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.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
Nature Communications Open Access 27 July 2021
Mechanical properties of graphene oxide–silk fibroin bionanofilms via nanoindentation experiments and finite element analysis
Friction Open Access 10 April 2021
A novel graphene-based micro/nano architecture with high strength and conductivity inspired by multiple creatures
Scientific Reports Open Access 14 January 2021
Subscribe to Journal
Get full journal access for 1 year
only $9.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Sarikaya, M. & Aksay, I. A. Biomimetic, Design and Processing of Materials (Woodbury, 1995).
Mayer, G. Rigid biological systems as models for synthetic composites. Science 310, 1144–1147 (2005).
Fratzl, P. & Weinkamer, R. Nature's hierarchical materials. Prog. Mater. Sci. 52, 1263–1334 (2007).
Barthelat, F. Biomimetics for next generation materials. Phil. Trans. R. Soc. A 365, 2907–2919 (2007).
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).
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).
Nair, A. K. et al. in Biomineralization Handbook: Characterization of Biomineral and Biomimetic Materials (ed. DiMasi, E. ) 337–349 (CRC Press, 2014).
Ritchie, R. O. The conflicts between strength and toughness. Nat. Mater. 10, 817–822 (2011).
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).
Barthelat, F. Architectured materials in engineering and biology: fabrication, structure, mechanics and performance. Int. Mater. Rev. 60, 413–430 (2015).
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).
Buehler, M. J. Tu(r)ning weakness to strength. Nano Today 5, 379–383 (2010).
Cranford, S. & Buehler, M. J. Biomateriomics (Springer, 2012).
Dunlop, J. W. C., Weinkamer, R. & Fratzl, P. Artful interfaces within biological materials. Mater. Today 14, 70–78 (2011).
Ritchie, R. O., Buehler, M. J. & Hansma, P. Plasticity and toughness in bone. Phys. Today 62, 41–47 (2009).
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).
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).
Yahyazadehfar, M. & Arola, D. The role of organic proteins on the crack growth resistance of human enamel. Acta Biomater. 19, 33–45 (2015).
Wang, R. Z., Suo, Z., Evans, A. G., Yao, N. & Aksay, I. A. Deformation mechanisms in nacre. J. Mater. Res. 16, 2485–2493 (2001).
Barthelat, F. & Espinosa, H. D. An experimental investigation of deformation and fracture of nacre–mother of pearl. Exp. Mech. 47, 311–324 (2007).
Currey, J. D. Mechanical properties of mother of pearl in tension. Proc. R. Soc. Lond. B 196, 443–463 (1977).
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).
Weiner, S. & Wagner, H. D. The material bone: structure mechanical function relations. Annu. Rev. Mater. Sci. 28, 271–298 (1998).
Rho, J. Y., Kuhn-Spearing, L. & Zioupos, P. Mechanical properties and the hierarchical structure of bone. Med. Eng. Phys. 20, 92–102 (1998).
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).
Mayer, G. New classes of tough composite materials — lessons from natural rigid biological systems. Mater. Sci. Eng. C 26, 1261–1268 (2006).
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).
Laaksonen, P., Szilvay, G. R. & Linder, M. B. Genetic engineering in biomimetic composites. Trends Biotechnol. 30, 191–197 (2012).
Studart, A. R. Towards high-performance bioinspired composites. Adv. Mater. 24, 5024–5044 (2012).
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).
Currey, J. D. & Taylor, J. D. The mechanical behavior of some molluscan hard tissues. J. Zool. 173, 395–406 (1974).
Jackson, A. P., Vincent, J. F. V. & Turner, R. M. The mechanical design of nacre. Proc. R. Soc. Lond. B 234, 415–440 (1988).
Colfen, H. & Antonietti, M. Mesocrystals: inorganic superstructures made by highly parallel crystallization and controlled alignment. Angew. Chem. Int. Ed. Engl. 44, 5576–5591 (2005).
Rousseau, M. et al. Multiscale structure of sheet nacre. Biomaterials 26, 6254–6262 (2005).
Marin, F., Le Roy, N. & Marie, B. The formation and mineralization of mollusk shell. Front. Biosci. (Schol. Ed.) 4, 1099–1125 (2012).
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).
Barthelat, F. & Rabiei, R. Toughness amplification in natural composites. J. Mech. Phys. Solids 59, 829–840 (2011).
Rabiei, R., Bekah, S. & Barthelat, F. Failure mode transition in nacre and bone-like materials. Acta Biomater. 6, 4081–4089 (2010).
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).
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).
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).
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).
Shao, C. & Keten, S. Stiffness enhancement in nacre-inspired nanocomposites due to nanoconfinement. Sci. Rep. 5, 16452 (2015).
