Vol 439|12 January 2006|doi:10.1038/nature04246 ARTICLES Widespread amphibian extinctions from epidemic disease driven by global warming J. Alan Pounds1, Martı´n R. Bustamante2, Luis A. Coloma2, Jamie A. Consuegra3, Michael P. L. Fogden1, Pru N. Foster4†, Enrique La Marca5, Karen L. Masters6, Andre´s Merino-Viteri2, Robert Puschendorf7, Santiago R. Ron2,8, G. Arturo Sa´nchez-Azofeifa9, Christopher J. Still10 & Bruce E. Young11 As the Earth warms, many species are likely to disappear, often because of changing disease dynamics. Here we show that a recent mass extinction associated with pathogen outbreaks is tied to global warming. Seventeen years ago, in the mountains of Costa Rica, the Monteverde harlequin frog (Atelopus sp.) vanished along with the golden toad (Bufo periglenes). An estimated 67% of the 110 or so species of Atelopus, which are endemic to the American tropics, have met the same fate, and a pathogenic chytrid fungus (Batrachochytrium dendrobatidis) is implicated. Analysing the timing of losses in relation to changes in sea surface and air temperatures, we conclude with ‘very high confidence’ (.99%, following the Intergovernmental Panel on Climate Change, IPCC) that large-scale warming is a key factor in the disappearances. We propose that temperatures at many highland localities are shifting towards the growth optimum of Batrachochytrium, thus encouraging outbreaks. With climate change promoting infectious disease and eroding biodiversity, the urgency of reducing greenhouse-gas concentrations is now undeniable. Humans are altering the Earth’s climate1–4 and thus the workings of these members of the toad family (Bufonidae)26. Brightly coloured living systems5–8, including pathogens and their hosts9–11. Among the and active during the day near streams, most are readily observed and predicted outcomes is the extinction of many species10,12,but identified. For the first time, data indicate when each of numerous detecting such an effect is difficult against a backdrop of other species was seen for the last time. changes, especially habitat destruction. One approach is to focus Our analyses capitalise on insights gained by alternating between on organisms for which current rates of extinction exceed large and small spatial scales35 (Supplementary Fig. 1). Since epi- those expected from habitat loss. Amphibians are a case in point. demics of Batrachochytrium are implicated in Atelopus extinctions in Thousands of species have declined, and hundreds are on the brink Central and South America26, we first explain that the predicted of extinction or have already vanished13. The Global Amphibian association with warm years, if juxtaposed with theory regarding this Assessment (GAA) lists 427 species as “critically endangered”, chytrid, is a paradox. We then: (1) assess large-scale altitudinal including 122 species that are “possibly extinct”13. A majority of patterns of extinction risk with this paradox in mind; (2) consider the former, and nearly all of the latter, have declined even in determinants of local climate in the case of the golden toad and the seemingly undisturbed environments. Monteverde harlequin frog to select large-scale temperature signals The causes have remained unclear, in part because of their for analysing the biological patterns; (3) show that the timing of the complexity14–16. Although pathogens are implicated14–28,their widespread extinctions is strongly tied to these signals; and (4) relationship to environmental change is poorly understood. Here explore local climate from a chytrid’s viewpoint to frame a solution we test the “climate-linked epidemic hypothesis”29–34, which predicts to the paradox. declines in unusually warm years but does not assume a particular disease or chain of events. Recent studies have considered this The climate–chytrid paradox idea15,18,21,23,28, yet data have not permitted a geographically broad The climate-linked epidemic hypothesis predicts amphibian declines test that examines landscape alteration, global warming and climate in unusually warm years, because shifts in temperature or related fluctuations on the timescale of El Nin˜o. Suffering widespread variables often influence disease dynamics9–11. As temperatures rise, extinctions often despite habitat protection, harlequin frogs (Atelo- climate fluctuations may cross thresholds for certain pathogens, pus) afford such a test. A new database, produced by 75 researchers, triggering outbreaks. Many diseases are expected to become more documents the case in unprecedented detail, owing to the nature of lethal, or to spread more readily, as the Earth warms9–11. 