Ecology of freshwater snails in south-western Nigeria. I: Distribution and habitat preferences

Dry and rainy season investigations of diverse freshwater habitats in south-western Nigeria revealed fourteen species of snail comprised of nine pulmonates: Biomphalaria pfeifferi Krauss, Bulinus globosus Morelet, Bulinus rohlfsi Clessin, Lymnaea natalensis Krauss, Physa ( Aplexa) waterloti Germain, Bulinus forskali Ehrenberg, Gyraulus costulatus Krauss, Ferrissia sp, Segmentorbis sp. and five prosobranchs namely, Lanistes libycus Morelet, Lanistes ovum Peters, Pila wernei Philippi, Potadoma moerchi Reeve and Melanoides tuberculata Müller.The influence of diverse chemical and physical properties of water on their occurrence as well as interspecific and snail-plant relationships are discussed and maps showing the distribution of the species encountered are presented. Among the intermediate hosts of Schistosoma, B. globosus was widely distributed and common, B. pfeieri was also widely distributed but infrequent and B. rohlfsi was rare.     

Snail predation by larvae of Sepedon scapularis Adams (Diptera: Sciomyzidae), a potential biocontrol agent of snail intermediate hosts of schistosomiasis in South Africa

Malacophagous larvae of the fly Sepedon scapularis Adams were shown experimentally to be effective predators of three species of aquatic pulmonate snails tested as prey: Bulinus africanus (Krauss) an important intermediate host of Schistosoma haematobium (Bilharz), Bulinus tropicus (Krauss) and the invasive species Physa acuta Draparnaud. Survival of S. scapularis larvae from instar to instar was negatively affected by the size of prey snails, since larvae tended to be asphyxiated by the mucous secretions of the snails, or by the larval hydrofuge hairs becoming entangled in snail faeces. In experiments to test the choice of S.scapularis larvae for different species and sizes of snails, B.africanus was significantly disfavoured compared with the other two snail species. Small snails (< 3 mm) were more frequently killed by all three larval instars of S.scapularis. First instars killed few, if any, large snails (> 7 mm), whereas second and third instars preyed effectively on all sizes of snails. Third instars killed significantly more snails than younger instars. For larvae offered only one species of snail as prey, the mean total number of snails killed per larva during its entire development was 49 B.africanus, 45 B.tropicus or 34 P.acuta. It is concluded that S.scapularis is potentially useful as a biological control agent for use against indigenous Bulinus and exotic Physa snails.     

The suitability of several aquatic snails as intermediate hosts for Angiostrongylus cantonensis.

Sixteen species of aquatic snails of four families were tested by quantitative technique under standardized conditions for their suitability as intermediate hosts for Angiostrongylus cantonensis. These species were the planorbid snails Biomphalaria glabrata, Biomphalaria alexandrina, Planorbis planorbis, Planorbis intermixtus, Bulinus truncatus, Bulinus contortus, Bulinus africanus, Bulinus tropicus and Helisoma sp.; the lymnaeid snails Lymnaea natalensis, Lymnaea tomentosa, Lymnaea stagnalis, and Stagnicola elodes; the physid snail Physa acuta (an Egyptian and a German strain) and the ampullariid snails Marisa cornuarietis and Lanistes carinatus. All these snail species proved to be susceptible to infection with A. cantonensis, and first stage larvae reached the infective third stage in all of them. However, the rate and intensity of infection varied with different species. B. glabrata was the most susceptible snail species with a 100% infection rate and an average percentage recovery of third stage larvae of 26.1. This was followed by S. elodes and B. africanus, with a 100% infection rate and an average percentage recovery of third stage larvae of 15.6 and 14.6 respectively. The rest of snail species proved to be less susceptible. For comparative evaluation of the suitability of the various snail species as intermediate hosts of A. cantonensis a "Capacity Index" was determined. This index should provide a useful method for the evaluation of the suitability of various snails as intermediate hosts of nematode parasites under standardized conditions in the laboratory.     

