Mammalian Mastication Research Articles

Symphyseal morphology and jaw muscle recruitment levels during mastication in musteloid carnivorans.

In studies of mammalian mastication, a possible relationship has been proposed between bilateral recruitment of jaw adductor muscle force during unilateral chewing and the degree of fusion of the mandibular symphysis. Specifically, species that have unfused, mobile mandibular symphyses tend to utilize lower levels of jaw adductor force on the balancing (nonchewing) than the working (chewing) side of the head, when compared to related species with fused symphyses. Here, we compare jaw adductor recruitment levels in two species of musteloid carnivoran: the carnivorous ferret (unfused symphysis), and the frugivorous kinkajou (fused symphysis). During forceful chewing, we observe that ferrets recruit far more working-side muscle force than kinkajous, regardless of food toughness and that high working-to-balancing side ratios are the result of increased working-side force, often coupled with reduced balancing-side force. We propose that in carnivorans, high working-to-balancing side force ratios coupled with an unfused mandibular symphysis are necessary to rotate the hemimandible for precise unilateral occlusion of the carnassial teeth and to sustain laterally oriented force on the jaw to engage the carnassial teeth during shearing of tough foods. In contrast, the kinkajou's flattened cheekteeth permit less precise occlusion and require medially-oriented forces for grinding, thus, a fused symphysis is mechanically beneficial.

Characterizing tongue deformations during mastication using changes in planar components of three-dimensional angles.

Understanding of tongue deformations during mammalian mastication is limited, but has benefited from recent developments in multiplanar imaging technology. Here, we demonstrate how a standardized radiopaque marker implant configuration and biplanar fluoroscopy can quantify three-dimensional shape changes during chewing in pigs. Transverse and sagittal components of the three-dimensional angle between markers enable characterizing deformations in anatomically relevant directions. The transverse component illustrates bending to the left or to the right, which can occur symmetrically or asymmetrically, the latter sometimes indicating regional widening. The sagittal component reflects 'arching' or convex deformations in the dorsoventral dimension symmetrically or asymmetrically, the latter characteristic of twisting. Trends are detected in both the transverse and sagittal planes, and combinations thereof, to modify tongue shape in complex deformations. Both the transverse and sagittal components were also measured at key jaw and tongue positions, demonstrating variability particularly with respect to maximum and minimum gape. This highlights the fact that unlike tongue position, tongue deformations are more independent of jaw position, likely in response to the ever-changing bolus shape and position. From a methodological perspective, our study showcases advantages of a repeatable three-marker implant configuration suitable for animals of different sizes and highlights considerations for different implant patterns. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Osteological correlates of evolutionary transitions in cetacean feeding and related oropharyngeal functions

Teeth are often the first structures that anatomists and paleontologists examine to understand the ecology and morphology of feeding, both because teeth are highly specialized structures that provide precise information, and because they are among the best and most commonly preserved fossils. Unfortunately, many fragmentary fossil and recent specimens lack teeth, and some come from edentulous individuals and taxa, as in mysticete (baleen) whales. In our broad comparative review, we survey non-dental osteological features that, due to size, shape, arrangement, and surface features reflecting muscle attachments, provide useful clues to general or specific aspects of prey capture, intraoral transport, processing, or swallowing. We focus on hyoid, palatal, and pterygoid bones, mandibular symphyses and processes such as the coronoid, and the temporal fossa and zygomatic arch, as well as adjacent cranial bones relating to oral and pharyngeal anatomy. These bones relate to muscles of five general locations especially indicative of feeding: mandibular, hyoid, tongue, pharyngeal, and facial regions. Together these bones and muscles affect feeding and related activities including suckling and breathing. We discuss osteological correlates that provide special relevance to key transitions in cetacean evolutionary history, such as the shift from predominantly terrestrial to aquatic feeding, the shift from typical mammalian mastication to swallowing prey entirely or nearly whole, and the separation of respiratory and digestive passages. We also point to examples of modern specialists in these anatomical optima for different modes of prey capture, intraoral transport, processing, and swallowing. Although we focus on cetaceans, our approach is broadly relevant to all vertebrates, notably other marine tetrapods.

The cost of chewing: The energetics and evolutionary significance of mastication in humans.

