Digenean Fauna of Cerastoderma Glaucum (Veneroidae, Cardidae) from Tunisian Coasts
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Bull. Eur. Ass. Fish Pathol., 31(1) 2011, 4 Digenean fauna of Cerastoderma glaucum (Veneroidae, Cardidae) from Tunisian coasts L. Gargouri Ben Abdallah1*, R. Antar1, K. Hosni2, N. Trigui El Menif2 and F. Maamouri1 1 Reasearch Unit Animal Bio-Ecology and Systematic Evolutionary, Faculty of Sciences, Tunis, University of Tunis El Manar, 2092, Tunis, Tunisia; 2 Laboratory of Environment Bio-monitoring (LBE), Faculty of Sciences, Bizerte, University 7th November Carthage, 7021 Zarzouna, Bizerte,Tunisia Abstract The study conducted on the cockle Cerastoderma glaucum from Tunisian coasts (Bizerte lagoon and Gulf of Gabes) showed the presence of two digenean species (sporocyst and cercaria of Bucephalus minimus and metacercaria of Meiogymnophallus strigatus). A description of these larvae and the behaviour of the naturally emerging cercaria are reported. The examination of the frequency of B. minimus and M. strigatus reveals some seasonal variation. This variation becomes more significant by comparing the sites. B. minimus has the highest frequency in the Bizerte lagoon, by contrast to that of M. strigatus which is the highest in the Gulf of Gabes. This variation is statistically significant. These results indicate that B. minimus and M. strigatus can be considered as biological indicators making it possible to predict the capture area of the cockle. Introduction The cockle, Cerastoderma glaucum, which has process of regulating of the natural popula- a significant economic value, is commonly tions of marine organisms, is a theme which exploited in several European countries. In was the subject of little attention because of the Tunisia, in spite of its abundance in several durability of the relation parasite-host (Combes, sites, in lagoons as well as in the sea, this species 1995). Recently, De Montaudouin et al. (2000), still remains unexploited. This bivalve, slightly Mouritsen (2002), Desclaux (2003) and Desclaux hidden in the sandy-muddy sediment of the et al. (2002) studied the impact of Digenea on intertidal zone, is among the benthic organisms the cockle populations. These authors conclude most exposed to organic and chemical pollut- that digenean parasitism does not necessarily ants debouched in the receiving environment. explain the marked reduction in the molluscs, Studies carried out in the Bay of Saint Brieuc even if the presence of digeneans can indirectly by Le Mao et al. (2002), on some species of bi- increase the mortality rate of the cockle (Cerasto- valves, show a marked decrease of the cockle derma edule, Austrovenus stutchburyi) by reducing between 1988 and 2000. Various hypotheses their capacity for burrowing in the sediment. were proposed to explain this reduction, among A multifactorial effect is therefore suspected in which, we can cite intensive fishing, as well cockle mortalities. as pollution and parasitism. Parasitism, as a * Corresponding author’s email: [email protected] Bull. Eur. Ass. Fish Pathol., 31(1) 2011, 5 Conscious of the ecological importance of distilled water and stained with boric carmine. the parasites, their action on the dynamics of After differentiation, the specimens were dehy- populations and the behaviour of the host, we drated in series of alcohol (70, 95, 100%), cleared investigated the digenean fauna of the cockle, in Gaulteria oil and mounted between slide and Cerastoderma glaucum and the spatiotemporal coverglass in Canada balsam. distribution of the parasites. Silversides collected from Kalaat El Andalous, Materials and methods a site known to be negative for the bucephalid The studied cockles (3200 specimens) were parasite, were exposed to cercaria released from sampled from the Bizerte lagoon (north-eastern C. glaucum to try the experimental infection. Tunisia) and the Gulf of Gabes (port of Sfax) (south-eastern Tunisia). The Bizerte lagoon, For histological preparations, cockles were fixed characterized by sandy-clay to clay-silt-sandy in Bouin’s fluid. After washing, samples were sediments, is rather deep (12 m) (Soussi et al., dehydrated through an ethanol series, treated 1983). In Bizerte Lagoon, the mean annual water with butyl alcohol, embedded in paraffin wax temperature is 18.28 ˚C and the mean annual and sectioned. The 5-µm sections were stained salinity is 34 ‰. In the Gulf of Gabes, charac- with Masson Trichrome (Martoja and Martoja- terized by sandy-muddy bottom sediments Pierson, 1967). (Amari, 1984), the annual mean temperature is 20.58 ˚C and the mean annual salinity is Illustrations and measurements of parasites 38.68‰. were made with the aid of Wild microscope drawing tube. The collected lamellibranchs were placed in small aquaria, which were examined daily with The nomenclature