Microstructure and mechanical properties of an alpha keratin bovine hoof wall

Highlights

• Fracture toughness and microstructure of the bovine hoof wall are investigated.

• Relations between the fracture toughness and the orientation/moisture content are obtained.

• The bovine hoof wall is characterized by the tubular structure and the arrangement of layers.

• A hypothetical model of the bovine hoof wall is proposed.

Abstract

Bovine hoof wall with an alpha keratin structure, as the interface between the ground and the body, can protect the bony skeleton from the impact and the destruction. Microstructure and mechanical properties of the bovine hoof wall are investigated by scanning electron microscope (SEM), transmission electron microscope (TEM) and quasi-static mechanical tests. Mechanical results show that the mean J-integral values of the LD specimens parallel to the tubular axis are higher than those of the TD specimens normal to the tubular axis, and the fracture toughness reaches the peak values (21 kJ/m², 33 kJ/m² for the TD and the LD specimens, respectively) at 16.5% moisture content. The morphology results show that the laminated keratin structure can form the extensive strain-transition interfaces and the tubules played an important role in twisting crack propagation. Angles of the laminated structures within the inter-tubular materials are not a uniform distribution varying from 0° to 90° against to the tubular axis. The interlocking interface in the tubular structure can provide increased the contact area and contribute to the bonding strength between the layers. We also propose models to illustrate the morphological structure and the crack propagation mechanism of the bovine hoof wall. This structure with the strong fracture resistance ability will provide a new inspiration for design of structural materials and architectures.

Introduction

After billions years of development, evolution of the biological materials has approached perfection, e.g. optimally refined multiscale, hierarchical structures, excellent mechanical properties and adaptability, self-healing ability (Buehler et al., 2008; Lee et al., 2011; Chen et al., 2012). These specific functions and unique structures of biomaterials can provide scientists the interesting inspiration to design new structural and functional materials. Salinas et al. (2017) found that the Gastropods shells’ precision control of the mineral and organic components within four-layer crossed lamellar structure offered a four-order of magnitude increase in the fracture toughness versus the abiotic aragonite. Suksangpanya et al. (2018) researched the high damage resistance of the Bouligand structure and found that the crack twisting, driven by the fiber architecture within a helicoidal biomimetic composite specimen, was the main fracture mechanisms. Sullivan et al. (2016) revealed the structure-function relationships within the seagull feather vane, and simplified the complex mechanism of the barbs and the interlocking. Huang et al. (2019) identified a thorough characterization of the hierarchical structure as well as the energy dissipation mechanisms of the equine hoof wall, and these findings could provide inspirations on design of the impact resistant and energy absorbent materials.

Most biological materials are multifunctional, and the hoof is a noteworthy example. As the interface between the ground and the body, the bovine hoof walls support the heavy body, and provide physical protection for the soft organs and prevent the skeletal bones from the impact and the destruction. It is known that the hoof wall cannot be repaired or remodeled once it is keratinized (Wang et al., 2016a), and can partly recover from the certain damages (Kasapi and Gosline, 1997). However, the hooves can withstand high repeated impact and do not generate any damage for the skeletal bones during galloping run.

Many scientists are devoted into studying the microstructure of the hoof. Researchers have proved that the main constituents of the hoof wall are α-keratin and keratinized cells (Wang et al., 2016a). The α-keratin is composed of α-helices bundling into a super-helix coiled-coil in some mammal's structure, such as hair (Yu et al., 2017), nails (Farran et al., 2009) and scales (Wang et al., 2016b). The α-helix chain units form a dimer with sulfur cross-links and assemble to form protofilaments, and then get together to form the intermediate filaments (IFs, ~7 nm in diameter (Wang et al., 2016a)). The IFs embedded in a sulfur-rich amorphous keratin matrix become the tubules and the inter-tubular materials (David and North, 1998). Buehler and Ackbarow (2007) used the large-scale atomistic and molecular model to demonstrate the deformation and the fracture of the IFs. What's more, the Ashby map (Wegst and Ashby, 2004) shows that the keratin is one of the toughest biological materials that have high toughness and modulus. This is a very interesting object that the keratin mainly containing organic proteins rather stronger than the other biological materials compositing with high mineral content, e.g. teeth. In addition, Baillie and Fiford (1996) described the structure of the bovine hooves as the tubules embedded into the inter-tubular materials. Franck et al. (2006), Clark and Petrie (2007) believed that the structure of the bovine hoof was partly similar to the equine hoof.

There are several papers presenting mechanical properties of the hoof walls. Douglas et al. (1996) measured the Young's modulus (E) of the equine hoof walls by the unidirectional tension test. The mean Young's modulus of the outer and the inner walls' specimens for the dorsal parts were 955 MPa and 502 MPa at 30% moisture content, respectively. And the Young's modulus of the medial and the lateral parts specimens were 607 MPa and 657 MPa, respectively, which were slightly equal to the average values of the inner and the outer walls for the dorsal part. Bertram and Gosline (1987, 1986) tested the fracture toughness of the equine hoof walls, and found that the maximum J-integral toughness was 22.8 kJ/m² at 75% relative humidity. It was much higher than that of the fresh bone (1.0–3.0 kJ/m² (Wright and Hayes, 1977)). It can be inferred that the hoof wall keratin had an excellent fracture-resistant ability. Magdalena et al. (2015) successfully used the finite element simulation method to build a model of an equine hoof and simulated its physical properties. However, there are few articles mentioned the mechanical properties of the bovine hoof walls.

This work aims to investigate the fracture toughness of the bovine hoof wall, especially the effects of the orientation and the moisture content, and to obtain the relationship between the morphological structure and the crack propagation in the bovine hoof wall, and to understand the essence of the α-keratin bovine hoof walls and except to use feasible methods and materials for bionic application.