An Action Plan for Darwin's Frogs Brings Key Stakeholders Together

A flagship for Austral temperate forest conservation: an action plan for Darwin's frogs brings key stakeholders together

C LAUDIO A ZAT,ANDRÉS V ALENZUELA-SÁNCHEZ,SOLEDAD D ELGADO A NDREW A. CUNNINGHAM,MARIO A LVARADO-RYBAK,JOHARA B OURKE R AÚL B RIONES,OSVALDO C ABEZA,CAMILA C ASTRO-CARRASCO,ANDRES C HARRIER C LAUDIO C ORREA,MARTHA L. CRUMP,CÉSAR C. CUEVAS,MARIANO DE LA M AZA S ANDRA D ÍAZ-VIDAL,EDGARDO F LORES,GEMMA H ARDING,ESTEBAN O. LAVILLA M ARCO A. MENDEZ,FRANK O BERWEMMER,JUAN C ARLOS O RTIZ,HERNÁN P ASTORE A LEXANDRA P EÑAFIEL-RICAURTE,LEONORA R OJAS-SALINAS J OSÉ M ANUEL S ERRANO,MAXIMILIANO A. SEPÚLVEDA,VERÓNICA T OLEDO C ARMEN Ú BEDA,DAVID E. URIBE-RIVERA,CATALINA V ALDIVIA S ALLY W REN and A RIADNE A NGULO

Abstract Darwin’sfrogsRhinoderma darwinii and Rhino- the Austral temperate forests of Chile and Argentina. This derma rufum are the only known species of amphibians recommendation forms part of the vision of the Bination- in which males brood their offspring in their vocal sacs. We al Conservation Strategy for Darwin’sFrogs,whichwas propose these frogs as flagship species for the conservation of launched in . The strategy is a conservation initiative

CLAUDIO AZAT* (Corresponding author, orcid.org/0000-0001-9201-7886), EDGARDO FLORES* Fundación Nahuelbuta Natural, Cañete, Chile MARIO ALVARADO-RYBAK*, ALEXANDRA PEÑAFIEL-RICAURTE* and CATALINA VALDIVIA GEMMA HARDING* Durrell Institute of Conservation and Ecology, School of Sustainability Research Centre, Life Sciences Faculty, Universidad Andres Anthropology and Conservation, University of Kent, Canterbury, UK Bello, Republica 440, Santiago, Chile. E-mail [email protected] ESTEBAN O. LAVILLA* Fundación Miguel Lillo, Consejo Nacional de ANDRÉS VALENZUELA-SÁNCHEZ*,† (Corresponding author, orcid.org/0000- Investigaciones Científicas y Técnicas, San Miguel de Tucumán, Argentina 0002-0445-9156) Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile MARCO A. MENDEZ* and JOSÉ MANUEL SERRANO†† Laboratorio de Genética y E-mail [email protected] Evolución, Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Santiago, Chile SOLEDAD DELGADO and DAVID E. URIBE-RIVERA ( orcid.org/0000-0001-5270- 9052)‡ Organización No Gubernamental Ranita de Darwin, Santiago and FRANK OBERWEMMER Zoo Leipzig, Leipzig, Germany Valdivia, Chile HERNÁN PASTORE Dirección Regional Patagonia Norte, Administración de ANDREW A. CUNNINGHAM*( orcid.org/0000-0002-3543-6504) Institute of Parques Nacionales, San Carlos de Bariloche, Argentina Zoology, Zoological Society of London, London, UK VERÓNICA TOLEDO Fundación Huilo Huilo, Panguipulli, Chile JOHARA BOURKE Department of Zoology, Tierärztliche Hochschule Hannover, Hannover, Germany CARMEN ÚBEDA Universidad Nacional del Comahue, San Carlos de Bariloche, Argentina RAÚL BRIONES Programa Conservación de Especies, División Manejo Ecosistémico, Bioforest, Forestal Arauco, Concepción, Chile SALLY WREN* Department of Zoology, University of Otago, Dunedin, New Zealand OSVALDO CABEZA* Zoológico Nacional, Parque Metropolitano de Santiago, Santiago, Chile ARIADNE ANGULO IUCN SSC Amphibian Specialist Group, Toronto, Canada

