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Predation versus protection: Fish teeth and scales evaluated by nanoindentation

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Abstract

Most biological materials are hierarchically structured composites that often possess exceptional mechanical properties. We show that nanoindentation can be a powerful tool for understanding the structure‑mechanical property relationship of biological materials and illustrate this for fish teeth and scales, not heretofore investigated at the nanoscale. Piranha and shark teeth consist of enameloid and dentin. Nanoindentation measurements show that the reduced modulus and hardness of enameloid are 4‑5 times higher than those of dentin. Arapaima scales are multilayered composites that consist of mineralized collagen fibers. The external layer is more highly mineralized, resulting in a higher modulus and hardness compared with the internal layer. Alligator gar scales are composed of a highly mineralized external ganoin layer and an internal bony layer. Similar design strategies, gradient structures, and a hard external layer backed by a more compliant inner layer are exhibited by fish teeth and scales and seem to fulfill their functional purposes.

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References

  1. 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 

  2. 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 

  3. A.Y-M. Lin and M.A. Meyers: Growth and structure in abalone shell. Mater. Sci. Eng., A 290, 27 (2005).

    Article  CAS  Google Scholar 

  4. M.A. Meyers, A.Y-M. Lin, P-Y. Chen, and J. Muyco: Mechanical strength of abalone nacre: Role of the soft organic layer. J. Mech. Behav. Biomed. Mater. 1, 76 (2008).

    Article  Google Scholar 

  5. P-Y. Chen, A.Y-M. Lin, J. McKittrick, and M.A. Meyers: Structure and mechanical properties of crab exoskeletons. Acta Biomater. 4, 587 (2008).

    Article  Google Scholar 

  6. J.C. Weaver, Q. Wang, A. Miserez, A. Tantuccio, R. Stromberg, K.N. Bozhilov, P. Maxwell, R. Nay, S.T. Heier, E. DiMasi, and D. Kisailus: Analysis of an ultra hard magnetic biomineral in chiton radular teeth. Mater. Today 13, 42 (2010).

    Article  CAS  Google Scholar 

  7. A. Miserez, T. Schneberk, C. Sun, F.W. Zok, and J.H. Waite: The transition from stiff to compliant materials in squid beaks. Science 318, 1817 (2008).

    Google Scholar 

  8. M.A. Meyers, A.Y-M. Lin, Y-S. Lin, E.A. Olevsky, and S. Georgalis: The cutting edge: Sharp biological materials. JOM 60, 19 (2008).

    Article  CAS  Google Scholar 

  9. T. Atkins: The Science and Engineering of Cutting (Butterworth-Heinemann, Oxford, UK, 2009), p. 230.

    Google Scholar 

  10. J.M. Diamond: How great white sharks, saber-toothed cats and solders kill. Nature 322, 773 (1986).

    Article  Google Scholar 

  11. S.M. Snodgrass and P.W. Gilbert: A shark bite meter, in Sharks, Skates and Rays, edited by P.W. Gilbert, R.F. Mathewson, and D.P. Rall (The Johns Hopkins University Press, Baltimore, 1967) p. 331.

    Google Scholar 

  12. H. Onozato and N. Watabe: Studies on fish scale formation and resorption. Cell Tissue Res. 201, 409 (1979).

    Article  CAS  Google Scholar 

  13. L. Zylberberg and G. Nicolas: Ultrastructure of scales in a teleost (Carassius auratus L.) after use of rapid freeze-fixation and freeze-substitution. Cell Tissue Res. 223, 349 (1982).

    Article  CAS  Google Scholar 

  14. L. Zylberberg, J. Bereiter-Hahn, and J.Y. Sire: Cytoskeletal organization and collagen orientation in the fish scales. Cell Tissue Res. 253, 597 (1988).

    Article  CAS  Google Scholar 

  15. A. Bigi, M. Burghammer, R. Falconi, H.J. Koch, S. Panzavolta, and C. Riekel: Twisted plywood pattern of collagen in teleost scales: An x-ray diffraction investigation. J. Struct. Biol. 136, 137 (2001).

    Article  CAS  Google Scholar 

  16. T. Ikoma, H. Kobayashi, J. Tanaka, D. Walsh, and S. Mann: Microstructure, mechanical, and biomimetic properties of fish scales from Pagrus major. J. Struct. Biol. 142, 327 (2003).

