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The morphology and behaviour of Cercaria lata Lesps, 1857 (, Faustulidae) from the Mediterranean clam Tapes decussata (L.)

Article in Journal of Helminthology · December 2008 DOI: 10.1017/S0022149X08125160 · Source: PubMed

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The morphology and behaviour of Cercaria lata Lespe´s, 1857 (Digenea, Faustulidae) from the Mediterranean clam Tapes decussata (L.)

L. Gargouri Ben Abdallah1*, N. Trigui El Menif2 and F. Maamouri1 1Department of Biology, Faculty of Science, Tunis, Tunisia: 2Department of Biology, Faculty of Science, Bizerte, Tunisia

Abstract

Cercaria lata (Digenea, Faustulidae), discovered by Lespe´s (1857) in Tapes decussata (L.) in the basin of Arcachon, was found for the first time, from the eastern Mediterranean, in the same lamellibranch from Tunisia (Bizerte and Tunis lagoons and Gulf of Gabes). These cercariae develop in daughter sporocysts, which develop in mother sporocysts in the gonads. Daughter sporocysts are observed in the gonads and sometimes in the digestive gland. A redescription and the behaviour of the naturally emerging cercariae and spatio-temporal distribution of the sporocysts are reported. A comparative study using multivariate analyses associated with morphology, biology and seasonality confirm the distinctness of Cercaria lata and the cercaria of Cercaria pectinata from Donax trunculus.

