Abstract
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.
Similar content being viewed by others
References
A. Fritsch and C. Hellmich: “Universal” microstructural patterns in cortical and trabecular, extracellular and extravascular bone materials: Micromechanics-based prediction of anisotropic elasticity. J. Theor. Biol. 244, 597 (2007).
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).
V. Bucur and N.F. Declercq: The anisotropy of biological composites studied with ultrasonic technique. Ultrasonics 44, e829 (2006).
S.P. Nicholls, L.J. Gathercole, A. Keller, and J.S. Shah: Crimping in rat tail tendon collagen: Morphology and transverse mechanical anisotropy. Int. J. Biol. Macromol. 5, 283 (1983).
S. Vogel: Comparative Biomechanics (Princeton University Press, Princeton, NJ, 2003), p. 175.
S. WooL-Y., W.H. Akeson, and G.F. Jemmott: Measurements of nonhomogeneous, directional mechanical properties of articular cartilage in tension. J. Biomech. 9, 785 (1976).
S.N. White, W. Luo, M.L. Paine, H. Fong, M. Sarikaya, and M.L. Snead: Biological organization of hydroxyapatite crystallites into a fibrous continuum toughens and controls anisotropy in human enamel. J. Dent. Res. 80, 321 (2001).
J.L. Katz and K. Ukraincik: On the anisotropic elastic properties of hydroxyapatite. J. Biomech. 4, 221 (1971).
L. Ng, A.J. Grodzinsky, J.D. Sandy, A.H.K. Plaas, and C. Ortiz: Individual cartilage aggrecan macromolecules and their constituent glycosaminoglycans visualized via atomic force microscopy. J. Struct. Biol. 143, 242 (2003).
L. Bozec, van der G. Heijden, and M. Horton: Collagen fibrils: Nanoscale ropes. Biophys. J. 92, 70 (2007).
K.A. Dill: Dominant forces in protein folding. Biochemistry 29, 7133 (1990).
D.A. Tirrel: Hierarchical Structures in Biology as a Guide for New Materials Technology (National Academic Press, Washington, DC, 1994).
H.A. Lowenstam and S. Weiner: On Biomineralization (Oxford University Press, New York, 1989).
S. Weiner, L. Addadi, and H.D. Wagner: Materials design in biology. Mater. Sci. Em., C11, 1 (2000).
S.A. Wainwright: Stress and design in bivalved mollusc shell. Nature 224, 777 (1969).
A. Al-Sawalmih, C.H. Li, S. Siegel, H. Fabritius, S.B. Yi, D. Raabe, P. Fratzl, and O. Paris: Microtexture and chitin/calcite orientation relationship in the mineralized exoskeleton of the American lobster. Adv. Funct. Mater. 18, 3307 (2008).
D. Chateigner, C. Hedegaard, and H-R Wenke: Mollusc shell microstructures and crystallographic textures. J. Struct. Geol. 22, 1723 (2000).
A.H Parsons: Structure of the egg shell. Poult. Sci. 61, 2013 (1982).
A.B. Rodriguez-Navarro, C. CabraldeMelo, N. Batista, N. Morimoto, P. Alvarez-Lloret, M. Ortega-Huertas, V.M. Fuenzalida, J.I. Arias, P. Wiff, and J.L. Arias: Microstructure and crystallographic-texture of giant barnacle (Austromegabalanus psittacus) shell. J. Struct. Biol. 156, 355 (2006).
F.C.M. Driessens and R.M.H. Verbeeck: Biominerals (CRC Press, Boca Raton, FL, 1990), p. 163.
B.J.F. Bruet, J.H. Song, M.C. Boyce, and C. Ortiz: Materials design principles of ancient fish armor. Nat. Mater. 7, 748 (2008).
J. Daget, M. Gayet, F.J. Meunier, and J-Y Sire: Major discoveries on the dermal skeleton of fossil and recent polypteriforms: A review. Fish Fish. 2, 113 (2001).
F.J. Meunier: Histological studies of the dermal skeleton in Poly-pteridae. Arch. Zool. Exp. Gén. 122, 279 (1980).
T. Ørvig: Phylogeny of tooth tissues: Evolution of some calcified tissues in early vertebrates, in Structural and Chemical Organization of Teeth, Vol. 1, edited by A.E.W. Miles (Academic Press, New York & London, 1967), p. 45.
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).
M. Danielsson, D.M. Parks, and M.C. Boyce: Three-dimensional micromechanical modeling of voided polymeric materials. J. Mech. Phys. Solids 50, 351 (2002).
M. Danielsson, D.M. Parks, and M.C. Boyce: Micromechanics, macromechanics and constitutive modeling of the elasto-viscoplastic deformation of rubber-toughened glassy polymers. J. Mech. Phys. Solids 55, 533 (2007).
W.T. Lee, M.T. Dove, and E.K.H. Salje: Surface relaxations in hydroxyapatite. J. Phys. Condens. Matter 12, 9829 (2000).
A.S. Posner and F. Betts: Molecular control of tissue mineralization, in Chemistry and Biology of Mineralized Connective tissues, edited by A. Veis (Elsevier, Amsterdam, 1981), pp. 257–266.
Leventouri Th.: Synthetic and biological hydroxyapatites: Crystal structure questions. Biomaterials 27, 3339 (2006).
C. Rey, C. Combes, C. Drouet, H. Sfihi, and A. Barroug: Physico-chemical properties of nanocrystalline apatites: Implications for biominerals and biomaterials. Mater. Sci. Em., C27, 198 (2007).
S. Weiner: Transient precursor strategy in mineral formation of bone. Bone 39, 431 (2006).
B. Viswannath, R. Raghavanb, U. Ramamurtyb, and N. Ravishankar: Mechanical properties and anisotropy in hydroxyapatite single crystals. Scr. Mater. 57, 361 (2007).
I.R. Spears: 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).
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).
R. Jayachandran, M.C. Boyce, and A.S. Argon: Design of multilayer polymeric coatings for indentation resistance. J. Comput. Aided Mater. Des. 2, 155 (1995).
M.J. Markey, R.P. Main, and C.R. Marshall: 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).
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).
I.R. Spears, van R. Noort, R.H. Crompton, G.E. Cardew, and I.C. Howard: The effects of enamel anisotropy on the distribution of stress in a tooth. J. Dent. Res. 72, 1526 (1993).
R. Hassan, A.A. Caputo, and R.F. Bunshaw: Fracture toughness of human enamel. J. Dent. Res. 60, 820 (1981).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wang, L., Juha, S., Ortiz, C. et al. Anisotropic design of a multilayered biological exoskeleton. Journal of Materials Research 24, 3477–3494 (2009). https://doi.org/10.1557/jmr.2009.0443
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1557/jmr.2009.0443