Outbreak of parasite-induced limb malformations in a declining amphibian species in Colorado.

The detection of severe limb malformations in metamorphosing northern leopard frogs (Rana pipiens) from a Colorado pond in August 2022 prompted questions about the cause(s) and concern over the implications. Northern leopard frogs, which are a Tier 1 Species of Greatest Conservation Need in Colorado, have declined over much of their range in the state, particularly along the Front Range. Although malformations in amphibians have been reported in other parts of the USA, they are rare in Colorado, and the current case represents the most severe hotspot reported in the state for over 70 years. Across three survey events in late summer and early fall of 2022, approximately 68% of captured leopard frogs (late-stage larvae and metamorphic frogs) exhibited one or more malformations. Malformations exclusively affected the hind limbs and were dominated by skin webbings (51.7% of the total), bony triangles (32.2%), and extra limbs or digits (11%). Many animals had multiple malformations that limited the movement of one or both limbs (average of 2.3 malformations per malformed frog). Dissection of a subset of animals coupled with 28S rDNA genetic sequencing revealed the occurrence of the trematode Ribeiroia ondatrae at an average of 75.2 trematode cysts (metacercariae) per frog. The parasite was also detected in 2.6% of dissected snails (Helisoma trivolvis), which function as the trematode's first intermediate host. The relatively high loads of infection detected here - coupled with the similarity of observed malformations to those previously linked to R. ondatrae in experimental studies and from other malformation hotspots in the USA - offer compelling evidence that the current case is the result of parasite infection. Unresolved questions include why malformation prevalence was so high in 2022 and the degree to which such abnormalities will affect population persistence for local leopard frogs, particularly if malformations continue.

Are novel or locally adapted pathogens more devastating and why? Resolving opposing hypotheses.

There is a rich literature highlighting that pathogens are generally better adapted to infect local than novel hosts, and a separate seemingly contradictory literature indicating that novel pathogens pose the greatest threat to biodiversity and public health. Here, using Batrachochytrium dendrobatidis, the fungus associated with worldwide amphibian declines, we test the hypothesis that there is enough variance in "novel" (quantified by geographic and phylogenetic distance) host-pathogen outcomes to pose substantial risk of pathogen introductions despite local adaptation being common. Our continental-scale common garden experiment and global-scale meta-analysis demonstrate that local amphibian-fungal interactions result in higher pathogen prevalence, pathogen growth, and host mortality, but novel interactions led to variable consequences with especially virulent host-pathogen combinations still occurring. Thus, while most pathogen introductions are benign, enough variance exists in novel host-pathogen outcomes that moving organisms around the planet greatly increases the chance of pathogen introductions causing profound harm.

Effects of predation risk on parasite-host interactions and wildlife diseases.

Landscapes of fear can determine the dynamics of entire ecosystems. In response to perceived predation risk, prey can show physiological, behavioral, or morphological trait changes to avoid predation. This in turn can indirectly affect other species by modifying species interactions (e.g., altered feeding), with knock-on effects, such as trophic cascades, on the wider ecosystem. While such indirect effects stemming from the fear of predation have received extensive attention for herbivore-plant and predator-prey interactions, much less is known about how they alter parasite-host interactions and wildlife diseases. In this synthesis, we present a conceptual framework for how predation risk-as perceived by organisms that serve as hosts-can affect parasite-host interactions, with implications for infectious disease dynamics. By basing our approach on recent conceptual advances with respect to predation risk effects, we aim to expand this general framework to include parasite-host interactions and diseases. We further identify pathways through which parasite-host interactions can be affected, for example, through altered parasite avoidance behavior or tolerance of hosts to infections, and discuss the wider relevance of predation risk for parasite and host populations, including heuristic projections to population-level dynamics. Finally, we highlight the current unknowns, specifically the quantitative links from individual-level processes to population dynamics and community structure, and emphasize approaches to address these knowledge gaps.

Diverging effects of host density and richness across biological scales drive diversity-disease outcomes.

Understanding how biodiversity affects pathogen transmission remains an unresolved question due to the challenges in testing potential mechanisms in natural systems and how these mechanisms vary across biological scales. By quantifying transmission of an entire guild of parasites (larval trematodes) within 902 amphibian host communities, we show that the community-level drivers of infection depend critically on biological scale. At the individual host scale, increases in host richness led to fewer parasites per host for all parasite taxa, with no effect of host or predator densities. At the host community scale, however, the inhibitory effects of richness were counteracted by associated increases in total host density, leading to no overall change in parasite densities. Mechanistically, we find that while average host competence declined with increasing host richness, total community competence remained stable due to additive assembly patterns. These results help reconcile disease-diversity debates by empirically disentangling the roles of alternative ecological drivers of parasite transmission and how such effects depend on biological scale.

Into the danger zone: How the within-host distribution of parasites controls virulence.

Despite the importance of virulence in epidemiological theory, the relative contributions of host and parasite to virulence outcomes remain poorly understood. Here, we use reciprocal cross experiments to disentangle the influence of host and parasite on core virulence components-infection and pathology-and understand dramatic differences in parasite-induced malformations in California amphibians. Surveys across 319 populations revealed that amphibians' malformation risk was 2.7× greater in low-elevation ponds, even while controlling for trematode infection load. Factorial experiments revealed that parasites from low-elevation sites induced higher per-parasite pathology (reduced host survival and growth), whereas there were no effects of host source on resistance or tolerance. Parasite populations also exhibited marked differences in within-host distribution: ~90% of low-elevation cysts aggregated around the hind limbs, relative to <60% from high-elevation. This offers a novel, mechanistic basis for regional variation in parasite-induced malformations while promoting a framework for partitioning host and parasite contributions to virulence.