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Comparison of embryonic and adult shells of Sepia officinalis (Cephalopoda, Mollusca)

Abstract

Development and evolution of the shell in cephalopods is difficult to establish as there is few species with a calcified shell that could be fossilized (stable in geological time). Internal cuttlebone of sepiids is so particular that homologies are difficult to find. The developmental sequence in embryos give some response elements by comparison with adult cuttlebone. The macro and microstructure of adult shell is well known but an approach at nanostructural level allows to determine structure and composition of the two main parts, the dorsal shield and chambered part. We evidence in the embryonic shell, mainly organic, a light calcification of the shell, which occurs directly as aragonite, as it is all along the formation of the shell and whatever the parts. In embryonic shell, the prismatic and/or lamellar layers, present in adult, are not differentiated and the dorsal shield grows progressively, from posterior to anterior. Despite microstructural differences, all layers of both chambered part and dorsal shield are composed of rounded nanogranules (between 50 and 100 nm), similar to what is found in other mollusc shells. Finally, the presence of pillars evidenced in embryo suggests either that their absence in extinct lineages of sepiids is the result of a diagenetic process or that they are a novelty in present sepiid species.

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References

  1. Adler HH, Kerr PF (1963) Infrared absorption frequency trends for anhydrous normal carbonates. Am Mineral 48:839–853

  2. Allcock AL, Lindgren A, Strugnell J (2015) The contribution of molecular data to our understanding of cephalopod evolution and systematics: a review. J Nat Hist 49:1373–1421

  3. Appellöf A (1893) Die Schalen von Sepia, Spirula und Nautilus Studien über den Bau und das Wachstum. K Svenska Akad Handl Stockholm 25(7):1–106

  4. Bandel K (1990) Cephalopod shell structure and general mechanisms of shell formation. In: Carter JG (ed) Skeletal biomineralization: patterns processes and evolutionary trends, vol 1. Van Nostrand Reinolds, New York, pp 97–115

  5. Bandel K, von Boletzky S (1979) A comparative study of the structure, development and morphological relationships of chambered cephalopod shells. Veliger 21(3):313–354

  6. Barskov IS (1973) Microstructure of the skeletal layers of Sepia and Spirula compared with the shell layers of other molluscs. Paleont J 3:285–294

  7. Bettencourt V, Guerra A (2001) Age studies on daily growth increments in statoliths and growth lamellae in cuttlebone of cultured Sepia officinalis. Mar Biol 139:327–334

  8. Boggild OB (1930) The shell structure of the molluscs. D Kgl Danske Vidensk Selsk Skr, naturvidensk og mathem 9(2):231–326

  9. Butler-Struben HM, Brophy SM, Johnson MA, Crook RJ (2018) In vivo recording of neural and behavioral correlates of anesthesia induction, reversal, and euthanasia in cephalopod molluscs. Front Physiol 9:109. https://doi.org/10.3389/fphys.2018.00109

  10. Cadež V, Škapin SD, Leonardi A, Križaj I, Kazazic S, Salopek-Sondi B, Sondi I (2017) Formation and morphogenesis of a cuttlebone’s aragonite biomineral structures for the common cuttlefish (Sepia officinalis) on the nanoscale: revisited. J Colloid Interface Sci 508:95–104

  11. Checa AG, Cartwright JHE, Sanchez-Almazo I, Andrade JP, Ruiz-Raya F (2015) The cuttlefish Sepia officinalis (Sepiidae, Cephalopoda) constructs cuttlebone from a liquid-crystal precursor. Sci Rep 5:11513. https://doi.org/10.1038/srep11513

  12. Cuif JP (2016) Calcification in the Cnidaria through time: an overview of their skeletal patterns from individual to evolutionary viewpoints. In: Goffredo S, Dubinsky Z (eds) The Cnidaria, past, present and future. Springer, Berlin, pp 163–179

  13. Cuif JP, Dauphin Y (2005) The two-step mode of growth in the scleractinian coral skeletons from the micrometre to the overall scale. J Struct Biol 150:319–331

  14. Cuif J, Dauphin Y, Denis A, Gaspard D, Keller JP (1983) Etude des caractéristiques de la phase minérale dans les structures prismatiques du test de quelques Mollusques. Bull Mus Natl Hist Nat 3:679–717

  15. Cuif JP, Bendounan A, Dauphin Y, Nouet J, Sirotti F (2013) Synchrotron-based photoelectron spectroscopy provides evidence for a molecular bond between calcium and mineralizing organic phases in invertebrate calcareous skeletons. Anal Bioanal Chem 405(27):8739–8748

  16. Dauphin Y (1976) Microstructure des coquilles de Céphalopodes: I. Spirula spirula L. (Dibranchiata, Decapoda). Bull Mus natn hist nat, Paris, 3è sér., 382. Sci Terre 54:197–238

