Structure and temporal variation of trematode and gastropod communities in a freshwater ecosystem.

The infro- and component community dynamics of digenetic trematodes in a freshwater gastropod community were examined over a 33-month period. The gastropod and trematode communities were composed of 17 and 10 species respectively. A total of 9,831 snails was collected; among them, 192 belonging to 14 species were infected by larval trematodes. The size of infected snails was significantly greater than that of healthy ones, and the increase of prevalence with size/age was interpreted as related to the increased probability of ultimately becoming parasitized. The trematode community was rich in allogenic species, but the most frequent trematode (cercariaeum) was autogenic and generalist (a range of 12 snail host species). There was a significantly positive relationship between the frequency of trematode species in the community and the number of first intermediate host species. A great temporal heterogeneity occurred in the prevalence of the snails, mainly attributed to the great temporal fluctuations of snail host populations and the variability of freshwater ecological conditions. The data on the occurrence of larval trematodes in 14 host species over the 33-month study allowed indicate a significant negative correlation between the abundance of gastropods and the prevalence of trematodes.     

Effects of trematode double infection on the shell size and distribution of snail hosts

Infection with larval trematodes sometimes alters the phenotypes of their snail hosts. While some trematode species have distinct effects on host phenotypes, it is still unclear how snail phenotypes are altered when they are parasitized with multiple trematode species. Here, we report that double infection with trematode species averages the effects of parasitic alteration on host phenotype. We found that snail hosts Batillaria attramentaria (Batillariidae) infected with Cercaria batillariae (Heterophyidae) have abnormally large shells and distribute in lower areas of the intertidal zone. Snails with another dominant trematode species, the renicolid cercaria I (Renicolidae), have slightly larger shells and distribute in upper areas of the intertidal zone. A number of double infections with both trematodes was observed in this study. Snails infected with both trematode species exhibited an intermediate size and inhabited a depth between those of snails solely infected with either trematode species, suggesting that the two trematodes simultaneously affected the snail phenotypes. Because altered host phenotypes are frequently beneficial to parasites, two trematode species may compete for successful transmission through alteration of host phenotypes.     

Environmental factors influencing community composition of gastropods and their trematode parasites in southern Ontario

Agricultural activity and landscape features have previously been associated with diversity and prevalence of trematode species in amphibian second intermediate hosts. In this study, the density, diversity, and size of snail first intermediate hosts, and the diversity and prevalence of their trematode species, were assessed in 2 types of ponds, i.e., those adjacent to cornfields and those from the same region in southwestern Ontario that were adjacent to nonagricultural settings. Species of trematodes included, but were not restricted to, those that are known parasites of larval and adult frogs. We also assessed landscape factors likely to influence use by definitive hosts. Presence of the herbicide atrazine in ponds was measured to check that ponds adjacent to agriculture had potential to be affected by agricultural runoff. Both snail size and the proportion of snails releasing cercariae were greater in nonagricultural ponds, contrasting with a previous finding of lower trematode infection in tadpoles from nonagricultural ponds. Percentage of forest cover was associated with prevalence of certain trematode species, but not with estimates of combined prevalence. Absence of relations of trematode prevalence to measures of road density also contrasted with previous studies. We interpret our results in light of how agricultural activity might influence trematode viability, snail growth, and use by wildlife definitive hosts, independently of landscape factors.     

Solving cryptogenic histories using host and parasite molecular genetics: the resolution of Littorina littorea's North American origin

Even after decades of investigation using multiple sources of evidence, the natural histories of some species remain unclear (i.e. cryptogenic). A key example is Littorina littorea , the most abundant intertidal snail in northeastern North America. Native to Europe, the snail's ecological history in North America has been debated for over 100 years with no definitive resolution. To resolve its cryptogenic status, we used molecular genetics from a novel combination of the snail and a highly associated trematode parasite, Cryptocotyle lingua . Based on mitochondrial sequences of 370 L. littorea and 196 C. lingua individuals, our results demonstrate a significant reduction in genetic diversity in North America vs. Europe, North American haplotypes nested within European haplotypes, and mean divergence estimates of ~500 years ago from Europe for both host and parasite — thus supporting a recent introduction of both host and parasite to North America from Europe. Our study therefore resolves not only a specific cryptogenic history, but it also demonstrates the success of our approach generally and could be used in resolving difficult invasion histories worldwide.     

