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On the Uncertain Taxonomic Identity of Adenomera Hylaedactyla (Cope, 1868) and the Composite Type Series of A

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On the Uncertain Taxonomic Identity of Adenomera Hylaedactyla (Cope, 1868) and the Composite Type Series of A Copeia 107, No. 4, 2019, 708–723 On the Uncertain Taxonomic Identity of Adenomera hylaedactyla (Cope, 1868) and the Composite Type Series of A. andreae (Muller,¨ 1923) (Anura, Leptodactylidae) Thiago R. de Carvalho1, Ariovaldo A. Giaretta2, Natan M. Maciel3, Diego A. Barrera4,Cesar´ Aguilar-Puntriano4,5,Celio´ F. B. Haddad1, Marcelo N. C. Kokubum6, Marcelo Menin7, and Ariadne Angulo4,5 Adenomera andreae and A. hylaedactyla are two widespread Amazonian frogs that have been traditionally distinguished from each other by the use of different habitats, toe tip development, and more recently through advertisement calls. Yet, taxonomic identification of these species has always been challenging. Herein we undertake a review of type specimens and include new phenotypic (morphology and vocalization) and mitochondrial DNA information for an updated diagnosis of both species. Our morphological analysis indicates that the single type (holotype) of A. hylaedactyla could either belong to lineages associated with Amazonian forest-dwelling species (A. andreae clade) or to the open-formation morphotype (A. hylaedactyla clade). Given the holotype’s poor preservation, leading to the ambiguous assignment of character states for toe tip development, as well as a vague type locality encompassing a vast area in eastern Ecuador and northern Peru, the identity of this specimen is uncertain. Morphology of toe tip fragments and the original species description suggest that A. hylaedactyla could correspond to at least two described species (A. andreae or A. simonstuarti) or additional unnamed genetic lineages of the A. andreae clade, all bearing toe tips expanded into discs. Analysis of morphometric data, however, clustered the holotype with the Amazonian open-formation morphotype (toe tips unexpanded). While additional data can be obtained from the holotype of A. hylaedactyla, at this time this type cannot be unequivocally assigned to any species of Adenomera distributed across eastern Ecuador and Peru’s northernmost region of Loreto. For the time being, the name A. hylaedactyla still accommodates the only Amazonian open-habitat species. As to the type series of Adenomera andreae, a forest-associated species with toe tips fully expanded (developed into small discs) from eastern Brazilian Amazonia, we found that one of its paratypes shares a morphotype with the open-habitat species and is reassigned to A. hylaedactyla. With the taxonomic identity of A. hylaedactyla unresolved, formal descriptions of cryptic species complexes within the A. andreae clade distributed across the type locality of A. hylaedactyla run the risk of a possible future synonymization with A. hylaedactyla. Yet, not naming more circumscribed and potentially threatened cryptic species puts them at risk, as they would probably not qualify for conservation funding. Given the current fire crisis in the Amazon Basin, the risk of losing species before they are described far outweighs the risk of synonymization. We recommend that researchers prioritize descriptions based on the potential extinction risk of new species. Adenomera andreae y A. hylaedactyla son dos especies de ranas amazonicas´ con una amplia distribucion´ que han sido tradicionalmente diferenciadas una de otra por el uso de diferentes ha´bitats, desarrollo de los d´ıgitos posteriores y ma´s recientemente a traves´ de sus cantos de anuncio. Sin embargo, la identificacion´ taxonomica´ de estas especies siempre ha sido dif´ıcil. Realizamos una revision´ del material tipo e incluimos nuevas informaciones fenot´ıpicas (morfolog´ıa y vocalizaciones) y de secuencias de ADN mitocondrial para sus diagnosticos´ actualizados. Nuestro ana´lisis morfologico´ indica que el tipo unico´ (holotipo) de A. hylaedactyla podr´ıa pertenecer a linajes asociados con especies de la selva amazonica´ (A. andreae clade) o al morfotipo de formacion´ abierta (A. hylaedactyla clade). Dada la pobre preservacion´ del holotipo, lo que lleva a la asignacion´ ambigua de estados de caracteres para el desarrollo de la punta del dedo del pie, as´ı como a una localidad tipo vaga que abarca una vasta a´rea en el este de Ecuador y el norte de Peru,´ la identidad de este especimen´ es incierta. La morfolog´ıa de los fragmentos de la punta del dedo del pie y la descripcion´ original de la especie sugieren que A. hylaedactyla podr´ıa corresponder al menos a dos especies descritas (A. andreae, A. simonstuarti)o linajes geneticos´ adicionales sin nombre del clado de A. andreae, todos con puntas de los pies expandidas en discos. Sin embargo, el ana´lisis de los datos morfometricos´ agrupo´ el holotipo con el morfotipo amazonico´ de formacion´ abierta (puntas de los dedos no expandidas). Si bien se pueden obtener datos adicionales del holotipo de A. hylaedactyla, en este momento este tipo no se puede asignar inequ´ıvocamente a ninguna especie de Adenomera distribuida en el este de Ecuador y la region´ ma´s al norte de Loreto en Peru.