Study of the ichthyofauna diet in the Ichkeul Lake (Tunisia)

Study of the ichthyofauna diet in the Ichkeul Lake (Tunisia) by Moez Shaiek* (1), Mohamed Salah RoMdhane (1) & François Le Loc’h (2) Abstract. – In order to define the structure of trophic network of Ichkeul Lake in Tunisia, diet of main teleost fish species was determined during two seasons, wet and dry. A total of 491 stomachs from 16 teleost species was analyzed. The analysis revealed spatial variability (East under marine influence and West with more continental effect) and temporal one (wet and dry seasons). Based on stomach contents, nine trophic groups were revealed, including eight monospecific groups. The main prey are mudflat snails (Hydrobia ventrosa, H. acuta), bivalves (Abra alba, Cerastoderma glaucum), amphipods and isopods, as well as seagrass (Potamogeton pectinatus, Ruppia cirrhosa) and water brackish algae (Ulva spp. and Chaetomorpha spp., Cladophora sp., Polysiphonia sp.). Résumé. – Étude du régime alimentaire de l’ichtyofaune du lac ichkeul (Tunisie). © SFI Received: 19 Jan. 2015 Accepted: 11 Jun. 2015 Editor: K. Rousseau Key words ichthyofauna Tunisia ichkeul Lake Stomach contents Prey diet Trophic group Afin d’établir la structure du réseau trophique du lac Ichkeul en Tunisie, le régime alimentaire des principales espèces de poissons téléostéens pendant deux saisons, humide et sèche, a été déterminé. 491 individus appartenant à 16 espèces de poissons ont été analysés. L’analyse des contenus stomacaux a révélé une variabilité spatiale (Est sous influence marine et Ouest plus continentale) et temporelle (saison humide et saison sèche). Sur la base des contenus stomacaux, neuf groupes trophiques ont été créés, dont huit sont mono-spécifiques. Les principales proies sont les gastéropodes des vasières (Hydrobia ventrosa, H. acuta), les bivalves (Abra alba, Cerastoderma glaucum), les amphipodes et isopodes, ainsi que les phanérogames (Potamogeton pectinatus, Ruppia cirrhosa) et les algues des eaux saumâtres (Ulva spp. et Chaetomorpha spp., Cladophora sp., Polysiphonia sp.) The trophic structure of ichthyofauna communities is difficult to characterize and to predict because of the diet plasticity according to the availability of food resources (Piet, 1998). The partition of trophic niche was recognized as head main factor in the communities structuring (Schoener, 1974; Ross, 1986; Sibbing et al., 1998). Fish diet informs on the presence, the abundance and the availability of prey, and also on trophic potential of the ecosystem. The strategies of searching food and variations of the species diet from an environment to another and/or from a season to another one, inform about the fish adaptation capacities in front of the environment constraints (Paugy and Lévêque, 1999). The analysis of stomach contents allows taxonomic identification of the various groups and species belonging to the structure of trophic network and the trophic interactions within the complex ecosystems (Piet, 1998; Paugy and Lévêque, 1999). The importance of the study site lies in its specificity; the ichkeul Lake represents one of the three main components of the ichkeul Park. it is a protected ecosystem recognized for the value of its biological heritage, in particular birds and fish species (BCEOM, 1995). Several studies on the lacutrine ichkeul ecosystem have focused on specific richness and bioecology of some fauna or floral species (BCEOM, 1995; Chaouachi and Ben Hassine, 1998; kraiem et al., 2003; casagranda et al., 2005b; Sellami et al., 2010) but none was interested in the structure and trophic functioning of this ecosystem (except for two works by casagranda et al. (2005b) and casagranda and Boudouresque (2010) that did present a simplified conception of the general functional model of ichkeul ecosystem). The knowledge of ingested preys and feeding habits of fishes in any environment is essential to understand their adaptation to the environmental drivers. This work aims to study spatiotemporal variability of ichthyic community diet of the ichkeul Lake. MATERIALS AND METHODS Study site The ichkeul Lake (80 km2) is situated in the north of Tunisia (37°81’00’’n; 9°83’30’’e). its area varies from a season to another, from 12,000 ha in winter to 8,000 ha in (1) Unité de recherche écosystèmes et ressources aquatiques (UR13aGRo1), institut national agronomique de Tunisie, 43 avenue charles nicolle, 1082 Tunis Mahrajène, Tunisie. [[email protected]] (2) UMR 6539 LeMaR (cnRS/UBo/iRd/iFReMeR), institut universitaire européen de la mer, Technopôle Brest-iroise, Rue dumont d’Urville, 29280 Plouzané, France. [[email protected]] * Corresponding author [[email protected]] Cybium 2015, 39(3): 193-210. Ichthyofauna diet in Ichkeul Lake summer (anPe, 2007). it is supplied by fresh water from a surrounding watershed of 8,000 km2 through seven oueds (rivers), and it is connected by Tinja canal along 5 km to the Bizerta lagoon, which opens on the Mediterranean Sea (Fig. 1). The average depth is 1 m with a maximum of 2 m registered in winter period. in summer, the high evaporation lowers the water level, which allows water of Bizerta lagoon dumping in the lake. The salinity shows considerable seasonal variability from 3 near the oued outfalls during springtime, to more than 45 on the Tinja channel (canal) during autumn season. Salinity and temperature were measured on the site during sampling trips using portable multimeter (Thermo orion meter, model 115a+). The sampling was designed as to cover whole lake sectors, by considering the oued embouchures, the variation of water level, the influence of fresh and/or marine water and finally the variability of macrophytes cover. Samples were performed in two seasons from March 2011 to april 2012; dry season from June 2011 to november 2011, wet season from March 2011 to May 2011 and from december 2011 to April 2012. For stomach content analysis, the fish specimens were collected by means of benthic dragnet (meshes of 10 mm) and trammel nets (meshes of 26/28 mm and 30/40 mm). These nets are deployed in the morning and recovered at the end of the day. additional commercial fish samples were collected from catches of “Tunisie lagunes company”, the only owner exploiting fishes of the lake. The fishing means vary between trammel nets (mesh of 30/40 mm), traps and fyke nets (capéchades) (mesh of 6 mm), fixed gillnet (eels dams) and fixed fisheries (weir deployed nearing Tinja canal sluice). Shaiek et al. nets are deployed in the afternoon before sunset and are recovered the following day in the morning. nets are deployed monthly to have seasonal samples covering all over the lake surface, as much as possible. The wet season is considered from december to May, while the dry season is defined from June to November. The small sizes species are sampled by means of dragnet, seine net and larvae net. as possible, from 15 to 20 individuals per species are collected to obtain 10 full stomachs. Sample processing The sampled individuals were beforehand weighed and their standard length (LS) was measured to the nearest millimetre. in the laboratory, each stomach was opened into a Petri dish before being kept preserved in ethanol solution. The observation of the stomach contents was realized under a binocular microscope. Preys were sorted and identified to the species level when possible. Stomach content analysis Several methods can be used for fish stomach content analysis. The choice of these methods must be in agreement with the studied objective and the type of required data (hyslop, 1980). For our study, the volumetric method of estimation was used (hynes, 1950; Rounsefell and everhart, 1953; Fao, 1974). Within the study framework, we opted for a volumetric analysis method, the method of points (Rounsefell and everhart, 1953; Fao, 1974). it is a variant of the visual estimation method. instead of directly evaluating volume using eyesight, a number of points were given for each item (prey) found in the stomach according to its volume. The category having the highest volume in the stomach content will have a Figure 1. - Geographic location of ichkeul Lake: its water network and its communication with Bizerta lagoon. 