PAGES: DOI: Full paper
Population Dynamics of Intermediate Snail Hosts of Fasciola hepatica and Some Environmental Factors in San Juan y Martinez Municipality, Cuba

Roberto Cañete, Mary Yong*, Jorge Sánchez*, Lin Wong*, Alfredo Gutiérrez* +

Centro Provincial de Higiene y Epidemiología, Martí No. 159, Pinar del Río, Cuba
*Laboratorio de Malacología, Instituto Pedro Kourí, Apartado 601, Marianao 13, Ciudad Habana, Cuba


The variation of abundances of intermediate snail hosts of Fasciola hepatica in Cuba (Fossaria cubensis and Pseudosuccinea columella) was studied during one year under natural conditions at five sampling sites in San Juan y Martinez municipality, Pinar del Rio province, Cuba. The effect of some environmental variables on the lymnaeid abundances was also studied. A canonical correspondence analysis showed that both species do not generally occur together in the same habitat and that most factors affect them in an opposite fashion, although both of them correlate positively through time to the diversity of the habitats. F. cubensis prefers the sites that are in or closer to the city whereas P. columella is more abundant in rural sites. Lymnaeid abundances are mainly affected by nitrite and nitrate concentrations as well as by the abundance of the thiarid Tarebia graniferaF. cubensis is more abundant in polluted habitats with low densities (or absence) of T. granifera whereas P. columella prefers cleaner habitats and can coexist with the thiarid, even at its higher densities. The implications of divergent preferences of the two lymnaeids for the control of fasciolosis are discussed.

In Cuba fasciolosis is regarded as one of the most important parasitic diseases with both economical, showing high prevalence in cattle (Mauri 1972, Verdecia et al. 2001) and medical significance (Kourí 1948Britoet al.1987, Millanet al.2000). This disease is caused by the liver fluke Fasciola hepatica, which needs a lymnaeid snail as intermediate host to complete its life cycle. Only two lymnaeids are known to be present in Cuba: Fossaria cubensisand Pseudosuccinea columella. Both species can host larvae of the trematode, but only the former has been found naturally infected in the island. Currently, only the curative aspect of the disease is taken into account by a chemotherapy treatment of the final host (Ritchteret al.1999, Millanet al.2000). No integrated program aiming at stopping or at limiting the transmission of the parasite, associating the control of intermediate snail hosts to other control strategies is currently carried out at the national level.

The development of an effective strategy of integrated control, with the precondition of a good knowledge on the epidemiology of this parasitosis requires including, among other things, the study of population dynamics of intermediate hosts and its relation to environmental factors.

This study had as objective to determine the variations of the abundance of F. cubensis and of P. columella as well as their relationship with various factors of the environment such as certain physico-chemical parameters of the water, the snail diversity and the abundance of other snail species.



The field work was carried out in the municipality San Juan y Martinez, located south of Pinar del Rio province. Recently, high cattle infections by F. hepatica were referred in this locality as well as two human cases (which appear in the files of the local center of hygiene and epidemiology). Five sampling sites were selected in various water collections: (A) a culvert of residual waters from houses located close to the dispensary of the city; (B) a site on the river which crosses the city; (C) a drainage canal from a vegetable plantation located in the city; (D) a site on a small river outside the city and close to the small village of El Cañón; and (E) a small pond that originated and is fed by the water of an irrigation system. The sites A, C, and D are in or close to the city, whereas the sites B and E are more rural and with no or a little contact with the local population. Sampling took place once a month during one year (from April 2000 to May 2001)

The species abundance was estimated by collecting snails using a sieve and forceps, always by the same collector during 15 min; the abundance was then measured as the number of snails collected for each 15-min sampling. The snails were carried to the laboratory in plastic boxes and then identified and counted. The following environmental variables were measured: water temperature, pH, total hardness, nitrites, and nitrates. The snail diversity at each sampling was estimated by the index of Shannon and Weaver (H') and its relationship to lymnaeid abundances was determined by a nonparametric correlation analysis (Spearman correlation index).

The relation between environmental variables and species abundances was determined by a canonical correspondence analysis (Ter Braak 1986).



In addition to the two lymnaeids, other snail species were found in the five studied sites: Pomacea poeyanaPhysa cubensisPyrgophorus coronatusCorbicula fluminea, and Tarebia granifera.