Any change in the energetic cost of mammalian mastication will affect the net energy gain from foods. Although the energetic efficiency of masticatory effort is fundamental in understanding the evolution of the human masticatory system, nothing is known currently about the associated metabolic costs of chewing different items. Here, using respirometry and electromyography of the masseter muscle, we demonstrate that chewing by human subjects represents a measurable energy sink. Chewing a tasteless odorless gum elevates metabolic rate by 10 to 15% above basal levels. Energy expenditure increases with gum stiffness and is paid for by greater muscle recruitment. For modern humans, it is likely that mastication represents a small part of the daily energy budget. However, for our ancestors, before the onset of cooking and sophisticated food processing methods, the costs must have been relatively high, adding a previously unexplored energetic dimension to the interpretation of hominin dentofacial fossils.

Shearing overbite and asymmetrical jaw motions facilitate food breakdown in a freshwater stingray, Potamotrygon motoro.

Many species of fish process their prey with cyclic jaw motions that grossly resemble those seen in mammalian mastication, despite starkly different tooth and jaw morphologies. The degree of similarity between the processing behaviors of these disparate taxa has implications for our understanding of convergence in vertebrate feeding systems. Here, we used XROMM (X-ray reconstruction of moving morphology) to investigate prey processing behavior of Potamotrygon motoro, the ocellate river stingray, which has recently been found to employ asymmetrical, shearing jaw motions to break down its prey. We found that P. motoro modulates its feeding kinematics to produce two distinct types of chew cycles: compressive cycles and overbite cycles. The latter are characterized by over-rotation of the upper jaw relative to the lower jaw, past the expected occlusal limit, and higher levels of bilateral asymmetry as compared with compressive chews. We did not find evidence of the mediolateral shearing motions typical of mammalian mastication, but overbite cycles appear to shear the prey item between the upper and lower toothplates in a propalinal fashion. Additionally, comparison of hyomandibular and jaw motions demonstrates that the angular cartilages decouple jaw displacement from hyomandibular displacement in rostrocaudal and mediolateral directions. The multiple similarities between mammalian mastication and the dynamic processing behavior of P. motoro support the use of sub-family Potamotrygoninae as a model for studying evolutionary convergence of mastication-like processing.

Evaluating the triplet hypothesis during rhythmic mastication in primates.

Mammalian mastication involves precise jaw movements including transverse movement of the mandible during the power stroke. Jaw elevation and transverse movement are driven by asymmetrical jaw elevator muscle activity, which is thought to include a phylogenetically primitive and conserved triplet motor pattern consisting of: triplet I (balancing side: superficial masseter and medial pterygoid; working side: posterior temporalis), which reaches onset, peak and offset first; and triplet II (working side: superficial masseter and medial pterygoid; balancing side: posterior temporalis), which is active second. Although the presence of a triplet motor pattern has been confirmed in several primate species, the prevalence of this motor pattern - i.e. the proportion of masticatory cycles that display it - has not been evaluated in primates. The present study quantifies the presence and prevalence of the triplet motor pattern in five different primate species, Eulemur fulvus, Propithecus verreauxi, Papio anubis, Macacafuscata and Pan troglodytes, using mean onset, peak and offset time relative to working superficial masseter. In all five of the species studied, the mean triplet motor pattern was observed at peak muscle activation, and in four out of the five species the triplet motor pattern occurred more frequently than expected at random at peak muscle activation and offset. Non-triplet motor patterns were observed in varying proportions at different time points in the masticatory cycle, suggesting that the presence or absence of the triplet motor pattern is not a binomial trait. Instead, the primate masticatory motor pattern is malleable within individual cycles, within individual animals and therefore within species.

Jaw movement in fossil mammals: analysis, description and visualization

A terminology for and visualizations of different mammalian mastication paths are provided, resulting from orientation of attritional and abrasional facets and striation on fossil (and extant) teeth. The occlusal motion of the left lower jaw is considered, and a moderate wear stage (IDAS 3) is used as standard. In contrast to conventional terminologies, the proposed nomenclature differentiates between the inclination and the direction of the lower jaw movement as projected onto a horizontal plane for each phase of the power stroke. The proposed mastication compass attempts to combine three aspects of the power stroke: (1) the number of phases, (2) the occlusal direction, and (3) the inclination of each phase. Descriptions and visualizations are given for several taxa in order to demonstrate its general applicability. The proposed new terminology and the mastication compass simplify comparisons of different modes of mastication in different mammalian taxa.

