The functional significance of primate mandibular form.

A stress analysis of the primate mandible suggests that vertically deep jaws in the molar region are usually an adaptation to counter increased sagittal bending stress about the balancing-side mandibular corpus during unilateral mastication. This increased bending stress about the balancing side is caused by an increase in the amount of balancing-side muscle force. Furthermore, this increased muscle force will also cause an increase in dorso-ventral shear stress along the mandibular symphysis. Since increased symphyseal stress can be countered by symphyseal fusion and as increased bending stress can be countered by a deeper jaw, deep jaws and symphyseal fusion are often part of the same functional pattern. In some primates (e.g., Cercocebus albigena), deep jaws are an adaptation to counter bending in the sagittal plane during powerful incisor biting, rather than during unilateral mastication. The stress analysis of the primate mandible also suggests that jaws which are transversely thick in the molar region are an adaptation to counter increased torsion about the long axis of the working-side mandibular corpus during unilateral mastication. Increased torsion of the mandibular corpus can be caused by an increase in masticatory muscle force, an increase in the transverse component of the postcanine bite force and/or an increase in premolar use during mastication. Patterns of masticatory muscle force were estimated for galagos and macaques, demonstrating that the ratio of working-side muscle force to balancing-side muscle force is approximately 1.5:1 in macaques and 3.5:1 in galagos during unilateral isometric molar biting. These data support the hypothesis that mandibular symphyseal fusion is an adaptative response to maximize unilateral molar bite force by utilizing a greater percentage of balancing-side muscle force.     

The human mandible: Lever or link?

The mammalian mandible, and in particular the human mandible, is generally thought to function as a lever during biting. This notion, however, has not gone unchallenged. Various workers have suggested that the mandible does not function as a lever, and they base this proposition on essentially two assertions: (1) the resultant of the forces produced by the masticatory muscles always passes through the bite point; (2) the condylar neck and/or the temporomandibular joint is unsuited to withstand reaction forces during biting. A review of the electromyographic data and of the properties of the tissues of the temporomandibular joint do not support the non-lever hypothesis of mandibular function. In addition, an analysis of the strength of the condylar neck demonstrates that this structure is strong enough to withstand the expected reaction force during lever action. Ordinarily the human mandible and the forces that act upon it are analyzed solely in the lateral projection. Moments are then usually analyzed about the mandibular condyle; however, some workers have advocated taking moments about other points, e.g., the instantaneous center of rotation. Obviously it makes no difference as to what point is chosen since the moments about any point during equilibrium conditions are equal to zero. It is also useful to analyze the forces acting on the mandible in the frontal projection, particularly during unilateral biting. The electromyographic data suggest that during powerful unilateral molar biting the resultant adductor muscle force is passing between the bite point and the balancing (non-biting side) condyle. Therefore, in order for this system to be in equilibrium there must be a reaction force acting on the balancing condyle. This suggests that reaction forces are larger on the balancing side than on the working side, and possibly explains why individuals with a painful temporomandibular joint usually prefer to bite on the side of the diseased joint.     

In vivo bone strain in the mandible of Galago crassicaudatus.

Single element foil strain gages were bonded to mandibular cortical bone in eight specimens of Galago crassicaudatus. The gage was bonded below the Pm4 or M2 adjacent to the lower border of the mandible. The bonded strain gage was connected to form one arm of a Wheatstone bridge. Following recovery from the general anesthetic, the restrained Galago bit either a piece of wood, a food object, or a bite force transducer. During these biting episodes, mandibular bone strain deformed the strain gage and the resulting change in electrical resistance of the gage caused voltage changes across the Wheatstone bridge. These changes, directly proportional to the amount of bone strain along the gage site, were recovered by a strip chart recorder. Bone strain was measured on both the working and balancing sides of the jaws. Maximum values of bone strain and bite force were 435 microstrain (compression) and 8.2 kilograms respectively. During bending of the mandible, the correlation between bone strain (tension or compression) and bite force ranged from -0.893 (tension) to 0.997 (compression). The experiments reported here demonstrate that only a small percentage of the Galago bite force is due to balancing side muscle force during isometric unilateral molar biting. In addition, these experiments demonstrate that the Galago mandible is bent in a predictable manner during biting. The amount of apparent mandibular bone strain is dependent on (1) the magnitude of the bite force and (2) the position of the bite point.     

