Abstract
A new protocol has been devised for determining elastic properties of natural biocomposites in the form of bivalve shells under wet and dry conditions. Four-point bending on shell slices of Mytilus edulis, Ensis siliqua, and Pecten maximus give generally lower and more reliable values of Young’s modulus, E, than those in the literature from three-point bending, due to the more even distribution of strain. Finite element analysis of the prismatic microstructure of Pinna nobilis, obtained by X-ray tomography, shows that values of E ≈ 20 GPa can be understood in terms of the real microstructure containing a small proportion of organic matrix phase with E ≈ 1 GPa and a dominant proportion of calcite with E ≈ 90 GPa. Higher values of E obtained by nanoindentation give results which are biased toward the properties of the carbonate phase rather than of the biocomposite as a whole.
Similar content being viewed by others
References
J.R. Curry: The design of mineralised hard tissues for their mechanical functions. J. Exp. Biol. 202, 3285 (1999).
M.A. Meyers, A.Y.M. Lin, Y. Seki, P-Y. Chen, B.K. Kad, and S. Bodde: Structural biological composites: An overview. JOM 58, 35 (2006).
M.A. Meyers, P-Y. Chen, A.Y.M. Lin, and Y. Seki: Biological materials: Structure and mechanical properties. Prog. Mater. Sci. 53, 1 (2008).
P-Y. Chen, A.Y.M. Lin, Y-S. Lin, Y. Seki, A.G. Stokes, J. Peyras, E.A. Olevsky, M.A. Meyers, and J. McKittrick: Structure and mechanical properties of selected biological materials. J. Mech. Behav. Biomed. Mater. 1, 208 (2008).
J. Barthelat, J.E. Rim, and H.D. Espinosa: A review on the structure and mechanical properties of mollusk shells—Perspectives on synthetic biomimetic materials. In Applied Scanning Probe Methods XIII: Biomimetics and Industrial Applications, B. Bhushan, H. Fuchs (eds.) (Springer, Switzerland, 2009); p. 17–44.
J.W.C. Dunlop and P. Fratzl: Biological composites. Annu. Rev. Mater. Res. 22, 1 (2010).
H. Ehrlich, P. Simon, W. Carrillo-Cabrera, V.V. Bazhenov, J.P. Botting, M. Ilan, A.V. Ereskovsky, G. Muricy, H. Worch, A. Mensch, R. Born, A. Springer, K. Kummer, D.V. Vyalikh, S.L. Molodtsov, D. Kurek, M. Kammer, S. Paasch, and E. Brunner: Insights into chemistry of biological materials: Newly discovered silica-aragonite-chitin biocomposites in demosponges. Chem. Mater. 22, 1462 (2010).
R. Bieler, P.M. Mikkelsen, T.M. Collins, E.A. Glover, V.L. González, D.L. Graf, E.M. Harper, J. Healy, G.Y. Kawauchi, P.P. Sharma, S. Staubach, E.E. Strong, J.D. Taylor, I. Tëmkin, J.D. Zardus, S. Clark, A. Guzmán, E. McIntyre, P. Sharp, and G. Giribet: Investigating the Bivalve Tree of Life—An exemplar-based approach combining molecular and novel morphological characters. Invertebr. Syst. 28, 32 (2014).
D. Kaplan: Mollusc shell structures: Novel design strategies for synthetic materials. Curr. Opin. Solid State Mater. Sci. 3, 232 (1998).
M. Rousseau: Nacre, a natural biomaterial. In Biomaterials Applications for Nanomedicine, R. Pignatello (ed.) (InTech, Rijeka, Croatia, 2011); p. 281–298.
Y-W. Kim, J.J. Kim, Y.H. Kim, and J.Y. Rho: Effects of organic matrix proteins on the interfacial structure at the bone–biocompatible nacre interface in vitro. Biomaterials 23, 2089 (2002).
