The activity of jaw and hyolingual muscles during the entire feeding sequence is examined in the lizard Agama stellio, with special focus on the intraoral transport and swallowing stages. Correlation of electromyography (EMG) data with kinematics shows that the kinematic phases (slow opening, SO; fast opening, FO; fast closing, FC; slow closing/power stroke, SC/PS) are characterised by distinct activities in the jaw and hyolingual muscles. The SO phase is clearly the result of tongue protraction (upon protraction, the tongue is pulled against the prey and consequently the lower jaw is pushed down), whereas the FO phase is caused by activity in the jaw opener and dorsal cervical muscles. Both the FC and SC/PS phases are characterised by pronounced activity in the jaw adductor muscles. Tongue retraction is produced by activity in the hyoid and tongue retractor muscles. A quantitative analysis of time-related EMG data shows that, in accordance with the kinematic analyses, three different stages can be recognised as components of the feeding cycle: prey capture, intraoral transport and swallowing. However, analysis of intensity-related data allowed a fourth stage, crushing, to be detected. Whereas there are indications that prey capture, intraoral transport and swallowing are controlled by different motor patterns, the differences between crushing and transport are likely to be caused by feedback mechanisms. Our results show the importance of including intensity-related data in quantitative analyses of EMG recordings in order to discriminate between feeding stages. Additionally, it is shown that both the jaw and the hyolingual muscles play crucial roles during feeding. During all stages, movements of the hyolingual apparatus are an essential part of the feeding cycle. Thus, when examining lizard feeding mechanisms, the activity patterns of the hyolingual muscles should not be neglected.

On the basis of observations on regularly chewing tetrapods (e.g. ruminating ungulates), it has been suggested that mammalian feeding cycles might be driven by simple motor pattern generators or neural oscillators (Thexton, 1974, 1976; Dellow, 1976). A comparable mechanism might also be applicable to the transport cycles of lower tetrapods since reptilian and mammalian transport cycles show many similarities (see Bramble and Wake, 1985). The mammalian masticatory cycle may therefore have evolved from the primitive reptilian chewing cycle with relatively little overall change in neuromotor programming (Bramble and Wake, 1985). However, as argued by Smith (1984), biting in lizards is irregular and takes place as independent chewing cycles, preceding or interrupting food transport, and so may not be driven by neural oscillators. Relatively few studies have examined reptilian jaw and hyolingual muscle activity patterns or their control mechanisms during feeding (Throckmorton, 1978; Gorniak et al. 1982; Smith, 1982, 1984, 1986; Gans et al. 1985; Gans and De Vree, 1986; Wainwright and Bennett, 1992a, b; Herrel et al. 1995). Hypotheses regarding the evolution of feeding cycles and the presence of neural oscillators in reptiles therefore remain speculative and need to be confirmed by further study.

It has likewise been suggested that a basic pattern of tongue function is present within vertebrates as a result of the retention of a primitive neural control pattern (Hiiemae et al. 1979; Bramble, 1980). However, the function of the tongue and hyolingual apparatus (especially the action patterns of the hyolingual muscles) remains poorly studied in lower tetrapods in general and in reptiles more specifically (Smith, 1984, 1986; Wainwright and Bennett, 1992a,b; Herrel et al. 1995).

Whether prey capture, intraoral transport and swallowing are driven by the same or a similar motor pattern in vertebrates remains unclear. Although it has been proposed that the intraoral transport cycle has an ancestral status with respect to prey capture for lower tetrapods in general, this may not be true for swallowing (Bramble and Wake, 1985). Tongue-dependent swallowing might even be a derived feature of amniotes (Bramble and Wake, 1985). Reptilian swallowing, in contrast to intraoral transport, is clearly divergent from the mammalian swallowing cycle. Whereas in mammals swallowing is integrated into the basic transport cycle, in lizards it seems to be a distinct stage (Smith, 1984). Relatively few studies have investigated prey capture, intraoral transport and swallowing in one animal (e.g. Delheusy and Bels, 1992; Urbani and Bels, 1995; Herrel et al. 1996), and no electromyographic studies investigating the activity of both jaw and hyolingual muscles during all feeding stages have been performed. Such an approach would allow the relationships between the feeding stages and the importance of the jaw and hyolingual systems to each of these stages to be examined.

The aims of the present study were, therefore, to provide a quantitative electromyographic analysis of the activity of the jaw and hyolingual muscles during the entire feeding sequence with a special focus on intraoral transport and swallowing in a lizard, Agama stellio. On the basis of these data, the role of the jaw and hyolingual muscles during different feeding stages, the relationships between them, and the evolution of the feeding cycle in lower tetrapods will be discussed.

Specimens

Five adult Agama stellio L. (total length 20±3 cm; mass 42±3 g, means + S.D.) were used in experiments. The specimens were collected in Israel and provided by Dr E. Kochva. The animals were kept in a glass vivarium on a 12 h:12 h light:dark cycle and were provided with water and food, consisting of crickets, grasshoppers and mealworms, ad libitum. The environmental temperature varied from 26 °C during the day to 20 °C at night; an incandescent bulb provided the animals with a basking place at a higher temperature (30 °C). An additional four animals were dissected and stained (Bock and Shear, 1972) to characterize all jaw and hyolingual muscles. Drawings were made of all stages of the dissection using a Wild M3Z dissecting microscope with a camera lucida.

Electromyographic recordings and analysis

The animals used in the electromyographic (EMG) experiments were anaesthetized using an intramuscular injection of Ketalar (200 mg kg−1 body mass) before electrode implantation. Bipolar electrodes (25 cm long) were prepared from Teflon-insulated 0.065 mm Ni–Cr wire. The insulation was removed at the tip, exposing 1 mm of electrode wire. The electrodes were implanted percutaneously into each muscle belly using hypodermic needles with 2 mm of the electrode bent back as it emerged from the needle barrel.

