ABSTRACT
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.
ABSTRACT
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.
Subject(s)
Parasites , Trematoda , Trematode Infections , Animals , Virulence , Host-Parasite Interactions , Trematode Infections/parasitology , Amphibians/parasitologyABSTRACT
The location of parasites within individual hosts is often treated as a static trait, yet many parasite species can occur in multiple locations or organs within their hosts. Here, we apply distributional heat maps to study the within- and between-host infection patterns for four trematodes (Alaria marcianae, Cephalogonimus americanus, Echinostoma spp. and Ribeiroia ondatrae) within the amphibian hosts Pseudacris regilla and two species of Taricha. We developed heatmaps from 71 individual hosts from six locations in California, which illustrate stark differences among parasites both in their primary locations within amphibian hosts as well as their degree of location specificity. While metacercariae (i.e., cysts) of two parasites (C. americanus and A. marcianae) were relative generalists in habitat selection and often occurred throughout the host, two others (R. ondatrae and Echinostoma spp.) were highly localised to a specific organ or organ system. Comparing parasite distributions among these parasite taxa highlighted locations of overlap showing potential areas of interactions, such as the mandibular inner dermis region, chest and throat inner dermis and the tail reabsorption outer epidermis. Additionally, the within-host distribution of R. ondatrae differed between host species, with metacercariae aggregating in the anterior dermis areas of newts, compared with the posterior dermis area in frogs. The ability to measure fine-scale changes or alterations in parasite distributions has the potential to provide further insight about ecological questions concerning habitat preference, resource selection, host pathology and disease control.
Subject(s)
Echinostomatidae , Trematoda , Animals , Metacercariae , Host-Parasite Interactions , Anura/parasitology , Salamandridae/parasitologyABSTRACT
Research with captive wildlife in Animal Biosafety Level 2 (ABSL2) and 3 (ABSL3) facilities is becoming increasingly necessary as emerging and re-emerging diseases involving wildlife have increasing impacts on human, animal, and environmental health. Utilizing wildlife species in a research facility often requires outside the box thinking with specialized knowledge, practices, facilities, and equipment. The USGS National Wildlife Health Center (NWHC) houses an ABSL3 facility dedicated to understanding wildlife diseases and developing tools to mitigate their impacts on animal and human health. This review presents considerations for utilizing captive wildlife for infectious disease studies, including, husbandry, animal welfare, veterinary care, and biosafety. Examples are drawn from primary literature review and collective 40-year experience of the NWHC. Working with wildlife in ABSL2 and ABSL3 facilities differs from laboratory animals in that typical laboratory housing systems, husbandry practices, and biosafety practices are not designed for work with wildlife. This requires thoughtful adaptation of standard equipment and practices, invention of customized solutions and development of appropriate enrichment plans using the natural history of the species and the microbiological characteristics of introduced and native pathogens. Ultimately, this task requires critical risk assessment, understanding of the physical and psychological needs of diverse species, creativity, innovation, and flexibility. Finally, continual reassessment and improvement are imperative in this constantly changing specialty area of infectious disease and environmental hazard research.
Subject(s)
Animals, Wild , Containment of Biohazards , Animal Welfare , Animals , Animals, Laboratory , Risk AssessmentABSTRACT
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.
Subject(s)
Adaptation, Biological , Amphibians/parasitology , Animal Distribution , Host-Parasite Interactions/genetics , Trematoda/genetics , Animals , Biological Evolution , Birds , Larva/parasitology , SnakesABSTRACT
Australapatemon spp. are cosmopolitan trematodes that infect freshwater snails, aquatic leeches, and birds. Despite their broad geographic distribution, relatively little is known about interactions between Australapatemon spp. and their leech hosts, particularly under experimental conditions and in natural settings. We used experimental exposures to determine how Australapatemon burti cercariae dosage (number administered to leech hosts, Erpobdella microstoma) affected infection success (fraction to encyst as metacercariae), infection abundance, host survival, and host size over the 100 days following exposure. Interestingly, infection success was strongly density-dependent, such that there were no differences in metacercariae load even among hosts exposed to a 30-fold difference in cercariae. This relationship suggests that local processes (e.g., resource availability, interference competition, or host defenses) may play a strong role in parasite transmission. Our results also indicated that metacercariae did not become evident until ~4 weeks post exposure, with average load climbing until approximately 13 weeks. There was no evidence of metacercariae death or clearance over the census period. Parasite exposure had no detectable effects on leech size or survival, even with nearly 1,000 cercariae. Complementary surveys of leeches in California revealed that 11 of 14 ponds supported infection by A. burti (based on morphology and molecular sequencing), with an average prevalence of 32% and similar metacercariae intensity as in our experimental exposures. The extended development time and extreme density dependence of A. burti has implications for studying naturally occurring host populations, for which detected infections may represent only a fraction of cercariae to which animals have been exposed. Future investigation of these underlying mechanisms would be benefical in understanding host-parasite relationships.
