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  • Review Article
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Structure and mechanics of interfaces in biological materials

Abstract

Hard biological materials — for example, seashells, bone or wood — fulfil critical structural functions and display unique and attractive combinations of stiffness, strength and toughness, owing to their intricate architectures, which are organized over several length scales. The size, shape and arrangement of the ‘building blocks’ of which these materials are made are essential for defining their properties and their exceptional performance, but there is growing evidence that their deformation and toughness are also largely governed by the interfaces that join these building blocks. These interfaces channel nonlinear deformations and deflect cracks into configurations in which propagation is more difficult. In this Review, we discuss comparatively the composition, structure and mechanics of a set of representative biological interfaces in nacre, bone and wood, and show that these interfaces possess unusual mechanical characteristics, which can encourage the development of advanced bioinspired composites. Finally, we highlight recent examples of synthetic materials inspired from the mechanics and architecture of natural interfaces.

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Figure 1: The structure, deformation and interfaces of nacre.
Figure 2: Mechanical tests on the interfaces in nacre.
Figure 3: The building blocks and interfaces of bone.
Figure 4: The mechanics of the interfaces within bone.
Figure 5: The structure and mechanics of wood.
Figure 6: The structure and mechanics of the interfaces between cellulose fibrils.
Figure 7: A material properties chart.
Figure 8: Synthetic materials based on the architectures and interfaces of biological materials.

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References

  1. Sarikaya, M. & Aksay, I. A. Biomimetic, Design and Processing of Materials (Woodbury, 1995).

    Google Scholar 

  2. Mayer, G. Rigid biological systems as models for synthetic composites. Science 310, 1144–1147 (2005).

    CAS  Google Scholar 

  3. Fratzl, P. & Weinkamer, R. Nature's hierarchical materials. Prog. Mater. Sci. 52, 1263–1334 (2007).

    CAS  Google Scholar 

  4. Barthelat, F. Biomimetics for next generation materials. Phil. Trans. R. Soc. A 365, 2907–2919 (2007).

    CAS  Google Scholar 

  5. Meyers, M. A., Chen, P.-Y., Lin, A. Y.-M. & Seki, Y. Biological materials: structure and mechanical properties. Prog. Mater. Sci. 53, 1–206 (2008).

    CAS  Google Scholar 

  6. Espinosa, H. D., Rim, J. E., Barthelat, F. & Buehler, M. J. Merger of structure and material in nacre and bone — perspectives on de novo biomimetic materials. Prog. Mater. Sci. 54, 1059–1100 (2009).

    CAS  Google Scholar 

  7. Nair, A. K. et al. in Biomineralization Handbook: Characterization of Biomineral and Biomimetic Materials (ed. DiMasi, E. ) 337–349 (CRC Press, 2014).

    Google Scholar 

  8. Ritchie, R. O. The conflicts between strength and toughness. Nat. Mater. 10, 817–822 (2011).

    CAS  Google Scholar 

  9. Naleway, S. E., Porter, M. M., McKittrick, J. & Meyers, M. A. Structural design elements in biological materials: application to bioinspiration. Adv. Mater. 27, 5455–5476 (2015).

    CAS  Google Scholar 

  10. Barthelat, F. Architectured materials in engineering and biology: fabrication, structure, mechanics and performance. Int. Mater. Rev. 60, 413–430 (2015).

    CAS  Google Scholar 

  11. Ackbarow, T. & Buehler, M. J. Hierarchical coexistence of universality and diversity controls robustness and multi-functionality in protein materials. J. Comput. Theor. Nanosci. 5, 1193–1204 (2008).

    CAS  Google Scholar 

  12. Buehler, M. J. Tu(r)ning weakness to strength. Nano Today 5, 379–383 (2010).

    CAS  Google Scholar 

  13. Cranford, S. & Buehler, M. J. Biomateriomics (Springer, 2012).

    Google Scholar 

  14. Dunlop, J. W. C., Weinkamer, R. & Fratzl, P. Artful interfaces within biological materials. Mater. Today 14, 70–78 (2011).

    Google Scholar 

  15. Ritchie, R. O., Buehler, M. J. & Hansma, P. Plasticity and toughness in bone. Phys. Today 62, 41–47 (2009).

    CAS  Google Scholar 

  16. Dastjerdi, A. K., Rabiei, R. & Barthelat, F. The weak interfaces within tough natural composites: experiments on three types of nacre. J. Mech. Behav. Biomed. Mater. 19, 50–60 (2013).

    CAS  Google Scholar 

  17. Spivak, D. I., Giesa, T., Wood, E. & Buehler, M. J. Category theoretic analysis of hierarchical protein materials and social networks. PLoS ONE 6, e23911 (2011).

    CAS  Google Scholar 

  18. Yahyazadehfar, M. & Arola, D. The role of organic proteins on the crack growth resistance of human enamel. Acta Biomater. 19, 33–45 (2015).