Molecular identification of schistosome intermediate hosts: case studies of Bulinus forskalii group species (Gastropoda: Planorbidae) from Central and East Africa

African freshwater snails of the genus Bulinus act as intermediate hosts for schistosomes, trematode parasites responsible for medical and veterinary forms of schistosomiasis. The relationship between these snails and their parasites is an intricate one, with particular species of snail susceptible to infection only by certain species of schistosome. In common with other self-fertile hermaphrodite gastropods, Bulinus consists of a number of closely related species complexes with restricted gene flow between populations of each taxon. Consequently, despite their medical and veterinary importance as intermediate hosts, unambiguous identification and differentiation of planorbid snails such as these remains problematic, often confounding attempts to define the distribution and evolutionary relationships of conchologically similar taxa. Here we consider how morphological methods of discrimination can be used in conjunction with molecular based approaches to improve snail identification, thereby achieving a better understanding of the epidemiology of schistosomiasis. Data are presented from Central and East African taxa which illustrate how PCR-based methods have begun to be used in combination with traditional analyses in an integrated approach to characterize the genus Bulinus , specifically the B. forskalii species group. Particular emphasis is given to the analyses of Random Amplified Polymorphic DNA (RAPDs) and the mitochondrial gene cytochrome oxidase I (COI).     

Microsatellites in the freshwater snail Bulinus globosus (Gastropoda: Planorbidae) from Zanzibar

Six microsatellite loci were isolated and characterized in Bulinus globosus, a freshwater snail with a wide distribution throughout sub‐Saharan Africa. Bulinus globosus is an intermediate host of Schistosoma haematobium, the causative agent of human urinary schistosomiasis. Microsatellites were tested using 32 snails from four populations collected from Pemba and Unguja islands of Zanzibar. The microsatellite loci displayed relatively low levels of variation, with between two and five alleles per locus. F_ST estimates indicate that gene flow is low, as has previously been suggested for other species of Bulinus.     

A molecular phylogenetic analysis of Bulinus (Gastropoda: Planorbidae) with conserved nuclear genes

Jørgensen, A., Madsen, H., Nalugwa, A., Nyakaana, S., Rollinson, D., Stothard, J. R. & Kristensen, T. K. A molecular phylogenetic analysis of Bulinus (Gastropoda: Planorbidae) with conserved nuclear genes. —Zoologica Scripta, 40, 126–136. Mutational saturation of inspected DNA loci and topological incongruence in the phylogenetic inferences have previously confounded attempts to resolve the evolutionary relationships within the freshwater snail genus Bulinus. Traditionally, the 37 species of Bulinus are placed within the four species groups and the evolutionary divergence between groups is substantial. With an intention to shed new light on species group relationships, the present study was designed to investigate the basal divergences in the phylogeny of Bulinus using highly conserved nuclear genes. The resolved phylogeny inferred that the four species groups of Bulinus were monophyletic and Shimodaira‐Hasegawa topology tests found them to be significantly supported. The Bulinus truncatus/tropicus species complex and Bulinus wrighti (Bulinus reticulatus group) formed a well‐supported sister‐group relationship. The Bulinus africanus species group was the sister‐group to the clade (Bulinus truncatus/tropicus + B. wrighti) with the Bulinus forskalii species group as the sister‐group to these taxa. The sister‐group relationship between Indoplanorbis and Bulinus was non‐significant and the basal clade support of Bulinus improved upon exclusion of Indoplanorbis. The finding of basal long branches of Bulinus species originating from Madagascar strongly suggests the presence of additional cryptic species and an evolutionary scenario influenced by this island’s geological vicariance from the African mainland. Speciation by polyploidy was inferred to have evolved within a clade in the Bulinus truncatus/tropicus species complex. Although the monophyletic status of each species group was firmly supported, it was difficult to establish species group concepts equally across the variations and place this precisely in a specific temporal framework.     

