The amphibian extinction crisis is still an emergency

doi:10.21203/rs.3.rs-2711241/v1

Download PDF

Article

The amphibian extinction crisis is still an emergency

https://doi.org/10.21203/rs.3.rs-2711241/v1

This work is licensed under a CC BY 4.0 License

Version 1

posted

You are reading this latest preprint version

Anthropogenic biodiversity loss is extreme in amphibians. Despite ongoing conservation action, it is difficult to determine where we stand in overcoming their extinction crisis 1,2. Extinction risk is not equally distributed across amphibians 3-5. Among the most threatened amphibians are the 131 Neotropical harlequin toads (Atelopus), many of which dramatically declined since the late 1980s with several considered possibly extinct 5,6. Recently, more than 30 species have been rediscovered7, raising hope for a reversing trend in the amphibian extinction crisis. We use harlequin toads, for which comprehensive past and present population status, threat and conservation action data are available, as a model for examining whether the amphibian extinction crisis is still in a state of emergency. We show that since 2004 no species has improved its population status, suggesting that the conservation community has not yet bent the curve. Threats such as pathogen spread and habitat change persist unabated; additionally, climate change is expected to be a future threat. More on-the-ground mitigation strategies need implementation, especially habitat protection and disease management, combined with captive conservation breeding. With harlequin toads serving as a model for amphibians with high extinction risk, it is clear that the amphibian extinction crisis is still underway.

Biological sciences/Ecology/Tropical ecology

Biological sciences/Ecology/Climate-change ecology

The Anthropocene is characterized by unparalleled levels of biodiversity loss ⁸. For more than two decades now, it has become clear that amphibians are among the most threatened vertebrates ^1,2,4,5. While populations are experiencing severe declines worldwide, strategies and tools have been identified to prevent further amphibian loss ⁹. At the recent UN Biodiversity Conference (COP15), held from 7–19 December 2022 in Montreal, almost 200 countries agreed that by 2050 the extinction rate and risk of all species will be reduced tenfold ¹⁰. In this context, we examine the amphibian extinction crisis taking harlequin toads (Atelopus), a species-rich genus from Central and South America, as a prime example of a worst-case scenario for the crisis ^4,6. We analyse trends in population status of harlequin toads from 2004–2022 and explore current and future threats and their mitigation in this highly imperiled genus.

Dimensions of the global amphibian extinction crisis

In the late 1980s, researchers started to witness amphibian declines at alarming rates with sudden and rapid population crashes all over the globe ^11,12. The 2004 IUCN Global Amphibian Assessment revealed that about 32% of 5,743 species were threatened with extinction and 34 species were already extinct ³. The most up-to-date IUCN Red List of Threatened Species (version 2022-2) now indicates that almost 35% of 7,486 evaluated species are threatened with extinction and 38 are extinct ⁵. In addition to ‘traditional’ threats (e.g., habitat destruction or degradation), novel and synergistically acting threats have been identified including climate change and emerging infectious diseases ^3,5,13,14. Of particular importance are pathogenic skin fungi from the genus Batrachochytrium causing the infectious disease chytridiomycosis. Human-mediated spread of these fungi has resulted in mass mortality events in many amphibians worldwide ^4,15.

The IUCN Amphibian Conservation Action Plan, regularly updated since 2007, frames strategies and tools to escape the amphibian emergency. Among others, this includes research at all levels from ecology to systematics, increased monitoring and continuous status assessments, habitat protection, disease mitigation efforts, in-country capacity building, community-based work, and ex situ conservation breeding ⁹.

While extinction threatens many amphibians, new ones are continuously being discovered, with more than 150 species descriptions per year over the last two decades ¹⁶. This makes assessing the amphibian crisis difficult as the true number of living amphibians is hard to estimate, and for this reason, it is challenging to assess our progress in overcoming the amphibian extinction crisis.

Dramatic declines of harlequin toads

Extinction risk is unequally distributed across amphibians ⁵. Some genera stand out as highly threatened, particularly those that contain many species with restricted ranges and high rates of population declines ². One of these ‘worst-cases’ are the harlequin toads, genus Atelopus, which scientists have closely monitored since the early 1990s ^{4,6,17,18,19,20}. More than 100 species of harlequin toads occur in tropical lowland and montane forests up to the paramos, from sea level to almost snowline in Central and South America (Supplementary Table 1). At least 27 species declined rapidly from 1984 to 2004 (Supplementary Table 2). By 2005, more than half of all species had not been seen for one decade or longer, and only 10 species had stable populations ⁶. The latest IUCN Red List assessed 94 harlequin toads and listed two thirds (62) of these as Critically Endangered (Fig. 1), of which 39 are Possibly Extinct. Only one species is categorized as Least Concern ⁵.

Decline of the decline?

