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Form and function of the tongue in agamid lizards with comments on its phylogenetic significance
Abstract
The morphology of the tongue of agamid lizards is reviewed and discussed in the context of its functional and phylogenetic significance. It is shown that in several features, including the development of the central musculature of the tongue into a ring muscle and the presence of a genioglossus internus muscle in adults, the tongue in most agamids is derived relative to that in other squamates. In some features, such as the vertical connective tissue septa, agamids share primitive features with Sphenodon . Some conditions found in agamids are also found in anoline iguanids. Two genera, Uromastyx and Leiolepis , differ significantly from other agamids in intrinsic tongue musculature.
The functional significance of the unique tongue morphology is that agamids utilize a different mechanism of tongue protrusion from that of other lizards. This mechanism involves the production of force against the lingual process, leading to an anterior slide of the tongue, and is detailed in this paper. Finally, I discuss the mechanical basis for the transformation series of tongue protrusion mechanisms from agamids to chamaeleonids. It is suggested that the mechanism of tongue protrusion in chamaeleonids is not unique, but is a highly derived state of the condition found in agamids.
... Smith, 1984Smith, , 1988Schwenk, 1986Schwenk, , 1988Bell, 1989;Delheusy et al., 1994;Herrel et al., 1997;see Schwenk, 2000a, for an overview). Although in lizards the hyobranchial apparatus is often referred to as the hyoid or hyoid apparatus, a more appropriate term is the "hyobranchial" apparatus, since in lizards a larger portion of the apparatus (compared to that in mammals) is comprised of the branchial elements (visceral arches 3-5) (Schwenk, 2000a). ...
... As chameleons possess the unique ability to ballistically project the tongue out of the mouth, they have been the subject of numerous morphological studies over the past two centuries (Houston, 1828;Rice, 1973;Bell, 1989; see Herrel et al., 2001, for an overview). Although it is generally assumed that chameleons are most closely related to agamids (Moody, 1980;Estes et al., 1988;Schwenk, 1988;Macey et al., 2000a, b), until relatively recently the morphological changes that accompany the evolution of this unique behavior had drawn relatively little attention (Smith, 1988;Schwenk and Bell, 1988;Herrel et al., 1995;Meyers and Nishikawa, 2000). Despite these numerous studies devoted to the hyobranchial system in iguanians, no consensus has been reached regarding the homology and, hence, the terminology of the elements of the hyobranchial apparatus or the associated hyobranchial musculature. ...
... The other intrinsic tongue muscles are not described in detail in the present study, as the homology of the different muscles in the different groups remains unclear. For detailed descriptions, see Delheusy et al. (1994) for the intrinsic muscle arrangement in iguanids, Smith (1988) for agamids, and Bell (1989) and Herrel et al. (2001) for chameleons. ...
The neuroanatomy and musculature of the hyobranchial system was studied in three species of iguanian lizards: Sceloporus undulatus, Pseudotrapelus sinaitus, and Chamaeleo jacksonii. The goal of this study was to describe and compare the innervation and arrangement of the hyobranchial musculature in the context of its function during tongue protrusion. A comparison of the hyobranchial innervation patterns revealed a relatively conserved innervation pattern in S. undulatus and P. sinaitus, and a modified version of this basic layout in C. jacksonii. All three species show anastomoses between sensory neurons of the trigeminal nerve and motor neurons of the hypoglossal nerve, suggesting that feedback may be important in coordinating tongue, jaw, and hyoid movements. The hyobranchial muscu-lature of S. undulatus is very similar to that of P. sinaitus; however, there are minor differences, including the presence of an M. genioglossus internus (GGI) muscle in S. undu-latus. Further differences are found mainly in functional aspects of the hyobranchial mus-culature, such as changes in the muscle lengths and the origins and insertions of the muscles. In C. jacksonii the hyobranchial system is comprised of largely the same components, but it has become highly modified compared to the other two species. Based on the innervation and morphological data gathered here, we propose a revision of the terminology for the hyo-branchial musculature in iguanian lizards.
... As iguanian lizards, the integration of tongue morphology and function in agamid lizards is particularly interesting for several reasons. The main points of interest are the diversity in tongue morphology (Gnanamuthu, 1937;Smith, 1988;Herrel et al. 1998), as it is used for prey capture, chemoreception and drinking (Herrel et al. 1995(Herrel et al. , 1998Schwenk, 2000;Schaerlaeken et al. 2007), the variability in diet (i.e. herbivorous, scavenger, insectivorous, omnivorous) and the mechanism of tongue function, as it is either considered to be similar to Sphenodon and other Iguanids (representing an ancestral state) or a cryptic intermediate between the ancestral state and the highly derived mode characteristic of Chamaeleonids (Schwenk & Bell, 1988). ...
... herbivorous, scavenger, insectivorous, omnivorous) and the mechanism of tongue function, as it is either considered to be similar to Sphenodon and other Iguanids (representing an ancestral state) or a cryptic intermediate between the ancestral state and the highly derived mode characteristic of Chamaeleonids (Schwenk & Bell, 1988). Tongue muscles and dorsal surface have been studied in some agamid species (Gnanamuthu, 1937;Smith, 1988;Herrel et al. 1995Herrel et al. , 1998 but not in the omnivorous P. vitticeps. ...
... The tongue contains skeletal striated muscles arranged in well-defined fascicles (Fig. 3A). The tongue musculature can be divided into extrinsic and intrinsic muscles, as described in detail by Gnanamuthu (1937) and Smith (1988). The extrinsic musculature (Fig. 3A) of the tongue; the M. genioglossus lateralis, which forms the lateral edge of the tongue; and the M. genioglossus internus, which separates the two portions of the M. hyoglossus in the anterior region of the tongue. ...
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.
... Comparative studies more limited in taxonomic scope include Sewertzoff (1929), Gnanamuthu (1937), de la Cerna de Esteban (1965) and Tanner and Avery (1982). A reasonably full set of references is listed in Tables 8.1 and 8.2, but key sources include Sphenodon (Schwenk, 1986); Squamata: Iguanidae (Oelrich, 1956;McDowell, 1972;Schwenk, 1988;Delheusy et al, 1994); Agamidae (Gandolfi, 1908;Sewertzoff, 1929;Gnanamuthu, 1937;Schwenk, 1988;Smith, 1988;Herrel et al, 1998c; Chamaeleoni-dae (Gnanamuthu, 1930(Gnanamuthu, , 1937Lubosch, 1932;Bell, 1989); Amphisbaenia (de la Cerna de Esteban, 1959;Schwenk, 1988); Gekkota (Zavattari, 1909;Sewertzoff, 1929;Gnanamuthu, 1937;Ping, 1931;Schwenk, 1988; Rehorek, in preparation); Scincomorpha (Sewertzoff, 1929;Gnanamuthu, 1937;de la Cerna de Esteban, 1965;Schwenk, 1988); and Anguimorpha (Sewertzoff, 1929;Sondhi, 1958b;McDowell, 1972;Smith, 1986;Schwenk, 1988;Smith and MacKay, 1990;Tobeau et al, 1994). ...
... Stout, conical papillae on the posterior limbs are often particularly well developed in agamids. Uniquely in some agamids, glandular crypts penetrate deeply into the musculature of the foretongue (Gandolfi, 1908;Gnanamuthu, 1937;Smith, 1988;Schwenk, unpublished results) (Fig. 8.12B). There is taxonomic variation in this trait and in the particular muscles invaded, but too few species have been examined to deduce phylogenetic patterns. ...
... In all squamates there is partial or complete loss of this septum. It is complete in the posteriormost portion of the verticalis in some agamids (Gnanamuthu, 1937;Schwenk, 1988;Smith, 1988) and nearly complete in Varanus (Smith, 1986). In most squamates, however, the verticalis is undivided and its fibers cross the midline. ...
This chapter considers the structure, function, and evolution of the feeding system in nonophidian lepidosaurs: tuatara, lizards, and amphisbaenians. The latter two groups comprise, along with snakes, the squamate reptiles (Squamata). Although snakes are cladistically nested within squamates, their feeding systems have diverged sufficiently from other taxa to merit separate treatment. They are, however, considered in this chapter generallly, as in the discussion of evolutionary patterns within Lepidosauria. Lepidosaurs offer a number of attributes that make them attractive subjects for study in the context of tetrapod feeding mechanisms. First, they are phylogenetically well positioned to be informative about evolutionary trends and patterns in the tetrapod clade. Second, the feeding apparatus, particularly the tongue, is highly variable among lepidosaurs and so provides the grist for basic evolutionary studies, including phylogenetic analyses, as well as studies of evolutionary pattern and process.
... Unlike most vertebrate skeletal muscles, many intrinsic tongue muscles do not have skeletal attachments, yet these muscular hydrostats are capable of producing extensive and intricate tongue movements (e.g. Smith, 1984Smith, , 1986Smith, , 1988. Kier and Smith (1985) pointed out that the constant-volume nature of muscular hydrostats is their most important mechanical feature. ...
... The chamaeleonid tongue shares numerous features with the tongue of agamid lizards, the clade thought to be the sister taxon to the Chamaeleonidae (Estes et al. 1988). Agamid lizards possess a less-developed accelerator muscle, which appears to enable these lizards to translate the tongue along the entoglossus (Smith, 1988;Schwenk and Bell, 1988). During lingual prey capture, agamids protract the tongue beyond the gape while the animal lunges towards the prey (Smith, 1988;Schwenk and Bell, 1988;Schwenk and Throckmorton, 1989;Kraklau, 1990), although these lizards lack a supercontracting hyoglossi muscle (retractor muscle) and are unable to project the tongue off the entoglossus. ...
... Agamid lizards possess a less-developed accelerator muscle, which appears to enable these lizards to translate the tongue along the entoglossus (Smith, 1988;Schwenk and Bell, 1988). During lingual prey capture, agamids protract the tongue beyond the gape while the animal lunges towards the prey (Smith, 1988;Schwenk and Bell, 1988;Schwenk and Throckmorton, 1989;Kraklau, 1990), although these lizards lack a supercontracting hyoglossi muscle (retractor muscle) and are unable to project the tongue off the entoglossus. ...
