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Seasonal dynamics and potential drivers of ranavirus epidemics in wood frog populations

Abstract

Epidemics in wildlife populations often display a striking seasonality. Ranaviruses can cause rapid, synchronous mass mortality events in populations of wood frog (Rana sylvatica) larvae in the summer. While there are several possible explanations for this pattern—from seasonal introductions of the virus to environmental stressors to windows of susceptibility to mortality from infection during development—most studies have focused on single factors in laboratory settings. We characterized the time course of ranavirus epidemics in eight ephemeral ponds in Connecticut, USA, measuring the prevalence and intensity of infections in wood frog larvae and Ranavirus DNA in water samples using environmental DNA methods. We found little evidence that the timing of pathogen introduction affected the timing of epidemics (rising prevalence) or the resulting die-offs. Instead, we observed a pulse in transmission asynchronous with die-offs; prevalence reached high levels (≥ 50%) up to 6 weeks before mortality was observed, suggesting that die-offs may be uncoupled from this pulse in transmission. Rather, mortality occurred when larvae reached later stages of development (hind limb formation) and coinciding water temperatures rose (≥ 15 °C), both of which independently increase pathogenicity (i.e., probability of host mortality) of infections in laboratory experiments. In summary, the strong seasonality of die-offs appears to be driven by development- and/or temperature-dependent changes in pathogenicity rather than occurring chronologically with pathogen introduction, after a pulse in transmission, or when susceptible host densities are greatest. Furthermore, our study illustrates the potential for eDNA methods to provide valuable insight in aquatic host–pathogen systems.

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Acknowledgements

This publication was developed under STAR Fellowship Assistance Agreement no. 91767901 awarded by the U.S. Environmental Protection Agency (EPA) to EMH. It has not been formally reviewed by EPA. The views expressed in this publication are solely those of E. M. Hall and co-authors, and EPA does not endorse any products or commercial services mentioned in this publication. This work was also funded by the Washington State University Elling Foundation. We would like to graciously thank A. Helton lab from University of Connecticut (Storrs, CT) for processing biogeochemical water samples. We are grateful for constructive feedback from P. Johnson and anonymous reviewers.

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Contributions

EMH, CSG, JLB, and EJC designed the experiment. EMH performed field work and processed samples. EMH and JLB analyzed data, and everyone contributed to writing the manuscript.

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Correspondence to Emily M. Hall.

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Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed. This research was approved by the Animal Care and Use Committee (Protocol #04520-001) of Washington State University. Collections were approved by the Connecticut Department of Energy and Environmental Protection (Scientific collections permit #1115003) and Yale Myers Forest.

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The authors declare that they have no conflict of interest.

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All data generated or analyzed during this study are included in this published article and its supplementary information files.

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Communicated by Pieter Johnson.

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Hall, E.M., Goldberg, C.S., Brunner, J.L. et al. Seasonal dynamics and potential drivers of ranavirus epidemics in wood frog populations. Oecologia 188, 1253–1262 (2018). https://doi.org/10.1007/s00442-018-4274-4

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  • DOI: https://doi.org/10.1007/s00442-018-4274-4

Keywords

  • Seasonal epidemiology
  • Ranavirus
  • Amphibian
  • Disease susceptibility
  • Environmental DNA