During the experiments, electrodes (a maximum of ten electrodes for one recording session) were placed in a number of muscle groups (for identification of muscles, see Fig. 1 and Table 1) of the major jaw closers: the musculus adductor mandibulae externus (superficial anterior and posterior, medial and profundus parts; MAMESA, MAMESP, MAMEM and MAMEP), the musculus pseudotemporalis (superficial and profundus parts; MPsTS and MPsTP), the musculus adductor mandibulae posterior (MAMP) and the musculus pterygoideus (lateral and medial parts; MPtlat and MPtmed). Electrodes were also placed in the jaw openers: the musculus depressor mandibulae (main and accessory heads; MDM and MDMA) and the musculus spinalis capitis (MSCa) and into several hyolingual muscles, the tongue protractors: the musculus genioglossus (lateral and medial parts; MGGL and MGGM); the musculus hyoglossus (MHG), the ring muscle (MRing); hyoid retractors: the musculus sternohyoideus (MSH), the musculus omohyoideus (MOH) and in the hyoid protractors: musculus mandibulohyoideus (parts 1 and 2; MMH1 and MMH2). Electrode placement was confirmed by dorsoventral and lateral X-rays after electrode implantation, and in two animals by dissection following experiments.

Table 1.

Origin and insertion points of the jaw and hyolingual musculature in Agama stellio

Origin and insertion points of the jaw and hyolingual musculature in Agama stellio
Origin and insertion points of the jaw and hyolingual musculature in Agama stellio
Fig. 1.

Schematic representation of jaw and hyolingual muscles of Agama stellio. (A) Lateral view of the skull; (B) ventral view of the lower jaw and the hyolingual apparatus. Arrows indicate the major jaw muscles and hyolingual muscles and their predominant lines of action. ar, articulare; BH, basihyoid; CBI, ceratobranchiale 1; CBII, ceratobranchiale 2; CH, ceratohyale; de, dentale; j, jugale; MAMEM, m. adductor mandibulae externus medialis; MAMEP, musculus adductor mandibulae externus profundus; MAMESA, m. adductor mandibulae externus superficialis anterior; MAMESP, m. adductor mandibulae externus superficialis posterior; MAMP, m. adductor mandibulae posterior; max, maxilla; MDM, m. depressor mandibulae; MDMA, m. depressor mandibulae accessorius; MGGL, m. genioglossus lateralis; MGGM, m. genioglossus medialis; MHG, m. hyoglossus; MMH1, m. mandibulohyoideus 1; MMH2, m. mandibulohyoideus 2; MMH3, m. mandibulohyoideus 3; MOH, m. omohyoideus; MPsTS, m. pseudotemporalis superficialis; MPsTP, m. pseudotemporalis profundus; MPtlat, m. pterygoideus lateralis; MPtmed, m. pterygoideus medialis; MRing, ring muscle; MSCa, m. spinalis capitis; MSH, m. sternohyoideus; MST, m. sternothyroideus; par, parietale; pe, processus entoglossus; po, postorbitale; q, quadratum; sa, surangulare; sq, squamosum; T, tongue.

Fig. 1.

Schematic representation of jaw and hyolingual muscles of Agama stellio. (A) Lateral view of the skull; (B) ventral view of the lower jaw and the hyolingual apparatus. Arrows indicate the major jaw muscles and hyolingual muscles and their predominant lines of action. ar, articulare; BH, basihyoid; CBI, ceratobranchiale 1; CBII, ceratobranchiale 2; CH, ceratohyale; de, dentale; j, jugale; MAMEM, m. adductor mandibulae externus medialis; MAMEP, musculus adductor mandibulae externus profundus; MAMESA, m. adductor mandibulae externus superficialis anterior; MAMESP, m. adductor mandibulae externus superficialis posterior; MAMP, m. adductor mandibulae posterior; max, maxilla; MDM, m. depressor mandibulae; MDMA, m. depressor mandibulae accessorius; MGGL, m. genioglossus lateralis; MGGM, m. genioglossus medialis; MHG, m. hyoglossus; MMH1, m. mandibulohyoideus 1; MMH2, m. mandibulohyoideus 2; MMH3, m. mandibulohyoideus 3; MOH, m. omohyoideus; MPsTS, m. pseudotemporalis superficialis; MPsTP, m. pseudotemporalis profundus; MPtlat, m. pterygoideus lateralis; MPtmed, m. pterygoideus medialis; MRing, ring muscle; MSCa, m. spinalis capitis; MSH, m. sternohyoideus; MST, m. sternothyroideus; par, parietale; pe, processus entoglossus; po, postorbitale; q, quadratum; sa, surangulare; sq, squamosum; T, tongue.

Electrical signals were amplified 2000 times with Tektronix 26A2 differential preamplifiers (range 100 Hz to 10 kHz) and Honeywell Accudata 117 d.c. amplifiers and recorded on a Honeywell 96 FM 14-channel tape recorder (medium bandpass) at a speed of 19.05 cm s−1.

The recorded EMG signals were digitized at 10 kHz using a Keithley DAS series 500 12-bit A/D convertor. After digitization, the signals were integrated following the procedure of Beach et al. (1982) and the number of spikes (S) as well as the average amplitude (A) and mean number of spikes multiplied by the average amplitude (S×A) per interval (bin) were calculated.

Twelve recording sessions were performed, each consisting of several feeding sequences. The results from two of these recording sessions (from two different animals) were analyzed quantitatively. These two recording sessions were chosen because they represented the maximal number of different jaw or hyolingual muscles implanted. The results from the other recording sessions were used in a qualitative analysis only. In the first recording session, results were obtained from four complete feeding sequences. This session included a total of four prey capture, 61 transport, 30 crushing and 79 swallowing cycles. Although ten electrodes were implanted during each recording session, only seven of these (and the pulse from the X-ray camera) could be amplified simultaneously. Thus, during the first two of these sequences (two prey capture, 43 transport, 15 crushing and 55 swallowing cycles), activity patterns from the MDM, MSCa, MAMESA, MPsTS, MAMP, MPtlat and MPtmed were recorded. During the following two sequences, activity patterns from the MDM, MAMESA, MAMEM, MPsTS, MAMP, MPtlat and MPtmed were recorded. The second recording session consisted of three sequences during which activity patterns of the MDM, MAMEM, MSH, MMH1, MGGM, MHG and MRing were recorded. This resulted in a total of three prey capture, 94 transport, 26 crushing and 67 swallowing cycles.

Time-based analysis of electromyograms

The muscle activity patterns recorded during a feeding sequence were first subdivided into separate cycles. Within one cycle, muscle activity patterns were subdivided into several activity bursts (usually three) on the basis of abrupt amplitude differences, if present. This does not necessarily mean that there was always more than one burst present within each cycle. For each muscle, the onset and the duration of all bursts within one cycle (and for all cycles analyzed) were recorded. Onset variables are expressed relative to the offset (onset plus duration) of the main activity burst in the MDM (=time 0) as this corresponds well to the time of maximal gape.

