Genotyping natural infections of Schistosoma mansoni in Biomphalaria alexandrina from Damietta, Egypt, with comparisons to natural snail infections from Kenya

The distribution of Schistosoma genotypes among individuals in snail populations provides insights regarding the dynamics of transmission and compatibility between schistosome and snail hosts. A survey of Biomphalaria alexandrina from Damietta (Nile Delta, Egypt), an area subjected to persistent schistosomiasis control efforts, provided only 17 snails infected with Schistosoma mansoni (6.1% overall prevalence), each shown by microsatellite analysis to have a single genotype infection. By contrast, recent studies of uncontrolled S. mansoni transmission foci in Kenya revealed that 4.3% Biomphalaria pfeifferi and 20-25% Biomphalaria sudanica snails had multiple genotype infections. Compared with the 3 Kenyan populations, the Egyptian population of S. mansoni also showed a lesser degree of genetic variability and was genetically differentiated from them. We suggest that tracking of genotype diversity in infected snails could be further developed to serve as an additional and valuable independent indicator of efficacy of schistosomiasis control in Egypt and elsewhere.     

Distribution of schistosome infections in molluscan hosts at different levels of parasite prevalence

Biomphalaria glabrata snails infected with Schistosoma mansoni were collected during consecutive seasons from a site in Brazil known to have a very high percentage of infected snails. Schistosoma mansoni cercariae from single snails were used to infect individual mice, and the recovered adult worms were genetically assessed using a mtVNTR marker. The number of unique parasite genotypes found per snail was compared to expected abundance values, based on the infection prevalence at the site, to determine the distribution of S. mansoni infections within the snail population. The observed distributions and those from previous studies were used to examine the relationship between schistosome prevalence and aggregation across a wide range of prevalence values. Our analysis showed that prevalence was inversely related to the degree of parasite overdispersion, and at high prevalence, S. mansoni infections were randomly distributed among snails.     

Genetic diversity and recruitment pattern of Schistosoma mansoni in a Biomphalaria glabrata snail population: a field study using random-amplified polymorphic DNA markers.

Random-amplified polymorphic DNA markers have been used to assess the amount and the distribution of the genetic diversity of Schistosoma mansoni within a natural population of Biomphalaria glabrata at a transmission site of the murine schistosomiasis focus of Guadeloupe. Despite high infection rate and heavy schistosome load within the definitive hosts (Ratus rattus), prevalences within intermediate snails ranged from 0.2 to 4.8%. Whatever the transmission season may be (rainy vs. dry), most of the infected snails were spatially aggregated and 88.4% of them harbored a single parasite genotype indicative of a monomiracidial infection; 4.7% had dual sex infections and a parasite intensity not exceeding 3 miracidia per snail. A substantial resistance level toward the parasite and recruitment regulatory process within snails may explain in part the observed low parasite prevalences and intensities. Considering such a distribution pattern of larval S. mansoni genetic diversity among B. glabrata, mobility of the definitive hosts, or rapid turnover of infected snails, or both, are required to maintain genetic heterogeneity within adult schistosome populations.     

Effects of snail size and age on the prevalence and intensity of avian schistosome infection: relating laboratory to field studies

Both the prevalence and intensity of patent infection by avian schistosomes (Trichobilharzia ocellata) increase with increasing size of lymnaeid snails (Stagnicola elrodi) collected in Flathead Lake, Montana. Because the size and age of a snail are positively correlated, snails of different sizes may have experienced differential duration of exposure to and development of infection. Another possibility is that infection itself induces snail gigantism. Each of these possibilities could lead to increased prevalence and intensity of infection among the oldest-largest snails. To decouple size variation from many correlated effects of age and to test for parasite-induced gigantism, laboratory experiments standardized snail size-age-at-infection, exposure history, inoculating dose, and duration of infection. The positive relationship between size and prevalence was eliminated in the laboratory, but the relationship between size and infection intensity remained. Laboratory results thus suggest that infection intensity is related to snail size per se, whereas prevalence in the field is related to snail size only through the correlation between size and age. In addition, under these experimental conditions, infected snails were no larger than uninfected snails, so the patterns observed in the field might not be attributable to gigantism.     

