Marine Biology

, Volume 162, Issue 3, pp 687–697 | Cite as

Shell growth, microstructure and composition over the development cycle of the European abalone Haliotis tuberculata

  • S. Auzoux-BordenaveEmail author
  • C. Brahmi
  • A. Badou
  • M. de Rafélis
  • S. Huchette
Original Paper


The shell of the European abalone Haliotis tuberculata is a model for studying mechanisms of mollusc shell formation, but the early steps of shell formation and calcification remain poorly documented. The microstructure and the mineralogical and geochemical composition of larval and juvenile shells were investigated by scanning electron microscopy, infrared spectroscopy and ion microprobe analyses (NanoSIMS). Analyses were performed on shells obtained from controlled fertilisations at the hatchery France-Haliotis (Plouguerneau, France) in July 2009 and 2010 using abalone from Roscoff. Shell cross sections revealed the microstructural arrangement of the developing shell, showing progressive biomineral organisation into two differentiated layers, i.e. the outer granular and the internal nacreous layer. Infrared analysis confirmed that the European abalone shell, at every stage of development, was mostly composed of CaCO3 in the form of aragonite. Variations in trace element composition, i.e. Sr/Ca, were measured in the different stages and correlated with micro-structural changes in the shells. Experimental manganese labelling of live abalones produced cathodoluminescence marks in the growing shell sections. The increase in shell thickness can be used to determine the growth rate of an early adult abalone shell.


Trace Element Composition Shell Layer Shell Growth Larval Shell Nacreous Layer 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was financed in part by the ATM program “Biomineralisation” of the MNHN funded by the Ministère délégué à l’Enseignement Supérieur et à la Recherche (Paris, France). We thank Pr Anders Meibom for the facilities and assistance for the NanoSIMS analysis ion microprobe (Muséum national d’Histoire naturelle, Paris, France). We are grateful to Claire E. Lazareth (UMR LOCEAN, Bondy, France) for her kind reading of the manuscript.

Supplementary material

227_2015_2615_MOESM1_ESM.pdf (33 kb)
Supplementary material 1 (PDF 32 kb)


