Kinematics of Feeding Behaviour in Oplurus Cuvieri (Reptilia: Iguanidae)

In tetrapods, the tongue and the jaws play a major role in basic functions (e.g. feeding and drinking) and also in exploratory and display functions. The precision with which these structural features are related to function is still largely unresolved for these types of behaviour. As in a lot of amphibians (Lauder and Shaffer, 1985; Larsen et al. 1989), iguanian lizards (Agamidae, Chameleontidae and Iguanidae) use the tongue for food capture. Several studies have focused on different biomechanical aspects of feeding steps (e.g. capture, reduction and transport) in various species (Gnanamuthu, 1930; Throckmorton, 1976, 1980; Frazzetta, 1983; Smith, 1984, 1986; Gans et al. 1985; Bels and Baltus, 1987, 1989; Schwenk and Bell, 1988; Schwenk and Throckmorton, 1989; Bell, 1990; Bels, 1990; Bels and Goosse, 1990; Kraklau, 1991; Wainwright et al. 1991; So et al. 1992). Although these studies have provided valuable information on feeding behaviour, kinematic analysis of all the successive phases of feeding in one species is critical at two levels: (1) for phylogenetic comparison among lizards, and (2) for testing the generalities of the feeding cycles of tetrapods (Bramble and Wake, 1985) and the evolutionary features of feeding in Amniota proposed by Reilly and Lauder (1990).

For food capture in iguanians, the tongue is protruded (Iguanidae, Agamidae) or projected onto the prey (Chameleontidae) and then retracted for bringing the prey into the buccal cavity. In general, during the other phases, the tongue moves within the buccal cavity for reducing and transporting the food into the oesophagus. Recent studies have described in detail the kinematic properties of the remarkable tongue projection in prey capture of chameleons (Bels and Baltus, 1987; Bell, 1990; Wainwright et al. 1991). Tongue protrusion has also been analyzed in agamids, the sister group of chameleontids (Schwenk and Bell, 1988; Schwenk and Throckmorton, 1989; Kraklau, 1991). From behavioural and morphological comparisons between the tongue and its displacements during prey capture, Schwenk and Bell (1988) hypothesized that tongue projection in chameleontids may be derived from tongue protrusion in agamids. The kinematic properties of tongue protrusion in iguanid and agamid lizards seem to be rather similar (Schwenk and Throckmorton, 1989; Bels, 1990).

For transport, kinematic properties of the jaw cycles involved in food processing have been analyzed in some agamids and iguanids by using high-speed cinematography, while reduction has only been studied in one agamid (Agama agama) and two iguanids (Anolis equestris and Ctenosaura similis) (Smith, 1984; Bels and Baltus, 1989; Schwenk and Bell, 1988; Schwenk and Throckmorton, 1989; Kraklau, 1991). Only in chameleontids have kinematic profiles of the tongue and gape cycles been compared during all the feeding phases (Bels and Baltus, 1987; Wainright et al. 1991; So et al. 1992). Displacements of the tongue within the buccal cavity during the reduction and transport phases have been presented in detail for only one iguanid, C. similis (Smith, 1984), using high-speed cineradiography. Relative displacements of the tongue and hyoid elements have been illustrated only in C. similis (Smith, 1984) and A. equestris (Bels and Goosse, 1989).

The primary purpose of this study was to provide a quantitative analysis of the kinematic properties of all the phases of feeding behaviour in one iguanid, Oplurus cuvieri. High-speed cinematography and cineradiography were used to describe the cyclic displacements of the jaws, head and the tongue-hyoid complex during prey capture, reduction, transport and cleaning. We focused on three main questions: (1) what role does the tongue play in the successive feeding phases, (2) are the kinematics of the different phases of prey processing similar in iguanians, and (3) how do the tongue and jaw displacements for each cycle compare to the Bramble and Wake (1985) and Reilly and Lauder (1990) models?

For high-speed cinematography, four adult male Oplurus cuvieri (Gray) (117±23mm snout-vent length) were filmed at 100 and 200 frames s⁻¹ with Eastman Ektachrome high-speed 7250 tungsten 16mm film, using a Photosonic 1PL camera. The lizards were filmed under two 1000 W tungsten photoflood lights. Each lizard was isolated in a vivarium 2 or 3 weeks before filming. Vivaria measured 500 mm X 400 mm X 400 mm. An incandescent bulb and two True-Lite tubes provided the animal with temperatures of 20°C (night) or 28°C (day). The relative humidity was maintained near 60%. Points of paint or natural spots on the lizards were used for digitizing. Seven capture, 30 reduction, 27 transport and six cleaning cycles of 20 sequences were analysed.

For cineradiography, lead markers were placed into the tongue of two O. cuvieri. In one lizard, a marker was placed in the mid tongue and, in the second lizard, two markers were placed, respectively, into the mid and hind tongue. Based on observations of frames, the markers in the mid tongue of the two lizards were similarly positioned. Compared to the position of the markers used by Smith (1984), the anterior marker in O. cuvieri corresponds to the second tongue marker in C. similis (Fig. 5 in Smith, 1984). The posterior marker in O. cuvieri was placed more posteriorly into the hind tongue. We did not succeed in placing a marker in the fore tongue, but use of a zoom lens during high-speed cinematography allowed us to observe deformations of the entire tongue. The markers were used to analyse (1) the tongue displacements and (2) the relative displacement of the mid and hind tongue. For placing the markers, animals were gradually anaesthetized with Ethrane gas administered in a closed cage. The markers were put into the tongue using a hypodermic needle (Injecta 16, diameter 0.55 mm). Five reduction and 20 transport cycles of 10 feeding sequences were recorded. Capture cycles were unusable because of the slow shutter speed of the camera.

