Marine Biology

, Volume 156, Issue 4, pp 699–708 | Cite as

Tissue, ontogenic and sex-related differences in δ13C and δ15N values of the oceanic squid Todarodes filippovae (Cephalopoda: Ommastrephidae)

  • Yves CherelEmail author
  • Camille Fontaine
  • George D. Jackson
  • Christine H. Jackson
  • Pierre Richard
Original Paper


Stable isotopes are increasingly used in the study of trophic interactions of many aquatic animals and most recently cephalopods. To evaluate the application of the method to squids, it is important to assess isotopic differences among and within consumer tissues that may confound the resolution of ecological relationships. Inter- and intra-tissue isotopic variation was examined in 55 individuals of the oceanic squid Todarodes filippovae that were collected at the beginning of April 2000 in the southwestern Indian Ocean (between 44°S, 76°E, and Saint Paul and Amsterdam islands, 38°S, 78°E). Delipidated soft tissues (mantle, arm, buccal mass, gill and reproductive organs) showed small δ13C and δ15N differences, which were probably tissue-specific. A lower carbon value was observed in the digestive gland as a consequence of incomplete lipid removal. Hard tissues, such as beaks and gladii, had lower 15N values than soft tissues, which can be explained by the presence of chitin, a 15N-depleted molecule. Females (n = 38) and males (n = 17) had identical δ13C values, but females showed higher δ15N values than males. The difference was size-related rather than sex-related, however, as females were generally larger than males. A comparison of similar-sized females and males produced identical nitrogen values. These data suggest dietary shifts from lower to higher trophic levels during growth, because δ15N values of large T. filippovae were much higher than that of small specimens. As expected, nitrogen values of lower beaks and gladii of large squids increased from the oldest to the most recently formed region, reflecting the progressive growth of chitinized tissues in parallel with dietary changes. Sequential sampling along the growth increments of squid beaks and gladii can likely be used to produce a chronological record of dietary information throughout an individual’s history.


Chitin Isotopic Signature Digestive Gland Stable Isotopic Signature Mantle Length 



The authors thank G. Duhamel, P. Provost, and the crew from La Curieuse for their help in collecting cephalopods at sea, and G. Guillou for stable isotope analysis. The present work was supported financially and logistically by the Institut Polaire Français Paul Emile Victor (IPEV, Programme No. 109, H. Weimerskirch), and the Terres Australes et Antarctiques Françaises. Stable isotope analysis was supported by a Hermon Slade grant awarded to G.D. Jackson.


