Research Article

Divergent impacts of warming weather on wildlife disease risk across climates

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Science  20 Nov 2020:
Vol. 370, Issue 6519, eabb1702
DOI: 10.1126/science.abb1702

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Climate change alters disease risks

Climate change appears to be provoking changes in the patterns and intensity of infectious diseases. For example, when conditions are cool, amphibians from warm climates experience greater burdens of infection by chytrid fungus than hosts from cool regions. Cohen et al. undertook a global metanalysis of 383 studies to test whether this “thermal mismatch” hypothesis holds true over the gamut of host-pathogen relationships. The authors combined date and location data with a selection of host and parasite traits and weather data. In the resulting model, fungal disease risk increased sharply under cold abnormalities in warm climates, whereas bacterial disease prevalence increased sharply under warm abnormalities in cool climates. Warming is projected to benefit helminths more than other parasites, and viral infections showed less obvious relationships with climate change.

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Structured Abstract

INTRODUCTION

Infectious disease outbreaks among wildlife have surged in recent decades alongside global climate change. However, the circumstances under which climate change is most likely to promote or inhibit infectious disease remain unknown for several reasons. First, researchers know little about how climate change will alter disease risk across hosts and parasites with diverse life history traits (e.g., host thermal biology, habitat, and parasite transmission mode). Second, not all parasites will be affected by climate change, but it remains unclear how the relative risk of disease caused by bacteria, viruses, fungi, and helminths is changing. Third, impacts of temperature abnormalities and variability, rather than increasing mean temperatures alone, remain largely unexplored. Finally, it is not clear which regions of the globe may become more amenable to disease and which may become less suitable.

RATIONALE

Recently, the thermal mismatch hypothesis has emerged to predict how infection risk is affected by temperature across climate zones in an amphibian-disease system. This hypothesis suggests that hosts adapted to cooler and warmer climates should be at greatest risk of infection under abnormally warm and cool conditions, respectively, because smaller-bodied parasites are more likely to maintain performance over a wider range of temperatures than larger-bodied hosts but are limited by extreme conditions. However, thermal mismatches may not affect diverse hosts and parasites equally because wildlife host and parasite traits can greatly influence disease outcomes. For example, thermal mismatches might exert an especially strong influence over disease outcomes in ectothermic hosts because their immune responses are highly temperature-dependent.

To address this challenge, we examined how disease risk was affected by temperature for diverse wildlife hosts and parasites that vary in ecologically important traits across a worldwide climatic gradient. We amassed a global, spatiotemporal dataset describing parasite prevalence across 7346 wildlife populations and 2021 host-parasite combinations. Further, we compiled long-term climate records at each location and short-term weather records during each survey. Our modeling approach investigated how relationships between parasite prevalence and weather depend on local climate and host and parasite traits. Finally, we projected broad-scale changes in disease risk based on thermal mismatches and ensemble climate change model predictions.

RESULTS

We found that on average, hosts from cool and warm climates experienced increased disease risk at abnormally warm and cool temperatures, respectively, as predicted by the thermal mismatch hypothesis. This effect was greatest among hosts that are ectothermic and nonmigratory and among systems in which the parasite is directly transmitted (without vectors or intermediate hosts). However, the thermal mismatch effect was similar in terrestrial and freshwater systems. Projections based on climate change models indicate that ectothermic wildlife hosts from temperate and tropical zones may experience sharp increases and moderate reductions in disease risk, respectively, though the magnitude of these changes depends on parasite taxa. Prevalence of helminth parasites increased most in temperate zones, whereas fungal parasite prevalence decreased most in tropical zones.

CONCLUSION

Cold-adapted hosts may experience increasing disease risk during abnormally warm periods. Meanwhile, the risk to warm-adapted hosts may increase during cool periods and mildly decrease during warm periods. Further, these effects are dependent on the identity and traits of the parasite and the host. Our results highlight the complexity of the influences of climate change on diverse host-parasite dynamics, whereas our broad-scale predictions suggest contrasting impacts of climate change across climate zones and diverse parasites. As climate change accelerates, hosts adapted to cooler or milder climates may suffer increasing risk of infectious disease outbreaks, whereas those adapted to warmer climates could see mild reductions in infectious disease risk.

The thermal mismatch hypothesis.

Predicted patterns of thermal host and parasite performance in isolation (top, left and right) versus patterns of host-parasite interactions (bottom, left and right). Because smaller organisms generally have broader thermal performance curves in isolation than larger organisms, peak parasite growth on hosts is likely at temperatures at which host performance is poor (arrows in top left and top right; curves in bottom left and bottom right). Cold-adapted hosts (left, top and bottom) and warm-adapted hosts (right, top and bottom) should thus experience maximal parasite growth at relatively warm and cool temperatures, respectively. Shaded areas span intermediate temperatures over which relationships between temperature and parasite performance on host are likely to be approximately linear.

Abstract

Disease outbreaks among wildlife have surged in recent decades alongside climate change, although it remains unclear how climate change alters disease dynamics across different geographic regions. We amassed a global, spatiotemporal dataset describing parasite prevalence across 7346 wildlife populations and 2021 host-parasite combinations, compiling local weather and climate records at each location. We found that hosts from cool and warm climates experienced increased disease risk at abnormally warm and cool temperatures, respectively, as predicted by the thermal mismatch hypothesis. This effect was greatest in ectothermic hosts and similar in terrestrial and freshwater systems. Projections based on climate change models indicate that ectothermic wildlife hosts from temperate and tropical zones may experience sharp increases and moderate reductions in disease risk, respectively, though the magnitude of these changes depends on parasite identity.

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