Herpetology Notes, volume 7: 703-706 (2014) (published online on 25 November 2014)

Distribution extension, new records and historical occurrence of taeniata (Girard, 1854) (Anura: ) in Chile

Claudio Correa1,2,*, Javiera Cisternas2,3, Nelson Velásquez3, Gabriel Lobos4 and Julio San Martín-Órdenes5

Due to their abundance, anurans of the genus Batrachyla Caiquenes (47.817° S) (Cisternas et al., 2013) (Table Bell, 1843 are an important component of austral South 1). Cei (1962) and Sallaberry et al. (1981) agree that American temperate forests (Formas, 1979; Rabanal B. taeniata is more abundant south of Concepción and Nuñez, 2008). Among the five currently recognized (36.833° S), but disagree regarding its distribution species, B. antartandica, B. leptopus and B. taeniata pattern north of this city (see the location of this city in are the most common and widely distributed in Chile Fig. 1). Cei (1962) mentions only five localities north of and marginally in Argentina, from 32.5° S (coast of the Chilean Valparaíso Region for B. taeniata) to 51.517° S (Chilean Magallanes Region for B. antartandica) (Cei, 1962; Atalah and Sielfeld, 1976; Sallaberry et al., 1981; Rabanal and Nuñez, 2008; IUCN, 2014). The other two species, B. fitzroya and B. nibaldoi, have more restricted ranges and are endemics to Argentina (Basso, 1994) and Chile (Rabanal, 2010), respectively. has the widest distribution range and occupies the greatest variety of habitats. Its distribution in Chile was defined historically between Zapallar (Valparaíso Region, 32.5° S) and Correntoso River (Aysén Region, 45.417° S) (Cei, 1962; reviewed by Sallaberry et al., 1981; Fig. 1), but afterwards was extended successively to Laguna San Rafael National Park (46.667° S; Díaz-Páez et al., 2002) and to Laguna

1 Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción. Concepción, Chile. 2 Organización de Desarrollo Aumen o El Eco de los Montes, Non-Governmental Organization. Coyhaique, Chile. 3 Instituto de Ciencias Biomédicas, Facultad de Medicina, Universidad de Chile. Santiago, Chile. 4 Centro de Gestión Ambiental y Biodiversidad, Facultad de Figure 1. Updated distributional map of Batrachyla taeniata Ciencias Veterinarias y Pecuarias, Universidad de Chile. in Chile. Hatched area represents the distribution range Santiago, Chile. according to Sallaberry et al. (1981); green circles: 13 localities 5 Programa de Doctorado en Ciencias Veterinarias, Facultad de compiled from the literature between 1981 and 2013 (Table Ciencias Veterinarias, Universidad de Concepción. Chillán, 1); numbered red circles: new localities reported in this study, Chile. 1: Ucúquer, 2: Laguna Amargo, 3: Tortel, 4: Río Mosco. For * Corresponding author e-mail: [email protected] reference, the location of Concepción city is given. 704 Claudio Correa et al.

Table 1. Localities of Batrachyla taeniata from Chile reported a.s.l.; two males and one female; December 2nd, 2011), in the literature between 1981 and 2013. Localities are sorted Tortel (47.794° S; 73.531° W; 40 m a.s.l.; two adult from north to south (see green points in Fig. 1). Coordinates are males; October 24th, 2011), and Río Mosco (48.483° given only to two decimal places because of the low precision S; 72.583° W; 263 m a.s.l.; one juvenile; October 22nd, of the original sources. *Authors did not provide coordinates 2011) (Fig. 1, red circles; see some specimens in Fig. for this locality. Tableȱ1ȱ 2). Ucúquer is a small temporary stream surrounded by sclerophyllous scrub located in the Mediterranean zone Locality Latitude (S) Longitude (W) Reference

Cabrería 37.78° 72.92° Penna and Veloso (1990) of central Chile (Fig. 2B). Specimens were collected at Valle de Collipulli* 37.97° 72.43° Cuevas and Cifuentes (2010) night in a period of the year (austral autumn) when the Monteverde 38.73° 72.60° Brieva and Formas (2001) call activity of this species in this zone is highest. Laguna Las Pataguas 40.23° 73.68° Méndez et al. (2005) Amargo is a natural lagoon, surrounded by Nothofagus Pantano La Barra 40.23° 73.70° Méndez et al. (2005)

Centinela 41.15° 73.45° Brieva and Formas (2001) forests, which drains into a dam located in the foothills

Bosque Olivillo 41.27° 73.85° Méndez et al. (2005) of Los Andes of central Chile. Specimens were collected Puntra 42.05° 73.97° Brieva and Formas (2001) during the day in late austral spring. Tortel corresponds Yaldad 43.12° 73.72° Brieva and Formas (2001) to a peat bog system with temporary pools mixed with Laguna San Rafael National Park 46.62° 74.03° Díaz-Páez et al. (2002) (Canal area) evergreen forest, whereas Río Mosco corresponds to Laguna San Rafael National Park 46.63° 73.85° Díaz-Páez et al. (2002) a riverbank within a mixed deciduous and evergreen (Glaciar area)

Laguna San Rafael National Park Nothofagus forest (Fig. 2D). Captures were done by 46.73° 73.93° Díaz-Páez et al. (2002) (San Quintín area) hand, on daytime, applying an active search method Laguna Caiquenes 47.82° 73.30° Cisternas et al. (2013)  during the austral spring. Specimens from Tortel were engaged in call activity. Taxonomic determination was based on the external diagnostic characteristics that Formas (1997) used to distinguish B. taeniata from B. Concepción (Zapallar, Aguas Claras, Quintero, Olmué nibaldoi (see below). All specimens were deposited in and Talca); all except Talca are located near the coast in the herpetological collection of the Departamento de the Valparaíso Region (32.5°-33.0° S), so his map shows Biología Celular y Genética of the Universidad de Chile distribution gaps of 275 km between Olmué (33.0° S) (DBGUCH) with collection numbers 1105021-1105024 and Talca (35.42° S), and 200 km between Talca and (Ucúquer), 1112009-1112011 (Laguna Amargo), Concepción. However, Sallaberry et al. (1981), based 1110113-1110114 (Tortel) and 1110107 (Río Mosco). on new records, which only fill partially the gap between Capture permit was provided by the Servicio Agrícola Olmué and Talca, suggested that the distribution of this Ganadero (SAG), resolution 5090 / 2011. species is continuous north of Concepción and that these Our new records extend the distribution of this gaps were probably due to a lack of exploration. species about ninety kilometers southeast from Laguna In this study the southern distribution limit of B. Caiquenes, its previous known southern distribution taeniata is extended, new localities north of Concepción limit (Cisternas et al., 2013). Furthermore, the localities are reported, and an updated map with records after of Tortel and Río Mosco reported here, as well as the 1981 is provided (Fig. 1, Table 1). This map is not recently described locality Laguna Caiquenes, increase based on a thorough review of the literature because the range of environmental conditions this species its main purpose is to highlight the general location of inhabits in southern Chile, since they are located within the new findings. The sources after 1981 are: Penna the Magellanic Forest Region, which has more extreme and Veloso (1990), Brieva and Formas (2001), Díaz- climate conditions than the temperate environments Páez et al. (2002), Méndez et al. (2005), Cuevas and (Pisano, 1992; Arroyo et al., 1995) of the previously Cifuentes (2010) and Cisternas et al. (2013) (Table known range. Sallaberry et al. (1981) argued that the 1). The localities obtained from these sources were scarcity of temporal pools and flood zones north of superimposed on the continuous distribution area drawn 32.5° S, and low temperatures and the onset of tundra by Sallaberry et al. (1981) (Fig. 1). vegetation south of 45.417° S could explain the The new localities from north to south are (geographic latitudinal limits for B. taeniata, but these new records coordinates, altitude, number of captured individuals, show that the ecological factors determining its southern and capture dates are given): Ucúquer (34.017° S; limit should be reassessed. 71.681° W; 198 m a.s.l.; four adult males; May 9th, Regarding the historical occurrence of this species, 2011), Laguna Amargo (36.328° S; 71.406° W; 781 m Sallaberry et al. (1981) suggested that the distribution is Distribution, new records and historical occurrence of Batrachyla taeniata 705

