Journal of the Marine Biological Association of the United Kingdom, 2008, 88(1), 183 –187. doi:10.1017/S0025315408000106 Printed in the United Kingdom #2008 Marine Biological Association of the United Kingdom Diet of Tetrapturus belone (Istiophoridae) in the central Mediterranean Sea luca castriota1, maria grazia finoia2, silvana campagnuolo1, teresa romeo3, antonio potoschi4 and franco andaloro1 1 Central Institute for Marine Research (ICRAM), STS Palermo, via Emerico Amari 124, 90139 Palermo, Italy, 2ICRAM, via di Casalotti 300, 00166 Roma, Italy, 3ICRAM, STS Palermo Laboratorio di Milazzo, via dei Mille 44, 98057, Milazzo (Me), Italy, 4 Dipartimento di Biologia Animale ed Ecologia Marina, Università di Messina, Salita Sperone, S. Agata, 98166 Messina, Italy The stomach contents of 69 Mediterranean spearfish Tetrapturus belone collected in the Strait of Messina, central Mediterranean Sea were examined. Of the total specimens, caught by harpoon, only three stomachs were empty. Their diet consisted mainly of pelagic fish and cephalopods. The most important piscine prey belonged to the families of Belonidae, Clupeidae and Scomberesocidae. Cephalopods were mainly represented by Tremoctopus violaceus in terms of per cent weight and by Illex coindetii in terms of per cent frequency of occurrence. Tetrapturus belone is an active predator on epipelagic fast-moving prey and school-forming species. Its ecological role is similar to that of other large pelagic species which share the same environment. Keywords: billfish, diet, Mediterranean Sea, Strait of Messina, feeding habits, Tetrapturus belone Submitted 21 September 2006; accepted 2 November 2007 INTRODUCTION The Mediterranean spearfish Tetrapturus belone (Rafinesque) is a pelagic species belonging to the family Istiophoridae. It is considered a highly migratory species (Nakamura, 1985) whose distribution is limited to the Mediterranean Sea, although some specimens have been recorded from the Atlantic side of the Strait of Gibraltar (Di Natale et al., 2005b). Like other billfish, this species probably swims in the upper 200 m water layer, generally above or within the thermocline (Nakamura, 1985). It is considerably abundant around Italy (Nakamura, 1985), particularly in the Tyrrhenian Sea, where it is caught as by-catch of large pelagic fisheries and in the Strait of Messina where it represents a target species (Di Natale et al., 2003). There, the Mediterranean spearfish is fished at the surface by harpoons with traditional boats called ‘feluche’ or ‘passerelle’, typically used to catch swordfish, Xiphias gladius L., only from late spring to summer. After the crisis in swordfish fishery of the last years, worsened by the European ban of driftnets since 2002 (UE Regulation no. 1239/98), the interest for the Mediterranean spearfish fishery is increasing, despite its lower commercial value when compared to that of swordfish. In the last decades, the catches by harpoon of this species in the Strait of Messina showed an increasing trend, from 39 kg total weight in 1976 to 1221.5 kg in 2003 (Di Natale et al., 2005a). Although the importance of this species is rising on the market, scanty information on its biology and ecology is available. Robins & De Sylva (1960, 1963) and Spartà (1953, 1961) studied its eggs and larval development; Cavaliere (1962) and Corresponding author: L. Castriota Email: castriotaluca@hotmail.com Potoschi (2000) reported a few data on the biology and fishery of the species in the Strait of Messina while catches from Italian seas are reported by Di Natale et al. (2003, 2005a, b). Some fishery and biological information are reported by De Sylva (1975) and by Nakamura (1985). Feeding ecology is an important aspect of the life-history strategy of fish and may be a precious tool for the comprehension of trophic dynamics and for the development of appropriate fishery management strategies. However, in the case of the Mediterranean spearfish, feeding ecology has been very poorly investigated. Based on the examination of stomach contents from a few specimens, a diet consisting of epipelagic organisms is reported (Spartà, 1961; Bini, 1968; Tortonese, 1975; Nakamura, 1985). As information about feeding of T. belone is still based on feeble, sometimes doubtful observations, in this paper we aim at describing its feeding habits in order to increase the knowledge of the biology of this scarcely studied species. MATERIALS AND METHODS The study of feeding habits was carried out on the stomach contents of 69 Mediterranean spearfish, caught at the surface by harpoons. Samples were collected from 1995 to 2004 in the Strait of Messina (Figure 1) at day-time, during the fishing season for swordfish and