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.

Gape drives regional variation in temporalis architectural dynamics in tufted capuchins.

Dynamic changes in jaw movements and bite forces depend on muscle architectural and neural factors that have rarely been compared within the same muscle. Here we investigate how regional muscle architecture dynamics-fascicle rotation, shortening, lengthening and architectural gear ratio (AGR)-vary during chewing across a functionally heterogeneous muscle. We evaluate whether timing in architecture dynamics relates to gape, food material properties and/or muscle activation. We also examine whether static estimates of temporalis fibre architecture track variation in dynamic architecture. Fascicle-level architecture dynamics were measured in three regions of the superficial temporalis of three adult tufted capuchins (Sapajus apella) using biplanar videoradiography and the XROMM workflow. Architecture dynamics data were paired with regional fine-wire electromyography data from four adult tufted capuchins. Gape accounted for most architectural change across the temporalis, but architectural dynamics varied between regions. Mechanically challenging foods were associated with lower AGRs in the anterior region. The timing of most dynamic architectural changes did not vary between regions and differed from regional variation in static architecture. Collectively these findings suggest that, when modelling temporalis muscle force production in extant and fossil primates, it is important to account for the effects of gape, regionalization and food material properties. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Dynamic finite element modelling of the macaque mandible during a complete mastication gape cycle.

Three-dimensional finite element models (FEMs) are powerful tools for studying the mechanical behaviour of the feeding system. Using validated, static FEMs we have previously shown that in rhesus macaques the largest food-related differences in strain magnitudes during unilateral postcanine chewing extend from the lingual symphysis to the endocondylar ridge of the balancing-side ramus. However, static FEMs only model a single time point during the gape cycle and probably do not fully capture the mechanical behaviour of the jaw during mastication. Bone strain patterns and moments applied to the mandible are known to vary during the gape cycle owing to variation in the activation peaks of the jaw-elevator muscles, suggesting that dynamic models are superior to static ones in studying feeding biomechanics. To test this hypothesis, we built dynamic FEMs of a complete gape cycle using muscle force data from in vivo experiments to elucidate the impact of relative timing of muscle force on mandible biomechanics. Results show that loading and strain regimes vary across the chewing cycle in subtly different ways for different foods, something which was not apparent in static FEMs. These results indicate that dynamic three-dimensional FEMs are more informative than static three-dimensional FEMs in capturing the mechanical behaviour of the jaw during feeding by reflecting the asymmetry in jaw-adductor muscle activations during a gape cycle. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Sagittal suture strain in capuchin monkeys (Sapajus and Cebus) during feeding.

OBJECTIVES: Morphological variation in cranial sutures is used to infer aspects of primate feeding behavior, including diet, but strain regimes across sutures are not well documented. Our aim is to test hypotheses about sagittal suture morphology, strain regime, feeding behavior, and muscle activity relationships in robust Sapajus and gracile Cebus capuchin primates. MATERIALS AND METHODS: Morphometrics of sinuosity in three regions of the sagittal suture were compared among museum specimens of Sapajus and Cebus, as well as in robust and gracile lab specimens. In vivo strains and bilateral electromyographic (EMG) activity were recorded from these regions in the temporalis muscles of capuchin primates while they fed on mechanically-varying foods. RESULTS: Sapajus and the anterior suture region exhibited greater sinuosity than Cebus and posterior regions. In vivo data reveal minor differences in strain regime between robust and gracile phenotypes but show higher strain magnitudes in the middle suture region and higher tensile strains anteriorly. After gage location, feeding behavior has the most consistent and strongest impact on strain regime in the sagittal suture. Strain in the anterior suture has a high tension to compression ratio compared to the posterior region, especially during forceful biting in the robust Sapajus-like individual. DISCUSSION: Sagittal suture complexity in robust capuchins likely reflects feeding behaviors associated with mechanically challenging foods. Sutural strain regimes in other anthropoid primates may also be affected by activity in feeding muscles.

Macaca mulatta is a good model for human mandibular fixation research.

