THE ANATOMICAL RECORD PART A 284A:561–573 (2005)

Comparative Functional Analysis of the Hyolingual Anatomy in Lacertid Lizards

ANTHONY HERREL,1* MEDIHA CANBEK,2 U¨ NAL O¨ ZELMAS,3 2 3 MUSTAFA UYANOG˘ LU, AND MUHARREM KARAKAYA 1Biology Department, University of Antwerp, Antwerp, Belgium 2General Biology Department, Histology, Osmangazi University, Eskis¸ehir, Turkey 3Zoology Department, Osmangazi University, Eskis¸ehir, Turkey

ABSTRACT The tongue is often considered a key innovation in the evolution of a terrestrial lifestyle as it allows animals to transport food items through the oral cavity in air, a medium with low density and viscosity. The tongue has been secondarily coopted for a wide diversity of functions, including prey capture, drinking, breathing, and defensive behaviors. Within basal lizard groups, the tongue is used primarily for the purpose of prey capture and transport. In more derived groups, however, the tongue appears specialized for chemoreceptive purposes. Here we examine the tongue structure and morphology in lacertid lizards, a group of lizards where the tongue is critical to both food transport and chemoreception. Because of the different me- chanical demands imposed by these different functions, regional morpho- logical specializations of the tongue are expected. All species of lacertid lizards examined here have relatively light tongue muscles, but a well developed hyobranchial musculature that may assist during food transport. The intrinsic musculature, including verticalis, transversalis, and longitu- dinalis groups, is well developed and may cause the tongue elongation and retraction observed during chemoreception and drinking. The papillary morphology is complex and shows clear differences between the tongue tips and anterior fore-tongue, and the more posterior parts of the tongue. Our data show a subdivision between the fore- and hind-tongue in both papillary structure and muscular anatomy likely allowing these animals to use their tongues effectively during both chemoreception and prey transport. More- over, our data suggest the importance of hyobranchium movements during prey transport in lacertid lizards. © 2005 Wiley-Liss, Inc.

Key words: tongue; hyobranchium; musculature; feeding; che- moreception; Lacertidae

The tongue is often considered a key innovation in the conditions in which animals use their tongues or the hyo- evolution of a terrestrial lifestyle as it allows animals to branchial system (i.e., water vs. air; see Iwasaki, 2002). transport food items through the oral cavity in a me- dium with low density and viscosity such as air (Iwasaki, 2002). Secondarily, the tongue and hyo- branchial system has been coopted for a wide diversity *Correspondence to: Anthony Herrel, Biology Department, of functions such as prey capture, drinking, breathing, University of Antwerp, Universiteitsplein 1, B-2610 Antwerpen, and defensive behaviors (e.g., see Bels et al., 1994; Belgium. Fax: ϩ32-38202271. E-mail: [email protected] Schwenk, 1995). Moreover, there are fairly strong cor- Received 17 May 2004; Accepted 17 January 2005 relations between tongue anatomy, its functional roles DOI 10.1002/ar.a.20195 (e.g., food transport and manipulation; see McClung and Published online 5 May 2005 in Wiley InterScience Goldberg, 2000; Schwenk, 2000), and the environmental (www.interscience.wiley.com).

