; Lele = Leptodactylus elenae; Lnot
= Leptodactylus notoaktites; Lpod = Leptodactylus podicipinus; Loce = Leptodactylus
ocellatus; Pcen = Physalaemus centralis; Pcuv = Physalaemus cuvieri; Pmar = Physalaemus
marmoratus; Pmys = Pseudopaludicola mystacalis; Psal = Pseudopaludicola saltica; Psp =
Pseudopaludicola sp.; Rsch = Rhinella schneideri; Sfum = Scinax fuscomarginatus, Sfus =
Scinax fuscovarius; Ssim = Scinax similis; Tven = Trachycephalus venulosus.
Figure 7. RDA analysis of microhbitat preferences of benthic tadpoles when explained by
the ecomorphological attributes of benthic tadpoles. The numbers after species abbreviations
indicates the species that are considered closely related in this analysis (see figure 2). Ccar =
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Chiasmocleis carvalhoi; Dnan = Dendropsophus nanus; Dmue = Dermatonotus muelleri;
Ebic = Elachistocleis bicolor; Enat = Eupemphix nattereri; Halb = Hypsiboas albopunctatus;
Hlun = Hypsiboas lundii; Hran = Hypsiboas raniceps; Lfus = Leptodactylus fuscus; Llab =
Leptodactylus labyrinthicus; Lele = Leptodactylus elenae; Lnot = Leptodactylus notoaktites;
Lpod = Leptodactylus podicipinus; Loce = Leptodactylus ocellatus; Pcen = Physalaemus
centralis; Pcuv = Physalaemus cuvieri; Pmar = Physalaemus marmoratus; Pmys =
Pseudopaludicola mystacalis; Psal = Pseudopaludicola saltica; Psp = Pseudopaludicola sp.;
Rsch = Rhinella schneideri; Sfum = Scinax fuscomarginatus, Sfus = Scinax fuscovarius;
Ssim = Scinax similis; Tven = Trachycephalus venulosus.

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CAPTULO 4 (submetido a revista Biotropica)
Are assemblages of aquatic-breeding anurans niche-structured or neutral?
Muryllo Melo1, Fernanda Fava1, Hugo Bonfim Arruda Pinto2, Fausto Nomura1, 3
1
Laboratrio de Herpetologia e Comportamento Animal, Departamento de Ecologia,
Instituto de Cincias Biolgicas, Universidade Federal de Gois, CP 131, CEP 74000-970,
Goinia, GO, Brasil

2
RAN - Centro Nacional de Pesquisa e Conservao de Rpteis e Anfbios, Setor Leste
Universitrio, CEP: 74.605.090, Rua 229, n 95, Goinia/GO, Brasil

3
Laboratrio de Ecologia de Comunidades, Departamento de Ecologia, Instituto de Cincias
Biolgicas, Universidade Federal de Gois, CP 131, CEP 74000-970, Goinia, GO, Brasil
ABSTRACT
Local niche processes (Grinnellian or Eltonian) and dispersal are considered to be important
determinants of community composition and species diversity. Studies focused on the
structure of anuran assemblages have found multiple responses relating to these effects. In
this study we analyzed the effects of environmental and spatial variables on anuran
assemblages, using partial redundancy analysis to evaluate the variation in 30 species of
anurans with aquatic development in savanna and forest habitats. We also used null model
analysis to investigate the existence of biological interactions affecting an anuran assemblage
of 33 breeding sites. An Eltonian niche was the unique predictor for the structure of the
aquatic-breeding anuran assemblages, whereby species tended to co-occur more often than
would be expected by chance. We suggest that the lack of a local heterogeneity effect could
be related to a difference in how species respond to habitat heterogeneity. The small

117
proportion of the observed variation measured by variation partitioning analysis can be
explained by the lack of a relationship between aquatic-breeding terrestrial frogs and habitat
heterogeneity. It could also be due to an unmeasured environmental axis that is uncommonly
found to affect anuran species distribution and generalist species composition. We suggest
that the dispersal restriction effects are explained by the lack of a spatial relationship.
Furthermore, we hypothesized that life-history traits, operating as isolating barriers, allow
local species coexistence and contribute to the structure of assemblages at this scale. Aquatic-
breeding anurans exhibit more sensitivity to environmental factors and to specific threats as
habitat split. Meanwhile, in comparison with the results of other studies, we hypothesized that
aquatic-breeding arboreal anurans are more threatened and sensitive than aquatic-breeding
terrestrial anurans.
Key words: co-occurrence, null model, community structure, Cerrado, Grinnellian niche,
Eltonian niche, redundancy analysis
INTRODUCTION
Much of the last five decades of community ecology have been widely focused on the
analysis and interpretation of the relationship between species niche and communities, in
order to understand more about the mechanisms that determine species distributions and the
structure of ecological communities (Hutchinson 1959, Gotelli & McCabe 2002, Kneitel &
Chase 2004). Ecological communities and assemblages are the result of short-term ecological
interactions and/or long-term evolutionary processes that operate at different timescales and
which therefore affect the number and identity of the species that co-occur in local
communities (Ricklefs 2004). Thus, for ecological communities, it is important to describe
how an organism can be affected by the distribution of resources, predators and/or
competitors and how these organisms or populations can alter those same biotic and abiotic
118
factors that describe the niches of ecological communities (Schoener 1974, Lamolino &
Brown 1998).
In this context, Grinnell (1917) emphasized the niche concept as representing the
abiotic requirements for species persistence. Thus, Grinnells niche is concerned with the
place in which an organism lives, characterized by a set of environmental conditions (Chase
& Belovsky 1994, Leibold 1995, Leibold & Mikkelson 2002). The pattern related to a
Grinnells niche is the result of physical structure, because habitat heterogeneity can be used
to describe the available niche volume, allowing a higher species diversity in an ecological
community because a higher habitat diversity has a higher niche volume (Hutchinson 1959,
Pianka 1966, Ricklefs 2004). On the other hand, other studies have pointed out that local
communities can be organized mainly by biotic process, reflecting Eltons concept of niche
processes at the local scale (Elton 1927). In the Eltonian niche, the emphasis has been placed
on the role of the relationships between species in organizing communities (Woodward 1983,
McCarthy 1997). Hence, the Eltonian niche is more focused on the role of species and higher-
order taxonomic groupings in the ecological community (Schoener 1989), and is useful for
understanding the community structure as determined by "assembly rules" (Diarmid 1975).
Eltonian niche components are generally analyzed using the co-occurrence patterns of species
(Albrecht & Gotelli 2001), in which species can show different levels of resource
monopolization and partitioning (spatial or temporal) or be locally absent due to competitive
exclusion (Roughgarden 1972, Lehtinen & Carfagno 2011).
Modern community ecologists have debated whether communities are independent or
not (Sokal 1978, Legendre 1993), suggesting that spatial structure plays an important role in
ecological processes (Legendre & Fortin 1989). Understanding organism movements, such as
dispersal and immigration, is more important, according to this concept, to explaining the
composition of ecological communities than are Eltonian or Grinnellian niches; this is known
119
as the neutral theory of biodiversity and biogeography (Hubbell 2011). This spatial
relationship also suggests that regional variables influence ecological communities because
they are spatially structured (Sokal 1978, Legendre & Legendre 1998). According to this
theory, the observed patterns in the ecological community structure are the result of stochastic
processes, such as ecological drift (Tilman 2004); these random communities are not
influenced by species traits and/or environmental conditions, thereby assuming that all
species are equal on a per-capita basis (Hubbell 1979, 2001, Bell 2001).
In general, anuran species are affected by the effects of local niche processes
(Grinnellian or Eltonian). Suitability of breeding habitats (Zimmerman & Bierregaard 1986),
hydroperiod (Baber et al. 2004) and complexity and heterogeneity of habitats (Ernst et al.
2006) are the most prominent of the abiotic factors that influence anuran species distribution.
Anuran assemblages are also niche-structured according to biotic interactions, which have
been widely observed and are mostly related to predation and competition for breeding
habitat (Morin 1983, Gascon 1995). In contrast, some studies suggest an apparent absence of
biotic or abiotic influences on the structure of anuran assemblages (Gotelli & McCabe 2002,
Santos et al. 2007), which could suggest that such niche effects have been important in the
past but do not influence the contemporary composition of anuran assemblages (Duellman &
Trueb 1994). Recent works suggest that spatial factors, though generally affecting
environmental variables (Parris 2004, Ernst & Rdel 2008), had a low influence on anuran
assemblages. Anuran species with different types of reproduction vary in their responses to
habitat change (Loyola et al. 2008). Using this approach, Menin et al. (2011) reported that the
structure of assemblages of aquatic-breeding anurans was influenced principally by their
distance from streams, whereas assemblage structures for terrestrial-breeding species were
influenced by topography and soil attributes (Menin et al. 2007).
In this study, we were interested in investigating how local, reflecting niche theory,
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and regional, reflecting neutral theory, processes affect the structure of anuran assemblages.
We determined whether anuran assemblages of the Extrativist Reserve Lago do Cedro
(ERLC) are niche-structured or neutral by answering the following questions. (1) Are anuran
assemblages the result of stochastic processes and spatially structured? (2) Are anuran
assemblages influenced by local habitat heterogeneity (Grinnellian niche)? (3) Are anuran
assemblages niche-structured, but reflect the interspecific interactions among anuran species
instead of habitat heterogeneity (Eltonian niche)?
MATERIALS AND METHODS
Study area
The ERLC (1437' S 5059' O) is the largest remaining protected area in the savanna region,
located in the northeastern region of Gois state, in the municipality of Aruan, Brazil. It has
an extent of approximately 173.37 km2, with a mean elevation of 250 m ASL, a mean
temperature of around 38.0C and annual rainfall of 1,751 mm (SIMEGO 2012). The
regional climate is tropical, with a defined dry season, classified as Aw according to the
KppenGeiger climate classification system (Latrubesse & Stevaux 2002). Our study was
conducted on the floodplain of the Middle Araguaia basin, which is a priority area for
biodiversity conservation of the threatened aquatic and terrestrial species of the Cerrado
biome (Klink & Machado 2005). This floodplain ecosystem is important for local
biodiversity, because it contains temporary lentic sites during the dry season, which promote
the exchange of organic matter across the floodplain and the Araguaia river (Junk et al.
1989). The ERLC is composed of a mosaic of Cerrado physiognomies (e.g. veredas, seasonal
forests and savannas). These mosaics can act as a local environmental filter, placing limits on
the distribution of particular species from the regional assemblage because they lack some
key traits necessary to occur in certain sites, as a result of differences in local habitat
121
heterogeneity or resource availability.
Sampling design
All samples were obtained at night, during the rainy season, in December 2010, February
2011 and March 2011. We sampled 33 breeding sites, at least 500 m apart from each other,
representing the regional landscape mosaic (Figure 1). All breeding sites were sampled by
visual and auditory encounter methods (Scott & Woodward 1994), during the course of one
walk around each breeding site, in order to control the sample effort according to the size of
the breeding site. For very large breeding sites, we walked around them until we had achieved
one hour of sampling effort. In these cases, the size of the breeding site was taken to be the
area sampled, not the breeding site total area. The visual and auditory encounter methods are
complementary and adequate for estimating the distribution and abundance of frogs in short-
term studies (Rdel & Ernst 2004). Only lentic sites were sampled, and were composed
mainly of swamps, permanent ponds or temporary puddles. Each specimen found was
identified to the species level and voucher specimens were deposited in the Zoological
Collection of Universidade Federal de Gois (ZUFG). The nomenclature of anuran species is
in accordance with Frost (2011).
Habitat characterization and spatial variables
We characterized local variables of breeding sites according to the phytophysiognomy,
heterogeneity and physico-chemical parameters of the water, resulting in the following
descriptors: (1) site dimension (largest length, width and depth), (2) water pH, conductivity,
turbidity, dissolved oxygen and temperature, (3) percentage of vegetation cover (herbaceous,
shrub and arboreal) at the margins and inside the site, margin inclination (sloped and plane)
and substrate of the bottom of the site (soil, clay, sand, litter and stones), and (4) the
geographical coordinates (latitude and longitude), obtained in decimal degrees using the
Global Positioning System (GPS).

