ABSTRACT
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.
Subject(s)
Host-Parasite Interactions , Predatory Behavior , Animals , Food Chain , Models, Biological , Animals, WildABSTRACT
Parasites represent a ubiquitous threat for most organisms, requiring potential hosts to invest in a range of strategies to defend against infection-these include both behavioural and physiological mechanisms. Avoidance is an essential first line of defence, but this behaviour may show a trade-off with host investment in physiological immunity. Importantly, while environmental stressors can lead to elevated hormones in vertebrates, such as glucocorticoids, that can reduce physiological immunity in certain contexts, behavioural defences may also be compromised. Here, we investigate anti-parasite behaviour and immune responses against a trematode (flatworm) parasite by larval amphibians (tadpoles) exposed or not to a simulated general stressor in the form of exogenous corticosterone. Tadpoles that were highly active in the presence of the trematode infectious stage (cercariae) had lower infection loads, and parasite loads from tadpoles treated only with dechlorinated water were significantly lower than those exposed to corticosterone or the solvent control. However, treatment did not affect immunity as measured through white blood-cell profiles, and there was no relationship between the latter and anti-parasite behaviour. Our results suggest that a broad range of stressors could increase host susceptibility to infection through altered anti-parasite behaviours if they elevate endogenous glucocorticoids, irrespective of physiological immunity effects. How hosts defend themselves against parasitism in the context of multiple challenges represents an important topic for future research, particularly as the risk posed by infectious diseases is predicted to increase in response to ongoing environmental change.
Subject(s)
Corticosterone , Host-Parasite Interactions , Larva , Animals , Trematoda/physiology , Behavior, Animal , GlucocorticoidsABSTRACT
Chemical defences against parasites and pathogens can be seen in a wide range of animal taxa, including insect pests such as the red flour beetle Tribolium castaneum. Antimicrobial quinone-based secretions can be used by these beetles to defend against various parasites, particularly the fungal entomopathogen Beauveria bassiana. While quinone secretions can inhibit B. bassiana growth, it is unknown how long they remain effective or how individual secretion compounds contribute to growth inhibition. Here, we tested each individual component of the quinone secretions (methyl-1,4-benzoquinone, ethyl-1,4-benzoquinone, and 1-pentadecene), as well as two mixed solutions that represent the composition range found in natural T. castaneum secretions, after aging for 0, 24, or 72 h. The two quinone compounds equally contributed to B. bassiana inhibition, but their efficacy was significantly reduced after 24 h, with no growth inhibition after 72 h. This indicates that quinones protect insects against B. bassiana for only a limited time, perhaps requiring constant secretion into the environment to effectively defend against this fungal threat. Future investigations may consider the extent to which quinone secretions are effective against other parasites, as well as how their ability to cause parasite damage changes with compound age.
Subject(s)
Beauveria , Coleoptera , Animals , Beauveria/physiology , Benzoquinones/pharmacology , Quinones/pharmacologyABSTRACT
Microplastics (MPs) and nanoplastics (NPs) are now widely recognized as a ubiquitous and pervasive environmental pollutant with important consequences for aquatic fauna in particular; however, little is known regarding their potential effects on interactions between hosts and their parasites or pathogens. We conducted a literature survey of published studies that have conducted empirical investigations of MP and NP influences on infectious disease dynamics to summarize the current state of knowledge. In addition, we examined the effects of microbead (MB) ingestion on the longevity of freshwater snails (Stagnicola elodes) infected by the trematode Plagiorchis sp., along with their production of infectious stages (cercariae), with a 3-week lab study during which snails were fed food cubes containing either 0, 10 or 100 polyethylene MBs sized 106-125 µm. We found 22 studies that considered MP and NP influences on host resistance or tolerance-20 of these focused on aquatic systems, but there was no clear pattern in terms of host effects. In our lab study, MB diet had marginal or few effects on snail growth and mortality, but snails exhibited a significant non-monotonic response with respect to cercariae production as this was greatest in those fed the high-MB diet. Both our literature summary and experimental study indicate that MPs and NPs can have complex and unpredictable effects on infectious disease dynamics, with an urgent need for more investigations that examine how plastics can affect aquatic fauna through direct and indirect means.
