Infection of Lymnaea truncatula and Lymnaea glabra by Fasciola hepatica and Paramphistomum daubneyi in farms of central France Mouna Abrous, Daniel Rondelaud, Gilles Dreyfuss, Jacques Cabaret

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Mouna Abrous, Daniel Rondelaud, Gilles Dreyfuss, Jacques Cabaret. Infection of Lymnaea truncatula and Lymnaea glabra by Fasciola hepatica and Paramphistomum daubneyi in farms of central France. Veterinary Research, BioMed Central, 1999, 30 (1), pp.113-118. ￿hal-00902562￿

HAL Id: hal-00902562 https://hal.archives-ouvertes.fr/hal-00902562 Submitted on 1 Jan 1999

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Infection of Lymnaea truncatula and Lymnaea glabra by Fasciola hepatica and Paramphistomum daubneyi in farms of central France

Mouna Abrousa Daniel Rondelauda Gilles Dreyfussb Jacques Cabaretc

a Laboratoire d’histopathologie parasitaire, faculté de médecine, 2, rue du Docteur Raymond Marcland, 87025 Limoges cedex, France h Laboratoire de parasitologie, faculté de pharmacie, 2, rue du Docteur Raymond Marcland, 87025 Limoges cedex, France C Station de pathologie aviaire et de parasitologie, Institut national de la recherche agronomique, unité d’écologie des parasites, 37380 Nouzilly cedex, France

(Received 27 April 1998; accepted 6 November 1998)

Abstract - Natural infection ofB’ml1aea L. and Lymnaeo iruncatula by Fasciola hehatica and/or Paramphistomum daubneyi was studied at two periods of risk (June-July and September-Octo- ber) in I 1 French farms known for their high prevalences ot F. hepatica infection in ruminants. A total of 1 778 L. truncatula and 2 396 L. glabra measuring 6 mm or more in height were collected to determine the prevalence of natural infection with F. hepatica and P. !/aM!M6’v/. The role of four fac- tors, i.e. season, snail co-infection (F. h(,Iiati(!a-P. daubnevi), ruminant host and the existence of single or mixed intermediate host communities, was investigated. There were no differences in preva- leiices between the two risk periods. Co-infections in L. glabra were more frequent than expected. The pi-evalences of infection with F. hepatica or P. daubneyi in L. glabra were higher in farms rearing sheep than in farms rearing cattle. A similar finding was also noted for L. Irul1catula infected with P. daub- l1evi only. L. glabra was a much better intermediate host for F. hepatica and P. elciiibtzen,i when it was the only available snail, possibly indicating an adaptation of parasites to their less usual host in local conditions. The two trematodes preferably developed in L. truncatula rather than in L. glabra when both host species lived in the same places. r0 Inra/Elsevier, Paris. Fasciola hepatica / Lynnaea glabra / Lymnaea truncatula / Paramphistomum daubneyi / natural infection

Résumé - L’infestation de Lymnaea truncatula et de Zj’m)Mfa glabra par Fasciola hepatica et Paramphistomum daubneyi dans des fermes du centre de la France. L’infestation naturelle de Lvm- Ilaea g/ahra et de Lvmnac a Iruucatulcr par Fascio/a hepatica et/ou Paral11phis/ol11l1l clnobneyi u été r Correspondence and reprints Tcl.: (33) 05 55 43 58 33! fax: (33) 05 55 43 58 93; e-muil : ;onddaud@pha;ma.unilim.6r étudiée lors de deux périodes à risque (juin juillet et septembre-octobre) dans 1 fermes françaises ayant des prévalences élevées de fasciolose chez les ruminants. Des limnées mesurant 6 mm de hau- teur et plus (1778 L. truncatula, 2396 L. glabra) y ont été récoltées afin de déterminer la prévalence de leur infestation naturelle. Les résultats ont été analysés en tenant compte de quatre facteurs, à savoir la saison, la co-infestation des mollusques par F. hepatica et P. daubneyi, l’espèce du ruminant et le type de peuplement pour les limnées (populations isolées ou colonies mixtes des deux espèces). Il n’y avait pas de différence entre les prévalences notées pour les deux périodes à risque. Les co-infes- tations étaient plus fréquentes que prévues chez L. glabra. Les prévalences notées chez L. glabra étaient plus élevées dans les prairies pâturées par les moutons que dans les pacages à bovins, quelle que soit l’espèce du trématode. Le même fait a été noté également chez L. truncatula infestée par P. daubneyi. L. glabra était un meilleur hôte intermédiaire pour F. hepatica et P. dciubneyi lorsqu’il était le seul mollusque disponible, ce qui indique la possibilité d’une adaptation des deux trématodes à cet hôte inhabituel dans des conditions locales. Fasciola hepatica et P. daubneyi se sont développés préférentiellement chez L. truncatula plutôt que chez L. glabra lorsque les deux hôtes vivaient dans les mêmes pâtures. © Inra/Elsevier, Paris. Fasciola hepatica / Lymnaea glabra / Lymnaea truncatula / Paramphistomum daubueyi / infestation naturelle

