INTRODUCTION
Albacore, Thunnus alalunga (Bonnaterre, 1788), is a highly migratory species found in both subtropical and temperate waters of three oceans. In the Atlantic, three stocks are commonly recognized by ICCAT (The International Commission for the Conservation of Atlantic Tunas): the northern and southern stocks separated by latitude 5oN, and the Mediterranean stock (ICCAT, 2006). The northern stock is considered to be independent of the Mediterranean stock based on the existence of an independent spawning zone in the Mediterranean (Dicenta, Reference Dicenta1975), different morphometrics (Bard, Reference Bard1981), different growth rates (Megalofonou, Reference Megalofonou2000) and ages of first maturity (Arena et al., Reference Arena, Potosci and Cefali1980), and distinct larval distribution (FAO, 1994). Tagging data are also concordant with this hypothesis, although some interstock migrations have been observed (Arrizabalaga et al., Reference Arrizabalaga, Costas, Juste, González-Garcés, Nieto and López-Rodas2004).
Albacore are top level carnivores and they opportunistically prey on schooling sardine, anchovy, mackerel and squid. Other authors have found that in the north-east Atlantic, the albacore diet is mainly composed of fish, primarily Trachurus trachurus (Ortiz de Zárate, Reference Ortiz de Zárate1987), and to a lesser extent, crustaceans (Hassani et al., Reference Hassani, Antoine and Ridoux1997); Bello (Reference Bello1999) reported the major diet in the Adriatic Sea to be cephalopods.
Albacore is not caught as a target species in the Turkish waters; rather it is a by-catch in bluefin tuna purse seine fishery and swordfish longline fishery. The catch quantity of albacore has not been recorded in the recent past before 2004, with a total catch of 27 MT (TUIK, 2004). Due to the decrease in the stocks of small pelagic species (anchovy and sardine), which are important for Turkish fishery, Turkish fishermen have changed their fishing areas and their target species in recent years. Albacore was caught as a target species in the Levantine Sea by driftnet between May and July in 2006 (Karakulak et al., Reference Karakulak, Bilgin and Gökoglu2007), after which time driftnet fishery was prohibited in the Turkish waters by the Turkish Ministry of Agriculture and Rural Affairs in September 2006 (Anonymous, 2006).
MATERIALS AND METHODS
The size of the albacore analysed ranged from 64 to 91 cm fork length (FL) (mean 73.9±4.9 cm), and they weighed between 4.8 and 12.7 kg (mean 6.9±1.4 kg); 116 stomachs were examined. The albacore were caught in Antalya Bay (Levantine Sea) by long line, set at the surface late in the afternoon and retrieved early in the morning, from May to July 2007, with the fishing ground depth ranging from 150 to 2300 m (Figure 1). The total length (FL) of the fish was measured to the nearest 0.1 cm and weight was recorded to the nearest 0.1 g.
Fig. 1. Sampling area.
Stomachs were removed immediately after capture of the fish and kept frozen waiting for processing in the laboratory. The beaks of cephalopods were separated for this study and stored in 70% ethanol. Identification of the cephalopod lower beak in the stomach contents was carried out according to Clarke (Reference Clarke1962, Reference Clarke1986), Mangold & Fioroni (Reference Mangold and Fioroni1966) and Lu & Ickeringill (Reference Lu and Ickeringill2002). All beaks were then compared to beaks from the personal collection of one of the authors (A.S.). For the species belonging to orders Sepiolida and Teuthida, the lower rostral length (LRL) was measured, while for the species of the order Octopoda, the hood length (HL) was measured. The systematic order of the species was determined according to Sweeney & Roper (Reference Sweeney, Roper, Voss, Vecchione, Toll and Sweeney1998). During specimen identification and measurement, a stereomicroscope (Olympus model SZ-60) with a micrometric ocular was used.
RESULTS
Fifty-five of the 116 stomachs examined were empty (~47%). In the remaining 61 full stomachs, most of the remnants of fish and crustaceans were digested to an unidentifiable condition; however, 633 lower beaks from cephalopods were identified.
Overall, cephalopod remains were present in 95.1% of the stomach contents in the albacore followed by teleosts at 47.5% and crustaceans at 39.3%. In addition, some plastic remains were present in the stomach contents (Table 1).
