Both parasites and predators can affect animals in a variety of complex ways in addition to directly affecting survival and reproduction. For instance, parasites can change how susceptible their hosts are to predators by affecting host behavior or other traits. Similarly, prey that sense a predator is near through visual or chemical cues (e.g., smell) may change their behavior, which may affect their susceptibility to parasites. Such complex effects can impact each species within a community differently, which may benefit some species at the expense of others. As a result, an animal community affected by the combination of predators and parasites may look very different than a community affected by only one type of these natural enemies. This project will evaluate how echinostomes (a trematode parasite) and predators interact to affect larval frog (tadpole) communities in ponds. First, the susceptibility of different species of larval frogs to echinostome infection in the presence and absence of predators will be measured. Second, the interactive effects of predators and parasites on a simple community of larval frogs will be examined. An experiment in artificial ponds will demonstrate the extent to which parasite infection rates depend on the composition of the amphibian community and the presence of predators. The results will also reveal how the combination of infection and predator cues affects competition for resources among larval frogs. Finally, a field survey will suggest how these effects play out in natural ponds in Southeast Michigan. This research will thus provide new insights into complex mechanisms through which parasites and predators affect communities.

The outcome will be valuable from a conservation perspective because echinostomes are present at higher levels in areas associated with human impacts, such as pollution and urbanization. Because predators have a strong impact on amphibian communities, their interactions with parasites in these ponds will be particularly important to understand. Additionally, amphibians are a class of special concern because many populations are in decline globally, in part due to disease. This research will involve collaboration with local organizations, undergraduate students, K-12 organizations, and landowners, which will provide an excellent opportunity for public outreach and education.

Project Report

Both predators and parasites can have strong effects on animal populations and communities, although parasites have received relatively less attention. Furthermore, the combination of these natural enemies can have complex effects that may be difficult to predict. This project examined the interactive effects of predators and trematode parasites on larval frogs, focusing on one family (echinostomes) that infect tadpoles’ kidneys and can cause disease. Our project had four major components. First, in a series of artificial pond and aquarium experiments, we addressed how effects of direct predation and predator stress influence larval frog-echinostome host-parasite interactions. We observed that the combination of predators and echinostomes had synergistic effects on larval frog survival, driven primarily by an effect of echinostome infective stages on larval frog behavior that increases susceptibility to predators. Second, in another series of artificial pond and laboratory experiments, we addressed how predators and parasites jointly influence interactions among larval frogs in a simple community. We observed that the effects of predators influenced competitive interactions among larval frogs, and we also found that the effects of parasites depend on competitive context (i.e., tadpole density and food resources). In particular, we found that the effects of parasites on growth and survival depended on tadpole density. Third, in aquaria experiments, we compared the effects of predators and parasites across eight species of larval frogs, which provided insight into potential effects of these natural enemies on amphibian community structure and the evolutionary response of tadpoles to natural enemies. We found that species differed in their susceptibility and response to both parasites and predators, and these responses depended in part on traits (i.e., habitat use, development rate, and breeding time). Most notably, we found that species differences in habitat use likely influence their behavioral response to parasite infective stages, which likely affects parasite transmission. Finally, in a field survey and a field experiment, we measured echinostome infection in the field and examined the potential consequences for larval frog populations. Our results suggest that pond characteristics (i.e., the proportion of days that a pond is dry) and seasonality strongly influenced observed levels of parasite infection. Additionally, our results suggest that parasites may reduce larval amphibian survivorship in natural ponds to a greater extent than is typically appreciated. Overall, the results of our project demonstrate that the context of the host-parasite interaction (i.e., the presence of predators or competitors) matters greatly for the effects of parasites on hosts. Furthermore, our results suggest potentially important effects of community structure on parasite transmission, given differences among species in susceptibility across contexts. Our results further suggest that interactions observed at a small scale (i.e., aquaria or artificial pond) may contribute to observed patterns in the field. Finally, our results have important conservation implications, because echinostomes and other trematode parasites are associated with human activities, such as urbanization, pollution, and agriculture, and amphibian populations are in decline worldwide, in part due to disease. Our results inform our understanding of the overall consequences of higher parasite abundances and the effects of multiple stressors on amphibians. This research involved coordination with local landowners and government agencies and directly involved ten undergraduate researchers and one high school student, several of whom were members of underrepresented groups. The results of this research were shared and discussed with colleagues and undergraduates during guest lectures and departmental seminars at the University of Michigan, and with middle and high school students through programs such as the University of Michigan BioKIDS program and the Belle Isle BioBlitz. The results were also presented at the Ecological Society of America Annual Meeting and the Ecology and Evolution of Infectious Diseases conference.

Agency
National Science Foundation (NSF)
Institute
Division of Environmental Biology (DEB)
Type
Standard Grant (Standard)
Application #
1110137
Program Officer
Douglas Levey
Project Start
Project End
Budget Start
2011-07-01
Budget End
2013-06-30
Support Year
Fiscal Year
2011
Total Cost
$14,155
Indirect Cost
Name
University of Michigan Ann Arbor
Department
Type
DUNS #
City
Ann Arbor
State
MI
Country
United States
Zip Code
48109