Fasciola gigantica and F hepatica: a comparative study of some characteristics of Fasciola infection in Lymnaea truncatula infected by either of the two trematodes Gilles Dreyfuss, Daniel Rondelaud

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Gilles Dreyfuss, Daniel Rondelaud. Fasciola gigantica and F hepatica: a comparative study of some characteristics of Fasciola infection in Lymnaea truncatula infected by either of the two trematodes. Veterinary Research, BioMed Central, 1997, 28 (2), pp.123-130. ￿hal-00902465￿

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Fasciola gigantica and F hepatica: a comparative study of some characteristics of Fasciola infection in Lymnaea truncatula infected by either of the two trematodes

G Dreyfuss D Rondelaud2

1 Laborntnirc de parasitologie. Faculté de p/wmlllcie, 2 1.fiborafoir« d’histo/lillhologie parasitaire, Faculté de iiié(le(.ine, 2, rue du /!fx’/fM;’-/

(Reccivcd 3 June 1996; acccpted 10 Septcmber 1996)

Summary ― Experimental infections were carried out using three Lymnueu truncatulo pop- ulations and two Fascio/a species in order to determine the trematode influence on six param- eters of snail infection by either of the two trematodes. All experiments were performed using snails 4 mm long, two miracidia for each L trtili(-(ittilti, and a constant temperature of 20 °C. No significant influence of trematode species was detected in the following parameters: snail sur- vival at day 30, the life span of infected snails (from miracidial exposure to snail death), the increase in shell length throughout the experiment, the duration of the patent period and the num- ber of cercariae shed by infected snails. The frequency of cercaria-shedding snails was closely correlated with the particular L truncotuln population and trematode species. A similar finding in two populations was also noted for the frequencies found in the infected snails who died with- out emission. The prepatent period had a longer duration in the Fasciola gigantica-infected groups. The percentages of floating cysts were greater in the Fa.s’c’w/« gig(ii7ti(-(i groups than in the Fasciola hepatica groups. cercaria / metacercaria / Fasciola sp / Lymnaea truncatula

Résumé ― Fasciola gigantica et F hepatica : étude comparative de plusieurs caractéris- tiques de l’infestation fasciolienne chez trois populations de Lymnaea truncatula infes- tées par l’un ou l’autre des trématodes. Des infestations expérimentales ont été réalisées

!:! Correspondence and reprints Tel: (33) 05 55 43 58 63; fax: (33) 05 55 43 58 OIII1 chez trois populations de Lymnaea truncatula afin de déterminer l’influence du trématode sur les caractéristiques de l’infestation lorsque la même souche est parasitée par Fasciola gigantica ou par F hepatica. Toutes les expériences ont été effectuées en utilisant des mollusques de 4 mm de longueur, deux miracidiums pour chaque L truncatula et une température constante de 20 °C pour l’élevage des limnées. L’espèce du trématode n’a pas eu d’effet sur la survie des limnées au 30e jour, la durée de vie des mollusques infestés (depuis l’exposition aux miracidiums jusqu’à la mort des mollusques), l’accroissement de la longueur de la coquille au cours de l’expérience, la durée de la période patente et le nombre total de cercaires produites par les limnées infestées. Les fréquences des mollusques avec des émissions cercariennes ont été étroitement corrélées à la souche de L truncatula et à l’espèce du trématode utilisées pour ces expériences. Il en a été de même pour les pourcentages relevés dans deux populations chez les mollusques infestés qui sont morts sans émission. Des durées plus longues ont été observées dans les trois séries infestées par F gigantica pour la période prépatente. Les pourcentages des kystes flottants étaient plus importants dans le cas de F gigantica que dans le cas de F hepatica. cercaire / métacercaire / Fasciola sp / Lymnaea truncatula