Introduction Lasiotocus longicystis Bartoli, 1965 (Monorchiidae) and Gymnophallus fossarum Bartoli, 1965 (Gymnophallidae). The clam, Tapes decussata (L.), a common lamellibranch In this paper, we limit our study to the sporocysts and of the Mediterranean coast, has been for centuries a very cercariae of C. lata. As indicated in the literature, this desirable species of high market value. Accordingly, it has cercaria has been generally believed to be the same as the been the subject of many investigations, in particular in others collected from various bivalve hosts. We carried parasitology. This bivalve can shelter various species of out a comparative study with another faustulid cercaria Protozoa and metazoan parasites. Among the Metazoa, found in Donax trunculus which has a strong morpho- digenean parthenitae are the most frequent parasites. This logical similarity to C. lata. mollusc play, a very important role in the life cycle of several of these platyhelminths (Bartoli, 1965, 1972, 1973, 1981, 1982, 1983, 1984; Hanafy et al., 1997, Gargouri Ben Materials and methods Abdallah, 2001; Gargouri Ben Abdallah & Maamouri, 2001, 2005; Trigui El Menif et al., 2004). Tapes decussata The study was conducted on T. decussata from the represents the first intermediate host and also, in certain Bizerte (4460 specimens) and Tunis (3790 specimens) cases, the second host. lagoons (north-eastern Tunisia) and the gulf of Gabes During our research on the digenean parthenitae in (1546 specimens) (south-eastern Tunisia). Samples were bivalves found on the Tunisian coasts, we collected collected at approximately monthly intervals. The lagoon four species belonging to four distinct families from of Bizerte, which is of sandy-clay to clay-silt-sandy facies, T. decussata: sporocysts and cercariae of labracis is rather deep (12 m) (Soussi et al., 1983). The lagoon of Paggi and Orecchia, 1965 () and Cercaria Tunis, where bottom sediments consist of muddy fine lata Lespe´s, 1857 (Faustulidae); and metacercariae of sand, shelly particles and organic matter, is variable in depth (1–4.5 m) (Jouirou, 1982). The annual mean water temperature of these two lagoons is 18.28C. Annual mean *E-mail: [email protected] salinity is 37.7‰ for the lagoon of Tunis and 34‰ for the 70 L. Gargouri Ben Abdallah et al. lagoon of Bizerte. The gulf of Gabes is characterized by changed into an orange colour when the cercariae sandy-muddy bottom sediments (Amari, 1984), an annual complete their development. No birth pore was observed mean temperature of 20.58C and an annual mean salinity in these sporocysts. However, on one side of the daughter of 38.68‰. sporocyst, a lysed area was detected, the opposite side The lamellibranchs collected were placed in small being perfectly intact (fig. 1b). The emergence of the aquaria, which were examined daily with a binocular cercariae is affected, undoubtedly, by the rupture of the microscope to detect spontaneous cercarial emergence. lysed wall of the daughter sporocyst. The number of Each infected mollusc was then kept in its own daughter sporocysts, which was often very high (exceed- aquarium. The number of cercariae produced daily was ing 500 specimens), caused severe disruption, such as the counted. The experiment was subjected to natural castration or death of the mollusc. The heavily parasitized lighting conditions only, except during the period gonads were completely invaded by the sporocysts and, when cercariae were counted under artificial light. If lacking sexual cells, the determination of the sex of the these examinations appeared negative, after 15 days host was not possible. The death of parasitized molluscs the molluscs were dissected to detect the possible occurred before the total emergence of the cercariae. The presence of young sporocysts. The parasites collected development of the larval stages was, therefore, achieved were studied directly in vivo under a stereomicroscope. at the expense of the parasitized host. The parasite diverts The nomenclature used in the analysis of the the metabolic activities of the mollusc for its own gain. frequencies of the larval-stage parasites according to The´ron et al. (1992) showed that the parasitism of the the seasons and collecting sites follows Margolis et al. mollusc Biomphalaria glabrata by Schistosoma mansoni (1982) and Bush et al. (1997). Sambon, 1907 is not accompanied by an increase of the In order to compare C. lata collected from T. decussata trophic activity of the mollusc, since the high quantity of with another faustulid found in D. trunculus,we energy consumed by the parasite is appropriated from the examined 2062 specimens of the latter bivalve collected mollusc. This capture of energy prevents the survival of from Kalaˆat El Andalous (situated at 35 km to the north- the mollusc. east of Tunis, with sandy facies, mean salinity of 37‰ Similar results were found with Dresseina polymorpha and mean temperature of 18.98C (El Arrim, 1996)). (Pallas, 1771) following their colonization by the The following features of the cercariae were measured sporocysts of Bucephalus polymorphus Baer, 1827 (Vom (mm): body length (BL), body breadth (BB), tail length Scheidt, 1984). In the same way Coustau et al. (1991) (TL), setae bundles length (SBL), length of oral sucker showed that the sporocysts of Prosorhynchus squamatus (LOS), breadth of oral sucker (BOS), length of ventral Odhner, 1905 caused the castration of the mollusc Mytilus sucker (LVS), breadth of ventral sucker (BVS), pharynx edulis Lamark, 1919 by releasing a factor that stimulates length (PL), pharynx breadth (PB), length of oesophagus the mobilization of glycogen and inhibits the division of (OEL), length of caeca (CL). All measurements were sexual cells. transformed by being divided by the body length to remove the effect of the size. Length itself was not used as a variable in the final analysis. The spatio-temporal distribution of the sporocysts To determine the multivariate relationship between In the north-east of Tunisia, molluscs containing 12 variables on 60 cercariae (30 from T. decussata and 30 sporocysts were collected in summer and autumn. In from D. trunculus) a principal components analysis (PCA) the gulf of Gabes, they were absent only in winter. The was applied. highest prevalence of infection was recorded in autumn for the all stations (table 1). However, these larval stages were more frequent in the gulf of Gabes and Results appeared more precociously (table 1). This may be due Sporocysts to the temperature of the water, which is slightly higher in the south of Tunisia. However, the higher Mother sporocysts summer temperature in this area can limit the White sporocysts, sausage-shaped, measuring 2600 mm longevity of the free larval stage (miracidia) and (2100–3800 mm) in length and 361 mm (245–463 mm) in consequently reduce the rate of infestation of molluscs. width, were observed in the gonads of T. decussata. Salinity also seems to influence the prevalence of these Each sporocyst harboured 20–26 immature daughter sporocysts. Indeed, there is a clear correlation between sporocysts and some germinal balls located at the the increase in salinity and the increase in the rate of periphery. No birth pore was observed in the mother parasitism. The lowest prevalence was observed in the sporocysts (fig. 1a). lagoon of Bizerte, prevalence was greater in the lagoon of Tunis and was greatest in the gulf of Gabes, the area with the highest salinity. The hydrodynamism of this Daughter sporocysts locality can also have an impact on the variation of Sporocysts, 2359 mm (1450–3600 mm) long and 337 mm these values. This factor, more important at sea than in (200–420 mm) wide, enclosing cercariae, infected gonadal the lagoons, plays a fundamental role in the displace- tissues and sometimes the digestive gland. The number of ment and the dispersion of the infesting stages and cercariae varied according to the maturation of the thus in their contact with the host. This variation can sporocyst. Small sporocysts contained 4–8 cercariae and also be the result of the availability, in the prospected large sporocysts contained 11–17 cercariae. The colour of areas, of the second intermediate host and the these sporocysts varied. The brown young sporocysts susceptible final host. Morphology and behaviour of Cercaria lata 71