Mandibular corpus bone strains during mastication in goats (Capra hircus): A comparison of ingestive and rumination chewing

ObjectiveTo compare the mechanical loading environment of the jaw in goats during ingestive and rumination chewing. DesignRosette strain gauges were attached to the external surface of the mandibular corpus in five goats to record bone strains during the mastication of hay and rumination. ResultsStrain magnitudes and maximum physiological strain rates during the mastication of hay are significantly higher than during rumination chewing on the working and balancing sides. Principal strain ratios and orientations are similar between the two chewing behaviours. Loading and chewing cycle duration are all longer during rumination chewing, whereas chew duty factor and variances in load and chewing cycle durations are higher during ingestive chewing. For most of the variables, differences in strain magnitudes or durations are similar at all three gauge sites, suggesting that rumination and ingestive chewing do not differentially influence bone at the three gauge sites. ConclusionsDespite lower strain magnitudes, the repetitive nature of rumination chewing makes it an important component of the mechanical loading environment of the selenodont artiodactyl jaw. However, similarities in principal strain orientations and ratios indicate that rumination chewing need not be considered as a unique loading behaviour influencing the biomechanics of the selenodont artiodactyl jaw. Differences in loading and chewing cycle durations during rumination and ingestion demonstrate flexibility in adult chewing frequencies. Finally, although the low within-sequence variability in chewing cycle durations supports the hypothesis that mammalian mastication is energetically efficient, chewing during rumination may not be more efficient than during ingestion.

Rhythmic chewing with oral jaws in teleost fishes: a comparison with amniotes

Intra-oral prey processing (chewing) using the mandibular jaws occurs more extensively among teleost fishes than previously documented. The lack of muscle spindles, gamma-motoneurons and periodontal afferents in fishes makes them useful for testing hypotheses regarding the relationship between these sensorimotor components and rhythmic chewing in vertebrates. Electromyography (EMG) data from the adductor mandibulae (AM) were used to quantify variation in chew cycle duration in the bowfin Amia, three osteoglossomorphs (bony-tongues), four salmonids and one esocid (pike). All species chewed prey using their oral jaw in repetitive trains of between 3 and 30 consecutive chews, a pattern that resembles cyclic chewing in amniote vertebrates. Variance in rhythmicity was compared within and between lineages using coefficients of variation and Levene's test for homogeneity of variance. These comparisons revealed that some teleosts exhibit degrees of rhythmicity that are comparable to mammalian mastication and higher than in lepidosaurs. Moreover, chew cycle durations in fishes, as in mammals, scale positively with mandible length. Chewing among basal teleosts may be rhythmic because it is stereotyped and inflexible, the result of patterned interactions between sensory feedback and a central pattern generator, because the lack of a fleshy tongue renders jaw-tongue coordination unnecessary and/or because stereotyped opening and closing movements are important for controlling fluid flow in the oral cavity.

Modulation of mandibular loading and bite force in mammals during mastication

Modulation of force during mammalian mastication provides insight into force modulation in rhythmic, cyclic behaviors. This study uses in vivo bone strain data from the mandibular corpus to test two hypotheses regarding bite force modulation during rhythmic mastication in mammals: (1) that bite force is modulated by varying the duration of force production, or (2) that bite force is modulated by varying the rate at which force is produced. The data sample consists of rosette strain data from 40 experiments on 11 species of mammals, including six primate genera and four nonprimate species: goats, pigs, horses and alpacas. Bivariate correlation and multiple regression methods are used to assess relationships between maximum (epsilon(1)) and minimum (epsilon(2)) principal strain magnitudes and the following variables: loading time and mean loading rate from 5% of peak to peak strain, unloading time and mean unloading rate from peak to 5% of peak strain, chew cycle duration, and chew duty factor. Bivariate correlations reveal that in the majority of experiments strain magnitudes are significantly (P<0.001) correlated with strain loading and unloading rates and not with strain loading and unloading times. In those cases when strain magnitudes are also correlated with loading times, strain magnitudes are more highly correlated with loading rate than loading time. Multiple regression analyses reveal that variation in strain magnitude is best explained by variation in loading rate. Loading time and related temporal variables (such as overall chew cycle time and chew duty factor) do not explain significant amounts of additional variance. Few and only weak correlations were found between strain magnitude and chew cycle time and chew duty factor. These data suggest that bite force modulation during rhythmic mastication in mammals is mainly achieved by modulating the rate at which force is generated within a chew cycle, and less so by varying temporal parameters. Rate modulation rather than time modulation may allow rhythmic mastication to proceed at a relatively constant frequency, simplifying motor control computation.

Generation of the Central Masticatory Pattern and Its Modification by Sensory Feedback

Mammalian mastication results from the interaction of an intrinsic rhythmical neural pattern and sensory feedback generated by the interaction of the effecter system (muscles, bones, joints, teeth, soft tissues) with food. The main variables that explain variation in the pattern of human mastication are the subjects themselves, their age, the type of food being eaten, and time during a sequence of movements. The intrinsic pattern of mastication is generated by a central pattern generator (CPG) located in the pons and medulla. The output of the CPG is modified by inputs that descend from higher centers of the brain and by feedback from sensory receptors. Intraoral touch receptors, muscle spindles in the jaw-closing muscles, and specialized mechanoreceptors in the periodontal ligament have especially powerful effects on movement parameters.