The effect of temperature,darkness, starvation and various food types on growth,survival and reproduction of Helisoma duryi,Biomphalaria alexandrina and Bulinus truncatus (Gastropoda: Planorbidae)

Helisoma duryi has been proposed as a biological control agent in schistosomiasis due to its superiority in laboratory competition experiments with various species of the intermediate host snails. Therefore it was considered important to evaluate the response of this snail species and the intermediate host species, Biomphalaria alexandrina and Bulinus truncatus, to various physical, chemical and biological factors under laboratory conditions in order to obtain information on the similarities in the ecological niches of these species. The factors considered in the present paper are: temperature, darkness, starvation and food. All three species had optimal growth and egg laying at 26–28 °C. Only H. duryi survived for a longer period at 33°C and it was capable of starting egg laying at this temperature although the onset was delayed. However, low temperature (18°C) caused a relatively larger decrease in egg laying of H. duryi than in the other two species. Growth and egg laying was reduced for H. duryi and B. truncatus kept under darkness and B. alexandrina could not tolerate maintenance under darkness. A few days of starvation of juvenile snails had no effect on later growth and egg laying capacity of the survivors, although mortality in B. truncatus was increased. B. alexandrina had a lower tolerance to starvation than the other two species. Egg laying of snails fed only one of the three laboratory food types decreased for all three species in the order: Vov-vov (dog food in dry pellets), Tetramin (fish food) and lettuce. Combinations of lettuce and one or more proteinaceous food types gave optimal growth and egg laying for all three species.     

Species diversity and distribution of schistosome intermediate snail hosts in The Gambia

There is a need for recent information on intermediate snail hosts of schistosomes in The Gambia; the previous studies were conducted over three decades ago. This study assessed the incidence, species diversity, distribution and infection status of schistosome intermediate snail hosts in the country. Malacological surveys were conducted in all 5 regions of The Gambia: Central River Region (CRR), Upper River Region (URR), Western Region (WR), Lower River Region (LRR) and North Bank Region (NBR). Sampling of snails was undertaken at 114 sites that included permanent water bodies such as streams (bolongs), rice fields, irrigation canals and swamps; and temporal (seasonal) laterite pools. Ecological and physicochemical factors of sites were recorded. Snails were identified morphologically and screened for schistosome infections using molecular techniques. Freshwater snails were found at more than 50% (60/114) of sites sampled. While three species of Bulinus were collected, no Biomphalaria snails were found in any of the sites sampled. Of the total 2877 Bulinus snails collected, 75.9% were identified as Bulinus senegalensis, 20.9% as Bulinus forskalii and 3.2% as Bulinus truncatus. Seasonal pools produced the largest number of snails, and CRR was the region with the largest number of snails. Bulinus senegalensis was found more in seasonal pools as opposed to permanent sites, where B. forskalii and B. truncatus were observed to thrive. Bulinus snails were more common in seasonal sites where aquatic vegetation was present. In permanent sites, the abundance of snails increased with increase in water temperature and decrease in water pH. Bulinus senegalensis was found infected with both S. haematobium and S. bovis, while B. forskalii and B. truncatus had only S. bovis infection. While the human parasite S. haematobium was restricted to just four sites, the livestock parasite S. bovis had a much more widespread geographical distribution across both CRR and URR. This new information on the distribution of intermediate snail hosts of schistosomes in The Gambia will be vital for the national schistosomiasis control initiative.     

OBSERVATIONS ON THE POPULATION DYNAMICS OF SNAIL HOSTS FOR SCHISTOSOMES IN THE DELTA OF THE SENEGAL RIVER BASIN

Between 1987 and 1990, snail surveys were carried out in theSenegal River Basin at Lampsar, in a natural ‘marigot’,and at Richard Toll, in an irrigation canal. Lymnaea natalensis.Bulinus guernet^* and B.forskalii, were regularly found at boththe sites. Bulinus globosus/jousseaumei and B. umbilicatus wereonly present at Lampsar. A decrease of the snail density wasobserved during the rainy season at Lampsar. The recent appearanceof Biomphalaria pfeifferi at Richard Toll is discussed. Thedata show that adult B. pfeiffert are present in the main irrigationcanal all through the year. Consequently parasite transmissionwill be possible throughout the year as well. (Received 23 October 1991; accepted 20 May 1992)     

Cercarial shedding patterns of Schistosoma bovis and S. haematobium from single and mixed infections of Bulinus truncatus

The cercarial shedding of Schistosoma bovis and S. haematobium were studied in single and mixed infections in the snail host Bulinus truncatus. The two species displayed a distinctive diurnal cercarial emergence with an earlier shedding pattern for S. bovis than S. haematobium (the average emergence peaks were respectively at 0800 h and 1200 h). In mixed infections, each species kept its own cercarial shedding rhythm with no marked alterations. The cercarial emergence pattern is proposed as a new method to identify natural mixed infections in the snail intermediate hosts. The interactions between the two parasites are discussed.     