Fig. 1. Mother (a) and daughter (b) sporocysts of Cercaria lata.

Cercaria of body. Cephalic glands (fig. 2b), 8–10 pairs, on each side of oesophagus, reaching anterior margin of ventral Morphology sucker; ducts run laterally to pharynx and opening A fully developed cercaria released from a sporocyst, with oval body and trichocercous tail, is shown in fig. 2a. beside oral sucker. Digestive system including mouth The tegument is armed with spines arranged on the entire located at base of oral sucker, muscular ovoid pharynx surface of body; dense spines covering the forebody followed by oesophagus bifurcating anterior to acetabu- become more sparsely distributed on the hindbody. lum. Cylindrical caeca reaching to level of testes. Spherical oral sucker subglobular; ventral sucker, Testes symmetrical postacetabular. Spherical ovary slightly smaller than oral sucker, approximately in middle situated postacetabular and on median axis of body. 72 L. Gargouri Ben Abdallah et al.

Table 1. Seasonal frequencies of Cercaria lata Lespe´s, 1857 from the three collecting sites.

Bizerte Gulf of lagoon Tunis lagoon Gabes

N P (%) N P (%) N P (%)

Autumn 1210 0.99 810 1.11 401 15.21 Winter 910 0 860 0 380 0 Spring 1010 0 890 0 374 4.81 Summer 1330 0.37 1230 0.49 391 2.55

N, Number of molluscs examined; P(%), prevalence.

Excretory vesicle Y-shaped with long arms reaching anterior to intestinal bifurcation. Two lateral collecting ducts opening into anterior extremity of bladder. Bladder containing up to about 60 excretory corpuscles immersed in clear liquid. Flame cell formula: 2[(2 þ 2) þ (2 þ 2)] ¼ 16. Tail tubule communicating with bladder. Surface of tail lacking spines provided with annular folded membranes. Twenty-five pairs (24–27) of setae bundles arranged laterally along the tail. Each bundle (fig. 2c) generally bearing 7–8 rib-like supports (rarely 9) joined by a fine membrane. Tail lacking flame cell. Cercaria lata appears to be closest to the faustulid cercaria found in D. trunculus (fig. 3). In order to determine whether or not these forms were distinguish- able morphologically, a principal components analysis (PCA) was carried out using metrical data (table 2) from 60 specimens. The results of the first two components (fig. 4), which explain 70.76% of the variance, indicate that the cercariae separated out clearly on the second axis (PCA2). There was also a slight separation between specimens on the first axis (PCA1). PCA of the characters analysed shows that those which had the highest coordinates, and therefore contributed most to the first axis were: body breadth (BB), length of oral sucker (LOS), breadth of oral sucker (BOS), length of ventral sucker (LVS), breadth of ventral sucker (BVS), pharynx length (PL), pharynx breadth (PB), and oesophagus length (OEL). The characters that contributed to the second axis (PCA2) were body length (BL), tail length (TL), setae bundles length (SBL), and caeca length (CL). This PCA shows that multivariate morphological features of the cercariae indicate that there are two types in Tunisian waters.

