, Volume 51, Issue 1–4, pp 60–65 | Cite as

Spirula—a window to the embryonic development of ammonoids? Morphological and molecular indications for a palaeontological hypothesis

  • Kerstin Warnke
  • Helmut Keupp
Original Article


Nautilus is not suitable as a model organism to infer biological functions, embryonic development, or mode of life in ammonoids. A brief review of the available morphological data is given and molecular data are added to discuss the usefulness of Spirula as a biological proxy for ammonoids. Indeed, there are many morphological hints indicating that Spirula could be a useful model organism for approaching the embryonic development of ammonoids. The molecular data seem to support this hypothesis. However, a universal model character of Spirula cannot be detected as, e.g., the mode of feeding probably differs between Spirula and ammonoids.


Coleoid Ammonoid Spirula Living model organism Phylogeny DNA analysis 



We are indebted to Dr. S. V. Boletzky for discussion and correction of the manuscript. Helpful critical comments of Dr. A. Nützel improved the manuscript. This research was supported by grants WA 1454/1-1 and WA 1454/1-2 of the Deutsche Forschungsgemeinschaft to Kerstin Warnke and by fishing operations of the Canarian Institute of Marine Sciences (Instituto Canario de Ciencias Marinas)


  1. Appellöf A (1893) Die Schalen von Sepia, Spirula und Nautilus. Studium über den Bau und das Wachstum. K Svenska Vetensk Akad Handl Stockholm 25:1–106Google Scholar
  2. Arnold JM, O’Dor R (1990) In vitro fertilization and embryonic development of oceanic squid. J Cephalopod Biol 1:21–36Google Scholar
  3. Bandel K (1982) Morphologie und Bildung der frühontogenetischen Gehäuse bei conchiferen Mollusken. Facies 7:1–198Google Scholar
  4. Bandel K (1990) Cephalopod shell structure and general mechanisms of shell formation. In: Carter JG (ed) Skeletal Biomineralization: Patterns, Processes and Evolutionary Trends. 1, pp 97–115Google Scholar
  5. Bandel K, von Boletzky S (1979) A comparative study of the structure, development and morphological relationships of chambered cephalopod shells. Veliger 21:313–354Google Scholar
  6. Berthold T, Engeser T (1987) Phylogenetic analysis and systematization of the Cephalopoda (Mollusca). Verh Naturwiss Ver Hamb NF 29:187–220Google Scholar
  7. von Boletzky S (1989) Recent studies on spawning, embryonic development, and hatching in the Cephalopoda. Adv Mar Biol 25:85–115Google Scholar
  8. von Boletzky S (1998) Cephalopod eggs and egg masses. Oceanogr Mar Biol, Ann Rev 36:341–371Google Scholar
  9. von Boletzky S (1999) Brève mise au point sur la classification des céphalopodes actuels. Bull Soc Zool France 124:271–278Google Scholar
  10. von Boletzky S (2003) Biology of early life stages in cephalopod molluscs. Adv Mar Biol 44:144–203Google Scholar
  11. Bonnaud L, Boucher-Rodoni R, Monnerot M (1994) Phylogeny of decapod cephalopods based on partial 16s DNA nucleotide sequences. C R Hebd Séanc Acad Sci (III) 317:581–588Google Scholar
  12. Bonnaud L, Boucher-Rodoni R, Monnerot M (1996) Relationships of some coleoid cephalopods established by 3’end of the 16S rDNA and cytochrome oxidase III gene sequence comparison. Amer Malac Bull 12:87–90Google Scholar
  13. Bruun AF (1943) The biology of Spirula spirula (L.). Dana Rep 24:49Google Scholar
  14. Carlini DB, Graves JE (1999) Phylogenetic analysis of the cytochrome oxidase I sequences to determine higher level relationships within the coleoid cephalopods. Bull Mar Sci 64:57–76Google Scholar
  15. Carlini DB, Reece KS, Graves JE (2000) Actin gene family evolution and the phylogeny of coleoid cephalopods (Mollusca: Cephalopoda). Mol Biol Evol 17:1353–1370PubMedGoogle Scholar
  16. Chun C (1910) Spirula australis Lam. Ber Math-Phys Kl K Sächs Ges Wiss Leipzig 62:171–188Google Scholar
  17. Chun C (1915) Die Cephalopoden. 2. Teil: Myopsida, Octopoda. Wiss Ergeb Dt Tiefsee Exp 18:414–476Google Scholar
  18. Clarke MR (1966) A review of the systematics and ecology of oceanic squids. Adv Mar Biol 4:91–300Google Scholar
  19. Clarke MR (1970) Growth and development of Spirula spirula. J Mar Biol Ass UK 50:53–64Google Scholar
  20. Denton EJ, Gilpin-Brown JB (1973) Floating mechanisms in modern and fossil cephalopods. Adv Mar Biol 11:197–268Google Scholar
