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Herpetological Review, 2013, 44(4), 583–590. © 2013 by Society for the Study of and Reptiles Status and Conservation of a Gondwana Legacy: Bullock’s False Toad, bullocki (Amphibia: Anura: )

Lowland temperate forests often suffer from anthropo- contains two (possibly three) other species: T. australis genic influences owing to their productive soils and ease of (Formas 1972), T. bullocki (Schmidt 1952), and, questionably, accessibility (Pérez et al. 2009). In fact, extensive alteration of Chile’s lowland temperate forests has occurred for over four DANTÉ B. FENOLIO* centuries (Armesto et al. 1994; Donoso and Lara 1996; Pérez Department of Conservation Research, Atlanta Botanical Garden, 1345 et al. 2009). The fragmented forests that remain in Chile are Piedmont Rd. NE, Atlanta, Georgia 30309, USA sandwiched between the Mountains to the east, the Pa- VIRGINIA MORENO-PUIG cific Ocean to the west, and the Atacama Desert to the north. A Ecology, Conservation & Behavior Group, Institute of Natural and narrow strip of southern Chile and adjacent Argentina house Mathematical Sciences, Massey University, Auckland, New Zealand all that remains of the temperate humid forests of the region e-mail: [email protected] (Aravena et al. 2002). These forests are biologically unique MICHAEL G. LEVY Department of Population Health and Pathobiology, North Carolina owing to isolation since the Tertiary Period and they host sig- State University College of Veterinary Medicine, 4700 Hillsborough Street, nificant numbers of endemic plants and (Aravena et Raleigh, North Carolina 27606, USA al. 2002; Armesto et al. 1996; Arroyo et al. 1996; Villagrán and e-mail: [email protected] Hinojosa 1997). South Chile’s forests play a key JOSÉ J. NÚÑEZ role in creating the microhabitats used by some of the region’s Instituto de Ciencias Marinas y Limnológicas, Universidad Austral de Chile, largely endemic fauna (Cuevas and Cifuentes Casilla 567, Valdivia, Chile 2009). There are minimally 37 anuran species unique to these e-mail: [email protected] forests, constituting no less than 85% of the regional amphib- WILLIAM W. LAMAR ian fauna including three endemic genera (, School of Sciences and Mathematics, The University of Texas at Tyler, Insuetophrynus, Telmatobufo) and an endemic family, the Ca- 3900 University Blvd., Tyler, Texas 75799, USA e-mail: [email protected] lyptocephalellidae (Ortiz and Díaz-Páez 2006; Díaz-Páez et al. MAURICIO O. FABRY 2008; Vidal et al. 2008). The genera Alsodes, , Ba- Zoológico Nacional, Parque Metropolitano de Santiago, Pío Nono 450, trachyla, , Eupsophus, Hylorina, and Rhi- Recoleta, Santiago, Código Postal 8420541, Chile noderma are unique to the region, some of which are found in e-mail: [email protected] both Chile and adjacent Argentina. MARCELA S. TIRADO An amphibian found only in these southern forests is Bull- Zoológico Nacional, Parque Metropolitano de Santiago, Pío Nono 450, ock’s False Toad, (Figs. 1–3). It is a relict Recoleta, Santiago, Código Postal 8420541, Chile species restricted to Nothofagus forest fragments in south Chile e-mail: [email protected] (Correa et al. 2006; Donoso et al. 2010; Núñez and Formas 2000; MARTHA L. CRUMP Sánchez 2010). This is infrequently observed as it spends Department of Biology, Utah State University, Logan, Utah 84322-5305, USA e-mail: [email protected] much of its time deep in forest litter. Because much of its habitat ANDRÉS CHARRIER** has been converted through silviculture and agriculture, and be- Centro de Estudios Avanzados de Ecología y Biodiversidad, Departamento cause so few specimens have been seen, the species is now listed de Ecología, Facultad de Ciéncias Biológicas P. Universidad Católica de Chile, by the IUCN as critically endangered (IUCN 2012). Santiago, Chile *Current address: Department of Conservation and Research, Telmatobufo San Antonio Zoo, 3903 N. St. Mary’s St., San Antonio, Texas 78212, USA Corresponding author; e-mail: [email protected] Philippi (1899) described Bufo venustus from four specimens **Current address: Departamento de Ecología, Facultad de Ciéncias collected in the Andean foothills of southern Chile. Schmidt, Biológicas P. Universidad Católica de Chile, IEB, Santiago, Chile in 1952, erected the genus Telmatobufo. Formas and Veloso re- e-mail: [email protected] assigned Bufo venustus to in 1982. The

Herpetological Review 44(4), 2013 584 CONSERVATION COLOR REPRODUCTION SUPPORTED BY THE THOMAS BEAUVAIS FUND FUND BEAUVAIS THOMAS THE REPRODUCTION BY SUPPORTED COLOR

Fig. 1. A female Bullock’s False Toad, Telmatobufo bullocki, found buried 0.7 m in forest loam beneath a log.