© 2005 WILEY-LISS, INC. 562 HERREL ET AL. Lizards are an especially interesting group to investi- Here we test whether the tongue of lacertid lizards is gate tongue function and morphology in, as the tongue is indeed functionally adapted to the different mechanical specialized for different functions in different clades (see demands imposed by chemoreception and prey transport. Cooper, 1995a; Schwenk, 2000). Whereas among basal Specifically, we expect a broad fleshy tongue with promi- lizard groups (Iguania), the tongue is used primarily for nent papillary structure and well-developed tongue pro- prey capture and transport (Cooper, 1994; Schwenk, and retractors to allow for effective prey transport (Smith, 2000), in more derived groups (Scleroglossa) the tongue 1988; Schwenk, 2000). However, we also expect well-de- appears specialized for chemoreceptive purposes (Cooper, veloped intrinsic tongue muscles that can cause the ob- 1995a; Schwenk, 2000). As the mechanical demands asso- served elongation of the tongue during chemorecptive ciated with these two behaviors are radically different, tongue extrusions (Kier and Smith, 1985) and smooth functional differences in tongue structure are expected scale-like papillae that facilitate smooth passage of the and observed between the two groups. Iguanians typically tongue along the largely closed jaws during tongue flick- have broad fleshy tongues that are moved within, or pro- ing (see also Goosse and Bels, 1992b). Because these mor- truded out of, the oral cavity during prey transport and phological specializations are incompatible, we expect re- capture, respectively. Having a large fleshy tongue is crit- gional differences in the anatomy of the tongue in lacertid ically important as the adhesive forces that keep the prey lizards with the fore-tongue being specialized for chemo- attached to the tongue are largely surface-dependent (Em- reception and the hind-tongue for prey transport. erson and Diehl, 1980; Herrel et al., 2000; Schwenk, 2000). Additionally, iguanians have well-developed tongue pro- MATERIALS AND METHODS and retractor muscles (m. genioglossus and m. hyoglossus) Gross Dissections and a complex papillary morphology characterized by the The tongue and hyobranchial system was dissected in presence of plumose or cylindrical papillae (see Smith, preserved adult specimens of the following species of lac- 1984, 1988; Rabinowitz and Tandler, 1986; Herrel et al., ertid lizards: Podarcis atrata (two), Gallotia galloti 1998; Schwenk, 2000). (three), Lacerta bedriagae (three), and Latastia longicau- Scleroglossans, on the other hand, generally have nar- data (three). All specimens were measured (snout-vent rower, bifid, and elongated tongues that are extended out length, head length, head width, head height, lower jaw of the oral cavity only during tongue flicking and drinking length as in Herrel et al., 1999a) before dissection using (Bels et al., 1993; Toubeau et al., 1994; Cooper, 1995a, digital calipers (Mitutoyo CD20 DC, Sakato, Japan). Mus- 1995b, 1997; Schwenk, 1995). As sampling a large volume cle masses and the mass of the tongue after dissection of air is important during tongue flicking (Gove, 1979; were determined to the nearest 0.01 mg using an elec- Schwenk, 1995), the extensibility and mobility of the tronic microbalance (MT5, Mettler) for all individuals of tongue is considered of prime importance (Cooper, 1997). the species G. galloti, L. bedriagae, and L. longicaudata. In these animals, the intrinsic tongue musculature is well Fiber lengths were determined for a single G. galloti after developed and diversified, and the tongue pro- and retrac- nitric acid digestion (see Loeb and Gans, 1986; Herrel et tors often much reduced compared to iguanians (see Kier al., 2001). Additionally, one adult specimen of the species and Smith, 1985; Smith, 1986; Schwenk, 2000). The pap- Lacerta oxycephala, Latastia longicaudata, Lacerta bed- illary morphology is also radically divergent and usually riagae, and Acanthodactylus pardalis were cleared and consists of low-profile scale-like papillae (e.g., Toubeau et stained using a modified Taylor and Van Dyke (1978) al., 1994; Schwenk, 2000). stain to examine the morphology of the hyobranchial ap- Although tongue structure and function have been in- paratus. vestigated in some detail in Iguanians and the highly derived varanid lizards (e.g., Smith, 1984, 1986; Herrel et Histology al., 1998; for an overview, see Schwenk, 2000), informa- Seven adult lizard specimens (three Lacerta parva, two tion is generally lacking for phylogentically and function- Lacerta trilineata galatiensis, two Lacerta danfordii ana- ally intermediate groups such as scincomorphs. Yet scin- tolica) that were collected from Eskis¸ehir, Turkey, were comorphs such as lacertid lizards are especially intriguing used. Specimens were killed by overexposure to CO2 gas animals because they rely heavily on the tongue for both and tongues were removed and fixed in a 10% aqueous food transport (Goosse and Bels, 1992a; Urbani and Bels, formaldehyde solution for 48 hr. Next, the tongues were 1995) and chemoreception (Goosse and Bels, 1992b), thus dehydrated in an increasing ethanol series. Samples were combining two (at first sight) very different functions. embedded in paraffin blocks and were cut serially along Quite unexpectedly, studies of the use and movement the sagittal plane at 5 ␮m on a Leica RM2025 microtome. patterns of the tongue during chemosensory exploration All sections were stained using Harris’ hematoxylin-eosin and food recognition (Goosse and Bels, 1992b) and during (Bancroft and Stevens, 1977; Clark, 1981). Samples were prey transport and drinking (Goosse and Bels, 1992a; Bels investigated by light microscopy using Spot Advanced et al., 1993; Urbani and Bels, 1995) have suggested that Software (V. 3.2.4; Diagnostic Instruments, Sterling the specialization of the tongue for chemoreceptive pur- Heights). Sections were digitally photographed using a poses has not adversely affected its function during prey Spot insight color 3.2.0 diagnostic camera. transport and drinking (Goosse, 1994). However, little is For comparative purposes, adult specimens of the spe- known regarding the (functional) anatomy of the tongue in cies Laudakia stellio, Phrynosoma douglassi, Chameleo lacertid lizards, making it difficult to understand its dual jacksonii, and Gekko gecko were obtained from the pet use during prey transport and chemoreception (but see trade. Animals were sacrificed by intramuscular injection Von Seiler, 1891; Camp, 1923; Iwasaki and Miyata, 1985; of an overdose of ketamine (500 mg/kg body mass). The Schwenk, 1985). heads of one (P. douglassi, G. gecko), two (P. stellio), or HYOLINGUAL MORPHOLOGY IN LACERTID LIZARDS 563 three (C. jacksonii) specimens of each species were pre- form eight roughly similarly sized bundles (see Camp, pared for paraffin histology using standard techniques 1923). Although our dissections of Gallotia confirm this, it (Humason, 1979). Serial 10 ␮m sections (both cross-sec- is very difficult to quantify the number of mandibulohyoi- tional and sagittal for P. stellio; cross-sectional, sagittal, dei bundles in some of the smaller species. and frontal for C. jacksonii; cross-sectional only for other The m. constrictor colli is one of the biggest hyolingual species) were made and colored using an improved muscles (Table 1). It originates dorsolaterally in the nu- trichrome stain (see also Herrel et al., 1998, 2001). chal region at the connective tissue associated with the dorsal cervical muscles and the suprascapula. From their Quantitative Analyses origin, the fibers run ventrad, curve medially, and insert To evaluate the functional importance of muscle groups, on a thin connective tissue sheet associated with the me- muscle mass data were summed for each of five functional dial edge of the m. omohyoideus. Anteriorly, a small bun- groups (hyobranchium protractors, hyobranchium retrac- dle of fibers originating at the connective tissue associated tors, tongue protractors, tongue retractors, and superficial with the terminal part of the epihyals of the ceratohyal constrictor muscles) within each individual. All data were and first ceratobranchial is observed. Its fibers run ven- trad, just overlapping the posterior part of the m. ptery- log10-transformed before further analyses. First we tested whether tongue mass and the mass of each functional goideus and insert ventrally on a central median raphe. group were significantly correlated to lizard body and These anterior fibers of the m. constrictor colli lie adjacent head size. Next, we regressed tongue mass and the mass of to the posteriormost fibers of the m. intermandibularis each functional group to lizard head length and extracted posterior and overlap them partially near their insertion. residuals. The residuals were then used as input for anal- The m. intermandibularis anterior is the smallest of the yses of variance (ANOVAs) to test for differences among two intermandibularis muscles and lies anterior to the m. species. All analyses were performed using SPSS V11.5 intermandibularis posterior. The fibers originate at the (SPSS, Chicago, IL). dorsal mesial border of the dentale, run ventrad, curve round the m. mandibulohyoideus and the m. genioglossus, RESULTS and insert on a mid-ventral raphe. This is the anterior- Hyobranchium most and superficialmost muscle in the throat region. The m. intermandibularis posterior originates on the The hyobranchium in lacertid lizards is composed of a ventrolateral border of the lower jaw, at the level of the m. centrally located cartilaginous lingual process (LP), a cen- adductor mandibulae externus superficialis posterior and tral cartilaginous and flat basibranchium (BB) with an the m. pterygoideus. The posteriormost fibers are also anterolaterally directed pair of hypohyalia (HH), and two connected to the connective tissue associated with the pairs of posteriorly directed ceratobranchialia (CB) at- rising distalmost part of the first ceratobranchial in Gal- tached. The hypohyalia and the first pair of cerato- branchialia show distinct articulatory facets at their con- lotia. The fibers run ventrad and mediad, running exter- nection with the basibranchium. The second pair of nal from the m. pterygoideus and hiding it in superficial ceratobranchials, however, is continuous with the basi- view, and insert on a mid-ventral raphe. branchium. Attached to the hypohyalia by means of a Hyoid protractor muscles. The m. mandibulohyoid- well-developed articulation are the ceratohyalia that dis- eus 1 is the biggest of the hyoid protractors. Its fibers tally bear small cartilagenous epibranchialia. Proximally originate broadly along the posterior two-thirds of the on the anterior aspect of the ceratohyalia, a flat cartilag- ventral side of the lower jaw, anterior to the insertion of inous expansion is present. The shape of the cartilaginous the m. pterygoideus. The fibers run directly posteriad and plate varies considerably between species (Fig. 1). The insert along the entire posteroventral border of the first lingual process is well developed and runs in the posterior ceratobranchial. two-thirds of the tongue, roughly up to the level of the The m. mandibulohyoideus 2, the smallest of the hyoid fore-tongue. It sits medially, in between the two hyoglos- protractors, originates roughly one-fourth down the man- sal bundles. The first pair of ceratobranchialia was calci- dible at its ventral aspect. From their origin, the fibers run fied in all specimens examined (L. longicaudata, L. posteriad and converge to the middle to insert directly on oxycephala, L. bedriagae, A. pardalis, P. atrata, G. gal- the entire ventral aspect of the basibranchium and the loti). The ceratobranchials run posteriad to curve dorsad hypohyals. In doing so, the fibers of the m. mandibulohy- in the nuchal region, about halfway down their length. oideus 2 cover the articulation of the ceratohyal with the The second pair is mostly cartilaginous and short. The two hypohyal. elements of the second pair of ceratobranchials are posi- The m. mandibulohyoideus 3 originates along the pos- tioned on either side of the trachea and occasionally curve terior third of the mandible anterior to the m. pterygoi- toward or away from the trachea at the posterior end. In deus. Its fibers run directly posteriad in a narrow bundle one species (L. oxycephala), the lingual process, hypohya- and insert along the anterior ventral border of the cerato- lia, ceratohyalia, and both pairs of ceratobranchialia show hyal. The insertion ranges from about one-third down the a tendency to ossify. However, the primitive condition for ceratohyal to the tip of the ceratohyal, thus largely cover- the group as represented by G. galloti is defined by an ing the m. hyoglossus and m. branchiohyoideus in ventral ossified first pair of certobranchials only. view. Muscular Anatomy (Fig. 2) Hyoid retractor muscles. The m. omohyoideus orig- Superficial transverse group. Lacertid lizards re- inates along the anterior border of the rising part of the tain the ancestral condition where the m. intermandibu- clavicula. Its fibers run anteromediad, diverge, and insert laris interdigitates with the mm. mandibulohyoidei to along the entire posterior border of the first cerato- 564 HERREL ET AL.

