Passive forces generated by the jaw adductor muscles and their connective tissues are thought to play a protective role in the feeding system by limiting gape to avoid hyperextension and minimize distractive forces at the temporomandibular joint. However, passive muscle forces have only been measured in individual jaw adductors of two non-primate mammals, and it is unknown how these forces translate to bite force at the occlusal surface and affect gape behaviors. We measured in vivo passive bite forces in eight adult Macaca mulatta at anterior (I1) and posterior (M1) bite points across linear gapes ranging from 15 to 50 mm. Active bite force data were collected at the anterior bite point from two of these macaques (one male, one female) using a custom-built bite force transducer across linear gapes ranging from 10 to 60 mm. We demonstrate that M. mulatta passive bite forces increase with gape and vary by bite point, with forces larger at M1 compared with I1 for both linear and angular gapes. Our experimental data and Hill-type muscle models of both active and passive forces suggest that passive bite forces are absolutely and relatively small at the occlusal surface in macaques and play a minimal role in constraining gape. These are the first empirical data on bite force passive tension in primates, and the first data to suggest that the macaque jaw adductor muscles exhibit unusually high compliance, potentially relating to selection for large gape behaviors.

The constrained lever model (CLM) predicts that the jaw adductor resultant muscle forces (RMFs) must pass through a 'triangle of support' (ToS) to prevent temporomandibular joint (TMJ) distraction during biting. The CLM defines distracting forces as perpendicular to the plane of the ToS, but the orientation of the ToS varies both within and between individuals based on bite point, gape, and differences in the height of the TMJ. We compare TMJ distractive forces estimated using a ToS plane versus a fixed, horizontal plane criterion across a range of gapes using muscle moments and forces for the three major jaw adductor muscles in 97 morphologically diverse primate species. At occlusion, 80% of the species experienced stabilizing compressive forces under a horizontal plane criterion, but only 44% of species had an RMF inside the ToS. This mismatch indicates that predictions of TMJ distraction and joint stability are highly dependent upon the comparison plane, which is challenging for comparisons between primates with varying TMJ heights, and consequently, ToS orientations. Joint stability increased with gape but varied little with taxonomy and across diet categories. These results provide strong evidence that the CLM is a poor predictor of the joint stability when the TMJs are elevated. These findings suggest future applications of the CLM should either focus on taxa with TMJs near the occlusal plane or calculate joint reaction forces directly to assess joint stability in mammals with elevated TMJs.

The jaw-adductor muscles drive the movements and forces associated with primate feeding behaviors such as biting and chewing as well as social signaling behaviors such as wide-mouth canine display. The past several decades have seen a rise in research aimed at the anatomy and physiology of primate chewing muscles to better understand the functional and evolutionary significance of the primate masticatory apparatus. This review summarizes variation in jaw-adductor fiber types and muscle architecture in primates, focusing on physiological, architectural, and behavioral performance variables such as specific tension, fatigue resistance, muscle and bite force, and muscle stretch and gape. Paranthropus and Australopithecus are used as one paleontological example to showcase the importance of these data for addressing paleobiological questions. The high degree of morphological variation related to sex, age, muscle, and species suggests future research should bracket ranges of performance variables rather than focus on single estimates of performance.

Movement at complex joints, such as the ankle, can be challenging to quantify from external kinematics alone. We compared X-ray reconstruction of moving morphology (XROMM) and angles derived from high-speed video footage to study dorsiflexion in the ankle of a rhesus macaque (Macaca mulatta) during stance phase. We found inconsistent correspondence between angles measured on standard videos using five approaches and those measured directly on the talocrural joint using XROMM, indicating that different measurement methods capture different kinematic processes. Many externally measured angles indicate a range of motion of 30 deg during stance phase. The XROMM data, however, demonstrate that the talocrural joint itself only dorsiflexes about 15 deg through stance phase, with much greater mobility during swing phase. This suggests that other parts of the foot, likely the midfoot, contribute substantially to dorsiflexion in stance phase, while the talocrural joint is actively held in place.

OBJECTIVES:Bite force has received significant attention in biological anthropology, but maximum bite force estimates for a single primate species often span hundreds of newtons. In this synthesis, we discuss the definitions of maximum bite force, review and highlight the variability in methods used to assess bite force in primates, and compare bite force ranges in macaques to bracket maximum force estimates between physiological and mechanical maxima. MATERIALS AND METHODS:Methods of estimating bite force in primates were gathered from the literature along with published estimates of maximum bite force for macaques (Macaca sp.). RESULTS:Maximum bite force can be defined physiologically or mechanically, and methods of estimating bite force can be grouped as in vivo, muscle-based, and craniodental within these two definitions. Physiological estimates occur under natural conditions modulated by sensorimotor feedback, whereas mechanical maximum bite forces ignore muscular and neural limitations. Published maximum bite forces for macaques at the molars vary from 127 N to 898 N, a 771 N range. Using a bracketing approach suggested here, we narrow the estimated bite force range at the incisors to 487-503 N and 503-898 N for the molars. DISCUSSION:This synthesis emphasizes the need for comparisons between in vivo, muscle-based, and craniodental bite force methods in living primates. We propose bracketing bite force estimates between physiological and mechanical maxima in order to provide more reliable bite force estimates and improve understanding of how bite force relates to primate functional morphology and feeding ecology.

