www.conservationandsociety.org

ISSN: 0972-4923

Conservation& Society

Volume 11 Number 3 2013

Conservation and Society 11(3): 291-319, 2013

Article

The Demise of the Golden Toad and the Creation of a Climate Change Icon Species

Leticia M. Ochoa-Ochoaa,#, Robert J. Whittakera, and Richard J. Ladlea,b

aSchool of Geography and the Environment, Oxford University Centre for the Environment, Oxford, UKbInstitute of Biological Sciences and Health, Federal University of Alagoas, Maceio, Brazil

#Corresponding author. E-mail: leticia.ochoa@ciencias.unam.mx

Copyright: © Ochoa-Ochoa et al. 2013. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and distribution of the article, provided the original work is cited.

AbstractThere is an unavoidable degree of uncertainty associated with future climate projections, and even more unpredictability about the potential impact of different climate scenarios on the ecology and distribution of organisms. Conservationists face a major public communications challenge to both raise awareness and mobilise support for conservation and climate change mitigation/adaptation policies while realistically representing complex and uncertain scientifi c information. Here, we illustrate the interplay of these competing communication goals through a review of the representations of the golden toad in the print media and peer-reviewed literature (in English and Spanish). Since its disappearance in 1989 the toad has become an important conservation fl agship species that has been frequently portrayed as the fi rst verifi ed extinction attributable to global warming. Moreover, there was an increase in the certainty of published news items regarding the toad and its demise, especially in the late 1990s. The uncertainty surrounding the toad’s disappearance (apparent in the primary research literature) was poorly represented in the popular press. The transformation of the toad into an iconic species for climate change advocacy may refl ect a perceived need to supply tangible evidence of biodiversity consequences arising from climate change and highlights the challenges facing conservation scientists in communicating scientifi c concerns and uncertainty via the media.

Keywords: amphibian decline, climate change, Bufo periglenes, conservation, Incilius periglenes, media representation, uncertainty

INTRODUCTION

“Perhaps the most common outcome of the scientifi c process is not facts, but uncertainty” Friedman et al. (1999: vii)

“For many, false prophecy is still less frightening than uncertainty” Reading (2004: 15)

Global concern about the conservation status of amphibians began to gather momentum at the fi rst World Conference of

Herpetology in 1989 (Sarkar 1996). Numerous scientists at this meeting argued that there was a general declining trend among amphibian populations in different parts of the world, but with no obvious single cause (Blaustein and Wake 1990; Blaustein 1994; Houlahan et al. 2000). Several hypotheses were suggested, such as ultraviolet radiation, pesticides, introduction of alien species, toxicants, deforestation, and pathogens (reviewed in Blaustein et al. 1998; Collins and Storfer 2003; Cushman 2006; see Appendix 1). These threats are not mutually exclusive and some have proved diffi cult to identify defi nitively or separate in the fi eld (Collins and Storfer 2003), possibly because sub-population decline is inevitable in metapopulation with high demographic variability—a characteristic of many amphibian populations (Alford and Richards 1999; Gillespie 2010).

The golden toad, Incilius (Bufo) periglenes (Savage 1966), is a classic example of a species for which the causes

Access this article onlineQuick Response Code:

Website:www.conservationandsociety.org

DOI: 10.4103/0972-4923.121034

292 / Ochoa-Ochoa et al.

of decline and eventual extinction are poorly understood, but which nevertheless has become an important species within climate change discourse. The golden toad was fi rst discovered in the cloud forest of the Monteverde region of Costa Rica in 1964 (Savage 1966). The small population size and extremely localised geographic distribution meant that the toad was always a conservation concern and, in 1972, a small reserve of less than 4 sq. km was established that encompassed the entire known global population (Crump et al. 1992). Subsequently the reserve was expanded to encompass around 105 sq. km.

Although the golden toad was diffi cult to survey accurately within the dense undergrowth of the cloud forest, accurate counts could be made for a few weeks in April when individuals emerged from the forest to mate in temporary pools (Crump et al. 1992). Thus, unlike the vast majority of extinctions (cf Ladle 2009), the fi nal, rapid disappearance of the golden toad was well documented. More than 1,500 toads were observed in 1987, but only a single toad was observed at the main known breeding site in 1988 and 1989 while seven adult males and two adult females were recorded 4–5 km away in 1988. No verified sightings have been reported since (Crump et al. 1992; Pounds and Crump 1994; Sarkar 1996). However, published accounts of the procedures used to survey and monitor amphibians in the Monteverde cloud forest reserve are limited and rather imprecise. Pounds et al. (1997: 1316) write that the “Monteverde reserve has been almost constantly patrolled for 25 years,” a comment that Wake and Vredenburg (2008) cited as “daily monitoring.” To our knowledge, there is no published account (in print or online) on the frequency of toad monitoring, the extent of the monitored area after 1990, the proportion of the research area that has been systematically sampled, sampling method (day or night samplings), or whether any other forests in the vicinity have been searched. This apparent lack of systematic sampling of the reserve and/or of the wider region introduces a degree of uncertainty into data on the rate and timing of the observed decline (Crump et al. 1992; Sarkar 1996).

Initially, the toad’s disappearance was linked to the severe neotropical droughts of 1987–1988 attributed to El Niño-Southern Oscillation (ENSO) conditions (Crump et al. 1992; Pounds and Crump 1994). However, shortly after the toad’s disappearance, Crump et al. (1992) acknowledged that other factors (e.g., non-specifi c pathogen attacks) might have played a role in the extinction and also commented that impacts of prior environmental degradation (initiated before monitoring work began) could not entirely be ruled out. The articles based on population monitoring leading up to the crash made no mention of disease playing a role in the toad’s decline. Indeed, Crump et al. (1992) commented that data to address this possibility were lacking. Pounds et al. (1999) subsequently published a high-profi le article in Nature arguing that climate change was probably responsible for the decline or disappearance of a number of species of birds, reptiles, and amphibians in the area, citing the golden toad as a specifi c example. Pounds et al. (2006) provided

additional climate-trend analyses and developed a more refined argument for the toad’s extinction based on the temperature-sensitivity of the behaviour of the pathogenic chytrid fungus Batrachochytrium dendrobatidis (but see Lips et al. 2008; Rohr et al. 2008; Cheng et al. 2011; Garner et al. 2011, for counterarguments against this hypothesis). Pounds et al. stated that their data supported with “very high confi dence” the case for large-scale climate warming being key to the loss of a number of amphibians and implicated this temperature-sensitive chytrid as an integral component of the causal nexus leading to amphibian declines. They focused on species in the genus Atelopus (harlequin frogs) for the most part, but also cited the golden toad as subject to the same drivers (Pounds et al. 2006). Signifi cantly, these later arguments did not cite any new evidence regarding the extinction of the golden toad.

To attribute climate change as the single major cause of any extinction event is problematic (Whitfi eld et al. 2007; Ladle 2009) because there is often no proper way of scientifi cally distinguishing a specific climate-change influence from historical variability in climate and other environmental conditions (Anchukaitis and Evans 2010). The arguments of Pounds et al. (1999, 2006) that climate change was the main causal factor in the extinction of the golden toad coincided with a marked increase in climate change discourse in conservation generally. This followed a shift from 1987 to 1992 in the United Nation’s focus from “poverty reduction in developed countries” to the “biodiversity crisis,” including climate change, biodiversity, and forests (McManus 2000). Climate change was one of the main issues during the United Nations Conference on Environment and Development (UNCED) in Rio 1992, the Conference of the Parties in Geneva 1996 (COP2), and Kyoto 1997 (COP3).

More generally, the focus of the international community on climate change has had signifi cant consequences for conservation (Jepson and Ladle 2010), not least because many sources of conservation research funding have become linked to understandable concerns about how changing climate might impact wildlife and ecosystems. Many conservationists and conservation organisations quickly aligned behind this increasingly dominant environmental theme (Ladle et al. 2005; Ladle and Jepson 2010). In this context, the transformation of the golden toad from an obscure species of mainly herpetological interest into a prominently cited example of a contemporary extinction event (e.g., Pearson 2011) and a global icon for climate change (Stork and Samways 1995) provides an intriguing window into the use of scientifi c information for conservation advocacy.

To better understand the demise of the golden toad and how its story has been used and relayed, we present a comparative assessment of the reporting of its extinction in the academic literature (peer-reviewed journal articles) and in the news media (internet and newspapers). We also reflect on the potential implications for public perceptions of science and conservation.

Golden toad as a climate change icon species / 293

MATERIALS AND METHODS

We searched the peer-reviewed journal literature via two databases: Scopus and the ISI Web of Knowledge. We obtained six results from Scopus that included “Bufo periglenes” (title, keywords, and body), and six that included “golden toad.” From the ISI Web of Knowledge, we obtained 18 articles that included the term “Bufo periglenes” and 29 that included “golden toad” (Appendix 2). We did not fi nd any peer-reviewed article that included “Incilius periglenes.” In total, we retrieved 40 peer-reviewed articles published between 1972 and 2010.

We used the LexisNexis® database to search all news articles from all available sources of published information (newspapers, newswires, magazines, broadcast transcripts, and some blogs) that contained the words “golden toad” and “sapo dorado” (common name in Spanish). This search included articles published and captured electronically from January 1983 to March 2010. In all, we obtained 530 articles published in Spanish and English. After screening and deleting duplicated news or reports not related to amphibians (such as cultural or sports news), we compiled a database of 400 articles.

We recorded the following information for peer-reviewed and news articles: title/headline, month, year, type of article/news, name of the source, country of release, and whether the author(s) mentioned other amphibian species or other species in general. We categorised presumed causes of disappearance for I. periglenes or population changes for other specifi cally mentioned amphibian species as: climate change, habitat loss (including deforestation), pollution (including pesticides, chemical wastes), ultraviolet radiation, alien species, acid rain, ENSO (i.e., climate variability as opposed to long-term change), and diseases (including viruses and fungi). If the identifi ed cause of population change did not fi t into

the above classifi cation, we recorded it as “other causes” and recorded any additional information on population status (decline, disappearance, extinction, etc.) mentioned in the article.

To further identify and characterise reports in media sources and academic journals we searched for signifi er keywords or statements in the headline or in the main body of the text such as: wiped out, extinct(ion), probably or believed to be extinct, not seen, endangered, threatened, disappeared, vanish(ed), declining, killed (fatal), mass extinction and “canaries in a coal mine.” We also recorded other information contained in media reports such as direct quotes attributed to non-governmental organisations (NGOs), university researchers, and government offi cials, as well as events such as conferences, and scientifi c articles related to the published news. Additionally, we surveyed 92 peer-reviewed articles (selected haphazardly from 385 papers identifi ed via Scopus in January 2011), which cited Pounds et al. (2006), to specifi cally assess how authors represented this important article in the scientifi c literature. To avoid operator variance the fi rst author performed all literature research, data extraction, and compilation to standardise interpretation and classifi cation of the information.

RESULTS

News items containing the term “golden toad” increased irregularly over time with four peaks in frequency (Figure 1) and an annual mean of 14.86 ± a standard deviation of 15.39. In contrast, the number of peer-reviewed articles in scientifi c journals containing either “golden toad” or “Bufo periglenes” or “B. periglenes” was consistently low over the study period, with a mean of 1.33 ± 1.33 articles per annum. The frequencies of news items and peer-reviewed articles were not correlated (adjusted R2 = 0.002, P = 0.31, Figure 1).

Figure 1Number of peer-reviewed articles (sources: ISI Web of Knowledge and Scopus) and news (via LexisNexis®) published

containing the term “golden toad” and/or “Bufo periglenes”. The description of the golden toad was in 1966, following which we could not fi nd peer-reviewed articles until 1983.

The fi rst news in the LexisNexis® database occurred in the same year.

294 / Ochoa-Ochoa et al.

Authors of popular articles invoked different causes for the disappearance of I. periglenes from Monteverde through time. Several causes were identifi ed shortly after the extinction event was reported; those causes typically were described as having high uncertainty. This changed over time and climate change and the amphibian fungal disease, chytridiomycosis, became the dominant reported causes by 2000 (Figure 2). As the number of articles varied through time, we used the proportion of the number of times that different causes were mentioned within the news to illustrate these trends (Figure 2). It should be noted that some of the articles discuss other amphibians in addition to I. periglenes.

We found it more difficult to quantify any trends in statements regarding causes of declines in the peer-reviewed articles due to the low number of published articles containing the search terms (Appendix 2). From the 40 peer-reviewed articles retrieved from the search, we were only able to use 32 in the analysis. One article provided only a description of the toad, three others were specifi cally related to life history, and we were unable to obtain copies of another four. Most remaining articles evaluated more than one cause. A large proportion (17) of the peer-reviewed articles highlighted the golden toad as an example of unexplained decline, another seven mentioned weather variability including ENSO, another fi ve chytridiomycosis, and one the pet trade. Six articles mentioned climate change as the main factor driving the extinction (Appendix 2). The change in the strength of the rhetoric used by the news media to tell the story of the golden toad is also refl ected in the increase in value-laden adjectives such as “wiped out” or “vanished”, which peaked in 2006 (Figure 3). The use of the phrase “mass extinction” in the news media also peaked that year.

Whilst a relatively small number of peer-reviewed articles have been published about the golden toad, some have had considerable impact throughout the popular and scientifi c media, most notably, the article by Pounds et al. (2006). This article has been cited for various reasons. Forty-eight articles cited Pounds et al. (2006) as an example of disease impacts promoted by climate change or by climatic or environmental variability. Twenty-one articles cited it as an example of species vulnerability to climate change per se, while six other articles referred to it as an example of chytridiomycosis, and nine challenged the hypothesis presented by Pounds et al. (2006). Finally, eight articles cited the paper as illustrating other causes of amphibian declines (Appendix 3).

DISCUSSION

The observed change in the public media’s descriptions of potential causes of the golden toad’s extinction and of the uncertainty associated with them could have been infl uenced by the way climate change has come to dominate discussions of global change (Liu et al. 2011). Authors of articles in the public media arguably refl ected some of the tone of high-profi le scientifi c articles and their associated press releases, such as Thomas et al. (2004) and Pounds et al. (2006). As commented on elsewhere, the former article was widely misrepresented in the news media, partly due to misunderstanding of the uncertainties involved in complex modelling studies and partly as a result of extrapolations contained in the associated press release (Ladle et al. 2004, 2005).

The four recent peaks in the frequency of popular news items about the golden toad (Figure 1) roughly coincide with particular

Figure 2Proportional number of times per annum that each of the possible causes of amphibian decline were mentioned in news that included the golden toad.

Not all the causes are necessarily related to the disappearance of the golden toad.

Golden toad as a climate change icon species / 295

media events or publications. The fi rst peak coincided with the Kyoto conference in December 1997; the second peak (2000) is contemporaneous with two separate events: the press releases of the WWF report Living planet and the publication in Nature of the article Quantitative evidence for global amphibian population declines by Houlahan et al. (2000). The third peak coincided with two high-profi le publications: one in Nature, by Thomas et al. (2004) titled Extinction risk from climate change, and the other in Science, by Stuart et al. (2004) titled Status and trends of amphibian declines and worldwide extinctions; and with the release of the IUCN Global Amphibian Assessment (GAA) (IUCN 2008). The fi nal peak, and by far the biggest in terms of the frequency of news items, occurred after the publication of the article in Nature entitled Widespread amphibian extinctions from epidemic disease driven by global warming, by Pounds et al. (2006).

