Fouling of gastropods: a role for parasites?

A sample of mud snails Hydrobia ulvae (Prosobranchia) from an intertidal population revealed that the shells of trematode-infected specimens were especially likely to be fouled with epibionts. Experimentally trematode-infected Biomphalaria glabrata (Pulmonata) appeared to be especially prone to develop epigrowth in comparison with uninfected conspecifics as well. These findings suggest an interaction between trematode infections and epibiosis in aquatic gastropods. The two most likely explanations for this are (1) that trematode infections weakens the snails' natural defences against epibionts, or (2) that the defences against epibionts also are effective against invading trematodes, causing snail specimens with a particularly good fouling defence to be less likely to become infected.     

Ecology of Biomphalaria (Gastropoda: Planorbidae) in Lake Albert, Western Uganda: snail distributions, infection with schistosomes and temporal associations with environmental dynamics

In Lake Albert, an ecological study was conducted, between June 2000 and May 2003, which assessed snail population dynamics, parasite infection patterns and interplay of environmental factors upon Biomphalaria. Monthly sampling surveys were conducted at 29 sites monitoring populations of Biomphalaria stanleyi and Biomphalaria sudanica. Altogether, a total of 21,715 B. stanleyi and 8452 B. sudanica were collected during the period. Both species could be found infected with Schistosoma mansoni although infection prevalence was significantly higher (p < 0.01**) in B. stanleyi (4.4%) than in B. sudanica (3.5%). Each species occupied slightly different aquatic niches with B. stanleyi preferring deeper water habitats whilst B. sudanica was found along the shoreline in shallower water. B. stanleyi was more widely distributed among the sampling locations (19 sites) than B. sudanica (10 sites). Of the four villages included in the study area, snails from sites near Piida and Bugoigo villages had the highest schistosome infection rates, presumably attributable to the closer proximity of people with intestinal schistosomiasis. After inspection of cross-correlation plots which identified most suitable time lags, snail density dynamics could be associated with seasonal variations inclusive of: air temperature, rainfall, lake level, water temperature, water conductivity and water pH. These temporal observations better reveal the relationship between snail populations and environmental factors, providing important information concerning the relative roles of B. stanleyi and B. sudanica in transmission of S. mansoni and development of integrated strategies for disease control around Lake Albert.     

Physiologic studies of snail-schistosome interactions and potential for improvement of in vitro culture of schistosomes

Summary Despite extensive efforts to develop suitable media for rearing the intramolluscan stages of schistosomes, successful in vitro culture of these parasites remains elusive. Recent³¹P NMR studies demonstrated that the levels of free phospholipids, particularly phosphatidylcholine, in the digestive gland of the snail,Biomphalaria glabrata, were dramatically reduced when the host was infected withSchistosoma mansoni. It was speculated that absorption of host phosphatides may be an important source of membrane phospholipid precursors and fatty acids for developing sporocysts and cercariae. During the present investigations,B. glabrata was maintained on a high fat diet of egg yolk, and the lipid composition of control uninfected and infected snails examined by³¹P and¹³C NMR. In addition, the levels of host hemolymph metabolites, including glucose and urea, considered as indicators of parasite nutrient uptake, were monitored. The lipid level of snails fed egg yolk was greatly increased, and hosts developed patent infections in approximately half the time of infected snails maintained on lettuce. The composition of the free phospholipids accumulated in the tissues ofB. glabrata fed egg yolk were the same as those previously reported in the cercarial stage ofS. mansoni. Moreover, the fatty acids ofS. mansoni and those reported here in the neutral lipids and free phosphatides in the host tissues were similar. Uninfected snails maintained on lettuce had higher hemolymph levels of glucose than those reared on egg yolk, and infected hosts on egg yolk had significantly lower levels of hemolymph urea. β-hydroxybutyrate was the principal hemolymph metabolite in snails fed egg yolk, but was not detected in snails maintained on lettuce. The level of β-hydroxybutyrate in the hemolymph of snails on egg yolk was significantly reduced by infection. The results indicated that the pattern of host hemolymph nutrient utilization by larval schistosomes may be markedly altered by host diet, and it was concluded that host lipids may directly and indirectly be important nutrients for developing schistosomes. Future studies on in vitro culture of the intramolluscan stages of schistosomes should emphasize the potential role of lipids and attempt to define the nutritive value of those medium components that presently supply lipids in culture media, most notably serum.     