Altered behavior of the snail Biomphalaria glabrata as a result of infection with Schistosoma mansoni

In this comparative behavioral study, the effect of infection with Schistosoma mansoni on its snail intermediate host Biomphalaria glabrata was investigated. Three groups of snails were compared for their activity: (1) uninfected, (2) infected with male parasites, and (3) infected with female parasites. In solitary movement trials, uninfected snails traveled greater distances at faster rates, explored more surface area, and had shorter rest periods than snails infected with either male or female schistosomes. In Y-maze experiments designed to determine attraction, the uninfected snails more often and more quickly moved toward other snails than the infected individuals. Snails from all 3 groups were more attracted to infected individuals than to uninfected ones. There was no difference in attraction toward snails infected with male or female parasites. These experiments provide evidence that behavioral alterations as a result of infection may lead to aggregation of infected snails in the field. We propose that such an effect may result in enhanced parasite transmission.     

Dose-dependent schistosome-induced mortality and morbidity risk elevates host reproductive effort

Parasitism changes the host environment and may influence resource allocation between reproductive effort and somatic maintenance. We characterized the impact of dose-dependent schistosome exposure and/or infection establishment on intermediate host survival and reproduction. Four matched groups of Biomphalaria glabrata snails were individually exposed to increasing doses of Schistosoma mansoni parasites, with a fifth control group remaining unexposed. Increased mortality was observed amongst both snails infected and also those snails exposed to the parasite but within which infection did not establish, although only exposed but uninfected snails showed a dose-dependent increase in mortality. Snails also facultatively altered their reproductive output in response to parasite exposure: egg mass production decreased with increasing parasite dose in patently infected snails, whilst, in contrast, exposed but uninfected snails demonstrated a positive association between egg mass production and parasite dose in the post-patent period. These results uniquely suggest an exposure-dose-dependent post-patent fecundity compensation occurring in relation to the risk of future parasite-associated mortality.     

Bulinus tropicus from Central Kenya acting as a host for Schistosoma bovis

One hundred and twelve snails were collected from two habitats on the Mau Escarpment, Kenya and were provisionally identified as Bulinus tropicus from the characteristics of their shell and soft parts, chromosome number (n = 18), electrophoresis of egg protein on cellulose acetate strip and isoelectric focusing of AcP, GPI, HBDH, MDH and PGM digestive gland enzymes. Of the 55 specimens examined alive in London, 10 were infected with amphistome and schistosome larvae, 9 with amphistome larvae and the remainder were uninfected. The GPI and MDH separations of known infected snails showed two distinct areas of activity: host and parasite. Individual hamsters were exposed to schistosome cercariae emanating from each snail with a double infection (apart from one which died prematurely) and examination of the resulting adult worms showed that all were monomorphic for AcP with a band of enzyme activity at pH 6.45, characteristic of Schistosoma bovis. Examination of eggs found in two infections proved to be S. bovis in shape and size. Exposure of laboratory-bred snails of B. tropicus from the Mau Escarpment and other populations of B. tropicus proved negative. Thus, it is suggested that the presence of the amphistome infection may have a suppressive effect on the immune system of the snail, thereby allowing S. bovis to develop.     

Larval development of Fasciola hepatica in experimental infections: variations with populations of Lymnaea truncatula

A retrospective study was undertaken on 70 French populations of Lymnaea truncatula experimentally infected with Fasciola hepatica to determine whether or not susceptibility of snails to infection influenced redial and cercarial production. Results were compared with those obtained from two control populations, known for prevalences higher than 60% when experimentally infected with F. hepatica. In the 70 other populations examined, the prevalences ranged from 2 to 75%. In 55 of these populations, where the prevalence was more than 20%, a high proportion (50.1-56.8%) of snails died after cercarial shedding, whereas in the other groups (non-shedding snails with the most differentiated larvae being free cercariae, rediae containing cercariae, immature rediae, or sporocysts, respectively), snail death was significantly less. In 11 populations, where the prevalence values were 5-19%, only 14% of snails died after cercarial shedding, whereas snails with free cercariae, rediae with cercariae, or immature rediae showed significant increases in snail mortality. In the remaining four snail populations, with prevalences of less than 5%, the most differentiated larval forms were only immature rediae and/or sporocysts. Overall, the number of rediae containing cercariae significantly decreased with decreasing prevalence values. The low prevalence of experimental infection in several populations of snails might be explained by the occurrence of natural infections with miracidia originating from a mammalian host other than cattle, and/or by genetic variability in the susceptibility of snails to infection.     