  1. Adam W (1974) Notes sur les céphalopodes. XXVI. Une nouvelle espèce de Todarodes (Todarodes filippovae sp. nov.) de l’Océan Indien. Bull Inst R Sci Nat Belg 50:1–10Google Scholar
  2. Arneson LS, MacAvoy SE (2005) Carbon, nitrogen, and sulphur diet-tissue discrimination in mouse tissues. Can J Zool 83:989–995. doi: CrossRefGoogle Scholar
  3. Bizikov VA (1991) A new method of squid age determination using the gladius. In: Jereb P, Ragonese S, von Boletzky S (eds) Squid age determination using statoliths, vol 1. NTR-ITPP Special Publication, pp 39–51Google Scholar
  4. Bodin N, Le Loc’h F, Hily C (2007) Effect of lipid removal on carbon and nitrogen stable isotope ratios in crustacean tissues. J Exp Mar Biol Ecol 341:168–175. doi: CrossRefGoogle Scholar
  5. Cherel Y, Hobson KA (2005) Stable isotopes, beaks and predators: a new tool to study the trophic ecology of cephalopods, including giant and colossal squids. Proc R Soc Lond B Biol Sci 272:1601–1607. doi: CrossRefGoogle Scholar
  6. Cherel Y, Hobson KA (2007) Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Mar Ecol Prog Ser 329:281–287. doi: CrossRefGoogle Scholar
  7. Cherel Y, Klages N (1998) A review of the food of albatrosses. In: Robertson G, Gales R (eds) Albatross biology and conservation. Surrey Beatty and Sons, Chipping Norton, pp 113–136Google Scholar
  8. Clarke MR (1965) “Growth rings” in the beaks of the squid Moroteuthis ingens (Oegopsida: Onychoteuthidae). Malacologia 3:287–307Google Scholar
  9. Clarke MR (1996) Cephalopods as prey III. Cetaceans. Philos Trans R Soc Lond B Biol Sci 351:1053–1065. doi: CrossRefGoogle Scholar
  10. DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506. doi: CrossRefGoogle Scholar
  11. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351. doi: CrossRefGoogle Scholar
  12. Hobson KA, Cherel Y (2006) Isotopic reconstruction of marine food webs using cephalopod beaks: new insight from captively raised Sepia officinalis. Can J Zool 84:766–770. doi: CrossRefGoogle Scholar
  13. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation. Condor 94:189–197. doi: CrossRefGoogle Scholar
  14. Hobson KA, Piatt JF, Pitocchelli J (1994) Using stable isotopes to determine seabird trophic relationships. J Anim Ecol 63:786–798. doi: CrossRefGoogle Scholar
  15. Houlihan DF, McMillan DN, Agnisola C, Trara Genoino I, Foti L (1990) Protein synthesis and growth in Octopus vulgaris. Mar Biol (Berl) 106:251–259. doi: CrossRefGoogle Scholar
  16. Hunt S, Nixon M (1981) A comparative study of protein composition in the chitin-protein complexes of the beak, pen, sucker disc, radula and oesophageal cuticle of cephalopods. Comp Biochem Physiol B 68:535–546. doi: CrossRefGoogle Scholar
  17. Jackson GD, Bustamante P, Cherel Y, Fulton A, Grist EPM, Jackson CH, Nichols PD, Pethybridge H, Phillips K, Ward RD, Xavier JC (2007a) Applying new tools to cephalopod trophic dynamics and ecology: perspectives from the Southern Ocean Cephalopod Workshop, 2–3 February 2006. Rev Fish Biol Fish 17:79–99. doi: CrossRefGoogle Scholar
  18. Jackson GD, Wotherspoon S, Jackson CH (2007b) Temporal life history plasticity of the Southern Ocean squid Todarodes filippovae from waters off Tasmania, Australia. Mar Biol (Berl) 150:575–584. doi: CrossRefGoogle Scholar
  19. Kaehler S, Pakhomov EA (2001) Effects of storage and preservation on the δ13C and δ15N signatures of selected marine organisms. Mar Ecol Prog Ser 219:299–304. doi: CrossRefGoogle Scholar
  20. Kojadinovic J, Richard P, Le Corre M, Cosson RP, Bustamante P (2008) Effects of lipid extraction on δ13C and δ15N values in seabird muscle, liver and feathers. Waterbirds 31:169–178. doi:[169:EOLEOC]2.0.CO;2 CrossRefGoogle Scholar
  21. Lipinski MR (1979) Universal maturity scale of the commercially important squids. The results of maturity classification of the Illex illecebrosus populations for the years 1973–77. ICNAF Res Doc 79/2/38, Serial 5364, International Commission for the Northwest Atlantic Fisheries, Dartmouth, CanadaGoogle Scholar
  22. Lorrain A, Paulet YM, Chauvaud L, Savoye N, Donval A, Saout C (2002) Differential δ13C and δ15N signatures among scallop tissues: implications for ecology and physiology. J Exp Mar Biol Ecol 275:47–61. doi: CrossRefGoogle Scholar
  23. McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulphur. Oikos 102:378–390. doi: CrossRefGoogle Scholar
