Zoosyst. Evol. 94 (2) 2018, 349–358 | DOI 10.3897/zse.94.25189 New populations of two threatened species of Alsodes (Anura, Alsodidae) reveal the scarce biogeographic knowledge of the genus in the Andes of central Chile Claudio Correa1,*, Paulo Zepeda2, Nicolás Lagos3, Hugo Salinas4, R. Eduardo Palma2, Dayana Vásquez2,* 1 Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Barrio Universitario S/N, Concepción, Chile 2 Departamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Alameda 340, Santiago, Chile 3 Alianza Gato Andino, Jenner 152, B° La Quinta, Segunda Sección Villa Carlos Paz, Córdoba, Argentina 4 Ecodiversidad Consultores, Riñihue 1022, Puente Alto, Santiago, Chile http://zoobank.org/D9185A98-A5A3-4B0B-9010-E81BC732E6FA Corresponding author: Claudio Correa ([email protected]) Abstract Received 21 March 2018 High Andean environments of central Chile (32°–38°S) are inhabited by several endemic Accepted 1 June 2018 species of the genus Alsodes. Two of them, A. pehuenche and A. hugoi, have geographic Published 17 July 2018 distributions restricted to their type locality and surroundings. The Chilean government classifies A. pehuenche as Critically Endangered (like the IUCN) and A. hugoi as Vul- Academic editor: nerable. In this study we report 16 new localities of Alsodes, corresponding to first order Peter Bartsch streams, located in the Andes of Chile between 35°58’ and 36°32’S (1800–2470 m). In some of these sites, adults and juveniles morphologically similar to A. pehuenche and Key Words A. hugoi were observed, as well as specimens of Alsodes that could not be identified by their external morphology. A Bayesian phylogenetic analysis with mitochondrial sequenc- Alsodes pehuenche es (cytochrome b) was performed to identify the new populations to species level. All Alsodes hugoi populations around 36°S belong to A. pehuenche, while most of those located south of that Chilean Andes area would be A. hugoi. The exception is Cajón de Plaza (36°23’S), where specimens with distribution extensions sequences of A. hugoi or A. pehuenche coexist, whose taxonomic status could not be deter- first order streams mined. These findings imply not only a westward range extension ofA. pehuenche in Chile conservation of about 14.5 km and of A. hugoi about 100 km southward, but also that practically all Critically Endangered the first order streams of the Andes of central Chile would be inhabited by populations of Vulnerable Alsodes. Both results demonstrate the scarce biogeographic knowledge of the genus in the Andes, which has important implications for its conservation at local and species levels. Introduction with five species A.( montanus (Lataste, 1902), A. tumultu- osus Veloso, Iturra & Galleguillos, 1979, A. hugoi Cuevas The amphibian fauna of the Andes of southern South Amer- & Formas, 2001, A. pehuenche Cei, 1976 and A. nodosus ica (Chile and Argentina) is relatively poor in comparison (Duméril & Bibron, 1841)) present in the western slopes to tropical high-altitude environments (Duellman 1979, (Chile) between 33° and 36°S (Charrier et al. 2017). Four 1999). In fact, only three anuran genera, Alsodes Bell, of these species are endemic to Chile, since A. pehuenche 1843, Rhinella Fitzinger, 1826 and Pleurodema Tschudi, is also present in Argentina in a small area around the bor- 1838, are represented in the Andes south of 30°S above der between these countries (Valle Pehuenche, its type lo- 1500 m. Alsodes is the most diversified of these genera, cality, 36°S) (Corbalán et al. 2010, Correa et al. 2013). * These authors contributed equally to this work. Copyright Claudio Correa et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 350 Claudio Correa et al..: New populations of two threatened species of Alsodes... There are few published records of Andean populations Critically Endangered and A. hugoi as Vulnerable. These of Alsodes in Chile and most of these were reported in the categories rest on the application of criterion B, which last decade. For instance, several reports since 2008 in- exclusively considers the extent of the geographical dis- creased significantly the distribution ranges and number of tribution. On the other hand, A. pehuenche is Critically known localities of A. montanus and A. tumultuosus from Endangered and A. hugoi is Data Deficient according to 33°20’ to 35°S (Araya and Riveros 2008, Correa et al. 2008, the IUCN (2017). This last categorization of A. pehu- Mora et al. 2015, Ramírez 2015, Correa 2017). Likewise, enche is fundamentally based on estimates of the extent new records of A. hugoi (Araya and Cisternas 2008) and of occurrence (about 9 km2) and area of occupancy (about A. pehuenche (Corbalán et al. 2010, Correa et al. 2013) ex- 5 km2) (IUCN SSC Amphibian Specialist Group 2013). tended their distributions, but in both cases within a small In this study we report new Andean localities of Al- area around their type localities. These last two studies are sodes situated in Chile between 35°58’ and 36°32’S. particularly relevant because they extended the distribu- These localities were found during three field campaigns tion of A. pehuenche to Chile, a species previously known aimed to locate new populations of A. pehuenche, one in just from its type locality in Argentina. The fifth species, the surroundings of the known localities in Chile (around A. nodosus, also inhabits the western slopes of Andes, but 36°S) and the other two south of the known distribution it is not clear what altitude it reaches (e.g. Cuevas 2013). range of the species. We performed a phylogenetic analy- Despite this significant increase in the number of known sis with mitochondrial cytochrome b sequences to identi- localities of Alsodes in the Andes, there are still substantial fy most of the populations discovered to species level. We distribution gaps. For example, there is a stretch of 380 lin- discuss the implications of these findings for the bioge- ear kilometers where only A. hugoi and A. pehuenche are ography and conservation of the genus in Chilean Andes. known, between the Tinguiririca River basin (34°55’S), the southern end of the distributions of A. montanus and A. tumultuosus, and San Ignacio de Pemehue, type locality of Material and methods A. vittatus (Philippi, 1902) (38°05’S) (Fig. 1). The distribution ranges of A. pehuenche and A. hugoi Field campaigns are extremely restricted. Alsodes pehuenche was first re- We carried out three field campaigns in the western slopes ported as Telmatobius montanus (now A. montanus) by of the Andes Range between 35°55’ and 36°35’S to locate Cei and Roig (1965) at two very close localities located on new populations of A. pehuenche in Chile (Fig. 1). The three each side of the border of Chile and Argentina (36°S). The areas explored are located almost entirely in the southeast Argentinean locality (Valle Pehuenche) became the type part of the Maule River basin, except for the southernmost locality when this species was formally described by Cei area that covers the northeast end of the Ñuble River basin. (1976), but the Chilean locality was subsequently ignored The explorations were focused on the surroundings and (see comment in Correa et al. 2013). For 45 years it was to the south of the known distribution of A. pehuenche in assumed that A. pehuenche inhabited only in its type local- Chile (Paso Pehuenche and Laguna del Maule, around 36°S ity, located in a drainage basin on the eastern slopes of the and 70°25’W; Correa et al. 2013). The longest campaign Andes (that ultimately flows into the Atlantic Ocean), until was carried out in 2016–2017 in the surroundings of Paso Corbalán et al. (2010) extended its distribution about 4 km Pehuenche and Laguna del Maule (Fig. 1B), where a total of to the southwest in Chile, in a contiguous drainage basin, nine sites between 2200 and 2500 m were explored (Table 1). but that drains to the west into the Pacific Ocean. Corbalán Two of these sites had previously been described (Corbalán et et al. (2010) also specified that on the Argentinian side the al. 2010, Correa et al. 2013). The other two campaigns were species only occupies five very close streams and indicat- carried out in 2016, the first in the surroundings of Laguna El ed that attempts to find individuals in other nearby streams Dial (around 36°27’S; six days, five sites explored between failed. Later, Correa et al. (2013) reported a second lo- 1830 and 2000 m; Fig. 1D), and the second in some eastern cality in Chile, which further extended the distribution tributaries of the Guaiquivilo River (around 36°08’S; five approximately 3.4 km west. Similarly, Alsodes hugoi was days, five sites explored between 1800 and 2160 m; Fig. 1C) known since its description only in its type locality (Altos (Table 1). The last two areas were reached on horseback with de Vilches, 35°33’S, 900 m, Cuevas and Formas 2001) the help of a guide and a muleteer. The searches focused on until Araya and Cisternas (2008) reported its presence in first order streams fed by melting snow, which are generally several sites around this locality. Although these new re- located in areas with a steep slope and are associated with cords extended the altitudinal range up to 2115 m, all sites flooded meadows, since this is the environment described are hydrologically connected to the Lircay River and the for A. pehuenche (Cei and Roig 1965, Corbalán et al. 2008, maximum distance between them does not exceed 10 km.