Grantee Research Project Results
Final Report: Airborne Agricultural Contaminants, Disease, and Amphibian Declines: Using Landscape-Scale Patterns to Evaluate the Severity of an Emerging Environmental Problem
EPA Grant Number: R830395Title: Airborne Agricultural Contaminants, Disease, and Amphibian Declines: Using Landscape-Scale Patterns to Evaluate the Severity of an Emerging Environmental Problem
Investigators: Davidson, Carlos , Knapp, Roland A.
Institution: California State University - Sacramento , University of California - Santa Barbara
EPA Project Officer: Chung, Serena
Project Period: January 1, 2002 through December 31, 2003 (Extended to November 30, 2005)
Project Amount: $214,848
RFA: Futures Research in Natural Sciences (2001) RFA Text | Recipients Lists
Research Category: Land and Waste Management , Ecological Indicators/Assessment/Restoration , Futures , Hazardous Waste/Remediation
Objective:
More than 40 percent of Earth’s 5,700+ amphibian species have undergone recent declines. In California, separate studies have implicated introduced fish, airborne pesticides, and disease (amphibian chytrid fungus, Batrachochytrium dendrobatidis) as causal agents. Given the likely involvement of multiple factors in causing the decline of amphibians in this system, understanding the relative importance of these factors is critical for the development of effective conservation efforts and environmental policies. In addition, if airborne pesticides are associated with amphibian declines, their typically low concentrations suggest that any effects are more likely to be indirect than direct (i.e., causing mortality). One potential mechanism for such indirect effects is the weakening of amphibian immune responses and the concomitant increase in disease susceptibility.
The objectives of this research project were to: (1) compare the role and relative effect of upwind pesticide use and fish on the distribution of a declining amphibian population after accounting for significant effects of habitat characteristics, and (2) describe the association between upwind pesticide use and the probability of amphibian population extinction and of B. dendrobatidis outbreaks after accounting for significant effects of nonnative fish and habitat characteristics. If analyses conducted as part of either objective supported our predictions, we also attempted to identify pesticides groups, pesticide classes, and individual pesticides that were associated most strongly with the observed relationship. Our study organism was the mountain yellow-legged frog (Rana muscosa), a species that was once abundant in California’s Sierra Nevada but has disappeared from 90 percent of its historic range during the past century.
To examine the role and relative effect of upwind pesticide use and fish on the mountain yellow-legged frog (R. muscosa), we used unusually detailed data sets that included: (1) spatially-explicit historic pesticide use records for California’s Central Valley; and (2) presence/absence of R. muscosa and nonnative fish as well as habitat characteristics at 6,831 water bodies in the adjacent Sierra Nevada. Habitat characteristics and presence/absence of R. muscosa and fish were quantified using field surveys. Pesticide use upwind of each site was calculated from pesticide application records and predominant wind directions.
To determine whether patterns of R. muscosa population extinctions and B. dendrobatidis outbreaks in these populations were consistent with the hypothesis that recent amphibian declines are the result of airborne pesticides facilitating the emergence of B. dendrobatidis, we used data collected during repeat surveys of all R. muscosa populations in study area (n = 515) between 2003 and 2005. The presence/absence of B. dendrobatidis at the study sites was determined based on inspections of tadpole mouthparts. In R. muscosa, B. dendrobatidis infection is indicated accurately by depigmentation of the upper jaw sheath in tadpoles. Pesticide use upwind of each site was calculated from pesticide application records and predominant wind directions.
Summary/Accomplishments (Outputs/Outcomes):
Objective 1
Using generalized additive models, we found that, after accounting for habitat effects, the probability of R. muscosa presence was reduced significantly by both fish and pesticides. As predicted, the odds of R. muscosa occurrence declined steeply with increasing upwind pesticide use. Based on odds ratios, the effect of upwind pesticide use was stronger than the effect of fish at 63 percent of the water bodies in our study area. In addition, “no fish” and “no pesticides” simulations indicated that pesticides had a much greater overall effect on R. muscosa presence/absence than did fish. The overall stronger effect of pesticides reflects the combination of a stronger single-site effect of pesticides and the wider distribution of pesticides than fish. The second pesticide-related variable in this analysis, the degree to which a site was sheltered from the predominant wind (and associated pesticides), also was a significant predictor of R. muscosa presence. In agreement with previous studies, water body location, water depth, elevation, isolation from other water bodies, and littoral zone substrate characteristics had additional significant effects on the distribution of R. muscosa. Taken together, these results represent the strongest evidence to date that airborne pesticides are contributing to amphibian declines in the Sierra Nevada. In addition, our results suggest that amphibian declines may have complex multifactorial causes and caution that single-factor studies that demonstrate the importance of one factor should not be used as evidence against the importance of other factors.
