Zootaxa 4238 (2): 268–274 ISSN 1175-5326 (print edition) http://www.mapress.com/j/zt/ Correspondence ZOOTAXA Copyright © 2017 Magnolia Press ISSN 1175-5334 (online edition) https://doi.org/10.11646/zootaxa.4238.2.8 http://zoobank.org/urn:lsid:zoobank.org:pub:3404BFA9-4297-4408-8DF2-03CB0A9E9CE3 Out of Amazonia: the unexpected trans-Andean distribution of resplendens (Lynch and Duellman, 1978) (Anura: Centrolenidae)

CLAUDIA MOLINA-ZULUAGA1, ESTEFANY CANO1, ADRIANA RESTREPO1, MARCO RADA2 & JUAN M. DAZA1,3 1Grupo Herpetológico de Antioquia, Instituto de Biología, Universidad de Antioquia, A.A. 1226, Medellín, 2Departamento de Zoologia, Instituto de Biociências; Universidade de São Paulo, Rua do Matão, trav. 14, 321, Cidade Universitária, 05508-090 São Paulo, Brazil 3Corresponding author. E-mail: [email protected]

The glassfrog Cochranella, with nine recognized , is distributed in the lowlands and mid elevation of the Neotropical forests, from Nicaragua to Bolivia (Guayasamin et al. 2009; Twomey et al. 2014). Four species are trans- Andean—C. granulosa (Taylor 1949) occurs in the lowlands and mountains, at mid elevation, of Central America, C. litoralis (Ruiz-Carranza & Lynch 1996) and C. mache Guayasamin & Bonaccorso 2004 occur in the Pacific lowlands and the western cloud forests of Colombia and Ecuador, and C. euknemos (Savage & Starrett 1967) occurs both in Central America and South America (northwestern Colombia).—The other five species have cis-Andean distributions in the Amazonian slopes and lowlands, from Colombia to Bolivia: C. nola Harvey 1996, C. guayasamini Twomey, Delia & Castroviejo-Fisher 2014, C. resplendens (Lynch & Duellman 1973), C. erminea Torres-Gastello, Suárez-Segovia & Cisneros-Heredia 2007, and C. phryxa Aguayo-Vedia & Harvey 2006. In Colombia, C. resplendens is known from the foothills of the Amazon versant in Caquetá (Malambo et al. 2013) and Putumayo (Lynch & Duellman 1973; Ruiz- Carranza et al. 1996). The species is also known from Ecuador (Lynch & Duellman 1973) and Peru (Twomey et al. 2014). Here, we report two new records of , extending the species distribution beyond the Amazonian lowlands into the northern Cordillera Central in Colombia. During recent fieldwork on the eastern versant of the northern Cordillera Central in the Department of Antioquia, we found two specimens that we assigned to Cochranella resplendens. The first record corresponds to an adult female (MHUA-A 9140; Fig. 1A) collected on June 13, 2015 at Finca El Chaquiral, vereda El Retiro, municipality of Anorí, Department of Antioquia (6°58’56.06”N, 75°7’48.72” W, 1699 m). The specimen was found at night, on a bush leaf next to a 2 meter-wide stream inside a regrowth forest. The second record, an adult male (MHUA-A 9540; Fig. 1B) was collected on August 27, 2015 at El Eden, vereda San Antonio, municipality of Alejandría, department of Antioquia (6°22’2.1” N, 75°1’38.03” W, 1309 m). The individual was captured during the day inside a mature secondary forest after falling from a tree next to a stream. Both localities correspond to Premontane Perhumid Forest life zone (Holdridge 1987). These records extend northward the species known distribution to the trans-andean region approximately 618 km north from its nearest published locality in Belén de los Andaquíes, departament of Caquetá (Malambo et al. 2013; Fig. 2). Cochranella resplendes is a rare species in herpetological collections. Because the unusual distribution of the specimens reported herein (i.e., outside the Amazon basin), and the high similarity among some other species (i.e C. mache, C. euknemos and C. phryxa), we present more information regarding how the specimens were identified as C. resplendens. We used molecular and morphological evidence to allocate the two specimens to C. resplendens. We sequenced a mitochondrial fragment corresponding to the 16S region following the protocols described in Guayasamin et al. (2008b). Sequence alignment was conducted using MAFFT under default parameters (Katoh 2013). We inferred a 16S gene tree using Maximum Likelihood using the TIM2+G+I model (Figure 3). Model of nucleotide evolution and phylogeny were estimated using the program IQ-TREE (Nguyen et al. 2015). Nodal support was estimated using the ultrafast bootstrap method implemented in IQ-TREE (Minh et al., 2013). Included taxa are shown in Table 1. Using Mega 7 (Tamura et al. 2013) we estimated uncorrected genetic distances between species in Cochranella (Table 2). The phylogenetic hypothesis and the genetic distances show that the two specimens can be unambiguously assigned to C. resplendens. A remarkable finding is that the sample of C. resplendens from the Amazon versant in Ecuador and the ones from the Central Andes in Colombia show very little genetic variation (0.4 %; Table 2), despite being located in two different biogeographic areas (Fig. 2).