    CAS  Google Scholar 

  19. Wang, R. Z., Suo, Z., Evans, A. G., Yao, N. & Aksay, I. A. Deformation mechanisms in nacre. J. Mater. Res. 16, 2485–2493 (2001).

    CAS  Google Scholar 

  20. Barthelat, F. & Espinosa, H. D. An experimental investigation of deformation and fracture of nacre–mother of pearl. Exp. Mech. 47, 311–324 (2007).

    Google Scholar 

  21. Currey, J. D. Mechanical properties of mother of pearl in tension. Proc. R. Soc. Lond. B 196, 443–463 (1977).

    Google Scholar 

  22. Barthelat, F., Tang, H., Zavattieri, P. D., Li, C. M. & Espinosa, H. D. On the mechanics of mother of pearl: a key feature in the material hierarchical structure. J. Mech. Phys. Solids 55, 306–337 (2007).

    CAS  Google Scholar 

  23. Weiner, S. & Wagner, H. D. The material bone: structure mechanical function relations. Annu. Rev. Mater. Sci. 28, 271–298 (1998).

    CAS  Google Scholar 

  24. Rho, J. Y., Kuhn-Spearing, L. & Zioupos, P. Mechanical properties and the hierarchical structure of bone. Med. Eng. Phys. 20, 92–102 (1998).

    CAS  Google Scholar 

  25. Giesa, T., Spivak, D. I. & Buehler, M. J. Category theory based solution for the building block replacement problem in materials design. Adv. Eng. Mater. 14, 810–817 (2012).

    Google Scholar 

  26. Mayer, G. New classes of tough composite materials — lessons from natural rigid biological systems. Mater. Sci. Eng. C 26, 1261–1268 (2006).

    CAS  Google Scholar 

  27. Kushner, A. M., Gabuchian, V., Johnson, E. G. & Guan, Z. Biomimetic design of reversibly unfolding cross-linker to enhance mechanical properties of 3D network polymers. J. Am. Chem. Soc. 129, 14110–14111 (2007).

    CAS  Google Scholar 

  28. Laaksonen, P., Szilvay, G. R. & Linder, M. B. Genetic engineering in biomimetic composites. Trends Biotechnol. 30, 191–197 (2012).

    CAS  Google Scholar 

  29. Studart, A. R. Towards high-performance bioinspired composites. Adv. Mater. 24, 5024–5044 (2012).

    CAS  Google Scholar 

  30. Chintapalli, R. K., Breton, S., Dastjerdi, A. K. & Barthelat, F. Strain rate hardening: a hidden but critical mechanism for biological composites? Acta Biomater. 10, 5064–5073 (2014).

    CAS  Google Scholar 

  31. Currey, J. D. & Taylor, J. D. The mechanical behavior of some molluscan hard tissues. J. Zool. 173, 395–406 (1974).

    Google Scholar 

  32. Jackson, A. P., Vincent, J. F. V. & Turner, R. M. The mechanical design of nacre. Proc. R. Soc. Lond. B 234, 415–440 (1988).

    Google Scholar 

  33. Colfen, H. & Antonietti, M. Mesocrystals: inorganic superstructures made by highly parallel crystallization and controlled alignment. Angew. Chem. Int. Ed. Engl. 44, 5576–5591 (2005).

    Google Scholar 

  34. Rousseau, M. et al. Multiscale structure of sheet nacre. Biomaterials 26, 6254–6262 (2005).

    CAS  Google Scholar 

  35. Marin, F., Le Roy, N. & Marie, B. The formation and mineralization of mollusk shell. Front. Biosci. (Schol. Ed.) 4, 1099–1125 (2012).

    Google Scholar 

  36. Li, X. D., Xu, Z. H. & Wang, R. Z. In situ observation of nanograin rotation and deformation in nacre. Nano Lett. 6, 2301–2304 (2006).

    CAS  Google Scholar 

  37. Barthelat, F. & Rabiei, R. Toughness amplification in natural composites. J. Mech. Phys. Solids 59, 829–840 (2011).

    Google Scholar 

  38. Rabiei, R., Bekah, S. & Barthelat, F. Failure mode transition in nacre and bone-like materials. Acta Biomater. 6, 4081–4089 (2010).

    CAS  Google Scholar 

  39. Levi-Kalisman, Y., Falini, G., Addadi, L. & Weiner, S. Structure of the nacreous organic matrix of a bivalve mollusk shell examined in the hydrated state using cryo-TEM. J. Struct. Biol. 135, 8–17 (2001).

    CAS  Google Scholar 

  40. Jackson, A. P. & Vincent, J. F. V. Application of surface analytical techniques to the study of fracture surfaces of mother of pearl. J. Mater. Sci. Lett. 5, 975–978 (1986).

    CAS  Google Scholar 

  41. Menig, R., Meyers, M. H., Meyers, M. A. & Vecchio, K. S. Quasi-static and dynamic mechanical response of Haliotis rufescens (abalone) shells. Acta Mater. 48, 2383–2398 (2000).

