CEPHALOPODS IN THE DIET OF ALBACORE, T H U N N U S A L A L U N G A, FROM THE ADRIATIC SEA

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1 J. Moll. Stud. (1999), 65, The Malacological Society of London 1999 CEPHALOPODS IN THE DIET OF ALBACORE, T H U N N U S A L A L U N G A, FROM THE ADRIATIC SEA GIAMBATTISTA BELLO Laboratorio Provinciale di Biologia Marina, Molo Pizzoli, Bari, Italy (Received 6 May 1998; accepted 13 July 1998) ABSTRACT The stomachs of 56 albacore (Thunnus alalunga) caught in the southern Adriatic Sea contained 222 cephalopods, or 29% of prey. Most cephalopod remains were from small specimens. Juveniles and adults of Heteroteuthis dispar (61.5% of cephalopods) were more frequently preyed upon in the inshore fishing area (bottom depth: m); early juveniles of Todarodes sagittatus (21.6%) were more abundant offshore (750 1,150 m); early juveniles of Histioteuthis bonnellii (16.4%) were exclusive of the latter area. The estimated overall number of cephalopods dying of predation by albacore is specimens/fishing season (two months). INTRODUCTION Present address: Acquario Provincia le Molo Pizzoli, Bari, Italy Studies of stomach contents of teuthivorous p r edators have proved to be a very valuable tool to gather information on the biology and e c o l o g y of both predators and cephalopods in their food, as well as on the systematics of the latter (e.g. Clarke, 1980). In this respect, several predators caught in the Adriatic Sea (eastern Mediterranean Sea) have been examined (Bello, 1997). The present paper deals with the cephalopods found in the stomach contents of albacore, Thunnus alalunga (Bonnaterre, 1788) (Osteichthyes: Scombridae), from the southern Adriatic Sea. The albacore is a large schooling fish. It is cosmopolitan, epi- and mesopelagic in oceanic waters and accomplishes seasonal migrations (Collette, 1986). In the southern Adriatic Sea it occurs from late September to late Novemberearly December. In this period of time, the albacore supports a seasonal longline fishery mostly based in Mola di Bari and Monopoli (province of Bari, Italy). On average, 40,000 specimens per year of this commercially important fish are caught (Marano, Bello, De Zio, Rositani & Vlora, 1996). Thunnus alalunga feeds on a variety of epipelagic and mesopelagic organisms, including bony fishes, squids, and crustaceans (Le Gall, 1974). A detailed study on cephalopods from the stomach contents of North-Atlantic albacore was made by Bouxin & Legendre (1936). The diet of Mediterranean albacore has not been studied before. MATERIALS AND METHODS The albacore were caught in the south-western Adriatic Sea by drifting longline, set at the surface late in the afternoon and retrieved early in the morning, in September October in both 1992 (35 specimens) and 1994 (21 specimens). The two batches of albacore were caught in different areas and were composed of specimens of different size and age. The batch from 1992 was caught by the commercial fleet based in Mola that fished in an inshore area from 100 to 700 m in depth (Fig. 1); the catch was mostly made of 1 year old fish. The other batch, from 1994, was caught by longliners from Monopoli fishing offshore over bottoms deep from 750 to 1,150 m; these albacore were older than 2 years (Marano et al., 1996). The stomachs were removed from the fish soon after landing and kept frozen until the moment of their examination. Prey items were sorted by large taxonomic categories and preserved in 80% ethanol. Most cephalopods were represented by hard parts (beaks, lenses, and a few fragments of gladii). A large fraction of beaks were from early juveniles and differed in shape to some extent from older beaks, so that the regular keys (e.g. Clarke, 1962 and 1986) were not sufficient to identify them. Therefore, beak identification was accomplished by comparison with series of vouched for beaks of decreasing size, including beaks from juvenile specimens. Both lower and upper beaks were identified since in many instances they were not paired, viz. the number of upper beaks did not match that of lower beaks. Beaks were measured (upper rostral length URL, lower rostral length LRL) according to Clarke (1962). Mantle lengths (ML) of Heteroteuthis dispar were estimated

