Using multi-response models to investigate pathogen coinfections across scales: insights from emerging diseases of amphibians.
ABSTRACT: Associations among parasites affect many aspects of host-parasite dynamics, but a lack of analytical tools has limited investigations of parasite correlations in observational data that are often nested across spatial and biological scales.Here we illustrate how hierarchical, multiresponse modeling can characterize parasite associations by allowing for hierarchical structuring, offering estimates of uncertainty, and incorporating correlational model structures. After introducing the general approach, we apply this framework to investigate coinfections among four amphibian parasites (the trematodes Ribeiroia ondatrae and Echinostoma spp., the chytrid fungus Batrachochytrium dendrobatidis, and ranaviruses) and among >2000 individual hosts, 90 study sites, and five amphibian host species.Ninety-two percent of sites and 80% of hosts supported two or more pathogen species. Our results revealed strong correlations between parasite pairs that varied by scale (from among hosts to among sites) and classification (microparasite versus macroparasite), but were broadly consistent across taxonomically diverse host species. At the host-scale, infection by the trematode R. ondatrae correlated positively with the microparasites, B. dendrobatidis and ranavirus, which were themselves positively associated. However, infection by a second trematode (Echinostoma spp.) correlated negatively with B. dendrobatidis and ranavirus, both at the host- and site-level scales, highlighting the importance of differential relationships between micro- and macroparasites.Given the extensive number of coinfecting symbiont combinations inherent to natural systems, particularly across multiple host species, multiresponse modeling of cross-sectional field data offers a valuable tool to identify a tractable number of hypothesized interactions for experimental testing while accounting for uncertainty and potential sources of co-exposure. For amphibians specifically, the high frequency of co-occurrence and coinfection among these pathogens - each of which is known to impair host fitness or survival - highlights the urgency of understanding parasite associations for conservation and disease management.
Project description:The rapid pace of environmental change is driving multi-faceted shifts in abiotic factors that influence parasite transmission. However, cumulative effects of these factors on wildlife diseases remain poorly understood. Here we used an information-theoretic approach to compare the relative influence of abiotic factors (temperature, diurnal temperature range, nutrients and pond-drying), on infection of snail and amphibian hosts by two trematode parasites (Ribeiroia ondatrae and Echinostoma spp.). A temperature shift from 20 to 25 °C was associated with an increase in infected snail prevalence of 10-20%, while overall snail densities declined by a factor of 6. Trematode infection abundance in frogs was best predicted by infected snail density, while Ribeiroia infection specifically also declined by half for each 10% reduction in pond perimeter, despite no effect of perimeter on the per snail release rate of cercariae. Both nutrient concentrations and Ribeiroia infection positively predicted amphibian deformities, potentially owing to reduced host tolerance or increased parasite virulence in more productive environments. For both parasites, temperature, pond-drying, and nutrients were influential at different points in the transmission cycle, highlighting the importance of detailed seasonal field studies that capture the importance of multiple drivers of infection dynamics and the mechanisms through which they operate.
Project description:Variation in host species composition can dramatically alter parasite transmission in natural communities. Whether diverse host communities dilute or amplify parasite transmission is thought to depend critically on species traits, particularly on how hosts affect each other's densities, and their relative competency as hosts. Here we studied a community of potential hosts and/or decoys (i.e. non-competent hosts) for two trematode parasite species, Echinostoma trivolvis and Ribeiroia ondatrae, which commonly infect wildlife across North America. We manipulated the density of a focal host (green frog tadpoles, Rana clamitans), in concert with manipulating the diversity of alternative species, to simulate communities where alternative species either (1) replace the focal host species so that the total number of individuals remains constant (substitution) or (2) add to total host density (addition). For E. trivolvis, we found that total parasite transmission remained roughly equal (or perhaps decreased slightly) when alternative species replaced focal host individuals, but parasite transmission was higher when alternative species were added to a community without replacing focal host individuals. Given the alternative species were roughly equal in competency, these results are consistent with current theory. Remarkably, both total tadpole and per-capita tadpole infection intensity by E. trivolvis increased with increasing intraspecific host density. For R. ondatrae, alternative species did not function as effective decoys or hosts for parasite infective stages, and the diversity and density treatments did not produce clear changes in parasite transmission, although high tank to tank variation in R. ondatrae infection could have obscured patterns.
Project description:This experiment examined the transcriptional response of juvenile amphibian hosts (common frog, Rana temporaria) to two important amphibian pathogens: Batrachochytrium dendrobatidis (Bd) and Ranavirus. Common frogs are non-model organisms which do not have a reference genome.
Project description: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.
Project description:The widespread emergence of human and wildlife diseases has challenged ecologists to understand how large-scale agents of environmental change affect host-pathogen interactions. Accelerated eutrophication of aquatic ecosystems owing to nitrogen and phosphorus enrichment is a pervasive form of environmental change that has been implicated in the emergence of diseases through direct and indirect pathways. We provide experimental evidence linking eutrophication and disease in a multihost parasite system. The trematode parasite Ribeiroia ondatrae sequentially infects birds, snails, and amphibian larvae, frequently causing severe limb deformities and mortality. Eutrophication has been implicated in the emergence of this parasite, but definitive evidence, as well as a mechanistic understanding, have been lacking until now. We show that the effects of eutrophication cascade through the parasite life cycle to promote algal production, the density of snail hosts, and, ultimately, the intensity of infection in amphibians. Infection also negatively affected the survival of developing amphibians. Mechanistically, eutrophication promoted amphibian disease through two distinctive pathways: by increasing the density of infected snail hosts and by enhancing per-snail production of infectious parasites. Given forecasted increases in global eutrophication, amphibian extinctions, and similarities between Ribeiroia and important human and wildlife pathogens, our results have broad epidemiological and ecological significance.