Biomechanical and clinical studies have yet to converge on the optimal fixation technique for angle fractures, one of the most common and controversial fractures in terms of fixation approach. Prior pre-clinical studies have used a variety of animal models and shown abnormal strain environments exacerbated by less rigid (single-plate) Champy fixation and chewing on the side opposite the fracture (contralateral chewing). However, morphological differences between species warrant further investigation to ensure that these findings are translational. Here we present the first study to use realistically loaded finite-element models to compare the biomechanical behaviour of human and macaque mandibles pre- and post-fracture and fixation. Our results reveal only small differences in deformation and strain regimes between human and macaque mandibles. In the human model, more rigid biplanar fixation better approximated physiologically healthy global bone strains and moments around the mandible, and also resulted in less interfragmentary strain than less rigid Champy fixation. Contralateral chewing exacerbated deviations in strain, moments and interfragmentary strain, especially under Champy fixation. Our pre- and post-fracture fixation findings are congruent with those from macaques, confirming that rhesus macaques are excellent animal models for biomedical research into mandibular fixation. Furthermore, these findings strengthen the case for rigid biplanar fixation over less rigid one-plate fixation in the treatment of isolated mandibular angle fractures.

Fracture Fixation Technique and Chewing Side Impact Jaw Mechanics in Mandible Fracture Repair.

Lower jaw (mandible) fractures significantly impact patient health and well-being due to pain and difficulty eating, but the best technique for repairing the most common subtype-angle fractures-and rehabilitating mastication is unknown. Our study is the first to use realistic in silico simulation of chewing to quantify the effects of Champy and biplanar techniques of angle fracture fixation. We show that more rigid, biplanar fixation results in lower strain magnitudes in the miniplates, the bone around the screws, and in the fracture zone, and that the mandibular strain regime approximates the unfractured condition. Importantly, the strain regime in the fracture zone is affected by chewing laterality, suggesting that both fixation type and the patient's post-fixation masticatory pattern-ipsi- or contralateral to the fracture- impact the bone healing environment. Our study calls for further investigation of the impact of fixation technique on chewing behavior. Research that combines in vivo and in silico approaches can link jaw mechanics to bone healing and yield more definitive recommendations for fixation, hardware, and postoperative rehabilitation to improve outcomes. © 2021 The Authors. JBMR Plus published by Wiley Periodicals LLC on behalf of American Society for Bone and Mineral Research.

Biomechanics of the mandible of Macaca mulatta during the power stroke of mastication: Loading, deformation, and strain regimes and the impact of food type.

Mandible morphology has yet to yield definitive information on primate diet, probably because of poor understanding of mandibular loading and strain regimes, and overreliance on simple beam models of mandibular mechanics. We used a finite element model of a macaque mandible to test hypotheses about mandibular loading and strain regimes and relate variation in muscle activity during chewing on different foods to variation in strain regimes. The balancing-side corpus is loaded primarily by sagittal shear forces and sagittal bending moments. On the working side, sagittal bending moments, anteroposterior twisting moments, and lateral transverse bending moments all reach similar maxima below the bite point; sagittal shear is the dominant loading regime behind the bite point; and the corpus is twisted such that the mandibular base is inverted. In the symphyseal region, the predominant loading regimes are lateral transverse bending and negative twisting about a mediolateral axis. Compared with grape and dried fruit chewing, nut chewing is associated with larger sagittal and transverse bending moments acting on balancing- and working-side mandibles, larger sagittal shear on the working side, and larger twisting moments about vertical and transverse axes in the symphyseal region. Nut chewing is also associated with higher minimum principal strain magnitudes in the balancing-side posterior ramus; higher sagittal shear strain magnitudes in the working-side buccal alveolar process and the balancing-side oblique line, recessus mandibulae, and endocondylar ridge; and higher transverse shear strains in the symphyseal region, the balancing-side medial prominence, and the balancing-side endocondylar ridge. The largest food-related differences in maximum principal and transverse shear strain magnitudes are in the transverse tori and in the balancing-side medial prominence, extramolar sulcus, oblique line, and endocondylar ridge. Food effects on the strain regime are most salient in areas not traditionally investigated, suggesting that studies seeking dietary effects on mandible morphology might be looking in the wrong places.