    CAS  Google Scholar 

  42. Lopez, M. I., Meza Martinez, P. E. & Meyers, M. A. Organic interlamellar layers, mesolayers and mineral nanobridges: contribution to strength in abalone (Haliotis rufescence) nacre. Acta Biomater. 10, 2056–2064 (2014).

    CAS  Google Scholar 

  43. Shao, C. & Keten, S. Stiffness enhancement in nacre-inspired nanocomposites due to nanoconfinement. Sci. Rep. 5, 16452 (2015).

    Google Scholar 

  44. Barthelat, F., Dastjerdi, A. K. & Rabiei, R. An improved failure criterion for biological and engineered staggered composites. J. R. Soc. Interface 10, 20120849 (2013).

    Google Scholar 

  45. Nabavi, A., Capozzi, A., Goroshin, S., Frost, D. L. & Barthelat, F. A novel method for net-shape manufacturing of metal–metal sulfide cermets. J. Mater. Sci. 49, 8095–8106 (2014).

    CAS  Google Scholar 

  46. Huang, Z. & Li, X. Nanoscale structural and mechanical characterization of heat treated nacre. Mater. Sci. Eng. C 29, 1803–1807 (2009).

    CAS  Google Scholar 

  47. Marin, F., Luquet, G., Marie, B. & Medakovic, D. Molluscan shell proteins: primary structure, origin, and evolution. Curr. Top. Dev. Biol. 80, 209–276 (2008).

    CAS  Google Scholar 

  48. Shen, X. Y., Belcher, A. M., Hansma, P. K., Stucky, G. D. & Morse, D. E. Molecular cloning and characterization of lustrin A, a matrix protein from shell and pearl nacre of Haliotis rufescens. J. Biol. Chem. 272, 32472–32481 (1997).

    CAS  Google Scholar 

  49. Smith, B. L. et al. Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites. Nature 399, 761–763 (1999).

    CAS  Google Scholar 

  50. Vincent, J. F. V. & Wegst, U. G. K. Design and mechanical properties of insect cuticle. Arthropod Struct. Dev. 33, 187–199 (2004).

    Google Scholar 

  51. Schaeffer, T. E. et al. Does abalone nacre form by heteroepitaxial nucleation or by growth through mineral bridges? Chem. Mater. 9, 1731–1740 (1997).

    CAS  Google Scholar 

  52. Weiss, I. M. Jewels in the pearl. ChemBioChem 11, 297–300 (2010).

    CAS  Google Scholar 

  53. Qi, H. J., Ortiz, C. & Boyce, M. C. Mechanics of biomacromolecular networks containing folded domains. J. Eng. Mater. Technol. 128, 509–518 (2006).

    CAS  Google Scholar 

  54. Lopez, M. I. & Meyers, M. A. The organic interlamellar layer in abalone nacre: formation and mechanical response. Mater. Sci. Eng. C 58, 7–13 (2016).

    CAS  Google Scholar 

  55. Weiss, I. M., Kaufmann, S., Heiland, B. & Tanaka, M. Covalent modification of chitin with silk-derivatives acts as an amphiphilic self-organizing template in nacre biomineralisation. J. Struct. Biol. 167, 68–75 (2009).

    CAS  Google Scholar 

  56. Suetake, T. et al. Chitin-binding proteins in invertebrates and plants comprise a common chitin-binding structural motif. J. Biol. Chem. 275, 17929–17932 (2000).

    CAS  Google Scholar 

  57. Suzuki, M. et al. An acidic matrix protein, Pif, is a key macromolecule for nacre formation. Science 325, 1388–1390 (2009).

    CAS  Google Scholar 

  58. Laaksonen, P. et al. Genetic engineering of biomimetic nanocomposites: diblock proteins, graphene, and nanofibrillated cellulose. Angew. Chem. Int. Ed. Engl. 50, 8688–8691 (2011).

    CAS  Google Scholar 

  59. Gent, A. N., Suh, J. B. & Kelly, S. G. Mechanics of rubber shear springs. Int. J. Non-Linear Mechan. 42, 241–249 (2007).

    Google Scholar 

  60. Pascal, J., Darqueceretti, E., Felder, E. & Pouchelon, A. Rubber-like adhesive in simple shear — stress-analysis and fracture morphology of a single lap joint. J. Adhes. Sci. Technol. 8, 553–573 (1994).

    Google Scholar 

  61. Song, F., Zhang, X. H. & Bai, Y. L. Microstructure and characteristics in the organic matrix layers of nacre. J. Mater. Res. 17, 1567–1570 (2002).

    CAS  Google Scholar 

  62. Currey, J. D. Bones: Structure and Mechanics (Princeton Univ. Press, 2002).

    Google Scholar 

  63. Wegst, U. G. K. & Ashby, M. F. The mechanical efficiency of natural materials. Philos. Mag. 84, 2167–2181 (2004).

    CAS  Google Scholar 

  64. Young, M. F. Bone matrix proteins: their function, regulation, and relationship to osteoporosis. Osteoporosis Int. 14, S35–S42 (2003).