Fig. 2. A female Bullock’s False Toad, Telmatobufo bullocki; this is a robust species with the ability to withstand strong currents of icy Fig. 3. A male Bullock’s False Toad, Telmatobufo bullocki. Despite its water as well as range into surrounding forest under moderately dry large size and imposing appearance, this remains one of the least- conditions. known amphibians in the world.

T. ignotus (Cuevas 2010). Formas et al. (2001) discussed taxo- have been collected. These have been from Cabrerías, Llanca- nomic relationships among the then-recognized three species hue, Cerro Püschel (T. australis); Parque Nacional Nahuelbuta, of Telmatobufo. Hypothesized phylogenetic relationships be- Rucapehuen (T. bullocki); and Altos de Vilches (T. venustus).” As tween Telmatobufo and Calyptocephalella (= Caudiverbera) have another example, adult T. venustus was recorded for the first time been proposed (e.g., Correa et al. 2006; Formas and Espinoza in 100 years in 1999 (Stuart et al. 2008; Veloso et al. 2004). The lar- 1975; Frost et al. 2006; Lynch 1978; Núñez et al. 2000). Correa va was not described until 1983 (Díaz et al. 1983), 84 years after et al. (2006) indicated that the closest living lineage of to the species’ description. Veloso (2006) reported that only adult Telmatobufo and Caudiverbera (now Calyptocephalella) (tribe specimens have been observed. Fenolio et al. (2011) reported Calyptocephalellini) are Australian myobatrachids and limno- that the only probable remaining locality for T. venustus is Altos dynastids. The Calyptocephalellini may be ancient; Núñez and de Vilches. During our recent (2011) surveys, we found several Formas (2000) indicated that the lineage that led to the Calypto- specimens of the less frequently encountered Telmatobufo bull- cephalellini diverged around 35 million years ago (mya) and that ocki in Nothofagus forests of the Butamalal River drainage sys- the lineage of Telmatobufo emerged approximately 20–25 mya. tem and in two more sites in the Nahuelbuta Mountains, which San Mauro et al. (2005) and Donoso et al. (2010) suggested that we report here. The tadpole of this species was not described the Calyptocephalellidae may represent a relict lineage of Gond- until 1988 (Formas, 1988), 36 years after the description of the wanian origin. species. The numbers of specimens that have been found in this study likely exceed the total of all Telmatobufo in museum col- Telmatobufo is a Reclusive Taxon Now Only found lections. However, T. bullocki remains one of the least-known in Forest Fragments amphibians in the world, and there are few images of the species available. Exceptions to this can be found at http://ramonreyes- Frogs of the genus Telmatobufo are seldom encountered. carrasco.blogspot.com/, at http://www.arkive.org/telmatobufo/ Cuevas (2010) noted that “Since the description of this genus telmatobufo-bullocki, and in Rabanal and Nuñez (2009) and (Schmidt 1952), specimens of only 20 adults of the three species Diez et al. (2011).

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yet the frogs can move considerable distances from drainage sys- tems. Donoso et al. (2010) found individuals over 300 m from the nearest stream, and we have found them in excess of this dis- tance. Bullock’s False Toads appear to spend much of their non- reproductive time buried beneath forest debris. Favored micro- habitats include areas deep below logs and rocks in Nothofagus forest (Formas et al. 2001; Rabanal and Nuñez 2009). Escobar et al. (2005) found an individual in a pine plantation, Pinus radiata, 90 meters from native forest.