The fear of witnessing the unprecedented extinction of an entire species-rich amphibian genus ²¹ did not materialize. Since 2005, only three species were added to the list of harlequin toads in decline (Supplementary Table 2). This is remarkable, given that Atelopus are among the best-studied and most sought-after amphibians in the Neotropics ^7,22. Instead, 30 species that had not been seen by scientists for many years have been rediscovered (Supplementary Table 3), suggesting a hypothetical reverse population trend in them. This also includes two species the IUCN Red List categorized as Extinct (Atelopus ignescens and A. longirostris; Fig. 1) ²³. Some of the sightings include true rediscoveries at historical localities, which have been regularly visited, while others were new discoveries at formerly unknown localities ⁷.

A ‘worst-case’ amphibian decline model

Given that the declines in harlequin toads are extreme, but that we recently documented several rediscoveries, they represent an extraordinary worst-case model to explore where we stand in managing the amphibian crisis. We define two phases: (i) the crisis with dramatic population declines, ca. 1984–2004; and (ii) post-2004, a hypothetical improvement of the population status in at least some species.

Two circumstances provide unique opportunities of Atelopus serving as a model. First, population monitoring data from two periods led to the assessment of population status of all known species in 2004 ⁶ and 2022. These are based on expert knowledge, which is common practice in conservation assessments ²⁴. As done in 2004, we assigned one of three population status categories to each species in 2022, resulting in two sets of standardized data 15 years apart (Fig. 2; Supplementary Table 1).

The second circumstance making harlequin toads an exemplary group is that we take a high degree of accuracy in taxonomy for granted, which is essential for effective species conservation ²⁵. Several of the authors have contributed to the taxonomy of Atelopus for many years and have established the contemporary taxonomic architecture of the genus. With this unparalleled advantage, we have a comprehensive data set on this genus far beyond the available published information, so that species status data are not markedly behind the taxonomic progress, as in other amphibians. In total, we evaluated 131 Atelopus species, of which 37 (28.2%) are not yet assessed on the IUCN Red List (Fig. 1; Supplementary Table 1). Next to acknowledging the taxonomic progress (i.e., new and revalidated species), our 2022 database includes 31 species identified but not yet formally described (e.g. A. sp. “wampukrum”, Fig. 1).

We did not detect change in the population status of the species assessed in 2004 and 2022 (Fig. 2), (Freeman-Halton extension of Fisher’s exact test for RxC table: p = 0.152), including for a 2022 reduced dataset containing only the 94 species listed in the 2004 assessment (p = 0.826). No species has improved its population status since 2004 (Fig. 2), even the shrinking species that were rediscovered after 2004 remain shrinking. Harlequin toads with shrinking population status mostly occur in Andean areas and Central America, while none of the species from the lower Amazon basin, the Guianas, the Colombian Sierra Nevada de Santa Marta and part of the species from the Chocó have shrinking populations (13 species in total) (Fig. 3a). Alarmingly, 61 species (46.6%) have ‘year last seen’ (YLS) in 2004 or earlier. These species have population status data pending or shrinking (depending on the knowledge on the population status prior their YLS) and 37 have probably vanished (Supplementary Table 1).

Persisting threats

The main drivers of Atelopus declines are habitat destruction and degradation ^5,6 and the skin fungus Batrachochytrium dendrobatidis (Bd) ^4,26. The 2022 expert data demonstrate that habitat destruction and degradation are a threat to 93 (71.0%) species (Fig. 3b), of which 37 have YLS 2004 or earlier (Supplementary Table 1). We noted the presence of Bd in 50 (38.2%) species, and of the 42 species with Bd whose population status is categorized as shrinking or data pending (Fig. 3b), 16 have YLS 2004 or earlier (Supplementary Table 1).

Habitat destruction and degradation as well as Bd continue to threaten harlequin toads today. The situation is dire, considering how habitat change can significantly affect Atelopus populations ²⁷. A vivid example is the recently rediscovered A. longirostris (Fig. 1) from the Intag Valley of Ecuador which is now the focus of a large copper mining project ²⁸. Regarding Bd, some populations compensate high mortality rates with a high reproductive output, which might cause life history shifts, e.g. in A. cruciger^29,30. That is, some Atelopus species can persist once the fungus becomes enzootic ^31,32. There are five species that continue to have steady populations despite the presence of Bd. However, these are fragile systems, because effects of Bd are more complex due to co-stressors ⁴.

Climate change as a future threat

Some studies suggest that unusual climatic conditions may play a role in Atelopus declines and might also exacerbate the effects of Bd^26,33,34. Climatic change is associated with an increase in the frequency of extreme weather events. Climate change for the period from present (1970–2000) to the year 2100 can be assessed using the Climatic Stability Index, CSI ³⁵. CSI values are higher in lowlands (i.e. climate is unstable), where most harlequin toads with steady populations occur (Fig. 3a), suggesting that climate change might become an important threat to currently steady lowland Atelopus in the future (Fig. 3c).

