Accelerating rates of species extinctions and disease emergence underscore the importance of understanding how changes in biodiversity affect disease outcomes. Over the past decade, a growing number of studies have reported negative correlations between host biodiversity and disease risk, prompting suggestions that biodiversity conservation could promote human and wildlife health. Yet the generality of the diversity-disease linkage remains conjectural, in part because empirical evidence of a relationship between host competence (the ability to maintain and transmit infections) and the order in which communities assemble has proven elusive. Here we integrate high-resolution field data with multi-scale experiments to show that host diversity inhibits transmission of the virulent pathogen Ribeiroia ondatrae and reduces amphibian disease as a result of consistent linkages among species richness, host composition and community competence. Surveys of 345 wetlands indicated that community composition changed nonrandomly with species richness, such that highly competent hosts dominated in species-poor assemblages whereas more resistant species became progressively more common in diverse assemblages. As a result, amphibian species richness strongly moderated pathogen transmission and disease pathology among 24,215 examined hosts, with a 78.4% decline in realized transmission in richer assemblages. Laboratory and mesocosm manipulations revealed an approximately 50% decrease in pathogen transmission and host pathology across a realistic diversity gradient while controlling for host density, helping to establish mechanisms underlying the diversity-disease relationship and their consequences for host fitness. By revealing a consistent link between species richness and community competence, these findings highlight the influence of biodiversity on infection risk and emphasize the benefit of a community-based approach to understanding infectious diseases.
Global amphibian declines have often been attributed to disease, but ignorance of the relative importance and mode of action of potential drivers of infection has made it difficult to develop effective remediation. In a field study, here we show that the widely used herbicide, atrazine, was the best predictor (out of more than 240 plausible candidates) of the abundance of larval trematodes (parasitic flatworms) in the declining northern leopard frog Rana pipiens. The effects of atrazine were consistent across trematode taxa. The combination of atrazine and phosphate--principal agrochemicals in global corn and sorghum production--accounted for 74% of the variation in the abundance of these often debilitating larval trematodes (atrazine alone accounted for 51%). Analysis of field data supported a causal mechanism whereby both agrochemicals increase exposure and susceptibility to larval trematodes by augmenting snail intermediate hosts and suppressing amphibian immunity. A mesocosm experiment demonstrated that, relative to control tanks, atrazine tanks had immunosuppressed tadpoles, had significantly more attached algae and snails, and had tadpoles with elevated trematode loads, further supporting a causal relationship between atrazine and elevated trematode infections in amphibians. These results raise concerns about the role of atrazine and phosphate in amphibian declines, and illustrate the value of quantifying the relative importance of several possible drivers of disease risk while determining the mechanisms by which they facilitate disease emergence.
The field of ecotoxicology is experiencing a surge in attention among ecologists as we gain a deeper appreciation for how contaminants can impact natural ecosystems. This interest is particularly strong in aquatic systems where many non-target organisms experience pesticides. In this article, we assess how pesticides affect freshwater systems by applying the conceptual framework of density-and trait-mediated indirect effects from the field of basic ecology. We demonstrate the utility of this framework for understanding the conditions under which pesticides affect species interactions, communities and ecosystems. Through the integration of laboratory toxicity tests and this ecological framework, ecotoxicologists should be better able to identify the mechanisms through which pesticides affect communities and ecosystems. We also identify several areas of research that are in critical need of empirical attention including synergistic effects between pesticides and natural stressors, the importance of pesticides on community assembly via habitat preferences and oviposition effects, the timing and frequency of pesticide applications, pesticide effects on population dynamics, the evolution of pesticide resistance in non-target organisms and ecosystem recovery. With this knowledge, one can improve upon management decisions and help protect nontarget species that are of conservation concern. Keywords Biodiversity, density-mediated indirect effects, ecosystem function, fungicide, herbicide, insecticide, trait-mediated indirect effects.Ecology Letters (2006) 9: 1157-1171 I N T R O D U C T I O NThe fields of ecology and toxicology have largely evolved as separate disciplines over the past century with unique journals, unique tools and a distinct jargon that has reinforced an allopatric evolution of ideas. While ecologists have focused on how biotic and abiotic factors affect species distribution and species interactions, toxicologists have traditionally focused on single-species toxicity tests. There is, however, the growing field of ecotoxicology, a name that naturally implies a hybrid of ideas and approaches from ecology and toxicology. Given that the number of ecotoxicological studies has experienced tremendous growth in the past decade, it is an excellent time to evaluate what we have learned. In this essay, we evaluate the study of ecotoxicology in freshwater systems, an arena that has received a great deal of research focus. In doing so, we examine how one can use general ecological theory to integrate ecology and ecotoxicology to better understand and conserve the ecology of aquatic systems.
Parasite infections often lead to dramatically different outcomes among host species. Although an emerging body of ecoimmunological research proposes that hosts experience a fundamental trade-off between pathogen defences and life-history activities, this line of inquiry has rarely been extended to the most essential outcomes of host-pathogen interactions: namely, infection and disease pathology. Using a comparative experimental approach involving 13 amphibian host species and a virulent parasite, we test the hypothesis that Ôpace-of-lifeÕ predicts parasite infection and host pathology. Trematode exposure increased mortality and malformations in nine host species. After accounting for evolutionary history, species that developed quickly and metamorphosed smaller (Ôfast-speciesÕ) were particularly prone to infection and pathology. This pattern likely resulted from both weaker host defences and greater adaptation by parasites to infect common hosts. Broader integration between life history theory and disease ecology can aid in identifying both reservoir hosts and species at risk of disease-driven declines.