Although high-profi le academic articles may generate news stories, we found no quantitative association between the frequencies of the news-media items we surveyed and that of peer-reviewed published articles about the golden toad. This is not surprising given that the global news media does not typically consider peer-reviewed articles newsworthy by themselves, especially those in less prominent journals. Moreover, the publication of peer-reviewed articles is dictated by factors not necessarily in step with the public media’s focus at any given time.

Like the Thomas et al. (2004) study, the Pounds et al. (2006) article is a complex modelling study published in a high-profi le journal that suggested more certainty to some readers than often is stated in scientifi c articles. For example, the authors

stated in the opening paragraph (which served as an executive summary): “we conclude with ‘very high confi dence’ (>99%, following the Intergovernmental Panel on Climate Change, IPCC) that large-scale warming is a key factor in the disappearances [of 67% of 110 species of harlequin frogs and the golden toad].” They concluded the abstract with the non sequitur that “the urgency of reducing greenhouse-gas concentrations is now undeniable.” Language such as ‘very high confi dence’ and ‘undeniable’ conveys technical meaning while also providing strong words for global news stories in the popular media. While the phrase ‘very high confi dence’ still denotes uncertainty, it indicates a very small measure of doubt, unlikely to produce concerns in the minds of the lay reader. Indeed, considering that the chain of argumentation in the paper relies on several untestable assumptions (given the lack of direct monitoring or other autoecological data and thus the poor resolution of what drove the population declines), the use of such a strong expression of confi dence appears unwarranted, and indicative of an effort to downplay uncertainty. The use of such a phrase can have consequences similar to those arising from the use of another technical expression common in bioclimatic envelope modelling—‘committed to extinction’ (e.g., Thomas et al. 2004), which means en route to eventual extinction if no mitigation is undertaken, but which frequently has been simplifi ed to ‘will be extinct by date x’ by the global news media (Ladle et al. 2005; Ladle and Jepson 2010).

It is hard to determine why it is that particular over-simplifi ed narratives encapsulated by statements such as… “golden toad driven to extinction by climate change”

Figure 3Frequency of use of different labels referring to the disappearance of the golden toad in news items

296 / Ochoa-Ochoa et al.

or “one million species extinct by 2050” gain traction via the media and conservation NGOs, when other explanations or narratives published in similarly respectable or highly cited journals do not (but see for e.g., Ladle et al. 2005). For instance, following the Pounds et al. (2006) paper, the golden toad became a major element of the story in the media, despite the main focus of the article being on a completely different genus, Atelopus. Although the golden toad is mentioned in the abstract alongside Atelopus, the article provides little further mention (and no new data) of the demise of the golden toad. In contrast, a recent article arguing that the extinction of the golden toad was caused by increased climate variability rather than directional climate change (Anchukaitis and Evans 2010) was not reported widely in public media, despite also being published in a high-profi le journal.

The elevation of the golden toad to iconic status illustrates how selected writings in scientifi c journals and the popular media are related and interpreted, despite scientific uncertainties or improved information over time. The biggest NGOs were quick to use the rhetorical potential of the golden toad and have been instrumental in turning the toad into a fl agship species for climate change (see Ladle and Jepson 2010). Stork and Samways (1995) defined fl agship species as “popular charismatic species that serve as symbols and rallying points to stimulate conservation awareness and action.” The important status of the golden toad is illustrated clearly by the following quotes from the websites of big NGOs and newspapers: conservation International’s website stated “For Ticos, as Costa Rican natives are known, reducing greenhouse gas emissions and stabilizing the climate is personally important, as the extinction of their emblematic golden toad (Bufo [Incilius] periglenes) due to climate change and altered weather patterns is still fresh” (Conservation International 2011); Mr Andrew Kerr of the World Wildlife Fund stated “Global warming has already claimed its fi rst species, with Costa Rica’s golden toad believed to have become extinct” (The Herald 2000); and The Independent (London), on September 18, 2006, stated “Human-induced climate change has already claimed its fi rst victims. The golden toad and the harlequin frog of Costa Rica have disappeared as a direct result of global warming” (The Independent 2006).

Conservation NGOs play an important role in determining conservation agendas, funding initiatives and interventions, liaising with politicians and policy makers, and, signifi cantly, communicating with the public (Jepson and Ladle 2010). However, information reported in scientifi c journals and further reported and possibly transformed in the public media can become asymmetrical, not necessarily tethered to scientifi cally recognised realities of uncertainty or improved analyses, and can take on a life of its own, even among relatively informed groups. More generally, our results provide insights into how reports in the peer-reviewed literature and the popular press can be closely related when peer-reviewed articles contain sensationalist or strident

headlines and poorly related when not. The results also show how information from both sources changed over time and suggest ways excerpts of scientifi c information, once established in the public media, can be used further in important environmental, social, and political contexts around the world.

Nearly two decades ago Pechmann and Wilbur (1994) argued that there was insuffi cient information about amphibian populations to confirm the perceived worldwide decline of amphibian populations. More recently Salvidio (2009) re-analysed 16 amphibian populations monitored for more than 15 years, and reported that all of them have shown stable long-term population dynamics. This fi nding is intriguing, although we emphasise that 16 species and 15 years are insuffi cient sample sizes on a global scale for us to draw any clear conclusions. We see no reason to doubt that amphibians are a threatened taxonomic group as a whole, with many species in danger of extinction due to a range of environmental factors, including climate change (Collins and Storfer 2003; Wake and Vredenburg 2008).

When Pechmann and Wilbur (1994) raised the question of “Playing it safe or crying frog?”, they were alluding to the potential negative repercussions of any incorrect reports of amphibian declines. Almost 20 years have passed since widespread amphibian declines were fi rst reported and population declines have been reported among many species, as they have for other taxonomic groups (e.g., Malcolm et al. 2006; Saino et al. 2011). Today, amphibians are no longer a forgotten group. Initiatives such as the Declining Amphibians Population Task Force (DAPTF) and others have increased general awareness and knowledge about amphibians substantially, although it remains the case that there is a lack of standardised monitoring data for most amphibian species/populations (e.g., Frías-Alvarez et al. 2010).

Communicating science via the popular media is diffi cult, yet critically important. As some authors have already emphasised, scientists, as sources in the media, have to think carefully about how the information they are giving is going to be interpreted (Friedman et al. 1999). The dynamics and goals of reporting information in the popular media often differ substantially from those of reporting research results in scientifi c journals (Schmidt 2009). This suggests that as a profession we need to strive harder yet to maintain the integrity of science in the public eye by stating clearly what we know and do not know when writing for a journal or communicating more directly with the public. Whilst scientists cannot control how the information they supply will be represented in the media and by interest groups and the polity, the following steps may reduce the probability of misrepresentation: careful drafting of press releases and responses to questions from the media; avoiding providing potentially misleading extrapolations or ‘sound bites’; and providing succinct summaries of their articles written in layman’s terms which are published on institutional websites as soon as media coverage is initiated. These summaries should include clear

Golden toad as a climate change icon species / 297

statements of the key assumptions and caveats of the research, the funding sources, and any confl icts of interest. We also recommend full use of digital communication platforms such as blogs (Ashlin and Ladle 2006) and social networking sites and that authors work closely with institutional press offi ces and take opportunities to participate in media training workshops and courses.

ACKNOWLEDGEMENTS

The fi rst author’s doctoral studies were supported by Consejo Nacional de Ciencia y Tecnología (CONACyT), Mexico and Secretaría de Educación Pública (SEP), Mexico. The authors thank R. de Villa Magallón, S. Nogué, two anonymous reviewers, and the handling editor for their insightful and helpful comments on the manuscript.

REFERENCES

Alford, R.A. and S.J. Richards. 1999. Global amphibian declines: a problem in applied ecology. Annual Review of Ecology and Systematics 30: 133–165.

Anchukaitis, K.J. and M.N. Evans. 2010. Tropical cloud forest climate variability and the demise of the Monteverde golden toad. Proceedings of the National Academy of Sciences of the United States of America 107(11): 5036–5040.

Ashlin, A. and R.J. Ladle. 2006. Environmental science adrift in the blogosphere. Science 312(5771): 201.

Blaustein, A.R. 1994. Chicken Little or Nero’s fi ddle? A perspective on declining amphibian populations. Herpetologica 50(1): 85–97.

Blaustein, A.R. and D.B. Wake. 1990. Declining amphibian populations: a global phenomenon? Trends in Ecology and Evolution 5(7): 203–204.

Blaustein, A.R., J.M. Kiesecker, D.P. Chivers, D.G. Hokit, A. Marco, L.K. Belden, and A. Hatch. 1998. Effects of ultraviolet radiation on amphibians: fi eld experiments. American Zoologist 38(6): 799–812.

Cheng, T.L., S.M. Rovito, D.B. Wake, and V.T. Vredenburg. 2011. Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences of the United States of America 108(23): 9502–9507.

Collins, J.P. and A. Storfer. 2003. Global amphibian declines: sorting the hypotheses. Diversity and Distributions 9(2): 89–98.

Conservation International. 2011. Costa Rica. http://www.conservation.org/where/north_america/costarica/Pages/costarica.aspx. Accessed in August, 2011.

Crump, M.L., F.R. Hensley, and K.L. Clark. 1992. Apparent decline of the golden toad: underground or extinct? Copeia 2: 413–420.

Cushman, S.A. 2006. Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biological Conservation 128(2): 231–240.

Frías-Alvarez, P., J. Zúñiga-Vega, and O. Flores-Villela. 2010. A general assessment of the conservation status and decline trends of Mexican amphibians. Biodiversity and Conservation 19(13): 3699–3742.

Friedman, S.M., S. Dunwoody, and C.L. Rogers. 1999. Communicating uncertainty: media coverage of new and controversial science. Mahwah, NJ: Lawrence Erlbaum Associates, Inc.

Garner, T.W.J., J.M. Rowcliffe, and M.C. Fisher. 2011. Climate change, chytridiomycosis or condition: an experimental test of amphibian survival. Global Change Biology 17(2): 667–675.

Gillespie, G. 2010. Population age structure of the spotted tree frog Litoria spenceri: insights into population declines. Wildlife Rescue 37(1): 19–26.

Houlahan, J.E., C.S. Findlay, B.R. Schmidt, A.H. Meyer, and S.L. Kuzmin.

2000. Quantitative evidence for global amphibian population declines. Nature 404(6779): 752–755.

IUCN (International Union for Conservation of Nature). 2008. The IUCN Red List of threatened species. 2008. http://www.iucnredlist.org/initiatives/amphibians/analysis. Accessed in February, 2011.

Jepson, P.J. and R.J. Ladle. 2010. Conservation: a beginner’s guide. Oxford: Oneworld.

Ladle, R.J. 2009. Forecasting extinctions: uncertainties and limitations. Diversity 1(2): 133–150.

Ladle, R.J. and P.J. Jepson. 2010. Origins, uses and transformation of extinction rhetoric. Environment and Society: Advances in Research 1(1): 96–115.

Ladle, R.J., P.J. Jepson, M.B. Araújo, and R.J. Whittaker. 2004. Dangers of crying wolf over risk of extinctions. Nature 428(6985): 799.

Ladle, R.J., P.J. Jepson, and R.J. Whittaker. 2005. Scientists and the media: the struggle for legitimacy in climate change and conservation science. Interdisciplinary Science Reviews 30(3): 231–240.

Lips, K.R., J. Diffendorfer, J.R. Mendelson III, and M.W. Sears. 2008. Riding the wave: reconciling the roles of disease and climate change in amphibian declines. Public Library of Science Biology 6(3): 0441–0454.

Liu, X., E. Lindquist, and A. Vedlitz. 2011. Explaining media and congressional attention to global climate change, 1969–2005: an empirical test of agenda-setting theory. Political Research Quarterly 64(2): 405–419.

Malcolm, J.R., C. Liu, R.P. Neilson, L. Hansen, and L. Hannah. 2006. Global warming and extinctions of endemic species from biodiversity hotspots. Conservation Biology 20(2): 538–548.

McManus, P.A. 2000. Beyond Kyoto? Media representation of an environmental issue. Australian Geographical Studies 38(3): 306–319.

Pearson, R. 2011. Driven to extinction. New York, NY: Sterling.Pechmann, J.H.K. and H.M. Wilbur. 1994. Putting declining amphibian

populations in perspective: natural fl uctuations and human impacts. Herpetologica 50: 65–84.

Pounds, J.A. and M.L. Crump. 1994. Amphibian declines and climate disturbance: the case of the golden toad and the harlequin frog. Conservation Biology 8(1): 72–85.

Pounds, J.A., M.P.L. Fogden, and J.H. Campbell. 1999. Biological response to climate change on a tropical mountain. Nature 398(6728): 611–615.

Pounds, J.A., M.P.L. Fogden, J.M. Savage, and G.C. Gorman. 1997. Tests of null models for amphibian declines on a tropical mountain. Conservation Biology 11(6): 1307–1322.

Pounds, J.A., M.R. Bustamante, L.A. Coloma, J.A. Consuegra, M.P.L. Fogden, P.N. Foster, E. La Marca, et al. 2006. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439(7073): 161–167.

Reading, A. 2004. Hope and despair. London: the Johns Hopkins University Press.

Rohr, J.R., T.R. Raffel, J.M. Romansic, H. McCallum, and P.J. Hudson. 2008. Evaluating the links between climate, disease spread and amphibian declines. Proceedings of the National Academy of Sciences of the United States of America 105(45): 17436–17441.

Saino, N., R. Ambrosini, D. Rubolini, J. von Hardenberg, A. Provenzale, K. Hüppop, O. Hüppop, et al. 2011. Climate warming, ecological mismatch at arrival and population decline in migratory birds. Proceedings of the Royal Society of London B: Biological Sciences 278(1707): 835–842.

Salvidio, S. 2009. Detecting amphibian population cycles: the importance of appropriate statistical analyses. Biological Conservation 142(2): 455–461.

Sarkar, S. 1996. Ecological theory and anuran declines. BioScience 46(3): 199–207.

Savage, J.M. 1966. An extraordinary new toad (Bufo) from Costa Rica. Revista de Biología Tropical 14: 153–167.

Schmidt, C.W. 2009. Communication gap: the disconnect between what

298 / Ochoa-Ochoa et al.

scientists say and what the public hears. Environmental Health Perspectives 117(12): A548–A551.

Stork, N.E. and M.J. Samways. 1995. Inventorying and monitoring of biodiversity. In: Global biodiversity assessment (ed. Heywood, V.H.). Pp. 453–544. Cambridge: Cambridge University Press.

Stuart, S.N., J.S. Chanson, N.A. Cox, B.E. Young, A.S.L. Rodrigues, D.L. Fischman, and R.W. Waller. 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306(5702): 1783–1786.

The Herald. 2000. Apocalypse soon for third of wildlife. http://www.highbeam.com/doc/1P2-23809769.html. August 31, 2000. Accessed in February, 2011.

The Independent. 2006. Industrial countries have a moral responsibility to lead. http://www.questia.com/library/1P2-2045378/industrial-countries-have-a-moral-responsibility-to. September 18, 2006. Accessed in February, 2011.

Thomas, C.D., A. Cameron, R.E. Green, M. Bakkenes, L.J. Beaumont, Y.C. Collingham, B.F.N. Erasmus, et al. 2004. Extinction risk from climate change. Nature 427(6970): 145–148.

Wake, D.B. and V.T. Vredenburg. 2008. Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proceedings of the National Academy of Sciences of the United States of America 105(Supplement 1): 11466–11473.

Whitfi eld, S.M., K.E. Bell, T. Philippi, M. Sasa, F. Bolaños, G. Chaves, J.M. Savage, et al. 2007. Amphibian and reptile declines over 35 years at La Selva, Costa Rica. Proceedings of the National Academy of Sciences of the United States of America 104(20): 8352–8356.