Figure 2. Examples of specimens and habitats of the new localities of Batrachyla taeniata. The number in brackets is the number of the red circle on the map in Fig. 1. A) Male from Ucúquer (1), B) Ucúquer, C) Female (not collected) from Río Mosco (4), D) Río Mosco.

continuous throughout its range, but they noted that most historical locality in this area where specimens have of the known localities at that time were located south of recently observed (2010) is the relict forest of Quintero Concepción. Subsequent studies that include or mention (Cei, 1962; 32.796° S, 71.513° W), a small protected locations of this species in Chile (specified above) area located within the Air Force Base of that coastal seem to confirm this pattern, as none of the reported city (Claudio Correa, personal observation). localities are north of that city (Fig. 1, green circles; We report two new localities north of Concepción Table 1). Moreover, Sallaberry et al. (1981) reported (one of which, Laguna Amargo, shows that the species 12 new localities in a reduced area of the northern part certainly is present in the foothills of the Andes north of the distribution (32.5°-34.333° S, Metropolitan and of 37° S), which are apparently the only two reported Valparaíso Regions), and mentioned that all known in this area for over 30 years. This paucity of reports localities north of Concepción are located in the coastal is consistent with the natural scarcity of populations in plains (the most) or in the central valley, and only farther this part of the distribution mentioned by Cei (1962) and south there are populations in the foothills of the Andes. Sallaberry et al. (1981), which is probably accentuated by In subsequent studies, only Díaz et al. (1987) mentioned profound landscape changes that may have diminished or included some of these 12 localities. Explorations or extinguished some populations (see above). in 2010 and 2011 failed to find populations of this The southern range extension of B. taeniata reported species in part of the area (32.8°-33.667° S) where here implies an overlap of distributions between this Sallaberry et al. (1981) discovered their new localities. species and B. nibaldoi. Recently, Rabanal (2010) Instead, landscape modifications caused by agricultural extended the southern range of B. nibaldoi to the activities and water pollution were observed (Claudio proximity of Villa O’Higgins (48.455° S, 72.566° W), Correa, Gabriel Lobos, personal observations). The only which is about 100 km SE of Tortel and only about 3 km 706 Claudio Correa et al. north of the Mosco River (both reported here). These Brieva, L.M., Formas, J.R. (2001): Allozyme variation and last records imply that the two species overlap in a wide geographic differentiation in the Chilean leptodactylid area extending between Abdao Island (42.667° S), the Batrachyla taeniata (Girard, 1854). Amphibia-Reptilia 22: 413- 420. northernmost known record of B. nibaldoi, and Villa Cei, J.M. (1962): Batracios de Chile. Santiago, Ediciones O’Higgins (48.455° S) (compare Figure 1 with the map Universidad de Chile. of Rabanal, 2010). Only Díaz-Páez et al. (2002) had Cisternas, J., Correa, C., Velásquez, N., Penna, M. (2013): previously reported the coexistence of these species in Reproductive features of grandisonae two sites within Laguna San Rafael National Park (Canal (Anura: Batrachylidae) within a protected area in Patagonia, and Glaciar areas, Table 1), although they mentioned the Chile. Revista Chilena de Historia Natural 86: 365-368. difficulty to distinguish them, both morphologically and Cuevas, C.C., Cifuentes, S.L. (2010): Amphibia, Anura, , Bell, 1843: New records by their calls. This observation is consistent with what updating and geographic distribution map, Chile. Check List 6: appears in the description of B. nibaldoi (Formas, 1997), 633-636. where is mentioned that this species is very similar in Díaz, N.F., Sallaberry, M., Valencia, J. (1987): Microhabitat and coloration and external morphology to B. taeniata. In reproductive traits in populations of the frog, Batrachyla this study, the species determination was based on the taeniata. Journal of Herpetology 21: 317-323. characters used by Formas (1997) for distinguishing Díaz-Páez, H., Williams, C., Griffiths, R.A. (2002): Diversidad B. taeniata from B. nibaldoi: unlike B. nibaldoi, B. y abundancia de anfibios en el Parque Nacional “Laguna San Rafael” (XI Región, Chile). Boletín del Museo Nacional de taeniata has thick fingers and toes with rounded tips, Historia Natural 51: 135-145. has outer metatarsal tubercle and relatively long legs Formas, J.R. (1979): La herpetofauna de los bosques temperados de (the tibiotarsal articulation of the adpressed hind limb Sudamérica. In: The South American Herpetofauna: Its Origin, exceeds the anterior border of tympanum). Considering Evolution, and Dispersal, p. 341-379. Duellman, W.E., Ed., the complete overlapping of geographic ranges of both Museum of Natural History, University of Kansas, Monograph species that implies our findings and the high phenotypic 7, Lawrence, Kansas. similitude between them, it would be useful to obtain Formas, J.R. (1997): A new species of Batrachyla (Anura: Leptodactylidae) from southern Chile. Herpetologica 53: 6-13. additional characters for distinguishing them, along IUCN (2014): The IUCN Red List of Threatened Species. Version with an evaluation of their geographic variation, and to 2014.1. Available at: http://www.iucnredlist.org. Last accessed examine more specimens for clarifying more precisely on 14 June 2014. their distribution limits. Méndez, M.A., Soto, E.R., Torres-Pérez, F., Veloso, A. (2005): Anfibios y reptiles de los bosques de la Cordillera de la Costa (X Región, Chile). In: Historia, Biodiversidad y Ecología de Acknowledgements. Claudio Correa thanks partial funding of los Bosques Costeros de Chile, p. 441-455. Smith-Ramírez, Fondecyt projects 3110040 (postdoctoral) and 79130032, and C., Armesto, J.J., Valdovinos, C., Eds., Santiago, Editorial Dusan Boric, Álvaro Zúñiga and Jaime Zúñiga for their help in Universitaria. the fieldwork at Ucúquer. Mauricio Valiente and Carla Marilaf Penna, M., Veloso, A. (1990): Vocal diversity in of the South assisted with field work in Laguna Amargo. Arturo Villanueva American Temperate Forest. Journal of Herpetology 24: 23-33. and Rodrigo Villalobos facilitated access to Laguna Amargo Pisano, E. (1992): Sectorización fitogeográfica del archipiélago specimens. CC and JC thank Lorena Palacios and Patricio sud patagónico-fueguino V: sintaxonomía y distribución de Saldivia for their help in preparing the map. las unidades de vegetación vascular. Anales del Instituto de la Patagonia, Serie Ciencias Naturales 21: 5-33. References Rabanal, F.E. (2010): Amphibia, Anura, Ceratophryidae, Formas, 1997: Latitudinal extension in Patagonia, Arroyo, M.K., Cavieres, L., Peñaloza, A., Riveros, M., Faggi, A.M. southern Chile, and distributional range actualization. Check (1995): Relaciones fitogeográficas y patrones regionales de List 6: 287-288. riqueza de especies en la flora del bosque lluvioso templado de Rabanal, F.E., Núñez, J.J. (2008): Anfibios de los bosques Sudamérica. In: Ecología de los Bosques Nativos de Chile, p. templados de Chile, First Edition. 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