Project description:A key challenge surrounding ongoing climate shifts is to identify how they alter species interactions, including those between hosts and parasites. Because transmission often occurs during critical time windows, shifts in the phenology of either taxa can alter the likelihood of interaction or the resulting pathology. We quantified how phenological synchrony between vulnerable stages of an amphibian host (<i>Pseudacris regilla</i>) and infection by a pathogenic trematode (<i>Ribeiroia ondatrae</i>) determined infection prevalence, parasite load and host pathology. By tracking hosts and parasite infection throughout development between low- and high-elevation regions (San Francisco Bay Area and the Southern Cascades (Mt Lassen)), we found that when phenological synchrony was high (Bay Area), each established parasite incurred a 33% higher probability of causing severe limb malformations relative to areas with less synchrony (Mt Lassen). As a result, hosts in the Bay Area had up to a 50% higher risk of pathology even while controlling for the mean infection load. Our results indicate that host-parasite interactions and the resulting pathology were the joint product of infection load and phenological synchrony, highlighting the sensitivity of disease outcomes to forecasted shifts in climate.
Project description:By definition, parasites harm their hosts. However, some forms of parasite-induced alterations increase parasite transmission between hosts, such that manipulated hosts can be considered extensions of the parasite's phenotype. While well accepted in principle, surprisingly few studies have quantified how parasite manipulations alter host performance and survival under field and laboratory conditions.By interfering with limb development, the trematode Ribeiroia ondatrae causes particularly severe morphological alterations within amphibian hosts that provide an ideal system to evaluate parasite-induced changes in phenotype. Here, we coupled laboratory performance trials with a capture-mark-recapture study of 1388 Pacific chorus frogs (Pseudacris regilla) to quantify the effects of parasite-induced malformations on host locomotion, foraging, and survival. Malformations, which affected ? 50% of metamorphosing frogs in nature, caused dramatic reductions in all measures of organismal function. Malformed frogs exhibited significantly shorter jumping distances (41% reduction), slower swimming speeds (37% reduction), reduced endurance (66% reduction), and lower foraging success relative to infected hosts without malformations. Furthermore, while normal and malformed individuals had comparable survival within predator-free exclosures, deformed frogs in natural populations had 22% lower biweekly survival than normal frogs and rarely recruited to the adult population over a two-year period.Our results highlight the ability of parasites to deeply alter multiple dimensions of host phenotype with important consequences for performance and survival. These patterns were best explained by malformation status, rather than infection per se, helping to decouple the direct and indirect effects of parasitism on host fitness.
Project description:Emerging diseases have been increasingly associated with population declines, with co-infections exhibiting many types of interactions. The chytrid fungus (Batrachochytrium dendrobatidis) and ranaviruses have extraordinarily broad host ranges, however co-infection dynamics have been largely overlooked. We investigated the pattern of co-occurrence of these two pathogens in an amphibian assemblage in Serra da Estrela (Portugal). The detection of chytridiomycosis in Portugal was linked to population declines of midwife-toads (Alytes obstetricans). The asynchronous and subsequent emergence of a second pathogen - ranavirus - caused episodes of lethal ranavirosis. Chytrid effects were limited to high altitudes and a single host, while ranavirus was highly pathogenic across multiple hosts, life-stages and altitudinal range. This new strain (Portuguese newt and toad ranavirus - member of the CMTV clade) caused annual mass die-offs, similar in host range and rapidity of declines to other locations in Iberia affected by CMTV-like ranaviruses. However, ranavirus was not always associated with disease, mortality and declines, contrasting with previous reports on Iberian CMTV-like ranavirosis. We found little evidence that pre-existing chytrid emergence was associated with ranavirus and the emergence of ranavirosis. Despite the lack of cumulative or amplified effects, ranavirus drove declines of host assemblages and changed host community composition and structure, posing a grave threat to all amphibian populations.
Project description:Amphibians are experiencing global declines and extinctions, with infectious diseases representing a major factor. In this study we examined the transcriptional response of metamorphic hosts (common frog, Rana temporaria) to the two most important amphibian pathogens: Batrachochytrium dendrobatidis (Bd) and Ranavirus. We found strong up-regulation of a gene involved in the adaptive immune response (AP4S1) at four days post-exposure to both pathogens. We detected a significant transcriptional response to Bd, covering the immune response (innate and adaptive immunity, complement activation, and general inflammatory responses), but relatively little transcriptional response to Ranavirus. This may reflect the higher mortality rates found in wild common frogs infected with Ranavirus as opposed to Bd. These data provide a valuable genomic resource for the amphibians, contribute insight into gene expression changes after pathogen exposure, and suggest potential candidate genes for future host-pathogen research.
Project description:Predators have documented post-encounter (density-mediated) effects on prey but their pre-encounter impacts, including behavioural alterations, can be substantial as well. While it is increasingly evident that this "ecology of fear" is important to understand for natural enemy-victim relationships, fear responses of hosts to the threat of infection by a parasite are relatively unknown. We examined larval amphibian (Lithobates pipiens) foraging choices by experimentally manipulating the presence of cues relating to predator (larval odonate) or parasite (the trematode Ribeiroia ondatrae) threats. Tadpoles avoided foraging where predator or parasite cues were present; however, they did not treat these as equal hazards. When both threats were simultaneously present, tadpoles strongly preferred to forage under the threat of parasitism compared to predation, likely driven by their relative lethality in our study. Our results indicate that altered spatial use is an important anti-parasite behaviour, and demonstrate that parasite avoidance can affect foraging in a manner similar to predators, warranting greater study of the pre-encounter effects of this enemy type.