Mitigation efforts

Multi-disciplinary approaches to improve the conservation status of Atelopus have been proposed and include habitat protection, scientific research, monitoring, environmental education, and conservation breeding ¹⁹. Recently, these were reinforced in the Atelopus Conservation Action Plan 2021–2041 along with elaborated targets for the coming decades. The plan was launched by the recently founded Atelopus Survival Initiative ³⁶, a multi-stakeholder collaborative and participative effort to stop the loss of this imperiled genus ²⁰.

Other initiatives, such as the El Valle Amphibian Conservation Center ³⁷, Project Golden Frog ³⁸ or the Panama Amphibian Rescue and Conservation Project ³⁹, have operated for more than 10 years now and have contributed to direct conservation efforts on Central American Atelopus species. They have promoted research to further understand the effects of Bd on population genetic structures ⁴⁰ and to explore the response of Bd to an altered skin microbiome ^15,41 or to skin secretions ^32,42. In addition, ex situ assisted reproductive technologies are being developed to preserve genetic diversity of some harlequin toads, for instance for Ecuadorian species ⁴³. Various local initiatives have been initiated recently to conserve particular species through community-based conservation action and habitat protection ^44,45, but their impact yet remains difficult to assess, however. To assess in situ conservation actions at a broader geographic and taxonomic scale, we here explored the number of Atelopus species in protected areas, which has increased from 84 to 96 from 2004 to 2022 (64.1 to 73.3%; Supplementary Table 1). Given that the populations of 43 of these species are shrinking, it is evident that habitat protection alone is not sufficient.

The special role of ex situ conservation breeding

For highly threatened species, captive assurance populations are strongly recommended as a possibly powerful tool allowing for reintroductions once the threat(s) can be mitigated. This is an extreme measure, especially for amphibian species that are vulnerable to Bd. In practice, ex situ conservation breeding allows us to buy time while appropriate mitigation and conservation strategies are developed and applied ⁹. Thus, conservation breeding is a crucial action to enhance the chances of harlequin toad survival ^19,35,46. So far, captive assurance colonies have been established for 26 Atelopus species and scientists have now started to study reintroductions of captive-born individuals in A. limosus⁴⁷; studies on additional species are in progress (authors’ unpubl. data). This underlines the potential of conservation breeding. So far, 16 species (13 with shrinking populations) have already successfully reproduced at least once at one institution, with offspring reaching maturity. However, only six Atelopus species have reproduced at two or more institutions with at least one institution successfully reproducing for more than one generation (Supplementary Table 4), showing that conservation breeding needs more efforts. Conservation breeding of A. zeteki (Fig. 1) has been a story of remarkable success ^38,46, with more than a thousand individuals being held in more than 50 institutions in three countries, independent from wild caught founders, for roughly 20 years. This species is considered shrinking and has likely already vanished in the wild. As a sharp contrast, in three Atelopus species, conservation breeding attempts have failed, with all individuals lost (Supplementary Table 4).

Captive breeding initiatives are regionally biased, with several in-country colonies covering mainly Ecuadorian and Panamanian species, while Brazil, Colombia and Venezuela have recently launched programs for one species each. Ex situ conservation efforts are lacking in other countries where harlequin toads occur, yet some species are or were bred in Europe and North America (Supplementary Table 4).

The amphibian extinction crisis is still an emergency

Our comparison of the 2004 and 2022 databases reveals that no harlequin toad has an improved population status. We reject the hypothesis that we have entered a hypothetical post-decline phase of improvement. Although reports on sudden and rapid population declines have lessened (Supplementary Table 2), many species continue to have shrinking populations, which implies that over time declines continue to happen more silently. This is reinforced by the observations that of the 29 species rediscovered since 2004, six have not been seen again for the past 10 years, despite targeted searches ⁷. These harlequin toads either occur in low numbers or are possibly extinct emphasizing that rediscoveries are not equating recoveries. At the same time habitat destruction and Bd persist to threaten harlequin toads, despite that 96 (75%) of the species occur in protected areas and (at least) some Atelopus can somehow cope with Bd. In addition, future threats through changing climate are expected.

Using harlequin toads as a worst-case model for amphibian species with high extinction risk ^2,5, the situation of these amphibians has not improved over the past two decades. Despite invaluable efforts, we so far have not been able to reverse the massive declines. The goal to massively reduce extinction rates within the next 20–30 years ¹⁰ will require immense efforts and investments, which need to be massively scaled up. More in situ mitigation strategies need to be implemented, including effective habitat protection and management, Bd mitigation measures and the expansion of ex situ capacities.

Given proper funding and support, with the Atelopus Conservation Action Plan 2021–2041 and the collaborative coalition of on-the-ground conservation organizations, zoos, governments and local communities, there is improvement in sight for the remaining harlequin toads. For most other threatened amphibians such focal plans and coordinated conservation efforts are still lacking.

Acknowledgments

For help with gathering data on harlequin toads we are grateful to the following colleagues Marvin Anganoy-Criollo, Ariadne Angulo, Jimy Barrantes-Madrigal, Leonardo Batallas, Merilyn A. Caballero Arias, Euclides Campos, Mauricio Carpio, Daniel Chávez, Patricio Dominguez, Rogemif D. Fuentes M., Gustavo Gonzalez Duran, Gustavo Gutiérrez, Paul Houser, Astrid Lizondro, Felipe Lievano, Albertina P. Lima, Madian Miranda, Daniel Orizano, Luis Oyagata, Daniel Padilla Jiménez, Luis Pino, Sergio Quiroz, Héctor E. Ramírez-Chaves, Ángel Sosa-Bartuano, Samuel Valdes, and Andrés Viuche Lozano. We also thank the entire Atelopus Survival Initiative for support and Luis F. Marin da Fonte, Jamie Voyles, and Corinne L. Richards-Zawacki for valuable comments on the manuscript.

Funding: Not applicable.

Author contributions: S.L., A.P., A.C. and E.L.M. contributed to the concept and design of this paper. A.P., S.L. and E.L.M. cured and analysed the data. S.L., A.P., A.C. and K.N. led the writing. All other authors contributed to the acquisition and interpretation of the data and contributed to or revised the writing.

Competing interests: None.

Data and materials availability: All data used is made available in the Supplementary Materials.

Mendelson, J. R. et al. Confronting amphibian declines and extinctions. Science. 313, 48 (2006).
Threatened Amphibians of the World. (Lynx Editions, 2008).
Stuart, S. N. et al. Status and trends of amphibian declines and extinctions worldwide. Science. 306, 1783–1786 (2004).
Scheele, B. C. et al. Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science. 363, 1459–1463 (2019).
IUCN. The IUCN Red List of Threatened Species. Version 2022-2. https://www.iucnredlist.org (2022).
La Marca, E. et al. Catastrophic population declines and extinctions in Neotropical harlequin frogs (Bufonidae: Atelopus). Biotropica. 37, 190–201 (2005).
Jaynes, K. E. et al. Harlequin frog rediscoveries provide insights into species persistence in the face of drastic amphibian declines. Biol. Conserv. 276, 109784 (2022).
Barnosky, A. D. et al. Has the Earth’s sixth mass extinction already arrived? Nature. 471, 51–57 (2011).
IUCN SSC Amphibian Specialist Group. The Amphibian Conservation Action Plan (ACAP): A status review and roadmap for global amphibian conservation. https://ecoevorxiv.org/brfas/. Preprint. DOI: 10.32942/osf.io/brfas (2022).
Convention on Biological Diversity. COP 15: Nations adopt four goals, 23 targets for 2030 in Landmark UN Biodiversity Agreement. Official CBD Press Release https://www.cbd.int/article/cop15-cbd-press-release-final-19dec2022 (2022).
Barinaga, M. Where have all the froggies gone. Science. 247, 1033 (1990).
Blaustein, A. R. & Wake, D. B. Declining amphibian populations: A global phenomenon? Trends Ecol. Evol. 5, 203–204 (1990).
Kiesecker, J., Blaustein, A. R. & Belden, L. K. Complex causes of amphibian population declines. Nature. 410, 681–684 (2001).
Collins, J. P. & Storfer, A. Global amphibian declines: Sorting the hypotheses. Divers. Distrib. 9, 89–98 (2003).
Woodhams, D. C. et al. Prodigiosin, Violacein, and Volatile organic compounds produced by widespread cutaneous bacteria of amphibians can inhibit two Batrachochytrium fungal pathogens. Microb. Ecol. 75, 1049–1062 (2018).
AmphibiaWeb. Newly described species by year. University of California, Berkeley https://amphibiaweb.org/amphibian/newspecies.html (2023).
La Marca, E. & Reinthaler, H. P. Population changes in Atelopus species of the Cordillera de Mérida, Venezuela. Herpetol. Rev. 22, 125–128 (1991).
Pounds, J. A. & Crump, M. L. Amphibian declines and climate disturbance: The case of the golden toad and the harlequin frog. Conserv. Biol. 8, 72–85 (1994).
Lötters, S. The fate of the harlequin toads – help through a synchronous multi-disciplinary approach and the IUCN ‘Amphibian Conservation Action Plan’? Mitt. Mus. Naturkunde Berl., Zoolog. Reihe. 83, 69–73 (2007).
Valencia, L. M. & Marin da Fonte L. F. Collaborative work brings hope for threatened harlequin toads. Oryx. 56, 12 (2022).
Lötters, S., La Marca, E., Stuart, S., Gagliardo, R. & Veith, M. A new dimension of current biodiversity loss? Herpetotropicos. 1, 29–31 (2004).
Ranas Arlequines. (Conservación Internacional, 2005).
Tapia, E. E., Coloma, L. A., Pazmiño-Otamendi, G. & Peñafiel N. Rediscovery of the nearly extinct longnose harlequin frog Atelopus longirostris (Bufonidae) in Junín, Imbabura, Ecuador. Neotrop. Biodivers. 3, 157–167 (2017).
Drescher, M. et al. Toward rigorous use of expert knowledge in ecological research. Ecosphere. 4, art83 (2013).
de Magalhães, R. F., Rocha, P. C., Santos, F. R., Strüssmann, C. & Giaretta, A. A. Integrative taxonomy helps to assess the extinction risk of anuran species. J. Nat. Conserv. 45, 1–10 (2018).
Lips, K. R. et al. Riding the Wave: Reconciling the roles of disease and climate change in amphibian declines. PLoS Biol. 6, e72 (2008).
Tarvin, R. D., Peña, P. & Ron, S. R. Changes in population size and survival in Atelopus spumarius (Anura: Bufonidae) are not correlated with chytrid prevalence. J. Herpetol. 48, 291–297 (2014).
Murphy, D. International and Local Conservation Groups Condemn Ecuadorian Court’s Decision to Allow Copper Mining in Intag Valley Cloud Forests. Froglog. 124, 23–24 (2022).
Ballestas, O., Lampo, M. & Rodríguez, D. Living with the pathogenic chytrid fungus: Exploring mechanisms of coexistence in the harlequin toad Atelopus cruciger. PLoS ONE. 16, e0254439 (2021).
Lampo, M., Señaris, C. & García, C. Z. Population dynamics of the Critically Endangered toad Atelopus cruciger and the fungal disease chytridiomycosis. PLoS ONE. 12, e0179007 (2017).
Lampo, M., Señaris, C., González, K. & Ballestas, O. Smaller size of harlequin toads from populations long exposed to the lethal fungal disease chytridiomycosis. Biotropica. In press (2023).
Voyles, J. et al. Shifts in disease dynamics in a tropical amphibian assemblage are not due to pathogen attenuation. Science. 30, 1517–1519 (2018).
Rohr, J. R., Raffel, T. R., Romansic, J. M., McCallum, H. & Hudson, P. J. Evaluating the links between climate, disease spread, and amphibian declines. Proc. Natl. Acad. Sci. U.S.A. 105, 17436–17441 (2008).
Ron, S. R., Duellman, W. E., Coloma, L. A. & Bustamante, M. R. Population decline of the jambato toad Atelopus ignescens (Anura: Bufonidae) in the Andes of Ecuador. J. Herpetol. 37, 116–126 (2003).