Summary In this paper we investigate the interaction between the accelerator muscle (the muscle that powers tongue projection) and the entoglossal process (the tongue's skeletal support) that occurs during tongue projection in chamaeleonid lizards. Previous work has shown that there is a delay of about 185 ms between the onset of accelerator muscle activity and the onset of tongue projection. In conjunction with anatomical observations, in vitro preparations of the accelerator muscle mounted on isolated entoglossal and surrogate processes were stimulated tetanically, and the resulting movements were recorded on video at 200 fields s"1. Three results indicate that morphological features of the entoglossus and the accelerator muscle delay the onset of tongue projection following the onset of accelerator contrac- tion: (I) the entoglossus is parallel-sided along the posterior 90% of its shaft, only tapering at the very tip, (2) the sphincter-like portion of the accelerator muscle, which effects tongue projection, makes up the posterior 63% of the muscle and does not contact the tapered region of the entoglossus at rest, and (3) accelerator muscles mounted on the entoglossus undergo longitudinal extension and lateral constriction for 83 ms following the onset of electrical stimulation, before projecting off the entoglossus. It is proposed that, during elongation of the accelerator muscle, the sphincter-like region ultimately comes into contact with the tapered region of the entoglossus, causing the onset of projection. This conclusion is supported by the observation that the time between the onset of stimulation and the onset of projection was longer in preparations with surrogate entoglossal processes that had no tapered tip and shorter with surrogate processes that had a tapered tip about four times as long as the natural entoglossus. Tetanically stimulated accelerator muscles reached 90% of peak force 110 ms after the onset of stimulation, indicating that the 185 ms delay between the onset of accelerator activity and the onset of projection seen in vivo allows the accelerator to achieve peak force prior to the onset of projection. Thus, the delay
... Both the morphology and the mechanism of tongue projection in chameleons have been extensively studied (Houston, 1828;Gnanamuthu, 1930;Zoond, 1933;Altevogt & Altevogt, 1954;Bell, 1989Bell, , 1990), yet few data exist on prey processing behaviours (Bels & Baltus, 1987). Comparative data are available for several other squamate taxa (Throckmorton, 1976(Throckmorton, , 1980Smith, 1984Smith, , 1988Bels & Goosse, 1989;Schwenk & Throckmorton, 1989), including representatives of the Iguanidae and Agamidae, taxa believed to be outgroups to the Chamaeleonidae (Estes, de Queiroz & Gauthier, 1988). Furthermore, a model has been proposed that attempts to summarize the transport cycles of many amniotes (Bramble & Wake, 1985), suggesting that there is a common, conservative pattern of head and hyoid movements found among generalized amniotes. ...
... Together with the Chamaeleonidae they comprise the Iguania, a monophyletic group within the Squamata (Estes et al., 1988). The condition found in agamids and iguanids thus represents a reasonable estimate of the more generalized condition from which the chameleon feeding apparatus evolved (Schwenk & Bell, 1988;Smith, 1988), and provides a basis for comparison of chameleonid prey transport behaviours. Below, we explore this comparison to test the possibility that there have been substantial modifications of chameleon prey transport in association with specialization of the prey capture mechanism. ...
... Comparative kinematic data for prey transport behaviour have been reported for several iguanian taxa (Throckmorton, 1976(Throckmorton, , 1980Smith, 1984Smith, , 1988Bels & Baltus, 1989;Schwenk & Throckmorton, 1989), including a second chameleon species (Bels & Baltus, 1987). Movements of the gape cycle during prey transport are the most frequently discussed, and data from several iguanian taxa are summarized in Fig. 6 . ...
This study develops a model of prey processing behaviours in lizards of the family Chamaeleonidae based on a kinematic analysis of videotaped feeding sequences in a representative species, Jackson's chameleon (Chamaeleo jacksonii). High-speed video (200 fields per second) and a computerized image analysis system were used, respectively, to film and quantify sequences of three individuals feeding on crickets. Two behaviours, chewing and prey transport, were identified a priori and compared in detail. Analyses of variance revealed significant differences between the two behaviours in seven of 11 kinematic variables. Patterns of correlation of variables within the entire data set were similar to correlations within each behaviour. A principal component analysis on the kinematic variables provided complete separation of the two behaviours in multivariate space. Chewing is distinct from prey transport behaviour in several ways: (1) chewing lacks extensive posterior movement in the hyoid skeleton while the jaws repeatedly open and close against the prey; (2) there is greater mouth opening in chewing; and (3) the entire gape cycle and its components occur more quickly in chewing. Prey transport involves extensive anterior posterior movements of the hyoid skeleton, which reflect the function of the tongue in transporting the prey from the oral cavity into the oesophagus. In both behaviours mouth opening is primarily associated with lower jaw depression rather than head elevation. Maximum hyoid retraction always occurs after peak gape is achieved. The body and head remain stationary with reference to the background, hence no inertial transport occurs. The kinematic profile of prey transport is compared to published feeding cycles of other iguanian lizards and a generalized model of prey processing in amniotes. Prey transport in chameleons follows the same kinematic patterns as reported for other iguanian lizards. We conclude that chameleons possess a generalized food processing system characteristic of other iguanian lizards, largely unmodified despite the presence of an extraordinary prey capture behaviour and its associated morphology.
... The morphology of the tongue of members of Squamata is known from a relatively large number of studies (e.g. Seiler 1891 Seiler , 1892 de Rooij 1915; Camp 1923; Gnanamuthu 1937; Schwenk 1985 Schwenk , 1986 Schwenk , 2000 Rabinowitz and Tandler 1986; Smith 1986 Smith , 1988 Iwasaki 1990 Iwasaki , 2002 Delheusy et al. 1994; Toubeau and Bels 1994; Herrel et al. 2005 ). Investigations of the gross anatomy of the squamate tongue, supplemented by light and electron microscopy, across a broad spectrum of subordinate taxa, have demonstrated considerable morphological variation in the structure of the dorsal lingual epithelium. ...
... Much attention has been paid to describing the features of the tongue surface, and the phylogenetic implications of these features have been extensively discussed (e.g. Schwenk 1985; Smith 1988). Several authors have also offered functional explanations for the morphological diversity evident in squamate tongue epithelia (e.g. ...
... Previous authors (e.g. Schwenk 1985; Smith 1988; Beisser et al. 1998 Beisser et al. , 2004 Iwasaki 2002; Herrel et al. 2005) have postulated that the presence of papillae on the tongue of sauropsids is explained either phylogenetically, or by the need for adaptation for food procurement and processing in a terrestrial environment. Food prehension is jaw-rather than tongue-based in Gekkotans (Delheusy and Bels 1999; Schwenk 2000; Bels 2003; Reilly and McBrayer 2007), leaving the tongue free for extra-oral functions. ...
Detailed descriptions of tongue morphology of members of Squamata that refer to functional implications other than food processing
are rare. Herein we focus on the morphology of the dorsal epithelium and internal structure of the tongue of the Leopard Gecko,
Eublepharis macularius, emphasizing the foretongue and its relation to fluid uptake. We employ both scanning electron microscopy and serial histology
to examine the morphology of the entire tongue, its component regions, and its situation in the oral chamber. We recognize
five distinct morphological regions of the dorsal tongue surface, each of which is distinctive both morphologically and histologically.
The foretongue bears papillae quite different in structure and spacing from those of all other tongue regions, and these non-glandular
structures are involved in gathering and transporting fluid from the environment. Fluid unloaded from the foretongue in the
region of the vomeronasal sinus is channeled through the network of cuboidal papillae and directed towards a pair of compartments
lateral to the tongue in which fluid pools during a drinking bout. This allows the dorsal surface of the mid- and hind-tongue,
which are involved in food processing and manipulation, to be largely segregated from the pathway of fluid flow. We relate
our findings to descriptions of the tongue of other taxa, and propose functional hypotheses for the observed morphology. This
study provides new anatomical information upon which future studies of the functional morphology of the buccal apparatus in
the Gekkota can be based.
... Since the tongue is a muscular hydrostat, its protrusion is accompanied by changes in its shape. Its movement has two phases: (i) elongation (Fig. 4a-c) and (ii) change in diameter (Fig. 4d) (Smith, 1988). Since the mouth is slightly open and the diameter of the cylindrical tongue decreases during protraction, the space between the dorsal surface of the mid-tongue and the palate increases. ...
... Such movements are similar for lizards that have markedly different lingual and buccopharyngeal morphologies (Wagemans et al., 1999). They relate directly to the tongue cycle because the throat and hyoid muscles that form the buccal floor provide a direct link between the hyolingual system and the jaws (Smith, 1984(Smith, , 1986(Smith, , 1988Bels et al., , 1994Bels et al., , 2019aSchwenk, 2000). To date, no electromyographic (EMG) data are available that document the sequential actions of the hyolingual and intrinsic lingual muscles during drinking in lizards. ...
Drinking permits amniote vertebrates to compensate for water loss. Lizards (non‐ophidian squamates) use their tongue to imbibe water, but for most lizards the tongue is also employed in other activities. To determine how these various demands can be accommodated alongside the tongue’s role in drinking, it is necessary to firstly determine the tongue’s function in water uptake and intraoral transport in a lizard that does not use this organ for chemoreception or food prehension. We selected the leopard gecko (Eublepharis macularius) for this purpose. We build upon previous morphological observations of the anatomy of its tongue and oral cavity and explore its drinking behaviour through high‐speed cinematography and cineradiography. This allows us to follow the movement of radio‐opaquely labelled water in association with tongue, jaw and throat movements. The tongue is modified to collect water and to release it into the anterior region of the buccal cavity. Repeated tongue cycles are associated with the shifting of the imbibed water into paired ventrolateral chambers and ultimately to its passage to a single, midline posterior chamber prior to swallowing. Tongue movements, capillarity and pressure changes due to hyolingual movements cause water to be moved posteriorly along specific pathways prior to swallowing, bypassing the airways and dorsal surface of the mid‐ and hind tongue. In this licking‐based lingually driven approach to drinking, only small volumes of water can be gathered at a time, with a drinking bout consisting of 20–30 tongue cycles before emersion and swallowing occur. This mechanism differs from drinking in turtles and snakes, which do not employ licking and may take in larger quantities of water. We advance the hypothesis that all lizards have conserved this pattern of tongue‐based water uptake and precisely directed intraoral fluid transport, with specializations for tongue‐based food capture and/or lingually based chemoreception being superimposed thereupon.
... Since the tongue is a muscular hydrostat, its protrusion is accompanied by changes in its shape. Its movement has two phases: (i) elongation (Fig. 4a-c) and (ii) change in diameter (Fig. 4d) (Smith, 1988). Since the mouth is slightly open and the diameter of the cylindrical tongue decreases during protraction, the space between the dorsal surface of the mid-tongue and the palate increases. ...
... Such movements are similar for lizards that have markedly different lingual and buccopharyngeal morphologies (Wagemans et al., 1999). They relate directly to the tongue cycle because the throat and hyoid muscles that form the buccal floor provide a direct link between the hyolingual system and the jaws (Smith, 1984(Smith, , 1986(Smith, , 1988Bels et al., , 1994Bels et al., , 2019aSchwenk, 2000). To date, no electromyographic (EMG) data are available that document the sequential actions of the hyolingual and intrinsic lingual muscles during drinking in lizards. ...
Living lizards exploit almost all terrestrial ecosystems where they play the roles of both predator and prey in complex food webs. Bels et al. (Biomechanics of feeding in Vertebrates, 197–240, 1994) and Schwenk (Feeding: form, function and evolution in Tetrapod Vertebrates, 459–485, 2000) provided first detailed overviews about the anatomical and functional traits of the feeding stages and phases of the feeding cycle in these tetrapods. Here, we synthesize recent literature in order to provide discussion of the evolution of their feeding behavior from capture to swallowing.
