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: [email protected]
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
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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.
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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
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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.
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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
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
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
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