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We combined fatty acid (FA) and stable isotope (SI) analyses to investigate the trophic ecology of different stages of European eels (Anguilla anguilla) across seawater (SW), brackish water (BW), and freshwater (FW) habitats. Salinity was the main driver of differences in the biochemical composition, and the greatest variation occurred between SW and FW eels. SW eels had a higher content of the FA indicator of carnivory, as well as the highest stable isotope ratios (C, N). In contrast, FW eels exhibited the highest lipid content and omega-6 polyunsaturated FA, but the lowest stable isotope ratios, suggesting major dietary differences between the eels in these two habitats. While the biochemical composition of BW eels was closer to those of SW eels, BW eels had the largest SI range, indicating higher dietary plasticity. FW individuals had better overall condition compared to SW eels. Independent of habitat, larger individuals were in the best condition, and had higher lipid content and monounsaturated FA. These findings suggest a biological advantage for eels to maintain a catadromous life history strategy.

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.

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.

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.

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 (

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.

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.

This is the peer reviewed version of the following article: Murray, R.L., S. Tah, J. Koprivnikar, L. Rowe, and S.J. McCauley. 2020. Exposure to potentially cannibalistic conspecifics induces an increased immune response. Ecological Entomology 45: 355 – 363. which has been published in final form at https://doi.org/10.1111/een.12806.

Little information is available on the effects of neonicotinoid insecticides on vertebrates. Previous work using amphibians found chronic exposure to some neonicotinoids had no detrimental effects on fitness-relevant traits. However, there is some evidence of more subtle effects of neonicotinoids on immune traits and evidence that other pesticides can suppress tadpole immunity resulting in elevated levels of parasitism in the exposed tadpoles. The objective of our study was to assess whether neonicotinoid exposure affected tadpole immunometrics and susceptibility to parasitic helminths. We assessed northern leopard frog tadpole (Lithobates pipiens) levels of parasitism and leukocyte profiles following exposure to environmentally relevant concentrations of clothianidin and free-living infective cercariae of a helminth parasite, an Echinostoma sp. trematode. When comparing tadpoles from controls to either 1 or 100 μg/L clothianidin treatments, we found similar measures of parasitism (i.e. prevalence, abundance and intensity of echinostome cysts) and similar leukocyte profiles. We also confirmed that clothianidin was not lethal for cercariae; however, slight reductions in swimming activity were detected at the lowest exposure concentration of 0.23 μg/L. Our results show that exposure to clothianidin during the larval amphibian stage does not affect leukocyte profiles or susceptibility to parasitism by larval trematodes in northern leopard frogs although other aspects such as length of host exposure require further study.

The negative effects of abiotic and biotic stressors on animal condition, physiology, behaviour, and fitness have become increasingly recognized, making it critical to understand how these may be mitigated, such as through diet. When consumed, dietary antioxidants (secondary metabolites produced by plants) provide protection from oxidative damage that can result from exposure to stressors. We examined the effects of dietary antioxidants (β-carotene and vitamin E) on the ability of Lithobates sylvaticus (wood frog) tadpoles to overcome the detrimental effects imposed by two common environmental stressors - exposure to the herbicide atrazine or infection by a pathogenic helminth parasite (Echinostoma trivolvis). Tadpoles which were fed high concentrations of either vitamin E or β-carotene had a greater immune response compared to those given trace diets of either compound as measured by circulating white blood cells and a phytohemaglutination assay (PHA). Similarly, tadpoles in the herbicide and parasitism treatments that were given trace antioxidant diets had significant weight loss, whereas those consuming high levels of vitamin E or β-carotene did not. Our results suggest that dietary antioxidants, specifically β-carotene and vitamin E, have a positive effect on tadpole immune systems and overall condition that likely allows them to better cope with natural stressors, with potential implications for their foraging behaviour.