Fig. 1. Cleared and stained hyobranchia of Latastia longicaudata and the second ceratobranchial are calcified in L. oxycephala. BB, (left) and Lacerta oxycephala (right): (A) ventral view; (B) lateral view; (C) basibranchium; CB I, first ceratobranchiale; CB II, second cerato- dorsal view. Elements staining blue indicate the presence of cartilage; branchiale; CH, ceratohyale; EH, epihyale; HH, hypohyale; LP, lingual red elements are calcified. Note that the proximal parts of the ceratohyal process. HYOLINGUAL MORPHOLOGY IN LACERTID LIZARDS 565

Fig. 2. (See overleaf.) 566 HERREL ET AL. TABLE 1. Muscle mass distribution in lacertid lizards* L. G. galloti L. bedriagae longicaudate Snout-vent length (mm) 103.38 Ϯ 8.88 74.20 Ϯ 4.01 91.50 Ϯ 6.25 Head length (mm) 25.36 Ϯ 3.57 18.42 Ϯ 1.87 19.82 Ϯ 1.37 Tongue mass (mg) 50.35 Ϯ 31.75 22.73 Ϯ 1.82 28.30 Ϯ 6.50 m. intermandibularis anterior 1.86 Ϯ 0.57 2.43 Ϯ 0.23 1.44 Ϯ 0.13 m. intermandibularis posterior 6.34 Ϯ 1.48 5.26 Ϯ 0.85 7.37 Ϯ 2.78 m. constrictor colli 25.54 Ϯ 4.63 20.42 Ϯ 1.46 18.20 Ϯ 3.24 m. mandibulohyoideus 1 10.87 Ϯ 0.83 14.05 Ϯ 1.35 7.80 Ϯ 1.37 m. mandibulohyoideus 2 3.71 Ϯ 1.96 3.91 Ϯ 1.34 5.22 Ϯ 0.57 m. mandibulohyoideus 3 3.49 Ϯ 0.76 3.21 Ϯ 0.99 5.88 Ϯ 0.12 m. omohyoideus 11.49 Ϯ 1.60 12.80 Ϯ 2.96 10.02 Ϯ 1.64 m. sternohyoideus pars superficialis 11.82 Ϯ 1.12 11.98 Ϯ 1.74 14.99 Ϯ 1.31 m. sternohyoideus pars profundus 10.43 Ϯ 0.33 9.36 Ϯ 0.65 8.53 Ϯ 2.12 m. branchiohyoideus 3.15 Ϯ 0.29 4.05 Ϯ 0.44 2.38 Ϯ 0.48 m. genioglossus pars medialis 2.24 Ϯ 1.17 1.66 Ϯ 0.49 2.67 Ϯ 0.27 m. genioglossus pars lateralis 4.18 Ϯ 1.15 5.81 Ϯ 2.14 7.49 Ϯ 1.47 m. hyoglossus 4.88 Ϯ 0.58 5.07 Ϯ 1.85 8.02 Ϯ 1.54 *Muscle mass data based on three specimens per species. All masses are expressed relative to the total hyolingual muscle mass.

