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Predation versus protection: Fish teeth and scales evaluated by nanoindentation

Published online by Cambridge University Press:  04 November 2011

Po-Yu Chen ,
Jeffrey Schirer ,
Amanda Simpson ,
Richard Nay ,
Yen-Shan Lin ,
Wen Yang ,
Maria I. Lopez ,
Jianan Li ,
Eugene A. Olevsky  and
Marc A. Meyers
Po-Yu Chen*
Affiliation:
Department of Materials Science and Engineering, National Tsing Hua University, Hsinchu 30013, Taiwan
Jeffrey Schirer
Affiliation:
Hysitron Inc., Minneapolis, Minnesota 55344
Amanda Simpson
Affiliation:
Hysitron Inc., Minneapolis, Minnesota 55344
Richard Nay
Affiliation:
Hysitron Inc., Minneapolis, Minnesota 55344
Yen-Shan Lin
Affiliation:
Department of Mechanical and Aerospace Engineering, University of California, San Diego, La Jolla, California 92093; and Department of Mechanical Engineering, San Diego State University, San Diego, California 92182
Wen Yang
Affiliation:
Materials Science and Engineering Program, University of California, San Diego, La Jolla, California 92093
Maria I. Lopez
Affiliation:
Materials Science and Engineering Program, University of California, San Diego, La Jolla, California 92093
Jianan Li
Affiliation:
School of Materials Science and Engineering, Shanghai Jiao Tong University, Shanghai 200240, People’s Republic of China
Eugene A. Olevsky
Affiliation:
Department of Mechanical Engineering, San Diego State University, San Diego, California 92182
Marc A. Meyers
Affiliation:
Department of Mechanical and Aerospace Engineering and Department of Nanoengineering, University of California, San Diego, La Jolla, California 92093
*
a)Address all correspondence to this author. e-mail: [email protected]
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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.

Keywords

BiologicalBiomaterialNanoindentation
Type
Articles
Information
Journal of Materials Research , Volume 27 , Issue 1: Focus Issue: Instrumented Indentation , 14 January 2012 , pp. 100 - 112
Copyright
Copyright © Materials Research Society 2011

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References

REFERENCES

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).Google Scholar
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).CrossRefGoogle ScholarPubMed
3.Lin, A.Y-M. and Meyers, M.A.: Growth and structure in abalone shell. Mater. Sci. Eng., A 290, 27 (2005).Google Scholar
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).Google Scholar
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).CrossRefGoogle ScholarPubMed
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).Google Scholar
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).Google Scholar
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).CrossRefGoogle Scholar
9.Atkins, T.: The Science and Engineering of Cutting (Butterworth-Heinemann, Oxford, UK, 2009), p. 230.Google Scholar
10.Diamond, J.M.: How great white sharks, saber-toothed cats and solders kill. Nature 322, 773 (1986).Google Scholar
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.Google Scholar
12.Onozato, H. and Watabe, N.: Studies on fish scale formation and resorption. Cell Tissue Res. 201, 409 (1979).Google Scholar
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).Google Scholar
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).Google Scholar
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).CrossRefGoogle Scholar
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).Google Scholar
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).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
19.Song, J., Ortiz, C., and Boyce, M.C.: Threat-protection mechanics of an armored fish. J. Mech. Behav. Biomed. Mater. 4, 699 (2011).Google Scholar
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).Google Scholar
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).Google Scholar
22.Currey, J.D.: Mechanical properties and adaptations of some less familiar bony tissues. J. Mech. Behav. Biomed. Mater. 3, 357 (2010).Google Scholar
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).Google Scholar
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).Google Scholar
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).Google Scholar
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).Google Scholar
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).Google Scholar
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).Google Scholar
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).Google Scholar
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).Google Scholar
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).Google Scholar
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).Google Scholar
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).Google Scholar
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).Google Scholar
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).Google Scholar
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).CrossRefGoogle ScholarPubMed
37.Habelitz, S., Marshall, G.W., Balooch, M., and Marshall, S.J.: Nanoindentation and storage of teeth. J. Biomech. 35, 995 (2002).Google Scholar
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).Google Scholar
39.Haque, F.: Application of nanoindentation to development of biomedical materials. Surf. Eng. 19, 255 (2003).Google Scholar
40.Ebenstein, D.M. and Pruitt, L.A.: Nanoindentation of biological materials. Nano Today 1, 26 (2006).Google Scholar
41.Angker, L. and Swain, M.V.: Nanoindentation: Application to dental hard tissue investigations. J. Mater. Res. 21, 1893 (2006).Google Scholar
42.Oyen, M.L.: Nanoindentation hardness of mineralized tissues. J. Biomech. 39, 2699 (2006).Google Scholar
43.Franke, O., Göken, M., and Hodge, M.A.: The nanoindentation of soft tissue: Current and developing approaches. JOM 60, 49 (2008).CrossRefGoogle Scholar
44.Dickinson, M.: Nanoindentation of biological composites. IOP Conf. Ser.: Mater. Sci. Eng. 4, 012015 (2009).Google Scholar
45.Oyen, M.L.: Nanoindentation of biological and biomimetic materials. Exp. Tech. (2011, in press).Google Scholar
46.Yao, H. and Gao, H.: Multi-scale cohesive laws in hierarchical materials. Int. J. Solids Struct. 45, 3627 (2008).Google Scholar
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).Google Scholar
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).Google Scholar
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).Google Scholar
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).Google Scholar