All hosts are not equal: explaining differential patterns of malformations in an amphibian community

1. Within a community, different host species often exhibit broad variation in sensitivity to infection and disease. Because such differences can influence the strength and outcome of community interactions, it is essential to understand differential disease patterns and identify the mechanisms responsible. 2. In North American wetlands, amphibian species often exhibit extraordinary differences in the frequency of limb malformations induced by the digenetic trematode, Ribeiroia ondatrae. By coupling field studies with parasite exposure experiments, we evaluated whether such patterns were due to differences in (i) parasite encounter rate, (ii) infection establishment, or (iii) parasite persistence within hosts. 3. Field results underscored the broad variation in malformations and infection between host species; while nearly 60% (n = 618) of emerging American toads exhibited severe limb deformities such as bony triangles, skin webbings and missing limbs, fewer than 4% (n = 251) of Eastern gray treefrogs from the same pond were abnormal. Despite similarities in the phenology and larval development period of these species, they differed sharply in Ribeiroia infection. On average, toads supported 75x more metacercariae than did metamorphic treefrogs. 4. Experimental exposures of larval toads and treefrogs to a realistic range of Ribeiroia cercariae revealed strong differences in the sensitivity of these species to infection; exposed toads suffered elevated mortality (up to 95%), delayed metamorphosis, and severe limb malformations consistent with field observations. Treefrogs, in contrast, exhibited limited mortality and no malformations, regardless of exposure level. Ribeiroia cercariae were substantially less successful in locating and infecting Hyla versicolor larvae. 5. Our results indicate that the observed differences in infection and malformations owe to a lower ability of Ribeiroia cercariae to both find and establish within larval treefrogs, possibly stemming from a heightened immune response to infection. Because Ribeiroia is a highly pathogenic parasite with negative effects on larval and metamorphic amphibian survival, variation in infection resistance among species could have important implications for understanding patterns of species co-occurrence, competition, and community diversity.     

Chance or choice? Understanding parasite selection and infection in multi-host communities

Ongoing debate over the relationship between biodiversity and disease risk underscores the need to develop a more mechanistic understanding of how changes in host community composition influence parasite transmission, particularly in complex communities with multiple hosts. A key challenge involves determining how motile parasites select among potential hosts and the degree to which this process shifts with community composition. Focusing on interactions between larval amphibians and the pathogenic trematode Ribeiroia ondatrae, we designed a novel, large-volume set of choice chambers to assess how the selectivity of free-swimming infectious parasites varied among five host species and in response to changes in assemblage composition (four different permutations). In a second set of trials, cercariae were allowed to contact and infect hosts, allowing comparison of host-parasite encounter rates (parasite choice) with infection outcomes (successful infections). Cercariae exhibited consistent preferences for specific host species that were independent of the community context; large-bodied amphibians, such as larval bullfrogs (Rana catesbeiana), exhibited the highest level of parasite attraction. However, because host attractiveness was decoupled from susceptibility to infection, assemblage composition sharply affected both per-host infection as well as total infection (summed among co-occurring hosts). Species such as the non-native R. catesbeiana functioned as epidemiological ‘sinks’ or dilution hosts, attracting a disproportionate fraction of parasites relative to the number that established successfully, whereas Taricha granulosa and especially Pseudacris regilla supported comparatively more metacercariae relative to cercariae selection. These findings provide a framework for integrating information on parasite preference in combination with more traditional factors such as host competence and density to forecast how changes within complex communities will affect parasite transmission.     

Host Density and Competency Determine the Effects of Host Diversity on Trematode Parasite Infection

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.     

Amphibian deformities and Ribeiroia infection: an emerging helminthiasis

Since their widespread appearance in the mid-1990s, malformed amphibians have evoked fear, as well as fascination within the scientific and public communities. Recent evidence from field and laboratory studies has implicated infection by a digenetic trematode--Ribeiroia ondatrae--as an important cause of such deformities. Ribeiroia spp. have a complex life cycle involving planorbid snails, amphibians and water birds. Under natural conditions, malformations might promote parasite transmission by increasing the susceptibility of infected amphibians to predation by definitive hosts. However, with respect to the recent outbreak of deformities, we suggest that exogenous agents (e.g. pesticides, nutrient run-off, introduced fishes) might be interacting with Ribeiroia, resulting in elevated infection levels, and we highlight the need for studies incorporating multiple stressor dynamics to further explore this problem.     