    CAS  Google Scholar 

  65. Hui, S. L., Slemenda, C. W. & Johnston, C. C. Age and bone mass as predictors of fracture in a prospective study. J. Clin. Invest. 81, 1804–1809 (1988).

    CAS  Google Scholar 

  66. Burr, D. B. The contribution of the organic matrix to bone's material properties. Bone 31, 8–11 (2002).

    CAS  Google Scholar 

  67. Reznikov, N., Shahar, R. & Weiner, S. Bone hierarchical structure in three dimensions. Acta Biomater. 10, 3815–3826 (2014).

    Google Scholar 

  68. Buehler, M. J. Nature designs tough collagen: explaining the nanostructure of collagen fibrils. Proc. Natl Acad. Sci. USA 103, 12285–12290 (2006).

    CAS  Google Scholar 

  69. Uzel, S. G. M. & Buehler, M. J. Molecular structure, mechanical behavior and failure mechanism of the C-terminal cross-link domain in type I collagen. J. Mech. Behav. Biomed. Mater. 4, 153–161 (2011).

    CAS  Google Scholar 

  70. Shen, Z. L., Dodge, M. R., Kahn, H., Ballarini, R. & Eppell, S. J. Stress-strain experiments on individual collagen fibrils. Biophys. J. 95, 3956–3963 (2008).

    CAS  Google Scholar 

  71. Hassenkam, T. et al. High-resolution AFM imaging of intact and fractured trabecular bone. Bone 35, 4–10 (2004).

    Google Scholar 

  72. Buehler, M. J. Molecular nanomechanics of nascent bone: fibrillar toughening by mineralization. Nanotechnology 18 295102 (2007).

    Google Scholar 

  73. Knott, L. & Bailey, A. J. Collagen cross-links in mineralizing tissues: a review of their chemistry, function, and clinical relevance. Bone 22, 181–187 (1998).

    CAS  Google Scholar 

  74. Launey, M. E., Buehler, M. J. & Ritchie, R. O. On the mechanistic origins of toughness in bone. Annu. Rev. Mater. Res. 40, 25–53 (2010).

    CAS  Google Scholar 

  75. Ural, A. & Vashishth, D. Hierarchical perspective of bone toughness — from molecules to fracture. Int. Mater. Rev. 59, 245–263 (2014).

    CAS  Google Scholar 

  76. Ritchie, R. O., Kinney, J. H., Kruzic, J. J. & Nalla, R. K. A fracture mechanics and mechanistic approach to the failure of cortical bone. Fatigue Fract. Eng. Mater. Struct. 28, 345–371 (2005).

    CAS  Google Scholar 

  77. Thurner, P. J. & Katsamenis, O. L. The role of nanoscale toughening mechanisms in osteoporosis. Curr. Osteoporosis Rep. 12, 351–356 (2014).

    Google Scholar 

  78. Zimmermann, E. A. et al. Age-related changes in the plasticity and toughness of human cortical bone at multiple length scales. Proc. Natl Acad. Sci. USA 108, 14416–14421 (2011).

    CAS  Google Scholar 

  79. Taylor, D., Hazenberg, J. G. & Lee, T. C. Living with cracks: damage and repair in human bone. Nat. Mater. 6, 263–268 (2007).

    CAS  Google Scholar 

  80. Gupta, H. S. et al. Fibrillar level fracture in bone beyond the yield point. Int. J. Fracture 139, 425–436 (2006).

    Google Scholar 

  81. Fantner, G. E. et al. Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nat. Mater. 4, 612–616 (2005).

    CAS  Google Scholar 

  82. Gupta, H. S. et al. Nanoscale deformation mechanisms in bone. Nano Lett. 5, 2108–2111 (2005).

    CAS  Google Scholar 

  83. Poundarik, A. A. et al. Dilatational band formation in bone. Proc. Natl Acad. Sci. USA 109, 19178–19183 (2012).

    CAS  Google Scholar 

  84. Schwiedrzik, J. et al. In situ micropillar compression reveals superior strength and ductility but an absence of damage in lamellar bone. Nat. Mater. 13, 740–747 (2014).

    CAS  Google Scholar 

  85. Nalla, R. K., Kinney, J. H. & Ritchie, R. O. Mechanistic fracture criteria for the failure of human cortical bone. Nat. Mater. 2, 164–168 (2003).

    CAS  Google Scholar 

  86. Fantner, G. E. et al. Influence of the degradation of the organic matrix on the microscopic fracture behavior of trabecular bone. Bone 35, 1013–1022 (2004).

    CAS  Google Scholar 

  87. Hang, F., Gupta, H. S. & Barber, A. H. Nanointerfacial strength between non-collagenous protein and collagen fibrils in antler bone. J. R. Soc. Interface 11, 20130993 (2014).