Comparison between in vivo and theoretical bite performance: Using multi-body modelling to predict muscle and bite forces in a reptile skull

In biomechanical investigations, geometrically accurate computer models of anatomical structures can be created readily using computed-tomography scan images. However, representation of soft tissue structures is more challenging, relying on approximations to predict the muscle loading conditions that are essential in detailed functional analyses. Here, using a sophisticated multi-body computer model of a reptile skull (the rhynchocephalian Sphenodon), we assess the accuracy of muscle force predictions by comparing predicted bite forces against in vivo data. The model predicts a bite force almost three times lower than that measured experimentally. Peak muscle force estimates are highly sensitive to fibre length, muscle stress, and pennation where the angle is large, and variation in these parameters can generate substantial differences in predicted bite forces. A review of theoretical bite predictions amongst lizards reveals that bite forces are consistently underestimated, possibly because of high levels of muscle pennation in these animals. To generate realistic bites during theoretical analyses in Sphenodon, lizards, and related groups we suggest that standard muscle force calculations should be multiplied by a factor of up to three. We show that bite forces increase and joint forces decrease as the bite point shifts posteriorly within the jaw, with the most posterior bite location generating a bite force almost double that of the most anterior bite. Unilateral and bilateral bites produced similar total bite forces; however, the pressure exerted by the teeth is double during unilateral biting as the tooth contact area is reduced by half.     

Mandibular function in Galago crassicaudatus and Macaca fascicularis: an in vivo approach to stress analysis of the mandible.

Single-element and/or rosette strain gages were bonded to mandibular cortical bone in Galago crassicaudatus and Macaca fascicularis. Five galago and eleven macaque bone strain experiments were performed and analyzed. In vivo bone strain was recorded from the lateral surface of the mandibular corpus below the postcanine tooth row during transducer biting and during mastication and ingestion of food objects. In macaques and galagos, the mandibular corpus on the balancing side is primarily bent in the sagittal plane during mastication and is both twisted about its long axis and bent in the sagittal plane during transducer biting. On the working side, it is primarily twisted about its long axis and directly sheared perpendicular to its long axis, and portions of it are bent in the sagittal plane during mastication and molar transducer biting. In macaques, the mandibular corpus on each side is primarily bent in the sagittal plane and twisted during incisal transducer biting and ingestion of food objects, and it is transversely bent and slightly twisted during jaw opening. Since galagos usually refused to bite the transducer or food objects with their incisors, an adequate characterization of mandibular stress patterns during these behaviors was not possible. In galagos the mandibular corpus experiences very little transverse bending stress during jaw opening, perhaps in part due to its unfused mandibular symphysis. Marked differences in the patterns of mandibular bone strain were present between galagos and macaques during the masticatory power stroke and during transducer biting. Galagos consistently had much more strain on the working side of the mandibular corpus than on the balancing side. These experiments support the hypothesis that galagos, in contrast to macaques, employ a larger amount of working-side muscle force relative to the balancing-side muscle force during unilateral biting and mastication, and that the fused mandibular symphysis is an adaption to use a maximal amount of balancing-side muscle force during unilateral biting and mastication. These experiments also demonstrate the effects that rosette position, bite force magnitudes, and types of food eaten have on recorded mandibular strain patterns.     

A functional analysis of carnassial biting

The jaw mechanism of carnivores is studied using an idealized model (Greaves, 1978). The model assumes: (i) muscle activity on both sides of the head, and (ii) that the jaw joints and the carnassial teeth are single points of contact between the skull and the lower jaw during carnassial biting. The model makes the following predictions: (i) in carnivores with carnassial teeth the resultant force of the jaw muscles will be positioned approximately 60% of the way from the jaw joint to the tooth—this arrangement delivers the maximum bite force possible together with a reasonably wide gape (remembering that bite force and gape cannot both be maximized); (ii) in an evolutionary sense, if greater bite force is required at the carnassial tooth, either the animal will get larger so as to deliver an absolutely larger bite force or the architecture of the muscles may change, becoming more pinnate, for example, but jaw geometry (i.e. the relative positions of the jaw joints, the carnassial tooth, and the muscle resultant force) will not change; (iii) if greater gape is required, the animal will get larger so as to have longer jaws and therefore an absolutely wider gape or change its muscle architecture allowing for greater stretch while the geometry remains unchanged; and (iv) in animals with a longer shearing region (e.g. the extinct hyaenodonts) the shearing region will be approximately 20% of jaw length and the muscle resultant force will be positioned approximately 60% of the way from the jaw joint to the most anterior shearing tooth.     