Predators kill and consume prey, but also scare living prey. Fitness of prey can be reduced by direct killing and consumption, but also by non-consumptive effects (NCEs) if prey show costly risk-induced trait responses (RITRs) to predators, which are meant to reduce predation risk. Recently, similarities between predators and parasites as natural enemies have been recognized, including their potential to cause victim RITRs and NCEs. However, plant-herbivore and animal host-parasite associations might be more comparable as victim-enemy systems in this context than either is to prey-predator systems. This is because plant herbivores and animal parasites are often invertebrate species that are typically smaller than their victims, generally cause lower lethality, and allow for further defensive responses by victims after consumption begins. Invertebrate herbivores can cause diverse RITRs in plants through various means, and animals also exhibit assorted RITRs to increased parasitism risk. This synthesis aims to broadly compare these two enemy-victim systems by highlighting the ways in which plants and animals perceive threat and respond with a range of induced victim trait responses that can provide pre-emptive defense against invertebrate enemies. We also review evidence that RITRs are costly in terms of reducing victim fitness or abundance, demonstrating how work with one victim-enemy system can inform the other with respect to the frequency and magnitude of RITRs and possible NCEs. We particularly highlight gaps in our knowledge about plant and animal host responses to their invertebrate enemies that may guide directions for future research. Comparing how potential plant and animal victims respond pre-emptively to the threat of consumption via RITRs will help to advance our understanding of natural enemy ecology and may have utility for pest and disease control.

Hypothesis – Snails with trematode infections and exposure to increased temperatures will show greater preference for antioxidant-rich foods

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.

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.

Neonicotinoids are a popular class of systemic insecticides registered for use in over 120 countries. Recent global water surveys have found neonicotinoid insecticides in waterbodies adjacent to agricultural fields. The presence of neonicotinoids in surface waters raises the concern of the potential risk of exposure to non-target aquatic species, with relevance for both free-living and parasitic taxa. The susceptibility of aquatic free-living parasitic stages to the lethal effects of neonicotinoids may influence the prevalence and intensity of host infection, and their availability as prey for a variety of organisms (e.g., fish, invertebrates). We examined the effects of two commonly used neonicotinoids on the survival of free-living infectious stages (cercariae) from two trematode (flatworm) species (Diplostomum sp. and Haematoloechus sp.). We found that exposure to commercially formulated imidacloprid and thiamethoxam, individually and in a binary mixture, had no significant effect on cercarial survival for either species at environmentally relevant concentrations. Further study is required to understand if the ability of the surviving cercariae to infect the next host in their life cycle is compromised in the presence of neonicotinoids, or if host defenses are compromised, as changes in parasite infectivity or host susceptibility could influence infection dynamics and have community- and ecosystem-level implications.

In nature, multiple waves of exposure to the same parasite are likely, making it important to understand how initial exposure or infection affects subsequent host infections, including the underlying physiological pathways involved. We tested whether experimental exposure to trematodes (Echinostoma trivolvis or Ribeiroia ondatrae) affected the stress hormone corticosterone (known to influence immunocompetence) in larvae representing five anuran species. We also examined the leukocyte profiles of seven host species after single exposure to R. ondatrae (including four species at multiple time points) and determined if parasite success differed between individuals given one or two challenges. We found strong interspecific variation among anuran species in their corticosterone levels and leukocyte profiles, and fewer R. ondatrae established in tadpoles previously challenged, consistent with defense "priming." However, exposure to either trematode had only weak effects on our measured responses. Tadpoles exposed to E. trivolvis had decreased corticosterone levels relative to controls, whereas those exposed to R. ondatrae exhibited no change. Similarly, R. ondatrae exposure did not lead to appreciable changes in host leukocyte profiles, even after multiple challenges. Prior exposure thus influenced host susceptibility to trematodes, but was not obviously associated with shifts in leukocyte counts or corticosterone, in contrast to work with microparasites.

Habitat attributes are known to influence infectious diseases such as those caused by parasites, but most studies have only considered single host and (or) parasite taxa, making it difficult to assess which features may be of general importance and to predict how alterations could affect disease dynamics. We examined infection with trematode (flatworm) parasites in two commonly co-occurring host taxa (larval amphibians and larval odonates (dragonflies and damselflies)) to investigate links with landscape-level features, including agricultural activity. We also assessed pond community composition with respect to the abundance and richness of aquatic arthropods known to prey upon tadpoles and (or) free-swimming trematode infectious stages. Larval amphibians from agricultural sites were most likely to be parasitized but had lower infection intensities, and infected hosts were positively associated with increasing distance to the nearest forest habitat, but negatively with road distance. The opposite was observed for larval odonate infection status; however, probability and intensity of parasitism in both host taxa was negatively associated with greater predatory arthropod abundance, consistent with the “dilution effect” of biodiversity on infectious diseases. Our approach demonstrates the importance of considering multiple host taxa when studying habitat links to diseases, and future studies incorporating even greater diversity will be needed.

