Host-parasite interactions are embedded within dynamic, often highly disturbed environments, which can sharply alter patterns of infection and disease risk among hosts. Changes in land use and the resulting shifts in biological communities have been linked to the emergence of pathogens with medical and veterinary importance. However, the ecological mechanisms responsible for increases in infection often remain conjectural. This proposal examines how the ongoing transformation of landscapes surrounding wetlands influences an emerging issue of conservation importance: amphibian limb deformities. The flatworm parasite Ribeiroia ondatrae, which sequentially infects freshwater snails, larval amphibians, and birds, has been linked to widespread limb deformities in amphibians. Infection and the resulting malformations also increase amphibian mortality, potentially causing declines in amphibian populations. Building upon previously funded NSF research and ecological theory, the current proposal combines broad-scale field surveys and mechanistic experiments to understand how land use change, by altering host density and host diversity, will promote or limit Ribeiroia abundance and amphibian malformations. This effort will specifically seek to identify how biodiversity losses in freshwater ecosystems affect the transmission of pathogenic parasites, such as Ribeiroia. Considering the growing number of emerging infections that threaten human health and wildlife conservation, results of the proposed efforts have broad application potential. Ribeiroia is not only growing in conservation importance itself, but is an excellent analog for other parasite infections of economic and human-health significance (e.g., human blood flukes). This proposal would further support cooperative efforts among amphibian biologists and ecologists to address ongoing declines in amphibian populations worldwide.
The goal of the current project was to understand how variation in land-use and the resulting changes in community diversity influence infectious diseases in wildlife. Given ongoing losses in biodiversity worldwide and proposed links between diversity and diseases of both humans and wildlife, this issue is broadly relevant to a wide range of disciplines. To this end, we combined field sampling and mechanistic experiments to (1) identify associations between dominant land-use patterns and infection, and (2) test hypotheses regarding the underlying ecological mechanisms. Over three years, we sampled 342 wetlands in California and examined more than 24,000 amphibians for signs of pathology. Limb malformations, which occur when infections by parasitic flatworms is high, were widespread and ranged in prevalence from 0% to >80% of emerging frogs at a site. Infection by the parasite explained roughly 76% of the variance in such deformities, emphasizing the overall importance of parasite infection in explaining amphibian malformations within this region, which is a topic that has generated significant controversy since malformations began to be widely observed in the 1990s. Alongside our data on parasite infection and pathology, we also obtained valuable information on amphibian diversity and the distribution of endangered, threatened, and invasive species. From 2009-2010 the California red-legged frog (Rana draytonii), which is federally endangered, was observed breeding at 73 wetlands; the California tiger salamander (Ambystoma californiense), also endangered, was noted breeding at 40 wetlands; the invasive American bullfrog (Rana catesbeiana) was recorded breeding at 42 ponds. Synthesis of the field and experimental data provided insights into how changes in aquatic community diversity affected pathogen transmission and disease risk in amphibians. Sampling of California wetlands indicated that host communities were strongly nested, with competent hosts for the trematode Ribeiroia ondatrae predominating in low-richness assemblages and unsuitable hosts increasingly present in more diverse communities. As a result, host species richness strongly moderated pathogen transmission and disease pathology, with a 78.4% decline in transmission in richer assemblages. The experimental components of the project included outdoor mesocosm experiments and laboratory manipulations evaluating how changes in host density and diversity affect parasite transmission and host disease. For the snail experiment, we found that increases in snail species richness (from 1 to 4 species) had sharply negative effects on the density of infected hosts (~90% reduction). In laboratory manipulations of amphibian diversity, increases in host richness from one to three species caused a 64% reduction in transmission. In outdoor mesocosms designed to mimic natural assemblages, both total infection (summed among host individuals and species) and per capita infections in P. regilla decreased by ~50% between the lowest (1 species) and highest richness (4 species) treatments. Correspondingly, increases in richness caused a decline in disease pathology. In conclusion, these findings indicate that (a) malformations are widespread among California anuran communities, (b) these malformations are detrimental to amphibian fitness and performance, (c) parasitic infection explains most of the variation in malformation occurrence and severity, (d) both amphibian and snail host communities show predictable patterns of assembly in which the most susceptible host species are early colonizers, and (e) as a result of these patterns, changes in diversity significantly alter the ability of Ribeiroia parasites to move among hosts consistent with predictions stemming from the dilution effect. With respect to educational and outreach activities, we have worked with five Research Experiences for Undergraduates (REU) students (two undergraduates from Humboldt State University and three undergraduates from the University of Colorado, including two Native Americans), one Research Experience for Teachers (RET) high school teacher (from Erie High), two Bioscience Undergraduate Research Skills and Training (BURST) students (from the University of Colorado), and two Summer Multicultural Access to Research and Training (SMART) students (one African Amercian student from Eastern Kentucky University and two Hispanic students from the University of Puerto Rico). Second, we organized and planned two symposia/special organized sessions at major meetings related to amphibian disease issues (American Society for Parasitology and Ecological Society of America). Third, we launched a new website describing the Amphibian Parasite Observatory (details presented below). Fourth, in addition to more than 38 published papers stemming from this research, members of the project presented results of the research at major scientific meetings, invited colloquia, educational outreach events, and local interest groups (e.g., ASP, ESA, California Parasitologists, UC Davis, Zurich Institute of Ecology, CO Herpetologists, Reactive Nitrogen Workshop, and several local schools). And fifth, together with our partners at Freshwaters Illustrated, we produced and distributed an informational brochure on amphibian diseases and deformities as well as developed a short video vignette composed of interviews, photographs, and lab- and field-clips that highlights the environmental complexity underlying land use changes, diversity loss and disease emergence. This video has been featured by PBS and National Geographic and is currently posted freely available on YouTube (with >1400 views).
