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.

Biomechanical and Cortical Control of Tongue Movements During Chewing and Swallowing.

Tongue function is vital for chewing and swallowing and lingual dysfunction is often associated with dysphagia. Better treatment of dysphagia depends on a better understanding of hyolingual morphology, biomechanics, and neural control in humans and animal models. Recent research has revealed significant variation among animal models in morphology of the hyoid chain and suprahyoid muscles which may be associated with variation in swallowing mechanisms. The recent deployment of XROMM (X-ray Reconstruction of Moving Morphology) to quantify 3D hyolingual kinematics has revealed new details on flexion and roll of the tongue during chewing in animal models, movements similar to those used by humans. XROMM-based studies of swallowing in macaques have falsified traditional hypotheses of mechanisms of tongue base retraction during swallowing, and literature review suggests that other animal models may employ a diversity of mechanisms of tongue base retraction. There is variation among animal models in distribution of hyolingual proprioceptors but how that might be related to lingual mechanics is unknown. In macaque monkeys, tongue kinematics-shape and movement-are strongly encoded in neural activity in orofacial primary motor cortex, giving optimism for development of brain-machine interfaces for assisting recovery of lingual function after stroke. However, more research on hyolingual biomechanics and control is needed for technologies interfacing the nervous system with the hyolingual apparatus to become a reality.

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'.

Head posture impacts mammalian hyoid position and suprahyoid muscle length: implication for swallowing biomechanics.

Instantaneous head posture (IHP) can extensively alter resting hyoid position in humans, yet postural effects on resting hyoid position remain poorly documented among mammals in general. Clarifying this relationship is essential for evaluating interspecific variation in hyoid posture across evolution, and understanding its implications for hyolingual soft tissue function and swallowing motor control. Using Didelphis virginiana as a model, we conducted static manipulation experiments to show that head flexion shifts hyoid position rostrally relative to the cranium across different gapes. IHP-induced shifts in hyoid position along the anteroposterior axis are comparable to in vivo hyoid protraction distance during swallowing. IHP also has opposite effects on passive genio- and stylohyoid muscle lengths. High-speed biplanar videoradiography suggests Didelphis consistently swallows at neutral to flexed posture, with stereotyped hyoid kinematics across different head postures. IHP change can affect suprahyoid muscle force production by shifting their positions on the length-tension curve, and redirecting lines of action and the resultant force from supra- and infrahyoid muscles. We hypothesize that demands on muscle performance may constrain the range of swallowing head postures in mammals. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Introduction: food processing and nutritional assimilation in animals.

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'.

Rhythmic chew cycles with distinct fast and slow phases are ancestral to gnathostomes.

Intra-oral food processing, including chewing, is important for safe swallowing and efficient nutrient assimilation across tetrapods. Gape cycles in tetrapod chewing consist of four phases (fast open and -close, and slow open and -close), with processing mainly occurring during slow close. Basal aquatic-feeding vertebrates also process food intraorally, but whether their chew cycles are partitioned into distinct phases, and how rhythmic their chewing is, remains unknown. Here, we show that chew cycles from sharks to salamanders are as rhythmic as those of mammals, and consist of at least three, and often four phases, with phase distinction occasionally lacking during jaw opening. In fishes and aquatic-feeding salamanders, fast open has the most variable duration, more closely resembling mammals than basal amniotes (lepidosaurs). Across ontogenetically or behaviourally mediated terrestrialization, salamanders show a distinct pattern of the second closing phase (near-contact) being faster than the first, with no clear pattern in partitioning of variability across phases. Our results suggest that distinct fast and slow chew cycle phases are ancestral for jawed vertebrates, followed by a complicated evolutionary history of cycle phase durations and jaw velocities across fishes, basal tetrapods and mammals. These results raise new questions about the mechanical and sensorimotor underpinnings of vertebrate food processing. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Three-dimensional mandibular kinematics of mastication in the marsupial Didelphis virginiana.

Didelphis virginiana (the Virginia opossum) is often used as an extant model for understanding feeding behaviour in Mesozoic mammaliaforms, primarily due to their morphological similarities, including an unfused mandibular symphysis and tribosphenic molars. However, the three-dimensional jaw kinematics of opossum chewing have not yet been fully quantified. We used biplanar videofluoroscopy and the X-Ray Reconstruction of Moving Morphology workflow to quantify mandibular kinematics in four wild-caught opossums feeding on hard (almonds) and soft (cheese cubes) foods. These data were used to test hypotheses regarding the importance of roll versus yaw in chewing by early mammals, and the impact of food material properties (FMPs) on jaw kinematics. The magnitude of roll exceeds that of yaw, but both are necessary for tooth-tooth or tooth-food-tooth contact between complex occlusal surfaces. We confirmed the utility of the four vertical kinematic gape cycle phases identified in tetrapods but we further defined two more in order to capture non-vertical kinematics. Statistical tests support the separation of chew cycle phases into two functional groups: occlusal and non-occlusal phases. The separation of slow close into two (occlusal) phases gives quantitative kinematic support for the long-hypothesized multifunctionality of the tribosphenic molar. 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'.