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Spatial and local effects on anuran assemblage composition
We used the spatial relationship of each reproductive site according to the geographic
coordinates to evaluate whether the anuran assemblages are randomly assembled (neutral
theory). We also used the structural descriptors of the reproductive sites to evaluate whether
the anuran assemblages are organized due to local heterogeneity (Grinnellian niche). To test
the contribution of each process in the organization of anuran assemblages we used a partial
canonical ordination technique (Bocard et al.1992).
For this analysis, the geographic coordinates were transformed by a Principal
Coordinates of Neighbor Matrix (PCNM) (Borcard & Legendre 2002), resulting in a
geographical distance matrix among reproductive sites. For each PCNM generated, we
calculated the Morans I index and selected those PCNMs that displayed positive spatial
correlation (i.e., with a Morans I larger than the expected value) to include in our model. The
PCNM calculations were made using the PCNM package, and the statistical test for Morans
I index was undertaken using a two-tailed parametric test with the AEM package in the R
software (R Core Team 2012).
Local heterogeneity data was transformed, with the exception of electrical
conductivity, by the Pavoine index to reduce the discrepancy in the environmental variables
(Pavoine et al. 2005). We utilized a principal coordinate analysis on the environmental and
species composition matrices to reduce the collinearity in the data-set (Legendre & Legendre
1998), and extracted the eigenvalues and eigenvectors that explained 90% of the variation in
the matrix (11 axes) for use as an explanatory matrix in our model.
The PCNM vectors and the environmental data were used as predictors of anuran
composition in the partial redundancy analysis (RDA), in order to partition out spatial and
environmental effects on the community composition (Borcard et al. 1992, Legendre 1993,
Diniz-Filho et al. 1998, Peres-Neto et al. 2006). The RDA is a method that combines a
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regression with a principal component analysis (PCA) (Legendre & Legendre 1998). We
evaluated the significance of the contribution of the pure environmental and pure spatial
components in explaining the total variance of anuran composition using an ANOVA-like
permutation procedure, after undertaking 9999 permutations of the RDA at the 5%
significance level (Anderson 2001, Oksanen et al. 2005). We performed RDA using the
Community ecology package in R version 1.17-3 (Oksanen 2010).
Co-occurrence patterns
In order to test whether species interactions are affecting the assemblage structure (Eltonian
niche) or whether the assemblage is randomly structured, we compared the observed co-
occurrence pattern of anuran species among reproductive sites with a null model (Gotelli
2000). Using this approach, we are able to detect if the anuran assemblage is structured by
any competition effect (Gotelli & Graves 2006).
We compared the observed co-occurrence pattern among species at different sites with
the expected frequency of co-occurrence generated by randomization of the observed matrix
of species co-occurrence (Gotelli 2000, Gotelli & Entsminger 2003). To describe the co-
occurrence pattern, we used the checkerboard score (C-score) as a co-occurrence index
(Stone & Roberts 1990), because it calculates the number of species pairs without requiring a
perfect checkerboard distribution, which is the total number of species pairs that do not co-
occur in different sites. The C-score is an index that has a negative correlation to species co-
occurrence (Gotelli & Entsminger 2008). Therefore, in a competitively structured community,
the C-score should be significantly higher than what would be expected by chance. If the
index from the original matrix lies within the 95% frequency distribution of the randomized
matrices, we there is no evidence for deterministic processes inuencing species distribution
and the null hypothesis is accepted. On the other hand, if the index is beyond the 95%
condence limits of the randomized matrices, there should be biological mechanisms

124
determining species co-occurrence, in which case we reject the null hypothesis (Ribas &
Schoereder 2002). The C-score measures the degree to which species can co-occur,
quantifying the mean number of unity of the checkerboard (that is, sites where one of the
species in the pair occurs and the other does not) for all possible pairs of species. The original
matrix of species co-occurrence was randomized to create 5,000 random matrices using the
software Ecosim v.7.2 (Gotelli & Entsminger 2001).
RESULTS
A total of 1188 specimens of 30 aquatic breeding species were found at the study site
belonging to ve families: Bufonidae (Rhinela, two species), Hylidae (Dendropsophus, four
species; Hypsiboas, six species; Lysapsus, one species; Phylomedusa, one species; Pseudis,
one species; Scinax, four species; Trachycephalus, one species), Leiuperidae (Eupemphix,
one species; Physalaemus, two species; Pseudopaludicula, one species), Leptodactylidae
(Leptodactylus; five species) and Microhylidae (Elachistocleis, one species) (Table 1).
Variance partitioning
No significant correlations were found in the variation partitioning, which presented a higher
unexplained variation (Table 1). Our models (pure environmental, pure spatial or
environmentspatial) did not explain the variance in the assemblage structure for the sampled
sites (Table 1). Thus, both the PCNM and environmental components were weak predictors
of the anuran assemblage composition. Therefore, we were unable to detect any Grinnellian
niche effect or a spatial autocorrelation in the environmental heterogeneity to explain the
composition of the anuran assemblage.
Co-occurrence patterns
The observed C-Score index was significantly lower than expected by chance (C-score
observed = 18.1; C-score simulated = 20.18; p = 0.0012). Thus, we found that the anuran
125
assemblages in the ERLC were structured by interspecific relationships among anuran
species, with some species pairs co-occurring more often than would be expected by chance
and reflecting the relative importance of Eltonian niche effects on local factors structuring
anuran assemblages in the ERLC.
DISCUSSION
Our results lead to several considerations regarding anuran assemblage structure in the
floodplain of the ERLC. Firstly, we found that the assemblage studied herein was structured
by contemporary factors and, secondly, that processes operating at the regional scale do not
play a major role in structuring the anuran assemblage, in disagreement with other works that
found a neutral effect on the anuran assemblages (Afonso & Eterovick 2007, Ernst & Rdel
2008). Neither were the anuran assemblages influenced by local environmental heterogeneity,
which is inconsistent with the Grinellian concept of the niche theory. This result contrasts
with other anuran studies that found a strong signal for the environmental heterogeneity effect
(e.g., vegetation cover and the presence or absence of specific breeding sites) (Parris 2004,
Both et al. 2009). Conversely, we found evidence that species interactions form the main
process structuring and regulating the anuran assemblage we studied, supporting an Eltonian
interpretation of the niche theory, in which the co-occurrence of species was the main
controller of species diversity and composition of local assemblages.
The species co-occurrence pattern was the main evidence for the anuran assemblage
in ERLC being regulated by species interactions, with some species co-occurring more often
than expected by chance. Several studies also observed niche-structured assemblages
organized by non-random co-occurrence patterns (MCloskey 1997, Baber et al. 2004,
Nomura et al. 2012). Non-random co-occurrence patterns in anurans are generally related to
differences in life-history traits, such as body shape, size, food niche breadth, calling site
126
choice, acoustic properties of the call and microhabitat use, that can result in temporal and
spatial partitioning of niche resources within the reproductive site (Crump 1974, Wells 1977,
Haddad et al. 1990, Kneitel & Chase 2004, Prado et al. 2005). Eltonian niche processes that
cause species coexistence are generally related to interspecific competition, resource
partitioning, distribution along a geographic gradient and predatorprey relationships (Gotelli
et al. 1997, Sanderson et al. 1998, Gottsberger & Gruber 2004, Prado et al. 2005). For our
data, competition does not explain the co-occurrence pattern that we found in the ERLC,
given that we found a larger than expected chance of some species co-occurring together.
Also, we did not detect any spatial effect; thus we considered that the co-occurrence pattern
we found is not explained by convergence to habitat preferences that are geographically
correlated. On the other hand, predation could decrease and/or avoid competition effects
(Lawler and Morin 1993, Parris 2004) and generate patterns in which species pairs have a
larger than expected chance of co-occurrence. Niche partitioning, due to local variation of
life-history traits in the species comprising the assemblage, in which species avoid negative
ecological interactions, can also generate patterns of species that co-occur more often than
expected by chance. The temporal mechanism, such as agesize relationship and temporal
partitioning, allow species to share geographically limited resources, increasing co-
occurrence among species (Lehtinen & Carfagno 2011). However, both the temporal,
predatorprey relationship and resource partitioning mechanisms may interact to increase the
chance of co-occurrence of anuran species with the same environmental requirements at
reproductive sites (Gottsberger & Gruber 2004).
The lack of the regional effect was evidenced by the insignificant correlation between
the spatial component in our model and species composition. Thus, proximity between
neighboring assemblages, i.e., breeding sites that were geographically close, did not influence
assemblage structure. This is some evidence that spatial processes, such as migration, do not
127
play a major role in structuring local assemblages in the ERLC. The influence of spatial
effects on anuran assemblages have been poorly studied in the neotropical region, but it is
often highlighted as a main factor (Ernst & Rdel 2008, Menin et al. 2011). For example, in
the Amazon forest biome, proximity among streams was the descriptor that better predicted
the assemblage composition of aquatic-breeding anurans (Menin et al. 2011). Thus, spatial
effects have been elected as a relevant structural process, when proximity among populations
explains species diversity and community composition (Ernst & Rdel 2006, Keller et al.
2009). In such cases, these assemblages are regulated by distance between sites and the
observed spatial pattern was due to dispersal restriction or other endogenous processes
(Keller et al. 2009). The dispersal behavior of frogs from their natal pond is not well studied,
but is generally associated to territoriality and site fidelity behavior, which assumes a poor
dispersal ability (Duellman 1994). However, the percentage of anuran species in a given
assemblage that present with territorial or site fidelity behaviors varies greatly among
neotropical biomes, which can result in different dispersal abilities, therefore affecting the
importance of spatial effects as a structural force (e.g., Nomura 2003). Thus, the assumption
of low dispersal capability of anuran species cannot be generalized for all biomes and needs
to be formally investigated.
In the ERLC, we were also unable to detect any significant pure environmental effect.
The theory predicts that more structurally complex habitats should provide more niche
diversity, allowing a large number of species to coexist (Collins & Wilbur 1979, Eason &
Fauth, 2001, Bosch & Martnez-Solano 2003, Parris 2004, Werner et al. 2007, Keller et al.
2009). This observed Grinnellian pattern may be due to a complex assemblage composed of
species of different physiognomies and the presence of important environmental
characteristics, such as vegetation features, litter cover, topography and soil attributes (Fauth
et al. 1989, Giaretta et al. 1999, Vonesh 2001). We suggest that the lack of any local
128
heterogeneity effect could be related to a difference in the species responses to habitat
heterogeneity (Duellman & Trueb 1994). Thus, one possible explanation for the lack of a
local heterogeneity effect may be that the pattern of movement differs between arboreal and
non-arboreal anurans with aquatic development. Thus, the habitat complexity should explain
a large portion of species diversity once the proportion of arboreal species increases in the
anuran assemblage, and once terrestrial anuran species were either not influenced or were
influenced negatively by habitat heterogeneity (Rossa-Feres & Jim 2001, Santos et al. 2007,
Silva et al. 2011). As in other studies, part of the unexplained variation may be due to
unmeasured environmental axes that are uncommonly found to affect anuran species
distribution (Parris 2004). Another possible explanation is that the majority of species found
are distributed across a wide geographic area and extensively exploit the variety of habitats
(e.g. Hypsiboas albopunctatus); these generalist species could not suffer from direct
environmental influences (Muniz et al. 2008). Also, we expect to find different responses to
local habitat components according to the life stage. For example, tadpoles are more affected
by the water physicochemical descriptors (Eterovick & Sazima 2000, Both et al. 2009), but
habitat descriptors are expected to be more important to tadpoles than adults (Eterovick &
Sazima 2000).
Our findings are particularly intriguing for amphibian anuran conservation, given we
have demonstrated that anuran assemblage composition and distribution are each highly
dependent on life-history traits (Gascon et al. 1995, Becker et al. 2007). Despite being unable
to detect any environmental effects, several studies focused on the structure of anuran
assemblages have found different results explaining assemblage composition (Parris &
McCarthy 1999, Ernst & Rdel, 2005, Keller et al. 2009). Given the importance of a
heterogeneous environment to aquatic-breeding arboreal anuran species, we suggest that
aquatic-breeding arboreal anurans may be more threatened and sensitive to habitat loss and
129
fragmentation than aquatic-breeding terrestrial anurans, but this prediction should be tested in
future investigations.
We recognized that the structure of anuran assemblages in the floodplain of the ERLC
was a product of biological interactions. Additionally, dispersal restriction and the lack of
relationships among aquatic-breeding non-arboreal frogs and habitat heterogeneity can
explain only a small proportion of the observed variation in the assemblage composition of
the reproductive sites. Furthermore, we hypothesized that functional traits operate as the main
explanation for local species coexistence and may be important to the anuran species in the
avoidance of negative ecological interactions. A future challenge to the study of anuran
assemblages is related to improvements in the understanding of the sources of variation
explaining the different compositions of habitats and biomes.
ACKNOWLEDGMENTS
We acknowledge with appreciation the help of Leonardo T. S. Cndido (chief of the ERLC)
and the opportunity given by him to develop this project. We are grateful to members of the
Laboratory of Animal Behavior & Herpetology / UFG for assistance with fieldwork and
comments on the manuscript. We also thank Denis Nogueira for his helpful comments on this
manuscript. We are also grateful to the CNPq and ICMBIO-RAN for financial support (N
472125/2010-9) and the collection license (N 24401).
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137
FIGURES
Figure 1. Histograms of the observed and expected values of the C-Score index of anuran
assemblages sampled in the ERLC.
Figure 2. Variation partitioning for anuran assemblages sampled in the RELC.