Mediterranean spearfish by harpoon, from late spring to summer. Specimens were measured to the nearest cm from the tip of the bill (upper jaw) to the posterior margin of the middle caudal rays (LF); total weight (W ) was also recorded to the nearest hectogram. The stomachs were removed and preserved in a 10% seawater –formalin solution for 24 h, and then transferred to 80% alcohol for subsequent analysis of contents. In the laboratory prey items were identified to the 183 184 luca castriota et al. Fig. 2. Length – frequency distribution of Tetrapturus belone from the Strait of Messina sampled for stomach contents analysis. Fig. 1. Map showing the sampling area of Tetrapturus belone in the central Mediterranean Sea. lowest possible taxonomic level, then counted and weighed to the nearest milligram. As hard parts resistant to digestion (i.e. cephalopod beaks) cumulate in the stomachs over more meals, leading to overestimation of the importance of prey they belong to, only prey bearing fleshy remains were considered for the analyses, as they were likely to have been recently eaten by the predator (see Santos et al., 2001). Cephalopod beak lengths—the lower rostral length and the lower hood length in decapods and octopods respectively (Clarke, 1986)—were used to estimate mantle length of digested cephalopods and to reconstitute their weights, using relationships either in the literature (Clarke, 1986; Bello, 1991), or from measurements on specimens in our reference collection (ICRAM collection). To assess the adequacy of the number of samples analysed, the cumulative number of new prey types against the cumulative number of non-empty stomachs were plotted (Ferry & Caillet, 1996). The PRIMER software was utilized to compute a prey species accumulation plot as an average of 999 curves based on different random orders of the stomachs. In order to assess whether the curve reached an asymptote, the logistic and linear regressions were calculated and their goodness of fit coefficients R2 were compared: the sample size was considered sufficient if the R2 for the logistic curve was higher than the R2 for the linear relation (Castriota et al., 2005). The importance of the different prey items was evaluated by calculating the frequency of occurrence (%F ¼ number of stomachs containing prey i/total number of stomachs containing prey  100), abundance (%N ¼ number of prey i/total number of prey  100) and reconstituted weight (%W ¼ weight of prey i/total weight of all prey  100). These values were used to calculate the index of relative importance (IRI) for each taxonomic category using mass instead of volume: IRI ¼ (%N þ %W )  (%F ) (Hyslop, 1980; Hacunda, 1981). Fullness index (IF ¼ no. stomachs with food/ no. total stomachs) was also calculated. The degree of diet specialization was given by the Levin’s standardized index (Hurlbert, 1978; Krebs, 1989), Bi ¼ [(Sjp2ij)21 2 1] (n 2 1)21 where: Bi ¼ Levin’s standardized index for predator i; pij ¼ proportion of diet of predator i that is made up of prey j; n ¼ number of prey items. This index ranges from 0 to 1; low values indicate diets dominated by few prey items (specialist predators), high values indicate generalist diets (Krebs, 1989). The binomial test was applied on the frequency of occurrence values of each prey category to select prevailing items in the diet of Tetrapturus belone: a prey category was considered as rare if its frequency of occurrence was significantly less than 5%, for P , 0.05. The binomial test was also repeated on the abundance values of each prey category. RESULTS Mediterranean spearfish caught had an average total weight of 11.0 kg (range 2.8 – 22.0 kg) and an average fork length of 149 cm (range 89 –191 cm). Of the total stomachs examined only three were empty, thus the fullness index was 0.96. Figure 2 shows the length – frequency distribution of the 69 specimens used for the stomach contents analysis. The cumulative prey types curve (Figure 3) for the entire data set resulted as fitting better with a logistic curve (R2 ¼ 0.97; F(1,64) ¼ 1627.2, P , 0.001) than with a linear relation (R2 ¼ 0.92, F(1,64) ¼ 734.2; P , 0.001); therefore the sample size was considered sufficient to describe the diet of Tetrapturus belone. The analysis of the stomach contents led to the identification of 27 prey items (Table 1), belonging to two main taxa: Pisces and Cephalopoda. A total of 421 fish, 59 cephalopods and 8 other invertebrates were found in the stomachs analysed, with a mean of 7.4 prey individuals (+ 0.6 SE) per stomach. Fig. 3. Prey species accumulation plot as an average of 999 curves based on different random orders of the stomachs extracted (number of stomachs ¼ 66). Vertical bars represent standard