Morphology and histochemistry of the hyolingual apparatus in chameleons.

We reexamined the morphological and functional properties of the hyoid, the tongue pad, and hyolingual musculature in chameleons. Dissections and histological sections indicated the presence of five distinctly individualized pairs of intrinsic tongue muscles. An analysis of the histochemical properties of the system revealed only two fiber types in the hyolingual muscles: fast glycolytic and fast oxidative glycolytic fibers. In accordance with this observation, motor-endplate staining showed that all endplates are of the en-plaque type. All muscles show relatively short fibers and large numbers of motor endplates, indicating a large potential for fine muscular control. The connective tissue sheet surrounding the entoglossal process contains elastin fibers at its periphery, allowing for elastic recoil of the hyolingual system after prey capture. The connective tissue sheets surrounding the m. accelerator and m. hyoglossus were examined under polarized light. The collagen fibers in the accelerator epimysium are configured in a crossed helical array that will facilitate limited muscle elongation. The microstructure of the tongue pad as revealed by SEM showed decreased adhesive properties, indicating a change in the prey prehension mechanics in chameleons compared to agamid or iguanid lizards. These findings provide the basis for further experimental analysis of the hyolingual system.

Cranial kinesis in geckoes: functional implications.

Although it is generally assumed that cranial kinesis is a plesiomorphic characteristic in squamates, experimental data tend to contradict this hypothesis. In particular, coupled kinesis (i.e. streptostyly and mesokinesis) presumably arose independently in only a limited number of highly specialised groups. In this study, we investigated cranial kinesis in one of the most specialised of these groups: geckoes. On the basis of cineradiographic and electromyographic data, the fast opening and the slow closing/power stroke phases were modelled to elucidate possible functions of the observed kinesis. The results of these analyses show that the retraction of the muzzle unit during crushing is a self-reinforcing system that increases bite force and reduces the joint forces; the active protraction of the kinetic system during jaw opening, in contrast, enhances opening speed through the coupling of the intracranial units. It can be argued that cranial kinesis in geckoes is probably not an adaptive trait as such but, instead, a consequence of the 'Bauplan' of the cranial system in these animals. Presumably as a result of constructional constraints on the size of the jaw musculature and eyes, the supratemporal and postorbital bars were lost, which resulted in enormous mobility in the skull. To counteract the potential negative factors associated with this (decrease in bite force, skull damage), the kinetic system may have become coupled, and thus functional.

Cranial kinesis in gekkonid lizards

Cranial kinesis was studied in two species of gekkonid lizard, Gekko gecko and Phelsuma madagascariensis, using cineradiography and electromyography. The skull of these geckoes showed the three types of kinesis described by Versluys at the beginning of this century: streptostyly, mesokinesis and metakinesis. In accordance with the later model of Frazzetta, the skull of these animals can be modelled by a quadratic crank system: when the mouth opens during feeding, the quadrate rotates forward, the palato-maxillary unit is lifted and the occipital unit swings forward. During jaw closing, the inverse movements are observed; during crushing, the system is retracted beyond its resting position. The data gathered here indicate that the coupled kinesis (streptostyly + mesokinesis) is most prominently present during the capture and crushing cycles of feeding and is largely absent during late intraoral transport, swallowing, drinking and breathing. The electromyographic data indicate a consistent pattern of muscular activation, with the jaw opener and pterygoid protractor always active during the fast opening phase, and the jaw closers active during closing and crushing. Our data generally support the model of Frazzetta. Although the data gathered here do not allow speculation on the functional significance of the kinesis, they clearly provide some key elements required for a further investigation of the functional and adaptive basis of the system.

Morphology of the feeding system in agamid lizards: ecological correlates.