138
CAPTULO 5 (a ser submetido para a revista Hydrobiologia)
INTRODUCTION
Organisms are not uniformly or randomly distributed in nature (Legendre & Fortin 1989).
They are aggregated in patches, forming gradients or present other types of spatial
structuration (Legendre & Fortin 1989). Sometimes, species may be absent in a specific place
not due to environmental conditions or biotic interactions, but simply because its distribution
does not reach that particular habitat (Tilman 1994). Therefore, limitation in the dispersal
ability, which hinders the colonization capacity of a species, may be a considerable structural
factor in the determination of species composition in local assemblages (Tilman 1994). The
search for these general principles of assembly rules, i.e., which determine how species
interact to shape communities (Belyea & Lancaster 1999), found three major factors: i)
environmental restrictions (e.g. abiotic factors), ii) spatial restrictions and iii) internal
dynamics (e.g. competition) (Belyea & Lancaster 1999). The interaction of these three factors
have been originated many hypothesis about community composition (Keller 2009), as the
environmental effect (Parris 2004) and the spatial effect (Parris 2004; Ernst & Rdel 2008).
Environmental heterogeneity has been largely used to explain the variation in species
diversity (Huston 1994). Usually, the microhabitat availability depends on the complexity of
the local structure. Then, we could expect more anuran species in complex environments than
homogeneous environments (e.g., Brando and Arajo 1998; Bernarde and Kokubum 1999).
In the environmental control model (Parris 2004), conditions are important because they
influence the physiological tolerance of individuals and affect, although indirectly, the
community composition (Parris 2004). Abiotic factors also influence the community by
restricting which species may establish on a given site (Belyea & Lancaster 1999). The
relationship between environmental factors and species composition reflects the casual
139
correspondence of life history traits in a given habitat (Ernst & Rodel 2008), where sites with
similar environmental conditions tend to have similar species composition (Parris 2004).
However, the geographical distance also could contribute to the level of similarity
between sets of specie, due to differences in the abilities of species to migrate and to colonize
new sites (Hubbell 2001; Eterovick & Barata 2006). Spatial variation in communities can be
resultant solely by the chance of a given event occur over time rather than environmental
heterogeneity and ecological adaptations of species (Hubbell 2001). In a local scale, such a
specific habitat, the organism may interact more often with their neighbor than distant
individuals (Tilman 1994), which also can generate a spatial effect, but resultant of biotic
processes such as competition and predation (Tilman 1994; McCarthy 1997; Whittaker et al.
2005). Therefore, sites geographically close tend to have more similar assemblages than those
that are further away (Legendre & Fortin 1989; Tilman 1994; Keller 2009).
Identify the relative contribution of these environmental and spatial effects in the
structure of ecological communities are an ecological and methodological challenge (Keller
2009). For example, studies focusing in amphibians community generally explain the local
assemblage composition by species interactions alone (Wells 2007). However, diversity
patterns and large-scale distribution may have an impact on local communities, because these
patterns define the landscape for interactions between species that co-occur (Wells 2007).
Most anuran amphibians have a life cycle with aquatic and terrestrial phases (Duellman &
Trueb 1994), being very dependent on the environmental integrity of these two habitat types.
Amphibian ecology larvae differ from adults in several ways (Wells 2007). Maybe the most
important difference is the fact that the initial composition of the larvae assembly is not
determined by the interactions between the tadpoles of different anuran species, but mainly as
a result of adult decisions, as the oviposition site selection (Alford 1999). Thus the breeding
site structure is an indirect determinant of the tadpole assemblage structure (Parris &
140
McCarthy 1999), because larval survival is dependent on their hatching and development in
an appropriate habitat (Duellman & Trueb 1994). Added to this parental effect, processes that
occur after oviposition are also important to determining the reproductive success of different
species in amphibians community (Wells 2007) and it is evident that the structure and
maintenance of tadpoles assemblages are dependent of a complex interaction between
physical factors, predation and inter and intraspecific competition (Duellman & Trueb 1994;
Fatorelli & Rocha 2008). Here we test the influence of environmental factors and geographic
position (as a surrogate of biotic processes) on the distribution pattern of anuran tadpoles
species in a Cerrado area.
MATERIAL AND METHODS
Study site
The study was conducted at Extractivist Reserve Lago do Cedro (ERLC) (Figure 1), Aruan
municipality, Gois state, Brazil. The ERLC has area of 17.337,616 ha and is under influence
of the Cerrado domain (Villanueva 2009). It is located in the same region as the
Environmental Protection Area (EPA) dos Meandros do Rio Araguaia, in the Rio Vermelho
microregion (Villanueva 2009). This region holds much of the faunal diversity of this
ecosystem and this diversity is directly linked to forest types in the region (Villanueva 2009).
The Cerrado herpetofauna is considered insufficiently known (Colli et al. 2002), with many
species still being described, and a large extension of biome not been adequately sampled
(Colli et al. 2002; Bini et al. 2006). Much of the diversity that is known should also be
described and cataloged (Linnean shortfall), and, similarly, for many taxa we have an
inadequate knowledge of their spatial distribution (Wallacean shortfall) (Whittaker et al.
2005). These problems show that many demographic and communities studies of many
groups are still required, such as herpetofauna (Colli et al. 2002).

141
The Cerrado has originally about two million km in length, covering 22% of the
country (Ratter et al. 2003). This biome is richest savanna in the world and houses an
immense flora and fauna diversity (Ratter et al. 2003), resulting from the different
environments presence, such as forest types, savanna and grassland (Alho 2005). Analyzing
endemism and threat degree, Myers (2000) classified the Cerrado as one of worldwide
hotspots, mainly due to advanced habitat loss. Soil degradation and native ecosystems as
well as the species exotic dispersal are major threats to biodiversity (Klink & Machado
2005). Thus, the agriculture expansion, mining, fire and development projects (e. g. dams,
roads and industries) are the main causes of this destruction (Silvano & Segalla 2005).
Sampling procedures
We sampled 33 ponds during three expeditions in the rainy season between December 2010
and March 2011. For each pond sampled, we estimate its geographical position by the Global
Position System (GPS) (Table 1). Tadpoles were collected between 12:00h and 19:00, with
dip net of wire mesh of 3 mm. All sites were sampled by one hour/person or untill all the site
perimeter was inspected. Tadpoles were anesthetized in a 5% benzocaine solution and fixed
in 10% formalin immediately after collection. Voucher individuals were deposited in the
Coleo Zoolgica da Universidade Federal de Gois (ZUFG). All tadpolpes were identified
with a dichotomous key (Rossa-Feres & Nomura 2006) or comparing with the larvae
description available in the literature.
Environmental variables
We also measured for each site the greatest length, the maximum depth, bottom type (e.g.,
mud, clay, sand, litter, and stones), area cover (e.g., trees, shrubs, herbaceous and grassy) in
the perimeter and within the water body, margin type (e.g., sloped, inclined and flat), pH,
conductivity, dissolved oxygen, water temperature, air temperature and relative humidity.
These variables were used to estimate the degree of environmental heterogeneity among
142
ponds.
Spatial variables
We transformed the geographic coordinates in a distance matrix using the Euclidean distance
and performed a Principal Coordinates of Neighbor Matrices (PCNM) (Borcard & Legendre
2004). Then, we calculated the Morans I index and selected only those PCNM that display
statistical significantly positive spatial correlation (i.e., PCNM with Morans I larger than
expected value) to include in our model. The PCNM calculations were made with the PCNM
package and the statistical test of Morans I index by a 2-tailed parametric test with AEM
package in the R software (R Core Team 2012).
Statistical analysis
To determine whether the tadpoles distribution pattern is shaped by environmental or spatial
variables we used the variance partition method (Diniz-Filho et al. 1998, Desdevises et al.
2003, Peres-Neto et al. 2006) using a Partial Redundancy Analysis (RDA) (Legendre &
Legendre 1998). The use of RDA allows us to measure the variation amount (eigenvalues
sum) in the species data that can be explained by each set of environmental variables (Bocard
1992). For this analysis, we used the diversity matrix of species abundance as a response
matrix. As a predictor matrix, we used a transformed environmental matrix, using the
environmental variables resumed by the Gower distance and submitted to a principal
coordinate analysis (PCoA) (Legendre e Legendre 1998). Later, we selected those vectors
that explained 90% of the total variance of the environmental heterogenetiy. Spatial and
environmental matrixes were used as predictors of variance found in the diversity matrix.
After evaluating the environmental and spatial total contribution, we tested the two terms
significance for the final model contribution using an ANOVA as a permutation test of the
RDA (Oksanen et al. 2005). All analyzes were done using the statistical software
environment R (R Development Core Team 2011).

143
RESULTS
Species composition
We sampled 806 individuals in the larval stage of 23 species belonging to 10 genera and four
families: Hylidae (Dendropsophus, Hypsiboas, Phyllomedusa, Scinax and Pseudis),
Leiuperidae (Pleurodema, Pseudopaludicola and Physalaemus) Leptodactylidae
(Leptodactylus) and Microhylidae (Elachistocleis). Families Hylidae (n = 12 spp.) and
Leuriperidae (n = 7 spp.) were the most representatives in number of anuran species, while
Leptodactylidae and Microhylidae had, respectivelly, two and one species (Table 2).
Partition of variance
The tadpole distribution pattern was explained by environmental variables (F=1.5421, df= 13
e p= 0.03; Figure 2), but there was not influence of the spatial variable (F=1.0889, df= 5 e p=
0.31; Figure 2). In diversity found, 22% of the variance can be explained by environmental
variables and just 2% by spatial.
DISCUSSION
Our results show that local factors (environmental variables) better explain the anuran tadpole
distribution than regional factors (geographical distance), i.e., interaction between different
species of tadpoles are best explained by their niche relationships and the fact that a
community is closer or distant from others does not explain the diversity found in ponds.
Although our findings are supported by others studies (Bosch et al. 2004; Both et al. 2011),
we are contradict by studies that shows that the amphibian assemblage are driven by local
and regional factors (Hamer & Parris 2011; Werner et al. 2009) or only due climatic
conditions (Vasconcelos & Rossa-Feres 2005). At local scale, the physical structure of the
environment is important, because it provides shelter and breeding sites, making them
dependent on the environment integrity. Also, for species with complex life cycle, the
144
landscape design is important to provide connectivity between breeding and shelter sites,
allowing the movement of the frogs during their lifespan. But as tadpoles are not able to
disperse between ponds, because the breeding sites choice is made from adult (Alford et al.
1999), they are submitted to an instable environment, like temporary ponds which may dry or
even permanents ponds that may contain more predators such as fish. Thus, tadpoles can use
bottom material or plants as shelter or use of a large phenotypic plasticity.
Fewer than half of variation found in community composition of anuran tadpoles in
ERLC can be explained by environmental and/ or spatial variables. Part of amount of
unexplained variation may be due to nondeterministic fluctuations (stochastic variations)
(Borcard et al. 1992; Parris 2004), to important variables not measured and may also be due
to insufficient sampling (Parris 2004). The spatial matrix can act as a synthetic descriptor of
unmeasured biological process (growth, predation) (Borcard et al. 1992). Basic process cant
be identified from data obtained and their actions in the community structure cant be fully
predicted by functions provides by spatial coordinates (Borcard et al. 1992).
In process of matrix variation explanation of abundance, generally relates to a data set
of environmental variables consisting, for example, of physicochemical, climate, or
geomorphological descriptors, it is often considered the most important determinant of
animal or plant pattern assemblies (Borcard et al. 1992). Variables such as oxygen
concentration, substrate type, temperature and vegetational structure influence the tadpole
distribution in the microhabitats (Hoff et al. 1999). However, due the little control over type
of habitat they occupy (permanent or temporary, lentic or lotic) species segregate spatially
within the same environment, using different microhabitats. Species respond individually in
relation to the habitat (Ernst e Rodel, 2006; Silva 2011), so the various local attributes will
differently affect each species. Thus, the more heterogeneous an environment, greater the
possibility of harboring different species, that use vegetation and substrate as shelter and
145
food.
Anuran species with different life-history traits respond to landscape disturbance in
different ways (Loyola et al. 2008). Anurans with larvae, aquatic-breeding anurans, were
exceptionally sensitive to microclimate and micro-habitat of breed habitat because they need
from the integrity and connection of the landscape to complete their biphasic life cycles, that
makes them species more vulnerable to fragmentation and loss of habitat to changes on
gradient environmental than terrestrial-breeding anurans (Becker et al 2007, 2010). Thus,
fragmented landscapes, such as current landscapes around suitable breeding sites on Cerrado,
may represent potential dispersal barriers to anurans moving across the landscape, in winch
can have a great negative impact on aquatic-breeding anurans population (Becker et al.
2007). Such dispersal barriers can generate metapoputation dynamics, that are species group
considered critically vulnerable to landscape fragmentation due their subpopulations
periodically go extinct locally (stochastic extinctions) and must be re-established by dispersal
processes from neighboring sites (Levins 1969, Hanski and Simberloff 1997, Semlitsch
2008).
The heterogeneity among the different environments leads to habitat-specific
adaptations (Keller et al. 2009) and the difference between habitats are strong enough to
result in different assemblies occurring in specific habitats almost independently of the spatial
distance (Keller et al. 2009). Considering the sampled sites in ERLC, that holds a typical
landscape of Cerrado, a savanna with a remarkable physiognomic variation (Ratter & Ribeiro
2003), the observed variation in community composition is attributed to the heterogeneity of
this area.
We conclude that the anuran tadpoles assemblage composition of ERLC is regulated
by local factors, with little influence of regional factors. Despite breeding sites selection is a
parental decision, local environmental variables are determinants for the anuran tadpoles
146
distribution and, therefore, the maintenance of these factors would be necessary to preserve a
suitable habitat for the anuran assemblage.
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TABLES
Tabela 1: Water bodies coordinates in Extractivist Reserve Lago do Cedro (ERLC), Aruan,
GO, sampled during three expeditions (a,b,c).
Water bodies Coordinates

