Daniel L. Preston

Biodiversity decreases disease through predictable changes in host community competence

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.

Host and parasite diversity jointly control disease risk in complex communities

Significance Ongoing losses of biodiversity underscore the need to understand how species loss affects infectious diseases. Recognizing that most communities include multiple hosts and pathogens, we tested how variation in host and parasite diversity influenced disease risk. By combining field surveys and experiments involving amphibian hosts and trematode parasites, we show that realistic changes in host and parasite richness inhibit transmission of the deadliest parasite, Ribeiroia ondatrae. Increased host richness consistently reduced infections by Ribeiroia and the total parasite community. Importantly, however, parasite richness further dampened pathogen transmission, and the most diverse assemblages reduced Ribeiroia transmission by >50%. These findings emphasize the “hidden” role of parasite communities in diversity–disease interactions and the value of a community-based approach to infectious disease. Host–parasite interactions are embedded within complex communities composed of multiple host species and a cryptic assemblage of other parasites. To date, however, surprisingly few studies have explored the joint effects of host and parasite richness on disease risk, despite growing interest in the diversity–disease relationship. Here, we combined field surveys and mechanistic experiments to test how transmission of the virulent trematode Ribeiroia ondatrae was affected by the diversity of both amphibian hosts and coinfecting parasites. Within natural wetlands, host and parasite species richness correlated positively, consistent with theoretical predictions. Among sites that supported Ribeiroia, however, host and parasite richness interacted to negatively affect Ribeiroia transmission between its snail and amphibian hosts, particularly in species-poor assemblages. In laboratory and outdoor experiments designed to decouple the relative contributions of host and parasite diversity, increases in host richness decreased Ribeiroia infection by 11–65%. Host richness also tended to decrease total infections by other parasite species (four of six instances), such that more diverse host assemblages exhibited ∼40% fewer infections overall. Importantly, parasite richness further reduced both per capita and total Ribeiroia infection by 15–20%, possibly owing to intrahost competition among coinfecting species. These findings provide evidence that parasitic and free-living diversity jointly regulate disease risk, help to resolve apparent contradictions in the diversity–disease relationship, and emphasize the challenges of integrating research on coinfection and host heterogeneity to develop a community ecology-based approach to infectious diseases.

Parasite transmission in complex communities: Predators and alternative hosts alter pathogenic infections in amphibians

While often studied in isolation, host-parasite interactions are typically embedded within complex communities. Other community members, including predators and alternative hosts, can therefore alter parasite transmission (e.g., the dilution effect), yet few studies have experimentally evaluated more than one such mechanism. Here, we used data from natural wetlands to design experiments investigating how alternative hosts and predators of parasites mediate trematode (Ribeiroia ondatrae) infection in a focal amphibian host (Pseudacris regilla). In short-term predation bioassays involving mollusks, zooplankton, fish, larval insects, or newts, four of seven tested species removed 62-93% of infectious stages. In transmission experiments, damselfly nymphs (predators) and newt larvae (alternative hosts) reduced infection in P. regilla tadpoles by -50%, whereas mosquitofish (potential predators and alternative hosts) did not significantly influence transmission. Additional bioassays indicated that predators consumed parasites even in the presence of alternative prey. In natural wetlands, newts had similar infection intensities as P. regilla, suggesting that they commonly function as alternative hosts despite their unpalatability to downstream hosts, whereas mosquitofish had substantially lower infection intensities and are unlikely to function as hosts. These results underscore the importance of studying host-parasite interactions in complex communities and of broadly linking research on predation, biodiversity loss, and infectious diseases.

Community ecology of invasions: direct and indirect effects of multiple invasive species on aquatic communities

With many ecosystems now supporting multiple nonnative species from different trophic levels, it can be challenging to disentangle the net effects of invaders within a community context. Here, we combined wetland surveys with a mesocosm experiment to examine the individual and combined effects of nonnative fish predators and nonnative bullfrogs on aquatic communities. Among 139 wetlands, nonnative fish (bass, sunfish, and mosquitofish) negatively influenced the probability of occupancy of Pacific treefrogs (Pseudacris regilla), but neither invader correlated strongly with occupancy by California newts (Taricha torosa), western toads (Anaxyrus boreas), or California red-legged frogs (Rana draytonii). In mesocosms, mosquitofish dramatically reduced the abundance of zooplankton and palatable amphibian larvae (P. regilla and T. torosa), leading to increases in nutrient concentrations and phytoplankton (through loss of zooplankton), and rapid growth of unpalatable toad larvae (through competitive release). Bullfrog larvae reduced the growth of native anurans but had no effect on survival. Despite strong effects on natives, invaders did not negatively influence one another, and their combined effects were additive. Our results highlight how the net effects of multiple nonnative species depend on the trophic level of each invader, the form and magnitude of invader interactions, and the traits of native community members.

