Telmatobufo Bullocki

n New distribution records of the critically endangered frog Telmatobufo bullocki

istributio Calyptocephalellidae) in southern Chile D Schmidt, 1952 (Anura: 1* 2 raphic Felipe E. Rabanal g eo

G and Virginia Moreno-Puig n

o 5090000, Valdivia, Chile. 1 Universidad Austral de Chile, Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Casilla 567, Campus Isla Teja, Zip Code

otes 2 Massey University, Institute of [email protected] and Mathematical Sciences, Ecology, Behaviour & Conservation Group, Private Bag 102-904, North Shore N Mail Centre, Albany, Auckland 0745, New Zealand. * Corresponding author. E-mail: Abstract: In an effort to assess the current geographic distribution of the critically endangered frog Telmatobufo bullocki

historic localities cited in the literature, and potential new localities in private forestry areas. Telmatobufo bullocki was Schmidt, 1952, we conducted several field surveys in the Nahuelbuta mountain range in central-south Chile. We surveyed of the species in at least four historic localities open new perspectives for the conservation of this threatened species. found in six localities: four historic and two new. The discovery of new populations and the confirmation of the persistence

The genus Telmatobufo Schmidt, 1952 comprises four species [T. australis Formas, 1972; T. bullocki Schmidt, 1952; T. ignotus Cuevas, 2010 and, T. venustus (Philippi, six localities on the western slopes. The species was also 1899)] distributed in the temperate forests of central (Escobarrecorded et in al. Quirihue 2005). A (Ñubleputative Province, third population Biobío Region),north of °10 S) (Cei 1962; Formas approximately 150 km north of the Nahuelbutaet al. (2010) range and Pugin 1979; Formas and Veloso 1982; Formas et in a small protected area of a Maulino deciduous forest in al.and 2001; southern Cuevas Chile 2010; (35°30′–41 2011). All′ Telmatobufo species Losthe Nahuelbuta Queules National range was Reserve, reported Maule by Donoso Region. However, are associated with cold mountain streams and their Cuevas (2010) considered this population to be the newly tadpoles are of the “mountain stream type”, Group IV, described Telmatobufo ignotus, and described this area as sensu Orton (1953). The tadpoles are adapted to live and the type locality of the species. However, it is possible that the Telmatobufo population in Quirihue corresponds to T. disc to anchor themselves to submerged boulders (Figure ignotus instead of T. bullocki, as it is geographically closer feed in fast flowing waters: they have a sucker-like oral to Los Queules National Reserve than the Nahuelbuta range. Most records of T. bullocki in the literature date from et1E), al. strong1983; Formas paddle-shaped 1988; Lavilla tails 1988). and a The dorso-ventrally adults have the 1960s to the 1990s, and the species was considered flattened body (Figures 1C and 1D) (Formas 1972; Díaz lost for several years as many surveys conducted in the toes (Figure 1B), and Péfaur (1971) noted that captive T. Nahuelbuta area by different specialist groups failed to bullockiwell-developed could remain inter-digital completely webbing submerged between for more theirthan In an effort to assess the current status of historic environments. T.find bullocki any specimens. oneCurrently and a half Telmatobufo hours, suggesting bullocki great (Figure affinity 1A) is with considered aquatic one of the most endangered species of amphibians in populations, and to find new localities, we conducted several field surveys between December endangered by the IUCN (2012), and listed as 5th of the the2008 Nahuelbuta and December range, 2012. mainly We in surveyed private several forestry historic areas. Chile and the world. It has been classified as critically locations, and previously un-surveyed localities within (EDGE 100 most Evolutionarilysensu Distinct Isaac andet al Globally Endangered Surveys were conducted under permit number 13-2011 ) amphibians (http://www.edgeofexistence.org), Forestal,IX, issued CONAF, by Departamento and permit de number Áreas Silvestres 6977 from Protegidas, Servicio based on EDGE Scores . (2007). This ranking Región de la Araucanía, of the Corporación Nacional andtakes a intodistinctive account evolutionary the level of historythreat and are phylogenygiven priority of the in conservationspecies, where action the taxa plans. with More major recently, conservation the species problems was Agrícola y Ganadero, SAG. Surveys were conducted during also listed as one of the 100 most endangered species in daylight hours (looking under logs, fallen tree trunks and the world, in a list which includes both animals and plants habitatother possible (in search refuges), of tadpoles and nocturnally and breeding (looking adults), for active and (Baillie and Butcher 2012). animals using a head-torch). We surveyed both aquatic Since its original description in 1952 by Schmidt, T. T. bullocki by visual inspection of characteristic bullocki terrestrial habitat adjacent to streams. Animals were eastern slopes of the Nahuelbuta mountain range, and in dorsalidentified and as paratoid gland pattern in adults (Schmidt has been recorded in at least five localities on the features such as their yellow inter-ocular spots and their