1. INTRODUCTION 2. MATERIALS AND METHODS

In the centre of France, cattle are fre- The 1 1 farms were located in seven different quently infected by two trematodes: Fasci- French departments and were grazed by cattle ola hepatica and Paramphistomum daub- (six farms) or sheep (five farms). Table I gives their characteristics. These farms were The of risk are principal neyi. periods high June-July known to have high prevalences of F. hepatica and when the September-October, major- (> 70 % of infected cattle or sheep) and low to ity of cercarial shedding by the snail inter- moderate prevalences of P. daubneyi. On four mediate host occurs. The two trematodes farms ( 14 habitats), L. glabra was the only use Lymnaea truncatula as an intermediate species recovered. On another four farms host (F. hepatica [9], P. daubneyi [3, 6]). (31 habitats), L. truncatula was found alone. Both were observed on the last three is also found in Lymnaea species Lymnaea glabra frequently farms (11 habitats with L. truncatula and four the pastures. It may act as an intermediate with L. glabra). host for both trematodes in experimental Snail was in the different conditions and is infected with F. sampling performed [1] hep- habitats located in the I farms in June-July and atica under natural conditions when L. trun- in September-October 1996. The choice of these catula is not found [2], possibly owing to a two periods was based on the fact that most cer- local adaptation of the parasite. Its suscep- carial sheddings from naturally infected snails tibility could possibly be increased when occurred during these months in central France dually infected with F. hepatica and P. and thus constituted risk periods for ruminants. As the larval forms of F. are more fre- as shown in infec- hepatica daubneyi experimental quent in adults than in juvenile L. truncatula [8], tions We in natural [1]. have, conditions, only snails measuring 6 mm or more in height compared the infection of L. truncatula and were searched visually and collected at each L. glabra in farms where F. hepatica and investigation period. They were dissected under P. daubneyi are available at two periods of a stereomicroscope to detect trematode larval high risk (interaction between parasites). forms and to classify infected snails into four groups: snails infected with F. hepatica only, P. Farms were chosen because of the presence daubneyi only, or both, and snails infected by of isolated populations or mixed communi- other trematode species. Cercaria-containing ties of L. truncatula and L. glabra (interac- rediae of F. hepatica possessed well-developed tion between hosts upon parasite infection). pharynxes, collar rings and pairs of appendages in the third posterior parts of their bodies 19]. In 3.RESULTS contrast, the rediae of P. daubneyi were shorter, with small pharynxes, and their bodies had no Table II the of natural collar or appendages [6]. Free cercariae of F. hep- gives prevalences atica were white-coloured, quick swimming infection in each farm when L. truncatula organisms [9]. The bodies of P. daubneyi cer- and/or L. glabra harboured F. hepatica only, cariae were dark brown and their was swimming P. daubneyi only, or both trematodes. When sluggish [6]. the pastures were colonized by L. truncatula only, the prevalence of infection ranged from The respective prevalences of natural infection 4.6 to 33.0 % for F. hepatica, from 0 to in each group of infected snails were calculated 20.6 % for P. daubtteyi, and from 0 to 5.9 % in each farm and at each A investigation period. for both trematodes. When the pastures were three-way variance analysis (ANOVA) and the inhabited by L. glabra only, the range of Kruskall-Wallis test were used to compare the prevalences of infection with F. hepatica only, prevalences was 4.2-14.5 %, 2.4-23.3 % P. daubneyi only, or both, and to establish the and 1.2-9.3 %, respectively. When both levels of significance. Lyrrtnaea species lived on the same pastures, the prevalences of L. truncatula did not sig- 4. DISCUSSION nificantly differ from those found in the habitats colonized by L. truncatula only, Works by Roberts [4], Rondelaud [5] and whereas the prevalences found in L. glabra Smith [7] demonstrated that in western were lower than 3 %. Other trematode Europe, cercariae of F. hepatica were shed L. truncatula in June or species were also noted in eight L. truncat- by spring-born July, and in after habitat aes- ula (Haplometra cylindracea: from 0 to September-October