  21. Doguzhaeva LA (1999) Early shell ontogeny in bactritoids and allied taxa: comparative morphology, shell wall ultrastructure, and phylogenetic implications. In: Histon K (ed) V Intern Symp Cephalopods—Present and Past, Vienna, Abstracts. Abh Geol Bundesanst 46:32Google Scholar
  22. Doguzhaeva LA, Mapes RH, Mutvei H (1999) A Late Carboniferous spirulid coleoid from the southern mid-continent (USA): shell wall ultrastructure and evolutionary implication. In: Oloriz F, Rodriguez-Tovar FJ (eds) Advancing Research on Living and Fossil Cephalopods. Kluwer Acad/Plenum Publ, New York, pp 47–57Google Scholar
  23. Doguzhaeva LA, Mapes RH, Mutvei H (2002) Beaks and radulae of Early Carboniferous goniatites. Lethaia 30:305–313Google Scholar
  24. Donovan D (1977) Evolution of the dibranchiate Cephalopoda. Symp Zool Soc London, 38:15–48Google Scholar
  25. Doyle P, Donovan D, Nixon M (1994) Phylogeny and systematics of the Coleoida. Palaeontol Contr Univ Kansas 5:1–15Google Scholar
  26. Dreyer H, Steiner G, Harper EM (2003) Phylogeny of Anomalodesmata (Mollusca: Bivalvia) inferred from 18S rDNA sequences. Zool J Linn Soc 139:229–246CrossRefGoogle Scholar
  27. Engeser T (1990a) Phylogeny of the fossil coleoid Cephalopoda (Mollusca). Berliner Geowiss Abh 124:123–191Google Scholar
  28. Engeser T (1990b) Major events in cephalopod evolution. In: Taylor PD, Larwood GP (eds) Major Evolutionary Radiations. Clarendon Press, Oxford, pp 119–138Google Scholar
  29. Engeser T (1996) The Position of the Ammonoidea within the Cephalopoda. In: Landman NH, Tanabe K, Davis RA (eds) Ammonoid Paleobiology. Plenum Press, New York, pp 3–19Google Scholar
  30. Engeser T, Bandel K (1988) Phylogenetic classification of coleoid cephalopods. In: Wiedmann J, Kullmann J (eds) Cephalopods, Present and Past. Schweizerbart, Stuttgart, pp 105–115Google Scholar
  31. Engeser T, Keupp H (2002) Phylogeny of the aptychi-possessing Neoammonoidea (Aptychophora nov., Cephalopoda). Lethaia 34:79–96CrossRefGoogle Scholar
  32. Erben HK (1966) Über den Ursprung der Ammonoidea. Biol Rev 41:641–658PubMedGoogle Scholar
  33. Flower RH (1961) Major divisions of the Cephalopoda. J Paleontology 35:569–574Google Scholar
  34. Gray JE (1845) On the animal of Spirula. Ann Nat Hist 15:57–261Google Scholar
  35. Harasewych MG, Adamkewicz SL, Blake JA, Saudek D, Spriggs T, Bult CJ (1997) Phylogeny and relationships of pleurotomariid gastropods (Mollusca: Gastropoda): an assessment based on partial 18S rDNA and cytochrome c oxidase I sequences. Mol Mar Biol Biotechnol 6:1–20PubMedGoogle Scholar
  36. Hewitt RA (1996) Architecture and strength of the ammonoid shell. In: Landman NH, Tanabe K, Davis RA (eds) Ammonoid Paleobiology. Plenum Press, New York, pp 297–339Google Scholar
  37. House MR (1981) On the origin, classification and evolution of the early Ammonoidea. In: House MR, Senoir JR (eds) The Ammonoidea. Syst Assoc, London, pp 3–36Google Scholar
  38. House MR (1988) Major features of cephalopod evolution. In: Wiedmann J, Kullmann J (eds) Cephalopods, Present and Past. Schweizerbart, Stuttgart, pp 1–16Google Scholar
  39. House MR (1996) Juvenile goniatite survival strategies following Devonian extinction events. In: Hart MB (ed) Biotic Recovery from Mass Extinction Events. Geol Soc Spec Publ 102:163–185Google Scholar
  40. Jacobs DK, Landman NH (1993) Nautilus - a poor model for the function and behavior of ammonoids? Lethaia 26:101–111Google Scholar
  41. Jacobs DK, Landman NH (1994) Nautilus - model or muddle? Lethaia 27:95–96Google Scholar
  42. Keupp H (2000) Ammoniten. Thorbecke, Stuttgart, 165 ppGoogle Scholar
  43. Landman NH (1988) Early Ontogeny of Mesozoic Ammonites and Nautilids. In: Wiedmann J, Kullmann J (eds) Cephalopods, Present and Past. Schweizerbart, Stuttgart, pp 215–228Google Scholar
  44. Landman NH, Tanabe K, Shigeta Y (1996) Ammonoid embryonic development. In: Landman NH, Tanabe K, Davis RA (eds) Ammonoid Paleobiology. Plenum Press, New York, pp 343–405Google Scholar
  45. Lehmann U (1966) Dimorphismus bei Ammoniten der Ahrensburger Lias-Geschiebe. Paläont Z 40:26–55Google Scholar
  46. Lehmann U (1967) Ammoniten mit Kieferapparat und Radula aus Lias-Geschieben. Paläont Z 41:38–45Google Scholar