... All extrinsic tongue muscles pass into the tongue ventrally. There are four major groups of intrinsic tongue muscles in lizards: the verticalis, the dorsal and ventral transverse and the dorsal longitudinal muscle, although variability in specific form exists (Oelrich, 1956;Schwenk, 1984Schwenk, , 1988Sewertzoff, 1929;Smith, 1984Smith, , 1986Smith, , 1988and references therein). In the majority of squamates the verticalis, dorsal transverse and ventral transverse combine to form a circular muscle that surrounds the hyoglossus (Fig. 10). ...
... In the majority of squamates the verticalis, dorsal transverse and ventral transverse combine to form a circular muscle that surrounds the hyoglossus (Fig. 10). In the most primitive groups such as Sphenodon (Schwenk, 1986), and agamid and iguanid lizards (Smith, 1984(Smith, , 1988 the tongue receives substantial structural support from the lingual process of the hyoid, although many tongue movements are independent of hyoid movement. Tongues that are totally independent of internal hyoid structural support are derived within lepidosaurs. ...
Data derived from studies of comparative anatomy, development, neuroanatomy, behaviour and the reconstruction of fossils are combined to evaluate the evolution of the oral-pharyngeal region in mammals. An important event in the evolution of the mammalian feeding apparatus was the development of a novel neuromuscular apparatus, consisting of a large series of striated muscles. The most important of these muscles are the pharyngeal elevators and constrictors, which appear to be without homologues in other amniotes. In addition to considerable peripheral neural and muscular modifications, the motor nuclei of the brain stem in mammals exhibit significant differences from other amniotes. The morphological features characteristic of mammals are reflected in behavioural differences, most significantly during swallowing and suckling. The neuromuscular changes in the mammalian oral-pharyngeal apparatus are at least as extensive as those involving the masticatory system, and have importance far beyond the separation of the airway and foodway, the foci of most previous studies. The hypothesis of neuromuscular conservativism in the evolution of the mammalian feeding mechanism is considered and it is concluded that few data exist to support this hypothesis.
... However, general hyoid organization of crocodilians and birds differ significantly from one another. Smith, 1988Smith, , 1992Bels et al., 1994;Schwenk 2000, and references therein for discussion of squamate hyoid musculature functional morphology). ...
... hyoglossus [Schumacher, 1973]). Hyolingual movements are driven by intrinsic and extrinsic tongue musculature as well as by hydrostatic forces and are highly variable across Sauropsida (Kier and Smith, 1985;Smith, 1988;Schwenk, 2000). ...
Crocodilians, dinosaurs, and birds are part of successful group of reptiles known as archosaurs, little is known about the evolution of the adductor chamber, which includes the jaw musculature, trigeminal nerves, and particular blood vessels, hindering hypotheses of homology and feeding function in fossil taxa such as crocodyliforms and non-avian dinosaurs. First, I review the cephalic musculature of dinosaurs and identify problems and prospects involved in inferring feeding form and function in the clade. Second, using a flamingo as a case study, I introduce a new CT imaging/dissection methodology that enables 3D visualization of cephalic vasculature and differentiation of adductor chamber contents. Third, I develop a robust hypothesis of jaw muscle homology by analyzing the topological patterns of soft tissues in the adductor chambers of extant reptiles. Fourth, I identify major evolutionary changes in the orbitotemporal region (e.g., trigeminal nerve, braincase, palate) during the evolution of crocodilians. Fifth, I identify major evolutionary changes in the orbitotemporal region of dinosaurs with respect to the evolution of birds. Sixth, I discuss the evolution of cranial kinesis and its functional significance in dinosaurs and other reptiles. The general results were: 1) Flamingos have a novel vascular device associated with the hyolingual system. 2) Crocodylians have a novel soft-tissue topological pattern that violates the trigeminal topological paradigm. 3) Sensory branches of the trigeminal nerves are topologically conservative and represent evolutionarily stable dermatomes. 4) Despite the suturing of the palate to the braincase early in their evolution, the epipterygoid was a persistent structure in the skull of crocodyliforms, evolved several different morphotypes, and was not eliminated until recently along the lines to modern crocodylians. 5) The trigeminal nerve, protractor muscles, and epipterygoid exhibit mosaic evolution among dinosaurs and prove to be phylogenetically and functionally informative structures. 6) Dinosaurs do not exhibit the suite of morphological characters indicative of cranial kinesis which suggests that intracranial synovial joints may more likely be related to growth rather than feeding function. Hence, jaw musculature and its neighboring tissues in the adductor chamber are key cephalic structures that exhibit characteristic morphological, functional, and phylogenetic patterns among extant and fossil archosaurs. System requirements: Adobe Acrobat reader. Mode of access: World Wide Web via OhioLINK's ETD Center. Title from PDF title page (viewed on Jan. 27, 2007). Thesis (Ph. D.)--Ohio University, 2006. Includes bibliographical references (p. 209-236).
... The development of lingual muscle groups is propositive of an important role the lingual extensions exhibit during chemoreception and drinking (Bels et al., 1993;Goosse & Bels, 1992). Moreover, the contractions of the transverse intrinsic muscle groups will tend to protract the tongue as a result of its hydrostatic nature (Kier & Smith, 1985;Smith, 1988), and the longitudinal intrinsic and hyoglossal muscles can allow retraction of the tongue backward. The intrinsic tongue muscles presumably also play an additional and important role during prey transport. ...
The present study aimed to illustrate comparative morphological, histological, and functional variations of the hyoid apparatus of Acanthodactylus boskianus and Ptyodactylus guttatus. The hyoid apparatuses and musculature of the two investigated species are well-developed. The hyoid apparatuses exhibit high mobility with different articulation sites between their skeletal elements. The degree of ossification of the hyoid apparatus of gecko is more developed than that of the lacertid lizard. In P. guttatus, a well-developed synchondrosis articulation appears between the basihyoid and ceratobranchialis of the hyoid apparatus. Meanwhile, in A. boskianus, the articular ligament which appears between basihyoid and ceratobranchialis is less developed and also appears as a ligament connection between the two parts of hyoid cornua in which ligaments provide more mobility to the hyoid of lacertid lizard. The results reflect a phylogenetically informative character about these clad and explain the different functional demands imposed on the hyoid apparatus as well as confirm the important role of hyoid apparatus in the movement of the tongue during the prey transport.
... Numerous studies have shown that, abundant lingual papillae are found on the dorsal side of the reptiles' tongue (Cizek et al., 2011). Lingual papillae covered with a stratified squamous epithe- lium that with thickness and keratinization in different extent (Smith, 1988), otherwise, also different in shape, size, number and function, all of these determined by the different of habitat, feeding habits and the processing of food (Iwasaki and Miyata, 1985). In addition to the branch area of the tip, the dorsal side surface of the S. tsinlingensis' tongue completely covered with the scale-shaped lingual papillae, and the similar structure have also discovered in T. tachydromoides (Iwasaki and Miyata, 1985) and Podaric sicula (Abbate et al., 2010). ...
... The extent of the chamber is obscured by matrix, but it appears to extend almost to the midline. (Smith, 1988). This tongue may have been used for food gathering or manipulation within the mouth. ...
Until recently, caenagnathids were a family of oviraptorosaurs represented only by fragmentary material. As such, caenagnathid biology has never been studied in depth. A well-preserved mandible provides new information on the anatomy and dietary habits of Chirostenotes. The mandible is edentulous, has a completely fused symphysis, with sharp occlusal margins and complex lingual surfaces. Finite element analysis shows that the lingual ridges are reinforced. This suggests that they had a function in food processing. These and other features suggest adaptations for an efficient shearing mechanism, and the overall morphology is poorly adapted for durophagous behaviour. Comparisons with three groups with convergently similar mandibles, especially dicynodonts, indicate caenagnathids were capable of handling an herbivorous diet. Here, an omnivorous diet is proposed for Chirostenotes, including folivory and small prey.
... The lingual surface in the present study consists of papillae with different shapes, sizes and distribution, these differences depend on dissimilarities in diet, feeding habits and handling of the food in the mouth (Iwasaki and Miyata, 1985). It has been reported that in most lizards the papillae are covered by a stratified squamous epithelium that differed only in thickness and degree of keratinization (Schwenk, 1986;Smith, 1988). This observation is in agreement with the present work. ...
The present study investigated the structure of the tongue of the toad, Bufo regularis and the lizard, Chalcides ocellatus. They have different feeding habits and live in different habitats. The tongue of the toad contains two types of lingual papillae; fungiform papillae and filiform papillae. The fungiform papillae are usually scattered among the filiform papillae and are believed to function in gustation and in the secretion of salivary fluid. Scanning electron microscopical studies revealed that no ciliated cells were observed on the surface of the filiform papillae or in the surrounding area of the sensory disc. In C. ocellatus the tip of the tongue is bifurcated and keratinized. The dorsal surface of the tongue is covered with several types of papillae; irregular, scale and ridge-shaped. Taste buds were present in the epithelium of the tongue. The lingual glands consist of mucous cells that form crypt-like invaginations between papillae. The present study revealed that there is a marked correlation between the structure of the tongue of both B. regularis and C. ocellatus and habitats and feeding mechanism of the two species.
... Histological studies of the tongue began as early as the second century and are continuing [11]. More recent, morphological studies of human [12] and animal tongues [13][14][15][16] focus more on function. Examples include studies of tongue function such as those of the chameleon and the toad [17][18][19][20]. ...
The aim of this study is to obtain information about the mouse tongue muscle rendered using micro-computed tomography (μCT) at low, middle, and high magnifications. Three-dimensional (3D) μCT is used in various fields. Most μCT observations are restricted to hard tissue in biomaterial samples. Recently, with the use of osmium tetroxide, μCT has been effectively employed to observe soft tissue; it is now believed that μCT observation of soft tissue is feasible. On the other hand, the structure of the tongue muscle has been well studied, but cross-sectional imaging enhanced by 3D rendering is lacking. We chose the mouse tongue as a soft tissue case study for μCT and generated cross-sectional images of the tongue enhanced by 3-D image rendering with histological resolution. During this observation, we developed new methods of low-magnification observation to show the relation between the tongue muscles and surrounding tissues. We also applied high-resolution μCT in high-magnification observation of muscle fiber fascicles. Our methodological techniques give the following results: (1) For low-magnification observation (field of view: 12,000 μm), pretreatment with decalcification and freeze drying is suitable for observing the area between the muscle of the tongue and the bone around the tongue using μCT. (2) For middle-magnification observation (Field of view: 3,500 μm), the use of osmium tetroxide to observe the muscle arrangement of the tongue by μCT is suitable. (3) For high-magnification observation (Field of view: 450 μm), high-resolution μCT is suitable for observation of the transversus muscle fiber fascicles.
... Many macroscopic and light microscopical (LM) studies have demonstrated considerable variations in the morphology and histology of the reptilian tongue (Albanese Carmignani and Zaccone, 1975;Schwenk, 1986;Smith, 1986Smith, , 1988Winokur, 1988;Delheusy et al., 1994). Additionally, electron microscopic studies have characterized ultrastructural features of the dorsal lingual epithelium of reptiles (Iwasaki and Miyata, 1985;Rabinowitz and Tandler, 1986;Iwasaki, 1990;Mao et al., 1991;Iwasaki and Kumakura, 1994). ...