Barthelat, F., Dastjerdi, A. K. & Rabiei, R. An improved failure criterion for biological and engineered staggered composites. J. R. Soc. Interface 10, 20120849 (2013).
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).
Huang, Z. & Li, X. Nanoscale structural and mechanical characterization of heat treated nacre. Mater. Sci. Eng. C 29, 1803–1807 (2009).
Marin, F., Luquet, G., Marie, B. & Medakovic, D. Molluscan shell proteins: primary structure, origin, and evolution. Curr. Top. Dev. Biol. 80, 209–276 (2008).
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).
Smith, B. L. et al. Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites. Nature 399, 761–763 (1999).
Vincent, J. F. V. & Wegst, U. G. K. Design and mechanical properties of insect cuticle. Arthropod Struct. Dev. 33, 187–199 (2004).
Schaeffer, T. E. et al. Does abalone nacre form by heteroepitaxial nucleation or by growth through mineral bridges? Chem. Mater. 9, 1731–1740 (1997).
Weiss, I. M. Jewels in the pearl. ChemBioChem 11, 297–300 (2010).
Qi, H. J., Ortiz, C. & Boyce, M. C. Mechanics of biomacromolecular networks containing folded domains. J. Eng. Mater. Technol. 128, 509–518 (2006).
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).
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).
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).
Suzuki, M. et al. An acidic matrix protein, Pif, is a key macromolecule for nacre formation. Science 325, 1388–1390 (2009).
Laaksonen, P. et al. Genetic engineering of biomimetic nanocomposites: diblock proteins, graphene, and nanofibrillated cellulose. Angew. Chem. Int. Ed. Engl. 50, 8688–8691 (2011).
Gent, A. N., Suh, J. B. & Kelly, S. G. Mechanics of rubber shear springs. Int. J. Non-Linear Mechan. 42, 241–249 (2007).
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).
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).
Currey, J. D. Bones: Structure and Mechanics (Princeton Univ. Press, 2002).
Wegst, U. G. K. & Ashby, M. F. The mechanical efficiency of natural materials. Philos. Mag. 84, 2167–2181 (2004).
Young, M. F. Bone matrix proteins: their function, regulation, and relationship to osteoporosis. Osteoporosis Int. 14, S35–S42 (2003).
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).
Burr, D. B. The contribution of the organic matrix to bone's material properties. Bone 31, 8–11 (2002).
Reznikov, N., Shahar, R. & Weiner, S. Bone hierarchical structure in three dimensions. Acta Biomater. 10, 3815–3826 (2014).
Buehler, M. J. Nature designs tough collagen: explaining the nanostructure of collagen fibrils. Proc. Natl Acad. Sci. USA 103, 12285–12290 (2006).
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).
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).
Hassenkam, T. et al. High-resolution AFM imaging of intact and fractured trabecular bone. Bone 35, 4–10 (2004).
Buehler, M. J. Molecular nanomechanics of nascent bone: fibrillar toughening by mineralization. Nanotechnology 18 295102 (2007).
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).
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).
Ural, A. & Vashishth, D. Hierarchical perspective of bone toughness — from molecules to fracture. Int. Mater. Rev. 59, 245–263 (2014).
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).
Thurner, P. J. & Katsamenis, O. L. The role of nanoscale toughening mechanisms in osteoporosis. Curr. Osteoporosis Rep. 12, 351–356 (2014).
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).
Taylor, D., Hazenberg, J. G. & Lee, T. C. Living with cracks: damage and repair in human bone. Nat. Mater. 6, 263–268 (2007).
Gupta, H. S. et al. Fibrillar level fracture in bone beyond the yield point. Int. J. Fracture 139, 425–436 (2006).
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).
Gupta, H. S. et al. Nanoscale deformation mechanisms in bone. Nano Lett. 5, 2108–2111 (2005).
Poundarik, A. A. et al. Dilatational band formation in bone. Proc. Natl Acad. Sci. USA 109, 19178–19183 (2012).
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).
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).
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).
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).
Poundarik, A. A. & Vashishth, D. Multiscale imaging of bone microdamage. Connect. Tissue Res. 56, 87–98 (2015).
Hansma, P. K. et al. Sacrificial bonds in the interfibrillar matrix of bone. J. Musculoskelet. Neuronal Interact. 5, 313–315 (2005).
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).
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).
Thompson, J. B. et al. Bone indentation recovery time correlates with bond reforming time. Nature 414, 773–776 (2001).
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).
Thurner, P. J. et al. Osteopontin deficiency increases bone fragility but preserves bone mass. Bone 46, 1564–1573 (2010).
Tai, K., Ulm, F.-J. & Ortiz, C. Nanogranular origins of the strength of bone. Nano Lett. 6, 2520–2525 (2006).