branchial. Near its insertion, this muscle lies in tight The m. genioglossus medialis originates at the posterior association with the anterior part of the m. sternohyoid- ventral aspect of the mandibular symphysis. Its fibers run eus superficialis. posteriad and insert at the medioventral aspect of the The m. sternohyoideus superficialis originates along the tongue, medial to the m. hyoglossus. anteroventral side of the interclavicula and the lateral- most anterior aspect of the sternum. From their origin, Tongue retractor muscles. The fibers from the m. the muscle fibers run anteriad to converge toward the hyoglossus originate on the posterior third of the first midline. The fibers insert along the posterior and ventral ceratobranchial. From their origin, the fibers run anteriad side of the basibranchium and the proximal most aspect of on either side of the entoglossal process through the entire the first ceratobranchial. tongue and stop just short of the bifurcated tongue tip. The m. sternohyoideus profundus originates along the anterior ventral surface of the sternum. The muscle also Intrinsic tongue muscles. The m. verticalis consists partially originates by means of a tendon running further of dorsoventrally oriented muscle fibers that run in be- posteriorly along the sternum. From their origin, the fi- tween the two bundles of the m. hyoglossus. Starting at bers diverge and insert along the posterior and dorsal side the level of the mid-tongue, the verticalis muscle starts to of the proximal half of the first ceratobranchial. wrap around the entire m. hyoglossus, thus forming in The m. branchiohyoideus originates along the posterior conjunction with the m. transversalis a functionally circu- and ventral aspect of the ceratohyal along its entire lar muscle. At the level of the hind-tongue, this arrange- length, beginning at the hypohyal-ceratohyal joint. The ment changes and the verticalis fibers remain only on the fibers run posteriad and slight laterad and insert on the ventral aspect of the hyoglossal bundles. posterior four-fifths, along the anterior and dorsal aspect The m. transversalis consists of transversely oriented of the first ceratobranchial. muscle fibers that run just below the m. longitudinalis and dorsal to the m. hyoglossus. The muscle is present and Tongue protractor muscles. The m. genioglossus well developed throughout the entire tongue and runs the lateralis originates partly tendinously at the posterior entire width of the tongue throughout the fore-tongue. dorsal aspect of the jaw symphysis. The fibers run poste- The m. longitudinalis consists of longitudinal muscle riad and slightly laterad and insert lateral to the m. hyo- fibers that run in the connective tissue in between the glossus along the posterior third of the ventral surface of epidermis and the m. transversalis. The fibers run along the tongue. the entire length of the tongue.

Fig. 2. schematic representation of the extrinsic tongue and hyolingual musculature in Gallotia galloti. Muscles have been color-coded to facilitate comparisons across different views. Top: Superficial ventral view on the hyolingual musculature after removal of part of the right m. constrictor colli, the right m. intermandibularis anterior, and the right m. intermandibularis posterior. Middle: Deep ventral view after removal of the m. constrictor colli, the entire m. intermandibularis group, the left and right m. omohyoideus, the left and right m. episternocleidomastoideus, the left and right m. mandibulohyoideus 1, the right m. mandibulohyoideus 2 and 3, and the right m. sternohyoideus superficialis. Bottom: Deepest view after removal of the m. constrictor colli, the intermandibularis group, the left and right m. episternocleidomastoideus, the left and right m. omohyoideus, the left and right m. sternohyoideus superficialis, the left and right m. mandibulohyoideus group, the right m. genioglossus pars medialis and lateralis, and the right m. hyoglossus. Note that the left m. genioglossus pars medialis has been pulled aside to show the left m. genioglossus pars lateralis. HYOLINGUAL MORPHOLOGY IN LACERTID LIZARDS 567

Fig. 3. Parasagittal section of the tongue of Lacerta parva showing the posteriorly directed filiform papillae (f) on the posterior two-thirds of the dorsal surface of the tongue. Also visible are the intrinsic tongue muscles (i) and the m. hyoglossus running (HG) through most of the length of the tongue.

Tongue Surface Morphology In L. parva and L. danfordii, the interpapillary spaces (lateral parts of papillae) are covered by a single-layered In all species examined, the bifurcated tongue tip is cylindirical epithelium, and in between these cells, mu- covered with a stratified squamous epithelium arranged cous secreting cells are present (Fig. 6A). In L. trilineata, in smooth scale-like papillae. the interpapillary spaces are covered by a nonkeratinized In Lacerta parva, two types of papillae are observed on stratified squamous epithelium (Fig. 6B). Cylindirical mu- ventral and dorsal surfaces of tongue’s apical regions pos- cous secreting cells are present on both the apex of the terior to the bifurcated tongue tip: filiform and fungiform papillae and in the interpapillary spaces. Additionally, papillae. Fungiform papillae are less abundant than fili- single-layered cylindrical epithelium cells are observed in form ones and are positioned irregularly in between the between the papillae. filiform papillae (Fig. 3). In Lacerta trilineata and Lacerta In all species examined, a distinct lamina propria posi- danfordii, however, three types of papillae are observed on tioned just under the epithelium is present and penetrates the ventral and dorsal sides of the apical region of the into the actual papillae. Additionally, a dense and irregular tongue: filiform, fungiform, and foliate papillae. In con- layer of connective tissue is observed under the epithelial trast to the situation observed in L. parva, filiform papil- layer (Fig. 6C). Skeletal muscle fibers originating from the lae are less abundant than fungiform ones (Fig. 4A). Fo- intrinsic muscle bundles are observed passing through the liate papillae are observed only on the ventral part of the lamina propria and connective tissue layers and running mid-tongue (Fig. 4B). into the papillae in all species (Fig. 6D). Pigment granules In both Lacerta parva and Lacerta trilineata, papillae are randomly distributed in the different tissues of tongue are observed on the dorsal and ventrolateral aspect of the with the exception of the epithelial layer (Figs. 3–6). tongue from the apical region to the mid-tongue only. However, no distinct papillae are observed on the ventro- Quantitative Analysis of Hyolingual Muscle lateral part the of mid- and hind-tongue regions. In L. danfordii, however, papillae are present on all regions of Mass the tongue, including the ventrolateral part of the mid- Our results show that the mass of the tongue and the and hind-tongue. mass of the hyolingual muscles are significantly corre- In all species, filiform papillae are turned with their lated to lizard head size (0.73 Ͻ r2 Ͻ 0.85; all P values Ͻ apex posteriorly toward the hind-tongue. In L. parva, the 0.001), with lizards with larger heads having heavier apex of the filiform papillae is covered by a stratified tongues and heavier hyolingual muscles (Fig. 7). An anal- squamous epithelium. Fungiform papillae, on the other ysis of the residual hyolingual muscle masses showed hand, are covered by a nonkeratinized stratified squa- significant species differences, with Latastia longicaudata mous epithelium (Figs. 4 and 5). In L. trilineata and L. having significantly lighter superficial constrictors (F ϭ danfordii, the apex of the papillae (all types) is covered by 6.91; P ϭ 0.028), hyobranchium protractors (F ϭ 12.77; a partly stratified squamous epithelium (Fig. 4D). P Ͻ 0.01), and hyobranchium retractors (F ϭ 6.56; P ϭ 568 HERREL ET AL.

