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 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’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 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’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, 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 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,