Prey selection by molluscivorous cichlids foraging on a schistosomiasis vector snail,Biomphalaria glabrata

Summary This paper considers prey size selection by four molluscivorous cichlids feeding on the intermediate host snail of Schistosoma parasites, Biomphalaria glabrata. Haplochromis ishmaeli obtains its prey by crushing the snails between the pharyngeal jaws, whereas H. xenognathus, H. sauvagei and Macropleurodus bicolor apply both pharyngeal crushing and oral shelling. The fishes crushed significantly more snails with the highest reward in biomass per second of crushing. Oral shelling occurred far less often than pharyngeal crushing. Encounter rates with prey showed significant variations between different size classes of prey. The fish have no overall knowledge of snail availability in a tank. The probability that a snail will be eaten at encounter, calculated from the number encountered and the number eaten, reflects the prey size preference of the fish. Those snails with the highest biomass/crushing-time ratio had the highest probability of being crushed; observed and predicted prey size preferences corresponded well. Although for oral shelling the potential reward in biomass per second is of the same magnitude as for crushing, the probability of successful shelling is very low. Apparently the fish prefer prey with lowest risks.     

An example of molecular co-evolution: reactive oxygen species (ROS) and ROS scavenger levels in Schistosoma mansoni/Biomphalaria glabrata interactions

The co-evolution between hosts and parasites involves huge reciprocal selective pressures on both protagonists. However, relatively few reports have evaluated the impact of these reciprocal pressures on the molecular determinants at the core of the relevant interaction, such as the factors influencing parasitic virulence and host resistance. Here, we address this question in a host-parasite model that allows co-evolution to be monitored in the field: the interaction between the mollusc, Biomphalaria glabrata, and its trematode parasite, Schistosoma mansoni. Reactive oxygen species (ROS) produced by the haemocytes of B. glabrata are known to play a crucial role in killing S. mansoni. Therefore, the parasite must defend itself against oxidative damage caused by ROS using ROS scavengers in order to survive. In this context, ROS and ROS scavengers are involved in a co-evolutionary arms race, and their respective production levels by sympatric host and parasite could be expected to be closely related. Here, we test this hypothesis by comparing host oxidant and parasite antioxidant capabilities between two S. mansoni/B. glabrata populations that have co-evolved independently. As expected, our findings show a clear link between the oxidant and antioxidant levels, presumably resulting from sympatric co-evolution. We believe this work provides the first supporting evidence of the Red Queen Hypothesis of reciprocal evolution for functional traits at the field-level in a model involving a host and a eukaryotic parasite.     

Effects of intermediate host genetic background on parasite transmission dynamics: a case study using Schistosoma mansoni

For parasites that require multiple hosts to complete their development, genetic interplay with one host may impact parasite transmission and establishment in subsequent hosts. In this study, we used microsatellite loci to address whether the genetic background of snail intermediate hosts influences life-history traits and transmission patterns of dioecious trematode parasites in their definitive hosts. We performed experimental Schistosoma mansoni infections utilizing two allopatric populations of Biomphalaria glabrata snails and assessed intensities and sex ratios of adult parasites in mouse definitive hosts. Our results suggest that the genetic background of hosts at one point in a parasite’s life cycle can influence the intensities and sex ratios of worms in subsequent hosts.     

Studies on resistance in snails: Specific resistance induced by irradiated miracidia of Echinostoma lindoense in Biomphalaria glabrata snails

In juvenile Biomphalaria glabrata snails exposed to irradiated Echinostoma lindoense miracidia, the sporocysts migrated to the heart at the same speed as did nonirradiated sporocysts in control snails. However, in each snail so exposed to irradiated miracidia, amebocyte clumps in the snail's heart destroyed the sporocysts within 2–9 days post-exposure. This process induced a strong, highly specific resistance to homologous reinfection in these previously susceptible snails. The snails remained susceptible to Schistosoma mansoni and Paryphostomum segregatum (Echinostomatidae), but were partially resistant to Echinostoma paraensei and E. liei, two echinostome species closely related to E. lindoense.     