Background
Turtles are adapted to different environments, such as freshwater, marine, and terrestrial habitats. Examination of histological and ultrastructural features of the dorsal lingual epithelium of the red-eared turtle, Trachemys scripta elegans, and comparison of the results with those of other turtles should elucidate the relationship between the morphology of tongues as well as the fine structure of lingual epithelia and chelonian feeding mechanisms.Methods
Light microscopical (LM) and scanning (SEM) and transmission (TEM) electron microscopical methods were used.ResultsSEM revealed a distribution of lingual papillae all over the dorsal tongue surface. Single epithelial cells can be discerned, with short microvilli on their surface. LM studies show differences within the stratified epithelium between the lateral and the apical side of the papillae. In TEM, these differences become more obvious; while the basal and deep intermediate layer is similar in both sides of the papillae, mucus granules begin to form at the edge of the superficial intermediate layer at the lateral side. Cells containing fine secretory granules are visible there, too. On the other hand, at the apical side, only fine-granule-containing cells are visible.Conclusions
This study indicates that the histology and ultrastructure of the lingual epithelium of Trachemys scripta elegans are similar to that of other turtles adapted to freshwater environments but differ from those of turtles living in marine or terrestrial habits. These differences can be explained in terms of the adaptation of turtles to their particular life circumstances. Anat. Rec. 250:127–135, 1998. © 1998 Wiley-Liss, Inc.
... The m. Pterygoideus Atypicus in Sphenodon, and other reptiles that posses it, may similarly offset reaction force to some extent. As previously described, the tongue morphology of Sphenodon is very similar to that of iguanian squamates (Oelrich 1956; Schwenk 1986 Schwenk , 1988 Smith 1988 ). Cladistic analyses based on morphological data (e.g Conrad 2008 ) suggest this shared tongue morphology may represent the ancestral condition for lepidosaurs. ...
Feeding in Sphenodon, the tuatara of New Zealand, is of interest for several reasons. First, the modern animal is threatened by extinction, and some populations are in competition for food with Pacific rats. Second, Sphenodon demonstrates a feeding apparatus that is unique to living amniotes: an enlarged palatine tooth row, acrodont dentition, enlarged incisor-like teeth on the premaxilla, a posterior extension of the dentary and an elongate articular surtace that permits prooral shearing. Third, Sphenodon has a skull with two complete lateral temporal bars and is therefore structurally analogous to the configuration hypothesised for the ancestral diapsid reptile. Furthermore, the fossil relatives of Sphenodon demonstrate considerable variation in terms of feeding apparatus and skull shape. Lastly, as Sphenodon is the only extant rhynchocephalian it represents a potentially useful reference taxon for both muscle reconstruction in extinct reptile taxa and determination of muscle homology in extant taxa.
... Contacts between tongue and prey surfaces should be less efficient in scleroglossans because the surface of the tongue is smoother, and anterior glands are not mucous (Schwenk, 1988;Urbani, 1992). In general, the tongue of scleroglossans, particularly the foretongue, is thinner (Smith, 1988;Schwenk, 1988;Iwasaki, 1990). Therefore, the tongue should move more anteriorly into the buccal cavity to produce efficient forces on the prey during retraction in scleroglossans and anterior movements of the tongue should be more pronounced in scleroglossans with larger foretongue modifications (i.e. ...
This paper deals with a description of feeding phases in the scleroglossan lizard Zonosaurus laticaudatus by using high-speed cinematography. Capture modes are compared with Lacerta viridis. Z. laticaudatus uses the tongue for capturing small prey while both species use jaw prehension for large prey. L. viridis always uses jaw prehension for small prey.
... Bischoff, 1840; Owen, 1841; Cuvier & Laurillard, 1849; Pollard, 1892; Gaupp, 1896; Allis, 1897 Allis, , 1922; Danforth, fish to modern humans – head and neck musculature, R. Diogo et al. Lubosch, 1914; Sewertzoff, 1928; Edgeworth, 1935; Brock, 1938; Piatt, 1938; Millot & Anthony, 1958; Osse, 1969; Larsen & Guthrie, 1975; Greenwood, 1977; Wiley, 1979a,b; Jollie, 1982; Bemis et al. 1983 Bemis et al. , 1997 Lauder & Shaffer, 1985, 1988 Bemis, 1986; Reilly & Lauder, 1989, 1990 Miyake et al. 1992; Wilga et al. 2000; Kardong, 2002; Carroll & Wainwright, 2003; Johanson, 2003; Kleinteich & Haas, 2007). Most authors agree that the branchial muscles sensu stricto are not present as a group in extant reptiles and extant mammals (Table 3). ...
In a recent paper Diogo (2008) reported the results of the first part of an investigation of the comparative anatomy, homologies and evolution of the head and neck muscles of osteichthyans (bony fish + tetrapods). That report mainly focused on actinopterygian fish, but also compared these fish with certain non-mammalian sarcopterygians. The present paper focuses mainly on sarcopterygians, and particularly on how the head and neck muscles have evolved during the transitions from sarcopterygian fish and non-mammalian tetrapods to monotreme and therian mammals, including modern humans. The data obtained from our dissections of the head and neck muscles of representative members of sarcopterygian fish, amphibians, reptiles, monotremes and therian mammals, such as rodents, tree-shrews, colugos and primates, including modern humans, are compared with the information available in the literature. Our observations and comparisons indicate that the number of mandibular and true branchial muscles (sensu this work) present in modern humans is smaller than that found in mammals such as tree-shrews, rats and monotremes, as well as in reptiles such as lizards. Regarding the pharyngeal musculature, there is an increase in the number of muscles at the time of the evolutionary transition leading to therian mammals, but there was no significant increase during the transition leading to the emergence of higher primates and modern humans. The number of hypobranchial muscles is relatively constant within the therian mammals we examined, although in this case modern humans have more muscles than other mammals. The number of laryngeal and facial muscles in modern humans is greater than that found in most other therian taxa. Interestingly, modern humans possess peculiar laryngeal and facial muscles that are not present in the majority of the other mammalian taxa; this seems to corroborate the crucial role played by vocal communication and by facial expressions in primate and especially in human evolution. It is hoped that by compiling, in one paper, data about the head and neck muscles of a wide range of sarcopterygians, the present work could be useful to comparative anatomists, evolutionary biologists and functional morphologists and to researchers working in other fields such as developmental biology, genetics and/or evolutionary developmental biology.
... Agamids typically use their tongue to capture prey. During capture, the tongue is protruded beyond the margin of the lower jaw (Schwenk and Throckmorton 1989; Smith 1988; Schwenk 2000). The hyoid, supporting the tongue, is also protracted during prey capture to a position where the entoglossal process is also protruding from the mouth. ...
Electromyography (EMG), or the study of muscle activation patterns, has long been used to infer central nervous system (CNS) control of the musculoskeletal system and the evolution of that control. As the activation of the muscles at the level of the periphery is a reflection of the interaction of descending influences and local reflex control, EMG is an important tool in integrated investigations of the evolution of coordination in complex, musculoskeletal systems. Yet, the use of EMG as a tool to understand the evolution of motor control has its limitations. We here review the potential limitations and opportunities of the use of EMG in studying the evolution of motor control in vertebrates and provide original previously unpublished data to illustrate this. The relative timing of activation of a set of muscles can be used to evaluate CNS coordination of the components in a musculoskeletal system. Studies of relative timing reveal task-dependent variability in the recruitment of different populations of muscle fibers (i.e., different fiber types) within a single muscle, and left-right asymmetries in activation that need to be taken into account in comparative studies. The magnitude of muscle recruitment is strongly influenced by the instantaneous demands imposed on the system, and is likely determined by local reflex-control systems. Consequently, using EMG to make meaningful inferences about evolutionary changes in musculoskeletal control requires comparisons across similar functional tasks. Moreover, our data show that inferences about the evolution of motor control are limited in their explanatory power without proper insights into the kinematics and dynamics of a system.
... The tongue body could be essential in the prey keeping inside the oral cavity preventing the escape not only for the aboral orientation of the papillae but also for the presence of deep inter-papillary spaces determinant for the adhesion, while the root could have an important role helping the deglutition for the presence of numerous caliciform cells. The morphological description matches that of other reptiles with terrestrial lifestyle and can be correlated, without any doubt, with the diet and also the different roles described are in accordance with the behaviour and ecological information about these species (Smith, 1986(Smith, , 1988Bell, 1989Bell, , 1990Delheusy et al., 1994;Cooper, 1997;Bonacci et al., 2008;Abbate et al., 2009). ...
With 4 figures
The Italian lizard (Podarcis sicula) is the most diffused reptile in Italy, but it is also present in other European countries. This lizard belongs to the Lacertidae family, lives near walls, slants and along the borders of the paths; its diet includes bugs and aracnids. No data are so far available in literature about the three-dimensional morphology of the tongue of Podarcis sicula, therefore the aim of the present paper was to study by scanning electron and light microscopy the three-dimensional characteristics of the dorsal lingual surface and moreover the presence of chemosensory receptors like the taste buds in the oral cavity. Our results demonstrate that the Podarcis sicula tongue is a triangular muscular membranous organ, dorsoventrally flattened and that three different areas can be observed: a bifid apex, a body and a root. No papillae were observed in the apex, characterized by a flattened mucosa and by two deep median pouches. In the body cylindrical papillae with a flat surface are present, aborally gradually substituted by imbricated papillae. Foliate-like papillae were observed in the lateral parts of the tongue body. No sensory structures were showed on the lingual dorsal surface, while they were numerous in the oral cavity, particularly on the gingival epithelium. The light microscopy shows, on the dorsal surface, a stratified pavimentous not keratinized epithelium, conversely keratinized along the ventral surface. Many caliciform cells on the lateral parts of the papillae, deputed to the secretion of mucus, were also observed. Therefore, the results obtained in this paper could give a contribution to the knowledge of the tongue anatomy in a species widely diffused in different European countries and could be of help for clinical purposes in reptiles.
... Therefore, the information about the taste of food being eaten could be given by other structures like the vomero-nasal organ as in other vertebrates with crossed tongue and hence, further investigations are necessary to confirm this hypothesis. The morphology of the tongue surface can be correlated with the diet and different roles, in accordance with that observed for other reptiles with a terrestrial lifestyle (Smith, 1986(Smith, , 1988Bell, 1989Bell, , 1990Delheusy et al., 1994), can be hypothesized for the different areas, thus matching all the behaviour and ecological information about this species (Greer, 1989;Cogger, 1994). There have been no previous three-dimensional morphological investigations of the lingual surface of this animal and hence our investigation could contribute morphological data for further studies on the oral cavity of Scincidae and could be of help for clinical purposes, considering the T. scincoides as a pet animal in many countries at present. ...