Effects of gape and tooth position on bite force and skull stress in the dingo (Canis lupus dingo) using a 3-dimensional finite element approach

Models of the mammalian jaw have predicted that bite force is intimately linked to jaw gape and to tooth position. Despite widespread use, few empirical studies have provided evidence to validate these models in non-human mammals and none have considered the influence of gape angle on the distribution of stress. Here using a multi-property finite element (FE) model of Canis lupus dingo, we examined the influence of gape angle and bite point on both bite force and cranial stress. Bite force data in relation to jaw gape and along the tooth row, are in broad agreement with previously reported results. However stress data showed that the skull of C. l. dingo is mechanically suited to withstand stresses at wide gapes; a result that agreed well with previously held views regarding carnivoran evolution. Stress data, combined with bite force information, suggested that there is an optimal bite angle of between 25 degrees and 35 degrees in C. l. dingo. The function of these rather small bite angles remains unclear.     

Mechanoreceptor distribution in stag beetle jaws corresponds to the material stress in fights

Male stag beetles (Lucanidae) use their extremely elongated jaws to pinch their rivals forcefully in male–male battles. The morphology of these jaws has to be a compromise between robustness (to withstand the bite forces), length and weight. Cyclommatus metallifer stag beetles circumvent this trade-off by reducing their bite force when biting with their slender jaw tips. Here we describe the functional mechanism behind the force modulation behaviour. Scanning Electron Microscopy and micro CT imaging show large numbers of small sensors in the jaw cuticle. We find a strong correlation between the distribution of these sensors and that of the material stress in the same jaw region during biting. The jaw sensors are mechanoreceptors with a small protrusion that barely protrudes above the undulating jaw surface. The sensors stimulate dendrites that extend from the neuronal cell body through the entire thickness of the jaw exoskeleton towards the sensors at the external surface. They form a sensory field that functions in a feedback mechanism to control the bite muscle force. This negative feedback mechanism enabled the stag beetles to evolve massive bite muscles without risking overloading their valuable jaws.     

Influence of bite force on jaw muscle activity ratios in subject-controlled unilateral isometric biting

Ratios of muscle activities in unilateral isometric biting are assumed to provide information on strategies of muscle activation independently from bite force. If valid, this assumption would facilitate experiments as it would justify subject-control instead of transducer-based force control in biting studies. As force independence of ratios is controversial, we tested whether activity ratios are associated with bite force and whether this could affect findings based on subject-controlled force. In 52 subjects, bite force and bilateral masseter and temporalis electromyograms were recorded during unilateral biting on a transducer with varying force levels and with uniform subject-controlled force. Working/balancing and temporalis/masseter ratios of activity peaks were related to bite force peaks. Activity ratios were significantly but weakly correlated with the bite force. The subject-controlled force varied within ±25% around the prescribed force in 95% of all bites. This scatter could cause a variation of group mean activity ratios of at most ±6% because of the weak correlation between bite force and ratios. As this small variation is negligible in most cases, subject-control of bite force can be considered an appropriate method to obtain group means of relative muscle activation in particular when force control with transducers is not feasible.     

Feedback control from the jaw joints during biting: An investigation of the reptile Sphenodon using multibody modelling

Sphenodon, a lizard-like reptile, is the only living representative of a group that was once widespread at the time of the dinosaurs. Unique jaw mechanics incorporate crushing and shearing motions to breakdown food, but during this process excessive loading could cause damage to the jaw joints and teeth. In mammals like ourselves, feedback from mechanoreceptors within the periodontal ligament surrounding the teeth is thought to modulate muscle activity and thereby minimise such damage. However, Sphenodon and many other tetrapods lack the periodontal ligament and must rely on alternative control mechanisms during biting. Here we assess whether mechanoreceptors in the jaw joints could provide feedback to control muscle activity levels during biting. We investigate the relationship between joint, bite, and muscle forces using a multibody computer model of the skull and neck of Sphenodon. When feedback from the jaw joints is included in the model, predictions agree well with experimental studies, where the activity of the balancing side muscles reduces to maintain equal and minimal joint forces. When necessary, higher, but asymmetric, joint forces associated with higher bite forces were achievable, but these are likely to occur infrequently during normal food processing. Under maximum bite forces associated with symmetric maximal muscle activation, peak balancing side joint forces were more than double those of the working side. These findings are consistent with the hypothesis that feedback similar to that used in the simulation is present in Sphenodon.     