used in the analysis of the a binocular microscope to detect spontaneous frequencies of the larval-stage parasites accord- cercarial emergence. Each infected mollusc was ing to the seasons and sampling sites follows then kept in its own aquarium. The number Margolis et al. (1982) and Bush et al. (1997). of cercariae produced daily was counted. The experiment was subjected to natural lighting To test the significance of the variation of the conditions only, except during the period when values of the frequency according to the locali- cercariae were counted under artificial light. If ties of capture, X2 test was applied. these examinations appeared negative, after 15 days the molluscs were dissected to detect the Results and discussions possible presence of young sporocysts or meta- Examination of the cockle Cerastoderma glaucum cercariae. The site of infection and the number collected from the Bizerte lagoon and the Gulf of each parasite were noted. The parasites col- of Gabes (port of Sfax) reveal that this mollusc lected were either studied directly in vivo under is parasitized by the same digenean fauna in the stereomicroscope, or treated for a later ob- both localities. Two species of digenean belong- servation. The parasites were fixed in Bouin’s ing to two distinct families were recorded: the fluid between slide and coverglass, washed by sporocyst and cercaria of Bucephalus minimus Bull. Eur. Ass. Fish Pathol., 31(1) 2011, 6 (Stossich, 1887) Maillard, 1976 (Bucephalidae) Cercaria and the metacercaria of Meiogymnophallus stri- Morphology gatus (Lebour, 1908) Ching, 1965 (Gymnophal- The gasterostome cercaria (Figure 3), measur- lidae). ing, on average, 360 µm in length and 90 µm in width. Anterior extremity armed with an Bucephalus minimus organ of penetration, the rhynchus contain- Sporocyst ing numerous glandular cells. The posterior Branched sporocyst, white with constructions margin, ending with the tail, composed of a and containing, according to the degree of caudal bulb, prolonged by two long retractile maturation, either the germinal balls or the furca with numerous small transverse folds cercariae (Figures 1 a, b). Sporocyst occurring on surface. Glandular cells, present on caudal in gonads and digestive gland of the cockle. bulb and furca, secreting adhesive substance With histological analysis, it was possible to allowing the attachment of the cercaria to the confirm the presence of sporocyst in analyzed second intermediate host. Digestive tract of the tissue (Figure 2 a, b). As reported by Khamdan cercaria including an equatorial mouth followed (1998) and Desclaux et al. (2002), these larvae by a muscular pharynx (30 µm diameter), a caused severe disruption such as the castration short oesophagus and a saccular sac. The main of the gonadal tissue, function alteration of the excretory tubules, resulting from the union of digestive gland or death of the mollusc. The anterior and posterior collecting tubules, joining development of the larval stages was, therefore, the excretory vesicle at the level of the mouth. achieved at the expense of the parasitized host. Excretory vesicle, saccular, thin-walled, and The parasite diverts the metabolic activities measuring on average 60 µm in length. 72 flame of the mollusc for its own gain. The death of cells (36 on the right, 36 on the left) present in parasitized molluscs occurred before the total the following arrangement: emergence of the cercariae. 2[(6+6+6) + (6+6+6)] = 72 200 µm a b Figure 1. Sporocyst containing cercariae of Bucephalus minimus from Cerastoderma glaucum, a: Drawing, b: photo Bull. Eur. Ass. Fish Pathol., 31(1) 2011, 7 a b Fig u re 2 . a: Histological section showing the presence of Bucephalus minimus sporocyst in gonads. b: Histological section showing the presence of Bucephalus minimus sporocyst in digestive gland. Sp: sporocyst. The Bucephalid cercaria, named Bucephalus haimeanus by Lacaze-Duthiers in 1954, was collected in the oyster Ostrea edulis L. 1758 in the Balearic Islands and in Cardium glaucum Bruguiere, 1789 in France coasts (Sete). Mat- thews (1973) found this parasite in Cardium edule and succeeded in obtaining experimentally the metacercaria by infecting the goby, Poma- toschistus microps. Maillard (1975, 1976) never found a bucephalid cercaria in Ostrea edulis at Sete whereas Cardium glaucum was parasitized. He concludes that the bucephalid parasite of the oyster and that of the cockle constitute two distinct species. However, this author, only on the basis of morphological criteria, attributed the bucephalid collected from Cardium edule and that taken from Cardium glaucum to the species which he named Labratrema minimus. However, all previous designations were considered as a synonym of Bucephalus minimus (Overstreet and Curran, 2002; Bartoli et al., 2006). 100 µm Behaviour The