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Marine Biology Research, 2011; 7: 314Á316

SHORT REPORT

Histioteuthis bonnellii (Cephalopoda: ): A new prey item of the leatherback turtle Dermochelys coriacea (Reptilia: Dermochelidae)

GIAMBATTISTA BELLO1*, ANDREA TRAVAGLINI2 & FLEGRA BENTIVEGNA2

1Arion, Mola di Bari, Italy, and 2Stazione Zoologica ‘Anton Dohrn’, Naples, Italy

Abstract One lower and two upper beaks of the bonnellii were collected from the digestive tract contents of a leatherback turtle, Dermochelys coriacea, drowned in a gill net in the eastern Tyrrhenian Sea (western Mediterranean). The beaks were derived from two individuals whose estimated sizes were, respectively, 17.5 cm mantle length and 1962 g weight, 19.8 cm mantle length and 2636 g weight. Histioteuthid are ammoniacal, slow moving , capable of hovering in the water column. They may therefore mimic the preferred prey of leatherback turtles, i.e. gelatinous planktonic organisms. This is the first record of H. bonnellii as a prey item of D. coriacea.

Key words: Cephalopoda, Dermochelys coriacea, feeding, , Reptilia

Introduction access to concentrations of jellyfish, it makes seasonal migrations from tropical and subtropical The leatherback turtle, Demochelys coriacea (Vandelli, breeding areas to temperate waters (Houghton 1761) (Reptilia: Dermochelidae), is the largest and most widely distributed living marine chelonian et al. 2006). Dermochelys coriacea is endangered throughout its species, being found in all oceans except the Southern Ocean (Davenport 1998). Large juveniles and adults global range; it has been listed as such since 1970 and of both sexes occur in the whole Mediterranean Sea, is included on Appendix I of CITES (Convention on where they are threatened by fishing operations International Trade in Endangered Species) (Murphy (Casale et al. 2003). & Murphy 2005). As a consequence, studies of its According to Davenport et al. (2009), the leather- feeding habits are mostly occasional and have to take advantage of cases of accidental death, as suggested by

Downloaded By: [Bello, Giambattista] At: 08:32 26 March 2011 back is an obligate feeder on gelatinous organisms, predominantly medusae (Cnidaria: Scyphozoa), Murphy & Murphy (2005) in their list of conservation pyrosomes (Tunicata: Pyrosomidae) and siphono- actions. phores (Cnidaria: Hydrozoa); it also feeds on salps In this note we report the occurrence of the (Tunicata: Salpidae) (Bjorndal 1996). squid Histioteuthis bonnellii (Fe´russac, 1835) (Ce- It seems likely D. coriacea is an opportunist phalopoda: Teuthida: Histioteuthidae) remains in rather than a specialist predator on fairly large, the digestive tract contents of a leatherback turtle slow-moving gelatinous prey (Davenport & Balazs drowned in a gill net off Punta Stendardo (pro- 1991). It has been shown that the leatherback vince of Latina, Italy), Gulf of Gaeta, eastern turtle can thrive on a low-energy diet of gelatinous Tyrrhenian Sea (western Mediterranean), in August prey items by eating large quantities of them, 2005. thanks to unique anatomical features (Davenport To the best of our knowledge, this is the first 1998; Davenport et al. 2009). In order to have record of such a prey item in D. coriacea.

*Correspondence: G. Bello, Via Colombo 34, 70042 Mola di Bari, Italy. E-mail: [email protected] Published in collaboration with the University of Bergen and the Institute of Marine Research, Norway, and the Marine Biological Laboratory, University of Copenhagen, Denmark

(Accepted 6 May 2010; Published online 28 March 2011) ISSN 1745-1000 print/ISSN 1745-1019 online # 2011 Taylor & Francis DOI: 10.1080/17451000.2010.492224 Histioteuthis bonnellii: new prey item of the leatherback turtle 315