洞庭湖外睾吸虫新种及其生活史

本文报告洞庭湖区鲶鱼肠道寄生的洞庭湖外睾吸虫Exorchis dongtinghuensis sp.nov(新种)及其全程生活史,其第一中间宿主为湖北钉螺Oncomelania hupensis;第二中间宿主为鲤鱼、鲫鱼和金鱼;终宿主为鲶鱼Parasilurus asotus。作者对各期宿主作了人工感染试验和现场自然感染调查。对其发育过程作了观察比较。     

Annotated key to the trematode species infecting Batillaria attramentaria (Prosobranchia: Batillariidae) as first intermediate host

In eastern Asia and western North America at least nine morphologically distinguishable species of digenean trematode infect the mud snail, Batillaria attramentaria (Sowerby 1855) (=B. cumingi (Crosse 1862)), as first intermediate host. Further, molecular and morphological evidence indicates that several of these trematode species comprise complexes of cryptic species. I present an identification key to these nine trematode morphospecies (including four newly reported species). Additionally, I provide an annotated list, which includes further diagnostic information on the larval stages (cercariae, parthenitae, and metacercariae), information on second intermediate host use, links to the previous relevant reports of trematodes infecting B. attramentaria and notes on other aspects of the species' biology.     

The phylogeny of the genus Indoplanorbis (Gastropoda,Planorbidae) from Africa and the French West Indies

Indoplanorbis exustus is a freshwater snail known as the intermediate host of various trematode parasites, including different species of the genus Schistosoma. Although its genetic diversity is well described in Asia, the phylogenetic diversity of strains from Africa and Guadeloupe (French West Indies) and their relationship to Asian and South‐East Asian strains remain unknown. To tackle this issue, we sampled individuals from Africa and Guadeloupe, and we computed phylogenetic reconstructions using five molecular markers: partial sequences of two mitochondrial genes, cox1 and 16S, and three nuclear markers, ITS1, ITS2 (Internal Transcribed Spacer 1 and 2) and 5.8S. Our results suggest that strains in Africa and Guadeloupe come from Asia and that they all belong to a single clade that is widespread around the globe.     

Differential Parasitism of Native and Introduced Snails: Replacement of a Parasite Fauna

The role of parasites in a marine invasion was assessed by first examining regional patterns of trematode parasitism in the introduced Japanese mud snail, Batillaria cumingi (= B. attramentaria), in nearly all of its introduced range along the Pacific Coast of North America. Only one parasite species, which was itself a non-native species, Cercaria batillariae was recovered. Its prevalence ranged from 3 to 86%. Trematode diversity and prevalence in B. cumingi and a native sympatric mud snail, Cerithidea californica, were also compared in Bolinas Lagoon, California. Prevalence of larval trematodes infecting snails as first intermediate hosts was not significantly different (14% in B. cumingi vs 15% in C. californica). However, while the non-native snail was parasitized only by one introduced trematode species, the native snail was parasitized by 10 native trematode species. Furthermore, only the native, C. californica, was infected as a second intermediate host, by Acanthoparyphium spinulosum(78% prevalence). Given the high host specificity of trematodes for first intermediate hosts, in marshes where B. cumingi is competitively excluding C. californica, 10 or more native trematodes will also become locally extinct.     