    Google Scholar 

  88. Poundarik, A. A. & Vashishth, D. Multiscale imaging of bone microdamage. Connect. Tissue Res. 56, 87–98 (2015).

    Google Scholar 

  89. Hansma, P. K. et al. Sacrificial bonds in the interfibrillar matrix of bone. J. Musculoskelet. Neuronal Interact. 5, 313–315 (2005).

    CAS  Google Scholar 

  90. Gupta, H. S. et al. Evidence for an elementary process in bone plasticity with an activation enthalpy of 1 eV. J. R. Soc. Interface 4, 277–282 (2007).

    Google Scholar 

  91. Seref-Ferlengez, Z., Basta-Pljakic, J., Kennedy, O. D., Philemon, C. J. & Schaffler, M. B. Structural and mechanical repair of diffuse damage in cortical bone in vivo. J. Bone Miner. Res. 29, 2537–2544 (2014).

    Google Scholar 

  92. Thompson, J. B. et al. Bone indentation recovery time correlates with bond reforming time. Nature 414, 773–776 (2001).

    CAS  Google Scholar 

  93. Fantner, G. E. et al. Nanoscale ion mediated networks in bone: osteopontin can repeatedly dissipate large amounts of energy. Nano Lett. 7, 2491–2498 (2007).

    CAS  Google Scholar 

  94. Thurner, P. J. et al. Osteopontin deficiency increases bone fragility but preserves bone mass. Bone 46, 1564–1573 (2010).

    CAS  Google Scholar 

  95. Tai, K., Ulm, F.-J. & Ortiz, C. Nanogranular origins of the strength of bone. Nano Lett. 6, 2520–2525 (2006).

    CAS  Google Scholar 

  96. Bailey, A. J. Molecular mechanisms of ageing in connective tissues. Mech. Ageing Dev. 122, 735–755 (2001).

    CAS  Google Scholar 

  97. Tang, S. Y., Zeenath, U. & Vashishth, D. Effects of non-enzymatic glycation on cancellous bone fragility. Bone 40, 1144–1151 (2007).

    CAS  Google Scholar 

  98. Ker, R. F. Mechanics of tendon, from an engineering perspective. Int. J. Fatigue 29, 1001–1009 (2007).

    CAS  Google Scholar 

  99. Puxkandl, R. et al. Viscoelastic properties of collagen: synchrotron radiation investigations and structural model. Phil. Trans. R. Soc. Lond. B 357, 191–197 (2002).

    CAS  Google Scholar 

  100. Khayer Dastjerdi, A. & Barthelat, F. Teleost fish scales amongst the toughest collagenous materials. J. Mech. Behav. Biomed. Mater. 52, 95–107 (2015).

    CAS  Google Scholar 

  101. Yang, W. et al. Protective role of Arapaima gigas fish scales: structure and mechanical behavior. Acta Biomater. 10, 3599–3614 (2014).

    Google Scholar 

  102. Ascenzi, M.-G. & Roe, A. K. The osteon: the micromechanical unit of compact bone. Front. Biosci. (Landmark Ed.) 17, 1551–1581 (2012).

    CAS  Google Scholar 

  103. Skedros, J. G., Holmes, J. L., Vajda, E. G. & Bloebaum, R. D. Cement lines of secondary osteons in human bone are not mineral-deficient: new data in a historical perspective. Anat. Rec. A Discov. Mol. Cell Evol. Biol. 286A, 781–803 (2005).

    Google Scholar 

  104. Burr, D. B., Schaffler, M. B. & Frederickson, R. G. Composition of the cement line and its possible mechanical role as a local interface inhuman compact bone. J. Biomech. 21, 939–945 (1988).

    CAS  Google Scholar 

  105. Koester, K. J., Ager, J. W., & Ritchie, R. O. The true toughness of human cortical bone measured with realistically short cracks. Nat. Mater. 7, 672–677 (2008).

    CAS  Google Scholar 

  106. Ascenzi, A. & Bonucci, E. Shearing properties of single osteons. Anat. Rec. 172, 499–510 (1972).

    CAS  Google Scholar 

  107. Bigley, R. F., Griffin, L. V., Christensen, L. & Vandenbosch, R. Osteon interfacial strength and histomorphometry of equine cortical bone. J. Biomech. 39, 1629–1640 (2006).

    Google Scholar 

  108. Dong, X. N., Zhang, X. & Guo, X. E. Interfacial strength of cement lines in human cortical bone. Mech. Chem. Biosyst. 2, 63–68 (2005).

    Google Scholar 

  109. O'Brien, F. J., Taylor, D. & Lee, T. C. Microcrack accumulation at different intervals during fatigue testing of compact bone. J. Biomech. 36, 973–980 (2003).

    Google Scholar 

  110. Zioupos, P. & Currey, J. D. The extent of microcracking and the morphology of microcracks in damaged bone. J. Mater. Sci. 29, 978–986 (1994).

    Google Scholar 

  111. Mellon, S. J. & Tanner, K. E. Bone and its adaptation to mechanical loading: a review. Int. Mater. Rev. 57, 235–255 (2012).

