The Mechanism of Tongue Projection in Chameleons: I. Electromyographic Tests of Functional Hypotheses

1992 ◽  
Vol 168 (1) ◽  
pp. 1-21 ◽  
Author(s):  
PETER C. WAINWRIGHT ◽  
ALBERT F. BENNETT

In this paper we document the activity of key muscles of the tongue, hyobranchial apparatus and head during prey capture in the lizard Chamaeleo jacksonii Boulenger and use these data to test current hypotheses of chameleon tongue function. Electromyographic recordings were made during 27 feedings from nine individuals and synchronized with high-speed video recordings (200 fields s−1), permitting an assessment of the activity of muscles relative to the onset of tongue projection, contact between tongue and prey, and tongue retraction. Four major results were obtained. (1) The hyoglossi muscles exhibit a single burst of activity that begins between 10 ms before and 20 ms after the onset of tongue projection and continues throughout the period of tongue retraction. (2) The accelerator muscle exhibits a biphasic activity pattern, with the first burst lasting about 185 ms and ending an average of 10.6 ms prior to the onset of projection. (3) The accelerator muscle shows regional variation in morphology that corresponds with variation in motor pattern. The anterior region of the muscle, unlike the posterior portion, exhibits only a single burst of activity that begins 2.5 ms after the onset of tongue projection and is thus not involved in launching the tongue. (4) The geniohyoidei, sternohyoidei, sternothyroidei, depressor mandibulae, adductor mandibulae and pterygoideus all exhibit activity patterns consistent with previously reported kinematic patterns and their proposed roles. The major implications of these results for models of the chameleon feeding mechanism are (1) that the hyoglossi do not act to hold the tongue on the entoglossal process during a loading period prior to tongue projection, and (2) that the presence of 185 ms of intense activity in the accelerator muscle prior to tongue projection suggests the presence of a preloading mechanism, the nature of which is the subject of the companion paper.

2002 ◽  
Vol 205 (17) ◽  
pp. 2591-2603 ◽  
Author(s):  
Eric D. Tytell ◽  
George V. Lauder

SUMMARYThe fast-start escape response is the primary reflexive escape mechanism in a wide phylogenetic range of fishes. To add detail to previously reported novel muscle activity patterns during the escape response of the bichir, Polypterus, we analyzed escape kinematics and muscle activity patterns in Polypterus senegalus using high-speed video and electromyography (EMG). Five fish were filmed at 250 Hz while synchronously recording white muscle activity at five sites on both sides of the body simultaneously (10 sites in total). Body wave speed and center of mass velocity, acceleration and curvature were calculated from digitized outlines. Six EMG variables per channel were also measured to characterize the motor pattern. P. senegalus shows a wide range of activity patterns, from very strong responses, in which the head often touched the tail, to very weak responses. This variation in strength is significantly correlated with the stimulus and is mechanically driven by changes in stage 1 muscle activity duration. Besides these changes in duration, the stage 1 muscle activity is unusual because it has strong bilateral activity, although the observed contralateral activity is significantly weaker and shorter in duration than ipsilateral activity. Bilateral activity may stiffen the body, but it does so by a constant amount over the variation we observed; therefore, P. senegalus does not modulate fast-start wave speed by changing body stiffness. Escape responses almost always have stage 2 contralateral muscle activity, often only in the anterior third of the body. The magnitude of the stage 2 activity is the primary predictor of final escape velocity.


2002 ◽  
Vol 205 (22) ◽  
pp. 3445-3457 ◽  
Author(s):  
Christopher P. J. Sanford ◽  
Peter C. Wainwright