The role of snail aestivation in transmission of schistosomiasis in changing climatic conditions

Schistosomiasis vector snails are subjected to extreme seasonal changes, particularly in ephemeral rivers and lentic waterbodies. In the tropics, aestivation is one of the adaptive strategies for survival and is used by snails in times of extremely high temperatures and desiccation. Aestivation therefore plays an important role in maintaining the transmission of schistosomiasis. This review assesses the possible impacts of climate change on the temporal and spatial distribution of schistosomiasis-transmitting snails with special emphasis on aestivation, and discusses the effect of schistosome infection on aestivation ability. The impacts of parasite development on snails, as well as physiological changes, are discussed with reference to schistosomiasis transmission. This review shows that schistosome-infected snails have lower survival rates during aestivation, and that those that survive manage to get rid of the infection. In general, snail aestivation ability is poor and survival chances diminish with time. Longer dry periods result in fewer, as well as uninfected, snails. However, the ability of the surviving snails to repopulate the habitats is high.     

Guild structure of larval trematodes in the snail Helisoma anceps: patterns and processes at the individual host level

Factors that influenced the infracommunity structure of trematodes parasitizing the pulmonate snail Helisoma anceps were studied over a 15-mo period; the guild included 8 species of parasites. Infracommunities were depauperate, with double patent infections observed in only 7 of 1,485 infected snails; a total of 4,899 was examined. Halipegus occidualis-Haematoloechus longiplexus was the most common dual infection. Both species share the same definitive host and, in both cases, eggs are the infective stage for the snail. Switches and losses of infections in individual snails were observed, suggesting the occurrence of dynamic interactions within the guild. A dominance hierarchy was constructed based on field observations and experimental infections. Echinostomatids were dominant; species without rediae in their life cycles were subordinates. Halipegus occidualis (which has rediae) was intermediate in dominance. Spatial and temporal heterogeneity in the distribution and abundance of trematode infective stages indicate that not all the snails have the same probability of becoming infected. Habitat structure, behavior of the definitive host, the nature of the infective stages, and snail population dynamics (mortality, recruitment, and size structure) generated spatial and temporal heterogeneity in this system. As a consequence, predictions of the probabilities of interspecific interactions based on an analysis of observed and expected frequencies of multiple infections could be inappropriate unless the potential sources of heterogeneity are considered.     

Effect of the digenean parasite Proterometra macrostoma on host morphology in the freshwater snail Elimia livescens

Parasitism can affect size in gastropods by altering the host's growth rate, but other morphological effects of parasitism have rarely been examined. In this study, the relationship between variation in host morphology and parasitism was examined in a population of the freshwater snail Elimia livescens. Differences were found in the morphology of snails infected with the digenean Proterometra macrostoma and uninfected snails. In order to differentiate between 2 hypotheses to explain these differences in morphology, snails were experimentally infected in the laboratory and several morphological traits were measured after 180 days. One hypothesis suggests that parasite-induced changes in shell development explain differences in morphology between infected and uninfected snails. The other hypothesis suggests that selective mortality of infected hosts explains the difference. In the experiment, differences were found between infected snails and uninfected snails in overall size but not in any measurements of shape. The short duration of the experiment relative to the duration of most infections may account for why field-infected snails differed in shape but experimentally infected snails did not. Parasite-induced changes in growth rate are the most likely explanation for the larger size of infected snails relative to uninfected snails.     

Lymnaea fuscus (Pfeiffer, 1821) as a potential intermediate host of Fascioloides magna in Europe

Experimental infections of two different populations of Lymnaea fuscus in France and Sweden, with a Czech isolate of Fascioloides magna were carried out to determine if this lymnaeid species enables parasite larval development. Species identification of both snail populations was performed using the morphology of the copulatory organ, and also confirmed by sequencing of the internal transcribed spacer 2 (ITS2) region of the snail genomic rDNA. Only juvenile snails measuring less than 3 mm (1–3 weeks of age) were successfully infected (the viable cercariae were recorded) and infection prevalence decreased with age, as documented by increased shell height. In both French and Swedish L. fuscus populations, prevalence ranged between 1.1% and 58.8%. The mean number of metacercariae obtained from cercariae-shedding snails was 13.7 (±11.4), while the total cercarial production noted in snails dissected at day 85 post-exposure was 147.5 (±56.6). Compared to uninfected control snails, we observed reduced growth of infected snails. Despite age-related resistance of snail to the parasite, and limited cercarial production in these experimentally infected snails, F. magna was still able to complete larval development in L. fuscus.     