Fig. 4. A: Sagittal section through the lateral aspect of the tongue tip the mid-tongue in Lacerta parva showing fungiform papillae (fu) covered in Lacerta danfordii. On the ventral side of the tongue, a fungifom papilla by nonkeratinized stratified squamous epithelium on the dorsal side of can be seen (fu). On the dorsal side, filiform papillae (fi) are present. the tongue. D: Sagittal section through the lateral anterior aspect of the Anterior to the left. B: Sagittal section through the lateral aspect of the mid-tongue in Lacerta trilineata. On the dorsal side of the tongue, the mid-tongue in Lacerta trilineata showing foliate papillae (fo) on the ven- apex of the papillae is covered by a partly stratified squamous epithe- tral side of the tongue. C: Sagittal section through the lateral aspect of lium.

0.031) for its body size than the other two species. In all associated musculature. The extensive variation in form species, the superficial throat constrictor, the m. constric- and degree of ossification in the hyobranchial elements is tor colli is the largest muscle in the hyolingual system rather unexpected and is suggestive of functional differ- (roughly 20% of the total hyolingual muscle mass; see ences in the use of the hyobranchium among the different Table 1). Hyoid retractors (30%) and protractors (18%) are species examined (e.g., during prey transport and dis- generally much better developed than the tongue pro- and play). Interestingly, in another species of lacertid lizard, retractors (roughly 7% of the total hyolingual muscle mass Lacerta viridis, the cortex of the ceratohyals, hypohyals, across all species). Latastia longicaudata does appear to first and second pair of ceratobranchials were ossified have relatively weaker developed hyoid protractors but (Bels et al., 1994) as observed here for L. oxycephala.As larger tongue protractors. Fibers are shortest for the m. both of these species belong to the same clade of lacertid intermandibularis anterior and longest in the posterior lizards (Arnold, 1989), it appears as if the degree of ossi- constrictor muscles and the hyobranchium protractors fication of the hyobranchial elements might be a phyloge- (Table 2). Fibers are of intermediate length in the hyo- netically informative character. Alternatively, the hyo- branchium retractors, the m. branchiohyoideus, and branchium of both species could be subjected to similar tongue pro- and retractors. functional demands on the hyobranchial system and ossi- DISCUSSION fications could simply be induced by higher muscular forces exerted on the hyobranchial system during, for ex- Tongue Structure and Function in Lacertid ample, prey transport (see Currey, 1984). This would in Lizards turn suggest a more prominent role of the hyobranchium The hyolingual apparatus of the lacertid lizards exam- during prey transport in these lizards. Clearly, this should ined here consists of a well-developed hyobranchium and be investigated further by examining both the degree of HYOLINGUAL MORPHOLOGY IN LACERTID LIZARDS 569 rather strongly connected to the hyolingual skeleton, movements of the hyobranchium will likely also have a direct effect on the movements of the tongue. This, how- ever, needs to be tested using cineradiography. Another common feature among the species examined here is the well-developed intrinsic tongue musculature, including distinct verticalis, transversalis, and longitudinalis groups in the fore- and mid-tongue regions. The degree of development of these muscle groups is suggestive of an important role during the extraoral lingual extensions observed during chemoreception and drinking (see Goosse and Bels 1992b; Bels et al., 1993). Whereas contractions of the transverse and dorsoventral intrinsic muscle will tend to elongate the tongue as a result of its hydrostatic nature (Kier and Smith, 1985; Smith, 1988), the longitudinal intrinsic and hyoglossal muscles can function to withdraw the tongue into the oral cavity. The intrinsic tongue mus- cles presumably also play an additional and important role during prey transport. As individual muscle fibers from the intrinsic muscle groups (mostly the fibers of the m. verticalis) actually run into the lingual papillae of the mid- and hind-tongue (Fig. 6), they may actively contrib- ute to changes in the position of individual tongue papillae to maximize contact area, and thus adhesive forces, be- tween the tongue and the prey. The papillary morphology of the tongue in lacertid liz- ards is complex and shows clear differences between the Fig. 5. Sagittal section through the lateral aspect of the mid-tongue tongue tips and anterior fore-tongue and the more poste- in Lacerta trilineata showing a keratinized stratified squamous epithelium rior parts of the tongue (see also Iwasaki and Miyata, on the dorsal tongue surface. Note the fibers of the m. hyoglossus (HG) running parallel to the long axis of the tongue as well as the fibers of the 1985; Bels et al., 1993). The hind-tongue in lacertid lizards intrinsic tongue muscles (L, m. longitudinalis; T, m. transversalis; V, m. is typically much broader (see also Cooper, 1995b; Sch- verticalis). wenk, 2000) and has a more diverse array of papillae that presumably help to generate friction between the tongue and the prey. The relatively broad hind-tongue, but exten- sible fore-tongue region (see Cooper, 1995b), coupled to ossification and the functional role of the hyobranchium differences in papillary morphology (this study; Iwasaki during different behaviors in a broad sample of lacertid and Miyata, 1985; Bels et al., 1993) and the extensive lizards. development of intrinsic muscle groups appear to reflect Unexpectedly, differences in the muscle masses of the the need for multiple tongue functions and are suggestive hyobranchium pro- and retractors were observed among of a functional subdivision of the tongue in these lizards. species. Latastia longicaudata showed a derived condition (compared to the data for Gallotia, the basal member of Comparative Analysis the group; see Arnold, 1989), where the mass of some Although the extrinsic hyolingual musculature in lac- hyobranchial muscles is reduced. Again, it cannot be de- ertids does not differ dramatically from the bauplan ob- termined at this point whether the observed variation is served in lizards in general (Tanner and Avery, 1982; the result of phylogenetic differences or differences in the Schwenk, 2000), clear differences in the organization and functional demands imposed on the system. Latastia lon- a prominent variation in the degree of development of gicaudata belongs to a clade of lacertid lizards that have certain muscle groups is obvious when comparing lac- radiated extensively on the African continent and is quite ertids to other lizard groups. Although little or no quan- distinct from the other groups of lacertid lizards (Arnold, titative data are available, there appears to be a domi- 1989). Consequently, it may well be that the observed nance of the tongue protractors and retractors over the variation in morphology is the result of a radical differ- hyobranchial muscles in iguanian lizards (see Smith, ence in design between different clades of lacertid lizards. 1988; Herrel et al., 1998). On the other hand, lacertid Alternatively, as species of the genus Latastia are typi- lizards also appear to be quite noticeably different from cally extremely narrow-headed, the reduction in hyo- highly specialized lizards such as varanids (Smith, 1986), branchial muscle mass may also be the result of the lat- snakes (Smith and Mackay, 1990), and chameleons (Her- eral compression of the hyobranchial system (Fig. 1). rel et al., 2001), where the tongue is highly specialized for Again, more quantitative data on a wider variety of taxa chemoreception (varanids and snakes) and prey capture are needed to address these hypotheses. (chameleons). In the varanids and snakes, this is reflected One aspect of the hyolingual musculature that was com- in an almost complete reduction of both the extrinsic mon to all species examined here is that the tongue pro- tongue and hyobranchium musculature, and changes in and retractor muscles are rather poorly developed when the organization of the intrinsic tongue muscles (Smith, compared to the muscles directly associated with the hyo- 1986; Smith and Mackay, 1990). In chameleons, on the branchium. However, as the tongue of lacertid lizards is other hand, both the extrinsic (m. hyoglossus) and intrin- 570 HERREL ET AL.

