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
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 . 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,
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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’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
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
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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 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
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
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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 Bab(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
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
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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, 2021, 55(3), 356–363 © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319001236
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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, 2021, 55(3), 356–363 © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319001236
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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
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- B AC I G A L U P E , L.D., V Á S Q U E Z , I.A., E S T AY , S.A., V A L E N Z U E L A -
derstanding of two known major threats: amphibian chytrid- S Á N C H E Z , A., A LVA R A D O -R Y B A K , M., P E Ñ A F I E L -R I C A U R T E , 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 B A R R O S , 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 B O U R K E , J., U L M E R , P., M U T S C H M A N N , F., B U S S E , K., W E R N I N G , H. &
(Uribe-Rivera et al., ). No information exists concerning B Ö H M E , 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 B O U R K E , J., B U S S E , K. & B Ö H M E , 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, , –.
B O U R K E , J., B U S S E , K. & B Ö H M E , 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 B U S S E , K. () Darwin’s frogs in danger; Rhinoderma, are there any
Rhinoderma rufum left in Chile? Reptilia, , –.
the first conservation strategy exclusively dedicated to am-
CONAF (C O R P O R AC I Ó N N A C I O N A L F O R E S T A L ) () 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.
C R U M P , M.L. () Natural history of Darwin’s frog Rhinoderma
flagship species for conservation, a role usually assigned to
darwinii. Herpetological Natural History, , –.
larger charismatic mammals. The development of the strat- C R U M P , M.L. & V E LO S O , 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
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. Bibliothek der Stiftung Tierärztliche Hochschule Hannover, on 17 Jul 2021 at 11:02:23, subject to the Cambridge Core terms of use, available at
https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605319001236Action plan for Darwin's frogs 363
Bosques Costeros de Chile (eds C. Smith-Ramírez, J.J. Armesto & S C H E E L E , B.C., P A S M A N S , F., B E R G E R , L., S K E R R AT , L.F., M A R T E L , A.,
C. Valdovinos), pp. –. Editorial Universitaria, Santiago, Chile. B E U K E M A , W. et al. () Amphibian fungal panzootic causes
C U E VA S , C.C. () Native forest loss impacts on anuran diversity: catastrophic and ongoing loss of biodiversity. Science, , –.
with focus on Rhinoderma rufum (Philippi ) S M I T H -R A M Í R E Z , C. () The Chilean coastal range: a vanishing
(Rhinodermatidae) in coastal range, south-central Chile. center of biodiversity and endemism in South American temperate
Gestión Ambiental, , –. rainforests. Biodiversity and Conservation, , –.
E C H E V E R R Í A , C., C O O M E S , D., S A L A S , J., R E Y -B E N AY A S , J.M., L A R A , S OT O -A Z AT , C., V A L E N Z U E L A -S Á N C H E Z , A., C O L L E N , B.,
A. & N E W T O N , A. () Rapid deforestation and fragmentation of R O W C L I F F E , J.M., V E LO S O , A. & C U N N I N G H A M , A.A. (a) The
Chilean Temperate Forests. Biological Conservation, , –. population decline and extinction of Darwin’s frogs. PLOS ONE,
F O R M A S , J.R. () External morphology, chondrocranium, , e.
hyobranchial skeleton, and external and internal oral features S OT O -A Z AT , C., V A L E N Z U E L A -S Á N C H E Z , A., C L A R K E , B.T., B U S S E ,
of Rhinoderma rufum (Anura, Rhinodermatidae). Zootaxa, K., O R T I Z , J.C., B A R R I E N T O S , C. et al. (b) Is chytridiomycosis
, –. driving Darwin’s frogs to extinction? PLOS ONE, , e.
F O R M A S , J.R., P U G Í N , E. & J O R Q U E R A , B. () La identidad del S OT O -A Z AT , C., V A L E N Z U E L A -S Á N C H E Z , A., O R T I Z , J.C., D Í A Z -
batracio chileno Heminectes rufus Philippi, . Physis Section C, P Á E Z , H., C A S T R O , C., C H A R R I E R , A. et al. () ASG Chile leads
, –. update of the extinction risk of Chilean amphibians for the IUCN
IPCC () Climate Change : Synthesis Report. Contribution of Red List of Threatened Species. FrogLog, , –.
Working Groups I, II and III to the Fifth Assessment Report of the S U P E R I N A , M., C O R T É S D U A R T E , A. & T R U J I L LO , F. () Connecting
Intergovernmental Panel on Climate Change (Core Writing Team, research, management, education and policy for the conservation of
eds R.K. Pachauri & L.A. Meyer). IPCC, Geneva, Switzerland. armadillos in the Orinoco Llanos of Colombia. Oryx, , –.
IUCN () Guidelines for Reintroductions and Other Conservation Ú B E D A , C.A. & P A S T O R E , H. () Distribución de Rhinoderma
Translocations. Version .. IUCN Species Survival Commission, darwinii en Argentina (Anura, Rhinodermatidae), con Comentarios
Gland, Switzerland. portals.iucn.org/library/efiles/documents/ sobre su Estatus y Conservación. Resúmenes to Congreso Chileno
-.pdf [accessed August ]. de Anfibios y Reptiles, Red Chilena de Herpetología, Valdivia, Chile.
