Using Metabolic Theory to Describe Temperature and Thermal Acclimation Effects on Parasitic Infection.

AbstractPredicting temperature effects on species interactions can be challenging, especially for parasitism, where it is difficult to experimentally separate host and parasite thermal performance curves. Prior authors proposed a possible solution based on the metabolic theory of ecology (MTE), using MTE-based equations to describe the thermal mismatch between host and parasite performance curves and account for thermal acclimation responses. Here, we use published infection data, supplemented with experiments measuring metabolic responses to temperature in each species, to show that this modeling framework can successfully describe thermal acclimation effects on two different stages of infection in a tadpole-trematode system. All thermal acclimation effects on host performance manifested as changes in one key model parameter (activation energy), with measurements of host respiration generating similar MTE parameter estimates and acclimation effects compared with measurements of the host's ability to clear encysted parasites. This result suggests that metabolic parameter estimates for whole-body metabolism can sometimes be used to estimate temperature effects on host and parasite performance curves. However, we found different thermal patterns for measurements of host prevention of initial parasite encystment emphasizing potential challenges when applying MTE-based models to complex parasite-host systems with multiple distinct stages of infection.

Once a reservoir, always a reservoir? Seasonality affects the pathogen maintenance potential of amphibian hosts.

Host species that can independently maintain a pathogen in a host community and contribute to infection in other species are important targets for disease management. However, the potential of host species to maintain a pathogen is not fixed over time, and an important challenge is understanding how within- and across-season variability in host maintenance potential affects pathogen persistence over longer time scales relevant for disease management (e.g., years). Here, we sought to understand the causes and consequences of seasonal infection dynamics in leopard frogs (Rana sphenocephala and Rana pipiens) infected with the fungal pathogen Batrachochytrium dendrobatidis (Bd). We addressed three questions broadly applicable to seasonal host-parasite systems. First, to what degree are observed seasonal patterns in infection driven by temperature-dependent infection processes compared to seasonal host demographic processes? Second, how does seasonal variation in maintenance potential affect long-term pathogen persistence in multi-host communities? Third, does high deterministic maintenance potential relate to the long-term stochastic persistence of pathogens in host populations with seasonal infection dynamics? To answer these questions, we used field data collected over 3 years on >1400 amphibians across four geographic locations, laboratory and mesocosm experiments, and a novel mathematical model. We found that the mechanisms that drive seasonal prevalence were different from those driving seasonal infection intensity. Seasonal variation in Bd prevalence was driven primarily by changes in host contact rates associated with breeding migrations to and from aquatic habitat. In contrast, seasonal changes in infection intensity were driven by temperature-induced changes in Bd growth rate. Using our model, we found that the maintenance potential of leopard frogs varied significantly throughout the year and that seasonal troughs in infection prevalence made it unlikely that leopard frogs were responsible for long-term Bd persistence in these seasonal amphibian communities, highlighting the importance of alternative pathogen reservoirs for Bd persistence. Our results have broad implications for management in seasonal host-pathogen systems, showing that seasonal changes in host and pathogen vital rates, rather than the depletion of susceptible hosts, can lead to troughs in pathogen prevalence and stochastic pathogen extirpation.

Thermal acclimation has little effect on tadpole resistance to Batrachochytrium dendrobatidis.

Given that climate change is predicted to alter patterns of temperature variability, it is important to understand how shifting temperatures might influence species interactions, including parasitism. Predicting thermal effects on species interactions is complicated, however, because the temperature-dependence of the interaction depends on the thermal responses of both interacting organisms, which can also be influenced by thermal acclimation, a process by which organisms adjust their physiologies in response to a temperature change. We tested for thermal acclimation effects on Lithobates clamitans tadpole susceptibility to the fungus Batrachochytrium dendrobatidis (Bd) by acclimating tadpoles to 1 of 3 temperatures, moving them to 1 of 5 performance temperatures at which we exposed them to Bd, and measuring Bd loads on tadpoles post-exposure. We predicted that (1) tadpole Bd load would peak at a lower temperature than the temperature for peak Bd growth in culture, and (2) tadpoles acclimated to intermediate temperatures would have overall lower Bd loads across performance temperatures than cold- or warm-acclimated tadpoles, similar to a previously published pattern describing tadpole resistance to trematode metacercariae. Consistent with our first prediction, Bd load on tadpoles decreased with increasing performance temperature. However, we found only weak support for our second prediction, as acclimation temperature had little effect on tadpole Bd load. Our results contribute to a growing body of work investigating thermal responses of hosts and parasites, which will aid in developing methods to predict the temperature-dependence of disease.

Thermal Performance Curves and the Metabolic Theory of Ecology-A Practical Guide to Models and Experiments for Parasitologists.