Large quantities of road salts are used for de-icing in temperate climates but often leach into aquatic ecosystems where they can cause harm to inhabitants, including reduced growth and survival. However, the implications of road salt exposure for aquatic animal susceptibility to pathogens and parasites have not yet been examined even though infectious diseases can significantly contribute to wildlife population declines. Through a field survey, we found a range of NaCl concentrations (50-560mg/L) in ponds known to contain larval amphibians, with lower levels found in sites close to gravel- rather than hard-surfaced roads. We then investigated how chronic exposure to environmentally-realistic levels of road salt (up to 1140mg/L) affected susceptibility to infection by trematode parasites (helminths) in larval stages of two amphibian species (Lithobates sylvaticus - wood frogs, and L. pipiens - northern leopard frogs) by considering effects on host anti-parasite behavior and white blood cell profiles. Wood frogs exposed to road salt had higher parasite loads, and also exhibited reduced anti-parasite behavior in these conditions. In contrast, infection intensity in northern leopard frogs had a non-monotonic response to road salts even though lymphocytes were only elevated at the highest concentration. Our results indicate the potential for chronic road salt exposure to affect larval amphibian susceptibility to pathogenic parasites through alterations of behavior and immunocompetence, with further studies needed at higher concentrations, as well as that of road salts on free-living parasite infectious stages.

The free-living infectious stages of macroparasites, specifically, the cercariae of trematodes (flatworms), are likely to be significant (albeit underappreciated) vectors of nutritionally important polyunsaturated fatty acids (PUFA) to consumers within aquatic food webs, and other macroparasites could serve similar roles. In the context of de novo omega-3 (n-3) PUFA biosynthesis, it was thought that most animals lack the fatty acid (FA) desaturase enzymes that convert stearic acid (18:0) into ɑ-linolenic acid (ALA; 18:3n-3), the main FA precursor for n-3 long-chain PUFA. Recently, novel sequences of these enzymes were recovered from 80 species from six invertebrate phyla, with experimental confirmation of gene function in five phyla. Given this wide distribution, and the unusual attributes of flatworm genomes, we conducted an additional search for genes for de novo n-3 PUFA in the phylum Platyhelminthes. Searches with experimentally confirmed sequences from Rotifera recovered nine relevant FA desaturase sequences from eight species in four genera in the two exclusively endoparasite classes (Trematoda and Cestoda). These results could indicate adaptations of these particular parasite species, or may reflect the uneven taxonomic coverage of sequence databases. Although additional genomic data and, particularly, experimental study of gene functionality are important future validation steps, our results indicate endoparasitic platyhelminths may have enzymes for de novo n-3 PUFA biosynthesis, thereby contributing to global PUFA production, but also representing a potential target for clinical antihelmintic applications.

Many temperate freshwater habitats are at risk for contamination by run-off associated with the application of road de-icing salts. Elevated salinity can have various detrimental effects on freshwater organisms, including greater susceptibility to infection by parasites and pathogens. However, to better understand the net effects of road salt exposure on host–parasite dynamics, it is necessary to consider the impacts on free-living parasite infectious stages, such as the motile aquatic cercariae of trematodes. Here, we examined the longevity and activity of cercariae from four different freshwater trematodes (Ribeiroia ondatrae, Echinostoma sp., Cephalogonimus sp. and an unidentified strigeid-type) that were exposed to road salt at five different environmentally relevant concentrations (160, 360, 560, 760 and 960 mg/ml of sodium chloride). Exposure to road salt had minimal detrimental effects, with cercariae activity and survival often greatest at intermediate concentrations. Only the cercariae of Cephalogonimus sp. showed reduced longevity at the highest salt concentration, with those of both R. ondatrae and the unidentified strigeid-type exhibiting diminished activity, indicating interspecific variation in response. Importantly, cercariae seem to be relatively unaffected by salt concentrations known to increase infection susceptibility in some of their hosts. More studies will be needed to examine this potential dichotomy in road salt effects between hosts and trematodes, including influences on parasite infectivity.