    CAS  Google Scholar 

  112. Ager, J. W., Balooch, G. & Ritchie, R. O. Fracture, aging, and disease in bone. J. Mater. Res. 21, 1878–1892 (2006).

    CAS  Google Scholar 

  113. Piekarsk, K. Fracture of bone. J. Appl. Phys. 41, 215–223 (1970).

    Google Scholar 

  114. Hiller, L. P. et al. Osteon pullout in the equine third metacarpal bone: effects of ex vivo fatigue. J. Orthopaed. Res. 21, 481–488 (2003).

    CAS  Google Scholar 

  115. Buehler, M. J. & Ackbarow, T. Fracture mechanics of protein materials. Mater. Today 10, 46–58 (2007).

    CAS  Google Scholar 

  116. Zhang, Z., Zhang, Y.-W. & Gao, H. On optimal hierarchy of load-bearing biological materials. Proc. R. Soc. B 278, 519–525 (2011).

    Google Scholar 

  117. Peterlik, H., Roschger, P., Klaushofer, K. & Fratzl, P. From brittle to ductile fracture of bone. Nat. Mater. 5, 52–55 (2006).

    CAS  Google Scholar 

  118. Zioupos, P., Currey, J. D. & Sedman, A. J. An examination of the micromechanics of failure of bone and antler by acoustic emission tests and laser scanning confocal microscopy. Med. Eng. Phys. 16, 203–212 (1994).

    CAS  Google Scholar 

  119. Gibson, L. J. The hierarchical structure and mechanics of plant materials. J. R. Soc. Interface 9, 2749–2766 (2012).

    CAS  Google Scholar 

  120. Jeronimidis, G. J. The fracture behavior of wood and the relations between toughness and morphology. Proc. R. Soc. Lond. B 208, 447–460 (1980).

    Google Scholar 

  121. Gordon, J. E. & Jeronimidis, G. Composites with high work of fracture. Phil. Trans. R. Soc. Lond. A 294, 545–550 (1980).

    CAS  Google Scholar 

  122. Lucas, P. W., Tan, H. T. W. & Cheng, P. Y. The toughness of secondary cell wall and woody tissue. Phil. Trans. R. Soc. Lond. B 352, 341–352 (1997).

    Google Scholar 

  123. Fratzl, P. Cellulose and collagen: from fibres to tissues. Curr. Opin. Colloid Interface Sci. 8, 145–155 (2003).

    Google Scholar 

  124. Pilate, G. et al. Lignification and tension wood. C. R. Biol. 327, 889–901 (2004).

    CAS  Google Scholar 

  125. Lichtenegger, H., Reiterer, A., Stanzl-Tschegg, S. E. & Fratzl, P. Variation of cellulose microfibril angles in softwoods and hardwoods — a possible strategy of mechanical optimization. J. Struct. Biol. 128, 257–269 (1999).

    CAS  Google Scholar 

  126. Jarvis, M. Cellulose stacks up. Nature 426, 611–612 (2003).

    CAS  Google Scholar 

  127. Sinko, R., Qin, X. & Keten, S. Interfacial mechanics of cellulose nanocrystals. MRS Bull. 40, 340–348 (2015).

    CAS  Google Scholar 

  128. Altaner, C. M. & Jarvis, M. C. Modelling polymer interactions of the ‘molecular Velcro’ type in wood under mechanical stress. J. Theor. Biol. 253, 434–445 (2008).

    CAS  Google Scholar 

  129. Salmén, L. Micromechanical understanding of the cell-wall structure. C. R. Biol. 327, 873–880 (2004).

    Google Scholar 

  130. Fratzl, P., Burgert, I. & Gupta, H. S. On the role of interface polymers for the mechanics of natural polymeric composites. Phys. Chem. Chem. Phys. 6, 5575–5579 (2004).

    CAS  Google Scholar 

  131. Cousins, W. J. Elasticity of isolated lignin: Young's modulus by a continuous indentation method. N. Z. J. For. Sci. 7, 107–112 (1977).

    CAS  Google Scholar 

  132. Cave, I. The anisotropic elasticity of the plant cell wall. Wood Sci. Technol. 2, 268–278 (1968).

    Google Scholar 

  133. Keckes, J. et al. Cell-wall recovery after irreversible deformation of wood. Nat. Mater. 2, 810–814 (2003).

    CAS  Google Scholar 

  134. Navi, P., Rastogi, P. K., Gresse, V. & Tolou, A. Micromechanics of wood subjected to axial tension. Wood Sci. Technol. 29, 411–429 (1995).

    CAS  Google Scholar 

  135. Spatz, H., Kö hler, L. & Niklas, K. J. Mechanical behaviour of plant tissues: composite materials or structures? J. Exp. Biol. 202, 3269–3272 (1999).

    CAS  Google Scholar 

  136. Kohler, L. & Spatz, H. C. Micromechanics of plant tissues beyond the linear-elastic range. Planta 215, 33–40 (2002).

