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.

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.

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'.

Ontogenetic changes in bite force and gape in tufted capuchins.

Bite force and gape are two important performance metrics of the feeding system, and these metrics are inversely related for a given muscle size because of fundamental constraints in sarcomere length-tension relationships. How these competing performance metrics change in developing primates is largely unknown. Here, we quantified in vivo bite forces and gapes across ontogeny and examined these data in relation to body mass and cranial measurements in captive tufted capuchins, Sapajus spp. Bite force and gape were also compared across geometric and mechanical properties of mechanically challenging foods to investigate relationships between bite force, gape and food accessibility (defined here as the ability to breach shelled nuts). Bite forces at a range of gapes and feeding behavioral data were collected from a cross-sectional ontogenetic series of 20 captive and semi-wild tufted capuchins at the Núcleo de Procriação de Macacos-Prego Research Center in Araçatuba, Brazil. These data were paired with body mass, photogrammetric measures of jaw length and facial width, and food geometric and material properties. Tufted capuchins with larger body masses had absolutely higher in vivo bite forces and gapes, and animals with wider faces had absolutely higher bite forces. Bite forces and gapes were significantly smaller in juveniles compared with subadults and adults. These are the first primate data to empirically demonstrate the gapes at which maximum active bite force is generated and to demonstrate relationships to food accessibility. These data advance our understanding of how primates meet the changing performance demands of the feeding system during development.

Does the model reflect the system? When two-dimensional biomechanics is not 'good enough'.

Models are mathematical representations of systems, processes or phenomena. In biomechanics, finite-element modelling (FEM) can be a powerful tool, allowing biologists to test form-function relationships in silico, replacing or extending results of in vivo experimentation. Although modelling simplifications and assumptions are necessary, as a minimum modelling requirement the results of the simplified model must reflect the biomechanics of the modelled system. In cases where the three-dimensional mechanics of a structure are important determinants of its performance, simplified two-dimensional modelling approaches are likely to produce inaccurate results. The vertebrate mandible is one among many three-dimensional anatomical structures routinely modelled using two-dimensional FE analysis. We thus compare the stress regimes of our published three-dimensional model of the chimpanzee mandible with a published two-dimensional model of the chimpanzee mandible and identify several fundamental differences. We then present a series of two-dimensional and three-dimensional FE modelling experiments that demonstrate how three key modelling parameters, (i) dimensionality, (ii) symmetric geometry, and (iii) constraints, affect deformation and strain regimes of the models. Our results confirm that, in the case of the primate mandible (at least), two-dimensional FEM fails to meet this minimum modelling requirement and should not be used to draw functional, ecological or evolutionary conclusions.

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.

The influence of jaw-muscle fibre-type phenotypes on estimating maximum muscle and bite forces in primates.

Numerous anthropological studies have been aimed at estimating jaw-adductor muscle forces, which, in turn, are used to estimate bite force. While primate jaw adductors show considerable intra- and intermuscular heterogeneity in fibre types, studies generally model jaw-muscle forces by treating the jaw adductors as either homogeneously slow or homogeneously fast muscles. Here, we provide a novel extension of such studies by integrating fibre architecture, fibre types and fibre-specific tensions to estimate maximum muscle forces in the masseter and temporalis of five anthropoid primates: Sapajus apella (N = 3), Cercocebus atys (N = 4), Macaca fascicularis (N = 3), Gorilla gorilla (N = 1) and Pan troglodytes (N = 2). We calculated maximum muscle forces by proportionally adjusting muscle physiological cross-sectional areas by their fibre types and associated specific tensions. Our results show that the jaw adductors of our sample ubiquitously express MHC α-cardiac, which has low specific tension, and hybrid fibres. We find that treating the jaw adductors as either homogeneously slow or fast muscles potentially overestimates average maximum muscle forces by as much as approximately 44%. Including fibre types and their specific tensions is thus likely to improve jaw-muscle and bite force estimates in primates.

Comparative biomechanics of the Pan and Macaca mandibles during mastication: finite element modelling of loading, deformation and strain regimes.

The mechanical behaviour of the mandibles of Pan and Macaca during mastication was compared using finite element modelling. Muscle forces were calculated using species-specific measures of physiological cross-sectional area and scaled using electromyographic estimates of muscle recruitment in Macaca. Loading regimes were compared using moments acting on the mandible and strain regimes were qualitatively compared using maps of principal, shear and axial strains. The enlarged and more vertically oriented temporalis and superficial masseter muscles of Pan result in larger sagittal and transverse bending moments on both working and balancing sides, and larger anteroposterior twisting moments on the working side. The mandible of Pan experiences higher principal strain magnitudes in the ramus and mandibular prominence, higher transverse shear strains in the top of the symphyseal region and working-side corpus, and a predominance of sagittal bending-related strains in the balancing-side mandible. This study lays the foundation for a broader comparative study of Hominidae mandibular mechanics in extant and fossil hominids using finite element modelling. Pan's larger and more vertical masseter and temporalis may make it a more suitable model for hominid mandibular biomechanics than Macaca.

