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Anisotropic design of a multilayered biological exoskeleton

  • Lifeng Wang (a1), Juha Song, Christine Ortiz (a2) and Mary C. Boyce (a1)


Biological materials have developed hierarchical and heterogeneous material microstructures and nanostructures to provide protection against environmental threats that, in turn, provide bioinspired clues to improve human body armor. In this study, we present a multiscale experimental and computational approach to investigate the anisotropic design principles of a ganoid scale of an ancient fish, Polypterus senegalus, which possesses a unique quad-layered structure at the micrometer scale with nanostructured material constituting each layer. The anisotropy of the outermost prismatic ganoine layer was investigated using instrumented nanoindentations and finite element analysis (FEA) simulations. Nanomechanical modeling was carried out to reveal the elastic-plastic mechanical anisotropy of the ganoine composite due to its unique nanostructure. Simulation results for nanoindentation representing ganoine alternatively with isotropic, anisotropic, and discrete material properties are compared to understand the apparent direction-independence of the anisotropic ganoine during indentation. By incorporating the estimated anisotropic mechanical properties of ganoine, microindentation on a quad-layered FEA model that is analogous to penetration biting events (potential threat) was performed and compared with the quad-layered FEA model with isotropic ganoine. The elastic-plastic anisotropy of the outmost ganoine layer enhances the load-dependent penetration resistance of the multilayered armor compared with the isotropic ganoine layer by (i) retaining the effective indentation modulus and hardness properties, (ii) enhancing the transmission of stress and dissipation to the underlying dentin layer, (iii) lowering the ganoine/dentin interfacial stresses and hence reducing any propensity toward delamination, (iv) retaining the suppression of catastrophic radial surface cracking, and favoring localized circumferential cracking, and (v) providing discrete structural pathways (interprism) for circumferential cracks to propagate normal to the surface for easy arrest by the underlying dentin layer and hence containing damage locally. These results indicate the potential to use anisotropy of the individual layers as a means for design optimization of hierarchically structured material systems for dissipative armor.


