Pathology and host responses induced by Schistosomatium douthitti in the freshwater snail Lymnaea catascopium.

Most Schitosomatium douthitti miracidia penetrated the esophageal wall of Lymnaea catascopium without provoking amoebocyte encapsulation responses or extensive pathological changes. Amoebocytes frequently attached to developing mother and daughter sporocysts, but did not encapsulate or destroy them. Pressure resulting from extensive growth of mother sporocysts ruptured the transverse membrane of some snails. After releasing daughter sporocysts, mother sporocysts in some snails were destroyed by amoebocytes. Many migrating cercariae became trapped in the tissues of L. catascopium, particularly in the posterior portion of the foot, and were encapsulated and destroyed. Large increases in numbers of amoebocytes in the anterior portion of the lung roof of infected snails were noted, even before cercarial production had been initiated. Atrophy of the digestive gland occurred in infected snails.     

Resistance to desiccation of Biomphalaria glabrata adults infested by various miracidia of Schistosoma mansoni

1200 adult Biomphalaria glabrata were submitted during 6 weeks to anhydrobiosis condition. Some snails were healthy, some were previously infected 3 days or 12 days ago with 8 +/- 2 miracidia of Schistosoma mansoni, others were shedding cercariae. The snails were put on soil or buried into hermetically closed, or ventilated, plastic boxes. There was no survival of snails kept in sealed boxes, or among positive snails, but 44% of control healthy snails and 40.6% of infected (for 3 or 12 days) snails in ventilated boxes were living at the term of the desiccation stage. Survival was better for "on soil" snails than for "buried" snails, but no difference was shown between 3-days and 12-days infection. The surviving desiccated B. glabrata had a lesser death rate and a lesser cercarial production than infected snails kept in water. An inferior production of male cercariae comparatively to female and to "mixed" cercariae was demonstrated by statistical analysis of the cercarial sheddings. In all positive snails, periodic variations of cercarial production was shown, whatever the sex of those cercariae. In addition many pauses of the sheddings were established by the authors.     

Schistosoma mansoni: Long-term maintenance of clones by microsurgical transplantation of sporocysts

Schistosoma mansoni sporocysts originally derived from monomiracidially infected Biomphalaria glabrata snails were serially transplanted into the cephalopedal sinus of anesthetized snails by the microsurgical implantation of fragments of parasitized hepato-pancreas and ovotestis. Three to six passages each of five male and five female clones were maintained for as long as 2.0 years. Of the recipient snails which survived surgery, 87% released cercariae, usually beginning 5–7 weeks after surgery. The percentage of snails which released cercariae increased with successive passages. The mean survival time of surgically infected snails after cercarial emergence began was 9.2 ± 0.5 weeks, nearly the same as that of miracidially infected snails. Longevities of snails infected with male or female clones were similar. Recipient snail size and age did not influence cloning success. Beginning 5 weeks from the onset of cercarial emergence large numbers of cercariae (a mean of 3900/snail from male clones and 1300/snail from females) were obtained during each shedding period. These results clearly demonstrate that the microsurgical transplantation of sporocysts is a practical means of maintaining and expanding populations of genetically homogeneous schistosomes (clones).     

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.     

The Early Worm Catches the Bird? Productivity and Patterns of Trichobilharzia szidati Cercarial Emission from Lymnaea stagnalis

Digenean trematodes are common and abundant in aquatic habitats and their free-living larvae, the cercariae, have recently been recognized as important components of ecosystems in terms of comprising a significant proportion of biomass and in having a potentially strong influence on food web dynamics. One strategy to enhance their transmission success is to produce high numbers of cercariae which are available during the activity peak of the next host. In laboratory experiments with 13 Lymnaea stagnalis snails infected with Trichobilharzia szidati the average daily emergence rate per snail was determined as 2,621 cercariae, with a maximum of 29,560. During a snail’s lifetime this summed up to a mass equivalent of or even exceeding the snail’s own body mass. Extrapolated for the eutrophic pond where the snails were collected, annual T. szidati biomass may reach 4.65 tons, a value equivalent to a large Asian elephant. Emission peaks were observed after the onset of illumination, indicating emission synchronizing with the high morning activities of the definitive hosts, ducks. However, high cercarial emission is possible throughout the day under favorable lightning conditions. Therefore, although bird schistosomes, such as T. szidati constitute only a fraction of the diverse trematode communities in the studied aquatic ecosystem, their cercariae can still pose a considerable risk for humans of getting cercarial dermatitis (swimmer''s itch) due to the high number of cercariae emitted from infected snails.     