    Google Scholar 

  137. Jin, K., Qin, Z. & Buehler, M. J. Molecular deformation mechanisms of the wood cell wall material. J. Mech. Behav. Biomed. Mater. 42, 198–206 (2015).

    CAS  Google Scholar 

  138. Adler, D. C. & Buehler, M. J. Mesoscale mechanics of wood cell walls under axial strain. Soft Matter 9, 7138–7144 (2013).

    CAS  Google Scholar 

  139. Liang, L., Perre, P., Frank, X. & Mazeau, K. A coarse-grain force-field for xylan and its interaction with cellulose. Carbohydr. Polym. 127, 438–450 (2015).

    Google Scholar 

  140. Saavedra Flores, E. I., DiazDelao, F. A., Friswell, M. I. & Ajaj, R. M. Investigation on the extensibility of the wood cell-wall composite by an approach based on homogenisation and uncertainty analysis. Compos. Struct. 108, 212–222 (2014).

    Google Scholar 

  141. Navi, P. & Heger, F. Combined densification and thermo–hydro-mechanical processing of wood. MRS Bull. 29, 332–336 (2004).

    Google Scholar 

  142. Fratzl, P., Burgert, I. & Keckes, J. Mechanical model for the deformation of the wood cell wall. Z. Metallkd. 95, 579–584 (2004).

    CAS  Google Scholar 

  143. Stiernstedt, J., Brumer, H., Zhou, Q., Teeri, T. T. & Rutland, M. W. Friction between cellulose surfaces and effect of xyloglucan adsorption. Biomacromolecules 7, 2147–2153 (2006).

    CAS  Google Scholar 

  144. Åkerholm, M. & Salmén, L. Interactions between wood polymers studied by dynamic FT-IR spectroscopy. Polymer 42, 963–969 (2001).

    Google Scholar 

  145. Wimmer, R. & Lucas, B. N. Comparing mechanical properties of secondary wall and cell corner middle lamella in spruce wood. IAWA J. 18, 77–88 (1997).

    Google Scholar 

  146. Whiting, P. & Goring, D. A. I. Chemical characterization of tissue fractions from the middle lamella and secondary wall of black spruce tracheids. Wood Sci. Technol. 16, 261–267 (1982).

    CAS  Google Scholar 

  147. Sorvari, J., Sjöström, E., Klemola, A. & Laine, J. E. Chemical characterization of wood constituents, especially lignin, in fractions separated from middle lamella and secondary wall of Norway spruce (Picea abies). Wood Sci. Technol. 20, 35–51 (1986).

    CAS  Google Scholar 

  148. Thuvander, F. & Berglund, L. A. In situ observations of fracture mechanisms for radial cracks in wood. J. Mater. Sci. 35, 6277–6283 (2000).

    CAS  Google Scholar 

  149. Ashby, M. F., Easterling, K. E., Harrysson, R. & Maiti, S. K. The fracture and toughness of woods. Proc. R. Soc. Lond. A 398, 261–280 (1985).

    Google Scholar 

  150. United States Department of Agriculture. Wood handbook: wood as an engineering material (Forest Products Laboratory, 1974).

  151. He, M. Y. & Hutchinson, J. W. Crack deflection at an interface between dissimilar elastic materials. Int. J. Solids Struct. 25, 1053–1067 (1989).

    Google Scholar 

  152. Chan, K. S., He, M. Y. & Hutchinson, J. W. Cracking and stress redistribution in ceramic layered composites. Mater. Sci. Eng. A 167, 57–64 (1993).

    Google Scholar 

  153. Gao, H. J. Application of fracture mechanics concepts to hierarchical biomechanics of bone and bone-like materials. Int. J. Fracture 138, 101–137 (2006).

    Google Scholar 

  154. Keten, S., Xu, Z., Ihle, B. & Buehler, M. J. Nanoconfinement controls stiffness, strength and mechanical toughness of β-sheet crystals in silk. Nat. Mater. 9, 359–367 (2010).

    CAS  Google Scholar 

  155. Evans, A. G. Design and life prediction issues for high-temperature engineering ceramics and their composites. Acta Mater. 45, 23–40 (1997).

    CAS  Google Scholar 

  156. Sarikaya, M. An introduction to biomimetics: a structural viewpoint. Microsc. Res. Tech. 27, 360–375 (1994).

    CAS  Google Scholar 

  157. Wegst, U. G. K., Bai, H., Saiz, E., Tomsia, A. P. & Ritchie, R. O. Bioinspired structural materials. Nat. Mater. 14, 23–36 (2015).

    CAS  Google Scholar 

  158. Munch, E. et al. Tough, bio-inspired hybrid materials. Science 322, 1516–1520 (2008).

    CAS  Google Scholar 

  159. Livanov, K. et al. Tough alumina/polymer layered composites with high ceramic content. J. Am. Ceram. Soc. 98, 1285–1291 (2015).

