Modulation of prey capture kinematics and the role of lingual sensory feedback in the lizard Pogona vitticeps.

Most organisms feed on a variety of prey that may differ dramatically in their physical and behavioural characteristics (e.g. mobility, mass, texture, etc.). Thus the ability to modulate prey capture behaviour in accordance with the characteristics of the food appears crucial. In animals that use rapid tongue movements to capture prey (frogs and chameleons), the coordination of jaws and tongue is based on visual cues gathered prior to the prey capture event. However, most iguanian lizards have much slower tongue-based prey capture systems suggesting that sensory feedback from the tongue may play an important role in coordinating jaw and tongue movements. We investigated the modulation of prey capture kinematics in the agamid lizard Pogona vitticeps when feeding on a range of food items differing in their physical characteristics. As the lizard is a dietary generalist, we expected it to be able to modulate its prey capture kinematics as a function of the (mechanical) demands imposed by the prey. Additionally, we investigated the role of lingual sensory feedback by transecting the trigeminal sensory afferents. Our findings demonstrated that P. vitticeps modulates its prey capture kinematics according to specific prey properties (e.g. size). In addition, transection of the trigeminal sensory nerves had a strong effect on prey capture kinematics. However, significant prey type effects and prey type by transection effects suggest that other sources of sensory information are also used to modulate the prey capture kinematics in P. vitticeps.

Built to bite: feeding kinematics, bite forces, and head shape of a specialized durophagous lizard, Dracaena guianensis (teiidae).

Most lizards feed on a variety of food items that may differ dramatically in their physical and behavioral characteristics. Several lizard families are known to feed upon hard-shelled prey (durophagy). Yet, specializations toward true molluscivory have been documented for only a few species. As snails are hard and brittle food items, it has been suggested that a specialized cranial morphology, high bite forces, and an adapted feeding strategy are important for such lizards. Here we compare head and skull morphology, bite forces, and feeding kinematics of a snail-crushing teiid lizard (Dracaena guianensis) with those in a closely related omnivorous species (Tupinambis merianae). Our data show that juvenile D. guianensis differ from T. merianae in having bigger heads and greater bite forces. Adults, however, do not differ in bite force. A comparison of feeding kinematics in adult Dracaena and Tupinambis revealed that Dracaena typically use more transport cycles, yet are more agile in manipulating snails. During transport, the tongue plays an important role in manipulating and expelling shell fragments before swallowing. Although Dracaena is slow, these animals are very effective in crushing and processing hard-shelled prey.

Jaw and hyolingual movements during prey transport in varanid lizards: effects of prey type.

The ability to modulate feeding kinematics in response to prey items with different functional properties is likely a prerequisite for most organisms that feed on a variety of food items. Variation in prey properties is expected to reveal variation in feeding function and the functional role of the different phases in a transport cycle. Here we describe the kinematics of prey transport of two varanid species, Varanus niloticus and Varanus ornatus. These species were selected for analysis because of their highly specialised hyolingual system and food transport mechanism (inertial food transport). In these animals, tongue and hyoid movements are expected to make no, or only a minor, contribution to prey transport. We observed statistically significant prey type effects that could be associated with prey properties such as mass, size and mobility. These data show that both species are capable of modulating the kinematics of food transport in response to different prey types. Moreover, not only the kinematics of the jaws were modulated in response to prey characteristics but also the anterior/posterior movements of the tongue and hyoid. This suggests a more important role of the tongue and hyolingual movements in these animals than previously suspected. In contrast, head movements were rather stereotyped and were not modulated in response to changes in prey type.

Are morphological specializations of the hyolingual system in chameleons and salamanders tuned to demands on performance?

Extremely specialized and long tongues used for prey capture have evolved independently in plethodontid salamanders and chameleons. In both systems, the demands on tongue projection are probably similar: to maximize projection velocity and distance. Consequently, many of the design features of the projection system in these two groups have converged to an astonishing degree. Both involve the use of power amplification systems based on helically wound muscle fibers that load internal connective tissue sheets as illustrated in previous studies. Demands imposed on tongue retraction, however, are different to some degree. Although in both groups there is a clear demand for retraction capacity (given the long projection distances), in chameleons there is an added demand for force because they eat large and heavy prey. As indicated by our data, plethodontid salamanders have extremely long tongue retractors with normal striated muscle. Chameleons, on the other hand, evolved long retractors of the supercontracting type. Interestingly, our data show that at least in chameleons, the extreme design of the tongue in function of prey capture appears to have consequences on prey transport, resulting in an increased dependence on the hyoid. In turn, this has lead to an increase in transport-cycle duration and an increase in the number of cycles needed to transport prey in comparison with closely related agamid lizards. Clearly, extreme morphological specializations are tuned to functional and ecological demands and may induce a reduced performance in other functions performed by the same set of integrated structures.

Inertial feeding in the teiid lizard Tupinambis merianae: the effect of prey size on the movements of hyolingual apparatus and the cranio-cervical system.

In most terrestrial tetrapods, the transport of prey through the oral cavity is accomplished by movements of the hyolingual apparatus. Morphological specializations of the tongue in some lizard taxa are thought to be associated with the evolution of vomerolfaction as the main prey detection mode. Moreover, specializations of the tongue are hypothesized to compromise the efficiency of the tongue during transport; thus, driving the evolution of inertial transport. Here we use a large teiid lizard, Tupinambis merianae, as a model system to test the mechanical link between prey size and the use of inertial feeding. We hypothesize that an increase in prey size will lead to the increased recruitment of the cranio-cervical system for prey transport and a reduced involvement of the tongue and the hyolingual apparatus. Discriminant analyses of the kinematics of the cranio-cervical, jaw and hyolingual systems show that the transport of large prey is indeed associated with a greater utilization of the cranio-cervical system (i.e. neck and head positioning). The tongue retains a kinematic pattern characteristic of lingual transport in other lizards but only when processing small prey. Our data provide evidence for an integration of the hyolingual and cranio-cervical systems; thus, providing partial support for an evolutionary scenario whereby the specialization of the tongue for chemoreception has resulted in the evolution of inertial transport strategies.

Modulation, individual variation and the role of lingual sensory afferents in the control of prey transport in the lizard Pogona vitticeps.

Most organisms feed on a variety of food items that may differ dramatically in their physical and behavioural characteristics (e.g. mobility, mass, texture, etc.). Thus the ability to modulate prey transport behaviour in accordance with the characteristics of the food appears crucial. Consequently, prey reduction and transport movements must be adjusted to the natural variation in material properties of the food, between and within feeding sequences and transport cycles. Here we describe an investigation of (1) the ability of the agamid lizard Pogona vitticeps to modulate prey transport kinematics when feeding on a range of food items differing in their physical characteristics and (2) the role of sensory feedback in controlling jaw and tongue movements by bilateral transection of the lingual trigeminal sensory afferents. Our findings demonstrate that P. vitticeps modulates the kinematics of its feeding behaviour in response to the mechanical demands imposed by different food types. In addition, transection of the trigeminal sensory afferents has an effect on the movements of jaws and tongue during transport, and increases the duration of transport cycles needed to process a given food type. However, after transection, transport cycles were still different for different food types suggesting that other sources of sensory information are also used to modulate prey transport in the lizard P. vitticeps.

The functional significance of the lower temporal bar in Sphenodon punctatus.

One of the major conundrums in the evolution of vertebrate cranial design is the early loss and frequent redevelopment of the lower temporal bar in diapsids. Whereas it has been proposed that the reduction of the lower temporal bar allows for an increase in jaw adductor mass and bite force, this has never been tested experimentally. As the sole recent representative of the Rhynchocephalia, Sphenodon punctatus is different from other extant lepidosaurians in having a fully diapsid skull and in using translation to shear food rather than using the typical puncture-crushing of other lizards. In the present study, we show that S. punctatus has lower bite forces compared with extant lepidosaurians. Moreover, dissection of the jaw muscles of an adult S. punctatus shows that the mass of the external jaw adductor muscle is significantly smaller than that of lizards, probably accounting for the lower measured bite forces. An analysis of the transport cycles suggests a less efficient prey transport in S. punctatus compared with an agamid lizard of similar size in terms of handling time and number of cycles needed to crush similar prey. Modelling of biting in S. punctatus suggests a different role of the jaw adductor muscles during biting and a clear functional role for the lower temporal bar. Future finite element models may provide better insights into the function of the lower temporal bar in S. punctatus.

