Editorial: Determinants of mammalian feeding system design

Knowledge of the variation in the elastic properties of mandibular cortical bone is essential for modeling bone function. Our aim was to characterize the elastic properties of rhesus macaque mandibular cortical bone and compare these to the elastic properties from mandibles of dentate humans and baboons. Thirty cylindrical samples were harvested from each of six adult female rhesus monkey mandibles. Assuming orthotropy, axes of maximum stiffness in the plane of the cortical plate were derived from ultrasound velocity measurements. Further velocity measurements with longitudinal and transverse ultrasonic transducers along with measurements of bone density were used to compute three-dimensional cor-tical elastic properties using equations based on Hooke's law. Results showed regional variations in the elastic properties of macaque mandibular cortical bone that have both similarities and differences with that of humans and baboons. So far, the biological and structural basis of these differences is poorly understood.

American Journal of Physical Anthropology, 2000

One important limitation of mechanical analyses with strain gages is the difficulty in directly estimating patterns of stress or loading in skeletal elements from strain measurements. Because of the inherent anisotropy in cortical bone, orientation of principal strains and stresses do not necessarily coincide, and it has been demonstrated theoretically that such differences may be as great as 45°(Cowin and Hart, 1990). Likewise, relative proportions of stress and strain magnitudes may differ. This investigation measured the elastic properties of a region of cortical bone on both the buccal and lingual surfaces of the lower border of the macaque mandible. The elastic property data was then combined with macaque mandibular strain data from published and a new in vivo strain gage experiment to determine directions and magnitudes of maximum and minimum principal stresses. The goal was to compare the stresses and strains and assess the differences in orientation and relative magnitude between them. The main question was whether these differences might lead to different interpretations of mandibular function. Elastic and shear moduli, and Poisson's ratios were measured using an ultrasonic technique from buccal and lingual cortical surfaces in 12 macaque mandibles. Mandibular strain gage data were taken from a published set of experiments , and from a new experiment in which rosette strain gauges were fixed to the buccal and lingual cortices of the mandibular corpus of an adult female Macaca fascicularis, after which bone strain was recorded during mastication. Averaged elastic properties were combined with strain data to calculate an estimate of stresses in the mandibular corpus. The elastic properties were similar to those of the human mandibular cortex. Near its lower border, the macaque mandible was most stiff in a longitudinal direction, less stiff in an inferosuperior direction, and least stiff in a direction normal to the bone's surface. The lingual aspect of the mandible was slightly stiffer than the buccal aspect. Magnitudes of stresses calculated from average strains ranged from a compressive stress of Ϫ16.00 GPa to a tensile stress of 8.84 GPa. The orientation of the principal stresses depended on whether the strain gage site was on the working or balancing side. On the balancing side of the mandibles,

Zoology, 2017

Highlights  The elastic properties of rhesus macaque mandibular cortical bone are characterized.  They are compared to the elastic properties from mandibles of dentate humans and baboons.  There are regional variations in the elastic properties of macaque mandibular cortical bone.  There are both similarities and differences with those of humans and baboons.  The biological and structural basis of these differences is poorly understood despite their biomechanical relevance.

American Journal of Physical Anthropology, 2016

Objectives: We investigated how heterogeneity in material stiffness affects structural stiffness in the cercopithecid mandibular cortical bone. We assessed (1) whether this effect changes the interpretation of interspecific structural stiffness variation across four primate species, (2) whether the heterogeneity is random, and (3) whether heterogeneity mitigates bending stress in the jaw associated with food processing. Materials and methods: The sample consisted of Taï Forest, Cote d'Ivoire, monkeys: Cercocebus atys, Piliocolobus badius, Colobus polykomos, and Cercopithecus diana. Vickers indentation hardness samples estimated elastic moduli throughout the cortical bone area of each coronal section of postcanine corpus. For each section, we calculated maximum area moment of inertia, I max (structural mechanical property), under three models of material heterogeneity, as well as spatial autocorrelation statistics (Moran's I, I MORAN). Results: When the model considered material stiffness variation and spatial patterning, I max decreased and individual ranks based on structural stiffness changed. Rank changes were not significant across models. All specimens showed positive (nonrandom) spatial autocorrelation. Differences in I MORAN were not significant among species, and there were no discernable patterns of autocorrelation within species. Across species, significant local I MORAN was often attributed to proximity of low moduli in the alveolar process and high moduli in the basal process. Discussion: While our sample did not demonstrate species differences in the degree of spatial autocorrelation of elastic moduli, there may be mechanical effects of heterogeneity (relative strength and rigidity) that do distinguish at the species or subfamilial level (i.e., colobines vs. cercopithecines). The potential connections of heterogeneity to diet and/or taxonomy remain to be discovered.