Linking community assembly and structure across scales in a wild mouse parasite community

Understanding what processes drive community structure is fundamental to ecology. Many wild animals are simultaneously infected by multiple parasite species, so host–parasite communities can be valuable tools for investigating connections between community structures at multiple scales, as each host can be considered a replicate parasite community. Like free‐living communities, within‐host–parasite communities are hierarchical; ecological interactions between hosts and parasites can occur at multiple scales (e.g., host community, host population, parasite community within the host), therefore, both extrinsic and intrinsic processes can determine parasite community structure. We combine analyses of community structure and assembly at both the host population and individual scales using extensive datasets on wild wood mice (Apodemus sylvaticus) and their parasite community. An analysis of parasite community nestedness at the host population scale provided predictions about the order of infection at the individual scale, which were then tested using parasite community assembly data from individual hosts from the same populations. Nestedness analyses revealed parasite communities were significantly more structured than random. However, observed nestedness did not differ from null models in which parasite species abundance was kept constant. We did not find consistency between observed community structure at the host population scale and within‐host order of infection. Multi‐state Markov models of parasite community assembly showed that a host's likelihood of infection with one parasite did not consistently follow previous infection by a different parasite species, suggesting there is not a deterministic order of infection among the species we investigated in wild wood mice. Our results demonstrate that patterns at one scale (i.e., host population) do not reliably predict processes at another scale (i.e., individual host), and that neutral or stochastic processes may be driving the patterns of nestedness observed in these communities. We suggest that experimental approaches that manipulate parasite communities are needed to better link processes at multiple ecological scales.     

Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk

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 'pace-of-life' 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 ('fast-species') 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.     

Experimental exposure of Helisoma trivolvis and Biomphalaria glabrata (Gastropoda) to Ribeiroia ondatrae (Trematoda)

Experimental infections provide an important foundation for understanding host responses to parasites. While infections with Ribeiroia ondatrae cause mortality and malformations in a wide range of amphibian second intermediate host species, little is known about how the parasite affects its snail first intermediate hosts or even what species can support infection. In this study, we experimentally exposed Helisoma trivolvis, a commonly reported host of R. ondatrae, and Biomphalaria glabrata, a confamilial snail known to host Ribeiroia marini, to increasing concentrations of embryonated eggs of R. ondatrae obtained from surrogate definitive hosts. Over the course of 8 wk, we examined the effect of parasite exposure on infection status, time-to-cercariae release, host size, and mortality of both snail species. Helisoma trivolvis was a highly competent host for R. ondatrae infection, with over 93% infection in all exposed snails, regardless of egg exposure level. However, no infections were detected among exposed B. glabrata, despite previous accounts of this snail hosting a congener parasite. Among exposed H. trivolvis, high parasite exposure reduced growth, decreased time-to-cercariae release, and caused marginally significant increases in mortality. Interestingly, while B. glabrata snails did not become infected with R. ondatrae, individuals exposed to 650 R. ondatrae eggs grew less rapidly than unexposed snails, suggesting a sub-lethal energetic cost associated with parasite exposure. Our results highlight the importance of using experimental infections to understand the effects of parasite exposure on host- and non-host species, each of which can be affected by exposure.     

Parasite establishment and host extinction in model communities

Studies of host–parasite dynamics usually consider one, or at most two, host species, neglecting the possible effects of other species on the focal hosts and vice versa. To explore the interaction of community structure with host–parasite dynamics, we model the invasion of stable communities of varying size by a parasite. The communities are generated with random interaction coefficients and connectance 0.5. Each community is invaded by parasites with different values of virulence (disease-induced host mortality rate), specificity and transmission rate. The result of each invasion is determined by numerically simulating the dynamics of the community. We classify the outcomes by whether the parasite successfully establishes in the focal host population(s), and, if so, by the proportion of host and non-host species that go extinct as a result of the parasite's introduction. We discuss how the structure of the community and the interaction between hosts and other species affect several important processes of disease ecology: the density threshold for parasite invasion, extinction cascades caused by the parasite, and the frequency of extinctions of hosts and non-hosts. In our simulated communities, non-host species went extinct more frequently than hosts, suggesting the importance of the community context of disease. In some cases, the parasite's invasion induced regular population cycles in the previously stable community.     

