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Taxonomic Assessment of Craugastor Podiciferus (Anura: Craugastoridae)

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Taxonomic Assessment of Craugastor Podiciferus (Anura: Craugastoridae) Offcial journal website: Amphibian & Reptile Conservation amphibian-reptile-conservation.org 13(1) [General Section]: 173–197 (e176). urn:lsid:zoobank.org:pub:0AB829CA-DAFF-4EE9-B7D7-FBC037B4B2B0 Taxonomic assessment of Craugastor podiciferus (Anura: Craugastoridae) in lower Central America with the description of two new species 1,2,3Erick Arias, 4,5Andreas Hertz, and 1,*Gabriela Parra-Olea 1Departamento de Zoología, Instituto de Biología, UNAM, AP 70-153 Ciudad Universitaria, CP 04510, Ciudad de México, MÉXICO 2Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Av. Ciudad Universitaria 3000, C.P. 04360, Coyoacán, Ciudad de México, MÉXICO 3Escuela de Biología, Universidad de Costa Rica, San Pedro, 11501-2060 San José, COSTA RICA 4Department of Biology, University of Massachusetts Boston, 100 Morrissey Blvd., Boston, MA 02125, USA 5Senckenberg Forschungsinstitut und Naturmuseum, Senckenberganlage 25, 60325, Frankfurt am Main, GERMANY Abstract.—The systematics and taxonomy of polytypic species Craugastor podiciferus are poorly understood due to the high level of phenotypic polymorphism between and within species and the lack of molecular data from topotypic specimens. Herein are reported results of a well-sampled study including all known species of the C. podiciferus species group, several localities from highlands in Costa Rica and western Panama, and for the frst time, samples from the type locality of C. podiciferus. A phylogenetic analysis based on the DNA sequences of the mitochondrial 16S rRNA (16S) and cytochrome oxidase 1 (COI) genes and a morphometric analysis are also included. Based on the results, we restrict C. podiciferus to the populations from the Cordillera Volcánica Central and Cordillera de Talamanca in Costa Rica and western Panama. Craugastor podiciferus sensu stricto and six additional clades from the highlands of Costa Rica constitute the well-supported C. podiciferus sensu lato clade. These analyses support the existence of three additional species from the Pacifc slope of southwestern Costa Rica and western Panama. Herein, two lineages are described as new species and revised descriptions for C. podiciferus and C. blairi are provided. The name C. blairi is resurrected and used for populations from the Cordillera de Talamanca and Cordillera Central in western Panama. Two additional species are named. One is easily differentiated by the presence of nuptial pads in adult males, a smooth venter, and fat subarticular tubercles. The other, named for populations from southwestern Costa Rica, is recognized by its coarsely areolate venter, projecting subarticular tubercles, and heel without a projecting tubercle. The recognition of these three species from the lower montane rainforest highlights the role of the highlands on the Pacifc slope of Costa Rica and Panama in the diversifcation of the C. podiciferus species group. Keywords. Brachycephaloidea, cryptic species, DNA barcoding, Talamanca, Terrarana, Costa Rica, Panama Citation: Arias E, Hertz A, Parra-Olea G. 2019. Taxonomic assessment of Craugastor podiciferus (Anura: Craugastoridae) in lower Central America with the description of two new species. Amphibian & Reptile Conservation 13(1): [General Section]: 173–197 (e176). Copyright: © 2019 Arias et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. The offcial and authorized publication credit sources, which will be duly enforced, are as follows: offcial journal title Amphibian & Reptile Conservation; offcial journal website: amphibian-reptile-conservation.org. Received: 18 January 2019; Accepted: 4 April 2019; Published: 13 May 2019 Introduction podiciferus species group is diffcult due to the extremely conserved morphological characters and the high level The direct-developing frogs of the Craugastor podic- of phenotypic polymorphism within species and popu- iferus species group (Hedges et al. 2008) are found from lations. The systematics and taxonomy of the C. podic- eastern Honduras to Central Panama (AmphibiaWeb iferus species group has been poorly studied; however, 2019; Savage 2002) with most of the species (nine out of previous molecular studies have suggested the existence ten) restricted to Isthmian Central America. The distribu- of several unnamed species that are masked under the tion of this group ranges from sea level to 2,700 m a.s.l. current names (Savage 2002; Crawford 2003; Crawford in a wide variety of habitats, from tropical rain forest and Smith 2005; Streicher et al. 2009). For example, and cloud forest, to montane forest (Savage 2002). The Crawford and Smith (2005) examined 10 samples (seven morphological delimitation between members of the C. species) of the C. podiciferus species group and found Correspondence. 