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Upper jaw protrusion is a prominent component of the feeding mechanism in most elasmobranchs and has received considerable attention over the years. In this paper, we review what is known of muscle activity during prey capture in elasmobranchs, particularly that of upper jaw protrusion, and evaluate the extent to which functional modifications have evolved through changes in anatomy or patterns of muscle activity. To date, motor activity during feeding has been documented in only four species of elasmobranchs, although they represent the three major elasmobranch groups: Galea (typical sharks); Squalea (dogfish sharks); and Batoidea (skates and rays). Our efforts show that while muscles involved in cranial elevation and lower jaw depression and elevation show a conserved pattern of motor activity and function across species, other muscles show a more variable history. Our observations of elasmobranch upper jaw protrusion mechanisms suggest a mosaic of character changes over the course of evolution that involve anatomical changes in all cases and modifications of muscle activation patterns in some cases. During the evolution of feeding mechanisms of elasmobranchs, there have been two structural changes incorporating a pre-existing motor pattern to yield an unmodified kinematic profile, the original preorbitalis and the descendent preorbitalis. One additional instance of structural modification is accompanied by an alteration in the motor pattern leading to a change in movement pattern, the levator palatoquadrati.
Suction feeding is recognized as the dominant mode of aquatic prey capture in fishes. While much work has been done identifying motor pattern variations of this behavior among diverse groups of actinopterygian fishes, many ray-finned groups are still not represented. Further, the substantial amount of inherent variation in electromyography makes much of the pioneering work of suction feeding motor patterns in several basal groups insufficient for evolutionary comparisons. Robust evolutionary comparisons have identified conserved qualitative traits in the order of muscle activation during suction feeding (jaw opening > buccal cavity expansion > jaw closing). However, quantitative traits of suction motor patterns (i.e., burst durations and relative onset times) have changed over evolutionary time among actinopterygian fishes. Finally, new motor pattern evidence is presented from a previously neglected group, the Elopomorpha. The results suggest that future investigations of the muscles influencing lateral expansion of the mouth cavity and head anatomy may provide valuable new insights into the evolution of suction feeding motor patterns in ray-finned fishes. In addition, the evidence illustrates the value of comprehensive EMG surveys of cranial muscle activities during suction feeding behavior.
Many fishes use a powerful bite of the oral jaws to capture or tear their prey. This behavior has received less study from functional morphologists and physiologists than suction feeding, and presents an opportunity to examine motor control of fish feeding across alternative prey-capture strategies. We used electromyography to compare muscle activity patterns of the feeding bite in five teleost fishes representing at least three lineages in which biting has been independently acquired: two parrotfish (Cetoscarus bicolor and Scarus iseri), a wrasse (Cheilinus chlorourus), and two serrasalmines, a pacu (Piaractus brachypomus) and a piranha (Pygocentrus nattereri). Multivariate analysis indicated that muscle activity patterns differed significantly among species, although a four-way ANOVA designed to test for differences within a phylogenetic hierarchy revealed that the biting motor pattern was largely similar for both narrow and broad phylogenetic comparisons. A comparison of the motor patterns of biting and suction feeding species revealed that biters had significantly shorter durations of the epaxialis and sternohyoideus and significantly longer relative onset times of the epaxialis, adductor mandibulae, and sternohyoideus. Character mapping of timing variables suggested that short relative onset times are primitive for suction feeders and that this characteristic is generally retained in more advanced species. Despite these differences, all species overlap extensively in multivariate EMG space. Our results demonstrate that change in the feeding motor pattern has accompanied morphological and behavioral change in transitions from suction to biting, which suggests that the neuromotor system has not acted as a constraint on the evolution of the feeding system in fishes.
