The case for biological control of snail intermediate hosts of Schistosoma mansoni.
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Biomedical subjects
J P Pointier
Publications and source records attributed to J P Pointier.
Biological control and invading freshwater snails. A case study.
Introductions of four species of freshwater snails occurred between 1972 and 1996 onto Guadeloupe Island. Two of them, Melanoides tuberculata and Marisa cornuarietis, were subsequently used as biological control agents against Biomphalaria glabrata, the snail intermediate host of intestinal schistosomiasis. In 1996, a general survey was carried out in 134 sites which had already been investigated in 1972. The total number of mollusc species had increased from 19 to 21. Site numbers housing B. glabrata and two other species had strongly declined. This decline may be mainly attributed to a competitive displacement by M. tuberculata and M. cornuarietis as illustrated by several biological control programmes. There were no changes in the remainder of the malacological fauna.
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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.
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Genetic evidence of two species in the Biomphalaria havanensis complex (Gastropoda. Planorbidae) from Cuba.
In Cuba, several species of freshwater gastropods belonging to the genus Biomphalaria have been described according to morphological characters. However, the taxonomy of this group remains unclear and a number of synonyms are often cited in the literature. This is the case for B. havanensis whose taxonomical status is not well established. Multilocus enzyme electrophoresis at 18 loci was carried out on adult snails of B. havanensis from the type locality in Havana and from several other sites harbouring a morphologically slightly different form, referred to here as Biomphalaria sp. Another local distinct species B. helophila was used as an outgroup. Allelic distribution showed the presence of nine and 12 diagnostic loci between B. havanensis and Biomphalaria sp. and B. helophila, respectively. We detected eight fixed alleles between Biomphalaria sp. and B. helophila. The genetic divergence estimated by absolute genetic distances strongly supports the assumption that Biomphalaria sp. is quite different from the sympatric B. havanensis, morphologically the closest species.
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Density and variability of dinucleotide microsatellites in the parthenogenetic polyploid snail Melanoides tuberculata.
Characterization of microsatellites in the parthenogenetic polyploid snail Melanoides tuberculata revealed an unusual high density of dinucleotide repeats. Multiple banding patterns were obtained at these loci, and interpreted as a consequence of polyploidy. Microsatellite variability was low within, but high between, shell morphotypes. Genotypes were wholly transmitted from mothers to offspring. These results suggest that reproduction is strictly apomictic, and that shell morphotypes are genetic clones.
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Natural Schistosoma mansoni infection in wild rats from Guadeloupe: parasitological and immunological aspects.
Rattus rattus is the predominant rodent in the mangrove area of Guadeloupe. Between 1990 and 1991 we found 73 R. rattus and five R. norvegicus. Among the infected rats with Schistosoma mansoni, 59% for R. rattus and 80% for R. norvegicus, the comparison of the median of the worm load was not statistically different. Both species of infected rats showed adult worms and eggs in the lungs and 20% of them showed, at the same time, two and even three generations of worms. Neither adults nor eggs were seen in the intestinal wall or stools of R. norvegicus, instead R. rattus had eggs in the liver, in the intestinal wall and the stools. Therefore, R. norvegicus gets infection as well as R. rattus, but does not participate in the transmission of the schistosomiasis. In order to elucidate this difference, we looked at the humoral recognition of these two rats, to the molecular antigens of the three stages of the parasite: cercaria, adult worm (AWA) and egg (SEA). In general, R. norvegicus recognized cercarial antigens more frequently than R. rattus, 73, 81 and 172 kDa being statistically different. Regarding AWA, molecules 82, 86, 117 and 150 kDa were recognized more often by R. rattus as compared to R. norvegicus. The reverse was true for the 18, 33 and 61 kDa. Only the differences between 61 and 150 kDa molecules were statistically significant. With respect to SEA, R. norvegicus recognized more 28, 45, 47, 49, 64 and 92 kDa molecules than R. rattus, but the latter recognized the 140 kDa molecules of SEA to a higher degree (95 and 140 kDa were significantly different). It is plausible that the immune response to cercarial invasion is more effective in R. norvegicus in allowing the parasites to reach adulthood, but it does not let them live in the mesenteric veins and therefore to lay their eggs in the intestinal wall and feces.
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Phylogeography and genetic divergence of some lymnaeid snails, intermediate hosts of human and animal fascioliasis with special reference to lymnaeids from the Bolivian Altiplano.
