Large-scale spatial drivers of avian schistosomes in Northern Michigan inland lakes.

Avian schistosomes are snail-borne trematode parasites (Trichobilharzia spp.) that can cause a nasty skin rash in humans when their cercariae mistake us for their normal bird hosts. We sought to investigate drivers of the spatial distribution of Trichobilharzia cercaria abundance throughout Northern Michigan lakes. For 38 sites on 16 lakes, we assessed several dozen potential environmental predictors that we hypothesized might have direct or indirect effects on overall cercaria abundance, based on known relationships between abiotic and biotic factors in wetland ecosystems. We included variables quantifying local densities of intermediate hosts, temperature, periphyton growth rates, human land use and hydrology. We also measured daily abundance of schistosome cercariae in the water over a 5-week period, supported by community scientists who collected and preserved filtered water samples for qPCR. The strongest predictor of cercaria abundance was Lymnaea host snail density. Lymnaea density was higher in deeper lakes and at sites with more deciduous tree cover, consistent with their association with cool temperature habitats. Contrary to past studies of human schistosomes, we also found a significant negative relationship between cercaria abundance and submerged aquatic vegetation, possibly due to vegetation blocking cercaria movement from offshore snail beds. If future work shows that these effects are indeed causal, then these results suggest possible new approaches to managing swimmer's itch risk in northern MI lakes, such as modifying tree cover and shallow-water vegetation at local sites.

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.

Temperature and mass scaling affect cutaneous and pulmonary respiratory performance in a diving frog.

Global climate change is altering patterns of temperature variation, with unpredictable consequences for species and ecosystems. The Metabolic Theory of Ecology (MTE) provides a powerful framework for predicting climate change impacts on ectotherm metabolic performance. MTE postulates that physiological and ecological processes are limited by organism metabolic rates, which scale predictably with body mass and temperature. The purpose of this study was to determine if different metabolic proxies generate different empirical estimates of key MTE model parameters for the aquatic frog Xenopus laevis when allowed to exhibit normal diving behavior. We used a novel methodological approach in combining a flow-through respirometry setup with the open-source Arduino platform to measure mass and temperature effects on 4 different proxies for whole-body metabolism (total O2 consumption, cutaneous O2 consumption, pulmonary O2 consumption, and ventilation frequency), following thermal acclimation to one of 3 temperatures (8°C, 17°C, or 26°C). Different metabolic proxies generated different mass-scaling exponents (b) and activation energy (EA ) estimates, highlighting the importance of metabolic proxy selection when parameterizing MTE-derived models. Animals acclimated to 17°C had higher O2 consumption across all temperatures, but thermal acclimation did not influence estimates of key MTE parameters EA and b. Cutaneous respiration generated lower MTE parameters than pulmonary respiration, consistent with temperature and mass constraints on dissolved oxygen availability, SA:V ratios, and diffusion distances across skin. Our results show that the choice of metabolic proxy can have a big impact on empirical estimates for key MTE model parameters.

Direct onshore wind predicts daily swimmer's itch (avian schistosome) incidence at a Michigan beach.

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.

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.

Ontogenetic changes in sensitivity to nutrient limitation of tadpole growth.

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.