Intensity-based analysis of electromyograms

As the number of spikes multiplied by the mean amplitude (S×A) is a measure of the intensity of muscle recruitment (Basmajian and De Luca, 1985; Loeb and Gans, 1986), further analyses of intensity-related variables were based primarily on this variable. The means (mean), maxima (max) and sums (sum) of the recruitment levels (RL, where RL=S×A) were calculated per bin (RLbin), per bite cycle (RLbite) and per burst (RLburst) as muscles often showed more than one activity burst during the course of a gape and/or tongue cycle. Within each recording session, the maximal RLbite values (max, sum, mean) recorded for each muscle were determined. The RLbite data for all bite cycles within each recording session were then normalised for each muscle according to their respective maxima. Recruitment levels for each muscle are therefore expressed as a percentage of their maximal RLbite values. A similar procedure was used on the RLburst data, where all values were normalised to the maximal RLburst value for each muscle.

Video and cineradiographic recordings

Video or cineradiographic recordings were obtained simultaneously with the EMG recordings. Cineradiography was carried out using a Siemens Tridoros-Optimatic 880 X-ray apparatus equipped with a Sirecon-2 image intensifier. Feeding bouts were recorded in side view using an Arriflex 16 mm ST camera equipped with a 70 mm lens at a film speed of 50 frames s−1. Before cineradiography, small lead markers were inserted subcutaneously to mark the positions of the upper and lower jaws, the base and the top of the quadrate, the tongue, the frontal and parietal bones and dorsally into the neck using a hypodermic needle (see Herrel et al. 1996).

During implantation of the radio-opaque markers, animals were anaesthetized as described above. Placement of the markers was checked using dorsoventral and lateral X-ray photography. During cineradiographic recordings, prey items were injected with barium sulphate to help visualise their position.

Additional recordings of the feeding process were made at a higher filming speed (500 frames s−1) using a NAC-1000 high-speed video system. Video torches (2.4 kW; Tri-Lite, Cool Light Co. Inc., Hollywood, USA) provided the necessary illumination. During both the cineradiographic and the high-speed video recording sessions, the animals were filmed in an acrylic cage (30 cm×10 cm×10 cm), while feeding on grasshoppers (body length 2–2.5 cm). The prey item was always placed less than 10 cm from the snout of the lizard. The output of a Tektronix wave-pattern generator was recorded together with the EMG recordings on the FM tape recorder and sent to a light-emitting diode placed in the field of view of the camera. This allowed synchronisation of the electromyographic and kinematic records. For a description of the video and cineradiographic analysis, see Herrel et al. (1996).

Statistical analyses

Several analyses were performed on the electromyographic data to explore similarities between successive feeding stages (prey capture, intraoral transport, swallowing). For these analyses, Statistica version 5.0 (Statsoft Inc.) was used.

First, a factor analysis (VARIMAX rotation) was performed on the data set consisting of the time-related variables (onset and duration variables for all muscles) of all bite cycles within one recording session. An analysis of variance (ANOVA) was then performed on the first three factors coupled to a Duncan multiple-range significance test (at the 0.05 level) to explore the relationships between the different stages (cycle types). Next, the same analysis was performed on the intensity-related data set including the RLbite values (max, sum and mean) of all cycles from the first recording session (mainly jaw muscles). The same analysis was then performed on a similar data set from the second recording session (mainly hyolingual muscles).

Morphology

The skull morphology of Agama stellio was described previously by El Toubi (1947) and Jollie (1960). A. stellio has very little or no intracranial mobility (A. Herrel, personal observations based on cineradiographic recordings during feeding). The hyoid apparatus has a distinct tapered entoglossal process, one pair of ceratohyals and two pairs of ceratobranchials (Fig. 1).

A schematic representation of the jaw and hyolingual muscles in Agama stellio is given in Fig. 1; the origins and insertions of the muscles are given in Table 1. For a more detailed description of the jaw and hyolingual muscles in A. stellio, see Herrel et al. (1995). For descriptions of the jaw and hyolingual musculature in agamids in general, see Gandolfi (1908), Gnanamuthu (1937), Haas (1973), Gomes (1974) and Smith (1988).

General description of prey capture

A feeding bout in Agama stellio consists of prey capture, intraoral transport (including both transport and crushing cycles; see Herrel et al. 1996) and swallowing. Prey capture always involves a lunge of the body and the use of the tongue to make contact with the prey. After prey contact, the jaws are opened further and the prey is taken into the mouth using the tongue (Herrel et al. 1995). Once the prey has been seized, a number of cyclic movements of the jaws and tongue are used to crush the prey and to transport it to the back of the oral cavity. Once the prey item has been adequately reduced and positioned lengthwise within the mouth, swallowing occurs. During swallowing, the tongue is first used to pull and then to push the prey down into the oesophagus (Herrel et al. 1996).

Electromyography

Quantitative analysis

On the basis of the movements of jaws and tongue, three distinct stages (prey capture, intraoral transport and swallowing) can be recognised in Agama stellio (Herrel et al. 1996). In order to investigate whether each of these stages is characterised by a distinct motor activation pattern, a quantitative analysis of the EMG data was performed. For prey capture, the EMG data reported by Herrel et al. (1995) from the same set of experiments were used.

Time-based data from the first recording session are given in Tables 2–4. Muscle activity patterns during three cycle types [prey capture (see Herrel et al. 1995), swallowing and intraoral transport] differ significantly (all effects: Rao’s R=27.2, P<0.01, d.f.=9, 318; univariate F-tests: factor 1, F=34.3, P<0.01; factor 2, F=40.1, P<0.01; factor 3, F=3.9, P=0.01, d.f.=3, 133). Using univariate analysis, the first factor (eigenvalue 15.0; 35.7 % of variation explained) separates prey capture significantly from both other stages. The onset variables for the pre and main burst of all muscles except for the MPtlat show high loadings on the first factor and can thus be used to discriminate between prey capture and the other stages (see Table 5). For the second factor (eigenvalue 7.0; 16.6 % of variation explained), prey capture and swallowing are separated from intraoral transport. Only the onset of the post burst of the MAMESA as well as the duration of the post burst of the MPtlat and MDM show high loadings on this factor (Table 5). For the third factor (eigenvalue 3.5; 8.2 % of variation explained), the different stages are no longer separated.

Table 2.

Average onset and duration times and intensity-related variables of jaw and hyolingual muscle activity during transport

Average onset and duration times and intensity-related variables of jaw and hyolingual muscle activity during transport
Average onset and duration times and intensity-related variables of jaw and hyolingual muscle activity during transport
Table 3.

