Biomimetic Structural Materials: Inspiration from Design and Assembly.

Nature assembles weak organic and inorganic constituents into sophisticated hierarchical structures, forming structural composites that demonstrate impressive combinations of strength and toughness. Two such composites are the nacre structure forming the inner layer of many mollusk shells, whose brick-and-mortar architecture has been the gold standard for biomimetic composites, and the cuticle forming the arthropod exoskeleton, whose helicoidal fiber-reinforced architecture has only recently attracted interest for structural biomimetics. In this review, we detail recent biomimetic efforts for the fabrication of strong and tough composite materials possessing the brick-and-mortar and helicoidal architectures. Techniques discussed for the fabrication of nacre- and cuticle-mimetic structures include freeze casting, layer-by-layer deposition, spray deposition, magnetically assisted slip casting, fiber-reinforced composite processing, additive manufacturing, and cholesteric self-assembly. Advantages and limitations to these processes are discussed, as well as the future outlook on the biomimetic landscape for structural composite materials.

A natural energy absorbent polymer composite: The equine hoof wall.

The equine hoof has been considered as an efficient energy absorption layer that protects the skeletal elements from impact when galloping. In the present study, the hierarchical structure of a fresh equine hoof wall and the energy absorption mechanisms are investigated. Tubules are found embedded in the intertubular matrix forming the hoof wall at the microscale. Both tubules and intertubular areas consist of keratin cells, in which keratin crystalline intermediate filaments (IFs) and amorphous keratin fill the cytoskeletons. Cell sizes, shapes and IF fractions are different between tubular and intertubular regions. The structural differences between tubular and intertubular areas are correlated to the mechanical behavior of this material tested in dry, fresh and fully hydrated conditions. The stiffness and hardness in the tubule areas are higher than that in the intertubular areas in the dry and fresh samples when loaded along the hoof wall; however, once the samples are fully hydrated, the intertubular areas become stiffer than the tubular areas due to higher water absorption in these regions. The compression behavior of hoof in different loading speed and directions are also examined, with the isotropy and strain-rate dependence of mechanical properties documented. In the hoof walls, mechanistically the tubules serve as a reinforcement, which act to support the entire wall and prevent catastrophic failure under compression and impact loading. Elastic buckling and cracking of the tubules are observed after compression along the hoof wall, and no shear-banding or severe cracks are found in the intertubular areas even after 60% compression, indicating the highly efficient energy absorption properties, without failure, of the hoof wall structure. STATEMENT OF SIGNIFICANCE: The equine hoof wall is found to be an efficient energy absorbent natural polymer composite. Previous studies showed the microstructure and mechanical properties of the hoof wall in some perspective. However, the hierarchical structure of equine hoof wall from nano- to macro-scale as well as the energy absorption mechanisms at different strain rates and loading orientations remains unclear. The current study provides a thorough characterization of the hierarchical structure as well as the correlation between structure and mechanical behaviors. Energy dissipation mechanisms are also identified. The findings in the current research could provide inspirations on the designs of impact resistant and energy absorbent materials.

A comparative analysis of the avian skull: Woodpeckers and chickens.

Woodpeckers peck at trees without any reported brain injury despite undergoing high impact loads. Amongst the adaptations allowing this is a highly functionalized impact-absorption system consisting of the head, beak, tongue and hyoid bone. This study aims to examine the anatomical structure, composition, and mechanical properties of the skull to determine its potential role in energy absorption and dissipation. An acorn woodpecker and a domestic chicken are compared through micro-computed tomography to analyze and compare two- and three-dimensional bone morphometry. Optical and scanning electron microscopy with energy dispersive X-ray spectroscopy are used to identify the structural and chemical components. Nanoindentation reveals mechanical properties along the transverse cross-section, normal to the direction of impact. Results show two different strategies: the skull bone of the woodpecker shows a relatively small but uniform level of closed porosity, a higher degree of mineralization, and a higher cortical to skull bone ratio. Conversely, the chicken skull bone shows a wide range of both open and closed porosity (volume fraction), a lower degree of mineralization, and a lower cortical to skull bone ratio. This structural difference affects the mechanical properties: the skull bones of woodpeckers are slightly stiffer than those of chickens. Furthermore, the Young's modulus of the woodpecker frontal bone is significantly higher than that of the parietal bone. These new findings may be useful to potential engineered design applications, as well as future work to understand how woodpeckers avoid brain injury.

Twisting cracks in Bouligand structures.