Schistosoma mansoni: influence of Biomphalaria glabrata size on susceptibility to infection and resultant cercarial production

Biomphalaria glabrata snails of the same age, but different sizes, were used to determine size-related susceptibility to Schistosoma mansoni miracidial infection and the influence of snail size on total cercarial production. Snails with shell diameters from less than 5 to greater than 17 mm were individually exposed to one or several miracidia, depending on the experiment. In snails exposed to multiple numbers of miracidia, the percentage of snails which developed patent infections was lower in snails with larger shell sizes. This was also reflected by fewer primary sporocysts per infected snail found in tissues of the larger snails. Upon determining cercarial production in these groups over a 1-month period there were no statistical differences between any groups in the numbers of cercariae produced per snail. However, upon determining the number of successful primary sporocysts found in cohort snails of each size group, cercarial production increased as a function of the number of successful primary sporocysts. This was verified by examining cercarial production in various size snails with known monomiracidial infections. Our data therefore confirm and extend earlier work using snails infected with unknown numbers of miracidia and clearly show that total S. mansoni cercarial development and decreased susceptibility of snails is a direct reflection of snail size and not necessarily age of the snail.     

Effects of diet on the development of Schistosoma mansoni in Biomphalaria glabrata and on the neutral lipid content of the digestive gland-gonad complex of the snail

In a previous study, when the snail Biomphalaria glabrata was infected with Schistosoma mansoni and maintained on a diet of hen's egg yolk, it produced fully developed cercariae in about one-half the time taken by snails fed Romaine lettuce. Increased lipids were also noted in the snails fed the yolk diet. The purpose of the present study was to further investigate nutritional effects of a high-lipid diet on larval schistosome development and to reexamine the time to cercarial patency in infected snails maintained on either the yolk or lettuce diet and to use high-performance thin-layer chromatography (HPTLC) to analyze the neutral lipids in the digestive gland-gonad complex (DGG) of snails maintained on both diets. Infected snails maintained at 26 C and fed either diet produced fully developed cercariae by 4 wk postinfection (PI). Likewise, infected snails maintained at 23 C and fed either diet produced fully developed cercariae by 6 wk PI. The contention that the yolk diet enhanced the time to cercarial patency was not confirmed. The HPTLC analysis of neutral lipids showed that the DGG of infected snails fed the yolk diet contained significantly greater amounts of free sterols and cholesteryl esters but not triacylglycerols than that of the infected snails fed the lettuce diet.     

Paramphistomum daubneyi: characteristics of infection in three lymnaeid species

Experimental infections of two South American lymnaeids (Lymnaea neotropica and L. viatrix var. ventricosa) with Paramphistomum daubneyi were carried out to determine if these snail species could sustain larval development of this digenean and, if so, to specify their potential for cercarial production. A French population of Galba truncatula infected and raised according to the same protocol served as controls. In both experiments, prevalence of P. daubneyi infections in snails did not significantly differ from each other. In snail groups evaluated for cercarial shedding (first experiment), a significantly lower number of shed cercariae was noted for L. neotropica, while those from G. truncatula and L. v. ventricosa did not differ significantly from each other. Dissection of infected snails at day 65 post-exposure at 20 °C (second experiment) found significantly lower burdens of P. daubneyi rediae and cercariae in the bodies of L. neotropica than in those of G. truncatula and L. v. ventricosa. Compared to total cercarial production observed in dissected snails, the percentage of cercariae which exited from snails was 75.6% for G. truncatula, 21.6% for L. neotropica, and 91.4% for L. v. ventricosa. This last species seems to be a good candidate for metacercarial production of P. daubneyi.     

