Skip to main content Accesibility Help

Predation versus protection: Fish teeth and scales evaluated by nanoindentation

  • Po-Yu Chen (a1), Jeffrey Schirer (a2), Amanda Simpson (a2), Richard Nay (a2), Yen-Shan Lin (a3), Wen Yang (a4), Maria I. Lopez (a4), Jianan Li (a5), Eugene A. Olevsky (a6) and Marc A. Meyers (a7)...

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.

Corresponding author
a)Address all correspondence to this author. e-mail:
Hide All
1.Meyers, M.A., Chen, P-Y., Lin, A.Y-M., and Seki, Y.: Biological materials: Structure and mechanical properties. Prog. Mater. Sci. 53, 1 (2008).
2.Chen, P-Y., Lin, A.Y-M., Lin, Y-S., Seki, Y., Stokes, A.G., Peyras, J., Olevsky, E.A., Meyers, M.A., and McKittrick, J.: Structure and mechanical properties of selected biological materials. J. Mech. Behav. Biomed. Mater. 1, 208 (2008).
3.Lin, A.Y-M. and Meyers, M.A.: Growth and structure in abalone shell. Mater. Sci. Eng., A 290, 27 (2005).
4.Meyers, M.A., Lin, A.Y-M., Chen, P-Y., and Muyco, J.: Mechanical strength of abalone nacre: Role of the soft organic layer. J. Mech. Behav. Biomed. Mater. 1, 76 (2008).
5.Chen, P-Y., Lin, A.Y-M., McKittrick, J., and Meyers, M.A.: Structure and mechanical properties of crab exoskeletons. Acta Biomater. 4, 587 (2008).
6.Weaver, J.C., Wang, Q., Miserez, A., Tantuccio, A., Stromberg, R., Bozhilov, K.N., Maxwell, P., Nay, R., Heier, S.T., DiMasi, E., and Kisailus, D.: Analysis of an ultra hard magnetic biomineral in chiton radular teeth. Mater. Today 13, 42 (2010).
7.Miserez, A., Schneberk, T., Sun, C., Zok, F.W., and Waite, J.H.: The transition from stiff to compliant materials in squid beaks. Science 318, 1817 (2008).
8.Meyers, M.A., Lin, A.Y-M., Lin, Y-S., Olevsky, E.A., and Georgalis, S.: The cutting edge: Sharp biological materials. JOM 60, 19 (2008).
9.Atkins, T.: The Science and Engineering of Cutting (Butterworth-Heinemann, Oxford, UK, 2009), p. 230.
10.Diamond, J.M.: How great white sharks, saber-toothed cats and solders kill. Nature 322, 773 (1986).
11.Snodgrass, S.M. and Gilbert, P.W.: A shark bite meter, in Sharks, Skates and Rays, edited by Gilbert, P.W., Mathewson, R.F., and Rall, D.P. (The Johns Hopkins University Press, Baltimore, 1967) p. 331.
12.Onozato, H. and Watabe, N.: Studies on fish scale formation and resorption. Cell Tissue Res. 201, 409 (1979).
13.Zylberberg, L. and Nicolas, G.: Ultrastructure of scales in a teleost (Carassius auratus L.) after use of rapid freeze-fixation and freeze-substitution. Cell Tissue Res. 223, 349 (1982).
14.Zylberberg, L., Bereiter-Hahn, J., and Sire, J.Y.: Cytoskeletal organization and collagen orientation in the fish scales. Cell Tissue Res. 253, 597 (1988).
15.Bigi, A., Burghammer, M., Falconi, R., Koch, H.J., Panzavolta, S., and Riekel, C.: Twisted plywood pattern of collagen in teleost scales: An x-ray diffraction investigation. J. Struct. Biol. 136, 137 (2001).
16.Ikoma, T., Kobayashi, H., Tanaka, J., Walsh, D., and Mann, S.: Microstructure, mechanical, and biomimetic properties of fish scales from Pagrus major. J. Struct. Biol. 142, 327 (2003).
17.Bruet, B.J.F., Song, J., Boyce, M.C., and Ortiz, C.: Materials design principles of ancient fish armor. Nat. Mater. 7, 748 (2008).
18.Torres, F.G., Troncoso, O.P., Nakamatsu, J., Grande, C.J., and Gomez, C.M.: Characterization of the nanocomposite laminate structure occurring in fish scales from Arapaima gigas. Mater. Sci. Eng., C 28, 1276 (2008).
19.Song, J., Ortiz, C., and Boyce, M.C.: Threat-protection mechanics of an armored fish. J. Mech. Behav. Biomed. Mater. 4, 699 (2011).
20.Lin, Y-S., Wei, C-T., Olevsky, E.A., and Meyers, M.A.: Mechanical properties and the laminate structure of Arapaima gigas scales. J. Mech. Behav. Biomed. Mater. 4, 1145 (2011).
21.Meyers, M.A., Lin, Y-S., Olevsky, E.A., and Chen, P-Y.: The scales of the Amazon arapaima: Bioinspiration for flexible ceramics. Adv. Biomater. (2011) (accepted).
22.Currey, J.D.: Mechanical properties and adaptations of some less familiar bony tissues. J. Mech. Behav. Biomed. Mater. 3, 357 (2010).
23.Daget, J., Gayet, M., Meunier, F.J., and Sure, J-Y.: Major discoveries on the dermal skeleton of fossil and recent polypteriforms: A review. Fish Fish. 2, 113 (2001).
24.Oliver, 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).
