Abstract
Oysters live permanently immobilised by cementation of the left valve to a hard substrate. The contact zone between oysters and natural substrata has been analysed using SEM imaging, electron dispersive X-ray microanalysis, electron backscatter diffraction and Raman spectroscopy and reveals the influence of both biogenic and non-biogenic processes in oyster cementation. Original adhesion is brought about by secretion of an organic component that acts as a nucleating surface onto which crystals precipitate. These crystals have a random orientation and are composed of high Mg calcite. This suggests that the crystals nucleating on the glue substrate are outwith the biological control experienced by the shell biomineralisation process and are formed by inorganic precipitation from seawater. It is proposed that oysters do not control or secrete crystalline cement. Instead, they adhere by secretion of an organic film onto which crystals precipitate from seawater.
Similar content being viewed by others
References
Bathurst RGC (1975) Carbonate cements and their diagenesis. Elsevier Scientific Publishing Company, Amsterdam
Bischoff WD, Bishop FC, Mackenzie FT (1983) Biogenically produced magnesian calcite inhomogeneities in chemical and physical—properties comparison with synthetic phases. Am Mineral 68:1183–1188
Bischoff WD, Sharma SK, Mackenzie FT (1985) Carbonate ion disorder in synthetic and biogenic magnesian calcites—a Raman spectral study. Am Mineral 70:581–589
Bogan A, Bouchet P (1998) Cementation in the freshwater bivalve family Corbiculidae (Mollusca: Bivalvia): a new genus and species from Lake Poso, Indonesia. Hydrobiologia 389:131–139
Braithwaite CJR, Taylor JD, Glover EA (2000) Marine carbonate cements, biofilms, biomineralization, and skeletogenesis: some bivalves do it all. J Sediment Res 70:1129–1138
Bromley RG, Heinberg C (2006) Attachment strategies of organisms on hard substrates: a palaeontological view. Palaeogeogr Palaeocl 232:429–453
Burton EA, Walter LM (1987) Relative precipitation rates of aragonite and Mg calcite from seawater: temperature or carbonate ion control? Geology 15:111–114
Carriker MR, Palmer RE, Prezant RS (1980) Functional ultra morphology of the dissoconch valves of the oyster Crassostrea virginica. Proc Natn Shellfish Ass 70:139–183
Chave KE, Suess E (1970) Calcium carbonate saturation in seawater: effects of dissolved organic matter. Limnol Oceanogr 15:633–637
Checa AG, Rodriguez-Navarro AB, Delgado FJE, Esteban-Delgado FJ (2005) The nature and formation of calcitic columnar prismatic shell layers in pteriomorphian bivalves. Biomaterials 26:6404–6414
Checa AG, Esteban-Delgado FJ, Ramirez-Rico J, Rodriguez-Navarro AB (2009) Crystallographic reorganization of the calcitic prismatic layer of oysters. J Struct Biol 167:261–270
Cranfield HJ (1973a) Observations on function of glands of foot of pediveliger of Ostrea edulis during settlement. Mar Biol 22:211–223
Cranfield HJ (1973b) Observations on the behaviour of pediveliger of Ostrea edulis during attachment and cementing. Mar Biol 22:203–209
Cranfield HJ (1973c) Study of morphology, ultrastructure and histochemistry of foot of pediveliger of Ostrea edulis. Mar Biol 22:187–202
Cranfield HJ (1974) Observations on the morphology of the mantle folds of the pediveliger of Ostrea Edulis and their function during settlement. J Mar Biol Ass UK 54:1–12
Cranfield HJ (1975) The ultrastructure and histochemistry of the larval cement of Ostrea edulis. J Mar Biol Ass UK 55:497–503
Cusack M, Pérez-Huerta A, Dalbeck P (2007) Common crystallographic control in calcite biomineralization of bivalved shells. CrystEngComm 9:1215–1218
Cusack M, Parkinson D, Freer A, Pérez-Huerta A, Fallick AE, Curry GB (2008) Oxygen isotope composition in Modiolus modiolus aragonite in the context of biological and crystallographic control. Mineral Mag 72:569–577
Dalbeck P, Cusack M (2006) Crystallography (electron backscatter diffraction) and chemistry (electron probe microanalysis) of the avian eggshell. Cryst Growth Des 6:2558–2562
De Bruyne NA (1962) The action of adhesives. Sci Am 206:114–126
Eltzholtz JR, Birkedal H (2009) Architecture of the biomineralized byssus of the saddle oyster (Anomia sp.). J Adhes 85:590–600
Esteban-Delgado FJ, Harper EM, Checa AG, Rodriguez-Navarro AB (2008) Origin and expansion of foliated microstructure in pteriomorph bivalves. Biol Bull 214:153–165
Friedman GM (1998) Rapidity of marine carbonate cementation—implications for carbonate diagenesis and sequence stratigraphy: perspective. Sediment Geol 119:1–4
Galtsoff PS (1964) The American Oyster Crassostrea Virginica Gmelin. Government Printing office, Washington
Gillet P, Biellmann C, Reynard B, McMillan P (1993) Raman spectroscopic studies of carbonates. 1. High pressure and high temperature behaviour of calcite, magnesite, dolomite and aragonite. Phys Chem Miner 20:1–18
Harper EM (1991) The role of predation in the evolution of cementation in bivalves. Palaeontology 34:455–460
Harper EM (1992) Postlarval cementation in the Ostreidae and its implications for other cementing Bivalvia. J Mollusc Stud 58:37–47
Harper EM (1997) Attachment of mature oysters (Saccostrea cucullata) to natural substrata. Mar Biol 127:449–453
Harper EM, Morton B (2000) The biology and functional morphology of Myochama anomioides Stutchbury, 1830 (Bivalvia: Anomalodesmata: Pandoroidea), with reference to cementation. J Mollusc Stud 66:403–416
Hillgartner H, Dupraz C, Hug W (2001) Microbially induced cementation of carbonate sands: are micritic meniscus cements good indicators of vadose diagenesis? Sedimentology 48:117–131
Lecuyer C, Reynard B, Martineaua F (2004) Stable isotope fractionation between mollusc shells and marine waters from Martinique Island. Chem Geol 213:293–305
Li Y-H, Takahashi T, Broecker WS (1969) Degree of saturation of CaCO3 in the oceans. J Geophys Res 74:5507–5525
MacDonald J, Freer A, Cusack M (2010) Alignment of crystallographic c-axis throughout the four distinct microstructural layers of the oyster Crassostrea gigas. Cryst Growth Des 10:1243–1246
Mitterer RM (1971) Influence of natural organic matter on CaCO3 precipitation. In: Bricker OP (ed) Carbonate cements. Studies in geology 19. The John Hopkins Press, Baltimore, pp 252–258
Morse JW, Mackenzie FT (1990) Geochemistry of sedimentary carbonates. Elsevier, Amsterdam
Morton B, Harper EM (2001) Cementation in Cleidothaerus albidus (Lamarck, 1819) (Bivalvia: Anomalodesmata: Pandoroidea). Molluscan Res 21:1–15
Perez FR, Martinez-Frias J (2003) Identification of calcite grains in the Vaca Muerta mesosiderite by Raman spectroscopy. J Raman Spectrosc 34:367–370
Pérez-Huerta A, Cusack M (2009) Optimizing electron backscatter diffraction of carbonate biominerals-resin type and carbon coating. Microsc Microanal 15:197–203
Pope MC, Grotzinger JP, Schreiber BC (2000) Evaporitic subtidal stromatolites produced by in situ precipitation: textures, facies associations, and temporal significance. J Sediment Res 70:1139–1151
Stenzel HB (1971) Oysters. In: Moore R (ed) Treatise of invertebrate paleontology. Part N. Mollusca. 6. Bivalvia, vol 3. Geological Association of America, pp N953–N1224
Tucker ME, Wright VP (1990) Carbonate sedimentology. Blackwell Scientific Publications, Oxford
Urmos J, Sharma SK, Mackenzie FT (1991) Characterisation of some biogenic carbonates with Raman spectroscopy. Am Mineral 76:641–646
Weiner S, Addadi L, Wagner HD (2000) Materials design in biology. Mater Sci Eng 11:1–8
Yamaguchi K (1993) Shell structure and behaviour related to cementation in oysters. Mar Biol 118:89–100
Yonge CM (1979) Cementation in bivalves. In: van der Spoel S, van Bruggen C, Lever J (eds) Pathways in malacology. Scheltema and Holkema, Utrecht, pp 83–106
Acknowledgments
Research is funded by a BBSRC DTA award which is gratefully acknowledged. We also thank Peter Chung for his assistance with SEM and EBSD analysis as well as John Gilleece and Nick Kamenos for assistance with sample preparation. Finally, many thanks to Colin Braithwaite for his assistance and advice throughout this study.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by F. Bulleri.
Rights and permissions
About this article
Cite this article
MacDonald, J., Freer, A. & Cusack, M. Attachment of oysters to natural substrata by biologically induced marine carbonate cement. Mar Biol 157, 2087–2095 (2010). https://doi.org/10.1007/s00227-010-1476-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-010-1476-7