    Article  Google Scholar 

  17. B.J.F. Bruet, J. Song, M.C. Boyce, and C. Ortiz: Materials design principles of ancient fish armor. Nat. Mater. 7, 748 (2008).

    Article  CAS  Google Scholar 

  18. F.G. Torres, O.P. Troncoso, J. Nakamatsu, C.J. Grande, and C.M. Gomez: Characterization of the nanocomposite laminate structure occurring in fish scales from Arapaima gigas. Mater. Sci. Eng., C 28, 1276 (2008).

    Article  CAS  Google Scholar 

  19. J. Song, C. Ortiz, and M.C. Boyce: Threat-protection mechanics of an armored fish. J. Mech. Behav. Biomed. Mater. 4, 699 (2011).

    Article  Google Scholar 

  20. Y-S. Lin, C-T. Wei, E.A. Olevsky, and M.A. Meyers: Mechanical properties and the laminate structure of Arapaima gigas scales. J. Mech. Behav. Biomed. Mater. 4, 1145 (2011).

    Article  CAS  Google Scholar 

  21. M.A. Meyers, Y-S. Lin, E.A. Olevsky, and P-Y. Chen: The scales of the Amazon arapaima: Bioinspiration for flexible ceramics. Adv. Biomater. (2011) (accepted).

    Google Scholar 

  22. J.D. Currey: Mechanical properties and adaptations of some less familiar bony tissues. J. Mech. Behav. Biomed. Mater. 3, 357 (2010).

    Article  CAS  Google Scholar 

  23. J. Daget, M. Gayet, F.J. Meunier, and J-Y. Sure: Major discoveries on the dermal skeleton of fossil and recent polypteriforms: A review. Fish Fish. 2, 113 (2001).

    Article  Google Scholar 

  24. W.C. Oliver and G.M. 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 

  25. J-Y. Rho, T.Y. Tsui, and G.M. Pharr: Elastic properties of human cortical and trabecular lamellar bone measured by nanoindentation. Biomater. 18, 1325 (1997).

    Article  CAS  Google Scholar 

  26. P.K. Zysset, X.E. Guo, C.E. Hoffler, K.E. Moore, and S.A. Goldstein: Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur. J. Biomech. 32, 1005 (1999).

    Article  CAS  Google Scholar 

  27. J-Y. Rho, M.E. Roy II, T.Y. Tsui, and G.M. Pharr: Elastic properties of microstructural components of human bone tissue as measured by nanoindentation. J. Biomed. Mater. Res. 45A, 48 (1999).

    Article  Google Scholar 

  28. S. Hengsberger, A. Kulik, and P. Zysset: Nanoindentation discriminates the elastic properties of individual human bone lamellae under dry and physiological conditions. Bone 30, 178 (2002).

    Article  CAS  Google Scholar 

  29. Z. Fan and J-Y. Rho: Effects of viscoelasticity and time-dependent plasticity on nanoindentation measurements of human cortical bone. J. Biomed. Mater. Res. 67A, 208 (2003).

    Article  CAS  Google Scholar 

  30. D.M. Ebenstein, A. Kuo, J.J. Rodrigo, A.H. Reddi, M. Ries, and L. Pruitt: Nanoindentation technique for functional evaluation of cartilage repair tissue. J. Mater. Res. 19, 273 (2004).

    Article  CAS  Google Scholar 

  31. O. Franke, K. Durst, V. Maier, M. Göken, T. Birkholz, H. Schneider, F. Hennig, and K. Gelse: Mechanical properties of hyaline and repair cartilage studied by nanoindentation. Acta Biomater. 3, 873 (2007).

    Article  CAS  Google Scholar 

  32. O. Franke, M. Göken, M.A. Meyers, K. Durst, and A.M. Hodge: Dynamic nanoindentation of articular porcine cartilage. Mater. Sci. Eng. C 31, 789 (2011).

    Article  CAS  Google Scholar 

  33. B. van Meerbeek, G. Willems, J.P. Celis, J.R. Roos, M. Braerm, P. Lanbrechrs, and G. Vanherle: Assessment by nanoindentation of the hardness and elasticity of the resin-dentin bonding area. J. Dent. Res. 72, 1434 (1993).

    Article  Google Scholar 

  34. J.H. Kinney, M. Balooch, S.J. Marshall, G.W. Marshall, and T.P. Weihs: Hardness and Young’s modulus of human peritubular and intertubular dentine. Arch. Oral Biol. 41, 9 (1996).

