The amphibians are long-term survivors, having endured four previous planetary mass extinctions. Through these extinctions, not only did all three orders of amphibians escape extinction, but most families and genera survived. However, the global loss of biodiversity is accelerating, and amphibians are the most threatened group of vertebrates. There are many potential causes for this, but an emerging infectious disease, chytridiomycosis, caused by a highly infectious fungal pathogen, is implicated in mass die offs and extinctions worldwide. Effects of climate change on amphibian physiology has been proposed as a mechanism initiating chytridiomycosis epidemics in Central and South America on the assumption that increased temperature variability reduces amphibian immunity to fungal infection. This project will investigate whether exposure to elevated temperatures increases susceptibility to disease by measuring thermal stress and infection dynamics in frogs at a range of sites in the Peruvian Andes. This project will also delineate the historic and present distribution of the fungus in highly susceptible amphibians throughout South America. Preserved museum specimens collected at many sites throughout South America over the last 8 decades will be tested to determine if fungal pathogen emergence is coincident with collapse of amphibian populations. Available site-specific climate data from the past 5 decades will be used to evaluate whether large-scale climatic events or warming trends are associated with the emergence of this fungal pathogen and subsequent extinction of amphibian species.

Results from this research will inform conservation efforts to prevent loss of amphibian species in tropical regions. Understanding the factors that contribute to outbreaks and subsequent persistence of disease in amphibian species is essential to developing strategies that can avert the loss of biodiversity and mitigate the impact of epidemics. This project will support an early career scientist, strengthen collaboration between researchers in the United States and Latin America, support the research training of a postdoctoral scholar, and provide field research experiences for two graduate students.

Project Report

Many scientists argue that we are entering the sixth mass extinction of life on earth. The amphibians, a major group of land vertebrates, are representative of the current global biodiversity crisis. More than 1/3 of known species are threatened with extinction, and human actions are implicated. This project investigated two global threats to biodiversity: climate change and emerging infectious disease. Specifically, we set out to test the effects of climate change and the emergence of a fungal pathogen, Batrachochytrium dendrobatidis (Bd), on Tropical Andean montane frog populations. This pathogen causes the amphibian disease chytridiomycosis, which is directly liked with the collapse of over 200 species of amphibians worldwide. In addition, recent studies hypothesize that tropical ectotherms (i.e. "cold blooded" animals) are particularly threatened by climate warming, because they are operating at temperatures that are close to their critical maximal temperatures (i.e. temperatures at which they cannot function normally). Our study area is a well-protected Biodiversity Hotspot containing over 140 species of amphibians, but our study focuses on ~50 species that occur in the montane habitats. In our previous work, we showed that Bd was associated with the pattern of declines but it is still unknown whether climate change played a role. This issue is hotly debated in current literature and it remains unclear whether climate change is implicated in chytridiomycosis disease outbreaks. This study uses on a wealth of research data we collected over the last 16 years in and near Manu National Park in the Andean highlands of Peru. The eastern slopes and foothills of the Andes host the greatest amphibian diversity of any area in the world. Our baseline information consists of surveys of amphibian populations along a broad transect between 600 and 3800 m elevation in Manu National Park in the southeastern area of Peru. Over this time period, we witnessed the collapse of these populations in recent years: the number of species (46 in 1999) declined by 36% overall between 1999 and 2008–2009. We document local extinctions of 55% of stream-dwelling and arboreal species and 22% terrestrial-breeding species. Our data include detailed species abundance and diversity patterns, elevational distributions, thermal tolerances, Bd prevalence and infection loads, as well as molecular phylogenetic relationships of 15 of the species that occur in the area. Our primary objectives were (1) to test whether frogs exposed to stressful temperature conditions are more vulnerable to Bd infection; (2) to contrast the effects of temperature and Bd infection on frog survival in reciprocal translocation experiments, coupled with a new intervention technique using symbiotic skin bacteria cultured by the Vredenburg Lab; (3) to evaluate the correlation between time series of biological observations (elevational distribution of frogs, Bd prevalence, incidence of malformations) and climate warming; and (4) to test the mechanistic basis of bioclimatic distribution models by relating the thermal physiology of frogs species to their distribution along steep elevational gradients. We assessed the vulnerability of frogs to Bd under different thermal regimes (objective 1) and found that frogs from higher elevations are actually less vulnerable to stress caused by temperature fluctuations than frogs from lower elevations. Frogs at high elevation are adapted to survive large daily fluctuations in temperature (i.e. night vs. day) whereas those living at lower elevations do not experience as much variation naturally. Due to our reduced budget, we did not conduct a reciprocal transplant experiment (objective 2), but were able to culture over 250 strains of symbiotic skin bacteria from hosts amphibians. Assays on petri dishes showed that nearly 30 bacterial species inhibited the growth of the fungal pathogen Bd. W tested tested over 7,000 amphibian museum specimens collected over the last century for the presence of the fungal pathogen (objective 3) using our PCR assay. We found a strong pattern of Bd arrival followed by species collapse throughout South America. We are currently combining these data with bioclimatic distribution models to test for relationships between frog physiology, climate change patterns and population declines and extinctions (objective 4). This project has broadened the participation of underrepresented groups in Science by supporting a principal investigator and a postdoctoral scholar which both have Hispanic heritage. The postdoc has since been able to secure a faculty position at a major US University. The project also trained two Peruvian university students, who are native Quechua, Amazonian and mixed-ethnicity people in educational and research activities in the field and lab (in Peru) and 2 Peruvian Park rangers. The projects results have been integrated into amphibian species accounts on (as a new bilingual section), an online research and conservation resource for amphibian biology that gets an average of 7.3 million successful queries / yr. since 2008. The project also helped support financially and train two graduate students, and two undergraduate students at San Francisco State University, California, USA.

National Science Foundation (NSF)
Division of Environmental Biology (DEB)
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Alan James Tessier
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San Francisco State University
San Francisco
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