Average onset and duration times and intensity-related variables of jaw and hyolingual muscle activity during crushing

Average onset and duration times and intensity-related variables of jaw and hyolingual muscle activity during crushing
Average onset and duration times and intensity-related variables of jaw and hyolingual muscle activity during crushing
Table 4.

Average onset and duration times (ms) and intensity-related variables (%) of jaw and hyolingual muscle activity during swallowing

Average onset and duration times (ms) and intensity-related variables (%) of jaw and hyolingual muscle activity during swallowing
Average onset and duration times (ms) and intensity-related variables (%) of jaw and hyolingual muscle activity during swallowing
Table 5.

Results from the factor analysis: rotated factor matrix based on a timing-related (onset and duration variables) data set containing all bites from the first recording session

Results from the factor analysis: rotated factor matrix based on a timing-related (onset and duration variables) data set containing all bites from the first recording session
Results from the factor analysis: rotated factor matrix based on a timing-related (onset and duration variables) data set containing all bites from the first recording session

Using the intensity-related data (Tables 2–4) from both the first (all effects: Rao’s R=18.6, P<0.01, d.f. 9, 409; univariate F-tests: factor 1, F=9.6, P<0.01; factor 2, F=19.6, P<0.01; factor 3, F=16.2, P<0.01, d.f.=3, 170) and the second (all effects: Rao’s R=18.8, P<0.01, d.f.=12, 495; univariate F-tests: factor 1, F=10.7, P<0.01; factor 2, F=48.3, P<0.01; factor 3, F=2.3, P=0.05, d.f.=4, 189) recording sessions, four stages (including crushing) are significantly different from one another. For data from the first recording session, prey capture and swallowing are separated by the first factor (eigenvalue 11.7; 64.7 % of variation explained), whereas crushing is separated from all other stages by the second factor (eigenvalue 2.4; 13.4 % of variation explained) and transport cycles are separated from all other stages by the third factor (eigenvalue 1.1; 6.2 % of variation explained). Both the MPtlat and the MPtmed RL (=S×A) show high loadings on the first factor (Table 6). Since prey capture and swallowing are separated by the first factor, the difference between these two stages is mainly caused by the activity of the MPt. The recruitment levels of the MAMESA, MPsT and MAMP show high loadings on the second factor, thus indicating their importance in separating crushing from the other stages (Table 6). The jaw opener (MDM) RL value shows high loadings on the third factor and can therefore be considered to be useful in separating transport from the other stages.

Table 6.

Results from factor analysis: rotated factor matrix based on an intensity-related (sum, maximum and mean S×A values) data set containing all bites from the first recording session

Results from factor analysis: rotated factor matrix based on an intensity-related (sum, maximum and mean S×A values) data set containing all bites from the first recording session
Results from factor analysis: rotated factor matrix based on an intensity-related (sum, maximum and mean S×A values) data set containing all bites from the first recording session

Using the intensity-related data set from the second recording session, all stages differ significantly from one another. Prey capture is separated from other stages by the first factor (eigenvalue 11.6; 55.4 % of variation explained); all other stages (with the exception of prey capture with respect to crushing) are separated from each other by the second factor (eigenvalue 2.9; 14.2 % of variation explained) and crushing is separated from prey capture by the third factor (eigenvalue 1.4; 6.7 % of variation explained). The RL (=S×A) values of the tongue and hyoid protractors show high loadings (Table 7) on the first factor and are therefore important in separating prey capture from the other stages. The jaw opener and closer RL values show high loadings with the second factor and can thus be considered to be variables relevant to all stages. The RL value of the hyoid retractor (MSH) is the only variable with high loadings on the third factor and is thus important in the separation of prey capture from crushing.

Table 7.

Results from factor analysis: rotated factor matrix based on an intensity-related (sum, maximum and mean S×A values) data set containing all bites from the first recording session

Results from factor analysis: rotated factor matrix based on an intensity-related (sum, maximum and mean S×A values) data set containing all bites from the first recording session
Results from factor analysis: rotated factor matrix based on an intensity-related (sum, maximum and mean S×A values) data set containing all bites from the first recording session

Qualitative analysis

The generalised muscle activity patterns of the jaw and hyolingual muscles are described below in relation to the kinematics of the jaws and tongue reported previously (Herrel et al. 1996). Transport and crushing cycles are discussed together as intraoral transport as it has been shown above that these two stages differ mainly in the intensity of muscular contraction rather than in the muscular activation pattern (EMG onset and duration). On the basis of the kinematic data, a gape cycle can be subdivided into four distinct phases: the slow opening phase, SO; the fast opening phase, FO; the fast closing phase, FC; and the slow closing/power-stroke phase, SC/PS (Bramble and Wake, 1985). For a description of muscle activity patterns during prey capture, see Herrel et al. (1995).

Intraoral transport

During intraoral transport, a jaw cycle begins with the slow opening phase (SO). During this phase, activity of both the muscles of the tongue (MGGM, MGGL) and the hyoid protractors (MMH1, MMH2) is present. The MHG and the MRing are also active (Figs 2, 3; Tables 2, 3). All these muscles show a gradual increase in their activity which ends just before or a short time after maximal gape. At the end of the SO phase, some of the jaw closers show low-intensity activity (e.g. Fig. 3; during the third cycle, a distinct period of low-intensity activity is present in the MAMESA, MPtlat and MPtmed). This is the SOII phase. At the end of this phase, the jaw closers cease their activity and the jaw openers (MDM, MDMA) and the dorsal craniocervical muscles (MSCa) become maximally active, resulting in fast opening of the mouth (the FO phase). Prior to the FO phase, the hyoid retractors (MSH, MOH) become active and cause retraction of the hyoid apparatus. A burst of activity in the MHG also results in retraction of the tongue. At maximal gape, the jaw openers (MDM, MDMA) cease their activity. The jaw closers become active simultaneously at (MPsT, MAMP, MPtlat and MPtmed) or just after (MAMESA, MAMEM) maximal gape and cause fast closure of the mouth (the FC phase). After a short pause, the jaw closers become active again (Fig. 3), thus initiating the slow closing (SC) phase, sometimes accompanied by a power-stroke (PS) phase characterised by pronounced activity of the jaw closers. During this phase, the jaw openers often show low-intensity activity. The jaw openers and closers are always bilaterally simultaneously activated.

Fig. 2.

