Understanding linkages between environmental changes and disease emergence in human and wildlife populations represents one of the greatest challenges to ecologists and parasitologists. While there ...is considerable interest in drivers of amphibian microparasite infections and the resulting consequences, comparatively little research has addressed such questions for amphibian macroparasites. What work has been done in this area has largely focused on nematodes of the genus
Rhabdias
and on two genera of trematodes (
Ribeiroia
and
Echinostoma
). Here, we provide a synopsis of amphibian macroparasites, explore how macroparasites may affect amphibian hosts and populations, and evaluate the significance of these parasites in larger community and ecosystem contexts. In addition, we consider environmental influences on amphibian–macroparasite interactions by exploring contemporary ecological factors known or hypothesized to affect patterns of infection. While some macroparasites of amphibians have direct negative effects on individual hosts, no studies have explicitly examined whether such infections can affect amphibian populations. Moreover, due to their complex life cycles and varying degrees of host specificity, amphibian macroparasites have rich potential as bioindicators of environmental modifications, especially providing insights into changes in food webs. Because of their documented pathologies and value as bioindicators, we emphasize the need for broader investigation of this understudied group, noting that ecological drivers affecting these parasites may also influence disease patterns in other aquatic fauna.
1. Many of the global losses of amphibians are believed to be caused by the chytrid fungus, Batrachochytrium dendrobatidis (Bd). Hence, determining its present and future environmental suitability ...should help to inform management and surveillance of this pathogen and curtail the amphibian biodiversity crisis. 2. In this issue of Journal of Applied Ecology, Murray et al. (2010) offer an important step in this direction by providing a species distribution model that projects the environmental suitability of Bd across Australia and predicts locations of chytridiomycosis and amphibian declines. Batrachochytrium dendrobatidis presence was predicted by diurnal temperature range (a measure of temperature variability) and mean precipitation. Human population density, a positive predictor of Bd, accounted for the most variation when removed from the statistical model. 3. This work represents an invaluable case study and has great potential for managing chytridiomycosis and associated amphibian declines, but its value in practice will depend on how well managers understand the limitations of species distribution models. 4. Synthesis and applications. To improve the management of chytridiomycosis, amphibian-chytrid research should attempt to understand how humans may affect the distribution of Bd, how climatic means and variances affect Bd transmission, how much variation in the distribution of Bd is unique to and shared among climate, human, and other factors, whether human-related factors and climate statistically interact, and how these potentially correlated factors and any interactions affect the predictability of species distribution models. In response to the swift spread of Bd and our rapidly changing planet, we encourage the application of Bd distribution models to other regions of the globe and predictions of Bd's distribution under future climate change scenarios.
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.
Food and parasites can independently play a role in destabilizing population fluctuations of animals, and yet, more than 50 years ago, David Lack proposed that these two factors should act in ...concert. We examined the role of these factors on the vital rates of free-living white-footed mice (Peromyscus leucopus) over the summer and autumn months. We used a replicated factorial experiment in which deer exclosures doubled acorn availability and anthelmintic application reduced gastrointestinal helminths. Specifically, we wanted to know if either factor or an interaction between the two accounted for the midsummer breeding hiatus observed in this species. We found no influence of habitat quality on mouse breeding, vital rates, or demography; however, anthelmintic treatment resulted in mice continuing to reproduce during the hiatus at the same rate as previously, and they also exhibited increased body condition, growth rate, and survival. These results provide evidence that gastrointestinal helminths reduce P. leucopus reproductive output in central Pennsylvania, and these effects on reproduction could play a role in the unstable dynamics of small mammals.
1. 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. 2. We generated predictions for differential effects of litter nutrition and secondary polyphenolic compounds on tadpole (Lithobates sylvaticd) 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). 3. 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. 4. 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. 5. 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'.
The pathogenic chytrid fungus Batrachochytrium dendrobatidis (Bd) is considered responsible for the population declines and extinctions of hundreds of amphibian species worldwide. The panzootic was ...likely triggered by human-assisted spread, but once the pathogen becomes established in a given region, its distribution is probably determined by local drivers. To assess the relative importance of potential drivers of infection in red-spotted newts (Notophthalmus viridescens), we measured Bd levels in 16 populations throughout central Pennsylvania. Infected individuals were detected in all but four populations, indicating that Bd is widespread in this region. We quantified local factors hypothesized to influence Bd, and found that infection levels were best predicted by the proportion of the pond substrate consisting of leaf litter or vegetation, along with a significant effect of water temperature. Bd infection in amphibians is temperature-dependent, and one possible explanation of the apparent substrate effect is that tree cover and vegetation provide shade, reducing the availability of shallow, warm-water patches in which newts might reduce or clear Bd infections. Alternatively, leaf litter and emergent vegetation might increase Bd infection more directly, perhaps by providing substrates for environmental growth of the fungus. We also observed a curvilinear relationship between Bd load and snout-vent length (a proxy for age), hinting that newts might develop acquired resistance to Bd infection. Though correlational, these results add to a growing body of evidence suggesting that environmental temperature is an important driver of Bd infection dynamics.
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 colimitation. 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.
Past studies have found a heterogeneous distribution of the amphibian chytrid fungal pathogen,
Batrachochytrium dendrobatidis
(Bd). Recent studies have accounted for some of this heterogeneity ...through a positive association between canopy cover and Bd abundance, which is attributed to the cooling effect of canopy cover. We questioned whether leaf litter inputs that are also associated with canopy cover might also alter Bd growth. Leaf litter inputs exhibit tremendous interspecific chemical variation, and we hypothesized that Bd growth varies with leachate chemistry. We also hypothesized that Bd uses leaf litter as a growth substrate. To test these hypotheses, we conducted laboratory trials in which we exposed cultures of Bd to leachate of 12 temperate leaf litter species at varying dilutions. Using a subset of those 12 litter species, we also exposed Bd to pre-leached litter substrate. We found that exposure to litter leachate and substrate reduced Bd spore and sporangia densities, although there was substantial variation among treatments. In particular, Bd densities were inversely correlated with concentrations of phenolic acids. We conducted a field survey of phenolic concentrations in natural wetlands which verified that the leachate concentrations in our lab study are ecologically relevant. Our study reinforces prior indications that positive associations between canopy cover and Bd abundance are likely mediated by water temperature effects, but this phenomenon might be counteracted by changes in aquatic chemistry from leaf litter inputs.
Several studies have demonstrated that competition between disparate taxa can be important in determining community structure, yet surprisingly, to our knowledge, no quantitative studies have been ...conducted on competition between carnivorous plants and animals. To examine potential competition between these taxa, we studied dietary and microhabitat overlap between pink sundews (Drosera capillaris) and wolf spiders (Lycosidae) in the field, and conducted a laboratory experiment examining the effects of wolf spiders on sundew fitness. In the field, we found that sundews and spiders had a high dietary overlap with each other and with the available arthropod prey. Associations between sundews and spiders depended on spatial scale: both sundews and spiders were found more frequently in quadrats with more abundant prey, but within quadrats, spiders constructed larger webs and located them further away from sundews as the total sundew trapping area increased, presumably to reduce competition. Spiders also constructed larger webs when fewer prey were available. In the laboratory, our experiment revealed that spiders can significantly reduce sundew fitness. Our findings suggest that members of the plant and animal kingdoms can and do compete.
The manner in which parasite intensity and aggregation varies with host age can provide insights into parasite dynamics and help identify potential means of controlling infections in humans and ...wildlife. A significant challenge is to distinguish among competing mechanistic hypotheses for the relationship between age and parasite intensity or aggregation. Because different mechanisms can generate similar relationships, testing among competing hypotheses can be difficult, particularly in wildlife hosts, and often requires a combination of experimental and model fitting approaches. We used field data, experiments, and model fitting to distinguish among ten plausible drivers of a curvilinear age-intensity relationship and increasing aggregation with host age for echinostome trematode infections of green frogs. We found little support for most of these proposed drivers but did find that the parsimonious explanation for the observed age-intensity relationship was seasonal exposure to echinostomes. The parsimonious explanation for the aggregated distribution of parasites in this host population was heterogeneity in exposure. A predictive model incorporating seasonal exposure indicated that tadpoles hatching early or late in the breeding season should have lower trematode burdens at metamorphosis, particularly with simulated warmer climates. Application of this multi-pronged approach (field surveys, lab experiments, and modeling) to additional parasite-host systems could lead to discovery of general patterns in the drivers of parasite age-intensity and age-distribution relationships.
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