Indirect effects of a parasite on a benthic community: an experiment with trematodes, snails and periphyton

1. Few studies have directly addressed the role played by parasites in the structure and function of ecosystems. Parasites influence the behaviour, reproduction and overall fitness of their hosts, but have been usually overlooked in community and ecosystem‐level studies. We investigated the effects of trematode parasites on snail–periphyton interactions. 2. Physa  acuta (Gastropoda: Pulmonata) snails infected with the trematode Posthodiplostomum minimum (often >30% of within‐shell biomass) grazed more rapidly than uninfected snails. Trematode effects on snail grazing indirectly affected the standing stock and community structure of periphyton. Populations of snails with 50% infected individuals reduced algal biomass by 20% more than populations with lesser (10% or 0%) infection rates. 3. The alga Cladophora glomerata dominated periphyton communities grazed by snail populations with 50% infection rates, whereas diatoms and blue–green algal taxa dominated when grazed by snail populations with lower infection rates. 4. Thus, trematodes indirectly affected periphyton communities by altering host snail behaviour, a trait‐mediated indirect effect. These results indicate that trematodes can indirectly influence benthic community structure beyond simple population fitness, with possible related effects on ecosystem function.     

Cost of resistance: relationship between reduced fertility and increased resistance in a snail—schistosome host—parasite system

Natural host populations often exhibit genetic variability in resistance to parasitism. One possible mechanism for maintaining such diversity is a trade-off between fitness costs associated with resistance and fitness costs associated with parasitism. However, little is known about the nature or magnitude of these costs in animal populations. Using artificial selection experiments in a Biomphalaria glabrata–Schistosoma mansoni host–parasite system, we demonstrated that resistance and susceptibility to infection are heritable. We then investigated whether resistance had any associated costs in terms of snail reproductive success. Susceptible-selected snail lines showed significantly higher fertility (number of offspring produced) than resistant-selected or unselected control snail lines, irrespective of current infection status. There were no consistent differences between snail lines in fecundity, proportion of abnormal egg masses produced, or mean number of eggs per egg mass. Mortality rate was higher among infected than uninfected snails. These results are consistent with snails incurring costs of resistance to schistosome infection in the absence of the parasite.     

Does parasitic infection compromise host survival under extreme environmental conditions? The case for Cerithidea californica (Gastropoda: Prosobranchia)

Summary This laboratory study examined the influence of parasitic infection by larval trematodes on the survival of extreme environmental conditions by the salt marsh snail, Cerithidea californica. Experimental treatments simulated the durations, combinations, and levels of potentially lethal environmental extremes to which the snail is exposed in its natural habitat, as determined from long-term field measurements. No significant difference was found in the rates of mortality suffered by infected and uninfected snails when exposed to simulated natural extremes of water temperature, water salinity, or exposure in air. Exposure to low levels of dissolved oxygen was the only treatment that caused differential mortality: infected snails died at higher rates than uninfected. This differential mortality was accentuated by high water temperature, and varied with the species of infecting parasite. The potential impact of this interaction between parasitism and anoxia on snail survival and population dynamics is discussed.     

Host life history and the effect of parasitic castration on growth: A field study of Cerithidea californica Haldeman (Gastropoda : Prosobranchia) and its trematode parasites

The prevalence of parasitic infection by larval digenetic trematodes in natural populations of the mud snail, Cerithidea californica Haldeman, was found to increase with snail length; all snails ≥ 33 mm were infected. Distributions of infections by the seven most common larval trematodes were heterogeneous due to two species being more common than expected in the smaller size classes of snails, two being more common than expected in the larger size-classes of snails and three species being most prevalent in snails of intermediate length. The relative abundances of trematodes in different size-classes reflected these distributional patterns.A mark-recapture field study of snail growth rates failed to demonstrate that parasitic infection causes gigantism in Cerithidea. Parasitism tended to stunt the growth of juvenile snails and to a lesser degree, that of adult snails. The effects of trematodes on snail growth was shown to be species specific. This finding contrasts with those of earlier studies in which gigantic growth was observed in infected snails. This discrepancy is attributed to differences in the life histories of the host snails. It is predicted that gigantism will occur commonly in short-lived or semelparous species of snails but rarely, if ever, in long-lived iteroparous species which are predominately marine.     