Summary of electromyographic activity in Agama stellio. Bars show mean onset and duration data from all analyzed feeding sequences. Different bursts in the same muscle within one cycle are referred to as pre, main and post bursts. The main burst is the first activity burst in which the muscles are fully active; this burst is often preceded by an activity burst of low intensity (pre) and followed by a burst of either high or low intensity (post). Narrow bars represent low-amplitude activity. Time is expressed relative to the time of maximal gape (=time 0). See Fig. 1 for definitions of muscle abbreviations.

Fig. 2.

Summary of electromyographic activity in Agama stellio. Bars show mean onset and duration data from all analyzed feeding sequences. Different bursts in the same muscle within one cycle are referred to as pre, main and post bursts. The main burst is the first activity burst in which the muscles are fully active; this burst is often preceded by an activity burst of low intensity (pre) and followed by a burst of either high or low intensity (post). Narrow bars represent low-amplitude activity. Time is expressed relative to the time of maximal gape (=time 0). See Fig. 1 for definitions of muscle abbreviations.

Fig. 3.

Representative electromyograms from the first recording session from an individual Agama stellio. Vertical lines indicate time of maximal gape. C, crushing; T, transport. See Fig. 1 for definitions of muscle abbreviations.

Fig. 3.

Representative electromyograms from the first recording session from an individual Agama stellio. Vertical lines indicate time of maximal gape. C, crushing; T, transport. See Fig. 1 for definitions of muscle abbreviations.

The muscular activation pattern described here is basically the same for both transport and crushing cycles. The major differences between these two stages are related to the intensity of muscular contractions in both the jaw openers and closers (Fig. 3). Although there were slight differences observed in onset and/or duration times between transport and crushing cycles (e.g. MAMESA in Fig. 3), on average they were not significantly different (see above). Within transport and/or crushing stages, there is also a substantial amount of variation between cycles present in the timing (e.g. onset and duration of the MAMESA, Fig. 3) and intensity (e.g. the MAMP, MPtlat, MPsT and MSCa, Fig. 3) of the muscular activity (Tables 2, 3). This presumably results from changes in the position of the prey within the oral cavity, as well as from changes in the degree of reduction of the prey during the intraoral transport stage.

Swallowing

During swallowing (Figs 2, 4; Table 4), the prey is transported from within the oral cavity to the pharynx. The associated EMGs are quite distinct from those of intraoral transport. Swallowing is characterised by a shorter FO phase, a much lower maximal gape value and the absence of an SC/PS phase (see Herrel et al. 1996); activity differences occur mainly in the jaw muscle activity patterns. As during intraoral transport, a cycle is initiated by pronounced activity of the tongue protractors (MGGM, MGGL). The hyoid protractors (MMH1, MMH2) then become active, but at a lower amplitude than during intraoral transport. Activity in the MHG and the MRing persists during swallowing. Nevertheless, differences in relative timing of the onset of activity are present (see Table 4). At the end of the SO phase, the MDM becomes active and the FO phase is initiated. Activity in the MDM is, as during intraoral transport, accompanied by activity in the MSCa. However, during late swallowing, the activity in the MDM and the MSCa may be absent. At maximal gape, the jaw opener muscles (MDM, MSCa) become silent and the jaw closers (MAMEP, MAMP, MPtlat, MPtmed) become active. However, in contrast to intraoral transport, only the deeper parts of the MAME, the MAMP and the MPt remain active during swallowing. The first muscles to cease their activity during swallowing are the MAMESA, MAMEM and MPsT (see Table 4, burst presence). Just before maximal gape, the hyoid retractor (MSH) becomes active and, in combination with the activity of the MHG, causes retraction of the hyolingual apparatus.

Fig. 4.

Representative electromyograms from the second recording session using an individual Agama stellio. Vertical lines indicate times of maximal gape. All records are for swallowing cycles (S). See Fig. 1 for definitions of muscle abbreviations.

Fig. 4.

Representative electromyograms from the second recording session using an individual Agama stellio. Vertical lines indicate times of maximal gape. All records are for swallowing cycles (S). See Fig. 1 for definitions of muscle abbreviations.

During swallowing, a substantial amount of variation was found (see Fig. 5; Table 4) in the intensity, onset and duration of the muscle activity. Differences observed during swallowing are generally less pronounced than during intraoral transport and are presumably related to the position of the prey with respect to the tongue.

Fig. 5.

Recruitment levels (S×A values, where S is the number of spikes and A is the average spike amplitude) of sequential bite cycles for three feeding sequences from the first recording session. The variability both within and between feeding sequences is clearly illustrated. MDM, m. depressor mandibulae; MPsT, m. pseudotemporalis.

Fig. 5.

Recruitment levels (S×A values, where S is the number of spikes and A is the average spike amplitude) of sequential bite cycles for three feeding sequences from the first recording session. The variability both within and between feeding sequences is clearly illustrated. MDM, m. depressor mandibulae; MPsT, m. pseudotemporalis.

Roles of jaw and hyolingual musculature

Despite the complexity of the squamate jaw musculature, muscle activity patterns are remarkably similar (all muscles becoming active approximately simultaneously and during the same kinematic phases) for all jaw closers (MAMESA, MAMESP, MAMEM, MAMEP, MPsTS, MPsTP, MAMP, MPtlat and MPtmed) during feeding in A. stellio. All jaw closers exhibited activity during one or more of three periods: during the second part of the SO phase of prey capture and intraoral transport, during the FC phase of prey capture, intraoral transport and swallowing, and during the SC/PS phase of prey capture and intraoral transport. However, in A. stellio, the jaw closers fulfil only one functional role: the closing of the jaws. Similarly, in Trachydosaurus rugosus (Gans et al. 1985), the jaw closers (MAME, MPsT and MPt) are also active simultaneously and can be considered to be true jaw closers. In Uromastix aegyptius (Throckmorton, 1978), however, the activity patterns of the superficial and deep portions of the MPt are different: activity in the superficial part occurs during jaw closing (simultaneously with activity of the MAME), while the deep part is active during jaw opening. Hence, the two parts are assumed to have different functions: jaw elevation for the superficial part and jaw protraction for the deep part. This functional subdivision of the activity of the MPt is related to the kinetic nature of the skull in U. aegyptius (Throckmorton, 1976, 1978). Another characteristic of jaw muscle activity patterns in A. stellio is the simultaneous activation of both sides in all muscles, suggesting a fairly simple motor pattern. While this is also observed in T. rugosus (Gans et al. 1985), in Varanus exanthematicus (Smith, 1982) temporal differentiation and even unilateral muscle activity may be present in the jaw adductors (MAME, MPsT, MPt).

