A new biomechanical model of the mammal jaw based on load path analysis.

The primary function of the tetrapod jaw is to transmit jaw muscle forces to bite points. The routes of force transfer in the jaw have never been studied, but can be quantified using load paths--the shortest, stiffest routes from regions of force application to support constraints. Here we use load path analysis to map force transfer from muscle attachments to bite point and jaw joint, and to evaluate how different configurations of trabecular and cortical bone affect load paths. We created three models of the mandible of the Virginia opossum, Didelphis virginiana, each with a cortical bone shell, but with different material properties for the internal spaces: a cortical-trabecular model, in which the interior space is modeled with bulk properties of trabecular bone; a cortical-hollow model, in which trabeculae and mandibular canal are modeled as hollow; and a solid-cortical model, in which the interior is modeled as cortical bone. The models were compared with published in vivo bite force and bone strain data, and the load paths calculated for each model. The cortical-trabecular model, which most closely approximates the actual morphology, was best validated by in vivo data. In all three models the load path was confined to cortical bone, although its route within the cortex varied depending on the material properties of the inner model. Our analysis shows that most of the force is transferred through the cortical, rather than trabecular bone, and highlights the potential of load path analysis for understanding form-function relationships in the skeleton.

The impact of measurement technique and sampling on estimates of skeletal muscle fibre architecture.

Skeletal muscle fibre architecture provides important insights into performance of vertebrate locomotor and feeding behaviours. Chemical digestion and in situ sectioning of muscle bellies along their lengths to expose fibres, fibre orientation and intramuscular tendon, are two classical methods for estimating architectural variables such as fibre length (Lf) and physiological cross-sectional area (PCSA). It has recently been proposed that Lf estimates are systematically shorter and hence less accurate using in situ sectioning. Here we addressed this hypothesis by comparing Lf estimates between the two methods for the superficial masseter and temporalis muscles in a sample of strepsirrhine and platyrrhine primates. Means or single-specimen Lf estimates using chemical digestion were greater in 17/32 comparisons (53.13%), indicating the probability of achieving longer fibres using chemical digestion is no greater than chance in these taxonomic samples. We further explored the impact of sampling on scaling of Lf and PCSA in platyrrhines applying a bootstrapping approach. We found that sampling-both numbers of individuals within species and representation of species across the clade significantly influence scaling results of Lf and PCSA in platyrrhines. We show that intraspecific and clade sampling strategies can account for differences between previously published platyrrhine scaling studies. We suggest that differences in these two methodological approaches to assessing muscle architecture are relatively less consequential when estimating Lf and PCSA for comparative studies, whereas achieving more reliable estimates within species through larger samples and representation of the full clade space are important considerations in comparative studies of fibre architecture and scaling.

Tradeoffs between bite force and gape in Eulemur and Varecia.

In 1974, Sue Herring described the relationship between two important performance variables in the feeding system, bite force and gape. These variables are inversely related, such that, without specific muscular adaptations, most animals cannot produce high bite forces at large gapes for a given sized muscle. Despite the importance of these variables for feeding biomechanics and functional ecology, the paucity of in vivo bite force data in primates has led to bite forces largely being estimated through ex vivo methods. Here, we quantify and compare in vivo bite forces and gapes with output from simulated musculoskeletal models in two craniofacially distinct strepsirrhines: Eulemur, which has a shorter jaw and slower chewing cycle durations relative to jaw length and body mass compared to Varecia. Bite forces were collected across a range of linear gapes from 16 adult lemurs (suborder Strepsirrhini) at the Duke Lemur Center in Durham, North Carolina representing three species: Eulemur flavifrons (n = 6; 3F, 3M), Varecia variegata (n = 5; 3F, 2M), and Varecia rubra (n = 5; 5F). Maximum linear and angular gapes were significantly higher for Varecia compared to Eulemur (p = .01) but there were no significant differences in recorded maximum in vivo bite forces (p = .88). Simulated muscle models using architectural data for these taxa suggest this approach is an accurate method of estimating bite force-gape tradeoffs in addition to variables such as fiber length, fiber operating range, and gapes associated with maximum force. Our in vivo and modeling data suggest Varecia has reduced bite force capacities in favor of absolutely wider gapes compared to Eulemur in relation to their longer jaws. Importantly, our comparisons validate the simulated muscle approach for estimating bite force as a function of gape in extant and fossil primates.

Ontogenetic changes in jaw leverage and skull shape in tufted and untufted capuchins.

The ontogeny of feeding is characterized by shifting functional demands concurrent with changes in craniofacial anatomy; relationships between these factors will look different in primates with disparate feeding behaviors during development. This study examines the ontogeny of skull morphology and jaw leverage in tufted (Sapajus) and untufted (Cebus) capuchin monkeys. Unlike Cebus, Sapajus have a mechanically challenging diet and behavioral observations of juvenile Sapajus suggest these foods are exploited early in development. Landmarks were placed on three-dimensional surface models of an ontogenetic series of Sapajus and Cebus skulls (n = 53) and used to generate shape data and jaw-leverage estimates across the tooth row for three jaw-closing muscles (temporalis, masseter, medial pterygoid) as well as a weighted combined estimate. Using geometric morphometric methods, we found that skull shape diverges early and shape is significantly different between Sapajus and Cebus throughout ontogeny. Additionally, jaw leverage varies with age and position on the tooth row and is greater in Sapajus compared to Cebus when calculated at the permanent dentition. We used two-block partial least squares analyses to identify covariance between skull shape and each of our jaw muscle leverage estimates. Sapajus, but not Cebus, has significant covariance between all leverage estimates at the anterior dentition. Our findings show that Sapajus and Cebus exhibit distinct craniofacial morphologies early in ontogeny and strong covariance between leverage estimates and craniofacial shape in Sapajus. These results are consistent with prior behavioral and comparative work suggesting these differences are a function of selection for exploiting mechanically challenging foods in Sapajus, and further emphasize that these differences appear quite early in ontogeny. This research builds on prior work that has highlighted the importance of understanding ontogeny for interpreting adult morphology.