Behaviour Emerged cercariae (200–300/day) are characteristi- cally positively phototactic. Changing the position of the light source generates a new regrouping of the cercariae. After emergence from the mollusc, these larvae quickly leave the bottom of the container to reach the surface of the water then plunge again. These vertical movements, between the bottom and the surface of the water, seem to be related to the search for the second intermediate host, probably a planktonic . The powerful tail propelling the body of the cercaria moves in a spiral. Swimming is intermittent and during the pauses the tail is folded along the Fig. 2. Cercaria lata from Tapes decussata (a) showing cephalic ventral face of the body. The life-span of the cercariae is glands (b) and bundle of setae (c). Morphology and behaviour of Cercaria lata 73

stops moving and in a few minutes is detached. The body then rests on the bottom and dies without encysting.

Discussion The non-oculate C. lata developed in T. decussata (Bivalve, Veneridae) extracted from the lagoons and the gulf of Gabes, possessing a spined tegument, a trichocercous tail without furcae, provided with bundles of setae described as being rib-like, with about 7–8 setae joined by a membrane, and a Y-shaped excretory system, belongs to subfamily Baccigerinae (sensu Bray, 1988). On the basis of molecular, morphological and life cycle data, Hall et al. (1999) removed the subfamily Baccigerinae from the Fellodistomidae and promoted it to familial status. The Baccigerinae Yamaguti, 1959 was considered as the junior synonym of the Faustulidae, Poche, 1926. Cercaria lata was first described by Lespe´s, 1857 in the same mollusc taken from the basin of Arcachon. The original description of this cercaria, limited to the digestive system and some elements of the excretory system, lacks any relevant information on the cephalic glands, the reproductive system, the number of flame- cells, the setae bundles and the rib-like supports of C. lata. Later, Palombi (1934a) found in T. decussata, collected from Naples, a ‘Steringophoridae’ cercaria and con- sidered it Bacciger bacciger. This was based only on the morphological similarity of the larval stage with the adult, and the life cycle of this species was described as: cercariae after escaping from sporocysts parasitizing the first intermediate host, T. decussata, penetrate and encyst as metacercariae in the Amphipoda Erichthonius difformis, and develop into adults in the alimentary tract of Atherina spp. Later, Palombi (1934b, 1940) and Dolgikh (1968) reported cercariae which appear to be the same species in Fig. 3. Cercaria pectinata from Donax trunculus. other bivalve hosts (Venerupis aurea (Veneridae), Chamelea gallina (Veneridae), Donax vittatus (Donacidae) and Barnea approximately 5–6 h at 158C. An increase of tempera- candida (Pholadidae)) and also attributed them to Bacciger ture (to 20–228C) shortens their survival to a few bacciger. Recently, Ramon et al. (1999) reported sporocysts minutes. Cercariae sink to the bottom of the container. and cercariae of Bacciger bacciger in D. trunculus The cercarial body shows slow contractions, the tail (Donacidae). The number and variety of bivalves

Table 2. Measurements (mm) of cercariae harvested from Tapes decussata and Donax trunculus collected from Tunisian coast and other localities; all measurements are lengths unless stated; the numbers in brackets are ranges.

Tapes decussata Donax trunculus

Present Palombi Present Ramon et al. (1999) study (n ¼ 30) (1934b) (Naples) (n ¼ ?) study (n ¼ 30) (Gulf of Valencia) (n ¼ 10)

Body 248 (200–285) 200–240 252 (220–285) 329.7 Body breadth 146 (120–160) 100 126 (112–140) 220.8 Tail 382 (315–430) 470 430 (400–535) Setae bundles 87 (70–110) 170 131 (100–170) 125 Oral sucker 50 (45–60) 41 45 (42–48) 54.2 Breadth oral sucker 45 (33–55) 41 (38–45) 54.9 Ventral sucker 44 (35–55) 40 38 (34–43) Breadth ventral sucker 42 (30–55) 35 (32–40) Pharynx 28 (18–33) 24 (20–30) Pharynx breadth 23 (15–27) 21 (18–26) Oesophagus 40 (30–50) 32 (26–40) Caeca 76 (60–90) 111 (90–130) 74 L. Gargouri Ben Abdallah et al.