CAMILA CASTRO-CARRASCO*,§,**, CLAUDIO CORREA* and JUAN CARLOS ORTIZ* *Also at: IUCN SSC Amphibian Specialist Group, Toronto, Canada Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas † & Centro de Reproducción ex situ de la Ranita de Darwin (Rhinoderma Also at: Organización No Gubernamental Ranita de Darwin, Santiago and darwinii), Universidad de Concepción, Concepción, Chile Valdivia, Chile ‡ ANDRES CHARRIER* Centro CapesUC, Pontificia Unversidad Católica de Chile, Also at: School of Biosciences, University of Melbourne, Melbourne, Australia Santiago, Chile §Also at: Facultad de Medicina Veterinaria, Universidad San Sebastián, MARTHA L. CRUMP Department of Biology and The Ecology Center, Utah State Concepción, Chile University, Logan, USA **Also at: Escuela de Medicina Veterinaria, Facultad de Recursos Naturales y CÉSAR C. CUEVAS* Departamento de Ciencias Biológicas y Químicas, Medicina Veterinaria, Universidad Santo Tomás, Concepción, Chile Universidad Católica de Temuco, Temuco, Chile ††Also at: Laboratorio de Comunicación Animal, Vicerrectoría de Investigación MARIANO DE LA MAZA and MAXIMILIANO A. SEPÚLVEDA Corporación Nacional y Postgrado, Universidad Católica del Maule, Talca, Chile Forestal, Ministerio de Agricultura, Santiago, Chile

SANDRA DÍAZ-VIDAL and LEONORA ROJAS-SALINAS División de Recursos Naturales Received  May . Revision requested  July . y Biodiversidad, Ministerio del Medio Ambiente, Santiago, Chile Accepted  October . First published online  July .

This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, Downloaded fromdistribution, https://www.cambridge.org/core and reproduction in any medium,. IP address: provided 170.106.202.58 the original work, on 03 is properly Oct 2021 cited. at 04:48:39, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/termsOryx, 2021, 55(3),. https://doi.org/10.1017/S0030605319001236 356–363 © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319001236 Action plan for Darwin's frogs 357

led by the IUCN SSC Amphibian Specialist Group, which in  convened  governmental, non-profit and private organizations from Chile, Argentina and elsewhere. Darwin’s frogs are iconic examples of the global amphibian conservation crisis: R. rufum is categorized as Critically Endangered (Possibly Extinct) on the IUCN Red List, and R. darwinii as Endangered. Here we articulate the conservation planning process that led to the development of the conservation strategy for these species and present its main findings and recommendations. Using an evidence-based approach, the Bi- national Conservation Strategy for Darwin’s Frogs contains a comprehensive status review of Rhinoderma spp., including critical threat analyses, and proposes  prioritized conservation actions. Its goal is that by , key information gaps on

Rhinoderma spp. will be filled, the main threats to these spe- PLATE 1 A brooding male southern Darwin’sfrogRhinoderma cies will be reduced, and financial, legal and societal support darwinii in a typical humid substrate of the Valdivian temperate will have been achieved. The strategy is a multi-disciplinary, forest. transnational endeavour aimed at ensuring the long-term viability of these unique frogs and their particular habitat.

