INTRODUCTION
The sperm whale (Physeter macrocephalus Linnaeus, 1758) has a cosmopolitan distribution, inhabiting all oceans and also reaching high latitudes (Whitehead, Reference Whitehead2003). In the Mediterranean Sea, sperm whales are widely distributed (Notarbartolo et al., Reference Notarbartolo di Sciara, Frantzis, Bearzi, Reeves, Reeves and Notarbartolo di Sciara2006), in both the Eastern (Frantzis et al., Reference Frantzis, Alexiadou, Paximadis, Politi, Gannier and Corsini-Foka2003) and Western basins (Gannier et al., Reference Gannier, Drouot and Goold2002). Sperm whale strandings along Italian coasts have been recorded in the past (Bolognari, Reference Bolognari1950) and were quite commonly reported in the last 20 years of strandings monitoring (Banca Dati Spiaggiamenti, 2011; Bearzi et al., Reference Bearzi, Pierantonio, Affronte, Holcer, Maio and Notarbartolo di Sciara2011; Mazzariol et al., 2011). Few data are available concerning population structure and abundance in these areas (Gannier et al., Reference Gannier, Drouot and Goold2002; Lewis et al., Reference Lewis, Gillespie, Lacey, Matthews, Danbolt, Leaper, McLanaghan and Moscrop2007), as well as the habitat use for this species (Azzellino et al., Reference Azzellino, Gaspari, Airoldi and Nani2008; Praca et al., Reference Praca, Gannier, Das and Laran2009). The feeding habits of sperm whale have been widely investigated throughout the oceans, establishing that cephalopods are its preferred prey, although some cases of predation upon other animal species and debris are reported (Clarke, Reference Clarke1980; Kawakami, Reference Kawakami1980; Santos et al., Reference Santos, Pierce, Boyle, Reid, Ross, Patterson, Kinze, Tougaard, Lick, Piatkowski and Hernandez-Garcia1999, Reference Santos, Pierce, Hartmann, Smeenk, Addink, Kuiken, Reid, Patterson, Lordan, Rogan and Mente2002; Whitehead, Reference Whitehead2003; Jacobsen et al., Reference Jacobsen, Massey and Gulland2010; Mazzariol et al., 2011). Moreover, little is known about the ecology and feeding habits in the Mediterranean Sea (Drouot et al., Reference Drouot, Gannier and Goold2004; Praca & Gannier, Reference Praca and Gannier2008); so far stomach content analysis was performed on one single specimen stranded in Crete (Roberts, Reference Roberts2003), resulting in cephalopod beaks only, belonging to seven different species, of which Histioteuthis bonnellii (Férussac, 1834) represented the great majority.
Recent advances in the investigation of the diving and foraging behaviour of sperm whale were obtained using tagging technologies (Madsen et al., Reference Madsen, Payne, Kristiansen, Wahlberg, Kerr and Møhl2002; Miller et al., Reference Miller, Johnson and Tyack2004; Zimmer et al., Reference Zimmer, Johnson, D'Amico and Tyack2003), resulting in the description of the predator–prey interactions and the use of creak sounds to locate prey.
The aim of this note is to provide a contribution to knowledge about the food habits of sperm whales in the Mediterranean Sea, considering that this is the first record available to date in the Western part, and to relate prey sizes and food requirements to recent results from observations on the diving behaviour of the species.
MATERIALS AND METHODS
On 16 May 1988, a sperm whale was sighted while swimming slowly near the coast of Forte dei Marmi, Tuscany (Figure 1); the day after, it was found stranded on the beach, already dead. The carcass was picked up and transported to the Natural History Museum of Milan for dissection. It was a male, which measured 11.75 m and weighed 18 t. Stomach contents were carefully removed and preserved in 70% ethanol for the analysis. The whole skeleton is now mounted in the Natural History Museum of Milan exhibition.
Stranding site ▴.