  1. Auzoux-Bordenave S, Badou A, Gaume B, Berland S, Helléouet M-N, Milet C, Huchette S (2010) Ultrastructure, chemistry and mineralogy of the growing shell of the European abalone Haliotis tuberculata. J Struct Biol 171:277–290. doi: 10.1016/j.jsb.2010.05.012 CrossRefGoogle Scholar
  2. Bice KL, Layne GD, Dahl K (2005) Application of secondary ion mass spectrometry to the determination of Mg/Ca in rare, delicate, or altered planktonic foraminifera: examples from the Holocene, Paleogene, and Cretaceous. Geochem Geophys Geosyst 6:1–13. doi: 10.1029/2005gc000974 CrossRefGoogle Scholar
  3. Bøggild OB (1930) The shell structure of the mollusks. Det Kongelige Danske Videnskabernes Selskab Skrifter-Naturvidenskabelig og Mathematisk Afdeling 9:231–326Google Scholar
  4. Brahmi C, Meibom A, Smith D, Stolarski J, Auzoux-Bordenave S, Nouet J, Doumenc D, Djediat C, Domart-Coulon I (2010) Skeletal growth, ultrastructure and composition of the azooxanthellate scleractinian coral Balanophyllia regia. Coral Reefs 29:175–189CrossRefGoogle Scholar
  5. Carre M, Bentaleb I, Bruguier O, Ordinola E, Barrett N, Fontugne M (2006) Calcification rate influence on trace element concentrations in aragonitic bivalve shells: evidences and mechanisms. Geochim Cosmochim Acta 70:4906–4920. doi: 10.1016/j.gca.2006.07.019 CrossRefGoogle Scholar
  6. Chateigner D, Hedegaard C, Wenk HR (2000) Mollusc shell microstructures and crystallographic textures. J Struct Geol 22:1723–1735CrossRefGoogle Scholar
  7. Clavier J, Richard O (1986) Growth of juvenile Haliotis tuberculata (Mollusca: Gastropoda) in their natural environment. J Mar Biol Assoc UK 66:497–503CrossRefGoogle Scholar
  8. 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 15:7–38Google Scholar
  9. Dauphin Y, Cuif J-P, Castillo-Michel H, Chevallard C, Farre B, Meibom A (2014) Unusual micrometric calcite–aragonite interface in the abalone shell Haliotis (Mollusca, Gastropoda). Microsc Microanal 20:276–284. doi: 10.1017/S1431927613013718 CrossRefGoogle Scholar
  10. Gaume B, Fouchereau-Peron M, Badou A, Helléouet M-N, Huchette S, Auzoux-Bordenave S (2011) Biomineralization markers during early shell formation in the European abalone Haliotis tuberculata, Linnaeus. Mar Biol 158:341–353. doi: 10.1007/s00227-010-1562-x CrossRefGoogle Scholar
  11. Gendron-Badou A, Coradin T, Maquet J, Fröhlich F, Livage J (2003) Spectroscopic characterization of biogenic silica. J Non-Cryst Solids 316:331–337CrossRefGoogle Scholar
  12. Gillikin DP, Lorrain A, Navez J, Taylor JW, André L, Keppens E, Baeyens W, Dehairs F (2005) Strong biological controls on Sr/Ca ratios in aragonitic marine bivalve shells. Geochem Geophys Geosyst 6:1–15CrossRefGoogle Scholar
  13. Guo D-J (2010) Microstructure and crystallography of abalone shells. Thesis, Research Master Degree, GlasgowGoogle Scholar
  14. Hawkes GP, Day RW, Wallace MW, Nugent KW, Bettiol AA, Jamieson DN, Williams MC (1996) Analyzing the growth and form of mollusc shell layers, in situ, by cathodoluminescence microscopy and Raman spectroscopy. J Shellfish Res 15:659–666Google Scholar
  15. Heinemann F, Launspach M, Gries K, Fritz M (2011) Gastropod nacre: structure, properties and growth: biological, chemical and physical basics. Biophys Chem 153:126–153. doi: 10.1016/j.bpc.2010.11.003 CrossRefGoogle Scholar
  16. Jackson A, Vincent J, Turner R (1990) Comparison of nacre with other ceramic composites. J Mater Sci 25:3173–3178CrossRefGoogle Scholar
  17. Jackson DJ, Wörheide G, Degnan BM (2007) Dynamic expression of ancient and novel molluscan shell genes during ecological transitions. BMC Evol Biol 7:160. doi: 10.1186/1471-2148-7-160 CrossRefGoogle Scholar
  18. Jardillier E, Rousseau M, Gendron-Badou A, Fröhlich F, Smith D, Martin M, Helléouet M-N, Huchette S, Doumenc D, Auzoux-Bordenave S (2008) A morphological and structural study of the larval shell from the abalone Haliotis tuberculata. Mar Biol 154:735–744CrossRefGoogle Scholar
  19. Jones GC, Jackson B (1993) Infrared transmission spectra of carbonate minerals. Chapman & Hall, LondonCrossRefGoogle Scholar
  20. Kinsman DJJ, Holland HD (1969) Co-precipitation of cations with CaCO3 IV. Co-precipitation of Sr2+ with aragonite between 16° and 96°C. Geochim Cosmochim Acta 33:1–17CrossRefGoogle Scholar
  21. Klein RT, Lohmann KC, Thayer CW, January R (1996) Sr/Ca and 13C/12C ratios in skeletal calcite of Mytilus trossulus: covariation with metabolic rate, salinity and carbon isotopic composition of seawater. Science 60:4207–4221Google Scholar