Animals were conditioned to feed on the cage bottom near a grid (10 mm x 10 mm for cinematography and 30 mm x 30 mm for cineradiography). In all the filming procedures, food consisted of live adult crickets (Acheta domesticus) all of a similar size (24±3mm). For cineradiography, a saturated solution of barium sulphate was introduced into the body of the insects.

All the sequences were projected onto a graphic table (AGMEE, ULg) using a NAC motion analyser and the data were digitized using a Copam AT microcomputer. Kinematic profiles were plotted for these sequences. Each sequence of frames was analysed by digitizing a combination of selected points on the head, the tongue and the prey. Fig. 1 shows the points used for plotting the graphs and calculating kinematic variables. The data were only plotted or computed for truly lateral sequences.

Displacements of the tongue were estimated by computing the position of its anteriormost tip when the tongue was visible between the jaws. During a capture cycle, the lizard moves towards the prey. The tongue displacements thus include the head displacements of the lizard. During reduction and transport cycles, the distance between the two tongue markers was calculated as the difference between the x-coordinates of these markers. Measuring the throat and hyoid displacements was not possible because there were several folds in the gular skin of the lizards and the hyoid apparatus was not marked.

Jaw displacements were calculated by computing displacements of the snout and the anteriormost tip of the mandible. Vertical displacements of the jaws were calculated relative to the displacements of the body (point N, Fig. 1) to avoid the effects produced by overall displacements of the lizard, y-coordinates of the point UJ illustrate the rotation of the neurocranium relative to the vertebral column, and y-coordinates of the point LJ correspond to the depression of the mandible. During reduction, the head is elevated. The increase in the y-coordinates of LJ and UJ are thus influenced by this elevation. The gape angle refers to the angle between the mandibular symphysis, the angulus oris and the tip of the snout, x- and y-coordinates of one point onto the thorax of the prey were used for analysing the relative displacements of the prey, the tongue and the jaws. In capture cycles, the linear distance between the mandible tip and the point onto the thorax of the insect was computed. In the other cycles, the prey was in the buccal cavity. Horizontal and vertical displacements of the prey in the graphs correspond to the horizontal and vertical distances between the point on the prey and the upper jaw tip.

Vertical (y) and horizontal (x) coordinates were recorded for successive frames for each digitized point. The data were stored in data files as tables of bipolar (x and y) coordinates. The files were then analysed using a set of computer programs developed by V. Bels and P. Theate for studying behaviour patterns in lizards. Frame 1 was arbitrarily chosen to occur at the commencement of the slow opening (SO) stage. The coordinates were plotted against time to provide the point displacements in the kinematic graphs. The digitized data were smoothed using a five-point equation (see Alexander, 1983, for details) for showing clearly the cyclic displacement of the kinematic variables. Both digitized and smooth curves are plotted on the kinematic graphs.

For analysing feeding profiles statistically, 20 variables were measured directly from plots of kinematic variables (digitized data) depicting tongue and jaw displacements over time: four stage maximal durations (slow opening SO I and II, fast opening FO, fast closing FC), maximal gape angle, time to maximal gape, four times to maximal amplitude and four maximal amplitudes (depression of the lower jaw, elevation of the upper jaw, x- and y-displacements of the tongue), total duration of the cycle, times to x and y maximal displacements and maximal displacements of the prey to (capture) and within (other cycles) the buccal cavity, and maximal head elevation. All of these measurements were obtained from time zero to the time of the maximal value for each variable.

The mean of all the variables was calculated for each phase. Time variables depicting the duration of gape stages, time to maximal gape and time to maximal depression of the lower jaw were calculated as a percentage of the total duration of the gape cycle.

Three analyses were performed on the set of variables to explore the similarities between capture, reduction, transport and cleaning phases. A correlation matrix was calculated to explore the relationships between the calculated variables in each phase. In order to explore the kinematic relationships between the capture, reduction, transport and cleaning phases, a principal component analysis was performed using eight variables (maximal gape angle, time to maximal gape angle, maximal depression of the lower jaw, time to maximal depression of the lower jaw, total duration of the cycle, and the duration of the SO, FO and FC stages). This analysis was coupled with a multivariate analysis of variance (ANOVA), run on the scores of the first two principal components, to test for differences among phases. All calculations were performed on untransformed data obtained from the kinematic plots of these variables. A two-way analysis of variance was performed on the kinematic variables of the reduction and transport cycles. This analysis was a mixed-model design that crossed the fixed behaviour effect (reduction and transport) with the random individual effect (four individuals). This analysis was not made on capture and cleaning behaviour because we obtained data for cleaning in one individual and for capturing in two individuals. We did not test inter-individual differences in the kinematic variables of these types of behaviour. However, as a first approach for testing the difference between the durations of the three successive stages between capture and transport cycles, we used a t-test with Bonferroni correction.

