Abstract
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.
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References
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 50:1–10
Arneson LS, MacAvoy SE (2005) Carbon, nitrogen, and sulphur diet-tissue discrimination in mouse tissues. Can J Zool 83:989–995. doi:https://doi.org/10.1139/z05-083
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 39–51
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:https://doi.org/10.1016/j.jembe.2006.09.008
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:https://doi.org/10.1098/rspb.2005.3115
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:https://doi.org/10.3354/meps329281
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 113–136
Clarke MR (1965) “Growth rings” in the beaks of the squid Moroteuthis ingens (Oegopsida: Onychoteuthidae). Malacologia 3:287–307
Clarke MR (1996) Cephalopods as prey III. Cetaceans. Philos Trans R Soc Lond B Biol Sci 351:1053–1065. doi:https://doi.org/10.1098/rstb.1996.0093
DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506. doi:https://doi.org/10.1016/0016-7037(78)90199-0
DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351. doi:https://doi.org/10.1016/0016-7037(81)90244-1
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:https://doi.org/10.1139/Z06-049
Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation. Condor 94:189–197. doi:https://doi.org/10.2307/1368808
Hobson KA, Piatt JF, Pitocchelli J (1994) Using stable isotopes to determine seabird trophic relationships. J Anim Ecol 63:786–798. doi:https://doi.org/10.2307/5256
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:https://doi.org/10.1007/BF01314808
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:https://doi.org/10.1016/0305-0491(81)90071-7
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:https://doi.org/10.1007/s11160-007-9055-9
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:https://doi.org/10.1007/s00227-006-0374-5
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:https://doi.org/10.3354/meps219299
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:https://doi.org/10.1675/1524-4695(2008)31[169:EOLEOC]2.0.CO;2
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, Canada
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:https://doi.org/10.1016/S0022-0981(02)00220-4
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:https://doi.org/10.1034/j.1600-0706.2003.12098.x
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:https://doi.org/10.1007/s10641-006-9020-9
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:https://doi.org/10.1016/0016-7037(84)90204-7
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:https://doi.org/10.1016/j.actbio.2006.09.004
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:https://doi.org/10.1126/science.1154117
Park YH, Gambéroni L, Charriaud E (1993) Frontal structure, water masses, and circulation in the Crozet Basin. J Geophys Res 98:12361–12385. doi:https://doi.org/10.1029/93JC00938
Parry M (2008) Trophic variation with length in two ommastrephid squids, Ommastrephes bartramii and Sthenoteuthis oualaniensis. Mar Biol (Berl) 153:249–256. doi:https://doi.org/10.1007/s00227-007-0800-3
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:https://doi.org/10.1139/cjfas-53-12-2837
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:https://doi.org/10.1046/j.1365-2435.1999.00301.x
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:https://doi.org/10.1007/s00442-006-0630-x
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:https://doi.org/10.2307/1937843
Raya CP, Hernandez-Gonzalez CL (1998) Growth lines within the beak microstructure of the octopus Octopus vulgaris Cuvier, 1797. S Afr J Mar Sci 20:135–142
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 207–215
Rodhouse PG, Nigmatullin CM (1996) Role as consumers. Philos Trans R Soc Lond B Biol Sci 351:1003–1022. doi:https://doi.org/10.1098/rstb.1996.0090
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:https://doi.org/10.3354/meps277275
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:https://doi.org/10.1017/S0025315406013324
Schimmelmann A, DeNiro MJ (1986) Stable isotopic studies on chitin. II. The 13C/12C and 15N/14N ratios in arthropod chitin. Contrib Mar Sci 29:113–130
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:https://doi.org/10.1016/j.jembe.2005.12.008
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:https://doi.org/10.1017/S0025315400002502
Vanderklift A, Ponsard S (2003) Sources of variation in consumer-diet δ15N enrichments: a meta-analysis. Oecologia 136:169–182. doi:https://doi.org/10.1007/s00442-003-1270-z
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:https://doi.org/10.1016/j.cbpa.2007.06.419
Webb S, Hedges REM, Simpson SJ (1998) Diet quality influences the δ13C and δ15N of locusts and their biochemical components. J Exp Biol 201:2903–2911
Acknowledgments
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.
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Communicated by J.P. Grassle.
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Cherel, Y., Fontaine, C., Jackson, G.D. et al. Tissue, ontogenic and sex-related differences in δ13C and δ15N values of the oceanic squid Todarodes filippovae (Cephalopoda: Ommastrephidae). Mar Biol 156, 699–708 (2009). https://doi.org/10.1007/s00227-008-1121-x
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DOI: https://doi.org/10.1007/s00227-008-1121-x