A population genetic study using starch gel electrophoresis was performed on populations of several species of lymnaeid snails acting as intermediate hosts for Fasciola hepatica (Trematoda, Plathyhelminth). Lymnaea viatrix was collected in 16 sites from the Bolivian Northern Altiplano. L. cubensis were obtained in one site from Venezuela, one site from Guadeloupe, three sites from Cuba and one site from the Dominican Republic. L. truncatula were collected in one site from France, one from Portugal and one from Morocco. Multilocus enzyme electrophoresis (MEE) were determined for 282 snails at 18 loci. A complete monomorphism was encountered at each geographic site. However, among these 18 loci, 13 are polymorphic and low and high levels of genetic divergence were observed between samples. Two genotypic groups can be differentiated by their multilocus genotypes. The western genotypic group associates together samples from Venezuela, Guadeloupe, Cuba and Dominican Republic (L. cubensis) while samples from France, Portugal and Morocco (L. truncatula) belong to the eastern genotypic group. Surprisingly, the Northern Bolivian Altiplano populations (L. viatrix) do not present any genetic divergence with the Portuguese sample. Therefore, the Bolivian snails belong entirely to the eastern genetic group. Within each group slight genetic divergences were observed. These results strongly support the European origin of the lymnaeid snails from the Northern Bolivian Altiplano.
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[Control of intestinal schistosomiasis in Martinique island].
The presence of schistosomiasis mansoni is known in Martinique since the beginning of the XXth century. A general survey of the distribution of the disease was carried out in 1977 and showed a mean prevalence of 12% (coprology and serology taken together) in the whole of the island. Following this survey, an integrated control programme associating sanitary education, detection and treatment of patients and improved sanitation, was developed. In addition, a biological control programme against the intermediate snail host, Biomphalaria glabrata using the competitor snail, Melanoides tuberculata, was developed in the transmission sites. The decline of snail populations and of its parasite, as well as a strong reduction of the prevalence in humans were recorded between 1977 and 1996. At the present time, only few cases corresponding to older infections are detected. This epidemiological situation is quite different from that in Guadeloupe island where, in spite of an excellent control programme which was achieved on the Basse-Terre district, an important focus is still functioning on Grande-Terre district with the black rat as host reservoir. Such foci do not exist on Martinique island.
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SSU rDNA characterization of lymnaeid snails transmitting human fascioliasis in South and Central America.
The small subunit (18S) rRNA gene sequences of the lymnaeid morphs I and II (Mollusca: Gastropoda: Basommatophora: Lymnaeidae) transmitting human fascioliasis in the high endemic zone of the northern Bolivian Altiplano and of Lymnaea cubensis from Mexico and Guadeloupe island (Caribbean) have been obtained by direct polymerase chain reaction PCR cycle sequencing and silver staining methods and compared to that of the 6 most common European Lymnaeidae species. Results allow us to establish definitively the distinction between the lymnaeids from the northern Bolivian Altiplano and L. cubensis. Lymnaea cubensis is a valid species distributed in North and Central America but absent in the northern Bolivian Altiplano. Lymnaeid morphs I and II from the northern Bolivian Altiplano both present the same 18S rDNA sequence, which is moreover identical to that of the European species Lymnaea truncatula. Significant nucleotide substitutions in helix E10-1 of the variable region V2 of the secondary structure suggest the need for distinguishing L. cubensis in the subgenus Lymnaea (Bakerilymnaea) with L. (B.) cubensis as type species. The subgenus Lymnaea (Fossaria) is retained, with L. (F.) truncatula as type species. The larger number of nucleotides in the 18S rDNA sequence of L. cubensis (1,860 bp) with regard to the other Lymnaea species (1,843-1,852 bp) is tentatively related to the more ancient paleogeographic origin of L. cubensis. The grouping of L. cubensis with L. truncatula and the relationship of Lymnaea auricularia with Lymnaea peregra in the phylogenetic trees obtained show an evolutionary parallelism with the digenean parasite species they transmit, namely Fasciola hepatica and Fasciola gigantica, respectively.
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Distribution of schistosome genetic diversity within naturally infected Rattus rattus detected by RAPD markers.