Table 1. Frequency of the general food groups in stomach contents of Thunnus alalunga (NS, number of occurrences in stomach contents; %FO, percentage frequency of occurrence).
In this study, 633 lower beaks of cephalopod specimens belonging to 14 species were found. The identified species are generally pelagic species and among them, Heteroteuthis dispar was the most abundant species (56%), followed by Onychoteuthis banksii (12%) and Chiroteuthis veranyi (8.6%). The percentage of frequency in the stomach was 50.8% for O. banksii and 49.1% for H. dispar, followed by C. veranyi (36%) and Todarodes sagittatus (27.2%) (Table 2). The pelagic species, Tremoctopus violaceus and Argonauta argo, constituted 9.5% of the content, and when counted together, the pelagic species were the third most-abundant species.
Table 2. Percentage distributions and frequency of occurrence of cephalopods found in stomach contents of Thunnus alalunga (NS, number of stomachs; NI, number of individuals; %N, percentage composition by number; %FO, percentage frequency of occurrence).
One of the most frequently found species inside the stomach of H. dispar, is a short pelagic Sepiolid that migrates to the surface at night (Roper, Reference Roper1974). Three hundred and fifty-seven lower beaks from this species were counted inside 30 of the stomachs and the length was estimated from the lower rostral length using the equation ML = 13.759 LRL1.574 (Relini, Reference Relini1995). The range of the lower rostral length was LRL 0.6–1.5 mm and the mantle lengths estimated from this equation are given in Figure 2. From the estimated length values, the specimens were considered to be sub adult and adult individuals.
Fig. 2. Relative distribution of estimated mantle lengths based on lower rostral length of the beaks of Heteroteuthis dispar found in the stomach of albacore, Thunnus alalunga.
Onychoteuthis banksii is a mid-sized, muscular squid; 78 specimens of this species were found inside 31 stomachs, making it the most frequently found species (50.8%) inside the examined stomachs (Table 2). The range of the LRL was between 0.4–2.3 mm, from which we estimated the mantle length using the equation ML = 2.31+32.75LRL given by Lu & Ickeringil (2002). We found these to be generally sub-adult specimens (Figure 3).
Fig. 3. Relative distribution of estimated mantle lengths based on lower rostral length of the beaks of Onychoteuthis banksii found in the stomach of albacore, Thunnus alalunga.
Todarodes sagittatus is a large muscular squid; 42 specimens of this species were found inside 17 stomachs and the range of the LRL was between 0.5–3.0 mm. The mantle lengths of the individuals were estimated using the equation l = −11.3+41.36r given by Clarke (Reference Clarke1986) and from these estimates, all individuals were considered to be immature specimens, according to Quetglas et al. (Reference Quetglas, Alemany, Carbonell, Merella and Sanchez1998) (Figure 4).
Fig. 4. Relative distribution of estimated mantle lengths based on lower rostral length of the beaks of Todarodes sagittatus found in the stomach of albacore, Thunnus alalunga.
Chiroteuthis veranyi is a luminous and gelatinous squid that lives in mesopelagic and bathypelagic zones. Knowledge about several Chiroteuthis species is still incomplete (Clarke, Reference Clarke1986), but the distribution of C. veranyi in the Mediterranean Sea is well-known (Mangold & Boletzky, Reference Mangold and Boletzky1987). Fifty-five lower beaks from this species were counted inside 22 stomachs and the range of the LRL was between 0.5–3.5 mm. The estimated mantle lengths of the individuals, using the equation l = 11.4+24.46r from Clarke (Reference Clarke1986) are summarized in Figure 5.
Fig. 5. Relative distribution of estimated mantle lengths based on lower rostral length of the beaks of Chiroteuthis veranyi found in the stomach of albacore, Thunnus alalunga.
Fifty-five specimens of the pelagic octopodan cephalopod, T. violaceus were found inside 13 stomachs and the range of the hood length of the lower beaks was between 0.4–1.1 mm. These beaks were of similar length to the 7–12 mm ML juvenile individual beaks, found in the Thunnus thynnus stomachs (unpublished data). Through comparison with this data, all specimens found in the stomach of T. alalunga were estimated to be juvenile individuals; the hood lengths of the specimens are presented in Figure 6.
