Morphology and fibre-type distribution in the tongue of the Pogona vitticeps lizard (Iguania, Agamidae)

Abstract

Agamid lizards use tongue prehension for capturing all types of prey. The purpose of this study was to investigate the functional relationship between tongue structure, both surface and musculature, and function during prey capture in Pogona vitticeps. The lack of a detailed description of the distribution of fibre-types in the tongue muscles in some iguanian lizards has hindered the understanding of the functional morphology of the lizard tongue. Three methodological approaches were used to fill this gap. First, morphological analyses were performed (i) on the tongue surface through scanning electron microscopy, and (ii) on the lingual muscle by histological coloration and histochemistry to identify fibre-typing. Secondly, kinematics of prey capture was quantified by using high-speed video recordings to determine the movement capabilities of the tongue. Finally, electromyography (EMG) was used to identify the motor pattern tongue muscles during prey capture. Morphological and functional data were combined to discuss the functional morphology of the tongue in agamid lizards, in relation to their diet. During tongue protraction, M. genioglossus contracts 420 ± 96 ms before tongue-prey contact. Subsequently, Mm. verticalis and hyoglossus contract throughout tongue protraction and retraction. Significant differences are found between the timing of activity of the protractor muscles between omnivorous agamids (Pogona sp., this study) and insectivorous species (Agama sp.), despite similar tongue and jaw kinematics. The data confirm that specialisation toward a diet which includes more vegetal materials is associated with significant changes in tongue morphology and function. Histoenzymology demonstrates that protractor and retractor muscles differ in fibre composition. The proportion of fast glycolytic fibres is significantly higher in the M. hyoglossus (retractor muscle) than in the M. genioglossus (protractor muscle), and this difference is proposed to be associated with differences in the velocity of tongue protrusion and retraction (5 ± 5 and 40 ± 13 cm s(-1) , respectively), similar to Chamaeleonidae. This study provides a way to compare fibre-types and composition in all iguanian and scleroglossan lizards that use tongue prehension to catch prey.

Keywords: Agamidae; capture; electromyography; fibre typing; muscle; tongue.

Fig. 1

Scanning electron micrographs of the tongue tip, foretongue and hindtongue in Pogona vitticeps. (A) Schematic illustration of the tongue showing the subdivision into three regions. 1: tongue tip, 2: foretongue and 3: hindtongue. The tongue tip (B) presents cylindriform papillae in this posterior area. Note the minor bifurcation (arrow) of the tongue (B) and the presence of numerous elevated plumose papillae (pl) in the foretongue (C) and less developed papillae in the hindtongue (D).

Fig. 2

A MRI transverse plane view of Pogona vitticeps head showing the large occupation of the tongue in the oral cavity. E, eye; Ep, entoglossal process; Gl, M. genioglossus lateralis; Gm, M. genioglossus medialis; H, M. hyoglossus; V, M. verticalis.

Fig. 3

(A) Parasagittal section through the lower jaw and the tongue of Pogona vitticeps showing the intrinsic and extrinsic muscles and elements of hyoid. Ep: entoglossal process; F, frenulum; Gl, M. genioglossus lateralis; Gm, M. genioglossus medialis; H, M. hyoglossus; L, M. lateralis; Md, mandible; T, M. transversalis; V, M. verticalis. (B) Tubular mucous-secreting glands (M) are concentrated at the hindtongue. (C) Serous-secreting glands (S) are located exclusively in the foretongue.

Fig. 4

Histochemical labelling on serial sections of the M. hyoglossus in Pogona vitticeps stained for the activities of (A) succinate dehydrogenase activity (SDH) and (B) a combination of histochemical reactions (see Material and methods). SO, slow oxidative fibres; FOG, fast oxidative-glycolytic fibres and FG, fast glycolytic fibres.

Fig. 5

Boxplots showing the percentage of different fibre types in the Mm. hyoglossus (A), genioglossus (B) and verticalis (C). Box plot values consist of the median (line), first and third quartiles (upper and lower edges of box). *Significant difference (P < 0.05). SO, slow oxidative fibres; FOG, fast oxidative-glycolytic fibres and FG, fast glycolytic fibres. n = 4.

Fig. 6

Right hyoglossus muscle of Pogona vitticeps stained in order to detect succinate dehydrogenase activity. The start is located in the dorsal region rich in FG fibres. By contrast, FOG and SO fibres dominate in the lower and lateral parts of the ring muscle.

Fig. 7

Boxplots showing the percentage of slow oxidative fibres (A), fast oxidative-glycolytic fibres (B) and fast glycolytic fibres (C) in the Mm. hyoglossus, genioglossus and verticalis. Box plot values consist of the median (line), first and third quartiles (upper and lower edges of box). *Significant difference (P < 0.05). n = 4.

Fig. 8

Time course of EMG activity in the Mm. depressor mandibulae, hyoglossus, genioglossus and verticalis during prey capture. Onset and offset of EMG activity are calculated with respect to the tongue–prey contact (time = 0 ms) and expressed in mean ± SE.