Conservation Threats

All members of the family Calyptocephalellidae are threat- ened with extinction (IUCN 2012). Coastal range Nothofagus forest is declining in quality and quantity (Wolodarsky-Franke and Díaz Herrera 2011; IUCN 2012). Habitat loss, particularly conversion of Nothofagus forests to pine and eucalyptus, is af- fecting Telmatobufo (Cuevas 2010; Fenolio et al. 2011; Rabanal and Núñez 2009; Stuart et al. 2008; Veloso et al. 2004). Remain- ing habitat has been reduced to isolated forest fragments sur- rounded by pine plantations and agriculture (Donoso et al. 2010; Echeverría et al. 2006; Sánchez 2010). Survey work is needed to determine the population status of all species (Stuart et al. 2008; Veloso et al. 2004) but we know that Bullock’s False Toad now 2 Fig. 4. False Toads of the genus Telmatobufo are reclusive for much inhabits less than 500 km , which is spread across several for- of their lives. When they are active, either during nocturnal foraging est fragments (IUCN 2009). Any use of heavy machinery in na- or during reproductive periods, they often inhabit moist drainages tive forests, or even in silviculture areas, could disturb terrestrial and spray zones. habitat as these amphibians burrow in forest litter. Cuevas and Cifuentes (2009) argued that the life history of frogs like Telmato- bufo, having a stream-adapted tadpole with specific habitat re- Distribution and Habitat of Telmatobufo bullocki quirements, puts them at risk owing to anthropogenic environ- mental changes in south Chile. Heavy sediments and siltation All known Telmatobufo are endemic to southern Chile. Bull- of breeding streams from human activities in the areas where ock’s False Toad, Telmatobufo bullocki, is found in coastal range Telmatobufo are found could adversely affect the larval stages Nothofagus forest between 35.9794°S and 38.0000°S and between of these ancient amphibians (Sánchez 2010). Roads (their con- 10 and 800 m elev. (Donoso et al. 2010; Escobar et al. 2005; For- struction and use) and timber harvesting have been document- mas et al. 2001). Most localities are just south of the Río Bío Bío ed as a source of fine sediments washing into aquatic habitats but several new sites north of the river have also been reported and degrading them relative to the needs of amphibians living (Donoso et al. 2010; Escobar et al. 2005). Smith-Ramírez (2004) there (Ashton et al. 2006; Trombulak and Frissell 2000; Welsh and cited a forest fragment (Los Queules National Reserve) as hous- Oliver 1998). Hydrologic alterations (such as “run-of-the-river” ing the northernmost population, also reported in Donoso et al. hydroelectric plants) or impoundments could alter larval habi- (2010). Formas et al. (2001) recognized nine localities but Veloso tat. Hydroelectric plants in Nahuelbuta are already in place and et al. (2004) argued that the species is known from fewer than new facilities are being constructed (e.g., on the Río Picoiquen five localities. The distribution of Telmatobufo bullocki has been and the Río Cayucupil, respectively). Forest fire comprises an- reviewed and/or commented upon by Cei (1962), Péfaur (1971), other significant threat to T. venustus (Veloso 2006), particularly Smith-Ramírez (2004), Escobar et al. (2005), and Donoso et al. in light of the recent conflagrations in south Chile. (2010); Donoso et al. (2010) included a range map. The only two There are additional threats to consider. Emergent infectious protected areas in which the species has been found are Nahuel- amphibian disease (amphibian chytrid fungus, Batrachochy- buta National Park and Los Queules National Reserve (Donoso trium dendrobatidis, or Bd) was first reported in Chile from an et al. 2010; Escobar et al. 2005). A fourth Telmatobufo species, invasive frog, Xenopus laevis (Solís et al. 2010), and subsequently T. ignotus (Cuevas, 2010), has been described from Los Queules in native amphibian species from south Chile (Bourke et al. 2010, National Reserve. Donoso et al. (2010) claim genetic confirma- 2011). Emergent infectious disease has been implicated in the tion of their specimens from the same site as T. bullocki, but this rapid decline of amphibian populations around the world (e.g., has been questioned by Cuevas (2010), who further suggested Berger et al. 1998; Daszak et al. 1999, 2000, 2003; Rachowicz et al. that the material found by Escobar might also prove to be T. ig- 2006). Epidemics may pose a greater extinction risk to species notus. So, the possibilities are that 1) T. bullocki exists in the Cor- with reduced distributions. dillera de la Costa where it 2) may or may not be syntopic with Introduced and invasive species could serve as an additional T. ignotus; or that 3) T. ignotus is conspecific with T. bullocki. We threat to Telmatobufo. There is no question that invasive spe- find the evidence in favor of recognizing T. ignotus as a distinct cies have damaged native Chilean fauna (De Buen 1959; Jaksic species unconvincing and thus regard the status of Telmatobufo 1998; Jaksic and Fuentes 1991; Jaksic et al. 2002; Lobos and Jak- in the Cordillera de la Costa as unresolved. Bullock’s False Toad is sic 2004; Lobos and Measey 2002; Lobos et al. 1999, 2005). The found near coastal range mountain streams (Donoso et al. 2010), rapid expansion of salmonid fishes, post-introduction, has been