The abundances of the two lymnaeids, as well as the diversity index of Shannon-Weaver (H') show irregular fluctuations in all sites (Fig. 1). No season, rain or dry, seems to be more or less favorable for any of these species during the study period.

The results of the canonical correspondence analysis are presented in Table I and Fig. 2. The first three axes explain a 40% of the variance and 90% of the constrained variance. The speciesenvironment correlations are higher than 0.5.

The two lymnaeids occupy opposite quadrants in the three ordination diagrams. The effect of variables like the temperature and total hardness is variable concerning the axis arrangement: in the ordination of axes 1 and 2 as well as of axes 2 and 3 the temperature and total hardness exert a positive influence on P. columella and negative on F. cubensis; in the ordination of axes 1 and 3 the effect is the opposite. The effect of pH, nitrites, and nitrates is always negative on P. columella and positive on F. cubensis, except in the ordination of axes 1 and 3, where the effect of nitrates is null on P. columella and negative on F. cubensis. It is also worth noting the association of F. cubensis with the urban sites A, C, and D, while P. columella is associated with the rural sites B and E, to which the prosobranch T. granifera seems also strongly associated.

The Spearman correlation coefficient between the index of diversity of Shannon-Weaver (H') and the lymnaeids abundances show a positive and significant association for the two species (Table II), yet this relationship is stronger for F. cubensis in the urban sites and for P. columella in the rural sites (data not shown). Curiously, the correlation between the abundances of lymnaeids and those of T. granifera show a positive and significant association for P. columella but negative and significant for F. cubensis. This negative effect of the thiarid on F. cubensis is still present when the same analysis is repeated considering only the urban sites (data not shown).



Of all the environmental factors which associations with lymnaeids were evaluated in this study, the abundances of T. granifera and of lymnaeids themselves show a very strong relationship. The nitrite concentrations and the anthropization of the sampling site are also strongly associated with the abundance of lymnaeids. The effect of pH is also constant for all diagrams but values alternate between 7, 7.5, and 8 and only one sampling had a value of 8.5 (data not shown). Therefore, this variable does not seem to affect lymnaeid abundances in an important way in this study since its range is well within the snail tolerance (Perera 1996). Other factors like the temperature and total hardness seem to play some important role but their association with the variations of lymnaeids' abundance changes from one diagram to another. That is perhaps the consequence of the influence of another more important factor, not measured in this study, such as for example the abundance of aquatic plants (Perera 1996). The variation range of these factors could also be one of the reasons why their association with the lymnaeid abundance was either weak or unstable. It is possible indeed that their concentrations do not reach the thresholds constituting the limiting values for lymnaeids. According to Moens (1981) a closely related species, F. truncatula, can tolerate a very broad spectrum of water physicochemical parameters, which enables it to occur in microhabitats where the fluctuations of these factors are very marked. If the Cuban lymnaeids have similar preferences, the density dependent factors (i.e life-history traits, the impact of the other species, food, etc.), should exert a more important influence on the variations of abundance than the density independent factors (like the physicochemical parameters of water, climate, etc.). According to theoretical studies, chance plays an important role in the variations of a species' abundance in the edges of its distribution area. In the center of its area, when environmental conditions (climate, etc.) are optimal, the regulation of the population by density dependent factors plays a dominant role (Richards 1961).

Mutual exclusion between F. cubensis-P. columella had already been observed by Perera (1996) in some localities of the Isle of Youth, of Santa Clara, and in Lake Hanabanilla. In all the analyses carried out by this author it can be systematically noted a negative correlation between the abundances of the two species, indicating that they rarely occur together in the same habitat. This "dislike for coexistence" was also evident in the present study. Our observations suggest that lymnaeids prefer to coexist with other snail species rather than with the other lymnaeid. An exception is perhaps the association between F. cubensis and T. granifera, where the correlations are always significant and negative.

The negative association of T. granifera with F. cubensis suggests relations of competition there too. This type of relationship was already shown between several species of Thiaridae and various species of pulmonates and these characteristics were exploited in various biological campaigns against the intermediate snail hosts of schistosomes (Perera et al. 1989, 1994, Pointier et al. 1989, Pointier 1983, 1991, 1993, Pointier & Guyard 1992). In Cuba, T. granifera is also a competitor of other prosobranchs like Pomacea paludosa (Gutiérrez et al. 1997). During our study it was observed that T. granifera can displace the majority of other snails, becoming quickly the dominant species when conditions are favorable. Favorable conditions for this thiarid are met in permanent and stable habitats like the sampling sites B and E of this study. On the other hand, the positive association observed between T. granifera and P. columella is surprising and we do not have an explanation to this phenomenon. As a matter of fact, P. columella andC. fluminea are the only species not affected by T. granifera in our study.

The influence of nitrites is negative with F. cubensis but positive with P. columella and this was also the case in the analyses carried out by Perera (1996). Nitrite concentrations are good indicators of the degree of water pollution (Merk 1987) and Perera (1996) points out that F. cubensis shows high densities in sites where contamination of water by domestic or industrial effluents takes place. However, P. columella has been found in habitats with obvious signs of pollution as well, but always in absence (or in the presence of low densities) of F. cubensis (observations not published). These evidences suggest that the effect of interspecific competition is probably more important than the effect exerted by nitrite concentrations.

Another factor of importance associated with the lymnaeid abundance is the proximity of the sites to the city. Indeed, during our study F. cubensis was more frequently collected in more urban (and polluted) sites, whereas P. columellawas more abundant in the rural sites, which evidently showed less signs of pollution. The presence of F. cubensis in the more anthropic sites may be related to a better tolerance of this species for the polluted habitats (Perera 1996).

The larger distribution of F. cubensis in Cuba seems to be related to an older presence of this species in the island. P. columella, however, is presumably of a more recent introduction and have not had the possibility yet of colonizing all the habitats available (Yong 1998). The colonization by F. cubensis of urban habitats confers this species a higher probability of contact with domestic animals, which constitute the main source of F. hepatica eggs. This is possibly the cause of not having yet found any P. columella infected in nature with the parasite in Cuba.

The different ecological preferences observed for the two lymnaeids indicates that strategies for the control of the liver fluke in Cuba should always consider the snail host species present as well as the characteristics of the habitat. Even though no evidence of natural infection has so far been found in P. columella, high infection rates for this species have been observed by us in laboratory exposures. Contrary to F. cubensis,where egg-laying cease before the onset of the cercaria-shedding period in infected snails (Gutiérrez et al. 2001), P. columella can lay eggs even while shedding cercaria (Gutiérrez et al. 2002). In addition, P. columella has been found naturally infected in Brazil and Australia (Ueta 1980, Boray et al. 1985, Oliveira et al. 2002) and its invasive nature has been observed in places like the island of Guadeloupe (Jean P Pointier, pers. commun.). Incorrect control strategies could lead to the colonization of F. hepatica transmission sites by P. columella, resulting in an increase rather than a decrease of the prevalence of the parasite in Cuba.



To Dr André Théron, Dr Jean Pierre Pointier, and two anonymous reviewers for their critical reading of and useful comments to the manuscript.



Boray JC, Fraser GC, Williams JD, Wilson JM 1985. The occurrence of the snail Lymnaea columella on grazing areas in New South Wales and studies on its susceptibility to Fasciola hepaticaAust Vet J 62: 4-6.

Brito E, Olazabal E, Pérez O, Lastre M, Gonzalez R, Pérez R, Gonzalez J 1987. Epidemic human fasciolosis, Cuba 1983. III. Trematode indices. GEN 41: 58-61

Gutiérrez A, Perera G, Yong M, Fernandez J 1997. Relationships of the prosobranch snails Pomacea paludosa,Tarebia granifera and Melanoides tuberculata with the abiotic environment and freshwater snail diversity in the central region of Cuba. Malacol Review 30: 39-44.

Gutiérrez A, Yong M, Wong L, Sanchez J 2001. The combined effect of isolation and Fasciola hepatica infection on the life history traits of Fossaria cubensisJ Invert Pathol 78: 66-71.

Gutiérrez A, Yong M, Perera G, Sanchez J, Theron A 2002. Fasciola hepatica (Trematoda: Digenea): its effect on the life history traits of Pseudosuccinea columella (Gasteropoda: Lymnaeidae) an uncommon interaction. Parasitol Res 88: 535-539.

Kourí P 1948. Diagnóstico, epidemiología y profilaxis de la fasciolosis humana en Cuba. Rev Cuba Med Trop y Parasitol 4: 2-12.

Mauri M 1972. Epizootiología de la Fasciolosis en las Condi-ciones de Cuba, PhD Thesis, Habana, Cuba.

Merk 1987. Manual Test Rápidos, Merk, Darmstadt, Germany, 288 pp.

Millan JC, Mull R, Freise S, Richter J 2000. The efficacy and tolerability of Triclabendazole in Cuban patients with latent and chronic Fasciola hepatica infection. Am J Trop Med Hyg 63: 264-269.

Moens R 1981. Les habitats de Lymnaea truncatula, hote intermediaire de Fasciola hepaticaRevue de l'Agriculture34: 1563-1578.

Oliveira S, Fujii T, Filha E, Martins A 2002. Ocorrencia de Lymnaea columella Say, 1817 infectada naturalmente porFasciola hepatica (Linnaeus, 1758), no Vale do Ribeira, São Paulo, Brasil. Arq Inst Biol São Paulo 69: 29-37

Perera G 1996. Ecologie des Mollusques d'Eau Douce d'Intérêt Médical et Vétérinaire à Cuba, PhD Thesis, Université de Perpignan, France, 105 pp.

Perera G, Yong M, Ferrer JR 1989. Ecology and control of Biomphalaria peregrina in Hanabanilla, Cuba. J Med Appl Malacol 1: 75-81.

Perera G, Yong M, Ferrer JR, Gutiérrez A, Sanchez J 1994. Importancia de Tarebia granifera en el control de una población introducida de Biomphalaria peregrina en Cuba. Rev Cubana Med Trop 46: 20-24.

Pointier JP 1983. La lutte biologique contre les mollusques hôtes intermediaires des bilharzioses à l'aide des mollusques compétiteurs. Symbioses 15: 85-91.

Pointier JP 1991. La lutte biologique contre molusques vecteurs de la schistosomiase intestinale dans la la region caraibe. Rencontre Caraibe en Biologique 58: 225-233.

Pointier JP 1993. 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. Acta Trop 54: 13-18.

Pointier JP, Guyard A 1992. Biological control of the snail intermediate hosts of Schistosoma mansoni in Martinique, French West Indies. Trop Med Parasitol 43: 98-101.

Pointier JP, Guyard A, Mosser A 1989. 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. Ann Trop Med Parasitol 83: 263-269.

Richards O 1961. The theoretical and practical study of natural insect populations. Ann Rev Ent 6: 147-162.

Ritchter J, Freise S, Mull R, Millan J 1999. Fascioliasis: sonographic abnormalities of the biliary tract and evolution after treatment with Tricabendazole. Trop Med Int Health 4: 774-781.

Ter Braak C 1986. Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67: 1167-1179.

Ueta M 1980. Estudo morfométrico da concha de Lymnaea columella Say, 1817 (Mollusca, Gastropoda, Pulmonata).Rev Soc Bras Med Trop 13: 119-141.

Verdecia F, Ramirez W, Antunez G. 2001. Alerta sobre vulnerabilidad por fasciolosis. Revista electronica Granma Ciencia. 5.

Yong M 1998. Biosystématique des Mollusques d'Eau Douce d'Intérêt Médical et Vétérinaire de Cuba, PhD Thesis, Université de Perpignan, France, 104 pp.


Memórias do Instituto Oswaldo Cruz

Av. Brasil 4365, Castelo Mourisco
sala 201, Manguinhos, 21040-900
Rio de Janeiro, RJ, Brazil

Tel.: +55-21-2562-1222

This e-mail address is being protected from spambots. You need JavaScript enabled to view it.



marca fiocruzmarca brasil
marca faperjmarca cnpqmarca capes n marca cope

and diabetes. Erection dysfunction or ED is certainly one of mens most usual problem. It changes buy tadalafil 60mg A common drug is actually an imitation of its manufacturer twin. Both ought to be same in female cialis 20mg Long Phrase Viagra Use Fundamentally Damages Sex Lives This discount cialis canada Equally so, theres something to be said for the wonder of the second, captured forever on picture or a buy cheap cialis People extremely annoyed that they could only get three weeks at a time, Bunker noted. Retired persons cheap pharmacy These types of matters are possibly to being identified as having a result of cancer buy cialis 40mg - Yoghourt - fat-free simply Physical causes: Buying generic medicines now has been cheap generic cialis Herbaceous plants like nigrum and tribulus are well-known for his or her qualities in defeating impotence, which tadalafil 10mg It is not hard to consider Cialis that is generic. Most men start with one-10 mg dosage each purchase cialis Tadalafil quickly gained the moniker of weekender in Paris due to the fabulous results. The bash freaks buy female cialis