WWF. 2000. Living planet report. http://wwf.panda.org/about_our_earth/all_publications/living_planet_report/living_planet_report_timeline/lpr00/. Accessed in February, 2011.

Received: July 2012; Accepted: December 2012

Golden toad as a climate change icon species / 299

Appendix 1Some examples of causes linked to amphibian populations declining around the world. Between parentheses are the numbers of articles found related to the topic at the moment of the search. The threats are divided into major groups (underlined), and divided further as fi ner processes.

Threat type Proposed mechanism Consequences or change in status (examples)Habitat loss

Habitat transformation (18) Amphibian species respond differentially to environmental changes

Richness was greatest in wetlands with forest permanency (Kolozsvary and Swihart 1999)

If intact, continuous forest continues to be harvested, species that require ponds with longer hydro-periods for successful metamorphosis would be prone to population declines

Populations decline (Neckel-Oliveira and Lannoo 2007)

Deforestation (68) Whereas forest specialists suffer direct negative effect from deforestation, generalist species can take advantage of forest alteration and the presence of farm animals

Population declines of specialist species (Cushman 2006; Furlani et al. 2009; Swift and Hannon 2010)

Low density, population variability, and high mobility coupled with restricted habitat needs predispose woodland amphibians to local extinction caused by habitat fragmentation

Decrease in species richness (Gibbs 1998)

Fragmentation (346) There is a negative correlation between the abundance of frogs in the matrix and their vulnerability to fragmentation; however, results varied with fragment size and species traits

Decrease in species abundance (Dixo and Metzger 2010)

Pollution

Pesticides and chemical wastes (499)

Pesticides can cause variation in enzymatic levels among several tadpole species

It appears that a conversion of native ecosystems to soybean crops may lead to increased ecological risks for anuran amphibians (Davidson 2004; Sparling and Fellers 2007; Rohr et al. 2008; Lajmanovich et al. 2010)

Acid rain (24) Low pH has a negative effect on body size (Frisbie and Wyman 1995)

Heavy metals (81): including iron, manganese, aluminum, mercury, cadmium, and bellyrium

Cadmium inhibits acid secretion in stimulated frog gastric mucosa; Cu affects the liver metallothionein

No apparent effect on population dynamics (Lefcort et al. 1998; Loumbourdis 2006; Cooper and Fortin 2010; Gerbino et al. 2010)

Ultraviolet radiation (242)Lab experiments: UV-B has an overall negative effect in Ambystoma mexicanum. Proportion of deformed embryos varied through the year (Frías-Alvarez et al. 2010).Field experiments: “no differences in survival to hatching among UV-B-exposed and UV-B-shielded treatment” for Rana muscosa, Bufo canorus, or Pseudacris regilla (Vrenderburg et al. 2010)

UV-B (280–315 nm) can be easily absorbed by living cells and causes DNA mutation and/or cell death; induces lethal and sub-lethal effects on different ontogenetic phases of development

1.1% of the distribution of Ambystoma macrodactylum is exposed to lethal levels of radiation (Palen and Schindler 2010)

Hatching success is unaffected by UV-B radiation. We suggest that UV-B radiation is an unlikely cause for declining populations of Rana aurora (Blaustein et al. 1996).Although UV-B radiation may not contribute to the population declines of all species, it may play a role in the population decline of some species (3 of 17) (Review of fi eld experiments; Blaustein et al. 1998)By itself, UV-B causes no signifi cant effects in Hyla chrysoselis and Rana blairi (Bruner et al. 2002)

DiseasesFungi (332): principally chytrids Focused principally in chytrids Mass mortality of several species in Central

America (Lips 1998, 1999; Lips et al. 2005; but see Kilpatrik et al. 2010)

Batrachochytrium dendrobatidis (Bd) destroys keratinised mouthparts in anuran tadpoles, which are essential for feeding

Bd infection reduces foraging effi ciency of anuran tadpoles by altering feeding kinematics and reduces host fi tness (Venesky et al. 2010)

Contd...

300 / Ochoa-Ochoa et al.

Appendix 1Contd...

Threat type Proposed mechanism Consequences or change in status (examples)Potentially disrupts osmoregulation or respiration across the skin of amphibians it infects, releases toxins into the host, or both

Results show inhibited rehydration in individuals exhibiting clinical signs of chytridiomycosis. However, aclinical chytridiomycosis does not severely affect amphibian skin function. From six (Litoria raniformis) individuals infected, only one died (Venesky et al. 2010).

Bacteria (105) Opportunistic pathogen associated with cutaneous infections and nodular granulomatous skin lesions

Lab experiments: the infection does not cause death (Sánchez-Morgado et al. 2009)

Red-legged disease (bacterial dermatosepticemia)

Can cause deaths (Densmore and Green 2007)

No lethal consequences (Davis and Cecala 2010)Viruses (110) Can cause mass mortality (Daszak et al. 1999; Collins and

Storfer 2003)Alien species Introduction of new predators Extinction, but species can recover if the alien species is

removed (Kats and Ferrer 2003)Climate variability Warmer temperatures than normal, especially

during the dry seasonNo clear signal between temperature and population decline (Alexander and Eischeid 2010)

Droughts: La Niña, El Niño events “Climate anomalies are not a feature of all extinctions, it is not unreasonable to expect that natural climate variability can interact with species life history and ecological community and population dynamics to contribute to extinctions”

Disappearance of B. periglenes (Anchukaitis and Evans 2010)

Combination of factors, unusual warm weather, and the presence of Bd

Extinction (Barrionuevo and Ponssa 2008)

Climate change Thermal-optimum for Bd growth Extinction (Pounds et al. 2006; but see Appendix 3 for cf references)

Climate envelope models Extinction and displacement of distribution ranges (several authors, including Lawler et al. 2010 and Ochoa-Ochoa et al. 2012)

Golden toad as a climate change icon species / 301

App

endi

x 2

List

of s

cien

tifi c

art

icle

s inc

ludi

ng th

e te

rms “

Buf

o pe

rigl

enes

” an

d/or

“go

lden

toad

” re

sulti

ng fr

om th

e se

arch

es in

bot

h Sc

opus

and

the

ISI W

eb o

f Kno

wle

dge,

as o

f Apr

il 20

10.

Aut

hors

Year

Title

Jour

nal

Exa

mpl

e of

po

pula

tion

decl

inin

g by

clim

ate

chan

geW

eath

er

vari

abili

tyO

ther

Exa

mpl

e of

un

expl

aine

d po

pula

tion

decl

inin

gC

omm

ents

Anc

huka

itis

and

Evan

s20

10Tr

opic

al c

loud

for

est c

limat

e va

riabi

lity

and

the

dem

ise

of th

e M

onte

verd

e go

lden

toad

Proc

eedi

ngs

of th

e Na

tiona

l Aca

dem

y of

Sc

ienc

es o

f the

Uni

ted

Stat

es o

f Am

eric

a

ENSO

Bar

rionu

evo

and

Pons

sa20

08D

eclin

e of

thre

e sp

ecie

s of

the

genu

s Te

lmat

obiu

s (A

nura

: Lep

toda

ctyl

idae

) fr

om T

ucum

an P

rovi

nce,

Arg

entin

a

Her

peto

logi

caYe

s

Bla

uste

in

and

Wak

e19

90D

eclin

ing

amph

ibia

n po

pula

tions

: a

glob

al p

heno

men

onTr

ends

in E

colo

gy

and

Evol

utio

nYe

s

Bla

uste

in

et a

l.19

96D

NA

rep

air

activ

ity a

nd r

esis

tanc

e to

so

lar

UV-

B r

adia

tion

in e

ggs

of th

e re

d-le

gged

fro

g

Con

serv

atio

n Bi

olog

yYe

s

Bla

uste

in

et a

l.19

98Ef

fect

s of

ultr

avio

let r

adia

tion

on

amph

ibia

ns: fi

eld

exp

erim

ents

Amer

ican

Zoo

logi

stYe

s

Bla

uste

in

et a

l.19

99D

NA

rep

air

and

resi

stan

ce to

UV-

B

radi

atio

n in

wes

tern

spo

tted

frog

sEc

olog

ical

Ap

plic

atio

nsYe

s

Bru

ner

et a

l.20

02D

evel

opm

enta

l effe

cts

of a

mbi

ent

UV-

B li

ght a

nd la

ndfi l

l lea

chat

e in

Ra

na b

lair

i and

Hyl

a ch

ryso

scel

is

Ecot

oxic

olog

y an

d En

viro

nmen

tal S

afet

yYe

s

Buc

hann

an19

94Se

xual

dim

orph

ism

in H

yla

squi

rella

: ch

rom

atic

and

pat

tern

var

iatio

n be

twee

n th

e se

xes

Cop

eia

Sexu

al

dim

orph

ism

Bur

row

es

et a

l.20

04Po

tent

ial c

ause

s fo

r am

phib

ian

decl

ines

in P

uerto

Ric

oH

erpe

tolo

gica

Yes

Exte

nsio

n of

the

dry

seas

on is

an

othe

r as

pect

of

clim

ate

chan

ge

that

has

bee

n su

gges

ted

to a

ffect

tro

pica

l am

phib

ians

(D

onne

lly

and

Cru

mp

1998

) an

d ha

s be

en

asso

ciat

ed w

ith th

e ex

tinct

ion

of

B. p

erig

lene

s in

Cos

ta R

ica

Bus

tarn

ante

et

al.

2005

Cha

nges

in d

iver

sity

of

seve

n an

uran

co

mm

uniti

es in

the

Ecua

doria

n A

ndes

Biot

ropi

caYe

sIn

crea

se in

the

num

ber

of d

ry d

ays

Cor

ser

2001

Dec

line

of d

isju

nct g

reen

sa

lam

ande

r (A

neid

es a

eneu

s)

popu

latio

ns in

the

sout

hern

A

ppal

achi

ans

Biol

ogic

al

Con

serv

atio

nYe

s

Cru

mp

1989

Life

his

tory

con

sequ

ence

s of

fee

ding

ve

rsus

non

-fee

ding

in a

fac

ulta

tivel

y no

n-fe

edin

g to

ad la

rva

Oec

olog

iaLi

fe h

isto

ry

Cru

mp

et a

l.19

92A

ppar

ent d

eclin

e of

the

gold

en to

ad:

unde

rgro

und

or e

xtin

ct?

Cop

eia

Too

early

to k

now

Beca

use

of it

s un

pred

icta

ble

and

fl uct

uatin

g br

eedi

ng h

abita

t (sm

all

pool

s pr

one

to o

verfl

owin

g or

cont

d...

302 / Ochoa-Ochoa et al.

App

endi

x 2

cont

d...

Aut

hors

Year

Title

Jour

nal

Exa

mpl

e of

po

pula

tion

decl

inin

g by

clim

ate

chan

geW

eath

er

vari

abili

tyO

ther

Exa

mpl

e of

un

expl

aine

d po

pula

tion

decl

inin

gC

omm

ents

desic

catio

n), B

. per

igle

nes

is a

spec

ies

vuln

erab

le to

vag

arie

s of

the

wea

ther

. Fo

r thi

s re

ason

, the

pop

ulat

ion

mig

ht

fl uct

uate

wid

ely

in s

ize

due

to v

aria

ble

recr

uitm

ent s

ucce

ssD

asza

k et

al.

1999

Emer

ging

infe

ctio

us d

isea

ses

and

amph

ibia

n po

pula

tion

decl

ines

Emer

ging

Inf

ectio

us

Dis

ease

sC

hytri

diom

ycos

isH

ypot

hesi

sed

link

with

glo

bal

extin

ctio

n of

gol

den

toad

, Buf

o pe

rigl

enes

Fogd

en19

96C

onse

rvat

ion

of th

e go

lden

toad

: a

brie

f hi

stor

yH

erpe

tolo

gica

l Bi

olog

yN

ot r

evie

wed

as

PDF

was

not

av

aila

ble/

acce

ssib

leFo

ster

1992

The

inte

rnat

iona

l com

pone

nt o

f m

anag

ing

biol

ogic

al d

iver

sity

57th

Nor

th A

mer

ican

wi

ldlif

e an

d na

tura

l res

ourc

es

conf

eren

ce-c

ross

road

s of

con

serv

atio

n:

500

year

s af

ter

Colu

mbu

s

Not

rev

iew

ed a

s PD

F w

as n

ot

avai

labl

e/ac

cess

ible

Funk

and

D

unla

p19

99C

olon

izat

ion

of h

igh-

elev

atio

n la

kes

by lo

ng-to

ed

sala

man

ders

(Am

byst

oma

mac

roda

ctyl

um)

afte

r th

e ex

tinct

ion

of in

trodu

ced

trout

pop

ulat

ions

Can

adia

n Jo

urna

l of

Zool

ogy

Yes

Goe

rck

1997

Patte

rns

of r

arity

in th

e bi

rds

of th

e A

tlant

ic f

ores

t of

Bra

zil

Con

serv

atio

n Bi

olog

ySm

all c

atas

troph

e or

dis

ease

Griffi t

hs20

01C

onse

rvat

ion

biol

ogy

and

decl

inin

g am

phib

ian

popu

latio

nsRi

vi I

drob

iolo

gyN

ot r

evie

wed

as

PDF

was

not

av

aila

ble/

acce

ssib

leH

ays

et a

l.19

96D

evel

opm

enta

l res

pons

es o

f am

phib

ians

to s

olar

and

artifi c

ial

UV

B s

ourc

es: a

com

para

tive

stud

y

Phot

oche

mis

try

and

Phot

obio

logy

Yes

Her

o et

al.

2005

Ecol

ogic

al tr

aits

of

decl

inin

g am

phib

ians

in u

plan

d ar

eas

of e

aste

rn

Aus

tralia

Jour

nal o

f Zoo

logy

Yes

Jaco

bson

1983

Shor

t sea

son

of th

e go

lden

toad

Inte

rnat

iona

l Wild

life

Not

rev

iew

ed a

s PD

F w

as n

ot

avai

labl

e/ac

cess

ible

Jaco

bson

an

d Va

nden

berg

1991

Rep

rodu

ctiv

e ec

olog

y of

th

e en

dang

ered

gol

den

toad

(B

ufo

peri

glen

es)

Jour

nal o

f H

erpe

tolo

gyPe

t tra

deYe

s

Lips

1998

Dec

line

of a

trop

ical

mon

tane

am

phib

ian

faun

aC

onse

rvat

ion

Biol

ogy

Chy

tridi

omyc

osis

Yes

Lips

1999

Mas

s m

orta

lity

and

popu

latio

n de

clin

es o

f an

uran

s at

an

upla

nd s

ite

in w

este

rn P

anam

a

Con

serv

atio

n Bi

olog

yYe

s

cont

d...

Golden toad as a climate change icon species / 303

App

endi

x 2

cont

d...

Aut

hors

Year

Title

Jour

nal

Exa

mpl

e of

po

pula

tion

decl

inin

g by

clim

ate

chan

geW

eath

er

vari

abili

tyO

ther

Exa

mpl

e of

un

expl

aine

d po

pula

tion

decl

inin

gC

omm

ents

Lips

et a

l.20

05A

mph

ibia

n po

pula

tion

decl

ines

in

Latin

Am

eric

a: a

syn

thes

isBi

otro

pica

Chy

tridi

omyc

osis

*Ye

s

Liza

na a

nd

Pedr

aza

1998

The

effe

cts

of U

V-B

radi

atio

n on

toad

m

orta

lity

in m

ount

aino

us a

reas

of

cent

ral S

pain

Con

serv

atio

n Bi

olog

yYe

sM

any

hypo

thes

es h

ave

been

pro

pose

d to

exp

lain

this

decl

ine:

nat

ural

fl u

ctua

tions

of

the

popu

latio

ns (

see

refe

renc

es in

Bla

uste

in e

t al.