  17. Dauphin Y (1979) Organisation ultrastructurale de l’os de seiche (Cephalopoda-Dibranchiata). C R Acad Sci Paris D 288:619–622

  18. Dauphin Y (1981) Microstructures des coquilles de Céphalopodes. II- La seiche (Dibranchiata, Decapoda). Palaeontogr A176:35–51

  19. Dauphin Y (1984) Microstructures des coquilles de Céphalopodes IV-Le "rostre" de Belosepia (Dibranchiata). Palaeontogr Z 58(1/2):99–117

  20. Dauphin Y (1985) Microstructural studies on cephalopod shells V-The apical part of Beloptera (Dibranchiata, Tertiary). N Jb Geol Palaeont Abh 170(3):323–341

  21. Dauphin Y (1986) Microstructure des coquilles de Céphalopodes: la partie apicale de Belopterina (Coleoidea). Bull Mus natn Hist nat 1:53–75

  22. Dauphin Y, Keller JP (1982) Mise en évidence d'un type microstructural coquillier spécifique des Céphalopodes dibranchiaux. C R Acad Sc 294:409–412

  23. Dauphin Y, Williams CT, Barskov IS (2007) Aragonitic rostra of the Turonian belemnitid Goniocamax: Arguments from diagenesis. Acta Palaeont Pol 52:85–97

  24. Dauphin Y, Luquet G, Salomé M, Bellot-Gurley L, Cuif JP (2017) Structure and composition of Unio pictorum shell: arguments for the diversity of the nacroprismatic arrangement in molluscs. J Microsc 270(2):156–169

  25. Degens ET, Spencer DW, Parker RH (1967) Paleobiochemistry of molluscan shell proteins. Comp Biochem Physiol 20(2):553–579

  26. Doguzhaeva L, Mutvei H, Weitschat W (2003) The pro-ostracum and primordial rostrum at early ontogeny of lower Jurassic belemnites from North-Western Germany. In: Warnke K, Keupp H, Boletzky von S (eds) Coleoid cephalopods through time. Berliner Paläobiol Abh 03, pp 79–89

  27. Doguzhaeva L, Dunca E (2015) Siphonal zone structure in the cuttlebone of Sepia officinalis. Swiss J Palaeontol 134:167–176

  28. Dorey N, Melzner F, Martin S, Oberhänsli F, Teyssié JL, Bustamante P, Gattuso JP, Lacoue-Labarthe T (2013) Ocean acidification and temperature rise: effects on calcification during early development of the cuttlefish Sepia officinalis. Mar Biol 160:2007–2022

  29. Drozdova TV, Karyakin AV, Krasnova VA (1971) Chemical composition and infra-red absorption spectra of the organic matrix of the shell in the squid Sepia pharaonis. J Evol Biochem Physiol 7(4):350–356

  30. Ehrenberg CG (1828–1831) Animalia evertebrata exclusis Insectis. Series prima. In: Hemprich FG, Ehrenberg CG (eds) Symbolae physicae, seu icones et descriptiones Mammalium, Avium, Insectorum et animalia evertebra, quae ex itinere per Africam borealem et Asiam occidentalem studio nova aut illustrata redierunt. 126 pp. (1831), 10 pls (1828)

  31. Erben (1972) Über die Bildung und das Wachstum von Perlmutt. Biomineralisation 4:15–46

  32. Florek M, Fornal E, Gomez-Romero P, Zieba E, Paszkowicz W, Lekki J, Nowak J, Kuczumow A (2009) Complementary microstructural and chemical analyses of Sepia officinalis endoskeleton. Mater Sci Eng C29:1220–1226

  33. Grégoire C (1961) Sur la structure de la nacre septale des Spirulidae, étudiée au microscope électronique. Arch Int Physiol Biochim 69(3):374–377

  34. Grégoire C (1967) Sur la structure des matrices organiques des coquilles de mollusques. Biol Rev 42:653–688

  35. Gutowska MA, Pörtner HO, Melzner F (2008) Growth and calcification in the cephalopod Sepia officinalis under elevated seawater pCO2. Mar Ecol prog Ser 373:303–309

  36. Haas W (2003) Trends in the evolution of the Decabrachia. Berliner Paläobiol Abh 3:11–12

  37. 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 68B:535–546

  38. Jones GC, Jackson B (1993) Infrared transmission spectra of carbonate minerals. Springer, Berlin, p 239

  39. Karthika R, Manigandan V, Saravanan R, Rajesh RP, Chandrikada B (2016) Structural characterization and in vitro biomedical activities of sulfated chitosan from Sepia pharaonis. Int J Biol Macromol 84:319–328