  24. Miller TW (2006) Tissue-specific response of δ15N in adult Pacific herring (Clupea pallasi) following an isotopic shift in diet. Environ Biol Fishes 76:177–189. doi: CrossRefGoogle Scholar
  25. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140. doi: CrossRefGoogle Scholar
  26. Miserez A, Li Y, Waite JH, Zok F (2007) Jumbo squid beak: inspiration for design of robust organic composites. Acta Biomater 3:139–149. doi: CrossRefGoogle Scholar
  27. Miserez A, Schneberk T, Sun C, Zok F, Waite JH (2008) The transition from stiff to compliant materials in squid beaks. Science 319:1816–1819. doi: CrossRefGoogle Scholar
  28. Park YH, Gambéroni L, Charriaud E (1993) Frontal structure, water masses, and circulation in the Crozet Basin. J Geophys Res 98:12361–12385. doi: CrossRefGoogle Scholar
  29. Parry M (2008) Trophic variation with length in two ommastrephid squids, Ommastrephes bartramii and Sthenoteuthis oualaniensis. Mar Biol (Berl) 153:249–256. doi: CrossRefGoogle Scholar
  30. Perez JAA, O’Dor R, Beck P, Dawe EG (1996) Evaluation of gladius dorsal surface structure for age and growth studies of the short-finned squid, Illex illecebrosus (Teuthoidea: Ommastrephidae). Can J Fish Aquat Sci 53:2837–2846. doi: Google Scholar
  31. Pinnegar JK, Polunin NVC (1999) Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Funct Ecol 13:225–231. doi: CrossRefGoogle Scholar
  32. Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montana CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189. doi: CrossRefGoogle Scholar
  33. Rau GH, Mearns AJ, Young DR, Olson RJ, Schafer HA, Kaplan IR (1983) Animal 13C/12C correlates with trophic level in pelagic food webs. Ecology 64:1314–1318. doi: CrossRefGoogle Scholar
  34. Raya CP, Hernandez-Gonzalez CL (1998) Growth lines within the beak microstructure of the octopus Octopus vulgaris Cuvier, 1797. S Afr J Mar Sci 20:135–142CrossRefGoogle Scholar
  35. Rodhouse PG (1998) Todarodes filippovae in the Southern Ocean: an appraisal for exploitation and management. In: Okutani T (ed) Large pelagic squids. Japan Marine Fishery Resources Research Center, Tokyo, pp 207–215Google Scholar
  36. Rodhouse PG, Nigmatullin CM (1996) Role as consumers. Philos Trans R Soc Lond B Biol Sci 351:1003–1022. doi: CrossRefGoogle Scholar
  37. Ruiz-Cooley RI, Gendron D, Aguinaga S, Mesnick S, Carriquiry JD (2004) Trophic relationships between sperm whales and jumbo squid using stable isotopes of C and N. Mar Ecol Prog Ser 277:275–283. doi: CrossRefGoogle Scholar
  38. Ruiz-Cooley RI, Markaida U, Gendron D, Aguinaga S (2006) Stable isotopes in jumbo squid (Dosidicus gigas) beaks to estimate its trophic position: comparison between stomach contents and stable isotopes. J Mar Biol Assoc U K 86:437–445. doi: CrossRefGoogle Scholar
  39. Schimmelmann A, DeNiro MJ (1986) Stable isotopic studies on chitin. II. The 13C/12C and 15N/14N ratios in arthropod chitin. Contrib Mar Sci 29:113–130Google Scholar
  40. Stowasser G, Pierce GJ, Moffat CF, Collins MA, Forsythe JW (2006) Experimental study on the effect of diet on fatty acid and stable isotope profiles of the squid Lolliguncula brevis. J Exp Mar Biol Ecol 333:97–114. doi: CrossRefGoogle Scholar
  41. Takai N, Onaka S, Ikeda Y, Yatsu A, Kidokoro H, Sakamoto W (2000) Geographical variations in carbon and nitrogen stable isotope ratios in squid. J Mar Biol Assoc U K 80:675–684. doi: CrossRefGoogle Scholar
  42. Vanderklift A, Ponsard S (2003) Sources of variation in consumer-diet δ15N enrichments: a meta-analysis. Oecologia 136:169–182. doi: CrossRefGoogle Scholar
  43. Vollaire Y, Banas D, Thomas M, Roche H (2007) Stable isotope variability in tissues of the Eurasian perch Perca fluviatilis. Comp Biochem Physiol A 148:504–509. doi: CrossRefGoogle Scholar
  44. Webb S, Hedges REM, Simpson SJ (1998) Diet quality influences the δ13C and δ15N of locusts and their biochemical components. J Exp Biol 201:2903–2911PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Yves Cherel
    • 1
    Email author
  • Camille Fontaine
    • 1
  • George D. Jackson
    • 2
  • Christine H. Jackson
    • 2
  • Pierre Richard
    • 3
  1. 1.Centre d’Etudes Biologiques de ChizéVilliers-en-BoisFrance
  2. 2.Institute of Antarctic and Southern Oceanic StudiesUniversity of TasmaniaHobartAustralia
  3. 3.Laboratoire Littoral, Environnement et Sociétés UMR 6250 du CNRS-Université de La RochelleLa RochelleFrance

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