Skip to main content
Log in

Stable isotopes (δ18O and δ13C) in Spirula spirula shells from three major oceans indicate developmental changes paralleling depth distributions

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Stable isotopes (δ18O and δ13C) were measured in successive chambers of the aragonitic shells of the small deep-sea squid Spirula spirula (Linnaeus 1758) (class Cephalopoda, subclass Coleoidea, order Sepioidea, family Spirulidae) to determine whether their depth distributions change with age. The spiral shells, ranging in diameter from 18 to 23 mm (30–38 chambers), were collected between 2000 and 2006 from beaches in six widely separated locations in three oceans, the Atlantic (Tobago and Canary Islands), Indian (Madagascar, Maldives, and Perth, Australia), and Pacific Oceans (Ulladulla, Australia). The patterns for both isotopes were highly correlated in specimens from all six sites. The δ18O data suggest that after hatching at depths >1,000 m at temperatures of 4–6°C, the squid migrate into shallower, warmer waters at 12–14°C at depths of 400–600 m. Subsequently, the increasing δ18O values suggest a migration back into somewhat cooler, deeper habitats. The δ13C values also revealed three ontogenetic stages in all six specimens, including a major shift from positive to negative values, which probably corresponds to sexual maturation, the initiation of reproduction, and concomitant changes in diet. In three of the six specimens (from Tobago, Canary Islands, and Maldives) a fourth embryonic stage (not detected in the oxygen data) was accompanied by markedly less positive δ13C values in the first few chambers. These data, combined with the scanty life history information from previous studies of S. spirula, can be used to compare the habitat requirements of related extant and fossil cephalopod genera.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Appellöff A (1893) Die Schalen von Sepia, Spirula und Nautilus. Studium über den Bau und das Wachstum. K svenska Vetensk Akad. Hand Stockholm 25:1–106

    Google Scholar 

  • Auclair A-C, Lecuyer C, Bucher H, Sheppard SMF (2004) Carbon and oxygen isotope composition of Nautilus macromphalus: a record of thermocline waters off New Caledonia. Chem Geol 207:91–100

    Article  CAS  Google Scholar 

  • Bandel K (1982) Morphologie und Bildung der frühontogenetischen Gehäuse bei conchiferen Mollusken. Facies 7:1–198

    Article  Google Scholar 

  • Böggild OB (1930) The shell structure of the molluscs. Kgl danske Vidensk Selsk Skr nat og mat 9:233–326

    Google Scholar 

  • Bruun AF (1943) The biology of Spirula spirula (L.). Dana Report 24:1–48

    Google Scholar 

  • 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 B 272:1601–1607

    Article  PubMed  Google Scholar 

  • Chun C (1910) Spirula australis Lam. Ber Math Phys Kl K Sächs Ges Wiss Leipzig 62:171–188

    Google Scholar 

  • Chun C (1915) Die Cephalopoda. 2 Teil: Myopsida, Octopoda. Wiss Ergeb Dt Tiefsee Exp 18:414–476

    Google Scholar 

  • Clarke MR (1966) A review of the systematics and ecology of oceanic squids. Adv Mar Biol 4:91–300

    Google Scholar 

  • Clarke MR (1969) Cephalopoda collected on the SOND cruise. J Mar Biol Ass UK 49:961–976

    Article  Google Scholar 

  • Clarke MR (1970) Growth and development of Spirula spirula. J Mar Biol Ass UK 50:53–64

    Google Scholar 

  • Clarke MR (1986) A handbook for the identification of cephalopod beaks. Clarendon Press, Oxford

    Google Scholar 

  • Cochran JK, Rye DM, Landman NH (1981) Growth rate and habitat of Nautilus pompilius inferred from radioactive and stable isotope studies. Paleobiology 7:469–480

    Google Scholar 

  • Dauphin Y (1976) Microstructure des coquilles de céphalopodes. I. Spirula spirula L. (Dibranchiata, Decapoda). Bull Mus Natn Hist Nat 382:197–238

