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Research Article

Predator diversity, intraguild predation, and indirect effects drive parasite transmission

Jason R. Rohr, David J. Civitello, Patrick W. Crumrine, Neal T. Halstead, Andrew D. Miller, Anna M. Schotthoefer, Carl Stenoien, Lucinda B. Johnson, and Val R. Beasley
  1. aDepartment of Integrative Biology, University of South Florida, Tampa, FL 33620;
  2. bDepartments of Biological Sciences and Geography and Environment, Rowan University, Glassboro, NJ 08028;
  3. cDepartment of Geography and Environmental Systems, University of Maryland, Baltimore County, Baltimore, MD 21250;
  4. dMarshfield Clinic Research Foundation, Marshfield, WI 54449;
  5. eDepartment of Ecology Evolution and Behavior, University of Minnesota, St. Paul, MN 55108;
  6. fNatural Resources Research Institute, University of Minnesota Duluth, Duluth, MN 55811; and
  7. gDepartment of Veterinary and Biomedical Sciences, The Pennsylvania State University, University Park, PA 16802

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PNAS March 10, 2015 112 (10) 3008-3013; first published February 23, 2015; https://doi.org/10.1073/pnas.1415971112
Jason R. Rohr
aDepartment of Integrative Biology, University of South Florida, Tampa, FL 33620;
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  • For correspondence: jasonrohr@gmail.com
David J. Civitello
aDepartment of Integrative Biology, University of South Florida, Tampa, FL 33620;
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Patrick W. Crumrine
bDepartments of Biological Sciences and Geography and Environment, Rowan University, Glassboro, NJ 08028;
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Neal T. Halstead
aDepartment of Integrative Biology, University of South Florida, Tampa, FL 33620;
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Andrew D. Miller
cDepartment of Geography and Environmental Systems, University of Maryland, Baltimore County, Baltimore, MD 21250;
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Anna M. Schotthoefer
dMarshfield Clinic Research Foundation, Marshfield, WI 54449;
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Carl Stenoien
eDepartment of Ecology Evolution and Behavior, University of Minnesota, St. Paul, MN 55108;
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Lucinda B. Johnson
fNatural Resources Research Institute, University of Minnesota Duluth, Duluth, MN 55811; and
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Val R. Beasley
gDepartment of Veterinary and Biomedical Sciences, The Pennsylvania State University, University Park, PA 16802
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  1. Edited by Burton H. Singer, University of Florida, Gainesville, FL, and approved January 23, 2015 (received for review August 19, 2014)

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Significance

Humans are altering biodiversity globally and infectious diseases are on the rise; thus, there is considerable interest in understanding how changes to biodiversity affect disease risk. We show that the diversity of predators that consume parasites was the best negative predictor of infections in frogs, suggesting that predation on parasites can be an important mechanism of disease reduction. Follow-up experiments, field data, and mathematical models revealed that intraguild predators, predators that consume both hosts and parasites, decrease macroparasite infections per host less than predators that only consume parasites, representing a general trait of predators that predicts their ability to reduce disease. Consequently, managing assemblages of non-intraguild and intraguild predators is an underutilized tool to minimize human and wildlife diseases.

Abstract

Humans are altering biodiversity globally and infectious diseases are on the rise; thus, there is interest in understanding how changes to biodiversity affect disease. Here, we explore how predator diversity shapes parasite transmission. In a mesocosm experiment that manipulated predator (larval dragonflies and damselflies) density and diversity, non-intraguild (non-IG) predators that only consume free-living cercariae (parasitic trematodes) reduced metacercarial infections in tadpoles, whereas intraguild (IG) predators that consume both parasites and tadpole hosts did not. This likely occurred because IG predators reduced tadpole densities and anticercarial behaviors, increasing per capita exposure rates of the surviving tadpoles (i.e., via density- and trait-mediated effects) despite the consumption of parasites. A mathematical model demonstrated that non-IG predators reduce macroparasite infections, but IG predation weakens this “dilution effect” and can even amplify parasite burdens. Consistent with the experiment and model, a wetland survey revealed that the diversity of IG predators was unrelated to metacercarial burdens in amphibians, but the diversity of non-IG predators was negatively correlated with infections. These results are strikingly similar to generalities that have emerged from the predator diversity–pest biocontrol literature, suggesting that there may be general mechanisms for pest control and that biocontrol research might inform disease management and vice versa. In summary, we identified a general trait of predators—where they fall on an IG predation continuum—that predicts their ability to reduce infections and possibly pests in general. Consequently, managing assemblages of predators represents an underused tool for the management of human and wildlife diseases and pest populations.

  • biodiversity–ecosystem function
  • dilution effect
  • schistosomiasis
  • snail
  • trophic cascade

Footnotes

  • ↵1To whom correspondence should be addressed. Email: jasonrohr{at}gmail.com.
  • Author contributions: J.R.R., D.J.C., P.W.C., A.M.S., and V.R.B. designed research; J.R.R., D.J.C., P.W.C., N.T.H., A.D.M., A.M.S., C.S., L.B.J., and V.R.B. performed research; J.R.R. and D.J.C. contributed new reagents/analytic tools; J.R.R. and P.W.C. analyzed data; and J.R.R. and D.J.C. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1415971112/-/DCSupplemental.

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Intraguild predation and the dilution effect
Jason R. Rohr, David J. Civitello, Patrick W. Crumrine, Neal T. Halstead, Andrew D. Miller, Anna M. Schotthoefer, Carl Stenoien, Lucinda B. Johnson, Val R. Beasley
Proceedings of the National Academy of Sciences Mar 2015, 112 (10) 3008-3013; DOI: 10.1073/pnas.1415971112

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Intraguild predation and the dilution effect
Jason R. Rohr, David J. Civitello, Patrick W. Crumrine, Neal T. Halstead, Andrew D. Miller, Anna M. Schotthoefer, Carl Stenoien, Lucinda B. Johnson, Val R. Beasley
Proceedings of the National Academy of Sciences Mar 2015, 112 (10) 3008-3013; DOI: 10.1073/pnas.1415971112
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