The presence of predators modifies the larval development of Fasciola hepatica in surviving Lymnaea truncatula

Experimental infections of Lymnaea truncatula with Fasciola hepatica were performed to study the consequences of the presence of predators (sciomyzid larvae or zonitid snails) on the characteristics of larval F. hepatica development in surviving snails. Controls consisted of infected snails that were not subjected to predators. Compared to controls, the survival rate at day 30 post-exposure, the duration of cercarial shedding, and the number of cercariae shed by surviving snails were significantly lower when predators were present in snail breeding boxes, whatever the type of predator used. In contrast, the prevalences of Fasciola infections in snails, and the length of time between exposure and the onset of cercarial shedding showed no significant variation. The progressive development of a stress reaction in surviving snails against predators during the first 30 days of experimental exposure to F. hepatica would influence snail survival during the cercarial shedding period and, consequently, the number of cercariae shed by the snails.     

Influence of low temperatures on the cercarial shedding of Paramphistomum daubneyi from the snail Lymnaea truncatula

Lymnaeids in nature are subjected to temperature fluctuations that may have an influence on the shedding of cercariae. Thus, experimental infections of Lymnaea truncatula by Paramphistomum daubneyi were performed to determine whether a sudden fall in temperature--daily dipping of infected snails into spring water at 14-15 degrees C, or at 6-8 degrees C--followed by its increase at 20 degrees C in the subsequent hour, had an influence on the characteristics of snail infection and cercarial production. The immersion of infected snails in cold water during a short period delayed the first cercarial shedding, at day 66 on average, in the 6-8 degrees C group vs at day 57 in the 14-15 degrees C group, or at day 49 in the 20 degrees C group. The percentage of cercaria-shedding snails was greater in the 6-8 degrees C group than in the 14-15 degrees C and the 20 degrees C ones: 41.8% vs 17.3% and 7.1%, respectively. The total number of cercariae given by each infected snail was also higher in the 6-8 degrees C group. A fall in the temperature of water during daily change, followed by its increase at 20 degrees C within the subsequent hour, stimulated the cercarial shedding of P. daubneyi.     

Emergence of cercariae of Echinostoma caproni and Schistosoma mansoni from Biomphalaria glabrata under different laboratory conditions

Release of Echinostoma caproni cercariae and Schistosoma mansoni from experimentally infected Biomphalaria glabrata snails maintained under different laboratory conditions was studied. Infected snails were isolated individually for 1 h in Stender dishes containing 5 ml of artificial spring water and the number of cercariae released during this time was recorded. Of numerous conditions tested, the addition of lettuce, the use of water conditioned by B. glabrata snails and a temperature of 35 degrees C significantly increased the release of E. caproni cercariae. A significant increase in cercarial release of S. mansoni was seen only in cultures fed lettuce. A temperature of 12 degrees C caused a significant decrease in cercarial release of both E. caproni and S. mansoni. Increased snail activity associated with feeding behaviour was probably responsible for the enhanced cercarial sheds observed in this study.     

Plagiorchis elegans (Digenea: Plagiorchiidae) infections in Stagnicola elodes (Pulmonata: Lymnaeidae): host susceptibility, growth, reproduction, mortality, and cercarial production.

Eggs of Plagiorchis elegans were readily ingested by Stagnicola elodes of all ages, but were more infective to immature than mature snails. Infection enhanced the growth of the host in a dose-dependent manner. The number of cercariae released by immature snails increased with the age of the snail host; mature snails yielded fewer cercariae. Heavily infected snails tended to die prematurely, thereby reducing their total production of cercariae to levels below those of more lightly infected individuals. Even light infections castrated the snail host. Snails that acquired the infection as juveniles never produced eggs. Actively reproducing snails ceased egg laying within days of infection and never recovered. All parasite effects on the growth and reproduction of the snail host first manifested themselves during the early stages of infection, long before the development of daughter sporocysts and cercariae, and are therefore attributable to the effects of mother sporocysts. The study provides insight into how this natural enemy of mosquito larvae may be established in natural snail populations by means of strategically timed introductions of parasite eggs, with a goal of maximizing cercarial production for the biological control of sympatric mosquito larvae.     

