Abstract
Trematodes are ubiquitous members of aquatic environments, have many functional roles in ecosystems, and can cause diseases in humans, livestock, and wild animals. Despite their importance and reports of parasite population declines, few studies have concurrently assessed the effects of aquatic contaminants on multiple hosts, multiple parasite life cycle stages, and on transmission-related host-parasite interactions. Here, we test the effects of environmentally relevant concentrations of the herbicide atrazine (0, 3, 30 μg/L) on the establishment and development of an amphibian trematode (Halipegus eccentricus) in a first-intermediate snail host (Physa acuta) and in a second-intermediate ostracod host (Cypridopsis sp.). Additionally, we test the interactive effects of atrazine and parasitism on snail and ostracod survival. Our results indicate that atrazine negatively affects trematode transmission by altering snail and ostracod host-parasite interactions. Although atrazine did not affect the survival of uninfected snails alone, atrazine acted synergistically with parasitism to reduce the longevity of infected snails. As a result, the number of cercariae (i.e., larval trematodes) produced by snails was 50.7 % (3 μg/L) and 14.9 % (30 μg/L) relative to controls. Atrazine exhibited direct negative effects on ostracod survival at 30 μg/L. However, when ostracods were also exposed to trematodes, the negative effects of atrazine on survival were diminished. Although infected ostracod survival remained high, trematode development was significantly reduced, resulting in reduced infectivity of metacercariae (i.e., nongravid adult cysts infective to definite host) to 32.2 % (3 μg/L) and 28.6 % (30 μg/L) relative to the controls. The combination of reduced cercaria production and reduced metacercarial infectivity in the 3 and 30 μg/L atrazine treatment groups reduced the net number of infective worms produced to 16.4 and 4.3 % (respectively) relative to the control. These results demonstrate the complex nature of pesticide effects on trematode infections and indicate that trematodes can affect their first- and second-intermediate hosts differently under different pesticide concentrations. Our work has broad implications for parasite transmission and conservation and provides a testable mechanism for understanding trematode population declines in contaminated wetlands.
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Acknowledgments
We thank Cedar Point Biological Station for laboratory space during our collections of bullfrogs. Additionally, we thank two anonymous reviewers for improving the manuscript.
Funding
This project was partially funded by two Southwestern Association of Parasitologists student research grants, one American Society of Parasitologists student research grant, a National Academy of Sciences Ford Foundation Dissertation Fellowship awarded to KDG, and by a National Science Foundation grant (DEB-0949951) awarded to MGB.
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Gustafson, K.D., Belden, J.B. & Bolek, M.G. Atrazine reduces the transmission of an amphibian trematode by altering snail and ostracod host-parasite interactions. Parasitol Res 115, 1583–1594 (2016). https://doi.org/10.1007/s00436-015-4893-1
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DOI: https://doi.org/10.1007/s00436-015-4893-1