SUMMARYSuction feeding in fishes is the result of a highly coordinated explosive expansion of the buccal cavity that results in a rapid drop in pressure. Prey are drawn into the mouth by a flow of water that is generated by this expansion. At a gross level it is clear that the expansion of the buccal cavity is responsible for the drop in pressure. However, attempts using high-speed video recordings to demonstrate a tight link between prey capture kinematics and suction pressure have met with limited success. In a study with largemouth bass Micropterus salmoides, we adopted a new technique for studying kinematics, sonomicrometry, to transduce the movement of skeletal elements of the head during feeding, and synchronized pressure recordings at a sampling rate of 500 Hz. From the positional relationships of six piezoelectric crystals we monitored the internal movements of the buccal cavity and mouth in both mid-sagittal and transverse planes. We found that peak subambient pressure was reached very early in the kinematic expansion of the buccal cavity, occurring at the time when the rate of percentage change in buccal volume was at its peak. Using multiple regression analyses we were consistently able to account for over 90%, and in the best model 99%, of the variation in buccal pressure among strikes using kinematic variables. Sonomicrometry shows great promise as a method for documenting movements of biological structures that are not clearly visible in the external view provided by film and video recordings.


1993 ◽  
Vol 180 (1) ◽  
pp. 209-227 ◽  
Author(s):  
P. C. Wainwright ◽  
R. G. Turingan

Teleost fishes typically capture prey with the oral jaws and perform most types of prey- processing behavior with the pharyngeal jaw apparatus. In these fishes, the motor patterns associated with the different stages of feeding are quite distinct, and fish can modify muscle activity patterns when feeding on different prey. We examined motor pattern variation in the queen triggerfish, Balistes vetula, a versatile predator that both captures and processes prey with its oral jaws. During feeding on three prey that differed in hardness and elusiveness, three distinct patterns of behavior could be identified on the basis of patterns of muscle activity: prey capture, buccal manipulation and blowing. During prey capture by suction feeding, the retractor arcus palatini muscle (RAP) commenced activity before the levator operculi muscle (LOP). In both buccal manipulation and blowing, the RAP began activity well after the onset of activity in the LOP. Both prey capture and buccal manipulation motor patterns varied when fish fed on different prey. When capturing hard-shelled and non-elusive prey, B. vetula did not employ suction feeding but, instead, the fish directly bit parts of its prey. The motor pattern exhibited during direct biting to capture prey was different from that during suction feeding, but was indistinguishable from the pattern seen during the repeated cycles of buccal manipulation. Harder prey elicited significantly longer bursts of activity in the jaw adductor muscles than did soft prey. In spite of the involvement of the oral jaws in virtually all stages of feeding, B. vetula shows levels of variation between patterns of behavior and types of prey characteristic of previously studied teleost fishes. Thus, the coupling of capture and processing behavior patterns in the repertoire of the oral jaws does not appear to constrain the behavioral versatility of this species.


2000 ◽  
Vol 203 (21) ◽  
pp. 3255-3263 ◽  
Author(s):  
A. Herrel ◽  
J.J. Meyers ◽  
P. Aerts ◽  
K.C. Nishikawa

Iguanian lizards generally use their tongue to capture prey. Because lingual prehension is based on surface phenomena (wet adhesion, interlocking), the maximal prey size that can be captured is small. However, published records show that prey items eaten by chameleons include small vertebrates such as lizards and birds, indicating that these lizards are using a different prey prehension mechanism. Using high-speed video recordings, cineradiography, electromyography, nerve transection and stimulation experiments, we investigated the function of the tongue during prey capture. The results of these experiments indicate that chameleons have modified the primitive iguanian system by including a suction component in their prehension mechanism. Suction is generated by the activity of two modified intrinsic tongue muscles that pull the tongue pad inwards. Moreover, we demonstrate that the mechanism described here is a prerequisite for successful feeding.


1980 ◽  
Vol 84 (1) ◽  
pp. 17-32
Author(s):  
G. V. LAUDER ◽  
S. M. NORTON

Prey capture in the spotted gar, Lepisosteus oculatus, was studied by high-speed cinematography synchronized with electromyographic recordings of cranial muscle activity. Muscle activity patterns were recorded during each of the three major phases of feeding: the initial strike at the prey, manipulation of the prey following capture, and swallowing. With one exception, the obliquus superioris, all muscles at the strike are active in a bilaterally symmetrical pattern. During the manipulation phase two distinct muscle activity patterns occur: one is characterized by symmetrical activity in the epaxial muscles and obliquus inferioris, the other by complete asymmetry between the right and left sternohyoideus, obliquus superioris, and epaxial muscles. Low-amplitude manipulatory movements are characterized by activity in one side of the sternohyoideus only, all other muscles being generally inactive. The adductor mandibulae and obliquus inferioris are always active symmetrically. Asymmetrical activity in the sternohyoideus, epaxial muscles, and obliquus superioris correlates with lateral head movements during feeding and acts to rotate prey into the preferred orientation for swallowing. The pattern of asymmetrical activity between right and left side muscles is discussed in relation to previous studies of feeding which utilized only unilateral muscle recordings.