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well-documented, as has been the ensuing threat to native wild- Table 1. Results of disease surveillance for amphibian chytrid fungus, Batrachochytrium dendrobatidis or Bd, in 45 wild Bullock’s False Toads, life (Soto et al. 2006). We surveyed streams for three species of Telmatobufo bullocki. Exact locality data / GPS coordinates not pro- Telmatobufo and suggest that there may be a negative correlation vided to ensure the safety of the focal populations. NMR = Nahuelbuta between the presence of introduced trout (Brown Trout, Salmo Mountain Range. No Bd was detected at NMR site No1, a 24% infection trutta, and Rainbow Trout, Oncorhynchus mykiss) and Telmato- rate of Bd was recorded among sampled individuals at NMR site No2, bufo tadpoles (Fenolio et al. 2011). Field observations by one of and a 50% infection rate of Bd was recorded among sampled individu- als at NMR site No3 (the exceptionally small sample size of NMR site the authors (JJN) indicate that when Brown Trout (Salmo trutta) No3 needs to be taken into consideration). are present, Telmatobufo tadpoles are not found; conversely, when Telmatobufo tadpoles are present in a given stream, there Locality Individual Date Result is an increased biodiversity in invertebrates and freshwater fish number (i.e., the ecosystem is intact). Observations reported in Soto-Azat and Valenzuela-Sánchez (2012) support this. During some of our NMR, site No1 Individual No.1 December 2011 Bd negative surveys of Telmatobufo breeding streams, we found that where NMR, site No1 Individual No.2 December 2011 Bd negative trout are absent (one stream for T. venustus, one stream for T. NMR, site No1 Individual No.3 December 2011 Bd negative bullocki, and one stream for T. australis), tadpoles existed. Tad- NMR, site No1 Individual No.4 December 2011 Bd negative poles were not found in many streams where trout were pres- NMR, site No1 Individual No.5 December 2011 Bd negative ent (> 12 streams sampled). During surveys in Altos de Lircay NMR, site No1 Individual No.6 October 2012 Bd negative National Reserve, we encountered adult T. venustus along three NMR, site No1 Individual No.7 October 2012 Bd negative streams but found tadpoles in only two of them. Rainbow Trout NMR, site No2 Individual No.8 February 2012 Bd positive are common in the stream where we have been unable to locate NMR, site No2 Individual No.9 February 2012 Bd positive tadpoles despite intensive searches. A local park ranger and a former landowner indicated that the trout were introduced to NMR, site No2 Individual No.10 February 2012 Bd positive the first stream in the mid-1960s. However, one of us (VM) has NMR, site No2 Individual No.11 February 2012 Bd positive found trout coexisting with T. bullocki tadpoles in many of the NMR, site No2 Individual No.12 February 2012 Bd negative streams in Nahuelbuta. Observations of trout with tadpoles do NMR, site No2 Individual No.13 February 2012 Bd positive not necessarily demonstrate that a negative interaction is absent NMR, site No3 Individual No.14 February 2012 Bd negative and might represent a stage in the process. Trout could prey on NMR, site No3 Individual No.15 February 2012 Bd positive or compete with the tadpoles; introduced fish have been impli- NMR, site No2 Individual No.16 October 2012 Bd negative cated in other montane stream amphibian declines (e.g., Adams NMR, site No2 Individual No.17 October 2012 Bd positive 1999; Collins and Storfer 2003; Kats and Ferrer 2003). NMR, site No2 Individual No.18 October 2012 Bd negative NMR, site No2 Individual No.19 October 2012 Bd positive Our Disease Surveys NMR, site No2 Individual No.20 October 2012 Bd negative Bullock’s False Toad was located in a forest fragment along NMR, site No2 Individual No.21 October 2012 Bd negative the Río Butamalal in January of 2011 during a frog survey orga- NMR, site No2 Individual No.22 October 2012 Bd negative nized by Felipe Rabanal and including Tomas Rivas, Edgardo NMR, site No2 Individual No.23 October 2012 Bd negative Flores, Ramon Reyes, and Virginia Moreno-Puig. They found NMR, site No2 Individual No.24 November 2012 Bd negative two individuals (Rabanal and Moreno-Puig, in press; http://elal- NMR, site No2 Individual No.25 November 2012 Bd negative madecayucupil.blogspot.co.nz/2011/01/excursion-nocturna- NMR, site No2 Individual No.26 November 2012 Bd negative en-butamalal.html). Subsequently, a group of conservationists NMR, site No2 Individual No.27 November 2012 Bd positive found the species there during a field trip after an amphibian NMR, site No2 Individual No.28 November 2012 Bd negative conservation symposium. We surveyed the forest fragment sev- NMR, site No2 Individual No.29 November 2012 Bd negative eral times in December of 2011 and October of 2012. Over 50 NMR, site No2 Individual No.30 November 2012 Bd negative person-hours were spent searching the area for T. bullocki. Ow- NMR, site No2 Individual No.31 November 2012 Bd negative ing to concerns about illegal collecting, the exact location is not included here. We located seven adults, all buried beneath forest NMR, site No2 Individual No.32 November 2012 Bd negative debris. More adult specimens were encountered at a second and NMR, site No2 Individual No.33 November 2012 Bd negative third site in the Nahuelbuta Mountain Range, during Febuary, NMR, site No2 Individual No.34 November 2012 Bd negative October, and November 2012, pursuant to a dissertation project NMR, site No2 Individual No.35 November 2012 Bd negative (Moreno-Puig, in prep.). Skin swabs from all