Subject(s)
Leeches/parasitology , Trematoda/physiology , Animals , Bayes Theorem , Binomial Distribution , California , Cercaria/physiology , Electron Transport Complex IV/chemistry , Electron Transport Complex IV/genetics , Leeches/growth & development , Leeches/physiology , Likelihood Functions , Linear Models , Poisson Distribution , Ponds , Trematoda/geneticsABSTRACT
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.
Subject(s)
Parasites , Animals , Anura , Biodiversity , Ecosystem , Host SpecificityABSTRACT
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.
Subject(s)
Anura/parasitology , Host-Parasite Interactions , Trematoda/physiology , Animals , Climate , PhenotypeABSTRACT
Studies of amphibian parasites have increased over the past 20 yr, in part because of their role in amphibian population declines and deformities. Such patterns underscore the importance of non-lethal methods for detecting and quantifying endoparasitic infections. The goal of this study was to compare results of indirect methods (fecal smears and fecal floats) with quantitative necropsies to detect endoparasitic infections in adult newts. In 2015, we collected fecal samples from 68 adult newts (Taricha granulosa and T. torosa) in the East Bay region of California and used fecal smears, sodium nitrate fecal flotation solution, and Sheather's sugar flotation solution to assess infection (i.e. the presence and/or abundance of a parasite). Across all methods, we detected 3 protozoans (Eimeria tarichae, Tritrichomonas sp., and Balantidium sp.) and 3 nematodes (Rhabdias tarichae, Cosmocercoides variabilis, and Chabaudgolvania sp.). Based on generalized linear mixed models, the likelihood of detection varied between hosts (with T. torosa showing more overall infection relative to T. granulosa) and by assessment method: while fecal smears were more sensitive in detecting protozoans, comprehensive necropsies were the most reliable for quantifying infections of R. tarichae. Nonetheless, both the likelihood of R. tarichae detection within fecal samples as well as the number of infectious stages observed correlated strongly with infection intensity from necropsy, highlighting the utility of non-lethal assessment methods. The overall congruence between indirect methods and gross necropsy helps to validate the use of less-invasive methods for parasite detection and abundance, especially for sensitive or protected host taxa such as amphibians.
Subject(s)
Nematoda , Amphibians , Animals , California , Feces , Nematoda/parasitology , SalamandridaeABSTRACT
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.
Subject(s)
Anura/parasitology , Biodiversity , Salamandridae/parasitology , Trematode Infections/transmission , Animals , Anura/growth & development , Biota , California , Host-Parasite Interactions , Larva/parasitology , Ponds , Salamandridae/growth & development , Trematoda/physiologyABSTRACT
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.
Subject(s)
Anura/parasitology , Host Specificity , Trematoda/physiology , Trematode Infections/veterinary , Animals , Anura/classification , Biodiversity , Trematoda/genetics , Trematode Infections/parasitologyABSTRACT
Hosts have two general strategies for mitigating the fitness costs of parasite exposure and infection: resistance and tolerance. The resistance-tolerance framework has been well developed in plant systems, but only recently has it been applied to animal-parasite interactions. However, difficulties associated with estimating fitness, controlling parasite exposure, and quantifying parasite burden have limited application of this framework to animal systems. Here, we used an experimental approach to quantify the relative influence of variation among host individuals and genetic families in determining resistance and tolerance within an amphibian-trematode system. Importantly, we used multiple, alternative metrics to assess each strategy, and employed a Bayesian analytical framework to compare among responses while incorporating uncertainty. Relative to unexposed hosts, exposure to the pathogenic trematode (Ribeiroia ondatrae) reduced the survival and growth of California newts (Taricha torosa) (survival: 93% vs. 74%; growth: 0.29 vs. -0.5 vs mm day -1). Similarly, parasite infection success (the inverse of resistance) ranged from 8% to 100%. Yet despite this broad variation in host resistance and tolerance among individual newts, we found no evidence for transmissable, among-family variation in any of the resistance or tolerance metrics. This suggests that opportunities for evolution of these traits is limited, likely requiring significant increases in mutation, gene flow, or environmental heterogeneity. Our study provides a quantitative framework for evaluating the importance of alternative metrics of resistance and tolerance across multiple time points in the study of host-parasite interactions in animal systems.