Biology Open ◽  
2021 ◽  
Vol 10 (3) ◽  
Author(s):  
Ismene Fertschai ◽  
Wade C. Sherbrooke ◽  
Matthias Ott ◽  
Boris P. Chagnaud

ABSTRACT Horned lizards (Phrynosoma) are specialized predators, including many species that primarily feed on seed harvester ants (Pogonomyrmex). Harvester ants have strong mandibles to husk seeds or defensively bite, and a venomous sting. Texas horned lizards possess a blood plasma factor that neutralizes harvester ant venom and produce copious mucus in the pharynx and esophagus, thus embedding and incapacitating swallowed ants. We used high-speed video recordings to investigate complexities of their lingual prey capture and handling behavior. Lizards primarily strike ants at their mesosoma (thorax plus propodeum of abdomen). They avoid the head and gaster, even if closer to the lizard, and if prey directional movement is reversed. Orientation of captured ants during retraction is with head first (rostral), thus providing initial mucus coating of the mandibles. Prey capture accuracy and precise handling illustrates the specificity of adaptations of horned lizards in avoiding harm, and the challenges lizards face when feeding on dangerous prey.


1996 ◽  
Vol 199 (8) ◽  
pp. 1727-1742 ◽  
Author(s):  
A Herrel ◽  
J Cleuren ◽  
F Vree

The kinematics of prey capture, intraoral transport and swallowing in lizards of the species Agama stellio (Agamidae) were investigated using cineradiography (50 frames s-1) and high-speed video recordings (500 frames s-1). Small metal markers were inserted into different parts of the upper and lower jaw and the tongue. Video and cineradiographic images were digitized, and displacements of the body, head, upper and lower jaw and the tongue were quantified. Twenty additional variables depicting displacements and timing of events were calculated. A factor analysis performed on the kinematic data separates prey capture and swallowing cycles from intraoral transport bites. However, the intraoral transport stage cannot be separated into chewing (reduction) and transport bites. The effect of prey type and size on the feeding kinematics of intraoral transport and swallowing cycles was investigated. During the intraoral transport stage, distinct aspects (e.g. durations, maximal excursions) of the gape and tongue cycle are modulated in response to both the size and type of the prey item. The results for A. stellio generally agree with a previous model, although it is the entire slow opening phase rather than solely the duration of the second part of this phase that is affected by the size of the prey. The intraoral transport cycles in A. stellio show the two synapomorphic characteristics of tetrapods (tongue-based terrestrial intraoral prey transport and the existence of a long preparatory period of prey compression). However, not all five characters of the feeding cycle previously proposed for amniotes are present in A. stellio. One major difference is that in A. stellio the recovery of the hyolingual apparatus does not take place during the slow opening phase but during the slow closing/powerstroke phase.


Materials ◽  
2021 ◽  
Vol 14 (3) ◽  
pp. 559
Author(s):  
Lakshminath Kundanati ◽  
Prashant Das ◽  
Nicola M. Pugno

Aquatic predatory insects, like the nymphs of a dragonfly, use rapid movements to catch their prey and it presents challenges in terms of movements due to drag forces. Dragonfly nymphs are known to be voracious predators with structures and movements that are yet to be fully understood. Thus, we examine two main mouthparts of the dragonfly nymph (Libellulidae: Insecta: Odonata) that are used in prey capturing and cutting the prey. To observe and analyze the preying mechanism under water, we used high-speed photography and, electron microscopy. The morphological details suggest that the prey-capturing labium is a complex grasping mechanism with additional sensory organs that serve some functionality. The time taken for the protraction and retraction of labium during prey capture was estimated to be 187 ± 54 ms, suggesting that these nymphs have a rapid prey mechanism. The Young’s modulus and hardness of the mandibles were estimated to be 9.1 ± 1.9 GPa and 0.85 ± 0.13 GPa, respectively. Such mechanical properties of the mandibles make them hard tools that can cut into the exoskeleton of the prey and also resistant to wear. Thus, studying such mechanisms with their sensory capabilities provides a unique opportunity to design and develop bioinspired underwater deployable mechanisms.


