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Ranavirus could facilitate local extinction of rare amphibian species

  • Conservation ecology – original research
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Abstract

There is growing evidence that pathogens play a role in population declines and species extinctions. For small populations, disease-induced extinction may be especially probable. We estimated the susceptibility of two amphibian species of conservation concern (the dusky gopher frog [Lithobates sevosus] and boreal toad [Anaxyrus boreas boreas]) to an emerging pathogen (ranavirus) using laboratory challenge experiments, and combined these data with published demographic parameter estimates to simulate the potential effects of ranavirus exposure on extinction risk. We included effects of life stage during pathogen exposure, pathogen exposure interval, hydroperiod of breeding habitat, population carrying capacity, and immigration in simulations. We found that both species were highly susceptible to ranavirus when exposed to the pathogen in water at environmentally relevant concentrations. Dusky gopher frogs experienced 100 % mortality in four of six life stages tested. Boreal toads experienced 100 % mortality when exposed as tadpoles or metamorphs, which were the only life stages tested. Simulations showed population declines, greater extinction probability, and faster times to extinction with ranavirus exposure. These effects were more evident with more frequent pathogen exposure intervals and lower carrying capacity. Immigration at natural rates did little to mitigate effects of ranavirus exposure unless immigration occurred every 2 years. Our results demonstrate that disease-induced extinction by emerging pathogens, such as ranavirus, is possible, and that threat may be especially high for species with small population sizes. For the species in this study, conservation organizations should incorporate ranavirus surveillance into monitoring programs and devise intervention strategies in the event that disease outbreaks occur.

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Acknowledgments

Funding for this research was provided by the University of Tennessee Institute of Agriculture (UTIA) and for the dusky gopher frog challenges by the Morris Animal Foundation (Grant #D14ZO-055). We thank Bobby Simpson and Roger Long with the UTIA East Tennessee Research and Education Center for providing laboratory space and logistical support. This work was partially conducted while a Postdoctoral Fellow (JEE) at the National Institute for Mathematical and Biological Synthesis, an Institute sponsored by the National Science Foundation, the US Department of Homeland Security, and the US Department of Agriculture through NSF Award #EF-0832858, with additional support from The University of Tennessee, Knoxville. Further postdoctoral support (JEE) was provided by the South Central Climate Science Center. The authors would like to thank the Institute of Museum and Library Services (IMLS) National Leadership Grant LG-25-09-0064-09, for funding the research that produced the captive-bred Mississippi Gopher Frogs and Boreal Toads. Finally, we thank David Lesbarrères and two anonymous referees for comments that improved our manuscript. Laboratory research was approved under the University of Tennessee IACUC protocol #2140 and USFWS permit #TE171493-0 (dusky gopher frogs).

Author contribution statement

JEE and MJG conceived the study and led analyses and manuscript writing, JCC, WBS, and CEL performed the laboratory experiments, AJK, CL, and JK propagated the animals for the experiments, RPW replicated and titrated the virus, RDH and DLM lead the qPCR and histopathology, and all authors contributed to manuscript revision.

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Author notes

  1. Andrew J. Kouba

    Present address: Department of Wildlife, Fisheries, and Aquaculture, Mississippi State University, Starkville, MS, 39762, USA

Authors and Affiliations

  1. Department of Natural Resource Ecology and Management, Oklahoma State University, Stillwater, OK, 74078, USA

    Julia E. Earl

  2. Center for Wildlife Health, Department of Forestry, Wildlife and Fisheries, University of Tennessee, Knoxville, TN, 37996, USA

    Jordan C. Chaney, Carson E. Lillard, Rachel D. Hill, Debra L. Miller & Matthew J. Gray

  3. Department of Agricultural and Environmental Sciences, Tennessee State University, Nashville, TN, 37209, USA

    William B. Sutton

  4. Conservation and Research Department, Memphis Zoological Society, Memphis, TN, 38112, USA

    Andrew J. Kouba

  5. Department of Biochemistry and Molecular Biology, Mississippi State University, Starkville, MS, 39762, USA

    Cecilia Langhorne

  6. Omaha’s Henry Doorly Zoo and Aquarium, Omaha, NE, 68107, USA

    Jessi Krebs

  7. Department of Biomedical and Diagnostic Sciences, University of Tennessee College of Veterinary Medicine, University of Tennessee, Knoxville, TN, 37996, USA

    Rebecca P. Wilkes & Debra L. Miller

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  1. Julia E. Earl
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Correspondence to Julia E. Earl.

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Communicated by Pieter Johnson.

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Earl, J.E., Chaney, J.C., Sutton, W.B. et al. Ranavirus could facilitate local extinction of rare amphibian species. Oecologia 182, 611–623 (2016). https://doi.org/10.1007/s00442-016-3682-6

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