INTRODUCTION hepatica (Boray, 1978) and a potential inter- mediate host of F gigantica under laboratory Species of the !v/wMcattle with Survival rate on day 30 was calculated using the chronic Fasciola infections and were incubated ratio between the number of survivors counted on for 20 days at 20 °C in complete darkness this day and the number of snails at the onset of (Ollerenshaw, 1971; Rakotondravao, 1984). experiment. The frequency of snails with cer- Table I gives the characteristics of the six carial shedding (first category) was calculated in relation to the number of snails on experimental groups. They were raised under surviving 30. A similar was used for the fre- constant conditions at 20 °C, with artificial light- day protocol of infected snails that died without emis- ing for 12 h (0700 to 1900 hours) at an inten- quency sion The differences between sity of 3 000 lux at the aquaria surface. Each (second category). the were a L truncatula was exposed to two miracidia for percentages analyzed using compari- son test of 4 h. The choice of two miracidia per snail was experimental frequencies (Stat-Itcf, 1988). preferred to that of one, three or more miracidia/snail because the infection rate was The life span of the control and infected snails optimal without large mortality. The snails were corresponded to the time interval between the subsequently raised until day 30 in closed-circuit onset of experiment or miracidial exposure, and aquaria in an air-conditioned room at 20 °C (five the snail’s death. The increase in the shell length snails per litre of water). Control groups of unin- throughout experiment corresponded to the dif- fected snails were also formed (25 animals for ference between the value measured at miracidial each population). At day 30, the surviving snails exposure and that determined at snail’s death. from the control and experimental groups were The duration of the prepatent period extended isolated in 35 mm diameter petri dishes with 2 or from miracidial exposure to the first day of cer- 3 mL of water and a piece of lettuce. The recip- carial shedding, whereas the patent period con- ients were placed in the same air-conditioned cerned the whole shedding period until the room at 20 °C. Every 2 days until the snail’s snail’s death. The total number of metacercariae death, a metacercarial count was performed and included all types (floating cysts, fixed cysts and free cysts). Mean values were determined infected groups. The trematode species had from the individual percentages of each param- a significant influence on the frequency of eter and standard deviations were calculated. infected snails with cercarial shedding These values were then analyzed by a one-way (P < 0.001 ), and on that of infected snails that analysis of variance (Stat-Itcf, 1988). died without emission in populations A and B (P < 0.001 ). Table III groups the results obtained from RESULTS the control and infected snails with or without cercarial shedding. Differences in the length Table I gives the survival rates on day 30 in of survival time according to snail category the experimental groups. The trematode were noted. Survival times were shorter in species had no significant influence on the each group of infected snails than in controls. survival time of snails in these groups. No They were also reduced in the snails without dead snails were observed among the 25 snails emission (category 2). Significant differences of control groups in the populations A and C. between the mean values of controls and In the colony B control group, the survival those of infected snails were noted for each rate was 96% (24 snails) on day 30. population separately considered (P < 0.0011 Table II indicates the number of snails in in the six groups), whereas the population and trematode had no each category and their frequency of infec- species significant influence. tion compared to the number of surviving snails on day 30. The percentage of snails Table III gives also the mean values found with cercarial shedding varied with trema- for the increase in shell length throughout the tode species and ranged from 15 to 19% in experiment. No significant difference in the the F gigantiw-infected groups and from 47 increase was noted between the three popu- to 5 1 % in the F hepatica-infected groups. lations of L truf/catu!u whatever the experi- Infected snails that died without emission mental group and the category of snails. were observed and their percentages ranged Table IV indicates the lengths of the from 1 1 to 18% in the F gigantica-infected prepatent period and those of the patent groups, from 14 to 37°lo in the F /?fMf;c<:;- period. Significant differences in the mean duration of the prepatent period between the DISCUSSION F gigantica groups and F hepatica-infected snails were noted for the three populations Many factors can affect intramolluscan-trema- (P < 0.001 ). Differences in the mean lengths tode dynamics. They include a variety of of the patent period between the three popu- forces, both internal and external to the snail, lations were not significant. and affect the manner in which the larval Table V groups the numbers of cercariae development occurs (Esch and Fernandez, Even the interactions between shed per snail in the six experimental groups. 1994). though the snail and the trematode on the Mean values ranged from 135 and 174 cer- depends cariae in the F gigantica-infected groups, and snail’s suitability for the parasite and perhaps from 121 to 209 in those with F hepatica. The on the frequency of natural encounters between the two in the field trematode species had no significant influ- partners (Ron- ence on these results. Some cercariae died delaud, 1993), it was interesting to determine after their exit from the snail but their number trematode influence on the parameters of snaill infection when the snail can assure was very low (0.06% in the six groups). Other species the of two trema- cercariae fixed on a support, or formed free complete larval development from same metacercariae on the bottom of the recipients, todes originating the family. or turned into floating cysts. In the F gigan- The survival rates found in the three pop- tica-infected groups, the percentage of float- ulations of L truncatula agree with the per- ing cysts ranged from 17.1 to 32.7%. In the centages reported by several authors in other groups with F hepatica, the percentage did French populations of L trul1catula when they not exceed l0%. used two miracidia of Fa.sciola sp per snail (Audousset et al, 1989; Rakotondravao and Barthe (1982) found a decrease in the snail Rondelaud, 1991; Dreyfuss and Rondelaud, survival rate on day 30 when the number of 1994a). Our results demonstrated that the miracidia used for each snail increased (from trematode species had no significant influ- 27 to 82% in snails each infected by I to 20 F ence on the survival of L truncatula on day hepatica miracidia, respectively). 30 when miracidial exposure was performed The frequency of snails with cercafial shed- using snails 4 mm long. However, this finding ding ranged widely and this variability must concerned only snails individually infected be attributed to the particular population of with two miracidia. Indeed, Rondelaud and snail and trematode species (Boray, 1966). In contrast, some infected snails died without contrast, the durations of the patent period shedding in all experimental groups and this found in F gigantica- and F hepatica-infected result was more difficult to interpret. The groups were similar, indicating the absence hypothesis propounded by Kendall (1950) of trematode influence on this parameter of that the absence of cercarial shedding from snail infection. F L hepatica- infected ylabra and L palustris Higher percentages of floating cysts were was due to the snail’s anatomical configura- recorded from F giganticn-infected snails and tion cannot be retained in the context of this suggested that they were trematode depen- study. The most valid assumption to explain dent. However, the species of the snail used this absence of shedding would be the tissue for the experimental infection had also an lesions which appeared in the snail after influence on these percentages, which were miracidium penetration and developed over 26.7°lo in L vatalen.sis (Da Costa et al, 1994) some weeks until snail death (Sindou et al, and 29.3% in L tomentosa (Dreyfuss and Ron- 1991a,b). Under these conditions, the physi- delaud, 1994b) when these snails were ological state of the intermediate host would infected by Fhepaticu under laboratory con- not permit cercaria shedding. ditions. Thus, the numbers of these floating on the The literature does not give any quantita- cysts depended particular trematode tive data on the survival time of infected and snail species. snails. Our results demonstrated greater values for snails manifesting cercarial shedding and REFERENCES can only be explained by assuming the prob- able existence of a selection; the absence of emission would induce snail’s death after a Audousset JL, Rondelaud D, Dreyfuss G, Vareille- certain time, under the influence of factors More] C ( 1989) Les emissions cercariennes de Fasciola hepalicn L chez le mollusque Lvnnmen whose nature must be determined. The pres- truncatula Mfllei. A propos de quelques obser- ence of shedding would result in greater snaill vations chronohiologiques. 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