The freshwater snail Bulinus tropicus (Planorbidae) in Namibia, characterised according to chromosome number, enzymes and morphology

Freshwater snails collected in central Namibia, south-western Africa, from 15 populations belonging to the Bulinus truncatus/tropicus complex (Planorbidae) are characterised in respect of their chromosome number, morphology, egg proteins and enzymes. The population samples were all consistently diploid and euphallic. The findings are compared with observations on this group of snails in other areas of Africa. It is concluded that the Namibian populations belong to a single species, B. tropicus (Krauss, 1848), of which B. parietalis (Mousson, 1887) is probably a synonym. No evidence was found of any occurrence of the tetraploid species B. truncatus or of snails belonging to the B. africanus group; lack of a potential intermediate host therefore precludes transmission of Schistosoma haematobium in this area.External Scientific Staff of the Medical Research Council of the UK     

Crayfish,catfish and snails: the perils of uncontrolled biological control

A recent proposal that the Australian redclaw crayfish Cherax quadricarinatus and hybrid catfish could potentially control the snail hosts of schistosomiasis has been criticised on the grounds that crayfish pose a severe threat to aquatic ecosystems into which it might be introduced. This note examines the issue further, pointing out that both lack the host-specificity requirement to be a successful biological control agent. The catfish Clarias gariepinus is an omnivore and snails form only a small proportion of its diet; there is no evidence to suggest that it controls snail populations anywhere in Africa. The same applies to other species that have been proposed as biological control agents. Simple laboratory experiments are not an adequate guide to the efficiency of an animal as a biological control agent and detailed ecological investigations would usually demonstrate that few African fish species have this capability.     

Effect of starvation on parasite-induced mortality in a freshwater snail (Potamopyrgus antipodarum)

The level of host exploitation is expected, under theory, to be selected to maximise (subject to constraints) the lifetime reproductive success of the parasite. Here we studied the effect of two castrating trematode species on their intermediate snail host, Potamopyrgus antipodarum. One of the trematode species, Microphallus sp., encysts in the snail host and the encysted larvae “hatch” following ingestion of infected snails by birds. The other species, Notocotylus gippyensis, by contrast, releases swimming larvae; ingestion of the snail host is not required for, and does not aid, transmission to the final host. We isolated field-collected snails for 3 months in the laboratory, and followed the survival of infected and uninfected snails under two conditions: not fed and fed ad libitum. Mortality of the infected hosts was higher than mortality of the uninfected ones, but the response to starvation treatment was parasite species specific. N. gippyensis induced significantly higher mortality in starved snails than did Microphallus. Based on these results, we suggest that host exploitation by different species of trematodes may depend on the type of transmission. Encysting in the snail host may select for a reduced rate of host exploitation so as to increase the probability of transmission to the final host. Received: 29 July 1998 / Accepted: 1 February 1999     

THE EFFECT OF CONSTANT TEMPERATURES ON THE HATCHING OF EGGS AND SURVIVAL OF THE FRESHWATER SNAIL BIOMPHALARIA GLABRATA (SAY)

SUMMARY

The incubation period and percentage hatching of eggs of pigmented and unpigmented Biomphalaria glabrata at constant temperatures were investigated in the range 14 °C to 34 °C. In order to determine the influence of extreme temperatures on adult snails, specimens of the same species were exposed to 0 °C and 40 °C for selected time periods. The results indicate that sustained temperatures below 16 °C and above 32 °C are detrimental to the development and hatching of B. glabrata embryos. The optimum temperatures for incubation period and hatching differ from each other. As far as temperature is concerned, this foreign snail species should be capable of successfully colonizing the warmer parts of southern Africa.     