individuals were NMR, site No2 Individual No.36 November 2012 Bd negative sent to the lab of MGL. The results for amphibian chytrid fungus, NMR, site No2 Individual No.37 November 2012 Bd negative Batrachochytrium dendrobatidis (Bd), are reported in Table 1. NMR, site No2 Individual No.38 November 2012 Bd negative Methods for detecting Bd were as follows. Frogs were handled NMR, site No2 Individual No.39 November 2012 Bd negative using a new set of vinyl gloves per specimen. Frogs were individ- NMR, site No2 Individual No.40 November 2012 Bd negative ually swabbed using sterile polyester-tipped applicators (Puritan NMR, site No2 Individual No.41 November 2012 Bd negative Medical, Guilford, Maine, USA), which were gently wiped on the NMR, site No2 Individual No.42 November 2012 Bd negative gular region, the flanks, the bottoms of the hands and feet, and along the ventral surface for 12 passes per body region. When NMR, site No2 Individual No.43 November 2012 Bd negative dry, the tips of the swabs were transferred to individual sterile NMR, site No2 Individual No.44 November 2012 Bd negative tubes and stored at 4°C until extracted and assayed. The tip of NMR, site No2 Individual No.45 November 2012 Bd negative the polyester applicator was transferred to a 2 mL cryovial; 100 µl of Prepman Ultra (Applied Biosystems, Foster City, California,

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USA) was added followed by 50 mg 0.5-mm glass beads for ex- two sites where Bd has been detected, we suspect that T. bullocki traction. The tubes were vortexed and homogenized for 1 min might be a carrier of Bd. Continued disease surveys are under in a Mini BeadBeate (Biospec Products), then placed in boiling way. We caution conservation authorities against any early dis- water for 10 min, cooled for 1 min, centrifuged at 14,000 rpm for missal of the threat of Bd to this species based on our findings; 3 min in a Marathon 16KM centrifuge (Fisher Scientific) after the disease has swept through amphibian populations in Gua- which the liquid was transferred using a micropipette to clean temala and Panama attesting to the potential speed and lethal- 0.6-ml microcentrifuge tubes. The recovered supernatant was ity of the pathogen (e.g., Mendelson et al. 2004). Our results re- then stored at 4°C until assayed using the quantitative real-time quire several years of verification before we can comment with PCR protocol of Boyle et al. (2004) using 1 µl of the extract as the authority as to the effects of Bd on T. bullocki. More intensive DNA template. disease surveys across south Chile should delineate the range of the pathogen, the susceptible species, and the speed at which it Conservation Actions is spreading. Chilean Native Forest Law (Ministerio de Agricultura) pro- An unpublished conservation assessment exists for the Bull- tects vegetation surrounding drainage systems, thereby indi- ock’s False Toad (Sánchez 2010). Subsequently, Soto-Azat et al. rectly protecting amphibian species living adjacent to streams. (2012) mirrored many of the recommendations made by Sán- With T. bullocki inhabiting sites as far away as 300 m or more chez (2010). Although we do not agree with all of the conclusions from the water during their non-reproductive season, they are made by Sánchez (2010), the assessment is a good starting point. susceptible to commercial tree plantation activities, including The document calls for several actions: 1) historical sites should the use of heavy machinery which compresses forest litter (habi- be searched for the frog during all times of the year; 2) vegeta- tat for adult animals). Silviculture activities that might threaten tion type should be recorded across the traditional range of the this species include application of herbicides and fertilizers and species to identify specific plant communities that might be im- mechanical disturbance during harvesting and thinning opera- portant to help identify habitat in unsurveyed areas; 3) study the tions (Donoso et al. 2010). Wider forest buffers around streams condition of the water across the range of the species to identify are needed to retain gallery forest that is critical to the non-re- critical hydrology for larvae; 4) evaluate the best uses of public productive habitat of Bullock’s False Toad (Donoso et al. 2010). outreach; 5) assess the impact of exotic wood culture in the re- Determining where populations of this species can be found gion; 6) evaluate all other amphibian species across the range of is of critical importance (Sánchez 2010; Rabanal and Moreno- T. bullocki; 7) tally area resource extraction; and 8) implement Puig, in prep.). Once occupied areas are identified, an intensive environmental education across the range of the frog. Sánchez effort needs to be made to safeguard these forest fragments. It is (2010) calls for an order of operations that focuses on current not enough to know where remaining populations are; we must threats once vegetation, water, and resource extraction analyses elevate the forest fragments to preserves because few popula- are performed. We respectfully disagree owing to the urgency of tions are contained presently within protected lands. the situation with the few remaining populations of this species. Once populations are identified, long-term monitoring pro- Most forest fragments where this species remains are unprotect- grams must be implemented so that we can better define the ed and could vanish before