American Journal of Physical Anthropology, 2009

Understanding the mechanical features of cortical bone and their changes with growth and adaptation to function plays an important role in our ability to interpret the morphology and evolution of craniofacial skeletons. We assessed the elastic properties of cortical bone of juvenile and adult baboon mandibles using ultrasonic techniques. Results showed that, overall, cortical bone from baboon mandibles could be modeled as an orthotropic elastic solid. There were significant differences in the directions of maximum stiffness, thickness, density, and elastic stiffness among different functional areas, indicating regional adaptations. After maturity, the cortical bone becomes thicker, denser, and stiffer, but less anisotropic. There were differences in elastic properties of the corpus and ramus between male and female mandibles which are not observed in human mandibles. There were correlations between cortical thicknesses and densities, between bone elastic properties and microstructural configuration, and between the directions of maximum stiffness and bone anatomical axes in some areas. The relationships between bone extrinsic and intrinsic properties bring us insights into the integration of form and function in craniofacial skeletons and suggest that we need to consider both macroscopic form, microstructural variation, and the material properties of bone matrix when studying the functional properties and adaptive nature of the craniofacial skeleton in primates. The differences between baboon and human mandibles is at variance to the pattern of differences in crania, suggesting differences in bone adaption to varying skeletal geometries and loading regimes at both phylogenetic and ontogenetic levels.

The relationship between primate mandibular form and diet has been previously analysed by applying a wide array of techniques and approaches. Nonetheless, most of these studies compared few species and/or infrequently aimed to elucidate function based on an explicit biomechanical framework. In this study, we generated and analysed 31 Finite Element planar models of different primate jaws under different loading scenarios (incisive, canine, premolar and molar bites) to test the hypothesis that there are significant differences in mandibular biomechanical performance due to food categories and/or food hardness. The obtained stress values show that in primates, hard food eaters have stiffer mandibles when compared to those that rely on softer diets. In addition, we find that folivores species have the weakest jaws, whilst omnivores have the strongest mandibles within the order Primates. These results are highly relevant because they show that there is a strong association between mandibular biomechanical performance, mandibular form, food hardness and diet categories and that these associations can be studied using biomechanical techniques rather than focusing solely on morphology. Diet is regarded as one of the main factor underlying the behavioural and ecological differences among living primates, and consequently primate diets have been more exhaustively documented than any other aspect of their behaviour 1. A substantial proportion of physiological and anatomical adaptations have as their fundamental objective the transformation of the ingesta that animals consume. Most primates have been habitually interpreted as mainly adapted to fruit consumption 2 , however it has been also acknowledged that some species occupy specific dietary niches ranging from omnivory to the pure folivory 1. Consequently, primates have been classified into three main diet categories: frugivores, folivores, and omnivores. These broad categories are coherent with much of the structural and nutritional characteristics of the food items observed in primates, and thus frugivores, foli-vores, and omnivores have characteristic features that enable them to process their different diets. Furthermore, some primates are adapted to the consumption of hard items (durophagy; hard-food eaters) whereas others are classified as soft-food consumers 3. The relationship between primate mandibular form and loading during biting has been analysed by numerous studies 4. This interest regarding shape and function in the mandible has not been restricted to primates; in fact, other mammalian clades such as Artiodactyla 5, 6 , Chiroptera 7 , and Carnivora 8, 9 have been studied as well. The close interaction between the mammalian feeding mechanism and the ingesta it processes represents a unique opportunity to study ecomorphological adaptations in extant species and potentially acquire valuable tools for the reconstruction of feeding behaviours in extinct taxa as well. The main function of the mammalian mandible is to transfer the forces generated by the masticatory muscles to the ingesta via the teeth. It has been proposed that mandibular shape is mostly involved in ensuring that the forces are transmitted without being dissipated or causing the mandible to fail structurally 10. Mandibular shape is related to diet through the frequency and magnitude of adductor muscle forces engaged during various oral activities. The greater the forces required to fracture food items (or their protective structures), and the more repeatedly such forces need to be produced (e.g. through repetitive biting), the stronger the mandible has to be to maintain its structural integrity 11. This has been experimentally tested by feeding animal with diets of different Published: xx xx xxxx OPEN