    Google Scholar 

  • Dauphin Y (2001a) Caractéristiques de la phase organique soluble des tests aragonitiques des trios genres de cephalopods actuels. N Jb Geol Paläont Mh 2001(2):103–123

  • Dauphin Y (2001b) Nanostructures de la nacre des tests de cephalopods actuels. Paläont Z 75:113–122

    Google Scholar 

  • Doguzhaeva LA (1996) Two Early Cretaceous spirulid coleoids of the North-Western Caucasus: their shell ultrastructure and evolutionary implications. Palaeontology 39:681–709

    Google Scholar 

  • Doguzhaeva LA (2000) The evolutionary morphology of siphonal tube, in Spirulida (Cephalopoda, Coleoidea). Rev Paléobiol Vol Spéc 8:83–94

    Google Scholar 

  • Donovan DT (1977) Evolution of the dibranchiate cephalopoda. In: Nixon M, Messenger JB (eds) The biology of cephalopods. Symp Zool Soc London, vol 38, Academic Press, London, pp 15–48

  • Eichler R, Ristedt H (1966) Untersuchungen zur Frühontogenie von Nautilus pompilius (Linné). Paläont Z 40:173–191

    Google Scholar 

  • Goodwin DH, Schöne BR, Dettman DL (2003) Resolution and fidelity of oxygen isotopes as palaeotemperature proxies in bivalve mollusc shell: models and observations. Palaios 18:110–125

    Article  Google Scholar 

  • Goud J (1985) Spirula spirula, een inktvis uit de diepzee. Vita marina, Zeebiol doku, pp 35–42

    Google Scholar 

  • Grossman EL, Ku T (1986) Oxygen and carbon isotope fractionation in biogenic aragonite: temperature effects. Chem Geol 59:59–74

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Joubin L (1995) Cephalopods from the scientific expeditions of Prince Albert I of Monaco. Vol. I, parts 1-III; Vol. 2 parts III-IV. Smithsonian Institution Libraries and Nati Sci Found, Washington, DC

    Google Scholar 

  • Kerr JG (1931) Notes upon the Dana specimens of Spirula and upon certain problems of cephalopod morphology. Dana Report 8:1–34

    Google Scholar 

  • Keupp H (2000) Ammoniten: Paläobiologische Erfolgsspiralen. Thorbecke Verlag, Stuttgart

    Google Scholar 

  • Landman NH, Rye DM, Shelton KL (1983) Early ontogeny of Eutrephoceras compared to Recent Nautilus and Mesozoic ammonites: evidence from shell morphology and light stable isotopes. Paleobiology 9:269–279

    Google Scholar 

  • Landman NH, Cochran JK, Rye DM, Tanabe K, Arnold JM (1994) Early life history of Nautilus: evidence from isotopic analysis of aquarium reared specimens. Paleobiology 20:40–51

    Google Scholar 

  • LEVITUS 94 (1994) World Ocean Atlas. http://ingrid.ldeo.columbia.edu/SOURCES/.LEVITUS94/

  • Lindgren AR, Giribet G, Nishiguchi MK (2004) A combined approach to the phylogeny of Cephalopoda (Mollusca). Cladistics 20:454–486

    Article  Google Scholar 

  • Linnaeus C (1758) Systema Naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Edito decimal, reformata. Holmiae: Laurentii Salvii vol 1, 824, p 710

  • Lu CC (1998) Order Sepioidea. Chap. 13. In: Beesley PL, Ross GJB, Wells A (eds) Mollusca. The southern synthesis. Fauna of Australia. Part A, vol. 5. CSIRO Publishing, Melbourne, pp 504–514

    Google Scholar 

  • McConnaughey TA, Burdett J, Whelan JF, Paull CK (1997) Carbon isotopes in biological carbonates: respiration and photosynthesis. Geochim Cosmochim Acta 61:611–622

    Article  CAS  Google Scholar 

  • Mutvei H (1964) On the shells of Nautilus and Spirula with notes on the shell secretion in non-cephalopod molluscs. Ark Zool 16:221–278

    Google Scholar 

  • Mutvei H, Donovan DT (2006) Siphuncular structure in some fossil coleoids and recent Spirula. Palaeontology 49:685–691

    Article  Google Scholar 

  • Naef A (1922) Die Fossilen Tintenfische. Gustav Fischer, Jena

    Google Scholar 

  • Nixon M, Dilly PN (1977) Sucker surfaces and prey capture. In: Nixon M, Messenger JB (eds) The biology of cephalopods. Symp Zool Soc London, vol 38. Academic Press, London, pp 447–511

  • Norman M (2007) Australian biological resources study. Species Bank. http://www.environment.gov.au/cgi-bin/species-bank/sbank-treatment.pl?id=77088

  • Pelseneer P (1895) Observations on Spirula. Bull Sci Fr Belg 26:1–55

    Google Scholar 

  • Rexfort A, Mutterlose J (2006) Stable isotope records from Sepia officinalis - a key to understand the ecology of belemnites? Earth Planet Sci Lett 247:212–221

    Article  CAS  Google Scholar 

  • Rosa R, Costa PR, Bandarra N, Nunes ML (2005) Changes in tissue. Biochemical composition and energy reserves associated with sexual maturation in the ommastrephid squids Illex coindetii and Todaropsis eblanae. Biol Bull 208:100–113

    Article  PubMed  CAS  Google Scholar 

  • Schmidt J (1922) Live specimens of Spirula. Nature 110, No. 2271, pp 788–790

  • Taylor BE, Ward PD (1983) Isotopic studies of Nautilus macromphalus Sowerby (New Caledonia) and Nautilus pompilius L. (Fiji). Palaeogeogr Palaeoclimatol Palaeoecol 41:1–16

    Article  Google Scholar 

  • Turek R (1933) Chemisch-analytische Untersuchungen an Molluskenschalen. Arch Naturgesch Leipzig Z Syst Zool 2:301–202

    Google Scholar 

  • Warnke K, Keupp H (2005) Spirula—a window to the embryonic development of ammonoids? Morphological and molecular indications for a palaeontological hypothesis. Facies 51:60–65

    Article  Google Scholar 

  • Warnke K, Plötner J, Santana JI, Rueda MJ, Llinás O (2003) Reflections on the phylogenetic position of Spirula (Cephalopoda): preliminary evidence from the 18S ribosomal RNA gene. Berliner Paläobiol Abh 03:253–260

    Google Scholar 

  • Young JZ (1977) Brain, behaviour and evolution of cephalopods. Symp Zool Soc Lond 38:377–434

    Google Scholar 

  • Young RE, Vecchione M, Donovan D (1998) The evolution of coleoid cephalopods and their present biodiversity and ecology. S Afr J Mar Sci 20:393–420

    Google Scholar 

Download references

Acknowledgments

We are grateful to Ortwin Schultz, Peter Sziemer, Franz Topka (all Natural History Museum Vienna) and Jens Hartmann (University of Hamburg) for providing Spirula spirula specimens. We thank Vera Hammer (Natural History Vienna) for geochemical analysis of the shell material. Two anonymous reviewers helped to improve the quality of the paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alexander Lukeneder.

Additional information

Communicated by J.P. Grassle.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM1 (DOC 19 kb)

ESM2 (TIF 2460 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lukeneder, A., Harzhauser, M., Müllegger, S. et al. Stable isotopes (δ18O and δ13C) in Spirula spirula shells from three major oceans indicate developmental changes paralleling depth distributions. Mar Biol 154, 175–182 (2008). https://doi.org/10.1007/s00227-008-0911-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-008-0911-5

Keywords

Navigation