A biomechanical model for analysis of muscle force,power output and lower jaw motion in fishes

Fish skulls are complex kinetic systems with movable components that are powered by muscles. Cranial muscles for jaw closing pull the mandible around a point of rotation at the jaw joint using a third-order lever mechanism. The present study develops a lever model for the jaw of fishes that uses muscle design and the Hill equation for nonlinear length-tension properties of muscle to calculate dynamic power output. The model uses morphometric data on skeletal dimensions and muscle proportions in order to predict behavior and force transmission mediated by lever action. The computer model calculates a range of dynamic parameters of jaw function including muscle force, torque, effective mechanical advantage, jaw velocity, bite duration, bite force, work and power. A complete list of required morphometrics is presented and a software program (MandibLever 2.0) is available for implementing lever analysis. Results show that simulations yield kinematics and timing profiles similar to actual fish feeding events. Simulation of muscle properties shows that mandibles reach their peak velocity near the start of jaw closing, peak force at the end of jaw closing, and peak power output at about 25% of the closing cycle time. Adductor jaw muscles with different mechanical designs must have different contractile properties and/or different muscle activity patterns to coordinate jaw closing. The effective mechanical advantage calculated by the model is considerably lower than the mechanical advantage estimated from morphological lever ratios, suggesting that previous studies of morphological lever ratios have overestimated force and underestimated velocity transmission to the mandible. A biomechanical model of jaw closing can be used to interpret the mechanics of a wide range of jaw mechanisms and will enable studies of the functional results of developmental and evolutionary changes in skull morphology and physiology.     

Mandibular biomechanics and temporomandibular joint function in primates.

There is disagreement as to whether the mandibular condyles are stress-bearing or stress-free during mastication. In support of alternative models, analogies have been drawn with Class III levers, links, and couple systems. Physiological data are reviewed which indicate that maximum masticatory forces are generated when maxillary and mandibular teeth are in contact, and that this phase lasts for over 100 msec during many chewing strokes. During this period, the mandible can be modeled as a beam with multiple supports. Equations of simple beam theory suggest that large condylar reaction forces are present during mastication. With unilateral molar biting in man, the total condylar reaction force may be over 75% of the bite force. Analysis of a frontal projection demonstrates that up to 80% of the total condylar reaction force is borne by the contralateral (balancing side) condyle during unilateral molar biting. A comparison of human, chimpanzee (P. troglodytes), spider monkey (A. belzebuth), and macaque (Macaca sp.) morphology indicates that the frugivorous chimpanzee and spider monkey have a relatively lower condylar reaction force than the omnivorous macaque or man during molar biting. The percentage reaction force during incisal biting is lower in man than in the other primates, and lower in the frugivorous primates than in the macaque.     

An electromyographic analysis of the biting mechanism of the lemon shark,Negaprion Brevirostris: Functional and evolutionary implications

The kinetics of the head and function of select jaw muscles were studied during biting behavior in the lemon shark, Negaprion brevirostris. High speed cinematography and electromyography of seven cranial muscles were recorded during bites elicited by a probe to the oral cavity. In weak bites mandible depression was followed by mandible elevation and jaw closure without cranial elevation. In strong bites cranial elevation always preceded lower jaw depression, lower jaw elevation, and cranial depression. The average duration of the strong bites was rapid (176 msec), considering the size of the animal relative to other fishes. Different electromyographic patterns distinguished the two forms of bite, primarily in activity of the epaxial muscles, which effect cranial elevation. A composite reconstruction of the activity of seven cranial muscles during biting revealed that epaxial muscle activity and consequently cranial elevation preceded all other muscle activity. Mandible depression was primarily effected by contraction of the common coracoarcual and coracomandibularis, with assistance by the coracohyoideus. Simultaneous activity of the levator hyomandibulae is believed to increase the width of the orobranchial chamber. The adductor mandibulae dorsal was the primary jaw adductor assisted by the adductor mandibulae ventral. This biomechanically conservative mechanism for jaw opening in aquatic vertebrates is conserved, with the exception of the coracomandibularis, which is homologous to prehyoid muscles of salamanders.     