The effect of Schistosoma haematobium infection on the growth and fecundity of three sympatric species of bulinid snails

Three species of bulinid snails were monitored to determine the effect of infection with 2 sympatric strains of Schistosoma haematobium on longevity, growth, and reproductive output, from the onset of cercarial production until death. Bulinus senegalensis was least affected by infection, with total fecundity reduced by less than 34%. Infected Bulinus truncatus showed an acceleration in growth accompanied by a 63% reduction in fecundity, although the majority of snails continued to oviposit at a low level. The longest-lived snails in this study, Bulinus globosus, showed decreased growth and survival when infected. In addition a significant proportion of infected individuals of this species failed to oviposit, and those that retained some reproductive capacity produced fewer embryos than controls. Total fecundity of B. globosus was reduced almost 90% by infection with S. haematobium, yet long-term monitoring of individuals showed that reproductive activity recovered when parasite productivity was low. Results from this and similar studies indicate that the time of infection by a trematode in relation to reproductive maturity of the molluscan host is important in determining the subsequent effects on host growth and fecundity.     

Studies on the prolonged storage of Metarhizium anisopliae conidia: effect of temperature and relative humidity on conidial viability and virulence against mosquitoes

The shell lengths, dried shell weights, soft tissue wet weights, and soft tissue dry weights were ascertained for noninfected Ilyanassa obsoleta and for the same snail species naturally infected with the following digeneans: Himasthla quissetensis, Zoogonus lasius, Cercaria dipterocerca, Lepocreadium setiferoides, Microphalloides nassicola, Stephanostomum tenue, and Microbilharzia variglandis. Analyses of the data obtained indicate that infection with all of the trematodes listed above causes neither enhanced growth of soft tissues nor accelerated lengthening of the shell. However, snails infected with sporocysts of Z. lasius have significantly heavier shells than do noninfected snails. These data suggest that infection with Z. lasius may have caused enhanced growth in the form of increased calcium deposition in the shell of I. obsoleta, possibly as a result of parasitic castration. In addition, the mean dry weight of the soft tissues of snails infected with M. variglandis, when normalized for shell length, is significantly lower than that of noninfected snails, possibly as a result of parasite-induced pathology. Finally, comparisons among infected snails indicate a trend toward increased soft tissue dry weight in snails infected with L. setiferoides, although the mean dry weight of these snails does not differ significantly from the mean dry weight of noninfected snails.     

Effect of light intensity on Opisthorchis viverrini cercarial shedding levels from Bithynia snails--a preliminary study

Opisthorchis viverrini requires Bithynia snails as the first intermediate host and cyprinid fish as the second intermediate host. Very low natural infection rates have been reported in Bithynia snails, but very high rates have been found in cyprinid fish in the same endemic region. This study investigated the effect of light intensity, the most important stimulus, on the quantity of O. viverrini cercariae shed from naturally infected Bithynia (Digoniostoma) siamensis goniomphalos snails. Snails were evaluated for cercariae output every hour after exposure to various light intensities for a total period of 7 h. The same infected snail was tested under different intensities of light: in the dark, and at 1000, 3000 and 5000 lx. The data showed that under exposure to 1000 and 3000 lx of light, the average percentage and number of cercariae released were higher than that exposed to 5000 lx during the first 2 h of the experiment. In contrast, under higher illumination (5000 lx) a longer time (6 h) was required to stimulate the peak emergence of cercariae. Darkness was not able to induce O. viverrini cercariae emergence. Among the three intensities of light, exposure at 1000 lx induced the highest average number of released cercariae per snail and the highest percentage of cercarial emergence within the first 2 h (125, 54.86%), followed by exposure at 3000 lx (69, 25.58%) and 5000 lx (12, 7.78%). The results suggest that the light intensity of 1000 lx for 2 h would be optimal for O. viverrini cercarial shedding from naturally infected B. (D.) siamensis goniomphalos snails.     