Decline of a sylvatic focus of Schistosoma mansoni in Guadeloupe (French West Indies) following the competitive displacement of the snail host Biomphalaria glabrata by Ampullaria glauca

Summary Grand Etang lake in Guadeloupe is a focus of intestinal schistosomiasis characterized by the virtual absence of human contact and the presence of a heavily infested rat population. The lake, with a surface area of 0.03 km², is situated in rain forest at an altitude of 450 m. Originally it contained an extensive belt of the floating plant Pistia stratiotes which provided a favourable habitat for Biomphalaria glabrata, the intermediate host snail of Schistosoma mansoni. In 1974 and 1975, a low prevalence (about 3%) of S. mansoni was observed in B. glabrata while a high prevalence (about 60%) was recorded in rats. The rat population was infected with another trematode, Ribeiroia guadeloupensis, which requires two intermediate hosts, B. glabrata and the fish Tilapia mossambica. In 1976, the prosobranch snail, Ampullaria glauca, was accidentally introduced into the lake. By 1980, this snail had spread over half of the lake and had caused marked regression of the P. stratiotes layer. Concomitantly, the population of B. glabrata declined to such a point that in 1985 only a small colony remained in the northern section of the lake. The consequences of these changes are reflected in a rapid decline of S. mansoni in the rat population from 61.3% in 1980 to 34.8% in 1981, 6.5% in 1982, 2.8% in 1983, 11.6% in 1984, and 0% in 1985 and 1986.     

Revised karyotyping and gene mapping of the Biomphalaria glabrata embryonic (Bge) cell line

The fresh water snail Biomphalaria glabrata (2n = 36) belongs to the taxonomic class Gastropoda (family Planorbidae) and is integral to the spread of the human parasitic disease schistosomiasis. The importance of this mollusc is such that it has been selected as a model molluscan organism for whole genome sequencing. In order to understand the structure and organisation of the B. glabrata’s genome it is important that gene mapping studies are established. Thus, we have studied the genomes of two B. glabrata embryonic (Bge) cell line isolates 1 and 2 grown in separate laboratories, but both derived from Eder L. Hansen’s original culture from the 1970s. This cell line continues to be an important tool and model system for schistosomiasis and B. glabrata. Using these cell line isolates, we have investigated the genome content and established a revised karyotype based on chromosome size and centromere position for these cells. Unlike the original karyotype (2n = 36) established for the cell line, our investigations now show the existence of extensive aneuploidy in both cell line isolates to the extent that the total complement of chromosomes in both greatly exceeds the original cell line’s diploid number of 36 chromosomes. The isolates, designated Bge 1 and 2, had modal chromosome complements of 64 and 67, respectively (calculated from 50 metaphases). We found that the aneuploidy was most pronounced, for both isolates, amongst chromosomes of medium metacentric morphology. We also report, to our knowledge for the first time using Bge cells, the mapping of single-copy genes peroxiredoxin (BgPrx4) and P-element induced wimpy testis (piwi) onto Bge chromosomes. These B. glabrata genes were mapped onto pairs of homologous chromosomes using fluorescence in situ hybridization (FISH). Thus, we have now established a FISH mapping technique that can eventually be utilized for physical mapping of the snail genome.     

The invasion of Biomphalaria pfeifferi by Schistosoma mansoni miracidia and the development of daughter sporocysts

Laboratory experiments have been carried out to determine the susceptibility of Gezira Biomphalaria pfeifferi snails to S. mansoni miracidia and the relationship between miracidia and daughter sporocyst production at the 10–17 day development stage. The relationship between snail numbers, miracidia numbers and water volume has also been studied. Two non susceptible snails, Bulinus truncatus and Cleopatra bulimoides, both of which occur naturally in Gezira canals, were tested to see if they act as decoys for S. mansoni miracidia.The results showed that the B. pfeifferi are 100% susceptible to S. mansoni invasion, at least to the daughter sporocyst development stage. The more miracidia that penetrated the more daughter sporocysts were produced, however individual variation and overlap were great. When one miracidium was released to find one snail it succeeded in low water volumes (5 m, 50 ml), but failed in 5 litres. When 100 miracidia were released mortality of snails was high suggesting superinfection particularly when only one or five snails were available. Among survivors daughter sporocyst counts were very high. Cleopatra and Bulinus snails do have a decoy effect when present in large numbers. In their presence the number of infected snails was marginally reduced and the number of daughter sporocysts greatly reduced. However, if superinfection is reduced by decoy effect, it is conceivable that Biomphalaria may be protected by decoy snails in circumstances where miracidia counts are high.