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Morphology and Histology of the Tongue and Oral Chamber of Eublepharis macularius (Squamata: Gekkonidae), with Special Reference to the Foretongue and its Role in Fluid Uptake and Transport
Abstract
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.
... Many species of squamates have developed highly specialized and agile tongues (Morgans & Heidt, 1978;Iwasaki & Kumakura, 1994;Berkhoudt et al., 1995;Iwasaki & Yoshihara, 2003;De Groot et al., 2004;Filoramo & Schwenk, 2009;Jamniczky et al., 2009), which represent an innovative regulatory factor in their evolutionary history (Iwasaki & Kumakura, 1994;Schwenk, 1994a;Vitt et al., 2003;Herrel et al., 2005;Baeckens et al., 2017a). In squamates, the tongue primarily functions in food transportation and manipulation (Schwenk, 2000;Iwasaki, 2002), drinking (Jamniczky et al., 2009;Cundall et al., 2012), prey capture (Keiser, 1975;Cooper, 1994), and defensive strategies (Mcdowell, 1972;Bels et al., 1994;Schwenk, 1995). ...
... Many species of squamates have developed highly specialized and agile tongues (Morgans & Heidt, 1978;Iwasaki & Kumakura, 1994;Berkhoudt et al., 1995;Iwasaki & Yoshihara, 2003;De Groot et al., 2004;Filoramo & Schwenk, 2009;Jamniczky et al., 2009), which represent an innovative regulatory factor in their evolutionary history (Iwasaki & Kumakura, 1994;Schwenk, 1994a;Vitt et al., 2003;Herrel et al., 2005;Baeckens et al., 2017a). In squamates, the tongue primarily functions in food transportation and manipulation (Schwenk, 2000;Iwasaki, 2002), drinking (Jamniczky et al., 2009;Cundall et al., 2012), prey capture (Keiser, 1975;Cooper, 1994), and defensive strategies (Mcdowell, 1972;Bels et al., 1994;Schwenk, 1995). The tongue is also deeply forked (hereafter, bifurcated) and co-opted for chemoreception (Cooper, 1997;Parker et al., 2008;Baeckens et al., 2017b) in snakes and some lacertids (De Groot et al., 2004;Herrel et al., 2005). ...
... Several studies have elucidated the mechanistic pathways by which squamates use their bifurcated tongues for chemo-and mechano-sensory reception. During probing action, the tongue darts out of the oral cavity and sweeps its apical tines through the air via oscillatory action; capturing airborne scent molecules and specific chemical cues (Gove, 1979;Schwenk 1993Schwenk , 1995Cooper, 1996;Jamniczky et al., 2009;Kaas, 2009;Clark, 2015). The tongue then retracts and transfers chemical cues to a specialized sensory organ in the roof of the buccal cavity, the vomeronasal organ (VNO) (Young, 1990;Graves, 1993;Iwasaki et al., 1996;Parker et al., 2008;Filoramo & Schwenk, 2009). ...
We describe the morphological adaptations of the tongue and gastrointestinal tract of the striped sand snake Psammophis sibilans and discuss their functional importance. Using standard histological, histochemical, and scanning electron microscopy techniques, we analyzed 11 adult snakes of both sexes. Our findings showed that the bifurcated non-papillate tongue exhibited chemoreceptive adaptions to squamate foraging behavior. The lingual apex tapered terminally with sensory spines, and the body of the tongue possesses a characteristic central odor–receptor chamber that might serve to trap and retain scent molecules. Furthermore, the intrinsic musculature showed interwoven and well-developed transverse, vertical and longitudinal muscle fibers that control contraction and retraction during probing and flicking. The esophagus displayed highly folded mucosa lined with columnar epithelium with goblet cells. In contrast, the stomach mucosa formed finger-like gastric rugae, encompassing tubular glands with dorsal gastric pits. The intestine is distinct from other vertebrates in lacking the crypts of Lieberkühn in the tunica mucosa and submucosa. The intestine mucosa is mostly arranged in interdigitating villi oriented perpendicular to the luminal surface. We extrapolated subtle variations for both acid and neutral mucopolysaccharides and glycoproteins localization as well as collagen fibers using histochemical analyses. The elaborate histo-morphological and functional adaptation of the tongue and digestive tract plays a pivotal role in foraging and feeding behavior.