Fig. 6. Relative distribution of hood length of the beaks of Tremoctopus violaceus found in the stomach of albacore, Thunnus alalunga.
DISCUSSION
In this study, cephalopods were found in 95% of the stomach contents of the albacore Thunnus alalunga in the eastern Mediterranean (Table 1). Six hundred and thirty-three cephalopod specimens from 14 species were found in the examined stomach contents (Table 2) and were generally found to be small and slow swimmers.
The ubiquitous species of the Mediterranean, Heteroteuthis dispar, as Bello (Reference Bello1999) reported, was also found to be the most abundant species (56.4%) in this study, followed by Onychoteuthis banksii (12.32%), Chiroteuthis veranyi (8.59%) and Todarodes sagittatus (6.64%) from the order Teuthida (Table 2). All of the sepiolid specimens (Heteroteuthis dispar) and nearly 75% of the specimens belonging to the Teuthida (Onychoteuthis banksii and Chiroteuthis veranyi) that were used as prey represent luminous species carrying photophores. Fourteen species were found in the stomach contents of albacore in the eastern Mediterranean, which is a high number when compared to the 4 species reported by Bello (Reference Bello1999) from the Adriatic Sea.
The benthic cephalopod specimens identified, Eledone moschata and Scaeurgus unicirrhus, were probably used as bait in long-line fishing.
The pelagic cephalopods (Argonauta argo and Tremoctopus violaceus) found in the stomach contents of T. alalunga in the eastern Mediterranean, were not reported by Bello (Reference Bello1999) in the Adriatic Sea. These two geographical areas also gave the same results for swordfish (Xiphias gladius) (Bello (Reference Bello1991) 3.5%; Salman (Reference Salman2004) 25.5%), which might be due to the higher surface water temperature in the eastern Mediterranean (28–29°C) compared to the western Mediterranean Sea and Adriatic Sea, causing a higher number of the pelagic cephalopods to be distributed in the temperate surface waters.
Even the cephalopod species number in the Atlantic Ocean has been reported to be greater than that in the Mediterranean and Adriatic Seas (Mangold & Boletzky, Reference Mangold and Boletzky1987; Bello Reference Bello1990); the deep waters around 1000 m in the eastern Mediterranean create an advantage for the distribution of oceanic species in the eastern Mediterranean compared to the Adriatic Sea.
In the first study on the stomach contents of albacore in the Mediterranean Sea, and in the results given by Bello (Reference Bello1999) for the Adriatic Sea, cephalopods were also reported to be the most abundant group (29%), followed by fish and crustaceans (26%). Albacores of similar length to the individuals in this study were examined by Pusineri et al. (Reference Pusineri, Vasseur, Hassani, Meynier, Spitz and Ridoux2005) in the Biscay Gulf, and these authors reported that fish were the most frequently found prey (92%) in the stomach, followed by cephalopods (29.4%). Similarly, Watanabe et al. (Reference Watanabe, Kubodera, Masuda and Kawahari2004) reported that the main prey of albacores in the central North Pacific was fish (59%), followed by cephalopods (27%). These results showed that, like in other predators, the dominant prey of this opportunist species can vary according to the abundance of the different prey species in the waters where they live.
The cephalopods were reported to contain more fatty acids and minerals than fish (Okuzumi & Fujii, Reference Okuzumi and Fujii2000). Due to the higher percentage of cephalopods as prey in our study area than in other regions of the Mediterranean, T. alalunga in the eastern Mediterranean may be growing faster than individuals in other regions. Future studies on the comparison of the diet and growth rates of this species in different regions of the Mediterranean Sea will have to provide the data necessary to understand the migration of albacore in the Mediterranean Sea and assess the importance of prey composition.
The white plastic pieces found in the stomach contents of the albacore with a rate of ~10% indicate that in the open sea, pollution affects even the top predators.
ACKNOWLEDGEMENTS
This study was financially supported by the Scientific and Technological Research Council of Turkey (TUBITAK) No. 108-O-483 and the Research Fund of The University of Istanbul with the project number BYP/1761. We are grateful to the fishing companies DARDANEL (Canakkale, Turkey), GROUP SAGUN (Antalya, Turkey), the Turkish Bluefin Tuna Farmers Association (OYID), Mr Tuncay Seker, Dr Burcu Bilgin and Dr Elif Özgür for their help.