The blue-tongue lizard (Tiliqua scincoides) is a variety of large skink common throughout Australia. There are seven species of Tiliqua and all of them have long bodies, short limbs and short and robust tails. T. scincoides occurs in a wide range of habitats; its diet is omnivorous. When threatened, it opens the mouth and protrudes its characteristic large fleshy cobalt blue tongue. It is currently found as a popular species and also as a pet animal in the European countries. No data are available in literature about the morphology of the tongue of T. scincoides; therefore, the aim of the present study was to investigate by means of scanning electron microscopy and light microscopy, the anatomy of the dorsal lingual surface. Our results demonstrate the presence of a tongue tip with a smooth surface without papillae. The foretongue was characterized by a stratified epithelium with foliate-like papillae and deep inter-papillar spaces in the middle part and cylindrical papillae with a flat surface in the lateral parts. All the posterior area of the tongue was characterized by more compacted papillae and the inter-papillar spaces were very narrow. Light microscopy showed the presence of melanin throughout the tongue. No taste buds were recognized on the lingual dorsal surface. Therefore, the papillae probably have a mechanical function showing an important role in the swallowing phase. The morphology of the tongue surface can be correlated to the diet and, different roles, as in other examined species, can be hypothesized for different areas.
A conspicuous feature of extant tetrapods is a movable tongue that plays a role in food uptake, mastication, and swallowing. The tongue is a muscle mass covered by a mucosal sheath, but the tongues of amphibians, reptiles, birds, and mammals are diverse in general morphology and function. For example, in frogs and toads, a component of the musculus genioglossus serves as an intrinsic tongue muscle, with the anterior part of the tongue attached to the floor of the oral cavity. Nevertheless, these features of the tongue have allowed Anurans to diversify and disperse worldwide. On the other hand, the salamander tongue is connected to the oral cavity by a root with a cartilage or a bony skeleton, and it is mainly comprised of projection and retractor muscles. In this respect, the salamander tongue seems more similar to that of reptiles and mammals than to those of frogs and toads. The morphology and function of the tongues of some reptiles, such as chameleons, and some mammals, such as nectar-feeding bats, are examples of extreme specialization. Finally, the tongue has become almost vestigial in a few species of anurans, turtles, and birds. This review summarizes and discusses many specializations of tongue form and function among tetrapods.
One of the major features of the aquatic-to-terrestrial transition in vertebrate evolution was the change in the mechanism used to transport prey from the jaws to the throat. Primarily, vertebrates use hydraulic transport, but the transition to terrestrial life was accompanied by modifications of the hyobranchial apparatus that permit tongue-based transport. Despite an extensive data base on amniote feeding systems and mechanisms of intraoral prey transport, few data are available on the mechanism of prey transport in anamniote tetrapods. Transport cycles of four Ambystoma tigrinum (Amphibia) feeding on worms and crickets were filmed at 150 flames per second to produce quantitative profiles of the intraoral transport cycles for the two prey types. During the transport cycle the head and body remain stationary relative to the background: transport in Ambystoma tigrinum thus does not involve inertial movements of the head or body. Prey type had little effect on the kinematics of prey transport. The process of prey transport may be divided into four phases: preparatory, fast opening, closing, and recovery. The preparatory phase itself is divided into two parts: an extended segment that may include slight slow opening and a static phase prior to mouth opening where no change in gape occurs. The kinematic profile of transport in terrestrial salamanders is extremely similar to that used by fishes during hydraulic (aquatic) prey transport. We hypothesize that the distinct recovery and preparatory phases in the transport cycle of anamniote tetrapods are together homologous to the slow opening phases of the amniote cycle, and that during the evolution of terrestrial prey processing systems the primitive extended preparatory phase has become greatly compressed and incorporated into the amniote gape cycle.
Introduction Prey location, capture, and subsequent processing are fundamentally important behaviors critical to the assimilation of food resources. All three of these behaviors involve movements of the tongue and jaws and it is well known that both tongue movements and tongue morphology vary widely among lizards (Schwenk, 2000). A central element of the sit-and-wait (ambush) vs. wide foraging paradigm involves the trade-off between prey capture function and chemosensory acuity. In general, ambush feeders are thought to use the tongue primarily to capture prey located visually, whereas wide foragers are thought to have traded tongue-based prey capture for tongue-flicking, which is critical to locating widely dispersed prey by using chemoreception (Pianka and Vitt, 2003; Cooper, 1997a). The switch to chemosensory tongue function among scleroglossan lizards is certainly linked to their wide-foraging strategy; in fact, this transition has enabled wide foragers to dominate lizard communities worldwide (Vitt et al., 2003). In this chapter we examine the trade-off between feeding behaviors (prey capture and subsequent prey processing) and chemosensory function in lizards with data available to date. First, we present new data and a review of kinematic patterns of “prey capture” behaviors. This analysis illustrates three basic prey capture modes used by lizards. Next, we review patterns of post-capture prey processing behavior that reveal three evolutionary transitions in lizard “chewing” behavior. Finally, we compare changes in lizard feeding behavior with quantified characteristics of the vomeronasal system, tongue morphology, prey discrimination ability, and foraging behavior from the literature to examine how changes in feeding function correlate with changes in chemosensory function. é Cambridge University Press 2007.
Background: The suitability of micro-computed tomography (CT) for soft tissue applications has been well documented. Although the application of micro-CT to the three dimensional (3D) structure of the tongue muscle has been reported, a 3D rendering and/or a schematic view of the tongue muscle has yet to be published. Material and Method: First, muse tongues were fixed and de-calcified, and then the vertical muscle (Ve), the transverse muscle (Tr), and/or the genioglossus muscle of the mouse tongue (Ge) were analyzed using micro-CT and are shown in this report in rendered images and pattern diagrams. Results: 1) The Tr is classified into three parts: the first part extends from the middle to the apical part of the tongue; the second part is strongly connected to the superior longitudinal muscles of the tongue (Lo); the third part fans out from the middle to the root of the tongue. 2) The Ve is classified into two main groups: the first group joins the dorsal and the lateral parts of the tongue; the second group joins the dorsal part and the floor of the tongue. 3) Ge is classified into four parts: three parts comprise the Ge apical and middle parts of the tongue, with one part in the inferior longitudinal muscles of the tongue, one joining the lingual septum of the tongue (LS), and the other joining the sub-surface of the dorsal part of the Lo. The remaining Ge exits in a fan-like manner through the root of the tongue and then joins the Tr.
The hyolingual system of Squamata is a highly versatile system used in different feeding, drinking, chemoreception, and social behaviors. In each of these activities, either the entire hyolingual system or one of its elements is used. For instance, in the majority of lizards, the tongue acts as the main element for liquid uptake, intraoral food and liquid transport, and in chemoreception, whereas the hyoid apparatus plays a major role during social interactions by acting on the ventral floor of the throat. In varanids, the hyoid apparatus is involved in both deglutition of foods and liquids, and during social displays.
This chapter focuses on the origin of the amniotic feeding mechanisms as a key event in the evolution of the vertebrate skull. However, it rather describes feeding systems within various amniotes clades, which have been viewed elsewhere. The analysis is centered on the single general theme and contents. In order to understand amniotic feeding mechanisms and their diversifications, it is essential first to understand the structure and the function of the feeding mechanisms in out-group clades. Thus, it examines the feeding mechanisms of fishes and amphibians as a method of determining the functional traits that are likely to have been primitively present in amniotes, and suggests that further experimental studies of extant amniotes and anmniotes taxa can provide a better understanding of evolution of amniotes and more generally vertebrate feeding mechanisms. Various examples for better understanding of general principles of divergence between aquatic and terrestrial feeding systems are discussed. It further explains many functional attributes of the feeding mechanisms of amniotes.
Publisher Summary
Within Neornithes (modern birds), monophyly of the nominal taxa Paleognathae is disputed. Divergence of the two putative lineages may have occurred as long as 120 million years ago during the Cretaceous period, but there is no consensus on which group is more phenotypically primitive. The large, sometimes giant, flightless ratites include 10 species in six extant genera and two extinct groups. Ratites are believed to have reached their modern pattern of distribution on southern land masses by means of vicariance and dispersal via land routes across Antarctica during the late Cretaceous and/or early Tertiary, approximately 80 to 50 million years ago. Paleognathous birds possess a small tongue, a mostly cartilaginous hyobranchial skeleton and feed cranioinertially. The purpose of this chapter is twofold. First, the morphology and function of the paleognathous hyolingual apparatus are described and compared to the generalized neognathous condition. Second, these data are compared to comparable data for fossil and extant reptilian outgroups to determine whether the paleognathous or the neognathous condition is representative of the primitive condition for neornithine birds. The evolutionary origins of the modern avian hyolingual apparatus and of two basic types of avian feeding—ratite (obligate) cranioinertial feeding and avian lingual feeding—are discussed.
The purpose of this study was to show the benefit of visualizing a tree-dimensional (3D) image of the tongue's muscle structure, which until now has been regarded as fully understood. Until now, no suitable 3D observation methods have been developed for soft tissue, such as the tongue, using histological magnification. For this purpose, this study used a micro-computed tomographic method (micro-CT) and image processing after the fixation, decalcification, and dehydration of a mouse tongue. Results: 3D rendered images of tongue muscles obtained by micro-CT showed every muscle and their relationships to each other. The superior longitudinal and the hyoglossus muscles of the tongue made up one group, while the inferior longitudinal and the styloglossus muscles of the tongue made up another. The boundary of the two muscles in each group was difficult to distinguish. On the other hand, what appear to be newly described muscles were identified. These results indicate that our micro-CT method is beneficial and that classical knowledge of tongue muscles derived from two-dimensional (2D) images does not fully describe the actual complexity of the tongue muscles. In our opinion, 3D rendered images mixed with raw structure can provide a more in-depth picture of the tongue from an integrated as well as an analytical perspective.
One of the major features of the aquatic-to-terrestrial transition in vertebrate evolution was the change in the mechanism used to transport prey from the jaws to the throat. Primarily, vertebrates use hydraulic transport, but the transition to terrestrial life was accompanied by modifications of the hyobranchial apparatus that permit tongue-based transport. Despite an extensive data base on amniote feeding systems and mechanisms of intraoral prey transport, few data are available on the mechanism of prey transport in anamniote tetrapods. Transport cycles of four Ambystoma tigrinum (Amphibia) feeding on worms and crickets were filmed at 150 frames per second to produce quantitative profiles of the intraoral transport cycles for the two prey types. During the transport cycle the head and body remain stationary relative to the background: transport in Ambystoma tigrinum thus does not involve inertial movements of the head or body. Prey type had little effect on the kinematics of prey transport. The process of prey transport may be divided into four phases: preparatory, fast opening, closing, and recovery. The preparatory phase itself is divided into two parts: an extended segment that may include slight slow opening and a static phase prior to mouth opening where no change in gape occurs. The kinematic profile of transport in terrestrial salamanders is extremely similar to that used by fishes during hydraulic (aquatic) prey transport. We hypothesize that the distinct recovery and preparatory phases in the transport cycle of anamniote tetrapods are together homologous to the slow opening phases of the amniote cycle, and that during the evolution of terrestrial prey processing systems the primitive extended preparatory phase has become greatly compressed and incorporated into the amniote gape cycle.