Age/size- and time-specific effects of Schistosoma mansoni on energy allocation patterns of its snail host Biomphalaria glabrata

Snail hosts of different ages constitute different resource environments for larval trematodes because each individual has a particular energy budget and energy allocation pattern at the time of infection. Effects of monomiracidial trematode infections on shell growth, body dry weight and reproductive effort of the snail host were compared between controls and infected juvenile and adult snails during the prepatent and patent periods. The results demonstrate phenotypic plasticity in the host response. There is an age/size-specific effect characterized by limitation of growth rate when snails are infected as juveniles and reduction of reproductive effort when snails are infected as adults, and a time-specific effect with early enhancement of growth rate and reproductive effort for infected juvenile and adult snails respectively during prepatency, before reduction and cessation during patency. The parasite is considered as a generalist in its energy exploitation strategy of the snail host, but taking into account the differential host responses observed relative to the host age, the possibility of a host preference for juvenile or adult snails is discussed. Received: 4 February 1997 / Accepted: 14 July 1997     

Phenoloxidase activity in the reproductive system and egg masses of the pulmonate gastropod,Biomphalaria glabrata

Phenoloxidase (PO) activity in the albumen gland (AG) and egg masses (EM) ofBiomphalaria glabrata was assessed using high-performance liquid chromatography combined with electrochemical detection and colorimetric techniques. Both AG and EM extracts catalyzed the hydroxylation ofl-tyrosine (monophenol oxidase activity, MPO) and oxidation ofl-dopa (diphenol oxidase activity, DPO). However, no PO activity was found in the ovotestis. Both MPO and DPO activities in AG and EM were significantly inhibited by 1-phenyl-2-thiourea and inactivated by boiling. Approximately 35% of MPO and 44% of DPO activities were detected in the soluble fraction of homogenized EM, in contrast to that of homogenized AG, which contained about 5% and 12%, respectively, of MPO and DPO activities. N-acetyl-dopamine, a diphenolic compound, enhanced the hydroxylation of tyrosine by the PO. The presence of both MPO and DPO activities also was confirmed by the accelerated accumulation of dopachrome during incubation of EM extracts withl-tyrosine in the absence of ascorbate. Temperature and pH optima for this enzyme were 30°C and 7.5, respectively. The potential roles of PO in egg formation inB. glabrata are discussed.     

Action competitive d'helisoma duryi,wetherby (Planorbidae : Helisomatinae) a l'egard de divers mollusques vecteurs de trematodoses humaines et animales. I. Biomphalaria glabrata,say

Laboratory experiments indicate that Helisoma duryi may be a promising biological control agent of human Schistosomiasis by acting as a predator of very young Biomphalaria glabrata and, when the two planorbid snails are maintained together, in influencing infection rate of Biomphalaria by miracidia of Schistosoma mansoni and their cercarial production.(avec la collaboration technique de R. THOMASSET)     

Characterization of the mannose 6-phosphate receptor (Mr 300 kDa) protein dependent pathway of lysosomal enzyme targeting in Biomphalaria glabrata mollusc cells