A typical feeding bout in O. cuvieri was divided into four phases: capture, reduction, transport and cleaning (sensuThrockmorton, 1980). The identification of the different phases of the feeding cycles was based on the position of the prey item with respect to the jaws. In the capture phase, the prey was outside the jaws and the feeding apparatus was used to bring the prey between the jaws. In the reduction phase, the prey was transversally orientated between the jaws. The transport phase corresponded to the displacement of the prey towards the oesophagus. This phase began as soon as the prey was longitudinally orientated with respect to the jaws. Transport of the prey is complex: the prey moved posteriorly in the buccal cavity, reached the pharynx and entered the oesophagus. We follow the definitions of food transport and pharyngeal packing given by Smith (1984) for separating these stages. The cycles used to move the prey posteriorly in the buccal cavity up to the pharynx belong to the first step (transport per se). The cycles in which the prey, beyond the tongue, was pushed from the pharynx to the oesophagus belong to the second step (pharyngeal packing). During transport, the prey was still visible in the buccal cavity, while only the tongue was visible when the gape increased during pharyngeal packing.

We follow previous workers in our use of terminology for describing each prey processing cycle (Bramble and Wake, 1985; Hiiemae and Crompton, 1985). In O. cuvieri, the slow opening stage (SO) began with the onset of mouth opening. Division of this stage into SO I and SO II was based on the gape angle. An increase in gape angle corresponded to SO I. During SO II, which always followed SO I, the gape angle remained stationary. The fast opening stage (FO) began with a sudden increase in the rate of mouth opening. The fast closing stage (FC) began with the first closure of the mouth. The closing of the mouth was identified as a fast closing because it corresponded to the stage called fast closing in the Bramble and Wake model.

We did not identify a slow closing/powerstroke stage because we did not measure clear variations in the gape velocity during the closing stage.

To catch the prey, the lizards oriented their head towards the prey item, protracted the tongue, touched the prey with the tongue and achieved prey capture with tongue and jaw displacements. As the gape increased, the tongue became visible in the mouth. Fig. 2 shows a typical example of kinematic profiles depicting relative displacements of the tongue and jaws during capture of a cricket. Changes in gape angle were divided into slow opening (SO), fast opening (FO) and fast closing (FC) stages (Fig. 2A). The SO stage was divided into SO I and SO II. During SO I, the mandible depressed and the neurocranium remained stationary (Fig. 2B). During SO II, the mandible and neurocranium depressed simultaneously towards the prey. SO II lasted for 50% of the total duration of the gape cycle (Table 1). A slight elevation of the neurocranium occurred at the end of the FO stage and beginning of the FC stage (Fig. 2B). Gape angle showed a slight decrease at the very end of SO II (Fig. 2A).

The FO and FC stages each represented only 8% of the total duration of gape cycle (Table 1) and maximal gape amplitude in prey capture was 35±7° for crickets (Table 2). The total duration of the capture cycle was highly variable, mainly because of variability in the duration of SO II (Table 2).

Tongue protraction occurred as soon as the mouth opened (Fig. 2C). At the end of the SO stage, the tongue tip moved beyond the mandible. As the tongue moved forward, it curled so that the tips were ventrally oriented and the anterior dorsal surface of the tongue was deformed and placed in line with the prey (Fig. 3). As soon as the tongue moved out of the buccal cavity, it appeared as two large rounded lateral masses separated by a medial hollow (Fig. 3 frames 4-5). When the tongue contacted the prey, these two anterior masses first touched the cuticle of the insect and then the entire anterior region of the tongue spread onto the prey (Fig. 3 frames 8-9). Tongue protrusion onto the prey required a mean of 0.29s from the appearance of the tongue between the jaws until its contact with the prey (Table 2).

Immediately after contact of the tongue with the prey, gape angle increased suddenly (FO stage). Prey retraction into the buccal cavity was complex. It was always produced by simultaneous displacement of the jaws around the prey and tongue retraction, which lasted only 0.03-0.04s (Fig. 3 frames 8-11).

The capture cycle was accompanied by body displacements of the lizard towards the prey. During tongue retraction, the head continued its forward and downward movement towards the prey (Figs 2D and 3).

The reduction phase involved cyclic jaw and tongue displacements associated with head elevation (Fig. 4A,B). The head was always elevated after the first reduction cycle and this elevation continued throughout the entire reduction and transport phases in 58% (N=30) of feeding bouts. The head remained in a maximally elevated position as the successive gape cycles occurred, without any large displacements. In general, 1-2 reduction cycles occurred before maximal elevation of the head (Fig. 4B).

Reduction cycles were divided into three stages (SO, FO, FC), but the first reduction cycle never involved an SO stage (Fig. 5, cycle 2). The mean duration of the SO stage represented 55% of the mean total duration of the gape cycle (Table 1), and its duration was highly variable (Fig. 5). In contrast, the durations of the FO and FC stages did not vary greatly. The FO stage made up 17% and the FC stage 28% of the total duration of the cycles (Table 1). Gape distance changes were mainly due to mandible depression (Fig. 6A,B). Elevation of the neurocranium, when it occurred, was always recorded at the end of the FO and during the FC stage (Fig. 6D). A clear stationary stage between two successive cycles was rarely observed. When it occurred, this stationary stage lasted 0.015-0.085s (N=45). After the FC stage, the gape angle of the next cycle increased rapidly (Fig. 6A).