Bailey, A. J. Molecular mechanisms of ageing in connective tissues. Mech. Ageing Dev. 122, 735–755 (2001).
Tang, S. Y., Zeenath, U. & Vashishth, D. Effects of non-enzymatic glycation on cancellous bone fragility. Bone 40, 1144–1151 (2007).
Ker, R. F. Mechanics of tendon, from an engineering perspective. Int. J. Fatigue 29, 1001–1009 (2007).
Puxkandl, R. et al. Viscoelastic properties of collagen: synchrotron radiation investigations and structural model. Phil. Trans. R. Soc. Lond. B 357, 191–197 (2002).
Khayer Dastjerdi, A. & Barthelat, F. Teleost fish scales amongst the toughest collagenous materials. J. Mech. Behav. Biomed. Mater. 52, 95–107 (2015).
Yang, W. et al. Protective role of Arapaima gigas fish scales: structure and mechanical behavior. Acta Biomater. 10, 3599–3614 (2014).
Ascenzi, M.-G. & Roe, A. K. The osteon: the micromechanical unit of compact bone. Front. Biosci. (Landmark Ed.) 17, 1551–1581 (2012).
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).
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).
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).
Ascenzi, A. & Bonucci, E. Shearing properties of single osteons. Anat. Rec. 172, 499–510 (1972).
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).
Dong, X. N., Zhang, X. & Guo, X. E. Interfacial strength of cement lines in human cortical bone. Mech. Chem. Biosyst. 2, 63–68 (2005).
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).
Zioupos, P. & Currey, J. D. The extent of microcracking and the morphology of microcracks in damaged bone. J. Mater. Sci. 29, 978–986 (1994).
Mellon, S. J. & Tanner, K. E. Bone and its adaptation to mechanical loading: a review. Int. Mater. Rev. 57, 235–255 (2012).
Ager, J. W., Balooch, G. & Ritchie, R. O. Fracture, aging, and disease in bone. J. Mater. Res. 21, 1878–1892 (2006).
Piekarsk, K. Fracture of bone. J. Appl. Phys. 41, 215–223 (1970).
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).
Buehler, M. J. & Ackbarow, T. Fracture mechanics of protein materials. Mater. Today 10, 46–58 (2007).
Zhang, Z., Zhang, Y.-W. & Gao, H. On optimal hierarchy of load-bearing biological materials. Proc. R. Soc. B 278, 519–525 (2011).
Peterlik, H., Roschger, P., Klaushofer, K. & Fratzl, P. From brittle to ductile fracture of bone. Nat. Mater. 5, 52–55 (2006).
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).
Gibson, L. J. The hierarchical structure and mechanics of plant materials. J. R. Soc. Interface 9, 2749–2766 (2012).
Jeronimidis, G. J. The fracture behavior of wood and the relations between toughness and morphology. Proc. R. Soc. Lond. B 208, 447–460 (1980).
Gordon, J. E. & Jeronimidis, G. Composites with high work of fracture. Phil. Trans. R. Soc. Lond. A 294, 545–550 (1980).
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).
Fratzl, P. Cellulose and collagen: from fibres to tissues. Curr. Opin. Colloid Interface Sci. 8, 145–155 (2003).
Pilate, G. et al. Lignification and tension wood. C. R. Biol. 327, 889–901 (2004).
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).
Jarvis, M. Cellulose stacks up. Nature 426, 611–612 (2003).
Sinko, R., Qin, X. & Keten, S. Interfacial mechanics of cellulose nanocrystals. MRS Bull. 40, 340–348 (2015).
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).
Salmén, L. Micromechanical understanding of the cell-wall structure. C. R. Biol. 327, 873–880 (2004).
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).
Cousins, W. J. Elasticity of isolated lignin: Young's modulus by a continuous indentation method. N. Z. J. For. Sci. 7, 107–112 (1977).
Cave, I. The anisotropic elasticity of the plant cell wall. Wood Sci. Technol. 2, 268–278 (1968).
Keckes, J. et al. Cell-wall recovery after irreversible deformation of wood. Nat. Mater. 2, 810–814 (2003).
Navi, P., Rastogi, P. K., Gresse, V. & Tolou, A. Micromechanics of wood subjected to axial tension. Wood Sci. Technol. 29, 411–429 (1995).
Spatz, H., Kö hler, L. & Niklas, K. J. Mechanical behaviour of plant tissues: composite materials or structures? J. Exp. Biol. 202, 3269–3272 (1999).
Kohler, L. & Spatz, H. C. Micromechanics of plant tissues beyond the linear-elastic range. Planta 215, 33–40 (2002).
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).
Adler, D. C. & Buehler, M. J. Mesoscale mechanics of wood cell walls under axial strain. Soft Matter 9, 7138–7144 (2013).