Some differences in activity patterns of the jaw muscles of A. stellio were observed. In general, all deep muscles (MAMEP, MAMP) and also the MPt continue their activity into the later parts of the feeding sequence, whereas the more superficial muscles (MAMES, MAMEM, MPsT) tend to cease their activity much earlier. A similar observation was made in Caiman crocodilus (Cleuren, 1996). In Alligator mississippiensis (Sato et al. 1992), it has been shown that the muscles (MAMEP, MAMP, MPsT) which remain active throughout the feeding sequence in C. crocodilus are primarily composed of red muscle fibres. Although no quantitative data on the muscle fibre composition are available for A. stellio, it is proposed that the different muscle activity patterns in this lizard may be due to similar differences in fibre composition (more red, aerobic muscle fibres in the deeper parts) of the different jaw adductors.

On the basis of tongue morphology and observations of tongue movements during feeding, several roles have been suggested for the hyolingual musculature (see Table 1 in Delheusy et al. 1994, for an overview). The hyolingual muscles in A. stellio can be subdivided into four basic groups: the tongue protractors (MGGL and MGGM), the hyoid protractors (MMH1 and MMH2), the hyoid retractors (MOH and MSH) and the m. hyoglossus (MHG). The MHG, which is active during both tongue protraction and retraction, can only function as a tongue retractor when working together with the hyoid retractors. During tongue protraction (activity in the MGG), activity in the MHG will cause shortening of the tongue. The combination of tongue protraction and tongue shortening causes the tongue to bulge, thus pushing it against the prey item. A similar function of the MHG during tongue protraction is found in Anolis equestris (J. Cleuren and F. De Vree, personal communication). Remarkably, the tongue and hyoid protractors are nearly always simultaneously active during all feeding stages, although the anatomical relationships of the tongue and hyoid indicate no obligatory correlation between tongue and hyoid movements (Smith, 1984).

Not only the extrinsic musculature (i.e. those muscles originating on the mandible or the hyoid and inserting on the tongue) but also the intrinsic tongue muscles (those muscles with their origin and insertion on the tongue) play an important role during feeding in A. stellio. Of the intrinsic muscles, activity could be recorded from only one, the MRing. Activity of the MRing resulting in whole-tongue movement occurs both during prey capture (Herrel et al. 1995) and during the other feeding stages. Thus, in A. stellio, two of the three mechanisms of tongue movement (tongue protraction by the MGG and whole-tongue movements caused by the sliding of the tongue on the entoglossal process and due to the activity of the MRing) proposed for lizards (Smith, 1984, 1988) are observed during feeding.

In summary, it can be stated that in A. stellio both jaw and hyolingual muscles are essential during all stages of a feeding sequence. During feeding, the jaw and hyolingual apparatus are integrated to form one functional feeding unit in which both components perform a specific role.

Relationships among feeding stages

Although we have shown that the jaw and hyolingual muscles perform similar tasks during all stages of feeding, quantitative EMG data for these muscles can be used to discriminate between the different feeding stages, depending on the type of data examined. Whereas prey capture, intraoral transport and swallowing can be separated irrespective of the type of data (kinematic, EMG) used, crushing and transport are only separable using intensity-related EMG data. Among lizards, only in Chamaeleo jacksonii has a separation of crushing and transport stages been demonstrated using kinematic data (So et al. 1992). However, in all other studies in which multivariate analyses were performed on kinematic data, no discrimination between crushing and transport stages was possible (Kraklau, 1991; Delheusy and Bels, 1992; Urbani and Bels, 1995; Herrel et al. 1996). So et al. (1992) state that: ‘chewing and transport behaviours may represent two extremes of a continuum rather than entirely distinct activities’. For all squamates examined, therefore, transport and crushing (chewing of So et al. 1992) are apparently closely related. Prey capture and swallowing are also kinematically similar in most species examined (Delheusy and Bels, 1992; Urbani and Bels, 1995). However, in A. stellio, prey capture, intraoral transport and swallowing seem to be distinct stages.

Quantitative electromyographic data for the whole feeding sequence are available for Caiman crocodilus (Cleuren, 1996).

In this crocodilian reptile, prey capture, transport, crushing, repositioning and swallowing stages are separable in multivariate space and significantly different on the basis of time-related EMG data. Hence, in Caiman crocodilus (Cleuren and De Vree, 1992; Cleuren, 1996), crushing can also be considered to be a distinct stage, clearly different from transport. However, the type of prey transport is completely different between the lizard A. stellio (lingual transport) and the crocodilian C. crocodilus (inertial transport), which may account for this difference. It is therefore likely that crushing cycles in other inertial feeders such as Varanus exanthematicus would also be separated from transport cycles (see Smith, 1982). As inertial transport mechanisms are considered to be derived (Bels et al. 1994) in lower tetrapods, the ancestral mechanism of prey crushing presumably involved modulation of the transport cycle (mainly in the intensity of muscle contraction) when needed. Evolution from a basic transport cycle into capture and/or swallowing cycles, whereby transitional stages would include modulations of the intensity as well as the onset of muscular activity, seems plausible.

It has been suggested that feeding cycles might be driven by simple motor pattern generators. According to Ewert et al. (1994), a motor pattern can be considered as the spatiotemporal pattern of excitation and inhibition in motoneurones necessary to activate and coordinate the muscle contractions. Can we determine, from our new EMG results for A. stellio, whether the different functional stages recognised are generated by different motor patterns? The separation of prey capture, swallowing and intraoral transport stages on the basis of both time-and intensity-related data suggests that different motor patterns are indeed used. However, as noted above, this observation might not apply to the distinction between transport and crushing as these cycle types are only separable using differences in intensity of the muscular activation.

Davis and Kovac (1981) and Rossignol et al. (1988) noted that sensory (proprioceptive) feedback will play a role in the coordination and maintenance of a motor pattern and, therefore, that the observed muscle activity patterns differ between feeding stages. This was also found in A. stellio in the recruitment levels of the jaw and hyolingual muscles during feeding. The recruitment levels of these muscle groups differ not only between feeding sequences and stages, but also within stages (bite-to-bite differences, see Fig. 5). It is possible that, during the SO phase of intraoral transport cycles (see Herrel et al. 1996), information regarding the food type, degree of reduction and/or food position is fed back to the control system. One should therefore be cautious in attributing the observed differences between cycles to separate motor patterns.

