Trematodes in Fishes of the Genus Diplodus

44, Bull. Eur. Ass. Fish Pathol., 33(2) 2013

ȱȱęȱȱȱȱ Diplodus (Teleostei, Sparidae) from Bizerte Lagoon (Northern coast of Tunisia)

R. Antar* and L. Gargouri Ben Abdallah

ȱǱȱȱȬ¢ȱȱ¢ȱ¢ǰȱ¢ȱ ȱǰȱ¢ȱȱȱȱǰȱŘŖşŘǰȱǰȱ

Abstract ȱȱȱȱ ȱȱȱȱȱȱȱŘŘřȱȱęȱȱȱȱ Diplodus (D. annularis, D. puntazzo, ǯȱȱand ǯȱ) sampled from Bizerte Lagoon (NE coast of Tunisia). D. annularis and ǯȱȱwere infected mainly by ȱ and the trematode fauna of ǯȱȱwas dominated by Proctoeces maculatus. Prodistomum polonii, was found ȱȱęȱȱȱD. annularis in Tunisian waters. Most of the trematode species show a broad Ě¡¢ȱȱȱȱȱȱ£ȱěȱȱȱȱȱǯ The exceptions are A. microcirrus, P. polonii and Z. rubellus, which are limited to the stomach, the posterior intestine and the rectum, respectively.

Introduction Diplodus species, in particular sharpsnout sea Fishes of the genus Diplodus (Teleostei, Sparidae) bream (D. puntazzoǼȱȱĴȱȱ- are widespread in the Mediterranean Sea, in the terest for Tunisian aquaculture due to their Black Sea and in the Eastern Atlantic Ocean. All high commercial value. Therefore, a number species are gregarious. D. annularis prefers sand of studies have examined the biology (Bradai sea beds or seagrass meadows, whereas other et al., 1998, 2001; Mouine et al., 2012; Cherif et Diplodus species live on coastal water with rocky al., 2008), growth (Bradai et al., 1998, 2001) and ȱ¢ȱĴǯȱ¢ȱ¢ȱȱȱȱ physiology (Bouhlel et al., 2007, 2009) of these varying from 0 to 150 m (Fischer et al., 1987). ęǯȱ ȱǰȱȱȱȱǰȱȱ Sexual maturity is reached during the second particular, helminths are not well known. So year of life for D. annularis, during the fourth far, only one paper has been published on the year for ǯȱ and ǯȱȱand during the trematodes of Tunisian coastal species of Dip- third year for D. puntazzo (Mouine et al., 2012). lodus (Gargouri Ben Abdallah and Maamouri, ȱ¢ȱȱȱęȱȱȱ ǰȱ- 2008). The aims of the present study are (i) to taceans, echinoderms, molluscs, hydrozoans provide a database of trematodes in Diplodus and algae (Fischer et al., 1987). Diplodus species species in Bizerte Lagoon (NE Tunisia) and ȱȱȱȱȱȱęȱ (ii) to compare this with the presence of these trade of Tunisia and represent a remarkable ȱěȱȱȱȱȱȱȱ resource. Moreover, during the last few years, Mediterranean coastal environments.

* Corresponding author’s email: [email protected] Bull. Eur. Ass. Fish Pathol., 33(2) 2013, 45