Fig. 4. Principal components analysis using metrical data of 60 cercariae (30 from Tapes decussata (T) and 30 from Donax trunculus (D)). recorded as first intermediate host casts some doubt on in particular, the oral sucker being slightly larger than the the conspecificity of all these cercariae. acetabulum, narrow caeca, the excretory system with two On the Tunisian coasts, in addition to finding C. lata in main collecting vessels prolonged by a caudal tubule, a T. decussata, we have found another faustulid cercaria in tail about twice as long as the body and having 27 pairs of D. trunculus. This cercaria presents a strong morpho- setae bundles composed by 7–8 rib-like supports. The logical similarity to C. lata but it differs in some synonymy between C. pectinata and B. bacciger according measurements, in particular those of the tail, the setae to Palombi (1933a, b) is not justified since the bundles and the caeca. To test the significance of these experimental life cycle was not determined. During our differences, we submitted the morphometric features to research on the life cycle of species of Bucephalus principal components analysis. This analysis has demon- (Gargouri Ben Abdallah, 2001) and on the digenean strated that the cercariae of T. decussata and D. trunculus fauna diversity in sparid fish from Tunisian coasts are distinct. Another difference worthy of notice regards (Gargouri Ben Abdallah & Maamouri, 2008) we have the spherules in the excretory vesicle. With about 60 in found two adult faustulids, B. bacciger in Atherina boyeri C. lata, these spherules are more numerous and much and Bacciger israelensis in Boops boops. Only experimentally smaller than in the other cercariae. The number of completed life cycles or molecular analysis will allow the cercariae within the sporocyst, their emergence beha- attribution of each cercaria to an adult stage. viour, the size and seasonal incidence are also different. Cercaria lata shows many affinities with Cercaria plumosa In fact, fewer cercariae (varying from 4 to 17) are found in Sinitzin, 1911, redescribed by Bayssade-Dufour & the sporocysts of C. lata than in the sporocysts from Maillard (1975), collected from Abra ovata (Bivalve, D. trunculus (8–22) (fig. 5). In addition, the size of the Semelidae) from the coastal ponds of the Mediterranean sporocysts from Tapes (at 1450–3600 mm) is slightly littoral of Languedoc. These two cercariae have, in smaller than those from Donax (at 1700–4200 mm). particular, the same number of flame cells (16); but Cercaria lata emerges from the sporocyst by the rupture C. plumosa, in addition to its greater size, is characterized of the lysed wall; however, cercariae of the other species by a higher number of rib-like supports (22–28) of the leave the sporocyst via the birth pore. The highest setae bundles and cephalic glands (12–15 pairs) prevalence of infection was recorded in autumn in distributed on either side of the median plane. The T. decussata and in summer in D. trunculus. Parasites were excretory tubule in the tail, prolonging the excretory absent in winter and spring from T. decussata and only in vesicle, observed in C. lata is replaced by two lines of large winter from D. trunculus. vacuoles in C. plumosa. The strong similarity between these two cercariae Cercaria lata also resembles Cercaria caribbea Cable, 1963 caused Pelseneer (1906) to attribute them to the same collected from Tellina martinicensis (Bivalve, Tellinidae) species. However, the strict specificity of the trematodes and Cercaria laevicardii Cable, 1954 taken from Laevicar- to the first intermediate host is reflected in the previously dium mortoni (Bivalve, Cardiidae). However, these two cited differences which confirm the distinctness of C. lata cercariae are distinguished from C. lata by a higher emerging from T. decussata from the cercaria from number of flame cells (24) (Cable, 1954; Yamaguti, 1975). D. trunculus. This latter cercaria presents the same The cephalic glands, composed of 8–10 pairs in C. lata, are morphology as the C. pectinata described by Huet absent in C. caribbea and C. laevicardii. The number of rib- (1891), Pelseneer (1906) and Matricon-Gondran (1966), like supports of the setae bundle also constitutes a Morphology and behaviour of Cercaria lata 75

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