Snails by their habitat could be grouped into two: aquatic and terrestrial. However, terrestrial snails are mostly found in wet and damp areas. Both aquatic and terrestrial snails are hosts to a range of parasites (Caron et al., 2014; Opisa et al., 2011; Betterton et al., 1988).
Snail consumption rate is rising because people are now avoiding red meat for perceived health reasons (Omole et. al., 2006). Snail meat offers the entire amino acid requirement in man (Adeyeye, 1996) with relatively high iron content and low fat (Agbogidi et al., 2008). Many of the snails consumed in Nigeria are sourced from the wild, only few are reared; hence, wild snail population have considerably declined. In addition, deforestation, pesticide use and bushfires have further reduced the number of snails (Esak & Takerhash, 1992).
Snail consumption could be one route to human infection particularly when eaten raw or undercooked. The African giant snail of Achatina achatina, A. fulica, Achachatina marginata with Limicolaria spp are the common edible land snails in Nigeria (Fagbuaro et al., 2006). A recent report has shown the susceptibility of the African giant snail to rat lungworm parasite (Angiostrongylus cantonensis) (Iwanowicz et al., 2015) with the increasing risk of transmission to man and animals (Alica 1966; Reece et al. 2013).
In spite of this, the identification of parasites of edible land snails including its prevalence is yet to be documented for Nigeria. We thus present baseline data on the different land snails collected in Edo State and the parasites they harbour. The implications of these results are also discussed.
Materials and Methods
Edo (6°30’N 6°00’E) is an inland state in southern Nigeria. It has a tropical climate characterised by two seasons, wet (April to October) and dry (November to March). In the north, the area is derived savanna, while in the south, it is a forest region. The riverine communities in the south have mainly mangrove swamp vegetation. Agriculture is the predominant occupation. The major cash crops are rubber, cocoa and oil palm. Four locations (Benin, Uromi, Ekpoma and Auchi) were surveyed and these are the major towns in the state (see Fig. 1).
Sizable snails that have largely developed to full maturity were handpicked in the wild (farm land, bushes and around homes) on soil, leaves, on the trunk of trees, and on wall-fences of homes across all study areas. Snail-scouting was simultaneously carried out by our team and the locals and therefore only this number (272) were collected and processed by our team. Collection in the rainy season was done twice in a week for four months between May and August of 2015; while in the dry season, collections were in three months (December 2015 to February 2016). In the dry season, few snails were seen and collected in the farms and surrounding bushes.
Snail identification and dissection
Snails were identified according to their shape, size, markings, colour, spire angle, sculpture and aperture form (Bequaert, 1950; Raut & Barker, 2002). Dissections to separate some organs (mucus gland, digestive gland, intestine, stomach, crop and ovotestis) were done using standard procedures. These organs and ‘others’ were separately processed to detect parasite.
Three methods [direct method (wet mount preparation), floatation technique (saturated salt solution) and concentration technique using formol-ether (Cheesbrough, 2006)] were used to process each snail sample in order to ensure that false negatives were not recorded. Samples were viewed under the microscope (AXL (3180976) Labo Germany) and parasites seen were identified and quantified.
In the rainy season months, a total of 272 large edible snails were collected and examined across locations. More than half of the snails (54.04 %) were positive to at least a species of parasite. The larvae of Strongyloides stercolaris were the most prevalent (Table 1). A few snails were positive of other parasites.
Prevalence of infected snails by location
|Location||No. examined||No. and % infected||No. and % infected with S. stercoralis||No. and % infected with Alaria spp.||No. and % infected with F. gigantica||No. and % infected with A. cantonesis||No. and % infected with D. dendriticum||No. and % infected with S. mansoni|
A total of six snail species were collected in the rainy season months (Archatina achatina, A. fulica, Achachatina.marginata, Limicolaria aurora, L. flammea and Limicolariopsis spp. Limicolariopsis were seen only in Ekpoma while others were collected in all surveyed areas. Six parasites (S. stercoralis, Alaria spp., Fasciola gigantica, Angiostrongylus cantonensis, Drocoelium dendtriticum and Schistosoma mansoni) were recovered in these snails. Four different parasites were isolated from A. fulica, three from L. flammea, while two each from L. aurora and Limicolariopsis spp. (Table 2). Generally, snails with other parasites were co-infected with S. stercoralis. Multiple infections were seen in A. fulica (1 snail) and L. flammea (1 snail).