Host-specific performance and host use in the kleptoparasitic marine snail<Emphasis Type="Italic"> Trichotropis cancellata</Emphasis>

Generalist parasites may disproportionately use certain hosts because of different benefits associated with each host species. I measured the growth rate of the marine snail Trichotropis cancellata, a facultative kleptoparasite that can suspension feed and steal food, on different hosts to determine the relative nutritional benefits of each host. The variation in tentacle (feeding structure) area among the hosts studied had the potential to provide parasitic snails with different amounts of nutrition for growth. In field experiments, suspension-feeding snails isolated from potential hosts grew at a similar rate to snails on brachiopods and significantly more slowly than snails on the following polychaete worms: Serpula columbiana (Serpulidae), Pseudopotamilla ocellata (Sabellidae), Schizobranchia insignis (Sabellidae), and Eudistylia vancouveri (Sabellidae). However, choice among worm hosts affected snail growth rates only in the fall, when phytoplankton levels are low. At this time, snails parasitizing the sabellids Schizobranchia and Eudistylia grew more quickly than snails on Serpula. In the spring and summer, with high levels of phytoplankton, Trichotropis grew at similar rates on all worm species tested. Trichotropis spent approximately the same time stealing food from each worm host species, >50% of the time the worms had their tentacles extended (the difference among hosts was not significant). This finding demonstrates that the similarity of snail growth rates on different worm species is not due to the snails compensating for poor hosts (worms that provide food at a slower rate) by spending more time stealing food. Snails in choice experiments preferred live Serpula to empty Serpula tubes, indicating that at least some of the cue(s) snails use to identify hosts are derived from living host tissues. In choice racks containing live Serpula and live Schizobranchia, snails did not choose one host worm significantly more often than the other. Because Trichotropis grows faster on sabellids than serpulids in the fall, I predicted that snails in nature would infect sabellids more often than other species. However, snails were usually distributed randomly among host species. In the few cases where the snails showed a significant preference among host species, proportionally more snails were found on serpulids than on sabellids or sabellarids. This study is the first to quantify under natural conditions the growth benefits of a kleptoparasite across the range of possible hosts, and implies that factors other than growth rate influence host choice specificity in the marine kleptoparasite T. cancellata.     

Food selection by freshwater snails in the Gezira irrigation canals,Sudan

Stomach content analysis was carried out on samples of the freshwater snail species Biomphalaria pfeifferi, Bulinus truncatus, Bulinus forskalii (Pulmonata, Planorbidae), Lymnaea natalensis (Pulmonata, Lymnaeidae), Melanoides tuberculata, Cleopatra bulimoides (Prosobranchia, Thiaridae) and Lanistes carinatus (Prosobranchia, Ampullariidae) from different irrigation canals in Sudan. In order to evaluate overlap in diet selection among these species, sites with two or more of the above-mentioned species present were selected. For some species food choice was examined in relation to size groupings. In addition, samples of Marisa cornuarietis (Prosobranchia, Ampullariidae) from small ponds in Sudan, samples of Biomphalaria pfeifferi and Helisoma duryi (Pulmonata, Planorbidae) from drainage canals in an irrigation scheme in northern Tanzania, and samples of H. duryi from fish ponds in the coastal area of Kenya were also analysed. The results indicate a great similarity in the food choice of these species, especially among the pulmonate species. All species feed on fine detritus, epiphytic algae and decaying macrophytes. No fresh fragments of aquatic macrophytes were found and animal remains were found only on a few occasions. However, the stomach contents of the ampullarid species were characterized by large fragments of dead macrophyte tissue, while the composition of the finer particles showed a great resemblance to that of the pulmonate species. The diet of the thiarid species is essentially the same as that of the pulmonate species, although in one site Cleopatra bulimoides showed a greater preference for green algae. Apart from the avoidance of blue-green algae, there was little evidence of selection of certain algal components of the Aufwuchs for the pulmonate species. Detritus constitutes the major component of the stomach content of all these snail species.     

The life-cycle,ecology and host specificity of the freshwater leech Alboglossiphonia polypompholyx (Glossiphoniidae) in Egypt

Alboglossiphonia polypompholyx spends most of its life cycle endoparasitic in the mantle cavity of the snail Bulinus truncatus — possibly its only host. Adult A. polypompholyx leaves the snail about one month before the commencement of egg-laying. Hatching occurred after about 15 d and after brooding on the venter of the parent for 7–10 d, the young briefly become free-living before entering the mantle cavity of B. truncatus. Within the mantle cavity, A. polypompholyx feeds and grows for 16–20 weeks before leaving the snail as adults. In the field and in laboratory experiments, adult leeches left the snails in August/September and January with cocoons produced in October/November and February/March, respectively. Free-living adult leeches do not feed and die 1–2 months after the cessation of brooding.     