Continental‐extent patterns in amphibian malformations linked to parasites,chemical contaminants,and their interactions

Widespread observations of malformed amphibians across North America have generated both concern and controversy. Debates over the causes of such malformations—which can affect >50% of animals in a population—have continued, likely due to involvement of multiple causal factors. Here, we used a 13‐year dataset encompassing 53,880 frogs and toads from 422 wetlands and 42 states in the conterminous USA to test hypotheses relating abnormalities and four categories of potential drivers: (i) chemical contaminants, (ii) land use practices, (iii) parasite infection, and (iv) targeted interactions between parasites and pesticides. Using a hierarchically nested, competing‐model approach, we further examined how these associations varied spatially among geographic regions. Although malformations were rare overall (average = 1.6%), we identified 96 hotspot sites with 5%–25% abnormal individuals. Using the full dataset of 934 collections (without data on parasite infection), malformation frequency was best predicted by the presence of oil and gas wells within the watershed. Among collections also examined for parasite infection (n = 154), average parasite load and its interaction with pesticide application positively predicted malformations: wetlands with a greater abundance of the trematode Ribeiroia ondatrae were more likely to have malformed amphibians, but these effects were strongest when pesticide application was also high, consistent with prior experimental research. Importantly, however, the influence of these factors also varied regionally, helping explain divergent results from previous studies at local scales; parasite infection was more influential in the West and Northeast, whereas pesticide application and oil/gas wells correlated with abnormalities in the Northeast, Southeast, and western regions of the USA. These results, based on the largest systematic sampling of amphibian malformations, suggest that increased observations of abnormal amphibians are associated with both parasite infection and chemical contaminants, but that their relative importance and interaction strength varied with the spatial extent of the analysis.     

Temperature‐driven shifts in a host‐parasite interaction drive nonlinear changes in disease risk

Climate change may shift the timing and consequences of interspecific interactions, including those important to disease spread. Because hosts and pathogens may respond differentially to climate shifts, however, predicting the net effects on disease patterns remains challenging. Here, we used field data to guide a series of laboratory experiments that systematically evaluated the effects of temperature on the full infection process, including survival, penetration, establishment, persistence, and virulence of a highly pathogenic trematode (Ribeiroia ondatrae), and the development and survival of its amphibian host. Our results revealed nonlinearities in pathology as a function of temperature, which likely resulted from changes in both host and parasite processes. Both hosts and parasites responded strongly to temperature; hosts accelerated development while parasites showed enhanced host penetration but reduced establishment (encystment) and survival outside the host. While there were no differences in host survival among treatments, we observed a mid‐temperature peak in parasite‐induced deformities (63% at 20 °C), with the lowest frequency of deformities (12%) occurring at the highest temperature (26 °C). This nonlinear effect could result from temperature‐driven changes in parasite burden owing to shifts in host penetration and/or clearance, reductions in host vulnerability owing to faster development, or both. Furthermore, despite strong temperature‐driven changes in parasite penetration, survival, and establishment, the opposing nature of these effects lead to no difference in tadpole parasite burdens shortly after infection. These findings suggest that temperature‐driven changes to the disease process may not be easily observable from comparison of parasite burdens alone, but multi‐tiered experiments quantifying the responses of hosts, parasites and their interactions can enhance our ability to predict temperature‐driven changes to disease risk. Climate‐driven changes to disease patterns will therefore depend on underlying shifts in host and parasite development rates and the timing of their interactions.     

Predation and disease: understanding the effects of predators at several trophic levels on pathogen transmission

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Parasites in the food web: linking amphibian malformations and aquatic eutrophication

Emerging diseases are an ever‐growing affliction of both humans and wildlife. By exploring recent increases in amphibian malformations (e.g. extra or missing limbs), we illustrate the importance of food web theory and community ecology for understanding and controlling emerging infections. Evidence points to a native parasite, Ribeiroia ondatrae, as the primary culprit of these malformations, but reasons for the increase have remained conjectural. We suggest that the increase is a consequence of complex changes to aquatic food webs resulting from anthropogenic disturbance. Our results implicate cultural eutrophication as a driver of elevated parasitic infection: (1) eutrophication causes a predator‐mediated shift in snail species composition toward Planorbella spp., (2) Planorbella are the exclusive first intermediate hosts of R. ondatrae and (3) Ribeiroia infection is a strong predictor of amphibian malformation levels. Our study illustrates how the effects of anthropogenic disturbance on epidemic disease can be mediated through direct and indirect changes in food web structure.     