Materials and methods pycnoporus, Lepocreadium album, ǯȱ and Between October 2008 and October 2009, a total Prodistomum polonii); Monorchiidae (Monorchis ȱŘŘřȱȱęȱȱȱȱDiplodus were parvus); Opecoelidae (ȱ) and collected in the Bizerte Lagoon (north east of Zoogonidae (Diphterostomum brusinae and Zoo- Tunisia, between 37°8’ and 37°16’N and 9°46’and ȱ) (Figure 1). 9°56’E (Dellali et al., 2001)) by Menzel Abder- ȱęǯȱȱęȱ ȱęȱȱ Most of the collected parasites were found in accordance to Fischer et al. (1987) and included several Diplodus species and therefore do not 130 individuals of D. annularis, 8 individuals of ¡ȱȱȱȱę¢ȱǻȱŗǼǯȱA. mi- D. puntazzo, 19 individuals of ǯȱȱand 66 crocirrus, P. polonii and Z. rubellus were limited individuals of D. . ȱȱęȱȱȱȱȱǰȱǯǯȱȱ stomach, the posterior intestine and the rectum, The specimens were measured, weighed and respectively. In contrast, the distribution of the dissected. The digestive tract was removed ȱȱȱ ȱȱěȱȱ ȱȱȱěȱȱǻoesophagus, showed wider distributions, and these species stomach, pyloric caeca, duodenum, mid-intes- ȱȱȱȱȱ ȱěȱȱȱȱ tine, posterior intestine, rectum) and examined intestine (Table 1). Thus, these parasites appear for trematodes under a binocular microscope. not to be very restrictive in their requirements, The localisation in the digestive tract for each although their niche dimensions within the individual was noted. The collected parasites digestive tract were variable according to the were studied either directly in vivo under the host species. Thus, the ecological niche of M. stereomicroscope or conserved for observation was limited to the mid-intestine in D. ǯȱȱȱ ȱę¡ȱȱȂȱĚȱ , whereas it extended to the duodenum between a slide and a coverglass, washed with and mid-intestine in ǯȱ and to three distilled water, stained with boric carmine, de- parts of intestine in D. annularisǯȱȱě- hydrated in a series of alcohol (70%, 95%, 100%), ences between hosts were found for D. brusinae, cleared in Gaulteria oil and mounted between H. pycnoporus and ǯȱȱ(Table 1). a slide and a coverglass in Canada balsam. Drawings were made using a light microscope Diplodus annularis, and to a lesser degree D. equipped with a drawing tube. , have the most diverse trematode fauna each hosting 10 and 8 species, respectively. D. Prevalence, mean intensity and abundance were harboured only 4 trematode species, calculated according to Bush et al. (1997). whereas in D. puntazzo we observed no trematode species, perhaps because of the small Results sample size (n = 8). The trematode fauna of D. In total, 11 species of trematodes belonging to annularis and ǯȱ were dominated by six families were found in the digestive tract of ǯȱ, and P. maculatus was the most Diplodus spp., i.e. Derogenidae (Arnola microcir- frequent parasite in ǯȱ (Table 1). rus); Fellodistomidae (Proctoeces maculatus and ȱ); Lepocreadiidae (Holorchis 46, Bull. Eur. Ass. Fish Pathol., 33(2) 2013

Figure 1.ȱ ȱȱěȱȱȱȱęȱȱȱDiplodus genus found in Bizerte lagoon. Bull. Eur. Ass. Fish Pathol., 33(2) 2013, 47

Table 1. Global Epidemiologic values (Prevalence: P (%), Abundance: A and Mean intensity: MI) of trematodes from Diplodusȱǯȱěȱ£ȱȱȱ ȱȱȱǻ ȱȱȱȱȱŘŖŖŞǼǯȱǰȱ oesophagus; B, Stomach; C, pyloric caeca, D, duodenum; E, mid-intestine; F, posterior intestine G, rectum.