  40. Kim BS, Kim JS, Sung HM, You HK, Lee J (2012) Cellular attachment and osteoblast differentiation of mesenchymal stem cells on natural cuttlefish bone. J Biomed Mater Res 100A:1673–1679

  41. Košt'ák M, Ruman A, Schlögl J, Hudácková N, Fuchs D, Mazuch M (2017) Miocene sepiids (Cephalopoda, Coleoidea) from Australia. Foss Rec 20:159–172

  42. Košt'ák M, Schlögl J, Hudáčková N, Kroh A, Halásová E, Gašparič R, Hyžný M, Wanzenböck G (2016) Sepia from the Miocene of the Central Paratethys: new taxa and notes on late Cenozoic cuttlefish diversity. J Syst Paleontol 14(12):1033–1057

  43. Kröger B, Vinther J, Fuchs F (2011) Cephalopod origin and evolution: a congruent picture emerging from fossils, development and molecules. BioEssays 33:602–613

  44. Le Pabic C, Rousseau M, Bonnaud-Ponticelli L, von Boletzky S (2016) Overview of the shell development of the common cuttlefish Sepia officinalis during early-life stages. Vie et Milieu 66(1):35–42

  45. Le Pabic C, Marie A, Marie B, Percot A, Bonnaud-Ponticelli L, Lopez PJ, Luquet G (2017) First proteomic analyses of the dorsal and ventral parts of the Sepia officinalis cuttlebone. J Proteom 150:63–73

  46. Le Pabic C, Derr J, Luquet G, Lopez P-J, Bonnaud-Ponticelli L (2019) Three-dimensional structural evolution of the cuttlefish Sepia officinalis shell from embryo to adult stages. J R Soc Interface 16(158):20190175. https://doi.org/10.1098/rsif.2019.0175

  47. Lemaire J (1970) Table de développement embryonnaire de Sepia officinalis L. (Mollusque, Céphalopode). Bull Soc zool Fr 95:773–782

  48. Linnaeus C (1758) Systema Naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Editio Decima, Reformata 1:824.

  49. Lowenstam HA, Weiner S (1989) On biomineralization. Oxford University Press, Oxford, p 323

  50. Marie B, Marin F, Marie A, Bédouet L, Dubost L, Alcaraz G, Milet C, Luquet G (2009) Evolution of nacre: biochemistry and proteomics of the shell organic matrix of the cephalopod Nautilus macromphalus. Eur J Chem Biol 10:1495–1506

  51. Mutvei H (1964) On the shells of Nautilus and Spirula with notes on the shell secretion in non cephalopod mollusks. Arkiv Zool 16:221–278

  52. Mutvei H (1970) Ultrastructure of the mineral and organic components of molluscan nacreous layers. Biomineralisation 2:48–61

  53. Mutvei H (2016) Siphuncular structure in the extant Spirula and other Coleoids (Cephalopoda). GFF 139(2):129–139

  54. Naef A (1922) Die fossilen Tintenfische. Carl Fisher, Jena, p 322

  55. Naef A (1928a) Die Cephalopoden Embryologie. In: Fauna und Flora des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. Friedländer, Berlin, p 357

  56. Naef A (1928b) Die Cephalopoden. In: Fauna und Flora des Golfes von Neapel. von R Friedländer & Sohn, Berlin, p 863.

  57. Ogasawara W, Shenton W, Davis SA, Mann S (2000) Template mineralization of ordered macroporous chitin-silica composites using a cuttlebone-derived organic matrix. Chem Mater 12:2835–2837

  58. Schoeppler V, Granasy L, Reich E, Poulsen N, de Kloe R, Cook P, Rack A, Pusztai T, Zlotnikov I (2018) Biomineralization as a paradigm of directional solidification: a physical model for Molluscan shell ultrastructural morphogenesis. Adv Mater 30(45):e1803855. https://doi.org/10.1002/adma.201803855

  59. Sen H (2013) The cuttlebone development of common cuttlefish [Sepia officinalis (Linneaus, 1758)]. Ege J Fish Aquac Sci 30:105–108

  60. Sherrard KM (2000) Cuttlebone morphology limits habitat depth in eleven species of Sepia (Cephalopoda: Sepiidae). Biol Bull 198:404–414

  61. Sigwart JD, Lyons G, Fink A, Gutowska MA, Murray D, Melzner F, Houghton JDR, Hu MY (2015) Elevated pCO2 drives lower growth and yet increased calcification in the early life history of the cuttlefish Sepia officinalis (Mollusca: Cephalopoda). ICES J Mar Sci 73:970–980

  62. Sykes AV, Domingues P, Andrade JP (2014) Sepia officinalis. In: Iglesias J, Fuentes L, Villanueva R (eds) Cephalopod culture. Springer, Dordrecht, pp 175–204