428 Rabanal and Moreno-Puig | New records of the critically endangered frog Telmatobufo bullocki

1952; Formas et al. S, 73°06

2001), and the oral disc (a sucker- Area), 5.4 km southeast from Lota (37°07′ ′ W; didlike not mouth, collect Figure any voucher 2E) and specimens, flattened but bodies all encountered in tadpoles 363 m asl). Despite several surveys, the species was not individuals(Formas 1988). were Due photographed. to its high risk Photographs conservation have status been we found at some historic locations: Ramadillas, Vanerías deposited at Herpetological Collection of Universidad de Butamalaland Estero is Cabrerías in a privately (Parque owned Nacional large patch Nahuelbuta), of mature and secondaryVegas Blancas. native The forest, newly while discovered the population population in Chivilingo in Río T. bullocki is in a very small privately owned secondary native forest (FigureConcepción, 2, Table Chile 1). (MZUC Four 34191). of these correspond to historic (Elicura,We found Estero specimens La Cueva, of Caramávida, at and six Estero localities Los Telmatobufo bullocki has been considered a rare species sincepatch itssurrounded description. by Onlyexotic a fewforestry specimens plantation. have ever been S, 73°10 Lleulles), and two are new localities for this species: Río named) only encountered the species on three occasions Butamalal, 19 km southeast from Cañete (37°50′ ′ collected, and even Dr. Bullock (after whom the species is W; 424 m asl); and Predio Chivilingo (Private Conservation

Figure 1. Specimens of T. bullocki

Gosner). Scale bar= 1 cm. from Butamalal River in the Nahuelbuta mountain range. A) Adult male, B) Inter-digital webbing between the toes of the adult specimen, C) Tadpole (Stage 27 Gosner), D) Pre-metamorphic specimen (Stage 38 Gosner), E) Sucker-like oral disc of the tadpole (Stage 26

429 Rabanal and Moreno-Puig | New records of the critically endangered frog Telmatobufo bullocki

Table 1. T. bullocki represented under the same label. Some references only give locality names, no coordinates provided. records including historic and new records (*Historic localities corroborated in the field; **New localities). Some close localities are LABEL LOCALITY NAME REFERENCE 1 Lota Venegas (1975) LATITUDE LONGITUDE 2** Predio Chivilingo This publication - - Ramadillas 3 37°07′ S 73°06′ W Formas and Veloso (1982) - - FormasDonoso-Barros et al. (2001) (1972) Caramávida - - Formas and Veloso (1982) - - Formas et al. (2001) - - This publication Rucapehuén - - 4* 37°42′ S 73°12′ W Estero La Cueva Formas (1988) 5* 37°40′ S 73°25′ W ThisNuñez publication and Formas (2000) 6** 37°40′ S 73°25′ W This publication 37°44′ S 73°08′ W 7 Cei (1962) Río Butamalal 37°50′ S 73°10′ W Elicura Sanfeliu (1969) 8* Estero Cabrerías - - This publication - - 9 37°54′ S 73°13′ W Péfaur (1971) Vanerías - - (Parque Nacional Nahuelbuta) Péfaur (1971) 10 Estero Cabrerías Vegas Blancas - - Cei (1962) (Parque Nacional Nahuelbuta) 11 Vegas de Rucapillán Péfaur (1971) - - Estero Los Lleulles Péfaur (1971) 12* - - - - This publication - - Duellman (1975) 37°47′ S 72°48′ W Sightings that followed its discovery were scarce, and in theduring IUCN his Rednumerous List population trips to Nahuelbuta assessment (Bullock the authors 1954). reported that ‘extensive fieldwork by several herpetologists within the range of this species from 1992-2002 turned up only a single adult (in 2002)’ (Veloso et al. 2010). This report generated the general idea that the species was our surveys we detected T. bullocki 2,not Table only 1).rare Nevertheless, but on the brink this increase of extinction. in detectability However, inis at six localities (Figure likely to reflect our improved ability to find them rather than a true increase in numbers. It is now recognized that previous field surveys failed to detect the species, surveysin part, showed because that they the were adults exclusively can be found focused in terrestrial on the aquatic environments (J. C. Ortiz, pers. comm.), while our (unpublished data). Also, most efforts were focused inside habitat far from streams during the non-breeding season surveyed by us, possibly because of restricted access due tothe private Nahuelbuta ownership National of forestry Park, excluding land. most of the areas