Biomass and productivity of trematode parasites in pond ecosystems

1. Ecologists often measure the biomass and productivity of organisms to understand the importance of populations and communities in the flow of energy through ecosystems. Despite the central role of such studies in the advancement of freshwater ecology, there has been little effort to incorporate parasites into studies of freshwater energy flow. This omission is particularly important considering the roles that parasites sometimes play in shaping community structure and ecosystem processes. 2. Using quantitative surveys and dissections of over 1600 aquatic invertebrate and amphibian hosts, we calculated the ecosystem-level biomass and productivity of trematode parasites alongside the biomass of free-living aquatic organisms in three freshwater ponds in California, USA. 3. Snails and amphibian larvae, which are both important intermediate trematode hosts, dominated the dry biomass of free-living organisms across ponds (snails = 3.2 g m(-2); amphibians = 3.1 g m(-2)). An average of 33.5% of mature snails were infected with one of six trematode taxa, amounting to a density of 13 infected snails m(-2) of pond substrate. Between 18% and 33% of the combined host and parasite biomass within each infected snail consisted of larval trematode tissue, which collectively accounted for 87% of the total trematode biomass within the three ponds. Mid-summer trematode dry biomass averaged 0.10 g m(-2), which was equal to or greater than that of the most abundant insect orders (coleoptera = 0.10 g m(-2), odonata = 0.08 g m(-2), hemiptera = 0.07 g m(-2) and ephemeroptera = 0.03 g m(-2)). 4. On average, each trematode taxon produced between 14 and 1660 free-swimming larvae (cercariae) infected snail(-1) 24 h(-1) in mid-summer. Given that infected snails release cercariae for 3-4 months a year, the pond trematode communities produced an average of 153 mg m(-2) yr(-1) of dry cercarial biomass (range = 70-220 mg m(-2) yr(-1)). 5. Our results suggest that a significant amount of energy moves through trematode parasites in freshwater pond ecosystems, and that their contributions to ecosystem energetics may exceed those of many free-living taxa known to play key roles in structuring aquatic communities.

Taming wildlife disease: bridging the gap between science and management

Summary Parasites and pathogens of wildlife can threaten biodiversity, infect humans and domestic animals, and cause significant economic losses, providing incentives to manage wildlife diseases. Recent insights from disease ecology have helped transform our understanding of infectious disease dynamics and yielded new strategies to better manage wildlife diseases. Simultaneously, wildlife disease management (WDM) presents opportunities for large‐scale empirical tests of disease ecology theory in diverse natural systems. To assess whether the potential complementarity between WDM and disease ecology theory has been realized, we evaluate the extent to which specific concepts in disease ecology theory have been explicitly applied in peer‐reviewed WDM literature. While only half of WDM articles published in the past decade incorporated disease ecology theory, theory has been incorporated with increasing frequency over the past 40 years. Contrary to expectations, articles authored by academics were no more likely to apply disease ecology theory, but articles that explain unsuccessful management often do so in terms of theory. Some theoretical concepts such as density‐dependent transmission have been commonly applied, whereas emerging concepts such as pathogen evolutionary responses to management, biodiversity–disease relationships and within‐host parasite interactions have not yet been fully integrated as management considerations. Synthesis and applications. Theory‐based disease management can meet the needs of both academics and managers by testing disease ecology theory and improving disease interventions. Theoretical concepts that have received limited attention to date in wildlife disease management could provide a basis for improving management and advancing disease ecology in the future.