Random amplified polymorphic DNA markers (RAPD) were used to visualize the genetic diversity within and between infrapopulations of Schistosoma mansoni recovered from the natural vertebrate host, Rattus rattus, trapped at an insular Guadeloupean focus. Phenotypes were characterized by the sex of the parasites and by 8 polymorphic markers generated by 3 primers. Among the 212 parasite individuals recovered from 10 infected rats, 78 genotypes were characterized. All the hosts naturally infected harboured multiple parasite genotypes with a maximum diversity of 28 genotypes/host. Phenotypic and genotypic diversity calculated by Shannon-Wiener's indices and Lynch and Milligan's estimators respectively is, on average, greater within than between hosts. Considering the very low snail infection rates observed in this focus and the rapid turnover of the vertebrate hosts, our results suggest that the high mobility of the vertebrate host and/or plurimiracidial snail infections could be factors responsible for parasite genetic diversity within hosts.
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The introduction of Melanoides tuberculata (Mollusca: Thiaridae) to the island of Saint Lucia (West Indies) and its role in the decline of Biomphalaria glabrata, the snail intermediate host of Schistosoma mansoni.
A malacological survey was carried out in May 1992 in the whole hydrographic system of Saint Lucia 11 years after the end of a biological control programme to eliminate Biomphalaria glabrata, the snail intermediate host of Schistosoma mansoni. A competitor snail, Melanoides tuberculata, was introduced to Saint Lucia in 1978 and field experiments in several habitats were conducted by Prentice between 1978 and 1986. At the present time M. tuberculata is the most common freshwater snail in Saint Lucia. The results of the survey, undertaken in sites where B. glabrata occurred in large populations in the past showed (i) the absence of the snail hosts from seven sites now extensively colonized by the competitor (ii) the presence of B. glabrata in low or very low densities in 17 sites together with the competitor and (iii) the presence of the intermediate hosts in large populations in only two sites where M. tuberculata was absent. These results confirm the positive results observed by Prentice. The presence of another planorbid snail, B. straminea, is reported for the first time in Saint Lucia.
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Long-term dynamics of natural populations of Schistosoma mansoni among Rattus rattus in patchy environment.
Dynamics of natural populations of Schistosoma mansoni were studied during 8 consecutive years among Rattus rattus populations from 8 transmission sites of the marshy forest focus of Guadeloupe (French West Indies). The schistosome population is over-dispersed (k = 0.119) within the murine hosts and ecological factors linked to the patchy environment may be responsible for such aggregated distribution. Analysis of the spatio-temporal variations in prevalences, intensities and abundances showed limited variations of the infection during the 8 years at the level of the whole parasite population but great spatial heterogeneity at the level of local schistosome populations. Inter-populational genetic variability linked to the degree of adaptation of this human parasite to the murine host may explain differences in transmission dynamics between the local populations of S. mansoni.
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Biological control of the snail intermediate hosts of Schistosoma mansoni in Martinique, French West Indies.
In Martinique water-cress beds constituted the last transmission sites for schistosomiasis. The competitor snail, Melanoides tuberculata, was introduced at the beginning of 1983 to a group of water-cress beds and eliminated the snail hosts, Biomphalaria glabrata and B. straminea, in less than two years. Following this first success, M. tuberculata was introduced to the other groups of beds which were inventoried at the beginning of the eighties. At the present time, B. glabrata and B. straminea have totally disappeared from eight sites and only a few individuals have been recorded from 12 sites. The two remaining water-cress beds have dried up and were abandoned.
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Influence of the nontarget mollusc Marisa cornuarietis on the hourly cercarial production of Schistosoma mansoni from Biomphalaria glabrata.
A comparative study of hourly cercarial productivities of Schistosoma mansoni from infected Biomphalaria glabrata was carried out in the presence of either healthy B. glabrata (control) or healthy Marisa cornuarietis (experimental). The results showed that, with M. cornuarietis, almost all the hourly cercarial productivities increased by a factor varying from 1.3 to 2.5 without modification of the shedding period.
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Biological control of the snail hosts of Schistosoma mansoni in the Caribbean area using Thiara spp.