Cephalopod lower beaks were identified by species using the reference collection of the laboratory, following the indication of Clarke (Reference Clarke1986). Lower rostral length (LRL) was measured to the nearest 0.01 mm with a digital Vernier caliper. Dorsal mantle length (DML) and wet weight (WW) for each ingested prey were estimated from the regressions of Clarke (Reference Clarke1986) for Galiteuthis armata Joubin, 1898 and Octopoteuthis sp., and from a new original regression for Histioteuthis bonnellii obtained on the basis of Ligurian Sea material. In fact, the relationships between LRL and both DML and WW published in the past were referred to other histioteuthid species and to the family as a whole (Clarke, Reference Clarke1986) or calculated by means of small specimens (Wurtz et al., Reference Wurtz, Poggi and Clarke1992), and were not representative of the entire size range of this species. Details about specimens used for this purpose are reported in Table 1. Larger individuals were collected during bottom trawl surveys (i.e. MEDITS surveys) or by monitoring professional trawl and longline fisheries, while smaller ones were caught by the 16 ft Isaacs-Kidd Midwater Trawl (IKMT) during oceanographic campaigns carried out with the aim to study the biodiversity of the mesopelagic fauna of the Ligurian Sea. The total ingested biomass was calculated as the sum of the weights of each single cephalopod. The total biomass of cephalopods with highly digested beaks was estimated by multiplying the average weight of cephalopods of that species found in the stomach by their number.
Details of Histioteuthis bonnellii specimens used to develop the new relationships between beak lower rostral length (LRL) and dorsal mantle length (DML) or weight. IKMT indicates specimens caught by Isaacs-Kidd Midwater Trawl during oceanographic campaigns.
RESULTS
Food items were made up of cephalopod beaks, 233 upper and 291 lower beaks, and one cephalopod eye lens: no flesh remains were found.
Of the 291 lower beaks examined, 288 belonged to Histioteuthis bonnellii, two to Galiteuthis armata and one to Octopoteuthis sp. (Table 2). All beaks were found at about the same digestion rate, except for 41 highly digested beaks: they were identified as all belonging to H. bonnellii.
Identified species, beak dimensions and estimated size and weight of cephalopods found in the stomach contents of sperm whale stranded in Italy.
On the basis of the Ligurian Sea material, the two new relationships for H. bonnellii can be expressed as follows:
$$\eqalign{\hbox{DML} &= 2.0012\hbox{LRL} - 2.1788 \;\lpar N = 34\semicolon \; r^{2} = 0.87 \rpar \cr \hbox{WW} &= 1.442\hbox{LRL}^{3.2462} \lpar N = 34\semicolon \; r^{2} = 0.91\rpar}$$They are represented in Figure 2, compared to the older Clarke equations. The relationships between LRL and DML are similar (Figure 2A), while a great difference is evident for the relationships between LRL and WW (Figure 2B), resulting in a great underestimation of the reconstructed biomass if the old Clarke equation was applied.
(A) Relationship of lower rostral length to dorsal mantle length in Histioteuthis bonnellii; (B) relationship of lower rostral length to wet weight in H. bonnellii.
The total estimated ingested biomass was 608.02 kg, which represents 3.38% of the total sperm whale body mass. The mean estimated WW of the ingested preys was 2089.42 g. In Figure 3, the LRL frequency distribution of H. bonnellii beaks is reported. By applying the newly calculated relationships, H. bonnellii ranged from 71.7 mm to 229.8 mm DML and from 214.6 g to 5341.1 g WW, with a mean size of 161.8 mm and a mean weight of 2108.6 g, representing about 1.38% in length and 0.012% in weight of the whale, respectively.
Lower rostral length frequency distribution of Histioteuthis bonnellii beaks found in the sperm whale stomach contents.
DISCUSSION
Caution is needed in analysing stomach contents of stranded animals (Santos et al., Reference Santos, Clarke and Pierce1998), as they may not be in a healthy condition, meaning that they are unable to feed for several days beforehand, or not able to feed properly. In our case, considering that no flesh remains were found and all beaks were in approximately the same digestion stage (except for the 41 highly digested beaks), we can assume that the whale could probably not feed properly during the last days and the stomach contents represent the last foraging day. As stated by MacLeod et al. (Reference MacLeod, Santos, Lopez and Pierce2006), cetaceans with reduced dentition (such as the sperm whale) specialize in using suction to capture prey, consuming a narrow range of relatively small organisms. In our case, the predator–prey size ratio (PPSR) was 1.37% of the sperm whale's body length, which is consistent with this hypothesis.
