Life-History Trade-Offs Influence Disease in Changing Climates: Strategies of an Amphibian Pathogen

Abstract

Life-history trade-offs allow many animals to maintain reproductive fitness across a range of climatic conditions. When used by parasites and pathogens, these strategies may influence patterns of disease in changing climates. The chytrid fungus, Batrachochytrium dendrobatidis, is linked to global declines of amphibian populations. Short-term growth in culture is maximal at 17 degrees-25 degrees C. This has been used in an argument that global warming, which increases the time that amphibians spend at these temperatures in cloud-covered montane environments, has led to extinctions. Here we show that the amphibian chytrid responds to decreasing temperatures with trade-offs that increase fecundity as maturation rate slows and increase infectivity as growth decreases. At 17 degrees-25 degrees C, infectious zoospores encyst (settle and develop a cell wall) and develop into the zoospore-producing stage (zoosporangium) faster, while at 7 degrees-10 degrees C, greater numbers of zoospores are produced per zoosporangium; these remain infectious for a longer period of time. We modeled the population growth of B. dendrobatidis through time at various temperatures using delayed differential equations and observational data for four parameters: developmental rate of thalli, fecundity, rate of zoospore encystment, and rate of zoospore survival. From the models, it is clear that life-history trade-offs allow B. dendrobatidis to maintain a relatively high long-term growth rate at low temperatures, so that it maintains high fitness across a range of temperatures. When a seven-day cold shock is simulated, the outcome is intermediate between the two constant temperature regimes, and in culture, a sudden drop in temperature induces zoospore release. These trade-offs can be ecologically important for a variety of organisms with complex life histories, including pathogenic microorganisms. The effect of temperature on amphibian mortality will depend on the interaction between fungal growth and host immune function and will be modified by host ecology, behavior, and life history. These results demonstrate that B. dendrobatidis populations can grow at high rates across a broad range of environmental temperatures and help to explain why it is so successful in cold montane environments.

Temperature variability and moisture synergistically interact to exacerbate an epizootic disease

“…These results are consistent with previous studies showing that Bd loads frequently correlate with precipitation patterns in the field, probably because Bd is an aquatic pathogen requiring water for zoospore dispersal [11 -13]. Our results are also consistent with previous experiments showing greater mortality due to infection and Bd abundance on frogs at lower temperatures [10,35,36], despite Bd growth in culture generally increasing with temperature up to a maximum growth temperature of approximately 238C [11, 37,38]. This might be because amphibian immune responses are stronger at higher temperatures, such that the temperature-dependence of infection depends on the relative rates at which parasite infectivity and host resistance increase with temperature [8].…”

Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease

“…Potential increases in host susceptibility with drops in temperature are of particular concern for Bd epidemics because decreases in temperature might benefit this relatively cold-tolerant pathogen (22,32,38). In addition, drops in temperature are also thought to stimulate the release of Bd zoospores (39). Hence, several lines of evidence suggest that temperature variability might be important in Bd outbreaks and related mass mortality events.…”

“…We suspect that, to thoroughly understand climatic effects on Bd-related declines, investigators will need to explicitly test how climate affects interactions between Bd and amphibian hosts, as well as consider other factors altering host-parasite dynamics or host fitness directly (39,(42)(43)(44). Additionally, the influence of climate on amphibians will almost certainly depend on the local scales at which organisms experience climatic conditions.…”

Global Amphibian Extinction Risk Assessment for the Panzootic Chytrid Fungus

“…Furthermore, the pathogen is known to be particularly temperature and moisture dependent [e.g., 9,10]. The in vitro growth optimum of Bd is at 17-25 °C, whereas temperatures higher than 29 °C, freezing and desiccation are lethal [11], findings that are supported by observations in the field [12][13][14][15][16].…”