Tongue displacements during the reduction phase are illustrated in Figs 6C and 7. During the stationary SO stage and the beginning of the FO stage, the tongue moved forward under the prey (Fig. 6C). At this time, it was also elevated (Fig. 7). It began to move backwards 0.016-0.032 s before the gape angle achieved its maximal amplitude (Fig. 6C). Retraction of the tongue was clearly associated with a period of flattening (Fig. 8). From cineradiographic frames, displacements of the markers in the tongue showed the same pattern as seen during transport cycles, except that vertical displacements were larger in reduction cycles (see below).

Transport and pharyngeal packing cycles involved SO, FO and FC stages (Figs 9A and 10A). Changes in gape angle were mainly due to mandible depression in transport and pharyngeal packing cycles (Fig. 9B). The duration of the stationary stage between two successive cycles was greater (0.045-0.250 s) than during reduction. The mean duration of the SO stage, which involved 58% of the mean total cycle duration (Table 1), was significantly greater in the transport phase than in the reduction phase (Table 3). The mean duration of the FO stage represented 19%, and of the FC stage 23%, of the mean total duration of the gape cycle (Table 1). Mean durations of FO and FC stages were not significantly different for reduction and transport phases (Table 3). Mean durations of the FO and FC stages of transport and capture cycles were not significantly different at the P⩽=0.05 level using a t-test (FO, t=-1.11, d.f.=28; FC, t=-1.97, d.f.=28). In contrast, the duration of the SO stage in transport is significantly shorter (t=4.44, d.f.=27; P⩽0.05; see, however, Materials and methods for restrictions on the use of this test). In addition, gape amplitude and time to maximal depression of the lower jaw were significantly greater in transport cycles than in reduction cycles (Table 3). However, differences among individuals were important for five of the eight variables (Table 3). Interactions between types of behaviour and individuals were only significant for gape amplitude and time to maximal depression of the lower jaw (Table 3).

The cycle of tongue movements relative to the prey and to the jaws in transport and pharyngeal packing was similar to that observed in reduction (Figs 6C, 7, 8, 9C and 10B,C). When the jaws were closed, and during the SO and FO stages, the tongue moved forward and upward relative to the prey (Figs 7 and 8). Tongue retraction occurred 0.01-0.07 s prior to maximal gape opening at the end of the FO stage and 0.03-0.06 s after the end of the SO stage (Fig. 10B).

The two markers placed in the mid and hind tongue moved forward simultaneously relative to the gape cycle, but the marker in the hind tongue moved more rapidly than the marker in the mid tongue. Consequently, the horizontal distance between the two markers was minimal prior to retraction (Fig. 10D) and subsequently increased during tongue retraction. The vertical distance between the two markers did not change because they were placed in the tongue floor (Fig. 11). Fig. 11 shows a typical pattern of intraoral tongue shape deformations during a transport cycle. The horizontal distance between the two markers in the tongue decreased during an increase in tongue width. Tongue retraction occurred simultaneously with an increase in the horizontal distance between the markers (Fig. 11). The tongue retracted by moving backwards and downwards (Fig. 10B,C). Some gape cycles during pharyngeal packing were accompanied by slight tongue protrusion out of the buccal cavity (Fig. 9C,D). In this case, the anterior-posterior cyclic displacements of the tongue were larger than those involving any protrusion of the tongue out of the mouth (Fig. 9D).

During each transport cycle, the prey moved posteriorly during tongue retraction, but also moved slightly anteriorly during its protraction in the next cycle. During pharyngeal packing, when the tongue moved out of the mouth, backward displacements of the prey towards the oesophagus were larger (Fig. 9E,F). During the other cycles involving only intraoral tongue displacements, posterior displacements of the prey were very small (Fig. 9E,F).

The cleaning cycle consisted of a small protraction of the anterior tongue out of the mouth followed by its wrapping around the mandible and retraction (Fig. 8). The kinematic profiles of the gape cycle were different from those reported for capture, reduction and transport (Fig. 12A). The principal differences were (1) a smaller amplitude of gape angle (Table 2), and (2) an absence of division into two stages of jaw opening. As in other cyclic jaw displacements, gape angle was mainly produced by depression of the mandible (Fig. 12B). The tongue protracted until the end of mouth opening (Fig. 12C) and the head remained stationary during these cycles (Fig. 12D,E).

The correlation matrix for the data set depicting timing variables, maximal gape angle and lower jaw depression confirmed the strong association between lower jaw displacements and gape cycles (Table 4).

The first principal component from the kinematic variables reflected the strong association among the timing variables, except the FO and FC variables (Table 5). A plot of the factor scores of the four phases on the first two principal components showed that capture, reduction and transport phases were not separated in the multivariate kinematic space (Fig. 13). In contrast, the cleaning phase was completely separated from the other phases, particularly along the second principal component. However, the multivariate ANOVArun on the scores on the first two principal components did not show a significant difference among the phases (MANOVA, Wilkes’ lambda=1.95, d.f.=3.28, F=0.1, F>0.05).

In this study, we describe quantitatively the kinematics of jaw and tongue displacements during capture, reduction, transport and cleaning phases of one species of Oplurinae. The data allow (1) comparisons of each phase with previously published data for scleroglossans and iguanians, and (2) testing of the generalities of tetrapod feeding kinematics and evolutionary trends proposed, respectively, by Bramble and Wake (1985) and Reilly and Lauder (1990). Each of these points is discussed below.