Field observations and experiments using thiarid snails as competitors of Biomphalaria spp., potential intermediate hosts of Schistosoma mansoni in the Caribbean area, are reviewed. The parthenogenetic snails, Thiara granifera and T. (= Melanoides) tuberculata, were introduced to the Neotropical area in recent decades. In numerous islands and countries, these oriental species have demonstrated their capacity to colonize rapidly and densely many types of habitats while at the same time reducing and even eliminating populations of Biomphalaria spp. The results of field experiments, carried out in several Caribbean islands, have shown the efficiency as well as the limitations of T. tuberculata as a competitor of B. glabrata and B. straminea. In St. Lucia, B. glabrata was apparently eliminated from marshes and streams, 6 to 22 months after the introduction of the competitor. In Martinique, T. tuberculata was introduced into two groups of water-cress beds which constituted the last transmission sites of schistosomiasis on the island. In just less than three years after the introduction of the competitor, both B. glabrata and B. straminea have been eliminated from the transmission sites. In Guadeloupe, several introductions have been carried out in different types of habitat such as permanent ponds, canals, streams and temporary marshes. The findings of all field experiments have indicated that thiarid snails as competitors of pulmonates are favoured by the presence of permanent and stable habitats, preferably shallow, with emergent plants and well oxygenated. On the other hand, the competitor snails are at a disadvantage in waterbodies which are temporary, extremely deep, poorly oxygenated or with a dense mat of floating aquatic vegetation.(ABSTRACT TRUNCATED AT 250 WORDS)
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Biological control of Biomphalaria glabrata and B. straminea by the competitor snail Thiara tuberculata in a transmission site of schistosomiasis in Martinique, French West Indies.
In Martinique, intestinal schistosomiasis was discovered at the beginning of this century. The intermediate host snail, Biomphalaria glabrata, was considered in the past as a common species in the different habitats of the island, but during the last decade it has been found only in water-cress beds. Several of these water-cress cultures contained mixed populations of B. glabrata and B. straminea. Moreover, these habitats also constituted transmission sites for Schistosoma mansoni infection. In 1979 the thiarid snail Thiara ( = Melanoides) tuberculata was discovered in Madame river, Fort-de-France, and in the following years at other sites. In 1983 a programme of biological control using this snail was started in two groups of water-cress beds. In 1981-1982 the study site, Roxelane valley, sheltered important populations of B. glabrata (45-256 individuals/m2) and of B. straminea (2-30 ind./m2). In January 1983 the competitor T. tuberculata was introduced into the two groups of water-cress beds (1.3 and 1.7 ind./m2 respectively) and during subsequent years snail population sampling was carried out. The results showed rapid colonization by the competitor snail, whose densities reached 178 and 325 ind./m2 in November 1983 and a maximum of 9941 and 13,388 ind./m2 in October 1984. During that time, B. glabrata populations declined: 153 and 41 ind./m2 in November 1983, 4 and 0 ind./m2 in October 1984, and 0 ind./m2 in the two groups of water-cress beds in October 1985. A similar phenomenon was observed for B. straminea. Since October 1985 neither planorbid species has been found by exhaustive sampling of the habitats.(ABSTRACT TRUNCATED AT 250 WORDS)
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[Factors responsible for preventing the carrying out of the Schistosoma mansoni cycle in the waters of Grande Terre of Guadeloupe (French Antilles)].
Different surveys which have been conducted in ponds and pools in the Grande Terre of Guadalupe, have demonstrated the absence of Schistosoma mansoni transmission in spite of apparent favourable ecological conditions. Four hypothesises can explain this absence of transmission: 1 - the presence of Biomphalaria glabrata populations non-susceptible to the infestation by S. mansoni. 2 - Ecological conditions unfavourable to the survival of parasitized snails. 3 - Ecological conditions unfavourable to the production, survival and infectivity of the S. mansoni cercariae. 4 - Factors causing the non-contamination of the snails. The results show that the transmission of schistosomiasis mansoni is possible in the ponds and pools of Grande Terre. Only human behaviour is responsible for the absence of actual transmission in the waterbodies of this area. Man breaks the life-cycle of the parasite by avoiding all fecal pollution and therefore all snail contamination.
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[Activities of a Schistosoma mansoni focus of transmission in Martinique (French Antilles)].
A focus of intestinal schistosomiasis was discovered in november 1981 in Martinique in the Saint-Pierre area. An analysis of its structure and of the mecanisms of the transmission of the parasite was carried out between 1981 and 1983. This focus presents the following particularities: a transmission site very small constituted by water cress beds; a small human population infected with a prevalence of 13% (positive stools) to 41,3% (positive serologies); a weak fecal contamination of the water; a non functioning sewage stabilization tank is responsible for this contamination; a rich population of the snail host Biomphalaria glabrata (40,5 to 256,3 Bg/m2) with a low prevalence of infestation (0,13 to 0,59%); low cercarial densities in the water cress bed waters; a very low contamination of the Roxelane river water in to which the water from the water cress beds flows. The epidemiological importance of this contamination has proved very low but not altogether absent. This focus appears as a particular case in Martinique because all the surveys which have been conducted in the island to date has not uncovered a similar example.
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