Gulf of Tunis Hosts Parasite species Present work (Gargouri and Maamouri, 2008) Sites P(%) A MI Sites P(%) A MI Arnola microcirrus B 0.8 0.01 1.0 Diphterostomum brusinae DFG 14.6 0.50 3.5 G 16.17 0.51 3.18 Holorchis pycnoporus DF 3.8 0.08 2.2 Lecithocladium excisum B 2.94 0.04 1.5 Diplodus Lepocreadium album ACF 11.5 0.40 3.8 DE 2.94 0.07 2.5 annularis ȱ CD 2.3 0.03 1.7 C 4.41 0.10 2.33 n= 130 ȱ DEF 13.1 0.40 3.3 DE 10.29 0.19 1.85 Monorchis parvus CD 8.5 0. 30 3.9 CD 44.12 4.11 9.63 Prodistomum polonii F 0.8 0.02 3.0 ¢ȱę E 2.94 0.07 2.5 ȱ D 0.8 0.01 1.0 ȱȱ G 0.8 0.01 2.0 G 1.47 0.01 1 Monorchis monorchis C 12 1.54 12.83 Diplodus Peracreadium characis De 18 0.50 2.77 puntazzo Proctoeces maculatus G 2 0.03 2 n= 8 ¢ȱęȱ DE 6 0.08 1.33 Arnola microcirrus B 1.42 0.01 1 Diphterostomum brusinae F 5.3 0.10 3.0 G 12.86 0.50 3.89 Holorchis pycnoporus DE 7.14 0.11 1.6 Lepocreadium album D 2.86 0.06 2 ȱ CD 10.5 0.10 1.5 Diplodus ȱ E 5.3 0.05 1.0 DE 18.57 0.34 1.87 Monorchis parvus C 1.43 0.04 3 n= 19 Peracreadium characis DE 1.43 0.17 12 Proctoeces maculatus FG 15.8 0.10 1.0 FG 8.57 0.19 2.17 ¢ȱę E 4.29 0.04 1 ȱ G 4.29 0.07 1.66 ȱ G 7.14 0.11 1.6 Diphterostomum brusinae FG 6.1 0.70 12.5 G 18.33 0.52 2.81 Holorchis pycnoporus F 1.5 0.01 1.0 DEF 1.66 0.03 2 Lecithocladium excisum B 1.66 0.02 1 Lepocreadium album C 3.33 0.05 1.5 ȱ D 1.5 0.01 1.0 Diplodus ȱ DE 19.7 0.30 1.5 DE 11.66 0.3 2.57 Monorchis parvus CF 10.6 0.20 1.6 CDEF 41.66 4 9.60 n= 66 Proctoeces maculatus FG 6.1 0.10 2.2 G 6.66 0.2 3 ¢ȱę EF 3.33 0.03 1 ¢ȱ F 1.66 0.02 1 ȱ F 1.5 0.01 1.0 ȱ G 3.33 0.08 2.50 ȱȱ G 1.5 0.04 3.0 G 1.66 0.05 2 48, Bull. Eur. Ass. Fish Pathol., 33(2) 2013