Fig. 6. A: Sagittal section through the hind-tongue of Lacerta parva mid-tongue in Lacerta trilineata showing a distinct lamina propiria posi- showing interpapillary spaces covered by a single-layered cylindirical tioned just under the epithelium and penetrating into the actual papillae. epithelium (CE). In between these cells, mucous secreting cells (MC) are Additionally, a dense and irregular layer of connective tissue is observed present. B: Sagittal section through the anterior aspect of the mid- under the epithelial layer. D: Sagittal section through the lateral aspect of tongue in Lacerta trilineata. On the dorsal side of the tongue, interpap- the hind-tongue in Lacerta trilineata showing skeletal muscle fibers illary spaces, covered by a nonkeratinized stratified squamous epithe- originating from the m. verticalis, passing through the lamina propria and lium, are visible. C: Sagittal section through the lateral aspect of the connective tissue layers, and running into the papillae.

sic (m. verticalis) tongue muscles that function to project and Goosse, 1990; Urbani and Bels, 1995). Still, in lacertid and retract the tongue are hypertrophied (see Herrel et lizards, the hyolingual apparatus is used to transport and al., 2001 and references therein). Additionally, changes in reposition prey within the buccal cavity (Goosse and Bels, the position and the orientation of the hyolingual retrac- 1992a). The muscle mass data suggest that movements of tors associated with the changes in the morphology and the hyobranchium may play an important role during prey use of the hyobranchium are observed in chameleons transport in these lizards. Unfortunately, no data are (Meyers et al., 2002). currently available to test whether in lacertid lizards the Unfortunately, very few studies provide quantitative hyobranchium shows more extensive fore-aft movements data on hyolingual muscle masses in lizards. The only than the tongue itself. However, previously published other study that we know of is that of Herrel et al. (2001), data based on external recordings of feeding behavior where hyolingual muscle masses are reported for two spe- (Goosse and Bels, 1992a) suggest extensive tongue move- cies of chameleons. A comparison of the relative mass ments during prey transport. To test whether tongue distribution of the data reported in Herrel et al. (2001) movements are independent of the movements of the hyo- with the data for the lacertid lizards analyzed here show branchium, or whether a tight coupling of the movements strong differences. Whereas in the chameleons the tongue of the tongue with those of the hyobranchium (as sug- muscles are the predominant muscle group (71.6% Ϯ 1.4% gested by the morphological data) exists in lacertid liz- of the total hyolingual muscle mass), the muscles associ- ards, cineradiographic data are needed. ated with the hyobranchium dominate in lacertid lizards Also, a number of qualitative differences are notable (roughly 50% of the total hyolingual muscle mass in lac- when comparing the hyolingual morphology of lacertids to ertids—see Table 1—versus only 23.3% Ϯ 2% in chame- that of other lizard groups. The most striking difference leons). This is suggestive of clear functional differences in lies in the origin of the musculus mandibulohyoideus 2. the use of the tongue and hyobranchium in these two Whereas this muscle originates tendinously at the jaw groups. Whereas in the chameleons the tongue is used to symphysis in iguanians (Avery and Tanner, 1971; Smith, capture and retract the prey into the mouth (Herrel et al., 1988; Delheusy et al., 1994; Herrel et al., 1998; Meyers 2000), lacertid lizards use their jaws to capture prey (Bels and Nishikawa 2000; Meyers et al., 2002) and derived HYOLINGUAL MORPHOLOGY IN LACERTID LIZARDS 571 TABLE 2. Fibre lengths of the hyolingual muscles in Gallotia galloti* Muscle Fiber length (cm) m. intermandibularis anterior 0.53 m. intermandibularis posterior 1.76 m. constrictor colli 1.54 m. mandibulohyoideus 1 1.79 m. mandibulohyoideus 2 1.62 m. mandibulohyoideus 3 1.89 m. omohyoideus 0.97 m. sternohyoideus pars profundus 0.72 m. branchiohyoideus 1.08 m. genioglossus pars medialis 1.27 m. hyoglossus 1.18 *Fiber lengths based on one specimen only. No fiber lengths could be measured for the m. genioglossus pars lateralis and the m. sternohyoideus pars superficialis.

