A Pan-Amazonian species delimitation: High species diversity within the genus Amazophrynella (Anura: Bufonidae)

Rommel R. Rojas; Antoine Fouquet; Santiago R. Ron; Emil José Hernández-Ruz; Paulo R. Melo-Sampaio; Juan C. Chaparro; Richard C. Vogt; Vinicius Tadeu de Carvalho; Leandra Cardoso Pinheiro; Robson W. Avila; Izeni Pires Farias; Marcelo Gordo; Tomas Hrbek

doi:10.7717/peerj.4941

A Pan-Amazonian species delimitation: High species diversity within the genus Amazophrynella (Anura: Bufonidae)

Rommel R. Rojas^*
, Antoine Fouquet
, Santiago R. Ron
, Emil José Hernández-Ruz
, Paulo R. Melo-Sampaio
, Juan C. Chaparro
, Richard C. Vogt
, Vinicius Tadeu de Carvalho
, Leandra Cardoso Pinheiro
, Robson W. Avila
, Izeni Pires Farias
, Marcelo Gordo
, Tomas Hrbek

^*Corresponding author for this work

Faculty of Exact and Natural Sciences

Research output: Contribution to journal › Article › peer-review

58 Scopus citations

Abstract

Amphibians are probably the most vulnerable group to climate change and climatechange associate diseases. This ongoing biodiversity crisis makes it thus imperative to improve the taxonomy of anurans in biodiverse but understudied areas such as Amazonia. In this study, we applied robust integrative taxonomic methods combining genetic (mitochondrial 16S, 12S and COI genes), morphological and environmental data to delimit species of the genus Amazophrynella (Anura: Bufonidae) sampled from throughout their pan-Amazonian distribution. Our study confirms the hypothesis that the species diversity of the genus is grossly underestimated. Our analyses suggest the existence of eighteen linages of which seven are nominal species, three Deep Conspecific Lineages, one Unconfirmed Candidate Species, three Uncategorized Lineages, and four Confirmed Candidate Species and described herein. We also propose a phylogenetic hypothesis for the genus and discuss its implications for historical biogeography of this Amazonian group.

Original language	English
Article number	e4941
Journal	PeerJ
Volume	2018
Issue number	7
DOIs	https://doi.org/10.7717/peerj.4941
State	Published - 2018

Bibliographical note

Publisher Copyright:
© 2018 Rojas et al.

Funding

The following grant information was disclosed by the authors: Coordenac¸ão de Aperfeic¸oamento de Pessoal de Nivel Superior (CAPES). Program Incentivo para la Publicación Efectiva de Artículos Científicos en Revistas Indexadas 2016 –1◦ corte. del Consejo Nacional de Ciencia: RDE 036, 20.04.2016. Tecnología e Innovación Tecnológica de Perú (CONCYTEC –FONDECYT (Cienciactiva)). This work was supported by Coordenac¸ão de Aperfeic¸oamento de Pessoal de Nivel Superior (CAPES), by the Program Incentivo para la Publicación Efectiva de Artículos Científicos en Revistas Indexadas 2016 –1◦ corte, (RDE 036, 20.04.2016) del Consejo Nacional de Ciencia, Tecnología e Innovación Tecnológica de Perú (CONCYTEC –FONDECYT (Cienciactiva)), by Concelho Nacional de Pesquisa (CNPq/SISBIOTA-BioPHAM grant no. CNPq 563348/2010), and an Investissement d’Avenir grant managed by Agence Nationale de la Recherche (CEBA, ref.ANR-10-LABX-25-01), France. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Field work and visits to museum collections were carried out between 2011 and 2017. Field collection of specimens followed the technique of visual encounter surveys and pitfall-barrier traps (Crump & Scott Jr, 1994). Museum acronyms are found in Sabaj (2016) except for Museo de Biodiversidad del Peru (MUBI; this collection is part of Museo de Historia Natural, Universidad Nacional de San Antonio Abad, Cusco, Peru). Collecting permits in Peru were granted by Dirección General Forestal y de Fauna Silvestre del Ministerio del Medio Ambiente (MINAN; No. AUT-IFS-2017-055), in Ecuador by Ministerio del Ambiente (MA; 001-1-IC-FAU-DNB/MA) and in Brazil by the Instituto Chico Mendes de Conservac¸ão da Biodiversidade (ICMBio; No. 39792-1 and No. 32401). The material of Amazophrynella teko from Mitaraka (French Guiana) was collected during the ‘‘Our Planet Reviewed’’ expedition, organized by the MNHN and Pro-Natura International. We examined topotypical material of A. minuta deposited at the collection of Amphibians and Reptiles of the Instituto Nacional de Pesquisas da Amazônia–INPA (INPA–H) and three syntypes (NHMG 462, NHMG 463, NHMG 464) deposited at the Göteborgs Naturhistoriska Museum, Sweden; five specimens of A. bokermanni (Izecksohn, 1993) from near the type locality (c. 30 Km) deposited at the INPA collection; the type series of A. vote (Ávila et al., 2012) deposited at the Colec¸ão Zoológica de Vertebrados of the Universidade Federal de Mato Grosso–UFMT, Cuiabá, Mato Grosso, Brazil (UFMT–A) and INPA; A. manaos (Rojas et al., 2014) deposited at the INPA; A. amazonicola and A. matses (Rojas et al., 2015) deposited at the Museo de Zoología–Universidad Nacional de la Amazonia Peruana–UNAP and A. javierbustamantei (Rojas et al., 2016) deposited at the Museo de Biodiversidad del Peru (MUBI), Museo de Historia Natural de la Universidad Nacional Mayor de San Marcos (MHNSM). A list of the examined specimens is found in Appendix S1. We would like to thank Ariane Silva, from the herpetological collection of the Instituto Nacional de Pesquisas da Amazônia (INPA) in Manaus, Brazil, to Fernando Ayala from the Pontificia Universidad Católica de Ecuador (PUC(E) in Quito-Ecuador, and to O Aguilar and R Orellana (MUBI) for providing administrative support and part of the material for this study. RR Rojas thanks Alexander Almeida, Ian Pool Medina, Richard Naranjito Curto for field support and Mario Nunes for laboratory assistance.This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Nivel Superior (CAPES), by the Program Incentivo para la Publicación Efectiva de Artículos Científicos en Revistas Indexadas 2016-1 corte, (RDE 036, 20.04.2016) del Consejo Nacional de Ciencia, Tecnología e Innovación Tecnológica de Perú (CONCYTEC-FONDECYT (Cienciactiva)), by Concelho Nacional de Pesquisa (CNPq/SISBIOTA-BioPHAM grant no. CNPq 563348/2010), and an Investissement d'Avenir grant managed by Agence Nationale de la Recherche (CEBA, ref.ANR-10-LABX-25-01), France. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.The following grant information was disclosed by the authors: Coordenação de Aperfeiçoamento de Pessoal de Nivel Superior (CAPES). Program Incentivo para la Publicación Efectiva de Artículos Científicos en Revistas Indexadas 2016-1 corte. del Consejo Nacional de Ciencia: RDE 036, 20.04.2016. Tecnología e Innovación Tecnológica de Perú (CONCYTEC-FONDECYT (Cienciactiva)).