The majority (70.7 %) of the individual hosts (ǯȱȱandȱǯȱ) andȱǯȱ, pre- harboured only one trematode species. Two viously not reported for the Gulf of Tunis. S. trematode species occurred in 22.0 % of the ǰȱȱȱȱęȱȱȱȱȱ hosts, while three and four parasite species oc- Spondyliosoma cantharus (Gargouri Ben Abdallah curred in 3.7% and 2.4% of the host specimens, and Maamouri, 2008), was found in D. annularis respectively. One D. ȱȱęȱ and ǯȱ. Thus, these sparids are new trematode species (D. brusinae, L. , M. recorded host species for this trematode in the , P. maculatus and Z. rubellus) in the Bizerte Lagoon. The abundance of ǯȱ in digestive tract, with three of them (D. brusinae, D. annularis and ǯȱȱwas low and its P. maculatus and Z. rubellus) occupying the same presence may be accidental. Furthermore, P. microbiotope (rectum). polonii, recorded from D. annularis was found, ȱȱęȱǰȱȱȱ ǯȱ¢ȱȱ Discussion ȱǻŗşşŖǼȱȱȱȱȱęȱ Eleven species of trematodes were found as in several families (Carangidae, Centracanthi- parasites in the digestive tract of four Diplodus dae, Gadidae, Engraulidae, Mullidae, Pomato- species in the Bizerte Lagoon. The niche dimen- midae, Scorpaenidae, Soleidae and Zeidae) in sions of these parasites in the digestive tracts the Atlantic Ocean and the Mediterranean Sea ȱȱȱȱ¢ȱȱęȱ ȱȱȱȱęǯȱP. polonii seems to be ȱęȱǯȱǰȱȱȱ a more generalist species. This can be related in the number of parasites in the tract and the to a wide spectrum of the second intermediate saturation of the ecological carrying capacity of host represented by several bivalvia (Bray and ȱěȱȱȱȱȱȱ Gibson, 1990). However, A. microcirrus and H. occupy marginal situations in order to escape pycnoporus have already been described as para- competition (Combes, 1995). Furthermore, the sites of D. annularis, respectively in the Black Sea trophic resources in the intestines are potentially (Gaevskaya and Korniychuk, 2003) and in other abundant and allow a high number of parasite regions of the Mediterranean (Bray and Cribb, species to coexist. Therefore, we hypothesize 1997). As recorded by Kostadinova et al. (2004), that the low species diversity of the infracom- A. microcirrus seems to show morphological munities is most likely dependent on the low ěȱȱȱȱǯȱȱě- rate of transmission of larval stages. ences were considered by these authors to be ȱȱȱȱȬęȱǯȱȱ The species richness and ecological variables like comparison of the frequency of trematode fauna prevalence, abundance and mean intensity were shows that, except for those of L. album,ȱǯȱ- ¢ȱ ȱȱęȱȱ£ȱȱ chis, P. maculatus which were much higher in the compared with those reported for the coastal Bizerte Lagoon, the frequency of the parasites of environments in the Gulf of Tunis (Gargouri other species were greatest in the Gulf of Tunis Ben Abdallah and Maamouri, 2008). New host (Gargouri Ben Abdallah and Maamouri, 2008). species were observed in Bizerte lagoon for A. microcirrus (D. annularis), P. polonii (D. annu- The low abundance of trematodes recorded in laris), H. pycnoporus (D. annularis), ǯȱȱ sparids from the Bizerte Lagoon can be related Bull. Eur. Ass. Fish Pathol., 33(2) 2013, 49 to the availability of the intermediate hosts and terranean (Bartoli and Gibson, 1989; Bartoli and the viability of the free larval stages (cercaria Bray, 1996; Bartoli et al., 1989a, 1989b, 2005; ȱǼȱȱęȱǲȱ Sasal et al., 1999; Ternengo et al., 2005, D’Amico the Bizerte Lagoon represents a receptor of et al., 2006; Kostadinova and Gibson, 2009). ȱĝȱȱȱȱȱ In the Eastern Mediterranean, the trematodes of several industrial wastes ǻęȱȱȬ ȱȱȱęȱȱȱĴȱȱ Shimi, 2004; Ben Said et al., 2010). Sures (2003) (Pogorel’tseva, 1952; Fischthal, 1980, 1982; ȱȱȱȱȱȱȱěȱ Saad-Fares, 1985). The species richness of the by environmental conditions. Pollution may trematode fauna of Diplodus spp. from Bizerte ¢ȱěȱȱȱȱȱȱ Lagoon was higher than those reported from the extinction. In addition, water pollution might eastern Mediterranean coast (Saad Fares, 1985), ȱȱěȱȱȱȱ and lower than those described in the western of heteroxenous parasites and thus reduce para- Mediterranean (Bartoli et al., 2005) (Table 2). The ȱǲȱȱěȱȱȱȱ ȱ¢ȱȱȱȱȱĴȱ parasites and consequently their occurrence to a lack of investigation in the sector or to the and distribution (Sures, 2008). Valtonen et al. Ĝ¢ȱȱ£ȱȱȱȱ¢ȱȱȱ (1997) and Williams and Mackenzie (2003) show parasites on the Lebanese coasts, characterized the existence of correlation between parasite by the absence of lagoons and ponds. abundance and the amount of pollution. Pi- etrock and Marcogliese (2003) believe that the Bartoli et al. (2005) explains the high trematode high concentrations of toxic substances such diversity and frequency of the Scandola nature as metals, deactivate certain enzymes of the reserve by the high general level of biodiversity larvae and consequently reduce their ability (Miniconi et al., 1990; Verlaque, 1990; Merella, to infect a new host. 1991; Verlaque et al., 1999) related to the stabil- ity of the ecosystem (absence of major pollut- The trematode fauna of Diplodus spp. has been ants) and to its direct opening on the Western the topic of many research in the Western Medi- Mediterranean basin.

Table 2. Number of trematodes species from Diplodus ǯȱȱěȱȱǯȱȱȱ size is given in parentheses.

Gulf of Tunis Scandola Nature Present (Gargouri Ben Lebanese coasts Hosts Reserve of Corsica work Abdallah and (Saad Fares, 1985) (Bartoli et al., 2005) Maamouri, 2008) D. annularis 10 (130) 8 (68) - 6 (54) D. puntazzo 0 (8) 4 (60) - 3 (3) ǯȱ 4 (19) 11 (70) 4 (?) 10 (69) ǯȱ 8 (66) 11 (60) 3 (?) 10 (43) 50, Bull. Eur. Ass. Fish Pathol., 33(2) 2013

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