Phenotypic evolution has been studied since Darwin established the fact of evolution. In contrast, molecular evolution has been a subject of study since the mid-1960s. Nevertheless, our understanding of the mechanisms of phenotypic evolution is far less developed than our knowledge of molecular evolution. This fact is often attributed to the greater “complexity” of phenotypic characters, although it is not always clear what complexity means. More specifically, there are two features of phenotypic evolution that make molecular and phenotypic evolution quite distinct problems. First, molecular evolution is a continuing process, often occurring over long periods of time at a nearly constant rate, even if there are variations in rate among lineages. In contrast, phenotypic evolution is perceived as a highly irregular process with long periods of stasis interrupted by short bursts of change (Gould and Eldredge, 1977; Kimura, 1983). Second, most phenotypic characters comprise many levels of organization from the molecular to the behavioral and the population level, and the rate of change is nonuniform across these levels of organization. Some attributes of the phenotype, such as color and size, vary widely and evolve rapidly whereas other aspects of the phenotype, such as mode of food acquisition, are remarkably stable. Furthermore, even the conservative elements of the phenotype are not immutable because they have evolved in ancestral lineages and may become variable in a descendant lineage. Molecular evolution, on the other hand, pertains to evolutionary change on only one level of organization.
Prey capture in Agama stellio was recorded by high-speed video in combination with the electrical activity of both jaw and hyolingual muscles. Quantification of kinematics and muscle activity patterns facilitated their correlation during kinematic phases. Changes in angular velocity of the gape let the strike be subdivided into four kinematic phases: slow open (SOI and SOII), fast open (FO), fast close (FC), and slow close-power stroke (SC/PS). The SOI phase is marked by initial activity in the tongue protractor, the hyoid protractor, and the ring muscle. These muscles project the tongue beyond the anterior margin of the jaw. During the SOII phase, a low level of activity in the jaw closers correlates with a decline of the jaw-opening velocity. Next, bilateral activity in the jaw openers defines the start of the FO phase. This activity ends at maximal gape. Simultaneously, the hyoid retractor and the hyoglossus become active, causing tongue retraction during the FO phase. At maximal gape, the jaw closers contract simultaneously, initiating the FC phase. After a short pause, they contract again and the prey is crushed during the SC/PS phase. Our results support the hypothesis of tongue projection in agamids by Smith ([1988] J. Morphol. 196:157–171), and show some striking similarities with muscle activity patterns during the strike in chameleons (Wainwright and Bennett [1992a] J. Exp. Biol. 168:1–21). Differences are in the activation pattern of the hyoglossus. The agamid tongue projection mechanism appears to be an ideal mechanical precursor for the ballistic tongue projection mechanism of chameleonids; the key derived feature in the chameleon tongue projection mechanism most likely lies in the changed motor pattern controlling the hyoglossus muscle.
Use of the tongue as a prehensile organ during the ingestion stage of feeding in lizards was studied cinegraphically in seven species. Within Squamata, lingual prehension is limited to a single clade, the Iguania (Iguanidae, Agamidae and Chamaeleontidae), which includes all ‘fleshy-tongued’ lizards. All remaining squamates (Scleroglossa) use the jaws alone for prey prehension. Lingual prehension and a ‘fleshy’ tongue are primitive squamate characteristics. Kinematically, lingual ingestion cycles are similar to previously described transport cycles in having slow open, fast open, fast close and slow close-power stroke phases. Tongue movements are sequentially correlated with jaw movements as they are in transport. However, during ingestion, anterior movement of the tongue includes an extra-oral, as well as intra-oral component. Tongue protrusion results in a pronounced slow open-II phase at a large gape distance. A high degree of variability in quantitative aspects of ingestion and transport cycles suggests that modulation through sensory feedback is an important aspect of lizard feeding. Preliminary evidence indicates an important role for hyoid movement in tongue protrusion. Our results are consistent with the Bramble & Wake (1985) model generalized feeding cycle and support their contention that specialized feeding mechanisms often represent modifications of a basic pattern, particularly modification of the slow open phase.
Tongue musculature in 24 genera of snakes was examined histologically. In all snakes, the tongue is composed of a few main groups of muscles. The M. hyoglossus is a paired bundle in the center of the tongue. The posterior regions of the tongue possess musculature that surrounds these bundles and is responsible for protrusion. Anterior tongue regions contain hyoglossal bundles, dorsal longitudinal muscle bundles and vertical and transverse bundles, which are perpendicular to the long axis of the tongue. The interaction of the longitudinal with the vertical and horizontal muscles is responsible for bending during tongue flicking. Despite general similarities, distinct patterns of intrinsic tongue musculature characterize each infraorder of snakes. The Henophidia are primitive; the Scolecophidia and Caenophidia are each distinguished by derived characters. These derived characters support hypotheses that these latter taxa are each monophyletic. Cylindrophis (Anilioidea) is in some characters intermediate between Booidea and Colubroidea. The condition in the Booidea resembles the lizard condition; however, no synapomorphies of tongue musculature confirm a relationship with any specific lizard family. Although the pattern of colubroids appears to be the most biomechanically specialized, as yet no behavioral or performance feature has been identified to distinguish them from other snakes.
Summary In this paper we document the activity of key muscles of the tongue, hyobranchial apparatus and head during prey capture in the lizard Chanzaeleo jacksonii Boulcnger and use these data to test current hypothescs of chameleon tongue function. Electromyographic recordings were made during 27 feedings from nine individuals and synchronized with high-speed video recordings (200fields sl), permitting an assessment of the activity of muscles relative to the onset of tongue projection, contact between tongue and prey, and tongue retraction. Four major results were obtained. (1) The hyoglossi muscles exhibit a single burst of activity that begins between 10 ms before and 20 ms after the onset of tongue projection and continues throughout the period of tongue retraction. (2) The accelerator muscle exhibits a biphasic activity pattern, with the first burst lasting about 185ms and ending an average of 10.6ms prior to the onset of projection. (3) The accelerator muscle shows regional variation in morphology that corresponds with variation in motor pattern. The anterior region of the muscle, unlike the posterior portion, exhibits only a single burst of activity that begins 2.5ms after the onset of tongue projection and is thus not involved in launching the tongue. (4) The geniohyoidei, sternohyoidei, sternothyroidei, depressor mandibulae, adductor mandibulae and pterygoideus all exhibit activity patterns consistent with previously reported kinematic patterns and their pro- posed roles. The major implications of these results for models of the chameleon feeding mechanism are (1) that the hyoglossi do not act to hold the tongue on the entoglossal process during a loading period prior to tongue projection, and (2) that the presence of 185 ms of intense activity in the accelerator muscle prior to tongue projection suggests the presence of a preloading mechanism, the nature of which is the subject of the companion paper.
High-speed cinematography was employed to study the mechanics of prey capture in Anolis equestris. Capture of live prey (adult locusts) consists of a cyclic movement of the upper and lower jaws combined with tongue protraction. Kinematic profiles are presented for the jaws, tongue, and forelimbs. The tongue is projected during the "slow open" stage and most of the "fast open" stage. The tongue protrudes beyond the mandibular symphysis during the slow open stage, and rotates simultaneously around a transverse anteromedian axis. The prey is thus contacted by the dorsal sticky surface of the tongue, and then pulled backward into the oral cavity by a combination of a forward movement of the jaws and retraction of the tongue. Gape angle, defined as the angle between the upper and lower jaws, continues to increase during the initial stages of tongue retraction. During the capture process, the anterior part of the body lunges forward, followed by a return to its original position; this displacement is mediated by the forelimbs, which usually remain well anchored to the floor. The cyclic food-capture movements of the jaws and tongue–hyoid system in A. equestris (Iguanidae) and Chameleo dilepis (Chamaeleontidae) are compared. I argue that one of the primary selection forces in the evolution of the different mechanisms of prey prehension in these two lizard groups was enhancement of the locomotor system and, consequently, foraging ability.
From lizards to snakes, the trophic system of squamates exhibits at least six major modifications correlated with different feeding strategies. Beginning in lizards, these include 1) shift from tongue to jaws as the primary means of prey capture, accompanied by specialization of the tongue for chemoreception, and 2) increasing skull kineticism. These features continue into snakes along with 3) unilateral jaw displacement during swallowing accompanied by 4) increasing skull kineticism, 5) development of the cervical vertebrae into a lever system for launching the strike, 6) addition of sensory modalities (thermoreception) in some snakes, and in advanced snakes, 7) shift from mechanical to chemical means of predation. Many fundamental features elaborated into the highly kinematic and jaw-based feeding system of snakes actually appear first within lizards. However, the highly kinetic skull of snakes represents not so much an extrapolation of lizard kinesis, as it does a rebuilding, even redesign, of the skull to achieve its high level of kinesis.
Scanning electron microscopy shows that lingual papillae occur all over the dorsal surface of the tongue of the freshwater turtle, Geoclemys reevesii. The surface of each papilla is composed of compactly distributed hemispherical bulges, each composed of a single cell. Microvilli are widely distributed over the surface of cells. Histological examination reveals that the connective tissue penetrates deep into the center of papillae and that the epithelium is stratified columnar. Under the transmission electron microscope, the cells of the basal and the deep intermediate layers of the epithelium appear rounded. A large nucleus lies in the central area of each cell. The cytoplasm contains mitochondria, endoplasmic reticulum and free ribosomes. The cell membrane form numerous processes. The shallow intermediate layer contains two types of cell. The cytoplasm of the first has numerous fine granules, in addition to mitochondria, ribosomes, and endoplasmic reticulum. The other type of cell contains highly electron-dense granules. The surface layer shows two cell types. One type consists of typical mucous cells. The other type of cell contains fine, electron-lucent granules. The latter cells lie on the free-surface side, covering the mucous cells, and have microvilli on their free surfaces.
High speed video recordings (200 fields per second) of prey capture and food processing in Agama agama permit the identification of strikes, chews and transport movements. Ten variables from strike movements and seven variables from chewing sequences are digitized; transport movements are inspected only. Univariate and multivariate statistical analyses disclose significant interindividual differences for three variables (maximum gape distance, maximum head angle, and maximum throat distance); but neither these nor principal components analysis show differences between strikes and chews for any of the gape change and hyoid depression variables. However, strikes and chews obviously differ in tongue protrusion and body movements. Chewing may be divided into four stages, comparable to those of transport cycles of other lizards and the generalized tetrapod model. Transport differs from chewing by having a shorter power stroke and relatively more cranial and less jaw movement. The kinematics of feeding in Agama agama are compared with those of other lizards studied previously.
A quantitative analysis of the muscle activity patterns (motor patterns) used by tiger salamanders (Ambystoma tigrinum) during terrestrial feeding is presented to provide comparative data on motor output during prey transport in amphibians, compare prey transport motor patterns to those used during initial prey capture, and test the generality of previously proposed models of the feeding cycle in tetrapods.