Prevalence of snail infection with parasite
|No. examined||No. and % infected||No. and % infected with larvae of S. stercoralis||No. and % infected with mesocercaria of Alaria spp||No. and % infected with sporocyst of F. gigantica||No. and % infected with larvae of A.cantonesis||No. and % infected with Cercariae of D. dendriticum||No. and % infected with sporocyst of S. mansoni|
|A, achatina||48||28 (58.33)||28 (100)||-||-||-||-||-|
|A. fulica||41||28 (68.29)||28 (100)||-||7(17.07)||7(17.07)||-||2(7.14)|
|A. marginata||42||19 (45.23)||19 (100)||-||-||-||-||-|
|L. aurora||48||39 (81.25)||39 (100)||1(3.44)||-||-||-||-|
|L. flammea||73||49 (67.12)||49 (100)||2(4.08)||-||-||2 (4.08)||-|
|Limicolariopsis||20||10 (50)||10 (100)||1(10)||-||-||-||-|
Of the organs (mucus gland, digestive gland, intestine, stomach, crop, ovotestis) examined for the presence of parasite, three (mucus gland, digestive gland and intestine) were positive (Table 3). Motile larvae of S. stercoralis were seen in all positive organs [65 % were L2, others were either L1 (20 %) or L3 (15 %)], while sporocysts of F. gigantica and S. mansoni were recovered only in the intestine. Additionally, motile larvae of D. dendtriticum were isolated in the intestine. Some parasites were recovered in the faeces (Table 3).
Parasite isolation in organs and faeces of snail
|Mucus gland||Digestive gland||Intestine||Crop||Stomach||Ovotestis|
|A.achatina||S. stercoralis||-||S. stercoralis||-||-||-||S. stercoralis||S. stercoralis|
|A. fulica||S. stercoralis||S. stercoralis||F. gigantica; A. cantonesis; S. mansonia||-||-||-||S. stercoralis||S. stercoralis; F. gigantica|
|A. marginata||S. stercoralis||-||S. stercoralis||-||-||-||S, stercoralis||S. stercoralis|
|L. aurora||S. stercoralis; Alaria spp.||-||S. stercoloralis||-||-||-||S. stercoralis||S. stercoralis|
|L. flammae||S. stercoralis; Alaria spp.||D. dendtriticum||S. stercoralis; Alaria spp; D. dentriticum||-||-||-||S. stercoralis||S. stercoralis; Alaria spp|
|Limicolariopsis||S. stercoralis||-||Alaria spp.||-||-||-||S. stercoralis||S. stercoralis|
The mean parasite load for S. stercoralis being pooled from all examined organs and faeces within the host were as follows: A. achatina (16 parasites/5 ml), A. marginata (18 parasites/5 ml), A. fulica (25 parasites/5 ml), L. flammea (6 parasites/5 ml), L. aurora (7 parasites/5 ml), Limicoriopsis (5 parasites/5 ml). Other parasites were relatively scanty (2 – 4 parasites/5 ml).
In the dry season months, a total number of 91 snails [A. archatina (31), A. fulica (21), A. maginata (18), L. aurora (12) and Limicolariopsis (9)] were collected. Among these, one or two snails from the various snail species, harboured non-motile larva of S. stercoralis with this mean load (0.1parasite/ml) for each species examined. Other parasites that were isolated in rainy season snails were not seen in the dry season.
Soil-transmitted helminth infections are found mainly in areas with warm and moist climates where sanitation and hygiene are poor. Snails are found on soil either scavenging for food or for purposes of reproduction; thus snails could get infected with parasites in the process. Strongyloides stercoralis being a soil parasite was the most isolated in snails. This could be attributed to its abundance in the soil coupled with its ability to easily locate snail host from the chemicals they possibly exude (Safer et al., 2007). Strongyloides stercoralis by its morphological feature could readily penetrate snail foot or any exposed area and infect the visceral organs. Geohelminths such as hookworm, Enterobious vermicularis, Ascaris lumbricoides which are also common soil parasites in these areas (Omorodion et al., 2012; Nmorsi et al., 2009) were not seen to infect snails. Hence, the adaptability of S. stercoralis as the major parasites of these land snails needs further investigation.
Another nematode, A. cantonensis larvae were seen only in A. fulica. This nematode has been isolated in giant African land snails elsewhere (Kim et al., 2014; Iwanowicz et al., 2015). Angiostrongylus cantonensis is a common parasite of rats and the cause of the emerging infectious neurologic rat lungworm disease (Jarvi et al. 2012). We thus incriminate A. fulica as the likely intermediate host of A. canonensis. Humans are at risk of the consequences of A. cantonensis infection particularly when infective larvae are ingested (Cross, 1987; Heyneman and Lim, 1967). In human-infected cases, most damages are seen in the intestinal walls resulting in abdominal pain and fever (Graeff-Teixeira et al., 1991). Eosinophilic meningoencephalitis has been reported in both man and animals (Morassutti et al., 2014).
Alaria parasites were isolated from some of the snails. The definitive host of Alaria fluke are dogs and cats, while the known intermediate hosts are fresh water snails (helisomid) and frogs. In helisomid snails, sporocyst develop into cercariae (Nithiuthai et al., 2004) and then released to actively penetrate the second intermediate host (tadpoles) which then develop to infective mesocercariae. Mesocercariae accumulate and may be ingested by a number of paratenic hosts (e.g., other frogs, snakes) or directly by the definitive host. Among the species of terrestrial snails examined, only Limicolaria spp and Limicolariopsis snails harboured the mesocercariae of Alaria parasite. It could therefore be that these species of snails are intermediate hosts. Further investigation on this is however required to clearly define the role of these snails within the context of parasite development and disease transmission. In any case, human infection has been reported after the consumption of Alaria-infected host (Otranto and Eberhard, 2011). Species of the freshwater snails from the family Lymnaeidae are well known for their roles as intermediate hosts in the life cycle of F. gigantica. However, an increasing number of other molluscan intermediate hosts of F. gigantica have been reported (Soliman, 2008). In this study, A. fulica harboured the widest range of parasites among the snail species collected; two of which are F. gigantica and S. mansoni. In Venezuela, A. fulica reportedly harboured S. mansoni (Libora et al. 2010). Fascioliosis is a disease of herbivorous animals while S. mansoni causes intestinal schistosomiasis in man (Crompton, 1999). Results indicate that only the sporocysts of these parasites were seen. It is likely that the conditions within the host (A. fulica) did not support further development.
The only land snail species positive of D. dendtriticum was L. flammea. Limicolaria flammea is native to Nigeria with oil palm and cocoa plantation their most preferred habitats (Tan and Clements, 2011). The parasite D. dendtriticum have two intermediate hosts (land snails and ants) and the sexually mature is often seen in the bile ducts of sheep, goats and pigs. We suggest that this snail could be the most likely intermediate host owing to the fact that cercariae were recovered in the digestive gland and intestine. The cercariae leave the snail to the environment, and are then picked up by ants within which it develops into the metacecariae.
In conclusion, this study enriches existing data regarding the role of land snails as likely intermediate hosts to a number of parasites. It also identified S. stercoralis as the most prevalent parasites of land snails. Also, the risk of eating undercooked snails with respect to human and animal health is thus affirmed.
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