Ann. Limnol. - Int. J. Lim. 46 (2010) 191–197 Available online at: Ó EDP Sciences, 2010 www.limnology-journal.org DOI: 10.1051/limn/2010014 Omphiscola glabra (Gastropoda, Lymnaeidae): Changes occurring in natural infections with Fasciola hepatica and Paramphistomum daubneyi when this snail species is introduced into new areas Gilles Dreyfuss*, Philippe Vignoles and Daniel Rondelaud UPRES EA nx 3174, Faculties of Medicine and Pharmacy, 87025 Limoges, France Received 22 February 2010; Accepted 11 May 2010 Abstract – Cross-transplantations of Omphiscola glabra between two French departments (Haute-Vienne and Indre) were carried out to study snail settlement in these new sites during six years and to determine if this snail species was well adapted to its local parasites (Fasciola hepatica and Paramphistomum daubneyi). Local snails placed in new sites for each department were used as controls. In Indre furrows, the number of adults per population and the area of each habitat peaked on the third year post-introduction. Similar findings were also noted in the Haute-Vienne furrows occupied by local snails but peaks were only observed on the fourth year. In contrast, in Haute-Vienne sites populated by introduced snails, there was a progressive decrease in snail abundance and habitat area from the second year. The local O. glabra transplanted in Haute- Vienne kept their same degree de susceptibility to F. hepatica and P. daubneyi, thus demonstrating a good adaptation of these snails to their parasites. In other groups of transplanted snails, the first natural infections were only noted from the second or third year post-introduction and their prevalence progressively increased over time. Local adaptation of these latter snails to parasites would be more progressive in time and would stretch over several snail generations. Key words: Calcium / Fasciola hepatica / Galba truncatula / natural infection / Omphiscola glabra / Paramphistomum daubneyi / snail settlement Introduction Spanish and Moroccan isolates of F. hepatica were more infective to French populations of G. truncatula than mir- According to the Red Queen hypothesis, parasites acidial isolates originating from central France (Gasnier should be better at infecting sympatric (local) populations et al., 2000; Goumghar et al., 2001). An explanation to of snails than allopatric host populations (Lively and interpret this set of conflicting results may be the change Dybdahl, 2000). Among the diverse investigations re- which had occurred in the infectivity of F. hepatica ported in the literature, parasites have been found to be miracidia from the 2000s. According to Dreyfuss et al. more infective to their sympatric hosts in several systems (2007), miracidia originating from triclabendazole-treated (Lively et al., 2004; Mun˜ oz-Antoli et al., 2010), thus cattle had a greater infectivity to their snail host than demonstrating local adaptation between both partners. miracidia coming from ruminants treated with broad- However, this hypothesis was not verified in other snail- spectrum anthelminthics. parasite systems (e.g. Prugnolle et al., 2006). This variable Contrary to parasites which had been more studied nature of results was also found in the Galba truncatula- before 2002, the transplantation of snails from a given area Fasciola hepatica system. If local adaptation between these in another area was not still very used to verify the partners was verified in the field (Abrous et al., 1999, 2000) occurrence of local adaptation hypothesis in a snail- and even during the larval development of F. hepatica parasite system. Nevertheless, this technique is interesting within its snail host (Belfaiza et al., 2005), other experi- because of the possibility of subjecting snail populations ments performed by our team have demonstrated that diversely susceptible or resistant to a digenean to another natural parasitic pressure exerted by the definitive host. *Corresponding author: [email protected] Since 2003, this technique was used in a field experiment Article published by EDP Sciences 192 G. Dreyfuss et al.: Ann. Limnol. - Int. J. Lim. 46 (2010) 191–197 to answer the following three questions: Did F. hepatica- susceptible snails keep the same degree of susceptibility when they were locally introduced into new sites located in the same district as the population of origin? Did this susceptibility change if these snails were placed in another district differing by geology and, as a consequence, by parasitological profile? If snail samples little susceptible to F. hepatica were introduced into a district where highly susceptible populations of belonging to the same species were living, did the susceptibility of the former snails increase in time? Cross-transplantations of snails were thus made in 2003 and were followed during six years to study their settlement into new sites and changes occurring in their susceptibility to natural infections with