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.

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.

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.

Previous studies have found that migratory birds generally have a more diverse array of pathogens such as parasites, as well as higher intensities of infection. However, it is not clear whether this is driven by the metabolic and physiological demands of migration, differential selection on host life-history traits or basic ecological differences between migratory and non-migratory species. Parasitic helminths can cause significant pathology in their hosts, and many are trophically transmitted such that host diet and habitat use play key roles in the acquisition of infections. Given the concurrent changes in avian habitats and migratory behaviour, it is critical to understand the degree to which host ecology influences their parasite communities. We examined nematode parasite diversity in 153 species of Anseriformes (water birds) and Accipitriformes (predatory birds) in relation to their migratory behaviour, diet, habitat use, geographic distribution and life history using previously published data. Overall, migrators, host species with wide geographic distributions and those utilizing multiple aquatic habitats had greater nematode richness (number of species), and birds with large clutches harboured more diverse nematode fauna with respect to number of superfamilies. Separate analyses for each host order found similar results related to distribution, habitat use and migration; however, herbivorous water birds played host to a less diverse nematode community compared to those that consume some animals. Birds using multiple aquatic habitats have a more diverse nematode fauna relative to primarily terrestrial species, likely because there is greater opportunity for contact with parasite infectious stages and/or consumption of infected hosts. As such, omnivorous and carnivorous birds using aquatic habitats may be more affected by environmental changes that alter their diet and range. Even though there were no overall differences in their ecology and life history compared with non-migrators, migratory bird species still harboured a more diverse array of nematodes, suggesting that this behaviour places unique demands on these hosts and warrants further study.

Increasing evidence indicates that parasites play an important role within many systems as prey for higher trophic levels. Predation on parasites can decrease their numbers and may affect host infection rates. Cercariae, a free-living infectious stage of trematode parasites, are abundant in freshwater systems and are directly consumed by a number of freshwater predators. However, few studies have tested whether predators exhibit a preference for cercariae when alternative prey are available or how these preferences vary across predator body sizes. We assessed whether dragonfly larvae (dot-tailed whiteface, Leucorrhinia intacta (Hagen, 1861)), top predators in freshwater systems without fish, foraged preferentially when presented with two prey types, cercariae and zooplankton, and whether foraging preferences changed across predator body size. Body size of larval dragonfly predators was found to be significantly, and negatively, related to the fraction of cercariae in the diet. Larger bodied dragonfly larvae shifted their diet choice from cercariae to zooplankton. Changes in foraging selectivity as body size increases across a predator’s ontogeny can alter the strength of predator–prey interactions. Further investigation into size-selective foraging on parasites may provide new insights into the effects of predation on parasite abundance and transmission in natural systems.

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.

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.

Prey should adjust their defences against natural enemies to match their current level of risk and balance other needs. This is particularly important when optimal defences represent trade-offs, as is the case with many predator-induced trait-mediated indirect effects (TMIEs) that are antagonistic to those promoting host resistance to parasites and pathogens. However, trade-offs may depend on whether different natural enemies are present simultaneously or represent temporally discrete threats. We found that larval amphibians ( Anaxyrus americanus ) previously exposed to predator cues did not engage in anti-parasite behaviours (activity increases) in response to a current risk of infection by a pathogenic trematode parasite compared to controls, resulting in higher infection intensities. This suggests that the memory of the likely more lethal threat (predation) had greater influence, maladaptively dampening tadpole activity. Incorporating complexity inherent in natural systems, including spatial and temporal overlap, is necessary to better understand natural enemy ecology and how TMIEs relate to infectious diseases.

Environmental changes are simultaneously affecting parasitic diseases and animal migrations, making it important to understand the disease dynamics of migratory species, including their range of infections and investment into defences. There is an urgent need for such knowledge because migratory animals, especially birds, are important for pathogen transmission and also particularly sensitive to environmental changes. Here we compare the nematode species richness and relative immune investment (via relative spleen size) of almost 200 migratory and non-migratory species within three diverse groups of birds (Anseriformes, Accipitriformes and Turdidae) with worldwide distributions and varied ecology. Our results provide the first large-scale demonstration that migratory birds face greater challenge from macroparasites as they have significantly dissimilar nematode fauna and higher nematode species richness compared to non-migratory species. Even though birds with relatively large spleens had more nematode species, there was no difference in relative spleen size between migratory and non-migratory bird species. The physiological stress of migration can be exacerbated by the potential range of pathologies induced by their richer nematode communities, particularly in combination with environmental perturbations. Altered migration stemming from global changes can also have important consequences for nematode transmission. Synthesis Most studies on parasites of migratory birds versus non-migratory birds focus upon blood parasites; here we compared the diversity of another important parasite group – nematodes (roundworms) in three orders of birds. We found for any given order, migratory species and species with proportionally larger spleens generally have a wider range of nematodes. It is unclear why migratory species harbour more nematode species. Global climate change is expected to influence both bird migration patterns and infectious diseases, which may increase host susceptibility to parasitism and also introduce diverse nematodes to new areas and potential hosts.

Hydroperiod strongly influences the breeding period and development time of many amphibians, and larvae of various species display developmental plasticity in response to habitat drying. Hydrologic alterations associated with anthropogenic activities potentially can influence host–parasite interactions in humans and wildlife, but few investigators have examined this possibility. Pathogens can delay amphibian development, so infections could constrain the ability of parasitized larvae to respond to a shortened hydroperiod under drying conditions. We examined the individual and joint effects of hydroperiod and infection with a pathogenic trematode parasite (Ribeiroia ondatrae) on larval development of Pacific chorus frogs (Pseudacris regilla) in mesocosms. Tadpoles subjected to accelerated drying were twice as likely to emerge early. However, this tendency was most pronounced among uninfected individuals (96% of early-emerging individuals) and may have arisen from differences in competitive ability ...

Despite the ubiquity of bilateral symmetry among animals, a long-standing mystery centers on why parasites that infect paired organs often do so non-randomly. Examples from diverse host and parasite taxa continue to accumulate, yet little is known about their causes or implications for host – parasite fi tness. We combined fi eld surveys, experimental infections, and parasite choice assays to evaluate both competing explanations for – and consequences of – asymmetric infections of amphibian kidneys by echinostome trematodes, which are widespread and potentially pathogenic infections of larval amphibians. Samples from 6001 hosts representing 26 species indicated that echinostome infections exhibit a consistent, right-kidney bias, with ∼ 62% of parasites in the right kidney. Th is pattern could not be explained by variation in kidney size or total infection. Experimental infections of three anuran species reproduced this pattern, with 64% of infections in the right kidney, and indicated it was not the result of diff erential host or parasite mortality. Based on sequential infection experiments and parasite choice assays, we further showed that earlier infections did not aff ect the distribution of subsequently colonizing parasites and that echinostome cercariae followed host-derived cues rather than exhibiting congenital ‘ sidedness ’ . We advance the hypothesis that variation in the position of the right kidney along the anterior – posterior axis controls cue strength in the right nephric duct and thus determines parasite encystment. Correspondingly, anatomical measurements from a subset of larval amphibian hosts revealed that the relative position of the right kidney explained 83% of the variation in infection bias, with no additional contributions associated with kidney volume or host size. We also show that the degree of right-kidney bias associated positively with host growth in experiments. Morphological asymmetries could therefore function as a unique form of tolerance to mitigate the consequences of infection, despite the oft-cited costs of asymmetry for mate selection and enemy vulnerability.

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 (

Along with immune defences, many animals exhibit effective anti-parasite behaviours such as parasite avoidance and removal that influence their susceptibility to infection. Host ecology and life history influence investment into comparatively fixed defences such as innate immunity but may affect the strength of anti-parasite behaviours as well. We investigated activity levels in five different species of larval amphibian with varying life histories and ecology in control, novel food stimulus, and trematode parasite (Echinoparyphium sp.) threat conditions. There was a significant interaction of species and treatment given that American toad (Bufo americanus), wood frog (Lithobates sylvaticus), and bullfrog (Lithobates catesbeianus) tadpoles generally increased their activity when parasite infectious stages were present while grey tree frogs (Hyla versicolor) and northern leopard frogs (Lithobates pipiens) did not, even though activity was negatively related to infection. In addition, there was considerable variation among species in their susceptibility to parasitism, with infection prevalence ranging from 17% in bullfrog tadpoles to 70% in wood frogs. However, amphibian life history (larval and adult traits) was not related to parasitism or level of anti-parasite behaviour at the species level. Consequently, we suggest that future investigations include more species with a range of life history traits and also consider host ecology, particularly if conspicuous anti-parasite behaviours are more likely in amphibian species that experience a relatively low risk of predation.