Coactivation of jaw muscles: recruitment order and level as a function of bite force direction and magnitude

The aim of this study was to obtain insight into the coactivation behaviour of the jaw muscles under various a priori defined static loading conditions of the mandible. As the masticatory system is mechanically redundant, an infinite number of recruitment patterns is theoretically possible to produce a certain bite force. Using a three-component force transducer and a feedback method, subjects could be instructed to produce a bite force of specific direction and magnitude under simultaneous registration of the EMG activity of anterior and posterior temporal, masseter and digastric muscles on each side. Forces were measured at the second premolars. Vertical, anterior, posterior, lateral and medial force directions were examined; in each direction force levels between 50 N and maximal voluntary force were produced. The results show that for all muscles the bite force-EMG relationship obeys a straight-line fit for forces exceeding 50 N. The relationship varies with bite force direction, except in the case of the digastric muscles. Variation is small for the anterior temporal and large for the posterior temporal and masseter muscles. The relative activation of muscles for a particular force in a particular direction in unique, despite the redundancy.     

Electromyography of the anterior temporalis and masseter muscles of owl monkeys (Aotus trivirgatus) and the function of the postorbital septum

Anthropoids and tarsiers are distinguished from all other vertebrates by the possession of a postorbital septum, which is formed by the frontal, alisphenoid, and zygomatic bones. Cartmill [(1980) In: Evolutionary Biology of the New World Monkeys and Continental Drift. New York: Plenum, p 243-274] suggested that the postorbital septum evolved in the stem lineage of tarsiers and anthropoids to insulate the eye from movements arising in the temporal fossa. Ross [(1996) Am J Phys Anthropol 91:305-324] suggested that the septum insulates the orbital contents from incursions by the line of action of the anterior temporal muscles caused by the unique combination of high degrees of orbital frontation and convergence. Both of these hypotheses must explain why insulation of the orbital contents could not be achieved by decreasing the size of the anterior temporal musculature with a corresponding increase in size of the remaining jaw adductors, rather than evolving a postorbital septum. One possibility is that the anterior temporalis is an important contributor to vertically directed bite forces during all biting and chewing activities. Another possibility is that reduction in anterior temporal musculature would compromise the ability to produce powerful bite forces, either at the incisors or along the postcanine toothrow. To evaluate these hypotheses, electromyographic (EMG) recordings were made from the masseter muscle and the anterior and posterior portions of the temporalis muscles of two owl monkeys, Aotus trivirgatus. The EMG data indicate that anterior temporalis activity relative to that of the superficial masseter is lower during incision than mastication. In addition, activity of the anterior temporalis is not consistently higher than the posterior temporalis during incision. The data indicate relatively greater activity of anterior temporalis compared to other muscles during isometric biting on the postcanine toothrow. This may be due to decreased activity in superficial masseter and posterior temporalis, rather than elevated anterior temporalis activity. The anterior temporalis is not consistently less variable in activity than the superficial masseter and posterior temporalis. The EMG data gathered here indicate no reason for suggesting that the anterior temporal muscles in anthropoids are utilized especially for incisal preparation of hard fruits. Maintenance of relatively high EMG activity in anterior temporalis across a wide range of biting behaviors is to be expected in a vertically oriented and rostrally positioned muscle such as this because, compared to the posterior temporalis, superficial masseter and medial pterygoid, it can contribute relatively larger vertical components of force to bites along the postcanine toothrow. The in vivo data do not support this hypothesis, possibly because of effects of bite point and bite force orientation.     

Incisal bite force direction in humans and the functional significance of mammalian mandibular translation

Incisal bite force direction was recorded and analyzed in ten human subjects using a specially designed force transducer. In all ten subjects the maxillary incisal bite force was vertically and anteriorly directed both during static biting and during biting associated with simultaneous mandibular translation and rotation. Since the resultant muscle force could not have been equal and opposite to the mandibular bite force, the mandibular condyles must have been loaded. These data demonstrate that the mandible acts as a lever during incisal biting and that there is no consistent relationship between incisal bite force direction and object size. In some individuals the bite force direction was more vertical during biting on a large transducer (30 mm high), while in other subjects it was more vertical during biting on a small transducer (10 mm high).     

