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Disease and thermal acclimation in a more variable and unpredictable climate


Global climate change is shifting the distribution of infectious diseases of humans and wildlife with potential adverse consequences for disease control1,2,3,4. As well as increasing mean temperatures, climate change is expected to increase climate variability5,6, making climate less predictable. However, few empirical or theoretical studies have considered the effects of climate variability or predictability on disease, despite it being likely that hosts and parasites will have differential responses to climatic shifts6,7. Here we present a theoretical framework for how temperature variation and its predictability influence disease risk by affecting host and parasite acclimation responses. Laboratory experiments conducted in 80 independent incubators, and field data on disease-associated frog declines in Latin America6, support the framework and provide evidence that unpredictable temperature fluctuations, on both monthly and diurnal timescales, decrease frog resistance to the pathogenic chytrid fungus Batrachochytrium dendrobatidis. Furthermore, the pattern of temperature-dependent growth of the fungus on frogs was opposite to the pattern of growth in culture, emphasizing the importance of accounting for the host–parasite interaction when predicting climate-dependent disease dynamics. If similar acclimation responses influence other host–parasite systems, as seems likely, then present models, which generally ignore small-scale temporal variability in climate7, might provide poor predictions for climate effects on disease.

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Figure 1: Graphical representation of the temperature variability hypothesis.
Figure 2: Evidence for increased susceptibility to infection following a shift in temperature.
Figure 3: Effects of random and diurnal temperature variation on B. dendrobatidis growth and frog mortality in the diurnal temperature experiment.

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  1. Lafferty, K. D. The ecology of climate change and infectious diseases. Ecology 90, 888–900 (2009).

    Article  Google Scholar 

  2. Patz, J. A., Campbell-Lendrum, D., Holloway, T. & Foley, J. A. Impact of regional climate change on human health. Nature 438, 310–317 (2005).

    Article  CAS  Google Scholar 

  3. Rohr, J. R. et al. Frontiers in climate change-disease research. Trends Ecol. Evol. 26, 270–277 (2011).

    Article  Google Scholar 

  4. Harvell, C. D. et al. Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162 (2002).

    Article  CAS  Google Scholar 

  5. Easterling, D. R. et al. Climate extremes: Observations, modeling, and impacts. Science 289, 2068–2074 (2000).

    Article  CAS  Google Scholar 

  6. Rohr, J. R. & Raffel, T. R. Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. Proc. Natl Acad. Sci. USA 107, 8269–8274 (2010).

    Article  CAS  Google Scholar 

  7. Paaijmans, K. P. et al. Influence of climate on malaria transmission depends on daily temperature variation. Proc. Natl Acad. Sci. USA 107, 15135–15139 (2010).

    Article  CAS  Google Scholar 

  8. Tabachnick, W. J. Challenges in predicting climate and environmental effects on vector-borne disease episystems in a changing world. J. Exp. Biol. 213, 946–954 (2010).

    Article  CAS  Google Scholar 

  9. Schar, C. et al. The role of increasing temperature variability in European summer heatwaves. Nature 427, 332–336 (2004).

    Article  Google Scholar 

  10. Yeh, S. W. et al. El Niño in a changing climate. Nature 461, 511–514 (2009).

    Article  CAS  Google Scholar 

  11. Fargues, J. & Luz, C. Effects of fluctuating moisture and temperature regimes on the infection potential of Beauveria bassiana for Rhodnius prolixus. J. Invertebr. Pathol. 75, 202–211 (2000).

    Article  CAS  Google Scholar 

  12. Stireman, J. O. et al. Climatic unpredictability and parasitism of caterpillars: Implications of global warming. Proc. Natl Acad. Sci. USA 102, 17384–17387 (2005).

    Article  CAS  Google Scholar 

  13. Zhou, G., Minakawa, N., Githeko, A. K. & Yan, G. Y. Association between climate variability and malaria epidemics in the East African highlands. Proc. Natl Acad. Sci. USA 101, 2375–2380 (2004).

    Article  CAS  Google Scholar 

  14. Jiang, L. & Morin, P. J. Temperature fluctuation facilitates coexistence of competing species in experimental microbial communities. J. Anim. Ecol. 76, 660–668 (2007).

    Article  Google Scholar 

  15. Knapp, A. K. et al. Rainfall variability, carbon cycling, and plant species diversity in a mesic grassland. Science 298, 2202–2205 (2002).

    Article  CAS  Google Scholar 

  16. Paaijmans, K. P., Read, A. F. & Thomas, M. B. Understanding the link between malaria risk and climate. Proc. Natl Acad. Sci. USA 106, 13844–13849 (2009).

