Skip to main content

Advertisement

SpringerLink
Log in

A morphological and structural study of the larval shell from the abalone Haliotis tuberculata

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The larval shell of the marine gastropod Haliotis tuberculata was investigated by polarised light microscopy, scanning electron microscopy, Raman microspectroscopy and infra-red spectroscopy. Trochophore and veliger larval sections were used for histological examination of the growing shell and each larval stage was related to the shell development and the appearance of calcified formations. We determined the stage of initial calcification by specific staining combined with polarised light examination. The shell of 30-h-old pre-veliger larvae was found to be mineralized, confirming that calcification occurred before larval torsion. Using both infra-red and Raman spectroscopy, we showed that CaCO3 deposition occurred at the pre-veliger stage and that the mineral phase initially deposited was essentially composed of aragonite.

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

Access this article

Log in via an institution

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
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Bandel K (1982) Morphologie und Bildung der frühontogenetischen Gehause bei conchiferen mollusken. Facies 7:1–198 (Translation by A. Beckmann, R. Collin)

    Article  Google Scholar 

  • Bielefeld U, Becker W (1991) Embryonic development of the shell in Biomphalaria glabrata (Say). Int J Dev Biol 35:121–131

    PubMed  CAS  Google Scholar 

  • Bøggild OB (1930) The shell structure of the mollusks. Det Kongelige Danske Videnskabernes Selskab Skrifter-Naturvidenskabelig og Mathematisk Afdeling 9:233–326

    Google Scholar 

  • Collin R, Voltzow J (1998) Initiation, calcification, and form of larval “Archaeogastropod” shells. J Morphol 235:77–89

    Article  Google Scholar 

  • Crofts DR (1937) The development of Haliotis tuberculata, with special reference to organogenesis during torsion. Phil Trans R Soc Lond B Biol Sci 228:219–268

    Article  Google Scholar 

  • Dauphin Y, Cuif J-P, Mutvei H, Denis A (1989) Mineralogy, chemistry and ultrastructure of the external shell-layer in ten species of Haliotis with reference to Haliotis tuberculata (Mollusca: Archaeogastropoda). Bull Geol Inst Univ Uppsala, N.S. 15:7–38

    Google Scholar 

  • Eyster LS (1986) Shell inorganic composition and onset of shell mineralization during bivalve and gastropod embryogenesis. Biol Bull 170:211–231

    Article  CAS  Google Scholar 

  • Eyster LS, Morse MP (1984) Early shell formation during molluscan embryogenesis with new studies on the surf clam Spisula solidissima. Am Zool 24:871–882

    Google Scholar 

  • Fröhlich F, Gendron-Badou A (2002) La spectroscopie infrarouge, un outil polyvalent. In: Miskovsky JC (ed) Géologie de la Préhistoire. AEEGP éditeur, Paris, pp 662–677

    Google Scholar 

  • Gendron-Badou A, Coradin T, Maquet J, Fröhlich F, Livage J (2003) Spectroscopic characterization of biogenic silica. J Non-crystalline Solids 316:331–337

    Article  CAS  Google Scholar 

  • Griffith WP (1970) Raman studies on rock-forming minerals. J Chem Soc A:286–291

    Google Scholar 

  • Hasse B, Ehrenberg H, Marxen JC, Becker W, Epple M (2000) Calcium carbonate modifications in the mineralized shell of the freshwater snail Biomphalaria glabrata. Chem A Eur J 6:3679–3685

    Article  CAS  Google Scholar 

  • Hickman CS (2001) Evolution and development of gastropod larval shell morphology: experimental evidence for mechanical defense and repair. Evol Dev 3:18–23

    Article  PubMed  CAS  Google Scholar 

  • Iwata K (1980) Mineralization and architecture of the larval shell of Haliotis discus hannai Ino (Archaeogastropoda). J Fac Sci Hokkaido Univ Ser 4(19):305–320

    Google Scholar 

  • Jablonski B, Lutz RA (1980) Molluscan larval shell morphology, ecological and paleontological applications. In: Rhoads DC, Lutz RA (eds) Skeletal growth of aquatic organisms. Plenum Press, New York, pp 323–377

    Google Scholar 

  • Kniprath E (1981) Ontogeny of the molluscan shell field: a review. Zool Scr 10:61–79

    Article  Google Scholar 

  • Koike Y (1978) Biological and ecological studies on the propagation of the ormer, Haliotis tuberculata Linnaeus. I. Larval development and growth of juveniles. La Mer Bull Soc Franco-japonaise Océanogr 16:124–136

    Google Scholar 

  • Lin A, Meyers MA (2005) Growth and structure in abalone shell. Mater Sci Eng A 390:27–41

    Article  CAS  Google Scholar 

  • Marin F, Luquet G (2004) Molluscan shell proteins. C R Palevol 3:469–492

    Article  Google Scholar 

  • Marxen JC, Becker W, Finke D, Hasse B, Epple M (2003a) Early mineralization in Biomphalaria glabrata: microscopic and structural results. J Molluscan Stud 69:113–121