Kinematic profiles and variables of head, gape and jaw movements in O. cuvieri are similar to those reported for other iguanians with different types of food (Bels and Baltus, 1987, 1989; Schwenk and Bell, 1988; Schwenk and Throckmorton, 1989; Bell, 1990; Bels, 1990; Kraklau, 1991; So et al. 1992): (1) maximal gape angle varies from 25 to 42° (35° for O. cuvieri, Table 2); (2) gape angle is mainly produced by depression of the lower jaw (Fig. 2B); (3) a slight reduction in gape angle (or distance) occurs before the FO stage (Fig. 2A); (4) the duration of the SO stage is highly variable (Table 2); (5) the head is depressed towards the prey during the SO and FO stages (Fig. 2D). The total duration of the gape cycle is highly variable because of the variation in the duration of the SO stage (Table 2). In general, the SO stage is divided into SO I (opening) and SO II (‘plateau’). However, SO II may be completely absent as in Anolis equestris (Bels, 1990) and Agama agama, where the jaws are continuously open during the SO stage (Fig. 7 in Kraklau, 1991). In O. cuvieri, SO II is produced by simultaneous depression of the upper and lower jaws (Fig. 2A,B).

Tongue shape and displacements are also similar for all iguanians studied. However, Schwenk and Throckmorton (1989) report an intrafamilial difference in conformation of the tongue prior to and during its protraction towards the prey. The shape of the tongue, when protruded for contacting prey in O. cuvieri, is similar to that previously described for iguanids (Fig. 3, and plate I in Schwenk and Throckmorton, 1989). However, the lateral expansion of the tongue in O. cuvieri into two anterior masses (Fig. 3) has not been clearly reported for other iguanids and agamids, except for Anolis equestris (Bels, 1990). This anterior deformation of the tongue may be related to changes of pressure in the lymphatic system of the fore tongue (Delheusy, 1991; V. Delheusy, V. L. Bels and G. Toubeau, in preparation).

It is very difficult to compare the timing variables of prey capture in O. cuvieri with the data described by Schwenk and Throckmorton (1989) because (1) the frame speeds of the films are different (32 and 64 frames s⁻¹ for Schwenk and Throckmorton and 200framess⁻¹ for this paper), and (2) very different types of food were used. The duration of tongue protrusion in O. cuvieri is not different (range 0.070-0.250 s) from that reported by Schwenk and Throckmorton (1989) for other iguanids and agamids (range 0.025-0.543 s). In contrast, the duration of tongue retraction (range 0.030-0.040 s) is shorter in O. cuvieri than in other iguanids (range 0.049-0.180 s). In Agama agama, feeding on a cricket, tongue retraction occurs over approximatively 0.020 s (variable TD in Fig. 7 of Kraklau, 1991). Compared with feeding on vegetables, tongue retraction in iguanians feeding on insects takes less time (Schwenk and Throckmorton, 1989; Bels, 1990; Kraklau, 1991). Variability in duration of tongue retraction may be related to the prey type, as indicated by the differences in this variable when moving (insects) and stationary (vegetables) food is being eaten. Visual stimuli from the prey may influence the motor pattern and kinematic variables of this retraction either before or during tongue protrusion.

All the iguanids and agamids exhibit a preparatory phase involving body responses, such as head orientation, accompanied of mouth opening. During this phase, the gape increases and the tongue is ‘prepared beyond the jaw margins’ as emphasized by Schwenk and Throckmorton (Fig. 2; Fig. 5 in Schwenk and Throckmorton, 1989; Bels, 1990) or slightly extended (Fig. 7 in Kraklau, 1991). In a successful prey capture, this preparation of the tongue is always followed by simultaneous head, jaw and tongue displacements towards the prey (Fig. 2).

The prey is moved into the buccal cavity by a short tongue retraction combined with displacements of the jaws around the prey (Figs 2C, 3). Lateral expansion of the dorsal surface of the fore tongue onto the prey has a very important function (Fig. 3). The prey is pressed firmly against the substratum as soon as the tongue contacts the prey, thus preventing its escape. Lingual ingestion of smaller prey items in other iguanians (Plates I, II and IV, in Schwenk and Throckmorton, 1989) involves upward movements of the prey from the substratum to the buccal cavity during tongue retraction. In contrast to O. cuvieri, these lizards use the tongue for bringing the prey into the buccal cavity. Such a difference in tongue use between O. cuvieri and iguanids such as Dipsosaurus dorsalis is related to prey size, prey weight or prey volume or corresponds to an adaptative behavioural difference related to a species-specific diet. The observation that the FO stage begins as soon as the prey is contacted by the tongue (Fig. 2A) in O. cuvieri supports the suggestion that tongue-prey contact is the stimulus for initiating this stage (Schwenk and Throckmorton, 1989).

Kraklau (1991) divided capture into three phases (preparatory, lunge and prey retraction) for A. agama, and suggested that the beginning of the lunge stage is the ‘committed’ step”. Therefore, for Kraklau (1991), the capture phase of the jaw cycle largely consists of locomotion towards the prey. Lingual ingestion in Phrynocephalus helioscopus does not involve a large vertical body displacement (Fig. 5 in Schwenk and Throckmorton, 1989). In chameleons, the first phase of prey capture is fixation (Bell, 1990; Wainwright et al. 1991). In O. cuvieri, forward and downward displacements of the head towards the prey (Fig. 2D) occur in a similar way to those in other iguanids and agamids. This would suggest that the coordination between locomotor and jaw displacements is rather similar for all iguanian lizards except chameleontids and, perhaps, P. helioscopus (Bels, 1990).