Electromyography and the evolution of motor control: limitations and insights.

Electromyography (EMG), or the study of muscle activation patterns, has long been used to infer central nervous system (CNS) control of the musculoskeletal system and the evolution of that control. As the activation of the muscles at the level of the periphery is a reflection of the interaction of descending influences and local reflex control, EMG is an important tool in integrated investigations of the evolution of coordination in complex, musculoskeletal systems. Yet, the use of EMG as a tool to understand the evolution of motor control has its limitations. We here review the potential limitations and opportunities of the use of EMG in studying the evolution of motor control in vertebrates and provide original previously unpublished data to illustrate this. The relative timing of activation of a set of muscles can be used to evaluate CNS coordination of the components in a musculoskeletal system. Studies of relative timing reveal task-dependent variability in the recruitment of different populations of muscle fibers (i.e., different fiber types) within a single muscle, and left-right asymmetries in activation that need to be taken into account in comparative studies. The magnitude of muscle recruitment is strongly influenced by the instantaneous demands imposed on the system, and is likely determined by local reflex-control systems. Consequently, using EMG to make meaningful inferences about evolutionary changes in musculoskeletal control requires comparisons across similar functional tasks. Moreover, our data show that inferences about the evolution of motor control are limited in their explanatory power without proper insights into the kinematics and dynamics of a system.

The evolution of cranial design and performance in squamates: Consequences of skull-bone reduction on feeding behavior.

The evolution of cranial design in lepidosaurians is characterized by a general trend toward the loss of cranial elements. The evolution of relatively lighter skulls in squamates appears tightly coupled to a reduction in relative mass of the jaw adductor, implying functional consequences for bite force and feeding behavior. Interestingly, among squamates the postorbital bar was reduced or lost at least twice independently and taxa characterized by the loss of these cranial elements (e.g., geckos and varanids) are generally reported as having a mobile skull. In Gekkotans, the loss of the postorbital bar was accompanied by a reduction of the supratemporal bar, resulting in a pronounced cranial kinesis. Our data show that having a kinetic skull has functional consequences and results in a reduction in bite force. The lower bite force may in turn be responsible for the decreased feeding efficiency as reflected in the longer duration of intra-oral transport cycles. Gekkotans, however, appear to exploit their intracranial mobility in ways that increases the velocity of jaw movement during opening and closing, which may allow them to capture more elusive prey. The morphological changes observed in the evolution of the cranial system in squamates appear tightly linked to functional and constructional demands on the skull, making squamate skull evolution a model system to investigate the consequences of morphological changes in a complex integrated system of performance, behavior, and ecology.

Modulation of intra-oral processing in mammals and lepidosaurs.

The mammalian masticatory apparatus is distinguished from the intra-oral processing systems of other amniotes by a number of morphological and functional features, including transverse movements of the teeth during the power stroke, precise occlusion, suspension of the teeth in the socket by a periodontal ligament, diphyodonty (reduction to two generations of teeth), a hard palate, and the presence of a single bone (the dentary) in the lower jaw which articulates with the skull at the temporomandibular jaw joint. The evolution of these features is commonly argued to have improved the efficiency of food processing in the oral cavity. The present aricle highlights the existence in mammals of the fusimotor system and afferent fibers from the periodontal ligament through which the CNS modulates the responses by the muscle spindles. Published data suggest that the fusimotor system and the periodontal afferents are important components in feed-forward (or anticipatory) control of chewing behavior. We hypothesize that this feed-forward control is used to maintain relatively constant cycle lengths in mammals in the face of intra-sequence and inter-sequence variation in material properties of the food, and that this enables them to maintain a higher average chewing frequency than that of lizards. These predictions were evaluated using data on mean cycle length and its variance from the literature and from our own files. On average, mammals have less variable cycle lengths than do lizards and shorter cycle lengths than do lizards of similar size. We hypothesize that by decreasing variance in cycle length, presumably close to the natural frequency of their feeding systems, mammals minimize energy expenditure during chewing, allowing them to chew for longer, thereby maintaining the high rates of food intake required for their high metabolic rates.