1a S 14 50.336 W 5102.088
2a S 14 48.702 W 5100.812
3a S 14 48.166 W 5100.572
4a S 14 46.478 W 5100.862
5a S 14 44.211 W 5100.776
6a S 14 52.194 W 5103.662
7a S 14 52.803 W 5103.929
1b S 14 52.029' W 5102.296'
2b S 1455.153' W 5100.025'
3b S 1452.318' W 5058.546'
4b S 1456.127' W 5100.465'
5b S 1453.494' W 5058.494'
6b S 1440.161' W 5054.459'
7b S 1439.502' W 5054.156'
8b S 1440.591' W 5054.388'
9b S 1441.391' W 5054.429'
10b S 1445.489' W 5057.499'
11b S 1449.092' W 5058.364'
12b S 1453.355' W 5104.545'
13b S 1456.568' W 5102.321'
14b S 1451.261 W 5058.462'
1c S 1449.540' W 5102.396'
2c S 1443.085' W 5059.193'
3c S 1445.100' W 5101.206'
4c S 1448.021' W 5101.207'
5c S 14 50.183 W 5102.785
6c S 1449.338' W 5102.311'
7c S 1447.136' W 5102.321'
8c S 1448.056' W 5101.521'
9c S 1449.531' W5102.363'
10c S 1449.357' W5101.389'
11c S 1448.542 W 5101.158'
12c S 1448.439' W 5101.051'
152
Table 2: Tadpoles abundance sampled in the 33 water bodies in Aruan, GO: Sp1: Dendropsophus cf. nanus, sp.2: Dendropsophus cf. jimi, Sp.3:
Dendropsophus minutus, Sp.4: Dendropsophus sp.1, Sp.5: Dendropsophus sp.2, Sp.6: Elachistocleis cesarii, Sp.7: Hypsiboas sp., Sp.8:
Hypsiboas raniceps, Sp.9: Leptodactylus fuscus, Sp.10: Leptodactylus podicipinus, Sp.11: Physalaemus marmoratus, Sp.12: Pseudis cf.
bolbodactyla, Sp.13: Pseudopaludicola sp.1, Sp.14: Pseudopaludicola sp.2, Sp.15: Pseudopaludicola sp.3, Sp.16: Pyllomedusa cf. azurea,
Sp.17: Physalaemus cf. centralis, Sp.18: Physalaemus cuvieri, Sp.19: Physalaemus sp., Sp.20: Scinax cf. fuscomarginatus, Sp.21: Scinax
fuscovarius, Sp.22: Scinax gr. ruber 1, Sp.23: Scinax gr. ruber 2.
Species 1a 2a 3a 4a 5a 6a 7a 1b 2b 3b 4b 5b 6b 7b 8b 9b 10b 11b 12b 13b 14b 1c 2c 3c 4c 5c 6c 7c 8c 9c 10c 11c 12c TOTAL
Sp.1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 4 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 4
Sp.2 0 0 0 0 0 0 0 0 2 0 0 1 1 2 0 0 1 0 0 1 0 0 0 0 0 1 6 0 0 0 0 3 6 24
Sp.3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 33 0 2 0 0 0 0 35
Sp.4 0 0 40 0 0 0 4 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 44
Sp.5 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 4 0 0 0 0 0 0 0 0 0 0 0 4
Sp.6 0 0 1 0 2 0 3 0 0 0 1 0 0 6 0 0 0 0 0 0 0 0 0 0 0 0 22 0 5 0 0 0 0 40
Sp.7 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 0 0 0 2
Sp.8 0 0 0 0 0 0 0 1 2 0 0 0 1 1 1 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 7
Sp.9 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 2
Sp.10 0 0 0 0 0 47 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 47
Sp.11 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 22 0 0 0 0 0 0 0 0 0 0 22
Sp.12 0 0 0 0 0 0 0 4 0 0 0 0 0 0 2 4 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 11
Sp.13 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 4
Sp.14 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2
Sp.15 0 0 0 0 0 0 0 0 0 0 0 5 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 0 0 0 0 2 0 9
Sp.16 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 2
Sp.17 0 0 0 0 0 0 0 0 0 0 0 0 5 26 0 13 0 0 0 0 1 0 5 0 0 0 0 2 0 34 0 0 0 86
Sp.18 8 6 0 0 22 0 4 0 0 0 5 0 0 2 0 0 0 1 0 0 0 0 11 8 0 0 7 0 9 0 0 3 1 87
Sp.19 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 41 0 0 0 0 0 0 0 0 0 0 41
Sp.20 0 0 0 0 0 0 0 4 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 4 2 0 0 0 0 0 0 12
Sp.21 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 0 0 0 0 87 0 0 0 0 0 0 89
Sp.22 22 20 0 13 0 0 35 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 18 0 0 0 0 109
Sp.23 0 0 0 0 0 0 0 0 21 5 4 2 2 15 23 0 4 7 10 9 5 0 2 0 0 0 0 0 0 0 4 1 9 123
153
FIGURES
Figure 1: Study area and sampling sites in Extractivist Reserve Lago do Cedro (ERLC).
Figura 2: Partition of variance results.

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CAPTULO 6 (aceito para publicao na revista Ethology Ecology & Evolution)
Does background colouration affect the behaviour of tadpoles? An
experimental approach with an odonate predator
F. NOMURA1,2,5, P. DE MARCO1, A.F.A. CARVALHO3 and D.C. ROSSA-FERES4
1 Departamento de Ecologia, ICB, Universidade Federal de Gois (UFG), CP 131, CEP
74001-970, Goinia, Gois, Brazil
2 Instituto Neotropical: Pesquisa e Conservao. Caixa Postal 19009, 81531-980 Curitiba,
PR, Brazil
3 Programa de Ps-Graduao em Microbiologia Aplicada, IB, Universidade Estadual
Paulista (UNESP), Av. 24-A, 1.515, CEP 13506-900, Rio Claro, So Paulo, Brazil
4 Departamento de Zoologia e Botnica, IBILCE, Universidade Estadual Paulista (UNESP),
Rua Cristvo Colombo, 2265, CEP 15054-000, So Jos do Rio Preto, So Paulo, Brazil
5 Corresponding author: Fausto Nomura. E-mail: fausto_nomura@yahoo.com.br, phone:
55-62-3521-1474, fax: 55-62-3521-1190
ABSTRACT
Predation is a primary driver of tadpole assemblages, and the activity rate is a good predictor
of the tadpoles tolerance for predation risk. The conflicting demands between activity and
exposure to predation can generate suboptimal behaviours. Because morphological
components, such as body colouration, may affect the activity of tadpoles, we predict that
environmental features that enhance or match the tadpole colouration should affect their
survival or activity rate in the presence of a predator. We tested this prediction
experimentally by assessing the mortality rate of tadpoles of Rhinella schneideri and

155
Eupemphix nattereri and the active time on two artificial background types: one bright-
coloured and one black-coloured. We found no difference in tadpole mortality due to the
background type. However, R. schneideri tadpoles were more active than E. nattereri
tadpoles, and the activity of R. schneideri was reduced less in the presence of the predator
than that of E. nattereri. Although the background colouration did not affect the tadpole
mortality rate, it was a stimulus that elicited behavioural responses in the tadpoles, leading
them to adjust their activity rate to the type of background colour.
Key words: Eupemphix nattereri; pattern of activity; habitat heterogeneity; Pantala
flavescens; predation; Rhinella schneideri.
INTRODUCTION
Predator-prey interactions have been analysed by many authors to explain the distribution of
tadpoles of different anuran species among ponds (e.g., HERO et al. 1998; AZEVEDO-RAMOS
et al. 1999; AZEVEDO-RAMOS & MAGNUSSON 1999) and among microhabitats (e.g., VAN
BUSKIRK 1988; CROSSLAND & ALFORD 1998; KOPP et al. 2006). As a response to their
predators, tadpoles present a variety of inducible defence mechanisms, related to
modifications in morphology and life history (KATS & DILL 1998; TOLLRIAN & HARVELL
1999), in which behaviour plays a major role (LIMA & DILL 1990; BRODIE et al. 1991; KATS
& DILL 1998). In this context, tadpoles make decisions about time allocation for foraging
activity by evaluating the predation risk based on indirect tactile, visual and chemical cues of
predator presence (HEYER & MUEDEKING 1976; DUELLMAN & TRUEB 1986; MORIN 1987;
PEARMAN 1995; KATS & DILL 1998; AZEVEDO-RAMOS et al. 1999; HERO et al. 2001;
TAKAHARA et al. 2012).
Tadpoles may exhibit a high or low activity rates as a predator induced behavioural
defence in predator-prey interactions, related to the time allocation decision (WERNER &
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ANHOLT 1993). In some anuran species, the tadpoles are highly active and do not modify, or
show only a slight reduction in, their activity rate in the presence of predators (HEYER et al.
1975; CROSSLAND & ALFORD 1998; CROSSLAND & AZEVEDO-RAMOS 1999; HERO et al.
2001), as observed in Rhinella marina (HEYER et al. 1975; BRODIE & FORMANOWICZ 1983),
Hypsiboas geographicus (AZEVEDO-RAMOS et al. 1992) and Hypsiboas semilineatus
(DHEURSEL & HADDAD 1999). For other anuran species, the tadpoles move less frequently
and display bursts of swimming and cryptic behaviour, i.e., their behaviour maximises the
ability to conceal itself, by strongly reducing its activity in the presence of the predator
(HEYER et al. 1975; NOMURA et al. 2003). This less active behaviour is known to occur in
Physalaemus marmoratus (NOMURA et al. 2003), Scinax ruber, Phyllomedusa tarsius
(AZEVEDO-RAMOS et al. 1992), Engystomops pustulosus (HEYER et al. 1975) and Rana
temporaria (VAN BUSKIRK & ARIOLI 2005).
Tadpoles that exhibit the active behaviour also have aposematic colouration, usually
black, because they generally have unpalatable substances in its skins (DHEURSEL &
HADDAD 1999). Conversely, tadpoles that exhibit the less active behaviour also have cryptic
colouration, commonly brownish and whitish colours (DHEURSEL & HADDAD 1999). These
correlations between behavioural and morphological traits could denote different solutions to
deal with the predation risk; while the aposematic colouration evolved to reduce the success
of predator attacks, the cryptic colouration reduces the chance of the individual being
detected by the predator (ENDLER 1991; RUXTON et al. 2004). Thus, one important
environmental trait that may affect the behaviour of tadpoles and the efficiency of their
survival in the presence of predators is the background colour. For example, the background
colouration could favour less active tadpoles by matching the tadpole colouration, which
enhances the cryptic behaviour. Conversely, the background colouration could favour active
tadpoles if it contrasts with the colour of unpalatable tadpoles, which enhances aposematism.
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For prey with a fixed appearance, there may be a range of background colourations that
confer the maximal performance for avoiding predators while maximising the activity rate,
and would be advantageous for the prey to recognise such microhabitats with favourable
background colour. In such cases, the colouration of tadpoles should be an important factor
that enhances behavioural inducible defences, and the background colouration would be used
as an indicator of favourable microhabitats.
As the background colouration could affect the efficiency of the cryptic behaviour and
the aposematism defence mechanisms (RUXTON et al. 2004), we would expect that tadpoles
of anuran species that present different defence mechanisms also differ in their predation risk
according to the background colouration, once it affect the chance of a predator to detect the
tadpole. This difference in predation risk could generate indirect interactions, mediated by
the defence mechanisms (LVAREZ & NICIEZA 2009), when occur between populations of
competitor species that shared a common predator and could modify the outcome of
competitive interactions (NOMURA et al. 2011). In the present study, we tested how the
background colouration and the presence of a predator affect the behaviour of Rhinella
schneideri (aposematic tadpole) and Eupemphix nattereri (cryptic tadpole). These two
species are common, widespread anuran species that live in open areas throughout south-
eastern Brazil (DUELLMAN 1999; FROST 2011) and share microhabitat preferences and diets
(ROSSA-FERES et al. 2004). However, the tadpoles of these two anuran species have different
behavioural strategies: E. nattereri is a brown-coloured tadpole with cryptic behaviour and
burst swimming. It is commonly found during the rainy season in temporary, rain-filled
ponds in pasture areas. In this type of habitat, the substrate on the bottom of the pond is
formed by loose, organic-rich soil, which matches the brownish colouration of the tadpole,
enhancing its cryptic behaviour. Conversely, R. schneideri is a conspicuous, black-coloured
tadpole that is unpalatable (ROSSA-FERES & NOMURA 2006; NOMURA et al. 2011). Rhinella
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schneideri tadpoles can be found in permanent ponds and frequently co-occur with fishes,
but they are also found in the same type of temporary ponds inhabited by E. nattereri
tadpoles, where odonate larvae are the main predator of the tadpoles (GASCON 1992; HERO
et al. 2001; JARA & PEROTTI 2010). To test how these two behavioural strategies of tadpoles
are affected by the background colouration, we designed two experiments that addressed the
following points: (1) whether the interaction between background colouration and tadpole
behaviour affects the predator preference and tadpole survival rate and (2) whether the
interaction between background colouration and the presence of a predator affects the
tolerance for predation risk, measured by the activity level of E. nattereri and R. schneideri
tadpoles.
We also investigated the maladaptive behaviour of R. schneideri tadpoles, which are
active in the presence of a predator, thereby increasing their predation risk. These tadpoles
are comparatively more active than cryptic tadpoles, because of the presence of distasteful
substances in their skin. The efficiency of this behaviour is dependent on the ability of the
predator to associate the tadpole colouration with the unpleasant taste of the tadpole skin.
However, many odonate larvae predators have the ability to consume tadpoles that are
unpalatable to other predator species (HEYER et al. 1975; CROSSLAND & ALFORD 1988;
BALLENGE & SESSIONS 2009), a trait that has been associated with an evolutionary
background (native predators vs non-native predators) and the presence of physiological
detoxifying mechanisms or a natural resistance to specific toxins (CROSSLAND & ALFORD
1998). Alternatively, BALLENGE & SESSIONS (2009) suggest that the odonate larvae are
capable of select specific prey parts to consume. We tested this idea by quantifying the
proportion of non-consumed parts of aposematic R. schneideri and cryptic E. nattereri
tadpoles during our experiments. Thus, we expected to provide a behavioural explanation for
the ability of odonate larvae predators to consume unpalatable tadpoles.

159
MATERIALS AND METHODS
Study System
Recently hatched tadpoles of R. schneideri and E. nattereri were collected in a temporary
pool in Nova Itapirema, So Paulo (210440S, 493223W) in September 2001 and kept
in aquariums, where they were fed ornamental fish food ad libitum. The tadpoles of R.
schneideri and E. nattereri are good experimental subjects because they share habitat and
food preferences (ROSSA-FERES et al. 2004), but they differ in colour and antipredator traits
(F. NOMURA pers. obs.; ROSSA-FERES & NOMURA 2006). These species are also members of
different anuran families, a trait that negates the convergence of life history traits between
taxa simply due to shared ancestry or phylogenetic nonindependence (QUADER et al. 2004).
We experimentally manipulated predation by the larvae of the Odonata Pantala
flavescens. Pantala flavescens larvae are solitary, generalist predators with benthic habits
that locate their prey by sight (PRITCHARD 1965; HEYER et al. 1975) and are usually found in
temporary lentic pools. The larvae of the odonate P. flavescens that were used in our
experiments were collected in artificial tanks at Universidade Estadual Paulista
(204710S, 492168W), Campus de So Jos do Rio Preto, So Paulo, in September
2001and January 2002, kept in aquariums and fed with damselfly larvae (Enallagma sp.,
Coenagrionidae Odonata). Thus, none of the P. flavescens larvae used in our experiments
had previous contact with E. nattereri or R. schneideri tadpoles. Odonate larvae are visual
and tactile predators, and their binocular vision aids in estimating the distance to an object
and its size (CORBET 1999). Although they are specialised to detect movement, odonate
larvae are capable of discriminating the shape (CORBET 1999) and colour (PRITCHARD 1965)
of immobile prey.
The total length of P. flavescens was 2.29 cm 0.24 SD and the tadpoles length were
standardized on the proportion of 2/3 of the odonate larvae total length to control for any
160
effect of tadpole size during experiments. At this size, the majority of the tadpoles had
reached developmental stage 30, varying between stages 28-32 (sensu GOSNER 1960). All
specimens, tadpoles and odonate larvae, were raised under natural conditions of temperature,
photoperiod and relative humidity.
We conducted the experiments between October 2001 and February 2002 in
polyethylene aquariums (16 x 24 x 8 cm) filled with aged well water under natural
temperatures (mean minimum temperature = 20.43 1.18 oC; mean maximum temperature =
32.62 0.60 oC). We used aquariums with reduced edges to prevent the tadpoles from
selecting microhabitats where predators are absent, which could confound our results with
predator avoidance mechanisms. No food was available during the experiments, and all
specimens were used only once per trial.
Predator Choice Experiment
To test whether the behaviours of aposematic and cryptic tadpoles are affected by
background colouration, ten tadpoles (five of each behaviour strategy) were exposed in an
aquarium to the P. flavescens predator on two background types: an aquarium with a black
polyethylene film (BPF) and an aquarium with a white polyethylene film (WPF). Before the
experimental trials, each P. flavescens larva was starved for 48 hr. After this period, one P.
flavescens larva, five cryptic tadpoles of E. nattereri and five aposematic tadpoles of R.
schneideri were transferred to an aquarium with 1 litre of tap water. We used this approach to
detect any shift in prey preference of P. flavescens larvae due to background types. Thus, by
offering the two tadpoles types, we would test whether the background colour could, in
addition to modify the tadpole behaviour, affect the predator prey preference. After 24 hr, the
tadpoles that were not captured by the odonate larvae were euthanised in a benzocaine
solution and preserved in 10% formalin. These conditions were replicated 13 times for BFP
and 27 times for WPF.

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Replicates in which the larvae died before preying upon any tadpole were not
included in the analysis (n = 4), and we assumed that the odonate larvae died due to
prolonged starvation. Replicates in which the larvae died after preying upon the first tadpole
were recorded. Because we did not observe all of the predation events, we used this
approach to determine which tadpole is most noxious to the P. flavescens larvae. After each
replicate, we collected the parts of the tadpoles that were not eaten by the predator. We
divided these not eaten tadpole parts in three categories: caudal remains (caudal fins and
musculature); body remains (formed by the anterior part of the body, including eye and
mouth); and snout remains (formed by the snout and nares). We associated these parts with
one of the tadpole species based upon differences in shape and colouration. After the
experiment, we pooled all tadpole remains despite the background type to determine whether
the predator consumed E. nattereri and R. schneideri tadpoles in a similar manner, once not
all aquaria contained not eaten parts of tadpoles.
Tadpole Activity Experiment
In a second experiment, the time spent by tadpoles in activity, thereby active time, was
recorded with a stopwatch for ten minutes in the presence of P. flavescens larvae and ten
minutes in the absence of P. flavescens larvae. For this experiment, we observed one tadpole
with the same background types used in the predation experiment (BPF and WPF). The
conditions were also the same as in the predator choice experiment, with one P. flavescens
larva, five cryptic tadpoles of E. nattereri and five aposematic tadpoles of R. schneideri
transferred to an aquarium with 1 litre of tap water. All specimens were used only once per
replicate and the predator was allowed to feed on the tadpoles. These conditions were
replicated 5 times per anuran species, with one tadpole observed per replicate, and for each
background type, and all animals were used only once. Replicates in which the focal animal
was captured before the end of the observation period were not considered in the analysis,
162
the experiment was disassembled, and a new replicate was performed. We considered that
tadpoles were active when they were moving from one point to another in the aquarium or
when presenting tail movements without displacement. To reduce the effect of the observer,
we used a cardboard screen with a small opening during observations.
Statistical Analysis
To determine whether the mortality rate differed among tadpole with different behavioural
strategies and background types, we used the proportion of tadpoles killed as a response
variable adjusted by a generalised linear model (GLM), with a binomial error structure.
Then, we compared the proportion of tadpoles killed using a two-way factorial ANOVA with
treatment (BPF and WPF) and tadpole behavioural strategy (aposematic and cryptic) as fixed
effects.
We tested the null hypothesis that the predator consumed tadpole parts of both species
equally by comparing the observed proportion of tadpole remains found in aquariums after
replicates using a Chi-squared test (2) for a 2 x 3 (two tadpoles species, three categories of
remains, n = 82 not eaten tadpole parts) contingency table with the Yates correction (ZAR
1999). We also used a Chi-squared test for a 2 x 2 (two tadpole species, two categories of
predator outcome death or no death, n = 68 P. flavescens larvae) contingency table to
verify whether the chance of P. flavescens larvae death after predation was independent of
the tadpole species. For this analysis, we counted the number of P. flavescens larvae that died
after eating E. nattereri or R. schneideri tadpoles.
The active time was compared using the proportion of active time as a response
variable adjusted by a GLM. However, as the proportion of active time was underdispersed,
we used a quasibinomial error structure. Then, we compared the proportion of active time
using a three-way factorial ANOVA with WPF and BPF treatments (two levels), predator
presence or absence (two levels) and tadpole behavioural strategy (two levels) as fixed
163
effects (ZAR 1999).
The Chi-squared (2) test was performed in the Past software v 2.13 (HAMMER et al.
2001). All other statistical procedures were performed using the R environment software (R
DEVELOPMENT CORE TEAM 2011).
RESULTS
Background Colouration and Mortality
The tadpole mortality rate did not differ between R. schneideri and E. nattereri (df = 1,
Deviance = 0.654, p > 0.05) and was not affected by the background colouration (df = 1,
Deviance = 0.637, p > 0.05; Fig. 1). Tadpole mortality was not affected by the interaction
between the background colouration and the behavioural type (df = 1, Deviance = 0.001, p >
0.05), although the power of the test was 0.718 for high effect sizes (DELTA > 1), thus we
are unable to infer if our result is not significant because the lack of a strong biological effect
or due our sample size. However, we observed odonate larvae mortality only after eating
tadpoles of R. schneideri (P. flavescens mortalityE. nattereri = 0%, P. flavescens
mortalityR.schneideri = 8.82%, 2 = 4.570, df = 1, P = 0.032). Additionally, we found a higher
quantity of tadpoles remains of R. schneideri when compared with tadpoles remains of E.
nattereri (E. nattereriproportion of remains = 29%, R. schneideriproportion of remains = 71%, 2 = 9.762,
df = 2, P < 0.01) (Fig. 2).
Background Colouration and Tadpole Activity
Tadpoles of R. schneideri had higher active time than tadpoles of E. nattereri, and this
difference was statistically significant (Table 1; Fig. 3). The active time for both E. nattereri
and R. schneideri tadpoles was significantly lower in the WPF than in the BPF treatment
(Table 1; Fig. 3), and it was significantly affected by the presence of the predator (Table 1;
Fig. 3). Also, the interactions of these factors, in any combination, were statistically
164
significant (Table 1). Thus, the activity of tadpoles of E. nattereri in the presence of the
predator was reduced more than the activity of R. schneideri tadpoles, but both species had
higher active time in the BPF background type (Fig. 3).
DISCUSSION
Background Colouration and Mortality
The efficiency of the behavioural strategies and morphological traits of tadpoles is dependent
on several environmental factors (RUXTON et al. 2004), once we found no evidence that the
larvae of P. flavescens preferred any of the two anuran species at both background types.
Pantala flavescens larvae have higher activity rates, resulting in higher prey-encounter and
prey-capture rates (JOHANSSON & SUHLING 2004), and the effectiveness of the cryptic
behaviour and reduction in the activity rate of E. nattereri tadpoles should be dependent on
the availability of enemy-free spaces. In natural ponds, many tadpole species associated
cryptic behaviour or burst displacement with the behaviour of staying partially burrowed
under detritus or in the sediment (ETEROVICK et al. 2002; KOLENC et al. 2009). This kind of
burrowing behaviour could provide an enemy-free space, because P. flavescens does not
forage under detritus. We suggested that, in a simplified environment, without detritus or
sediment, the substrate colouration alone is not sufficient to reduce the mortality rate of
cryptic tadpoles. Conversely, the efficiency of aposematism of R. schneideri tadpoles
appears to be dependent on the predator type (NOMURA et al. 2011). Some authors believe
that the aposematic colouration of black tadpoles and unpalatability are more efficient
against predators that swallow or chew their prey, such as odonate larvae and fish, than those
that suck body fluids, such as notonectids and dytiscidae larvae (HEYER et al. 1975; VAN
BURSKIRK 1988; HERO et al. 2001). However, many odonate larvae are not affected by
tadpole toxins and, therefore, are able to prey on generally unpalatable tadpoles (CROSSLAND
165
& ALFORD 1998; HERO et al. 2001; SMITH et al. 2008; BALLENGE & SESSIONS 2009;
NOMURA et al. 2011). In our experiment, the predator P. flavescens larvae were able to
consume R. schneideri tadpoles, despite the fact that the skin toxin of these tadpoles is an
efficient deterrent of fish predation (NOMURA et al. 2011).
We detected a higher number of non-consumed parts of R. schneideri tadpoles when
compared to the non-consumed parts of E. nattereri. Also, we recorded the death of six P.
flavescens larvae after the predation of R. schneideri tadpoles, but we did not register any P.
flavescens larvae deaths after the predation of E. nattereri tadpoles. If the predator had no
previous contact with R. schneideri tadpoles, then P. flavescens larvae had no knowledge that
the prey was toxic before capturing and tasting the tadpole. In this case, it is possible that
some P. flavescens larvae ingested more pieces of tadpoles than others before making the
decision to release the tadpole. Thus, it is possible that there is intrapopulational variation in
the P. flavescens resistance to the toxins of bufonid tadpoles, similar to what has been found
in other tadpole predators (notonectids, dytiscid larvae and leeches; CROSSLAND & ALFORD
1998). The tolerance of P. flavescens to the toxin of bufonid tadpoles may provide this
species with the opportunity to exploit a resource unavailable to others predators, by
selecting only the palatable parts of the tadpoles, such as the intestine and viscera, as
opposed to the unpalatable parts. Thus, the known gustative ability of odonate larvae,
although not important to prey selection (PRITCHARD 1965; HEYER et al. 1975), may be
important for selecting which parts of the prey can be eaten. This predator behavioural
response (selection of non-toxic or less-toxic prey parts to consume) is also an alternative to
the evolution of metabolic pathways to process tadpole toxins once behavioural
modifications are considered to precede and, generally, drive physiological and
morphological adaptations (HUEY et al. 2003).
Substratum Colouration and Foraging Activity