The data from O. cuvieri confirm that the lunge phase, once initiated, goes to completion. However, rapid changes in prey position relative to the lizard during this phase will allow us to see whether any modulations occur during this phase. In contrast to scleroglossans such as Lacerta viridis (Goosse and Bels, 1992), O. cuvieri never uses several successive jaw cycles to capture its prey (Fig. 2A). When the prey is not captured, O. cuvieri stops (for as long as a few seconds) and begins a new combined locomotor and head-jaw cyclic displacement. This is also the case for previously described agamids and iguanids (Schwenk and Throckmorton, 1989; Bels 1990; Kraklau, 1991). Our data from O. cuvieri and recent data from agamids (Kraklau, 1991) support the suggestion that transformations in the tongue projection mechanism may also be accompanied by transformations of the jaw-locomotor pattern relationship (Bels, 1990).

In comparison with other lizards, four main conclusions about the kinematics of reduction and transport cycles can be emphasized: (1) mastication and transport cycles are organized into two successive periods; (2) the jaw cycles of the reduction and transport phases do not show any obvious differences from those described for other lizards; (3) tongue displacements out of the buccal cavity and related variables are similar in all iguanians; and (4) inertial feeding (head elevation) is used during prey consumption.

In O. cuvieri, masticatory and transport cycles are sequentially organized, as in A. equestris (Bels and Baltus, 1989) and Chameleo jacksonii (So et al. 1992). This observation does not accord with those of Smith (1984) and Schwenk and Throckmorton (1989), who reported that masticatory (=biting or reduction) cycles occur during the intraoral transport phase. In the reduction cycle, the prey is positioned transversally within the jaws (Fig. 8). In transport cycles, the prey orientation changes drastically and becomes longitudinal for entry into the oesophagus (Fig. 8). The first transport cycle may also be accompanied by reduction. This reduction only occurs with large prey. Changes in prey orientation occur at the end of the reduction or at the beginning of the transport phases (Fig-5).

In O. cuvieri, jaw profiles (SO, FO and FC stages) in the reduction and transport cycles are similar (Figs 6B and 9B). This similarity is in agreement with the data from iguanians and scleroglossans (Smith, 1984; Goosse and Bels, 1992). From a comparison of the kinematic profiles, our data support the suggestion of Schwenk and Throckmorton (1989) that mastication is a subset of the transport cycle. However, four of the eight kinematic variables (maximal gape amplitude, total duration of the cycle, duration of SO, and time to maximal depression of the lower jaw) are significantly different between the two cycles (Table 3). These differences may be due to the position of the prey and/or its contacts with the tongue. For instance, maximal gape amplitude should be larger during the transport cycle in order to move the prey posteriorly. The other variables are mainly related to the slow stage of the gape cycle and they are larger during the transport phase (Table 2) because these are the characteristics of the jaw cycles that allow the tongue to move more easily under the prey and to move the prey efficiently in the oesophagus.

Smith (1984) reported a difference in tongue displacement with respect to the jaws between the biting and the transport cycles. In C. similis, the tongue moves forward during the SO and FO stages of the biting cycle, while in the transport cycle it is in its anteriormost position at the end of the SO stage. Such a difference was not observed in O. cuvieri (Figs 6C, 7 and 10B). The two markers placed in the mid and hind tongue allowed us to show that forward and backward displacements of the tongue are similar in both reduction and transport cycles (Fig. 10B,C). Vertical displacements of the tongue in reduction cycles are often larger than those in transport cycles.

Anterior and posterior tongue markers in C. similis move backwards and upwards rather than upwards and forwards during the SO stage (=opening one in Smith, 1984) in pharyngeal packing cycles. A similar timing difference in tongue displacements was observed during the last transport cycles in O. cuvieri (Fig. 9C). This difference was clearer when the tongue moved out of the buccal cavity. When the food is posterior to the hind tongue, it occupies the entire pharynx (Fig. 8) and its passage into the oesophagus is very slow, as shown by the small prey displacements at each pharyngeal packing cycle (Fig. 9E). The crickets fill the entire pharynx in O. cuvieri (Fig. 11). The friction of the tongue against the prey may be very important in O. cuvieri and thus greatly influence the amplitude of horizontal and vertical tongue displacements.

Some pharyngeal packing cycles involve displacements of the tongue out of the buccal cavity (Fig. 9D). During backward displacements of the tongue in these cycles, the prey is moved more posteriorly than in the other cycles (Fig. 9D). Smith (1984) showed that cyclic tongue displacement in C. similis and T. nigro-punctatus was larger in the anterior-posterior direction during pharyngeal packing than during transport. This is also the case for O. cuvieri, particularly when the tongue moves out of the buccal cavity. An increase in tongue displacement, produced by protrusion of the tongue from the mouth, is used to provide larger forces against the bolus and to open the oesophageal sphincter.

