Temperature drives epidemics in a zooplankton-fungus disease system: A trait-driven approach points to transmission via host foraging

Marta S. Shocket, Alexander T. Strauss, Jessica L. Hite, Maja Šljivar, David J. Civitello, Meghan A. Duffy, Carla E. Cáceres, Spencer R. Hall

Research output: Contribution to journalArticlepeer-review

17 Scopus citations

Abstract

Climatic warming will likely have idiosyncratic impacts on infectious diseases, causing some to increase while others decrease or shift geographically. A mechanistic framework could better predict these different temperature-disease outcomes. However, such a framework remains challenging to develop, due to the nonlinear and (some-times) opposing thermal responses of different host and parasite traits and due to the difficulty of validating model predictions with observations and experiments. We address these challenges in a zooplankton-fungus (Daphnia dentifera–Metschnikowia bicuspidata) system. We test the hypothesis that warmer temperatures promote disease spread and produce larger epidemics. In lakes, epidemics that start earlier and warmer in autumn grow much larger. In a mesocosm experiment, warmer temperatures produced larger epidemics. A mechanistic model parameterized with trait assays revealed that this pattern arose primarily from the temperature dependence of transmission rate (β), governed by the increasing foraging (and, hence, parasite exposure) rate of hosts (f). In the trait assays, parasite production seemed sufficiently responsive to shape epidemics as well; however, this trait proved too thermally insensitive in the mesocosm experiment and lake survey to matter much. Thus, in warmer environments, increased foraging of hosts raised transmission rate, yielding bigger epidemics through a potentially general, exposure-based mechanism for ectotherms. This mechanistic approach highlights how a trait-based framework will enhance predictive insight into responses of infectious disease to a warmer world.

Original languageEnglish (US)
Pages (from-to)435-451
Number of pages17
JournalAmerican Naturalist
Volume191
Issue number4
DOIs
StatePublished - Apr 2018

Bibliographical note

Funding Information:
K. Boatman assisted with 2009 and 2010 field sampling, Z. Brown assisted with 2011 field sampling, and A. Bowling assisted with 2014 field sampling. S. Siscoe, R. Ronk, B. Feaster, and T. Stoelting at the Indiana Department of Natural Resources facilitated the field survey. A. Magnante assisted with the mesocosm experiment. Thanks to J. Kruschke, T. E. X. Miller, and the Enhancing Linkages between Math and Ecology program at Michigan State University for advice and instruction on Bayesian inference. A.T.S. and M.S.S. were supported by the National Science Foundation’s (NSF) Graduate Research Fellowship Program. D.J.C. and J.L.H. were supported by Environmental Protection Agency Science to Achieve Results fellowships. This work was supported in part by the NSF Department of Environmental Biology (grants 0841679, 0841817, 1120316, 1120804, 1353749, 1353806, and 1354407). Statement of authorship: M.S.S., S.R.H., C.E.C., and M.A.D. designed the study. M.S.S., A.T.S., J.L.H., M.Š., and D.J.C. collected data. M.S.S. performed analyses. M.S.S. wrote the first draft of the manuscript, and all authors contributed to revisions.

Funding Information:
B. Feaster, and T. Stoelting at the Indiana Department of Natural Resources facilitated the field survey. A. Magnante assisted with the mesocosm experiment. Thanks to J. Kruschke, T. E. X. Miller, and the Enhancing Linkages between Math and Ecology program at Michigan State University for advice and instruction on Bayesian inference. A.T.S. and M.S.S. were supported by the National Science Foundation’s (NSF) Graduate Research Fellowship Program. D.J.C. and J.L.H. were supported by Environmental Protection Agency Science to Achieve Results fellowships. This work was supported in part by the NSF Department of Environmental Biology (grants 0841679, 0841817, 1120316, 1120804, 1353749, 1353806, and 1354407).

Keywords

  • Daphnia
  • Fungal disease
  • Infectious disease
  • Metschnikowia
  • Temperature
  • Transmission rate

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