    Article  CAS  Google Scholar 

  17. Angilletta, M. J. Thermal Adaptation: A Theoretical and Empirical Synthesis (Oxford Univ. Press, 2009).

    Book  Google Scholar 

  18. Plytycz, B. & Jozkowicz, A. Differential effects of temperature on macrophages of ectothermic vertebrates. J. Leukocyte Biol. 56, 729–731 (1994).

    Article  Google Scholar 

  19. Raffel, T. R., Rohr, J. R., Kiesecker, J. M. & Hudson, P. J. Negative effects of changing temperature on amphibian immunity under field conditions. Funct. Ecol. 20, 819–828 (2006).

    Article  Google Scholar 

  20. Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001).

    Article  CAS  Google Scholar 

  21. Wake, D. B. & Vredenburg, V. T. Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc. Natl Acad. Sci. USA 105, 11466–11473 (2008).

    Article  CAS  Google Scholar 

  22. Woodhams, D. C., Alford, R. A., Briggs, C. J., Johnson, M. & Rollins-Smith, L. A. Life-history trade-offs influence disease in changing climates: Strategies of an amphibian pathogen. Ecology 89, 1627–1639 (2008).

    Article  Google Scholar 

  23. Longcore, J. E., Pessi, A. P. & Nichols, D. K. Batrachochytrium dendrobatidisgen et sp nov, a chytrid pathogenic to amphibians. Mycologia 91, 219–227 (1999).

    Article  Google Scholar 

  24. Carey, C. et al. Experimental exposures of boreal toads (Bufo boreas) to a pathogenic chytrid fungus (Batrachochytrium dendrobatidis). EcoHealth 3, 5–21 (2006).

    Article  Google Scholar 

  25. Kriger, K. M. & Hero, J. M. Large-scale seasonal variation in the prevalence and severity of chytridiomycosis. J. Zool. 271, 352–359 (2007).

    Google Scholar 

  26. Retallick, R. W. R., McCallum, H. & Speare, R. Endemic infection of the amphibian chytrid fungus in a frog community post-decline. PLoS Biol. 2, 1965–1971 (2004).

    Article  CAS  Google Scholar 

  27. Rohr, J. R., Raffel, T. R., Romansic, J. M., McCallum, H. & Hudson, P. J. Evaluating the links between climate, disease spread, and amphibian declines. Proc. Natl Acad. Sci. USA 105, 17436–17441 (2008).

    Article  CAS  Google Scholar 

  28. Salichos, L. & Rokas, A. The diversity and evolution of circadian clock proteins in fungi. Mycologia 102, 269–278 (2010).

    Article  CAS  Google Scholar 

  29. Terblanche, J. S. & Chown, S. L. The relative contributions of developmental plasticity and adult acclimation to physiological variation in the tsetse fly, Glossina pallidipes (Diptera, Glossinidae). J. Exp. Biol. 209, 1064–1073 (2006).

    Article  Google Scholar 

  30. Kuris, A. M. et al. Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515–518 (2008).

    Article  CAS  Google Scholar 

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Thanks to A. Blaustein, P. Hudson and members of the Rohr lab for thoughts on this paper, M. McGarrity for assisting with frog collections, V. Vasquez for providing the B. dendrobatidis isolate, M. McCoy for suggesting zero-inflated negative binomial regression, C. Steffan for technical assistance and undergraduate assistants for assisting with experiments: J. Guirguis, L. Garibova, C. Hall, D. Marante, L. Caicedo, D. Bradberry, M. Chawdry, C. Kobasa, J. Hudson, P. Michel, J. Heet, A. Makhijani, L. Domaradzki, S. Agaj, H. Dorling, E. Esterrich, J. Waldman, D. Litowchak, M. Derakhshan, R. Rai, A. Drennen, T. Pham, P. Michel, D. Litowchak, A. Congelosi, N. Donn, M. Mancao and E. Sites. Financial support came from the National Science Foundation (NSF; DEB-0809487) and US Department of Agriculture (NRI 2008-00622 and 2008-01785) grants to J.R.R., a US Environmental Protection Agency STAR (R83-3835) grant to J.R.R. and T.R.R, an EPA CAREER (no. 83518801) grant to J.R.R. and a NSF grant to T.R.R. and P. T. Johnson (IOS-1121529). This work has not been subjected to review by these agencies providing financial support and therefore does not necessarily reflect the views of, or official endorsement by, these agencies.

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T.R.R. and J.R.R. should be considered joint first authors of this work. T.R.R. conducted mathematical modelling and statistical analyses. T.R.R. and J.R.R. conceived the experiments and obtained financial support. J.R.R. compiled field data. All authors assisted with writing the manuscript and with design and execution of the experiments.

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Correspondence to Thomas R. Raffel.

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Raffel, T., Romansic, J., Halstead, N. et al. Disease and thermal acclimation in a more variable and unpredictable climate. Nature Clim Change 3, 146–151 (2013).

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