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

Abstract

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

Comparative functional analysis of the hyolingual anatomy in lacertid lizards

“…The heads of one (P. douglassi, G. gecko), two (P. stellio), or three (C. jacksonii) specimens of each species were prepared for paraffin histology using standard techniques (Humason, 1979). Serial 10 m sections (both cross-sectional and sagittal for P. stellio; cross-sectional, sagittal, and frontal for C. jacksonii; cross-sectional only for other species) were made and colored using an improved trichrome stain (see also Herrel et al, 1998Herrel et al, , 2001). …”

“…Although little or no quantitative data are available, there appears to be a dominance of the tongue protractors and retractors over the hyobranchial muscles in iguanian lizards (see Smith, 1988;Herrel et al, 1998). On the other hand, lacertid lizards also appear to be quite noticeably different from highly specialized lizards such as varanids (Smith, 1986), snakes (Smith and Mackay, 1990), and chameleons (Herrel et al, 2001), where the tongue is highly specialized for chemoreception (varanids and snakes) and prey capture (chameleons).…”

“…The most striking difference lies in the origin of the musculus mandibulohyoideus 2. Whereas this muscle originates tendinously at the jaw symphysis in iguanians (Avery and Tanner, 1971;Smith, 1988;Delheusy et al, 1994;Herrel et al, 1998;Meyers and Nishikawa 2000;Meyers et al, 2002) and derived lizards such as helodermatids and varanids (McDowell, 1972;Smith, 1986), it does not originate at the mandibular symphysis in lacertid lizards. Rather, it originates at the mesial side of the mandible, about one-third down its length away from the symphysis (Fig.…”

“…Having a large fleshy tongue is critically important as the adhesive forces that keep the prey attached to the tongue are largely surface-dependent (Emerson and Diehl, 1980;Herrel et al, 2000;Schwenk, 2000). Additionally, iguanians have well-developed tongue proand retractor muscles (m. genioglossus and m. hyoglossus) and a complex papillary morphology characterized by the presence of plumose or cylindrical papillae (see Smith, 1984Smith, , 1988Rabinowitz and Tandler, 1986;Herrel et al, 1998;Schwenk, 2000).…”

“…Although tongue structure and function have been investigated in some detail in Iguanians and the highly derived varanid lizards (e.g., Smith, 1984Smith, , 1986Herrel et al, 1998; for an overview, see Schwenk, 2000), information is generally lacking for phylogentically and functionally intermediate groups such as scincomorphs. Yet scincomorphs such as lacertid lizards are especially intriguing animals because they rely heavily on the tongue for both food transport (Goosse and Bels, 1992a;Urbani and Bels, 1995) and chemoreception (Goosse and Bels, 1992b), thus combining two (at first sight) very different functions.…”