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Nanoscale Morphology and Indentation of Individual Nacre Tablets from the Gastropod Mollusc Trochus Niloticus

  • B.J.F. Bruet (a1), H.J. Qi (a2), M.C. Boyce (a2), R. Panas (a1), K. Tai (a1), L. Frick (a1) and C. Ortiz (a1)
  • DOI:
  • Published online: 01 March 2011

The inner nacreous layer of gastropod mollusc Trochus niloticus is composed of ∼95 wt% planar arrays of polygonal aragonite-based tablets (∼8 μm wide, ∼0.9 μm thick, stacked ∼40 nm apart) and ∼5 wt% biomacromolecules. High-resolution tapping mode atomic force microscope images enabled nanoscale resolution of fractured tablet cross-sections, the organic component, and deformation of individual nanoasperities on top of tablet surfaces. Nanoindentation was performed on individual nacre tablets and the elastic modulus E and yield stress σy were reduced from elastic-plastic finite element simulations yielding E = 92 GPa, σy = 11 GPa (freshly cleaved samples) and E = 79 GPa, σy = 9 GPa (artificial seawater soaked samples). Images of the indents revealed extensive plastic deformation with a clear residual indent and surrounding pileup.

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This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

1A.P. Jackson , J.F.V. Vincent and R.M. Turner : The mechanical design of nacre. Proc. R. Soc. London B Biol. Sci. 234, 415 (1988).

2S. Weiner and L. Addadi : Design strategies in mineralized biological materials. J. Mater. Chem. 7, 689 (1997).

4R. Menig , M.H. Meyers , M.A. Meyers and K.S. Vecchio : Quasi-static and dynamic mechanical response of Haliotis rufescens (abalone) shells. Acta Mater. 48, 2383 (2000).

5A.P. Jackson , J.F.V. Vincent and R.M. Turner : Comparison of nacre with other ceramic composites. J. Mater. Sci., 25, 3173 (1990).

6J.D. Currey : Mechanical properties of mother of pearl in tension. Proc. R. Soc. London B Biol. Sci. 196(1125), 443 (1977).

9D.J.M. Bevan , E. Rossmanith , D.K. Mylrea , S.E. Ness , M.R. Taylor and C. Cuff : On the structure of aragonite— Lawrence Bragg revisited. Acta Crystallogr. B. Struct. Sci. B 58, 448 (2002).

10H. Mutvei : Ultrastructural characteristics of the nacre in some gastropods. Zool. Scr. 7, 287 (1978).

11X. Li , W-C. Chang , Y.J. Chao , R. Wang and M. Chang : Nanoscale structural and mechanical characterization of a natural nanocomposite material: The shell of red abalone. Nano Lett. 4, 613 (2004).

12G. Bevelander and H. Nakahara : An electron microscope study of the formation of the nacreous layer in the shell of certain bivalve molluscs. Calc. Tiss. Res. 3, 84 (1969).

15T.E. Schäffer , C. Ionescu-Zanetti , R. Proksch , M. Fritz , D.A. Walters , N. Almqvist , C.M. Zaremba , A.M. Belcher , B.L. Smith , G.D. Stucky , D.E. Morse and P.K. Hansma : Does abalone nacre form by heteroepitaxial nucleation or by growth through mineral bridges? Chem. Mater. 9, 1731 (1997).

16S. Manne , C.M. Zaremba , R. Giles , L. Huggins , D.A. Walters , A. Belcher , D.E. Morse , G.D. Stucky , J.M. Didymus , S. Mann and P.K. Hansma : Atomic force microscopy of the nacreous layer in mollusc shells. Proc. R. Soc. London B Bio. Sci. 256, 17 (1994).

18X. Shen , A.M. Belcher , P.K. Hansma , G.D. Stucky and D.E. Morse : Molecular cloning and characterization of lustrin A, a matrix protein from shell and pearl nacre of Haliotis rufescens J. Bio. Chem. 272, 32472 (1997).

19Y. Zhang , L. Xie , Q. Meng , T. Jiang , R. Pu , L. Chen and R. Zhang : A novel matrix protein participating in the nacre framework formation of pearl oyster, Pinctada fucata. Comp. Biochem. Physiol. Part B 135, 565 (2003).

20S. Blank , M. Arnold , S. Khoshnavaz , L. Treccani , M. Kuntz , K. Mann , G. Grathwohl and M. Fritz : The nacre protein perlucin nucleates growth of calcium carbonate crystals. J. Microsc. 212, 280 (2003).

21F. Song , A.K. Soh and Y.L. Bai : Structural and mechanical properties of the organic matrix layers of nacre. Biomaterials 24, 3623 (2003).

23B.A. Wustman , D.E. Morse and J.S. Evans : Structural analyses of polyelectrolyte sequence domains within the adhesive elastomeric biomineralization protein lustrin A. Langmuir 18, 9901 (2002).

24S. Weiner and W. Traub : Macromolecules in mollusc shells and their functions in biomineralization. Philos. Trans. R. Soc. London, Series B Bio. Sci. 304, 425 (1984).

25I.M. Weiss , S. Kaufmann , K. Mann and M. Fritz : Purification and characterization of perlucin and perlustrin, two new proteins from the shell of the mollusc Haliotis laevigata Biochem. Biophys. Res. Commun. 267, 17 (2000).

26I.M. Weiss , C. Renner , M.G. Strigl and M. Fritz : A simple and reliable method for the determination and localization of chitin in abalone nacre. Chem. Mater. 14, 3252 (2002).

27L. Pereira-Mouriès , M. Almeida , C. Ribeiro , J. Peduzzi , M-J. Barthélemy , C. Milet and E. Lopez : Soluble silk-like organic matrix in the nacreous layer of the bivalve Pinctada maxima Eur. J. Biochem. 269, 4994 (2002).

28L. Bédouet , M.J. Schuller , F. Marin , C. Milet , E. Lopez and M. Giraud : Soluble proteins of the nacre of the giant oyster Pinctada maxima and of the abalone Haliotis tuberculata: Extraction and partial analysis of nacre proteins. Comp. Biochem. Physiol. Part B: Biochem. Mol. Bio. 128, 389 (2001).

30S. Weiner and W. Traub : X-ray diffraction study of the insoluble organic matrix of mollusk shells. FEBS Lett. 111, 311 (1980).

31S. Weiner , Y. Talmon and W. Traub : Electron diffraction of mollusc shell organic matrices and their relationship to the mineral phase. Int. J. Biol. Macromol. 5, 325 (1983).

32N. Watabe : Studies on shell formation XI. Crystal-matrix relationships in the inner layers of mollusk shells. J. Ultrastruct. Res. 12, 351 (1965).

33A.M. Belcher , X.H. Wu , R.J. Christensen , P.K. Hansma , G.D. Stucky and D.E. Morse : Control of crystal phase switching and orientation by soluble mollusc-shell proteins. Nature 381, 56 (1996).

34R.Z. Wang , H.B. Wen , F.Z. Cui , H.B. Zhang and H.D. Li : Observations of damage morphologies in nacre during deformation and fracture. J. Mater. Sci. 30, 2299 (1995).

36J.D. Currey and J.D. Taylor : The mechanical behavior of some molluscan hard tissues. J. Zool. London 173, 395 (1974).

39B. Ji and H. Gao : A study of fracture mechanisms in biological nano-composites via the virtual internal bond model. Mater. Sci. Eng. A 366, 96 (2004).

43M.T. Hanson : The elastic field for spherical hertzian contact including sliding friction for transverse isotropy. J. Tribology 114, 606 (1992).

45S.S. Sheiko and M. Moller : Visualization of macromolecules: A first step to manipulation and controlled response. Chem. Rev. 101, 4099 (2001).

46D.C. Harris : Quantitative Chemical Analysis, 4th ed. (W. H. Freeman and Company, New York, 1995.).

47E.M. Arruda and M.C. Boyce : A three-dimensional constitutive model for the large stretch behavior of rubber-elastic materials. J. Mech. Phys. Solids 41, 389 (1993).

48J.E. Bischoff , E.M. Arruda and K. Grosh : Orthotropic hyperelasticity in terms of an arbitrary molecular chain model. J. Appl. Mech. 69, 198 (2002).

49J.E. Bischoff , E.M. Arruda and K. Grosh : A microstructurally based orthotropic hyperelastic constitutive law. J. Appl. Mech. 69, 570 (2002).

50J.G. Skedros , R.D. Bloebaum , K.N. Bachus and T.M. Boyce : The meaning of graylevels in backscattered electron images of bone. J. Biomed. Mater. Res. 27, 47 (1993).

51G.E. Lloyd : Atomic number and crystallographic contrast images with the SEM: A review of backscattered electron techniques. Min. Mag. 51, 3 (1987).

52S.P. Kotha , Y. Li and N. Guzelsu : Micromechanical model of nacre tested in tension. J. Mater. Sci. 36, 2001 (2001).

53B.L. Smith , T.E. Schäffer , M. Viani , J.B. Thompson , N.A. Frederick , J. Kindt , A. Belcher , G.D. Stucky , D.E. Morse and P.K. Hansma : Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites. Nature 399, 761 (1999).

54C.G. Kontoyannis and N.V. Vagenas : Calcium carbonate phase analysis using XRD and FT-Raman spectroscopy. Analyst 125, 251 (2000).

56J. Balmain , B. Hannoyer and E. Lopez : Fourier transform infrared spectroscopy (FTIR) and x-ray diffraction analyses of mineral and organic matrix during heating of mother of pearl (nacre) from the shell of the mollusc Pinctada maxima J. Biomed. Mater. Res. 48(5), 749 (1999).

58Q.L. Feng , H.B. Li , F.Z. Cui , H.D. Li and T.N. Kim : Crystal orientation domains found in the single lamina in nacre of the Mytilus edulis shell J. Mater. Sci. Lett. 18, 1547 (1999).

59Q.L. Feng , G. Pu , Y. Pei , F.Z. Cui , H.D. Li and T.N. Kim : Polymorph and morphology of calcium carbonate crystals induced by proteins extracted from mollusk shell. J. Cryst. Growth 216, 459 (2000).

60H. Sturges : The choice of a class interval. J. Am. Statist. Assoc. 21, 65 (1926).

61D.W. Scott : On optimal and data-based histograms. Biometrika 66, 605 (1979).

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