25.Rho, J-Y., Tsui, T.Y., and Pharr, G.M.: Elastic properties of human cortical and trabecular lamellar bone measured by nanoindentation. Biomater. 18, 1325 (1997).
26.Zysset, P.K., Guo, X.E., Hoffler, C.E., Moore, K.E., and Goldstein, S.A.: Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur. J. Biomech. 32, 1005 (1999).
27.Rho, J-Y., Roy, M.E. II, Tsui, T.Y., and Pharr, G.M.: Elastic properties of microstructural components of human bone tissue as measured by nanoindentation. J. Biomed. Mater. Res. 45A, 48 (1999).
28.Hengsberger, S., Kulik, A., and Zysset, P.: Nanoindentation discriminates the elastic properties of individual human bone lamellae under dry and physiological conditions. Bone 30, 178 (2002).
29.Fan, Z. and Rho, J-Y.: Effects of viscoelasticity and time-dependent plasticity on nanoindentation measurements of human cortical bone. J. Biomed. Mater. Res. 67A, 208 (2003).
30.Ebenstein, D.M., Kuo, A., Rodrigo, J.J., Reddi, A.H., Ries, M., and Pruitt, L.: Nanoindentation technique for functional evaluation of cartilage repair tissue. J. Mater. Res. 19, 273 (2004).
31.Franke, O., Durst, K., Maier, V., Göken, M., Birkholz, T., Schneider, H., Hennig, F., and Gelse, K.: Mechanical properties of hyaline and repair cartilage studied by nanoindentation. Acta Biomater. 3, 873 (2007).
32.Franke, O., Göken, M., Meyers, M.A., Durst, K., and Hodge, A.M.: Dynamic nanoindentation of articular porcine cartilage. Mater. Sci. Eng. C 31, 789 (2011).
33.van Meerbeek, B., Willems, G., Celis, J.P., Roos, J.R., Braerm, M., Lanbrechrs, P., and Vanherle, G.: Assessment by nanoindentation of the hardness and elasticity of the resin-dentin bonding area. J. Dent. Res. 72, 1434 (1993).
34.Kinney, J.H., Balooch, M., Marshall, S.J., Marshall, G.W., and Weihs, T.P.: Hardness and Young’s modulus of human peritubular and intertubular dentine. Arch. Oral Biol. 41, 9 (1996).
35.Fong, H., Sarikaya, M., White, S.N., and Snead, M.L.: Nano-mechanical properties profiles across dentin–enamel junction of human incisor teeth. Mater. Sci. Eng., C 7, 119 (2000).
36.Habelitz, S., Marshall, S.J., Marshall, G.W., and Balooch, M.: Mechanical properties of human dental enamel on the nanometre scale. Arch. Oral Biol. 46, 173 (2001).
37.Habelitz, S., Marshall, G.W., Balooch, M., and Marshall, S.J.: Nanoindentation and storage of teeth. J. Biomech. 35, 995 (2002).
38.Kinney, J.H., Marshall, S.J., and Marshall, G.W.: The mechanical properties of human dentin: A critical review and re-evaluation of the dental literature. Crit. Rev. Oral Biol. Med. 14, 13 (2003).
39.Haque, F.: Application of nanoindentation to development of biomedical materials. Surf. Eng. 19, 255 (2003).
40.Ebenstein, D.M. and Pruitt, L.A.: Nanoindentation of biological materials. Nano Today 1, 26 (2006).
41.Angker, L. and Swain, M.V.: Nanoindentation: Application to dental hard tissue investigations. J. Mater. Res. 21, 1893 (2006).
42.Oyen, M.L.: Nanoindentation hardness of mineralized tissues. J. Biomech. 39, 2699 (2006).
43.Franke, O., Göken, M., and Hodge, M.A.: The nanoindentation of soft tissue: Current and developing approaches. JOM 60, 49 (2008).
44.Dickinson, M.: Nanoindentation of biological composites. IOP Conf. Ser.: Mater. Sci. Eng. 4, 012015 (2009).
45.Oyen, M.L.: Nanoindentation of biological and biomimetic materials. Exp. Tech. (2011, in press).
46.Yao, H. and Gao, H.: Multi-scale cohesive laws in hierarchical materials. Int. J. Solids Struct. 45, 3627 (2008).
47.Whitenack, L.B., Sinkins, D.C. Jr., Motta, P.J., Hirai, M., and Kumar, A.: Young’s modulus and hardness of shark tooth biomaterials. Arch. Oral Biol. 55, 203 (2001).
48.Imbeni, V., Kruzic, J.J., Marshall, G.W., Marshall, S.J., and Ritchie, R.O.: The dentin-enamel junction and the fracture of human teeth. Nat. Mater. 4, 229 (2003).
49.Munch, E., Launey, M.E., Alsem, D.H., Saiz, E., Tomsia, A.P., and Ritchie, R.O.: Tough bio-inspired hybrid materials. Science 322, 1515 (2008).
50.Launey, M.E., Munch, E., Alsem, D.H., Barth, H.D., Saiz, E., Tomsia, A.P., and Ritchie, R.O.: Designing highly toughened hybrid composites through nature-inspired hierarchical complexity. Acta Mater. 57, 2919 (2009).
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Journal of Materials Research
  • ISSN: 0884-2914
  • EISSN: 2044-5326
  • URL: /core/journals/journal-of-materials-research
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed