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.
According to ecological stoichiometry (ES), the growth of a consumer with abundant resources should increase as body and resource stoichiometry become more similar. However, for organisms with complex life cycles involving distinct changes in biology, nutrient demands might change in response to ontogenetic changes in body stoichiometry. Tadpole growth and development has been found to be largely nitrogen (N) limited, as predicted for organisms developing N-rich tissues like muscle. However, tadpole metamorphosis includes periods of rapid development of phosphorus (P)-rich bones in preparation for a terrestrial lifestyle. We hypothesized that tadpole growth and development will exhibit variable nutrient demands during different stages of ontogeny, due to predictable changes in body tissue stoichiometry. To test this, we raised tadpoles on four diets with varying N:P ratios and assessed growth and developmental rates. Specifically, we predicted that tadpoles would be sensitive to N limitation throughout ontogeny (consistent with previous studies), but also sensitive to P limitation during the process of long-bone ossification. Consistent with our prediction, tadpole growth rates and development were sensitive to N limitation throughout ontogeny. Increased dietary N led to a shorter time to metamorphosis and a larger mass at metamorphosis. Also as predicted, growth rates were sensitive to both N and P during the period of peak bone ossification, indicative of co-limitation. These results indicate that P limitation changes through tadpole ontogeny consistent with, and can be predicted by, shifts in body tissue stoichiometry. Future studies should investigate whether ontogenetic shifts in tadpole P limitation lead to seasonal shifts in wetland nutrient cycling.
Swimmer's itch (SI) is a painful rash caused by skin penetration by free-swimming infectious cercariae of avian schistosomes, snail-borne helminth parasites related to the causative agents of human schistosomiasis. The goal of this study was to determine if commonly collected environmental data could be used to predict daily fluctuations in SI incidence at an inland beach in northwestern Michigan. Lifeguards collected daily data over four summers, including the number of self-reported SI cases, total swimmers, water temperature, wind speed and wind direction. Mixed-effects binomial regression revealed that wind direction, wind speed and time of day were the best predictors of daily SI risk. Swimmers entering the water in the morning or on days with direct onshore wind perpendicular to the shoreline had the greatest SI risk. However, there was a negative effect of wind speed after accounting for direction, where SI risk was greatest on days with a gentle breeze originating directly offshore. These results suggest that at this beach, direct onshore winds generate a surface-water current that causes SI cercariae to aggregate in the shallow waters used by swimmers. Data are needed from additional sites to confirm whether the onshore wind is a generally important driver of SI incidence.
Cercarial dermatitis (‘swimmer's itch’; SI), characterized by small itchy bumps caused by schistosome parasites of birds and mammals, is a common problem in Michigan. Research on avian schistosomes began nearly 100 years ago in Michigan inland lakes, yet scientists are still uncovering basic biological information including the identification of local snail and parasite species that cause SI. Previous research primarily focused on lakes in the northern half of Michigan's lower peninsula, although SI occurs throughout the state. We surveyed snails and snail-borne trematodes in lakes across Michigan's lower peninsula and used quantitative polymerase chain reaction analysis of filtered water samples to identify parasites to the species level, including a recently discovered parasite species that uses the snail Planorbella (Helisoma) trivolvis as its intermediate host. Most SI mitigation efforts have focused on a parasite species hosted by the snail Lymnaea catescopium ( = Stagnicola emarginata); however, lymnaeid snails and their associated schistosome species were largely restricted to northern lakes. In contrast, P. trivolvis and its associated parasite species were common in both northern and southern Michigan lakes. A third schistosome species associated with physid snails was also present at low levels in both northern and southern lakes. These results indicate that the recently discovered parasite species and its planorbid snail intermediate host may be more important drivers of Michigan SI than previously thought, possibly due to increased definitive host abundance in recent decades. These results have potentially important implications for SI mitigation and control efforts.
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