Funders	Funder number
Concelho Nacional de Pesquisa
Consejo Nacional de Ciencia, Tecnología e Innovación Tecnológica de Perú
Coordenac¸ão de Aperfeic¸oamento de Pessoal de Nivel Superior	RDE 036, 20.04.2016
Dirección General Forestal y de Fauna Silvestre del Ministerio del Medio Ambiente
MINAN	AUT-IFS-2017-055
Ministerio del Ambiente	001-1-IC-FAU-DNB/MA
SISBIOTA-BioPHAM
Agence Nationale de la Recherche
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Fondo Nacional de Desarrollo Científico y Tecnológico
Conselho Nacional de Desenvolvimento Científico e Tecnológico	563348/2010
Instituto Chico Mendes de Conservação da Biodiversidade	32401, 39792-1
Consejo Nacional de Ciencia, Tecnología e Innovación Tecnológica

Keywords

Amazon
Amphibians
Cryptic diversity
Integrative taxonomy
Species delimitation

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10.7717/peerj.4941

Cite this

Rojas, R. R., Fouquet, A., Ron, S. R., Hernández-Ruz, E. J., Melo-Sampaio, P. R., Chaparro, J. C., Vogt, R. C., Carvalho, V. T. D., Pinheiro, L. C., Avila, R. W., Farias, I. P., Gordo, M., & Hrbek, T. (2018). A Pan-Amazonian species delimitation: High species diversity within the genus Amazophrynella (Anura: Bufonidae). PeerJ, 2018(7), Article e4941. https://doi.org/10.7717/peerj.4941

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abstract = "Amphibians are probably the most vulnerable group to climate change and climatechange associate diseases. This ongoing biodiversity crisis makes it thus imperative to improve the taxonomy of anurans in biodiverse but understudied areas such as Amazonia. In this study, we applied robust integrative taxonomic methods combining genetic (mitochondrial 16S, 12S and COI genes), morphological and environmental data to delimit species of the genus Amazophrynella (Anura: Bufonidae) sampled from throughout their pan-Amazonian distribution. Our study confirms the hypothesis that the species diversity of the genus is grossly underestimated. Our analyses suggest the existence of eighteen linages of which seven are nominal species, three Deep Conspecific Lineages, one Unconfirmed Candidate Species, three Uncategorized Lineages, and four Confirmed Candidate Species and described herein. We also propose a phylogenetic hypothesis for the genus and discuss its implications for historical biogeography of this Amazonian group.",

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AU - Melo-Sampaio, Paulo R.

AU - Chaparro, Juan C.

AU - Vogt, Richard C.

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AU - Pinheiro, Leandra Cardoso

AU - Avila, Robson W.

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AB - Amphibians are probably the most vulnerable group to climate change and climatechange associate diseases. This ongoing biodiversity crisis makes it thus imperative to improve the taxonomy of anurans in biodiverse but understudied areas such as Amazonia. In this study, we applied robust integrative taxonomic methods combining genetic (mitochondrial 16S, 12S and COI genes), morphological and environmental data to delimit species of the genus Amazophrynella (Anura: Bufonidae) sampled from throughout their pan-Amazonian distribution. Our study confirms the hypothesis that the species diversity of the genus is grossly underestimated. Our analyses suggest the existence of eighteen linages of which seven are nominal species, three Deep Conspecific Lineages, one Unconfirmed Candidate Species, three Uncategorized Lineages, and four Confirmed Candidate Species and described herein. We also propose a phylogenetic hypothesis for the genus and discuss its implications for historical biogeography of this Amazonian group.

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ER -

A Pan-Amazonian species delimitation: High species diversity within the genus Amazophrynella (Anura: Bufonidae)

Abstract

Bibliographical note

Funding

Keywords

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