Skip to main content
Log in

Deconvolution of the elastic properties of bivalve shell nanocomposites from direct measurement and finite element analysis

  • Nanomechanics and Testing
  • Article
  • Published:
Journal of Materials Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8

Similar content being viewed by others

References

  1. J.R. Curry: The design of mineralised hard tissues for their mechanical functions. J. Exp. Biol. 202, 3285 (1999).

    Article  Google Scholar 

  2. 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).

    Article  CAS  Google Scholar 

  3. 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).

    Article  CAS  Google Scholar 

  4. 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).

    Article  Google Scholar 

  5. 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.

    Chapter  Google Scholar 

  6. J.W.C. Dunlop and P. Fratzl: Biological composites. Annu. Rev. Mater. Res. 22, 1 (2010).

    Article  CAS  Google Scholar 

  7. 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).

    Article  CAS  Google Scholar 

  8. 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).

    Article  Google Scholar 

  9. D. Kaplan: Mollusc shell structures: Novel design strategies for synthetic materials. Curr. Opin. Solid State Mater. Sci. 3, 232 (1998).

    Article  CAS  Google Scholar 

  10. M. Rousseau: Nacre, a natural biomaterial. In Biomaterials Applications for Nanomedicine, R. Pignatello (ed.) (InTech, Rijeka, Croatia, 2011); p. 281–298.

    Google Scholar 

  11. 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).

    Article  CAS  Google Scholar 

  12. 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).

    Google Scholar 

  13. 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).

    Article  Google Scholar 

  14. J. Taylor and M. Layman: The mechanical properties of bivalve (Mollusca) shell structures. Palaeontology 15, 73 (1972).

    Google Scholar 

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

    Article  Google Scholar 

  16. J.D. Currey: Further studies on the mechanical properties of mollusk shell material. J. Zool. 180, 445–453 (1976).

    Article  Google Scholar 

  17. J.D. Currey: Mechanical properties of mother of pearl in tension. Proc. R. Soc. London, Ser. B 196, 443 (1977).

    Article  Google Scholar 

  18. J.D. Currey: Mechanical properties of mollusc shell. Symp. Soc. Exp. Biol. 34, 75 (1980).

    CAS  Google Scholar 

  19. 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).

    Article  Google Scholar 

  20. 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).

    Article  CAS  Google Scholar 

  21. 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).

    Article  CAS  Google Scholar 

  22. 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).

    Article  CAS  Google Scholar 

  23. K.S. Katti, B. Mohanty, and D.R. Katti: Nanomechanical properties of nacre. J. Mater. Res. 21, 1237 (2006).

    Article  CAS  Google Scholar 

  24. 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).

    Article  CAS  Google Scholar 

  25. K.S. Katti and D.R. Katti: Why is nacre so tough and strong? Mater. Sci. Eng., C 26, 1317 (2006).

    Article  CAS  Google Scholar 

  26. 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).

    Article  CAS  Google Scholar 

  27. 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).

    Article  CAS  Google Scholar 

  28. 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).

    Article  CAS  Google Scholar 

  29. 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).

    Article  CAS  Google Scholar 

  30. D. Scurr and S. Eichhorn: Analysis of local deformation in indented Ensis siliqua mollusk shells using Raman spectroscopy. J. Mater. Res. 21, 3099 (2006).

    Article  CAS  Google Scholar 

  31. X. Li and P. Nardi: Micro/nanomechanical characterization of a natural nanocomposite material—The shell of Pectinidae. Nanotechnology 15, 211 (2004).

    Article  CAS  Google Scholar 

  32. 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).

    Article  CAS  Google Scholar 

  33. 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).

    Article  Google Scholar 

  34. 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).

    Article  CAS  Google Scholar 

  35. 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).

    Article  CAS  Google Scholar 

  36. 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).

    Article  CAS  Google Scholar 

  37. 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).

    Article  CAS  Google Scholar 

  38. 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).

    Article  CAS  Google Scholar 

  39. X. Li, Z-H. Xu, and R. Wang: In situ observation of nanograin rotation and deformation in nacre. Nano Lett. 6, 2301–2304 (2006).

    Article  CAS  Google Scholar 

  40. 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).

    Article  Google Scholar 

  41. 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).

    Article  CAS  Google Scholar 

  42. 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.

    Google Scholar 

  43. 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).

    Article  CAS  Google Scholar 

  44. A.C. Fischer-Cripps: Nanoindentation; Mechanical Engineering Series (Springer, New York, 2011); p 282.

    Book  Google Scholar 

  45. J. Menčík: Uncertainties and errors in nanoindentation. In Nanoindentation in Materials Science, J. Nemecek (ed.) (InTech, Rijeka, Croatia 2012); p. 53–86.

    Google Scholar 

  46. X-Q. Chen, H. Niu, D. Li, and Y. Li: Modeling hardness of polycrystalline materials and bulk metallic glasses. Intermetallics 19, 1275 (2011).

    Article  CAS  Google Scholar 

  47. Online source: Physics modules. Available at: https://www.synopsys.com/simpleware/products/software/physics-modules.html (accessed December, 2016).

Download references

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

Authors

Corresponding author

Correspondence to Michael A. Carpenter.

Supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1557/jmr.2019.159

Navigation