1994

b),

glob

al c

hang

es in

clim

ate,

long

dr

ough

t per

iods

, or

the

depl

etio

n of

th

e oz

one

laye

rN

adka

rni

and

Sola

no20

02Po

tent

ial e

ffect

s of

clim

ate

chan

ge o

n ca

nopy

com

mun

ities

in a

trop

ical

clo

ud

fore

st: a

n ex

perim

enta

l app

roac

h

Oec

olog

iaYe

sEN

SO

Not

t et a

l.19

95Ex

tinct

ions

rat

es: m

oder

n ex

tinct

ions

in

the

kilo

-dea

th r

ange

Cur

rent

bio

logy

Yes

Pasm

ans

et a

l.20

06A

mph

ibia

n de

clin

e: th

e ur

gent

nee

d fo

r am

phib

ian

rese

arch

in E

urop

eVe

teri

nary

Jou

rnal

Chy

tridi

omyc

osis

The

clas

sic e

xam

ple

of a

pa

ndem

ic a

mph

ibia

n di

seas

e is

chyt

ridio

myc

osis,

a f

unga

l dise

ase

caus

ed b

y Ba

trach

ochy

trium

de

ndro

batid

is th

at is

hel

d re

spon

sible

fo

r m

assiv

e am

phib

ian

die-

offs

and

ev

en f

or th

e ex

tinct

ion

of s

ever

al

spec

ies

wor

ldw

ide,

the

mos

t fam

ous

of w

hich

is th

e Co

sta R

ican

gol

den

toad

(Bu

fo p

erig

lene

s)Pe

chm

an

and

Wilb

ur19

94Pu

tting

dec

linin

g am

phib

ian

popu

latio

ns in

per

spec

tive:

nat

ural

fl u

ctua

tions

and

hum

an im

pact

s

Her

peto

logi

caN

atur

al

caus

es (

drou

ghts

)Th

e po

ssib

ility

rem

ains

that

they

are

st

ill p

rese

nt in

und

ergr

ound

or

othe

r re

treat

s, an

d th

at th

eir

appa

rent

di

sapp

eara

nces

rep

rese

nt e

xtre

me

natu

ral fl

uct

uatio

nsPh

illip

s19

90W

here

hav

e al

l the

fro

gs a

nd to

ads

gone

?Bi

osci

ence

Yes

Poun

ds19

90D

isap

pear

ing

gold

BBC

Wild

life

Not

rev

iew

ed a

s PD

F w

as n

ot

avai

labl

e/ac

cess

ible

Poun

ds a

nd

Cru

mp

1994

Am

phib

ian

decl

ines

and

clim

ate

dist

urba

nce:

the

case

of

the

gold

en

toad

and

the

harle

quin

fro

g

Con

serv

atio

n Bi

olog

yYe

s?EN

SO

Poun

ds

et a

l.19

97Te

sts

of n

ull m

odel

s fo

r am

phib

ian

decl

ines

on

a tro

pica

l mou

ntai

nC

onse

rvat

ion

Biol

ogy

Unu

sual

w

eath

erPo

unds

et

al.

2006

Wid

espr

ead

amph

ibia

n ex

tinct

ions

fr

om e

pide

mic

dis

ease

driv

en b

y gl

obal

war

min

g

Nat

ure

Yes

Poun

ds

et a

l.19

99B

iolo

gica

l res

pons

e to

clim

ate

chan

ge

on a

trop

ical

mou

ntai

nN

atur

eYe

s

Con

td...

304 / Ochoa-Ochoa et al.

App

endi

x 2

cont

d...

Aut

hors

Year

Title

Jour

nal

Exa

mpl

e of

po

pula

tion

decl

inin

g by

clim

ate

chan

geW

eath

er

vari

abili

tyO

ther

Exa

mpl

e of

un

expl

aine

d po

pula

tion

decl

inin

gC

omm

ents

Sava

ge19

72Th

e sy

stem

atic

sta

tus

of B

ufo

sim

us

with

des

crip

tion

of a

new

toad

fro

m

wes

tern

Pan

ama

Jour

nal o

f H

erpe

tolo

gyD

escr

iptio

n of

B. p

erip

atte

s

Vaira

2002

Anu

rans

of

a su

btro

pica

l mon

tane

fo

rest

in n

orth

wes

tern

Arg

entin

a:

ecol

ogic

al s

urve

y an

d a

prop

osed

list

of

spe

cies

of

cons

erva

tion

conc

ern

Biod

iver

sity

and

C

onse

rvat

ion

Yes

Wak

e an

d V

rede

nbur

g20

08A

re w

e in

the

mid

st o

f th

e si

xth

mas

s ex

tinct

ion?

A v

iew

fro

m th

e w

orld

of

amph

ibia

ns

Proc

eedi

ngs

of th

e N

atio

nal A

cade

my

of

Scie

nces

of t

he U

nite

d St

ates

of A

mer

ica

Yes

Golden toad as a climate change icon species / 305

App

endi

x 3

A se

lect

ion

of p

aper

s citi

ng P

ound

s et a

l. 20

06. T

he p

aper

s wer

e se

lect

ed h

apha

zard

ly, w

ith n

o pa

rtic

ular

cri

teri

a in

min

d, b

ut d

o no

t, st

rict

ly sp

eaki

ng, c

onst

itute

a ra

ndom

sam

ple.

The

sam

ple

of

92 c

ases

repr

esen

ts a

ppro

xim

atel

y 23

% o

f the

art

icle

s, se

lect

ed fr

om 3

85 p

aper

s in

Janu

ary

2011

, fro

m S

copu

s.

Art

icle

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

ch

ytri

diom

ycos

is

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

clim

ate

chan

ge

Exa

mpl

e of

cl

imat

e ch

ange

pr

omot

ing

chyt

ridi

omyc

osis

No

caus

e m

entio

ned

Exa

mpl

e of

A

PD b

ut n

o re

late

d ca

use

Exa

mpl

e of

ch

alle

ngin

g th

e C

TOH

Quo

tes

Aba

rca,

J.,

G. C

have

s, A

. G

arcí

a-Ro

dríg

uez,

and

R.

Varg

as. 2

010.

Rec

onsid

erin

g ex

tinct

ion:

red

iscov

ery

of I

ncili

us

hold

ridge

i (A

nura

: Buf

onid

ae)

in C

osta

Ric

a af

ter

25 y

ears

. H

erpe

tolo

gica

l Rev

iew

41(2

):150

–152

Yes

Thes

e di

sapp

eara

nces

hav

e be

en

attri

bute

d to

diff

eren

t cau

ses,

incl

udin

g cl

imat

e ch

ange

(Po

unds

19

97, 2

001)

and

em

erge

nt

dise

ases

suc

h as

chy

tridi

omyc

osis

(L

ips

et a

l. 20

06),

or th

e sy

nerg

istic

effe

ct b

etw

een

thes

e tw

o ag

ents

(Po

unds

et a

l. 20

06).

How

ever

, our

dis

cove

ry o

f a

popu

latio

n of

Inc

ilius

hol

drid

gei

in a

reg

ion

with

wel

l doc

umen

ted

chyt

ridio

myc

osis

(Pu

sche

ndor

f et

al.

2006

), al

low

s a

test

of

its

vuln

erab

ility

to th

is d

isea

se.

Aça

kaya

, R.H

., S.

H.M

. But

char

t, G

.M. M

ace,

S.N

. Stu

art,

and

C.

Hilt

on-T

aylo

r. 20

06. U

se a

nd m

isus

e of

the

IUC

N r

ed li

st c

riter

ia in

pr

ojec

ting

clim

ate

chan

ge im

pact

s on

bi

odiv

ersi

ty. G

loba

l Cha

nge

Biol

ogy

12(1

1): 2

037–

2043

Yes

Rec

ent s

tudi

es d

emon

stra

te th

at

clim

ate

chan

ge c

an a

ffect

spe

cies

vi

abili

ty m

uch

fast

er th

an im

plie

d by

ran

ge s

hifts

, whe

n it

inte

ract

s w

ith o

ther

fac

tors

.

Ago

sta,

S.J.

, N. J

anz,

and

D.R

. B

rook

s. 20

10. H

ow s

peci

alis

ts c

an

be g

ener

alis

ts: r

esol

ving

the

“par

asite

pa

rado

x” a

nd im

plic

atio

ns f

or

emer

ging

infe

ctio

us d

isea

se. Z

oolo

gia

27(2

): 15

1–16

2

Yes

The

curr

ent e

mer

ging

infe

ctio

us

dise

ase

(EID

) cr

isis

is “

new

” on

ly in

the

sens

e th

at th

is is

the

fi rst

suc

h ev

ent t

hat s

cien

tists

ha

ve w

itnes

sed

dire

ctly

.

Al-A

ttar,

A.M

. 201

0. H

emat

olog

ical

, bi

oche

mic

al a

nd h

istop

atho

logi

cal

studi

es o

n m

arsh

fro

g, R

ana

ridib

unda

, na

tura

lly in

fect

ed w

ith W

alto

nella

du

boisi

. Int

erna

tiona

l Jou

rnal

of

Zool

ogic

al R

esea

rch

6(3)

: 199

–213

Yes

Ale

mu,

J.B

., M

.N.E

. Caz

abon

, L.

Dem

pew

olf,

A. H

aile

y, R

.M.

Leht

inen

, R.P

. Man

nette

, K.T

. N

aran

jit, a

nd A

.C.J.

Roa

ch. 2

008.

Pr

esen

ce o

f th

e ch

ytrid

fun

gus

Batr

acho

chyt

rium

den

drob

atid

is

in p

opul

atio

ns o

f th

e cr

itica

lly

enda

nger

ed f

rog

Man

noph

ryne

ol

mon

ae in

Tob

ago,

Wes

t Ind

ies.

EcoH

ealth

5(1

): 34

–39

Yes

Chy

tridi

omyc

osis

is p

rese

ntly

en

dem

ic in

this

spe

cies

, with

a

prev

alen

ce o

f ab

out 2

0% a

nd n

o as

soci

ated

clin

ical

dis

ease

[…

] Th

us a

lthou

gh g

loba

l war

min

g m

ight

incr

ease

the

susc

eptib

ility

of

mon

tane

am

phib

ians

by

brin

ging

thei

r en

viro

nmen

ts

with

in th

e op

timum

tem

pera

ture

ra

nge

of B

. den

drob

atid

is th

is

is u

nlik

ely

in th

e lo

wla

nd a

nd

low

er-m

onta

ne f

rog

M. o

lmon

ae.

Con

td...

306 / Ochoa-Ochoa et al.

App

endi

x 3

Con

td...

Art

icle

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

ch

ytri

diom

ycos

is

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

clim

ate

chan

ge

Exa

mpl

e of

cl

imat

e ch

ange

pr

omot

ing

chyt

ridi

omyc

osis

No

caus

e m

entio

ned

Exa

mpl

e of

A

PD b

ut n

o re

late

d ca

use

Exa

mpl

e of

ch

alle

ngin

g th

e C

TOH

Quo

tes

Alfo

rd, R

.A.,

K.S

. Bra

dfi e

ld, a

nd

S.J.

Ric

hard

s. 20

07. E

colo

gy: g

loba

l w

arm

ing

and

amph

ibia

n lo

sses

. N

atur

e 44

7(71

44):

E3–E

4

Yes

We

ques

tion

the

anal

ysis

of

Poun

ds e

t al.,

whi

ch s

o fa

r pr

ovid

es th

e on

ly g

eogr

aphi

cally

br

oad

test

of

this

idea

. Con

trary

to

thei

r w

orki

ng m

odel

1,

our

Figu

res

1, 2

indi

cate

that

m

ultiy

ear

war

m p

erio

ds m

ay b

e m

ore

impo

rtant

in a

mph

ibia

n de

clin

es th

an s

ingl

e w

arm

ye

ars.

By

focu

sing

on

the

latte

r, th

e au

thor

s’ te

st c

ould

be

inco

nclu

sive

.A

lford

, R.A

. and

S.J.

Rich

ards

. 19

97. L

ack

of e

vide

nce

for e

pide

mic

di

seas

e as

an

agen

t in

the

catas

troph

ic

decli

ne o

f Aus

tralia

n ra

in fo

rest

frogs

. Co

nser

vatio

n Bi

olog

y 11

(4):

1026

–102

9A

lterm

att, F

. and

D. E

bert.

200

8. G

eneti

c di

versi

ty o

f Dap

hnia

mag

na p

opul

ation

s en

hanc

es re

sistan

ce to

par

asite

s. Ec

olog

y Le

tters

11(

9): 9

18–9

28

Yes

Para

sites

are

of

gene

ral i

mpo

rtanc

e in

all

natu

ral s

yste

ms,

and

epid

emic

s ca

n le

ad to

pop

ulat

ion

extin

ctio

ns (

Poun

ds e

t al.

2006

).*A

lton,

L.A

., R

.S. W

ilson

, and

C.E

. Fr

ankl

in. 2

010.

Ris

k of

pre

datio

n en

hanc

es th

e le

thal

effe

cts

of U

V-B

in

am

phib

ians

. Glo

bal C

hang

e Bi

olog

y 16

(2):

538–

545

Yes

It ha

s be

en s

ugge

sted

that

sub

tle

envi

ronm

enta

l cha

nges

occ

urrin

g at

a g

loba

l sca

le (

e.g.

glo

bal

clim

ate

chan

ge a

nd in

crea

sing

U

V-B

rad

iatio

n) m

ay b

e in

tera

ctin

g w

ith s

tress

ors

actin

g at

loca

l and

reg

iona

l sc

ales

(e.

g. a

cidifi c

atio

n,

cont

amin

ants

and

dis

ease

) to

ne

gativ

ely

impa

ct a

mph

ibia

n po

pula

tions

(Po

unds

et a

l. 20

06).

Anc

huka

itis,

K.J.

and

M.N

. Eva

ns.

2010

. Tro

pica

l clo

ud f

ores

t clim

ate

varia

bilit

y an

d th

e de

mis

e of

the

Mon

teve

rde

gold

en to

ad. P

roce

edin

gs

of th

e N

atio

nal A

cade

my

of S

cien

ces

of th

e U

nite

d St

ates

of A

mer

ica

107(

11):

5036

–504

0

Yes

Rat

her,

the

extin

ctio

n of

the

Mon

teve

rde

gold

en to

ad (

Bufo

pe

rigl

enes

) ap

pear

s to

hav

e co

inci

ded

with

an

exce

ptio

nally

dr

y in

terv

al c

ause

d by

the

1986

–198

7 El

Niñ

o ev

ent.

Berg

, M.P.

, E. T

oby

Kie

rs, G

. Drie

ssen

, M

. van

der

Hei

jden

, B.W

. Koo

i, F.

K

uene

n, M

. Lie

fting

, et a

l. A

dapt

or

disp

erse

: und

ersta

ndin

g sp

ecie

s pe

rsist

ence

in a

cha

ngin

g w

orld

. Glo

bal

Chan

ge B

iolo

gy 1

6(2)

: 587

– 59

8

Yes

Yes

Rece

nt s

tudi

es in

dica

te th

at

robu

stnes

s of

spe

cies

inte

ract

ions

un

der

clim

ate

chan

ge is

det

erm

ined

by

var

iatio

n in

the

tem

pera

ture

se

nsiti

vity

of

thei

r co

mm

unity

co

mpo

nent

s (P

ound

s et

al.