  22. Lartaud F, de Rafelis M, Ropert M, Emmanuel L, Geairon P, Renard M (2010) Mn labelling of living oysters: artificial and natural cathodoluminescence analyses as a tool for age and growth rate determination of C. gigas (Thunberg, 1793) shells. Aquaculture 300:206–217. doi: 10.1016/j.aquaculture.2009.12.018 CrossRefGoogle Scholar
  23. Lazareth CE, Guzman N, Poitrasson F, Candaudap F, Ortlieb L (2007) Nyctemeral variations of magnesium intake in the calcitic layer of a Chilean mollusk shell (Concholepas concholepas, Gastropoda). Geochim Cosmochim Acta 71:5369–5383CrossRefGoogle Scholar
  24. Lazareth CE, Le Cornec F, Candaudap F, Freydier R (2013) Trace element heterogeneity along isochronous growth layers in bivalve shell: consequences for environmental reconstruction. Palaeogeogr Palaeoclimatol Palaeoecol 373:39–49. doi: 10.1016/j.palaeo.2011.04.024 CrossRefGoogle Scholar
  25. Lin A, Meyers MA (2005) Growth and structure in abalone shell. Mat Sci Eng A 390:27–41CrossRefGoogle Scholar
  26. Lorrain A, Gillikin DP, Le Mercier A (2005) Strong kinetic effects on Sr/Ca ratios in the calcitic bivalve Pecten maximus. Geology 12:965–968CrossRefGoogle Scholar
  27. Mahé K, Bellamy E, Lartaud F, de Rafélis M (2010) Calcein and manganese experiments for marking the shell of the common cockle (Cerastoderma edule): tidal rhythm validation of increments formation. Aquat Living Res 23:239–245. doi: 10.1051/alr/2010025 CrossRefGoogle Scholar
  28. Meibom A, Cuif J-P, Houlbreque F, Mostefaoui S, Dauphin Y, Meibom KL, Dunbar R (2008) Compositional variations at ultra-structure length scales in coral skeleton. Geochim Cosmochim Acta 72:1555–1569CrossRefGoogle Scholar
  29. Mutvei H, Dauphin Y, Cuif J-P (1985) Observations sur l’organisation de la couche externe du test des Haliotis (Gastropoda): un cas exceptionnel de la variabilité minéralogique et microstructurale. Bulletin du Muséum national d’Histoire naturelle, Paris, 4e série 7, section A, 1:73–91Google Scholar
  30. Nakahara H, Bevelander G, Kakei M (1982) Electron microscopic and amino acid studies on the outer and inner shell layers of Haliotis rufescens. Venus (Japan J Malacol), pp 33–46Google Scholar
  31. Pichard C, Fröhlich F (1986) Analyses infrarouges quantitatives des sédiments. Exemple du dosage du quartz et de la calcite. Revue de l’Institut français du Pétrole 41:809–819Google Scholar
  32. Purton L, Shields G, Brasier M, Grime G (1999) Metabolism controls Sr/Ca ratios in fossil aragonitic mollusks. Geology 27:1083–1086CrossRefGoogle Scholar
  33. Purton-Hildebrand LMA, Shields GA, Brasier MD (2001) The use of external micro-PIXE to investigate the factors determining the Sr:Ca ratio in the shells of fossil aragonitic molluscs. Science 181:506–510Google Scholar
  34. Roussel S, Huchette S, Clavier J, Chauvaud L (2011) Growth of the European abalone (Haliotis tuberculata L.) in situ: seasonality and ageing using stable oxygen isotopes. J Sea Res 65:213–218. doi: 10.1016/j.seares.2010.10.001 CrossRefGoogle Scholar
  35. Su X, Belcher AM, Zaremba CM, Morse DE, Stucky GD, Heuer AH (2002) Structural and microstructural characterization of the growth lines and prismatic microarchitecture in red abalone shell and the microstructures of abalone “flat pearls”. Chem Mater 14:3106–3117CrossRefGoogle Scholar
  36. Weiner S, Dove PM (2003) An overview of biomineralization processes and the problem of the vital effect. In: Dove PM, De Yoreo JJ, Weiner S (eds) Biomineralization. American Mineralogical Society, Washington, DC, pp 1–29Google Scholar
  37. Zacherl DC, Paradis G, Lea DW (2003) Barium and strontium uptake into larval protoconchs and statoliths of the marine neogastropod Kelletia kelletii. Geochim Cosmochim Acta 67:4091–4099CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • S. Auzoux-Bordenave
    • 1
    • 2
    Email author
  • C. Brahmi
    • 3
  • A. Badou
    • 1
  • M. de Rafélis
    • 4
  • S. Huchette
    • 5
  1. 1.UMR BOREA “Biologie des Organismes et Ecosystèmes Aquatiques”, MNHN/CNRS 7208/IRD 207/UPMCMuséum national d’Histoire naturelle, Station de Biologie Marine de ConcarneauConcarneauFrance
  2. 2.Sorbonne Universités, UPMCUniversité Paris 6ParisFrance
  3. 3.UMR EIOUniversité de Polynésie françaiseFaa’aFrench Polynesia
  4. 4.UMR 7193 “Biominéralisations et Environnements sédimentaires”UPMC-ISTePParisFrance
  5. 5.Ecloserie France-HaliotisPlouguerneauFrance

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