deviation. diet of tetrapturus belone in mediterranean Table 1. Percent frequency of occurrence (%F), percent of total number (%N), percent of total weight (%W), index of relative importance (IRI) and percent index of relative importance (%IRI) for food items of Tetrapturus belone. %IRI Prey Categories %F %N %W Pisces unid. Belonidae Belonidae unid. Belone belone Belone svetovidovi Carangidae Seriola dumerili juv. Trachurus sp. Centriscidae Macroramphosus scolopax juv. Clupeidae Clupeidae unid. Alosa sp. Sardina pilchardus Sardinella aurita Coryphaenidae Coryphaena hippurus juv. Engraulididae Engraulis encrasicolus Gobiidae Scomberesocidae Scomberesox saurus Scombridae Sparidae Oblada melanura TOTAL PISCES Cephalopoda unid. Octopoda Tremoctopus violaceus Teuthoidea Ancistrocheirus lesueuri Histioteuthis bonnellii Illex coindetii Todarodes sagittatus TOTAL CEPHALOPODS Invertebrates unid. Tunicata Salpida Siphonophora Diphyidae 43.9 30.7 4.3 1538.6 36.8 6.1 33.3 1.5 3.3 21.1 0.2 1.3 20.5 0.1 27.6 1388.4 0.4 0.7 33.2 ,0.1 1.5 3.0 0.2 1.2 0.2 0.5 0.6 5.2 ,0.1 0.1 6.1 4.5 0.1 27.9 0.7 4.5 4.5 1.5 16.7 4.7 1.0 0.2 6.4 0.6 0.8 ,0.1 12.3 24.4 8.3 0.3 310.4 0.6 0.2 ,0.1 7.4 1.5 0.2 0.6 1.2 ,0.1 3.0 1.5 1.0 0.8 0.1 ,0.1 3.5 1.3 0.1 ,0.1 18.2 3.0 9.8 0.6 10.6 0.1 372.3 2.0 8.9 ,0.1 IRI 1.5 0.2 0.1 0.5 ,0.1 97.0 86.3 52.2 13435.1 87.1 10.6 3.7 0.2 41.0 1.0 1.5 0.2 ,0.1 0.3 ,0.1 7.6 2.7 43.7 351.3 8.4 4.5 0.8 0.9 4.5 1.0 0.3 10.6 3.1 1.7 3.0 0.6 1.0 33.3 12.1 47.7 3.0 0.4 ,0.1 1.5 0.2 ,0.1 1.5 1.0 ,0.1 7.9 0.2 5.9 0.1 50.7 1.2 4.7 0.1 1992.3 12.9 1.3 ,0.1 0.3 ,0.1 1.6 ,0.1 Fish were the dominant group according to all numerical indicators and were mostly composed of pelagic species. Ten families were identified among them, with the dominance of Belonidae which represented 41.2% of the total preyed fish in terms of %IRI. The families Clupeidae and Scomberesocidae were also well represented (%IRI ¼ 12.9 and 8.7 of the total preyed fish respectively). The species Belone belone (L.), Scomberesox saurus (Walbaum) and Sardinella aurita Valenciennes played the major role in the feeding of Mediterranean spearfish (Table 1). Cephalopods occurred in 33.3% of the stomachs analysed and accounted for 12.1% in number, and 47.7% in weight of the total preyed organisms. Cephalopod remains were attributed to 5 species, all pelagic. Tremoctopus violaceus Delle Chiaje was the most important species among them in terms of %W, while Illex coindetii (Verany) was the most represented in terms of %F. Levin’s standardized index, calculated for the evaluation of diet breadth, was 0.2 for the numerical abundance and 0.1 for the biomass of the prey items. The results of the binomial test indicated Belonidae, Clupeidae, Scomberesocidae and Teuthoidea as the significantly non-rare prey categories in terms of frequency of occurrence. The same results were obtained in terms of abundance except for Teuthoidea which were at the limit of significance (P ¼ 0.05). DISCUSSION Very few studies have been carried out on the biology of the Mediterranean spearfish and none on its feeding habits. Based on examination of stomach contents from a few specimens, some authors propose that it probably feeds on pelagic fish, such as sardines (Clupeidae), flyingfish (Exocoetidae), carangids, scombrids, dolphinfish (Coriphaenidae) and, around Sicily, Atlantic sauries, sardine-like fish, needlefish and pilotfish (Bini, 1968; De Sylva, 1975; Tortonese, 1975; Nakamura, 1985). Partial teuthophagy is also reported in the Ligurian Sea (Garibaldi & Orsi Relini, 2005). Diet preference of Tetrapturus belone for pelagic fish would justify occasionally catches with surrounding nets used for the fishery of the Atlantic saury in the Strait of Messina (Cavaliere, 1962; Spartà, 1961; Tortonese 1975). Our results confirmed fish as the main prey of the Mediterranean spearfish, although cephalopods were also well represented in terms of frequency of occurrence and reconstituted weight (Figure 4). If we also consider the large numbers of accumulated beaks in most stomachs examined, the frequency of occurrence of cephalopods increases from 33.3% to 58.2% and their abundance rises to 41.8%, confirming their important role in the diet of T. belone. Looking at the diets of other pelagic predators, cephalopods seem to play a most important part as food of the Atlantic white marlin T. albidus Poey, a very close congener of T. belone, also known from the Mediterranean Sea (Nakamura, 1985). They are also preyed upon by large predacious fish such as tunas, swordfish, sharks and other billfish (Roper et al., 1984; Bello, 1990, 1991, 1999; Abitı́a-Cárdenas et al., 2002; Rosas-Alayola et al., 2002; Vaske et al., 2004). The most represented fish