Based on studies of a few model taxa, amphibians have been considered stereotyped in their feeding movements relative to other vertebrates. However, recent studies on a wide variety of amphibian species have revealed great diversity in feeding mechanics and kinematics, and illustrate that stereotypy is the exception rather than the rule in amphibian feeding. Apparent stereotypy in some taxa may be an artifact of unnatural laboratory conditions. The common ancestor of lissamphibians was probably capable of some modulation of feeding movements, and descendants have evolved along two trajectories with regard to motor control: (1) an increase in modulation via feedback or feed-forward mechanisms, as exemplified by ballistic-tongued plethodontid salamanders and hydrostatic-tongued frogs, and (2) a decrease in variation dictated by biomechanics that require tight coordination between different body parts, such as the tongue and jaws in toads and other frogs with ballistic tongue projection. Multi-joint coordination of rapid movements may hamper accurate tongue placement in ballistic-tongued frogs as compared to both short-tongued frogs and ballistic tongued-salamanders that face simpler motor control tasks. Decoupling of tongue and jaw movements is associated with increased accuracy in both hydrostatic-tongued frogs and ballistic-tongued salamanders.
Aquatic feeding strikes on agile prey in snake-necked turtles involve fast neck extension, bucco-pharyngo-oesophageal expansion, and head retraction. The ultimate, rectilinear acceleration of the head towards the prey requires complex vertebral rotations, that vary widely from strike to strike. This poses complex motor control issues for the numerous intrinsic neck-muscles, which are the sole neck extensors. Mathematical modelling reveals that extensor activity might be superfluous for this phase of the strike. The ultimate acceleration of the head at the end of the strike always coincides with forceful oropharyngeal expansion. The momentum of the induced flow of water is sufficient to pull the head (and the neck) straight towards the prey. This buccal expansion proceeds identically to that observed in primary aquatic feeders: a rostro-caudal expansion sequence characterized by an optimal timing of the functional components supporting the expansion wave. Yet distinct structural solutions, both at the skeletal, and muscular level, are involved. This points towards prominent hydrodynamic constraints. Head and neck are retracted by extrinsic neck muscles. Given the high number of degrees of freedom, this musculo-skeletal system is obviously under-determined, which compromises control. We propose that erroneous folding of the neck (i.e., diverging from the highly persistent retracted configuration) might be avoided through the presence of a subtle click system at the level of the joint between cervical vertebrae 5 and 6.
Previous research indicated that the evolution of feeding motor patterns across major taxonomic groups might have occurred without large modifications of the control of the jaw and hyolingual muscles. However, the proposal of this evolutionary scheme was hampered by the lack of data for some key taxa such as lizards. Recent data on jaw and hyolingual feeding motor patterns of a number of lizard families suggest extensive variability within and among species. Although most lizards respond to changes in the structural properties of food items by modulating the activation of the jaw and hyolingual muscles, some food specialists might have lost this ability. Whereas the overall similarity in motor patterns across different lineages of lizards is large for the hyolingual muscles, jaw muscle activation patterns seem to be more flexible. Nevertheless, all data suggest that both the jaw and hyolingual system are complexly integrated. The elimination of feedback pathways from the hyolingual system through nerve transection experiments clearly shows that feeding cycles are largely shaped by feedback interactions. Yet, novel motor patterns including unilateral control seem to have emerged in the evolution from lizards to snakes.
Most snakes ingest and transport their prey via a jaw ratcheting mechanism in which the left and right upper jaw arches are advanced over the prey in an alternating, unilateral fashion. This unilateral jaw ratcheting mechanism differs greatly from the hyolingual and inertial transport mechanisms used by lizards, both of which are characterized by bilaterally synchronous jaw movements. Given the well-corroborated phylogenetic hypothesis that snakes are derived from lizards, this suggests that major changes occurred in both the morphology and motor control of the feeding apparatus during the early evolution of snakes. However, most previous studies of the evolution of unilateral feeding mechanisms in snakes have focused almost exclusively on the morphology of the jaw apparatus because there have been very few direct observations of feeding behavior in basal snakes. In this paper I describe the prey transport mechanisms used by representatives of two families of basal snakes, Leptotyphlopidae and Typhlopidae. In Leptotyphlopidae, a mandibular raking mechanism is used, in which bilaterally synchronous flexions of the lower jaw serve to ratchet prey into and through the mouth. In Typhlopidae, a maxillary raking mechanism is used, in which asynchronous ratcheting movements of the highly mobile upper jaws are used to drag prey through the oral cavity. These findings suggest that the unilateral feeding mechanisms that characterize the majority of living snakes were not present primitively in Serpentes, but arose subsequently to the basal divergence between Scolecophidia and Alethinophidia.