Materials and methods their cartilaginous parts because of the digestive processes; they were otherwise in good condition. The specimen of Dermochelys coriacea had drowned All three beaks were identified as belonging to in a gill net set in the eastern Tyrrhenian Sea off Histioteuthis bonnellii. Beak sizes and squid estimated Punta Stendardo (Gulf of Gaeta). It was retrieved on sizes are reported in Table 1. 22 August 2005. The leatherback turtle dimensions The sizes of upper beak no. 1 and that of the only were 130 cm curved carapace length and 95 cm lower beak suggest that these beaks were probably curved carapace width. It was a non-gravid female. paired, i.e. they were derived from the same squid. The necropsy of the freshly dead turtle was Hence the three beaks most probably corresponded conducted following standard procedures. The to two individuals. The beak ‘maturity’ stage, i.e. digestive tract (oesophagus, stomach and intestine) completely darkened wings and walls (Clarke 1986), contents were rinsed in fresh water through a 1-mm and the estimated sizes indicate that the mesh sieve. Then the organic material was fixed in prey squid were adults of H. bonnellii (cf. Voss et al. 70% alcohol solution and the inorganic fraction was 1998). air-dried. Each organic item was identified to the lowest possible taxonomic level. The cephalopod beaks were identified after Clarke Discussion (1986) and by comparison with a beak collection The present record adds a new item to the prey list held by one of us (GB). The body sizes Á mantle of Dermochelys coriacea. length (ML) and body weight (W) of the squid, from According to the literature (e.g. Bjorndal 1996; which the beaks came, were estimated from lower Davenport et al. 2009), the leatherback turtle rostral length (LRL) by the equations given by appears to prefer gelatinous, slow-moving animals Quetglas et al. (2010) correlating ML to LRL and living in the water column. This is further corrobo- W to ML. The correspondence between upper and rated by the present results. However, the known lower beaks was checked by the ratio between upper prey items of leatherbacks, i.d. gelatinous plankters, and lower rostral lengths: URL/LRL1.14 (Bello have a very low energy density (ED) (e.g. jellyfish 1994); this ratio was also used to estimate the ED2.14Á3.73 kJ g1 dry mass (Doyle et al. corresponding LRL of an unpaired upper beak. 2007)), one order of magnitude smaller than Histioteuthis spp. (ED21.52 kJ g1 dry mass Results (Clarke et al. 1985)). Hence even a small component of squid in the leatherback diet may contribute a The items retrieved from the leatherback turtle large portion of its energy intake. digestive tract included remains of tunicates (asci- To understand the predatory relationship between dians, Salpidae and Pyrosomidae), sponges and the D. coriacea and H. bonnellii, one has to consider that seagrass Posidonia oceanica together with inorganic histioteuthid squids are neutrally buoyant, weakly debris such as plastics, woods, fishing lines and muscled that rely on ammoniacal fluids pieces of fishing nets. for buoyancy (Clarke et al. 1979). They are com- The leatherback turtle stomach contained three Downloaded By: [Bello, Giambattista] At: 08:32 26 March 2011 paratively slow-moving, and are capable of hovering loose cephalopod beaks, two upper and one lower, in the water column, forming a ‘squid ball’ (M. with no flesh remains (Figure 1). The beaks had lost Vecchione, pers. comm.); that is, to some extent, their mode of living looks like that of jellyfish. Moreover, H. bonnellii, like all other members of the family Histioteuthidae, produces biolumines- cence thanks to the many luminous organs distrib- uted all over its body, which may attract the

Table 1. Rostral lengths of Histioteuthis bonnellii beaks found in the leatherback turtle stomach contents and estimated squid sizes. RL, rostral length; ELRL, estimated lower rostral length; EML, estimated mantle length; EW, estimated body weight.

RL ELRL EML EW Beaks (mm) (mm) (cm) (g)

Figure 1. Beaks of Histioteuthis bonnellii from the stomach con- Lower 9.3 Á 17.5 1962 tents of Dermochelys coriacea. From left to right: lower beak, upper Upper no. 1 10.5 Á beak probably paired with the lower beak, unpaired upper beak. Upper no. 2 12.0 10.5 19.8 2636 Ruler numbered subdivisions in cm. 316 G. Bello et al.