During reduction and transport cycles, the hind tongue moves anteriorly more rapidly than the mid tongue (Figs 10B and 11). During the SO stage, forward displacements of the two tongue markers occur simultaneously with tongue bulging (Fig. 11). During bulging, the hind tongue contracts relative to the mid and fore tongue, as shown by the decrease in horizontal distance between the two tongue markers (Fig. 10D). The tongue flattens out, the markers move pos-teriorly, and the distance between them increases as soon as the tongue retracts during the FC stage (Fig. 10D). Contraction of the hind tongue relative to the mid tongue may store energy in the elastic structures of the tongue, such as the laryngohyoid ligament (Delheusy, 1991). This ligament may act as a spring, which is compressed during the SO and FO stages and then acts upon the bolus by recovering its initial form during the FC stage. By restoring this energy, the ligament, and thus the hind tongue, act powerfully to displace the prey posteriorly. This may also explain the large posterior displacement of the prey associated with displacement of the tongue out of the mouth in some pharyngeal packing cycles (Fig. 9E).

The reduction phase often involves elevation of the head (Figs 4 and 6). This elevation has previously been reported for other iguanians such as P. helioscopio (Fig. 5 in Schwenk and Throckmorton, 1989). In this agamid, the head moves upwards during each jaw opening and downwards during each jaw closure. In contrast, the first two reduction cycles following prey capture in D. dorsalis involve only head repositioning. In a typical reduction phase in O. cuvieri, opening of the mouth during the first reduction cycle occurs without any large vertical displacement of the head. The head is only repositioned because it was depressed towards the prey during capture (Fig. 4B). During the closing phase of this first reduction cycle and the opening phase of the next cycle, the head moves suddenly backwards and upwards (Figs 4B and 8). From the second reduction cycle, this may produce an important backward displacement of the prey into the buccal cavity while the prey is reduced. The prey is thus moved near the angulus oris and the closing forces of the jaws against the prey are stronger. The use of head displacements during reduction is highly variable (Fig. 8) and may depend on stimuli from the prey.

For the later transport cycles, vertical displacements of the head are smaller than for reduction cycles. At the fast opening stage of the first transport cycle, the head moves backwards and upwards (Fig. 8). During transport, the prey is positioned parallel to the jaws (Figs 7 and 8). Tongue retraction occurring during the FO stage (Fig. 10B) and a simultaneous elevation of the head facilitate backward displacement of the prey towards the oesophageal opening.

Cleaning cycles were very rare and we did not record them with cineradiography. These cycles, which appear after the transport phase, may have the same effect on the prey as the pharyngeal packing cycles involving tongue protrusion. They were described separately because they did not occur before or after one or several cyclic jaw displacements without tongue protrusion. The size of the alimentary bolus, and thus the relative difficulty with which it passes into the oesophagus, may explain the presence or absence of these cycles. Unlike the pharyngeal packing cycle, the angle of the jaws in the cleaning cycle is lower than in capture, reduction and transport cycles (Table 2). However, vertical and horizontal displacements of the tongue do not differ in the cleaning and pharyngeal packing cycles (Figs 9 and 12C,D).

Fig. 13 confirms the similarities between the reduction, transport and capture cycles in a multivariate space analysis obtained from kinematic variables. The data match those obtained in Agama agama by Kraklau (1991), but differ from the data obtained from Chamaeleo jacksonii by So et al. (1992). In both O. cuvieri and A. agama, capture and reduction cycles overlap largely in the principal component analysis multivariate space. Transport and reduction cycles in chameleontids are distinct, whereas they overlap strongly in O. cuvieri.

The separation in C. jacksonii is related to the larger hyoid retraction, mouth opening and the velocity of the gape cycle during reduction. In O. cuvieri, gape amplitude (mouth opening) varies considerably among individuals (Table 3), whereas it varies between types of behaviour in the chameleon. In O. cuvieri, the durations of the FO and FC stages are similar for capture (see t-test with restriction), reduction and transport, whereas the durations of the SO stage, and thus the total duration of the cycle, are significantly different not only for the reduction and transport phases (Table 3) but also between the capture and transport phases (see t-test with restriction). Only a principal component analysis using the same kinematic variables for all lizards will allow us to show whether either the variables chosen for each study or the specialization of tongue-hyoid system in chameleontids produces the separation between reduction and transport phases in C. jacksonii.

The principal component analysis reveals that the cleaning phase is distinct from the other phases (Fig. 13). This difference may be explained by the change in gape profile. For instance, the opening stage in the gape cycle is not divided into an SO and an FO stage (Fig. 12).

The generalized feeding model of Bramble and Wake (1985) is only partially supported by our data in O. cuvieri. The principal implications of this model are (1) that the gape angle is divided into five stages [slow opening I, slow opening II, fast opening, fast closing and slow closing/powerstroke (SC/PS) stages], (2) that SO II is related to a slight depression of the lower jaw while the upper jaw remains stationary, (3) that the upper jaw elevates during FO and depresses during FC, (4) that hyoid-tongue retraction begins during FO, (5) that hyoid-tongue protraction occurs during SC/PS, SO I, SO II and the beginning of FO, (6) that the head is elevated at the end of FO and during FC (Fig. 13-3 in Bramble and Wake, 1985).

They speculate that the tongue moves anteriorly under the food during SO I, fits to the food during SO II, retracts during FO and FC, and reaches its maximal posterior position during SC/PS (Fig. 13-5). They also speculate that SO II increases for larger or heavier food items.