Subject(s)
Communicable Diseases , Microplastics , Humans , Host-Parasite Interactions , Plastics , PolyethyleneABSTRACT
Helminth parasites are part of almost every ecosystem, with more than 300 000 species worldwide. Helminth infection dynamics are expected to be altered by climate change, but predicting future changes is difficult owing to lacking thermal sensitivity data for greater than 99.9% of helminth species. Here, we compiled the largest dataset to date on helminth temperature sensitivities and used the Metabolic Theory of Ecology to estimate activation energies (AEs) for parasite developmental rates. The median AE for 129 thermal performance curves was 0.67, similar to non-parasitic animals. Although exceptions existed, related species tended to have similar thermal sensitivities, suggesting some helminth taxa are inherently more affected by rising temperatures than others. Developmental rates were more temperature-sensitive for species from colder habitats than those from warmer habitats, and more temperature sensitive for species in terrestrial than aquatic habitats. AEs did not depend on whether helminth life stages were free-living or within hosts, whether the species infected plants or animals, or whether the species had an endotherm host in its life cycle. The phylogenetic conservatism of AE may facilitate predicting how temperature change affects the development of helminth species for which empirical data are lacking or difficult to obtain.
Subject(s)
Helminths , Parasites , Animals , Ecosystem , Helminths/physiology , Host-Parasite Interactions/physiology , PhylogenyABSTRACT
Research Highlight: Hobart, B. K., Moss, W. E., McDevitt-Galles, T., Stewart Merrill, T. E., Johnson, P. T. J. (2021). It's a worm-eat-worm world: Consumption of parasite free-living stages protects hosts and benefits predators. Journal of Animal Ecology, https://doi.org/10.1111/1365-2656.13591 Many parasites and pathogens have infectious stages that are vulnerable to consumption by non-host organisms. This consumption can benefit both the predators that consume this unusual food resource and the hosts which are less likely to encounter infectious propagules. Yet the importance of these benefits may also depend on parasite transmission, which can influence consumer opportunities to feed upon free-living infectious stages. Hobart et al. (2021) report that freshwater snails with high densities of symbiotic oligochaetes are less likely to be parasitized by trematodes (Platyhelminthes) with an 'active' versus 'passive' (motile or stationary, respectively) mode of transmission, supporting a protective effect via oligochaete predation upon infectious propagules. However, these predators benefit from snails harbouring passively acquired infections, and likely achieve their higher abundance from easy access to prey in the form of a second infectious stage emerging from these hosts. Consumption of free-living infectious stages is thus beneficial to hosts and predators, but varies with parasite life history and ecology.
Subject(s)
Parasites , Trematoda , Animals , Ecology , Predatory Behavior , SnailsABSTRACT
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.
Subject(s)
Odonata , Parasites , Trematoda , Animals , Ecosystem , Predatory BehaviorABSTRACT
Lipids, particularly fatty acids (FAs), are major sources of energy and nutrients in aquatic ecosystems and play key roles during vertebrate development. The European eel Anguilla anguilla goes through major biochemical and physiological changes throughout its lifecycle as it inhabits sea- (SW), and/or brackish- (BW) and/or freshwater (FW) habitats. With the ultimate goal being to understand the reasons for eels adopting a certain life history strategy (FW or SW residency vs. 'habitat shifting'), we explored differences in lipid content and FA composition of muscle, liver and eyes from eels collected across Norwegian SW, BW and FW habitats, and at different lifecycle stages (yellow to silver). FW and SW eels had a higher lipid content overall compared to BW eels, reflecting differences in food availability and life history strategies. SW eels had higher proportions of certain monounsaturated FAs (MUFAs; 18:1n-9, 20:1n-9), and of the essential polyunsaturated FAs 20:5n-3 (eicosapentaenoic acid, EPA) and 22:6n-3 (docosahexaenoic acid) than FW eels, reflecting a marine-based diet. In contrast, the muscle of FW eels had higher proportions of 18:3n-3, 18:2n-6 and 20:4n-6 (arachidonic acid), as is typical of FW organisms. MUFA proportions increased in later stage eels, consistent with the hypothesis that the eels accumulate energy stores prior to migration. In addition, the decrease of EPA with advancing stage may be associated with the critical role that this FA plays in eel sexual development. Lipid and FA information provided further understanding of the habitat use and overall ecology of this critically endangered species.