166
Tadpole activity is directly related to predation risk (WERNER & ANHOLT 1993). In our
experiments, although the tadpole predation rate by P. flavescens was not affected by
substrate colouration, the tadpole activity was affected. Tadpoles use chemical and visual
cues to indirectly assess the presence and activity of predators (MCCOLLUM & LEIMBERGER
1997; PEROTTI et al. 2006; TAKAHARA et al. 2012), and the tadpoles respond to these
indirectly cues by altering their behaviour or morphology to reduce their predation risk
(MCINTYRE et al. 2004). When a predator is detected, the tadpoles could tune their behaviour
according to the colour of the substrate, based on visual cues, and the presence of the
predator. DONG et al. (2009) demonstrated that tadpoles exposed to visual stimulus only,
such as size or colour patterns, displayed avoidance behaviour and were able to distinguish
small changes in colour in a visually noisy environment. The activity of the cryptic tadpoles
of E. nattereri was higher in the BPF treatment, where the substrate matched the tadpole
colour more closely, increasing the inconspicuousness effect of the tadpole colouration when
compared to the brighter substrate colouration (WPF). The aposematic tadpoles of R.
schneideri were less active in the WPF treatment than in the BPF treatment, where the black
colouration of the tadpole body greatly contrasted with the bright substrate. Thus, R.
schneideri tadpoles performed like cryptic tadpoles, modulating their level of activity
according to the substrate colouration, avoiding higher activity rates when the substrate
colouration contrasted with their body colouration. There is some evidence, based on
computational simulations, that aposematic signals could be derived from cryptic colouration
(MERILAITA & TULLBERG 2005), which could explain why the aposematic tadpoles of R.
schneideri use a cryptic strategy despite the presence of toxins in their skin. Additionally, the
behaviour exhibited is not defined by the intrinsic costs of the behaviour per se, but
according to its relative costs in relation to the ecological context, such as background
colouration, predator presence or an interaction of these factors (MERILAITA & TULLBERG

167
2005; MERILAITA & RUXTON 2007; NOMURA et al. 2011).
The unpalatability seems to be advantageous in comparison to cryptic behaviour
because it allows tadpoles to sustain their activity level and remain relatively safe from
predation. At the population level, the unpalatability associated with aposematic colouration
could optimize the prey survivability by accelerating predator learning (GITTLEMAN et al.
1980; LEE et al. 2010). In order to be efficient, a predator should learn more quickly based
on an aposematic clue than crypsis (LEE et al. 2010). In predator-prey system in which exists
variation in the tolerance of predators to the prey defences, the lack of learning could result
in higher prey mortality rates (HERO et al. 2001; LEE et al. 2010; NOMURA et al. 2011).
Moreover, unpalatability may not be an effective deterrent of odonate larval predators
because the conspicuousness of many species would enhance the probability of tadpoles
being perceived and preyed upon by the predators (AZEVEDO-RAMOS et al. 1992; CHOVANEC
1992; HERO et al. 2001). Thus, it seems reasonable to infer that even unpalatable tadpoles
could benefit from the ability to modulate their predation risk by altering their active time,
but depending on the ecological context or situation, unpalatable tadpoles could display
suboptimal behaviours.
Suboptimal behaviour and limited plasticity
The differences in the behaviour of the tadpoles of E. nattereri (cryptic, less active and
highly plastic behavioural display) and R. schneideri (aposematic, more active and relatively
static behavioural display) were consistent between the different ecological situations tested
in our experiments (predator presence/absence and bright/dark background colour). This type
of correlation between behaviour and ecological situations can lead to suboptimal
behavioural displays within a given situation (SIH et al. 2003). For example, R. schneideri
should favour higher activity in the absence of predators or during competitive interactions,
but this behaviour might be disadvantageous in situations when the higher activity increases
168
the predation risk (SIH et al. 2003; NOMURA et al. 2011). The opposite is true for the
consistently less active E. nattereri tadpoles (which the lower activity is advantageous in the
presence of a predator, but mighty be disadvantageous during competitive interactions).
Suboptimal behaviour could arise when an important general behavioural tendency is
conserved over another similar context or situation (SIH et al. 2004b). For R. schneideri,
unpalatability is a compensatory trait that reduces the cost of an increased activity rate when
it is disadvantageous (predator presence). Conversely, E. nattereri compensates for the cost
of exploratory behaviour with another behavioural trait, cryptic behaviour. These differences
in the compensatory traits of a costly behaviour (the activity rate, which increases the
predation risk) represent different adaptive strategies: a fixed trait associated with limited
plasticity in the behavioural response maximises the exploration of a stable environment
(proactive coping style), whereas a flexible behavioural trait maximises the resource
exploration of an unpredictable environment (reactive coping style) (KOOLHASS et al. 1999;
SIH et al. 2004a; NOMURA & ROSSA-FERES 2011).
These proactive and reactive behavioural adaptive strategies differ in the amount of
environmental information that the organism requires to be efficient. The reactive E. nattereri
should be more dependent on external stimuli to better adjust their behaviour to a specific
ecological situation and could modify their activity rate according to an environmental
change. Rhinella schneideri tadpoles are also capable of modifying their behaviour in this
manner, but to a much more limited degree, displaying a limited plasticity in their behaviour.
Sustaining nearly the same activity level despite the ecological situation prevents the tadpole
from gathering information before making decisions about time allocation in foraging or
hiding. Thus, limited behavioural plasticity should persist if its costs are mediated by
compensatory traits (morphological or behavioural) or when the organism is capable of
avoiding situations where the costs are maximised (e.g., when the behaviour increases the
169
predation risk) (SIH et al. 2004b). Thus, we suggest that the substrate colouration could be an
important stimulus for the tadpole in evaluating its predation risk and modulating its
behaviour accordingly; even the proactive R. schneideri tadpole is affected by the background
colour.
CONCLUSION
The tadpoles of R. schneideri and E. nattereri present behavioural and morphological traits
that appears together (aposematism and active behaviour, cryptic colouration and cryptic
behaviour) and the response to the predator presence, or its indirect cues, is dependent of the
interaction of these behavioural and morphological traits (KATS & DILL 1998; LIMA 1998).
Although we were unable to show any evidence that the background colouration affect the
predator preference and tadpole mortality, the background colour could affect the tadpole
evaluating of the predation risk, which adjust their behaviour accordingly, and may affect the
tadpole tolerance to cues of predator presence. Thus, visual cues of predator presence are
relatively less important to tadpoles when evaluating its predation risk (TAKAHARA et al.
2012), but should be important to select adequate patches of microhabitat in which the
background coloration maximizes the effect of behavioural induced defences. This behaviour
adjustment was observed even among the aposematic tadpoles of R. schneideri, which
reduced their activity and adjusted their behaviour according to the background colour,
although within a much limited degree than the cryptic tadpoles of E. nattereri. Our
conclusions should be contrasted with more complex systems, with the presence of more
prey species in different ecological contexts.
The differences in the behavioural responses of R. schneideri (proactive) and E.
nattereri (reactive) tadpoles to the presence of a predator and the background colouration
represent different adaptive strategies corresponding to different levels of environmental

170
unpredictability. Whereas R. schneideri tadpoles displayed a limited plasticity in their
activity level despite the ecological context, which would be advantageous in stable
environments, E. nattereri had a higher degree of behavioural plasticity between the tested
ecological situations, which would be favoured in unpredictable environments. The ability to
modulate the activity level according to the background colouration, rather than selecting
only perfectly matching background areas, also reduces the costs associated with cryptic
behaviour (RUXTON et al. 2004).
ACKNOWLEDGMENTS
We thank AL Carvalho for identifying the odonate larvae, EG Freitas, L Schiesari, GQ
Romero, MV Cianciaruso and two anonymous reviewers for their critical suggestions of the
manuscript. Research was funded by Conselho Nacional de Desenvolvimento Cientfico e
TecnolgicoCNPq (Grants 563075/2010-4 and 472125/2010-9) and Fundao de Amparo
Pesquisa do Estado de So PauloFAPESP (Grant 10/52321-7).
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TABLES
Table 1. GLM (active time ~ substrate coloration * tadpole species * predator presence)
analysis of the effect of tadpole behaviour (tadpoles), substrate colouration (substrate) and
predator presence/absence (predator) on tadpole active time.
Residual
Source df Deviance Residual df P
Deviance
Substrate 1 0.016 38 0.650 0.023
Predator 1 0.003 37 0.646 0.012
Tadpole 1 0.475 36 0.171 0.006
Substrate vs Predator 1 0.004 35 0.167 0.029
Substrate vs Tadpole 1 0.003 34 0.163 0.032
Predator vs Tadpole 1 0.040 33 0.123 0.015
Substrate vs Predator vs.

1 0.021 32 0.101 0.037
Tadpole
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FIGURE LEGENDS
Fig. 1. Proportion of cryptic (E. nattereri) and aposematic (R. schneideri) tadpoles
mortality in two different background colouration. WPF White Polyethylene Film; BPF
Black Polyethylene Film. Vertical bars represent the upper and lower limits of the confidence
interval.
Fig. 2. Non-consumed parts of cryptic (E. nattereri) and aposematic (R. schneideri)
tadpoles found in the aquariums after the experimental trials. CF&M Caudal fins and
musculature; S&E Snout and eyes; S Snout only.

179
Fig. 3. Mean foraging time of cryptic tadpoles of E. nattereri and aposematic tadpoles of
R. schneideri in two background colouration types, black polyethylene film (BPF) and white
polyethylene film (WPF), in the presence and absence of the predator Pantala flavescens.
Vertical bars represent the upper and lower limits of the confidence interval.
180
CAPTULO 7 (a ser submetido para a revista Iheringia: srie Zoologia)
Avaliao de risco e plasticidade comportamental limitada em girinos de
Rhinella ornata (Anura: Bufonidae)
Renan N. Costa1 & Fausto Nomura2
1 Programa de Ps-Graduao em Ecologia e Evoluo, Universidade Federal de Gois.
2 Laboratrio de Herpetologia e Comportamento Animal, Universidade Federal de Gois.
RESUMO
Os girinos de anfbios anuros so elementos importantes das redes trficas de ambientes
aquticos, sendo recurso alimentar de diversos tipos de predadores. Desta maneira, os girinos
apresentam uma grande variedade de mecanismos de defesa morfolgicos, comportamentais
e fisiolgicos. A impalatabilidade, decorrente do acmulo de substncias txicas na pele,
um mecanismo comum presente nos girinos de alguns grupos de anuros. No entanto, algumas
espcies de predadores no so afetadas por estas substncias txicas, o que pode favorecer o
surgimento de mecanismos alternativos de defesa contra predao. Neste contexto, nosso
objetivo avaliar se girinos de Rhinella ornata, que apresentam substncias impalatveis na
sua pele, podem apresentar mecanismos comportamentais de defesa contra predao na
presena de predadores que no so afetados pelas substncias txicas em sua pele. Para
testar nossa hiptese, utilizamos dois tipos de predadores: um heterptera aqutico do gnero
Belostoma e uma larva de liblula do gnero Aeshna. As larvas de anuros foram colocados
em aqurios com pistas visuais e qumicas ou somente pistas qumicas dos predadores e o
comportamento de natao foi observado durante 5 minutos. Durante os experimentos no
houve alterao no comportamento de natao por parte dos girinos.