Figure 2. T. bullocki in the Nahuelbuta mountain range. Green dots are localities where we found the species recently. Red dots speciesWe confirm was not thatfound this at speciessome of is its rare, historic even localities now that is we of are historic Distribution localities where of the species has not been found recently. mosthave betterconcern, knowledge but it comes of its as habitat no surprise. use. The The fact Nahuelbuta that the Numbers correspond to labels in Table 1. range has suffered a dramatic change during the past only state protected area where the species was thought century, where native forest has been Pinusextensively radiata cleared) and eucalyptusand replaced (Eucalyptus first by cattle globulus and agriculture,), which today and then covers by (Péfaurto be present. 1971). Despite This is ofseveral great herpetologicalconcern as the surveys, habitat hasthe exotic forestry plantations of pine ( remainedspecies was untouched, last seen and inside there the is no park obvious during evidence the 1960s for this decline. Although we cannot rule out the possibility nearly 70% of the area (CONAF 2008; Wolodarsky-Franke that the species is present, but undetected on our surveys, smalland Díaz fragments Herrera of2011). what Some once of was the historic a continuous localities native are forest.covered Of by special these concern exotic plantations, is the apparent and others disappearance are only it is likely that at least some historic populations no longer exist. On the other hand, some historic populations in of the species from the Nahuelbuta National Park, the localities that have been under significantly more pressure 430 Rabanal and Moreno-Puig | New records of the critically endangered frog Telmatobufo bullocki from forestry development still persist (e.g. Los Lleulles), distribution map. Check List showing that the species has at least some degree of Schmidt, 1952: Distribution extension, habitat use and geographic resilience to habitat change and disturbance. Aruncus Phillippi. Boletín de 6(2): la Sociedad 298–300. de Biología de Concepción Most of the localities where we found the species Donoso-Barros, R. 1972. Contribución al conocimiento del género are currently owned by private forestry companies; and Collection specimen Telmatobufo venustus (=T. bullocki44: 109–116. Kansas University Herps we found T. bullocki in both native forest and mature Duellman,Collection W.E. 1975. pine plantation. Some of these areas, particularly those Captured). on Catalogue 02 May 2012. number 161438, in: comprised of mature native forest are already considered . Accessible at http://collections.nhm.ku.edu/HerpsWeb. of high conservation value (e.g. Quebrada de Caramávida), Escobar, M.A.H, Herpetological C.F, Estades, Review M. Falcy and M.A. Vukasovik. and receive active protection from forestry companies. 2005. Telmatobufo bullocki (Bullock’s Frog) [Geographic However, populations that occur in small native fragments, Distribution]. Journal of Herpetology36(1): 77. 3. Formas, J.R. 1972. A second species of ChileanTelmatobufo frog genus bullocki Telmatobufo and individuals living in pine plantations face imminent Leptodactylidae).(Anura: Leptodactylidae). Herpetologica 6(1): 1– Formas, J.R. 1988. The tadpole of Telmatobufo (Anura: australis 44: 458–460. Journal of Formas,Herpetology J.R. and E. Pugin.361. 1979. New observations of therisk private from timber owners industry and forestry activities, companies especially as clear- main (Anura: Leptodactylidae) in SouthernBufo venustus Chile. Philippi, cutting operations. Consequently, itT. bullocki is critical populations. to involve 13: 359– Proceedings of Formas,Biological J.R. and Society A. Veloso. of Washington 1982. Taxonomy693. of The results we present here represent the most thorough 1899 (Anura: Leptodactylidae) from Central Chile. andstakeholders updated accountin the conservation of the distribution of of this species and 95: 688– Formas,género J.R., Telmatobufo J.J. Nuñez (Lept andodactylidae). L.M. Brieva. Revista Chilena2001. deOsteología, Historia Naturaltaxonomía y 387. relaciones filogenéticas de las ranas del distribution,represent one we of can the now first focus steps on towards the study its ofconservation. the natural 74: 365– history,With our ecology improved and behavior knowledge of the aboutspecies, its to promote current Isaac,phylogeny. N.J.B., S.T. Plos Turvey, One B. Collen, C. Waterman and J.E.M. Baillie. 