2 234 GIAMBATTISTA BELLO Figure 1. Albacore fishing areas in the southern Adriatic Sea. A inshore area (1992); B offshore area (1994). Depths in m. (After Marano et al., 1996) by the lower rostral lengths using the equation given by Orsi Relini (1995): ML LRL It was not possible to estimate mantle lengths and weights of teuthoids due to their very small size which fell outside the validity range of the available regression equations correlating LRL to ML and weight (e. g. Clarke, 1986). A three-stage digestionscale was used. Stage A: early digestion, the prey is identifiable by body features; stage B: advanced digestion stage, fleshy remains (arm crowns, buccal masses) are not useful to identify prey; stage C: very advanced digestion, only hard parts remain (beaks, lenses, gladii). No stomach content index, such as IRI, was calculated since very few prey items were represented by fleshy remains. RESULTS Six albacore stomachs ( 10.7%) did not contain any food. In all, remains of 222 cephalopods were found, which represent 29% of prey items, i. e. cephalopods are the numerically most important food category. Other items belonged to bony fishes (26%), crustaceans (26%), and gelatinous organisms (19%). The proportion of cephalopods by weight is much lower ( 1 %), because of the presence of very few specimens at early digestion stages. Only four specimens were at digestion stage A and three specimens at stage B. The vast majority of preycephalopods (97%) was represented by beaks only and many of these were not complete because of digestion. The species composition of cephalopods from albacore stomach contents is low in diversity. Only four species were found: Heteroteuthis dispar (Rüppell, 1844), Todarodes sagittatus (Lamarck, 1798), Histioteuthis bonnellii (Férussac, 1835) and an unidentified octopodine (Table 1). All of them, except the octopodine (an early juvenile), are oceanic. Fragments of nine upper beaks and one lower beak were not

3 identified; however, they probably belonged to one or more of the three most abundant species. The coefficients of prey-cephalopod frequency in albacore stomachs and the mean n u m b e r of cephalopods per stomach are reported in Table 2. Highly significant differences were found between the numerical compositions of prey-cephalopods of 1992 and 1994 samples by the 2 (Kimball s corrected) applied 2 to H. dispar, H. bonnellii and T. sagittatus: , df 2, p Hence, the diets of albacore from the two samples differed from each other. Heteroteuthis dispar is a small-sized sepiolid squid that migrates towards the surface at night (Roper, 1974). Albacore contained remains of both juveniles and adults. The only specimens at an early digestion stage were an unsexed juvenile (ML 5.7 mm), a subadult female (ML 13 mm), and a fully mature male (ML CEPHALOPODS IN THE DIET OF ALBACORE mm), all of them retrieved from a single inshore albacore stomach. An offshore albacore stomach contained an arm crown with buccal mass and a few lose spermatophores, which indicates the occurrence of mature males over a wide depth range. Heteroteuthis dispar was much more abundant in the stomachs of inshore- than offshore-caught albacore. LRLs range from 0.3 to 1.5 mm; URLs range from 0.3 to 1.2 mm. The size frequency distributions for lower and upper beaks are graphed in Fig. 2. The estimated mantle lengths (EML) range from 2.1 to 25.8 mm; some selected EML values are reported in Fig. 2. The rostral length distributions hint at the presence of two size-age cohorts, but this is most probably an artefact due to the sum of distinct size frequencies of the inshore and offshore samples. Most beaks from inshore-caught albacore were from adult specimens and from offshore-caught Table 1. Diversity and abundance of cephalopod remains in albacore stomach contents. Percentages were only calculated for identified taxa inshore (1992) offshore (1994) overall n % n % n % Order Sepiolioidea Family Sepiolidae Heteroteuthis dispar Order Teuthoidea Family Ommastrephidae Todarodes sagittatus Family Histioteuthidae Histioteuthis bonnellii Order Octopoda Family Octopodidae Octopodine sp Unidentified cephalopods Total Table 2. Coefficients of prey-cephalopod frequency (Fp) and mean number of cephalopods per stomach (p ). F p n p / N p 100, where n p is the number of stomachs containing prey of each taxon and N p is the number of stomachs containing prey; p number of cephalopods / N p inshore (1992) offshore (1994) overall F p p F p p F p p Heteroteuthis dispar Todarodes sagittatus Histioteuthis bonnellii Octopodine sp all cephalopods

4 236 GIAMBATTISTA BELLO Figure 2. Upper (URL) and lower (LRL) rostral length distributions for Heteroteuthis dispar. Estimated mantle lengths (in mm) at selected LRL values (lowest, mean, highest) are reported in the LRL graph.

