▪ Abstract The term bone refers to a family of materials, all of which are built up of mineralized collagen fibrils. They have highly complex structures, described in terms of up to 7 hierarchical levels of organization. These materials have evolved to fulfill a variety of mechanical functions, for which the structures are presumably fine-tuned. Matching structure to function is a challenge. Here we review the structure-mechanical relations at each of the hierarchical levels of organization, highlighting wherever possible both underlying strategies and gaps in our knowledge. The insights gained from the study of these fascinating materials are not only important biologically, but may well provide novel ideas that can be applied to the design of synthetic materials.

THE MATERIAL BONE: Structure-Mechanical Function Relations

Biological materials: Structure and mechanical properties

Materials that are strong, ultralightweight, and tough are in demand for a range of applications, requiring architectures and components carefully designed from the micrometer down to the nanometer scale. Nacre, a structure found in many molluscan shells, and bone are frequently used as examples for how nature achieves this through hybrid organic-inorganic composites. Unfortunately, it has proven extremely difficult to transcribe nacre-like clever designs into synthetic materials, partly because their intricate structures need to be replicated at several length scales. We demonstrate how the physics of ice formation can be used to develop sophisticated porous and layered-hybrid materials, including artificial bone, ceramic-metal composites, and porous scaffolds for osseous tissue regeneration with strengths up to four times higher than those of materials currently used for implantation.

http://science.sciencemag.org/content/sci/311/5760/515.full.pdf

Freezing as a path to build complex composites.

Natural materials such as bone, tooth, and nacre are nanocomposites of proteins and minerals with superior strength. Why is the nanometer scale so important to such materials? Can we learn from this to produce superior nanomaterials in the laboratory? These questions motivate the present study where we show that the nanocomposites in nature exhibit a generic mechanical structure in which the nanometer size of mineral particles is selected to ensure optimum strength and maximum tolerance of flaws (robustness). We further show that the widely used engineering concept of stress concentration at flaws is no longer valid for nanomaterial design.

https://www.pnas.org/content/pnas/100/10/5597.full.pdf

Materials become insensitive to flaws at nanoscale: lessons from nature.

Extended and oriented nanostructures are desirable for many applications, but direct fabrication of complex nanostructures with controlled crystalline morphology, orientation and surface architectures remains a significant challenge. Here we report a low-temperature, environmentally benign, solution-based approach for the preparation of complex and oriented ZnO nanostructures, and the systematic modification of their crystal morphology. Using controlled seeded growth and citrate anions that selectively adsorb on ZnO basal planes as the structure-directing agent, we prepared large arrays of oriented ZnO nanorods with controlled aspect ratios, complex film morphologies made of oriented nanocolumns and nanoplates (remarkably similar to biomineral structures in red abalone shells) and complex bilayers showing in situ column-to-rod morphological transitions. The advantages of some of these ZnO structures for photocatalytic decompositions of volatile organic compounds were demonstrated. The novel ZnO nanostructures are expected to have great potential for sensing, catalysis, optical emission, piezoelectric transduction, and actuations.

Complex and oriented ZnO nanostructures

Mother-of-pearl (nacre) is a platelet-reinforced composite, highly filled with calcium carbonate (aragonite). The Young modulus, determined from beams of a span-to-depth ratio of no less than 15 (a necessary precaution), is of the order of 70 GPa (dry) and 60 GPa (wet), much higher than previously recorded values. These values can be derived from ‘shear-lag’ models developed for platey composites, suggesting that nacre is a near-ideal material. The tensile strength of nacre is of the order of 170 MPa (dry) and 140 MPa (wet), values which are best modelled assuming that pull-out of the platelets is the main mode of failure. In three-point bending, depending on the span-to-depth ratio and degree of hydration, the work to fracture across the platelets varies from 350 to 1240 J m -2 . In general, the effect of water is to increase the ductility of nacre and increase the toughness almost tenfold by the associated introduction of plastic work. The pull-out model is sufficient to account for the toughness of dry nacre, but accounts for only a third of the toughness of wet nacre. The additional contribution probably comes from debonding within the thin layer of matrix material. Electron microscopy reveals that the ductility of wet nacre is caused by cohesive fracture along platelet lamellae at right angles to the main crack. The matrix appears to be well bonded to the lamellae, enabling the matrix to be stretched across the delamination cracks without breaking, thereby sustaining a force across a wider crack. Such a mechanism also explains why toughness is dependent on the span-to-depth ratio of the test piece. With this last observation as a possible exception, nacre does not employ any really novel mechanisms to achieve its mechanical properties. It is simply ‘well made’. The importance of nacre to the mollusc depends both on the material and the size of the shell. Catastrophic failure will be very likely in whole, undamaged shells which behave like unnotched beams at large span-to-depth ratios. This tendency is increased by the fact that predators act as ‘soft’ machines and store strain energy which can be fed into the material very quickly once the fracture stress has been reached. It may therefore be advantageous to have a shell made of an intrinsically less tough material which is better at stopping cracks (e. g. crossed lamellar). However, nacre may still be preferred for the short, thick shells of young molluscs, as these have a low span-to-depth ratio and can make better use of ductility mechanisms.

The Mechanical Design of Nacre

Mother-of-pearl, the highly filled ceramic composite of mollusc shell, is compared with other, less highly filled, artificial ceramics. Stiffness is fairly simply related to volume fraction of ceramic, but no model seems to be adequate to describe this relationship. Strength, stress-intensity factor and the work of fracture are also dependent on the ceramic content but in a much more complex manner. Nacre has the highest value for all these parameters.

A. P. Jackson

Papers

The Mechanical Design of Nacre

Comparison of nacre with other ceramic composites

A physical model of nacre

Application of surface analytical techniques to the study of fracture surfaces of mother-of-pearl