Skip to main content Accessibility help
Hostname: page-component-559fc8cf4f-7x8lp Total loading time: 0.762 Render date: 2021-03-02T14:21:14.762Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": false, "newCiteModal": false, "newCitedByModal": true }

Anisotropic design of a multilayered biological exoskeleton

Published online by Cambridge University Press:  31 January 2011

Lifeng Wang
Department of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139
Christine Ortiz
Department of Materials Science and Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139
Mary C. Boyce
Department of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139
E-mail address:
Get access


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.

Copyright © Materials Research Society 2009

Access options

Get access to the full version of this content by using one of the access options below.


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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle Scholar
3.Bucur, V. and Declercq, N.F.: The anisotropy of biological composites studied with ultrasonic technique. Ultrasonics 44, e829 (2006).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle Scholar
5.Vogel, S.: Comparative Biomechanics (Princeton University Press, Princeton, NJ, 2003), p. 175.Google Scholar
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle ScholarPubMed
8.Katz, J.L. and Ukraincik, K.: On the anisotropic elastic properties of hydroxyapatite. J. Biomech. 4, 221 (1971).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle ScholarPubMed
10.Bozec, L., van der Heijden, G., and Horton, M.: Collagen fibrils: Nanoscale ropes. Biophys. J. 92, 70 (2007).CrossRefGoogle ScholarPubMed
11.Dill, K.A.: Dominant forces in protein folding. Biochemistry 29, 7133 (1990).CrossRefGoogle ScholarPubMed
12.Tirrel, D.A.: Hierarchical Structures in Biology as a Guide for New Materials Technology (National Academic Press, Washington, DC, 1994).Google Scholar
13.Lowenstam, H.A. and Weiner, S.: On Biomineralization (Oxford University Press, New York, 1989).Google Scholar
14.Weiner, S., Addadi, L., and Wagner, H.D.: Materials design in biology. Mater. Sci. Em., C 11, 1 (2000).CrossRefGoogle Scholar
15.Wainwright, S.A.: Stress and design in bivalved mollusc shell. Nature 224, 777 (1969).CrossRefGoogle Scholar
16.Al-Sawalmih, A., Li, C.H., Siegel, S., Fabritius, H., Yi, S.B., Raabe, D., Fratzl, P., and Paris, O.: Microtexture and chitin/calref orientation relationship in the mineralized exoskeleton of the American lobster. Adv. Funct. Mater. 18, 3307 (2008).CrossRefGoogle Scholar
17.Chateigner, D., Hedegaard, C., and Wenke, H-R.: Mollusc shell microstructures and crystallographic textures. J. Struct. Geol. 22, 1723 (2000).CrossRefGoogle Scholar
18. AH Parsons: Structure of the egg shell. Poult. Sci. 61, 2013 (1982).CrossRefGoogle Scholar
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).CrossRefGoogle ScholarPubMed
20.Driessens, F.C.M. and Verbeeck, R.M.H.: Biominerals (CRC Press, Boca Raton, FL, 1990), p. 163.Google Scholar
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).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
23.Meunier, F.J.: Histological studies of the dermal skeleton in Poly-pteridae. Arch. Zool. Exp. Gén. 122, 279 (1980).Google Scholar
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.Google Scholar
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).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
28.Lee, W.T., Dove, M.T., and Salje, E.K.H.: Surface relaxations in hydroxyapatite. J. Phys. Condens. Matter 12, 9829 (2000).CrossRefGoogle Scholar
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.Google Scholar
30.Leventouri, Th.: Synthetic and biological hydroxyapatites: Crystal structure questions. Biomaterials 27, 3339 (2006).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle Scholar
32.Weiner, S.: Transient precursor strategy in mineral formation of bone. Bone 39, 431 (2006).CrossRefGoogle Scholar
33.Viswannath, B., Raghavanb, R., Ramamurtyb, U., and Ravishankar, N.: Mechanical properties and anisotropy in hydroxyapatite single crystals. Scr. Mater. 57, 361 (2007).CrossRefGoogle Scholar
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle Scholar
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).CrossRefGoogle Scholar
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle ScholarPubMed
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).CrossRefGoogle Scholar
40.Hassan, R., Caputo, A.A., and Bunshaw, R.F.: Fracture toughness of human enamel. J. Dent. Res. 60, 820 (1981).CrossRefGoogle ScholarPubMed

Full text views

Full text views reflects PDF downloads, PDFs sent to Google Drive, Dropbox and Kindle and HTML full text views.

Total number of HTML views: 0
Total number of PDF views: 128 *
View data table for this chart

* Views captured on Cambridge Core between September 2016 - 2nd March 2021. This data will be updated every 24 hours.

Send article to Kindle

To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Anisotropic design of a multilayered biological exoskeleton
Available formats

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Anisotropic design of a multilayered biological exoskeleton
Available formats

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Anisotropic design of a multilayered biological exoskeleton
Available formats

Reply to: Submit a response

Your details

Conflicting interests

Do you have any conflicting interests? *