Four trematode cercariae from the New Zealand intertidal snail Zeacumantus subcarinatus (Batillariidae)

Abstract

The cercariae and sporocysts (or rediae) of four trematode species are described from the intertidal snail Zeacumantus subcarinatus: a distome xiphidiocercaria assigned to the genus Renicola (family Renicolidae); a monostome xiphidiocercaria belonging either to the genus Microphallus or Megalophallus (family Microphallidae); a magnacercous cercaria of the genus Galactosomum (family Hetero‐phyidae); and a cercaria of the genus Philophthalmus (family Philophthalmidae). The morphological features of these cercariae are compared to previously described cercariae of the same genera. In addition, since the philophthalmid cercaria encysts readily on artificial substrates in the laboratory, the metacercaria of this species is also described. These cercariae are part of a diverse community of at least six digenean species parasitising the snail Z. subcarinatus that, together, have a major impact on the ecology and evolution of this snail.     

Aquatic snails of the Bulinus africanus group in Zambia identified according to morphometry and enzymes

The Bulinus africanus species group (Planorbidae) of freshwater snails has been reported to be represented in Zambia by two species, B. africanus (Krauss) and B. globosus (Morelet), both named as intermediate hosts for Schistosoma haematobium. Uncertainty in identification of these snails from morphology led to the present investigation, combining morphometry (shell and copulatory organ) with enzyme analysis. Observations of both kinds were made usually on the same individual snails, from collecting sites mostly in the Lusaka area or at Lake Kariba. Particular attention was given to the proportional relationship between the penis sheath and the preputium of the copulatory organ, a character used previously to distinguish B. africanus from B. globosus in south-eastern Africa. The enzyme profile MDH-1, AcP-2, PGD-1 and PGM-2 was common to all snails examined from 25 populations; GPI and HBDH were polymorphic. The enzyme data indicate that the samples represent a single species. Shell characters varied continuously. The copulatory organ was generally of the form known for B. globosus. Although the copulatory organ of a few individuals had proportions overlapping the range reported for B. africanus, the present variation was continuous and was not bimodal. It is concluded that all these specimens are conspecific and may be identified as B. globosus. Previous identifications of B. africanus from Zambia appear to need substantiation and it seems that if this species is present at all in the sampled areas, it must be uncommon. It is relevant in regard to possible strain differences within S. haematobium in Zambia, that our observations indicate that only a single species of intermediate host is involved in transmission.     

Spatio-Temporal Distribution of Freshwater Snail Species in Relation to Migration and Environmental Factors in an Irrigated Area from Morocco

Nine sites were sampled 19 times over 2 years in an irrigation system in Morocco in order to study species abundance in a snail community in relation to environmental parameters (including human activities) and migration (geographic distance) among sites. Each site was made of a sink and the first meters of the downstream canal. The snail community included four species (Bulinus truncatus, Lymnaea truncatula, Mercuria similis and Physa acuta). Strong spatial variation in species occurrence and abundance was detected which might be partly due to variation in water availability. However abundance in sinks and canals in which water availability differs were correlated. There was, as predicted, limited evidence in favor of isolation by distance which might be due to fast water current. Dispersal might therefore be an important factor structuring this community. On the other hand, the temporal variation was much more limited. This is consistent with the analysis of individual size distributions in B. truncatus, since no clear-cut cohorts were detected. The environmental parameters recorded (e.g. temperature, occurrence of macrophytes or cleaning of sinks) were extremely variable in time and space, except temperature. Analyzing their association with species through multidimensional methods indicated that P. acuta is ubiquitous and B. truncatus positively associated with macrophytes. These two species were associated in sinks. Less clear trends were detected for the two other species. Annual cleaning of sinks affected all species, but population recovery was fast in B. truncatus and P. acuta.