268 Accepted by S. Castroviejo-Fisher: 6 Jan. 2017; published: 3 Mar. 2017 TABLE 1. Taxa and Genbank accession numbers included in the phylogenetic analysis.

Species Voucher Genbank accesion number Cochranella erminea CORBIDI 10477 KM068264 Cochranella erminea MHNC 13932 KM068258 Cochranella erminea MHNC 7247 KF534360 Cochranella erminea MNCN 45949 KM068257 AJC 1687 KR863138 Cochranella euknemos AJC 1688 KR863137 Cochranella euknemos AJC 1850 KR863135 Cochranella euknemos CH5109 EU663008 Cochranella euknemos CH 6423 KR863136 Cochranella euknemos CH 6440 KR863139 Cochranella euknemos CH 6696 KR863141 Cochranella euknemos CH 6766 KR863134 Cochranella euknemos CH 6864 KR863140 Cochranella euknemos KRL 0803 FJ784377 Cochranella euknemos KRL 0841 FJ784396 Cochranella euknemos KRL 0937 FJ784443 Cochranella euknemos KRL 1054 FJ784458 Cochranella euknemos KRL 1055 FJ784459 KRL 1011 FJ784455 Cochranella granulosa USNM 559082 EU663010 Cochranella guayasamini CORBIDI 8956 KM068265 Cochranella guayasamini MHNC 13930 KM068259 Cochranella litoralis QCAZ 27693 EU662990 QCAZ 27747 EU663013 Cochranella nola CBG 814 EU663015 Cochranella nola CBG 1094 EU663016 Cochranella resplendens MHUAA 9140 KY347026 Cochranella resplendens MHUAA 9540 KY347027 Cochranella resplendens QCAZ 38088 KF534361 Cochranella sp. 1 AJC 2718 KF534362 Cochranella sp. CBG 1096 EU663021 Espadarana prosoblepon UCR 17102 EU662995

Both specimens referred to here as Cochranella resplendens exhibited the diagnostic characteristics described by Lynch & Duellman (1973): i) white parietal and visceral peritonea; ii) color in life green to dark green with white to bluish-green flecks; iii) round snout in dorsal view and gradually inclined anteroventrally in lateral view; iv) extensive webbing between outer fingers; v) dorsal skin shagreened with elevated warts corresponding to flecks; vi) crenulated dermal fold on the outer edge of hands, forearms, and elbows, on heels, tarsi, and feet; vii) pigmented nuptial excrescence, Type I; concealed prepollex; viii) humeral spines in adult males absent (crista ventralis not protruding); ix) cloacal ornamentation composed of enameled tubercules, folds, and crenulated flaps. Within the genus, the only species that lack humeral spines and have inclined snouts in lateral view are Cochranella euknemos (Savage & Starrett 1967), C. mache (Guayasamin & Bonaccorso 2004), and C. phryxa (Aguayo-Vedia & Harvey 2006). However, C. resplendens is distinguished by having well crenulated folds on hands, ulnae, tarsi and feet (Fig. 1A, C; less crenulated fold in C. euknemos; Fig. 1D), color in life green to dark green with white to bluish-green flecks (green or bluish-green dorsum with yellow flecks in C. euknemos and C. mache), well defined and visible tympanum (Fig. 1A, C; not visible externally in C. phryxa), and lacking a large dull yellow-colored patch on the top of the head (present in C. mache).