5 albacore were from juvenile specimens. The overall distribution of lower beak size is moved to the right with respect to that of upper beaks. This is due to the fact that in each pair of beaks the lower rostral length exceeds that of the upper rostrum by about mm. Todarodes sagittatus is a muscular, large squid that is represented in albacore stomach contents by beaks from early juveniles only (LRL mm; URL mm). It was more frequent in offshore- than in inshorecaught albacore. The rostral length frequency distributions are roughly unimodal. In each pair of beaks, LRL URL therefore the LRL distribution is further to the right than that of URL (Fig. 3). Histioteuthis bonnellii is a poorly-swimming, large-sized oceanic squid. Offshore albacore preyed upon early juvenile stages of this squid (LRL mm; URL mm). In the stomachs of inshore-caught albacore only two pairs of beaks were found; they were the largest beaks found and were from juvenile specimens (LRL 3.7 and 4.8 mm; URL 3.9 and 5.2 mm). All beaks were immature (Clarke, CEPHALOPODS IN THE DIET OF ALBACORE ). Most lower beaks had lost their wings. In each pair of beaks of H. bonnellii, URL is slightly longer than LRL (mean URL/LRL 1.04 [Bello, 1994]), so that the frequency distribution of URLs is slightly moved to the right with respect to LRLs (barely visible in Fig. 4). Both distributions are unimodal. The octopodine early juvenile, with ink sac in the mantle cavity and two rows of suckers on arms, ML 7 mm, was in bad condition. DISCUSSION The albacore appears to prefer small-size, mostly slow-moving prey, despite its size and swimming capabilities. In addition to small and tiny cephalopods, other prey found in the albacore stomach contents include small fishes, gelatinous planktonic animals and the amphipod Platyscelus ovoides which is usually associated with jellyfishes. Also Bouxin & Legendre (1936) reported that cephalopods preyed upon by North-Atlantic albacore were Figure 3. Upper (URL) and lower (LRL) rostral length distributions for Todarodes sagittatus.

6 238 GIAMBATTISTA BELLO Figure 4. Upper (URL) and lower (LRL) rostral length distributions for Histioteuthis bonnellii. mainly juveniles. They found a large variety of prey-cephalopods (i.e. some 24 different species, including the three cephalopod species preyed upon by Adriatic albacore) which conflicts with the present results. The North- Atlantic teuthofauna is more diverse than those of the Mediterranean and the Adriatic (cf. Guerra, 1992; Mangold & Boletzky, 1987; Bello, 1990); nevertheless all teuthophagous predators from the southern Adriatic Sea examined to date contained in their stomachs a wider range of prey items (Bello, 1997). Furthermore, on the whole, the beaks found in albacore stomach contents were the smallest ever found among those from pelagic and demersal Adriatic predators examined. Some alimentary niche overlap with other large pelagic predators, e.g. the swordfish and some dolphins, is due to the ubiquitous H. dispar. Most probably, the albacore had fed in the upper layers (see also Bouxin & Legendre, 1936). This is in agreement with the fact that in September November albacore are available to fishermen at the sea surface all day long; during daytime they are fished by hook-and-line sport fishermen and during night-time by professional fishermen. However some movements of albacore towards deeper layers have been recorded (Aloncle & Delaporte, 1973). The presence of very few undigested cephalopods and many hard part remains depends on the diel migrating behaviour of oceanic cephalopods which move towards the surface at night- time (Roper, 1974). According to Aloncle & Delaporte (1973) albacore feeding activity follows circadian rhythms with three peaks: at dawn, 2 3 p.m., and sunset. Taking into account the albacore feeding periodicity, cephalopod diel migrations, conditions of cephalopod