The Bouligand structure, which is found in many biological materials, is a hierarchical architecture that features uniaxial fiber layers assembled periodically into a helicoidal pattern. Many studies have highlighted the high damage-resistant performance of natural and biomimetic Bouligand structures. One particular species that utilizes the Bouligand structure to achieve outstanding mechanical performance is the smashing Mantis Shrimp, Odontodactylus Scyllarus (or stomatopod). The mantis shrimp generates high speed, high acceleration blows using its raptorial appendage to defeat highly armored preys. The load-bearing part of this appendage, the dactyl club, contains an interior region [16] that consists of a Bouligand structure. This region is capable of developing a significant amount of nested twisting microcracks without exhibiting catastrophic failure. The development and propagation of these microcracks are a source of energy dissipation and stress relaxation that ultimately contributes to the remarkable damage tolerance properties of the dactyl club. We develop a theoretical model to provide additional insights into the local stress intensity factors at the crack front of twisting cracks formed within the Bouligand structure. Our results reveal that changes in the local fracture mode at the crack front leads to a reduction of the local strain energy release rate, hence, increasing the necessary applied energy release rate to propagate the crack, which is quantified by the local toughening factor. Ancillary 3D simulations of the asymptotic crack front field were carried out using a J-integral to validate the theoretical values of the energy release rate and the local stress intensity factors.

Microstructural and geometric influences in the protective scales of Atractosteus spatula.

Atractosteus spatula has been described as a living fossil (having existed for 100 Myr), retaining morphological characteristics of early ancestors such as the ability to breathe air and survive above water for hours. Its highly effective armour consists of ganoid scales. We analyse the protective function of the scales and identify key features which lead to their resistance to failure. Microstructural features include: a twisted cross-plied mineral arrangement that inhibits crack propagation in the external ganoine layer, mineral crystals that deflect cracks in the bony region in order to activate the strength of mineralized collagen fibrils, and saw-tooth ridges along the interface between the two scale layers which direct cracks away from the intrinsically weak interface. The macroscale geometry is additionally evaluated and it is shown that the scales retain full coverage in spite of minimal overlap between adjacent scales while conforming to physiologically required strain and maintaining flexibility via a process in which adjacent rows of scales slide and concurrently reorient.

Structural analysis of the tongue and hyoid apparatus in a woodpecker.

UNLABELLED: Woodpeckers avoid brain injury while they peck at trees up to 20Hz with speeds up to 7m/s, undergoing decelerations up to 1200g. Along with the head, beak and neck, the hyoid apparatus (tongue bone and associated soft tissues) is subjected to these high impact forces. The shape of the hyoid apparatus is unusual in woodpeckers and its structure and mechanical properties have not been reported in detail. High-resolution X-ray micro-computed tomography and scanning electron microscopy with energy dispersive X-ray spectroscopy were performed and correlated with nanoindentation mapping. The hyoid apparatus has four distinct bone sections, with three joints between these sections. Nanoindentation results on cross-sectional regions of each bone reveal a previously unreported structure consisting of a stiff core and outer, more compliant shell with moduli of up to 27.4GPa and 8.5GPa, respectively. The bending resistance is low at the posterior section of the hyoid bones, indicating that this region has a high degree of flexibility to absorb impact. These new structural findings can be applied to further studies on the energy dissipation of the woodpecker during its drumming behavior, and may have implications for the design of engineered impact-absorbing structures. STATEMENT OF SIGNIFICANCE: Woodpeckers avoid brain injury while they peck at trees, which results in extreme impact conditions. One common adaptation in woodpeckers is the unusual shape of the elongated tongue, also called the hyoid apparatus. The relationship between the structure and mechanical properties of the bony part of the hyoid apparatus has not been previously reported. A three dimensional model of the bony tongue was developed, and the hardness and stiffness were evaluated. A new type of bone structure, which is opposite of typical skeletal bone structure was found. The combined microstructural and mechanical property analysis indicate possible energy absorption routes for the hyoid apparatus and are applicable to the design of engineered structures.

A Sinusoidally Architected Helicoidal Biocomposite.

A fibrous herringbone-modified helicoidal architecture is identified within the exocuticle of an impact-resistant crustacean appendage. This previously unreported composite microstructure, which features highly textured apatite mineral templated by an alpha-chitin matrix, provides enhanced stress redistribution and energy absorption over the traditional helicoidal design under compressive loading. Nanoscale toughening mechanisms are also identified using high-load nanoindentation and in situ transmission electron microscopy picoindentation.