... Many species of squamates have developed highly specialized and agile tongues (Morgans & Heidt, 1978;Iwasaki & Kumakura, 1994;Berkhoudt et al., 1995;Iwasaki & Yoshihara, 2003;De Groot et al., 2004;Filoramo & Schwenk, 2009;Jamniczky et al., 2009), which represent an innovative regulatory factor in their evolutionary history (Iwasaki & Kumakura, 1994;Schwenk, 1994a;Vitt et al., 2003;Herrel et al., 2005;Baeckens et al., 2017a). In squamates, the tongue primarily functions in food transportation and manipulation (Schwenk, 2000;Iwasaki, 2002), drinking (Jamniczky et al., 2009;Cundall et al., 2012), prey capture (Keiser, 1975;Cooper, 1994), and defensive strategies (Mcdowell, 1972;Bels et al., 1994;Schwenk, 1995). ...
... Many species of squamates have developed highly specialized and agile tongues (Morgans & Heidt, 1978;Iwasaki & Kumakura, 1994;Berkhoudt et al., 1995;Iwasaki & Yoshihara, 2003;De Groot et al., 2004;Filoramo & Schwenk, 2009;Jamniczky et al., 2009), which represent an innovative regulatory factor in their evolutionary history (Iwasaki & Kumakura, 1994;Schwenk, 1994a;Vitt et al., 2003;Herrel et al., 2005;Baeckens et al., 2017a). In squamates, the tongue primarily functions in food transportation and manipulation (Schwenk, 2000;Iwasaki, 2002), drinking (Jamniczky et al., 2009;Cundall et al., 2012), prey capture (Keiser, 1975;Cooper, 1994), and defensive strategies (Mcdowell, 1972;Bels et al., 1994;Schwenk, 1995). The tongue is also deeply forked (hereafter, bifurcated) and co-opted for chemoreception (Cooper, 1997;Parker et al., 2008;Baeckens et al., 2017b) in snakes and some lacertids (De Groot et al., 2004;Herrel et al., 2005). ...
... Several studies have elucidated the mechanistic pathways by which squamates use their bifurcated tongues for chemo-and mechano-sensory reception. During probing action, the tongue darts out of the oral cavity and sweeps its apical tines through the air via oscillatory action; capturing airborne scent molecules and specific chemical cues (Gove, 1979;Schwenk 1993Schwenk , 1995Cooper, 1996;Jamniczky et al., 2009;Kaas, 2009;Clark, 2015). The tongue then retracts and transfers chemical cues to a specialized sensory organ in the roof of the buccal cavity, the vomeronasal organ (VNO) (Young, 1990;Graves, 1993;Iwasaki et al., 1996;Parker et al., 2008;Filoramo & Schwenk, 2009). ...
We describe the morphological adaptations of the tongue and gastrointestinal tract of the striped sand snake Psammophis sibilans and discuss their functional importance. Using standard histological, histochemical, and scanning electron microscopy techniques, we analyzed 11 adult snakes of both sexes. Our findings showed that the bifurcated non-papillate tongue exhibited chemoreceptive adaptions to squamate foraging behavior. The lingual apex tapered terminally with sensory spines, and the body of the tongue possesses a characteristic central odor–receptor chamber that might serve to trap and retain scent molecules. Furthermore, the intrinsic musculature showed interwoven and well-developed transverse, vertical and longitudinal muscle fibers that control contraction and retraction during probing and flicking. The esophagus displayed highly folded mucosa lined with columnar epithelium with goblet cells. In contrast, the stomach mucosa formed finger-like gastric rugae, encompassing tubular glands with dorsal gastric pits. The intestine is distinct from other vertebrates in lacking the crypts of Lieberkühn in the tunica mucosa and submucosa. The intestine mucosa is mostly arranged in interdigitating villi oriented perpendicular to the luminal surface. We extrapolated subtle variations for both acid and neutral mucopolysaccharides and glycoproteins localization as well as collagen fibers using histochemical analyses. The elaborate histo-morphological and functional adaptation of the tongue and digestive tract plays a pivotal role in foraging and feeding behavior.
... The Gekkota (on the grounds both of their relatively basal position in squamate phylogeny and the absence of the use of the tongue in food capture or vomerolfaction) afford the opportunity to establish the required baseline for subsequent comparative study. Previously, we explored the morphology of the tongue and oral chamber of the eublepharid Eublepharis macularius (Jamniczky et al., 2009) to provide a foundation for the current study. We selected Eublepharis because it is a member of the Eublepharidae, the only clade of geckos that ancestrally retains mobile eyelids, thereby circumventing any modifications of the tongue associated with the grooming behaviour of spectacle-wiping (Bustard, 1963;Russell & Rosenberg, 1981). ...