1Golden Toad Laboratory for Conservation, Monteverde Cloud Forest Preserve and Tropical Science Center, Santa Elena, Puntarenas 5655-73, Costa Rica. 2Museo de Zoologı´a, Centro de Biodiversidad y Ambiente, Escuela de Biologı´a, Pontificia Universidad Cato´lica del Ecuador, Avenida 12 de Octubre 1076 y Roca, Apartado 17-01-2184, Quito, Ecuador. 3Department of Environmental Science, Barnard College, Columbia University, 3009 Broadway, New York, New York 10027, USA. 4Center for Climate Studies Research, University of Tokyo, Kombaba, 4-6-1, Meguro-ku, Tokyo 153-8904, Japan. 5Laboratorio de Biogeografı´a, Escuela de Geografı´a, Facultad de Ciencias Forestales y Ambientales, Universidad de Los Andes, Apartado 116, Me´rida 5101-A, Venezuela. 6Council for International Educational Exchange, Monteverde, Puntarenas 5655-26, Costa Rica. 7Escuela de Biologı´a, Universidad de Costa Rica, San Pedro, Costa Rica. 8Texas Memorial Museum and Department of Integrative Biology, University of Texas, Austin, Texas 78712, USA. 9Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta T6G 2E3, Canada. 10Department of Geography, 3611 Ellison Hall, University of California at Santa Barbara, Santa Barbara, California 93106, USA. 11NatureServe, Monteverde, Puntarenas 5655-75, Costa Rica. †Present address: Department of Earth Sciences, University of Bristol, Wills Memorial Building, Queen’s Road, Bristol BS8 1RJ, UK. 161 © 2006 Nature Publishing Group ARTICLES NATURE|Vol 439|12 January 2006 Chytridiomycosis, caused by Batrachochytrium, is thought to be an well as high ones may limit the impact of Batrachochytrium. The exception10. This chytrid grows on amphibian skin and produces altitudinal effects remain significant when we control for range size, aquatic zoospores22,24. Widespread and ranging from deserts and which also influences extinction probability. Average range size lowland rainforests to cold mountain tops27, it is sometimes a non- decreases from lower to higher zones as defined in Fig. 1, but is lethal parasite and possibly a saprophyte19,25. It is associated with host similar for the upper two. mortality in highlands or during winter22, and, according to theory, These altitudinal patterns contribute to the severity of losses. For becomes more pathogenic at lower temperatures19,22. Hence, the idea instance, the zone losing the highest percentage of species had the that it causes declines in warm years is paradoxical. Moreover, the greatest diversity (Fig. 1). Our overall estimate that 67% of the species fungus is apparently more lethal under moist conditions24,26, yet, at have disappeared is weighted by the number of species per zone. many affected sites, warm years are comparatively dry. Although extinction probabilities are independent of tier, an Ideas of two sorts could resolve this paradox. First, warm or dry unweighted estimate based on tier one alone (57%) under-represents conditions may stress amphibians, possibly increasing susceptibility the severely affected mid-elevation species. to disease29. Second, warm years could favour Batrachochytrium GAA data for New World amphibians13 suggest similar altitudinal directly. The prevailing idea—that lower temperatures benefit the patterns (Supplementary Fig. 2). The percentage of species extinct or chytrid19,22—might be an oversimplification of the pathogen’s threatened is largest at middle elevations, even though higher- response to climate. elevation species generally have smaller ranges. Clearly, the role of climate needs re-evaluating. Altitudinal patterns of extinction risk This prevailing idea predicts greater extinction risk for higher- Temperature signals elevation species. Many are already prone to extinction, because To select temperature signals, we consider the scale at which local geographic ranges tend to decrease in size with increasing elevation. climates are determined. In Costa Rica’s Monteverde cloud forest, The probability of disappearance might thus be expected to increase reduced mist frequency in warm years is associated with shifts from lowlands to mountain tops. in populations of birds, reptiles and amphibians, including the For a preliminary test with Atelopus, we consider 100 species for disappearance of the golden toad and the Monteverde harlequin which data indicate the last year of observation (LYO). We recognize frog31. Whereas nearby lowland deforestation might have influenced two tiers. According to La Marca et al. (ref. 26), the population data conditions36, temperatures in Central and South America agree are sufficient to judge whether tier-one species (n ¼ 51) have with simulated responses to greenhouse-gas accumulation3.Here declined, but not tier-two species (n ¼ 49). Throughout our ana- we quantify the extent and timing of deforestation upwind of lyses, patterns are similar for tier one and for tiers one and two Monteverde, model regional climate, and consider how local