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.

It's a worm-eat-worm world: Consumption of parasite free-living stages protects hosts and benefits predators.

Predation on parasites is a common interaction with multiple, concurrent outcomes. Free-living stages of parasites can comprise a large portion of some predators' diets and may be important resources for population growth. Predation can also reduce the density of infectious agents in an ecosystem, with resultant decreases in infection rates. While predator-parasite interactions likely vary with parasite transmission strategy, few studies have examined how variation in transmission mode influences contact rates with predators and the associated changes in consumption risk. To understand how transmission mode mediates predator-parasite interactions, we examined associations between an oligochaete predator Chaetogaster limnaei that lives commensally on freshwater snails and nine trematode taxa that infect snails. Chaetogaster is hypothesized to consume active (i.e. mobile), free-living stages of trematodes that infect snails (miracidia), but not the passive infectious stages (eggs); it could thus differentially affect transmission and infection prevalence of parasites, including those with medical or veterinary importance. Alternatively, when infection does occur, Chaetogaster can consume and respond numerically to free-living trematode stages released from infected snails (cercariae). These two processes lead to contrasting predictions about whether Chaetogaster and trematode infection of snails correlate negatively ('protective predation') or positively ('predator augmentation'). Here, we tested how parasite transmission mode affected Chaetogaster-trematode relationships using data from 20,759 snails collected across 4 years from natural ponds in California. Based on generalized linear mixed modelling, snails with more Chaetogaster were less likely to be infected by trematodes that rely on active transmission. Conversely, infections by trematodes with passive infectious stages were positively associated with per-snail Chaetogaster abundance. Our results suggest that trematode transmission mode mediates the net outcome of predation on parasites. For trematodes with active infectious stages, predatory Chaetogaster limited the risk of snail infection and its subsequent pathology (i.e. castration). For taxa with passive infectious stages, no such protective effect was observed. Rather, infected snails were associated with higher Chaetogaster abundance, likely owing to the resource subsidy provided by cercariae. These findings highlight the ecological and epidemiological importance of predation on free-living stages while underscoring the influence of parasite life history in shaping such interactions.

The cost of travel: How dispersal ability limits local adaptation in host-parasite interactions.

Classical theory suggests that parasites will exhibit higher fitness in sympatric relative to allopatric host populations (local adaptation). However, evidence for local adaptation in natural host-parasite systems is often equivocal, emphasizing the need for infection experiments conducted over realistic geographic scales and comparisons among species with varied life history traits. Here, we used infection experiments to test how two trematode (flatworm) species (Paralechriorchis syntomentera and Ribeiroia ondatrae) with differing dispersal abilities varied in the strength of local adaptation to their amphibian hosts. Both parasites have complex life cycles involving sequential transmission among aquatic snails, larval amphibians and vertebrate definitive hosts that control dispersal across the landscape. By experimentally pairing 26 host-by-parasite population infection combinations from across the western USA with analyses of host and parasite spatial genetic structure, we found that increasing geographic distance-and corresponding increases in host population genetic distance-reduced infection success for P. syntomentera, which is dispersed by snake definitive hosts. For the avian-dispersed R. ondatrae, in contrast, the geographic distance between the parasite and host populations had no influence on infection success. Differences in local adaptation corresponded to parasite genetic structure; although populations of P. syntomentera exhibited ~10% mtDNA sequence divergence, those of R. ondatrae were nearly identical (<0.5%), even across a 900 km range. Taken together, these results offer empirical evidence that high levels of dispersal can limit opportunities for parasites to adapt to local host populations.

How predator and parasite size interact to determine consumption of infectious stages.