remains, and fishing time, it is supposed that most cephalopods found in the stomach contents had been ingested the night before albacore capture. The differences in prey-cephalopod spectra for the 1992 and 1994 samples may be due to differences in the oceanic cephalopod taxocoenosis of the two years (cf. Le Gall, 1974). However the most important factor, in my opinion, to explain such differences is the depth of the areas where the two albacore batches were caught. Histioteuthis bonnellii and Todar - odes sagittatus appear to prefer areas with depths over 500 m (Clarke, 1966) and probably the areas inhabited by their early juveniles are even deeper. Hence they were preyed upon by albacore mainly in the offshore fishing area. Heteroteuthis dispar is already frequent in areas 500 m deep. (No age-related food preference may be invoked to explain differences in diet of the two albacore batches, since this fish is quite an opportunistic predator [Le Gall, 1974]). All three identified prey items are keystone elements in Mediterranean oceanic food webs (Bello, 1997). Heteroteuthis dispar is the most abundant cephalopod preyed upon by Adriatic

7 albacore. Specimens of every size, hence age, were found at the same time in albacore stomach contents. Juvenile specimens appear to be comparatively more abundant offshore than inshore, which might be related to preference in spawning areas. An egg of this species was collected on the bottom at 540 m of depth off Banyuls-sur-Mer, Catalan Sea (Boletzky, 1978). Heteroteuthis dispar, despite its small size, is a keystone element in Adriatic trophic webs involving oceanic cephalopods: it was found in demersal chondrichthyan fishes (Bello, 1995) as well as in large pelagic animals, such as swordfish and dolphins (Bello, 1991, 1997). This bobtail squid pays a very heavy toll to teuthivorous predators. Just the albacore ingests on the average an estimated specimens, both juveniles and adults, during the fishing season (see further). The presence of H. dispar in the Adriatic Sea was first recorded thanks to specimens found in predators stomach contents (Bello, 1990). Histioteuthis bonnellii is also a prey common in the diet of several Adriatic predators (Bello, 1997). It is an ammoniacal squid and a poor swimmer preyed upon by small and large predators, including the sperm whale (Clarke, 1980) and, in the Adriatic Sea, the blue shark Prionace glauca, a sluggish predator (Politi, 1991). The present records are the first concerning very young specimens as prey. Todarodes sagittatus, a muscular squid, is preferred by active predators such as the swordfish (Bello, 1991). Juveniles are preyed upon also by sluggish predators. As far as cephalopods are concerned, the albacore appears to occupy a peculiar alimentary niche, viz. mostly preying upon very small specimens, either juveniles of large-sized species or juveniles and adults of small-sized species. Based on an estimated mean seasonal catch of 40,000 albacore (Marano et al., 1996) and a supposed total mortality rate Z 0.8, the estimated mean number of albacore present during the two-months fishing season is 200,000. (No mortality rate values are available for the Mediterranean albacore stock; since the North- Atlantic and Mediterranean stocks appear to be in a similar status of exploitation, the value of natural mortality rate, M 0.3, and the data to calculate the mean fishing mortality rate, F 0.5, over a 19 years period for the North- Atlantic albacore stock [ICCAT, 1996] were used to calculate Z M F). In turn, the average number of cephalopods dying of predation (P) by the southern Adriatic subpopulation of Thunnus alalunga during the fishing season may be estimated by the equation: CEPHALOPODS IN THE DIET OF ALBACORE ,000 P N c 56 where 200,000 is the mean number of albacore, 56 is the number of stomachs examined, N c is the number of