Structure-property relationships of velar bone tissue from the energy absorbing horncore of bighorn sheep rams

The bony horncore of bighorn sheep absorbs substantial energy during head-to-head impacts which reduces brain cavity accelerations and helps protect the brain from injury [1]. Despite this finding, investigations on the properties of bovid horncore bone are few [2,3]. One study on the horncore bone of the common eland demonstrated that mechanical properties are highest at the proximal base of the horn, where contact and bending stresses from combat are at a maximum [2]. In another study, cortical bone from the horncore of bighorn sheep was found to be similar in toughness to other cortical bone tissues, suggesting it does not offer an advantage for energy absorption during ramming [3]. However, most of the bighorn sheep horncore consists of a unique bone material referred to as velar bone [4]. Within the volume of the entire horncore, velar bone has a similar bone volume fraction to mammalian trabecular bone (∼20%), but larger sail thickness (2.87 ± 0.78 mm) and separation (11.91 ± 0.88 mm) compared to analogous measures of trabecular strut thickness (0.12 ± 0.02 mm) and separation (0.57 ± 0.08 mm) in the proximal tibia of grizzly bears [4]. The solid portions of velar bone are also more sail-like in morphology compared to the strut-like features of trabeculae bone (Figure 1) [4]. Trabecular bone is found extensively in various mammalian bones, but velar bone is unknown to exist outside of bovid horncore bone, suggesting it may be adapted specifically for the unique mechanical function of protecting the brain during intraspecific combat. The material behavior of velar bone tissue has not been characterized despite its apparent role in injury mitigation during high-impact head butting. Quantification of velar bone tissue microstructure, composition, and mechanical properties will provide insight into the high energy absorption mechanisms of horncore bone and improve computational modeling of bighorn sheep ramming.

Previous studies of bone tissue have extensively demonstrated phenotypic plasticity (short-term) and evolutionary (long-term) functional adaptations to mechanical loading [5], [6], [7], [8], [9], [10]. Short term remodeling processes respond to external loading to alter whole bone geometry and tissue level microstructure to maintain physiological strain magnitudes [5], [6], [7], [8]. Intracortical remodeling produces secondary osteons with cement line boundaries that arrest and deflect propagating cracks to toughen bone [11], [12], [13], [14], [15]. These toughening mechanisms are particularly effective in bone tissue since remodeling also allows bone to repair microdamage to mitigate damage accumulation and the risk of catastrophic failure. This may be one advantage of rams absorbing large amounts of energy via the bony horncore instead of the impacted horn, since the avascular horn cannot repair itself once damaged. Bone is a composite material with a mineral phase that contributes to strength and stiffness and a protein phase that contributes to ductility and toughness. There is evidence that long-term evolutionary adaptation has resulted in specialized bones with tissue compositions that are well suited to meet specific functional demands. For example, compared to femoral bone, antler bone has reduced mineral content that provides increased work-to-fracture which is beneficial for supporting the high stresses generated during combat [9,10]. Furthermore, the composite nature of bone results in viscoelastic material properties such as strain rate sensitivity. Bone becomes stiffer and more brittle as loading rates increase, which plays a role in traumatic fractures from impacts (e.g., falls or car crashes) [16], [17], [18]. Based on the evolutionary adaptation of bone tissue demonstrated previously, it is possible that velar bone has a unique composition that provides superior energy absorption under impact loading.

Since osteons effectively toughen bone tissue and bone composition can adapt to its mechanical environment, it is possible that horncore velar bone has a unique microstructure and composition that provide efficient material-level energy absorption to mitigate brain injury during ramming. We hypothesized that the modulus of toughness is positively correlated with osteon population density in velar bone. Additionally, we hypothesized the modulus of toughness and damping factor are negatively correlated with bone mineral content in velar bone. The aims of this study were to quantify the microstructure, composition, and mechanical properties of velar bone at the tissue-level, and compare them to similar measures published for other mammalian bone tissues. This work increases our understanding of unique mechanical adaptations in bone tissue [19,20], improves our ability to computationally model bighorn sheep ramming [1,21], and provides insight for bioinspired design of energy absorbing materials for impact applications [22,23].

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