The interaction of organismal design with ecology, and its evolutionary development are the subject of many functional and ecomorphological studies. Many studies have shown that the morphology and mechanics of the masticatory apparatus in mammals are adapted to diet. To investigate the relations between diet and the morphological and physiological properties of the lizard jaw system, a detailed analysis of the structure of the jaw apparatus was undertaken in the insectivorous lizard Plocederma stellio and in closely related herbivorous lizards of the genus Uromastix. The morphological and physiological properties of the jaw system in P. stellio and U. aegyptius were studied by means of dissections, light microscopy, histochemical characterisations, and in vivo stimulation experiments. The skull of Uromastix seems to be built for forceful biting (high, short snout). Additionally, the pterygoid muscle is modified in P. stellio, resulting in an additional force component during static biting. Stimulation experiments indicate that jaw muscles in both species are fast, which is supported by histochemical stainings. However, the oxidative capacity of the jaw muscles is larger in Uromastix. Contraction characteristics and performance of the feeding system (force output) are clearly thermally dependent. We conclude that several characteristics of the jaw system (presence of extra portion of the pterygoid muscle, large oxidative capacity of jaw muscles) in Uromastix may be attributed to its herbivorous diet. Jaw muscles, however, are still faster than expected. This is presumably the result of trade-offs between the thermal characteristics of the jaw adductors and the herbivorous lifestyle of these animals.

Tongue flicking in agamid lizards: morphology, kinematics, and muscle activity patterns.

We wanted to examine whether a relation between foraging strategy, morphology, the mechanics of tongue protrusion, and prey chemical detection and discrimination exists in agamid lizards. Tongue-flick behavior was observed in two species of this family: Uromastix acanthinurus and Plocederma stellio. Potential prey chemical discrimination by means of tongue flicking was examined by using applicator tests. Tongue flicks were subsequently recorded by high-speed video in combination with the electrical activity of a number of jaw and hyolingual muscles. The kinematics of jaws and tongue and the muscle activity patterns were quantified. To investigate if the observed differences in tongue-flick behavior (mainly in the frequency of use) are translated into corresponding differences in tongue morphology, the tongues of both species were examined by light and scanning electron microscopy. The species differed mainly in the surface morphology of the foretongue and in the abundance and distribution of taste buds on the tongue and oral cavity. These differences can be related to behavioural observations; whereas U. acanthinurus readily uses tongue flicks to detect and discriminate between food items, P. stellio does not. However, differences in tongue-flick mechanics (kinematics, electromyograms) between both species were minor. Based on the data gathered in this study and from previously published data, an evolutionary transformation series leading to the complex tongue-flick cycles as observed in snakes is proposed. The required morphological and mechanical changes that accompany such an evolutionary sequence are discussed.

Quantitative electromyography of the masticatory muscles of Pteropus giganteus (Megachiroptera).

Mastication has been studied by cinematography and quantitative electromyography while flying foxes, Pteropus giganteus, were freely feeding on standardized pieces of apple, soaked raisin, and banana. The primarily orthal mandibular movements are caused by mainly bilaterally symmetrical firing of all the masticatory muscles. Asymmetric activity in the superficial and deep masseter and medial pterygoid causes slight protrusion early in opening. Slight lateral deviations at the end of opening and at the start of closing are caused by asymmetric and asynchronous activity in the pterygoids and digastrics, and by asynchronous firing of the deep temporalis and zygomaticomandibularis. Food consistency affects movement characteristics as well as characteristics of muscular activity. In this study electromyograms were digitized and the number of spikes and mean amplitude per interval (set by the filming rate) recorded. Although a significant correlation exists between descriptors, the product thereof appears to be the best predictor of certain kinematic variables (cycle length and maximum excursion of the mandible). On the other hand, the changes in magnitude of muscular activity as a function of the position of a cycle in the reduction sequence and as a function of food consistency are more translated in a variation of the mean amplitude than in a variation of the number of spikes per interval. Observed variation differs among muscles studied. It is most apparent in the superficial and deep masseter and least in the temporalis and zygomaticomandibularis. Late cycles of apple and raisin mastication are long and exhibit large gapes but almost no anterior movement. The adductor activity frequently shows a synchronized, pulsatile pattern leading to an unfused tetanus.

Functional bases of fiber length and angulation in muscle.

