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

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A flagship for Austral temperate forest conservation: 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
                         CLAUDIO AZAT, ANDRÉS VALENZUELA-SÁNCHEZ, SOLEDAD DELGADO
                       ANDREW A. CUN NI NGHAM, MARIO ALVARADO-RYBAK, J OH ARA B OURKE
             RAÚL BRIONES, OS VA L DO CAB EZA, CA M I LA CASTRO-CARRASCO, ANDRES CHARRIER
              CLAUDIO CORREA, M ARTHA L. CRUMP, CÉSAR C. CUE VAS, MARIANO DE LA M AZA
              SANDRA DÍAZ-VIDAL, EDGARDO FLORES, GEMMA HARDING, ESTEBAN O. LAVILLA
             MARCO A. MENDEZ, FRANK OBERWEMMER, JUAN CARLOS ORTIZ, HERNÁN PASTORE
                                   ALEXANDRA PEÑAFIEL-RICAURTE, LEONORA ROJAS-SALINAS
                    JOSÉ MANUEL SERRANO, MAXIMILIANO A. SEPÚLVEDA, VERÓNICA TOLEDO
                             CARMEN ÚBEDA, DAVID E. URIBE-RIVERA, CATALINA VALDIVIA
                                                            S A L L Y W R E N and A R I A D N E A N G U L O

            Abstract Darwin’s frogs Rhinoderma 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’s Frogs, which was
            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 claudio.azat@gmail.com
                                                                                                           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 andresvalenzuela.zoo@gmail.com                                                          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 .

            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,
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A flagship for Austral temperate forest conservation: an action plan for Darwin's frogs brings key stakeholders together
2         C. Azat et al.

             led by the IUCN SSC Amphibian Specialist Group, which in
              convened  governmental, non-profit and private or-
             ganizations from Chile, Argentina and elsewhere. Darwin’s
             frogs are iconic examples of the global amphibian conserva-
             tion 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 conserva-
             tion 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’s frog Rhinoderma
             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 via-
             bility 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’s frogs
                                                                                                     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, popu-
                                                                                                     lation 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
             H       alting biodiversity loss depends largely on developing
                     effective conservation policies and planning (Johnson
             et al., ). Evidence-based, inclusive, participatory conser-
                                                                                                     frogs, evidenced by several independent and uncoordinated
                                                                                                     research and conservation efforts. The majority (%) of all
                                                                                                     publications on Darwin’s frogs indexed in the Web of
             vation strategies are recommended when specific actions
                                                                                                     Science were published during –, when a number
             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’s frog (Rhino-
                                                                                                     In  the Chilean section of the IUCN SSC Amphibian
             derma rufum and Rhinoderma darwinii) are named after
                                                                                                     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

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A flagship for Austral temperate forest conservation: an action plan for Darwin's frogs brings key stakeholders together
Action plan for Darwin’s frogs   3

                                                                                                    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 dis-
                                                                                                    cussed 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 strat-
                                                                                                    egy workshop where we: () formulated the strategy’s vision,
                                                                                                    () defined the strategy’s time frame, () discussed the cur-
                                                                                                    rent 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

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4         C. Azat et al.

             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 pro-
                                                                                                     vides 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

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Action plan for Darwin’s frogs   5

           institutions, local communities, NGOs and the private sec-
           tor; 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 ex-
           tinction 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). The size of extant populations is c. – re-                          (Valenzuela-Sánchez et al., ).
           productive individuals (Crump, ; Soto-Azat et al., 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 , % of Maulino for-                            habitat for this species by –%. Bourke et al. () pre-
           est remaining (Smith-Ramírez, ; Echeverría et al., ).                            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.

           Oryx, Page 5 of 8 © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319001236
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6         C. Azat et al.

             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 popu-
                                                                                                     lation 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’s Frogs
             ( 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

                                  Oryx, Page 6 of 8 © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319001236
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Action plan for Darwin’s frogs                    7

           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’s objec-                         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
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