Subject(s)
Anguilla , Ecosystem , Anguilla/metabolism , Anguilla/physiology , Animals , Fatty Acids , Fresh WaterABSTRACT
Despite their ubiquity and considerable biomass, the roles played by parasites in aquatic food webs are still not well understood, especially those of their free-living infectious stages. For instance, cercariae, the motile larvae of parasitic flukes (trematodes) may be a key source of nutrients and energy for consumers. As cercariae clonally reproduce within the digestive-gonadal gland complex of gastropod intermediate hosts that acquire nutritionally important polyunsaturated fatty acids (PUFA) mainly from their diets (e.g., by grazing on primary producers), cercariae could transfer snail-derived PUFA if consumed. Through fatty acid (FA) analysis, we explored whether a change in the diet of parasitized hosts altered the FA profiles of both snail-only and trematode-containing snail tissue, thereby affecting their nutritional values. Freshwater snails (Stagnicola elodes) infected with Plagiorchis sp. were fed three different diets (cyanobacteria, green algae, and diatoms) that differed in nutritional quality with respect to FA profiles. While diet influenced the overall FA composition of both snail-only tissue and snail tissue containing trematodes, levels of certain PUFA (mainly omega-3) were largely unaffected. Trematode-containing snail tissue also generally contained more PUFA relative to snail-only tissue. Notably, both tissue types had far higher levels of PUFA than found in their diets. Our results suggest that freshwater snail hosts, and possibly their associated trematode parasites, could be trophic upgraders of key PUFA despite anthropogenically induced changes in algal communities that may lead to overall diminished PUFA contents. As such, cercariae-mediated trophic transfers of PUFA may play important roles in aquatic food webs.
Subject(s)
Parasites , Trematoda , Animals , Fatty Acids , Fatty Acids, Essential , Fresh Water , Nutritive Value , SnailsABSTRACT
Parasites remainunderstudied members of most ecosystems, especially free-living infectious stages, such as the aquatic cercariae of trematodes (flatworms). Recent studies are shedding more light on their roles, particularly as prey for a diverse array of aquatic predators, but the possible fates of cercariae remain unclear. While this is critical to elucidate because cercariae represent a large potential source of energy and nutrients, determining the fate of cercariae-derived organic matter involves many logistical challenges. Previous studies utilized elemental and stable isotope analysis when examining host-parasite interactions, but none has used such approaches to track the movement of cercariae biomass within food webs. Here we report that Plagiorchis sp. cercariae were effectively labelled with 13C by introducing this compound in the food of their snail host. We then added 13C-labelled cercariae as a potential food source to experimental mesocosms containing a simplified model freshwater food web represented by diving beetles (Dytiscidae sp.), dragonfly larvae (Leucorrhinia intacta), oligochaete worms (Lumbriculus variegatus), and a zooplankton community dominated by Daphnia pulex. The oligochaetes had the highest ratio of 13C to 12C, suggesting benthic detritivores are substantial, but previously unrecognized, consumers of cercariae biomass. In an experiment where L. variegatus were fed mass equivalents of dead D. pulex or cercariae, growth was greater with the latter diet, supporting the importance of cercariae as food source for benthic organisms. Given the substantial cercariae biomass possible in natural settings, understanding their contributions to energy flow and nutrient cycling is important, along with developing methods to do so.
Subject(s)
Carbon Cycle , Cercaria/physiology , Fresh Water , Trematoda/physiology , Animals , Aquatic Organisms/classification , Aquatic Organisms/growth & development , Aquatic Organisms/metabolism , Biomass , Carbon Isotopes/analysis , Carbon Isotopes/metabolism , Cercaria/growth & development , Cercaria/metabolism , Ecosystem , Food Chain , Fresh Water/chemistry , Fresh Water/parasitology , Trematoda/growth & development , Trematoda/metabolismABSTRACT
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
Parasites have been neglected from most biodiversity surveys even though they are an essential component of ecosystems and intimately associated with the free-living communities within them. Parasites with complex life cycles, such as digenean trematode flatworms, utilize at least two host species within an ecosystem for their development and transmission, taking advantage of species networks to complete their life cycles. Despite this knowledge, our understanding of the processes that contribute to parasite community assembly, and which limit their geographic distributions, are rudimentary, including the importance of host diversity. Utilizing recent advancements in the identification of cryptic trematode species through molecular barcoding, we examined patterns of community assembly involving 79 species in six Alberta lakes over three years. Specifically, we focused on spatiotemporal variation in trematode diversity within their snail first intermediate hosts (component communities), how this might relate to host diversity through the specificity of host-parasite relationships, and the role of certain environmental factors in structuring these communities. We found substantial natural fluctuations of trematode communities through space and time within these lakes. Trematode communities were diverse, showing an overall positive relationship with snail diversity, but were often dominated by a few common species. We found that ecoregion and lake trophic status were key predictors for the presence of these trematode species. Such information is key for understanding how biodiversity alterations may affect parasite community composition, as well as our ability to formulate predictive models, by considering how this could influence both species richness and evenness.