The differences in angulation and length observed for the fibers of anatomical muscles may reflect two distinct mechanical requirements: arrangement for pinnation, reflecting an increase in physiological cross-section and arrangement for equivalent placement of sarcomeres, possibly associated with coordination. The observed differences in fiber angulation and length have different effects upon the responses of sarcomeres, specifically on their extent and rate of shortening and on the force they may generate. The basic mechanisms governing these effects and the various arrangements of muscles are reviewed. Fiber length and angulation in the complex M. adductor mandibulae externus 2 of a lizard were measured stereotactically; these values correlate well with the hypothesis that the muscle shows equivalence and demonstrate that angulation for pinnation is less constant. An outline for the study of muscle architecture and function, detailing the kinds of information require to estimate forces and evaluate muscle and fiber placements, is presented.

Usage pattern of the complex masticatory muscles in the shingleback lizard, Trachydosaurus rugosus: A model for muscle placement.

This wide-ranging, omnivorous lizard of Australia has a very complex adductor muscle mass, with fibers differing in length by a factor of three and in insertion angle by 90 degrees. Stimulated muscles produce maximal moment with the mouth nearly fully open. The opening mechanism appears to involve only simple rotation and no translation of the mandible. EMGs indicate that the entire mass is activated equivalently in crushing and there are no temporal subdivisions, for instance, matching activity to angle of opening. During crushing of hard objects, the chin is brought into contact with the ground so that the subvertebral muscles may aid buccal closure. The lizards also activate the muscles in a pulsatile staircase effect leading to an unfused tetanus that generates forces several times the twitch level. Application in parallel of a maximum number of sarcomeres to the crushing bite appears to be the major design characteristic. Hence, this species offers an ideal case for analysis of the effects of different sarcomere placements on the simple movement generated. For the primary adductor muscles, the angles of fiber insertion relative to the lines connecting each insertion with the jaw joint are equivalent; this relation persists as the mouth opens. Also, fiber lenghts are proportional to the distance between jaw joint and site of insertion so that each sarcomere contributes equally to the movement generated. Complex tendons provide additional space for muscle placement. Some of these also extend beyond the bony attachment sites, producing tendinous "coronoid processes." The fibers of laterally and ventrally placed muscles are short relative to the length of the entire muscle, insert at relatively short moment arms, and undergo short excursion during opening; however, there are many such fibers. Also, muscles with a low incident angle are crossed; they apparently protect the jaw joint from horizontal (disarticulating) forces.

Movements of the mandibles and tongue during mastication and swallowing in Pteropus giganteus (megachiroptera): a cineradiographical study.

Quantitative lateral and dorsoventral cineradiography shows that the masticatory movements of the mandible, condyles, tongue, and hyoid of Pteropus giganteus (Chiroptera) move along highly regular paths that are characteristic for each of the three food types tested. Mandibular movements are predominantly orthal, although a small forward translation occurs early in opening and small lateral deflections occur in both opening and closing phases. These deflections are related to the existence of active (bolus bearing) and balancing sides of the jaws, chewing being not truly bilateral. The deflections are associated with a shift of both condyles toward one side. In consequence the active condyle is located in a lateral part of the associated fossa, the inactive condyle in a medial part. Food transfer from side to side involves a reversal of the chewing direction during opening. Such reversals are especially frequent near the end of a chewing sequence. The fore, middle, and hind parts of the tongue differ in their movement patterns. Movements of the fore part, and to a lesser extent of the middle part, follow the open-close movements of the lower jaw. The hind part of the tongue moves predominantly dorsally during slow closing and ventrally during fast opening and fast closing. All three parts move forward during slow closing and slow opening, and backward during fast opening and fast closing. Movements of the hyoid are closely synchronized with those of the hind part of the tongue. Furthermore, tongue and hyoid movements are synchronized with jaw movements. All cycles of Pteropus giganteus are transport cycles, and the synchrony appears to reflect the consistency of the food (soft pulp, juices). Food consistency also accounts for the high swallowing rate and the absence of any significant difference between nonswallowing and swallowing cycles.