Keywords Amphibians, Argentina, Chile, conservation et al., ). Rhinoderma rufum has not been recorded since strategy, Darwin’s frogs, extinction, Rhinoderma darwinii,  and remaining populations of R. darwinii are small and Rhinoderma rufum isolated (Soto-Azat et al., a;IUCN,). Darwin’sfrogs are found only in native forest (generally old-growth), and Supplementary material for this article is available at R. darwinii abundance has been positively correlated with    doi.org/ . /S the structural complexity of its forest habitat (Valenzuela- Sánchez et al., a). Although habitat loss is a threat, population declines and extirpations have also been documented within protected areas and undisturbed ecosystems (Crump Introduction & Veloso, ; Soto-Azat et al., a). Recently, there has been growing concern about Darwin’s alting biodiversity loss depends largely on developing frogs, evidenced by several independent and uncoordinated effective conservation policies and planning (Johnson H research and conservation efforts. The majority (%) of all et al., ). Evidence-based, inclusive, participatory conser- publications on Darwin’s frogs indexed in the Web of vation strategies are recommended when specific actions Science were published during –,whenanumber are needed to save species from extinction (IUCN, ). of in situ and ex situ conservation projects were established Key species can act as umbrellas or flagships, transforming for R. darwinii. Thus, we identified an opportunity for species-level conservation plans into ecosystem-wide bene- collaboration to provide efficient and cost-effective conserva- fits (Superina et al., ). tion outcomes for these unique and highly threatened frogs. The northern and the southern Darwin’sfrog(Rhino- In  the Chilean section of the IUCN SSC Amphibian derma rufum and Rhinoderma darwinii)arenamedafter Specialist Group convened stakeholders to develop a conser- Charles Darwin, who was the first to collect R. darwinii, vation plan for Darwin’s frogs, and as a result the Binational in . These species are the only known amphibians in Conservation Strategy for Darwin’s Frogs was launched in which the males brood their offspring within their vocal . Here we summarize the process of the strategy’s devel- sacs (Plate ). In R. rufum the later larval stages develop in opment, present its main findings and recommendations and water, whereas in R. darwinii the entire larval development, discuss the major challenges and opportunities of implemen- lasting up to  weeks and including metamorphosis, takes tation. This work adds to the scarce peer-reviewed literature place within the male’s vocal sac (Formas et al., ; on species conservation planning and seeks to stimulate its Formas, ; Supplementary Fig. ). Endemic to the Austral use as a biodiversity conservation tool. temperate forests of South America, both species are highly threatened as a result of dramatic population declines, par-   ticularly during the last decades (Crump & Veloso, ; Study area Bourke et al., ; Soto-Azat et al., a). The habitat of Darwin’s frogs is an ecoregion characterized by a high degree The Austral temperate forests, which include the habitat of of endemism and is thus of high conservation priority (Myers Darwin’s frogs (– °S), cover .  million ha, mainly in

Oryx, 2021, 55(3), 356–363 © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319001236 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.58, on 03 Oct 2021 at 04:48:39, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605319001236 358 C. Azat et al.

Methods

Conservation assessment

In July ,  Chilean herpetologists met at Universidad Andres Bello in Santiago to update the IUCN Red List assessment of Chilean amphibians (Soto-Azat et al., ). This work highlighted the urgent need for conservation planning for Darwin’s frogs. Re-assessments of R. darwinii and R. rufum followed the IUCN Red List methodology: literature and data searches, assessments by experts and external review.

Development of the strategy

Development of the Binational Conservation Strategy for Darwin’s Frogs was facilitated by an Amphibian Specialist Group co-chair, a programme officer and a thematic group chair and followed IUCN guidelines for species conservation planning (IUCN, ). Initially, a -day symposium in September  convened  participants interested in the conservation of Darwin’s frogs. Here,  national and international speakers presented advances on Rhinoderma spp. research and conservation, and discussed IUCN guidelines for effective conservation planning (IUCN, ). Subsequently,  stakeholders that had been selected for their expertise, influence, and representation of relevant organizations, attended a -day conservation strategy workshop where we: () formulated the strategy’s vision, () defined the strategy’s time frame, () discussed the current status of Darwin’s frogs, () assessed the challenges, barriers and threats to their conservation, () established working groups (see below), () developed conservation goals, objectives and actions, () prioritized objectives and actions and () elected the coordination structure. We

FIG. 1 Distribution of Darwin’s frogs in Chile and Argentina. formed four working groups based on identified conserva- Historical distribution of Rhinoderma rufum, Rhinoderma tion needs: () habitat loss, () captive breeding, research darwinii and the area of sympatry around Concepción. Localities and climate change, () policy and education, and () dis- with known current presence of R. darwinii are shown in solid eases and invasive species. Following a SMART (Specific, dots. No population of R. rufum is currently known, but Measurable, Achievable, Realistic and Time-bound) ap- historical localities are shown in open dots. There is one unusual proach, each working group proposed goals, objectives and historical record for R. rufum in the Chilean foothills of the Andes (Barros, ). actions, which were later discussed, validated and prioritized by all workshop participants. After the workshop, a draft of the strategy was distributed among participants and others     Chile but also in Argentina ( . and . million ha for involved in the development of the strategy, for comment  R. rufum and R. darwinii, respectively; IUCN, ). and approval. Rhinoderma rufum is endemic to the coastal range of Chile at – m altitude (Bourke et al., ; Soto-Azat   et al., a; Cuevas, ). Rhinoderma darwinii is found Results in both the coastal range of Chile (including Mocha Island and the Chiloé Archipelago) and the Andes of Chile and Conservation assessment Argentina (Soto-Azat et al., a)at–, m altitude (Úbeda & Pastore, ). Historical distributions of Rhino- Rhinoderma rufum is categorized as Critically Endan- derma spp. are shown in Fig. . gered (Possibly Extinct) based on criterion D because its