Research that identifies the potential host range of generalist pathogens as well as variation in host susceptibility is critical for understanding and predicting the dynamics of infectious diseases within ecological communities. Ranaviruses have been linked to amphibian die-off events worldwide with the greatest number of reported mortality events occurring in the United States. While reports of ranavirus-associated mortality events continue to accumulate, few data exist comparing the relative susceptibility of different species. Using a series of laboratory exposure experiments and comparative phylogenetics, we compared the susceptibilities of 19 amphibian species from two salamander families and five anurans families for two ranavirus isolates: frog virus 3 (FV3) and an FV3-like isolate from an American bullfrog culture facility. We discovered that ranaviruses were capable of infecting 17 of the 19 larval amphibian species tested with mortality ranging from 0 to 100%. Phylogenetic comparative methods demonstrated that species within the anuran family Ranidae were generally more susceptible to ranavirus infection compared to species from the other five families. We also found that susceptibility to infection was associated with species that breed in semi-permanent ponds, develop rapidly as larvae, and have limited range sizes. Collectively, these results suggest that phylogeny, life history characteristics, and habitat associations of amphibians have the potential to impact susceptibility to ranaviruses.
While the importance of changes in host biodiversity for disease risk continues to gain empirical support, the influence of natural variation in parasite diversity on epidemiological outcomes remains largely overlooked. Here, we combined field infection data from 2,191 amphibian hosts representing 158 parasite assemblages with mechanistic experiments to evaluate the influence of parasite richness on both parasite transmission and host fitness. Using a guild of larval trematode parasites (six species) and an amphibian host, our experiments contrasted the effects of parasite richness vs. composition, observed vs. randomized assemblages, and additive vs. replacement designs. Consistent with the dilution effect hypothesis extended to intrahost diversity, increases in parasite richness reduced overall infection success, including infections by the most virulent parasite. However, the effects of parasite richness on host growth and survival were context dependent; pathology increased when parasites were administered additively, even when the presence of the most pathogenic species was held constant, but decreased when added species replaced or reduced virulent species, emphasizing the importance of community composition and assembly. These results were similar or stronger when community structures were weighted by their observed frequencies in nature. The field data also revealed the highly nested structure of parasite assemblages, with virulent species generally occupying basal positions, suggesting that increases in parasite richness and antagonism in nature will decrease virulent infections. Our findings emphasize the importance of parasite biodiversity and coinfection in affecting epidemiological responses and highlight the value of integrating research on biodiversity and community ecology for understanding infectious diseases.microbiome | parasite competition | emerging infectious disease | ecosystem function | amphibian decline E cological research has focused increasingly on the importance of changes in biodiversity, thereby forming a fundamental link between community and ecosystem ecology (1-4). The loss or gain of species into a community, often in association with anthropogenic activities, can have remarkable effects on productivity, carbon storage, nutrient cycling, and species invasions (5-8). More recently, this line of inquiry has been extended to explore the role of biodiversity in affecting parasite transmission (i.e., the dilution effect; ref. 9). Building from historical research on agricultural plant communities (10), a series of recent studies has reported an inverse relationship between host diversity and the risk of disease in humans, plants, birds, amphibians, and corals (9). On the basis of experimental manipulations of host diversity, common mechanisms for this relationship involve changes in susceptible host density, such that higher diversity leads to a concomitant decline in susceptible hosts, or in encounter reduction, with added species interfering with parasite transmission (11,12).Des...
The last decade has seen an explosion in the number of studies exploring predator-induced plasticity. Recently, there has been a call for more comprehensive approaches that can identify functional relationships between traits, constraints on phenotypic responses, and the cost and benefits of alternative phenotypes. In this study, we exposed Helisoma trivolvis, a freshwater snail, to a factorial combination of three resource levels and five predator environments (no predator, one or two water bugs, and one or two crayfish) and examined ten traits including behavior, morphology, and life history. Each predator induced a unique suite of behavioral and morphological responses. Snails increased near-surface habitat use with crayfish but not with water bugs. Further, crayfish induced narrow and high shells whereas water bugs induced wide shells and wide apertures. In terms of life history, both predators induced delayed reproduction and greater mass at reproduction. However, crayfish induced a greater delay in reproduction that resulted in reduced fecundity whereas water bugs did not induce differences in fecundity. Resource levels impacted the morphology of H. trivolvis; snails reared with greater resource levels produced higher shells, narrower shells, and wider apertures. Resource levels also impacted snail life history; lower resources caused longer times to reproduction and reduced fecundity. Based on an analysis of phenotypic correlations, the morphological responses to each predator most likely represent phenotypic trade-offs. Snails could either produce invasion-resistant shells for defense against water bugs or crush-resistant shells for defense against crayfish, but not both. Our use of a comprehensive approach to examine the responses of H. trivolvis has provided important information regarding the complexity of phenotypic responses to different environments, the patterns of phenotypic integration across environments, and the potential costs and benefits associated with plastic traits.
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