COCHRANELLA RESPLENDENS Zootaxa 4238 (2) © 2017 Magnolia Press · 269 TABLE 2. Percentage of uncorrected genetic distances among Cochranella species based on DNA sequences of a 864 bp fragment of the mitochondrial gene 16S. Bold numbers in the diagonal indicate intraspecific genetic variation, interspecific genetic distances are shown below and above the diagonal, mean and range, respectively. Taxon sampling shown in Figure 3.

12345 1 erminea 2.8 0.4–5.5 3.5–5.0 3.7–4.4 5.9–6.2 2 euknemos 4.6 1.1 3.5–4.8 3.7–4.5 5.6–6.0 3 granulosa 4.3 4.3 0.2 3.3–4.3 4.5–5.2 4 guayasamini 4.1 4.0 3.6 0.0 5.1–5.6 5 litoralis 6.1 5.8 4.9 5.4 --- 6 mache 4.3 2.8 4.1 3.6 5.9 7 nola 6.1 5.2 5.4 5.1 5.5 8 resplendens 4.8 5.5 3.6 4.9 5.7 9 AJC2718 3.8 4.7 3.8 2.0 6.0 10 CBG1096 6.1 5.8 5.4 5.9 5.5 continued.

678910 1 erminea 4.1–4.5 5.6–6.6 4.4–5.2 3.5–4.0 5.4–6.5 2 euknemos 2.5–2.9 4.8–5.3 4.5–5.9 4.3–5.2 5.2–6.1 3 granulosa 3.8–4.4 4.8–6.0 3.2–4.1 3.2–4.4 5.3–5.5 4 guayasamini 3.5–3.8 4.8–5.5 4.7–5.4 1.8–2.2 5.9–5.9 5 litoralis --- 5.4–5.5 5.5–5.8 ------6 mache --- 5.1–5.3 4.3–4.8 ------7 nola 5.2 0.4 5.3–6.3 5.9–6.0 2.9–3.0 8 resplendens 4.5 5.7 0.4 4.8–5.5 5.8–6.3 9 AJC2718 4.6 5.9 5.1 ------10 CBG1096 4.9 2.9 6.0 6.2 ---

For decades, the fauna from the eastern side of the Andes has been considered very distinct from the trans- Andean region (Duellman 1979). Few examples of species inhabiting both sides of the Andes (mid to high elevations, including internal valleys in Colombia) are: buckleyi (Ruiz-Carranza et al. 1996; Guayasamin 2010; both sides of the Andes and internal valleys), posadae (Guayasamin et al. 2006; western slope of Cordillera Central in Huila and Caldas departments and Amazonian versant of the Andes), “Centrolene” medemi (Suárez-Mayorga 1999; western and eastern slopes on the Cordillera Oriental and Cordillera Central in Caquetá and Tolima departments), Centrolene geckoideum (Bolivar et al. 2004; both sides of the Andes and internal valleys), Pristimantis w-nigrum (Castro et al. 2010b; both sides of the Andes and internal valleys), and Pristimantis petersi (Guayasamin et al. 2008a; Castro et al. 2010a; eastern slope of the Cordillera Oriental in Caquetá and Putumayo departments and western slope of Cordillera Central in Huila department). Here, we report an unusual finding of a glassfrog species previously known only from the lowlands of the Amazon basin. It is relevant that the new record increases the elevation limit for the species more than 1200 meters. Considered as a lowland species in the Amazon basin, the trans-Andean records correspond to Andean habitat. These findings also highlight the need for a thorough taxonomic revision and the validity of C. phryxa, a species very similar to C. resplendens and described from a single specimen from Bolivia (Aguayo-Vedia & Harvey 2006). Lastly, recent biogeographic studies of centrolenids (Hutter et al. 2013; Castroviejo-Fisher et al. 2014) have focused their questions at the family level but questions regarding historical demography and phylogeographic patterns in single species are lacking. Due to its unique geographic distribution, C. resplendens has potential as a model to understand how natural populations can maintain gene flow despite large geographic distances and separated by different biogeographic provinces.

270 · Zootaxa 4238 (2) © 2017 Magnolia Press MOLINA-ZULUAGA ET AL. FIGURE 1. (A) Cochranella resplendens MHUAA 9140, Anorí, Antioquia, Colombia, Photo by J.M. Daza. (B) Cochranella resplendens MHUAA 9540, Alejandría, Antioquia, Colombia, Photo by Hernán Martínez. (C) Cochranella resplendens unpreserved voucher, Florencia, Caquetá, Colombia, Photo by Caroline Molina. (D) Cochranella euknemos AJC 1687, Darién, Panamá, Photo by A.J. Crawford.