181
Palavras-Chave: Rhinella ornata; predao; comportamento defensivo; predadores
invertebrados; sinais qumicos.
INTRODUO
Conhecer as interaes entre predadores e presas um fator-chave para o entendimento de
padres e propriedades de comunidades naturais (Sih et al. 1998, Werner & Peacor 2003).
Estudos experimentais tem evidenciado o papel dos predadores na regulao do tamanho
populacional das presas (Sih et al. 1985, Lima & Dill 1990), alm da deteco e do
reconhecimento de mecanismos antipredao, como a impalatabilidade e o comportamento
crptico (Nomura et al. 2011).
Os girinos de anfbios anuros so bons modelos para estudos experimentais sobre
predao, pois, fazem parte da dieta de um grande nmero de vertebrados (e. g. peixes, aves,
anfbios) e invertebrados (e. g. baratas dgua, larvas de odonata e aranhas) (Duellman &
Trueb 1994). Geralmente, os girinos apresentam alta plasticidade fenotpica, podendo alterar
sua morfologia, fisiologia e/ou comportamento quando submetidos presso de predadores
(McCollum & Van Buskirk 1996, Altig & McDiarmid 1999, Relyea 2001, Moore et al.
2004). Nesses casos, dentre as respostas dos girinos aos predadores incluem a formao de
agregados, abandono de microambiente, busca de refgios, comportamento crptico,
imobilidade ou reduo da atividade de forrageio (Eterovick 2000; Wells 2007). Estas
mudanas so geralmente induzidas por pistas indiretas, como o reconhecimento de
substncias qumicas liberadas por predadores ou pela predao de coespecficos (Perotti et
al. 2006), e so fundamentais para a coexistncia de girinos e seus predadores (Hero et al.
2001).
Os girinos de algumas espcies apresentam colorao e comportamento crptico, o que
diminui a chance de serem detectados em ambientes estruturados, enquanto outros

182
apresentam colorao aposemtica, o que destaca o girino no ambiente em uma advertncia
aos predadores sobre a presena de substncias impalatveis em sua pele (Wells 2007). A
eficincia das estratgias defensivas podem variar de acordo com o tipo de estratgia de
forrageio (Hero et al. 2001; Nomura et al. 2011) e com o nvel de sensibilidade s substncias
impalatveis (Heyer et al. 1975, Hero et al. 2001) dos predadores. Por exemplo, girinos do
gnero Rhinella so conhecidamente impalatveis e apresentam colorao de alerta, podendo
ainda formar agregados de indivduos, o que aumentaria a intensidade desse sinal (Eterovick
2000). Entrentato, este tipo de proteo mais eficiente contra predadores que engolem a
presa inteira, como peixes, ou que mastigam a presa antes de consum-la, como larvas de
odonata (Van Burskirk 1988, Hero et al. 2001). Outros predadores que no engolem a presa
ou a mastigam, como baratas-dgua do gnero Belostoma, no so afetados pela
impalatabilidade (Tobler et al. 2007). As baratas-dgua injetam toxinas que paralisam a
presa e liberam enzimas digestivas que causam necrose nos tecidos da vtima
(Swart & Felgenhauer 2003). Algumas larvas de liblula (e.g., gnero Aeshna) tambm no
so afetadas pela impalatabilidade, apesar de mastigarem suas presas (Crossland & Alford
1998, Nomura et al. 2011), e so consideradas importantes predadoras de girinos (Hero et al.
2001).
Muitos estudos relatam que girinos de Rhinella alteram seu comportamento na
presena de diferentes predadores, sendo que a resposta mais comum a reduo de sua
atividade (Skelly & Werner 1990, Anholt et al. 1996, Perotti et al. 2006; Stav et al. 2007,
Jara & Perotti 2009, 2010). No entanto, essas defesas induzidas so muito plsticas e podem
ser influenciadas pelo estgio de desenvolvimento ontogentico do girino, diferentes nveis
de palatabilidade, coexistncia com predadores especficos, entre outros (Relyea 2003,
Richter-Boix et al. 2007, Jara & Perotti 2009).
Quando predadores de diferentes espcies ocorrem em um mesmo ambiente, a presso

183
e os efeitos sobre a populao de presas podem variar de acordo com as interaes entre os
potenciais competidores (Finke & Denno 2002). Interaes entre predadores podem ter
efeitos aditivos, sinrgicos ou antagnicos. Efeitos aditivos ocorrem quando a soma dos
efeitos individuais dos predadores causa um maior impacto nas populaes de presas (Chang
1966). Interaes sinrgicas acontecem em situaes onde um predador facilita o impacto do
outro, podendo ser resultado de mtodos de forrageio complementares (Losey & Denno
1998). J as interaes antagnicas podem ser mediadas por mtodos de forrageio similares,
onde o efeito de um predador se sobrepe ao efeito do outro e vice-versa (Moran et al. 1996).
Neste caso, h uma diminuio na captura de presas alm da possvel predao intraguilda
(Polis & Holt 1992).
Neste contexto, nosso objetivo avaliar se o comportamento de girinos de Rhinella
ornata alterado diante do risco de predao. Mais especificamente, esperamos testar se na
presena de predadores, os girinos de R. ornata reduzem sua atividade natatria. Tambm
testaremos se existe um efeito da presena de predadores competidores sobre as taxas de
predao de girinos de R. ornata. Neste caso, esperamos que quando os indivduos de
Belostoma sp. e de Aeshna sp. ocorram juntos promovam um efeito aditivo sobre a populao
de presas, causando maior impacto sobre as presas em um menor tempo. Adicionalmente,
testaremos se apenas o sinal qumico deixado pelo predador modifica o comportamento do
girino. Neste caso, esperamos que o tempo de natao dos girinos seja reduzido com o sinal
qumico deixado pelo predador.
MATERIAL E MTODOS
Sistema de estudo
Os girinos de R. ornata foram coletados com um pu de tela de arame em um corpo dgua
lntico de restinga prximo praia (232131.42 S; 442123.66 O), totalizando 80

184
indivduos. Neste mesmo ambiente coletamos amostras de folhio e pedras para servir de
substrato durante os experimentos. Os predadores invertebrados foram coletados em um
corpo dgua em uma rea de capoeira, totalizando 45 indivduos de Belostoma sp. e 45
indivduos de Aeshna sp. (232138.49 S; 445002.65 O). Todos os espcimes utilizados
foram coletados no ms de Julho de 2012 no ncleo Picinguaba do Parque Estadual da Serra
do Mar, localizado no municpio de Ubatuba-SP.
Todos os indivduos de Belostoma sp. e Aeshna sp. foram deixados sem alimento por
24h antes do incio do experimento. Usando potes pequenos auxiliares, posicionamos os
indivduos lado a lado antes de cada observao e visualmente selecionamos aqueles que
apresentavam tamanho corporal semelhante. Utilizamos girinos de R. ornata entre os estgios
35-39 (sensu Gosner 1960) e que tambm apresentavam tamanho semelhante entre si, mas
sempre menor que metade do tamanho da larva de liblula.
O tempo de deslocamento foi considerado apenas quando o girino se locomovia entre
pontos distintos no aqurio. Em ambos os experimentos, cada unidade experimental foi
observada durante 5 minutos e o tempo de deslocamento dos girinos foi mensurado com
auxlio de um cronmetro digital. Atividade de movimentao da cauda que no resultava em
deslocamento no foi medido durante a observao. Os experimentos foram realizados no
perodo diurno, pela manh, em local sombreado e sob as mesmas condies ambientais.
Pinas, aqurios e peneiras foram individualizadas por tratamento, evitando misturar
predadores e/ou compostos qumicos liberados pelos mesmos. Antes de cada rplica, alm de
trocar o folhio e a gua, sempre substitumos os predadores e os girinos. Todos os
indivduos foram utilizados apenas uma vez.
Experimento de risco direto
Para testar se os girinos modificam o seu comportamento de natao quando expostos ao
risco de predao, realizamos um experimento criando microcosmos em quatro aqurios

185
plsticos redondos (110 cm x 80 cm). Em todos os aqurios adicionamos a mesma quantidade
de folhio e o mesmo nmero de pedras, dispostas de maneira semelhante dentro de cada
aqurio, com 320 ml de gua limpa. Em cada microcosmo, os girinos foram submetidos a
presena dos predadores nos seguintes tratamentos: controle (Co) sem a presena de
predadores; Belostoma sp. (Bel) dois indivduos de Belostoma sp.; Aeshna sp. (Aes) dois
indivduos de Aeshna sp.; e Misto (Mi) um indivduo de Belostoma sp. e um indivduo de
Aeshna sp. Desta forma, esperamos controlar o efeito da abundncia de predadores entre os
tratamentos. Os predadores foram adicionados ao mesmo tempo em todos os aqurios e
deixados para se aclimatar no novo ambiente durante 1 minuto. Os girinos foram adicionados
aos aqurios aps o perodo de aclimatao dos predadores e as observaes do
comportamento do girino se iniciavam aps 30 segundos. O tempo de aclimatao dos girinos
foi menor, comparado ao tempo de aclimatao dos predadores, devido ao risco de predao
(experimento letal). Nos aqurios que ocorreram eventos de predao, a observao foi
encerrada, o predador registrado e o tempo de deslocamento dos girinos foi ponderado em
relao ao tempo total da observao do experimento. Ao final das observaes, realizamos
11 rplicas de cada tratamento, totalizando 44 aqurios observados e aproximadamente
03h30min de observao direta.
Experimento de risco indireto
No experimento de deteco do sinal qumico, utilizamos os mesmos aqurios e a mesma
quantidade de folhio e pedras detalhados no experimento anterior. Entretanto, foram
adicionados apenas 80 ml de gua limpa e um girino de R. ornata em trs aqurios diferentes.
Os girinos foram mantidos 5 minutos em cada aqurio para aclimatao. Aps esse perodo, o
restante da gua dos aqurios foi completada com a gua de dois aqurios auxiliares onde 10
indivduos de Belostoma sp. e 10 indivduos de Aeshna sp. foram mantidos por 12 horas, com
intuito de concentrar qumicos liberados na gua. Nos aqurios, os girinos foram submetidos
186
a trs tratamentos: Controle (Contr) controle adio de 240 ml de gua limpa; Belostoma
sp. (Belos) adio de 240 ml de gua dos aqurios com indivduos de Belostoma sp.; e
Aeshna sp. (Aeshn) adio de 240 ml de gua dos aqurios com indivduos de Aesha sp. A
gua foi adicionada de forma gradual e cuidadosa ao aqurio para reduzir o estresse dos
girinos. Realizamos 10 rplicas de cada tratamento, totalizando 30 aqurios observados e
aproximadamente 02h30min de observao direta.
Anlise de dados
No primeiro experimento realizamos uma ANOVA Fatorial para comparar o tempo de
natao dos girinos em relao presena e aos tipos de predadores no tratamento.
Utilizamos como varivel resposta a proporo do tempo de deslocamento, ponderada em
relao ao tempo total de durao de cada experimento, e cada predador como um fator (dois
nveis, presena ou ausncia). No segundo experimento, realizamos uma ANOVA para
comparar se apenas o sinal qumico deixado pelo predador altera o comportamento de
natao dos girinos entre os tratamentos (Zar 1999).
RESULTADOS
No houve reduo na atividade de natao dos girinos de R. ornata na presena de
predadores Belostoma sp. (F(1,11)= 0,36; p= 0,54), na presena de larvas de Aeshna sp. (F(1,11)=
2,40 ; p= 0,12) ou na presena de ambos os predadores (F(1,11)= 1,65; p= 0,20) (Fig. 1). Desta
maneira, os girinos de R. ornata apresentam atividade de deslocamento constante,
independente do risco de predao ou do tipo de predador. Entretanto, apesar da ausncia de
resposta ao risco de predao, observamos nove eventos de predao, quatro no tratamento
Aes (44,4%), com um evento resultando na morte do girino, e cinco no tratamento Mis.
Entretanto, no tratamento Mis, todos os eventos de predao observados foram realizados por
Belostoma sp. as quais capturaram tanto girinos (33,3%) quanto larvas de Aeshna sp.
187
(22,2%).
No experimento de risco indireto, os girinos de R. ornata no apresentaram diferenas
significativas no tempo de deslocamento entre os tratamentos aos quais foram expostos
(F(2,10)= 0,06; p= 0,93) (Fig. 2). Desta maneira, girinos de R. ornata no distinguiram a
presena ou tipo de predador em funo das pistas qumicas presentes na gua.
DISCUSSO
Comportamento Subtimo
Diferentes tipos de predadores exercem diferentes presses evolutivas sobre as populaes de
presas (Brodie Jr. et al. 1991). Com a presena de predadores, os girinos podem apresentar
diversos mecanismos antipredao (DHeursel & Haddad 1999), os quais so dependentes
dos padres comportamentais apresentado pelas espcies (Sih 1985, Jara & Perotti 2010). De
modo geral, o comportamento dos animais considerado uma caracterstica com grande
plasticidade intra-individual. Em nosso experimento, espervamos que girinos de R. ornata
modulassem o tempo de deslocamento em funo da presena e do tipo de predador, como
forma de compensar o risco predao. No entanto, no observamos nenhuma modulao no
tempo de deslocamento independentemente do risco ou tipo de predador, o que pode ser
interpretado como um comportamento subtimo.
A associao entre as diferentes situaes ou contextos ecolgicos e a plasticidade
comportamental limitada (i.e., limitao na capacidade de modificar o comportamento em
funo do contexto ecolgico) podem fazer com que uma tendncia comportamental
importante seja conservada ao longo de um gradiente de uma determinada situao ou
contexto ecolgico (Sih et al. 2003). Desta maneira, quando a taxa de exibio de um
comportamento observada em um contexto isolado, este comportamento pode ser
interpretado como no-adaptativo ou subtimo. Por exemplo, em nossos experimentos, os