2006

).C

ontd

...

Golden toad as a climate change icon species / 307

App

endi

x 3

Con

td...

Art

icle

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

ch

ytri

diom

ycos

is

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

clim

ate

chan

ge

Exa

mpl

e of

cl

imat

e ch

ange

pr

omot

ing

chyt

ridi

omyc

osis

No

caus

e m

entio

ned

Exa

mpl

e of

A

PD b

ut n

o re

late

d ca

use

Exa

mpl

e of

ch

alle

ngin

g th

e C

TOH

Quo

tes

Bic

kfor

d, D

., S.

D. H

owar

d, D

.J.J.

Ng,

and

J.A

. She

ridan

. 201

0. I

mpa

cts

of c

limat

e ch

ange

on

the

amph

ibia

ns

and

rept

iles

of S

outh

east

Asi

a.

Biod

iver

sity

and

Con

serv

atio

n 19

(4):

1043

–106

2

Yes

Add

ition

ally

, inc

reas

ed

met

abol

ic r

ates

ofte

n dr

aw o

n en

ergy

nor

mal

ly a

lloca

ted

for

mai

nten

ance

(Fi

tzpa

trick

197

6;

Scot

t and

For

e 19

95),

resu

lting

in

incr

ease

d su

scep

tibili

ty to

di

seas

e (P

ound

s et

al.

2006

).B

laus

tein

, A.R

. and

A. D

obso

n. 2

006.

Ex

tinct

ions

: a m

essa

ge f

rom

the

frog

s. N

atur

e 43

9(70

73):

143–

144

Yes

Poun

ds a

nd c

olle

ague

s pr

ovid

e co

mpe

lling

evi

denc

e th

at a

nthr

opog

enic

clim

ate

chan

ge h

as a

lread

y al

tere

d tra

nsm

issi

on o

f a

path

ogen

tha

t af

fect

s am

phib

ians

, lea

ding

to

wid

espr

ead

popu

latio

n de

clin

es

and

extin

ctio

ns.

Bla

uste

in, A

.R. a

nd P

.T.J.

Joh

nson

. 20

10. C

onse

rvat

ion

biol

ogy:

whe

n an

infe

ctio

n tu

rns

leth

al. N

atur

e 46

5:

881–

882

Yes

Inte

nsity

thre

shol

d of

B.

dend

roba

tidis

var

ies

acro

ss

spec

ies

or w

ith e

nviro

nmen

tal

cond

ition

s, an

d w

hat p

art

is p

laye

d by

env

ironm

enta

l co

fact

ors

such

as

clim

ate

chan

ge.

Bot

kin,

D.B

., H

. Sax

e, M

.B. A

raúj

o,

R. B

etts

, R.H

.W. B

rads

haw

, T.

Ced

hage

n, P

. Che

sson

, et a

l. 20

07.

Fore

cast

ing

the

effe

cts

of g

loba

l w

arm

ing

on b

iodi

vers

ity. B

ioSc

ienc

e 57

(3):

227–

236

Yes

(clim

atic

va

riabi

lity)

… a

mph

ibia

n de

clin

es d

ue

to o

utbr

eaks

of

a pa

thog

enic

ch

ytrid

fun

gus

(Bat

rach

ochy

triu

m

dend

roba

tidis

) ar

e re

late

d to

the

annu

al r

ange

of

tem

pera

ture

s, no

t to

the

mea

n te

mpe

ratu

re.

Brig

gs, C

.J., R

.A. K

napp

, and

V.T

. V

rede

nbur

g. 2

010.

Enz

ootic

and

ep

izoo

tic d

ynam

ics

of th

e ch

ytrid

fu

ngal

pat

hoge

n of

am

phib

ians

. Pr

ocee

ding

s of

the

Nat

iona

l Aca

dem

y of

Sci

ence

s of

the

Uni

ted

Stat

es o

f Am

eric

a 10

7(21

): 96

95–9

700

Yes

This

mod

el c

an e

asily

inco

rpor

ate

the

effe

cts

of te

mpe

ratu

re

or o

ther

env

ironm

enta

l co

nditi

ons

(suc

h as

wat

er fl

ow

rate

) on

Bd

grow

th.*

Bro

ok, B

.W.,

N.S

. Sod

hi, a

nd C

.J.A

. B

rads

haw

. 200

8. S

yner

gies

am

ong

extin

ctio

n dr

iver

s un

der

glob

al

chan

ge. T

rend

s in

Eco

logy

and

Ev

olut

ion

23(8

): 45

3–46

0

Yes

An

exce

llent

rea

l-wor

ld e

xam

ple

com

es f

rom

the

high

land

for

ests

of

Cos

ta R

ica,

whe

re 4

0%

of 5

0 en

dem

ic f

rog

and

toad

sp

ecie

s di

sapp

eare

d fo

llow

ing

sync

hron

ous

popu

latio

n cr

ashe

s du

ring

the

late

198

0s. R

ecen

t w

ork

has

linke

d th

ese

extin

ctio

ns

to a

n in

tera

ctio

n be

twee

n gl

obal

w

arm

ing

and

dise

ase.

Con

td...

308 / Ochoa-Ochoa et al.

App

endi

x 3

Con

td...

Art

icle

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

ch

ytri

diom

ycos

is

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

clim

ate

chan

ge

Exa

mpl

e of

cl

imat

e ch

ange

pr

omot

ing

chyt

ridi

omyc

osis

No

caus

e m

entio

ned

Exa

mpl

e of

A

PD b

ut n

o re

late

d ca

use

Exa

mpl

e of

ch

alle

ngin

g th

e C

TOH

Quo

tes

Broo

ks, D

.R. a

nd E

.P. H

ober

g. 2

007.

H

ow w

ill g

loba

l clim

ate

chan

ge a

ffect

pa

rasit

e-ho

st as

sem

blag

es?

Tren

ds in

Pa

rasit

olog

y 23

(12)

: 571

–574

Yes

Acc

eler

ated

per

turb

atio

n in

glo

bal

ecos

yste

ms

can

initi

ate

even

ts

that

link

clim

ate

chan

ge, l

oss

of b

iodi

vers

ity a

nd e

mer

ging

in

fect

ious

dis

ease

s.Br

ooks

, T.M

., S.

J. W

right

, and

D

. She

il. 2

009.

Eva

luat

ing

the

succ

ess

of c

onse

rvat

ion

actio

ns in

sa

fegu

ardi

ng tr

opic

al f

ores

t bio

dive

rsity

. Co

nser

vatio

n Bi

olog

y 23

(6):

1448

–145

7

Yes

Littl

e is

kno

wn

abou

t oth

er

driv

ers

of b

iodi

vers

ity lo

ss w

ithin

PA

s. Ex

ampl

es in

clud

e di

seas

e,

whi

ch c

ause

d th

e ex

tinct

ion

of th

e go

lden

toad

(In

ciliu

s pe

rigl

enes

) in

Cos

ta R

ica’

s R

eser

va B

ioló

gica

Mon

teve

rde.

Bru

ijnze

el, L

.A.,

M. M

ullig

an,

and

F.N

. Sca

tena

. 201

1.

Hyd

rom

eteo

rolo

gy o

f tro

pica

l m

onta

ne c

loud

for

ests

: em

ergi

ng

patte

rns.

Hyd

rolo

gica

l Pro

cess

es

25(3

): 46

5–49

8

Yes

In r

ecen

t yea

rs, c

limat

ic w

arm

ing

and

dryi

ng r

elat

ed to

glo

bal o

r re

gion

al c

limat

e ch

ange

hav

e be

com

e an

incr

easin

gly

impo

rtant

fa

ctor

that

can

pot

entia

lly

thre

aten

trop

ical

mon

tane

clo

ud

fore

st (T

MCF

) hy

drol

ogic

al

func

tioni

ng, i

n ad

ditio

n to

hav

ing

a de

vasta

ting

effe

ct o

n pa

rticu

larly

vu

lner

able

pla

nt a

nd a

nim

al g

roup

s lik

e m

osse

s an

d am

phib

ians

.Br

uno,

J.F

., E.

R. S

elig

, K.S

. Cas

ey,

C.A

. Pag

e, B

.L. W

illis,

C.D

. Har

vell,

H

. Sw

eatm

an, e

t al.

2007

. The

rmal

str

ess

and

cora

l cov

er a

s dr

iver

s of

cor

al d

iseas

e ou

tbre

aks.

Publ

ic

Libr

ary

of S

cien

ce B

iolo

gy 5

(6):

1220

–122

7

Yes

Tem

pera

ture

and

clim

ate

chan

ge

have

also

bee

n im

plic

ated

in p

lant

an

d an

imal

dise

ase

outb

reak

s in

bot

h te

rrestr

ial a

nd a

quat

ic

habi

tats.

Buc

kley

, L.B

. and

W. J

etz.

200

7.

Envi

ronm

enta

l and

his

toric

al

cons

train

ts o

n gl

obal

pat

tern

s of

am

phib

ian

richn

ess.

Proc

eedi

ngs

of th

e Ro

yal S

ocie

ty B

: Bi

olog

ical

Sc

ienc

es 2

74(1

614)

: 116

7–11

73

Yes

Am

phib

ians

hav

e re

peat

edly

bee

n us

ed a

s an

indi

cato

r gr

oup

for

envi

ronm

enta

l cha

nge.

*

Bus

h, M

.B. a

nd T

.E. L

ovej

oy. 2

007.

A

maz

onia

n co

nser

vatio

n: p

ushi

ng th

e lim

its o

f bi

ogeo

grap

hica

l kno

wle

dge.

Jo

urna

l of B

ioge

ogra

phy

34(8

): 12

91–1

293

Yes

The

syne

rgism

indu

ced

in

Am

azon

ia th

roug

h sim

plify

ing

ecol

ogic

al s

truct

ure

from

the

com

plex

ity o

f fo

rest

to th

e sim

plic

ity o

f so

ybea

n fi e

lds

or r

anch

land

, the

incr

ease

d pr

obab

ility

of

hum

an-s

et fi

res,

and

com

plex

eco

logi

cal i

nter

actio

ns.

Golden toad as a climate change icon species / 309

App

endi

x 3

Con

td...

Art

icle

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

ch

ytri

diom

ycos

is

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

clim

ate

chan

ge

Exa

mpl

e of

cl

imat

e ch

ange

pr

omot

ing

chyt

ridi

omyc

osis

No

caus

e m

entio

ned

Exa

mpl

e of

A

PD b

ut n

o re

late

d ca

use

Exa

mpl

e of

ch

alle

ngin

g th

e C

TOH

Quo

tes

med

iate

d by

clim

ate,

e.g

., ba

cter

ial

dise

ases

(Po

unds

et a

l. 20

06).

Busta

man

te, H

.M.,

L.J.

Livo

, and

C.

Care

y. 2

010.

Effe

cts

of te

mpe

ratu

re

and

hydr

ic e

nviro

nmen

t on

surv

ival

of

the

Pana

man

ian

gold

en f

rog

infe

cted

w

ith a

pat

hoge

nic

chyt

rid f

ungu

s. In

tegr

ativ

e Zo

olog

y 5(

2): 1

43–1

53

Yes

Poun

ds e

t al.

(200

6) p

ropo

se

a “c

limat

e-lin

ked

epid

emic

hy

poth

esis

,” o

r, m

ore

spec

ifi ca

lly,

a “c

hytri

d-th

erm

al-o

ptim

um

hypo

thes

is.”

But

ler,

G. 2

010.

Fun

gal s

ex a

nd

path

ogen

esis

. Clin

ical

Mic

robi

olog

y Re

view

s 23

(1):

140–

159

Yes

Oth

ers

caus

e di

seas

e in

ani

mal

s, su

ch a

s th

e ch

ytrid

spe

cies

Ba

trac

hoch

ytri

um d

endr

obat

idis

, w

hich

is d

evas

tatin

g th

e gl

obal

am

phib

ian

popu

latio

n.C

alos

i, P.

, D.T

. Bilt

on, a

nd J

.I.

Spic

er. 2

008.

The

rmal

tole

ranc

e,

accl

imat

ory

capa

city

and

vul

nera

bilit

y to

glo

bal c

limat

e ch

ange

. Bio

logy

Le

tters

4(1

): 99

–102

Yes

Dur

ing

perio

ds o

f ra

pid

clim

ate

chan

ge, t

axa

that

are

una

ble

to

shift

thei

r ge

ogra

phic

al r

ange

s ar

e pa

rticu

larly

at r

isk

from

ex

tinct

ion

(Pou

nds

et a

l. 20

06).

Can

nate

lla, D

.C. 2

008.

Com

men

t on

“H

abita

t spl

it an

d th

e gl

obal

de

clin

e of

am

phib

ians

”. S

cien

ce 3

20:

874d

–874

d

Yes

Am

phib

ians

are

impo

rtant

in

dica

tors

of

envi

ronm

enta

l de

grad

atio

n an

d cl

imat

e ch

ange

.

Car

nava

l, A

.C. a

nd J

.M. B

ates

. 20

07. A

mph

ibia

n D

NA

sho

ws

mar

ked

gene

tic s

truct

ure

and

track

s Pl

eist

ocen

e cl

imat

e ch

ange

in

north

east

ern

Bra

zil.

Evol

utio

n 61

(12)

: 29

42–2

957

Yes

(clim

atic

an

omal

ies)

Our

dat

a sh

ow B

. den

drob

atid

is to

be

pres

ent i

n Br

azil

in

the

early

198

0s. W

hen

tied

to H

eyer

et a

l.’s

(198

8) a

nd

Wey

gold

t’s (

1989

) ob

serv

atio

ns o

n lo

cal c

limat

e an

omal

ies,

our

resu

lts

are

cons

isten

t with

a h

ypot

hesis

of

a c

limat

e-lin

ked

epid

emic

ev

ent l

eadi

ng to

am

phib

ian

decl

ines

(Po

unds

et a

l. 20

06).

Car

valh

o, S

.B.,

J.C. B

rito,

E.J.

C

resp

o, a

nd H

.P. P

ossi

ngha

m. 2

010.

Fr

om c

limat

e ch

ange

pre

dict

ions

to

actio

ns: c

onse

rvin

g vu

lner

able

ani

mal

gr

oups

in h

otsp

ots

at a

reg

iona

l sc

ale.

Glo

bal C

hang

e Bi

olog

y 16

(12)

: 32

57–3

270

Yes

Clim

ate

war

min

g is

pro

ject

ed

to in

duce

the

spre

ad o

f ch

ytrid

iom

ycet

e fu

ngus

.

Cas

adev

all,

A. a

nd L

.A. P

irofs

ki.

2007

. Acc

iden

tal v

irule

nce,

cry

ptic

pa

thog

enes

is, m

artia

ns, l

ost h

osts

and

th

e pa

thog

enic

ity o

f en

viro

nmen

tal

mic

robe

s. Eu

kary

otic

Cel

l 6(1

2):

2169

–217

4

Yes?

The

ongo

ing

deci

mat

ion

of

amph

ibia

n po

pula

tions

by

a ch

ytrid

fu

ngus

may

refl

ect

a s

imila

r ph

enom

enon

, whe

reby

eco

logi

cal

chan

ges

mig

ht s

elec

t for

var

iant

s w

ith e

nhan

ced

viru

lenc

e.C

ontd

...

310 / Ochoa-Ochoa et al.

App

endi

x 3

Con

td...