    Article  Google Scholar 

  • Marxen JC, Witten PE, Finke D, Reelsen O, Rezgaoui M, Becker W (2003b) A light- and electron-microscopic study of enzymes in the embryonic shell-forming tissue of the freshwater snail, Biomphalaria glabrata. Invertebr Biol 122:313–325

    Article  Google Scholar 

  • Nasdala L, Smith DC, Kaindl R, Ziemann MA (2004) Raman spectroscopy: analytical perspectives in mineralogical research. In: Beran A, Libowitzky E (eds) EMU notes in mineralogy, Chap 7. EMU School on Spectroscopic Methods in Mineralogy, pp 281–343

  • Page LR (1997) Ontogenetic torsion and protoconch form in the archaeogastropod Haliotis kamtschatkana: evolutionary implications. Acta Zool 78:227–245

    Article  Google Scholar 

  • Perrin C, Smith DC (2007) Earliest steps of diagenesis in living scleractinian corals: evidence from ultrastructural pattern and Raman spectroscopy. J Sediment Res 77:495–507

    Article  CAS  Google Scholar 

  • Pichard C, Fröhlich F (1986) Analyses infrarouges quantitatives des sédiments. Exemple du dosage du quartz et de la calcite. Rev Inst Fr Pétrole 41:809–819

    CAS  Google Scholar 

  • Rousseau M, Lopez E, Couté A, Mascarel G, Smith DC, Naslain R, Bourrat X (2004) Multi-scale structure and growth of nacre: a new model for bioceramics. Key Eng Mater 254–256:1009–1012

    Google Scholar 

  • Rousseau M, Lopez E, Couté A, Mascarel G, Smith DC, Naslain R, Bourrat X (2005) Sheet nacre growth mechanism: a Voronoi model. J Struct Biol 149:149–157

    Article  PubMed  Google Scholar 

  • Silve C, Lopez E, Vidal B, Smith DC, Camprasse S, Camprasse G, Couly G (1992) Nacre initiates biomineralization by human osteoblasts maintained in vitro. Calcif Tissue Int 51:363–369

    Article  PubMed  CAS  Google Scholar 

  • Smith DC, Dellinger M, Guillaume M (1999) The Raman spectrum of monohydrocalcite. In: Congress GEORAMAN’99 abstracts, Special Publication, Universidad Valladolid Press, Valladolid, abstracts vol, pp 81–82

  • Thompson JB, Paloczi GT, Kindt JH, Michenfelder M, Smith BL, Stucky GD, Morse DE, Hansma PK (2000) Direct observation of the transition from calcite to aragonite growth as induced by abalone shell proteins. Biophys J 79:3307–3312

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Watabe N, Wilbur KM (1960) Influence of the organic matrix on crystal type in molluscs. Nature 188:334

    Article  Google Scholar 

  • Weiss IM, Tuross N, Addadi L, Weiner S (2002) Mollusc larval shell formation: amorphous calcium carbonate is a precursor phase for aragonite. J Exp Zool 293:478–491

    Article  PubMed  CAS  Google Scholar 

  • Wilbur KM, Saleuddin ASM (1983) Shell formation. In: The mollusca, vol 4. Academic Press, New York, pp 235–285

Download references

Acknowledgments

This work was supported by grants from the Centre National de la Recherche Scientifique (CNRS, Paris, France) and the Muséum National d’Histoire Naturelle (MNHN, Paris, France). We thank Gérard Mascarel for his assistance in electron microscopy work. We also thank Professor Jean-Pierre Cuif for his helpful discussions and Dr. Andrea Bullock for her critical reading of the manuscript. The experiments complied with the current French laws.

Author information

Authors and Affiliations

  1. UMR 5178 CNRS/MNHN/UPMC, Station de Biologie Marine, MNHN, BP 225, 29182, Concarneau Cedex, France

    E. Jardillier, M.-N. Helléouet & S. Auzoux-Bordenave

  2. UMR 5178 CNRS/MNHN/UPMC, Muséum National d’Histoire Naturelle, 75005, Paris, France

    M. Rousseau, M. Martin & D. Doumenc

  3. UMR 5198, Centre de Spectroscopie Infrarouge, Département Préhistoire, Muséum National d’Histoire Naturelle, 17, Place du Trocadéro, 75016, Paris, France

    A. Gendron-Badou & F. Fröhlich

  4. USM 205 LEME, Département Histoire de la Terre, Muséum National d’Histoire Naturelle, 75231, Paris Cedex 05, France

    D. C. Smith

  5. France-Haliotis, Kérazan, 29880, Plouguerneau, France

    S. Huchette

Authors
  1. E. Jardillier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Rousseau
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Gendron-Badou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. Fröhlich
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. D. C. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M.-N. Helléouet
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. S. Huchette
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. D. Doumenc
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. S. Auzoux-Bordenave
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. Auzoux-Bordenave.

Additional information

Communicated by J.-M. Gili.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jardillier, E., Rousseau, M., Gendron-Badou, A. et al. A morphological and structural study of the larval shell from the abalone Haliotis tuberculata . Mar Biol 154, 735–744 (2008). https://doi.org/10.1007/s00227-008-0966-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-008-0966-3

Keywords

Search

Navigation