An investigation of the interactions of some factors influencing the infectivity of Schistosoma mansoni miracidia to Biomphalaria glabrata

Sturrock R. F. and Upatham E. S. 1973. An investigation of the interactions of some factors influencing the infectivity of Schistosoma mansoni miracidia to Biomphalaria glabrata. International Journal for Parasitology3: 35–41. A 3³ replicated factorial experiment showed that there were significant first-order interactions between the effects of turbidity, salinity and pH on the infectivity of Schistosoma mansoni miracidia to Biomphalaria glabrata. The main factor effects resembled those obtained when the factors were studied individually. There was a negative regression of infection rate on the logarithm of the level of both turbidity and salinity, and a curvilinear regression on pH, with a peak between 7 and 8. However, as the main factors only accounted for little over half of the observed variance, the interactions are extremely important and greatly reduce the chance of a miracidium infecting a snail. These findings are relevant to natural transmission sites in endemic areas and also suggest that quite minor variations in other factors may enhance the adverse effect of increased salinity on transmission in estuaries, and thus minimize the importance of such areas in the epidemiology of the parasite.     

Field studies on the population dynamics of Biomphalaria glabrata, intermediate host of Schistosoma mansoni on the West Indian Island of St. Lucia

Growth curves, calculated for field populations of B. glabrata, were not materially affected by habitat, altitude or season. A mean growth curve was therefore used to estimate the age-frequency distribution of snails in successive field samples. These data permitted the construction of ecological life tables and the estimation of r, the intrinsic rate of natural increase (or decrease) of the different populations. The calculated values of r were inserted in a simple model of unlimited population growth but the resultant curves poorly represented the observed data. A model for unlimited growth was more satisfactory for pond and marsh populations but, apparently, immigration made it less satisfactory for stream and banana drain populations. Nevertheless, r may still be of value in predicting repopulation rates in certain habitats after a mollusciciding which does not kill the entire snail population.     

Effects of environmental calcium on fecundity and cercarial production of Biomphalaria glabrata (Say) infected with Schistosoma mansoni Sambon

Biomphalaria glabrata were reared in stock culture and subjected to either 7-day or 60-day acclimation periods in complex CaCO3 media with calcium values ranging from 1.5 mg/L to 75 mg/L. Following 60-day acclimation, snails from series I were each exposed to 8 miracidia of Schistosoma mansoni. Snails of series II were each exposed to a single miracidium. Snails of both experimental regimens were observed for mortality, growth, rate of infection, and number of cercariae shed. Series I snails were also monitored for fecundity during acclimation and following miracidial exposure. Calcium levels of 1.5 and 75 mg/L resulted in significant snail mortality. Shell growth and rates of infection were positively correlated with calcium maintenance level. Snails with high fecundity prior to miracidial exposure subsequently shed more cercariae. In contrast, post-exposure (PE) fecundity of snails reared in media with up to 30 mg/L Ca++ were negatively correlated with calcium level, infection rate, and number of cercariae shed. Maximal cercarial emergence occurred at 30 mg/L Ca++. These results suggest that environmental calcium affects both the distribution patterns of snail hosts of human schistosomes and the productivity of intramolluscan schistosome infection.     

Location of Biomphalaria pfeifferi by Schistosoma mansoni miracidia in stagnant and running water under field conditions

The efficiency of S. mansoni miracidia in locating and infecting Biomphalaria pfeifferi in Gezira canals has been studied under field conditions. When S. mansoni eggs were introduced into clean stagnant water in small field channels, the miracidia hatched to infect 100% of 30 snails in cages at the release point. Fifteen metres upstream and downstream 13% of caged snails were infected but no infections were found in snails 20 m away.When eggs were released into the same canal in flowing water (8.3 cm · s^–1), no infections were detected in any of the caged snails placed 0–100 m downstream. Releasing hatched miracidia instead of eggs resulted in infections in all cages at 5 m intervals from 0-100 m. The release of eggs into flowing water was likened to the method by which S. haematobium eggs are deposited during urination. The 0% infection suggests that eggs will be swept away from the point of contamination by the flow. Thus only urination into stagnant water will lead to heavy snail infection rates.When eggs were released into a small pond-like minor canal tail end snail infection rates were only 3%. This was probably due to the larger water volume, smaller number of caged snails, and the presence of vegetation and other fauna which may be decoys or predators.The results highlight how very high snail infection rates can be produced under ideal conditions but also show how large snail and miracidia numbers are required in natural situations.     