Objective 2
Using generalized additive models, we found that, after accounting for habitat and fish effects, the probability of R. muscosa population extinction and of B. dendrobatidis presence both were associated significantly with upwind pesticide use. Instead of the predicted linear increase in both probabilities with increasing upwind pesticide use, however, response curves indicated that although both probabilities increased between the lowest and intermediate pesticide use levels, they then declined substantially before increasing again at the highest pesticide use levels. The probability of R. muscosa population extinction also was associated significantly with the degree to which a site was sheltered from the predominant wind (and associated pesticides), presence/absence of fish, water body location, and water depth. In addition to upwind pesticide use, the probability of B. dendrobatidis outbreaks was associated significantly with water body location and the number of tadpoles inspected per site. We lack any explanation for the dip in the probability of R. muscosa population extinction and B. dendrobatidis outbreaks at intermediate pesticide use levels and, as a consequence, these results provide limited support for the hypothesis that the negative effect of pesticides on R. muscosa is the result of facilitation by pesticides of amphibian diseases.
Conclusions:
We conclude that although our analyses indicated a strong negative effect of upwind pesticides on the distribution of R. muscosa, our analyses of the association between upwind pesticides and either the probability of R. muscosa population extinction or B. dendrobatidis outbreaks produced results that were considerably more ambiguous. We suggest that pesticides deserve greater attention and concern than they have received to date, and that progress in understanding the indirect effects of airborne pesticides will require a combination of additional amphibian and disease surveys, measurement of site-specific pesticide concentrations, and field and laboratory experiments.
Journal Articles on this Report : 3 Displayed | Download in RIS Format
Other project views: | All 3 publications | 3 publications in selected types | All 3 journal articles |
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Davidson C, Knapp RA. Multiple stressors and amphibian declines: dual impacts of pesticides and fish on yellow-legged frogs. Ecological Applications 2007;17(2):587-597. |
R830395 (Final) |
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Hoh E, Hites RA. Brominated flame retardants in the atmosphere of the east-central United States. Environmental Science & Technology 2005;39(20):7794-7802. |
R830395 (Final) R830397 (Final) |
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Knapp RA, Morgan JAT. Tadpole mouthpart depigmentation as an accurate indicator of chytridiomycosis, an emerging disease of amphibians. Copeia 2006;2006(2):188-197. |
R830395 (Final) |
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Supplemental Keywords:
agriculture, air, aquatic, amphibian decline, Batrachochytrium dendrobatidis, California, CA, chemicals, ecological effects, ecology, EPA Region 9, extinction, generalized additive models, indicators, modeling, pathogens, pesticides transport, Rana muscosa, sensitive populations, surveys, water,, RFA, Scientific Discipline, ENVIRONMENTAL MANAGEMENT, Geographic Area, ECOSYSTEMS, Ecosystem Protection/Environmental Exposure & Risk, Ecosystem/Assessment/Indicators, State, Ecological Effects - Environmental Exposure & Risk, Ecological Monitoring, Ecological Risk Assessment, Ecology and Ecosystems, Biology, Risk Assessment, aquatic ecosystem, ecological exposure, pesticide exposure, airborne agricultural contaminants, ecosystem assessment, aquatic habitat, chemical contaminants, immune dysfunction, ecological assessment, agrochemcial, lanscape scale patterns, aquatic ecology, California (CA), amphibian population, diseaseRelevant Websites:
http://www.mylfrog.info Exit
http://bss.sfsu.edu/cdavidson/ Exit
http://www.msi.ucsb.edu/resrchrs/knapp/text/name.html Exit
Progress and Final Reports:
Original AbstractThe perspectives, information and conclusions conveyed in research project abstracts, progress reports, final reports, journal abstracts and journal publications convey the viewpoints of the principal investigator and may not represent the views and policies of ORD and EPA. Conclusions drawn by the principal investigators have not been reviewed by the Agency.