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1.Fritsch, A. and Hellmich, C.: “Universal” microstructural patterns in cortical and trabecular, extracellular and extravascular bone materials: Micromechanics-based prediction of anisotropic elasticity. J. Theor. Biol. 244, 597 (2007).
2.Barthelat, F., Li, C-M., Comi, C., and Espinosa, H.D.: Mechanical properties of nacre constituents and their impact on mechanical performance. J. Mater. Res. 21, 1977 (2006).
3.Bucur, V. and Declercq, N.F.: The anisotropy of biological composites studied with ultrasonic technique. Ultrasonics 44, e829 (2006).
4.Nicholls, S.P., Gathercole, L.J., Keller, A., and Shah, J.S.: Crimping in rat tail tendon collagen: Morphology and transverse mechanical anisotropy. Int. J. Biol. Macromol. 5, 283 (1983).
5.Vogel, S.: Comparative Biomechanics (Princeton University Press, Princeton, NJ, 2003), p. 175.
6.Woo, S.L-Y., Akeson, W.H., and Jemmott, G.F.: Measurements of nonhomogeneous, directional mechanical properties of articular cartilage in tension. J. Biomech. 9, 785 (1976).
7.White, S.N., Luo, W., Paine, M.L., Fong, H., Sarikaya, M., and Snead, M.L.: Biological organization of hydroxyapatite crystallites into a fibrous continuum toughens and controls anisotropy in human enamel. J. Dent. Res. 80, 321 (2001).
8.Katz, J.L. and Ukraincik, K.: On the anisotropic elastic properties of hydroxyapatite. J. Biomech. 4, 221 (1971).
9.Ng, L., Grodzinsky, A.J., Sandy, J.D., Plaas, A.H.K., and Ortiz, C.: Individual cartilage aggrecan macromolecules and their constituent glycosaminoglycans visualized via atomic force microscopy. J. Struct. Biol. 143, 242 (2003).
10.Bozec, L., van der Heijden, G., and Horton, M.: Collagen fibrils: Nanoscale ropes. Biophys. J. 92, 70 (2007).
11.Dill, K.A.: Dominant forces in protein folding. Biochemistry 29, 7133 (1990).
12.Tirrel, D.A.: Hierarchical Structures in Biology as a Guide for New Materials Technology (National Academic Press, Washington, DC, 1994).
13.Lowenstam, H.A. and Weiner, S.: On Biomineralization (Oxford University Press, New York, 1989).
14.Weiner, S., Addadi, L., and Wagner, H.D.: Materials design in biology. Mater. Sci. Em., C 11, 1 (2000).
15.Wainwright, S.A.: Stress and design in bivalved mollusc shell. Nature 224, 777 (1969).
16.Al-Sawalmih, A., Li, C.H., Siegel, S., Fabritius, H., Yi, S.B., Raabe, D., Fratzl, P., and Paris, O.: Microtexture and chitin/calcite orientation relationship in the mineralized exoskeleton of the American lobster. Adv. Funct. Mater. 18, 3307 (2008).
17.Chateigner, D., Hedegaard, C., and Wenke, H-R.: Mollusc shell microstructures and crystallographic textures. J. Struct. Geol. 22, 1723 (2000).
18. AH Parsons: Structure of the egg shell. Poult. Sci. 61, 2013 (1982).
19.Rodriguez-Navarro, A.B., CabraldeMelo, C., Batista, N., Morimoto, N., Alvarez-Lloret, P., Ortega-Huertas, M., Fuenzalida, V.M., Arias, J.I., Wiff, P., and Arias, J.L.: Microstructure and crystallographic-texture of giant barnacle (Austromegabalanus psittacus) shell. J. Struct. Biol. 156, 355 (2006).
20.Driessens, F.C.M. and Verbeeck, R.M.H.: Biominerals (CRC Press, Boca Raton, FL, 1990), p. 163.
21.Bruet, B.J.F., Song, J.H., Boyce, M.C., and Ortiz, C.: Materials design principles of ancient fish armor. Nat. Mater. 7, 748 (2008).
22.Daget, J., Gayet, M., Meunier, F.J., and Sire, J-Y.: Major discoveries on the dermal skeleton of fossil and recent polypteriforms: A review. Fish Fish. 2, 113 (2001).
23.Meunier, F.J.: Histological studies of the dermal skeleton in Poly-pteridae. Arch. Zool. Exp. Gén. 122, 279 (1980).
24.Ørvig, T.: Phylogeny of tooth tissues: Evolution of some calcified tissues in early vertebrates, in Structural and Chemical Organization of Teeth, Vol. 1, edited by Miles, A.E.W. (Academic Press, New York & London, 1967), p. 45.
25.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).
26.Danielsson, M., Parks, D.M., and Boyce, M.C.: Three-dimensional micromechanical modeling of voided polymeric materials. J. Mech. Phys. Solids 50, 351 (2002).
27.Danielsson, M., Parks, D.M., and Boyce, M.C.: Micromechanics, macromechanics and constitutive modeling of the elasto-viscoplastic deformation of rubber-toughened glassy polymers. J. Mech. Phys. Solids 55, 533 (2007).
28.Lee, W.T., Dove, M.T., and Salje, E.K.H.: Surface relaxations in hydroxyapatite. J. Phys. Condens. Matter 12, 9829 (2000).
29.Posner, A.S. and Betts, F.: Molecular control of tissue mineralization, in Chemistry and Biology of Mineralized Connective tissues, edited by Veis, A. (Elsevier, Amsterdam, 1981), pp. 257266.
30.Leventouri, Th.: Synthetic and biological hydroxyapatites: Crystal structure questions. Biomaterials 27, 3339 (2006).
31.Rey, C., Combes, C., Drouet, C., Sfihi, H., and Barroug, A.: Physico-chemical properties of nanocrystalline apatites: Implications for biominerals and biomaterials. Mater. Sci. Em., C 27, 198 (2007).
32.Weiner, S.: Transient precursor strategy in mineral formation of bone. Bone 39, 431 (2006).
33.Viswannath, B., Raghavanb, R., Ramamurtyb, U., and Ravishankar, N.: Mechanical properties and anisotropy in hydroxyapatite single crystals. Scr. Mater. 57, 361 (2007).
34.Spears, I.R.: A three-dimensional finite element model of prismatic enamel: A re-appraisal of the data on the Young's modulus of enamel. J. Dent. Res. 76, 1690 (1997).
35.Katti, D.R., Katti, K.S., Sopp, J.M., and Sarikaya, M.: 3D finite element modeling of mechanical response in nacre-based hybrid nanocomposites. Comput. Theor. Polym. Sci. 11, 397 (2001).
36.Jayachandran, R., Boyce, M.C., and Argon, A.S.: Design of multilayer polymeric coatings for indentation resistance. J. Comput. Aided Mater. Des. 2, 155 (1995).
37.Markey, M.J., Main, R.P., and Marshall, C.R.: Vivo cranial suture function and suture morphology in the extant fish Polypterus: Implications for inferring skull function in living and fossil fish. J. Exp. Biol. 209, 2085 (2006).
38.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).
39.Spears, I.R., van Noort, R., Crompton, R.H., Cardew, G.E., and Howard, I.C.: The effects of enamel anisotropy on the distribution of stress in a tooth. J. Dent. Res. 72, 1526 (1993).
40.Hassan, R., Caputo, A.A., and Bunshaw, R.F.: Fracture toughness of human enamel. J. Dent. Res. 60, 820 (1981).



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