OBJECTIVES:Wild juvenile capuchins exhibit lower feeding success than adults, particularly for mechanically challenging foods, but ontogenetic changes in oral food processing behaviors related to this reduced success are unknown. We test how oral food processing efficiency varies across development in an experimental setting in tufted capuchins (Sapajus spp.). Further, we simulate discontinuous feeding observations to test the comparability of behaviors measured in wild and captive settings. MATERIALS AND METHODS:Twenty-nine captive and semi-wild infants (n = 2), juveniles (n = 12), older juveniles (n = 4), and subadults-adults (n = 11) were video recorded while feeding at the Núcleo de Procriação de Macacos-Prego Research Center (Araçatuba, Brazil). Each animal was offered a series of five foods ranging in volume, toughness, and elastic modulus. RESULTS:Measures of oral food processing inconsistently varied with sex; however, younger animals were less efficient in food processing than older individuals. Larger and more mechanically challenging foods were associated with longer feeding sequence durations and an increased frequency of anterior ingestion, posterior ingestion, and chewing during a feeding sequence. Simulated discontinuous data from the first and last halves of the feeding sequences closely replicated continuous results. CONCLUSIONS:Our results indicate younger capuchins have reduced oral food processing efficiency compared to adults through increased duration, behavioral frequencies, number of chews, and behavioral patterns. Further, our continuous and discontinuous comparisons support the use of discontinuous feeding behaviors from the first and last halves of the feeding sequence. We caution that researchers should be careful to capture infrequent behaviors when using discontinuous data.

Objectives: Cortical bone geometry is commonly used to investigate biomechanical properties of primate mandibles. However, the ontogeny of these properties is less understood. Here we investigate changes in cortical bone cross-sectional properties throughout capuchin ontogeny and compare captive versus wild, semi-provisioned groups. Tufted capuchins (Sapajus spp.) are known to consume relatively hard/tough foods, while untufted capuchins (Cebus spp.) exploit less mechanically challenging foods. Previous research indicates dietary differences are present early in development and adult Sapajus mandibles can resist higher bending/shear/torsional loads. Materials and methods: This study utilized microCT scans of 22 Cebus and 45 Sapajus from early infancy to adulthood from three sample populations: one captive Cebus, one captive Sapajus, and one semi-provisioned, free-ranging Sapajus. Mandibular cross-sectional properties were calculated at the symphysis, P3, and M1. If the tooth had not erupted, its position within the crypt was used. A series of one-way ANOVAs were performed to assess differences between and within the sample populations. Results: Mandible robusticity increases across ontogeny for all three sample populations. Sapajus were better able to withstand bending and torsional loading even early in ontogeny, but no difference in shear resistance was found. Semi-provisioned, free-ranging Sapajus tend to show increased abilities to resist bending and torsional loading but not shear loading compared to captive Sapajus. Discussion: This study helps advance our understanding of the primate masticatory system development and opens the door for further studies into adaptive plasticity in shaping the masticatory apparatus of capuchins and differences in captive versus free-ranging sample populations.

Orienting a food item held in the hand to withdraw and optimally place it in the mouth for eating (withdraw-to-eat) is mediated by vision in catarrhine anthropoids and by nonvisual strategies in strepsirrhine primates. The present study asks whether vision contributes to the withdraw-to-eat movements in a platyrrhine anthropoid Cebus imitator, a member of a monophyletic primate suborder whose stem group diverged from catarrhines about 40 million years ago. Cebus imitator’s gaze and hand use for foraging for fruit is examined in its fine branch niche, the terminal branches of trees. Video of reach, grasp and withdraw-to-eat movements with associated gaze were examined frame-by-frame to assess food manipulation and its sensory control. Cebus imitator uses vision and touch to reach for and grasp food items with precision and whole hand grasps. They use vision to orient food items held in-hand into a precision grip and their withdraw-to-eat is assisted with a vertically oriented hand. The conjoint use of vision, a precision grasp, and hand posture and a central representation of object control likely originated in stem anthropoids and was derived from the staged evolution of the visual manipulation of food and other objects.

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.

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.

How animals process and absorb nutrients from their food is a fundamental question in biology. Despite the continuity and interaction between intraoral food processing and post-oesophageal nutritional extraction, these topics have largely been studied separately. At present, we lack a synthesis of how pre- and post-oesophageal mechanisms of food processing shape the ability of various taxa to effectively assimilate nutrients from their diet. The aim of this special issue is to catalyse a unification of these distinct approaches as a functional continuum. We highlight questions that derive from this synthesis, as well as technical advances to address these questions. At present, there is also a skew toward vertebrates in studies of feeding form-function mechanics; by including perspectives from researchers working on both vertebrates and invertebrates, we hope to stimulate integrative and comparative research on food processing and nutritional assimilation. Below, we discuss how the papers in this issue contribute to these goals in three areas: championing a functional-comparative approach, quantifying performance and emphasizing the effects of life history, and food substrate and extrinsic factors in current and future studies of oral food processing and nutritional assimilation. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

There are no comparative, empirical studies of the energetic costs of feeding in mammals. As a result, we lack physiological data to better understand the selection pressures on the mammalian feeding apparatus and the influence of variables such as food geometric and material properties. This study investigates interspecific scaling of the net energetic costs of feeding in relation to body size, jaw-adductor muscle mass and food properties in a sample of 12 non-human primate species ranging in size from 0.08 to 4.2 kg. Net energetic costs during feeding were measured by indirect calorimetry for a variety of pre-cut and whole raw foods varying in geometric and material properties. Net feeding costs were determined in two ways: by subtracting either the initial metabolic rate prior to feeding or subtracting the postprandial metabolic rate. Interspecific scaling relationships were evaluated using pGLS and OLS regression. Net feeding costs scale negatively relative to both body mass and jaw-adductor mass. Large animals incur relatively lower feeding costs indicating that small and large animals experience and solve mechanical challenges in relation to energetics in different ways. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.