Temporomandibular Joint Hypofunction Secondary to Unilateral Partial Discectomy Attenuates Degeneration in Murine Mandibular Condylar Cartilage.

Mechanical overloading of the temporomandibular joint (TMJ) promotes both the initiation and progression of TMJ osteoarthritis (OA). New preclinical animal models are needed for the evaluation of the molecular basis of cellular load transmission. This would allow a better understanding of the underlying mechanisms of TMJ-OA pain and disability, and help identify new therapeutics for its early diagnosis and management. The purpose of this study was to evaluate the role of mechanical loading in the progression of TMJ-OA in surgical instability arising from unilateral partial discectomy (UPD) in a murine model. In the theoretical modelling employed, lower joint reaction forces were observed on the chewing (working) side of the TMJ in the murine craniomandibular musculoskeletal system. Hypofunction was induced secondary to UPD through surgically manipulating the working side using an unopposed molar model. When the working side was restricted to the same side as that on which UPD was performed, late-stage degeneration of the cartilage showed a significant reduction (p<0.05), with diminished fibrillation and erosion of the articular cartilage, cell clustering, and hypocellularity. Condylar remodelling and proteolysis of proteoglycans were less affected. Thus, select and specific late-stage changes in TMJ-OA were contextually linked with the local mechanical environment of the joint. These data underscore the value of the UPD mouse model in studying mechanobiological pathways activated during TMJ-OA, and suggest that therapeutically targeting mechanobiological stimuli is an effective strategy in improving long-term biological, clinical, and patient-based outcomes.

The Mechanical Effect of the Periodontal Ligament on Bone Strain Regimes in a Validated Finite Element Model of a Macaque Mandible.

The primary anatomical function of the periodontal ligament (PDL) is to attach teeth to their sockets. However, theoretical and constitutive mechanical models have proposed that during mastication the PDL redistributes local occlusal loads and reduces the jaw's resistance to torsional deformations. These hypotheses imply that accurately modeling the PDL's material properties and geometry in finite element analysis (FEA) is a prerequisite to obtaining precise strain and deformation data. Yet, many finite element studies of the human and non-human primate masticatory apparatus exclude the PDL or model it with simplicity, in part due to limitations in µCT/CT scan resolution and material property assignment. Previous studies testing the sensitivity of finite element models (FEMs) to the PDL have yielded contradictory results, however a major limitation of these studies is that FEMs were not validated against in vivo bone strain data. Hence, this study uses a validated and subject specific FEM to assess the effect of the PDL on strain and deformation regimes in the lower jaw of a rhesus macaque (Macaca mulatta) during simulated unilateral post-canine chewing. Our findings demonstrate that the presence of the PDL does influence local and global surface strain magnitudes (principal and shear) in the jaw. However, the PDL's effect is limited (diff. ~200-300 µÎµ) in areas away from the alveoli. Our results also show that varying the PDL's Young's Modulus within the range of published values (0.07-1750 MPa) has very little effect on global surface strains. These findings suggest that the mechanical importance of the PDL in FEMs of the mandible during chewing is dependent on the scope of the hypotheses being tested. If researchers are comparing strain gradients across species/taxa, the PDL may be excluded with minimal effect on results, but, if researchers are concerned with absolute strain values, sensitivity analysis is required.

Joint angular excursions during cyclical behaviors differ between tetrapod feeding and locomotor systems.