J.D. Taylor, W.J. Kennedy, and A. Hall: The shell structure and mineralogy of the Bivalvia. Introduction, nuculacea–trigonacea. Bull. Br. Mus. (Nat. Hist.) Zool. 3, 1 (1969).
J.D. Taylor, W.J. Kennedy, and A. Hall: The shell structure and mineralogy of the Bivalvia. II. Lucinacea–Clavagellacea, conclusions. Bull. Br. Mus. (Nat. Hist.) Zool. Suppl. 22, 253 (1973).
J. Taylor and M. Layman: The mechanical properties of bivalve (Mollusca) shell structures. Palaeontology 15, 73 (1972).
J.D. Currey and J.D. Taylor: The mechanical behaviour of some molluscan hard tissues. J. Zool. 173, 395 (1974).
J.D. Currey: Further studies on the mechanical properties of mollusk shell material. J. Zool. 180, 445–453 (1976).
J.D. Currey: Mechanical properties of mother of pearl in tension. Proc. R. Soc. London, Ser. B 196, 443 (1977).
J.D. Currey: Mechanical properties of mollusc shell. Symp. Soc. Exp. Biol. 34, 75 (1980).
A.P. Jackson, J.F.V. Vincent, and R.M. Turner: The mechanical design of nacre. Proc. R. Soc. London, Ser. B 234, 415 (1988).
D.R. Katti and K.S. Katti: Modeling microarchitecture and mechanical behavior of nacre using 3D finite element techniques part I elastic properties. J. Mater. Sci. 36, 1411 (2001).
D.R. Katti, K.S. Katti, J.M. Sopp, and M. Sarikaya: 3D finite element modeling of mechanical response in nacre-based hybrid nanocomposites. Comput. Theor. Polym. Sci. 11, 397 (2001).
K. Katti, D.R. Katti, J. Tang, S. Pradhan, and M. Sarikaya: Modeling mechanical responses in a laminated biocomposite part II nonlinear responses and nuances of nanostructure. J. Mater. Sci. 40, 1749 (2005).
K.S. Katti, B. Mohanty, and D.R. Katti: Nanomechanical properties of nacre. J. Mater. Res. 21, 1237 (2006).
H. Tang, F. Barthelat, and H.D. Espinosa: An elasto-viscoplastic interface model for investigating the constitutive behavior of nacre. J. Mech. Phys. Solids 55, 1410 (2007).
K.S. Katti and D.R. Katti: Why is nacre so tough and strong? Mater. Sci. Eng., C 26, 1317 (2006).
J. 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, 749 (1999).
P. Stempflé, O. Pantale, M. Rousseau, E. Lopez, and X. Bourrat: Mechanical properties of the elemental nanocomponents of nacre structure. Mater. Sci. Eng., C 30, 715 (2010).
F. Barthelat, C.M. Li, C. Comi, and H.D. Espinosa: Mechanical properties of nacre constituents and their impact on mechanical performance. J. Mater. Res. 21, 1977 (2006).
C. Bignardi, M. Petraroli, and N.M. Pugno: Nanoindentations on conch shells of Gastropoda and Bivalvia molluscs reveal anisotropic evolution against external attacks. J. Nanosci. Nanotechnol. 10, 6453 (2010).
D. Scurr and S. Eichhorn: Analysis of local deformation in indented Ensis siliqua mollusk shells using Raman spectroscopy. J. Mater. Res. 21, 3099 (2006).
X. Li and P. Nardi: Micro/nanomechanical characterization of a natural nanocomposite material—The shell of Pectinidae. Nanotechnology 15, 211 (2004).
F.D. Fleischli, M. Dietiker, C. Borgia, and R. Spolenak: The influence of internal length scales on mechanical properties in natural nanocomposites: A comparative study on inner layers of seashells. Acta Biomater. 4, 1694 (2008).