throat extensions would, however, be needed to test for correlations between the morphology of the hyobranchial system and its use as a display organ. The papillary structure of the tongue in lacertid lizards is also quite distinct. The mid- and hind-tongue regions show a complex papillary structure that presumably helps to generate friction with the prey. The anterior parts of the tongue, however, have a much simpler papillary struc- ture (this paper; Iwasaki and Miyata, 1985; Bels et al., 1993) and may be designed for smooth passage along the largely closed jaws during tongue flicking (see also Goosse and Bels, 1992). The papillary structure in lacertids ap- pears intermediate between the papillary structure ob- served in iguanians (agamids, iguanids, and chameleons; Fig. 8) (De la Serna de Esteban, 1965; Rabinowitz and Tandler, 1986; Delheusy and Bels, 1994; Herrel et al., Fig. 7. Top: Graph showing the relationship between head length 1998; Schwenk, 2000; Herrel et al., 2001) and that ob- and tongue mass in three species of lacertid lizards belonging to three served in other scleroglossan lizards such as anguino- distinct clades. Bottom: Graph illustrating the relationship between morphs and scincids, where large parts of the tongue are tongue mass and hyobranchium retractor muscle mass. Note how covered by highly modified scale-like papillae (see Latastia longicaudata has a significantly lower hyobranchium retractor muscle mass than the other two species. Note the log scale on X- and Toubeau et al., 1994; Schwenk, 2000). The tongue in geck- Y-axes. oes also plays an important role to clean the spectacles and this appears to be reflected in the smooth papillae found on mid- and hind-tongue regions (Fig. 8) (De la Serna de Esteban, 1965; Iwasaki, 1990; Schwenk, 2000). lizards such as helodermatids and varanids (McDowell, Thus, the tongue structure in geckoes appears to be quite 1972; Smith, 1986), it does not originate at the mandibu- unique even though the tongue is also used predominantly lar symphysis in lacertid lizards. Rather, it originates at to transport prey in these animals (Delheusy et al., 1995; the mesial side of the mandible, about one-third down its Herrel et al., 1999b). length away from the symphysis (Fig. 2). This condition In conclusion, our data do suggest a functional subdivi- resembles that observed in other scincomorphs (personal sion between the fore- and hind-tongue in both papillary observations) and some anguids (McDowell, 1972). The m. structure and muscular anatomy, allowing lacertid lizards branchiohyoideus is also striking and particularly well to use their tongues effectively during both chemorecep- developed in lacertid lizards. This muscle is typically as- tion and prey transport. The fore-tongue has a smooth sociated with the use of the hyobranchial apparatus as a epithelium and the intrinsic muscles are well developed, display organ in lizards such as Anolis lizards and other allowing considerable and complex tongue extensions. The iguanids (Bels, 1990; Font and Rome, 1990; Bels et al., hind-tongue, on the other hand, is broader and has a more 1994). Yet, unlike iguanids, lacertid lizards typically do complex epithelium that can help generate friction be- not use extensive throat displays in agonistic interactions. tween the tongue and the prey. Although the tongue pro- One exception is Gallotia galloti, where the throat region and retractors are generally not well developed in contrast is colored darkly and bears bright blue UV-reflective spots to our predictions, our muscle mass data suggest that they (Thorpe and Richard, 2001). Quantitative data on the are rather the movements of the hyobranchium that are development of the m. branchiohyoideus and the use of crucial during prey transport in these lizards. 572 HERREL ET AL.

Fig. 8. A: Mid-sagittal section through the tongue of an agamid lizard those observed in lacertid and agamid lizards. E: Close-up of a fungiform (Laudakia stellio) showing the typical elongated cylindriform papillae on papilla on the dorsolateral aspect of the hind-tongue of Gekko gecko. the posterior four-fifths of the dorsal tongue surface. Note the overall Note the similarity to the fungiform papillae of lacertid lizards shown in short, thick, and stocky appearance of the tongue of this animal when Figure 4. F: Frontal section showing a close-up of the plumose-like compared with the lacertid tongue shown in Figure 3. B: Close-up of the papillae found on the lateral aspect of the tongue of a chameleonid lizard papillae near the mid-tongue illustrating their shape. Note how the (Chameleo jacksonii). Note the difference in structure when compared to papillae have a large lumen. Abundant secretory cells and glandular the papillae observed in other lizards. G: Cross-section through the crypts are found at the base of the papillae. C: Cross-section through the mid-tongue of an iguanid lizard (Phrynosoma douglassi) showing plu- mid-tongue of a gekkonid lizard (Gekko gecko) showing fan-shaped mose papillae very similar to those observed on the lateral tongue of the papillae covering the entire dorsal surface. D: Close-up of the fan- chameleon. shaped papillae. Note the difference of these papillae when compared to

ACKNOWLEDGMENTS LITERATURE CITED

The authors thank K. Metzger for feedback on an earlier Arnold EN. 1989. Towards a phylogeny and biogeography of the version of the paper, Dr. D. Adriaens for allowing us to use Lacertidae: relationships within an old-world family of lizards de- his microscope equipped with digital camera and take rived from morphology. Bull Br Mus Nat Hist (Zool) 44:291–339. pictures of the sections of P. stellio, G. gecko, C. jacksonii, Avery DF, Tanner WW. 1971. Evolution of the iguanine lizards (Sau- and P. douglassi. A.H. is a postdoctoral fellow of the Fund ria, Iguanidae) as determined by osteological and myological char- for Scientific Research, Flanders, Belgium. acters. Brigham Young Univ Sci Bull Biol Ser 12:1–79. HYOLINGUAL MORPHOLOGY IN LACERTID LIZARDS 573