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).
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).
Navi, P. & Heger, F. Combined densification and thermo–hydro-mechanical processing of wood. MRS Bull. 29, 332–336 (2004).
Fratzl, P., Burgert, I. & Keckes, J. Mechanical model for the deformation of the wood cell wall. Z. Metallkd. 95, 579–584 (2004).
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).
Åkerholm, M. & Salmén, L. Interactions between wood polymers studied by dynamic FT-IR spectroscopy. Polymer 42, 963–969 (2001).
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).
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).
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).
Thuvander, F. & Berglund, L. A. In situ observations of fracture mechanisms for radial cracks in wood. J. Mater. Sci. 35, 6277–6283 (2000).
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).
United States Department of Agriculture. Wood handbook: wood as an engineering material (Forest Products Laboratory, 1974).
He, M. Y. & Hutchinson, J. W. Crack deflection at an interface between dissimilar elastic materials. Int. J. Solids Struct. 25, 1053–1067 (1989).
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).
Gao, H. J. Application of fracture mechanics concepts to hierarchical biomechanics of bone and bone-like materials. Int. J. Fracture 138, 101–137 (2006).
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).
Evans, A. G. Design and life prediction issues for high-temperature engineering ceramics and their composites. Acta Mater. 45, 23–40 (1997).
Sarikaya, M. An introduction to biomimetics: a structural viewpoint. Microsc. Res. Tech. 27, 360–375 (1994).
Wegst, U. G. K., Bai, H., Saiz, E., Tomsia, A. P. & Ritchie, R. O. Bioinspired structural materials. Nat. Mater. 14, 23–36 (2015).
Munch, E. et al. Tough, bio-inspired hybrid materials. Science 322, 1516–1520 (2008).
Livanov, K. et al. Tough alumina/polymer layered composites with high ceramic content. J. Am. Ceram. Soc. 98, 1285–1291 (2015).
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).
Bonderer, L. J., Studart, A. R. & Gauckler, L. J. Bioinspired design and assembly of platelet reinforced polymer films. Science 319, 1069–1073 (2008).
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).
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).
Mirkhalaf, M., Dastjerdi, A. K. & Barthelat, F. Overcoming the brittleness of glass through bio-inspiration and micro-architecture. Nat. Commun. 5 3166 (2014).
Tang, Z. Y., Kotov, N. A., Magonov, S. & Ozturk, B. Nanostructured artificial nacre. Nat. Mater. 2, 413–418 (2003).
Guan, Z. Supramolecular design in biopolymers and biomimetic polymers for properties. Polym. Int. 56, 467–473 (2007).
Barthelat, F. & Zhu, D. J. A novel biomimetic material duplicating the structure and mechanics of natural nacre. J. Mater. Res. 26, 1203–1215 (2011).
Bouville, F. et al. Strong, tough and stiff bioinspired ceramics from brittle constituents. Nat. Mater. 13, 508–514 (2014).
Ashby, M. Materials Selection in Mechanical Design 4th edn (Butterworth–Heinemann, 2010).
Evans, A. G. Perspective on the development of high-toughness ceramics. J. Am. Ceram. Soc. 73, 187–206 (1990).
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).
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).
Kim, J.-K. & Mai, Y.-W. Engineered Interfaces in Fier Reinforced Composites (Elsevier Sciences, 1998).
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).
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).
Gent, A. N. & Lindley, P. B. Internal rupture of bonded rubber cylinders in tension. Proc. R. Soc. Lond. A 249, 195–205 (1959).
Mooney, M. Stress–strain curves of rubbers in simple shear. J. Appl. Phys. 35, 23–26 (1964).
Qin, Z. Dimas, L., Adler, D., Bratzel, G. & Buehler, M. J. Biological materials by design. J. Phys. Condens. Matter 26 073101 (2014).
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).
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).
Z.Y. was partially supported by a McGill Engineering Doctoral Award from the Faculty of Engineering at McGill University.
The authors declare no competing interests.
About this article
Cite this article
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
This article is cited by
A numerical study to assess the role of pre-stressed inclusions on enhancing fracture toughness and strength of periodic composites
International Journal of Fracture (2023)
Biologically enhanced 3D printed micro-nano hybrid scaffolds doped with abalone shell for bone regeneration
Advanced Composites and Hybrid Materials (2023)
All-natural bioinspired nanolignocellulose-derived bulk engineering materials with excellent mechanical properties and environmental stability
Bioinspiration: Pull-Out Mechanical Properties of the Jigsaw Connection of Diabolical Ironclad Beetle’s Elytra
Acta Mechanica Solida Sinica (2022)
Printable, castable, nanocrystalline cellulose-epoxy composites exhibiting hierarchical nacre-like toughening