Herrando-Moraira, S. et al. Climate Stability Index maps, a global high resolution cartography of climate stability from Pliocene to 2100. Sci. Data. 9, 48 (2022).
Atelopus Survival Initiative. Save harlequin Toads. https://www.atelopus.org/ (2021).
El Valle Amphibian Conservation Center. https://www.evaccfoundation.org (2023).
Project Golden Frog. https://www.ranadorada.org/ (2023).
Gratwicke, B. et al. Evaluating the probability of avoiding disease-related extinctions of Panamanian amphibians through captive breeding programs. Anim. Conserv. 19, 324–336 (2016).
Byrne, A. Q. et al. Whole exome sequencing identifies the potential for genetic rescue in iconic and critically endangered Panamanian harlequin frogs. Glob. Chang. Bio. 27, 50–70 (2020).
Becker, M. H. et al. Genetically modifying skin microbiome to produce violacein and augmenting microbiome did not defend Panamanian golden frogs from disease. ISME Communic. 4281, 57 (2021).
Gass, J. & Voyles, J. When defences fail: Atelopus zeteki skin secretions increase growth of the pathogen Batrachochytrium dendrobatidis. Integr. Comp. Biol. 62, 1595–1605 (2022).
Naranjo, R. E. et al. Development of assisted reproductive technologies for the conservation of Atelopus sp. (spumarius complex). Cryobiology. 105, 20–31 (2022).
Alianza Jambato. https://alianzajambato.org/ (2023).
Fundación Atelopus. https://www.fundacionatelopus.org (2023).
Lewis, C. H. R. et al. Conserving Panamanian harlequin frogs by integrating captive breeding and research programs. Biol. Cons. 236, 180–187 (2019).
Estrada, A., Medina, D., Gratwicke, B., Ibáñez & Belden, L. K. Body condition, skin bacterial communities and disease status: insights from the first release trial of the limosa harlequin frog, Atelopus limosus. Proc. Biol. Sci. 289, 20220586 (2022).
[From here on literature cited in the online section only]
McBride, M. F. et al. Structured elicitation of expert judgments for threatened species assessment: a case study on a continental scale using email. Methods Ecol. Evol. 3, 906–620 (2012).
Sutherland, W. J. & Burgman, M. A. Use experts wisely. Nature. 526, 317–318 (2015).
Krueger, T., Page, T., Hubacek, K., Smith, L. & Hiscock, K. The role of expert opinion in environmental modelling. Environ. Model. Softw. 36, 4–18 (2012).
Lötters, S. et al. The gastromyzophorous tadpole of the pink harlequin frog from Suriname with comments on the taxonomy of Guianan Clade Atelopus (Amphibia, Bufonidae). Zootaxa. 5087: 591–598 (2022).
Booth, T. H., Nix, H. A., Busby, J. R. & Hutchinson, M. F. Bioclim: the first species distribution package, its early applications and relevance to mot current MaxEnt studies. Divers. Distrib. 20, 1–9 (2014).
Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).
Coloma, L. A. et al. Five new (extinct?) species of Atelopus (Anura: Bufonidae) from Andean Colombia, Ecuador, and Peru. Zootaxa. 2574, 1–54 (2010).
La Marca, E. & Lötters, S. Population declines in Venezuelan Atelopus (Amphibia: Anura: Bufonidae). in Herpetologia Bonnensis. – Proceedings of the 8th Ordinary General Meeting Societas Europeae Herpetologica (SEH) (eds. Böhme, W., Bischoff, W. & Ziegler, T.) 207–213 (Societas Europeae Herpetologica (SEH), 1997).
Lampo, M., Rodriguez-Contreras, A., La Marca, E. & Daszak, P. A chytridiomycosis epidemic and a severe dry season precede the disappearance of Atelopus species from the Venezuelan Andes. Herpetol. J. 16, 395–402 (2006).
Berger, L. et al. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc. Natl. Acad. Sci. U.S.A. 95, 9031–9036 (1998).
Lips, K. R. Mass mortality and population declines of anurans at an upland site in western Panama. Conserv. Biol. 13, 117–125 (1999).
Bonaccorso, E., Guayasamin, J. M., Mendez, D. & Speare, R. Chytridiomycosis as a possible cause of population declines in Atelopus cruciger (Anura: Bufonidae). Herpetol. Rev. 34, 331–334 (2003).
Manzanilla, J. & La Marca, E. Population status of the Rancho Grande harlequin frog (Atelopus cruciger Lichtenstein and Martens 1856), a proposed critically endangered species from the Venezuelan coastal range. Mem. Soc. Cienc. Nat. 62, 5–29 (2004).
Catenazzi, A., Lehr, E., Rodriguez, L. O. & Vredenburg, V. T. Batrachochytrium dendrobatidis and the collapse of anuran species richness and abundance in the upper Manu National Park, southeastern Peru. Conserv. Biol. 25, 382–391 (2010).
Acosta-Galvis, A. R., Rueda-Almonacid, J. V., Velásquez-Álvarez, Á. A., Sánchez-Pacheco, S. J. & Peña-Prieto, J. A. Descubrimiento de una nueva especie de Atelopus (Bufonidae) para Colombia: ¿Una luz de esperanza o el ocaso de los sapos arlequines? Rev. Acad. Colomb. Cienc. Exactas Fis. Nat. 30, 279–290 (2006).
García, I. J., Albornoz, R. & La Marca, E. Perturbaciones climáticas y disminución de Atelopus oxyrhynchus (Amphibia: Anura) en los Andes de Venezuela. Herpetotropicos. 2, 63–71 (2005).
Venegas, P. J., Catenazzi, A., Siu-Ting, K. & Carrillo, J. Two new harlequin frogs (Anura: Atelopus) from the Andes of northern Peru. Salamandra. 44, 163–176 (2008).
Gómez-Hoyos, D. A. et al. The population decline of Atelopus quimbaya (Anura: Bufonidae) in the Andes of Colombia. Rev. Latinoam. Herpetol. 1, 34–42 (2018).
McCaffery, R., Richards Zawacki, C. L. & Lips, K. R. The demography of Atelopus decline: Harlequin frog survival and abundance in central Panama prior to and during a disease outbreak. Glob. Ecol. Conserv. 4, 232–242 (2015).
Barrio-Amorós, C. L., Chaves, G. & Puschendorf, R. Current status and natural history of the Critically Endangered Variable Harlequin Toad (Atelopus varius) in Costa Rica. Reptil. Amphib. 28, 374–388 (2021).
Mayer, L. R. Found: Lost starry night harlequin toad makes radiant return to science Global Wildlife Conservation. https://www.rewild.org/press/found-lost-starry-night-harlequin-toad-makes-radiant-return-to-science (2019).
Hance, J. Researchers rediscover one of the world´s most sought-after lost frogs. Mongabay news & inspiration from nature´s frontline https://news.mongabay.com/2011/02/researchers-rediscover-one-of-the-worlds-most-sought-after-lost-frogs/ (2011).
Coloma, L. A., Lötters, S. & Quiguango-Ubillús, A. Atelopus bomolochos. Anfibios de Ecuador http://www.anfibiosecuador.ec/index.php?ss,Atelopus&bomolochos (2016).
Barrio-Amorós, C. L. & Torres, D. Atelopus carbonerensis Rivero, 1974: A long-awaited rediscovery through citizen science. Reptil. Amphib. 30, e18534 (2023).
Rueda Solano, L. A. Colorful harlequin frog re-discovered in Colombia. Froglog. 86, 1–2 (2008).
Kay, A. Atelopus coynei observed February 7, 2012, research-grade observations. iNaturalist http://www.inaturalist.org/observations/55996 (2012).
Rodriguez-Contreras, A., Señaris, J. C., Lampo, M. & Rivero, R. Rediscovery of Atelopus cruciger (Anura: Bufonidae): Current status in the Cordillera de La Costa, Venezuela. Oryx. 42, 301–304 (2008).
Tovar-Siso, P., García-Pérez, J. E. & La Marca, E. Sapito amarillo y rojo de Niquitao, Atelopus chrysocorallus. in Libro Rojo de la Fauna Venezolana (eds. Rodríguez, J. P., García-Rawlins, A. & Rojas-Suárez, F.) 177 (Provita y Fundación Empresas Polar, 2015).
Santa-Cruz, R., Delgado, W. L., Medina, C. E., Treviño, E. & von May, R. Distribution and conservation status of the critically endangered harlequin frog Atelopus epikeisthos (Anura: Bufonidae). Salamandra. 53, 423–425 (2017).
Jervis, P. et al. Disease reservoirs threaten the recently rediscovered Podocarpus stubfoot toad (Atelopus podocarpus). Amphib. Reptile Conserv. 14, 157–164 (2020).
Coloma LA, Quiguango-Ubillús A. Atelopus nanay. Anfibios de Ecuador http://www.anfibiosecuador.ec/index.php?ss,Atelopus&nanay*listaroja#listaroja (2016).
Carvajalino-Fernández, J. M., Cuadrado-Peña, B. & Ramirez-Pinilla, M. P. Registros adicionales de Atelopus nahumae y Atelopus laetissimus para la Sierra Nevada de Santa Marta, Colombia. Actual. Biol. 30, 97–103 (2008).
WCS Colombia. A harlequin frog that reappeared after almost two decades of absence has its refuge in Choachí. WCS Colombia NEWS https://colombia.wcs.org/en-us/WCS-Colombia/News/articleType/ArticleView/articleId/14267/A-HARLEQUIN-FROG-THAT-REAPPEARED-AFTER-ALMOST-TWO-DECADES-OF-ABSENCE-HAS-ITS-REFUGE-IN-CHOACHI.aspx (2020).
Conservation International. ‘Extinct’ frog rediscovered in Colombia. Mongabay news & inspiration from nature´s frontline https://news.mongabay.com/2006/05/extinct-frog-rediscovered-in-colombia/ (2006).
Barrio-Amorós, C. L. et al. Back from extinction: rediscovery of the harlequin toad Atelopus mindoensis Peters, 1973 in Ecuador. Herpetol. Notes. 13, 325–328 (2020).
Barrio-Amorós, C. L. Atelopus mucubajiensis still survives in the Andes of Venezuela. Froglog. 66, 2–3 (2004).
Carvajalino-Fernández, J. M., Cuadrado-Peña, B. & Ramírez-Pinilla, M. P. Registros adicionales de Atelopus nahumae y Atelopus laetissimus para la Sierra Nevada de Santa Marta, Colombia. Actual. Biol. 30, 97–103 (2008).
Coloma LA, Quiguango-Ubillús A. Atelopus ignescens. Anfibios de Ecuador http://www.anfibiosecuador.ec/index.php?ss,Atelopus&ignescens (2018).
Yánez-Muñoz, M. H., Veintimilla, D. A., Smith, E. N., Altamirano-Benavides, M. & Franklin, C. J. Descubrimiento de dos poblaciones sobrevivientes de sapos arlequín (Amphibia: Bufonidae: Atelopus) en los Andes de Ecuador. Avances en Ciencias e Ingeniería. 2, B74-B77 (2010).
Pereira-Muñoz, A., García-Pérez, J. E. & La Marca, E. Sapito verdirrojo de Piñango, Atelopus pinangoi. in Libro Rojo de la Fauna Venezolana (eds. Rodríguez, J. P., García-Rawlins, A. & Rojas-Suárez, F.) 181 (Provita y Fundación Empresas Polar, 2015).
Enciso-Calle, M. P., Viuche-Lozano, A., Anganoy-Criollo, M. & Bernal, M. H. Rediscovery of Atelopus subornatus Werner, 1899 (Anura: Bufonidae), with a redescription of the tadpole. Zootaxa. 4344, 160–162 (2017).
Pacheco-Suarez, M. New evidence for the presence of Atelopus tricolor (Anura: Bufonidae) in the montane forests of Bolivia, 16 years after its last observation. Salamandra. 56, 392–394 (2020).
González-Maya, J. F. et al. Renewing hope: The rediscovery of Atelopus varius in Costa Rica. Amphib.-Reptil. 34, 573–578 (2013).
Barrio-Amorós, C. L., Rojas-Runjaic, F. J. M. & Señaris, J. C. Catalogue of the amphibians of Venezuela: Illustrated and annotated species list, distribution, and conservation. Amphib. Reptile Conserv. 13, 1–198 (2019).
La Marca, E. & Hidalgo, M. A. A finding that brings hope for a still unknown harlequin frog Amphibian Survival Alliance. https://www.amphibians.org/news/a-finding-that-brings-hope-for-a-still-unknown-harlequin-frog/ (2021).