Subject(s)
Echinostomatidae/pathogenicity , Salamandridae/parasitology , Trematode Infections/veterinary , Animals , Bayes Theorem , Binomial Distribution , Disease Resistance , Echinostomatidae/immunology , Host-Parasite Interactions , Ponds , Salamandridae/genetics , Salamandridae/growth & development , Salamandridae/physiology , Snails/parasitology , Trematode Infections/genetics , Trematode Infections/immunology , Trematode Infections/parasitologyABSTRACT
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.
ABSTRACT
Disciplines such as business and economics often rely on the assumption of rationality when explaining complex human behaviours. However, growing evidence suggests that behaviour may concurrently be influenced by infectious microorganisms. The protozoan Toxoplasma gondii infects an estimated 2 billion people worldwide and has been linked to behavioural alterations in humans and other vertebrates. Here we integrate primary data from college students and business professionals with national-level information on cultural attitudes towards business to test the hypothesis that T. gondii infection influences individual- as well as societal-scale entrepreneurship activities. Using a saliva-based assay, we found that students (n = 1495) who tested IgG positive for T. gondii exposure were 1.4× more likely to major in business and 1.7× more likely to have an emphasis in 'management and entrepreneurship' over other business-related emphases. Among professionals attending entrepreneurship events, T. gondii-positive individuals were 1.8× more likely to have started their own business compared with other attendees (n = 197). Finally, after synthesizing and combining country-level databases on T. gondii infection from the past 25 years with the Global Entrepreneurship Monitor of entrepreneurial activity, we found that infection prevalence was a consistent, positive predictor of entrepreneurial activity and intentions at the national scale, regardless of whether previously identified economic covariates were included. Nations with higher infection also had a lower fraction of respondents citing 'fear of failure' in inhibiting new business ventures. While correlational, these results highlight the linkage between parasitic infection and complex human behaviours, including those relevant to business, entrepreneurship and economic productivity.
Subject(s)
Entrepreneurship/statistics & numerical data , Toxoplasmosis/epidemiology , Adult , Antibodies, Protozoan/blood , Female , Humans , Immunoglobulin G/blood , Male , Middle Aged , Prevalence , Risk Factors , Seroepidemiologic Studies , Toxoplasma/physiology , Toxoplasmosis/parasitologyABSTRACT
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.
Subject(s)
Host-Parasite Interactions , Mycoses/veterinary , Phenotype , Salamandridae , Tetrodotoxin/metabolism , Animals , Biodiversity , California/epidemiology , Chytridiomycota/isolation & purification , Female , Male , Microbiota , Mycoses/epidemiology , Mycoses/microbiology , Mycoses/parasitology , Parasite Load/veterinary , Parasites/isolation & purification , Salamandridae/geneticsABSTRACT
Circadian rhythms of parasites and their hosts can influence processes such as transmission, pathology and life cycle evolution. For trematode parasites that depend on free-living infectious stages (i.e. cercariae) to move among host species, the timing of parasite release is hypothesized to increase the likelihood of contacting a host. Yet, a persistent challenge in studying such biorhythms involves selection of appropriate analytical techniques. Here, we extend a generalized linear mixed modelling (GLMM) framework to cosinor analyses, thereby allowing flexibility in the statistical distribution of the response variable, incorporation of multiple covariates and inclusion of hierarchical grouping effects. By applying this approach to 93 snails infected with trematode parasites from freshwater pond ecosystems, we detected non-random rhythms in six of eight species, with variation in both the timing of peak cercariae release (between 5:10 and 21:46 h) and its magnitude (between 13 and 386). The use of GLMM yielded more accurate and precise estimates of the cosinor parameters compared with classical least-squares (LS) based on a simulation-based sensitivity analysis. The sensitivity analysis revealed that the amplitude and rhythm-adjusted mean values from the LS models diverged from the true values at some limits. We highlight the importance of novel analytical approaches for evaluating parasite circadian rhythms and investigating their underlying mechanisms.