Does timing matter? How priority effects influence the outcome of parasite interactions within hosts

In nature, hosts are exposed to an assemblage of parasite species that collectively form a complex community within the host. To date, however, our understanding of how within-host–parasite communities assemble and interact remains limited. Using a larval amphibian host (Pacific chorus frog, Pseudacris regilla) and two common trematode parasites (Ribeiroia ondatrae and Echinostoma trivolvis), we experimentally examined how the sequence of host exposure influenced parasite interactions within hosts. While there was no evidence that the parasites interacted when hosts were exposed to both parasites simultaneously, we detected evidence of both intraspecific and interspecific competition when exposures were temporally staggered. However, the strength and outcome of these priority effects depended on the sequence of addition, even after accounting for the fact that parasites added early in host development were more likely to encyst compared to parasites added later. Ribeiroia infection success was reduced by 14 % when Echinostoma was added prior to Ribeiroia, whereas no such effect was noted for Echinostoma when Ribeiroia was added first. Using a novel fluorescent-labeling technique that allowed us to track Ribeiroia infections from different exposure events, we also discovered that, similar to the interspecific interactions, early encysting parasites reduced the encystment success of later arriving parasites by 41 %, which could be mediated by host immune responses and/or competition for space. These results suggest that parasite identity interacts with host immune responses to mediate parasite interactions within the host, such that priority effects may play an important role in structuring parasite communities within hosts. This knowledge can be used to assess host–parasite interactions within natural communities in which environmental conditions can lead to heterogeneity in the timing and composition of host exposure to parasites.     

Fine-scale variation in vector host use and force of infection drive localized patterns of West Nile virus transmission

The influence of host diversity on multi-host pathogen transmission and persistence can be confounded by the large number of species and biological interactions that can characterize many transmission systems. For vector-borne pathogens, the composition of host communities has been hypothesized to affect transmission; however, the specific characteristics of host communities that affect transmission remain largely unknown. We tested the hypothesis that vector host use and force of infection (i.e., the summed number of infectious mosquitoes resulting from feeding upon each vertebrate host within a community of hosts), and not simply host diversity or richness, determine local infection rates of West Nile virus (WNV) in mosquito vectors. In suburban Chicago, Illinois, USA, we estimated community force of infection for West Nile virus using data on Culex pipiens mosquito host selection and WNV vertebrate reservoir competence for each host species in multiple residential and semi-natural study sites. We found host community force of infection interacted with avian diversity to influence WNV infection in Culex mosquitoes across the study area. Two avian species, the American robin (Turdus migratorius) and the house sparrow (Passer domesticus), produced 95.8% of the infectious Cx. pipiens mosquitoes and showed a significant positive association with WNV infection in Culex spp. mosquitoes. Therefore, indices of community structure, such as species diversity or richness, may not be reliable indicators of transmission risk at fine spatial scales in vector-borne disease systems. Rather, robust assessment of local transmission risk should incorporate heterogeneity in vector host feeding and variation in vertebrate reservoir competence at the spatial scale of vector-host interaction.     

Eutrophication,biodiversity loss,and species invasions modify the relationship between host and parasite richness during host community assembly

Host and parasite richness are generally positively correlated, but the stability of this relationship in response to global change remains poorly understood. Rapidly changing biotic and abiotic conditions can alter host community assembly, which in turn, can alter parasite transmission. Consequently, if the relationship between host and parasite richness is sensitive to parasite transmission, then changes in host composition under various global change scenarios could strengthen or weaken the relationship between host and parasite richness. To test the hypothesis that host community assembly can alter the relationship between host and parasite richness in response to global change, we experimentally crossed host diversity (biodiversity loss) and resource supply to hosts (eutrophication), then allowed communities to assemble. As previously shown, initial host diversity and resource supply determined the trajectory of host community assembly, altering post‐assembly host species richness, richness‐independent host phylogenetic diversity, and colonization by exotic host species. Overall, host richness predicted parasite richness, and as predicted, this effect was moderated by exotic abundance—communities dominated by exotic species exhibited a stronger positive relationship between post‐assembly host and parasite richness. Ultimately, these results suggest that, by modulating parasite transmission, community assembly can modify the relationship between host and parasite richness. These results thus provide a novel mechanism to explain how global environmental change can generate contingencies in a fundamental ecological relationship—the positive relationship between host and parasite richness.     

Host community similarity and geography shape the diversity and distribution of haemosporidian parasites in Amazonian birds

Identifying the mechanisms driving the distribution and diversity of parasitic organisms and characterizing the structure of parasite assemblages are critical to understanding host–parasite evolution, community dynamics, and disease transmission risk. Haemosporidian parasites of the genera Plasmodium and Haemoproteus are a diverse and cosmopolitan group of bird pathogens. Despite their global distribution, the ecological and historical factors shaping the diversity and distribution of these protozoan parasites across avian communities and geographic regions remain unclear. Here we used a region of the mitochondrial cytochrome b gene to characterize the diversity, biogeographical patterns, and phylogenetic relationships of Plasmodium and Haemoproteus infecting Amazonian birds. Specifically, we asked whether, and how, host community similarity and geography (latitude and area of endemism) structure parasite assemblages across 15 avian communities in the Amazon Basin. We identified 265 lineages of haemosporidians recovered from 2661 sampled birds from 330 species. Infection prevalence varied widely among host species, avian communities, areas of endemism, and latitude. Composition analysis demonstrated that both malarial parasites and host communities differed across areas of endemism and as a function of latitude. Thus, areas with similar avian community composition were similar in their parasite communities. Our analyses, within a regional biogeographic context, imply that host switching is the main event promoting diversification in malarial parasites. Although dispersal of haemosporidian parasites was constrained across six areas of endemism, these pathogens are not dispersal‐limited among communities within the same area of endemism. Our findings indicate that the distribution of malarial parasites in Amazonian birds is largely dependent on local ecological conditions and host evolutionary relationships.     

Nonhost species reduce parasite infection in a focal host species within experimental fish communities

The dilution effect describes the negative association between host biodiversity and the risk of infectious disease. Tests designed to understand the relative roles of host species richness, host species identity, and rates of exposure within experimental host communities would help resolve ongoing contention regarding the importance and generality of dilution effects. We exposed fathead minnows to infective larvae of the trematode, Ornithodiplostomum ptychocheilus in minnow‐only containers and in mixed containers that held 1–3 other species of fish. Parasite infection was estimated as the number of encysted worms (i.e., brainworms) present in minnows following exposure. The results of exposure trials showed that nonminnow fish species were incompatible with O. ptychocheilus larvae. There was no reduction in mean brainworm counts in minnows in mixed containers with brook sticklebacks or longnose dace. In contrast, brainworm counts in minnows declined by 51% and 27% in mesocosms and aquaria, respectively, when they co‐occurred with emerald shiners. Dilution within minnow + shiner containers may arise from shiner‐induced alterations in minnow or parasite behaviors that reduced encounter rates between minnows and parasite larvae. Alternatively, shiners may act as parasite sinks for parasite larvae. These results highlight the role of host species identity in the dilution effect. Our results also emphasize the complex and idiosyncratic effects of host community composition on rates of parasite infection within contemporary host communities that contain combinations of introduced and native species.     

Frontiers in research on biodiversity and disease

Global losses of biodiversity have galvanised efforts to understand how changes to communities affect ecological processes, including transmission of infectious pathogens. Here, we review recent research on diversity–disease relationships and identify future priorities. Growing evidence from experimental, observational and modelling studies indicates that biodiversity changes alter infection for a range of pathogens and through diverse mechanisms. Drawing upon lessons from the community ecology of free‐living organisms, we illustrate how recent advances from biodiversity research generally can provide necessary theoretical foundations, inform experimental designs, and guide future research at the interface between infectious disease risk and changing ecological communities. Dilution effects are expected when ecological communities are nested and interactions between the pathogen and the most competent host group(s) persist or increase as biodiversity declines. To move beyond polarising debates about the generality of diversity effects and develop a predictive framework, we emphasise the need to identify how the effects of diversity vary with temporal and spatial scale, to explore how realistic patterns of community assembly affect transmission, and to use experimental studies to consider mechanisms beyond simple changes in host richness, including shifts in trophic structure, functional diversity and symbiont composition.     

Towards an eco‐phylogenetic framework for infectious disease ecology

Identifying patterns and drivers of infectious disease dynamics across multiple scales is a fundamental challenge for modern science. There is growing awareness that it is necessary to incorporate multi‐host and/or multi‐parasite interactions to understand and predict current and future disease threats better, and new tools are needed to help address this task. Eco‐phylogenetics (phylogenetic community ecology) provides one avenue for exploring multi‐host multi‐parasite systems, yet the incorporation of eco‐phylogenetic concepts and methods into studies of host pathogen dynamics has lagged behind. Eco‐phylogenetics is a transformative approach that uses evolutionary history to infer present‐day dynamics. Here, we present an eco‐phylogenetic framework to reveal insights into parasite communities and infectious disease dynamics across spatial and temporal scales. We illustrate how eco‐phylogenetic methods can help untangle the mechanisms of host–parasite dynamics from individual (e.g. co‐infection) to landscape scales (e.g. parasite/host community structure). An improved ecological understanding of multi‐host and multi‐pathogen dynamics across scales will increase our ability to predict disease threats.     

Disease and the extended phenotype: parasites control host performance and survival through induced changes in body plan

Background

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.

Methodology/Principal Findings

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.

Conclusions/Significance

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.