In contrast to Schwenk and Throckmorton (1989), we did not observe an SO II stage in transport cycles and the SO stage was not always distinct from the FO stage during reduction and transport phases (Figs 6, 9 and 10A). Furthermore, a clear SO stage was often absent in pharyngeal packing cycles, as assumed by Smith (1984) for C. similis, and was completely absent in cleaning cycles (Fig. 12A). Our data do not support the model of Bramble and Wake or their speculation about the relationship between SO II duration and the size of the prey. In this study, the food item completely filled the buccal cavity (Fig. 11). If the SO stage is related to forward displacements of the hyolingual complex under the food, as speculated by Bramble and Wake and observed in O. cuvieri (Figs 6C, 8, 9D and 10B), frictional forces of the tongue on the prey may have a great influence on the duration of the SO I but do not imply a long SO II. In conclusion, constraints at the prey-tongue contact surface appear to play a very important role in the duration of the SO I stage.

Furthermore, the position of the tongue may also be important in the presence or absence of, or in the duration of, SO I. For instance, the first reduction cycle does not exhibit an SO stage because the tongue is positioned more anteriorly in the buccal cavity after its retraction with the prey (Figs 4 and 6A). After capture, the tongue certainly adheres strongly to the prey cuticle. The first reduction cycle may be used mainly to decrease contact between the tongue and the prey. This decrease in contact may occur during the fast depression of the lower jaw that immediately follows the capture cycle (Fig. 6B). Because the tongue does not move horizontally, gape angle does not exhibit an SO stage.

In general, the SO stage during the three following reduction cycles increases (Fig. 5). Such an increase in duration may be related to an increase in the anterior-posterior displacements of the tongue, which has less contact with the prey after the first reduction cycle. During reduction, the prey item is oriented transversely to the jaws (Fig. 8). This orientation changes during the two last reduction cycles and/or the first transport cycle (Fig. 5). In these cycles, the duration of the SO stage increases, which could be related to the change in prey orientation. At this time, the tongue may show displacements and deformations to change the prey orientation.

Schwenk and Throckmorton (1989) and Kraklau (1991) have compared the Bramble and Wake model with the capture cycle. Such a comparison in O. cuvieri is possible because capture and transport cycles are closely related in multivariate kinematic space (Fig. 13). During the SO stage of the capture cycle, the neurocranium in O. cuvieri does not move as predicted by the model of Bramble and Wake (1985). The long SO II stage was produced by simultaneous depression of both jaws (Fig. 2A,B).

Thus, the variability of the SO stage is strongly related to tongue-prey contacts. Division of this stage into SO I and SO II, and the characteristics of these stages as proposed for the model of Bramble and Wake, are not general.

Reilly and Lauder (1990) proposed two synapomorphic characters for all tetrapods (tongue-based intraoral prey transport and a long preparatory phase prior to the FO stage) and five derived characters for all Amniota (an SO stage prior to the FO stage, gape increase mainly by depression of the lower jaw, a recovery stage compressed into the gape cycle, inertial feeding present and extensive intraoral food processing).

The data in this study confirm the model of Reilly and Lauder (1990). In O. cuvieri, gape- and tongue-related displacements exhibit the two synapomorphic characters for capture, reduction and transport cycles (Figs 3–12). Gape increase is mainly dependent on lower jaw depression (Table 4). The SO stage always occurs before the FO stage in transport, but not in the subsequent reduction cycle (Fig. 7). The extensive intraoral prey processing is well developed in iguanians such as O. cuvieri because the cycles belong to a reduction or transport phase.

The role of the cleaning cycles that occur after transport is not yet clear. In iguanians, these cycles belong either to the transport phase (pharyngeal packing) or to another phase that becomes very important in scleroglossan lizards (Goosse and Bels, 1992).

 
• EH

  maximal elevation of the head

 
• FC

  duration of the fast closing stage

 
• FO

  duration of the fast opening stage

 
• GA

  maximal gape

 
• MDLJ

  maximal depression of the lower jaw

 
• MDTO

  maximal vertical displacement of the tongue

 
• MEUJ

  maximal elevation of the upper jaw

 
• MHDP

  maximal horizontal displacement of the prey

 
• MHDTO

  maximal horizontal displacement of the tongue

 
• MVDP

  maximal vertical displacement of the prey

 
• SO I

  duration of slow opening stage I

 
• SO II

  duration of slow opening stage II

 
• TC

  total duration of the cycle

 
• TGA

  time to maximal gape

 
• TMDLJ

  time to maximal depression of the lower jaw

 
• TMDTO

  time to maximal vertical displacement of the tongue

 
• TMEUJ

  time to maximal elevation of the upper jaw

 
• TMHDP

  time to maximal horizontal displacement of the prey

 
• TMHDTO

  time to maximal horizontal displacement of the tongue

This study was supported by F.R.F.C. grant 2.9006.90. We are extremely grateful to Sabine Renous and Jean-Pierre Gasc from the National Museum of Natural History of France (Paris) who allowed us to use their cineradiographic apparatus. Their help at that stage of our study was greatly appreciated. Christine Noël provided some of the illustrations. We thank Mark Westneat, an anonymous reviewer and Elizabeth A. Howes very much for their invaluable assistance in improving this paper.