Subject(s)
Circadian Rhythm , Host-Parasite Interactions , Linear Models , Trematoda/physiology , Animals , Ecosystem , Host Specificity , Life Cycle Stages , Snails/parasitology , Trematode Infections/parasitologyABSTRACT
The dermal glands of many amphibian species secrete toxins or other noxious substances as a defense strategy against natural enemies. Newts in particular possess the potent neurotoxin tetrodotoxin (TTX), for which the highest concentrations are found in species within the genus Taricha. Adult Taricha are hypothesized to use TTX as a chemical defense against vertebrate predators such as garter snakes (Thamnophis spp.). However, less is known about how TTX functions to defend aquatic-developing newt larvae against natural enemies, including trematode parasites and aquatic macroinvertebrates. Here we experimentally investigated the effects of exogenous TTX exposure on survivorship of the infectious stages (cercariae) of five species of trematode parasites that infect larval amphibians. Specifically, we used dose-response curves to test the sensitivity of trematode cercariae to progressively increasing concentrations of TTX (0.0 [control], 0.63, 3.13, 6.26, 31.32, and 62.64 nmol L-1) and how this differed among parasite species. We further compared these results to the effects of TTX exposure (0 and 1000 nmolL-1) over 24 h on seven macroinvertebrate taxa commonly found in aquatic habitats with newt larvae. TTX significantly reduced the survivorship of trematode cercariae for all species, but the magnitude of such effects varied among species. Ribeiroia ondatrae - which causes mortality and limb malformations in amphibians - was the least sensitive to TTX, whereas the kidney-encysting Echinostoma trivolvis was the most sensitive. Among the macroinvertebrate taxa, only mayflies (Ephemeroptera) showed a significant increase in mortality following exogenous TTX exposure, despite the use of a concentration 16x higher than the maximum used for trematodes. Our results suggest that maternal investment of TTX into larval newts may provide protection against certain trematode infections and highlight the importance of future work assessing the effects of newt toxicity on both parasite infection success and the palatability of larval newts to invertebrate predators.
Subject(s)
Insecta/drug effects , Tetrodotoxin/pharmacology , Trematoda/drug effects , Animals , Larva/drug effects , Larva/parasitology , Predatory Behavior/physiology , Salamandridae/growth & development , Salamandridae/parasitologyABSTRACT
Parasitic infections are increasingly recognized as influential forces in the migratory behaviors of hosts ranging from butterflies to whales. In aquatic zooplankton, diel vertical migrations (DVMs) are among the most recurrent behaviors with implications for predator-prey interactions, nutrient cycling, and energy flow, yet how parasitism affects such migrations remains an open question. Here, we tested the effects of sporangia cluster disease (SCD) on DVM of the large-bodied Daphnia pulicaria, which is often considered a key component of lake food webs. By collecting depth-specific zooplankton samples across diel cycles, between years, and among lakes, we show that infection is associated with strong inhibition of host DVM; while all Daphnia tended to occur deeper during the day, uninfected Daphnia and especially gravid individuals migrated to shallower waters at night. In contrast, infected hosts-which could comprise 40% of the population-were more likely to remain deep regardless of time of day. Among infected hosts, the intensity of SCD (sporangia count per host) predicted the degree of DVM inhibition. These observations-coupled with lab-based assays showing that infected hosts exhibited fewer swimming movements and persisted at lower depths than uninfected conspecifics-suggest that parasite-induced inhibition of DVM is a "sickness behavior" resulting from increasing morbidity and energy depletion as the infection intensifies toward host death. Considering the importance of large-bodied Daphnia as regulators of water clarity and prey for fishes, parasite-induced alterations of host migratory behavior have broad potential to affect the redistribution of energy and nutrients within lake ecosystems.
ABSTRACT
Antimicrobial peptides (AMPs) contribute to the immune defenses of many vertebrates, including amphibians. As larvae, amphibians are often exposed to the infectious stages of trematode parasites, many of which must penetrate the host's skin, potentially interacting with host AMPs. We tested the effects of the natural AMPs repertoires on both the survival of trematode infectious stages as well as their ability to infect larval amphibians. All five trematode species exhibited decreased survival of cercariae in response to higher concentrations of adult bullfrog AMPs, but no effect when exposed to AMPs from larval bullfrogs. Similarly, the use of norepinephrine to remove AMPs from larval bullfrogs, Pacific chorus frogs, and gray treefrogs had only weak (gray treefrogs) or non-significant (other tested species) effects on infection success by Ribeiroia ondatrae. We nonetheless observed strong differences in parasite infection as a function of both host stage (first- versus second-year bullfrogs) and host species (Pacific chorus frogs versus gray treefrogs) that were apparently unrelated to AMPs. Taken together, our results suggest that AMPs do not play a significant role in defending larval amphibians against trematode cercariae, but that they could be one mechanism helping to prevent infection of post-metamorphic amphibians, particularly for highly aquatic species.