Climate change will affect host-parasite dynamics in complex ways. The development of forecast models is necessary for proactive disease management, but past studies have frequently reported thermal performance data in idiosyncratic ways that have limited use for parameterizing thermal host-parasite models. Development of improved forecast models will require strong collaborations between experimental parasitologists and disease modelers. The purpose of this article is to facilitate such collaborations by reviewing practical considerations for describing thermal performance curves of parasite and host performance traits, and using them to predict climate change impacts on host-parasite systems. In the first section, we provide an overview of how thermal performance curves can be embedded in life-cycle-based dynamical models of parasitism, and we outline how such models can capture the net effect of multiple nonlinear temperature dependencies affecting the host-parasite dynamics. We also discuss how macroecological generalities based on the metabolic theory of ecology (MTE) can be used to determine a priori parameter estimates for thermal performance curves to derive null models for data-deficient species, but we note that most of the generalities suggested by MTE remain to be tested for parasites. In the second section, we discuss empirical knowledge gaps for the temperature dependence of parasite and host performance traits, and we outline the types of data that need to be collected to inform MTE-based models for data-deficient species. We specifically emphasize the importance of (1) capturing the entire thermal response of performance traits, including lower and upper temperature thresholds, and (2) experimentally or statistically separating out the thermal responses of different performance traits (e.g., development and mortality) rather than only reporting composite measures (e.g., apparent development). Not adhering to these principles can lead to biased climate change impact predictions. In the third section, we provide a practical guide outlining how experimentalists can contribute to fill data gaps by measuring the temperature dependence of host and parasite performance traits in ways that are systematic, statistically rigorous, and consistent with the requirements of life cycle-based host-parasite models. This guide includes recommendations and practical examples illustrating (1) the use of perturbation analyses to determine experimental priorities, (2) experimental design tips for quantifying thermal response curves, and (3) statistical methods for estimating the parameters of thermal performance curves. Our hope is that this article helps researchers to maximize the value and use of future data collections for both empirical and modelling studies investigating the way in which temperature influences parasitism.

Bottom-up and trait-mediated effects of resource quality on amphibian parasitism.

Leaf litter subsidies are important resources for aquatic consumers like tadpoles and snails, causing bottom-up effects on wetland ecosystems. Recent studies have shown that variation in litter nutritional quality can be as important as litter quantity in driving these bottom-up effects. Resource subsidies likely also have indirect and trait-mediated effects on predation and parasitism, but these potential effects remain largely unexplored. We generated predictions for differential effects of litter nutrition and secondary polyphenolic compounds on tadpole (Lithobates sylvatica) exposure and susceptibility to Ribeiroia ondatrae, based on ecological stoichiometry and community-ecology theory. We predicted direct and indirect effects on key traits of the tadpole host (rates of growth, development and survival), the trematode parasite (production of the cercaria infective stages) and the parasite's snail intermediate host (growth and reproduction). To test these predictions, we conducted a large-scale mesocosm experiment using a natural gradient in the concentrations of nutrients (nitrogen) and toxic secondary compounds (polyphenolics) of nine leaf litter species. To differentiate between effects on exposure vs. susceptibility to infection, we included multiple infection experiments including one with constant per capita exposure. We found that increased litter nitrogen increased tadpole survival, and also increased cercaria production by the snail intermediate hosts, causing opposing effects on tadpole per capita exposure to trematode infection. Increased litter polyphenolics slowed tadpole development, leading to increased infection by increasing both their susceptibility to infection and the length of time they were exposed to parasites. Based on these results, recent shifts in forest composition towards more nitrogen-poor litter species should decrease trematode infection in tadpoles via density- and trait-mediated effects on the snail intermediate hosts. However, these shifts also involve increased abundance of litter species with high polyphenolic levels, which should increase trematode infection via trait-mediated effects on tadpoles. Future studies will be needed to determine the relative strength of these opposing effects in natural wetland communities. [Correction added after online publication on 5 January 2017: wording changed to 'which should increase trematode infection via trait-mediated effects on tadpoles'.].

Host and parasite thermal acclimation responses depend on the stage of infection.

Global climate change is expected to alter patterns of temperature variability, which could influence species interactions including parasitism. Species interactions can be difficult to predict in variable-temperature environments because of thermal acclimation responses, i.e. physiological changes that allow organisms to adjust to a new temperature following a temperature shift. The goal of this study was to determine how thermal acclimation influences host resistance to infection and to test for parasite acclimation responses, which might differ from host responses in important ways. We tested predictions of three, non-mutually exclusive hypotheses regarding thermal acclimation effects on infection of green frog tadpoles (Lithobates clamitans) by the trematode parasite Ribeiroia ondatrae with fully replicated controlled-temperature experiments. Trematodes or tadpoles were independently acclimated to a range of 'acclimation temperatures' prior to shifting them to new 'performance temperatures' for experimental infections. Trematodes that were acclimated to intermediate temperatures (19-22 °C) had greater encystment success across temperatures than either cold- or warm-acclimated trematodes. However, host acclimation responses varied depending on the stage of infection (encystment vs. clearance): warm- (22-28 °C) and cold-acclimated (13-19 °C) tadpoles had fewer parasites encyst at warm and cold performance temperatures, respectively, whereas intermediate-acclimated tadpoles (19-25 °C) cleared the greatest proportion of parasites in the week following exposure. These results suggest that tadpoles use different immune mechanisms to resist different stages of trematode infection, and that each set of mechanisms has unique responses to temperature variability. Our results highlight the importance of considering thermal responses of both parasites and hosts when predicting disease patterns in variable-temperature environments.