    Article  CAS  Google Scholar 

  35. H. Fong, M. Sarikaya, S.N. White, and M.L. Snead: Nano-mechanical properties profiles across dentin–enamel junction of human incisor teeth. Mater. Sci. Eng., C 7, 119 (2000).

    Article  Google Scholar 

  36. S. Habelitz, S.J. Marshall, G.W. Marshall, and M. Balooch: Mechanical properties of human dental enamel on the nanometre scale. Arch. Oral Biol. 46, 173 (2001).

    Article  CAS  Google Scholar 

  37. S. Habelitz, G.W. Marshall, M. Balooch, and S.J. Marshall: Nanoindentation and storage of teeth. J. Biomech. 35, 995 (2002).

    Article  Google Scholar 

  38. J.H. Kinney, S.J. Marshall, and G.W. Marshall: The mechanical properties of human dentin: A critical review and re-evaluation of the dental literature. Crit. Rev. Oral Biol. Med. 14, 13 (2003).

    Article  CAS  Google Scholar 

  39. F. Haque: Application of nanoindentation to development of biomedical materials. Surf. Eng. 19, 255 (2003).

    Article  Google Scholar 

  40. D.M. Ebenstein and L.A. Pruitt: Nanoindentation of biological materials. Nano Today 1, 26 (2006).

    Article  Google Scholar 

  41. L. Angker and M.V. Swain: Nanoindentation: Application to dental hard tissue investigations. J. Mater. Res. 21, 1893 (2006).

    Article  CAS  Google Scholar 

  42. M.L. Oyen: Nanoindentation hardness of mineralized tissues. J. Biomech. 39, 2699 (2006).

    Article  Google Scholar 

  43. O. Franke, M. Göken, and M.A. Hodge: The nanoindentation of soft tissue: Current and developing approaches. JOM 60, 49 (2008).

    Article  CAS  Google Scholar 

  44. M. Dickinson: Nanoindentation of biological composites. IOP Conf. Ser.: Mater. Sci. Eng. 4, 012015 (2009).

    Article  Google Scholar 

  45. M.L. Oyen: Nanoindentation of biological and biomimetic materials. Exp. Tech. (2011, in press).

    Google Scholar 

  46. H. Yao and H. Gao: Multi-scale cohesive laws in hierarchical materials. Int. J. Solids Struct. 45, 3627 (2008).

    Article  Google Scholar 

  47. L.B. Whitenack, D.C. Sinkins Jr., P.J. Motta, M. Hirai, and A. Kumar: Young’s modulus and hardness of shark tooth biomaterials. Arch. Oral Biol. 55, 203 (2001).

    Article  CAS  Google Scholar 

  48. V. Imbeni, J.J. Kruzic, G.W. Marshall, S.J. Marshall, and R.O. Ritchie: The dentin-enamel junction and the fracture of human teeth. Nat. Mater. 4, 229 (2003).

    Article  CAS  Google Scholar 

  49. E. Munch, M.E. Launey, D.H. Alsem, E. Saiz, A.P. Tomsia, and R.O. Ritchie: Tough bio-inspired hybrid materials. Science 322, 1515 (2008).

    Article  CAS  Google Scholar 

  50. M.E. Launey, E. Munch, D.H. Alsem, H.D. Barth, E. Saiz, A.P. Tomsia, and R.O. Ritchie: Designing highly toughened hybrid composites through nature-inspired hierarchical complexity. Acta Mater. 57, 2919 (2009).

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Ryan Anderson (CalIT2) for the help on the scanning electron microscopy. Valuable insights and discussion with Ms. Dianne Ulery are greatly appreciated. She kindly donated the alligator gar scales for research purposes. We thank Professor Joanna McKittrick for her enthusiastic support of this project. This research is funded by the National Science Foundation, Division of Materials Research, Biomaterials Program (DMR 0510138) and Ceramics Program (DMR 1006931).

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Correspondence to Po-Yu Chen.

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Chen, PY., Schirer, J., Simpson, A. et al. Predation versus protection: Fish teeth and scales evaluated by nanoindentation. Journal of Materials Research 27, 100–112 (2012). https://doi.org/10.1557/jmr.2011.332

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  • DOI: https://doi.org/10.1557/jmr.2011.332

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