tivation. The snails collected during these 0.7 %; Notocotylus sp.: from 0 to 1.6 %) two to the same and in 12 L. (an unidentified periods belonged genera- glabra species: tion and had similar prevalences of infec- from 0 to 3.4 %). tion, for F. hepatica as well as for P. daub- nevi. The actual prevalence of infection in The prevalence of natural infection with F. or P. in L. was dually infected snails (table In was com- hepatica daubneyi glabra low when this snail lived with L. pared to the prevalence that might be species expected using the following formula: truncatula in the same pastures. However, it was when L. was the [(prevalence of F. hepatica infection only clearly higher glabra only lymnaeid species in the habitat. This + prevalence of dual infection) x (preva- agrees with the results reported by Bouix- lence of P. infection + daubneyi only preva- Busson and Rondelaud [2!. They stated that lence of dual infection)]. Co-infections were the prevalence of F. hepatica infection was more frequent than expected only in L. 2 % in juvenile L. glabra when this species = The were glabra (P 0.01 ). prevalences was associated with L. truncatula, whereas also compared to determine the eventual it was 11 % when L. glabra was the only influence of the following three factors: the lymnaeid species in the pastures. This could investigation period (June-July, or Septem- be the result of a local adaptation between ber-October), the type of ruminants in the host and parasite: when only the less sus- farms (cattle or sheep), and the type of com- ceptible L. glabra is available, the population munity for Lymnaea species (isolated pop- of F. hepatica must adapt to this host or dis- ulations or mixed species). The prevalences appear. for both trematodes did not differ signifi- Our results also demonstrated that preva- cantly when the investigation period was lences of P. daubneyi infection in L. glabra considered. The prevalences of infection in and L. truncatula were higher when these L. glabra collected in farms rearing sheep snails lived in pastures grazed by sheep. One can that there is a were higher than the corresponding per- only speculate higher pos- sible infection of P. in which centages obtained in farms rearing cattle. daubneyi sheep result in snail infec- This variation was significant using might subsequent higher tion. infec- ANOVA in F. hepatica-infected L. glabra Only comparative experimental tions in sheep and cattle could give support (F = 5.75; P = 0.04) and in P. daubneyi- or infirm this speculation. infected L. glabra (F = 8.8; P = 0.01 ). Higher prevalence of P. daubneyi infection (Kruskall-Wallis test: P = 0.008; ANOVA: REFERENCES F = 8.7; P = 0.01) was also noted in L. trun- catula when collected in pastures grazed by [ I ] Abrous M., Rondelaud D., Dreyfuss G., and Fasciola sheep. Lastly, L. glabra was more often Paramphistomum daul7llevi hepatica: the effect of dual infection on infected both P = by parasites (F. laepatica: prevalence and cercarial shedding in pread- 0.002; P. daubneyi: P = 0.002) when it was ult Lvmnae(i glabra, J. Parasitol. 82 (1996) the only available snail in the pastures. 1026-1029. [2] Bouix-Busson D., Rondelaud D., Etude de Muller en Limousin, Rev. Med. Vet. 125 )’aptitude à l’infestation fasciolienne chez (1974)237-250. Muller et chez L. truncatula Lymnaea glabra [6] Sey 0., Life-cycle and distri- Muller dans des mono- et bis- geographical peuplements bution of Din- Bull. Soc. Fr. Parasitol. 3 Paramphistomum daubneyi pecifiques, (1985) 1962 95-98. nik, (Trematoda: Paramphistomata), Acta Vet. Acad. Sci. Hung. 27 (1979) [3] Dinnik J.A., Paramphistomum daubneyi sp. 115-130. nov. from cattle and its snail host in the Kenya Highland, Parasitology 52 (1962) [7] Smith G., The relationship between the size 143-151. of Lymnaea truncatula naturally infected with Fasciola hepatica and the intensity and Roberts E.W., Studies on the of [4] life-cycle of the redial infection, J. Helminthol. Fasciola L. and of its snail maturity hepatica host, 58 (1984) ]23-)27. Limnaea (Galba) truncatula Muller, in the field and under controlled conditions in the [8] Taylor E.L., Fascioliasis and the liver-fluke, laboratory, Ann. Trop. Med. Parasitol. 44 F.A.O. Agricultural Studies, no. 64, 1965. (1950) 187-206. [9] Thomas A.P., The natural history of the liver [5] Rondelaud D., L’6volution des redies de Fas- fluke and the prevention of rot, J. Roy. Agric. ciola hepatica L. chez Galba truncatula Soc. Engl. 19 (1883) 276-305.