  47. Lu CC, Guerra A, Palumbo F, Summers WC (1992) Order Spioidea Naef, 1916. In: Sweeney MJ, Roper CFE, Mangold KM, Clarke MR, von Boletzky S (eds) “Larval” and juvenile cephalopods: A manual for their identification. Smithson Contr Zool 513:21–36Google Scholar
  48. Martin AW, Catala-Stucki I, Ward PD (1978) The growth rate and reproductive behaviour of Nautilus macromphalus. N Jb Geol Paläont Abh 156:207–225Google Scholar
  49. Mikami S, Okutani T (1977) Preliminary observations on maneuvering, feeding, copulating and spawning behaviours of Nautilus macromphalus in captivity. Venus 36:29–41Google Scholar
  50. Mutvei H (1964) On the shells of Nautilus and Spirula with notes on the shell secretion in cephalopod molluscs. Ark Zool 16:223–278Google Scholar
  51. Mutvei H (1975) The mode of life in ammonoids. Paläont Z 49:196–206Google Scholar
  52. Mutvei H, Reyment RA (1973) Buoyancy control and siphuncle function in ammonoids. Palaeontology 16:623–636Google Scholar
  53. Naef A (1921–1923) Die Cephalopoden (Systematik). Fauna Flora Golf Napoli 35(I-1):1–863[English translation, Jerusalem, Israel program for scientific translations, available from Smithsonian Institution Libraries, Washington, DC, 20560, USA]Google Scholar
  54. Naef A (1922) Die fossilen Tintenfische. Fischer, Jena, 322 pp [English translation: Berl. Paläobiol. Abh.]Google Scholar
  55. Nesis KN (1987) Cephalopods of the world. Squids, cuttlefishes, octopuses and allies. TFH Publ, Neptune City, New Jersey, 351 ppGoogle Scholar
  56. Nixon M (1996) Morphology of the jaws and radula in ammonoids. In: Landman NH, Tanabe K, Davis RA (eds) Ammonoid Paleobiology. Plenum Press, New York, pp 23–42Google Scholar
  57. Nixon M, Young JZ (2003) The brains and lives of cephalopods. Oxford Univ Press, New York, 392 ppGoogle Scholar
  58. Norman M (2000) Cephalopods, a world guide. ConchBooks, Hackenheim, 318 ppGoogle Scholar
  59. Owen R (1832) Memoir on the pearly Nautilus (Nautilus Pompilius, Linn.) with illustrations of its external form and internal structure. Counc R Collage Surgeons, LondonGoogle Scholar
  60. Reyment RA (1980) Floating orientation of cephalopod shell models. Paleontology 23:931–936Google Scholar
  61. Schindewolf OH (1933) Vergleichende Morphologie und Phylogenie der Anfangskammern tetrabranchiater Cephalopoden, Vol. 148. Abh Preuss Geol Landesanst, NF, pp 1–115Google Scholar
  62. Saunders WB, Ward D (1994) Nautilus is not a model for the function and behaviour of ammonoids. Lethaia 27:47–48Google Scholar
  63. Tanabe K, Fakuda Y, Obata I (1980) Ontogenetic development and functional morphology in the early growth-stages of three Cretaceous ammonites. Bull Natn Sci Mus Ser C (Geol) 6:9–26Google Scholar
  64. Tanabe K, Landman NH, Mapes RH, Faulkner CJ (1993) Analysis of a Carboniferous embryonic ammonoid assemblage from Kansas, U.S.A.-Implications for ammonoid embryology. Lethaia 26:215–224Google Scholar
  65. Teichert C (1988) Main Features of Cephalopod Evolution. In: Wilbur KM, Trueman ER, Clarke MR (eds) The Mollusca, 12. Paleontology and Neontology of Cephalopods. Academic Press, New York, pp 11–79Google Scholar
  66. Ward PD, von Boletzky S (1984) Shell implosion depth and implosion morphologies in three species of Sepia (Cephalopoda) from the Mediterranean Sea. J Mar Biol Ass UK 64:955–966Google Scholar
  67. Warnke K, Plötner J, Santana JI, Rueda MJ, Llinas O (2003) Reflections on the phylogenetic position of Spirula (Cephalopoda): Preliminary evidence from the 18S ribosomal RNA gene. Berliner Paläobiol Abh 3:253–260Google Scholar
  68. Willey A (1902) Zoological results, part IV. Cambridge Univ Press, Cambridge, 750 ppGoogle Scholar
  69. Winnepenninckx B, Reid D, Backeljau T (1998) Performance of 18S rRNA in littorinid phylogeny (Gastropoda: Caenogastropoda). J Mol Evol 47:586–596PubMedGoogle Scholar
  70. Wollscheid E, Wägele H (1999) Initial results on the molecular phylogeny of the Nudibranchia (Gastropoda, Opisthobranchia) based on 18S rDNA data. Mol Phyl Evol 13:215–226CrossRefGoogle Scholar
  71. Young JZ (1977) Brain, behaviour and evolution of cephalopods. Symp Zool Soc London 38:377–434Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Freie Universität BerlinFR PaläontologieBerlinGermany

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