Simultaneous electromyographic and kinematic recordings during prey transport reveal four phases in the prey transport cycle. The Preparatory phase precedes prey transport with activity found mainly in muscles of the buccal floor (genioglossus, geniohyoideus, interhyoideus, and inter-mandibularis), but with all muscles silent at the end of this phase. Prey transport occurs during the Fast Opening and Closing phases. The Fast Opening phase begins with near simultaneous onset of activity in all jaw and hyoid muscles, including anatomical antagonists such as the depressor mandibulae and adductor mandibulae. The subarcualis rectus one muscle is active during the Fast Opening and Closing phases of transport despite the lack of accompanying tongue projection and may function to stabilize the hyobranchial apparatus. The motor pattern of terrestrial prey transport differs considerably from that of initial prey capture, but appears to be similar to the motor pattern used during aquatic prey capture and hydraulic prey transport. We hypothesize that post-metamorphic tiger salamanders accomplish terrestrial prey transport by retaining the larval motor pattern employed during suction feeding. The motor pattern and kinematics of prey transport in Ambystoma tigrinum differ in nearly all aspects from previous models of the generalized tetrapod feeding cycle.
Hypotheses of secondary evolutionary change, where alteration in a particular feature is thought to result in change in another, can be tested in two main ways. First, phylogenies can be used to identify separate cases where one of the features changes and each case can then be examined to see whether the other change also actually takes place and if the perceived sequence of the alterations is appropriate. Secondly, the mechanism by which change in the second feature is supposed to be effected can be scrutinized and, in some cases, subjected to experimental investigation.
This approach was applied to a recent hypothesis, that backward spread of the caudifemoralis longus muscle in the tail base of lizards was the primary cause of loss of capacity to autotomize the tail. Some 23 to 25 independent cases of total autotomy loss in adult lizards were identified. In all but six of these there was no substantial spread of the muscle. In two of the remainder, the muscle appears to have spread ufiev autotomy loss, and another case cannot be tested properly as information about relationships is equivocal. The final three cases exhibit extension of the caudifemoralis longus before autotomy loss, but the latter is not found in related species that also inherit muscle extension, which suggests that other causal factors may be involved. In about 15 other cases, where autotomy becomes restricted to the tail base, there is no marked spread of the caudifemoralis longus. The proposed functional link between muscle extension and autotomy loss is also discussed and discounted
Anolis carolinensis has two aggressive displays involving movements of the hyoid apparatus: erection of the throat and extension of the dewlap. Erection of the throat is an enlargement of the gular region and dewlap extension consists of a vertical erection of the gular flap. Cinefluoroscopy and high speed cinematography show that the dewlap is extended in three phases: 1) protraction of the entire hyoid apparatus; 2) forward pivoting movement of the ceratobranchials II; and 3) retraction of the ceratobranchials II and the entire hyoid apparatus. The cartilaginous elements of the hyoid apparatus are variably mineralized. The entoglossal process and the hypohyals are the most calcified elements. The mineralized portion of the hyoid body, to which the other elements articulate, presents a complex pattern. The calcification of entoglossal process and the hypohyals stop just where they are fused with the hyoid body. The hyoid body presents four mineralized masses, two central corresponding to the base of the ceratobranchials II and two lateral being the head of the ossified ceratobranchials I. The lateral masses articulate on the central masses by a synovial joint. Morphologically, the ceratobranchials II form the hyoid body and become separated at the mid length of the synovial articulation of the ceratobranchials I and the hyoid body. The calcified matrix of the ceratobranchials II gradually changes from a large calcified mass (within the hyoid body) to a semicircle, opened ventrally, which permits their bending during dewlap extension. The highly mineralized posterior tip of the entoglossal process and the hyoid body serve as a pivot to pivoting forward movement of the ceratobranchials II producing at the change of the pattern of mineralization. Forward movement of the ceratobranchials II is produced by electrical stimulation of the M. branchio hyoideus. The opposition of the throat skin to the movement of the ceratobranchials II produces the bending of those longest elements. Electrical stimulation of the hyoid muscles confirms the key role of M. branchiohyoideus during dewlap extension. Simultaneous contractions of all the hyoid and extrinsic tongue (retractor and protractor) muscles with the M. branchiohyoideus during dewlap extension may be a possible motor pattern for dewlap extension in Anolis lizards.
The feeding mechanism of Epibulus insidiator is unique among fishes, exhibiting the highest degree of jaw protrusion ever described (65% of head length). The functional morphology of the jaw mechanism in Epibulus is analyzed as a case study in the evolution of novel functional systems. The feeding mechanism appears to be driven by unspecialized muscle activity patterns and input forces, that combine with drastically changed bone and ligament morphology to produce extreme jaw protrusion. The primary derived osteological features are the form of the quadrate, interopercle, and elongate premaxilla and lower jaw. Epibulus has a unique vomero-interopercular ligament and enlarged interoperculo-mandibular and premaxilla-maxilla ligaments. The structures of the opercle, maxilla, and much of the neurocranium retain a primitive labrid condition. Many cranial muscles in Epibulus also retain a primitive structural condition, including the levator operculi, expaxialis, sternohyoideus, and adductor mandibulae. The generalized perciform suction feeding pattern of simultaneous peak cranial elevation, gape, and jaw protrusion followed by hyoid depression is retained in Epibulus. Electromyography and high-speed cinematography indicate that patterns of muscle activity during feeding and the kinematic movements of opercular rotation and cranial elevation produce a primitive pattern of force and motion input. Extreme jaw protrusion is produced from this primitive input pattern by several derived kinematic patterns of modified bones and ligaments. The interopercle, quadrate, and maxilla rotate through angles of about 100 degrees, pushing the lower jaw into a protruded position. Analysis of primitive and derived characters at multiple levels of structural and functional organization allows conclusions about the level of design at which change has occurred to produce functional novelties.
The movements of the hyoid apparatus ofAnolis equestris, during mechanical reduction of prey, have been studied by cinefluoroscopy. In the SO and FO stages, ceratobranchials I move forward faster than the ceratohyals. Muscle stimulation experiments show that contractions of the m. ceratohyoideus and m. mandibulohyoideus I produce this movement. The other hyoid and extrinsic muscles of the tongue may be divided into protractors and retractors. In the FC-SC stage, the tongue-hyoid complex moves backward. The movements of ceratobranchials II follow those of the other elements after a short delay.
We have developed a quantitative model of an example of a muscular hydrostat, a reptilian tongue, and have used this model to study a functional movement, protrusion and retrusion, a form of lapping. The model tongue consists of a longitudinal muscle that shortens the tongue when it contracts, and a circumferential muscle wrapped around the longitudinal muscle that lengthens the tongue when it contracts. The anatomy of the model tongue and the pattern of activation of its muscles are based on studies of the tongue of the lizard Tupinambis nigropunctatus (Smith 1984). The mechanics of pressure vessels were used to derive a relationship between the forces in the two muscles. Muscle force production was modelled as the product of length/tension properties, force/velocity properties, and activation due to neural inputs (incorporating both recruitment and firing period). Passive forces were modeled as a force in parallel with the longitudinal muscle. Muscle activation dynamics were modeled as a first order low pass filter. When the model tongue is short, the two muscles can lengthen or shorten it with comparable forces, but as it lengthens, the force that the circumferential muscle can exert drops precipitously. When the tongue is long, it can neither be very stiff, nor can it generate much force. The model also reproduces the kinematics of lapping movements actually observed in Tupinambis.
The morphology and histology of the tongue in Sphenodon punctatus are described and used to infer function and to determine character state polarities in lepidosaurs. The tongue lacks an anterior notch and is covered with filamentous papillae, including specialized gustatory papillae containing taste buds. Lingual glands are restricted to mucocytes covering the papillae. Three intrinsic tongue muscles are identified and shown to be discrete fiber systems and not merely elaborations of the M. hyoglossus. These muscles interact with a connective tissue skeleton, particularly three septal planes, to cause changes in tongue shape. Tongue protrusion is probably caused by hyoid protraction and contraction of posterior genioglossus fibers; retraction by hyoid retraction, hyoglossus contraction, and contraction of anterior genioglossus fibers.
It is argued that taste is important in prey discrimination and possibly in courtship. Vomeronasal function is probably mediated by inhalation and not tongue movement.
Insertion of genioglossus fibers into the buccal floor is a derived feature of lepidosaur tongues. Derived features of squamate tongues include an anterior bifurcation, a divided genioglossus comprising medial and lateral portions, ventral transverse and circular muscle fiber systems around the hyoglossus, and the presence of a median septum. The tongue of the squamate family Iguanidae shares many plesiomorphic features with Sphenodon .
The tongue and oral epithelium beneath and lateral to the tongue have been examined in 37 species of lizard representing all families except the Helodermatidae and Lanthonotidae. Taste buds occur in all species examined except Varanus indicus (Varanidae). They are found on the tongues of all remaining species except Gonatodes antillensis (Gekkonidae) and in the oral epithelia of all species except Chamaeleo jacksoni (Chamaeleonidae). Taste buds may be abundant, particularly in the Iguanidae, in which densities greater than 104/ mm2 occur. These observations are contrary to statements in the literature which have assumed taste buds to be rare or absent in lizards. Lingual taste buds are more or less restricted to regions of thick, stratified squamous epithelium. They occur most frequently on the tongue tip and the ventrolateral margins of the foretongue, though they may be found anywhere. Insufficient data exist to distinguish between taste and vomeronasal function as the basis for chemosensory-mediated behavior in lizards. It is, therefore, premature to assume the latter. Substrate licking might mediate gustation rather than vomeronasal function, particularly in iguanian lizards.
Amphibolurus barbatus has a threat display which includes the erection of the gular regions as a frill and may also include wide opening of the mouth to display a yellow mouth lining. Frill erection involves protraction, depression, and lateral expansion of the hyoid apparatus. Electrical stimulation of the hyoid muscles and dissection of the hyoid apparatus were used to examine specializations for producing frill erection. Specializations of the hyoid skeleton include the absence of a ceratobranchial II, presence of a synovial joint between the ceratohyal and body of the hyoid, and combined shortening of the entoglossal process and lengthening of the posterior arches. The only apparent specialization of the hyoid musculature is the anterior displacement of the origin of m. hyomandibularis. All of the hyoid muscles are involved in some way in frill erection and the actions of each muscle is described. The characteristic frill erection in the threat display of Amphibolurus barbatus is possible because of the 1:2 ratio of the anterior and posterior parts of the apparatus and the absence of the ceratobrnchial II.