Mammalian feeding and primate evolution: An overview

Most of the papers included in this volume are derived from presentations in a symposium on Mammalian Feeding at the 65th Annual Meetings of the American Association of Physical Anthropologists in North Carolina in 1996. The aims of this symposium were to gather together the preeminent researchers on mammalian mastication and document the state of research in that field. The symposium emphasized in vivo studies of mammalian feeding because of a paucity of recent reviews of this field, but included morphometric and modeling papers as well. Subsequently the papers were revised, and were submitted in spring 1998 for publication, pending the outcome of peer review. Copyright 2000 Wiley-Liss, Inc.

Biomechanics of Mammalian Feeding and Primate Evolution. Proceedings of a symposium. Research Triangle Park, North Carolina, USA. April 9-13, 1996.

ABSTRACT Most of the papers included in this volume are derived frompresentations in a symposium on Mammalian Feeding at the 65th AnnualMeetings of the American Association of Physical Anthropologists in NorthCarolina in 1996. The aims of this symposium were to gather together thepreeminent researchers on mammalian mastication and document the stateof research in that field. The symposium emphasized in vivo studies ofmammalian feeding because of a paucity of recent reviews of this field, butincluded morphometric and modeling papers as well. Subsequently the pa-pers were revised, and were submitted in spring 1998 for publication, pend-ing the outcome of peer review. Am J Phys Anthropol 112:449–453, 2000. © 2000 Wiley-Liss, Inc. The study of feeding behavior in nonpri-mate mammals is relevant to the study ofprimate mastication in two ways. First,comparison of primates and nonprimatemammals can reveal ways in which pri-mates differ from other mammals, inform-ing hypotheses of the origin and radiation ofprimates. Second, study of a broad range ofmammals generates insights into the rulesand principles governing the evolution ofthe feeding apparatus in general, of whichthe primate system is an example.Many of the papers in this symposiumdealt with issues surrounding anthropoidorigins. The fossil record of the anthropoidstem group has greatly improved recentlywith the discovery of Early-Middle EoceneAsian taxa exhibiting a combination of pro-simian-like primitive and crown anthro-poid-like derived features of the jaws andteeth (Beard et al., 1996; Jaeger et al.,1999). Future work on these animals prom-ises to greatly enhance our understandingof the origins of the anthropoid feeding ap-paratus. Extant anthropoids that have beenstudied differ from strepsirrhine primatesin an array of features of the skull that aredemonstrably or have been hypothesized tobe part of the feeding apparatus, e.g., onto-genetically early fusion of the mandibularsymphysis, late activity in the balancing-side deep masseter muscle during the powerof mastication (Hylander et al., 1987; Hy-lander and Johnson, 1994), relatively greateractivity of balancing-side muscles (Hylander1977), greater isognathy (widths of upper andlower dental arcades are roughly similar; Ra-vosa and Hylander, 1994), relatively largerphase II occlusal facets, a longer power stroke(Hiiema¨e and Kay, 1973), and a postorbitalseptum (Cachel, 1979). Ravosa et al. (2000a,this volume) observe that crown anthropoidshave more isodontic molars (upper andlower molars roughly the same width) andmore vertically oriented superficial masse-ters than do strepsirrhines.Ross and Hylander (2000, this volume)evaluate hypotheses relating the function ofthe anterior temporalis muscles to the evo-lution of the postorbital septum (Ross,

An optimization model for mastication and swallowing in mammals.

Mammalian mastication is a process combining simultaneous food comminution and lubrication. The initiation of swallowing, which is voluntary, has been thought to depend on separate thresholds for food particle size and for particle lubrication. Instead of this duality, we suggest that swallowing is initiated when it is sensed that a batch of food particles is binding together under viscous forces so as to form a bolus. Bolus formation ensures that when the food mass is swallowed, it will pass the pharyngeal region safely without risk of inhaling small particles into the lower respiratory tract. Crucial for bolus formation is food particle size reduction by mastication. This allows the tongue to pack particles together tightly by pressure against the hard palate. A major function of salivation is to fill the gradually reducing spaces between particles, so increasing viscous cohesion and promoting bolus formation. If swallowing is delayed, excessive saliva floods the bolus, separating particles and reducing cohesion. Swallowing then becomes more precarious. Our model suggests that there is an optimum moment for a mammal to swallow, defined in terms of a peak cohesive force between food particles. The model is tested on human mastication with two foods, brazil nut and raw carrot, which have very different particle size breakdown rates. The peak cohesive force is much greater with brazil nuts but both foods are predicted to be swallowed after similar numbers of chews despite the very different food particle size reductions achieved at that stage. The predicted number of chews to swallow is in broad agreement with published data.