Both the anatomy and function of the mammalian masticatory system have attracted substantial interest. This review will discuss the general mammalian feeding patterns. An overview will be given of the evolutionary development and ontogeny of these patterns, the influence of occlusal forces, and recent developments in computer modeling. In mammals, basic symmetrical food transport cycles have been described for lapping and soft food ingestion. To increase chewing efficiency, a unilateral occlusal motion has been evolved replacing the slow closing phase in the basic cycle. The relative uniformity of the mammalian jaw-closer motor patterns during this chewing behavior, as characterized by electromyography (EMG), is striking. Nevertheless, several adaptations, clearly different from the primitive mammalian asymmetric masticatory motor pattern, can be distinguished. In contrast to the relative uniformity in motor patterns, the anatomical diversity of jaw systems is impressive and probably reflects the adaptation to diet. Detailed studies on the influence of occlusal force have been performed in the last decade. Data suggest that the masticatory cycles are largely shaped by sensory feedback. Also, the suckling food intake preceding mastication has been a point of interest. The suckling motor pattern resembles that of mastication, suggesting that the transition could be gradual during postnatal development. Recently, dynamic computer 3D-modeling has emerged as an analytical tool. The approach has the potential to help explain how structure and function interact.
The avian neck is a complex, kinematically redundant system, which plays a role during inter alia food prehension and manipulation. Kinematical analysis shows that chickens (Gallus domesticus) move their vertebrae according to a geometric principle that maximizes angular rotation efficiency. The movement pattern shows simultaneous rotations in some joints, while not in the others. Anseriformes show a pattern of successive, rather than simultaneous rotations in the rostral part of the neck. A kinematical model indicates that the geometric principle produces an anseriform-like pattern only if a constraint on the movement of the caudal vertebrae is introduced. The strength of this constraint, required for a realistic simulation, is related to the amount of stretch in the long dorsal neck muscles (M. biventer and M. longus colli dorsalis), which have a different configuration in Anseriformes compared to the chicken. To investigate whether the difference in movement pattern is a result of differences in anatomy only, or also of differences in neuromotor patterns, the EMG-patterns of the neck muscles of the mallard and chicken during drinking and pecking were studied. Considerable overlap in the activity of antagonists is found in mallards, but not in chickens. Muscles in the rostral part of the neck are activated successively in mallards, but simultaneously in chickens. We conclude that the difference in movement patterning between chickens and Anseriformes, results from both a difference in the control system of the neck, and a difference in the anatomy. The anseriform pattern is found in water as well as on land, which suggests that neck movement in both environments is controlled by the same neuromotor patterns. The modifications in motor control system and anatomy of the Anseriformes may have evolved as an adaptation to aquatic feeding, since the anseriform pattern is energetically more beneficial in an aquatic environment than on land.
During feeding in anurans, the mouth opens while the tongue, which is attached to the mandible at the front of the mouth, rotates forward. Due to the relative simplicity of its anatomy and the complexity of its motion, tongue protraction in frogs presents an ideal system for exploring the neural control of multijoint movements. In this study, we used a forward dynamic, rigid body model with four segments and two muscles to investigate open loop control of tongue protraction in the Australian white-lipped tree frog, Litoria caerulea. Model parameters include the mass distribution, initial position and initial angular velocity of each segment and the anatomy and physiology of each muscle. Model variables include the level of muscle activation at each time step and impulsive torques to open and close the mouth. The model gives X,Y coordinates of each segment and joint angles at each time step as output. The model was tested using scaled, normalized EMG signals and impulsive joint torques to predict the paths of the lower jaw tip and tongue tip. Predicted paths were compared to experimentally observed paths using Pearson product-moment correlation coefficients. Simulations demonstrate that the genioglossus muscles likely play a minor role, if any, in determining the trajectory of the tongue in most anurans. Most of the force for tongue protraction comes from angular momentum transferred to the tongue by the opening jaws. In anurans, tongue protraction is dynamically stable and will occur as long as the musculoskeletal elements are in the correct initial position.