Art

icle

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

ch

ytri

diom

ycos

is

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

clim

ate

chan

ge

Exa

mpl

e of

cl

imat

e ch

ange

pr

omot

ing

chyt

ridi

omyc

osis

No

caus

e m

entio

ned

Exa

mpl

e of

A

PD b

ut n

o re

late

d ca

use

Exa

mpl

e of

ch

alle

ngin

g th

e C

TOH

Quo

tes

Cho

wn,

S.L

., K

.J. G

asto

n, M

. van

K

leun

en, a

nd S

. Clu

sella

-Tru

llas.

2010

. Pop

ulat

ion

resp

onse

s w

ithin

a la

ndsc

ape

mat

rix: a

m

acro

phys

iolo

gica

l app

roac

h to

un

ders

tand

ing

clim

ate

chan

ge

impa

cts.

Evol

utio

nary

Eco

logy

24(

3):

601–

616

Yes

Alth

ough

the

ultim

ate

caus

es o

f am

phib

ian

decl

ines

in tr

opic

al

Cen

tral A

mer

ica

rem

ain

the

subj

ect o

f de

bate

(e.

g. P

ound

s et

al.

1999

, 200

6; R

ohr

et a

l. 20

08),

chan

ges

in w

ater

av

aila

bilit

y ow

ing

to g

loba

l te

mpe

ratu

re c

hang

e an

d lo

cal h

abita

t des

truct

ion

are

impo

rtant

(R

ovito

et a

l. 20

09).

Cho

wn,

S.L

. and

J.S

. Ter

blan

che.

20

06. P

hysi

olog

ical

div

ersi

ty in

in

sect

s: e

colo

gica

l and

evo

lutio

nary

co

ntex

ts. A

dvan

ces

in I

nsec

t Ph

ysio

logy

33:

50–

152

Yes

In m

any

case

s, cl

imat

e ch

ange

ef

fect

s ar

e ne

gativ

e an

d ha

ve

eith

er r

esul

ted

in o

r ar

e pr

edic

ted

to g

ive

rise

to s

peci

es e

xtin

ctio

ns.

Cis

nero

s-H

ered

ia, D

.F.,

J. D

elia

, M

.H. Y

áñez

-Muñ

óz, a

nd H

.M.

Orte

ga-A

ndra

de. 2

010.

End

emic

Ec

uado

rian

glas

sfro

g C

ochr

anel

la

mac

he is

crit

ical

ly e

ndan

gere

d be

caus

e of

hab

itat l

oss.

Ory

x 44

(1):

114–

117

Yes

Dis

ease

s an

d gl

obal

war

min

g ha

ve b

een

linke

d to

som

e of

th

ese

decl

ines

but

the

caus

es o

f m

ost r

emai

n po

orly

und

erst

ood.

Cla

rk, D

.A. 2

007.

Det

ectin

g tro

pica

l fo

rest

s’ re

spon

ses

to g

loba

l clim

atic

an

d at

mos

pher

ic c

hang

e: c

urre

nt

chal

leng

es a

nd a

way

for

war

d.

Biot

ropi

ca 3

9(1)

: 4–1

9

Yes

As

rece

ntly

illu

stra

ted

by a

n an

alys

is o

f fr

og e

xtin

ctio

ns

in C

osta

Ric

a (P

ound

s et

al.

2006

), el

evat

iona

l tra

nsec

ts o

f co

ntin

uous

trop

ical

for

est o

ffer

an im

porta

nt o

ppor

tuni

ty f

or

dete

ctin

g th

e ef

fect

s of

clim

ate

chan

ge o

n tro

pica

l for

est p

lant

s.C

olom

a, L

.A.,

S. L

ötte

rs, W

.E.

Due

llman

, and

A. M

irand

a-Le

iva.

20

07. A

taxo

nom

ic r

evis

ion

of A

telo

pus

pach

yder

mus

and

de

scrip

tion

of tw

o ne

w (

extin

ct?)

sp

ecie

s of

Ate

lopu

s fr

om

Ecua

dor

(Anu

ra: B

ufon

idae

). Zo

otax

a 15

57: 1

–32

Yes

Yes

Ecua

doria

n am

phib

ian

spec

ies

are

unde

r ca

tego

ries

of e

xtin

ctio

n ris

k, w

e em

phas

ize

on th

e ch

alle

nge

of a

rap

id r

espo

nse

and

fund

amen

tal c

hang

es in

pol

icie

s an

d ac

tions

that

are

req

uire

d in

or

der

to a

ddre

ss th

e am

phib

ian

cris

is...

giv

en th

e no

vel t

hrea

ts

mos

tly im

pose

d by

glo

bal

war

min

g an

d pa

thog

ens.

Con

trera

s, V.

, E. M

artín

ez-M

eyer

, E.

Val

ient

e, a

nd L

. Zam

bran

o.

2009

. Rec

ent d

eclin

e an

d po

tent

ial

dist

ribut

ion

in th

e la

st r

emna

nt a

rea

of th

e m

icro

ende

mic

Mex

ican

Yes

Clim

ate

chan

ge h

as a

lso

been

id

entifi

ed

as a

n im

porta

nt in

dire

ct

thre

at f

or a

mph

ibia

n po

pula

tions

in

rec

ent d

ecad

es.

Golden toad as a climate change icon species / 311

App

endi

x 3

Con

td...

Art

icle

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

ch

ytri

diom

ycos

is

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

clim

ate

chan

ge

Exa

mpl

e of

cl

imat

e ch

ange

pr

omot

ing

chyt

ridi

omyc

osis

No

caus

e m

entio

ned

Exa

mpl

e of

A

PD b

ut n

o re

late

d ca

use

Exa

mpl

e of

ch

alle

ngin

g th

e C

TOH

Quo

tes

axol

otl (

Amby

stom

a m

exic

anum

). Bi

olog

ical

Con

serv

atio

n 14

2(12

): 28

81–2

885

Coo

per,

N.,

J. B

ielb

y, G

.H. T

hom

as,

and

A. P

urvi

s. 20

08. M

acro

ecol

ogy

and

extin

ctio

n ris

k co

rrel

ates

of

fro

gs. G

loba

l Eco

logy

and

Bi

ogeo

grap

hy 1

7(2)

: 211

–221

Yes

(cha

nges

in

the

envi

ronm

ent)

Thes

e en

viro

nmen

tal v

aria

bles

m

ay a

lso

be li

nked

dire

ctly

to

ext

inct

ion

risk

in f

rogs

si

nce

thes

e ta

xa a

re v

ery

sens

itive

to c

hang

es in

the

envi

ronm

ent (

Poun

ds e

t al.

2006

) th

at c

an a

lso

incr

ease

thei

r su

scep

tibili

ty to

oth

er th

reat

s, fo

r ex

ampl

e th

e ch

ytrid

fun

gus.

Cor

ey, S

.J. a

nd T

.A. W

aite

. 200

8.

Phyl

ogen

etic

aut

ocor

rela

tion

of e

xtin

ctio

n th

reat

in g

loba

lly

impe

rille

d am

phib

ians

. Div

ersi

ty a

nd

Dis

trib

utio

ns 1

4(4)

: 614

–629

Yes

Cra

usba

y, S

.D. a

nd S

.C. H

otch

kiss

. 20

10. S

trong

rel

atio

nshi

ps b

etw

een

vege

tatio

n an

d tw

o pe

rpen

dicu

lar

clim

ate

grad

ient

s hi

gh o

n a

tropi

cal

mou

ntai

n in

Haw

ai’i.

Jou

rnal

of

Biog

eogr

aphy

37(

6): 1

160–

1174

Yes

Som

e of

the

few

stu

dies

that

do

sho

w e

vide

nce

of tr

opic

al

biol

ogic

al r

espo

nse

also

de

mon

strat

e th

at r

espo

nse

to

clim

ate

chan

ge c

an b

e co

mpl

icat

ed

by p

ower

ful s

econ

dary

effe

cts,

incl

udin

g fi r

e, d

iseas

e an

d in

vasiv

e sp

ecie

s (H

emp

2005

; Pou

nds

et a

l. 20

06).

Cru

tzen

, P.J.

200

6. A

lbed

o en

hanc

emen

t by

stra

tosp

heric

sul

fur

inje

ctio

ns: a

con

tribu

tion

to r

esol

ve

a po

licy

dile

mm

a? C

limat

ic C

hang

e 77

(3):

211–

219

Yes

Alre

ady

maj

or s

peci

es e

xtin

ctio

ns

by c

urre

nt c

limat

e w

arm

ing

have

be

en r

epor

ted

by P

ound

s et

al.

Dal

glei

sh, H

.J., D

.N. K

oons

, and

P.B

. A

dler

. 201

0. C

an li

fe-h

istor

y tra

its

pred

ict t

he r

espo

nse

of f

orb

popu

latio

ns

to c

hang

es in

clim

ate

varia

bilit

y?

Jour

nal o

f Eco

logy

98(

1): 2

09–2

17

Yes

Dal

y, G

.L.,

Y.D

. Lei

, C. T

eixe

ira,

D.C

.G. M

uir,

L.E.

Cas

tillo

, and

F.

Wan

ia. 2

007.

Acc

umul

atio

n of

cu

rrent

-use

pes

ticid

es in

neo

tropi

cal

mon

tane

for

ests.

Env

ironm

enta

l Sci

ence

an

d Te

chno

logy

41(

4): 1

118–

1123

Yes

Even

thou

gh p

atho

gens

in

com

bina

tion

with

glo

bal w

arm

ing

have

rec

ently

bee

n im

plic

ated

in

the

decl

ine

of a

mph

ibia

n po

pula

tions

in th

e N

eotro

pics

, th

is d

oes

not e

xclu

de a

pot

entia

l ro

le o

f co

ntam

inan

ts in

this

di

stur

bing

phe

nom

enon

.C

ontd

...

312 / Ochoa-Ochoa et al.

App

endi

x 3

Con

td...

Art

icle

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

ch

ytri

diom

ycos

is

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

clim

ate

chan

ge

Exa

mpl

e of

cl

imat

e ch

ange

pr

omot

ing

chyt

ridi

omyc

osis

No

caus

e m

entio

ned

Exa

mpl

e of

A

PD b

ut n

o re

late

d ca

use

Exa

mpl

e of

ch

alle

ngin

g th

e C

TOH

Quo

tes

Dei

chm

ann,

J.L

., G

.B. W

illia

mso

n,

A.P

. Lim

a, a

nd W

.D. A

llmon

. 201

0.

A n

ote

on a

mph

ibia

n de

clin

e in

a

cent

ral A

maz

onia

n lo

wla

nd f

ores

t. Bi

odiv

ersi

ty a

nd C

onse

rvat

ion

19(1

2): 3

619–

3627

Yes

Enig

mat

ic d

eclin

e ha

s be

en

attri

bute

d to

a n

umbe

r of

pr

oxim

al c

ause

s in

clud

ing

clim

ate

chan

ge.

Eugs

ter,

W.,

R. B

urka

rd, F

. Hol

wer

da,

F.N

. Sca

tena

, and

L.A

. Bru

ijnze

el.

2006

. Cha

ract

eris

tics

of f

og a

nd

fogw

ater

fl ux

es in

a P

uerto

Ric

an

elfi n

clo

ud f

ores

t. Ag

ricul

tura

l and

Fo

rest

Met

eoro

logy

139

(3):

288–

306

Envi

ronm

enta

l co

nditi

ons

Clo

ud f

ores

ts h

ave

been

rep

orte

d to

be

very

sus

cept

ible

to c

hang

es

in e

nviro

nmen

tal c

ondi

tions

.

Fouq

uet,

A.,

G.F

. Fic

etol

a, A

. Hai

gh,

and

N. G

emm

ell.

2010

. Usi

ng

ecol

ogic

al n

iche

mod

ellin

g to

infe

r pa

st, p

rese

nt a

nd f

utur

e en

viro

nmen

tal

suita

bilit

y fo

r Le

iope

lma

hoch

stette

ri,

an e

ndan

gere

d N

ew Z

eala

nd n

ativ

e fro

g. B

iolo

gica

l Con

serv

atio

n 14

3(6)

: 13

75–1

384

Yes

This

has

bee

n th

e ca

se

for

New

Zea

land

nat

ive

frog

s (L

eiop

elm

a) w

ith

serio

us d

eclin

es d

ue to

a

clim

ate

driv

en e

pide

mic

of

chyt

ridio

myc

osis

(B

ell e

t al.

2004

a; P

ound

s et

al.

2006

).

Fran

co, A

.M.A

., J.K

. Hill

, C.

Kits

chke

, Y.C

. Col

lingh

am, D

.B.

Roy

, R. F

ox, B

. Hun

tley,

et a

l. 20

06.

Impa

cts

of c

limat

e w

arm

ing

and

habi

tat l

oss

on e

xtin

ctio

ns a

t spe

cies

’ lo

w-la

titud

e ra

nge

boun

darie

s. G

loba

l C

hang

e Bi

olog

y 12

(8):

1545

–155

3

Yes

Extin

ctio

ns w

ill o

ften

be d

riven

by

clim

ate

chan

ge a

nd o

ther

th

reat

s ac

ting

in c

once

rt sp

ecie

s.

Gac

hon,

C.M

.M.,

T. S

ime-

Nga

ndo,

M

. Stri

ttmat

ter,

A. C

ham

bouv

et, a

nd

G.H

. Kim

. 201

0. A

lgal

dis

ease

s:

spot

light

on

a bl

ack

box.

Tre

nds

in

Plan

t Sci

ence

15(

11):

633–

640

Yes

Clim

ate

chan

ge a

lread

y af

fect

s di

seas

e pa

ttern

s w

orld

wid

e, a

nd

is in

crim

inat

ed in

mas

sive

sud

den

extin

ctio

ns (

e.g.

‘fr

og k

iller

fu

ngus

’).

Gar

ner,

T.W

.J., J

.M. R

owcl

iffe,

and

M

.C. F

ishe

r. 20

11. C

limat

e ch

ange

, ch

ytrid

iom

ycos

is o

r co

nditi

on: a

n ex

perim

enta

l tes

t of

amph

ibia

n su

rviv

al. G

loba

l Cha

nge

Biol

ogy

17(2

): 66

7–67

5

Yes

The

amph

ibia

n ho

st/

Batr

acho

chyt

rium

de

ndro

batid

is (

Bd)

par

asite

sy

stem

is c

onsi

dere

d by

man

y to

be

stro

ngly

influ

ence

d by

ch

ange

s in

env

ironm

enta

l te

mpe

ratu

re (

Poun

ds e

t al.

2006

; B

osch

et a

l. 20

07; M

uths

et a

l. 20

08, b

ut s

ee L

ips

et a

l. 20

08):

evid

ence

for

this

is e

quiv

ocal

.G

ilman

, S.E

., M

.C. U

rban

, J.

Tew

ksbu

ry, G

.W. G

ilchr

ist,

and

R.D

. H

olt.

2010

. A f

ram

ewor

k fo

r

Yes

Empi

rical

evi

denc

e su

gges

ts

that

clim

ate-

driv

en c

hang

es in

in

tera

ctin

g sp

ecie

s, in

clud

ing. C

ontd

...

Golden toad as a climate change icon species / 313

App

endi

x 3

Con

td...