Evolutionary implications

Similarities in jaw muscle activity patterns between A. stellio and other lepidosaurian reptiles from such groups as diverse as the Rhynchocephalia (Sphenodon punctatus; Gorniak et al. 1982), Scincidae (Trachydosaurus rugosus; Gans et al. 1985), Agamidae (Uromastix aegyptius; Throckmorton, 1978) and Varanidae (Varanus sp.; Smith, 1982) suggest a common basic muscular activation pattern (see Bramble and Wake, 1985). Key elements in this basic pattern are the activation of the jaw opener (MDM) and dorsal cervical muscles (MSCa) during the FO phase and bilaterally simultaneous activation of both external (MAMESA, MAMESP, MAMEM, MAMEP, MAMP) and internal (MPsTS, MPsTP, MPtlat, MPtmed) adductors during the FC and SC/PS phases. Within the different lepidosaurian groups, this basic pattern differs in relation to specialisations of the feeding apparatus (e.g. specialisations for inertial feeding in Varanus exanthematicus, a kinetic skull in U. aegyptius, a unique shearing mechanism in S. punctatus and adaptations to durophagy in T. rugosus).

As noted above, both the jaw and the hyolingual apparatus play crucial roles during feeding in lizards. Functional similarities in the hyolingual musculature within lizards are common. The muscle activation patterns seen in A. stellio do not diverge greatly from the results for other lizards (Smith, 1984, 1986) or the activity patterns suggested for the primitive mode of food transport and reduction (Bels et al. 1994). There are even a number of similarities present between lizards and mammals in the movements of the hyolingual apparatus and the coordination of the jaw and hyolingual systems (see Smith, 1984). On the basis of these similarities, a basic vertebrate pattern of tongue function has been proposed (Hiiemae et al. 1979; Bramble, 1980). However, as noted by Smith (1984), these similarities may also be due to convergence or to the retention of a primitive pattern. Our data do not allow further speculation on this topic, but do suggest the presence of a basic lepidosaurian pattern of tongue function as proposed by Bels et al. (1994). Again, specialisations of the hyolingual apparatus related to vomerolfaction as in Varanus sp. (Smith, 1986), social display as in Anolis carolinensis and A. equestris (Bels, 1990; Font and Rome, 1990) or ballistic prey capture as in chameleons (Wainwright and Bennett, 1992a) might cause deviations from this basic pattern.

Before any firmer conclusions can be drawn regarding the evolutionary transformation of the jaw and hyolingual systems, more data regarding the jaw and hyolingual motor patterns and, especially their control mechanisms in lepidosaurian reptiles, are needed.

We thank Dr R. Van Damme for help with the statistical analysis, Dr P. Aerts and B. Vanhooydonck for comments on an earlier version of the manuscript, two anonymous reviewers for helpful discussions and critical comments on the manuscript, Dr E. Kochva for providing us with the first specimens of A. stellio and Mrs J. Fret for technical assistance. This study was supported by IWT grant 943039 to A.H. and FKFO grant G.0221.96 to F.D.V.