Field studies on the transmission of Schistosoma mansoni and on the bionomics of its intermediate host, Biomphalaria glabrata, on St. Lucia, West Indies

Schistosoma mansoni is transmitted by the snail Biomphalaria glabrata on the West Indian island of St. Lucia. A 2$\text{1}\text{2}$-year study of natural snail populations is reported together with simultaneous observations on the transmission of the parasite. Populations in static habitats (pools, marshes and lateral banana drains) were maximal during the rainy part of the year (June–December) but declined during dry spells between January and May. Low infection rates (< 1 %) were observed sporadically in these populations. Higher, more persistent infection rates (5–15%) were obtained in flowing habitat populations (streams and main banana drains) which, however, only became established in periods of low rainfall. The importance of seasonal transmission through flowing habitat colonies was borne out by mouse exposures, supplementary snail studies and human incidence data which between them also gave an insight into the dynamics of transmission. These findings have been used to design a mollusciciding programme as one of several methods of controlling transmission currently being evaluated on St. Lucia.     

Effects of the desiccation on Biomphalaria tenagophila (Orbigny, 1835) (Mollusca) infected by Schistosoma mansoni Sambon, 1907

Specimens of Biomphalaria tenagophila exposed to miracidia of Schistosoma mansoni were submitted to different desiccation periods as follows: group I: 24 h after exposure, desiccated for 28 days; group II: after cercariae elimination, desiccated for 7 days; group III: 21 days after exposure, desiccated for 7 days; group IV: 14 days after exposure, desiccated for 14 days; group V: 7 days after exposure, desiccated for 21 days. From the obtained data it was verified that desiccation was not capable of interrupting the development of larvae of S. mansoni in mollusks. A delay in the development of S. mansoni larvae in groups I, III, IV and V was observed. A pause was verified in the development of S. mansoni larvae in groups II, III, IV and V. Some larvae, in groups I, III, IV and V, did not suffer as a result of desiccation and continued their development. Larvae in the cercariae stage were shown to be more sensitive to desiccation. It was possible to obtain clearing of mollusks infected by sporocysts II and cercariae using a period of 7 days of desiccation.     

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.     

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.     

Influence of Echinostoma paraensei (Lie and Basch, 1967) infection on the calcium content in Biomphalaria glabrata (Say, 1818)

The calcium content in the hemolymph and shell of Biomphalaria glabrata (Say, 1818) was determined after exposure to different parasite burdens (5 and 50 miracidia) of Echinostoma paraensei (Lie and Basch, 1967). The snails were dissected 1, 2, 3, and 4 weeks after infection to collect the hemolymph and shell. An increase in calcemia was observed in snails infected with both miracidial doses. A significant decrease in the calcium ions in the shell was observed, coinciding with the calcemia peak in the hemolymph. This indicates greater mobilization of calcium between the shell and hemolymph to regulate the calcium content in the body when the snail is exposed to stress conditions, as has also been observed in some other infected snail species. The results obtained indicate that in this model, the calcium metabolism depends on the miracidial dose used.     

Malacological assessment and natural infestation of Biomphalaria straminea (Dunker, 1848) by Schistosoma mansoni (Sambon, 1907) And Chaetogaster limnaei (K. Von Baer, 1827) in an urban eutrophic watershed.

The objective of this study was to perform a malacological assessment at the Ibirité reservoir watershed in the metropolitan region of Belo Horizonte (Minas Gerais) and to evaluate the natural infestation rate of Biomphalaria straminea (Gastropoda: Planorbidae) by Schistosoma mansoni (Platyhelminthes: Trematoda) and Chaetogaster limnaei (Oligochaeta: Naididae). The samples were collected from July to August 2002. The B. straminea individuals collected were kept in the laboratory; the natural infestation rate by S. mansoni and C. limnaei was assessed weekly. The malacological assessment identified five mollusk species present in the Ibirité reservoir watershed: B. straminea, Physa marmorata, Lymnea sp., Melanoides tuberculatus, and Pomacea austrum. Laboratory observations showed that the B. straminea individuals were infected by C. limnaei rather than S. mansoni. Although there was no infection of B. straminea by S. mansoni, presence of B. straminea in itself merits close attention due to possible risk of human schistosomiasis by the local population.     