Parasites are important players in ecological communities that can shape community structure and influence ecosystem energy flow. Yet beyond their effects on hosts, parasites can also function as an important prey resource for predators. Predators that consume infectious stages in the environment can benefit from a nutrient-rich prey item while concurrently reducing transmission to downstream hosts, highlighting the broad importance of this interaction. Less clear, however, are the specific characteristics of parasites and predators that increase the likelihood of consumption. Here, we determine what combination(s) of predator and parasite morphological traits lead to high parasite consumption. We exposed the infectious stages (cercariae) of five trematode (fluke) taxa to aquatic insect predators with varying foraging strategies and morphologies. Across the 19 predator-parasite combinations tested, damselfly predators in the family Coenagrionidae were, on average, the most effective predators of cercariae, consuming between 13 and 55% of administered cercariae. Large-bodied cercariae of Ribeiroia ondatrae had the highest average vulnerability to predation, with 37-48% of cercariae consumed. The interaction between predator head width and cercariae tail size strongly influenced the probability of consumption: small-bodied predators were the most effective consumers, particularly for larger tailed parasites. Thus, the likelihood of parasite consumption depended strongly on the relative size between predator and parasite. Our study helps establish that predation on free-living parasites largely follows a broader predator-prey framework. This will help to identify which predator and parasite combinations will likely have high consumptive interactions, potentially reducing parasite transmission in natural populations.

Resilience of native amphibian communities following catastrophic drought: Evidence from a decade of regional-scale monitoring.

The increasing frequency and severity of drought may exacerbate ongoing global amphibian declines. However, interactions between drought and coincident stressors, coupled with high interannual variability in amphibian abundances, can mask the extent and underlying mechanisms of drought impacts. We synthesized a decade (2009 - 2019) of regional-scale amphibian monitoring data (2273 surveys, 233 ponds, and seven species) from across California's Bay Area and used dynamic occupancy modeling to estimate trends and drivers of species occupancy. An extreme drought during the study period resulted in substantial habitat loss, with 51% of ponds drying in the worst year of drought, compared to <20% in pre-drought years. Nearly every species exhibited reduced breeding activity during the drought, with the occupancy of some species (American bullfrogs and California newts) declining by >25%. Invasive fishes and bullfrogs were also associated with reduced amphibian occupancy, and these taxa were locally extirpated from numerous sites during drought, without subsequent recovery-suggesting that drought may present an opportunity to remove invaders. Despite a historic, multi-year drought, native amphibians rebounded quickly to pre-drought occupancy levels, demonstrating evidence of resilience. Permanent waterbodies supported higher persistence of native species during drought years than did temporary waterbodies, and we therefore highlight the value of hydroperiod diversity in promoting amphibian stability.

Phenological synchrony shapes pathology in host-parasite systems.

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 (Pseudacris regilla) and infection by a pathogenic trematode (Ribeiroia ondatrae) 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.

Tracking the assembly of nested parasite communities: Using ß-diversity to understand variation in parasite richness and composition over time and scale.

Community composition is driven by a few key assembly processes: ecological selection, drift and dispersal. Nested parasite communities represent a powerful study system for understanding the relative importance of these processes and their relationship with biological scale. Quantifying ß-diversity across scales and over time additionally offers mechanistic insights into the ecological processes shaping the distributions of parasites and therefore infectious disease. To examine factors driving parasite community composition, we quantified the parasite communities of 959 amphibian hosts representing two species (the Pacific chorus frog, Pseudacris regilla and the California newt, Taricha torosa) sampled over 3 months from 10 ponds in California. Using additive partitioning, we estimated how much of regional parasite richness (γ-diversity) was composed of within-host parasite richness (α-diversity) and turnover (ß-diversity) at three biological scales: across host individuals, across species and across habitat patches (ponds). We also examined how ß-diversity varied across time at each biological scale. Differences among ponds comprised the majority (40%) of regional parasite diversity, followed by differences among host species (23%) and among host individuals (12%). Host species supported parasite communities that were less similar than expected by null models, consistent with ecological selection, although these differences lessened through time, likely due to high dispersal rates of infectious stages. Host individuals within the same population supported more similar parasite communities than expected, suggesting that host heterogeneity did not strongly impact parasite community composition and that dispersal was high at the individual host-level. Despite the small population sizes of within-host parasite communities, drift appeared to play a minimal role in structuring community composition. Dispersal and ecological selection appear to jointly drive parasite community assembly, particularly at larger biological scales. The dispersal ability of aquatic parasites with complex life cycles differs strongly across scales, meaning that parasite communities may predictably converge at small scales where dispersal is high, but may be more stochastic and unpredictable at larger scales. Insights into assembly mechanisms within multi-host, multi-parasite systems provide opportunities for understanding how to mitigate the spread of infectious diseases within human and wildlife hosts.

Community disassembly and disease: realistic-but not randomized-biodiversity losses enhance parasite transmission.

Debates over the relationship between biodiversity and disease dynamics underscore the need for a more mechanistic understanding of how changes in host community composition influence parasite transmission. Focusing on interactions between larval amphibians and trematode parasites, we experimentally contrasted the effects of host richness and species composition to identify the individual and joint contributions of both parameters on the infection levels of three trematode species. By combining experimental approaches with field surveys from 147 ponds, we further evaluated how richness effects differed between randomized and realistic patterns of species loss (i.e. community disassembly). Our results indicated that community-level changes in infection levels were owing to host species composition, rather than richness. However, when composition patterns mirrored empirical observations along a natural assembly gradient, each added host species reduced infection success by 12-55%. No such effects occurred when assemblages were randomized. Mechanistically, these patterns were due to non-random host species assembly/disassembly: while highly competent species predominated in low diversity systems, less susceptible hosts became progressively more common as richness increased. These findings highlight the potential for combining information on host traits and assembly patterns to forecast diversity-mediated changes in multi-host disease systems.

Of poisons and parasites-the defensive role of tetrodotoxin against infections in newts.

Classical research on animal toxicity has focused on the role of toxins in protection against predators, but recent studies suggest these same compounds can offer a powerful defense against parasites and infectious diseases. Newts in the genus Taricha are brightly coloured and contain the potent neurotoxin, tetrodotoxin (TTX), which is hypothesized to have evolved as a defense against vertebrate predators such as garter snakes. However, newt populations often vary dramatically in toxicity, which is only partially explained by predation pressure. The primary aim of this study was to evaluate the relationships between TTX concentration and infection by parasites. By systematically assessing micro- and macroparasite infections among 345 adult newts (sympatric populations of Taricha granulosa and T. torosa), we detected 18 unique taxa of helminths, fungi, viruses and protozoans. For both newt species, per-host concentrations of TTX, which varied from undetectable to >60 µg/cm2 skin, negatively predicted overall parasite richness as well as the likelihood of infection by the chytrid fungus, Batrachochytrium dendrobatidis, and ranavirus. No such effect was found on infection load among infected hosts. Despite commonly occurring at the same wetlands, T. torosa supported higher parasite richness and average infection load than T. granulosa. Host body size and sex (females > males) tended to positively predict infection levels in both species. For hosts in which we quantified leucocyte profiles, total white blood cell count correlated positively with both parasite richness and total infection load. By coupling data on host toxicity and infection by a broad range of micro- and macroparasites, these results suggest that-alongside its effects on predators-tetrodotoxin may help protect newts against parasitic infections, highlighting the importance of integrative research on animal chemistry, immunological defenses and natural enemy ecology.

Drought attenuates the impact of fish on aquatic macroinvertebrate richness and community composition.

Identifying ecological niche filters that shape species community composition is a critical first step in understanding the relative contributions of deterministic and stochastic processes in structuring communities. Systems with harsh ecological filters often have a more deterministic basis to community structure. Although these filters are often treated as static, investigations into their stability through time are rare, particularly in combination with extreme forms of environmental change such as drought.We examined the richness and composition of aquatic macroinvertebrate communities from 36 ponds over four years during the onset of a megadrought to answer the following questions: (1) what are the relative influences of non-native fish presence and pond permanence in structuring communities? And (2) how do the magnitudes of such filters vary through time?As predicted, fish presence had a strong, negative effect on both alpha and gamma diversity, lowering average invertebrate richness in pond communities by 23%. However, fish presence and sample year interacted to determine both richness and taxa composition: as drought conditions intensified, the effects of fish weakened such that there were no differences in the richness or composition between fish and fishless ponds by the later sampling years. Moreover, large-bodied invertebrate groups - often considered highly vulnerable to fish predation - were detected within fish-occupied sites by the final year of the study.This pattern was associated with progressive decreases in precipitation due to a severe drought in California, emphasizing the importance of exogenous, regional factors in moderating the strength of biotic niche filters on local community structure over time. Given that all detected fish species were non-native, these results also have application to understanding and forecasting changes in the diversity of native insects and other aquatic invertebrates.

Parasite richness and abundance within aquatic macroinvertebrates: testing the roles of host- and habitat-level factors.

The importance of parasites as both members of biological communities and as structuring agents of host communities has been increasingly emphasized. Yet parasites of aquatic macroinvertebrates and the environmental factors regulating their richness and abundance remain poorly studied. Here we quantified parasite richness and abundance within 12 genera of odonate naiads and opportunistically sampled four additional orders of aquatic macroinvertebrates from 35 freshwater ponds in the San Francisco Bay Area of California, USA. We also tested the relative contributions of host- and habitat-level factors in driving patterns of infection abundance for the most commonly encountered parasite (the trematode Haematoloechus sp.) in nymphal damselflies and dragonflies using hierarchical generalized linear mixed models. Over the course of two years, we quantified the presence and intensity of parasites from 1,612 individuals. We identified six parasite taxa: two digenetic trematodes, one larval nematode, one larval acanthocephalan, one gregarine, and a mite, for which the highest infection prevalence (39%) occurred in the damselfly genus, Ishnura sp. Based on the hierarchical analysis of Haematoloechus sp. occurrence, infection prevalence and abundance were associated predominantly with site-level factors, including definitive host (frog) presence, nymphal odonate density, water pH and conductivity. In addition, host suborder interacted with the presence of fishes, such that damselflies had higher infection rates in sites with fish relative to those without, whereas the opposite was true for dragonfly nymphs. These findings offer insights into the potential interaction between host- and site-level factors in shaping parasite populations within macroinvertebrate taxa.

The influence of landscape and environmental factors on ranavirus epidemiology in a California amphibian assemblage.

A fundamental goal of disease ecology is to determine the landscape and environmental processes that drive disease dynamics at different biological levels to guide management and conservation. Although ranaviruses (family Iridoviridae) are emerging amphibian pathogens, few studies have conducted comprehensive field surveys to assess potential drivers of ranavirus disease dynamics.We examined the factors underlying patterns in site-level ranavirus presence and individual-level ranavirus infection in 76 ponds and 1,088 individuals representing 5 amphibian species within the East Bay region of California.Based on a competing-model approach followed by variance partitioning, landscape and biotic variables explained the most variation in site-level presence. However, biotic and individual-level variables explained the most variation in individual-level infection.Distance to nearest ranavirus-infected pond (the landscape factor) was more important than biotic factors at the site-level; however, biotic factors were most influential at the individual-level. At the site level, the probability of ranavirus presence correlated negatively with distance to nearest ranavirus-positive pond, suggesting that the movement of water or mobile taxa (e.g., adult amphibians, birds, reptiles) may facilitate the movement of ranavirus between ponds and across the landscape.Taxonomic richness associated positively with ranavirus presence at the site-level, but vertebrate richness associated negatively with infection prevalence in the host population. This might reflect the contrasting influences of diversity on pathogen colonization versus transmission among hosts.Amphibian host species differed in their likelihood of ranavirus infection: American bullfrogs (Rana catesbeiana) had the weakest association with infection while rough-skinned newts (Taricha granulosa) had the strongest. After accounting for host species effects, hosts with greater snout-vent length had a lower probability of infection.Our study demonstrates the array of landscape, environmental, and individual-level factors associated with ranavirus epidemiology. Moreover, our study helps illustrate that the importance of these factors varies with biological level.