194 Cybium 2015, 39(3) Shaiek et al. maximum of 16 points. other items will have points varying between 8, 4, 2, 1 and 0 according to their volume compared to the major prey category. The volume percentages of each prey were then calculated (hynes, 1950; Rounsefell and everhart, 1953; Fao, 1974). For each prey item, its volume percentage (%V) was calculated using the following formula: % V prey volume (i) = [number of points for prey (i)/(number of points for all preys)] x100. The results of the stomach content analysis were quantified using numerical indexes (hynes, 1950; Fao, 1974; hyslop, 1980). The most known index is the Frequency index (iF): iF = ni/n x 100, where ni is the number of stomach contents for the species i, and n is the number of non-empty analyzed stomachs. For each fish species, we expressed the volume percentages (%V) of preys, which constitute its diet. The vacuity coefficient (Cv) is the ratio of the number of empty analyzed stomachs ne relative to the total number of analyzed stomachs by each species nt. cv = ne/nt, where nt is the total number of analyzed stomachs per species and ne the number of empty analyzed stomachs. Statistical analysis diet variations were studied according to the sector and season sampled for each species. Diet similarities between the different fish species were evaluated using the simplified Morisita index, proposed by horn (1966), which is also known as the horn-Morisita index (krebs, 1999). This similarity index was calculated using the reconstruction of the weight data using the following formula: cmh is the similarity index of horn-Morisita between the predator species a and B; S is the total number of prey species identified in the two predators diets, Pa,i is the reconstituted average weight proportion of prey i consumed by species a and PB,i is the reconstituted average weight proportion of prey i consumed by species B (Potier et al., 2007). The similarity index varies between 0 (no preys in common) and 1 (complete similarity) for a similarity threshold generally set at 0.6 for a “significant” similarity between two species (Zaret and Rand, 1971). cmh was calculated within a 95% as confidence interval. The diet similarity matrix of cmh index was completed by a hierarchical ascendant classification (hac) using 1 – cmh (euclidian distance, single link) in order to identify groups having similar diets (Zaret and Rand, 1971). Cybium 2015, 39(3) Ichthyofauna diet in Ichkeul Lake a correspondence analysis (ca) (Benzécri, 1973; Benzécri and Benzécri, 1984) based on the abundance and occurrence of prey species was used to examine the trophic tendencies of the sampled species. The aim of this analysis was to find groups with similar diet affinities. The CA, the similarity indices and the hac were performed using Past software version 3.0.1 (hammer et al., 2001). RESULTS Environmental characteristics The annual temperature of ichkeul Lake varies between 33.8°c in summer and a minimum of 10.1°c in winter. There is some thermal variation between eastern and western sectors of the lake. The temperature is slightly hotter in the eastern sector during the months of July, august and September, as well as months of February and april (Fig. 2a). The annual salinity oscillates between salty marine waters during hot season and freshwater during cold season, with autumn maximum at 37.5 and winter minimum at 0.2. The eastern and western parts are characterized by highly different salinity from May to September, with eastern zone having the highest salty rates (Fig. 2B). Figure 2. - evolution of the average temperature (°c) (a) and salinity (B) in both East and West sectors of Ichkeul Lake during the sampling period. 195 Ichthyofauna diet in Ichkeul Lake Stomach content analysis a total of 491 individuals belonging to 16 actinopterygii fish species were analyzed during this study. Identification has allowed us to recognize nine marine species (i.e. having a part of life cycle in the sea; Anguilla anguilla (Linnaeus, 1758) (ana), Dicentrarchus labrax (Linnaeus, 1758) (dil), Belone belone (Linnaeus, 1761) (Beb), Solea senegalensis (kaup, 1858) (Sos), Engraulis encrasicolus (Linnaeus, 1758) (ene), Mugil cephalus (Linnaeus, 1758) (Muc), Liza ramada (Risso, 1827) (Lir), Liza aurata (Risso, 1810) (Lia) and Liza saliens (Risso, 1810) (Lis), six sedentary species (i.e. living their entire life cycle within the lake; Aphanius fasciatus (Valenciennes, 1821) (apf), Atherina boyeri (Risso, 1810) (atb), Pomatochistus microps (krøyer, 1838) (Pom), Syngnathus abaster (Risso, 1827) (Syab), Syngnathus acus (Linnaeus, 1758) (Syac) and Syngnathus typhle (Linnaeus, 1758) (Syty) and one freshwater species (i.e. living a part of their life cycle in the rivers; Barbus callensis (Valenciennes, 1842) (Bac)) were represented in our sampling. Shaiek et al. The 16 species were collected during the two seasons, but in different quantities. 256 and 235 stomachs were analyzed, during the dry season since June 2011 to november 2011, and during the wet season since december 2011 to May 2012, respectively. The annual vacuity rate cv for all species varied between 0% (L. ramada, E. encrasicolus, P. microps, A. fasciatus) to 33% (A. anguilla). This index showed a high variability between species, sectors and seasons (appendix i). Fish diets The Garfish needle (B. belone) was characterized by diet based on insects (%V > 30%) and peracarid crustaceans (%V = 40%). The diet of D. labrax was more diversified with the dominance of animal fraction essentially constituted by fish (%V = 30%) and animal debris (%V > 25%). The anchovies were characterized by a zooplankton dominated diet (%V > 70%). P. microps presented a more diverse diet composed basically by zooplankton (%V = 45%), zoobenthos (%V = 23%) and amphipod/isopod crustaceans Figure 3. - General annual evolution in the volumetric percentages (%V) of the prey categories found in the stomach contents of ichkeul fish species (the number of non-empty stomachs analyzed for each species is indicated above each species. Ana: Anguilla anguilla, apf: Aphanius fasciatus, atb: Atherina boyeri, Bac: Barbus callensis, Beb: Belone belone, dil: Dicentrarchus labrax, ene: Engraulis encrasicolus, Lia: Liza aurata, Lir: Liza ramada, Lis: Liza saliens, Muc: Mugil cephalus, Pom: Pomatochistus microps, Syab: Syngnathus abaster, Syac: Syngnathus acus, Syty: Syngnathus typhle and Sos: Solea senegalensis. 