Bancroft JD, Stevens A. 1977. Theory and practice of histological Herrel A, Meyers JJ, Nishikawa KC, De Vree F. 2001. Morphology techniques. New York: Churchill Livingstone. and histochemistry of the hyolingual apparatus in chameleons. J Bels VL. 1990. The mechanism of dewlap extension in Anolis caroli- Morphol 249:154–pr170. nensis (Reptilia: Iguanidae) with histological analysis of the hyoid Iwasaki S, Miyata K. 1985. Scanning electron microscopy of the lin- apparatus. J Morph 206:225–244. gual dorsal surface of the japanese lizard, Takydromus tachydro- Bels VL, Goosse V. 1990. Comparative kinematic analysis of prey moides. Okajimas Folia Anat Jpn 62:15–26. capture in Anolis carolinensis (Iguania) and Lacerta viridis (Sclero- Iwasaki S. 1990. Fine structure of the lingual epithelium of the lizard glossa). J Exp Zool 255:120–124. Gekko japonicus (Lacertilia, Gekkonidae). Am J Anat 187:12–20. Bels VL, Goosse V, Kardong KV. 1993. Kinematic analysis of drinking Iwasaki S. 2002. Evolution of the structure and function of the ver- by the lacertid lizard, Lacerta viridis (Squamates, Scleroglossa). J tebrate tongue. J Anat 201:1–13. Zool Lond 229:659–682. Kier WM, Smith KK. 1985. Tongues, tentacles and trunks: the bio- Bels VL, Chardon M, Kardong KV. 1994. Biomechanics of the hyolin- mechanics of movement in muscular hydrostats. Zool J Linn Soc gual system in squamata. In: Bels VL, Chardon M, Vandewalle P, 83:307–324. editors. Biomechanics of feeding in vertebrates. Berlin: Springer Loeb GE, Gans C. 1986. Electromyography for experimentalists. Chicago: University of Chicago Press. Verlag. p 197–240. McClung JR, Goldberg SJ. 2000. Functional anatomy of the hypoglos- Camp CL. 1923. Cassification of the lizards. Bull Am Mus Nat Hist sal innervated muscles of the rat tongue: a model for elongation and 48:289–481. protrusion of the mammalian tongue. Anat Rec 260:378–386. Clark G. 1981. Staining procedures, 4th ed. New York: Williams and McDowell SB. 1972. The evolution of the tongue of snakes and its Wilkins. bearing on snake origins. In: Dobzhansky T, Hecht MK, Steere WC, Cooper WE Jr. 1994. Multiple functions of extraoral lingual behavior editors. Evolutionary biology. New York: Appleton Century Crofts. in iguanian lizards: prey capture, grooming and swallowing, but not p 191–273. prey detection. Anim Behav 47:765–775. Meyers JJ, Nishikawa KC. 2000. Comparative study of tongue pro- Cooper WE Jr. 1995a. Foraging mode, prey chemical discrimination, trusion in three iguanian lizards: Sceloporus undulatus, Pseudo- and phylogeny in lizards. Anim Behav 50:973–985. trapelus sinaitus and Chamaeleo jacksonii. J Exp Biol 203:2833– Cooper WE Jr. 1995b. Evolution and function of lingual shape in 2849. lizards, with emphasis on elongation, extensibility and chemical Meyers JJ, Herrel A, Nishikawa KC. 2002. Comparative study of the sampling. J Chem Ecol 21:477–505. innervation patterns of the hyobranchial musculature in three Cooper WE Jr. 1997. Correlated evolution of prey chemical discrimi- iguanian lizards: Sceloporus undulatus, Pseudotrapelus sinaitus, nation with foraging, lingual morphology and vomeronasal chemo- and Chameleo jacksonii. Anat Rec 267:177–189. receptor abundance in lizards. Behav Ecol Sociobiol 41:257–265. Rabinowitz T, Tandler, B. 1986. Papillary morphology of the tongue of Currey J. 1984. The mechanical adaptations of bones. Princeton, NJ: the american chameleon: Anolis carolinensis. Anat Rec 216:483– Princeton University Press. 489. De La Serna De Esteban C. 1965. Anatomia microscopica comparada Schwenk K. 1985. Occurrence, distribution and functional signifi- de la lengua de algunos saurios Argentinos. Anais Congr Latino- cance of taste buds in lizards. Copeia 1985:91–101. amer Zool 2:235–245. Schwenk K. 1995. Of tongues and noses: chemoreception in lizards Delheusy V, Toubeau G, Bels VL. 1994. Tongue structure and func- and snakes. Trends Rev Ecol Evol 10:7–12. tion in Oplurus cuvieri (Reptilia: Iguanidae). Anat Rec 238:263– Schwenk K. 2000. Feeding in lepidosaurs. In: Schwenk K, editor. 276. Feeding: form, function and evolution in tetrapod vertebrates. San Delheusy V, Brillet C, Bels VL. 1995. Etude cinematique de la prise de Diego, CA: Academic Press. p 175–291. nourriture chez Eublepharis macularius (Reptilia, Gekkonidae) et Smith KK. 1984. The use of the tongue and hyoid apparatus during comparaison au sein des geckos. Amphibia Reptilia 15:185–201. feeding in lizards (Ctenosaura similis and Tupinambis nigropunc- Emerson SB, Diehl D. 1980. Toe pad morphology and mechanisms of tatus). J Morph 202:115–143. sticking in frogs. Biol J Linn Soc 13:199–216. Smith KK. 1986. Morphology and function of the tongue and hyoid Font E, Rome LC. 1990. Functional morphology of dewlap extension apparatus in Varanus (Varanidae, Lacertilia). J Morph 187:261– in the lizard Anolis equestris (Iguanidae). J Morphol 206:245–258. 287. Gove DA. 1979. A comparative study of snake and lizard tongue- Smith KK. 1988. Form and function of the tongue in agamid lizards with comments on its phylogenetic significance. J Morph 196:157– flicking, with an evolutionary hypothesis. Z Tierpsychol 51:58–76. 171. Goosse V. 1994. Etude des mouvements de la teˆte du lezard vert Smith KK, Mackay KA. 1990. The morphology of the intrinsic tongue (Lacerta viridis, Laurenti 1768) dans la perspective de l’e´volution musculature in snakes (Reptilia, Ophidia): functional and phyloge- comportementale. PhD thesis. Lie`ge: Universite´ de Lie`ge. netic implications. J Morph 205:307–324. Goosse V, Bels VL. 1992a. Kinematic and functional analysis of feed- Tanner WW, Avery DF. 1982. Buccal floor of reptiles, a summary. ing behaviour in Lacerta viridis (Reptilia: Lacertidae). Zool Jb Anat Great Basin Naturalist 42:273–349. 122:187–202. Taylor WR, Van Dyke GC. 1978. Revised procedures for staining and Goosse V, Bels VL. 1992b. Kinematic analysis of tongue movements clearing small fishes and other vertebrates for bone and cartilage during chemosensory behaviour in the European green lizard, La- study. Privately printed. certa viridis (Reptilia: Lacertidae). Can J Zool 70:1886–1896. Thorpe RS, Richard M. 2001. Evidence that ultraviolet markings are Herrel A, Timmermans J-P, De Vree F. 1998. Tongue flicking in associated with patterns of molecular gene flow. Proc Natl Acad Sci agamid lizards: morphology, kinematics and muscle activity pat- 98:3929–3934. terns. Anat Rec 252:102–116. Toubeau G, Cotman C, Bels VL. 1994. Morphological and kinematic Herrel A, Spithoven L, Van Damme R, De Vree F. 1999a. Sexual study of the tongue and buccal cavity in the lizard Anguis fragilis dimorphism of head size in Gallotia galloti: testing the niche diver- (Reptilia: Anguidae). Anat Rec 240:423–433. gence hypothesis by functional analyses. Funct Ecol 13:289–297. Urbani J-M, Bels VL. 1995. Feeding behaviour in two scleroglossan Herrel A, De Vree F, Delheusy V, Gans C. 1999b. Cranial kinesis in lizards: Lacerta viridis (Lacertidae) and Zonosaurus laticaudatus gekkonid lizards. J Exp Biol 202:3687–3698. (Cordylidae). J Zool Lond 236:265–290. Herrel A, Meyers JJ, Aerts P, Nishikawa KC. 2000. The mechanics of Von Seiler RF. 1891. Ueber die Zungendrusen von Anguis, Pseudopus prey prehension in chameleons. J Exp Biol 203:3255–3263. und Lacerta. Arch Fur Mikrosk Anat 38:177–265.