IUCN () Guidelines for Species Conservation Planning. Version U R I B E -R I V E R A , D.E., S O T O -A Z A T , C., V A L E N Z U E L A -S Á N C H E Z , A.,
.. IUCN, Gland, Switzerland. portals.iucn.org/library/sites/ B I Z A M A , G., S I M O N E T T I , J.A. & P L I S C O F F , P. () Dispersal
library/files/documents/-.pdf [accessed August ]. and extrapolation on the accuracy of temporal predictions from
IUCN () The IUCN Red List of Threatened Species. Version distribution models for the Darwin’s frog. Ecological Applications,
-. IUCN, Gland, Switzerland. iucnredlist.org [accessed , –.
August ]. U R R U T I A -J A L A B E R T , R., G O N Z Á L E Z , M.E., G O N Z Á L E Z -R E Y E S , Á.,
IUCN ASG–C H I L E () Estrategia Binacional de Conservación de L A R A , A. & G A R R E A U D , R. () Climate variability and forest fires
la Ranitas de Darwin. IUCN SSC Amphibian Specialist Group– in central and south-central Chile. Ecosphere, , e.
Chile, Santiago, Chile. estrategiarhinoderma.org [accessed V A L E N Z U E L A -S Á N C H E Z , A., H A R D I N G , G., C U N N I N G H A M , A.A.,
August ]. C H I R G W I N , C. & S OT O -A Z A T , C. () Home range and social
J O H N S O N , C.N., B A L M F O R D , A., B R O O K , B.W., B U E T T E L , J.C., analyses in a mouth brooding frog: testing the coexistence of paternal
G A L E T T I , M., G U A N C H U M , L. et al. () Biodiversity losses and care and male territoriality. Journal of Zoology, , –.
conservation responses in the Anthropocene. Science, , –. V A L E N Z U E L A -S Á N C H E Z , A., C U N N I N G H A M , A.A. & S O T O -A Z AT , C.
M Á R Q U E Z -G A R C Í A , M., J AC O B S O N , S.K. & B A R B O S A , O. () () Geographic body size variation in ectotherms: effects of
Evaluating biodiversity workshops in Chile: are farmers responding seasonality on an anuran from the southern temperate forest.
with conservation action? Environmental Education Research, Frontiers in Zoology, , .
, –. V A L E N Z U E L A -S Á N C H E Z , A., S C H M I D T , B.R., U R I B E -R I V E R A , D.E.,
M O L I N A -B U R G O S , B.E., V A L E N Z U E L A -S Á N C H E Z , A., A LVA R A D O - C O S TA S , F., C U N N I N G H A M , A.A. & S O T O -A Z AT , C. () Cryptic
R Y B A K , M., K L A R I A N , S. & S O T O -A Z AT , C. () Trophic ecology disease-induced mortality may cause host extinction in an
of the Endangered Darwin’s frog inferred by stable isotopes. apparently-stable host–parasite system. Proceedings of the Royal
Endangered Species Research, , –. Society B, , .
M Y E R S , N., M I T T E R M E I E R , R.A., M I T T E R M E I E R , C.G., D A F O N S E C A , V A L E N Z U E L A -S Á N C H E Z , A., O’H A N LO N , S.J., A LVA R A D O -R Y B A K , M.,
G.A.B. & K E N T , J. () Biodiversity hotspots for conservation U R I B E -R I V E R A , D.E., C U N N I N G H A M , A.A., F I S H E R , M.C. et al.
priorities. Nature, , –. () Genomic epidemiology of the emerging pathogen
R A N I TA D E D A R W I N (a) Iniciativa de Conservación de Tierras Batrachochytrium dendrobatidis from native and invasive
para Anfibios. Organización No Gubernamental Ranita de Darwin, amphibian species in Chile. Transboundary and Emerging Diseases,
Santiago and Valdivia, Chile. ranitadedarwin.org/ , –.
conservaciondetierras [accessed April ]. V A L E N Z U E L A -S Á N C H E Z , A., S C H M I D T , B.R., P É R E Z , C., A LTA M I R A N O ,
R A N I TA D E D A R W I N (b) Proyecto Emerge. Estudio T., T O L E D O , V., P É R E Z , Í. et al. (a) Assessing habitat quality
Metapoblacional de Ranas del Bosque Templado Austral y Gestión when forest attributes have opposing effects on abundance and
Epidemiológica. Organización No Gubernamental Ranita de detectability: a case study on Darwin’s frogs. Forest Ecology and
Darwin, Santiago and Valdivia, Chile. ranitadedarwin.org/emerge Management, , –.
[accessed April ]. V A L E N Z U E L A -S Á N C H E Z , A., C AY U E L A , H., S C H M I D T , B.,
S A N TA N G E L I , A., A R R O Y O , B., D I C K S , L.V., H E R Z O N , I., K U K K A L A , A. C U N N I N G H A M , A.A. & S O T O -A Z A T , C. (b) Slow natal dispersal
S., S U T H E R L A N D , W.J. et al. () Voluntary non-monetary across a homogeneous landscape suggests the use of mixed
approaches for implementing conservation. Biological Conservation, movement behaviours in the Darwin’s frog. Animal Behaviour,
, –. , –.
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
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