Basmajian
,
J. V.
and
De Luca
,
C. J.
(
1985
).
Muscles Alive: Their Functions Revealed by Electromyography.
Baltimore
:
Williams and Wilkins. 561pp
.
Beach
,
J.
,
Gorniak
,
G. C.
and
Gans
,
C.
(
1982
).
A method for quantifying electromyograms
.
J. Biomech.
15
,
611
617
.
Bels
,
V. L.
(
1990
).
The mechanism of dewlap extension in Anolis carolinensis (Reptilia; Iguanidae) with histological analysis of the hyoid apparatus
.
J. Morph.
206
,
225
244
.
Bels
,
V. L.
,
Chardon
,
M.
and
Kardong
,
K. V.
(
1994
).
Biomechanics of the hyolingual system in Squamata
. In
Advances in Comparative and Environmental Physiology
, vol.
18
(ed.
V. L.
Bels
,
M.
Chardon
and
P.
Vandewalle
), pp.
197
240
.
Berlin
:
Springer
.
Bock
,
W. J.
and
Shear
,
C. R.
(
1972
).
A staining method for gross dissection
.
Anat. Anz
.
130
,
222
227
.
Bramble
,
D.
(
1980
).
Feeding in tortoises and mammals: why so similar?
Am. Zool.
20
,
931
.
Bramble
,
D.
and
Wake
,
D. B.
(
1985
).
Feeding mechanisms of lower tetrapods
. In
Functional Vertebrate Morphology
(ed.
M.
Hildebrand
,
D.
Bramble
,
K.
Liem
and
D.
Wake
), pp.
230
261
. Cambridge MA: Harvard University Press.
Cleuren
,
J.
(
1996
).
Functionele morfologie van het craniocervicaal en hyolinguaal apparaat van Caiman crocodilus tijdens de inertiële voedselopname. PhD thesis. University of Antwerp, Belgium
.
Cleuren
,
J.
and
De Vree
,
F.
(
1992
).
Kinematics of the jaw and hyolingual apparatus during feeding in Caiman crocodilus
.
J. Morph.
212
,
141
154
.
Davis
,
W. J.
and
Kovac
,
M. P.
(
1981
).
The command neuron and the organisation of movement
.
Trends Neurosci.
4
,
73
76
.
Delheusy
,
V.
and
Bels
,
V. L.
(
1992
).
Kinematics of feeding behaviour in Oplurus cuvieri (Reptilia: Iguanidae)
.
J. exp. Biol.
170
,
155
186
.
Delheusy
,
V.
,
Toubeau
,
G.
and
Bels
,
V. L.
(
1994
).
Tongue structure and function in Oplurus cuvieri
.
Anat. Rec.
238
,
263
276
.
Dellow
,
P. G.
(
1976
).
The general physiological background of chewing and swallowing
. In
Mastication and Swallowing: Biological and Clinical Correlates
(ed.
B. J.
Sessle
and
A. G.
Hannam
), pp.
6
9
. Toronto: University of Toronto Press.
El Toubi
,
M. R.
(
1947
).
Some observations on the osteology of the lizard, Agama stellio
.
J. Morph.
81
,
135
149
.
Ewert
,
J.-P.
,
Beneke
,
T. W.
,
Schurg-Pfeiffer
,
E.
,
Schwippert
,
W. W.
and
Weerasuriya
,
A.
(
1994
).
Sensorimotor processes that underlie feeding behaviour in tetrapods
. In
Advances in Comparative and Environmental Physiology
, vol.
18
(ed.
V. L.
Bels
,
M.
Chardon
and
P.
Vandewalle
), pp.
119
162
.
Berlin
:
Springer
.
Font
,
E.
and
Rome
,
L. C.
(
1990
).
Functional morphology of dewlap extension in the lizard Anolis equestris (Iguanidae)
.
J. Morph
.
206
,
245
258
.
Gandolfi
,
H.
(
1908
).
Die Zunge der Agamidae und Iguanidae
.
Zool. Anz.
32
,
569
580
.
Gans
,
C.
and
De Vree
,
F.
(
1986
).
Shingle-back lizards crush snail shells using temporal summation (tetanus) to increase the force of the adductor muscles
.
Experientia
42
,
387
389
.
Gans
,
C.
,
De Vree
,
F.
and
Carrier
,
D.
(
1985
).
Usage pattern of the complex masticatory muscles in the shingleback lizard, Trachydosaurus rugosus: a model for muscle placement
.
Am. J. Anat.
173
,
219
240
.
Gnanamuthu
,
C. P.
(
1937
).
Comparative study of the hyoid and tongue of some typical genera of reptiles
.
Proc. zool. Soc., Lond. B
107
,
1
63
.
Gomes
,
N. M. B.
(
1974
).
Anatomie comparée de la musculature trigéminale des lacertiliens
.
Mem. Mus. nat. Hist. nat., Paris A
90
,
1
107
.
Gorniak
,
G. C.
,
Rosenberg
,
H. I.
and
Gans
,
C.
(
1982
).
Mastication in the tuatara, Sphenodon punctatus (Reptilia: Rhynchocephalia), structure and activity of the motor system
.
J. Morph.
171
,
321
353
.
Haas
,
G.
(
1973
).
Muscles of the jaws and associated structures in the Rhynchocephalia and Squamata
. In
Biology of the Reptilia
, vol.
4
(ed.
C.
Gans
and
T.
Parsons
), pp.
285
490
.
London
:
Academic Press
.
Herrel
,
A.
,
Cleuren
,
J.
and
De Vree
,
F.
(
1995
).
Prey capture in the lizard Agama stellio
.
J. Morph.
224
,
313
329
.
Herrel
,
A.
,
Cleuren
,
J.
and
De Vree
,
F.
(
1996
).
Kinematics of feeding in the lizard Agama stellio
.
J. exp. Biol.
199
,
1727
1742
.
Hiiemae
,
K. M. A. J.
and
Crompton
,
A. W.
(
1979
).
Intra-oral food transport: the fundamental mechanism of feeding
. In
Muscle Adaptation in the Cranio-facial Region
(ed.
D. S.
Carlson
and
J. A.
Mcnamara
), pp.
181
208
. Ann Arbor: University of Michigan.
Jollie
,
M. T.
(
1960
).
The head skeleton of the lizard
.
Acta zool.
41
,
1
64
.
Kraklau
,
D. M.
(
1991
).
Kinematics of prey capture and chewing in the lizard Agama agama
.
J. Morph.
210
,
195
212
.
Loeb
,
G. E.
and
Gans
,
C.
(
1986
).
Electromyography for Experimentalists.
Chicago
:
The University of Chicago Press
.
373pp
.
Rossignol
,
S.
,
Lund
,
J. P.
and
Drew
,
T.
(
1988
).
The role of sensory inputs in regulating patterns of rhythmical movements in higher vertebrates
. In
Neural Control of Rhythmic Movements in Vertebrates
(ed.
A. V.
Cohen
,
S.
Rossignol
and
S.
Grillner
), pp.
201
283
.
New York
:
Wiley
.
Sato
,
I.
,
Shimada
,
K.
,
Sato
,
T.
and
Kitagawa
,
T.
(
1992
).
Histochemical study of jaw muscle fibres in the American alligator (Alligator mississippiensis)
.
J. Morph.
211
,
187
199
.
Smith
,
K. K.
(
1982
).
An electromyographic study of the function of the jaw adducting muscles in Varanus exanthemathicus
.
J. Morph.
173
,
137
158
.
Smith
,
K. K.
(
1984
).
The use of the tongue and hyoid apparatus during feeding in lizards (Ctenosaura similis and Tupinambis nigropunctatus)
.
J. Zool. (Lond.)
202
,
115
143
.
Smith
,
K. K.
(
1986
).
Morphology and function of the tongue and hyoid apparatus in Varanus (Varanidae, Lacertilia)
.
J. Morph.
187
,
261
287
.
Smith
,
K. K.
(
1988
).
Form and function of the tongue in agamid lizards with comments on its phylogenetic significance
.
J. Morph.
196
,
157
171
.
So
,
K. K. J.
,
Wainwright
,
P. C.
and
Bennett
,
A. F.
(
1992
).
Kinematics of prey processing in Chamaeleo jacksonii: conservation of function with morphological specialisation
.
J. Zool., Lond.
202
,
115
143
.
Thexton
,
A. J.
(
1974
).
Oral reflexes and neural oscillators
.
J. Dent.
2
,
137
141
.
Thexton
,
A. J.
(
1976
).
To what extent is mastication programmed and independent of peripheral feedback? In Mastication
(ed.
D. J.
Anderson
and
B.
Matthews
), pp.
213
224
. Bristol: John Wright.
Throckmorton
,
G. S.
(
1976
).
Oral food processing in two herbivorous lizards, Iguana iguana (Iguanidae) and Uromastix aegyptius (Agamidae)
.
J. Morph.
148
,
363
390
.
Throckmorton
,
G. S.
(
1978
).
Action of the pterygoideus muscle during feeding in the lizard Uromastix aegyptius (Agamidae)
.
Anat. Rec.
190
,
217
222
.
Urbani
,
J. M.
and
Bels
,
V. L.
(
1995
).
Feeding behaviour in two scleroglossan lizards: Lacerta viridis (Lacertidae) and Zonosaurus laticaudatus (Cordylidae)
.
J. Zool., Lond.
236
,
265
290
.
Wainwright
,
P. C.
and
Bennett
,
A. F.
(
1992a
).
The mechanism of tongue projection in chameleons. I. Electromyographic tests of functional hypotheses
.
J. exp. Biol.
168
,
1
21
.
Wainwright
,
P. C.
and
Bennett
,
A. F.
(
1992b
).
The mechanism of tongue projection in chameleons. II. Role of shape change in a muscular hydrostat
.
J. exp. Biol.
168
,
23
40
.