Multiple regions of sensorimotor cortex encode bite force and gape.

The precise control of bite force and gape is vital for safe and effective breakdown and manipulation of food inside the oral cavity during feeding. Yet, the role of the orofacial sensorimotor cortex (OSMcx) in the control of bite force and gape is still largely unknown. The aim of this study was to elucidate how individual neurons and populations of neurons in multiple regions of OSMcx differentially encode bite force and static gape when subjects (Macaca mulatta) generated different levels of bite force at varying gapes. We examined neuronal activity recorded simultaneously from three microelectrode arrays implanted chronically in the primary motor (MIo), primary somatosensory (SIo), and cortical masticatory (CMA) areas of OSMcx. We used generalized linear models to evaluate encoding properties of individual neurons and utilized dimensionality reduction techniques to decompose population activity into components related to specific task parameters. Individual neurons encoded bite force more strongly than gape in all three OSMCx areas although bite force was a better predictor of spiking activity in MIo vs. SIo. Population activity differentiated between levels of bite force and gape while preserving task-independent temporal modulation across the behavioral trial. While activation patterns of neuronal populations were comparable across OSMCx areas, the total variance explained by task parameters was context-dependent and differed across areas. These findings suggest that the cortical control of static gape during biting may rely on computations at the population level whereas the strong encoding of bite force at the individual neuron level allows for the precise and rapid control of bite force.

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.

The biomechanics of chewing and suckling in the infant: A potential mechanism for physiologic metopic suture closure.

Craniosynostosis is a condition with neurologic and aesthetic sequelae requiring invasive surgery. Understanding its pathobiology requires familiarity with the processes underlying physiologic suture closure. Animal studies have shown that cyclical strain from chewing and suckling influences the closure of cranial vault sutures, especially the metopic, an important locus of craniosynostosis. However, there are no human data correlating strain patterns during chewing and suckling with the physiologically early closure pattern of the metopic suture. Furthermore, differences in craniofacial morphology make it challenging to directly extrapolate animal findings to humans. Eight finite-element analysis (FEA) models were built from craniofacial computer tomography (CT) scans at varying stages of metopic suture closure, including two with isolated non-syndromic metopic craniosynostosis. Muscle forces acting on the cranium during chewing and suckling were simulated using subject-specific jaw muscle cross-sectional areas. Chewing and suckling induced tension at the metopic and sagittal sutures, and compressed the coronal, lambdoid, and squamous sutures. Relative to other cranial vault sutures, the metopic suture experienced larger magnitudes of axial strain across the suture and a lower magnitude of shear strain. Strain across the metopic suture decreased during suture closure, but other sutures were unaffected. Strain patterns along the metopic suture mirrored the anterior to posterior sequence of closure: strain magnitudes were highest at the glabella and decreased posteriorly, with minima at the nasion and the anterior fontanelle. In models of physiologic suture closure, increased degree of metopic suture closure correlated with higher maximum principal strains across the frontal bone and mid-face, a strain regime not observed in models of severe metopic craniosynostosis. In summary, our work provides human evidence that bone strain patterns from chewing and suckling correlate with the physiologically early closure pattern of the metopic suture, and that deviations from physiologic strain regimes may contribute to clinically observed craniofacial dysmorphism.

Robust cortical encoding of 3D tongue shape during feeding in macaques.

Dexterous tongue deformation underlies eating, drinking, and speaking. The orofacial sensorimotor cortex has been implicated in the control of coordinated tongue kinematics, but little is known about how the brain encodes-and ultimately drives-the tongue's 3D, soft-body deformation. Here we combine a biplanar x-ray video technology, multi-electrode cortical recordings, and machine-learning-based decoding to explore the cortical representation of lingual deformation. We trained long short-term memory (LSTM) neural networks to decode various aspects of intraoral tongue deformation from cortical activity during feeding in male Rhesus monkeys. We show that both lingual movements and complex lingual shapes across a range of feeding behaviors could be decoded with high accuracy, and that the distribution of deformation-related information across cortical regions was consistent with previous studies of the arm and hand.

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.

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.

Iyuku raathi, a new iguanodontian dinosaur from the Early Cretaceous Kirkwood Formation, South Africa.

We name and describe a new iguanodontian dinosaur from the Early Creteceous Kirkwood Formation, Eastern Cape Province, South Africa. This dinosaur is one of only two ornithopod dinosaurs known from the Cretaceous of southern Africa, and is unique in being represented primarily by hatchling to young juvenile individuals as demonstrated by bone histological analysis. All of the juvenile material of this new taxon comes from a single, laterally-restricted bonebed and specimens were primarily recovered as partial to complete single elements, although rare articulated materials and one partial skeleton were found. Sedimentology of the bonebed suggests that this horizon heralds a change in environment upsection to a drier and more seasonal climate. This accumulation of bones is interpreted as seasonal mortality from a nesting site or nesting grounds and may be linked to this environmental shift.

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.