Methods

We used the original database of La Marca et al. ⁶, which compiled information from experts on Atelopus population trends through February 2004. This database was updated with the revised taxonomy, as well as new input and data from experts, and our study period was defined as March 2004 to December 2022 (Supplementary Table 1). We interviewed 105 experts (a diverse group of scientists and conservationists with considerable knowledge on Atelopus species), sometimes on multiple occasions, from October 2019 to December 2022. All 75 original database contributors to La Marca et al. ⁶ were contacted, but we received updated information from only 13. The additional 92 contributing researchers were Atelopus taxonomists and conservationists. Original contributions included initial estimates on population status and general threats as well as field data on the species ecology and threats at the site level. Data was reviewed and summarized species-wise prior to a second round, where experts were able to provide corrected estimates, as has been proven successful for obtaining robust expert data ^48,49. Still, we are well-aware that expert opinions carry an unavoidable uncertainty and need to be considered carefully ^49,50. Most of the experts who contributed data also contributed to the writing of this paper and became co-authors.

In this study, we refer the term ‘species’ to described taxa that we consider valid and to forms that are undescribed and are expected to represent valid species. Also, we tentatively consider suggested subspecies as species here. According to this, we refer to 131 species of which 100 are formally described, while the 2004 database considered 94 taxa. Alphataxonomic problems remain for some harlequin toads, e.g. A. hoogmoedi which could be more than one species ⁵¹.

Following La Marca et al. ⁶, for each species we updated the information on distribution, the known altitudinal range, and local endemism by number of known populations (1, 2, >2). We recorded: species population status; the year last seen (YLS); information on Bd presence; occurrence in any governmental or private protected area. In order to address threats that have been identified to play a key role in Atelopus declines ^6,34, we additionally assessed the potential future impact of climate change for each species. For detailed data see Supplementary Table 1. Details on how data were assessed are described below.

The population status was coded following definitions of La Marca et al. ⁶. However, we change the terminology to avoid confusion with terms used by the IUCN Red List of Threatened Species. We used ‘steady’ (= stable) when one or more populations are known to have persisted and no population has declined by more than 50%; ‘shrinking’ (= declining) when at least one population has declined by more than 50%; ‘data pending’ (= data deficient) when insufficient population trend data are available to judge whether a decline has occurred. This also includes species where unsystematic survey efforts were invested, but the species could not be detected. We additionally coded species as ‘probably vanished’ or ‘probably vanished in the wild’, when experts agreed that the particular species has possibly gone extinct (or extinct in the wild). However, as extinction is difficult to confirm, and as rediscoveries of formerly thought to be extinct species are common in the genus, this is not a separate status category.

In addition to information on Bd presence through direct testing of Atelopus specimens (including diagnosis both by PCR or histology), we provide information on presumed Bd presence for Atelopus species that have not been tested for Bd. We consider likely presence of Bd in an Atelopus species when Bd infection is known in other amphibian species at Atelopus localities. For this purpose, we used Bd records available from the Aquatic Parasite Observatory (http://www.aquaticparasites.org/, accessed 8 June 2022) and the Amphibian Disease Portal (https://amphibiandisease.org/, accessed 28 September 2022). Employing ArcGIS Pro (ESRI), we then buffered (5 km) 776 georeferenced Atelopus records of 102 species. If a Bd record was within a buffer, we considered the Atelopus species to potentially have Bd.

To assess the potential future impact of climate change at Atelopus sites, we used the Climate Stability Index (CSI). It provides information on climate vulnerability for the time span Pliocene (3.3 Ma) to the year 2100 ³⁵. The CSI operates using the standard deviation over time at grid cells with resolution 2.5 arc-min. It is based on 9 general circulation models and 19 bioclimatic variables ⁵² available from WorldClim 2 ⁵³. Of the different underlying climate change scenarios (Shared Socioeconomic Pathways, SSP), we chose, a priori, SSP5-8.5 from present (1970-2000) to the year 2100 for our study because it is among the most extreme (‘worst-case’) scenarios for Central and South America ³⁵. CSI data were downloaded from Figshare (https://doi.org/10.6084/m9.figshare.14672637, accessed 2 March 2022). CSI values range 0-1 (most to least stable).

With the goal of obtaining information on Atelopus conservation breeding, we contacted all existing institutions, to our knowledge, that hold or held captive assurance colonies of harlequin toads to compile a dataset on the species kept and breeding success (Supplementary Table 4). We received information from all seven institutions located in Atelopus range countries as well as from numerous North American and European institutions, partially coordinated through the multinational Project Golden Frog ³⁸.

There is NO Competing Interest.

Download PDF

Version 1

posted

You are reading this latest preprint version

The amphibian extinction crisis is still an emergency

Status:

Version 1

Abstract

Figures

Main

Declarations

Acknowledgments

References

Online content

Additional Declarations

Supplementary Files

Status:

Version 1