FIG. 2 Conceptual model showing a threat assessment for Darwin’s frogs (R. rufum and R. darwinii). We identified direct and indirect threats, barriers presented by lack of knowledge, contributing factors and pressures, and plotted their interactions with each other and within the binational conservation strategy. *OIE = World Animal Health Organization.

population size is estimated to be ,  mature individuals and () provide the financial, legal and societal support (IUCN, ). The species has not been recorded since  needed for the proposed conservation actions. To this despite intense searches across its historical range (Busse, end, the strategy contains  actions, grouped under  ; Bourke et al., ; Soto-Azat et al., a;Cuevas, objectives (Supplementary Table ). Each conservation ac- ). Rhinoderma darwinii is categorized as Endangered tion lists responsible stakeholders, deadlines, indicators, following criteria Bab(iii) (IUCN, )because()its potential collaborators and funding sources. The strategy  current area of occupancy is estimated to be  km (IUCN ASG–Chile, ) has been distributed among rele-  (,  km threshold; B), () extant populations are small vant authorities, conservation organizations, local commu- and isolated (a), and () the extent and quality of its re- nities and the general public. maining habitat continues to decline (b(iii); Crump & Veloso, ; Soto-Azat et al., a; Uribe-Rivera et al., ; Bourke et al., ). Only R. darwinii has been kept Website and bred in captivity. The full Binational Conservation Strategy for Darwin’s Frogs can be downloaded from the strategy’s website (see A conservation strategy full reference in IUCN ASG–Chile, ). This website provides information on Rhinoderma biology and conservation ‘ ’ Under the vision Darwin s frogs, unique in the world for along with relevant literature and other resources. The strat- their reproductive peculiarity, are conserved and valued egy is intended to be a dynamic and adaptive document, as an emblem for the protection of the native forests of and the website will help with the coordination of identified ’ southern Chile and Argentina , the Binational Conservation actions. Strategy for Darwin’s Frogs was launched in October . The strategy is divided into two main components: a status review of Rhinoderma spp., and the conservation strategy Darwin’s Frog Alliance itself, comprising a threat assessment (Fig. ) and a list of prioritized conservation actions. The strategy aims to A key outcome of the conservation planning process was achieve the following goals by :() obtain key informa- the creation of the Darwin’s Frog Alliance, a network of  tion on the biology, management and status of Rhinoderma individuals, representing  institutions and a diverse array populations, () reduce the main threats to Darwin’s frogs, of stakeholders (from academia, government, zoological

institutions, local communities, NGOs and the private sector; Supplementary Table ), to enhance collaboration for the conservation of Darwin’s frogs. The Alliance is led by members of the Amphibian Specialist Group, and endorsed by the Chilean and Argentinian Ministries of Environment.

Threat assessment

The status review supported previous claims that the decline of Darwin’s frogs has been largely driven by habitat loss, chytridiomycosis and climate change (Bourke et al., , , ; Soto-Azat et al., a, b; Uribe-Rivera et al., ; Valenzuela-Sánchez et al., ). Here we provide FIG. 3 Boxplot (median, th, and th percentiles) of relative a brief synthesis of this review. changes in the extent of potential habitat (suitable and accessible) of R. darwinii, projected to two temporal windows ( and ) and two climate change scenarios (Relative Status of populations Using species distribution modelling, Concentration Pathway . and .; IPCC, ). The dashed line Bourke et al. () identified areas with potential remnant R. represents a scenario of no change compared to the present rufum populations, providing guidance for future efforts to situation. rediscover this species. Soto-Azat et al. (a) dated its extinction to  (%CI:–) using historical sight- ings. In contrast, R. darwinii is found in small and isolated Chilean amphibians collected since the s (Soto-Azat populations (Soto-Azat et al., a; Valenzuela-Sánchez et al., et al., b). This coincides with the documented onset of ). During the development of the strategy, we iden- South American amphibian declines (Scheele et al., ). tified  extant populations in Chile and  in Argentina Surveys in Chile have demonstrated that B. dendrobatidis (Fig. ). In Chile, R. darwinii has recently disappeared from, is infecting R. darwinii in the wild (Bourke et al., ), or drastically declined in, many localities where it was abun- with evidence of lethal chytridiomycosis (Soto-Azat et al., dant only decades ago (Crump & Veloso, ; Soto-Azat b), which leads to extirpation of infected populations et al., a).Thesizeofextantpopulationsisc.– re- (Valenzuela-Sánchez et al., ). productive individuals (Crump, ;Soto-Azatetal.,a; Valenzuela-Sánchez et al., , , a). In Argentina, the species has been less well studied but, based on museum Climate change Because of its specific habitat requirements collections, it was probably much more abundant in the past (Valenzuela-Sánchez et al., a), slow life-history strategy (Úbeda & Pastore, ). (Valenzuela-Sánchez et al., ) and dispersal limitations (Valenzuela-Sánchez et al., , b), Rhinoderma spp. are expected to be particularly susceptible to climate change Habitat loss The original habitats of R. rufum, the Coastal (Soto-Azat et al., a). Using a dispersal-constrained species Mediterranean and Maulino deciduous forests (– °S), have distribution model, Uribe-Rivera et al. () estimated that been almost completely replaced by exotic pine and eu- during –, climate change led to a reduction of suitable calypt plantations and agriculture, with , %ofMaulinofor- habitat for this species by –%. Bourke et al. ()pre- est remaining (Smith-Ramírez, ;Echeverríaetal.,). dicted an expansion of climatically suitable areas for R. dar- The Valdivian temperate rainforest (– °S) is the typical winii by , especially in the south of its range. However, habitat of R. darwinii. To the north, the situation for R. dar- unless assisted by translocations, R. darwinii would not nat- winii is similar to that for R. rufum, but further south the urally colonize most of the emerging suitable areas (Uribe- native forest becomes more continuous as the coverage of Rivera et al., ). Incorporating dispersal limitations protected areas increases, thus providing more suitable habi- analyses of climate change projections for  and  tat for the species. show reductions of –% in the potential distribution of R. darwinii (Fig. ; Uribe-Rivera et al., ). Amphibian chytridiomycosis Caused by the fungus Batr- achochytrium dendrobatidis, this emerging disease is known Other threats for its catastrophic and ongoing impacts on amphibian populations worldwide (Scheele et al., ). This pathogen Collection of wild Rhinoderma spp., mainly for hobbyists has been identified from museum specimens of wild and museums, was common in the past (J.C. Ortiz, pers.

obs., ; Soto-Azat et al., a; Supplementary Fig. ). () in this country are in two large and contiguous national Other threats and barriers include livestock farming in for- parks: Lanín and Nahuel Huapi (Úbeda & Pastore, ). est habitats, non-compliance with current legislation, and Private reserves (which cover . million ha in central and lack of public awareness and engagement (Fig. ). southern Chile) are key for the conservation of Darwin’s frogs. Similarly, a partnership with the forestry sector can boost the protection of Darwin’s frog habitat. Forestal Ongoing conservation Arauco is the largest forestry company in South America (owning . million ha in Chile and Argentina) and a par- Although there are  protected areas ( in Chile and two ticipating member of the Binational Conservation Strategy in Argentina) within the range of R. darwinii, none protect for Darwin’s Frogs. Most of their land is planted with exotic any of the historical sites of R. rufum. Since , three pines and eucalypts, but . , ha of native forests are in situ conservation projects have been implemented for protected as conservation areas, five of which currently pro- R. darwinii: in Huilo Huilo, Tantauco and Melimoyu pri- tect populations of R. darwinii (Arauco, ). Improving vate parks. Currently, there are two independent ex situ con- the conservation status of Darwin’s frogs depends on in- servation projects for R. darwinii: one led by Universidad creasing the area and connectivity of its habitat (Soto-Azat de Concepción in conjunction with Zoo Leipzig, Germany et al., a). The traditional approach to achieving this (since ), and another by the National Zoo of Chile would be to create or expand protected areas (Smith- (since ). There are also several education initiatives fo- Ramírez, ), but a novel initiative is being implemented cused on Darwin’s frogs: one at the National Zoo of Chile in southern Chile. In collaboration with local landowners (visited by . , people in ), a Darwin’s frog edu- and regional government, NGO Ranita de Darwin promotes cation centre in Huilo Huilo (. , visitors in ), amphibian conservation by voluntary agreements (Ranita and an education programme run by NGO Ranita de Dar- de Darwin, a) to encourage planting of native forest, win, which has reached . , people in local commu- habitat management and monitoring of the Darwin’s frog nities within the range of Rhinoderma spp. population by landowners (Santangeli et al., ).

