The fracture mechanics of biological and bioinspired materials

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troduction Nature is well ahead of engineers in terms of sophistication and efficiency in making tough materials.1 While stiff materials are generally hard,2 high toughness usually comes at the expense of hardness.3 Fracture toughness, the ability of a material to resist crack propagation, is critical to achieve high tensile strength, reliability, robustness, damage tolerance, and notch performance (i.e., the suppression of stress concentra­ tions at the notch to delay failure). Fracture toughness is meas­ ured by mechanically loading a sample to propagate a crack from an initial notch (Figure 1a). Depending on the loading condition, sample geometry, and material, crack propagation may be stable or unstable (catastrophic), and it may follow a straight or convoluted path. Figure 1b shows typical crack­resistance curves for nacre from mollusk shells, for human cortical bone, and for human tooth enamel. In these materials, the toughness increases as the crack advances, and the maximum toughness is 2–6 times higher than the crack initiation toughness. This rise in crack resistance (or “R­curve behavior”) is due to powerful tough­ ening mechanisms such as process zone toughening and crack bridging that are activated upon crack propagation. Rising crack resistance is key to damage tolerance, because any crack that may propagate from defects or microdamage in the material will be immediately stabilized. The toughness of these biological materials is similar to high performance engi­ neering ceramics (for comparison the toughness of aluminum

oxide is about 3.5 MPa m1/2),4 which is striking considering that hard biological materials are built from relatively weak components: soft biopolymers (proteins, polysaccharides) and biominerals (calcium carbonate, hydroxyapatite). While many engineering materials (metals, composites) are stiffer and tougher than natural materials, the “amplification” of toughness found in natural materials compared to their based constituents is currently not matched by any engineering materials5–10 (Figure 1c).2,11–13

Toughening mechanisms in biological materials A multitude of compositions, architectures, and fracture mechanisms have been reported in biological materials over the past 30 years. More recent efforts have identified construc­ tion rules and micromechanisms, which are universal in the biological world14 and transcend the boundaries of the animal species.

Building blocks and architecture In mineralized tissues, minerals are in the form of building blocks that are joined by softer interfaces and matrices, form­ ing complex three­dimensional (3D) architectures. A notable example is nacre, the material of pearls, which is commonly found on the inner shell layer of many mollusks and snails. In nacre, the mineral building blocks are microscopic aragonite tablets joined by nanometer­thick biopolymer mortar to form a 3D brick wall (Figure 1e). In tooth enamel, the building

J. William Pro, McGill University, Canada; [email protected] Francois Barthelat, McGill University, Canada; francois.