Art

icle

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

ch

ytri

diom

ycos

is

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

clim

ate

chan

ge

Exa

mpl

e of

cl

imat

e ch

ange

pr

omot

ing

chyt

ridi

omyc

osis

No

caus

e m

entio

ned

Exa

mpl

e of

A

PD b

ut n

o re

late

d ca

use

Exa

mpl

e of

ch

alle

ngin

g th

e C

TOH

Quo

tes

com

mun

ity in

tera

ctio

ns u

nder

clim

ate

chan

ge. T

rend

s in

Eco

logy

and

Ev

olut

ion

25(6

): 32

5–33

1

path

ogen

pre

vale

nce,

phe

nolo

gies

or

beh

avio

rs o

f co

mpe

titor

s or

m

utua

lists

, pre

dato

r or

com

petit

or

effi c

ienc

y, a

nd c

hang

es in

the

body

siz

e of

pre

y ca

n dr

ive

loca

l ex

tinct

ions

, but

sur

pris

ingl

y fe

w

gene

ral p

atte

rns

have

em

erge

d.G

rass

o, R

.L.,

R.M

. Col

eman

, and

C.

Dav

idso

n. 2

010.

Pal

atab

ility

and

an

tipre

dato

r re

spon

se o

f Yos

emite

To

ads

(Ana

xyru

s ca

noru

s) to

non

nativ

e Br

ook

Trou

t (Sa

lvel

inus

font

inal

is)

in th

e Si

erra

Nev

ada

Mou

ntai

ns o

f Ca

lifor

nia.

Cop

eia

3: 4

57–4

62

Yes

Jigu

et, F

., R

. Jul

liard

, C.D

. Tho

mas

, O

. Deh

orte

r, S.

E. N

ewso

n, a

nd D

. C

ouve

t. 20

06. T

herm

al r

ange

pre

dict

s bi

rd p

opul

atio

n re

silie

nce

to e

xtre

me

high

tem

pera

ture

s. Ec

olog

y Le

tters

9(

12):

1321

–133

0

Yes

Proj

ecte

d re

spon

ses

of s

peci

es

to c

limat

e ch

ange

pro

vide

stro

ng

evid

ence

that

ant

hrop

ogen

ic

clim

ate

chan

ge r

epre

sent

s a

serio

us th

reat

to b

iodi

vers

ity.

John

son,

P.T

.J. 2

006.

Am

phib

ian

dive

rsity

: dec

imat

ion

by d

isea

se.

Proc

eedi

ngs

of th

e N

atio

nal A

cade

my

of S

cien

ces

of th

e U

nite

d St

ates

of

Amer

ica

103(

9): 3

011–

3012

Yes

Rece

nt w

ork

by P

ound

s et

al.

(12)

, for

exa

mpl

e, su

gges

ts th

at te

mpe

ratu

re s

hifts

pro

mot

e Ba

trach

ochy

trium

infe

ctio

n at

ce

rtain

ele

vatio

ns a

nd m

ay th

eref

ore

have

indi

rect

ly d

riven

the

loss

of

num

erou

s ha

rlequ

in f

rog

spec

ies

in

Cent

ral a

nd S

outh

Am

eric

a.K

arvo

nen,

A.,

P. R

inta

mák

i, J.

Joke

la, a

nd E

.T. V

alto

nen.

201

0.

Incr

easi

ng w

ater

tem

pera

ture

an

d di

seas

e ris

ks in

aqu

atic

sy

stem

s: c

limat

e ch

ange

incr

ease

s th

e ris

k of

som

e, b

ut n

ot a

ll,

dise

ases

. Int

erna

tiona

l Jou

rnal

for

Para

sito

logy

40(

13):

1483

–148

8

Yes

The

risk

of p

aras

ite a

nd p

atho

gen

infe

ctio

ns m

ay a

lso

incr

ease

.

Kilp

atric

k, A

.M.,

C.J.

Brig

gs, a

nd P

. D

asza

k. 2

010.

The

eco

logy

and

impa

ct

of c

hytri

diom

ycos

is: a

n em

ergi

ng

dise

ase

of a

mph

ibia

ns. T

rend

s in

Ec

olog

y an

d Ev

olut

ion

25(2

): 10

9–11

8

Yes

Koc

h, P

.L. a

nd A

.D. B

arno

sky.

2006

. La

te Q

uate

rnar

y ex

tinct

ions

: sta

te o

f th

e de

bate

. Ann

ual R

evie

w of

Eco

logy

, Ev

olut

ion

and

Syste

mat

ics

37: 2

15–2

50

Yes

Glo

bal e

xtin

ctio

ns o

f so

me

smal

ler

anim

als

are

attri

bute

d to

cu

rren

t war

min

g.

Con

td...

314 / Ochoa-Ochoa et al.

App

endi

x 3

Con

td...

Art

icle

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

ch

ytri

diom

ycos

is

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

clim

ate

chan

ge

Exa

mpl

e of

cl

imat

e ch

ange

pr

omot

ing

chyt

ridi

omyc

osis

No

caus

e m

entio

ned

Exa

mpl

e of

A

PD b

ut n

o re

late

d ca

use

Exa

mpl

e of

ch

alle

ngin

g th

e C

TOH

Quo

tes

Laur

ance

, W.F

. 200

8. G

loba

l war

min

g an

d am

phib

ian

extin

ctio

ns in

eas

tern

A

ustra

lia. A

ustra

l Eco

logy

33(

1): 1

–9

Yes

Ris

ing

tem

pera

ture

s co

uld

also

al

ter

othe

r fe

atur

es o

f m

onta

ne

area

s, su

ch a

s... t

he d

iver

sity

and

vi

rule

nce

of p

atho

gens

.La

wle

r, J.J

., S.

L. S

hafe

r, an

d A

.R.

Bla

uste

in. 2

010.

Pro

ject

ed c

limat

e im

pact

s fo

r th

e am

phib

ians

of

the

wes

tern

hem

isph

ere.

Con

serv

atio

n Bi

olog

y 24

(1):

38–5

0

Yes

Love

joy,

T.E

. 200

6. P

rote

cted

are

as:

a pr

ism f

or a

cha

ngin

g w

orld

. Tre

nds

in E

colo

gy a

nd E

volu

tion

21(6

): 32

9–33

3

Yes

It is

a co

mpl

ex m

ulti-

fact

oria

l sit

uatio

n in

volv

ing

pollu

tant

s, ha

bita

t des

truct

ion,

clim

ate

chan

ge

and

an e

pide

mic

pat

hoge

n (a

ch

ytrid

fun

gus)

, with

incr

easin

g ev

iden

ce o

f sy

nerg

ism a

mon

g th

ese.

Loyo

la, R

.D.,

C.G

. Bec

ker,

U. K

ubot

a,

C.F.

B. H

adda

d, C

.R. F

onse

ca, a

nd

T.M

. Lew

inso

hn. 2

008.

Hun

g ou

t to

dry

: cho

ice

of p

riorit

y ec

oreg

ions

fo

r con

serv

ing

thre

aten

ed n

eotro

pica

l an

uran

s de

pend

s on

life

-hist

ory

traits

. Pu

blic

Lib

rary

of S

cien

ce O

NE

3(5)

: e21

20

Yes

Mai

nka,

S.A

. and

G.W

. How

ard.

20

10. C

limat

e ch

ange

and

inva

sive

sp

ecie

s: d

oubl

e je

opar

dy. I

nteg

rativ

e Zo

olog

y 5(

2): 1

02–1

11

Yes

Clim

ate

is c

hang

ing

natu

re

befo

re o

ur e

yes.

Spec

ies

extir

patio

ns (

loca

l ext

inct

ions

) an

d ex

tinct

ions

of

amph

ibia

ns h

ave

been

link

ed w

ith c

limat

e ch

ange

.M

cGin

nity,

P.,

E. J

enni

ngs,

E. D

eEyt

o,

N. A

llott,

P. S

amue

lsson

, G. R

ogan

, K

. Whe

lan, e

t al.

2009

. Im

pact

of

natu

rally

spa

wni

ng c

aptiv

e-br

ed A

tlant

ic

salm

on o

n w

ild p

opul

ation

s: de

pres

sed

recr

uitm

ent a

nd in

crea

sed

risk

of

clim

ate-m

ediat

ed e

xtin

ction

. Pro

ceed

ings

of

the

Roya

l Soc

iety

B: B

iolo

gica

l Sc

ience

s 27

6(16

73):

3601

–361

0

Yes

Mee

gask

umbu

ra, M

., K

. M

anam

endr

a-A

rach

chi,

C.J.

Schn

eide

r, an

d R.

Pet

hiya

goda

. 200

7. N

ew

spec

ies

amon

gst S

ri La

nka’

s ex

tinct

sh

rub

frogs

(A

mph

ibia

: Rha

coph

orid

ae:

Phila

utus

). Zo

otax

a 13

97: 1

–15

Yes

Clim

ate-

driv

en e

pide

mic

dis

ease

.

Con

td...

Golden toad as a climate change icon species / 315

App

endi

x 3

Con

td...

Art

icle

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

ch

ytri

diom

ycos

is

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

clim

ate

chan

ge

Exa

mpl

e of

cl

imat

e ch

ange

pr

omot

ing

chyt

ridi

omyc

osis

No

caus

e m

entio

ned

Exa

mpl

e of

A

PD b

ut n

o re

late

d ca

use

Exa

mpl

e of

ch

alle

ngin

g th

e C

TOH

Quo

tes

Men

dels

on, J

.R.,

K.R

. Lip

s, J.E

. D

iffen

dorf

er, R

.W. G

aglia

rdo,

G.B

. R

abb,

J.P

. Col

lins,

P. D

asza

k, e

t al.

2006

. Bio

dive

rsity

: con

fron

ting

amph

ibia

n de

clin

es a

nd e

xtin

ctio

ns.

Scie

nce

313(

5783

): 48

–48

Yes

Glo

bal c

limat

e ch

ange

may

be

enco

urag

ing

loca

l con

ditio

ns

idea

l for

Bd’

s pe

rsis

tenc

e an

d/or

spr

ead.

Mill

ero,

F.J.

200

7. T

he m

arin

e in

orga

nic

carb

on c

ycle

. Che

mic

al

Revi

ews

107(

2): 3

08–3

41

Yes

The

incr

ease

in th

e te

mpe

ratu

re

may

cau

se th

e ex

tinct

ion

of

anim

als.

Mur

ray,

K.A

., L.

F. Sk

erra

tt, R

. Spe

are,

an

d H

. McC

allum

. 200

9. Im

pact

an

d dy

nam

ics o

f dise

ase

in s

pecie

s th

reate

ned

by th

e am

phib

ian c

hytri

d fu

ngus

, Bat

rach

ochy

trium

den

drob

atid

is.

Cons

erva

tion

Biol

ogy

23(5

): 12

42–1

252

Yes

Ther

e is

no

evid

ence

that

clim

atic

an

omal

ies

caus

ed th

ese

decl

ines

, ei

ther

dire

ctly

or

as s

ugge

sted

by

curr

ent m

odel

s of

clim

ate-

linke

d di

seas

e ou

tbre

aks.

Oliv

ier,

A.,

C. B

arbr

aud,

E.

Ros

ecch

i, C

. Ger

mai

n, a

nd M

. C

heyl

an. 2

010.

Ass

essi

ng s

patia

l an

d te

mpo

ral p

opul

atio

n dy

nam

ics

of c

rypt

ic s

peci

es: a

n ex

ampl

e w

ith

the

Euro

pean

pon

d tu

rtle.

Eco

logi

cal

Appl

icat

ions

20(

4): 9

93–1

004

Yes

(but

clim

atic

an

omal

ies)

Clim

ate

anom

alie

s ha

ve b

een

prop

osed

as

trigg

ers

of d

ie-o

ffs

by p

rovi

ding

opp

ortu

nitie

s fo

r fa

tal c

hytri

d ou

tbre

aks.

Page

, R.A

. and

M.J.

Rya

n. 2

006.

So

cial

tran

smis

sion

of

nove

l for

agin

g be

havi

our

in b

ats:

fro

g ca

lls a

nd th

eir

refe

rent

s. C

urre

nt B

iolo

gy 1

6(12

): 12

01–1

205

Yes

The fl e

xibi

lity,

expl

orat

ory

beha

vior

, an

d so

cial

lear

ning

we

docu

men

t in

this

study

end

ow th

e ba

ts w

ith

the

pote

ntia

l to

resp

ond

rapi

dly

to

chan

ges

in p

rey

cond

ition

s. W

ith

the

cata

strop

hic

and

wor

ldw

ide

decl

ine

of a

mph

ibia

ns (

Poun

ds

et a

l. 20

06),

thei

r pr

edat

ors’

abili

ty

to tr

ack

such

cha

nges

bec

omes

in

crea

singl

y cr

itica

l.Pa

rmes

an, C

. 200

6. E

colo

gica

l and

ev

olut

iona

ry r

espo

nses

to r

ecen

t cl

imat

e ch

ange

. Ann

ual R

evie

w of

Ec

olog

y Ev

olut

ion

and

Syste

mat

ics

37:

637–

669

Yes

Poun

ds e

t al.

(200

6) h

ypot

hesi

sed

that

rec

ent t

rend

s to

war

d w

arm

er n

ight

s an

d in

crea

sed

dayt

ime

clou

d co

ver

have

sh

ifted

mid

-ele

vatio

n si

tes

(100

0-24

00 m

), w

here

the

prep

onde

ranc

e of

ext

inct

ions

hav

e oc

curr

ed, i

nto

ther

mal

ly o

ptim

um

cond

ition

s fo

r th

e ch

ytrid

fun

gus,

Batr

acho

chyt

rium

den

drob

atid

is.

Con

td...

316 / Ochoa-Ochoa et al.

App

endi

x 3

Con

td...

Art

icle

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

ch

ytri

diom

ycos

is

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

clim

ate

chan

ge

Exa

mpl

e of

cl

imat

e ch

ange

pr

omot

ing

chyt

ridi

omyc

osis

No

caus

e m

entio

ned

Exa

mpl

e of

A

PD b

ut n

o re

late

d ca

use

Exa

mpl

e of

ch

alle

ngin

g th

e C

TOH

Quo

tes

Paul

i, H

., M

. Got

tfrie

d, K

. Rei

ter,

C. K

lettn

er, a

nd G

. Gra

bher

r. 20

07.

Sign

als

of r

ange

exp

ansi

ons

and

cont

ract

ions

of

vasc

ular

pla

nts

in

the

high

Alp

s: o

bser

vatio

ns (

1994

-20

04)

at th

e G

LOR

IA*

mas

ter

site

Sc

hran

koge

l, Ty

rol,

Aus

tria.

Glo

bal

Cha

nge

Biol

ogy

13(1

): 14

7–15

6

Yes

Clim

ate

war

min

g-as

soci

ated

shi

fts

or e

xtirp

atio

ns a

t the

rea

r ed

ges

of s

peci

es h

ave

been

det

ecte

d.

Pede

rsen

, A.B

., K

.E. J

ones

, C.L

. N

unn,

and

S. A

ltize

r. 20

07.

Infe

ctio

us d

isea

ses

and

extin

ctio

n ris

k in

wild

mam

mal

s. C

onse

rvat

ion

Biol

ogy

21(5

): 12

69–1

279

Yes

Piha

, H.,

M. L

uoto

, M. P

iha,

and

J.

Mer

ilä. 2

007.

Anu

ran

abun

danc

e an

d pe

rsis

tenc

e in

agr

icul

tura

l lan

dsca

pes

durin

g a

clim

atic

ext

rem

e. G

loba

l C

hang

e Bi

olog

y 13

(1):

300–

311

Yes

Glo

bal c

limat

e ch

ange

has

bee

n sh

own

to b

e ne

gativ

ely

rela

ted

with

the

surv

ival

, dist

ribut

ion

and

abun

danc

e of

am

phib

ians

, as

wel

l as

influ

ence

thei

r bre

edin

g ph

enol

ogy.