Many fields in the biological sciences have witnessed a shift away from organism- or taxon-focused research and teaching in favor of more conceptual and process-driven paradigms. The field of parasitology is no exception, despite the diversity of topics and taxa it encompasses. Concurrently, however, interest in disease ecology has increased dramatically, suggesting new opportunities that merit exploration, as well as the need for parasitology to promote its long history of ecological research to do so. Here we undertake a quantitative analysis of metrics relating to publications, research funding, career opportunities, and undergraduate teaching to comprehensively illustrate the rising prominence of disease ecology. While we distinguish generally between the fields of parasitology and disease ecology, we also emphasize the common interests and complementary approaches that enhanced integration could offer. To illustrate why enhanced integration between these 2 fields is increasingly critical, we highlight 2 successful areas in which parasitology and disease ecology have intersected (community assembly and scale, and the effects of natural enemies on life history traits). We conclude by identifying "frontier topics" that will benefit from greater cooperation and interaction between these currently relatively separate areas and the need for principal investigators to identify and communicate changes in their discipline to students and trainees, which will collectively result in many possible new benefits and prospects for current and future researchers.

Agricultural activity can alter host-parasite interactions through associated contam- inants and habitat perturbations. It is critical to determine whether agricultural effects are widespread or limited to specific types of agriculture. We examined influences of soybean agriculture on trematode parasitism of larval amphibians (grey tree frogs; Hyla versicolor) to assess the potential effects of a commonly applied pesticide (glyphosate) and landscape factors relative to previous field studies focusing on the herbicide atrazine. Overall, trematode parasite infection did not differ between soybean-adjacent and nonagricultural ponds (87.7% and 72.6% mean infection, respectively). However, host-generalist echinostome species were more common in tadpoles from soybean-associated ponds (86.3% mean infection versus 36.2% in nonagricultural ponds) as well as sites with large or short average distances to forest cover and roads, respectively. In contrast, the occurrence of a host-specialist (Alaria sp.) group was greater in nonagricultural ponds (50.3% mean infection versus 9.8% in soybean-associated ponds) and increased with shorter distances to the closest forest patch and smaller average forest distance. Because glyphosate was not detected at any site and landscape influences were parasite-specific, we suggest that agriculture may have broad effects on wildlife diseases through habitat alterations that affect pathogen transmission via host habitat suitability. Notably, nonagricultural ponds had a lower mean distance to the nearest forest patch and lower mean forest distance compared with soybean-adjacent ponds. As a result, we emphasize the need for wider investigations of habitat perturbations generally associated with agriculture for host-pathogen interactions, and consequently, wildlife conservation and management strategies.

Understanding linkages between environmental changes and disease emergence in human and wildlife populations represents one of the greatest challenges to ecologists and parasitologists. While there is considerable interest in drivers of amphibian microparasite infections and the resulting consequences, comparatively little research has addressed such questions for amphibian macroparasites. What work has been done in this area has largely focused on nematodes of the genus Rhabdias and on two genera of trematodes (Ribeiroia and Echinostoma). Here, we provide a synopsis of amphibian macroparasites, explore how macroparasites may affect amphibian hosts and populations, and evaluate the significance of these parasites in larger community and ecosystem contexts. In addition, we consider environmental influences on amphibian-macroparasite interactions by exploring contemporary ecological factors known or hypothesized to affect patterns of infection. While some macroparasites of amphibians have direct negative effects on individual hosts, no studies have explicitly examined whether such infections can affect amphibian populations. Moreover, due to their complex life cycles and varying degrees of host specificity, amphibian macroparasites have rich potential as bioindicators of environmental modifications, especially providing insights into changes in food webs. Because of their documented pathologies and value as bioindicators, we emphasize the need for broader investigation of this understudied group, noting that ecological drivers affecting these parasites may also influence disease patterns in other aquatic fauna.

Environmental stressors have the potential to greatly impact the transmission of parasites with complex, multi-host life cycles such as those of trematodes. The commonly used herbicide atrazine has been shown to affect the susceptibility of second intermediate hosts (such as larval amphibians) to trematode infection, as well as the longevity and infectivity of the free-swimming cercariae, but not eggs or the free-swimming miracidia that infect the gastropod first intermediate hosts. However, we do not know if this pesticide influences the survival of infected snails or whether it affects cercariae production within, or emergence from, these hosts. In addition, previous studies of host-parasite dynamics have only examined the parent atrazine compound, not any of the long-lasting metabolites commonly present in water bodies. Here, we report that a concentration of 0.33 µg/L of an atrazine metabolite, desethyl atrazine, increased the mortality of freshwater gastropods ( Stagnicola elodes ) infected with a gymnocephalus type of cercaria but not that of uninfected snails or those harboring a mature or dormant infection of Echinoparyphium sp. In contrast, 2 wk of exposure to desethyl atrazine did not affect the emergence of gymnocephalus cercariae from snails, although a trend for a decrease in the emergence of Echinoparyphium sp. cercariae was observed. We suggest that simultaneous trematode infection and exposure to contaminants may represent a significant combined stress to gastropods, but this is likely parasite species-specific as well as dependent on whether cercariae are being actively produced.

Given the importance of temperature for the shedding of trematode infective stages (cercariae) from gastropod first intermediate hosts, we investigated the response to temperature increases of trematodes of the intertidal snail Zeacumantus subcarinatus collected from different latitudes (differing in mean annual summer temperature) on the South Island of New Zealand. We investigated whether shedding of cercariae at elevated temperatures differed both between species (interspecific variation) and among populations of each trematode species (intraspecific variation). The shedding of one trematode species, Maritrema novaezealandensis (Microphallidae), appears to decrease with increased temperature and differed among locations. In contrast, the shedding of a second species, Acanthoparyphium sp. (Echinostomatidae), increased at warmer temperatures. In particular, Acanthoparyphium sp.-infected snails from 1 location showed the greatest increase in the shedding of cercariae in response to elevated temperature. Our results demonstrate that different trematode species and populations may be dissimilarly impacted by temperature changes resulting from global warming. In addition, both interspecific and intraspecific variation may result in different impacts of trematodes on ecosystems at different locales.

Parasites, in particular trematodes, are unseen but ubiquitous components of marine intertidal ecosystems. Although parasites are known to affect population dynamics and food web structure, their potential function as an unrecognized path of energy flow in these ecosystems is yet to be quantified. We use published data on rates at which trematodes produce free-swimming infective larvae (cercariae) that are released from their gastropod intermediate hosts to investigate patterns in cercarial output as a function of different variables, and to calculate the annual production of cercariae in different marine benthic systems. Across 18 trematode species, cercarial output (no. cercariae shed snail-1 d-1) ranged over 4 orders of magnitude and was positively correlated with snail host species size. While cercarial output did not correlate with latitude, it did correlate negatively with the size of cercariae, and was influenced by the type of downstream host sought by cercariae, being highest when this host was a vertebrate. Our estimates of annual cercarial production (kJ m-2 yr-1), which take into account the density of infected snails in the habitat, were within the range of production values reported for free-living invertebrates inhabiting benthic ecosystems. These estimates would be much higher if they included all trematode species in an ecosystem, and not just single-species values. Overall, results suggest that trematode cercariae represent potentially important paths of energy flow in benthic systems as well as a potentially important food supply to benthic organisms.

Population density and infection with parasites often are important factors affecting the growth and development of individuals. How these factors co-occur and interact in nature should have important consequences for individual fitness and higher-order phenomena, such as population dynamics of hosts and their interactions with other species. However, few studies have examined the joint effects of density and parasitism on host growth and development. We examined the co-influences of rearing density and parasitism, by the trematode Echinostoma trivolvis, on the growth and development of larval frogs, Rana (=Lithobates) pipiens. We also examined the potential role of parasite-mediated intraspecific competition by observing how unparasitized individuals performed when housed with other unparasitized tadpoles, versus housing with a combination of unparasitized and parasitized hosts. Mean mass and mean developmental stage were reduced under high rearing densities. The presence of parasitized conspecifics had no significant effect, but there was a significant interaction of density and parasitism presence on host mass, due to the fact that parasitized conspecifics grew poorly at high densities. Unparasitized individuals reared with parasitized and unparasitized conspecifics fared no better than unparasitized individuals reared only with one another. This result indicates that infected hosts compete as much as uninfected hosts for resources, even though infected individuals have reduced mass under high-density conditions. Resource acquisition and resource allocation are different processes, and parasitism, if it only affects the latter, might not have a discernible impact on competitive interactions.