    CAS  Google Scholar 

  160. Wang, J., Cheng, Q., Lin, L. & Jiang, L. Synergistic toughening of bioinspired poly(vinyl alcohol)–clay–nanofibrillar cellulose artificial nacre. ACS Nano 8, 2739–2745 (2014).

    CAS  Google Scholar 

  161. Bonderer, L. J., Studart, A. R. & Gauckler, L. J. Bioinspired design and assembly of platelet reinforced polymer films. Science 319, 1069–1073 (2008).

    CAS  Google Scholar 

  162. Cavelier, S., Barrett, C. J. & Barthelat, F. The mechanical performance of a biomimetic nanointerface made of multilayered polyelectrolytes. Eur. J. Inorg. Chem. 2012, 5380–5389 (2012).

    CAS  Google Scholar 

  163. Dimas, L. S., Bratzel, G. H., Eylon, I. & Buehler, M. J. Tough composites inspired by mineralized natural materials: computation, 3D printing, and testing. Adv. Funct. Mater. 23, 4629–4638 (2013).

    CAS  Google Scholar 

  164. Mirkhalaf, M., Dastjerdi, A. K. & Barthelat, F. Overcoming the brittleness of glass through bio-inspiration and micro-architecture. Nat. Commun. 5 3166 (2014).

    CAS  Google Scholar 

  165. Tang, Z. Y., Kotov, N. A., Magonov, S. & Ozturk, B. Nanostructured artificial nacre. Nat. Mater. 2, 413–418 (2003).

    CAS  Google Scholar 

  166. Guan, Z. Supramolecular design in biopolymers and biomimetic polymers for properties. Polym. Int. 56, 467–473 (2007).

    CAS  Google Scholar 

  167. Barthelat, F. & Zhu, D. J. A novel biomimetic material duplicating the structure and mechanics of natural nacre. J. Mater. Res. 26, 1203–1215 (2011).

    CAS  Google Scholar 

  168. Bouville, F. et al. Strong, tough and stiff bioinspired ceramics from brittle constituents. Nat. Mater. 13, 508–514 (2014).

    CAS  Google Scholar 

  169. Ashby, M. Materials Selection in Mechanical Design 4th edn (Butterworth–Heinemann, 2010).

    Google Scholar 

  170. Evans, A. G. Perspective on the development of high-toughness ceramics. J. Am. Ceram. Soc. 73, 187–206 (1990).

    CAS  Google Scholar 

  171. Clegg, W. J., Kendall, K., Alford, N. M., Button, T. W. & Birchall, J. D. A simple way to make tough ceramics. Nature 347, 455–457 (1990).

    CAS  Google Scholar 

  172. Cook, J., Gordon, J. E., Evans, C. C. & Marsh, D. M. A mechanism for the control of crack propagation in all-brittle systems. Proc. R. Soc. Lond. A 282, 508–520 (1964).

    Google Scholar 

  173. Kim, J.-K. & Mai, Y.-W. Engineered Interfaces in Fier Reinforced Composites (Elsevier Sciences, 1998).

    Google Scholar 

  174. Yu, H. N., Longana, M. L., Jalalvand, M., Wisnom, M. R. & Potter, K. D. Pseudo-ductility in intermingled carbon/glass hybrid composites with highly aligned discontinuous fibres. Composites, Part A 73, 35–44 (2015).

    CAS  Google Scholar 

  175. Baldan, A. Adhesively-bonded joints and repairs in metallic alloys, polymers and composite materials: adhesives, adhesion theories and surface pretreatment. J. Mater. Sci. 39, 1–49 (2004).

    CAS  Google Scholar 

  176. Gent, A. N. & Lindley, P. B. Internal rupture of bonded rubber cylinders in tension. Proc. R. Soc. Lond. A 249, 195–205 (1959).

    Google Scholar 

  177. Mooney, M. Stress–strain curves of rubbers in simple shear. J. Appl. Phys. 35, 23–26 (1964).

    Google Scholar 

  178. Qin, Z. Dimas, L., Adler, D., Bratzel, G. & Buehler, M. J. Biological materials by design. J. Phys. Condens. Matter 26 073101 (2014).

    Google Scholar 

  179. Mirzaeifar, R., Dimas, L. S., Qin, Z. & Buehler, M. J. Defect-tolerant bioinspired hierarchical composites: simulation and experiment. ACS Biomater. Sci. Eng. 1, 295–304 (2015).

    CAS  Google Scholar 

  180. Dimas, L. S. & Buehler, M. J. Modeling and additive manufacturing of bio-inspired composites with tunable fracture mechanical properties. Soft Matter 10, 4436–4442 (2014).

    CAS  Google Scholar 

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Acknowledgements

Z.Y. was partially supported by a McGill Engineering Doctoral Award from the Faculty of Engineering at McGill University.

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Barthelat, F., Yin, Z. & Buehler, M. Structure and mechanics of interfaces in biological materials. Nat Rev Mater 1, 16007 (2016). https://doi.org/10.1038/natrevmats.2016.7

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