Poun

ds, J

.A.,

A.C

. Car

nava

l, R

. Pu

sche

ndor

f, C

.F.B

. Had

dad,

and

K

.L. M

aste

rs. 2

006.

Res

pond

ing

to

amph

ibia

n lo

ss. S

cien

ce 3

14(5

805)

: 15

41–1

542

Yes

Evid

ence

sug

gest

s th

at c

limat

e ch

ange

and

oth

er f

acto

rs m

ay

cont

ribut

e to

dec

lines

by

trigg

erin

g di

seas

e ou

tbre

aks,

whi

ch m

ight

trav

el v

aryi

ng

dist

ance

s in

wav

elik

e pa

ttern

s.Po

unds

, J.A

., M

.R. B

usta

man

te, L

.A.

Col

oma,

J.A

. Con

sueg

ra, M

.P.L

. Fo

gden

, P.N

. Fos

ter,

E. L

a M

arca

, et

al.

2007

. Eco

logy

–Pou

nds

et a

l. re

ply.

Nat

ure

447:

E5–

E6

Yes

Pusc

hend

orf,

R. a

nd F

. Bol

años

. 20

06. D

etec

tion

of B

atra

choc

hytr

ium

de

ndro

batid

is in

Ele

uthe

roda

ctyl

us

fi tzi

nger

i: ef

fect

s of

ski

n sa

mpl

e lo

catio

n an

d hi

stol

ogic

sta

in. J

ourn

al

of W

ildlif

e D

isea

ses

42(2

): 30

1–30

6

Yes

The

chyt

rid f

ungu

s Ba

trac

hoch

ytri

um d

endr

obat

idis

ha

s be

en im

plic

ated

in a

mph

ibia

n de

clin

es a

roun

d th

e w

orld

.

Pusc

hend

orf,

R.,

F. C

asta

ñeda

, an

d J.R

. McC

rani

e. 2

006.

C

hytri

diom

ycos

is in

wild

fro

gs f

rom

Pi

co B

onito

Nat

iona

l Par

k, H

ondu

ras.

EcoH

ealth

3(3

): 17

8181

Yes

Poun

ds e

t al.

(200

6) f

ound

that

m

ost o

f th

e m

issi

ng h

arle

quin

fr

og s

peci

es v

anis

hed

in w

arm

er

than

ave

rage

yea

rs.

Con

td...

Golden toad as a climate change icon species / 317

App

endi

x 3

Con

td...

Art

icle

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

ch

ytri

diom

ycos

is

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

clim

ate

chan

ge

Exa

mpl

e of

cl

imat

e ch

ange

pr

omot

ing

chyt

ridi

omyc

osis

No

caus

e m

entio

ned

Exa

mpl

e of

A

PD b

ut n

o re

late

d ca

use

Exa

mpl

e of

ch

alle

ngin

g th

e C

TOH

Quo

tes

Raf

fel,

T.R

., J.R

. Roh

r, J.M

. K

iese

cker

, and

P.J.

Hud

son.

200

6.

Neg

ativ

e ef

fect

s of

cha

ngin

g te

mpe

ratu

re o

n am

phib

ian

imm

unity

un

der fi e

ld c

ondi

tions

. Fun

ctio

nal

Ecol

ogy

20(5

): 81

9–82

8

Yes

Incr

ease

d in

fect

ion

risk

due

to

war

min

g tre

nds

has

rece

ntly

bee

n im

plic

ated

in th

e ex

tinct

ion

of

man

y tro

pica

l fro

g sp

ecie

s.

Ram

sey,

J.P

., L.

K. R

eine

rt, L

.K.

Har

per,

D.C

. Woo

dham

s, an

d L.

A.

Rol

lins-

Smith

. 201

0. I

mm

une

defe

nces

aga

inst

Bat

rach

ochy

triu

m

dend

roba

tidis

, a f

ungu

s lin

ked

to

glob

al a

mph

ibia

n de

clin

es, i

n th

e So

uth

Afr

ican

cla

wed

fro

g, X

enop

us

laev

is. I

nfec

tion

and

Imm

unity

78(

9):

3981

–399

2

Yes

Rea

ding

, C.J.

200

7. L

inki

ng g

loba

l w

arm

ing

to a

mph

ibia

n de

clin

es

thro

ugh

its e

ffect

s on

fem

ale

body

con

ditio

n an

d su

rviv

orsh

ip.

Oec

olog

ia 1

51(1

): 12

5–13

1

Yes

Wha

t has

not

bee

n de

mon

stra

ted,

ho

wev

er, i

s ho

w th

e lin

k be

twee

n ‘g

loba

l war

min

g’ a

nd a

mph

ibia

n de

clin

es o

pera

tes

(Col

lins

and

Stor

fer

2003

) th

ough

Pou

nds

et a

l. (2

006)

hav

e su

gges

ted

that

tem

pera

ture

s in

man

y hi

ghla

nd a

reas

are

shi

fting

to

war

ds th

e gr

owth

opt

imum

fo

r th

e pa

thog

enic

chy

trid

fung

us (

Batr

acho

chyt

rium

de

ndro

batid

is),

ther

eby

enco

urag

ing

outb

reak

s.R

odde

r, D

., M

. Vei

th, a

nd S

. Lo

tters

. 200

8. E

nviro

nmen

tal

grad

ient

s ex

plai

ning

the

prev

alen

ce

and

inte

nsity

of

infe

ctio

n w

ith th

e am

phib

ian

chyt

rid f

ungu

s: th

e ho

st’s

pe

rspe

ctiv

e. A

nim

al C

onse

rvat

ion

11(6

): 51

3–51

7

Yes

Roh

r, J.R

., T.

R. R

affe

l, J.M

. R

oman

sic,

H. M

cCal

lum

, and

P.J.

H

udso

n. 2

008.

Eva

luat

ing

the

links

be

twee

n cl

imat

e, d

isea

se s

prea

d an

d am

phib

ian

decl

ines

. Pro

ceed

ings

of

the

Nat

iona

l Aca

dem

y of

Sci

ence

s of

the

Uni

ted

Stat

es o

f Am

eric

a 10

5(45

): 17

436–

1744

1

Yes

Con

td...

318 / Ochoa-Ochoa et al.

App

endi

x 3

Con

td...

Art

icle

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

ch

ytri

diom

ycos

is

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

clim

ate

chan

ge

Exa

mpl

e of

cl

imat

e ch

ange

pr

omot

ing

chyt

ridi

omyc

osis

No

caus

e m

entio

ned

Exa

mpl

e of

A

PD b

ut n

o re

late

d ca

use

Exa

mpl

e of

ch

alle

ngin

g th

e C

TOH

Quo

tes

Ros

a, I

.D.,

F. S

imon

celli

, A. F

agot

ti,

and

R. P

asco

lini.

2007

. Eco

logy

: the

pr

oxim

ate

caus

e of

fro

g de

clin

es?

Nat

ure

447(

7144

): E4

–E5

Yes

We

ther

efor

e th

ink

that

the

focu

s by

Pou

nds

et a

l. (2

006)

on

a si

ngle

pat

hoge

n is

har

d to

just

ify

beca

use

the

host

-par

asite

eco

logy

is

at p

rese

nt s

o po

orly

und

erst

ood.

Shea

rer,

C.A

., E.

Des

cals

, B.

Koh

lmey

er, J

. Koh

lmey

er, L

. M

arva

nová

, D. P

adge

tt, D

. Por

ter,

et a

l. 20

07. F

unga

l bio

dive

rsity

in

aqua

tic h

abita

ts. B

iodi

vers

ity a

nd

Con

serv

atio

n 16

(1):

49–6

7

Yes

This

chy

trid,

Bat

rach

ochy

triu

m

dend

roba

tidis

, par

asiti

zes

and

kills

am

phib

ians

(B

erge

r et

al.

1999

) an

d m

ay b

e re

spon

sibl

e,

alon

g w

ith c

hang

es in

en

viro

nmen

tal f

acto

rs s

uch

as

tem

pera

ture

(Po

unds

et a

l. 20

06),

for

the

glob

al a

mph

ibia

n de

clin

e.Sm

ith, K

.G.,

K.R

. Lip

s, an

d J.M

. C

hase

. 200

9. S

elec

ting

for

extin

ctio

n:

nonr

ando

m d

isea

se-a

ssoc

iate

d ex

tinct

ion

hom

ogen

izes

am

phib

ian

biot

as. E

colo

gy L

ette

rs 1

2(10

): 10

69–1

078

Yes

Rec

ent a

naly

ses

indi

cate

that

th

ere

is p

rese

ntly

littl

e di

rect

ev

iden

ce f

or a

rol

e of

clim

ate

as

the

wid

espr

ead,

pro

xim

ate

caus

e of

am

phib

ian

decl

ines

in L

ower

C

entra

l Am

eric

a (c

f. Po

unds

et

al.

2006

; Lip

s et

al.

2008

; R

ohr

et a

l. 20

08).

Tylia

naki

s, J.M

., R

.K. D

idha

m,

J. B

asco

mpt

e, a

nd D

.A. W

ardl

e.

2008

. Glo

bal c

hang

e an

d sp

ecie

s in

tera

ctio

ns in

terr

estri

al e

cosy

stem

s. Ec

olog

y Le

tters

11(

12):

1351

–136

3

Yes

(but

EN

SO)

Und

erw

ood,

E.C

. and

B.L

. Fi

sher

. 200

6. T

he r

ole

of a

nts

in

cons

erva

tion

mon

itorin

g: if

, whe

n an

d ho

w. B

iolo

gica

l Con

serv

atio

n 13

2(2)

: 166

–182

Yes

Incr

ease

s in

CO

2 an

d ot

her

gree

nhou

se g

ases

in th

e at

mos

pher

e ar

e an

ticip

ated

to

caus

e de

trim

enta

l cha

nges

to th

e en

viro

nmen

t.Vo

yles

, J.,

E.B

. Ros

enbl

um, a

nd L

. B

erge

r. 20

11. I

nter

actio

ns b

etw

een

Bat

rach

ochy

trium

den

drob

atid

is a

nd

its a

mph

ibia

n ho

sts:

a r

evie

w o

f pa

thog

enes

is a

nd im

mun

ity. M

icro

bes

and

Infe

ctio

n 13

(1):

25–3

2

Yes

The

impo

rtanc

e of

tem

pera

ture

al

so p

rom

pted

the

hypo

thes

is

that

glo

bal c

limat

e ch

ange

mig

ht

crea

te o

ptim

al th

erm

al c

ondi

tions

fo

r di

seas

e sp

read

(i.e

. the

chy

trid

ther

mal

opt

imum

hyp

othe

sis)

.W

ason

ga, D

.V.,

A. B

ekel

e, S

. Lo

tters

, and

M. B

alak

rishn

an. 2

007.

A

mph

ibia

n ab

unda

nce

and

dive

rsity

in

Mer

u N

atio

nal P

ark,

Ken

ya. A

frica

n Jo

urna

l of E

colo

gy 4

5(1)

: 55–

61

Yes

The

surv

ival

of

the

amph

ibia

n fa

una

all o

ver

the

wor

ld is

und

er

thre

at a

s a

resu

lt of

a v

arie

ty

of c

ause

s, ap

pare

ntly

rel

ated

to

glob

al c

hang

e.

Con

td...

Golden toad as a climate change icon species / 319

App

endi

x 3

Con

td...

Art

icle

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

ch

ytri

diom

ycos

is

Exa

mpl

e of

vu

lner

abili

ty

tow

ards

clim

ate

chan

ge

Exa

mpl

e of

cl

imat

e ch

ange

pr

omot

ing

chyt

ridi

omyc

osis

No

caus

e m

entio

ned

Exa

mpl

e of

A

PD b

ut n

o re

late

d ca

use

Exa

mpl

e of

ch

alle

ngin

g th

e C

TOH

Quo

tes

Will

iam

s, S.

E., L

.P. S

hoo,

J.L

. Is

aac,

A.A

. Hof

fman

n, a

nd G

. La

ngha

m. 2

008.

Tow

ards

an

inte

grat

ed f

ram

ewor

k fo

r as

sess

ing

the

vuln

erab

ility

of

spec

ies

to c

limat

e ch

ange

. Pub

lic L

ibra

ry o

f Sci

ence

Bi

olog

y 6(

12):

2621

–262

6

Yes

Witt

e, C

.L.,

M. S

redl

, A.S

. Kan

e,

and

L.L.

Hun

gerfo

rd. 2

008.

Ep

idem

iolo

gic

anal

ysis

of

fact

ors

asso

ciat

ed w

ith lo

cal d

isap

pear

ance

s of

nat

ive

rani

d fro

gs in

Ariz

ona.

C

onse

rvat

ion

Biol

ogy

22(2

): 37

5–38

3

Yes

Woo

dham

s, D

.C.,

R.A

. Alfo

rd,

C.J.

Brig

gs, M

. Joh

nson

, and

L.A

. Ro

llins

-Sm

ith. 2

008.

Life

-hist

ory

trade

-offs

infl u

ence

dise

ase

in c

hang

ing

clim

ates

: stra

tegi

es o

f an

am

phib

ian

path

ogen

. Eco

logy

89(

6): 1

627–

1639

Yes

Woo

dham

s, D

.C.,

K. A

rdip

radj

a, R

.A.

Alfo

rd, G

. Mar

ante

lli, L

.K. R

eine

rt,

and

L.A

. Rol

lins-

Smith

. 200

7.

Res

ista

nce

to c

hytri

diom

ycos

is v

arie

s am

ong

amph

ibia

n sp

ecie

s an

d is

co

rrela

ted

with

ski

n pe

ptid

e de

fens

es.

Anim

al C

onse

rvat

ion

10(4

): 40

9–41

7

Yes

Woo

dham

s, D

.C.,

N. K

enyo

n, S

.C.

Bell,

R.A

. Alfo

rd, S

. Che

n, D

. Bi

llhei

mer

, Y. S

hyr,

et a

l. 20

11.

Ada

ptat

ions

of

skin

pep

tide

defe

nces

an

d po

ssib

le r

espo

nse

to th

e am

phib

ian

chyt

rid f

ungu

s in

pop

ulat

ions

of

Aus

tralia

n gr

een-

eyed

tree

frogs

, Li

toria

gen

imac

ulat

a. D

iver

sity

and

Dist

ribut

ions

16(

4): 7

03–7

12

Yes

(but

en

viro

nmen

tal

co-f

acto

rs)

Envi

ronm

enta

l cof

acto

rs v

ary

amon

g po

pula

tions

. The

se m

ay

be p

artic

ular

ly im

porta

nt in

the

dyna

mic

s of

chy

tridi

omyc

osis

.

Zam

bran

o, L

., E.

Veg

a, M

.L.G

. H

erre

ra, E

. Pra

do, a

nd V

.H. R

eyno

so.

2007

. A p

opul

atio

n m

atrix

mod

el

and

popu

latio

n vi

abili

ty a

naly

sis

to

pred

ict t

he f

ate

of e

ndan

gere

d sp

ecie

s in

hig

hly

man

aged

wat

er s

yste

ms.

Anim

al C

onse

rvat

ion

10(3

): 29

7–30

3

Yes

Acr

onym

s: a

mph

ibia

n po

pula

tion

decl

ine

(APD

), an

d ch

ytrid

-ther

mal

-opt

imum

hyp

othe

sis (

CTO

H).

*Ind

icat

es m

is-c

itatio

n of

Pou

nds e

t al.

2006