Echinostoma lindoense: larval antigens from the snail intermediate host, Biomphalaria glabrata

Passive hemagglutination using chromic chloride proved to be a rapid and useful method for a study of minute quantities of antigen extracted from larval Echinostoma lindoense (Sandground and Bonne), a trematode that develops in the snail intermediate host, Biomphalaria glabrata (Say). Parasite rediae were initially fragmented by three different procedures. Their soluble proteins were separated into two bands by electrophoresis on cellulose acetate, and into three fractions by molecular sieve chromatography. Rabbit antiserum was prepared from six weekly intramuscular injections of soluble redial protein in complete Freund's adjuvant, followed after 1 month by a single inoculation of alum-precipitated antigen. Antiserum was absorbed free of anti-snail antibodies and the immune complexes were removed by ion-exchange chromatography over DEAE-cellulose, producing an immunochemically pure IgG. Study of the rabbit anti-trematode antibody by precipitation, complement fixation, hemagglutination (HA), and inhibition of HA revealed a specific and high titered anti-larval antibody. These methods offer an approach to the problem of measuring the snail host's protective response against trematode reinfection; they also can be used to study the antigenic maturation of successive larval stages in the intermediate host.     

Spatial covariation between infection levels and intermediate host densities in two trematode species

Both theoretical arguments and empirical evidence suggest that parasite transmission depends on host density. In helminths with complex life cycles, however, it is not clear which host, if any, is the most important. Here, the relationships between the abundance of metacercariae in second intermediate hosts, and the local density of both the first and second intermediate hosts of two trematode species, are investigated. Samples of the snail Potamopyrgus antipodarum, the amphipod Paracalliope fluviatilis and the isopod Austridotea annectens were collected from ten stations in a New Zealand lake. In the trematode Coitocaecum parvum, neither the density of the snail first intermediate host nor that of the amphipod second intermediate host correlated with infection levels in amphipods. In contrast, in the trematode Microphallus, infection levels in isopod second intermediate hosts were positively associated with isopod density and negatively associated with the density of snail first intermediate hosts. These relationships are explained by a negative correlation between snail and isopod densities, mediated in part by their different use of macrophyte beds in the lake. Overall, the results suggest that, at least for Microphallus, local infection levels depend on local intermediate host densities.     

Host diversity and latitude drive trematode diversity patterns in the European freshwater fauna

Aim We investigated the relationship between host and parasite diversity as well as latitudinal gradients in parasite diversity on a continental scale in European freshwater trematodes. Location European freshwaters. Methods We extracted distributional data for 564 freshwater trematodes across 25 biogeographical regions in Europe from the Limnofauna Europaea and used multiple regression analyses to test for correlations between the diversity of definitive (vertebrates) or first intermediate (gastropods) hosts and that of trematodes, and for latitudinal gradients in trematode diversity. In particular, we investigated patterns in beta diversity among latitudinal bands and between trematode species that parasitize host groups with low (autogenic) and high (allogenic) dispersal capacity. We also tested for a latitudinal gradient in the proportional representation of these two trematode groups within regional faunas. Results Latitude or first intermediate host richness had no effect on trematode richness, but definitive host richness was a strong predictor of trematode richness, among both allogenic and autogenic parasites. We found that beta diversity of trematode faunas within latitudinal bands decreased to the north, with similar values for allogenic and autogenic trematodes. Finally, we observed an increasing proportion of autogenic species toward the north of Europe. Main conclusions The richness of definitive hosts appears to be the driver of trematode diversity at a continental scale. The latitudinal gradient in beta diversity reflects patterns observed in free‐living species and probably results from recolonization in the aftermath of the ice ages. The similar beta‐diversity patterns of allogenic and autogenic trematodes and the increasing proportion of autogenic trematodes with increasing latitude are surprising. We suggest that the geographical scale of our analysis or confounding factors such as differences in habitat utilization and specialization may partly explain these patterns.     

Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts

An unappreciated facet of biodiversity is that rich communities and high abundance may foster parasitism. For parasites that sequentially use different host species throughout complex life cycles, parasite diversity and abundance in 'downstream' hosts should logically increase with the diversity and abundance of 'upstream' hosts (which carry the preceding stages of parasites). Surprisingly, this logical assumption has little empirical support, especially regarding metazoan parasites. Few studies have attempted direct tests of this idea and most have lacked the appropriate scale of investigation. In two different studies, we used time-lapse videography to quantify birds at fine spatial scales, and then related bird communities to larval trematode communities in snail populations sampled at the same small spatial scales. Species richness, species heterogeneity and abundance of final host birds were positively correlated with species richness, species heterogeneity and abundance of trematodes in host snails. Such community-level interactions have rarely been demonstrated and have implications for community theory, epidemiological theory and ecosystem management.     

Component community of larval trematodes in the mudsnail Hydrobia ventrosa: temporal variations in prevalence in relation to host life history

Temporal variations in the prevalence of larval trematodes in the short-lived prosobranch mudsnail Hydrobia ventrosa (Montagu) were investigated in relation to host life history and season for 4 successive years in temperate windflats of the southern Baltic Sea. The component community of trematode larvae in H. ventrosa comprises at least 10 species; families (and species) represented include Notocotylidae (1), Echinostomatidae (1 or 2), Heterophyidae (2), Monorchidae (1), Microphallidae (3 or 4), Psilostomatidae (1), and Hemiuridae (1). The notocotylid Paramonostomum alveatum was the most prevalent species, followed by the microphallids Maritrema subdolum and Microphallus sp. Trematode prevalence in H. ventrosa fluctuated seasonally. Prevalence usually peaked in summer between July and September-October and decreased in late winter-early spring. This seasonal change is chiefly explained by the life history patterns of the semelparous snail host. Hydrobia ventrosa has a maximum life span of about 2 yr and reproduces between June and November of its second calendar year. The first trematode infections appeared annually in May when the most abundant cohort of H. ventrosa, the second-calendar-year snails, mature. The prevalence continued to increase until August-September, throughout the reproductive period of the second-calendar-year snails, Prevalence decreased during winter, when most of the second-calendar-year snails died after reproduction. On the basis of longterm laboratory experiments, it has been shown that the late autumn-winter mortality was not the result of trematode infections. Seasonal patterns of prevalence were similar among the trematode species except for the monorchid Asymphylodora demeli, the only one using fish definitive hosts. Species-specific differences in the seasonal occurrence of prepatent infections and the predominance of certain larval stages in winter are interpreted as different strategies of the trematode species to survive the harsh winter conditions, or to survive the death of the first intermediate host in autumn-winter, or both.     

Rapid colonisation of Lymnaea stagnalis by larval trematodes in eutrophic ponds in central Europe

High recruitment rates of multiple species and hierarchical competition are the keys to a competitive exclusion model of community assembly in larval trematode communities in molluscs. Eutrophic environments provide conditions for accelerating trematode transmission and this would increase the strength of interspecific interactions. To test these predictions, we provide the first known assessment for a pulmonate snail host, and for highly productive aquatic environments, of the rates of colonisation and extinction at the level of individual snail host patches, of a large guild of trematode species. Using a uniquely large dataset from a relatively long-term mark-recapture study of Lymnaea stagnalis in six eutrophic fishponds in central Europe, we demonstrate extraordinarily rapid colonisation by trematodes of a snail host, thus meeting the assumptions of the competitive exclusion model. Overall annual colonisation rates ranged from 243% to 503% year⁻¹ so that the odds of trematode establishment in an individual snail in these ponds are two to five times per year. Extinction rates were substantially lower than colonisation rates and, therefore, would not result in turnover rates high enough to significantly affect prevalence patterns in the snail populations. At the species level, analyses of sample-based estimates of probabilities of colonisation revealed that shared species traits associated with transmission and competitive abilities determined the limits of colonisation abilities. Colonisation rates were exceedingly high for the species transmitted to the snails passively via eggs. There was a significant effect of species competitive abilities on colonisation rates due to subordinate species being substantially better colonisers than both strong and weak dominants, a pattern consistent with the predictions of the competition-colonisation trade-off hypothesis. Our results suggest that, with the extraordinarily high trematode colonisation potential in the area studied, the spatial and temporal patterns of intraspecific heterogeneity in recruitment may provide conditions for intensification of interspecific interactions so that complex community assembly rules may be involved.     