Morphology and behavior of the feeding apparatus in Cryptobranchus alleganiensis (Amphibia: Caudata).

Cine and high-speed videographic analyses of feeding in Cryptobranchus alleganiensis demonstrate that prey are captured by either inertial suction or a strike combined with suction. Movements of cephalic elements during capture are generally similar to those of other suction-feeding vertebrates but more variable than those of most aquatic salamanders. Following capture, prey frequently are manipulated and transported into and out of the buccal cavity across the teeth. Specific features of the skull, mandibles, hyoid apparatus, and cephalic musculature of Cryptobranchus correlate directly with behavior. Although the skull is massive, sutures of the anterior braincase permit limited torsion, the maxillae move on their attachments to the braincase, and left and right mandibles are separated by elastic connective tissues. These features provide flexibility and permit asynchronous and asymmetric movements of the mandibles. Equivalent asymmetry and asynchrony of hyobranchial movements are also correlated with specific structural arrangements that may be neither paedomorphic nor primitive. Its feeding mechanics suggest that Cryptobranchus represents a unique and highly derived condition among salamanders. Its ability to modulate movements of the left and right sides of its head argues strongly for the existence of bilaterally asynchronous motor patterns, and patterns of force generation, similar to but much faster than those employed in mammalian mastication. © 1994 Wiley-Liss, Inc.

Functional Morphology of Mammalian Mastication

SYNOPSIS. While chewing is not unique to mammals, it is one of their most distinctive characteristics. Historically, studies of food processing in mammals were intended to provide evolutionary insights, but more progress has been made in understanding mechanistic aspects. Mastication is considered under five headings. (1) Interaction of teeth with food .Knowledge of comparative dental anatomy and function is advanced in comparison to understanding of foods and how they are broken down. (2) Chewing force and its resistance by the skull . The traditional assumption that occlusal force is maximized is not always justified, and experimental results suggest that skull loading is far more dynamic and variable than had been envisioned from theoretical analyses. (3) How the jaw moves . The most important masticatory movement is that of the power stroke, and in most but not all species this is influenced more by the inclined planes of the teeth and jaw joints than by the musculature. (4) The role of muscles in producing both force and movement . The most fundamental distinction among jaw muscles is whether they have a rostral or caudal direction of pull, as this determines their role in transverse jaw movements. Reliance on anatomical names tends to obscure functional similarities and differences among species. (5) Intraoral structures . Because they are difficult to study, the actions of the tongue and pharynx are still debated. Even the fundamental question of whether mammals can breathe and swallow at the same time has not been definitively answered.

Asymmetric suction feeding in primitive salamanders

During suction feeding, the primitive aquatic salamandersCryptobranchus alleganiensis andAndrias japonicus frequently display asymmetric movements of the lower jaw and hyoid apparatus that have some similarity to working and blancing side kinematics of mammalian mastication.

Research in Mammalian Mastication

Ongoing research efforts in mammalian mastication have defined several broad areas of mutual interest to workers in the discipline. They are (1) interrelationships between masticatory movements, (2) actions of the masticatory muscles, (3) comparisons between masticatory structures and functions, (4) developmental aspects, (5) comparisons between limbs and jaws, and (6) neurophysiologic considerations. The roles (potential and actual) of masticatory central pattern generators, cerebral “mastication areas,” different neural mechanisms between mammalian taxa, neurophysiologic/morphologic interactions, and biochemical factors within the total milieu of mammalian mastication are discussed.

Analysis of mammalian masticatory mechanisms: progress and problems.

SummaryDirect measurement of bone movements and muscle activation in mammalian mastication is now possible. Early results indicate that the patterns are quite variable and depart from the stereotyped versions sometimes reported. Most mammals masticate unilaterally; only a few chew simultaneously on both sides. Orbital movements are complex and three‐dimensional. While most muscles are active during the reduction phase, it is difficult to define phases by sharp transitions of activity. The fascicles of pinnate muscles differ in fiber architecture and physiology; they tend to function at different times and with distinct mechanical advantages.Interspecific diversity and marked responses to food consistency and size, still preclude generalizations. Improved methods for comparisons among orbits, for correlation of forces and excursions, and automated correlations of movements, forces and electromyograms are beginning to be available and need to be more generallv applied to analysis.