1 [email protected] (corresponding author); 1,2,3 [email protected]; 4,5 [email protected] Amphib. Reptile Conserv. 173 May 2019 | Volume 13 | Number 1 | e176 Arias et al. the presence of two unnamed species (Craugastor sp. B Materials and Methods and Craugastor sp. C); they also found C. stejnegerianus (Cope, 1893) to be paraphyletic. Recently, Arias et al. Species criterion: The general metapopulation lineage (2016) showed that populations formerly considered to species concept is followed here (Simpson 1951; Wiley be part of the C. stejnegerianus from southwestern Costa 1978; de Queiroz 2007). Consistent with this concept, a Rica and western Panama belonged to a different species species is recognized when there is evidence of metapopu- and described them as C. gabbi Arias, Chaves, Crawford, lation lineage separation, preferably based on multiple and Parra-Olea, 2016. lines of evidence following a consensus protocol for inte- Craugastor podiciferus (Cope, 1875) is the most com- grative taxonomy (Dayrat 2005; Padial et al. 2010). plicated taxon within the C. podiciferus species group. Its morphological polymorphism has been recognized since Taxon sampling: The frogs were collected in the feld, eu- its description by Cope (1875), who described it based on thanized, fxed in 10% formalin, and processed in 70% eth- four varieties plus two additional species (C. muricinus anol for long-term storage. A tissue sample was preserved and C. habenatus) in the same paper, with specimens from in 96% ethanol or RNAlater and used for genetic analysis. the same locality. In addition, Cope (1875) stated that “the Museum collection acronyms follow Frost (2019) with the colors of this species vary remarkably, more than I have addition of AH for Andreas Hertz feld numbers, EAP for observed to be the case in any other frog.” Subsequently, Erick Arias feld numbers, and CRARC for the Costa Rica Barbour (1928) described C. blairi using specimens from Amphibian Research Center private collection. western Panama, which Taylor (1952) later synonymized Amplifcation and sequencing: Partial sequences of the together with C. muricinus and C. habenatus under C. large subunit ribosomal RNA (16S) mitochondrial gene podiciferus. An additional species, C. jota (Lynch 1980), were determined for six specimens of Craugastor sp. 1 was named using specimens from western Panama, and (Arias et al. 2018), Craugastor sp. 2 (Arias et al. 2018), was suggested to be related to C. podiciferus. More re- and Craugastor sp. B (Crawford and Smith 2005) from cently, the name C. podiciferus has been used for speci- the Pacifc slopes of southwestern Costa Rica and west- mens from several highland populations (1,089–2,650 m ern Panama (Fig. 1). The sequences obtained herein were a.s.l.) on both slopes of the mountain ranges in Costa Rica compared with those available in GenBank for the C. and western Panama (Savage 2002). Streicher et al. (2009) podiciferus species group. The protocols for DNA extrac- used specimens from several populations referred to as C. tion, amplifcation, sequencing, and editing follow those podiciferus to perform a well-sampled phylogenetic study of Arias et al. (2018). The list of vouchers and GenBank of this complex. They found C. podiciferus is represented accession numbers used in this study are provided in Ap- by six clades, each likely representing distinct species. pendix I. In addition, the populations from western Panama were not grouped with the main C. podiciferus clade, but were Phylogenetic analyses: Sequence alignments used the called Craugastor sp. B. MAFFT software (Katoh et al. 2017) under the “auto” Although the molecular and geographical evidence strategy and default parameters, and were trimmed to shown by Streicher et al. (2009) supported the presence of the point where a majority of the taxa had sequence several species under the name C. podiciferus, taxonomic data. The sequence data were partitioned by gene, and changes have not yet been implemented, mainly due to the the COI data were further partitioned by codon posi- lack of topotypic specimens of C. podiciferus. The correct tion. PartitionFinder v1.1.1 (Lanfear et al. 2012) and type locality has been discussed by Savage (1970), and the Bayesian information criterion (BIC) were used to Arias and Chaves (2014) concluded it is on the Caribbean select both the best partition scheme and the best mod- slopes of Cerro Kamuk. el of sequence evolution for each partition. A single Here, specimens of Craugastor podiciferus from
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