Fiber-type phenotype of the jaw-closing muscles in Gorilla gorilla, Pan troglodytes, and Pan paniscus: A test of the Frequent Recruitment Hypothesis.

Skeletal muscle fiber types are important determinants of the contractile properties of muscle fibers, such as fatigue resistance and shortening velocity. Yet little is known about how jaw-adductor fiber types correlate with feeding behavior in primates. Compared with chimpanzees and bonobos, gorillas spend a greater percentage of their daily time feeding and shift to herbaceous vegetation when fruits are scarce. We thus used the African apes to test the hypothesis that chewing with unusually high frequency is correlated with the expression in the jaw adductors of a high proportion of type 1 (slow, fatigue-resistant) fibers at the expense of other fiber types (the Frequent Recruitment Hypothesis). We used immunohistochemistry to determine the presence and distribution of the four major myosin heavy chain (MHC) isoforms in the anterior superficial masseter (ASM), superficial anterior temporalis, and deep anterior temporalis of four Gorilla gorilla, two Pan paniscus, and four Pan troglodytes. Serial sections were stained against slow (MHC-1/-α-cardiac) and fast (MHC-2/-M) fibers. Fibers were counted and scored for staining intensity, and fiber cross-sectional areas (CSAs) were measured and used to estimate percentage of CSA of each MHC isoform. Hybrid fibers accounted for nearly 100% of fiber types in the masseter and temporalis of all three species, resulting in three main hybrid phenotypes. As predicted, the gorilla ASM and deep anterior temporalis comprised a greater percentage of CSA of the slower, fatigue-resistant hybrid fiber type, significantly so for the ASM (p = 0.015). Finally, the results suggest that fiber phenotype of the chewing muscles contributes to behavioral flexibility in ways that would go undetected in paleontological studies relying solely on morphology of the bony masticatory apparatus.

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.

Muscle architecture dynamics modulate performance of the superficial anterior temporalis muscle during chewing in capuchins.

Jaw-muscle architecture is a key determinant of jaw movements and bite force. While static length-force and force-velocity relationships are well documented in mammals, architecture dynamics of the chewing muscles and their impact on muscle performance are largely unknown. We provide novel data on how fiber architecture of the superficial anterior temporalis (SAT) varies dynamically during naturalistic feeding in tufted capuchins (Sapajus apella). We collected data on architecture dynamics (changes in muscle shape or the architectural gear ratio) during the gape cycle while subjects fed on foods of different mechanical properties. Architecture of the SAT varied with phases of the gape cycle, but gape distance accounted for the majority of dynamic changes in architecture. In addition, lower gear ratios (low muscle velocity relative to fascicle velocity) were observed when animals chewed on more mechanically resistant foods. At lower gear ratios, fibers rotated less during shortening resulting in smaller pinnation angles, a configuration that favors increased force production. Our results suggest that architectural dynamics may influence jaw-muscle performance by enabling the production of higher bite forces during the occlusal phase of the gape cycle and while processing mechanically challenging foods.

The dental microwear of hard-object feeding in laboratory Sapajus apella and its implications for dental microwear formation.

OBJECTIVES: This study seeks to determine if (a) consumption of hard food items or a mixture of food items leads to the formation of premolar or molar microwear in laboratory capuchin monkeys (Sapajus apella) in one feeding session and (b) rates of microwear formation are associated with the number of food items consumed. MATERIALS AND METHODS: Five adult male capuchins were used in two experiments, one where they were fed unshelled Brazil nuts, and the other where they were fed a mixture of food items. Dental impressions were taken before and after each feeding session. Epoxy casts made from those impressions then were used in SEM analyses of rates of microwear formation. Upper and lower premolars and molars were analyzed. Qualitative comparisons were made and Spearman's rank-order correlations used to examine the relationship between rates of microwear formation and number of Brazil nuts consumed. RESULTS: Premolars and molars generally showed new microwear in the form of pits and scratches. However, the incidence of those features was low (0-6%). Rates of microwear formation were highest during the consumption of Brazil nuts. DISCUSSION: Variations in the rate of microwear formation on the premolars likely reflected patterns of ingestion whereas consistency in the rate of microwear on the molars likely reflected patterns of chewing. While dental microwear formation seemed to be correlated with the number of hard objects consumed, rates did differ between individuals. Differences in results between the two experiments demonstrate some of the limitations in our knowledge of dental microwear formation.

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.