cephalopods found in their stomach contents, and 8 is the number of weeks in the two-months fishing season. (The turnover of cephalopod beaks in albacore stomachs is not known; a value of one week was chosen, which is surely overestimated, in order to yield a conservative, safe estimate of cephalopods dying of predation.) The estimated overall number of cephalopods eaten by south Adriatic albacore during the fishing season is P , of which are H. dispar, are juvenile T. sagittatus and are juvenile H. bonnellii. ACKNOWLEDGEMENTS I wish to express my gratitude to Dr. Malcolm R. Clarke for the critical reading of the manuscript and the editorial work. REFERENCES ALONCLE, H. & DELAPORTE, F Données nouvelles sur le germon Thunnus alalunga Bonnaterre 1788 dans le nord-est Atlantique Première partie. Revue des Travaux Institut des Pêches mar - itimes Nantes, 37: BELLO, G The cephalopod fauna of the Adriatic. Acta Adriatica, 31: BELLO, G Role of cephalopods in the diet of the swordfish, Xiphias gladius, from the eastern Mediterranean Sea. Bulletin of Marine Science, 49: BE L L O, G Histioteuthis bonnellii ( C e p h a l o p o d a : Histioteuthidae) in the Adriatic Sea: evidence from predator stomach contents. Bollettino Malaco - l o g i c o, 3 0: BELLO, G Heteroteuthis dispar (Cephalopoda: Sepiolidae) nella dieta di selaci demersali. Biologia Marina Mediterranea, 2(2): BELLO, G Teuthophagous predators as collectors of oceanic cephalopods: the case of the Adriatic Sea. Bollettino Malacologico, 32: BOLETZKY, S.V Premières données sur le développement embryonnaiere du sepiolide pelagique Heteroteuthis (Mollusca, Cephalopoda). Hali - otis, 9: BO U X I N, J. & LE G E N D R E, R La faune pélagique de l Atlantique au large du Golfe de Gascogne, recueillie dans des estomacs de Germons Deuxième Partie: Céphalopodes. Annales de l Institute O c é a n o g r a p h i q u e, 1 6(1): CL A R K E, M.R The identification of cephalopod 8

8 240 GIAMBATTISTA BELLO beaks and the relationship between beak size and total body weight. Bulletin of the British Museum (Natural History), Zoology, 8: CLARKE, M.R A review of the systematics and ecology of oceanic squids. Advances in Marine Biology, 4: CL A R K E, M.R Cephalopods in the diet of sperm whales of the southern hemisphere and their bearing on sperm whale biology. Discovery Reports, 3 7: CL A R K E, M.R A handbook for the identific a t i o n of cephalopod beaks. Clarendon Press, Oxford. COLLETTE, B.B Scombridae. In: Fishes of the North-eastern Atlantic and the Mediterranean (P.J.P. Whitehead, M.-L. Bauchot, J.-C. Hureau, J. Nielsen & E. Tortonese, eds.), 2: Unesco, Paris. GUERRA, A Mollusca, Cephalopoda. Fauna Ibérica, 1. Museo Nacional de Ciencias Naturales, CSIC, Madrid. ICCAT SCRS Detailed Report on Albacore. ICCAT Collective Volume of Scientific Papers, 42(2): 1-12, LE GALL, J.-Y Exposé synoptique des données biologiques sur le Germon Thunnus alalunga (Bonnaterre, 1788) de l Océan Atlantique. FAO Synopsis sur les Pêches, 109: MA N G O L D, K. & BO L E T Z K Y, S.v Céphalopodes. In: Fiches FAO d identification des espèces pour les besoins de la pêche. (Révision 1). Méditerranée et mer Noire (W. Fischer, M.-L. Bauchot & M. Schneider, eds.), FAO, Rome. MARANO, G., BELLO, G., DE ZIO, V., ROSITANI, L. & VLORA, A Aspetti biologici di Thunnus alalunga nell Adriatico meridionale (Osteichthyes: Scombridae). Biologia Marina Mediterranea, 3: ORSI RELINI, L Notes on midwater collections of Heteroteuthis dispar (Cephalopoda, Sepiolidae). Bulletin de l Institut océanographique Monaco, n o spéc. 16: POLITI, E Analisi dei contenuti stomacali della verdesca, Prionace glauca (Linné, 1758) nell alto e medio Adriatico. Laurea Thesis, University of Milan. ROPER, C.F.E Vertical and seasonal distribution of pelagic cephalopods in the Mediterranean Sea. Preliminary report. Bulletin of the American Malacological Union, May 1974: