Hostname: page-component-7c8c6479df-94d59 Total loading time: 0 Render date: 2024-03-26T13:17:09.626Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  03 March 2011

B.J.F. Bruet
Affiliation:
Department of Materials Science and Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139
H.J. Qi
Affiliation:
Department of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139
M.C. Boyce
Affiliation:
Department of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139
R. Panas
Affiliation:
Department of Materials Science and Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139
K. Tai
Affiliation:
Department of Materials Science and Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139
L. Frick
Affiliation:
Department of Materials Science and Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139
C. Ortiz*
Affiliation:
Department of Materials Science and Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139
*
b) Address all correspondence to this author. e-mail: cortiz@mit.edu
Get access

Abstract

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.

Type
Articles
Copyright
Copyright © Materials Research Society 2005

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

1Jackson, A.P., Vincent, J.F.V. and Turner, R.M.: The mechanical design of nacre. Proc. R. Soc. London B Biol. Sci. 234, 415 (1988).Google Scholar
2Weiner, S. and Addadi, L.: Design strategies in mineralized biological materials. J. Mater. Chem. 7, 689 (1997).CrossRefGoogle Scholar
3Wang, R.Z., Suo, Z., Evans, A.G., Yao, N. and Aksay, I.A.: Deformation mechanisms in nacre. J. Mater. Res. 16, 2485 (2001).CrossRefGoogle Scholar
4Menig, R., Meyers, M.H., Meyers, M.A. and Vecchio, K.S.: Quasi-static and dynamic mechanical response of Haliotis rufescens (abalone) shells. Acta Mater. 48, 2383 (2000).CrossRefGoogle Scholar
5Jackson, A.P., Vincent, J.F.V. and Turner, R.M.: Comparison of nacre with other ceramic composites. J. Mater. Sci., 25, 3173 (1990).CrossRefGoogle Scholar
6Currey, J.D.: Mechanical properties of mother of pearl in tension. Proc. R. Soc. London B Biol. Sci. 196(1125), 443 (1977).Google Scholar
7Erban, H.K.: On the structure and growth of the nacreous tablets in gastropods. Biomineralisation 7, 14 (1974).Google Scholar
8Taylor, J.D., Kennedy, W.J. and Hall, A.: Shell structure and minerology of the bivalvia: Introduction Nuculacea-Trigonacea. Bull. Brit. Museum Natural. History Zool. Suppl. 3, 1 (1969).Google Scholar
9Bevan, D.J.M., Rossmanith, E., Mylrea, D.K., Ness, S.E., Taylor, M.R. and Cuff, C.: On the structure of aragonite— Lawrence Bragg revisited. Acta Crystallogr. B. Struct. Sci. B 58, 448 (2002).CrossRefGoogle ScholarPubMed
10Mutvei, H.: Ultrastructural characteristics of the nacre in some gastropods. Zool. Scr. 7, 287 (1978).CrossRefGoogle Scholar
11Li, X., Chang, W-C., Chao, Y.J., Wang, R. and Chang, M.: Nanoscale structural and mechanical characterization of a natural nanocomposite material: The shell of red abalone. Nano Lett. 4, 613 (2004).CrossRefGoogle Scholar
12Bevelander, G. and Nakahara, H.: An electron microscope study of the formation of the nacreous layer in the shell of certain bivalve molluscs. Calc. Tiss. Res. 3, 84 (1969).CrossRefGoogle ScholarPubMed
13Wada, K.: Nucleation and growth of aragonite crystals in the nacre of some bivalve molluscs. Biomineralisation 6, 141 (1972).Google Scholar
14Mutvei, H.: On the internal structures of the nacreous tablets in molluscan shells. Scanning Electron Microsc. 2, 457 (1979).Google Scholar
15Schäffer, T.E., Ionescu-Zanetti, C., Proksch, R., Fritz, M., Walters, D.A., Almqvist, N., Zaremba, C.M., Belcher, A.M., Smith, B.L., Stucky, G.D., Morse, D.E. and Hansma, P.K.: Does abalone nacre form by heteroepitaxial nucleation or by growth through mineral bridges? Chem. Mater. 9, 1731 (1997).CrossRefGoogle Scholar
16Manne, S., Zaremba, C.M., Giles, R., Huggins, L., Walters, D.A., Belcher, A., Morse, D.E., Stucky, G.D., Didymus, J.M., Mann, S. and Hansma, P.K.: Atomic force microscopy of the nacreous layer in mollusc shells. Proc. R. Soc. London B Bio. Sci. 256, 17 (1994).Google Scholar
17Mutvei, H.: Ultrastructural studies on cephalopod shells, Part 1: The septa and siphonal tube in Nautilus. Bull. Geol. Inst. Univer. Upsala (N.S.) 3, 237 (1972).Google Scholar
18Shen, X., Belcher, A.M., Hansma, P.K., Stucky, G.D. and Morse, D.E.: Molecular cloning and characterization of lustrin A, a matrix protein from shell and pearl nacre of Haliotis rufescens J. Bio. Chem. 272, 32472 (1997).CrossRefGoogle ScholarPubMed
19Zhang, Y., Xie, L., Meng, Q., Jiang, T., Pu, R., Chen, L. and Zhang, R.: A novel matrix protein participating in the nacre framework formation of pearl oyster, Pinctada fucata. Comp. Biochem. Physiol. Part B 135, 565 (2003).CrossRefGoogle ScholarPubMed
20Blank, S., Arnold, M., Khoshnavaz, S., Treccani, L., Kuntz, M., Mann, K., Grathwohl, G. and Fritz, M.: The nacre protein perlucin nucleates growth of calcium carbonate crystals. J. Microsc. 212, 280 (2003).CrossRefGoogle ScholarPubMed
21Song, F., Soh, A.K. and Bai, Y.L.: Structural and mechanical properties of the organic matrix layers of nacre. Biomaterials 24, 3623 (2003).CrossRefGoogle ScholarPubMed
22Song, F., Zhang, X.H. and Bai, Y.L.: Microstructure and characteristics in the organic matrix layers of nacre. J. Mater. Res. 17, 1567 (2002).CrossRefGoogle Scholar
23Wustman, B.A., Morse, D.E. and Evans, J.S.: Structural analyses of polyelectrolyte sequence domains within the adhesive elastomeric biomineralization protein lustrin A. Langmuir 18, 9901 (2002).CrossRefGoogle Scholar
24Weiner, S. and Traub, W.: Macromolecules in mollusc shells and their functions in biomineralization. Philos. Trans. R. Soc. London, Series B Bio. Sci. 304, 425 (1984).Google Scholar
25Weiss, I.M., Kaufmann, S., Mann, K. and Fritz, M.: 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).CrossRefGoogle ScholarPubMed
26Weiss, I.M., Renner, C., Strigl, M.G. and Fritz, M.: A simple and reliable method for the determination and localization of chitin in abalone nacre. Chem. Mater. 14, 3252 (2002).CrossRefGoogle Scholar
27Pereira-Mouriès, L., Almeida, M., Ribeiro, C., Peduzzi, J., Barthélemy, M-J., Milet, C. and Lopez, E.: Soluble silk-like organic matrix in the nacreous layer of the bivalve Pinctada maxima Eur. J. Biochem. 269, 4994 (2002).CrossRefGoogle ScholarPubMed
28Bédouet, L., Schuller, M.J., Marin, F., Milet, C., Lopez, E. and Giraud, M.: 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).CrossRefGoogle ScholarPubMed
29Bowen, C.E. and Tang, H.: Conchiolin-protein in aragonite shells of mollusks. Comp. Biochem. Physiol. Part A: Phys. 115A, 269 (1996).CrossRefGoogle Scholar
30Weiner, S. and Traub, W.: X-ray diffraction study of the insoluble organic matrix of mollusk shells. FEBS Lett. 111, 311 (1980).CrossRefGoogle Scholar
31Weiner, S., Talmon, Y. and Traub, W.: Electron diffraction of mollusc shell organic matrices and their relationship to the mineral phase. Int. J. Biol. Macromol. 5, 325 (1983).CrossRefGoogle Scholar
32Watabe, N.: Studies on shell formation XI. Crystal-matrix relationships in the inner layers of mollusk shells. J. Ultrastruct. Res. 12, 351 (1965).CrossRefGoogle ScholarPubMed
33Belcher, A.M., Wu, X.H., Christensen, R.J., Hansma, P.K., Stucky, G.D. and Morse, D.E.: Control of crystal phase switching and orientation by soluble mollusc-shell proteins. Nature 381, 56 (1996).CrossRefGoogle Scholar
34Wang, R.Z., Wen, H.B., Cui, F.Z., Zhang, H.B. and Li, H.D.: Observations of damage morphologies in nacre during deformation and fracture. J. Mater. Sci. 30, 2299 (1995).CrossRefGoogle Scholar
35Handbook of Elastic Properties of Solids, Liquids and Gases, edited by Levy, M., Bass, H., Stern, R., Every, A.G., and Sachse, W. (Academic, San Diego, CA, 2001).Google Scholar
36Currey, J.D. and Taylor, J.D.: The mechanical behavior of some molluscan hard tissues. J. Zool. London 173, 395 (1974).CrossRefGoogle Scholar
37Evans, A.G., Suo, Z., Wang, R.Z., Aksay, I.A., He, M.Y. and Hutchinson, J.W.: Model for the robust mechanical behavior of nacre. J. Mater. Res. 16, 2475 (2001).CrossRefGoogle Scholar
38Katti, D.R., Pradhan, S.M. and Katti, K.S.: Modeling the organic-inorganic interfacial nanoasperities in a model bio-nanocomposite, nacre. Rev. Adv. Mater. Sci. 6, 162 (2004).Google Scholar
39Ji, B. and Gao, H.: A study of fracture mechanisms in biological nano-composites via the virtual internal bond model. Mater. Sci. Eng. A 366, 96 (2004).CrossRefGoogle Scholar
40Qi, H.J., Bruet, B.J.F., Palmer, J.S., Ortiz, C. and Boyce, M.C. Micromechanics and macromechanics of the tensile deformation of nacre, in Mechanics of Biological Tissues, Proceedings of International Union of Theoretical and Applied Mechanics (IUTAM), edited by Holzapfel, G.A. and Ogden, R.W. (Springer Verlag, Graz, Austria, 2005), p. 175.Google Scholar
41Qi, H.J., Ortiz, C. and Boyce, M.C. Protein forced unfolding and its effects on the finite deformation stress-strain behavior of biomacromolecular solids, in Structure and Mechanical Behavior of Biological Materials, edited by Fratzl, P., Landis, W.J., Wang, R., and Silver, F.H. (Mater. Res. Soc. Symp. Proc., 874, Warrendale, PA, 2005), L4.31.Google Scholar
42Barthelat, F. and Espinosa, H.D.: Elastic properties of nacre aragonite tablets, presented at the SEM Annual Conference and Exposition on Experimental and Applied Mechanics, Session 68, Paper 187, Charlotte, North Carolina, 2003; and F. Barthelat and H.D. Espinosa: Mechanical properties of nacre constituents: An inverse method approach, in Mechanical Properties of Bioinspired and Biological Materials, edited by Viney, C., Katti, K., Ulm, F-J., and Hellmich, C. (Mater. Res. Soc. Symp. Proc. 844, Warrendale, PA, 2005), Y.7.5.1, p. 67.Google Scholar
43Hanson, M.T.: The elastic field for spherical hertzian contact including sliding friction for transverse isotropy. J. Tribology 114, 606 (1992).CrossRefGoogle Scholar
44Oliver, W.C. and Pharr, G.M.: An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J. Mater. Res. 7, 1564 (1992).CrossRefGoogle Scholar
45Sheiko, S.S. and Moller, M.: Visualization of macromolecules: A first step to manipulation and controlled response. Chem. Rev. 101, 4099 (2001).CrossRefGoogle ScholarPubMed
46Harris, D.C.: Quantitative Chemical Analysis, 4th ed. (W. H. Freeman and Company, New York, 1995.).Google Scholar
47Arruda, E.M. and Boyce, M.C.: A three-dimensional constitutive model for the large stretch behavior of rubber-elastic materials. J. Mech. Phys. Solids 41, 389 (1993).CrossRefGoogle Scholar
48Bischoff, J.E., Arruda, E.M. and Grosh, K.: Orthotropic hyperelasticity in terms of an arbitrary molecular chain model. J. Appl. Mech. 69, 198 (2002).CrossRefGoogle Scholar
49Bischoff, J.E., Arruda, E.M. and Grosh, K.: A microstructurally based orthotropic hyperelastic constitutive law. J. Appl. Mech. 69, 570 (2002).CrossRefGoogle Scholar
50Skedros, J.G., Bloebaum, R.D., Bachus, K.N. and Boyce, T.M.: The meaning of graylevels in backscattered electron images of bone. J. Biomed. Mater. Res. 27, 47 (1993).CrossRefGoogle ScholarPubMed
51Lloyd, G.E.: Atomic number and crystallographic contrast images with the SEM: A review of backscattered electron techniques. Min. Mag. 51, 3 (1987).CrossRefGoogle Scholar
52Kotha, S.P., Li, Y. and Guzelsu, N.: Micromechanical model of nacre tested in tension. J. Mater. Sci. 36, 2001 (2001).CrossRefGoogle Scholar
53Smith, B.L., Schäffer, T.E., Viani, M., Thompson, J.B., Frederick, N.A., Kindt, J., Belcher, A., Stucky, G.D., Morse, D.E. and Hansma, P.K.: Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites. Nature 399, 761 (1999).CrossRefGoogle Scholar
54Kontoyannis, C.G. and Vagenas, N.V.: Calcium carbonate phase analysis using XRD and FT-Raman spectroscopy. Analyst 125, 251 (2000).CrossRefGoogle Scholar
55 Power Diffraction File (PDF) 00-041-1475 (International Centre for Diffraction Data; Newtown Square, PA).Google Scholar
56Balmain, J., Hannoyer, B. and Lopez, E.: 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).3.0.CO;2-P>CrossRefGoogle ScholarPubMed
57Feng, Q.L., Su, X.W., Cui, F.Z. and Li, H.D.: Crystallographic orientation domains of flat tablets in nacre. Biomimetics 3, 159 (1995).Google Scholar
58Feng, Q.L., Li, H.B., Cui, F.Z., Li, H.D. and Kim, T.N.: Crystal orientation domains found in the single lamina in nacre of the Mytilus edulis shell J. Mater. Sci. Lett. 18, 1547 (1999).CrossRefGoogle Scholar
59Feng, Q.L., Pu, G., Pei, Y., Cui, F.Z., Li, H.D. and Kim, T.N.: Polymorph and morphology of calcium carbonate crystals induced by proteins extracted from mollusk shell. J. Cryst. Growth 216, 459 (2000).CrossRefGoogle Scholar
60Sturges, H.: The choice of a class interval. J. Am. Statist. Assoc. 21, 65 (1926).CrossRefGoogle Scholar
61Scott, D.W.: On optimal and data-based histograms. Biometrika 66, 605 (1979).CrossRefGoogle Scholar