Mammalian mannose 6-phosphate receptors (MPR 300 and 46) are involved in the targeting of newly synthesized lysosomal enzymes and only MPR 300 also participates in the endocytosis of various exogenous ligands. The present study describes for the first time the MPR 300 dependent pathway of lysosomal enzyme sorting in the Biomphalaria glabrata embryonic (Bge) cells. Lysosomal enzymes (arylsulfatase A, β-hexosaminidase and α-fucosidase) were identified by their enzymatic activities and by immunoprecipitation with specific antisera. Exposure of Bge cells to unio MPR 300 antiserum resulted in a dramatic loss of MPR 300 protein with a shortened half life of ∼20 min as compared to control cells exposed to preimmune serum in which the half life of MPR 300 was of ∼13 h. Loss of receptor proteins resulted in a significant misrouting of newly synthesized lysosomal enzymes and their secretion in cell culture medium as demonstrated by immunoprecipitation. The ability of Bge cells to uptake and internalize labeled arylsulfatase A, β-hexosaminidase and α-fucosidase enzymes contained in cell secretion products also indicated the role of B. glabrata MPR 300 (CIMPR) protein in internalization and targeting of lysosomal enzymes. M6P dependent binding of lysosomal enzymes to MPR 300 was shown by confocal microscopy and coimmunoprecipitation experiments.     

Thin layer chromatographic analysis of glucose and maltose in estivated Biomphalaria glabrata snails and those infected with Schistosoma mansoni

Thin layer chromatography was used to analyze the glucose and maltose concentrations of the digestive gland–gonad complex (DGG) of uninfected-estivated Biomphalaria glabrata snails and estivated B. glabrata patently infected with Schistosoma mansoni. All snails were estivated in a most chamber at a relative humidity of 98 ± 1% and a temperature of 23 ± 1 °C for 14 days. Carbohydrates were extracted from the DGG with 70% aqueous ethanol, and extracts were analyzed on silica gel preadsorbent plates using ethyl acetate–glacial acetic acid–methanol–water (60:15:15:10) mobile phase, α-naphthol–sulfuric acid detection reagent, and quantification by densitometry. The concentrations of glucose and maltose were significantly reduced in both uninfected-estivated snails and infected-estivated snails.     

Fine-scale population structure and dispersal in Biomphalaria glabrata, the intermediate snail host of Schistosoma mansoni, in Venezuela

Biomphalaria glabrata is the main intermediate host of Schistosoma mansoni in America and one of the most intensely studied species of freshwater snails, yet very little is known about its population biology. Here, we used seven highly polymorphic microsatellite loci to analyse genetic diversity in the Valencia lake basin, which represents the core of the endemic area for schistosomiasis in Venezuela. Populations were sampled at short spatial scale (a few kilometres), both inside the lake and in ponds or rivers near the lake. Our results indicate that B. glabrata essentially cross-fertilizes, with little variation in selfing rates among populations. Our markers detected considerable genetic variation, with an average heterozygosity of 0.60. More diversity per population was found within than outside the lake, suggesting an influence of connectivity among populations on the levels of genetic diversity. A marked population structure was detected and lake populations were less structured than other populations. Most individuals were assigned to their population of origin using an assignment test. No strong demographic signal (e.g. bottleneck) was detected, though lake populations are likely to experience bottlenecks more frequently than the other populations analysed. Differences in gene flow therefore seem to play an important role in population differentiation and in the restoring of genetic diversity in demographically unstable populations.     

The ecology of Biomphalaria sudanica in Lake Ziway, Ethiopia

A longitudinal study was made over a period of 24 months from January 2001 to December 2002 in Lake Ziway, Ethiopia, to elucidate factors influencing changes in the population density of Biomphalaria sudanica and to identify seasons of peak transmission of Schistosoma mansoni. Between January 2001 and December 2002, bimonthly visits were made to the lake to collect data on snail population density and schistosome infection in snails, vegetation and lake water level. Water samples were collected during the dry and rainy seasons and chemical analyses were made for major cations, anions, electrical conductivity, total hardness and pH using standard methods for the examination of water and wastewater. The seasonal fluctuation in the population density of B. sudanica was found to be highly associated with rainfall, water level of the lake and vegetation availability and abundance. Water chemical analysis showed that major cations and anions were all within the range reported for other African freshwaters. Both malacological and meteorological data show that snail population density in Lake Ziway peaks at the end of the long rainy season (June–August), coinciding with a seasonal transmission peak of schistosomiasis.