188
girinos de R. ornata no apresentaram uma reduo no tempo de deslocamento na presena
de predadores como forma de reduzir sua exposio ao risco de ser predado. Entretanto, ao
avaliarmos o mesmo comportamento em outras situaes ou contextos ecolgicos, estes
comportamentos podem propiciar uma aptido maior ao indivduo (Sih et al. 2003). Em um
experimento realizado por Nomura et al. (2011), os autores observaram que os girinos de R.
schneideri maximizam a atividade de forrageamento, apresentando maior aptido na ausncia
de predadores e durante interaes competitivas com a espcie E. nattereri (Nomura et al.
2011). Entretanto, R. schneideri tambm apresentou maior atividade de forrageamento na
presena de predadores quando comparados a girinos de E. nattereri, o que aumentava o seu
risco predao (Nomura et al. 2011), da mesma maneira que os girinos de R. ornata em
nosso experimento. Assim, a maior atividade exploratria dos girinos de R. ornata devem
propiciar aos indivduos uma maior aptido durante interaes competitivas, mas tambm
aumentaria o custo associado ao risco de predao. Nestes casos, os organismos podem
desenvolver traos compensatrios para reduzir o custo da estratgia comportamental, como a
impalatabilidade (Nomura et al. in press). Em R. ornata, a impalatabilidade provavelmente
um trao fixo que evoluiu para sustentar a maior atividade exploratria, compensando o risco
predao e maximizando o potencial competitivo da espcie. Este padro de
comportamento tambm conhecido como padro proativo (proactive coping style) e
vantajoso em ambientes previsveis (Koolhaas et al. 1999).
A atividade de forrageamento dos girinos est diretamente relacionada ao risco de
serem predados (Werner & Anholt 1993) e pode ser mediada por pistas qumicas e/ou visuais
deixadas por predadores (McCollum & Leimberger 1997, Takahara et al. 2012). Estas pistas
indiretas podem provocar mudanas no comportamento de defesa dos girinos, que poderiam
atenuar o risco de serem predados (Perotti et al. 2006). No entanto, a eficincia de algumas
estratgias de defesa independente da deteco do predador ou tipo de predador, como a

189
impalatabilidade (Semlitsch & Gavasso 1992), o que permite que os indivduos mantenham a
sua taxa de forrageio constante mesmo na presena de predadores (Nomura et al. in press).
Em nosso experimento, os girinos de R. ornata no responderam s pistas indiretas (sinal
qumico) dos predadores e no modularam seu tempo de deslocamento. Neste caso,
provvel que girinos de R. ornata apresentem um padro de comportamento proativo, onde
no necessita da anlise do ambiente para tomada de deciso entre forrageio e busca por
abrigos. Alm disto, a impalatabilidade atua como um mecanismo de defesa que no depende
da deteco prvia de um predador, mas baseado em um contexto de aprendizagem. Este
tipo de estratgia pode favorecer a espcie em ambientes com baixa presso de predadores ou
em situaes onde a impalatabilidade eficiente como, por exemplo, em ambientes onde os
peixes so os principais predadores (Hero et al. 2001, Nomura et al. 2011).
Predao Intraguilda
Diferentes comportamentos predatrios podem reduzir a aptido de uma espcie de predador
na presena de outras espcies competidoras (Finke & Denno 2002). Geralmente, as larvas de
Aeshna sp. so mais eficientes predando girinos que apresentam atividade natatria constante
(Nomura et al. 2011). Nosso experimento nos permite inferir uma tendncia de interao
antagnica entre Aeshna sp. e Belostoma sp.: a eficincia de predao de Aeshna sp. foi
menor quando estava no mesmo aqurio de Belostoma sp. Um resultado semelhante foi
encontrado por Huang & Sih (1991), que estudaram a interao entre peixes (Lepomis sp.) e
salamandras (Ambystoma sp.) se alimentando de larvas de ispodas (Lirceus sp.). As
salamandras sozinhas se alimentam mais de ispodas do que os peixes, porm, quando os
predadores esto juntos a situao se inverte. Com a presena dos peixes, as salamandras
buscam refgios que so similares aos usados pelos ispodas, os quais ficam mais expostos
ao risco de predao, aumentando o sucesso dos peixes. Estas interaes antagnicas entre
predadores podem reduzir o risco de predao das presas (Sih et al. 1998). Rosenheim et al.
190
(1993) observaram que as populaes de afdeos (Aphis) so totalmente reduzidas com a
presena de predadores do gnero Chrysoperla. No entanto, insetos predadores dos gneros
Geocoris, Nabis e Zelus predam afdeos com menor intensidade, porm, so mais vorazes ao
predar indivduos de Chrysoperla, liberando os afdeos do efeito massivo destes predadores.
provvel que em ambientes temporrios Belostoma sp. tambm possa produzir este efeito
antagnico da predao intraguilda, reduzindo o impacto da predao de larvas de Aeshna sp.
sobre as populaes de girinos. Entretanto, esta hiptese necessita de comprovao em
estudos futuros.
CONCLUSO
O comportamento de natao dos girinos de R. ornata no foi afetado pela presena ou pistas
indiretas da presena dos predadores. Aparentemente, R. ornata apresenta uma plasticidade
comportamental limitada nas suas respostas antipredatrias, o que pode ser vantajoso em
ambientes de alta previsibilidade. Belostoma sp. pode afetar positivamente as populaes de
girinos, uma vez que pode reduzir as populaes de Aeshna sp., no entanto, esta hiptese
necessita ser comprovada por estudos futuros.
AGRADECIMENTOS
Agradeo ao coordenador da disciplina, Dr. Gustavo Romero e ao curso de Ps-graduao
em Ecologia da Unicamp, pela oportunidade oferecida. Agradeo tambm equipe do ncleo
Picinguaba do Parque Estadual da Serra do Mar pelo apoio.
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195
FIGURAS
Figura 1. Atividade de natao de girinos de R. ornata na ausncia e presena de predadores.
Barras verticais representam os limites superiores e inferiores do intervalo de confiana.
Figura 2. Atividade de natao de girinos de R. ornata em aqurios com gua sem pista de
predadores (Controle), com pistas de Belostoma sp. (gua retirada de aqurios com 20
indivduos de Belostoma sp.) e com pistas de Aeshna sp. (gua retirada de aqurios com 20
indivduos de Aeshna sp.). Barras verticais representam os limites superiores e inferiores do
intervalo de confiana.

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HERANA OU AMBIENTE?

VS PROCESSOS ECOLGICOS NA DETERMINAO DAS

CARACTERSTICAS MORFOLGICAS EM GIRINOS

Prof. Dr. Fausto Nomura

RELATRIO FINAL de projeto apresentado ao

Introduo Geral ..................................................................................................................... 4

Referncias Bibliogrficas .......................................................................................... 6

Principais Dificuldades Enfrentadas no Perodo ................................................................. 9

Captulo 4 ............................................................................................................................. 116

Captulo 5 ............................................................................................................................. 138

Captulo 6 ............................................................................................................................. 154

Captulo 7 ............................................................................................................................. 180

Para a teoria de nicho, comunidades ecolgicas no so formadas por associaes

puramente casuais de espcies e diversos parmetros so utilizados para pesquisar os padres

lineares simples de caracteres externos ou osteolgicos possvel inferir padres e processos

variedade de formas de girinos, larvas de anfbios anuros, resultando numa classificao

baseado no aspecto morfolgico, no hbito e no comportamento. Entretanto, apesar da

importncia de fatores ecolgicos na classificao destas guildas ecomorfolgicas, tambm

ocorre influncia de componentes filogenticos na evoluo de determinados caracteres

morfolgicos. O grau em que componentes filogenticos e ecolgicos moldam a morfologia

externa de girinos ainda no totalmente compreendida. Esta interao entre ecologia e

filogenia na determinao da forma dos girinos ilustrativa de dois processos envolvidos na

estruturao de comunidades: seleo de espcies em funo de filtros ambientais e

interaes competitivas, que so diretamente relacionados com a similaridade fenotpica e o

relacionamento filogentico de espcies co-ocorrentes. Desta maneira, nosso objetivo

quais caracteres so resultantes de processos filogenticos e quais so resultantes de processos

ecolgicos. Para isso, propomos a utilizao da anlise morfomtrica geomtrica, juntamente

com a morfometria tradicional, e a otimizao de caracteres em propostas filogenticas

Para a teoria de nicho, comunidades ecolgicas no so formadas por associaes puramente

casuais de espcies (Adler et al. 2007). Ao contrrio, as comunidades ecolgicas apresentam

padres de organizao e os eclogos tm tentado compreender quais processos geram e

Assim, uma das questes centrais da ecologia de comunidades explicar a origem e

manuteno das combinaes de espcies que coexistem em determinadas situaes

ambientais (Lewinsohn 1990).

Diversos parmetros so utilizados para pesquisar padres em comunidades

biolgicas, incluindo o nmero de espcies e suas abundncias absolutas e relativas, os tipos

uso e partilha de recursos (Pianka 1994). Em teoria, diferenas de nicho limitam o

o crescimento de outras, promovendo a coexistncia (Chesson 2000). Neste contexto,

determinados aspectos da morfologia de uma espcie podem estar relacionados ao modo de

pela comparao de medidas lineares simples de caracteres externos ou osteolgicos, a

determinao dos padres e processos adaptativos que estruturam a partilha de recursos em

Existe uma grande variedade de formas de girinos, larvas de anfbios anuros,

representadas por um amplo espectro de tamanhos, formas de corpo, modos de alimentao,

(nutrem-se de fontes parentais durante todo seu desenvolvimento) e girinos exotrficos

1989). Apenas entre espcies exotrficas de ambientes lnticos e lticos, possvel

reconhecer a existncia de diversas guildas baseadas na morfologia geral de alguns caracteres,

& Altig 1999), tambm ocorre influncia de componentes filogenticos na evoluo de

Por exemplo, as guildas neustnicas e bentnicas parecem formar um complexo de

equivalentes ecolgicos, reunindo girinos de diversas famlias de anuros, enquanto que a

(McDiarmid & Altig 1999).

O grau em que componentes filogenticos e ecolgicos moldam a morfologia externa

maneira, apesar de girinos filogeneticamente relacionados apresentarem morfologias

semelhantes (Fatorelli & Rocha 2008), no necessariamente as guildas ecomorfolgicas so

resultantes de processos filogenticos. Esta interao entre ecologia e filogenia na

determinao da forma e do comportamento dos girinos ilustrativa de dois processos

envolvidos na estruturao de comunidades ecolgicas: seleo de espcies em funo de

esto diretamente relacionados com a similaridade fenotpica e o relacionamento filogentico

de espcies co-ocorrentes (Tofts & Silvertown 2000, Webb 2000). Se espcies

filogeneticamente relacionadas compartilham caractersticas morfolgicas similares e

apresentam conservatismo de nicho, os filtros ambientais promovem a coexistncia de

espcies aparentadas, resultando em um padro chamado de agrupamento filogentico

(phylogenetic clustering, Cavender-Bares et al. 2004). Entretanto, a excluso competitiva

pode limitar a coexistncia de espcies relacionadas filogeneticamente que partilham recursos

limitantes e gerar um padro oposto ao do agrupamento filogentico, denominado disperso