Schistosoma mansoni: characterization of clones maintained by the microsurgical transplantation of sporocysts

Five male and 5 female clones of Schistosoma mansoni were established and maintained for 3 yr by the serial microsurgical transplantation of sporocysts from infected to uninfected Biomphalaria glabrata snails. The clones were initially derived from 10 randomly selected snails with monomiracidial infections. Clones were characterized by several criteria, including their infectivities for mice and snails, their cercarial outputs, and their ability to produce immunity in mice. The mean infectivities of individual clones in mice ranged from 26 to 44%, and were highly consistent within each clone. The infectivities of cloned sporocysts in snails ranged from 44 to 100% and were also highly consistent within clones. Mean cercarial outputs from individual clones ranged from 450 to 4,300 per snail. In mice, clones differed significantly from each other in their ability to immunize and in their susceptibility to immunity. Each clone was unique and did not appear to differ with time or subpassaging through snails, suggesting that the differences had a genetic basis.     

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.     

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.     

Effect of exposure to Echinostoma itliei miracidia on growth and survival of young Biomphalaria glabrata snails

Kuris A. M. 1980. Effect of exposure to Echinostoma liei miracidia on growth and survival of young Biomphalaria glabrata snails. International Journal for Parasitology10: 303–308. Exposure to miracidia of Echinostoma liei resulted in increased mortality and reduced growth of 1–2 mm albino Biomphalaria glabrata snails whether or not the snails became infected. Growth rates for infected and exposed but uninfected snails were significantly more variable than growth rates of unexposed snails. Retarded growth and increased mortality were detected as rapidly as seven to nine days after exposure. Neither growth nor survivorship of 4–6 mm snails was altered upon exposure to or infection by E. liei.     

Interactions between natural populations of human and rodent schistosomes in the Lake Victoria region of Kenya: a molecular epidemiological approach

Background

Schistosoma mansoni exists in a complex environmental milieu that may select for significant evolutionary changes in this species. In Kenya, the sympatric distribution of S. mansoni with S. rodhaini potentially influences the epidemiology, ecology, and evolutionary biology of both species, because they infect the same species of snail and mammalian hosts and are capable of hybridization.

Methodology/Principal Findings

Over a 2-year period, using a molecular epidemiological approach, we examined spatial and temporal distributions, and the overlap of these schistosomes within snails, in natural settings in Kenya. Both species had spatially and temporally patchy distributions, although S. mansoni was eight times more common than S. rodhaini. Both species were overdispersed within snails, and most snails (85.2% for S. mansoni and 91.7% for S. rodhaini) only harbored one schistosome genotype. Over time, half of snails infected with multiple genotypes showed a replacement pattern in which an initially dominant genotype was less represented in later replicates. The other half showed a consistent pattern over time; however, the ratio of each genotype was skewed. Profiles of circadian emergence of cercariae revealed that S. rodhaini emerges throughout the 24-hour cycle, with peak emergence before sunrise and sometimes immediately after sunset, which differs from previous reports of a single nocturnal peak immediately after sunset. Peak emergence for S. mansoni cercariae occurred as light became most intense and overlapped temporally with S. rodhaini. Comparison of schistosome communities within snails against a null model indicated that the community was structured and that coinfections were more common than expected by chance. In mixed infections, cercarial emergence over 24 hours remained similar to single species infections, again with S. rodhaini and S. mansoni cercarial emergence profiles overlapping substantially.

Conclusions/Significance

The data from this study indicate a lack of obvious spatial or temporal isolating mechanisms to prevent hybridization, raising the intriguing question of how the two species retain their separate identities.