196 Cybium 2015, 39(3) Ichthyofauna diet in Ichkeul Lake Shaiek et al. Table I. - Horn-Morisita index of diets similarity between fish species sampled in Ichkeul Lake. Significance reported to Cmh > 0.6. ene Pom Syt Beb dil Sos Bac apf atb Muc Lir Lis Lia ana Syab Syac ene 1 0.84 0.69 0.02 0.14 0.17 0.16 0.29 0.11 0.29 0.32 0.26 0.23 0.12 0.45 0.75 Pom Syt Beb dil Sos Bac apf atb Muc Lir Lis 1 0.84 0.34 0.17 0.39 0.32 0.53 0.35 0.37 0.35 0.31 0.22 0.09 0.46 0.62 1 0.45 0.63 0.55 0.53 0.62 0.15 0.19 0.20 0.21 0.27 0.21 0.14 1 0.91 0.85 0.86 0.61 0.72 0.70 0.74 0.61 0.62 0.50 1 0.95 1 0.71 0.80 1 0.68 0.68 0.51 1 0.66 0.73 0.58 0.73 1 0.55 0.22 0.63 0.49 0.67 0.67 0.33 0.41 0.38 0.36 0.29 0.53 0.69 1 0.47 0.51 0.52 0.41 0.40 0.47 0.40 0.41 0.40 0.62 0.31 1 0.71 0.72 0.75 0.85 0.86 0.87 0.78 0.62 0.56 1 0.84 0.48 0.58 0.53 0.52 0.40 0.77 0.47 (%V > 15%). S. typhle showed a diet essentially composed by zooplankton (%V = 38%) and amphipod/isopod crustaceans (%V > 35%) (Fig.3). S. acus fed on almost equal quantity on zooplankton (%V = 40%) and vegetals (macrophytes/ algae; %V = 42%), whereas S. abaster ingested a more important animal fraction (%V > 70%) mainly composed by animal debris (%V > 30%), zooplankton (%V = 20%) and micro-gastropods (%V = 10%) (Fig. 3). The food diet of A. anguilla was mainly composed by bivalves (%V = 30%), macrophytes/algae (%V > 35%) and to a less extent by crustaceans (%V = 10%) and fish (%V = 10%). Mullets were characterized by a common trophic spectrum for the four Mugilidae species (L. aurata, L. ramada, L. saliens and M. cephalus). This food spectrum was essentially composed by macrophytes/algae (%V = 20-40%), zoobenthos (%V = 10-15%) and gastropods (%V > 10%). The ingested sediment fraction showed different contribution in each species and varied between 10% (L. aurata) to 25% (M. cephalus). The Barb B. callensis showed a diet which mainly included peracarid crustaceans (%V = 15-35%), various animal debris (%V = 6-20%) and a vegetal fraction (%V = 10-25%). The Big-scale sand smelt A. boyeri exhibited a prey gastropods contribution (Hydrobia spp.) of 20%, while the South european Toothcarp A. fasciatus was characterized by a diet with less gastropods (1%) and amphipod/isopod crustaceans (%V = 25%) contributions (Fig. 3). The S. senegalensis diet was the more diverse, with an important predation on benthic crustaceans (%V = 15-40%), Nereis diversicolor (%V = 7%), insects, hydrobies and meiofauna. The different sampled and identified preys in the fish fauna stomach contents are detailed in table ii. Their voluCybium 2015, 39(3) 1 0.44 0.60 0.59 0.58 0.47 0.67 0.43 1 0.89 0.92 0.80 0.52 0.58 0.54 1 0.98 0.96 0.72 0.77 0.74 Lia ana Syab Syac 1 metric prey contributions (%V) and occurrence coefficients (iF) are summarized in table iii. Trophic groups Inter-species diet similarities at the threshold of 0.60 for horn-Morisita index, the hac revealed nine trophic groups among them, eight were monospecific: B. belone, E. encrasicolus, P. microps, S. typhle, S. acus, S. abaster, A. anguilla and D. labrax (Fig. 4). B. belone had a carnivorous diet with an affinity for insects, while E. encrasicolus was zooplanktonophagous and P. microps was carnivorous with an affinity for zooplankton. The trophic categories resulting from this stomach content study (Figs 5, 6) were different from those mentioned in the other studies (appendix ii). The environment, trophic potentialities, and availability of preys influence the trophic behaviour of fish species in the living space. B. belone had a carnivorous diet with an affinity for insects, while E. encrasicolus was zooplanktonophagous and P. microps was carnivorous with an affinity for zooplankton. among Syngnathidae, the diet of S. typhle was very different from the other representative of its family, with an affinity for amphipods/isopods/zooplankton. Whereas, the other two Syngnathidae presented diets with zooplanktonic affinity. eel was distinguished by its benthophagous carnivorous diet, while the european seabass presented piscivorous affinity. The remaining species constituted a large multispecific cluster, which grouped the four Mugilidae species, as well as the barb, the big-scale sand smelt, the South european toothcarp and the sole. Mugilidae presented the highest inter-species similarity (chm between 0.8 and 0.98). The same observation was also noted for B. callensis and 197 Ichthyofauna diet in Ichkeul Lake Shaiek et al. Table II. - Abbreviations key of the several items (prey) identified in the stomach contents of the Ichkeul fish species. Prey groups abbreviation Bivalves Biv Gastropods Gast Fishes Fish decapod crustaceans Peracarid crustaceans Prey species Ab_alb Cera_gl Debri_biv Hydrobia Gast_debri Moll_ter Fish Shirp deca_crst Crab Pera_crst Pera_debri Ido_balth Sphaero Gamar Worms Worm insects insect Coroph Annel Plath Insect animal scraps Zooplankton anm_scrap Mosqt Chiron Anim_debri Cop Other_zooplk Zooplk Mysid Clado Zoobenthos Zoobent Ostrac Foram Rodo Rupp Plant_seed Macrophtyte Green algae Mphyt/alg Plant_debri Alg_green Micro_benth other Unidentifed Sediment [Substratum] other Other_[Unident] Sedim Sedim nb FAS nb AS nb ES Cv 198 details Abra alba (probably Abra sp. and/or Scrobicularia plana) Cerastoderma glaucum Bivalves debris (Abra alba and/or Cerastoderma glaucum) Hydrobia spp. (H. ventrosa and/or H. acuta) Gastropods debris (probably Haminoea sp.) Terrestrial molluscs (gastropods [snail]) Fish scraps (scales, fins, vertebrae, spines, etc.) Shrimp (probably Atyaephyra desmaresti incidentally juvenile of Parapenaeus longirostris and / or Penaeus sp.) crabs [decapods] (debris, hooks, pincers) (Carcinus aestuarii and / or Potamon algeriense) Peracarid crustaceans debris (amphipods and isopods) Idotea balthica Sphaeroma hookeri Gammarus spp. (Gammarus aequicauda, Gammarus insensibilis and probably Gammarus locusta) Corophium volutator annelids (Nereis diversicolor) Plathelminths insects (insect scraps: hymenoptera wings [Formicidae], scraps, mandibles, coleopera hook [Blaps] or potentially odonata) Mosquito larvae [culicinae] (larvae, nymphs and other forms) chironoms (insects) Various animal debris copepods (oithonidae, acartiidae, potentially Temoridae) other zooplankton (egg, larvae, veliger larvae, artemia, nauplii etc.) Mysid? (Unconfirmed, may be confused with a larval form euphausiids or other decapod) cladocerans (Zooplankton, crustacea, Branchiopoda: several species) ostracods (crustacea, zoobenthos) Foraminifera (benthic protozoa) Rhodophyta (Polysiphonia sp.) Ruppia maritima Plant seeds (probably seeds of Potamogeton maritimus, incidentally seeds (akene) of Ruppia maritima or Scirpus maritimus) Plant debris (Potamogeton maritimus and/or phragmites and potentially terrestrial plant debris) Ulva spp. and Chaetomorpha spp., Cladophora sp.) ([grazing]) microalgae and sediment superficial vegetal film (benthic grazing film ([grazing]) Unidentified; Organic aggregates, Mineral aggregats, calcareous annelid tubules annelids, others Sediment (mud / silt / clay / with sometimes a sand fraction in small proportions) number of full stomach analysed number of analysed stomach number of empty stomach Vacuity coefficient Cybium 2015, 39(3) Marine species A. anguilla D. labrax S. senegalensis B. belone M. cephalus Freshwater species Sedentary species L. ramada L. aurata L. saliens E. encrasicolis P. microps A. fasciatus A. boyeri S. abaster S. acus S. typhle B. callensis %V iF %V iF %V iF %V iF %V iF %V iF %V iF %V iF %V iF %V iF %V iF %V iF %V iF %V iF %V iF %V iF Abra alba 25 0.36 0 0.00 0 0.03 0 0.00 1 0.05 0 0.04 2 0.26 2 0.20 0 0.00 0 0.00 0 0.00 0 0.04 0 0.00 0 0.00 0 0.00 0 0.06 Cerastoderma glaucum 3 0.05 0 0.00 2 0.10 0 0.00 1 0.11 1 0.13 1 0.19 2 0.20 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 4 0.21 Prey Bivalves debris 1 0.05 0 0.00 0 0.00 0 0.00 0 0.09 1 0.09 0 0.02 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.20 0 0.00 0 0.00 4 0.18 Hydrobia spp. 1 0.12 0 0.00 4 0.43 0 0.10 11 0.57 11 0.57 8 0.51 13 0.70 0 0.00 3 0.38 1 0.21 17 0.68 9 1.00 5 0.67 5 0.73 4 0.41 Gasteropods debris 0 0.00 1 0.05 0 0.00 0 0.00 0 0.02 0 0.00 0 0.05 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 Terrestrial molluscs 0 0.00 0 0.00 0 0.00 0 0.00 0 0.05 0 0.00 0 0.02 0 0.05 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.09 Fish 8 0.24 31 0.68 3 0.37 15 0.57 4 0.30 3 0.22 2 0.23 3 0.25 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 5 0.35 Shrimps 1 0.10 1 0.05 2 0.20 0 0.00 0 0.05 0 0.04 0 0.02 0 0.00 0 0.00 0 0.00 8 0.44 0 0.07 0 0.00 0 0.00 0 0.00 1 0.03 crabs 0 0.02 0 0.00 0 0.03 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.06 Peracarid debris 1 0.05 4 0.11 2 0.27 2 0.19 2 0.11 3 0.13 2 0.21 1 0.10 0 0.00 18 0.77 25 0.91 0 0.00 4 0.90 5 0.78 1 0.47 3 0.15 Idotea balthica 2 0.12 0 0.00 0 0.00 7 0.33 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 2 0.25 0 0.00 0 0.00 1 0.13 1 0.09 Sphaeroma hookerisha 2 0.12 0 0.00 14 0.43 14 0.62 0 0.05 1 0.09 1 0.07 1 0.05 0 0.00 0 0.00 0 0.00 9 0.71 0 0.00 0 0.00 2 0.40 4 0.32 Gammarus spp. 3 0.14 0 0.00 7 0.43 4 0.24 0 0.02 0 0.00 2 0.05 2 0.05 0 0.00 0 0.00 0 0.00 19 0.96 2 0.40 1 0.22 27 1.00 7 0.26 Corophium volutator 1 0.10 0 0.00 3 0.37 14 0.62 0 0.00 0 0.00 1 0.05 1 0.05 0 0.00 0 0.00 0 0.00 7 0.61 0 0.00 0 0.00 6 0.73 2 0.15 annelids 0 0.00 0 0.00 3 0.27 0 0.00 1 0.16 0 0.04 5 0.14 3 0.10 0 0.00 0 0.00 2 0.37 0 0.00 0 0.00 0 0.00 0 0.00 2 0.12 Plathelminths 1 0.12 0 0.00 0 0.00 0 0.00 2 0.25 1 0.09 0 0.05 1 0.20 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.06 insects 1 0.17 6 0.26 2 0.23 29 1.00 1 0.23 1 0.17 0 0.12 1 0.15 0 0.00 3 0.23 1 0.16 0 0.07 0 0.00 0 0.00 0 0.00 7 0.65 Mosquito larvae 1 0.07 6 0.16 0 0.00 2 0.24 0 0.05 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 1 0.20 1 0.32 1 0.30 0 0.00 1 0.27 0 0.00 chironoms 0 0.00 0 0.00 2 0.10 2 0.24 0 0.02 0 0.00 0 0.00 0 0.05 0 0.00 5 0.46 1 0.14 0 0.00 2 0.40 1 0.22 2 0.27 1 0.12 animal debris 4 0.14 26 0.58 9 0.50 2 0.29 6 0.41 9 0.39 5 0.30 5 0.35 0 0.00 0 0.00 23 0.64 18 0.93 31 1.00 3 0.56 2 0.33 5 0.24 copepods 0 0.05 1 0.11 0 0.07 0 0.00 3 0.18 2 0.26 1 0.19 1 0.15 11 0.41 0 0.00 0 0.01 0 0.00 4 0.70 7 0.89 10 1.00 0 0.00 other zooplanktons 1 0.07 3 0.21 3 0.30 0 0.00 5 0.30 7 0.48 3 0.49 4 0.45 63 1.00 16 0.77 10 0.63 3 0.68 14 0.90 31 1.00 27 1.00 2 0.18 Mysids 0 0.00 1 0.05 0 0.07 0 0.00 1 0.09 1 0.13 1 0.14 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.11 1 0.27 0 0.00 cladocera 0 0.05 0 0.05 0 0.00 0 0.00 0 0.02 0 0.00 0 0.12 1 0.10 0 0.00 29 0.85 0 0.09 0 0.00 1 0.30 2 0.44 0 0.07 0 0.00 1 0.10 0 0.05 4 0.43 1 0.33 8 0.70 6 0.57 7 0.49 9 0.70 12 0.65 15 0.54 11 0.59 4 0.43 4 0.80 4 0.67 4 0.60 3 0.44 Foraminifera 0 0.07 0 0.00 2 0.30 0 0.00 6 0.61 5 0.52 1 0.12 3 0.35 1 0.24 8 0.77 1 0.07 0 0.11 1 0.30 0 0.00 0 0.00 5 0.24 Rhodophyta 0 0.07 0 0.16 0 0.03 1 0.29 1 0.14 0 0.13 0 0.07 0 0.15 0 0.00 0 0.00 2 0.43 5 0.68 5 0.90 5 0.78 2 0.47 0 0.09 Ruppia maritima 2 0.19 2 0.26 1 0.23 1 0.24 1 0.25 2 0.22 0 0.05 1 0.05 4 0.53 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 1 0.24 Green algae 7 0.40 2 0.26 6 0.40 0 0.05 3 0.48 5 0.52 4 0.35 5 0.55 4 0.35 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.07 5 0.53 Plant debris 28 0.79 8 0.63 13 0.87 3 0.29 13 0.84 26 0.96 34 0.88 23 0.90 2 0.29 0 0.00 11 0.64 14 0.96 21 1.00 38 1.00 9 0.73 18 0.79 Plant seeds 0 0.05 0 0.11 0 0.07 0 0.00 1 0.18 0 0.09 0 0.09 0 0.15 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 1 0.26 Benthic mircoalgae 0 0.00 0 0.00 0 0.00 0 0.00 0 0.05 0 0.00 1 0.09 0 0.05 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.00 0 0.09 others 1 0.10 4 0.42 10 0.97 2 0.38 4 0.45 4 0.35 6 0.67 1 0.10 3 0.47 3 0.23 3 0.21 1 0.07 0 0.00 0 0.11 0 0.07 5 0.35 4 0.19 3 0.26 5 0.13 1 0.14 24 0.80 12 0.52 10 0.40 15 0.45 0 0.00 0 0.00 0 0.11 0 0.00 0 0.00 0 0.00 0 0.00 9 0.47 100 - 100 - 100 - 100 - 100 - 100 - 100 - 100 - 100 - 100 - 100 - 100 - 100 - 100 - 100 - 100 - Sediment 199 Total Ichthyofauna diet in Ichkeul Lake ostracoda Shaiek et al. Cybium 2015, 39(3) Table III. - Volumetric percentage contribution (%) and occurrence coefficient (IF) of prey ingested by Ichkeul fish species. Ichthyofauna diet in Ichkeul Lake Shaiek et al. Figure 4. - hierarchical cluster analysis (HCA) of fish species according to their diet. The threshold value of HornMorisita distance adopted to extract groups was 0.6. See figure 3 for species names. S. senegalensis (chm = 0.91) as for A. boyeri and A. fasciatus (chm = 0.84) (Tab. i). Spatio-temporal diet variability The individuals caught in the West were distinguished by a less important vegetal fraction than those caught in the east of the lake. The eel food diet was marked by an interseasonal and an intersectoral variability (Fig. 5a). during the dry season, the hca showed a clear inter-sector differences; eel consumed more bivalves in the West than in the east part of the lake (Fig. 8). A. fasciatus showed a stable diet profile during the different seasons with equal contributions of plant, zooplankton, zoobenthos, animal debris and amphipod/isopod crustaceans (Fig. 5B). The big-scale sand smelt A. boyeri exhibited low diet variability along the two seasons in the same lake sector. however, the contribution of micro-gastropods (Hydrobia ventrosa) was more important ( > 20%) in the West, while in the east it is characterized by a more important amphipod/ isopod contribution ( > 50%) (Figs 5c, 8). For the barb, the wet season was marked by more important plant contribution than the dry season. The peracarid crustacean fraction varied between the West (16-18%) and the East (6-7%) (Fig. 5D). The bivalve contribution (12-14%) in the eastern sector 200 (wet season) and the western sector (dry season), respectively, as well as that of insects (6-9%), in the eastern part (wet season) and the western part (dry season), respectively, are to be underlined. in the eastern sector, B. callensis exhibited a food diet rich in macrophytes/algae, crustaceans and bivalves, while in the western sector the animal fraction was more important and more diverse with an affinity for gastropods. during the wet season, B. belone showed a diet essentially composed by insects and amphipods/isopods; the species was characterized by its affinity towards peracarid crustaceans and insects (Fig. 7). These two prey categories represented more than 80% of the species food diet. during the dry season, B. belone showed a diet with more important insect and fish contributions in the eastern than in the western part. D. labrax was characterized by an ichthyophagous diet. These prey proportions varied between 23% in the East sector-Dry season (ED) to 45% in the West sector-Wet season (WW). The animal fraction varied also according to season and sector sampled between 75% (ed) to 84% in the West sector-Dry season (WD) (Figs 5F, 7, 8). a pronounced variability in the diet composition of S. senegalensis appeared; during the wet season, amphipods and isopods fraction was very important. during the dry season, gastropods, plant and sediment fraction were dominant Cybium 2015, 39(3) Shaiek et al. Ichthyofauna diet in Ichkeul Lake Figure 5. - Spatiotemporal evolution of volumetric percentages (%V) of the different prey categories found in the stomach contents. A: Anguilla anguilla; B: Aphanius fasciatus; C: Atherina boyeri; D: Barbus callensis; E: Belone belone; F: Dicentrarchus labrax; G: Engraulis encrasicolus; H: Solea senegalensis, in the Ichkeul Lake. ED: East sector-Dry season; EW: East sector-Wet season; WD: West sector-Dry season; WW: West sector-Wet season; n = N: number of non-empty analyzed stomachs for each species. Cybium 2015, 39(3) 201 Ichthyofauna diet in Ichkeul Lake Shaiek et al. Figure 6. - Spatio-temporal evolution of volumetric percentages (%V) of the different prey categories found in the stomach contents. A: Liza aurata; B: Liza ramada; C: Liza saliens; D: Mugil cephalus; E: Pomatoschistus microps; F: Syngnathus abaster; G: Syngnathus acus; H: Syngnathus typhle, in the Ichkeul Lake. ED: East sector-Dry season; EW: East sector-Wet season; WD: West sector-Dry season; WW: West sector-Wet season; n = N: number of non-empty analyzed stomachs for each species. 202 Cybium 2015, 39(3) Shaiek et al. Ichthyofauna diet in Ichkeul Lake Figure 7. - correspondence analysis (CA) between fish species and food diets during the wet season. The additive symbol attributed for each species referred to sectors; [e] for eastern sector and [W] for Western sector. Figure 8. - correspondence analysis (ca) between fish species and food diets during the dry season. The additive symbol attributed for each species referred to sectors; [e] for Eastern sector and [W] for Western sector. Cybium 2015, 39(3) 203 Ichthyofauna diet in Ichkeul Lake Figure 9. - Structural diagram of the ichkeul Lake trophic web and trophic relationships (prey-predator) between ichthyofauna and their main prey (thick line = high predation; single line = ordinary to low predation; dashed lines: larvae + juvenile of fishes (Predation fish to fish), thick dashed line = hight predation, thin dased line = ordinary to low predation). 204 Shaiek et al. (Fig. 5h). The macrophytes and algae percentages varied between both lake sectors, but this variability was not the same for the four mugilid species. This prey variability was more important in the western part than the eastern one for L. aurata, when it was more important in the eastern sector than in the western one for L. ramada and L. saliens (Fig. 6a-c). The diet composition was characterized by little changing percentages across sectors and seasons for M. cephalus (Fig. 6d). in the western sector, L. aurata seemed to ingest more detritus and sediment than in the eastern one. L. saliens and M. cephalus were characterized by a diet with a low variability during the wet season for both sectors (Fig. 7). The diet of the Gobiidae P. microps was distinguished by the presence of six prey categories with same proportions for both seasons in the eastern part of the lake. The inter-seasonal variations of P. microps diet concerned the zoobenthos (between 18 and 38%), zooplankton (between 25 and 50%) and amphipod/ isopod crustaceans (between 16 and 22%) (Fig. 6e). The ca showed that diets of P. microps and S. typhle were characterized by a zooplankton/zoobenthos affinity (Fig. 7). The two Syngnathidae S. abaster and S. acus presented a similar diet in both wet and dry seasons (Fig. 6F, G). Their diet was dominated by macrophytes/algae and zooplankton (Figs 7, 8). The spatio-temporal evolution of the different stomachal analysis indices (nbAS, nbES, Cv) of the different fish species is detailed in appendix ii. Figure 9 shows the main trophic relations linking the principal prey and fishes. it highlights the predation relationships between fish species under the ichkeul lacustrine ecosystem. The main prey were at a lower trophic level compared to fish. They were mainly peracarid crutaceans, gastropods, bivalves, worms, zooplankton, zoobenthos, macrophytes and algae. carnivorous species such as A. anguilla and D. labrax occupied particular positions and were characterized by the predation of both high (mainly fish) and low level preys, particularly small-sized prey and fry of other fish species with a lower trophic level (Appendix ii). B. belone was characterized by a more specific and piscivorous diet (appendix ii). Syngnathidae, E. encrasicolus and P. microps occupied monospecific positions, while Mugilidae, S. senegalensis, B. callensis, A. fasciatus and A. boyeri represented multispecific groups in the fish food webs (Fig. 9). Cybium 2015, 39(3) Ichthyofauna diet in Ichkeul Lake Shaiek et al. DISCUSSION Environmental characteristics, sampling Environmental characteristics during this study, temperature and salinity values were typical to the studied environment and presented the same tendancy recorded in previous studies (anPe, 2002-2007; Ben M’Barek and Slim-Shimi, 2002; casagranda and Boudouresque, 2010). in particular, salinity is characterized by important seasonal variations. Temperature tends to show spatio-seasonal variations and the eastern sector appears as the region presenting the lowest temperatures during the whole year, except during the dry months (July, august and September). This tend was already shown by Ben RejebJenhani (1989), Ben Garali et al. (2008) and casagranda and Boudouresque (2010). This could be explained by the influence of water currents introduced across the Tinja oued and its role on marine-lagooner (Bizerta lagoon) water masses mixing in the eastern sector (kraïem et al., 2003; Shili et al., 2007). The western sector and the central zone are less dynamic; they are shallower than the eastern area (BceoM, 1995; Ben M’Barek and Slim-Shimi, 2002; Ben Garali et al., 2008). The large macrophytal (Potamogeton pectinatus, Ruppia cirrhosa) coverage contributes also to heat waters of this region, in particular during the dry session (but still less than eastern temperature during the dry period) when there is the decomposition of a huge quantity of these plants (Shili et al., 2007). The annual salinity oscillates between marine salinity during the hot season and freshwater salinity during the cold season (Ben Rejeb-Jenhani, 1989; casagranda and Boudouresque, 2010). The variability of the surface area and the water level are directly related to the water supplies routed to the lake and mainly to the region pluviometry (BceoM, 1995, Ben M’Barek, 2001; Ben M’Barek and Slim-Shimi, 2002; anPe, 2002-2007; casagranda and Boudouresque, 2010). Trophic diet The choice of volumetric analysis for point method did allow the analysis of fish diets when the microscopic organism measurement (microalgae, zooplankton, etc.) is difficult and time-consuming (Fao, 1974; hyslop, 1980). For many species, the low sample number (scarcity and difficulty to catch these species, particularly those of small size (Syngnathidae, P. microps, E. encrasicolus, A. boyeri) allows only to get a superficial idea of their diets, and the results of their stomach content analysis should be taken with much caution. it is an important problem of this work. however, it is the first study which covers the whole trophic functioning of the fish community in this lacustrine ecosystem. This study highlights the trophic relationships between prey and fish, and among fishes. This is an important step to characCybium 2015, 39(3) terize the food webs and understand the trophic functioning of this particular ecosystem. Prey like insects, micro-zoobenthos, percarids and benthic micro-gastropods are always present in the totality of the stomach contents analyzed, which characterizes the ichkeul trophic network. in fact, the presence of these species is one of paralic ecosystem characteristics and were present in the same time in lacustrine, mudflats (swamp) and lagoonmarine habitats. From an abiotic point of view, these paralic environments are characterized by shallowness, water stratification and high confinement that generate a high phytoplanktonic biomass (Frisoni et al., 1983; Guelorget et al., 1989) and high macrophytal biomass (casagranda et al., 2005a; casagranda et al., 2006; Shili et al., 2007). The omnipresence of vegetal fraction within the stomach contents of numerous species attests the importance of the vegetal biomass in the lacustrine ecosystem functioning. This structural trophic network characteristics of ichkeul Lake are similar to those observed in other similar environments, like the neighbouring lakes and estuaries of north africa (Guelorget et al., 1989; Bouchereau et al., 2000; Bazairi et al., 2005) or the lakes and transitional environments of south europe: doñana and Mar Menor (South of Spain) (Giordani et al., 2009), Ria Formosa (Gamito et al., 2003) et Ria d’aveiro (Garnerot et al., 2004) (South of Portugal), Fogliano Lake and caprolace Lake (Tyrrhenian basin, central West, Italy) (Mariani 2001), Vaccarès pond and Or pond (camargue, Rhône delta, South of France) (Mouillot et al., 2005 ; Vizzini et al., 2005 ; dierking et al., 2012); and La Palme pond (natural park of narbonnaise, South of France ) (carlier et al., 2008). The fact that a prey is found in the stomach contents of big-sized predator fish (A. anguilla, B. callensis, D. labrax) and in those of small-sized ones (B. belone, A. fasciatus, A. boyeri) suggests that food diet reflects more the availability and richness of prey in the environment than a direct influence of fish size (morphological intrinsic parameter) or confinement degree (physico-chemical abiotic parameter), as it was already observed in other Mediterranean lagoons such as nador or aveiro (Bouchereau et al., 2000; Garnerot et al., 2004). This availability was confirmed by the previous studies in ichkeul Lake, which pointed out the high biomass of hydrobies, percarid crustaceans and marcophytal biomass (casagranda et al., 2006; Shili et al., 2007; Mancinelli, 2012). according to Bazairi et al. (2005), the trophic organization of environments similar to ichkeul is depending on a low number of species that dominate quantitively fauna communities, particularly bivalves (Cerastoderma spp., Abra spp., Scrobicularia plana) and amphipod/isopod crustaceans, when micro-grazers and herbivores are generally scarce, except some specific species such as hydrobies. The benth205 Ichthyofauna diet in Ichkeul Lake Shaiek et al. ic macrofauna is composed of strictly paralic species such as peracarid crustaceans (Corophium sp. Gammarus sp., Sphaeroma hookeri), polychaetes (Nereis sp.), chironomid larvae and filter feeder pelecypods (Abra sp., Cerastoderma glaucum, Scrobicularia plana), in addition to Hydrobia sp. This latter genus presents a quasi-monospecific population usually in the most confined zones (Guelorget et al., 1989; Lam hoai and amanieu, 1989; Garnerot et al., 2004). according to Frisoni et al. (1983) and to Guelorget et al. (1989), this benthic macrofauna is distributed all over those environments, depending on zones and confinement degrees. These are actually low diversified communities, with mixed strictly paralic species and some representatives of freshwater fauna in the marginal remotes and outfalls of oueds following the lake contour (Guelorget et al., 1989). Moreover, only a few crustaceans living in paralic environments constitute a principal prey for most of the Ichkeul fish species. amphipods and isopods constitute an important biomass in this environment (casagranda et al., 2006; Mancinelli, 2008) and their high availability may explain their occurrence in the food diet of fishes (particularly carnivores). Other groups can be also considered as main fish prey. Small meiofauna organisms (ostracods and foraminifera) (Guelorget et al., 1999) are found regularly within digestive tracts of fish, from small sized strictly benthophagous species (Syngnathus spp., cyprinodon, etc.) to bigger piscivorous species (eel, seabass), as well as in detritivorous/omnivorous species (mullets and barb). These incidentally ingested preys are constantly present in almost all aquatic ecosystems (Zaîbi et al., 2011). Environment predator-prey relationship The important biomass of the prey categories (amphipods, isopods) and their predators (cyprinodon, sand smelt, anchovy, etc.) is due to the relative ‘stability’ of the varying ecological and trophic conditions, which are favourable to these species (water quality, physico-chemical parameters and nutrients availability). This can explain the low degree of spatiotemporal diet variability of predator fishes; the fact that Ichkeul Lake does not have a pronounced confinement gradient (ovoidal form, important freshwater supplies, strong marine influence and typical hydrodynamism) induces an important biomass of benthic macrofauna (Frisoni et al., 1983; Bouchereau et al., 2000; Garnerot et al., 2004). This hypothesis is supported by works of Mancinelli (2012) and kuan-Yi et al. (2009) about the close relationship between macrophytal biomass and their associated epiphytes and epifauna, particularly the peracarid crustaceans, which were found amply into fish stomach contents. The bivalves were found particularly in stomach contents of eels during the dry season. These molluscs were found in important quantities in muddy or/and muddy-slimy lacustrine sediments (Gamito et al., 2003; Bouchereau et al., 2009a, b). The benthophagous behaviour of eels was already demonstrated in Prévost pond, ingril and Mauguio lagoons (Guélorget and Perthuisot, 1982; Bouchereau et al., 2009b). Small-sized fish species, such as Aphanius fasciatus and Atherina boyeri, represented an important part of the diet of piscivorous and carnivorous species (D. labrax and A. anguilla). Figure 9 proposes a synthetic diagram of the trophic relationships evidenced in the present study that link fishes to their principal prey within the Ichkeul Lake ecosystem. Spatio-seasonal variability The spatiotemporal variability of stomach contents was characterized for many fish species. This variability could be related to different factors: trophic preferences versus resource availability according to sector and season. The second factor is closely linked to the influence of salty and freshwater interface (marine water versus continental water) (Mariani, 2001). The structure of the lacustrine prey and fish community reflects the physical, geochemical and hydrodynamical characteristics of the environment. The fish distribution is correlated with marine influence degree on such lacustrine ecosystems as ichkeul Lake (Guelorget and Perthuisot, 1983, 1992; Mariani, 2001). added to the constraints of these abiotic parameters, one should also consider the opportunity for each fish species to find food adapted to its size and physiological needs. This relation between size, diet, prey and ecological conditions constitutes an important parameter to understand the space occupation by a species (Paugy and Lévêque, 1999). Seasonality Seasonality of fish diet was not observed for all fish species sampled. a clear seasonality and a noticeable diet change, between dry and wet seasons, are particularly obvious for A. anguilla, S. senegalensis and B. callensis. This last species is characterized by a high diet variability compared to the two other fish species, as it does not find the same prey in the freshwater environment of rivers, in which it ascends during the dry season, than those available during the wet season in the ichkeul Lake. The availability of the lacustrine prey for the barb is especially concentrated in the western sector, which is more influenced by continental water supplies (casagranda et al., 2005a, 2006). Thus, D. labrax, S. senegalensis, B. callensis and A. anguilla showed a spatio-temporal variability of their diet. The benthophagous diet of these species varies considerably between wet and dry seasons. in fact, the transition of a diet (i.e zoobenthophagous to detritivorous) was already observed in shallow paralic environments, which are influenced by abiotic parameters, particularly salinity and tem- 206 Cybium 2015, 39(3) Ichthyofauna diet in Ichkeul Lake Shaiek et al. perature (Paugy and Lévêque, 1999; casagranda et al., 2005a, 2006; casagranda and Boudouresque, 2010). Therefore, except these previously mentioned species, there is no trophic variability for the other fish species despite a high physico-chemical seasonality of the lacustrine ecosystem (salinity, temperature, water level, macrophyte coverage) (casagranda et al., 2005a, 2006 casagranda and Boudouresque, 2010). This can be explained by the abundance of resources during the whole year, which constitutes the main prey of most fish species. Some of those preys are constantly available in the environment and their biomasses are very important. This obervation was confirmed by many authors like Guelorget et al. (1987, 1989) or Garnerot et al. (2004). indeed, biomasses of zoobenthos prey species are high in paralic environments, while specific richness is low. These prey have a large tolerance and high ecological amplitude valence, which allow them to adapt to the physico-chemical variability of their environment (Mariani, 2001; Garnerot et al., 2004; Mancinelli, 2012). Species like mullets, syngnathidae, cyprinodons, that showed a low spatial and/or seasonal variability of their food diet, composed a distinct multispecific trophic group. These species presented more or less similar diet composition as they move easily from eastern to western lake sectors during wet and dry seasons. CONCLUSION Prey ingested by fish species in Ichkeul Lake belonged mainly to lacustrine benthic macrofauna, in particular gastropods (Hydrobia spp.), bivalves (Abra alba, Cerastoderma glaucum), and peracarid crustaceans (amphipods/isopods). The omnipresence of vegetal fraction into stomach contents of the majority of fish sampled demonstrates its trophic importance, as well as the importance of this biomass in the lacustrine ecosystem. The majority of fish trophic categories defined according to food diet are the detritivores and the benthophagous carnivores. The seasonal and spatial variability of food diet differed greatly from a species to another. Anguilla anguilla, Solea senegalensis and Barbus callensis presented the strongest variations. These variations were particularly related to the nature and the proportions of the ingested preys. The trophic clusters and the spatiotemporal food variability of fish species reflected the lacustrine trophic network structure and its evolution. The hydrological changes, linked to the water resources rarefaction supplying ichkeul Lake, leads us to question its repercussion on the possible structuring of the trophic networks. Cybium 2015, 39(3) Acknowledgements. – We would like to thanks the two reviewers that greatly improved the paper. We also thank Adnen Sanaa and Belaid hadj Salem for improving english and helping to edit the manuscript. REFERENCES ANPE, 2002. - Rapport sur le suivi scientifique au Parc National de l’ichkeul, année 2002-2003. 58 p. Ministère de l’environnement et du développement durable, République tunisienne. ANPE, 2003. - Rapport sur le suivi scientifique au Parc National de l’ichkeul, année 2003-2004. 60 p. Ministère de l’environnement et du développement durable, République tunisienne. ANPE, 2004. - Rapport sur le suivi scientifique au Parc National de l’ichkeul, année 2004-2005. 74 p. Ministère de l’environnement et du développement durable, République tunisienne. ANPE, 2005. - Rapport sur le suivi scientifique au Parc National de l’ichkeul, année 2005-2006. 64 p. Ministère de l’environnement et du développement durable, République tunisienne. ANPE, 2006. - Rapport sur le suivi scientifique au Parc National de l’ichkeul, année 2006-2007. 79 p. Ministère de l’environnement et du développement durable, République tunisienne. ANPE, 2007. - Rapport sur le suivi scientifique au Parc National de l’ichkeul, année 2006-2007. 86 p. Ministère de l’environnement et du développement durable, République tunisienne. BaZaiRi h., BaYed a. & hiLY c., 2005. - Structure et bioévaluation de l’état écologique des communautés benthiques d’un écosystème lagunaire de la côte atlantique marocaine. C. R. Biol., 328: 977-990. BceoM, 1995. - Étude pour la sauvegarde du Parc national de l’ichkeul. Rapport de 3e partie. Mesures et études spécifiques. 421 p. Ministère de l’environnement et de l’aménagement du Territoire, anPe, BceoM, Tunis. Ben GaRaLi a., oUakad M. & GUeddaRi M., 2008. hydrologie, sédimentologie et géochimie de l’oued Tinja (Tunisie septentrionale). Bull. Inst. Nat. Tech. Mer. Salammbo, 35: 161-168. Ben M’BaRek n., 2001. - Étude de l’écosystème de lac ichkeul et de son bassin versant : caractéristiques physiques et géochimiques des eaux et des sédiments. Thèse de doctorat, 231 p. Univ. Tunis ii, Tunisie. Ben M’BaRek n. & SLiM-ShiMin n., 2002. - Évolution des paramètres physico-chimiques des eaux du lac ichkeul après la réalisation des aménagements hydrauliques (Tunisie). Proc. of Int. Symp. and Workshop on Environmental Pollution control and Waste Management Tunis (EPCOWM’2002), pp. 20-27. Tunis. Ben ReJeB-Jenhani a., 1989. - Le lac ichkeul : conditions de milieu, peuplements et biomasses phytoplanctoniques. Thèse de doctorat, 221 p. Univ. de Tunis, Tunisie. BenZÉcRi J.P., 1973 . - L’analyse des données. Tome 2 : L’analyse des correspondances. 619 p. Paris: dunod. BenZÉcRi JP. & BenZÉcRi F., 1984. - Pratique de l’analyse des données. i. analyse des correspondances, exposé élémentaire. 456 p. Paris: dunod. BoUcheReaU J.L., dUReL J.S., GUeLoRGeT o. & ReYnaUd-LoUaLi L., 2000. - L’ichtyofaune dans l’organisation biologique d’un système paralique : la lagune de nador, Maroc. Mar. Life, 10: 69-76. BoUcheReaU J.L., MaRQUeS c, PeReiRa P, GUeLoRGeT o. & VeRGne Y., 2009a. - Food of the european eel Anguilla anguilla in the Mauguio lagoon (Mediterranean, France). Act. Adriat., 50(2): 159-170. 207 Ichthyofauna diet in Ichkeul Lake BoUcheReaU J.L, MaRQUeS c, PeReiRa P, GUeLoRGeT o., LoURie S.M. & VeRGne Y., 2009b. - Feeding behaviour of Anguilla anguilla and trophic resources in the ingril lagoon (Mediterranean, France). Cah. Biol. Mar., 50: 319-332. caRLieR a., RieRa P., aMoURoUX J.M., BodioU J.Y., deSMaLadeS M., GReMaRe a., 2008. - Food web structure of two Mediterranean lagoons under varying degree of eutrophication. J. Sea Res., 60: 264-275. caSaGRanda c. & BoUdoUReSQUe c.F., 2010. - a first quantification of the overall biomass, from phytoplankton to birds, of a Mediterranean brackish lagoon: revisiting the ecosystem of Lake ichkeul (Tunisia). Hydrobiologia., 637: 73-85. caSaGRanda c., BoUdoUReSQUe c.F. & FRancoUR P., 2005a - abundance, population structure and production of Hydrobia ventrosa (Gastropoda: Prosobranchia) in a Mediterranean brackish lagoon, Lake ichkeul, Tunisia. Arch. Hydrobiol., 164(3): 411-428. caSaGRanda c., BoUdoUReSQUe c.F. & FRancoUR P., 2005b - Trophic flows in the macroinvertebrate community of a Mediterranean brackish lagoon, Lake ichkeul (Tunisia) using a functional model. Proceedings of International Workshop on “The Protection of coastal and environment”, 9-11 november 2005, izmir-Turkey. inoc-coMSTec-iSeSco, 2005: 153162. caSaGRanda c., dRidi M.S. & BoUdoUReSQUe c.F., 2006. - abundance, population structure and production of macro-invertebrate shredders in a Mediterranean brackish lagoon, Lake ichkeul, Tunisia. Estuar. Coast. Shelf Sci., 66: 437-446. chaoUachi B. & Ben haSSine o.k., 1998. - The status of fish biodiversity in Ichkeul Lagoon, Tunisia. Ital. J. Zool., 65: 303-304. dieRkinG J., MoRaT F., LeToURneUR Y. & haRMeLinViVien M., 2012. - Fingerprints of lagoonal life: migration of the marine flatfish Solea solea assessed by stable isotopes and otolith microchemistry. Estuar. Coast. Shelf Sci., 104: 23-32. Fao, 1974. - Methods of Resource investigation and their application. Manual of Fisheries Science Part 2. Fish. Tech. Paper, 115: 115-255. FRiSoni G.F., GUeLoRGeT o., XiMeneS M.c. & PeRThUiSoT J.P., 1983. - Étude écologique de trois lagunes de la plaine orientale corse (Biguglia, diana, Urbino) : expressions biologiques qualitatives et quantitatives du confinement. J. Rech. Oceanogr., 8: 57-80. GaMiTo S., PiReS a., PiTa c. & eRZini k., 2003. - Food availability and the feeding ecology of ichthyofauna of a Ria Formosa (South Portugal). Water Reservoir Estuar., 26: 938-948. GaRneRoT F., BoUcheReaU J.P., ReBeLo J.e., & GUeLoRGeT o., 2004. -L’ichtyofaune dans l’organisation biologique d’un système paralique de type lagunaire, la Ria d’aveiro (Portugal), en 1987-1988 et 1999-2000. Cybium, 28: 63-75. GioRdani G., ZaLdiVaR J.M. & ViaRoLi P., 2009. - Simple tools for assessing water quality and trophic status in transitional water ecosystems. Ecol. Indicat., 9: 982-991. GUeLoRGeT o. & PeRThUiSoT J.P., 1982. - Structure et évolution des peuplements en milieu paralique. composition entre un modèle dessalé (l’etang du Prévost, France) et un modèle sursalé (La Bahiret el Biban, Tunisie). conséquence biologique et géologique. J. Rech. Océano., 7: 2-11. GUeLoRGeT o. & PeRThUiSoT J.P., 1983. - Le domaine paralique, expressions géologiques, biologiques et économiques du confinement. Travaux du Laboratoire de Géologie, Presses enS, 16, 136 p. Paris. 208 Shaiek et al. GUeLoRGeT o. & PeRThUiSoT J.P., 1992. - Paralic ecosystems. Biological organization and functionning. Vie Milieu, 42: 215-251. GUeLoRGeT o., PeRThUiSoT J-P., FRiSoni G.-F. & MonTi D., 1987. - Le rôle du confinement dans l’organisation biogéologique de la lagune de nador (Maroc). Oceanol. Acta., 10: 435-444. GUeLoRGeT o., FRiSon G.F., XiMeneS M.c. & PeRThUiSOT J.P., 1989. - Expressions biogéologiques du confinement dans une lagune méditerranéenne : le lac Melah (algérie). Reo. Hydr. Trop., 22(2): 87-99. GUeLoRGeT o., FaVRY a., deBenaY J.P. & PeRThUiSoT J.P., 1999. - Les écosystèmes paraliques : distribution des peuplements de foraminifères actuels dans les étangs de diana et d’Urbino (corse). Vie Milieu, 49(1): 51-68. haMMeR Ø., haRPeR d.a.T. & RYan P.d., 2001. - PaST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron., 4(1): 1-9. hoRn h.S., 1966. - Measurement of overlap in comparative ecological studies. Am. Nat., 100: 419-424. hYneS h.B.n., 1950. - The food of the freshwater sticklebacks (Gastrosteus aculeatus) and Pygosteus pungitius) with a review of methods used in studies of the food of fishes. J. Anim. Ecol., 19: 36-58. hYSLoP e J., 1980. - Stomach contents analysis: a review of methods and their application. J. Fish. Biol., 17: 411-429. kaRachLe P.k. & STeRGioU ki., 2012. - Morphometrics and allometry in fishes. In: Morphometrics (Wahl C., ed.), Chapter 4: 65-86. InTech. available from: http://www.intechopen.com/ articles/show/title/ morphometrics-and-allometry-in-fishes. kRaÏeM M.M., RaMdani M., FaThi a.a., aBdeLZaheR H.M.A. & FLOWER R., 2003. - Analyse de la biodiversité et de la production ichtyque dans trois lacs nord africains : Merja Zerga (Maroc), Garaat ichkeul (Tunisie) et lac edku (Égypte). Bull. Inst. Nat. Sci., 30: 5-13. kReBS c.J., 1999. - ecological Methodology. 2nd edit., 624 p. Menio-Park, California: Addison-Wesley Educational Publishers inc. KUAN-YI L., ZHENG-WEN L., YAO-HUI H. & HONG-WEI Y., 2009. - Snail herbivory on submerged macrophytes and nutrient release: implications for macrophyte management. Ecol. Engineer., 35: 1664-1667. LaM hoai T. & aManieU M., 1989. - Structures spatiales et évolution saisonnière du zooplancton superficiel dans deux écosystèmes lagunaires nord-méditerranéens. Oceanol. Acta, 12(1): 65-77. MancineLLi G., 2008. - Quantitative assessment of animalinduced leaf damage: a test with three brackish crustaceans feeding on leaf detritus. Trans. Waters Bull., 4: 38-48. MancineLLi G., 2012. - To bite, or not to bite? a quantitative comparison of foraging strategies among three brackish crustaceans feeding on leaf litters. Estuar. Coast. Shelf Sci., 110: 125133. MaRiani S., 2001. - can spatial distribution of ichthyofauna describe marine influence on coastal lagoons? A Central Mediterranean case study. Estuar. Coast. Shelf Sci., 52: 261-267. MoUiLLoT d., GaiLLaRd S., aLiaUMe c., VeRLaQUe M., BeLSheR T., TRoUSSeLieR M. & do chi T., 2005. - ability of taxonomic diversity indices to discriminate coastal lagoon environments based on macrophyte communities. Ecol. Indic., 5: 1-17. PaUGY d. & LÉVÊQUe c. (eds), 1999. - Régime alimentaire et réseaux trophiques. In: Les Poissons des eaux continentales africaines : diversité, Écologie, Utilisation par l’homme, pp. 167-190. Paris: iRd editions. Cybium 2015, 39(3) Ichthyofauna diet in Ichkeul Lake Shaiek et al. PieT G.J., 1998. - ecomorphology of a size-structured tropical freshwater fish community. Environ. Biol. Fish., 51: 67-86. PoTieR M., MaRSac F., cheReL Y., LUcaS V., SaBaTiÉ R., MaURY o. & MÉnaRd F., 2007. - Forage fauna in the diet of three large pelagic fishes (lancetfish, swordfish and yellow fin tuna) in the western equatorial. Indian Ocean Fish. Res., 83: 60-72. RoSS S.T., 1986. - Resource partitioning in fish assemblages: a review of field studies. Copeia., 2: 352-388. ROUNSEFELL G.A. & EVERHART W.H., 1953. - Fisheries Science: its Methods and Applications. 444 p. New York: Wiley and Sons. SCHOENER T.W., 1974. - Resource partitioning in ecological communities. Science, 185: 27-39. SeLLaMi R., chaoUachi B. & Ben haSSine o.k., 2010. impacts anthropiques et climatiques sur la diversité ichtyque d’une lagune méditerranéenne (ichkeul, Tunisie). Cybium, 34: 5-10. ShiLi a., Ben MaiZ n., BoUdoUReSQUe c.F. & TRaBeLSi e.B., 2007. - abrupt changes in Potamogeton and Ruppia beds in a Mediterranean lagoon. Aquat. Bot., 87: 181-188. SiBBinG F.a., naGeLkeRke L.a.J., STeT R.J.M. & oSSe J.W.M., 1998. - Speciation of endemic Lake Tana barbs (cyprinidae, ethiopia) driven by trophic resource partitioning; a molecular and ecomorphological approach. Aquat. Ecol., 32: 217-227. ViZZini S., SaVona B., do chi T. & MaZZoLa a., 2005. Spatial variability of stable carbon and nitrogen isotope ratios in a Mediterranean coastal lagoon. Hydrobiologia, 550: 73-82. ZaÎBi c., caRBoneL P., kaMoUn F., aZRi c., khaRRoUBi a., kaLLeL n., JedoUi Y., MonTaceR M. & FonTUGne M., 2011. - Évolution du trait de côte à l’holocène supérieur dans la Sebkha el-Guettiate de Skhira (Golfe de Gabès, Tunisie) à travers sa faune d’ostracodes et de foraminifères. Geobios, 44: 101-115. ZaReT M.R. & Rand a.S., 1971. - competition in tropical stream fishes: support for the competitive exclusion principle. Ecology, 52: 336-342. appendix i. - Number of analyzed stomachs, number of empty stomachs, vacuity coefficient Cv (%) between sector and seasons for the several fish species. Cv: Vacuity coefficient; ED: East sector-Dry season; EW: East sector-Wet season; N: number of non-empty analyzed stomachs for each species; nt: number of analyzed stomachs for each specie; ne: number of empty analyzed stomachs; WD: West sectorDry season; WW: West sector-Wet season. Species nt ana 25 dil 6 Sos 7 Beb 10 Muc 11 Lir 1 Lia 6 Lis 0 ene 11 Pom 3 apf 0 atb 6 Syab 5 Syac 5 Syt 9 Bac 0 Cybium 2015, 39(3) ed ne cv nt 7 28.0 27 1 16.6 4 0 0.0 15 0 0.0 10 1 9.0 16 0 0.0 0 0 0.0 30 0 0.0 5 0 0.0 1 0 0.0 10 0 0.0 9 3 50.0 8 1 20.0 7 1 20.0 5 1 11.1 7 0 0.0 4 EW ne 13 1 2 3 2 0 1 2 0 0 0 0 1 0 0 0 cv nt 48.1 6 25.0 8 13.3 6 30.0 4 12.5 19 0.0 8 3.3 9 40.0 14 0.0 0 0.0 0 0.0 50 0.0 11 14.2 0 0.0 0 0.0 0 0.0 16 WD ne 1 1 0 0 3 0 2 0 0 0 0 1 0 0 0 2 cv nt 16.6 5 12.5 4 0.0 4 0.0 0 15.7 10 0.0 14 22.2 2 0.0 4 0.0 5 0.0 0 0.0 11 9.0 7 0.0 0 0.0 0 0.0 0 12.5 17 WW ne 0 0 0 0 2 0 0 1 0 0 0 0 0 0 0 1 cv nt 0.0 63 0.0 22 0.0 32 0.0 24 20.0 51 0.0 23 0.0 46 25.0 23 0.0 17 0.0 13 0.0 70 0.0 32 0.0 12 0.0 10 0.0 16 5.8 37 annual ne cv 21 33.3 3 13.6 2 6.2 3 12.5 7 13.7 0 0.0 3 6.5 3 13.0 0 0.0 0 0.0 0 0.0 4 12.5 2 16.6 1 10.0 1 6.2 3 8.1 209 Ichthyofauna diet in Ichkeul Lake Shaiek et al. Appendix II. - Trophic level and classification by trophic category of the several species according to fishbase (www.fishbase.org) and karachle and Stergiou, 2012. Species Anguilla anguilla Aphanius fasciatus Atherina boyeri Barbus callensis Belone belone Dicentrarchus labrax Engraulis encrasicolus Liza aurata Liza ramada Liza saliens Mugil cephalus Solea senegalensis Syngnathus abaster Syngnathus acus Syngnathus typhle Pomatoschistus microps Trophic level * Trophic category** Trophic category (www.fishbase.org) (www.fishbase.org) (karachle & Stergiou, 2012) 3.5 ± 0.6 2.7 ± 0.2 2.3 ±0.3 2.8 ±0.3 4.2 ± 0.7 3.8 ± 0.6 3.1 ± 0.4 2.5 ± 0.2 2.2 ± 0.1 3.0 ± 0.2 2.1 ±0.2 3.1 ±0.3 3.2 ± 0.4 3.4 ± 0.6 4.3 ± 0.8 3.3 ± 0.4 oa/cd oV oV oa cc cc oa oV oV oa oV oa oa oa cc oa carnivores mesophagous detritivores (omnivores) carnivores microphagous detritivores (omnivores) Piscivores carnivores mesophagous/macrophagous carnivores mesophagous detritivores detritivores detritivores detritivores carnivores mesophagous carnivores mesophagous carnivores mesophagous Piscivores carnivores mesophagous * Calculated from diet study species trophic category was identified using their trophic level τ (www.fishbase.org) ** Trophic category (Karachle & Stergiou, 2012): According to this classification; H = pure herbivores (2,0 <τ <2.1); VO = omnivores with vegetal preference (2,1 <τ <2,9); OA = omnivores with animal preference (2,9 <τ <3,7); CD = carnivores with preference for decapods/fish (3,7 <τ <4,0); CC = carnivores with preference for fish/cephalopods (4.0 <τ <4,5). 210 Cybium 2015, 39(3)