Discussion Managing wildfires Wildfires are considered an emerging ’   Multi-pronged strategies that combine research, manage- threat to Darwin s frogs. During and , central and ment, education and policy are required to achieve suc- southern Chile experienced the largest wildfires in recent .     cessful species conservation (Superina et al., ). The history; , ha were burnt in , % of which  Binational Conservation Strategy for Darwin’s Frogs is a involved native forest (CONAF, ). Climate change pro- multi-sectoral, participatory effort and follows an evidence- jections predict a trend of increasing damage by wildfires  based process to achieve the long-term conservation of (Urrutia-Jalabert et al., ). Fire prevention or rapid con- Darwin’s frogs. Additionally, this strategy promotes these tainment is a key aspect of future conservation management species as non-traditional flagships for the conservation of plans for Rhinoderma spp. the Austral temperate forest, which has been identified as ’  one of the world s biodiversity hotpots (Myers et al., Reintroductions There are plans to reintroduce R. darwinii  ). individuals from captive breeding projects to areas from which they have been extirpated, or to use them for population reinforcement. Translocation success will depend on Conservation challenges evidence-based management of the threats that led to the extirpations or declines at the release sites (IUCN, ; Habitat protection The coastal range of central Chile has Molina-Burgos et al., ). the greatest terrestrial species richness in the country, but almost entirely lacks protection and has experienced a rapid loss of biodiversity (Smith-Ramírez, ), especially Policy and public engagement The Chilean Ministry of since the s (Echeverría et al., ). If R. rufum is redis- Environment administers the legal instrument of Recovery, covered, it will be challenging to guarantee its immediate in Conservation and Management (RECOGE) Plans to execute situ protection, considering that it may occur on private research, protection and conservation programmes for threat- land. In contrast, protected areas have allowed the persis- ened species. The Ministry has been part of the development tence of R. darwinii. In Chile, % of known populations of the Binational Conservation Strategy for Darwin’sFrogs ( out of ; Fig. ) are within areas with some level of pro- since its inception; inclusion of RECOGE criteria in the strat- tection, mostly private parks (%). Although , % of the egy will facilitate its adoption. In Argentina, where R. darwi- range of R. darwinii lies in Argentina, all known populations nii is present only in two national parks, the National Park

Administration is responsible for implementing the strategy. robust instrument to combat the amphibian extinction cri- Once signed by the environment authorities of both coun- sis. This multi-disciplinary conservation planning initia- tries, the strategy will facilitate interdisciplinary and inter- tive is an effort to coordinate existing work in Chile and national working amongst public agencies. Another area in Argentina and to catalyse further conservation actions which both countries can take action involves animal health based on scientific evidence. Successful implementation of departments, with the enforcement of amphibian import reg- the strategy will help to ensure the long-term viability of ulations and the implementation of biosecurity protocols these unique frogs and, by extension, of their habitat, the aimed at limiting the spread of B. dendrobatidis (and Austral temperate forest. other invasive species) both at national and local levels (Valenzuela-Sánchez et al., ; Bacigalupe et al., ). Acknowledgements We thank Zoo Leipzig, Huilo Huilo Foundation, Universidad Andres Bello, Fundación MERI, Forestal Official recognition of the strategy is also relevant for estab- Arauco, Darwin Vineyards and Cerveza Tropera for financial support lishing nation-wide conservation education programmes. for the development of the Binational Conservation Strategy for Improving the public’s knowledge of and attitudes towards Darwin’s Frogs, and Anne Baker (Amphibian Ark) for her support Darwin’s frogs will be critical to achieve the strategy’sobjec- with the preparation of facilitation materials. CA and AV-S are sup- tives (Márquez-García et al., ). ported by Fondecyt grants no. 1181758 and 3180107, respectively.