F. Wählisch, N.J. Peter, O.T. Abad, M.V. Oliveira, A.S. Schneider, W. Schmahl, E. Griesshaber, and R. Bennewitz: Surviving the surf: The tribomechanical properties of the periostracum of Mytilus sp. Acta Biomater. 10, 3978 (2014).
H-M. Ji and X-W. Li: Microstructural characteristic and its relation to mechanical properties of Clinocardium californiense shell. J. Am. Ceram. Soc. 97, 3991 (2014).
C-C. Chen, C-C. Lin, L-G. Liu, S.V. Sinogeikin, and J.D. Bass: Elasticity of single-crystal calcite and rhodochrosite by Brillouin spectroscopy. Am. Mineral. 86, 1525–1529 (2001).
L-G. Liu, C-C. Chen, C-C. Lin, and Y-J. Yang: Elasticity of single-crystal aragonite by Brillouin spectroscopy. Phys. Chem. Miner. 32, 97 (2005).
X. Li, W-C. Chang, Y.J. Chao, R. Wang, and M. Chang: Nanoscale structural and mechanical characterisation of a natural nanocomposite material: The shell of red abalone. Nano Lett. 4, 613 (2004).
M. Rousseau, E. Lopez, P. Stempflé, M. Brendlé, L. Franke, A. Guette, R. Naslain, and X. Bourrat: Multiscale structure of sheet nacre. Biomaterials 26, 6254 (2005).
X. Li, Z-H. Xu, and R. Wang: In situ observation of nanograin rotation and deformation in nacre. Nano Lett. 6, 2301–2304 (2006).
E.M. Harper, A. Checa, and A. Rodríguez-Navarro: Organization and mode of secretion of the granular prismatic microstructure of Entodesma navicula (Bivalvia: Mollusca). Acta Zool. 90, 132 (2009).
W. Oliver and G. Pharr: An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J. Mater. Res. 7, 1564 (1992).
F. Barthelat and H.D. Espinosa: Mechanical properties of nacre constituents: An inverse method approach. In Mechanical Properties of Bioinspired and Biological Materials, C. Viney (ed.); Materials Research Society Symposium Proceedings, Vol. 844 (Warrendale, Pennsylvania, 2005); p. 67–78.
K.W. Siu and A.H.W. Ngan: The continuous stiffness measurement technique in nanoindentation intrinsically modifies the strength of the sample. Philos. Mag. 93, 449 (2013).
A.C. Fischer-Cripps: Nanoindentation; Mechanical Engineering Series (Springer, New York, 2011); p 282.
J. Menčík: Uncertainties and errors in nanoindentation. In Nanoindentation in Materials Science, J. Nemecek (ed.) (InTech, Rijeka, Croatia 2012); p. 53–86.
X-Q. Chen, H. Niu, D. Li, and Y. Li: Modeling hardness of polycrystalline materials and bulk metallic glasses. Intermetallics 19, 1275 (2011).
Online source: Physics modules. Available at: https://www.synopsys.com/simpleware/products/software/physics-modules.html (accessed December, 2016).
Acknowledgments
We thank Andrew Rayment for help with nanoindentation and four-point bending, Gray Williams, Director of the Swire Institute of Marine Sciences (SWIMS) and his student Camilla Camponati for collecting and sending the Saccostrea cucullata specimens from Hong Kong, and Iris Hendriks, from the Mediterranean Institute for Advanced Studies (IMEDEA), for collecting and sending Pinna nobilis specimens from Mallorca. These were collected from spat collectors under a permit granted by the Government of the Balearic Islands.
Author information
Authors and Affiliations
Corresponding author
Supplementary material
Rights and permissions
About this article
Cite this article
O’Toole-Howes, M., Ingleby, R., Mertesdorf, M. et al. Deconvolution of the elastic properties of bivalve shell nanocomposites from direct measurement and finite element analysis. Journal of Materials Research 34, 2869–2880 (2019). https://doi.org/10.1557/jmr.2019.159
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1557/jmr.2019.159