A. Hadj Taieb *, A. Derbali, M. Ghorbel, N. Ben Hadj Hamida, O. Jarboui

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1 Vie et milieu - Life and environment, 2013, 63 (1): Variation of diet composition of Diplodus vulgaris (Sparidae) from the Gulf of Gabes (central Mediterranean) A. Hadj Taieb *, A. Derbali, M. Ghorbel, N. Ben Hadj Hamida, O. Jarboui Institut National des Sciences et Technologies de la Mer (Centre de Sfax) BP 1035, 3018 Sfax, Tunisie * Corresponding author: aymen.haj.82@gmail.com TROPHIC ECOLOGY TWO BANDED SEA BREAM SOUTHERN TUNISIA ABSTRACT. From March 2008 to February 2010, 2,013 two banded sea bream Diplodus vulgaris (Sparidae) ranging from 5.5 to 25.8 cm in total length (TL), fished in the Gulf of Gabes (south Tunisia, central Mediterranean Sea), were used to investigate feeding habits of the species. This study was based mainly on the variation of the index of relative importance (IRI) with respect to sex, fish size and season. Among 2,013 stomachs examined, 1,374 were empty (vacuity index: %VI = 68.26). This index (% VI) differed significantly across months and declined slightly among the seasons. A total of 22 species representing eight different families belonging to three major groups: molluscs, crustaceans, and echinoderms, were identified in stomach contents of Diplodus vulgaris. This species is primarily a generalist carnivorous fish with a diet consisting of a wide range of species. Molluscs were found in the majority of stomachs, with a total relative importance (% IRI) of %. The Pectinids were the most important bivalve family (% IRI = 8.49), while crustaceans were the second most important food category consumed (19.07 %). There were significant differences in the diet between males and females through the seasons and between juveniles and adults. INTRODUCTION MATERIALS AND METHODS The two banded sea bream Diplodus vulgaris (Geoffroy Saint-Hiliaire, 1817) is a demersal species distributed in the Mediterranean and along the eastern Atlantic coast from France to Senegal, including the Madeira, the Azores and the Canaries Archipelagos (Bauchot & Hureau 1986, 1990). It can be found close to rocky and sandy bottoms to a maximum depth of 160 m. Juveniles often live in coastal lagoons and estuaries (Monteiro 1989) and it is considered a resident species in artificial reefs (Santos 1997). There are no reliable statistics on D. vulgaris landings on the Tunisian coasts. The entire genus Diplodus is mixed in one statistical category. Currently, this species is still abundant in the Gulf of Gabes (south of Tunisia) and it is an economically important demersal species. However, despite its abundance, very little is known about the trophic ecology of this species in the Gulf of Gabes. In the Atlantic Ocean, off the south-west coast of Portugal, Gonçalves & Erzini (1998) studied the diet of D. vulgaris. Ara (1937), Rosecchi (1987), Rosecchi & Nouaze (1987), Sala & Ballesteros (1997), Pallaoro et al. (2006) and Osman & Mahmoud (2009) studied the feeding habits of D. vulgaris in the Mediterranean Sea and Bradai et al. (1998), mainly along the Tunisian coasts, provided qualitative descriptions of the diet of D. vulgaris. The purpose of the present study was to investigate the diet and feeding habits of D. vulgaris in the Gulf of Gabes, including the effects of predator sex, size and season on stomach contents. In the Gulf of Gabes, from the parallel 35 N to the Tunisian- Libyan border (Fig. 1), Diplodus vulgaris is caught mainly by different types of artisan fishing gears (seine nets, gill nets, fyke nets); 2,013 specimens collected monthly between March 2008 and February 2010 ranging in size from 5.8 to 25.6 cm were examined fresh (1,012 males, 777 females, 40 intersexual individuals and 184 fish could not be determined macroscopically) (Table I). Immediately after capture, the total length (TL) of each fish was measured to the nearest 0.1 cm and weighed to the nearest 0.1 g. The analysis of stomach contents was made after storage in 4 % formalin. Prey were identified to the lowest possible taxon Fig. 1. Geographical position of the Gulf of Gabes (Tunisia).

2 54 A. HADJ TAIEB, A. DERBALI, M. GHORBEL, N. BEN HADJ HAMIDA, O. JARBOUI Table I. Sampling data of two banded sea bream Diplodus vulgaris caught from Gulf of Gabes (Tunisia), size range and % of empty stomachs (March 2008-February 2010). Month N Average Females Size range % Empty stomachs N Average Males Size range % Empty stomachs March April May June July August September October November December January February N: number of fish collected and weighed (wet) to the nearest g. Numerous indices have been calculated to quantify the importance of different prey items in the diet of fish. Dietary descriptions of fish and other aquatic vertebrates are greatly influenced by the choice of method used to quantify the relative importance or contribution of each prey type to the diet. This is because the most commonly used methods (frequency of occurrence (% O), numerical abundance (% N) and weight estimations (% W)) convey different types of information on feeding habits (e.g., MacDonald & Green 1983, Bigg & Perez 1985, Cortés 1997). This limitation of single indices led Pinkas et al. (1971) to propose the index of relative importance (IRI) a compound index that describes the relative contribution of stomach contents to the diet. Cortés (1997) proposed to include the IRI standardized to 100% (% IRI), in addition to reporting the three single measures (% O, % N and % W), to facilitate comparisons between dietary studies. The percentage index of relative importance puts results into a common metric, more amenable for use in diet comparisons and calculation of other trophic indices. In the present study, the following indices were used: Vacuity index (% VI) = number of empty stomachs 100/total number of examined stomachs; Percentage frequency of occurrence (% O) = number of stomachs in which a food item was found 100/the total number of full stomachs; Percentage numerical abundance (% N) = number of each prey item 100/the total number of prey in all stomachs; Percentage gravimetric composition (% W) = wet weight of each prey item 100/the total wet weight of stomach contents. The main food items were determined using the index of relative importance (IRI): IRI = % O (% N + % W). This index was expressed in percentage as follows: % IRI = (IRI/ IRI 100). Prey species were sorted in decreasing order according to IRI and the cumulative %IRI was calculated and recorded for the major forage categories (Hyslop 1980) and compared among different groups according to size, season and sex. This index was examined for four size-groups that corresponded to juveniles ( 10 cm TL), sub-adults (10 < TL cm 15) and adults (15 < TL cm 20 and > 20 cm TL) of Diplodus vulgaris (Hadj Taieb et al. 2012). Statistical differences (P < 0.05) in diet composition with respect to length-class and season were assessed by the Chisquare test of the frequencies of a given prey (Sokal & Rohlf 1981). The variation in vacuity index (% VI) was also tested using the Chi-square test over a contingency table of the number of empty stomachs. RESULTS Feeding intensity Among 2,013 stomachs of Diplodus vulgaris examined, 1,374 were empty (VI% = 68.26). The proportion of empty stomachs varied significantly over the year (χ² = 40.43, P < 0.05). The highest percent of empty stomachs was found in June (82.78 %) and July (77.97 %), while the lowest was observed in January (55.56 %) (Table I). The proportion of empty stomachs was not significantly different among the two size-classes (χ² = 0.31, P > 0.05), and corresponded to juveniles (VI % = %) and adults (VI % = %), respectively.

3 FEEDING HABITS OF DIPLODUS VULGARIS 55 Diet composition Five major prey groups: molluscs, crustaceans, echinoderms, annelids and teleosts were identified in the stomach contents of Diplodus vulgaris. A total of 22 species representing 8 different families were identified. Molluscs constitute the most frequently observed group, with 59.1 % of the total % IRI, followed by crustaceans (%IRI = 19.1), while the other taxa, i.e. Spongia and Plantae were scarcely found (%IRI < 1) (Table II) and for this reason are not indicated in all figures. At the family level, Pectinidae was the major prey consumed by D. vulgaris (% IRI = 8.5), followed by Nereidae (Nereis sp.) (% IRI = 4.3) and Sepiidae (% IRI = 3.6) (Table II). Diet composition in relation to sex Overall, molluscs had a higher percentage of IRI than crustaceans. The % IRI of molluscs and crustaceans in female two banded sea bream (67.3 % and 15.4 %, respec- Table II. Diet composition of Diplodus vulgaris of the Gulf of Gabes (Tunisia). Group Family Item (species) O% N% W% IRI IRI% Crustaceans Isopoda Cymodoce truncata Sphaeroma sp Gammaridae Ampelisca diadema Panaeidae Metapenaeus monoceros Trachysalambria curvirostris Processidae Processa edulis Non-identified shrimps Carididae Carcinus maenas Majidae Macropodia longirostris Amphipoda Gen. Sp Non-identified crustaceans Total crustaceans Molluscs Pectinidae Pecten jacobaeus Flexopecten glaber Chlamys sp Cardiidae Cerastoderma glaucum Non-identified Bivalvia Cerithiidae Cerithium scabridium Bullidae Bulla striata Non-identified Gastropoda Sepiidae Sepia officinalis Total molluscs Echinoderms Echinoidea Hotoloroidea Ophiuroidea Total echinoderms Teleosts Clupeidae Sardinella aurita, Sardina pilchardus Engraulidae Engraulis encrasicolus Gobiidae Gobius niger Mullidae Mullus surmuletus Non-identified Teleosts Total teleosts Annelids Nereidae Nereis sp Spongia Tunicate Ascidiacea Plantae Non-identified

4 56 A. HADJ TAIEB, A. DERBALI, M. GHORBEL, N. BEN HADJ HAMIDA, O. JARBOUI Fig. 2. Diet composition of Diplodus vulgaris in the Gulf of Gabes for males and females, based on the percentage index of relative importance values of the major prey groups: n = number of non-empty stomachs analysed in each sex. crustaceans was comparatively low (% IRI = 2.5). The frequency of crustaceans significantly decreased with increasing size (χ² = 8.2, P < 0.05). Annelids occurred in stomachs of specimens belonging to medium size-class (sub-adults, 10 < TL cm 15). In the large size-class (adults, > 20 cm TL) molluscs represented more than 78 % of the total IRI. Significant differences among size-classes were found for molluscs (χ² = 16.2, P < 0.05), crustaceans (χ² = 8.2, P < 0.05), echinoderms (χ² = 11.7, P < 0.05) and annelids (χ² = 40.2, P < 0.05). Diet composition in relation to season There were some seasonal variations in food habits of D. vulgaris (Fig. 4). Molluscs were the dominant prey group during the seasons. Crustaceans were also present in the stomachs throughout the year, with a peak value recorded in autumn (% IRI = 29.7). Echinoderms were found in winter, autumn and spring. Significant differences among seasons were found for the major prey groups (molluscs: χ² = 29.1, P < 0.05; crustaceans: χ² = 14.9, P < 0.05; echinoderms: χ² = 9.3, P < 0.05; annelids: χ² = 10.5, P < 0.05 and fishes: χ² = 13.6, P < 0.05). Fig. 3. Diet composition of Diplodus vulgaris in the Gulf of Gabes among size-classes, based on the percentage index of the relative importance values of the major prey groups: n = number of non-empty stomachs analysed in each size-class. Fig. 4. Diet composition of Diplodus vulgaris in the Gulf of Gabes throughout the year based on the percentage index of relative importance values of the major prey group: n = number of non-empty stomachs analysed in each season. tively) were similar to that observed in males (63.4 % and 15.1 %, respectively). There were appreciable dietary differences between males and females in prey categories of annelids (χ² = 13.5, P < 0.05) (Fig. 2). Diet composition in relation to fish size Molluscs and crustaceans were the major prey groups present in the diet of all size-classes (Fig. 3). Molluscs were the most important prey group in the large size-class (> 20 cm TL) (% IRI = 78.6), while the contribution of DISCUSSION Dietary studies of Diplodus vulgaris in the Gulf of Gabes, central Mediterranean, show a high proportion of empty stomachs and few prey items per stomach, most of them in advanced stages of digestion. Bradai et al. (1998) reported that the percentage was higher than 88 % on the Tunisian coasts, but it was less than 19 % in the eastern Adriatic Sea (Pallaoro et al. 2006). The high %VI may be related to the fact that captures occurred at night, which is when the fish are most active generally because they are feeding. The individuals caught were hauled onboard the following morning, so some of them may have remained in the net for several hours, and their capture may have occurred before the ingestion of prey or after digestion. As a result, many specimens had an empty stomach at the moment they were collected. Our study indicates that Diplodus vulgaris is a generalist predator that consumes a wide range of prey items. It is mainly a mollusc-based carnivorous species, as are most of the species of the genus Diplodus (Rosecchi 1987, Bradai 2000, Osman & Mahmoud 2009). Its most common prey groups, which represent 59.1 % or more of the total IRI, can be considered as the main food. The other prey groups (i.e. echinoderms, teleosts and annelids) were of minor importance and may be considered as occasional food. The common cuttlefish Sepia officinalis and the Pectinid Pecten jacobeus have the highest index of relative importance in the diet of D. vulgaris. Penaeidae (i.e.