In the families Agamidae, Gerrhosauridae, Iguanidae, and Scincidae, species that weigh more than 300 g are almost all herbivores, whereas those weighing less than 50-100 g are carnivores. Juveniles of large herbivorous species tend to be carnivorous until they reach body weights of 50-300 g. Diet is compared to metabolic expenditure in these lizards. Although smaller animals have higher weight-specific metabolic rates, the greater total metabolic rate of larger animals requires a greater caloric intake. Juvenile animals and species of small body size are primarily insectivorous. It is postulated that larger animals of these families are unable to meet caloric demands on a diet of insects, have no practical alternative animal prey, and rely instead on vegetation. The families Anguidae, Chamaeleontidae, Helodermatidae, Teiidae, and Varanidae do not include herbivorous species, although each family has species that weigh more than 300 g. Morphological, ecological, and physiological specializations in these families account for the absence of herbivorous species. For an unspecialized lizard, evolution of large body size both requires and permits an herbivorous diet.
Thesis (Ph. D. in Zoology)--University of California, Berkeley, Dec. 1984. Includes bibliographical references.
The form and texture of the tongue has long been one of the major bases for the classification of lizards, as evidenced by such herpetological catalogues as de Rooij (1915) that base the “synopsis of families” principally on the tongue, and by the “-gjossa” names for higher groups of lizards in the older literature (e.g., Pachyglossa, Leptoglossa, Thecaglossa, Diploglossa, all used by Cope, 1900, but taken by him from earlier authors). I can find no case where a lizard was referred to a particular group on the basis of tongue structure but subsequently found, from other evidence, to be unrelated. On the other hand, in two cases families of lizards have been referred to higher groups against the evidence of the tongue, and subsequent study of the osteology has shown such reference to be in error: the Pygopodidae were referred by Camp (1923) to the same group as that containing Anguidae, Xenosauridae, Anniellidae, Helodermatidae, and Varani-dae, in spite of a very different tongue; but McDowell and Bogert (1954) and Underwood (1957) showed that the Pygopodidae are most closely related to the Gekkonidae, with which they agree in tongue structure as well as many other features.
A study of wild Agama bibroni indicated that adults fed largely on Orthoptera with an active selection for species in the middle to large size range. The juvenile diet was mainly of Hymenoptera, Formicidae. This dietary difference led to a study of jaw mechanisms suggesting that due to a differential growth of the cranial bones, particularly those of the lower jaw, the mechanical advantages of the adult and juvenile jaws differed considerably. This allowed the rapid bite of the adult to be two and a half times more powerful, per unit area, than that of the juvenile. During slow close there was almost no difference in efficiency. From this it is suggested that the differing diets are not only the result of different habitats but also due to skeletal arrangements.
• 1The hyoid apparatus and tongues of fifteen reptiles are described and discussed.
• 2The patterns formed by the transverse muscles of the throat are classificatory importance, as are also the intrinsic muscles of the tongue. The study of these muscles throws new light on the position of the families Iguanidae and Chameleontidæ.
• 3The hyoid apparatus and its muscles exhibit variations too numerous to provide data of taxonomic importance. The gular structures, as well as protrusible tongues, are aided by specially modified devices of the hyoid apparatus.
• 4The mechanism of the protrusible tongues of reptiles is described.
• 5The hyoid apparatus and the muscles of the tongue and throat co-operate in making the buccal cavity an active agent in the respiratory mechanism of most reptiles.
The dentition of the African lizard Agama agama was examined in a range of material from late embryos and hatchlings to individuals of advanced age. Most of the skulls were prepared as dry specimens, but observations were also made on the living lizards in captivity and some records of tooth replacement collected.
The gross anatomy of the dentition is described and its growth and elaboration from the hatchling to the adult. Attachment of the two types of tooth, both acrodont and pleurodont, is considered and the replacement process is found to be sufficiently different from that of other lizards to justify a separate descriptive category.
Evidence from both dead and living material as to the order of tooth replacement in Agama is analysed and found to conform to the hypothesis of Edmund (1960). Other agamid genera are briefly described.
The similarity between agamid and mammalian dentitions is pointed out and a connection suggested between polyphyodent reptilian dentitions and the diphyodont mammalian dentition which is more correctly regarded as being composed of two Zahnreihen.
The use of the tongue and hyoid is examined in cineradiographic and electromyographic investigations of feeding in two species of lizards, Ctenosaura similis (Iguanidae) and Tupinambis nigropunctatus (Teiidae). In both animals food is transported through the oral cavity by regular cycles of the tongue. Tongue movements correlate with jaw and hyoid movement. Similarities between the two animals in the use of the tongue in food transport, lapping, pharyngeal packing, and pharyngeal emptying are detailed. Mechanisms of tongue protrusion are examined and it is shown that the tongue in Tupinambis is relatively more protrusible than in Ctenosaura. This difference is complementary with data on the greater reliance of Tupinambis on the tongue as a sensory organ. Tupinambis further differs from Ctenosaura in possessing a greater mobility of the hyoid. In many features of tongue use in food transport, lizards resemble mammals, supporting postulations of a basic pattern of intra-oral food transport. However, whether this pattern can be attributed to convergence or a common, primitive neural pattern of control cannot be distinguished. Lizards lack two major characteristics of mammalian food transport: regular masticatory cycles and an internal swallowing mechanism.
The morphology and function of the tongue and hyoid apparatus in Varanus were examined by anatomical and experimental techniques. Morphological features unique to Varanus include a highly protrusible tongue that has lost a roughened dorsal surface, an exceptionally strong and mobile hyobranchial apparatus, a well-defined joint between the ceratohyal and anterior process, and a series of distinct muscles inserting at the anterior hyobranchial region. Varanus is also unusual among lizards in a number of feeding behaviors; it ingests prey entirely by inertial feeding, as the tongue does not participate in food transport. Further specializations include an increased reliance on hyobranchial movements in drinking and pharyngeal packing and compression. The long, narrow tongue is most likely related to the mechanics of tongue protrusion; the increased amount, strength, and complexity of hyobranchial movement is related to the fact that the hyobranchium in Varanus replaces the tongue in many functions. Previous hypotheses for the origin of these adaptations are discussed, and the difficulties of attributing these specializations to any specific scenario of adaptation or constraint are emphasized.
Many lizards and all snakes flick their tongues. It is known that this unique behavioral pattern serves to collect airborne and substrate chemicals which give the animal information via Jacobson's Organ about the location of food, conspecifics, and possibly other environmental factors. However, a comparative topographic analysis of tongue movements in squamate reptiles is lacking, and it might shed light on the evolution of this behavior.
In this study, a survey was made of the lizards and snakes which tongue-flick. Observations and films were made of 25 lizard species representing 10 families and 30 snake species representing 5 families.
The information from observations and film analyses of representative species was used to hypothesize the steps of the evolution of tongue-flicking from the simple downward extensions of primitive lizards to the complex multiple oscillations of snakes.
Muscular-hydrostats, muscular organs which lack typical systems of skeletal support, include the tongues of mammals and lizards, the arms and tentacles of cephalopod molluscs and the trunks of elephants. In this paper the means by which such organs produce elongation, shortening, bending and torsion are discussed. The most important biomechanical feature of muscular-hydrostats is that their volume is constant, so that any decrease in one dimension will cause a compensatory increase in at least one other dimension. Elongation of a muscular-hydrostat is produced by contraction of transverse, circular or radial muscles which decrease the cross-section. Shortening is produced by contraction of longitudinal muscles. The relation between length and width of a constant volume structure allows amplification of muscle force or displacement in muscular-hydrostats and other hydrostatic systems. Bending requires simultaneous contraction of longitudinal and antagonistic circular, transverse or radial muscles. In bending, one muscle mass acts as an effector of movement while the alternate muscle mass provides support for that movement. Torsion is produced by contraction of muscles which wrap the muscular-hydrostat in a helical fashion.
Thesis (Ph. D.)--Jena University, 1932. Reprinted from "Jenaischen Zeitschrift für Naturwissenschaft", v. LXVI, pt. 3.
http://deepblue.lib.umich.edu/bitstream/2027.42/56338/1/MP094.pdf
The three-dimensional structure of alveolar epithelial type II cells was imaged using a computer-based system designed for reconstruction and quantitative analysis of serially sectioned specimens. Six type II cells were reconstructed from serial ultrathin sections of lungs from two Sprague Dawley male rats and the results were compared to standard morphometric estimates of type II cell composition from five other Sprague Dawley male rats. A minor portion of the type II cell surface was in contact with the alveolar airspace while most of the cell surface was embedded in the alveolar septal interstitium. The type II cells contained multiple Golgi regions located close to the nucleus. Mitochondria formed a few branching filamentous networks extending throughout the cell. The reconstructed cells appeared to represent a homogeneous population having fractional volumes of intracellular organelles very similar to those found by morphometric techniques. The spatial distribution of secretory organelle volume suggests that the organization of this cell type reflects an ordered progression of secretory particle maturation which is consistent with earlier hypotheses of lamellar body assembly.
Williams and Lissner: Biomechanics of Human Motion (second edition)
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Le Veau, B. (1977) Williams and Lissner: Biomechanics of Human Motion (second edition). Philadelphia: W.B. Saunders Co.
Three-dimensional reconstruction and quantitative analysis Of rat lung type 11 cells: A computer-based Study) I muscoli ioidei dei sauri in rapport0 con i muscoli ioidei degli altri vertebrati. Mem. Reale Accad. Scienze Torino
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On the cranial osteology of Uromastix hardwickii (Gray)
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Animal Tissue Techniques1895) Observations on the frilled lizard Chla-mydosaurus kingi
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Humason, G.L. (1979) Animal Tissue Techniques. San Francisco: W.H. Freeman & Co. FORM AND FUNCTION OF THE TONGUE IN AGAMIDS Kent, W.S. (1895) Observations on the frilled lizard Chla-mydosaurus kingi. Proc. Zool. SOC. Lond. 46:712-719.
192213) a e r das Zungenbein der Repti-lien. Bijd. Dierk. Amsterdam
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Comparative morphology of the lep-idosaur tongue and its relevance to squamate phylog-eny The Phylogenetic Relationships of the Lizard Families: Essays Com-memorating Charles L. Camp Chameleon-like tongue protrusion in an agamid lizard
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Schwenk, K. (1988) Comparative morphology of the lep-idosaur tongue and its relevance to squamate phylog-eny. In R. Estes and G. Pregill (eds): The Phylogenetic Relationships of the Lizard Families: Essays Com-memorating Charles L. Camp. Palo Alto, CA: Stanford Univ. Press, pp. Schwenk, K., and D.A. Bell (1986) Chameleon-like tongue protrusion in an agamid lizard. Am. Zool 26t65A.
Die Zunge der Agamidae und Iguanidae
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Evolutionary Morphology ofthe Lep-idosam Tongue. Unpublished ph.D. Thesis, University of California) Occurrence, distribution and func-tional significance of taste buds in lizards
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Schwenk, K. (1984) Evolutionary Morphology ofthe Lep-idosam Tongue. Unpublished ph.D. Thesis, University of California, Berkeley, 174 pp. Schwenk, K. (1985) Occurrence, distribution and func-tional significance of taste buds in lizards. Copeia 1985:91-101. &One.
Ecological observations on the Egyptian spiny‐tailed lizard Uromastix aegyptius: I—On food and feeding habits, with notes on the climate and vegetation of the study area
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