Ecosystems are often exposed to mixtures of chemical contaminants, but the scientific community lacks a theoretical framework to predict the effects of mixtures on biodiversity and ecosystem ...properties. We conducted a freshwater mesocosm experiment to examine the effects of pairwise agrochemical mixtures fertiliser, herbicide (atrazine), insecticide (malathion) and fungicide (chlorothalonil) on 24 species‐ and seven ecosystem‐level responses. As postulated, the responses of biodiversity and ecosystem properties to agrochemicals alone and in mixtures was predictable by integrating information on each functional group's (1) sensitivity to the chemicals (direct effects), (2) reproductive rates (recovery rates), (3) interaction strength with other functional groups (indirect effects) and (4) links to ecosystem properties. These results show that community ecology theory holds promise for predicting the effects of contaminant mixtures on biodiversity and ecosystem services and yields recommendations on which types of agrochemicals to apply together and separately to reduce their impacts on aquatic ecosystems.
Although studies on biodiversity and ecosystem function are often framed within the context of anthropogenic change, a central question that remains is how important are direct vs. indirect (via ...changes in biodiversity) effects of anthropogenic stressors on ecosystem functions in multitrophic‐level communities. Here, we quantify the effects of the fungicide chlorothalonil on 34 species‐, 2 community‐ and 11 ecosystem‐level responses in a multitrophic‐level system. At ecologically relevant concentrations, chlorothalonil increased mortality of amphibians, gastropods, zooplankton, algae and a macrophyte (reducing taxonomic richness), reduced decomposition and water clarity and elevated dissolved oxygen and net primary productivity. These ecosystem effects were indirect and predictable based on changes in taxonomic richness. A path analysis suggests that chlorothalonil‐induced reductions in biodiversity and top‐down and bottom‐up effects facilitated algal blooms that shifted ecosystem functions. This work emphasises the need to re‐evaluate the safety of chlorothalonil and to further link anthropogenic‐induced changes in biodiversity to altered ecosystem functions.
Anthropogenic factors can have simultaneous positive and negative effects on parasite transmission, and thus it is important to quantify their net effects on disease risk. Net effects will be a ...product of changes in the survival and traits (e.g., susceptibility, infectivity) of both hosts and parasites. In separate laboratory experiments, we exposed cercariae of the trematode Echinostoma trivolvis, and its first and second intermediate hosts, snails (Planorbella trivolvis) and green frog tadpoles (Rana clamitans), respectively, to one of four common pesticides (atrazine, glyphosate, carbaryl, and malathion) at standardized, ecologically relevant concentrations (201.0, 3700.0, 33.5, and 9.6 micrograms/L, respectively). We measured effects of pesticide exposure on six mechanisms important to this host-parasite interaction: (1) survival of E. trivolvis cercariae over 26 hours, (2) tadpole survival over two weeks, (3) snail survival over four weeks, (4) snail growth and fecundity, (5) cercarial infectivity, and (6) tadpole susceptibility to a fixed number of cercariae. Pesticides, in general, caused significantly greater mortality of E. trivolvis cercariae than did control treatments, but atrazine was the lone chemical to significantly reduce cercarial survival (LC50 value = 267 mg/L) and then only at concentrations greater than commonly found in aquatic ecosystems (≥200 micrograms/L). None of the pesticides significantly enhanced E. trivolvis virulence, decreased tadpole survival, or reduced snail survival, growth, or fecundity. Sublethal exposure of the cercariae to the pesticides (4 h) did not significantly affect trematode encystment in R. clamitans. In contrast, sublethal exposure of R. clamitans to each of the four pesticides increased their susceptibility as measured by the percentage of cercariae that encysted. The reduction in exposure to trematodes due to pesticide-induced cercarial mortality (a density-mediated effect) was smaller than the pesticide-induced increase in amphibian susceptibility (a trait-mediated effect), suggesting that the net effect of exposure to environmentally realistic levels of pesticides will be to elevate amphibian trematode infections. These findings highlight the importance of elucidating the lethal and sublethal effects of anthropogenic factors on both hosts and parasites to understand the mechanisms underlying changes in parasite transmission and virulence, an approach that is especially needed for amphibians, a taxon experiencing global disease-related declines.
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.
Pesticide pollution can alter parasite transmission, but scientists are unaware if effects of pesticides on parasite exposure and host susceptibility (i.e. infection risk given exposure) can be ...generalised within a community context. Using replicated temperate pond communities, we evaluate effects of 12 pesticides, nested in four pesticide classes (chloroacetanilides, triazines, carbamates organophosphates) and two pesticide types (herbicides, insecticides) applied at standardised environmental concentrations on larval amphibian exposure and susceptibility to trematode parasites. Most of the variation in exposure and susceptibility occurred at the level of pesticide class and type, not individual compounds. The organophosphate class of insecticides increased snail abundance (first intermediate host) and thus trematode exposure by increasing mortality of snail predators (top–down mechanism). While a similar pattern in snail abundance and trematode exposure was observed with triazine herbicides, this effect was driven by increases in snail resources (periphytic algae, bottom–up mechanism). Additionally, herbicides indirectly increased host susceptibility and trematode infections by (1) increasing time spent in susceptible early developmental stages and (2) suppressing tadpole immunity. Understanding generalisable effects associated with contaminant class and type on transmission is critical in reducing complexities in predicting disease dynamics in at‐risk host populations.
ABSTRACT
Chytridiomycosis, caused by the pathogenic fungus Batrachochytrium dendrobatidis (Bd), is one of the largest threats to wildlife and is putatively linked to the extirpation of numerous ...amphibians. Despite over a decade of research on Bd, conflicting results from a number of studies make it difficult to forecast where future epizootics will occur and how to manage this pathogen effectively. Here, we emphasize how resolving these conflicts will advance Bd management and amphibian conservation efforts. We synthesize current knowledge on whether Bd is novel or endemic, whether amphibians exhibit acquired resistance to Bd, the importance of host resistance versus tolerance to Bd, and how biotic (e.g. species richness) and abiotic factors (e.g. climate change) affect Bd abundance. Advances in our knowledge of amphibian–chytrid interactions might inform the management of fungal pathogens in general, which are becoming more common and problematic globally.
Freshwater systems are critical to life on earth, yet they are threatened by the increasing rate of synthetic chemical pollution. Current predictions of the effects of synthetic chemicals on ...freshwater ecosystems are hampered by the sheer number of chemical contaminants entering aquatic systems, the diversity of organisms inhabiting these systems, the myriad possible direct and indirect effects resulting from these combinations, and uncertainties concerning how contaminants might alter ecosystem metabolism via changes in biodiversity. To address these knowledge gaps, we conducted a mesocosm experiment that elucidated the responses of ponds composed of phytoplankton and zooplankton to standardized concentrations of 12 pesticides, nested within four pesticide classes, and two pesticide types. We show that the effects of the pesticides on algae were consistent within herbicides and insecticides and that responses of over 70 phytoplankton species and genera were consistent within broad taxonomic groups. Insecticides generated top‐down effects on phytoplankton community composition and abundance, which were associated with persistent increases in ecosystem respiration. Insecticides had direct toxic effects on cladocerans, which led to competitive release of copepods. These changes in the zooplankton community led to a decrease in green algae and a modest increase in diatoms. Herbicides did not change phytoplankton composition but reduced total phytoplankton abundance. This reduction in phytoplankton led to short‐term decreases in ecosystem respiration. Given that ponds release atmospheric carbon and that worldwide pesticide pollution continues to increase exponentially, scientists and policy makers should pay more attention to the ways pesticides alter the carbon cycle in ponds via changes in communities, as demonstrated by our results. Our results show that these predictions can be simplified by grouping pesticides into types and species into functional groups. Adopting this approach provides an opportunity to improve the efficiency of risk assessment and mitigation responses to global change.
We conducted a mesocosm experiment that elucidated responses of phytoplankton and zooplankton to 12 pesticides, nested within four pesticide classes, and two pesticide types. The effects of the pesticides on algae were consistent within herbicides and insecticides and within taxonomic groups of phytoplankton. Insecticides generated top‐down effects on phytoplankton community composition and abundance, which were associated with persistent increases in ecosystem respiration. Insecticides had direct toxic effects on cladocerans, which led to competitive release of copepods. Herbicides did not change phytoplankton composition but reduced total phytoplankton abundance. This reduction in phytoplankton led to short‐term decreases in ecosystem respiration.
Summary
High temperatures (e.g., fever) and gut microbiota can both influence host resistance to infection. However, effects of temperature‐driven changes in gut microbiota on resistance to parasites ...remain unexplored. We examined the temperature dependence of infection and gut bacterial communities in bumble bees infected with the trypanosomatid parasite Crithidia bombi. Infection intensity decreased by over 80% between 21 and 37°C. Temperatures of peak infection were lower than predicted based on parasite growth in vitro, consistent with mismatches in thermal performance curves of hosts, parasites and gut symbionts. Gut bacterial community size and composition exhibited slight but significant, non‐linear, and taxon‐specific responses to temperature. Abundance of total gut bacteria and of Orbaceae, both negatively correlated with infection in previous studies, were positively correlated with infection here. Prevalence of the bee pathogen‐containing family Enterobacteriaceae declined with temperature, suggesting that high temperature may confer protection against diverse gut pathogens. Our results indicate that resistance to infection reflects not only the temperature dependence of host and parasite performance, but also temperature‐dependent activity of gut bacteria. The thermal ecology of gut parasite‐symbiont interactions may be broadly relevant to infectious disease, both in ectothermic organisms that inhabit changing climates, and in endotherms that exhibit fever‐based immunity.
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.
There is growing interest in the ecological consequences of fear, as evidenced by the numerous studies on the nonconsumptive, trait-mediated effects of predators. Parasitism, however, has yet to be ...fully integrated into research on the ecology of fear, despite it having direct negative and often lethal effects on hosts and being the most common life history strategy on the planet. This might at least be partly due to the traditional, but untested, assumption that anti-parasite responses are weak relative to anti-predator responses. To test this hypothesis, we quantified the activity and location responses of Bufo americanus tadpoles to one of six chemical cues: water; cercariae of Echinostoma trivolvis, a trematode which infects and can kill amphibians; a snail releasing E. trivolvis cercariae; an uninfected snail; food; or conspecific alarm chemicals signaling predation. There is also literature encouraging research on the context dependency and pollution-induced disruption of fear responses. Consequently, before quantifying responses to the chemical cues, half of the B. americanus were exposed to the herbicide atrazine (201 μg/l for 4 days), a reported inhibitor of fear responses in fish. Tadpoles were attracted to food, were indifferent to an uninfected snail, avoided alarm chemicals, and exhibited avoidance and elevated activity in response to a snail shedding cercariae and cercariae alone. Atrazine had no detectable effects on B. americanus' responses to the tested cues despite the use of a higher concentration and longer exposure duration than has been repeatedly shown to inhibit chemical cue detection in fish. The magnitude of anti-parasite and anti-predator responses were qualitatively similar, suggesting that the fear of disease and its ecological consequences could be comparable to that of predation. Consequently, we call for a greater integration of parasites into research on the ecology of fear and trait-mediated indirect effects.
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