Acknowledgements Specimen collection was conducted under permit No. 112–0046 granted by the Corporación Autónoma Regional CORNARE and the ANLA under Auto 186 of January 28 of 2014. Caroline Molina kindly provided a photograph of Cochranella resplendens (voucher to be deposited at Universidad del Quindío—Herpetología-UQ). This study was funded by Isagen and the Universidad de Antioquia under contract 47/574. Author contributions: CMZ, AR, EC and JMD conducted fieldwork. MR and JMD confirmed the identification. JMD and AR conducted the molecular analysis. CMZ, MR and JMD wrote the text.

COCHRANELLA RESPLENDENS Zootaxa 4238 (2) © 2017 Magnolia Press · 271 FIGURE 2. Geographical distribution of Cochranella resplendens, indicating in green the two new records in northern Colombia.

272 · Zootaxa 4238 (2) © 2017 Magnolia Press MOLINA-ZULUAGA ET AL. FIGURE 3. Maximum Likelihood tree inferred from up to 864 bp of 16S. Numbers on nodes indicate branch support using the ultrafast bootstrap (see main text for details).

References Aguayo-Vedia, C.R. & Harvey, M.B. (2006) A new glassfrog of the Cochranella granulosa group (Anura: Centrolenidae) from a Bolivian cloud forest. Herpetologica, 62, 323–330. https://doi.org/10.1655/0018-0831(2006)62[323:ANGOTC]2.0.CO;2 Bolivar, W., Coloma, L.A., Ron, S.,Cisneros-Heredia, D., Wild, E. & Yánez-Muñoz, M. (2004) Centrolene geckoideum. The IUCN Red List of Threatened Species 2004: e.T54911A11221686. https://doi.org/10.2305/IUCN.UK.2004.RLTS.T54911A11221686.en Castro, F., Herrera, M.I., Coloma, L.A., Ron, S., Lynch, J.D., Almeida, D. & Nogales, F. (2010a) Pristimantis petersi. The IUCN Red List of Threatened Species 2004: e.T56849A11544869. https://doi.org/10.2305/IUCN.UK.2010-2.RLTS.T56849A11544869.en Castro, F., Herrera, M.I., Coloma, L.A., Ron, S., Lynch, J.D., Cisneros-Heredia, D. & Yánez-Muñoz, M. (2010b). Pristimantis w- nigrum. The IUCN Red List of Threatened Species 2010: e.T57057A11575834. https://doi.org/10.2305/IUCN.UK.2010-2.RLTS.T57057A11575834.en Castroviejo-Fisher, S., Guayasamin, J.M., Gonzalez-Voyer, A. & Vilà, C. (2014) Neotropical diversification seen through glassfrogs. Journal of Biogeography, 41, 66–80. https://doi.org/10.1111/jbi.12208 Duellman, W.E. (1979) The South American herpetofauna: its origin, evolution, and dispersal. Monograph of the Museum of Natural History, the University of Kansas. No. 7. Museum of Natural History, University of Kansas, Lawrence, Kan, 485 pp. https://doi.org/10.5962/bhl.title.3207 Guayasamin, J.M. (2010) Centrolene buckleyi. The IUCN Red List of Threatened Species 2010: e.T54908A11220443. https://doi.org/10.2305/IUCN.UK.2010-2.RLTS.T54908A11220443.en Guayasamin, J.M. & Bonaccorso, E. (2004) A new species of glassfrog (Centrolenidae: Cochranella) from the lowland of the northwestern Ecuador, with comments on the Cochranella granulosa group. Herpetologica, 60, 485–494. https://doi.org/10.1655/03-64 Guayasamin, J.M., Bustamante, M.R., Almeida-Reinoso, D. & Funk, W.C. (2006) Glass (Centrolenidae) of Yanayacu Biological

