INTRODUCTION
The Mediterranean spearfish Tetrapturus belone (Rafinesque) is a pelagic species belonging to the family Istiophoridae. It is considered a highly migratory species (Nakamura, Reference Nakamura1985) 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., Reference Di Natale, Mangano, Celona and Valastro2005b). Like other billfish, this species probably swims in the upper 200 m water layer, generally above or within the thermocline (Nakamura, Reference Nakamura1985). It is considerably abundant around Italy (Nakamura, Reference Nakamura1985), 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., Reference Di Natale, Mangano, Celona, Navarra and Valastro2003). 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., Reference Di Natale, Celona and Mangano2005a).
Although the importance of this species is rising on the market, scanty information on its biology and ecology is available. Robins & De Sylva (Reference Robins and De Sylva1960, Reference Robins and De Sylva1963) and Spartà (Reference Spartà1953, Reference Spartà1961) studied its eggs and larval development; Cavaliere (Reference Cavaliere1962) and Potoschi (Reference Potoschi2000) 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. (Reference Di Natale, Mangano, Celona, Navarra and Valastro2003, Reference Di Natale, Celona and Mangano2005a, Reference Di Natale, Mangano, Celona and Valastrob). Some fishery and biological information are reported by De Sylva (Reference De Sylva1975) and by Nakamura (Reference Nakamura1985). 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, Reference Spartà1961; Bini, Reference Bini1968; Tortonese, Reference Tortonese1975; Nakamura, Reference Nakamura1985).
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.
Fig. 1. Map showing the sampling area of Tetrapturus belone in the central Mediterranean Sea.
Specimens were measured to the nearest cm from the tip of the bill (upper jaw) to the posterior margin of the middle caudal rays (L F); 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 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., Reference Santos, Clarke and Pierce2001). Cephalopod beak lengths—the lower rostral length and the lower hood length in decapods and octopods respectively (Clarke, Reference Clarke1986)—were used to estimate mantle length of digested cephalopods and to reconstitute their weights, using relationships either in the literature (Clarke, Reference Clarke1986; Bello, Reference Bello1991), 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, Reference Ferry, Caillet, MacKinlay and Shearer1996). 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., Reference Castriota, Scarabello, Finoia, Sinopoli and Andaloro2005).
The importance of the different prey items was evaluated by calculating the frequency of occurrence (%F = number of stomachs containing prey i/total number of stomachs containing prey * 100), abundance (%N = number of prey i/total number of prey * 100) and reconstituted weight (%W = weight of prey i/total weight of all prey * 100). These values were used to calculate the index of relative importance (I RI) for each taxonomic category using mass instead of volume: I RI = (%N + %W) × (%F) (Hyslop, Reference Hyslop1980; Hacunda, Reference Hacunda1981). Fullness index (I F = no. stomachs with food/ no. total stomachs) was also calculated.
The degree of diet specialization was given by the Levin's standardized index (Hurlbert, Reference Hurlbert1978; Krebs, Reference Krebs1989), Bi = [(Σjpij2)−1−1] (n−1)−1 where:
Bi = Levin's standardized index for predator i;
pij = proportion of diet of predator i that is made up of prey j;
n = 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, Reference Krebs1989).
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.
Fig. 2. Length–frequency distribution of Tetrapturus belone from the Strait of Messina sampled for stomach contents analysis.
The cumulative prey types curve (Figure 3) for the entire data set resulted as fitting better with a logistic curve (R2 = 0.97; F(1,64) = 1627.2, P < 0.001) than with a linear relation (R2 = 0.92, F(1,64) = 734.2; P < 0.001); therefore the sample size was considered sufficient to describe the diet of Tetrapturus belone.
Fig. 3. Prey species accumulation plot as an average of 999 curves based on different random orders of the stomachs extracted (number of stomachs = 66). Vertical bars represent standard deviation.
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.
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 (%I RI) for food items of Tetrapturus belone.
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 %I RI. The families Clupeidae and Scomberesocidae were also well represented (%I RI = 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 = 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, Reference Bini1968; De Sylva, Reference De Sylva1975; Tortonese, Reference Tortonese1975; Nakamura, Reference Nakamura1985). Partial teuthophagy is also reported in the Ligurian Sea (Garibaldi & Orsi Relini, Reference Garibaldi and Orsi Relini2005). 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, Reference Cavaliere1962; Spartà, Reference Spartà1961; Tortonese Reference Tortonese1975).
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, Reference Nakamura1985). They are also preyed upon by large predacious fish such as tunas, swordfish, sharks and other billfish (Roper et al., Reference Roper, Sweeney and Nauen1984; Bello, Reference Bello1990, Reference Bello1991, Reference Bello1999; Abitía-Cárdenas et al., Reference Abitía-Cárdenas, Muhlia-Melo, Cruz-Escalona and Galván-Magaña2002; Rosas-Alayola et al., Reference Rosas-Alayola, Hernandez-Herrera, Galvan-Magana, Abitia-Cardenas and Muhlia-Melo2002; Vaske et al., Reference Vaske, Vooren and Lessa2004).
Fig. 4. Frequency of occurrence (%F), abundance (%N) and biomass (%W) of main prey categories (tel = unidentified teleosts; bel = Belonidae; sco = Scomberesocidae; clu = Clupeidae; oct = Octopoda; teu = Teuthoidea) in the diet of Tetrapturus belone from the Strait of Messina. Dashed lines refer to total fish (left) and total cephalopods (right).
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, Reference Spartà1961); 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 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 (Abitía-Cárdenas et al., Reference Abitía-Cárdenas, Muhlia-Melo, Cruz-Escalona and Galván-Magaña2002).
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, Reference Somvanshi and Varghese2001; Abitía-Cárdenas et al., Reference Abitía-Cárdenas, Muhlia-Melo, Cruz-Escalona and Galván-Magaña2002; Vaske et al., Reference Vaske, Vooren and Lessa2004). 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, Reference Nakamura1985), 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., Reference Andaloro, Campo, Sinopoli, Castriota, Campagnuolo and Pinheiro de Carvalho2003), when the swordfish fishing season by harpoon is about to finish.
According to De Sylva (Reference De Sylva1975), 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., Reference Trias, Marcano and Alio1996). 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, Reference Roper1974). 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, Reference Sanchez1982; Marabello et al., Reference Marabello, Guglielmo, Granata, Sidoti and Albertelli1996), 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, Reference De Sylva1975) 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., Reference Romeo, Ancora, Manganaro, Andaloro and Fossi2001), as confirmed by catch records by harpoon fishery over about three decades, from 1976 to 2003 (Di Natale et al., Reference Di Natale, Celona and Mangano2005a). Their concentration in this area, as well as that of T. belone, is possibly due to the considerable upwelling of food and nutrients into the upper layers of the Strait. Thus, they may be considered potential competitors for food, although they possibly adopt different strategies for exploiting the same environment (Dagorn et al., Reference Dagorn, Menczer, Bach and Olson2000).
ACKNOWLEDGEMENTS
The authors are grateful to V. Esposito for the analysis with PRIMER, to M. Falautano and anonymous referees for their constructive criticisms, and to P. Perzia for technical support.