the proposed analyses are complete. needs of the species and have an understanding of their popu- All of the proposed analyses could be performed after critical lation ecology. These efforts should be based on standardized habitat is secured and without impact on remaining popula- field methods, which need to be developed based on the eco- tions. Sánchez and colleagues found no specimens of T. bullocki, logical knowledge of the species. The “rarity” of T. bullocki is at and their report notes the difficulty of finding specimens and least partly due to inappropriate field techniques. The detection the paucity of basic information regarding biology and ecology. probability of the species is low, but it is also a function of other That study does not suggest captive reproduction as a conserva- variables (observer, weather, time of the year, etc.) and this could tion tool (presumably because they could not find frogs) despite be confounded with low abundance (or absence in some cases). support for assurance colonies by Conservation International, Long-term monitoring of wild populations should be systematic Amphibian Ark, and in published documents such as the Am- and carefully planned. One of the authors (VM) is collecting data phibian Conservation Action Plan. Despite their stated order of for her dissertation which includes habitat use and movement operations, Sánchez (2010) concludes by arguing for protecting patterns, impact of land-use (plantations) on the species, and remaining forest fragments as the main thrust of a conservation conservation genetics (population structure, genetic diversity, effort; we concur. Finally, the report notes considerable local and gene flow). interest in the conservation of the species during conservation Any proposed reduction or impoundment of the flow of lar- workshops. A recommendation from the report calls for estab- val streams and rivers needs to be assessed for potential impact lishing T. bullocki as a flagship species for the conservation of on larvae. How are “run-of-the-river” hydroelectric plants affect- the region. Sánchez (2010) includes several valuable conserva- ing larvae? When drainage systems are reduced to the “environ- tion suggestions. We base our proposals on our field experiences, mental flow” (defined as 10% of the yearly average flow), how from suggestions in the literature, and from recommendations does that impact T. bullocki, especially the larvae? in other conservation assessments. Our recommendations also Systematic studies need to be conducted to determine the presume the ability to find live specimens and in doing so, draw impact of introduced salmonid fishes on the larvae of Telmato- from suggestions proposed in the Amphibian Conservation Ac- bufo. If introduced salmonid fishes are preying on or competing tion Plan (Gascone et al. 2007). with Telmatobufo larvae, the interaction could remove recruit- The presence of Bd in two of three focal populations of T. ment from many, if not most, of the drainage systems across the bullocki is alarming (Table 1); however, no mortality has been range of all known species. If the fish are feeding on the tadpoles, recorded. With frogs persisting at the infected sites, and in light salmonid abatement programs must be implemented to elimi- of an infection rate of 24% and 50% of surveyed individuals at the nate the predator from critical larval habitats. The resistance of

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government and local authorities owing to tourism dollars gen- Campaign and EAZA members for funding our grant proposal, “The erated via fishing could be considerable. Conservation of Chile’s Imperiled Amphibians”—as well as addi- Based on the habitat loss and subsequent population frag- tional EAZA support for VM, Tree Walkers International, the Sophie mentation that all Telmatobufo species have suffered, we pro- Danforth Conservation Biology Fund, the George and Mary Rabb Foundation, the Chicago Board of Trade Endangered Species Fund, pose that ex-situ assurance colonies of Telmatobufo, including T. Cisco Systems, the Chicago Herpetological Society, the Mohamed bullocki, be established immediately. The National Zoo of Chile bin Zayed Species Conservation Fund, the Rufford Small Grants in Santiago, the San Antonio Zoo, and the Atlanta Botanical Gar- Foundation, and the Sedgwick County Zoo. Becas Chile (CONICYT) den have a six-year-old partnership that developed facilities to provided a scholarship to VM for her work on this species. The fol- support a captive assurance colony of Darwin’s Frogs, Rhino- lowing provided permits: Forestal Arauco S.A., Forestal Mininco, SAG derma darwinii, at the National Zoo of Chile. That facility is now (Servicio Agricola Ganadero) Permit Nos. 0373, 2355, 5604, 6977. We operational, amphibian keepers have been trained and are in thank anonymous reviewers for comments and corrections. Klaus place, and the program has reproducing groups of R. darwinii. Busse helped throughout our project. ZooMed Laboratories pro- The National Zoo of Chile in Santiago and the San Antonio Zoo vided generous assistance. Robert Hill and Mark Mandica offered are looking to expand their program to support other threatened suggestions as we developed the conservation breeding centers. Os- valdo Cabezas, amphibian keeper at the National Zoo of Chile, has amphibians of Chile. Facilities exist and permits have been ob- been instrumental in keeping our animals happy and healthy. Jaime tained for the creation of assurance colonies of three species of Garcia and Ricardo León were helpful in implementation of the con- Telmatobufo (T. venustus, T. bullocki, and T. australis). The goal servation breeding labs. T. Elgueta, C. Aguayo, and E. Flores provided is to establish the assurance colonies before wild populations field assistance. drop to numbers so low that assurance colonies cannot be cre- ated. Another goal includes the development of captive care and Literature Cited reproduction protocols, which will be published to share meth- odology with all interested stakeholders. Amphibian specialists Adams, M. J. 1999. Correlated factors in amphibian decline: exotic from the San Antonio Zoo’s conservation program, with experi- species and habitat change in western Washington. J. Wildl. Man- ence in captive breeding of endangered amphibians, will sup- age. 63(4):162–1171. port the effort at the National Zoo of Chile in the same way that Aravena, J. C., M. R. Carmona, C. A. Pérez, and J. J. Armesto. 2002. the zoo was supported while the Darwin’s Frog facility was cre- Changes in tree species richness, stand structure and soil proper- ated and populated with groups of frogs. Fundraising is a joint ties in a successional chronosequence in northern Chiloé Island, venture. Although breeding protocols may be developed outside Chile. Rev. Chilena Hist. Nat. 75:339–360. of Chile, involved stakeholders believe that retaining the assur- Armesto, J. J., C. Donoso, and C. Villagrán. 1994. Desde la era glacial a ance colonies within Chile encourages local enthusiasm for the la industrial: La historia del bosque templado Chileno. Ambiente conservation of native and endangered amphibians, resulting in y Desarrollo 10:64–71. Arroyo, M. T. K., L. Caviares, A. Peñaloza, M. Riveros, and A. M. Faggi. a project that is likely to endure. 1996. Relaciones fitogeográficas y patrones regionales de riqueza Finally, public education and outreach is a critical compo- de especies en la flora del bosque lluvioso templado de Sudaméri- nent of any conservation effort, particularly coming from zoos, ca. In J. J. Armesto, C. Villagrán, and M. T. K. Arroyo (eds.), Ecología aquariums, botanical gardens, and natural history museums de los Bosques Nativos de Chile, pp. 71–99. Editorial Universitaria, (Miller et al. 2004). Our project has developed a bilingual web- Santiago, Chile. site to promote conservation and contact with the public (www. Ashton, D. T., S. B. Marks, and H. H. Welsh Jr. 2006. Evidence of con- savedarwinsfrogs.org). We have developed interpretive signage tinued effects from timber harvesting in redwood forests of north- at the National Zoo of Chile around one of the amphibian breed- western California. Forest Ecol. Manage. 122(1–3):183–193. ing labs to involve the public in the project. Sánchez (2010) pro- Berger, L., R. Speare, P. Daszak, D. E. Green, A. A. Cunningham, C. L. posed promoting T. bullocki as a regional flagship species for Goggin, R. Slocombe, M. A. Ragan, A. D. Hyatt, K. R. McDonald, H. B. Hines, K. R. Lips, G. Marantelli, and H. Parkes. 1998. Chytridio- conservation in the coastal range of south Chile. The suggestion mycosis causes amphibian mortality associated with population is valuable based on local public interest in the species and its declines in the rain forests of Australia and Central America. Proc. conservation; further development of the idea within regional Nat. Acad. Sci. 95(15):9031–9036. conservation circles should be supported. Bourke, J., F. Mutschmann, T. Ohst, P. Ulmer, A. Gutsche, K. Busse, H. Ensuring survival of the ancient Calyptocephalellidae re- Werning, and W. Boehme. 2010. Batrachochytrium dendrobatidis quires an expansion of existing partnerships to involve the zoo- in Darwin’s frog Rhinoderma spp. in Chile. Dis. Aq. Org. 92:217– logical community, amphibian conservation-oriented programs 221. (such as those at the San Antonio Zoo), the Chilean Forestry –––––, T. Ohst, Y. Gräser, W. Böhme, and J. Plötner. 2011. New records industry, and governmental wildlife authorities and respective of Batrachochytrium dendrobatidis in Chilean frogs. Dis. Aq. Org. agencies. Only with support from all pertinent parties can work 95:259–261. Boyle, D. G., D. B. Boyle, V. Olsen, J. A. T. Morgan, and A. D. Hyatt. 2004. toward a comprehensive conservation program occur. Such a Rapid quantitative detection of (Batrachochy- program could be modeled after a collaborative effort like Part- trium dendrobatidis) in amphibian samples using real-time PCR ners for Amphibian and Reptile Conservation (PARC; see Gib- assay. Dis. Aq. Org. 60:141–148. bons 2005; http://www.parcplace.org/). Cei, J. 1962. Batracios de Chile. Universidad de Chile, Santiago, Chile. 128 pp. Acknowledgments.—We are grateful to M. Suyemoto for expert Collins, J. P., and A. Storfer. 2003. Global amphibian declines: sorting technical assistance with PCR analysis, and Karen Gore for assistance the hypotheses. Divers. Distrib. 9(2):89–98. with Bd samples and management of data. The following provided Correa, C., A. Veloso, P. Iturra, and M. A. Méndez. 2006. Phylogenetic funding assistance: the Shared Earth Foundation, the Association of relationships of Chilean leptodactylids: a molecular approach Zoos and Aquariums Conservation Endowment Fund (grant No. 08- based on mitochondrial genes 12S and 16S. Rev. Chilena Hist. Nat. 809), the European Association of Zoos and Aquariums’ Amphibian 79:435–450.

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Herpetological Review, 2013, 44(4), 590–594. © 2013 by Society for the Study of Amphibians and Reptiles Deconstructing a Southern Portuguese Monster: The Effects of a Children’s Story on Children’s Perceptions of Geckos

Amphibians and reptiles carry the unfortunate burden of be- regions and historic sociocultural settings, deriving from folk- ing feared and hated throughout the world. As a result, herpe- lore and cultural-specific interpretations (Bauer and Russell tologists and others dealing directly with herpetofaunal conser- 1987; Ceríaco et al. 2011). These situations are often unknown to vation are often faced with widespread public misinformation the majority of investigators and conservationists, contributing and, in many areas, folklore-based misconceptions that depict to a poor understanding of this phenomenon at a global level. amphibians and reptiles as evil, dangerous, or disease-carrying Additionally, these specific situations are rarely brought to the animals. These situations constitute a serious conservation attention of institutions and international agencies dedicated to problem, as they often result in a lack of support for conserva- the conservation of biodiversity (Mascia et al. 2003). Therefore, tion campaigns, a general disregard for these animals in environ- the importance of bridging the gap between conservation biol- mental impact assessments, and even episodes of direct perse- ogy and the study of folklore is far more pressing than might have cution and killing of animals (Ceríaco 2012). In the reptile world, been imagined some years ago (Mascia et al. 2003). snakes are by far the most feared and misunderstood animals Folklore can be loosely defined as a series of legends, music, globally. This may be explained by cultural interpretations and oral history, proverbs, taboos, jokes, popular beliefs, and cus- snake-related folklore in most human societies, but is also due in toms that are the traditions of a given culture, sub-culture, or part to an apparent genetic aversion that primates have towards group that have been passed from person to person or genera- snakes (Ohman and Mineka 2003; Ohman and Soares 1994). tion to generation by oral transmission or imitation (Medin and However, snakes are not the only herpetofaunal group hated and Atran 1999). Recently, Ceríaco et al. (2011) investigated folklore feared by humans. Other cases are quite specific to particular regarding geckos in southern Portugal and identified several resulting conservation issues. Both gecko species occurring in mainland Portugal, the Mediterranean House Gecko (Hemidac- LUIS MIGUEL PIRES CERÍACO* tylus turcicus) and the Common House Gecko (Tarentola mau- Centro de Estudos de História e Filosofia da Ciência, Universidade de Évora, Palácio do Vimioso, Largo Marques de Marialva, 8, 7000-809 Évora, Portugal ritanica), are depicted as venomous, “sticky,” and “disgusting” and carriers of a dermatological disease, the “cobro,” which affects Museu Nacional de História Natural e da Ciência, Rua da Escola Politécnica, humans through direct or indirect contact by this (Cería- 58, 1250 Lisboa, Portugal co et al. 2011). This idea is quite prevalent throughout south- MARIANA PIMENTEL MARQUES ern Portugal, but also extends through Arab or Arab-influenced Departamento de Biologia, Universidade de Évora, Herdade da Mitra, 7000 countries such as Morocco, Egypt, and Pakistan, suggesting a Évora, Portugal common folkloric origin. However, this concept is nearly absent e-mail: [email protected] in other European countries where both species occur but his- *Corresponding author; e-mail: [email protected] torical Arabic influence has been less substantial (Ceríaco et al. 2011). This widespread folklore directly contributes to the killing

Herpetological Review 44(4), 2013