COCHRANELLA RESPLENDENS Zootaxa 4238 (2) © 2017 Magnolia Press · 273 Station, Ecuador, with the description of a new species and comments on centrolenid systematics. Zoological Journal of the Linnean Society, 147, 489–513. https://doi.org/10.1111/j.1096-3642.2006.00223.x Guayasamin, J.M., Cisneros-Heredia, D.F. & Castroviejo-Fisher, S. (2008a) Taxonomic identity of Cochranella petersi Goin, 1961 and Centrolenella ametarsia Flores, 1987. Zootaxa, 1815, 25–34. Guayasamin, J.M., Castroviejo-Fisher, S., Ayarzagüena, J., Trueb, L. & Vilá, C. (2008b) Phylogenetic relationship of glassfrogs (Centrolenidae) based on mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution, 48, 574–595. https://doi.org/10.1016/j.ympev.2008.04.012 Guayasamin, J.M., Castroviejo-Fisher, S., Trueb, L., Ayarzagüena, J. Rada, M. & Vilá, C. (2009) Phylogenetic systematics of glassfrogs (Amphibia: Centrolenidae) and their sister taxon Allophryne ruthveni. Zootaxa, 2100, 1–97. Harvey, M.B. (1996) A new species of (Anura: Centrolenidae: Cochranella) from Bolivia, and the taxonomic status of Cochranella flavidigitata. Herpetologica, 52, 427–435. Holdridge, L. (1987) Ecología basada en zonas de vida. Instituto Interamericano de cooperación para la agricultura, San José, Costa Rica, 261p. Hutter, C.R., Guayasamin, J.M. & Wiens, J.J. (2013) Explaining Andean megadiversity: the evolutionary and ecological causes of glassfrog elevational richness patterns. Ecology Letters, 16, 1135–1144. https://doi.org/10.1111/ele.12148 Katoh, S. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. https://doi.org/10.1093/molbev/mst010 Lynch, J.D. & Duellman. W.E. (1973) A review of the Centrolenid frogs of Ecuador, with description of new species. Occasional Papers of the Museum of Natural History of the University of Kansas, 16, 1–66. Malambo, C., González-Ibarra, J.F. & Gómez-Polania, Y.C. (2013) Amphibia, Anura, Centrolenidae midas (Lynch and Duellman, 1973) and Cochranella resplendens (Lynch and Duellman, 1973): First and second record respectively for Colombia. Check List, 9, 894–896. https://doi.org/10.15560/9.4.894 Minh, B.Q., Nguyen, M.A.T. & von Haeseler, A. (2013) Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution, 30, 1188–1195. https://doi.org/10.1093/molbev/mst024 Nguyen, L.T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274. https://doi.org/10.1093/molbev/msu300 Ruiz-Carranza, P.M., Ardila-Robayo, M.C. & Lynch, J.D. (1996) Lista actualizada de la fauna de Amphibia de Colombia. Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, 20 (77), 365–415. Ruiz-Carranza, P.M. & Lynch, J.D. (1996) Ranas centrolenidos de Colombia. IX. Dos nuevas especies del suroeste de Colombia. Lozania, 68, 1–11. Savage, J.M. & Starrett, P.H. (1967) A new fringe-limbed tree-frog (family Centrolenidae) from lower Central America. Copeia, 1967, 604–609. https://doi.org/10.2307/1442239 Suárez-Mayorga, A.M. (1999) Lista preliminar de la fauna amphibia presente en el transecto La Montañita - Alto de Gabinete, Caquetá, Colombia. Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, 23, 395–405. Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725–2729. https://doi.org/10.1093/molbev/mst197 Taylor, E.H. (1949) Costa Rican frogs of the genera Centrolene and Centrolenella. University of Kansas Science Bulletin, 33, 257– 270. https://doi.org/10.5962/bhl.part.16128 Torres-Gastello, C.P., Suárez-Segovia, J. & Cisneros-Heredia, D.F. (2007) Cochranella erminea, a new species of Centrolenidae (Amphibia: Anura: Athesphatanura) from Amazonian Peru. Journal of the National Museum in Prague. Natural History Series/ Casopis Národního muzea v Praze, 176, 1–12. Twomey, E., Delia, J. & Castroviejo-Fisher, S. (2014) A review of Northern Peruvian glassfrogs (Centrolenidae), with the description of four new remarkable species. Zootaxa, 3851 (1), 1–87. https://doi.org/10.11646/zootaxa.3851.1.1

274 · Zootaxa 4238 (2) © 2017 Magnolia Press MOLINA-ZULUAGA ET AL.