Life history cost of trematode infection in Helisoma anceps using mark-recapture in Charlie's Pond

Parasitism has the potential to affect key life history traits of an infected host. Perhaps the most studied interactions are in snail-trematode systems, where infection can result in altered growth rates, survival, and/or fecundity of the individual. Positive correlations between host size and parasite prevalence are often attributed to changes in growth rates or mortality, which have been observed in the laboratory. Extending lab-based conclusions to the natural setting is problematic, especially when environmental conditions differ between the laboratory and the field. The present study uses reproduction experiments and mark-recapture methods to directly measure key life history traits of the pulmonate snail Helisoma anceps in Charlie's Pond. Based on previous laboratory and field experiments on H. anceps, we predict a significant reduction in fecundity, but not growth rate or survival, of infected snails. Individual capture histories were analyzed with multistate models to obtain estimates of survival and infection probabilities throughout the year. Recaptured individuals were used to calculate specific growth rates. Trematode infection resulted in complete castration of the host. However, neither survival nor growth rates were found to differ between infected and uninfected individuals. The probability of infection exhibited seasonal variation, but it did not vary with size of the snail. These results suggest that the correlation between host size and trematode prevalence is not due to differential mortality or changes in growth rates. Instead, the infection accumulates in large snails via the growth of smaller, infected individuals.     

Longitudinal Study on the Natural Infection of Biomphalaria straminea and B. glabrata by Schistosoma mansoni in an Endemic Area of Schistosomiasis in Pernambuco,Brazil

The abundance of snail hosts and the rates of infection with Schistosoma mansoni were monitored monthly for four years in two representative localities subjected to repeated chemotherapy of infected persons. Snail abundance varied from 1.0 to 4.4 collected per person/minute/station for Biomphalaria straminea and from 0.1 to 7.0 for B. glabrata. Infection rates of snails in nature varied from 0% to 15% for the former and from 0% to 70% for the latter species. Human infection increased from 35.5% to 61.9% in the locality occupied by B. straminea, and decreased from 40.3% to 20.8% in that occupied by B. glabrata. No relationship could be detected between human infection and the snail variables. Despite seasonal variations, natural infection persisted throughout the monitoring period in both snail species. It reached remarkably high levels in B. straminea when compared to those obtained by other authors probably because of differences in methodology. It is recommended that longitudinal studies should be carried out focally and periodically to avoid underestimating the prevalence of schistosome infection in snails.     

Parasite-induced changes in nitrogen isotope signatures of host tissues

To estimate isotopic changes caused by trematode parasites within a host, we investigated changes in the carbon and nitrogen isotope ratios of the freshwater snail Lymnaea stagnalis infected by trematode larvae. We measured carbon and nitrogen stable isotopes within the foot, gonad, and hepatopancreas of both infected and uninfected snails. There was no significant difference in the delta13C and delta15N values of foot and gonad between infected and uninfected snails; thus, trematode parasite infections may not cause changes in snail diets. However, in the hepatopancreas, delta15N values were significantly higher in infected than in uninfected snails. The 15N enrichment in the hepatopancreas of infected snails is caused by the higher 15N ratio in parasite tissues. Using an isotope-mixing model, we roughly estimated that the parasites in the hepatopancreas represented from 0.8 to 3.4% of the total snail biomass, including the shell.     

Tissue responses exhibited by Biomphalaria alexandrina snails from different Egyptian localities following Schistosoma mansoni exposure

Snails’ susceptibilities to infection with Schistosoma mansoni were determined through observation of infection rates, total cercarial production and tissue responses of the first generation (F1) of Biomphalaria alexandrina snails, originally collected from different Egyptian governorates (Giza, Fayoum, Kafr El-Sheikh, Ismailia and Damietta) and responses were compared between groups. The emergence of cercariae for a 3-month period and the calculation of survival and infection rates, in control (Schistosome Biological Supply Center; SBSC) and infected snails were evaluated. SBSC and Giza snails showed greater susceptibilities to infection and lower mortality rates. In addition, at 6 and 72 h post-exposure to miracidia all the snail groups showed no difference in the anatomical locations of sporocysts. The larvae were found in the head-foot, the mantle collar and the tentacles of the snails. Sporocysts showed normal development with low tissue reactions in SBSC and Giza snail groups infected with S. mansoni miracidia (SBSC). However, in Fayoum, Kafr El-Sheikh, Ismailia and Damietta snail groups, variable tissue responses were observed in which numerous hemocytes made direct contact with S. mansoni larvae forming capsules. The results suggested that, different responses of B. alexandrina snail’s hemocytes towards S. mansoni are related to the degree of susceptibility of these snails. So this is important in planning the strategy of schistosomiasis control.