1991 ◽  
Vol 159 (1) ◽  
pp. 109-133 ◽  
Author(s):  
PETER C. WAINWRIGHT ◽  
DAVID M. KRAKLAU ◽  
ALBERT F. BENNETT

The kinematics of prey capture by the chamaeleonid lizard Chamaeleo oustaleti were studied using high-speed cinematography. Three feeding sequences from each of two individuals were analyzed for strike distances of 20 and 35 cm, at 30°C. Ten distances and angles were measured from sequential frames beginning approximately 0.5 s prior to tongue projection and continuing for about 1.0 s. Sixteen additional variables, documenting maximum excursions and the timing of events, were calculated from the kinematic profiles. Quantified descriptions of head, hyoid and tongue movements are presented. Previously unrecognized rapid protraction of the hyobranchial skeleton simultaneously with the onset of tongue projection was documented and it is proposed that this assists the accelerator muscle in powering tongue projection. Acceleration of the tongue occurred in about 20ms, reaching a maximum acceleration of 486 m s−2 and maximum velocity of 5.8m s−1 in 35 cm strikes. Deceleration of the tongue usually began within 5 ms before prey contract and the direction of tongue movement was reversed within 10 ms of prey contact. Retraction of the tongue, caused by shortening of the retractor muscles, reached a maximum velocity of 2.99 ms−1 and was complete 330 ms after prey contact. Projection distance influences many aspects of prey capture kinematics, particularly projection time, tongue retraction time and the extent of gape and head movements during tongue retraction, all of which are smaller in shorter feedings. Though several features of the chameleon strike have apparently been retained from lizards not capable of ballistic tongue projection, key differences are documented. Unlike members of a related family, the Agamidae, C. oustaleti uses no body lunge during prey capture, exhibits gape reduction during tongue projection and strongly depresses the head and jaws during tongue retraction. Note: Present address: Department of Biological Sciences, Florida State University, Tallahassee, FL 32306, USA.


1992 ◽  
Vol 70 (10) ◽  
pp. 1886-1896 ◽  
Author(s):  
Véronique Goosse ◽  
Vincent L. Bels

High-speed cinematography (100 frames/s) was used to allow quantitative analysis of the kinematic profiles of tongue and jaw displacements during chemosensory activities in the scleroglossan lizard Lacerta viridis. The types of tongue flicking were simple downward extensions (SDE), single oscillations (SOC), and submultiple oscillations (SMOC) of the tongue out of the mouth. The SMOC type involves a downward or upward movement of the tongue performed before a typical oscillation and it is therefore suggested that this is an intermediate category of flick between the typical SOC and MOC of lizards. Closing and opening of the mouth in SDE, SOC, and SMOC cycles may or may not be separated by a stationary stage during which the jaws are held open at a constant gape. The duration of this stationary interval increases from SDE to SMOC. Gape cycles do not show any division into slow and fast stages. The gape is produced largely by depression of the lower jaw; the upper jaw is slightly elevated by protrusion of the tongue. Patterns of correlation of kinematic variables depicting jaw and tongue movements differed between SDE, SOC, and SMOC. A principal component analysis shows that the three flick types overlap in a multivariate space constructed from the kinematic variables depicting jaw and tongue displacements. Overlap between SOC and SMOC categories is greater than that between SOC, SMOC, and SDE categories. The kinematic patterns of tongue displacement during SMOC in Lacerta viridis show similarities with those of MOC in other lizards and in snakes. Kinematically, the pattern of jaw and tongue displacements of Lacerta viridis during chemosensory activities shows similarities with those that occur during drinking and prey capture.


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