5 FEEDING HABITS OF DIPLODUS VULGARIS 57 Metapenaeus monoceros and Trachypenaeus curvurostris), Isopoda (i.e. Cymodoce truncata) and Clupeidae (Sardinella aurita and Sardina pilchardus) were of secondary importance. Nevertheless in the east Adriatic, D. vulgaris is an opportunistic predator species and feeds primarily on echinoids (Pallaoro et al. 2006). The feeding patterns of Diplodus vulgaris observed in the present study agree well with field distribution patterns of several mollusc species. For example, the Pectinid Pecten jacobaeus, commonly present in Tunisian waters (Zamouri Langar et al. 2011, El Lakhrach et al. 2012), especially in the Gulf of Gabes, was frequently found in the stomachs of this species, whereas, the other molluscs: Cerastoderma glaucum, Pinctada radiata and Cerithium scabridium were less frequently encountered. Diet often changes with geographical area and this was observed for D. vulgaris as well. In the Gulf of Gabes, D. vulgaris seems to have a diet different from that of other areas, with few similarities. In the Atlantic Ocean (Gonçalves & Erzini 1998), the primary food of this species consists mainly of a wide range of small prey which are often very frequent (polychaetes, ophiuroids, amphipods) with large prey being rare (cephalopods). Bradai et al. (1998) also reported that molluscs, crustaceans and echinoderms were present in the stomach contents in the same area. Taken together, the results of these studies confirm the importance of molluscs and crustaceans in the diet of D. vulgaris. Rosecchi (1987) reported that D. vulgaris from the Gulf of Lions is mainly a carnivorous fish. The observed variations suggest that the diet composition of D. vulgaris may be greatly modified in response to the availability of prey and/or different benthic faunal communities in the two areas. Ara (1937) in Naples (Italy) and Quéro (1984) in France reported that the two banded sea bream was a generalist feeder, with crustaceans and molluscs forming the basis of the diet. Bauchot & Hureau (1986) considered this a carnivorous species, feeding mainly on crustaceans, molluscs, and worms. These authors did not attribute much importance to echinoderms and polychaetes, which may be due to regional differences in faunal composition, given the lack of information on feeding selectivity in these studies. In comparison to other Sparidae, the diet of Diplodus vulgaris in the Gulf of Gabes most closely resembles that of Spondyliosoma cantharus (Bradai et al. 1998), both species feeding on molluscs and crustaceans. However, the diet of the Sharpsnout sea bream, Diplodus puntazzo, from the Tunisian coasts (Bradai et al. 1998) and the eastern central Adriatic Sea (Dulčić et al. 2006) were mainly zooplanktonic crustaceans, while Spongids were of minor importance. In this study, the obtained results show that food habits considerably change as fish grow. While the juveniles had a higher proportion of crustaceans in their diet than adults, molluscs were still the dominant prey group for all size classes. Juveniles tended to consume a less diverse range of prey species, comprising mostly zooplanktonic crustaceans (larvae of shrimps, Isopoda and Gammaridae), Annelids and small pelagic fish and fish larvae. Larger specimens appear to become more piscivorous and therefore capable of capturing large teleosts that have a high percentage of stomach content weight. These differences could be attributed to the size of the specimens. Adults of D. vulgaris have diets comprising mostly molluscs, teleosts and crustaceans. In our study, the stomach contents of D. vulgaris showed seasonal variations, but molluscs were the dominant prey group during all seasons. Crustaceans were also present in the stomachs throughout the year, with a peak value recorded in autumn. Echinoderms were found in winter, autumn and spring. In conclusion, D. vulgaris is mainly a carnivorous fish. The diet in the Gulf of Gabes as well as in the north-east Atlantic waters consists mainly of molluscs and crustaceans. The importance of molluscs differed significantly among seasons as well as between small and large sizeclasses. The feeding activity of this species throughout the year was probably related to fish abundance and seawater temperature and spawning period. Future monitoring of the Gulf of Gabes feeding ecology of D. vulgaris could help us better understand the inter- and intra-specific interactions that occur in this region, and how climate change, overexploitation and pollution affect these interactions. Ack n o w l e d g e m e n t s. Special thanks to the technical and supporting staff of INSTM (Centre de Sfax) for their practical assistance in laboratory analysis. We thank N Kallel, an English teacher at the Faculty of Sciences (Sfax), for proof-reading our manuscript. The authors are also grateful to the anonymous referees whose suggestions and comments improved the submitted manuscript. REFERENCES Ara L Contributo allo studio dell alimentazione dei pesci: Sargus vulgaris Geoffr, - Sargus annularis L. Sargus sargus L. Boll Pesca Piscicolt Idrobiol 13(4): Bauchot ML, Hureau JC Sparidae. In Whitehead PJP, Bauchot, ML, Hureau JC, Nielsen J, Tortonese E (eds), Fishes of the North-Eastern Atlantic and the Mediterranean II. UNESCO, Paris: Bauchot ML, Hureau JC Sparidae. In Quero JC, Hureau JC, Karrer C, Post A, Saldanha L (eds), Checklist of the fishes of the eastern tropical Atlantic (CLOFETA). 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