Tetrapod musculoskeletal diversity is usually studied separately in feeding and locomotor systems. However, comparisons between these systems promise important insight into how natural selection deploys the same basic musculoskeletal toolkit - connective tissues, bones, nerves and skeletal muscle - to meet the differing performance criteria of feeding and locomotion. In this study, we compare average joint angular excursions during cyclic behaviors - chewing, walking and running - in a phylogenetic context to explore differences in the optimality criteria of these two systems. Across 111 tetrapod species, average limb-joint angular excursions during cyclic locomotion are greater and more evolutionarily labile than those of the jaw joint during cyclic chewing. We argue that these findings reflect fundamental functional dichotomies between tetrapod locomotor and feeding systems. Tetrapod chewing systems are optimized for precise application of force over a narrower, more controlled and predictable range of displacements, the principal aim being to fracture the substrate, the size and mechanical properties of which are controlled at ingestion and further reduced and homogenized, respectively, by the chewing process. In contrast, tetrapod limbed locomotor systems are optimized for fast and energetically efficient application of force over a wider and less predictable range of displacements, the principal aim being to move the organism at varying speeds relative to a substrate whose geometry and mechanical properties need not become more homogeneous as locomotion proceeds. Hence, the evolution of tetrapod locomotor systems has been accompanied by an increasing diversity of limb-joint excursions, as tetrapods have expanded across a range of locomotor substrates and environments.

In vivo bone strain and finite element modeling of a rhesus macaque mandible during mastication.

Finite element analysis (FEA) is a commonly used tool in musculoskeletal biomechanics and vertebrate paleontology. The accuracy and precision of finite element models (FEMs) are reliant on accurate data on bone geometry, muscle forces, boundary conditions and tissue material properties. Simplified modeling assumptions, due to lack of in vivo experimental data on material properties and muscle activation patterns, may introduce analytical errors in analyses where quantitative accuracy is critical for obtaining rigorous results. A subject-specific FEM of a rhesus macaque mandible was constructed, loaded and validated using in vivo data from the same animal. In developing the model, we assessed the impact on model behavior of variation in (i) material properties of the mandibular trabecular bone tissue and teeth; (ii) constraints at the temporomandibular joint and bite point; and (iii) the timing of the muscle activity used to estimate the external forces acting on the model. The best match between the FEA simulation and the in vivo experimental data resulted from modeling the trabecular tissue with an isotropic and homogeneous Young's modulus and Poisson's value of 10GPa and 0.3, respectively; constraining translations along X,Y, Z axes in the chewing (left) side temporomandibular joint, the premolars and the m1; constraining the balancing (right) side temporomandibular joint in the anterior-posterior and superior-inferior axes, and using the muscle force estimated at time of maximum strain magnitude in the lower lateral gauge. The relative strain magnitudes in this model were similar to those recorded in vivo for all strain locations. More detailed analyses of mandibular strain patterns during the power stroke at different times in the chewing cycle are needed.

Functional correlates of the position of the axis of rotation of the mandible during chewing in non-human primates.

The location of the axis of rotation (AoR) of the mandible was quantified using the helical axis (HA) in eight individuals from three species of non-human primates: Papio anubis, Cebus apella, and Macaca mulatta. These data were used to test three hypotheses regarding the functional significance of anteroposterior condylar translation - an AoR located inferior to the temporomandibular joint (TMJ) - during chewing: minimizing impingement of the gonial region on cervical soft tissue structures during jaw opening; avoiding stretching of the inferior alveolar neurovascular bundle (IANB); and increasing jaw-elevator muscle torques. The results reveal that the HA is located near the occlusal plane in Papio and Cebus, but closer to the condyle in Macaca; is located anteroinferior to the TMJ during both opening and closing in Papio, as well as during opening in Macaca and Cebus; and varies in its location during closing in Macaca and Cebus. The impingement hypothesis is not supported by interspecific variation in HA location: species with larger gonial angles like Cebus do not have more inferiorly located HAs than species with more obtuse mandibular angles like Papio. However, intraspecific variation provides some support for the impingement hypothesis. The HA seldom passes near or through the lingula, falsifying the hypothesis that its location is determined by the sphenomandibular ligament, and the magnitudes of strain associated with a HA at the TMJ would not be large enough to cause problematic stretching of the IANB. HA location does affect muscle moment arms about the TMJ, with implications for the torque generation capability of the jaw-elevator muscles. In Cebus, a HA farther away from the TMJ is associated with larger jaw-elevator muscle moment arms about the joint than if it were at the TMJ. The effects of HA location on muscle strain and muscle moment arms are largest at large gapes and smallest at low gapes, suggesting that if HA location is of functional significance for primate feeding system performance, it is more likely to be in relation to large gape feeding behaviors than chewing. Its presence in humans is most parsimoniously interpreted as a primitive retention from non-human primate ancestors and explanations for the presence of anteroposterior condylar translation in humans need not invoke either the uniqueness of human speech or upright posture.