The sperm whale shows a great variety of prey throughout all seas and oceans. This may be due to geographical, seasonal or sex- and age-related factors. In some areas it prefers ammoniacal, slow swimming squids (Whitehead, Reference Whitehead2003), which are also dominant or abundant in the stomach contents of sperm whales that have not been stranded, but directly killed by whaling (Clarke, Reference Clarke1980; Clarke et al., Reference Clarke, Martins and Pascoe1993). In other cases, it can largely feed on muscular squids (Clarke & Paliza, Reference Clarke and Paliza2001) or fish (Martin & Clarke, Reference Martin and Clarke1986).
In the Mediterranean Sea, as far as we know, there are no squid as big as some species found in other oceans, which probably have a higher calorific value, except for ommastrephid squids (i.e. Todarodes sagittatus (Lamarck, 1798) and Ommastrephes bartramii (Lesueur, 1821)) or Thysanoteuthis rhombus Troschel, 1857, and only a few records of very large squid (Bello, Reference Bello2003). All other pelagic cephalopods in the Mediterranean are represented by small-sized species, except Histioteuthis bonnellii, which can grow up to more than 6 kg in weight.
The results derived from some studies carried out in recent years using D-Tag allow us to understand much more about the diving behaviour of sperm whales in the Ligurian Sea; it seems that the sperm whale starts clicking at 96.7 m depth during its descent, and the foraging phase starts at a depth of 635.6 m (Watwood et al., Reference Watwood, Miller, Johnson, Madsen and Tyack2006). Considering that the most important prey is H. bonnellii, both in the Mediterranean (Roberts, Reference Roberts2003; Mazzariol et al., Reference Mazzariol, Di Guardo, Marsili, Fossi, Leonzio, Petrella, Ferrante, Airoldi, Frantzis, De Beraldo Quiros, Pavan, Podestà, Garibaldi, Vizzini, Gaspari, Zizzo, Traversa, Marcer, Cozzi and Fernandez2011; Praca et al., Reference Praca, Laran, Lepoint, Thomé, Quetglas, Belcari, Sartor, Dhermain, Ody, Tapie, Budzinski and Das2011; present study) and in some areas of the Atlantic (Clarke et al., Reference Clarke, Martins and Pascoe1993; Spitz et al., Reference Spitz, Cherel, Bertin, Kiszka, Dewez and Ridoux2011), it is possible that sperm whales go to the correct depth to catch this species that undergoes significant vertical migrations, even if the largest specimens are preferably found in deeper water. In fact, Voss et al. (Reference Voss, Stephen, Dong, Sweeney, Roper, Mangold, Clarke and Boletzky1992) found larger juveniles and sub-adults at night in the Eastern Atlantic between 200 m and 800 m, and all but one mature animal at a depth below 600 m, with the great majority below 1000 m.
Histioteuthids are an important food source for several top predator species, such as fish, sharks and cetaceans (Orsi Relini & Garibaldi, Reference Orsi Relini and Garibaldi2005). In particular, comparing our results with those obtained by Roberts (Reference Roberts2003) in waters around Crete and in the Ionian Sea (Mazzariol et al., Reference Mazzariol, Di Guardo, Marsili, Fossi, Leonzio, Petrella, Ferrante, Airoldi, Frantzis, De Beraldo Quiros, Pavan, Podestà, Garibaldi, Vizzini, Gaspari, Zizzo, Traversa, Marcer, Cozzi and Fernandez2011), H. bonnellii represents the main prey species for the sperm whale and it is thought that its importance in the cetacean diet of the Mediterranean has been generally underestimated in the past.
ACKNOWLEDGEMENTS
The authors thank all of the people from the Natural History Museum of Milan who participated in the dissection of the stranded sperm whale and also made possible the collection of the stomach contents. The MEDITS specimens were collected by Dr A. Mannini and L. Lanteri. Thanks to Graziella Perini for the map drawing. Many thanks to the anonymous referees who contributed with valuable suggestions and comments.
FINANCIAL SUPPORT
The relationships between LRL and DML or WW for Histioteuthis bonnellii were calculated from old material collected by Professor L. Orsi Relini and in the framework of a project funded by the Italian Ministry for the Environment and the Protection of the Land and the Sea on biodiversity of cephalopods in the Pelagos Cetacean Sanctuary.