Many animals respond behaviourally to the infective stages of parasites, but the efficacy of such responses in reducing risk of parasitism often is not established. It was found that tadpoles of Rana clamitans Latr., 1801 (green frogs) and R. sylvatica LeConte, 1825 (wood frogs) increased their activity when exposed to live infective stages (cercariae) of the trematode Echinostoma trivolvis Rudolphi, 1809. The susceptibility to parasitism for green frog tadpoles subjected to three different treatments was compared. Tadpoles were housed at 20 8C and allowed to respond to cercariae, held at 6- 8 8C and showing reduced behavioural responses, or anesthetized and showing no responses. Low levels of parasitism were found for tadpoles that responded behaviourally to cercariae; such responses are expected to occur under normal field conditions in the absence of factors suppressing activity of tadpoles. We also demonstrate that infectivity of E. trivolvis cercariae to non-responding (anesthetized) wood frog tadpoles was higher at warm than at cool temperatures. Thus, low- ered parasitism at warm temperatures in the first experiment likely resulted from host behavioural responses and not from low infectivity of cercariae. These results have implications for observing effects of environmental factors on susceptibility to parasitism where susceptibility is thought or known to be mediated by host behaviour. Resume ´ : De nombreux animaux reagissent par leur comportement aux stades infectieux des parasites, mais l'efficacitede telles reactions dans la reduction du risque de parasitisme n'est souvent pas etablie. Exposes aux stades infectieux (cerc- aires) du trematode Echinostoma trivolvis Rudolphi, 1809, les tetards de Rana clamitans Latr., 1801 (grenouilles vertes) et R. sylvatica LeConte, 1825 (grenouilles des bois) augmentent leur activite ´. Nous avons comparela susceptibilitede tetards de la grenouille verte au parasitisme dans trois conditions experimentales. Les tetards ont etegardesa ` 20 8C et libres de reagir aux cercaires, ou alors maintenus a ` 6-8 8C et capables seulement d'une reaction comportementale reduite, ou enfin anesthesies et incapables de reagir. Les tetards qui ont des reactions comportementales aux cercaires ont de faibles taux de parasitisme; de telles reactions se produisent probablement en nature en l'absence de facteurs qui inhibent l'activitedes te ˆ- tards. Nous demontrons aussi que l'infectivitedes cercaires de E. trivolvis chez les tetards inactifs (anesthesies) de la gre- nouille des bois est plus importante aux temperatures chaudes qu'aux frao ˆches. Le parasitisme reduit aux temperatures elevees dans la premiere experience resulte donc vraisemblablement des comportements de reaction des hotes et non d'une infectivitereduite des cercaires. Ces resultats ont des consequences lorsqu'on observe les effets des facteurs environnemen- taux sur la susceptibiliteau parasitisme, si l'on sait ou l'on soupconne que la susceptibiliteest reliee au comportement de l'hote. (Traduit par la Redaction)

The emergence or increased prevalence of various parasites may be linked to alterations in host-parasite interactions caused by environmental changes. We investigated prevalence of trematode infections in grey tree frog (Hyla versicolor) tadpoles from ponds in nonagricultural settings versus ponds adjacent to cornfields in southern Ontario. We found that agricultural activity was a significant factor in determining the percentage of tadpoles infected by 1 or more trematodes from 1 or more species (combined trematode infection). However, we found no associations between combined trematode infection and forest cover; pond size; road density; and measures of water quality, such as nitrate level and the presence of the herbicide atrazine. Although combined trematode prevalence was associated only with agricultural activity, prevalence of Alaria species showed a positive association with forest cover. This latter result probably reflects the importance of habitat suitability for the canid definitive hosts of this trematode species.