´ Por el momento, el nombre A. hylaedactyla todav´ıa alberga la unica´ especie de ha´bitat abierto de la Amazon´ıa. En cuanto a la serie tipo de A. andreae, una especie asociada al bosque con 1 Laboratorio´ de Herpetologia, Departamento de Zoologia e Centro de Aquicultura, Universidade Estadual Paulista (UNESP), Rio Claro 13506- 900, Sa˜o Paulo, Brazil; Email: (TRC) [email protected]; and (CFBH) [email protected]. Send reprint requests to TRC. 2 Laboratorio´ de Taxonomia e Sistema´tica de Anuros Neotropicais, Faculdade de Cienciasˆ Integradas do Pontal, Universidade Federal de Uberlaˆndia, Ituiutaba, Minas Gerais, Brazil; Email: [email protected]. 3 Laboratorio´ de Herpetologia e Comportamento Animal, Instituto de Cienciasˆ Biologicas,´ Universidade Federal de Goia´s, Campus Samambaia, Goiaˆnia, Goia´s, Brazil; Email: [email protected]. 4 Departamento de Herpetolog´ıa, Museo de Historia Natural de San Marcos (MUSM), Lima, Peru; Email: (DAB) [email protected]; and (CAP) [email protected]. 5 UCN SSC Amphibian Specialist Group, Toronto, Canada; Email: (AA) [email protected]. 6 Laboratorio´ de Herpetologia, Unidade Academicaˆ de Cienciasˆ Biologicas,´ Centro de Saude´ e Tecnologia Rural, Universidade Federal de Campina Grande, Patos, Para´ıba, Brazil; Email: [email protected]. 7 Laboratorio´ de Taxonomia e Ecologia de Anf´ıbios e Repteis´ and Programa de Pos-Gradua¸´ ca˜o em Zoologia, Instituto de Cienciasˆ Biologicas,´ Universidade Federal do Amazonas, Manaus, Amazonas, Brazil; Email: [email protected]. Submitted: 21 May 2019. Accepted: 1 October 2019. Associate Editor: B. Stuart. Ó 2019 by the American Society of Ichthyologists and Herpetologists DOI: 10.1643/CH-19-237 Published online: 22 November 2019 de Carvalho et al.—On the type specimens of Amazonian Adenomera 709 puntas de los dedos completamente expandidas (desarrolladas en pequenos˜ discos) desde el este de la Amazon´ıa brasilena,˜ descubrimos que uno de sus paratipos comparte un morfotipo con la especie de ha´bitat abierto y es reasignado a A. hylaedactyla. Con la identidad taxonomica´ de A. hylaedactyla sin resolver, las descripciones formales de los complejos de especies cr´ıpticas dentro del clado de A. andreae distribuidos en la localidad tipo de A. hylaedactyla corren el riesgo de una posible sinonimizacion´ futura con A. hylaedactyla. Sin embargo, no nombrar especies cr´ıpticas ma´s circunscritas y potencialmente amenazadas las pone en riesgo, ya que probablemente no calificar´ıan para fondos de conservacion.´ Dada la actual crisis de incendios en la cuenca del Amazonas, el riesgo de perder especies antes de que se describan supera con creces el riesgo de sinonimizacion.´ Recomendamos que los investigadores prioricen las descripciones basadas en el riesgo potencial de extincion´ de nuevas especies. DENOMERA andreae (Muller,¨ 1923) and A. hylaedac- recorded and collected A. andreae from two other localities tyla (Cope, 1868) are two leptodactylid frog species in eastern Brazilian Amazonia, state of Para´ (Belem:´ A with widespread distributions in Amazonia; the latter 1.4497608S, 48.4443518W; and Santa Ba´rbara do Para´: is also distributed throughout the Cerrado savanna region 1.1930568S, 48.2694448W), as well as from other Amazonian and northern Atlantic Forest in Brazil (Heyer, 1973; Fouquet regions in Brazil (Manaus, state of Amazonas: 3.0919648S, et al., 2014). These species are usually distinguished by their 59.9712348W; and Serra do Navio, state of Amapa´: morphology and the use of different habitats: forests (A. 0.8958708N, 52.0009208W) and Peru (Tambopata National andreae) and open formations (A. hylaedactyla; Heyer, 1973, Reserve, Region of Madre de Dios: 12.8359308S, 1977, 1984). Since its description, the vocalization of A. 69.2728708W). Localities are mapped in Figure 1. andreae has been described from different Amazonian regions We recorded and collected A. hylaedactyla from many (e.g., Zimmerman and Bogart, 1984; Boistel et al., 2006). On regions throughout South America, but only specimens and the other hand, acoustic data and DNA sequences remain associated sound recordings from the following localities in unknown for the type locality, originally designated as the Brazilian and Peruvian Amazonia were included in this ‘‘Peixeboi (a. d. Bragan¸cabahn), Staat Para`, Brasilien’’ by study (Fig. 1): Brazil (state of Roraima, Canta´: 2.7665318N, Muller¨ (1923). The exact type locality was a railway station, 60.6089288W; state of Amazonas: Sa˜o Gabriel da Cachoeira: the ‘‘Esta¸ca˜o de Bragan¸ca,’’ which was located in the small
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