ABSTRACT
Free-living parasite infectious stages, such as motile cercariae of trematodes (flatworms), can constitute substantial biomass within aquatic ecosystems and are frequently eaten by various consumers, potentially serving as an important source of nutrients and energy. However, quantitative data on their nutritional value (e.g., essential fatty acids [EFA]) are largely lacking. As EFA are leading indicators of nutritional quality and underpin aquatic ecosystem productivity, we performed fatty acid (FA) analysis on an aggregate of ~ 30,000 cercariae of the freshwater trematode, Ribeiroia ondatrae. Individual cercariae contained 15 ng of total FA, and considerable quantities of EFA, including eicosapentaenoic (EPA, at 0.79 ng cercaria-1) and docosahexaenoic (DHA, at 0.01 ng cercaria-1) acids. We estimated annual EFA production by R. ondatrae cercariae for a series of ponds in California to be 40.4-337.0 µg m-2 yr-1 for EPA and 0.7-6.2 µg m-2 yr-1 for DHA. To investigate viability of cercariae as prey, we also compared growth and FA profiles of dragonfly larvae (naiads of Leucorrhinia intacta) fed equivalent masses of either R. ondatrae or zooplankton (Daphnia spp.) for 5 weeks. Naiads raised on the two diets grew equally well, with no significant differences found in their EFA profiles. While zooplankton are widely recognized as a vital source of energy, and an important conduit for the movement of EFA between algae and higher trophic levels, we suggest a similar role for trematode cercariae by 'unlocking' EFA from the benthic environment, highlighting their potential importance as a nutrient source that supports animal health.
Subject(s)
Odonata , Parasites , Animals , California , Ecosystem , Fatty Acids , Fatty Acids, Essential , Fresh Water , LipidsABSTRACT
Parasites and pathogens (hereafter parasites) commonly challenge organisms, but the extent to which their infections are physiologically stressful to hosts remains unclear. Importantly, vertebrate hormones, glucocorticoids (GCs), have been reported to increase, decrease or show no alterations stemming from infections, challenging the generality of parasite-associated GC responses and motivating a search for important moderator variables. We undertook the first meta-analysis of changes in vertebrate GCs following experimental infection with parasites, extracting 146 effect sizes from 42 studies involving 32 host and 32 parasite species to test for general patterns of GC following infection, as well as the influence of moderators. Overall, infection increased GCs relative to preliminary or control levels when the single largest effect sizes from repeated measures studies were examined, suggesting that parasites of vertebrate hosts can be thought of generally as physiological stressors by elevating GCs. When all effect sizes were included along with the moderator of sampling time post-infection (tPI), parasite infection still had a positive effect on host GCs. However, the strength of that effect did not relate consistently to tPI, illustrating temporal differences in GC changes during the course of infection among parasite taxa (e.g. arthropod vs. bacterial infections). Other moderator variables examined did not influence GC responses. Studies broadening the range of host and parasite taxa, and sampling during critical time windows, would aid in our understanding of variation in the host stress response and its consequences for fitness of both vertebrate hosts and their parasites.
Subject(s)
Parasites , Parasitic Diseases , Animals , Glucocorticoids , Host-Parasite Interactions , VertebratesABSTRACT
Free-living parasite infectious stages, such as the cercariae of trematodes (flatworms), can represent substantial biomass in aquatic ecosystems, yet their interactions with other planktonic fauna are poorly understood. Given that cercariae are consumed by various aquatic predators, sometimes even preferentially over zooplankton, their presence may decrease predation pressure on free-living organisms within similar trophic niches by serving as alternate prey. Here, we experimentally examined how the presence of cercariae (Plagiorchis sp.) affected the population dynamics of common freshwater zooplankton (Daphnia sp.) in the presence of a predator (the larval dragonfly, Leucorrhinia intacta) known to consume both. After seeding 48 mesocosms with starting populations of Daphnia, we used four treatments (12 replicates each) representing a factorial combination of the absence/presence of both cercariae and dragonfly larvae and tracked Daphnia populations over 4 weeks. We found a significant interaction between the presence of cercariae and predators on Daphnia population size. When faced with predation pressure, Daphnia reached ~ 50% higher numbers when accompanied by cercariae than without, suggesting a "protective" effect of the latter by acting as substitute prey. Within aquatic ecosystems, an abundance of trematodes may prove advantageous for zooplankton communities that share common predators, but further studies will be needed to determine how this varies depending on the predator, trematode, and zooplankton taxa involved.