Sagittal Plane Kinematics of the Jaw and Hyolingual Apparatus During Swallowing in Macaca mulatta.

Studies of mechanisms of feeding behavior are important in a society where aging- and disease-related feeding disorders are increasingly prevalent. It is important to evaluate the clinical relevance of animal models of the disease and the control. Our present study quantifies macaque hyolingual and jaw kinematics around swallowing cycles to determine the extent to which macaque swallowing resembles that of humans. One female and one male adult Macaca mulatta were trained to feed in a primate chair. Videofluoroscopy was used to record kinematics in a sagittal view during natural feeding on solid food, and the kinematics of the hyoid bone, thyroid cartilage, mandibular jaw, and anterior-, middle-, and posterior-tongue. Jaw gape cycles were defined by consecutive maximum gapes, and the kinematics of the swallow cycles were compared with those of the two consecutive non-swallow cycles preceding and succeeding the swallow cycles. Although there are size differences between macaques and humans, and macaques have shorter durations of jaw gape cycles and hyoid and thyroid upward movements, there are several important similarities between our macaque data and human data reported in the literature: (1) The durations of jaw gape cycles during swallow cycles are longer than those of non-swallow cycles as a result of an increased duration of the jaw-opening phase; (2) Hyoid and thyroid upward movement is linked with a posterior tongue movement and is faster during swallow than non-swallow cycles; (3) Tongue elevation propagates from anterior to posterior during swallow and non-swallow cycles. These findings suggest that macaques can be a useful experimental model for human swallowing studies.

Scaling of rotational inertia of primate mandibles.

The relative importance of pendulum mechanics and muscle mechanics in chewing dynamics has implications for understanding the optimality criteria driving the evolution of primate feeding systems. The Spring Model (Ross et al., 2009b), which modeled the primate chewing system as a forced mass-spring system, predicted that chew cycle time would increase faster than was actually observed. We hypothesized that if mandibular momentum plays an important role in chewing dynamics, more accurate estimates of the rotational inertia of the mandible would improve the accuracy with which the Spring Model predicts the scaling of primate chew cycle period. However, if mass-related momentum effects are of negligible importance in the scaling of primate chew cycle period, this hypothesis would be falsified. We also predicted that greater "robusticity" of anthropoid mandibles compared with prosimians would be associated with higher moments of inertia. From computed tomography scans, we estimated the scaling of the moment of inertia (Ij) of the mandibles of thirty-one species of primates, including 22 anthropoid and nine prosimian species, separating Ij into the moment about a transverse axis through the center of mass (Ixx) and the moment of the center of mass about plausible axes of rotation. We found that across primates Ij increases with positive allometry relative to jaw length, primarily due to positive allometry of jaw mass and Ixx, and that anthropoid mandibles have greater rotational inertia compared with prosimian mandibles of similar length. Positive allometry of Ij of primate mandibles actually lowers the predictive ability of the Spring Model, suggesting that scaling of primate chew cycle period, and chewing dynamics in general, are more strongly influenced by factors other than scaling of inertial properties of the mandible, such as the dynamic properties of the jaw muscles and neural control. Differences in cycle period scaling between chewing and locomotion systems reinforce the suggestion that displacement and force control are more important in the design of feeding systems than energetics and speed.

Speed-dependent modulation of wing muscle recruitment intensity and kinematics in two bat species.