Studies of the relationship between Schistosoma and their intermediate hosts. III. The genus Biomphalaria and Schistosoma mansoni from Egypt, Kenya, Sudan, Uganda, West Indies (St. Lucia) and Zaire (two different strains: Katanga and Kinshasa)

The compatibility between strains of Schistosoma mansoni from Egypt, Kenya, Sudan, Uganda, the West Indies, and Zaire (two strains which came from Katanga and from Kinshasa), and various species and strains of Biomphalaria, i.e. Biomphalaria pfeifferi, B. alexandrina, B. glabrata and B. camerunensis was investigated. Data as mortality, rate of infection of the surviving snails, duration of infection, cercarial production per day per positive snail, etc., were observed. The main emphasis was placed on determining the total cercarial production per 100 exposed snails for each snail population. It was possible to infect all the tested populations of B pfeifferi with the various strains of S. mansoni, but the observation as e.g. TCP/100 exposed snails varied greatly according to the population of snail and the strain of S. mansoni. The results for the remaining species of Biomphalaria varied greatly, depending on the combination, e.g. B. alexandrina was only susceptible to the local S. mansoni from Egypt. The highest TCP/100 exposed snails was more than 1 million for the strains of S. mansoni from Egypt, Kenya and the West Indies in B. alexandrina, B. pfeifferi and B. glabrata, respectively. The next group, with a TCP/100 exposed snails on 7--800 000 consists of S. mansoni from Sudan, Uganda and Zaire (Katanga) all in B. pfeifferi. The last tested strain of S. mansoni, Zaire (Kinshasa) yielded a cercarial production on 500 000 per 100 exposed snails in B. pfeifferi and B. camerunensis. The shortest prepatent period, 19 days, was observed for S. mansoni from Kinshasa, Zaire, in B. camerunensis, and the longest prepatent period, 25 days, was found for strains from Egypt and from the West Indies in B. alexandrina and B. glabrata, respectively. In general, a very long duration of infection, lasting up to 200 days, was observed.     

Phylogeography of Biomphalaria glabrata and B. pfeifferi, important intermediate hosts of Schistosoma mansoni in the New and Old World tropics

The historical phylogeography of the two most important intermediate host species of the human blood fluke Schistosoma mansoni, B. glabrata in the New World, and B. pfeifferi in the Old World, was investigated using partial 16S and ND1 sequences from the mitochondrial genome. Nuclear sequences of an actin intron and internal transcribed spacer (ITS)-1 were also obtained, but they were uninformative for the relationships among populations. Phylogenetic analyses based on mtDNA revealed six well-differentiated clades within B. glabrata: the Greater Antilles, Venezuela and the Lesser Antilles, and four geographically overlapping Brazilian clades. Application of a Biomphalaria-specific mutation rate gives an estimate of the early Pleistocene for their divergence. The Brazilian clades were inferred to be the result of fragmentation, due possibly to climate oscillations, with subsequent range expansion producing the overlapping ranges. Within the Venezuela and Lesser Antilles clade, lineages from each of these areas were estimated to have separated approximately 740 000 years ago. Compared to B. glabrata, mitochondrial sequences of B. pfeifferi are about 4x lower in diversity, reflecting a much younger age for the species, with the most recent common ancestor of all haplotypes estimated to have existed 880 000 years ago. The oldest B. pfeifferi haplotypes occurred in southern Africa, suggesting it may have been a refugium during dry periods. A recent range expansion was inferred for eastern Africa less than 100 000 years ago. Several putative species and subspecies, B. arabica, B. gaudi, B. rhodesiensis and B. stanleyi, are shown to be undifferentiated from other B. pfeifferi populations.