Effects of pesticides on exposure and susceptibility to parasites can be generalised to pesticide class and type in aquatic communities

Pesticide pollution can alter parasite transmission, but scientists are unaware if effects of pesticides on parasite exposure and host susceptibility (i.e. infection risk given exposure) can be generalised within a community context. Using replicated temperate pond communities, we evaluate effects of 12 pesticides, nested in four pesticide classes (chloroacetanilides, triazines, carbamates organophosphates) and two pesticide types (herbicides, insecticides) applied at standardised environmental concentrations on larval amphibian exposure and susceptibility to trematode parasites. Most of the variation in exposure and susceptibility occurred at the level of pesticide class and type, not individual compounds. The organophosphate class of insecticides increased snail abundance (first intermediate host) and thus trematode exposure by increasing mortality of snail predators (top–down mechanism). While a similar pattern in snail abundance and trematode exposure was observed with triazine herbicides, this effect was driven by increases in snail resources (periphytic algae, bottom–up mechanism). Additionally, herbicides indirectly increased host susceptibility and trematode infections by (1) increasing time spent in susceptible early developmental stages and (2) suppressing tadpole immunity. Understanding generalisable effects associated with contaminant class and type on transmission is critical in reducing complexities in predicting disease dynamics in at‐risk host populations.     

Component community dynamics of larval trematodes in the freshwater snail Semisulcospira nakasekoae in the Uji River, central Japan

The component community of larval trematodes in the freshwater snail Semisulcospira nakasekoae (Caenogastropoda: Sorbeoconcha: Pleuroceridae) was surveyed over 13 months from April 1996 to April 1997 inclusive. Temporal and spatial fluctuation of trematode prevalence, the frequency of multiple infections, and the duration of cercarial shedding were examined as factors that might affect trematode community structure. The spatial prevalence of some species varied significantly, but the dynamics were too small to allow an explanation of the overall pattern. The prevalence of sanguinicolids fluctuated temporally, despite a stable size distribution in the host populations (> 6.0 mm shell width), suggesting the life-cycle phenology of this species. Some pairs of species had statistically positive associations, but no pairs had negative associations. This shows the importance of positive association possibly as a result of suppression of the host defensive response on trematode community structures in molluscan hosts. The length of the patent period, which is part of the persistent period, varied among trematode species, suggesting it to be one of the factors determining prevalence in the host population.     

Infrapopulation sizes of co-occurring trematodes in the snail Ilyanassa obsoleta

This study addresses the infrapopulation sizes of 2 larval trematode species Himasthla quissetensis and Zoogonus rubellus as they co-occur within their estuarine snail host Ilyanassa obsoleta. Rediae of H. quissetensis and sporocysts of Z rubellus were counted in snails singly infected with each parasite and in snails infected with both. Comparisons of the counts indicate that infrapopulations of H. quissetensis were unaffected by co-occurrence with Z rubellus. However, Z. rubellus infrapopulations were reduced when co-occurring with H. quissetensis. It is proposed that this situation does not result from an interspecific interaction between parasite species. Although this double infection is relatively frequent in certain snail populations, it is contended that these trematode species do not co-occur often enough to evolve responses to one another. However, the host environment must be encountered in each life cycle, and both trematode species must be adapted to use it. On this basis, whatever happens when these 2 species occupy the same host is based on adaptations of the parasites to the host. It is proposed that these parasites are adapted to self-limit their infrapopulations in the snail host. They can, thus, preserve and use the host for many years and thereby enhance total cercarial transmission (fitness). Infrapopulation sizes would be determined by host resource levels, which, among other factors, would be influenced by the presence of multiple parasite species. In single infections, by far the most common situation, host resource levels would be set by the nutritional status or age (size) of the host (or both). The reduced infrapopulation sizes of Z rubellus on co-occurrence suggest that this trematode is more sensitive to host resource levels than is H. quissetensis.     

Do trematode parasites disrupt defence-cell signalling in their snail hosts?

More than a decade ago, it was postulated that components derived from trematode parasites block receptors on the defence cells of their snail intermediate hosts, thus preventing host-cell activation and parasite elimination. This phenomenon has still not been investigated extensively. However, recent work concerning the molecular regulation of the molluscan defence response provides a new framework for studies that focus on an extension of this original concept - subversion of host cell signalling by trematode parasites. The hypothesis is that, to facilitate survival and replication in their intermediate hosts, trematode parasites down regulate host defence responses by interfering with key signal-transduction pathways in snail defence cells.     

Bacterial community dynamics following antibiotic exposure in a trematode parasite

Parasites harbour rich microbial communities that may play a role in host-parasite interactions, from influencing the parasite’s infectivity to modulating its virulence. Experimental manipulation of a parasite’s microbes would be essential, however, in order to establish their causal role. Here, we tested whether indirect exposure of a trematode parasite within its snail intermediate host to a variety of antibiotics could alter its bacterial community. Based on sequencing the prokaryotic 16S ssrRNA gene, we characterised and compared the bacterial community of the trematode Philophthalmus attenuatus before, shortly after, and weeks after exposure to different antibiotics (penicillin, colistin, gentamicin) with distinct activity spectra. Our findings revealed that indirectly treating the parasites by exposing their snail host to antibiotics resulted in changes to their bacterial communities, measured as their diversity, taxonomic composition, and/or the relative abundance of certain taxa. However, alterations to the parasite’s bacterial community were not always as predicted from the activity spectrum of the antibiotic used. Furthermore, the bacterial communities of the parasites followed significantly divergent trajectories in the days post-exposure to antibiotics, but later converged toward a new state, i.e. a new bacterial community structure different from that pre-exposure. Our results confirm that a trematode’s microbial community can be experimentally altered by antibiotic exposure while within its snail host, with the dynamic nature of the bacterial assemblage driving it to a new state over time after the perturbation. This research opens new possibilities for future experimental investigations of the functional roles of microbes in host-parasite interactions.     

Whether larval amphibians school does not affect the parasite aggregation rule: testing the effects of host spatial heterogeneity in field and experimental studies

Almost all macroparasites show over‐dispersed infections within natural host populations such that most parasites are distributed among a few heavily‐infected individuals. Despite the importance of parasite aggregation for understanding system stability, the potential for population regulation, and super‐spreading events, many questions persist about its underlying drivers. Theoretically, aggregation results from heterogeneity in host exposure, resistance, and tolerance. However, few studies have examined how host spatial arrangement – which likely affects both parasite encounter and density‐dependent interactions – influences infection and dispersion, representing a critical gap in our current knowledge regarding the possible drivers of parasite aggregation. Using field data from over 165 ponds and 8000 hosts, we evaluated how the spatial clustering of amphibian larvae within ponds 1) varied among different amphibian species, and 2), affected the distribution of parasites within the host population using Taylor's power law. A complementary mesocosm experiment used field‐guided manipulations of the spatial arrangement of larval amphibians to create a gradient in host clustering while controlling host density, thereby testing for spatial effects on both infection success and aggregation by three different trematode species. Our field data indicated that larval amphibians exhibited significant spatial clustering that was well captured by Taylor's power law (R² 0.92 to 0.97 for different host species), but the residual variation only weakly correlated with observed patterns of trematode parasite over‐dispersion. Correspondingly, experimental manipulation of host clustering had no effects on parasite infection success or the degree of parasite aggregation among cages or mesocosms. Given the importance of parasite over‐dispersion for host populations and disease dynamics, we advocate for further investigations of host and parasite spatial aggregation, particularly studies that incorporate and/or control for heterogeneity in exposure and susceptibility.