The effects of biting and pulling on the forces generated during feeding in the Komodo dragon (Varanus komodoensis)

In addition to biting, it has been speculated that the forces resulting from pulling on food items may also contribute to feeding success in carnivorous vertebrates. We present an in vivo analysis of both bite and pulling forces in Varanus komodoensis, the Komodo dragon, to determine how they contribute to feeding behavior. Observations of cranial modeling and behavior suggest that V. komodoensis feeds using bite force supplemented by pulling in the caudal/ventrocaudal direction. We tested these observations using force gauges/transducers to measure biting and pulling forces. Maximum bite force correlates with both body mass and total body length, likely due to increased muscle mass. Individuals showed consistent behaviors when biting, including the typical medial-caudal head rotation. Pull force correlates best with total body length, longer limbs and larger postcranial motions. None of these forces correlated well with head dimensions. When pulling, V. komodoensis use neck and limb movements that are associated with increased caudal and ventral oriented force. Measured bite force in Varanus komodoensis is similar to several previous estimations based on 3D models, but is low for its body mass relative to other vertebrates. Pull force, especially in the ventrocaudal direction, would allow individuals to hunt and deflesh with high success without the need of strong jaw adductors. In future studies, pull forces need to be considered for a complete understanding of vertebrate carnivore feeding dynamics.     

The human mandible: Lever,link, or both?

Hylander ('78) recently published important new data on bite force in humans, and showed that the human mandible cannot function purely as a link during incisal biting. He concluded instead that the mandible acts as a lever. Reexamination of Hylander's data suggests that the mandible cannot function purely as a lever either, and in fact it probably functions simultaneously as both lever and link during incisal biting.     

Functional morphology of bite mechanics in the great barracuda (Sphyraena barracuda)

The great barracuda, Sphyraena barracuda, is a voracious marine predator that captures fish with a swift ram feeding strike. While aspects of its ram feeding kinematics have been examined, an unexamined aspect of their feeding strategy is the bite mechanism used to process prey. Barracuda can attack fish larger than the gape of their jaws, and in order to swallow large prey, can sever their prey into pieces with powerful jaws replete with sharp cutting teeth. Our study examines the functional morphology and biomechanics of 'ram-biting' behavior in great barracuda where the posterior portions of the oral jaws are used to slice through prey. Using fresh fish and preserved museum specimens, we examined the jaw mechanism of an ontogenetic series of barracuda ranging from 20 g to 8.2 kg. Jaw functional morphology was described from dissections of fresh specimens and bite mechanics were determined from jaw morphometrics using the software MandibLever (v3.2). High-speed video of barracuda biting (1500 framess(-1)) revealed that prey are impacted at the corner of the mouth during capture in an orthogonal position where rapid repeated bites and short lateral headshakes result in cutting the prey in two. Predicted dynamic force output of the lower jaw nearly doubles from the tip to the corner of the mouth reaching as high as 58 N in large individuals. A robust palatine bone embedded with large dagger-like teeth opposes the mandible at the rear of the jaws providing for a scissor-like bite capable of shearing through the flesh and bone of its prey.     

Molar occlusion and jaw mechanics of the Eocene primate Adapis

Wear facets on molars of the Eocene primate Adapis magnus are described. Striations on these wear facets indicate three separate directions of mandibular movement during mastication. One direction corresponds to a first stage of mastication involving orthal retraction of the mandible. The remaining two directions correspond to buccal and lingual phases of a second stage of mastication involving a transverse movement of the mandible. The mechanics of jaw adduction are analysed for both the orthal retraction and transverse stages of mastication. During the orthal retraction stage the greatest component of bite force is provided by the temporalis muscles acting directly against the food with the mandible functioning as a link rather than as a lever. A geometrical argument suggests that during the transverse stage of mastication bite force is provided by the temporalis muscles of both sides, the ipsilateral medial and lateral pterygoid muscles, and the contralateral masseter muscle.