F. hepatica. To verify these results, local transplantations of snails (controls) were also performed by placing them in new sites located in the same district. Materials and methods Lymnaeid species and French departments chosen for this study As G. truncatula is the main snail host of F. hepatica in central France (Rondelaud et al., 2009), the lymnaeid chosen was a close related species: Omphiscola glabra. Natural infections of this latter snail with F. hepatica and/or another digenean, Paramphistomum daubneyi were reported from the 2000s by several authors (Mage et al., Fig. 1. Geographic location of study areas in central France. Each figure (in italics) indicates the number of meadows used for 2002; Dreyfuss et al., 2003, 2005) on the acid soils of the experiment. Haute-Vienne. If miracidia of both digenean species penetrate O. glabra during the same time interval (4 h) at exposure, the first parasite which enters the snail favours the development of the other digenean (Augot et al., 1996) ditch along the road D46, on the commune of Chitray, so that natural infections with F. hepatica, P. daubneyi,or whereas that of northern Haute-Vienne was located in a both can be noted. According to Mage et al. (2002), this small water collection (46x4'42''N, 1x6'47''E) along the snail co-infection was frequent on acid soil because of road D72, on the commune of Saint-Junien-les-Combes. the presence of both digenean species in the same cattle. The distance between both populations was 55 km. In Nevertheless, if single-miracidium infections were per- each population, 30 samples of snails, each comprising formed with O. glabra, only juvenile snails measuring less 100 adults (more than 14 mm in height), were collected in than 2 mm in height at exposure can sustain the larval April 2003. development of F. hepatica (Boray, 1978; Bouix-Busson Snail samples were placed in new sites i.e. thirty hygro- and Rondelaud, 1986), whereas all experiments made with mesophilous meadows in both departments (Table 1). P. daubneyi were negative. In northern Haute-Vienne, the 17 meadows were each Contrary to Haute-Vienne, the parasitic conditions located at the bottom of a valley. As the underlying subsoil were different in a close geographical area on sedimentary was composed of granite, an open drainage network was soil (department of Indre, subdistrict of south-eastern dug to allow water evacuation coming from spring heads Brenne). No natural infections with F. hepatica and/or and rains. In this department, the pH of running water P. daubneyi were noted from 1996 to 2003 in local ranged from 5.6 to 7 and the quantity of dissolved calcium populations of O. glabra, whereas the first infections with in water was less than 20 mg.Lx1 (Guy et al., 1996). P. daubneyi in cattle were detected from 2001 and in In contrast, the 13 meadows chosen in the department of G. truncatula from 2003 (unpublished data). Indre were flatter and their hygrophilous zone was more reduced so that there were few open drainage furrows. Snail populations and sites chosen As the soils of these pastures were composed of silt and for the introduction of snail samples sand, supported by a calcareous subsoil, the pH of running water was higher (from 6.7 to 7.8) with 26–35 mg.Lx1 In the department of Indre (Fig. 1), the population of of dissolved calcium. All meadows were grazed by cattle O. glabra (46x40'27''N, 1x21'19''E) was living in a road during the present study. G. Dreyfuss et al.: Ann. Limnol. - Int. J. Lim. 46 (2010) 191–197 193 Table 1. Origin and number of snail samples placed in new sites in March 2003, with indication of the number of populations found at the end of the experiment (2009). Snail samples Number of snail populations Department Introduction into Number in Two years Four years At the end of (subdistrict) furrows located in April 2003 after snail introduction experiment (and %) Indre (south-eastern Indre* (local snails) 13 13 11 10 (76.9) Brenne) Haute-Vienne* (introduced snails) 17 12 10 8 (61.5) Haute-Vienne Haute-Vienne (local snails) 17 17 16 13 (76.4) (Basse Marche) Indre (introduced snails) 13 11 7 3 (17.6) * Location of meadows: Indre (communes of Chitray, Migne´and Nuret-le-Ferron), Haute-Vienne (communes of Berneuil, Blanzac, Breuilaufa, Me´zie` res-sur-Issoire and Saint-Junien-les-Combes). The furrows chosen in the present study were devoid of to avoid levelling of furrow walls by cattle trampling any O. glabra populations before the introduction of each throughout the year. sample. In contrast, G. truncatula was present in all thirty meadows, with populations living in furrows different from those in which O. glabra was placed. All meadows Parameters studied were subjected to the same climatic conditions, with a For each furrow colonized by a sample of O. glabra, continental climate strongly modulated by wet winds three parameters were measured at mid-May from 2004 to which came from the Atlantic Ocean.