Animals respond to changes in power requirements during locomotion by modulating the intensity of recruitment of their propulsive musculature, but many questions concerning how muscle recruitment varies with speed across modes of locomotion remain unanswered. We measured normalized average burst EMG (aEMG) for pectoralis major and biceps brachii at different flight speeds in two relatively distantly related bat species: the aerial insectivore Eptesicus fuscus, and the primarily fruit-eating Carollia perspicillata These ecologically distinct species employ different flight behaviors but possess similar wing aspect ratio, wing loading and body mass. Because propulsive requirements usually correlate with body size, and aEMG likely reflects force, we hypothesized that these species would deploy similar speed-dependent aEMG modulation. Instead, we found that aEMG was speed independent in E. fuscus and modulated in a U-shaped or linearly increasing relationship with speed in C. perspicillata This interspecific difference may be related to differences in muscle fiber type composition and/or overall patterns of recruitment of the large ensemble of muscles that participate in actuating the highly articulated bat wing. We also found interspecific differences in the speed dependence of 3D wing kinematics: E. fuscus modulates wing flexion during upstroke significantly more than C. perspicillata Overall, we observed two different strategies to increase flight speed: C. perspicillata tends to modulate aEMG, and E. fuscus tends to modulate wing kinematics. These strategies may reflect different requirements for avoiding negative lift and overcoming drag during slow and fast flight, respectively, a subject we suggest merits further study.

In vivo bone strain in the mandibular corpus of Sapajus during a range of oral food processing behaviors.

It has been hypothesized that mandibular corpus morphology of primates is related to the material properties of the foods that they chew. However, chewing foods with different material properties is accompanied by low levels of variation in mandibular strain patterns in macaques. We hypothesized that if variation in primate mandible form reflects adaptations to feeding on foods with different material and geometric properties, then this variation will be driven primarily by differences in oral food processing behavior rather than differences in chewing per se. To test this hypothesis, we recorded in vivo bone strain data from the lateral and medial surfaces of the mandibular corpus during complete feeding sequences in three adult male Sapajus as they fed on foods with a range of sizes and material properties. We assessed whether variation in mandibular corpus strain regimes is associated with variation in feeding behaviors and/or chewing on different foods, and we quantified the relative variation in mandibular corpus strain regimes associated with chewing on foods of different material properties versus a range of oral food processing behaviors (incisor, premolar, and molar biting; pulling on incisors; mastication). Feeding behavior had a significant effect on mandibular corpus strain regimes, as did chewing side and the cycle number in a feeding sequence. However, food type had weaker effects and usually only through interaction effects with chewing side and/or cycle type. Strain regimes varied most across different chew sides, then across different behaviors, and lastly between mastication cycles on different foods. Strain magnitudes associated with premolar, molar, and incisor biting were larger than those recorded during mastication. These data suggest that intra- and inter-specific variation in mandible morphology is a trade-off between performance requirements of different oral food processing behaviors and of variation in chewing side, with direct effects of food type being less important.

What does feeding system morphology tell us about feeding?

Feeding is the set of behaviors whereby organisms acquire and process the energy required for survival and reproduction. Thus, feeding system morphology is presumably subject to selection to maintain or improve feeding performance. Relationships among feeding system morphology, feeding behavior, and diet not only explain the morphological diversity of extant primates, but can also be used to reconstruct feeding behavior and diet in fossil taxa. Dental morphology has long been known to reflect aspects of feeding behavior and diet but strong relationships of craniomandibular morphology to feeding behavior and diet have yet to be defined.

In vivo cranial bone strain and bite force in the agamid lizard Uromastyx geyri.

In vivo bone strain data are the most direct evidence of deformation and strain regimes in the vertebrate cranium during feeding and can provide important insights into skull morphology. Strain data have been collected during feeding across a wide range of mammals; in contrast, in vivo cranial bone strain data have been collected from few sauropsid taxa. Here we present bone strain data recorded from the jugal of the herbivorous agamid lizard Uromastyx geyri along with simultaneously recorded bite force. Principal and shear strain magnitudes in Uromastyx geyri were lower than cranial bone strains recorded in Alligator mississippiensis, but higher than those reported from herbivorous mammals. Our results suggest that variations in principal strain orientations in the facial skeleton are largely due to differences in feeding behavior and bite location, whereas food type has little impact on strain orientations. Furthermore, mean principal strain orientations differ between male and female Uromastyx during feeding, potentially because of sexual dimorphism in skull morphology.