Author contributions Writing: CA, AV-S, AAC; revision: all authors. Future research Conflict of interests None. Studies on population trends and threats to R. darwinii in Argentina are lacking and little is known about the genetic Ethical standards This work abided by the Oryx guidelines on diversity of Rhinoderma. There have been no genetic studies ethical standards. of R. rufum and limited information is available for R. darwinii (Crump & Veloso, ). A characterization of the genetic structure of Rhinoderma spp. across their References range would inform in situ management and assessment   of potential reintroductions using captive-bred animals ARAUCO ( ) Sustainability Report. Forestal Arauco,  Santiago, Chile. arauco.cl/na/sostenibilidad/reportes-de- (IUCN, ). sostenibilidad [accessed  February ]. Other critical investigations include improving our un- BACIGALUPE, L.D., VÁSQUEZ, I.A., ESTAY, S.A., VALENZUELA- derstanding of two known major threats: amphibian chytrid- SÁNCHEZ, A., ALVARADO-RYBAK, M., PEÑAFIEL-RICAURTE,A. iomycosis and climate change (Soto-Azat et al., b; et al. () The amphibian-killing fungus in a biodiversity hotspot: Uribe-Rivera et al., ). For R. darwinii, research is under- identifying and validating high-risk areas and refugia. Ecosphere, ,e. way to assess mitigation actions addressing infections with  ‘ ’  BARROS,R.( ) Notas sobre el sapito vaquero (Rhinoderma B. dendrobatidis (Ranita de Darwin, b). Besides phe- darwinii Dum. & Bibron). Revista Chilena de Historia Natural, notypic plasticity, amphibians have two options to deal , –. with climate change: evolutionary adaptation and dispersal BOURKE, J., ULMER, P., MUTSCHMANN, F., BUSSE, K., WERNING,H.&  ’ (Uribe-Rivera et al., ). No information exists concerning BÖHME,W.( ) Batrachochytrium dendrobatidis in Darwin s frog (Rhinoderma darwinii), Chile. Diseases of Aquatic Organisms, evolutionary or phenotypic responses to rapid and ongoing  –  , . climate change (IPCC, ); studies addressing this issue BOURKE, J., BUSSE,K.&BÖHME,W.() Searching for a lost frog will allow us to predict, and potentially mitigate, the impacts (Rhinoderma rufum): identification of the most promising areas for of climate change on Rhinoderma. future surveys and possible reasons of its enigmatic decline. North-Western Journal of Zoology, , –. BOURKE, J., BUSSE,K.&BÖHME,W.() Potential effects of climate Conclusions change on the distribution of the Endangered Darwin’s frog. North-Western Journal of Zoology, , –. The Binational Conservation Strategy for Darwin’s Frogs is BUSSE,K.() Darwin’s frogs in danger; Rhinoderma, are there any  – the first conservation strategy exclusively dedicated to am- Rhinoderma rufum left in Chile? Reptilia, , . CONAF (CORPORACIÓN NACIONAL FORESTAL)() Análisis de la phibians at the species level in both Chile and Argentina. Afectación y Severidad de los Incendios Forestales Ocurridos en Enero It provides an informative case study of a comprehensive y Febrero de  sobre los Usos de Suelo y los Ecosistemas Naturales programme for iconic, yet under-appreciated, fauna and Presentes entre las Regiones de Coquimbo y Los Ríos de Chile. an example of how small ectothermic animals can become Informe Técnico, Santiago, Chile.  ’ flagship species for conservation, a role usually assigned to CRUMP, M.L. ( ) Natural history of Darwin s frog Rhinoderma darwinii. Herpetological Natural History, , –. larger charismatic mammals. The development of the strat- CRUMP, M.L. & VELOSO,A.() El aporte de observaciones de egy is a constructive example of stakeholders, including local terreno y del análisis genético para la conservación de Rhinoderma communities and industry, working together to generate a darwinii en Chile. In Historia, Biodiversidad y Ecología de los

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