  63. Urmos J, Sharma SK, Mackenzie FT (1991) Characterization of some biogenic carbonates with Raman spectroscopy. Am Mineral 76:641–646

  64. von Boletzky S, Andouche A, Bonnaud-Ponticelli L (2016) A developmental table of embryogenesis in Sepia officinalis. Vie Milieu 66(1):25–34

  65. Wehrmeister U, Jacob DE, Soldati AL, Loges N, Häger T, Hofmeister W (2011) Amorphous, nanocrystalline and crystalline calcium carbonates in biological materials. J Raman Spectrosc 42:926–935

  66. Winlow W, Polese G, Moghadam H-F, Ahmed IA, Di Cosmo A (2018) Sense and insensibility—an appraisal of the effects of clinical anesthetics on gastropod and cephalopod molluscs as a step to improve welfare of cephalopods. Front Physiol 9:1147. https://doi.org/10.3389/fphys.2018.01147

  67. Yancey TE, Garvie CL, Wicksten M (2010) The middle Eocene Belosaepia ungula (Cephalopoda: Coleoida) from Texas: structure, ontogeny and function. J Paleontol 84(2):267–287

  68. Ylmen R, Jäglid U (2013) Carbonation of Portland cement studied by diffuse reflection Fourier transform infrared spectroscopy. Int J Concr Struct Mater 7(1):119–125

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Acknowledgements

This work was financially supported by the ATM "Interactions Minéral-Vivant" funding of the Muséum national d'Histoire naturelle (SEPIOM project). The authors thank all the members of the Max Planck Institute for Interfaces and Colloids (Golm, Germany) for their help. We thank C. Jozet-Alves and the CREC (University of Caen) for providing eggs of Sepia officinalis. LBP thanks G. Patriache and L. Largeau (CNRS-LPN) for the first tests on mineral composition of embryonic shell several years ago.

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Correspondence to Yannicke Dauphin or Laure Bonnaud-Ponticelli.

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Terminology used for the orientation of the fractures and polished sections studied using SEM and AFM (TIF 11378 kb)

Variations in morphology and structure of the chambered zone of adult and embryonic shells. A Enlargement of the basal part of a pillar of an adult shell; fracture fixed and etched (chromium sulphate pH 3.5 for 4 h.); SE - SEM. B Pillars are covered by an organic membrane (upper part); under the membrane, the granular structure of the pillar is visible; adult sample. SE - SEM. C Etched fracture trough a pillar of an adult shell showing the empty middle part (NaOH 0.5M for 4h at 100°C, pronase pH 7.6 for 6 h at 34°C, chitinase pH 5.6 for 22 h at 24°C); SE - SEM. D Etched vertical section through the pillar of an adult shell showing the different behaviour of the middle and external parts (NaOH 1 M for 4h 30 at 100°C, then 4 days at 20°C, lipase 1 mg/ml pH 9 for 28 h at 35°C); SE - SEM. E Pillars in the first septa of an adult shell. SE - SEM. F Unetched granular surface of the lateral growing edge of a larval shell; BSE - SEM. G Unetched tangential fracture showing the zig zag “wall” made by coalescent pillars in an adult shell. H-I Stage 25/26 embryonic shell after 24h in vitro incubation of the embryo in a calcein-containing sea water (30 mg/L; CNAM, Sigma) followed by 48h incubation in sea water, H Optical image, I Fluorescence image showing that calcification occurs during the growth at the distal extremities of the pillars (TIF 11950 kb)

FTIR spectra of the soluble and insoluble organic matrices extracted from the dorsal shield and ventral zone of an adult shell, showing the similarity between the insoluble matrix and the crab chitin. The dorsal shield and the ventral zone were mechanically separated in adult samples, immersed in 3% NaClO for 1 h to remove organic contaminants, rinsed with Milli-Q water, dried, and ground into powder by grinding with an electric mortar for 10 min to obtain homogeneous granulometry. Powdered samples were immersed in Milli-Q water and decalcified by progressive addition of 50% acetic acid so that the pH (automatically controlled with a titrimeter) is above 4. The entire extract was centrifuged at 21,000 g for 15 min, which separated the supernatant (soluble) and precipitated (insoluble) fractions. The soluble fraction was desalted by exchange with Milli-Q water on a Microconcentrator (Filtron) using a 3-kDa cut-off membrane and lyophilized. Powdered samples and KBr were oven-dried at 38°C overnight. Then, they were mixed (about 5% powdered samples in KBr) and loaded into the sample cup (TIF 7340 kb)

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Dauphin, Y., Luquet, G., Percot, A. et al. Comparison of embryonic and adult shells of Sepia officinalis (Cephalopoda, Mollusca). Zoomorphology (2020). https://doi.org/10.1007/s00435-020-00477-2

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Keywords

  • Sepia
  • Embryonic shell
  • Structure
  • Composition