Subject(s)
Odonata , Parasites , Animals , Ecosystem , Food Chain , Predatory Behavior , ZooplanktonABSTRACT
Eutrophication of aquatic habitats has become a global problem, with implications for host-parasite dynamics. Blooms of certain cyanobacteria are associated with cyanotoxins, particularly microcystins such as microcystin-LR (MC-LR). These potent toxins have been shown to adversely affect freshwater fauna and can increase host susceptibility to parasite infection. However, to understand how cyanotoxins influence infection outcomes in nature, it is necessary to investigate whether free-living parasite infectious stages, such as that of trematode cercariae, are also affected given their demonstrated sensitivity to various contaminants. Here we examined the effects of environmentally relevant levels of MC-LR representing relatively high (82 µg/L) and low (11 µg/L) concentrations on the activity and survival of four different types of cercariae ( Echinostoma sp., Cephalogonimus sp., Alaria sp., and an unidentified strigeid type) over 24 hr. Exposure to MC-LR did not affect the activity of any cercarial type, nor was survival reduced. In fact, the strigeid-type cercariae had significantly increased longevity if exposed to either MC-LR solution, with the greatest longevity in the highest concentration. Our results indicate that MC-LR may have opposing effects on aquatic parasites and their hosts, potentially increasing host susceptibility but having a neutral or positive effect on motile infectious stages such as cercariae. Cyanobacterial blooms could thus enhance trematode transmission; however, the effects of other cyanotoxins must be studied, as well as a broader range of host and parasite species.
Subject(s)
Bacterial Toxins/toxicity , Marine Toxins/toxicity , Microcystins/toxicity , Trematoda/drug effects , Animals , Cercaria/drug effects , Cyanobacteria Toxins , Dose-Response Relationship, Drug , Echinostoma/drug effects , Eutrophication , Linear Models , Ponds , Snails/parasitologyABSTRACT
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
Animals infected by parasites or pathogens can exhibit altered behaviors that may reduce the costs of infection to the host or represent manipulations that benefit the parasite. Given that temperature affects many critical physiological processes, changes in thermoregulatory behaviors are an important consideration for infected hosts, especially ectotherms. Here we examined the temperature choices of freshwater snails (Helisoma trivolvis) that were or were not infected by a trematode (flatworm) parasite (Echinostoma trivolvis). Active snails that explored the experimental temperature gradient differed in their thermal preference based on their infection status, as parasitized snails chose to position themselves at a significantly higher temperature (mean: 25.4°C) compared to those that were uninfected (mean: 23.3°C). Given that snails rarely eliminate established trematode infections, we suggest that this altered thermal preference shown by infected hosts likely benefits the parasite by increasing the odds of successful transmission, either through enhanced production and emergence of infectious stages or by increasing spatial overlap with the next hosts of the complex life cycle. Further studies that employ experimental infections to examine temperature selection at different time points will be needed to understand the extent of altered host thermal preferences, as well as the possible benefits to both host and parasite.
Subject(s)
Behavior, Animal/physiology , Echinostomiasis/parasitology , Snails/parasitology , Temperature , Animals , Echinostoma , Host-Parasite Interactions/physiology , Movement , Snails/physiologyABSTRACT
Understanding how parasite communities are assembled, and the factors that influence their richness, can improve our knowledge of parasite-host interactions and help to predict the spread of infectious diseases. Previous comparative analyses have found significant influences of host ecology and life history, but focused on a few select host taxa. Host diet and habitat use play key roles in the acquisition of parasitic helminths as many are trophically transmitted, making these attributes potentially key indicators of infection risk. Given the paucity of comparative studies with non-piscine, non-avian or non-mammalian hosts, it is critical to examine the degree to which host ecology influences parasite communities in other host taxa in order to identify common drivers. We examined helminth diversity in over 350 species of lizards in relation to their body mass, ecology (diet and habitat use) and life history (clutch size, and ovo- or viviparity) using previously published data. Overall, lizard species with herbivorous diets harboured fewer types of helminths (especially larval stages), with similar results for traits that were ultimately strongly associated with diet (host mass and habitat use). Large hosts tended to be herbivores with few helminth types, whereas species utilizing arboreal habitats typically consumed some animal matter and hosted more helminths. Understanding how host ecology and life history are related to their parasite assemblages has significant implications for the risk of acquiring novel parasites. Our results indicate an overwhelming influence of host diet such that many helminths may be relatively easily acquired by hosts in new ranges, or through dietary shifts.