Elsevier

Bone

Volume 44, Issue 6, June 2009, Pages 1105-1110
Bone

Inhomogeneous fibril stretching in antler starts after macroscopic yielding: Indication for a nanoscale toughening mechanism

https://doi.org/10.1016/j.bone.2009.02.009Get rights and content

Abstract

Antler is a unique mineralized tissue, with extraordinary toughness as well as an ability to annually regenerate itself in its entirety. The high fracture resistance enables it to fulfill its biological function as a weapon and defensive guard during combats between deer stags in the rutting season. However, very little is quantitatively understood about the structural origin of the antler's high toughness. We used a unique combination of time-resolved synchrotron small angle X-ray diffraction together with tensile testing of antler cortical tissue under physiologically wet conditions. We measured the deformation at the nanoscale from changes in the meridional diffraction pattern during macroscopic stretch-to-failure tests. Our results show that on average fibrils are strained only half as much as the whole tissue and the fibril strain increases linearly with tissue strain, both during elastic and inelastic deformation. Most remarkably, following macroscopic yielding we observe a straining of some fibrils equal to the macroscopic tissue strain while others are hardly stretched at all, indicating an inhomogeneous fibrillar strain pattern at the nanoscale. This behavior is unlike what occurs in plexiform bovine bone and may explain the extreme toughness of antler compared to normal bone.

Introduction

Antlers are found in most deer species, but unlike keratin-covered horns, they are made solely of bone tissue (mineralized collagen) [1]. All antlers have main beams and occasionally side tines (branching from the main beam) and all are built of a compact cortical shell, surrounding a trabecular tissue, which fills the entire beam and tines. Similar to other bones they are composed of protein (mainly collagen type I) mineral (carbonated hydroxyapatite) and water. However, antlers contain 30–35 wt.% organic substance which is markedly higher than in bone (20–30 wt.%) and 55–60 wt.% mineral which is lower than the mineral content of bone (60–70 wt.%) [2]. Such a difference in composition is known to have a significant effect on the elastic deformation behavior of biomineralized tissues: bending tests of bones from various species show that the Young's modulus and hence the stiffness correlates positively with the mineral content of bone [3], [4].

The most distinctive feature of antler bone is that it is also a remarkably tough mineralized tissue [2], [5], [6]. The magnitude of a material's toughness is determined by the ability of the material to sustain inelastic deformation and the amount of energy dissipated thereby. Examples of structural toughening mechanisms at the micrometer scale are microcracking or crazing in polymers [7], where the energy given to the system is dissipated by the formation of new surfaces. The occurrence of microcracks in bone and its importance for the toughening in the inelastic deformation is well known [8], [9], [10]. The ability to form microcracks during in vitro mechanical loading however, varies in bones of different species, as shown for human and bovine cortical bone as well as for red deer antler [11], [12] where antler showed the most microcracks followed by bovine bone and human bone. Moreover, a higher number of microcracks in bovine bone were shown to correlate with higher fracture toughness compared with human bone [8].

However, little is known about toughening mechanisms at the nanoscale. The basic building block of bone at this hierarchical level is the mineralized collagen fibril, known to be a staggered periodic assemblage of collagen molecules [13], [14]. The mineral platelets within the collagen fibrils are arranged in layers with their main axis parallel to the long axis of the fibril [15]. Recent work has considered the importance of nanoscale deformation mechanisms in bone. It has been shown that in bovine fibrolamellar bone strains gradually decrease with lower hierarchical levels, suggesting that shearing occurs between the building blocks at the nanoscale [16], [17], [18]. However the extreme toughness of antler suggests that previously unexplored toughening mechanisms might play an important role. Indeed, shearing alone cannot explain the remarkable response to load of such bone as antler.

In this study we take a closer look at the inelastic deformation of antler samples, and study the process of load re-distribution in the tissue. We carried out in situ micromechanical tensile testing on compact antler bone while acquiring time resolved small-angle X-ray diffraction patterns (SAXD). We were thus able to track, simultaneously, strains at the macroscale (tissue level) and nanoscale (fibril level), as described in [17], [19]. We show that on average fibrils take up only half of the tissue strain, and that during inelastic deformation a progressive inhomogeneous fibril stretching takes place.

Section snippets

Sample preparation

Samples were extracted from antlers of a 1.5 year old Iberian red deer (Cervus elaphus hispanicus). The antlers were fully developed (Fig. 1), having been cut off at the beginning of the rutting season, and allowed to dry under ambient conditions for several months. Because recent studies have shown that the management of the deer (mainly nutrition and health treatments) greatly affects both composition and mechanical properties at the macroscopic length scale [20], [21], animals were chosen

Results

A typical evolution of the width and height of the 3rd-order collagen peak at three different stress levels is shown in Fig. 3. The inset shows the corresponding stress–strain curve, indicating the respective values for tissue stress and strain. In the unloaded state the majority of fibrils exhibit a peak position q0 around 0.2865 nm 1, which corresponds to a meridional D-spacing of 65.8 nm. With rising tissue stress the collagen peak shifts to lower values of the scattering vector which is a

Discussion

Antlers are well known for their remarkable fracture toughness, and our findings reveal important information about the nanostructural mechanisms involved. We show that when an external load is applied, an initial uniform stretching of all fibrils in an elastic manner evolves into inhomogeneous fibril strain that is observed following macroscopic yielding. Prior to yielding, all fibrils stretch about half the tissue strain, whereas after yielding some fibrils feel almost no strain while others

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    Current address: School of Engineering and Materials Science, Queen Mary University of London, Mile End Road, London E1 4NS, UK.

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