leatherback turtles at night, or at depth, as was Bjorndal KA. 1996. Foraging ecology and nutrition of sea turtles. already supposed in the case of Pyrosoma spp. In: Lutz PL, Musick JA, editors. The Biology of Sea Turtles. Boca Raton, FL: CRC Press, p 199 231. (Davenport & Balazs 1991). Á Casale P, Nicolosi P, Freggi D, Turchetto M, Argano R. 2003. Histioteuthis bonnellii, which occurs throughout the Leatherback turtles (Dermochelys coriacea) in Italy and in the Atlanto-Mediterranean region (Quetglas et al. Mediterranean basin. Herpetological Journal 13:135Á39. 2010), is a typical oceanic squid inhabiting a broad Clarke A, Clarke MR, Holmes LJ, Waters TD. 1985. Calorific vertical range from the surface to probably 2000 m values and elemental analysis of eleven species of oceanic squid depth and accomplishing diel vertical migrations (: Cephalopoda). Journal of the Marine Biological Association of the United Kingdom 65:983 86. (Voss et al. 1998). The leatherback turtle is capable Á Clarke MR (ed.). 1986. A Handbook for the Identification of of deep dives, down to at least 1280 m, which have Cephalopod Beaks. Oxford: Clarendon Press. xiii273 pages. been recorded throughout its broad range (Houghton Clarke MR, Denton EJ, Gilpin-Brown JB. 1979. On the use of et al. 2008). Hence the cephalopods found in the ammonium for buoyancy in squids. Journal of the Marine leatherback turtle stomach may have been preyed Biological Association of the United Kingdom 59:259Á76. upon anywhere in the water column. Davenport J. 1998. Sustaining endothermy on a diet of cold jelly: Energetics of the leatherback turtles Dermochelys coriacea. Despite its elusiveness with respect to man-made British Herpetological Society Bulletin 62:4Á8. collecting devices, H. bonnellii is very abundant in Davenport J, Balazs GH. 1991. ‘Fiery bodies’ Á are pyrosomas the Mediterranean Sea, where it plays an important important items in the diet of Leatherback turtles? British role in pelagic food webs (Bello 2000). Its remains Herpetological Society Bulletin 37:33Á38. have been recorded in the stomach contents of a Davenport J, Fraher J, Fitzgerald E, McLaughlin P, Doyle T, wide variety of Mediterranean predators as small as Harman L, Cuffe T. 2009. Fat head: An analysis of head and neck insulation in the leatherback turtle (Dermochelys coriacea). the giant red shrimp Aristaeomorpha foliacea (Bello & Journal of Experimental Biology 212:2753Á59. Pipitone 2002) and as large as the Doyle TK, Houghton JDR, McDevitt R, Davenport J, Hays GC. Physaeter macrocephalus (Roberts 2003) (see also 2007. The energy density of jellyfish: Estimates from bomb- Voss et al. 1998, for a worldwide review). calorimetry and proximate-composition. Journal of Experi- To conclude, the present finding supports the mental Marine Biology and Ecology 343:239Á52. hypothesis put forth by Davenport & Balazs (1991) Houghton JDR, Doyle TK, Wilson MW, Davenport J, Hays GC. 2006. Jellyfish aggregations and leatherback turtle foraging that D. coriacea is an opportunist predator that feeds patterns in a temperate coastal environment. Ecology 87: upon fairly large, slow moving gelatinous Á or indeed 1967Á72. ammoniacal in the present case Á prey. Houghton JDR, Doyle TK, Davenport J, Wilson RP, Hays GC. 2008. The role of infrequent and extraordinary deep dives in Acknowledgements leatherback turtles (Dermochelys coriacea). Journal of Experi- mental Biology 211:2566Á75. We are grateful to Prof. John Davenport for critically Murphy S, Murphy T. 2005. Leatherback turtle/Dermochelys reading the manuscript and Prof. Graeme Hays for coriacea. Available online at: www.dnr.sc.gov/cwcs/pdf/Leather some suggestions. backtutle.pdf Quetglas A, de Mesa A, Ordines F, Grau A. 2010. Life history of the deep-sea cephalopod family Histioteuthidae in the western References Mediterranean. Deep-Sea Research Part 1 57:999Á1008. Roberts SM. 2003. Examination of the stomach contents from a Bello G. 1994. Histioteuthis bonnellii (Cephalopoda: Histioteuthi-

Downloaded By: [Bello, Giambattista] At: 08:32 26 March 2011 Mediterranean sperm whale found south of Crete, Greece. dae) in the Adriatic Sea: Evidence from predator stomach Journal of the Marine Biological Association of the United contents. Bollettino Malacologico 30:43Á48. Kingdom 83:667Á70. Bello G. 2000. How rare is Histioteuthis bonnellii (Cephalopoda: Voss NA, Nesis KN, Rodhouse PG. 1998. The cephalopod family Histioteuthidae) in the eastern Mediterranean Sea? Journal of Histioteuthidae (): Systematics, biology, and biogeo- Molluscan Studies 66:575Á77. Bello G, Pipitone C. 2002. Predation on cephalopods by the giant graphy. Smithsonian Contributions to Zoology 586:293Á372. red shrimp Aristaeomorpha foliacea. Journal of the Marine Biological Association of the United Kingdom 82:213Á18. Editorial responsibility: Haakon Hop

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