species in the diet of T. belone (i.e. Belone belone, Scomberesox saurus and Sardinella aurita) are widely distributed in the Strait of Messina (Spartà, 1961); they used to form large schools that would allow the Mediterranean spearfish to maximize the efficiency of predation. Billfish require large amounts of energy to survive and coming across schools of fish or cephalopods Fig. 4. Frequency of occurrence (%F), abundance (%N) and biomass (%W) of main prey categories (tel ¼ unidentified teleosts; bel ¼ Belonidae; sco ¼ Scomberesocidae; clu ¼ Clupeidae; oct ¼ Octopoda; teu ¼ Teuthoidea) in the diet of Tetrapturus belone from the Strait of Messina. Dashed lines refer to total fish (left) and total cephalopods (right). 185 186 luca castriota et al. helps them in providing the large rations necessary to support their high metabolic demands. This chasing strategy has been also observed in other billfish as well as in other pelagic predators (Abitı́a-Cárdenas et al., 2002). Other prey found in the stomachs of T. belone, such as juvenile Macroramphosus scolopax (L.), carangids, juvenile dolphinfish, sparids, juvenile scombrids, juvenile gobiids and European anchovies, may be considered as secondary or accidental prey, at least in the sampling period; all grouped, they accounted for only 1.7% in weight and 8.8% in number. All preyed specimens were epipelagic organisms, also including juveniles of demersal or benthic fish which spend their early life stages in the upper waters. Overall, according to the prey species composition found, T. belone pursues epipelagic prey. As confirmed by the low Levin’s index, few species accounted for most of the prey consumed, indicating specialist feeding at least in the sampling period, which was limited to summer months. This result is atypical for billfish which are usually referred to as generalists (Somvanshi & Varghese, 2001; Abitı́a-Cárdenas et al., 2002; Vaske et al., 2004). Resource composition and prey turn-over in the area over the short sampling period may explain this result. Some species such as Coryphaena hippurus L. and Naucrates ductor (L.), which are reported as prey of T. belone (Nakamura, 1985), were scarcely represented or absent in the stomachs of the Mediterranean spearfish from the Strait of Messina. These two species do increase in abundance in Sicilian waters from August to December (Andaloro et al., 2003), when the swordfish fishing season by harpoon is about to finish. According to De Sylva (1975), the Mediterranean spearfish, like other billfish, is typically a clear-water species, requiring high transparency waters for its feeding which is largely visual. Diurnal feeding is also reported for other istiophorids, albeit it may extend till night-time depending on moon phases (Trias et al., 1996). However, in the stomachs of T. belone from the Strait of Messina, we have found highly digested bodies and hard part remains of cephalopods. These organisms are known to undergo diel vertical migrations, wherein they commonly inhabit deep water during the day, then ascend towards the surface at night (Roper, 1974). Hence, their high occurrence and abundance and the condition of their remains in the stomachs of specimens caught at day-time suggest that they were probably ingested the night before the Mediterranean spearfish capture, thus revealing potential nocturnal predatory behaviour. As cephalopods are predators upon mesopelagic organisms (Sanchez, 1982; Marabello et al., 1996), they represent, in terms of trophic webs and energetic fluxes, a major link between mesopelagic and epipelagic environments. Generally, T. belone is presumed to feed upon organisms whose distribution is closely determined by oceanographic and trophic conditions: organisms concentrated at or just above the thermocline (De Sylva, 1975) as well as those moving upward for trophic reasons should be expected to attract this predator for feeding purposes. In the Strait of Messina, T. belone shares the habitat with other large pelagic predators, mainly the bluefin tuna Thunnus thynnus (L.), the swordfish X. gladius and the dolphinfish C. hippurus (Romeo et al., 2001), as confirmed by catch records by harpoon fishery over about three decades, from 1976 to 2003 (Di Natale et al., 2005a). 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Correspondence should be addressed to: Luca Castriota Central Institute for Marine Research (ICRAM) STS Palermo via Emerico Amari 124 90139 Palermo Italy castriotaluca@hotmail.com Romeo T., Ancora S., Manganaro A., Andaloro F. and Fossi C. (2001) The swordfish fishing by harpoon in the Strait of Messina. Rapports de la Commission Internationale pour l’Exploration Scientifique de la Mer Méditerranée 36, 318. 187