Journal of Morphology, 2009

The anterior mandibular corpus of anthropoid primates is routinely subjected to masticatory loads that result in relatively high local levels of stress and strain. While structural morphological responses to these loads have been extensively explored, relatively little is known about material property variation in mandibular bone of nonhuman primates. Consequently, the role of regional and local variation in bone stiffness in conditioning stress and strain gradients is poorly understood. We sampled elastic modulus variation in the bone of the anterior mandibular corpus in two species (N = 3 each) of sympatric colobine monkeys, Procolobus badius and Colobus polykomos. These monkeys were chosen for comparison owing to their distinctive dietary regimens, as P. badius rarely includes hard objects in its diet while C. polykomos habitually processes obdurate items during feeding. Elastic modulus is determined through bone hardness data obtained via microindentation, which enables the description of stiffness variation on sub-millimeter scales. Labial bone stiffness exceeds that of lingual bone in the sample overall. Female mandibular bone is generally stiffer than that found in males, and overall Procolobus mandibular bone is stiffer than that in Colobus. These results, interpreted collectively, suggest that the material response to elevated masticatory stress is increased compliance of the affected bone. J. Morphol., 2009. © 2008 Wiley-Liss, Inc.

American Journal of Physical Anthropology, 2003

Local variation in cortical bone thickness in the postcanine mandibular corpus appears to be stereotypical among anthropoids. Specifically, at sections under the molars, lingually situated cortical bone is typically thinner than that along the lateral aspect. This pattern applies despite phylogenetic, dietary, and allometric differences among the anthropoids sampled to date. Demes et al. (Food Acquisition and Processing in Primates [1984] New York: Plenum Press, p. 369–390) employed a theoretical analysis of mastication in Gorilla and Homo to argue that this pattern could be explained with reference to biomechanical stresses. Specifically, they proposed that the combined effects of torsion and direct shear on the working-side corpus create a condition in which net stresses and strains are reduced along the lingual cortical plate. Demonstration of this effect would suggest a functional linkage between localized differences in bone mass and strain gradients in the facial skeleton. We conducted an empirical evaluation of the effects of the combined loads of torsion and direct shear in vitro on a sample of formalin-fixed human mandibles. Rosette strain gages were affixed to the lateral and medial aspects of the corpus in each specimen, and surface strains were recorded separately under controlled torsional and occlusal loads, and under simultaneous application of these loads. The hypothesis that lingual strains are reduced under combined twisting and occlusal loads was generally supported; however, we observed reduction in surface strains at some sites along the lateral aspect of the corpus under these combined loads as well. These unexpected findings are attributable to unanticipated loading conditions imposed by occlusal forces, which result from sources of stress in addition to direct shear. These experiments provide provisional support for the hypothesis that superposed sources of bone strain produce large strain gradients between buccal and lingual aspects of the mandibular corpus, and that local variation in bone mass may be associated with these gradients. Am J Phys Anthropol, 2003. © 2003 Wiley-Liss, Inc.

Journal of Human Evolution, 1997

Journal of Human Evolution, 2006

When a force is applied to an object, the resulting pattern of strain is a function of both the object's geometry and its elastic properties. Thus, knowledge of elastic properties in craniofacial cortical bone is indispensable for exploring the biomechanics and adaptation of primate skulls. However, elastic properties, such as density and stiffness, cannot be measured in all species, particularly extinct species known only from fossils. In order for advanced engineering techniques such as finite element analysis (FEA) to be applied to questions of primate and hominid craniofacial functional morphology, it is important to understand interspecific patterns of variation in elastic properties. We hypothesized that closely related species would have similar patterns of bone elastic properties, and that similarities with extant species should allow reasonable predictions of elastic properties in the skeletons of extinct primate species. In this study, we tested this hypothesis by measuring elastic properties in five areas of the external cortex of the baboon craniofacial skeleton using an ultrasonic technique, and by comparing the results to existing data from macaque and human crania. Results showed that cortical density, thickness, elastic and shear moduli, and anisotropy varied among areas in the baboon cranium. Similar variation had previously been found in rhesus and human crania, suggesting area-specific elastic patterns in the skulls of each species. Comparison among species showed differences, suggesting species-specific patterns. These patterns were more similar between macaques and baboons for density, maximum elastic and shear stiffness, and anisotropy than between either of these and humans. This finding demonstrates that patterns of cortical elastic properties are generally similar in closely related primate species with similar craniofacial morphology. Thus, reasonable estimates of cortical bone elastic properties should be possible for extinct species through the study of phylogenetically related and functionally similar modern forms. For example, reasonable elastic property estimates of cortical bone from fossil hominid skulls should be possible once adequate information about such properties in extant great apes is added to our current data from humans, macaques, and baboons. Such data should eventually allow FEA of craniofacial function in fossil hominids.