2007. IUCNMammals 2011. IUCN on the Red EDGE: List Conservation of Threatened priorities Species. based Version on threat 2011.2. and the in-situ conservation of the populations and assess the 2(3): e296. need for ex-situ conservation if natural conditions are not 2012. Accessible at http://www.iucnredlist.org/. Captured on 16 October diagnoses based on larval characters. Occasional Papers of the Lavilla,Museum E. 1988. of Natural Lower History,Telmatobiinae the University (Anura: of Leptodactylidae): Kansas 19. Generic likelyAcknowledgments to provide suitable: habitat in the long term. genus Telmatobufo 124: 1– The authors thank CONAF, Arauco S.A. and Nuñez,Amphibia-Reptilia J.J. and J.R. Formas. 2000.356. Evolutionary history of the Chilean frog Bioforest S.A. for access permits, D. Alarcón, C. Aguayo, T. Elgueta, E. Orton, G.L. 1953. The systematics (Leptodactylidae): of vertebrae an larvae. immunological Systematics approach. Zoology Flores, B. Álvarez and C. Elton, for their enthusiastic assistance in the field 21: 351– Amphibianand P. J. Bishop Conservation for comments Fund on and the the manuscript. Rufford Small This Grants work was Foundation. partially Telmatobufo bullocki (Anura, Leptodactylidae). funded by The Mohamed bin Zayed Species Conservation Fund, the EAZA Boletín2: 63–75. del Museo de Historia Natural de Chile Literature Cited Sanfeliu,Péfaur, J. 1971. I. Nota 1969. sobre Collection specimen Telmatobufo bullocki, Priceless or Worthless? The world’s MCZBASE: 32: The 723–725. Database of the most threatened species Zoological Collections, Museum of Comparative Zoology, Harvard Baillie, J.E.M. and E.R. Butcher. 2012. UniversityCatalogue number A-78829, in: . London: Zoological Society ofBoletín London, del JardínUnited Zoológico Kingdom. de 124 Concepción, pp. Chile Schmidt, K.P. 1952.. Accessible A new leptodactylid at http://mczbase.mcz.harvard.edu/guid/ frog from Chile. Fieldiana Zoology Bullock, D. 1954.Batracios Una especie de Chile nueva de rana de Nahuelbuta. MCZ:Herp:A-78829.15. Captured on 02 May 2012. 128 pp. 1(2): 1–3. Telmatobufo bullocki CONAFCei, J.M. 2008. 1962. Catastro y Evaluación. Santiago: de los Recursos Editorial Vegetacionales Universidad de Nativos Chile. 2012.34: 11 IUCN– Red List of Threatened Species Version 2012.2. Accessible de Chile. Veloso, A., H. Núñez and R. Formas. 2010. , in: IUCN Aruncus venustus (Philippi) 2011. Santiago, Chile: Corporación Nacional Forestal. Accessible at 1899at http://www.iucnredlist.org/. (=Telmatobufo bullocki Schmidt, Captured 1952). on 03 BoletínMarch 2013. Sociedad de Cuevas,http://territorial.sinia.cl/portal/descargas.php. C. 2010. A new species of Telmatobufo (Schmidt Captured 1852) on (Anura,24 May VenegasBiología S., W.de Concepción 1975. Los cromosomas de Calyptocephalellidae) from a remnant of the Maulino Forest, central Cordillera de Chile. Gayana 112. Nahuelbuta. Reserva Mundial 49: 71–77. de Biodiversidad. Cuevas, C. 2011. New geographic records of Telmatobufo australis Formas, Wolodarsky-Franke, A. and S. Díaz Herrera. 2011. 74: 102– Valdivia: WWF. 56 pp. Boletín de Biodiversidad de Chile 1972 (Amphibia: Anura: Calyptocephallelidae)1983. The tadpole in southernof Telmatobufo Chile. venustus 5: 28–35. Díaz,relationships. N., M. Sallaberry Herpetologica and H. Núñez. (Anura: Leptodactylidae) with a consideration of generic Received: September 2013 2010. Amphibia, Anura, Calyptocephalellidae, 39: 111–113. Telmatobufo bullocki Accepted: December 2013 Donoso, D.S., C. Correa Q., P. Henriquez, N.F. Lagos and M.A. Méndez. Published online: May 2014 Editorial responsibility: Ross MacCulloch

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