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From widespread to microendemic: molecular and acoustic analyses show that Ischnocnema guentheri (Amphibia: Brachycephalidae) is endemic to Rio de Janeiro, Brazil

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Abstract

Many species of tropical amphibians are restricted to very small ranges, and this microendemism coupled with ongoing habitat loss and susceptibility to emerging pathogens imperils the long-term persistence of these species. Incomplete taxonomic and distributional knowledge may obscure conservation assessment, particularly in putatively widespread species that are typically considered to be of Least Concern in Red List assessments, but that in fact may constitute complexes of partly microendemic species. Such is the case in the Steindachner’s Robber Frog, Ischnocnema guentheri which, together with the recently recognized Ischnocnema henselii, is thought to occupy most of the Brazilian Atlantic Forest. To test whether these taxa may constitute a species complex of range-restricted and thus potentially threatened species, we analyzed 160 samples of I. guentheri and/or I. henselii for two molecular markers, 16S rRNA (16S) and recombination activation gene 1 (RAG1). To verify the monophyly of the complex, closely related species were also included in the 16S analysis. Congruent evidence from the molecular data and from analyses of advertisement calls support the existence of six distinct species within the complex: I. guentheri and I. henselii as well as four candidate new species. The lineages are distributed as a mosaic in the Atlantic Forest and are sympatric at some localities without indication of admixture. Their phylogeographical pattern partially agrees with paleo-models for the Atlantic Forest, but also suggests the existence of micro-refugia in less stable areas. I. guentheri, previously considered to be widespread, was found only in its type locality, a reserve within the urban area of Rio de Janeiro city. Although none of the species studied appears highly threatened with extinction, we recommend their IUCN threat status to be re-evaluated carefully for the next comprehensive update of the Red List of Brazil’s amphibians.

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Acknowledgments

The authors are grateful to numerous friends and colleagues who provided samples and/or information. They are in debit with Gláucia Maria Funk Pontes, Diego Baldo, José Pombal Jr., Miguel T. U. Rodrigues, Hussan Zaher and Vivian Trevine who collected and/or provided samples. They thank Maria Tereza Thomé, Tuliana Brunes and João Paulo Soares de Cortes for helping during field work; Mariana Lyra for helping with sample management and shipping logistics; Meike Kondermann and Gabi Keunecke for helping with laboratory procedures. They also thank the two anonymous reviewers who provided valuable suggestions. MG was supported by a Ph.D. scholarship of the Katholischer Akademischer Ausländer-Dienst—KAAD. CC was supported by post-doctoral fellowships Fundação de Amparo à Pesquisa do Estado de São Paulo—FAPESP and Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior/Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro—CAPES/FAPERJ. CFBH acknowledges support by Fundação de Amparo à Pesquisa do Estado de São Paulo—FAPESP and Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq. MV acknowledges support by the Deutsche Forschungsgemeinschaft (grant VE247/7-1). Collection permits were granted by Instituto Chico Mendes – ICMBio to MG (21710-2), CC (14846-3; 20768ß-1) and CFBH (22511-1).

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Authors and Affiliations

  1. Division of Evolutionary Biology, Zoological Institute, Technical University of Braunschweig, Mendelssohnstr. 4, 38106, Braunschweig, Germany

    Marcelo Gehara & Miguel Vences

  2. Departamento de Zoologia, Instituto de Biociências, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Rio Claro, SP, 13506-900, Brazil

    Clarissa Canedo & Célio F. B. Haddad

  3. Departamento de Vertebrados, Universidade Federal do Rio de Janeiro, Museu Nacional, Rio de Janeiro, RJ, 20940-040, Brazil

    Clarissa Canedo

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  1. Marcelo Gehara
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  3. Célio F. B. Haddad
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  4. Miguel Vences
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Correspondence to Marcelo Gehara.

Electronic supplementary material

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10592_2013_488_MOESM1_ESM.pdf

List of all samples analyzed in this study with respective tissue and voucher specimen numbers, and species / candidate species assignment, as well as haplotypes numbers identified in the RAG1 analysis as in Fig. 2 (see fig S1 for an additional network showing haplotype numbers), and GenBank accession numbers. na indicates those individuals from which only tissue samples had been taken. Asterisks indicate those individuals from which advertisement calls were analyzed. Supplementary material 1 (PDF 24 kb)

10592_2013_488_MOESM2_ESM.tif

Nuclear RAG1 median-joining haplotype network. Colors of the haplotypes are assigned based on the grouping of samples in major mitochondrial clades (Fig 1). Branch lengths are proportional to the number of mutational steps which are shown only in branches with more than one mutational step. Numbers of haplotypes are shown according to Table S1. Supplementary material 2 (TIFF 4,830 kb)

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Gehara, M., Canedo, C., Haddad, C.F.B. et al. From widespread to microendemic: molecular and acoustic analyses show that Ischnocnema guentheri (Amphibia: Brachycephalidae) is endemic to Rio de Janeiro, Brazil. Conserv Genet 14, 973–982 (2013). https://doi.org/10.1007/s10592-013-0488-5

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