Species diversity reduces parasite infection through cross‐generational effects on host abundance

With growing interest in the effects of biodiversity on disease, there is a critical need for studies that empirically identify the mechanisms underlying the diversity-disease relationship. Here, we combined wetland surveys of host community structure with mechanistic experiments involving a multi-host parasite to evaluate competing explanations for the dilution effect. Sampling of 320 wetlands in California indicated that snail host communities were strongly nested, with competent hosts for the trematode Ribeiroia ondatrae predominating in low-richness assemblages and unsuitable hosts increasingly present in more diverse communities. Moreover, competent host density was negatively associated with increases in snail species richness. These patterns in host community assembly support a key prerequisite underlying the dilution effect. Results of multigenerational mesocosm experiments designed to mimic field-observed community assemblages allowed us to evaluate the relative importance of host density and diversity in influencing parasite infection success. Increases in snail species richness (from one to four species) had sharply negative effects on the density of infected hosts (-90% reduction). However, this effect was indirect; competition associated with non-host species led to a 95% reduction in host density (susceptible host regulation), owing primarily to a reduction in host reproduction. Among susceptible hosts, there were no differences in infection prevalence as a function of community structure, indicating a lack of support for a direct effect of diversity on infection (encounter reduction). In monospecific conditions, higher initial host densities increased infection among adult hosts; however, compensatory reproduction in the low-density treatments equalized the final number of infected hosts by the next generation, underscoring the relevance of multigenerational studies in understanding the dilution effect. These findings highlight the role of interspecific competition in mediating the relationship between species richness and parasite infection and emphasize the importance of field-informed experimental research in understanding mechanisms underlying the diversity-disease relationship.

Disease Ecology Meets Ecosystem Science

Growing evidence indicates that parasites—when considered—can play influential roles in ecosystem structure and function, highlighting the need to integrate disease ecology and ecosystem science. To strengthen links between these traditionally disparate fields, we identified mechanisms through which parasites can affect ecosystems and used empirical literature searches to explore how commonly such mechanisms have been documented, the ecosystem properties affected, and the types of ecosystems in which they occur. Our results indicate that ecosystem-disease research has remained consistently rare, comprising less than 2% of disease ecology publications. Existing studies from terrestrial, freshwater, and marine systems, however, demonstrate that parasites can strongly affect (1) biogeochemical cycles of water, carbon, nutrients, and trace elements, (2) fluxes of biomass and energy, and (3) temporal ecosystem dynamics including disturbance, succession, and stability. Mechanistically, most studies have demonstrated density-mediated indirect effects, rather than trait-mediated effects, or direct effects of parasites, although whether this is representative remains unclear. Looking forward, we highlight the importance of applying traits-based approaches to predict when parasites are most likely to exert ecosystem-level effects. Future research should include efforts to extend host–parasite studies across levels of ecological organization, large-scale manipulations to experimentally quantify ecosystem roles of parasites, and the integration of parasites and disease into models of ecosystem functioning.

Habitat heterogeneity drives the host-diversity-begets-parasite-diversity relationship: evidence from experimental and field studies

Despite a century of research into the factors that generate and maintain biodiversity, we know remarkably little about the drivers of parasite diversity. To identify the mechanisms governing parasite diversity, we combined surveys of 8100 amphibian hosts with an outdoor experiment that tested theory developed for free-living species. Our analyses revealed that parasite diversity increased consistently with host diversity due to habitat (i.e. host) heterogeneity, with secondary contributions from parasite colonisation and host abundance. Results of the experiment, in which host diversity was manipulated while parasite colonisation and host abundance were fixed, further reinforced this conclusion. Finally, the coefficient of host diversity on parasite diversity increased with spatial grain, which was driven by differences in their species-area curves: while host richness quickly saturated, parasite richness continued to increase with neighbourhood size. These results offer mechanistic insights into drivers of parasite diversity and provide a hierarchical framework for multi-scale disease research.

Food web including infectious agents for a California freshwater pond

This data set presents a comprehensive food web for Quick Pond, a northern California pond ecosystem. The web includes organisms from all regions of the pond (i.e., littoral, limnetic, profundal, and benthic zones) as well as terrestrial organisms that interact with the aquatic community or have aquatic life-stages. The food web has three attributes that are often omitted from freshwater food webs: inclusion of (1) parasites and other infectious agents, (2) ontogenetic stages of most animals with complex life cycles, and (3) biomass information for many animals. Data on species presence was obtained over three years using field sampling techniques (i.e., seine- and D-nets, stove-pipe samplers, and visual encounter surveys) and laboratory examinations of free-living organisms for infectious agents (primarily metazoan parasites, but also some microbes). We collected body size and biomass data for abundant aquatic animals >1 mm and for trematode parasites, which were the most abundant parasitic group. Inform...