... We selected Eublepharis because it is a member of the Eublepharidae, the only clade of geckos that ancestrally retains mobile eyelids, thereby circumventing any modifications of the tongue associated with the grooming behaviour of spectacle-wiping (Bustard, 1963;Russell & Rosenberg, 1981). Jamniczky et al. (2009) recognized five morphologically and histologically distinct regions of the dorsal tongue surface of E. macularius, each having specific spatial relationships with regions of the oral chamber. On anatomical grounds, Jamniczky et al. (2009) suggested the manner in which water is taken up by the tongue, brought to the mouth, unloaded therefrom and passed through a series of intraoral chambers (Fig. 1, chambers C1, C2 and C3) towards the oesophagus prior to swallowing. ...
... Jamniczky et al. (2009) recognized five morphologically and histologically distinct regions of the dorsal tongue surface of E. macularius, each having specific spatial relationships with regions of the oral chamber. On anatomical grounds, Jamniczky et al. (2009) suggested the manner in which water is taken up by the tongue, brought to the mouth, unloaded therefrom and passed through a series of intraoral chambers (Fig. 1, chambers C1, C2 and C3) towards the oesophagus prior to swallowing. These suggestions implied that certain regions of the tongue and specific intraoral compartments are used, and others avoided, as water progresses from the point of intake to its point of swallowing (Fig. 1). ...
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.
... The morphological characteristics and histological structure of the tongue and lingual papillae have been studied, by using light and electron microscopes, in most vertebrates classes such as amphibians (Mahabady et al., 2010), reptiles (Herrel et al., 1998;Herrel et al., 2001;Wassif, 2001;Herrel et al., 2005;Jamniczky et al., 2009;El-Sayyad et al., 2011;Darwish, 2012), birds (Crole and Soley, 2009;Emura et al., 2008aEmura et al., ,b, 2009Dehkordi et al., 2010;El-Bakary, 2011a;Santos et al., 2011) and Mammals (Ciuccio et al., 2008(Ciuccio et al., , 2010Abayomi et al., 2009;Adeniyi et al., 2010;El-Bakary, 2011b;Nasr et al., 2012;Yoshimura et al., 2012). The aim of this study is to complement the previous studies on the anatomical features and histological structure with emphasis on some histochemical aspects of the tongue in two species of animals from two different classes of vertebrates, which is feed almost the same type of food. ...
... This design appeared also in most vertebrates species Nonaka et al., 2008;Adeniyi et al., 2010;Darwish, 2012;Nasr et al., 2012). In the present study, T.vittata possessed bifid of lingual apex which completely missing in H. auritus, similar structure was appeared in the other reptilians as in Diamondback Water Snake , Black Rat Snake (Morgans and Heidt,1978), Agamid Lizards (Herrel et al., 1998), scincine lizard (Wassif, 2001), Lacertid Lizards (Herrel et al., 2005), Eublepharis macularius (Jamniczky et al., 2009), Psammophis sibilans (El-Sayyad et al.,2011) and Stenodactylus petrii (Darwish,2012), also Owl (Strix uralensis) and other birds Emura et al., 2008a;El-Bakary, 2011a). Forked tongues may provide more surfaces available for sensory function in lizards (Darwish,2012). ...
... These differences depend on diet variety, feeding habits and mouth handling of the food (Iwasaki and Miyata, 1985;Darwish, 2012;Nasr et al., 2012). In the T.vittata and H. auritus the apex, body and root of the tongue covered by a large number of lingual papillae, their types were filiform, fungiform that also appeared in reptiles (Wassif, 2001;Herrel et al., 2005;Jamniczky et al., 2009;Darwish, 2012), mammals (Ciuccio et al., 2008(Ciuccio et al., , 2010Abayomi et al., 2009;Adeniyi et al., 2010;Nasr et al., 2012;Yoshimura et al., 2012) and other vertebrates (Crole and Soley, 2009;Emura et al., , 2009Dehkordi et al., 2010;Mahabady et al., 2010;El-Bakary, 2011b;Santos et al., 2011). The encouraging results of this study that highlighted the presence of especial lingual papillae that is a cuboidal papillae in the tongue apex and body of T.vittata, this papillae type also founded in the Eublepharis macularius (Jamniczky et al., 2009), as well Iwasaki (1990) described the domeshaped which correspond to the cuboidal papillae in Gekko japonicas (Iwasaki, 1990). ...
This study aimed to determine the anatomical features and histological structure as well as some histochemical aspects of tongue of two species of insectivorous vertebrates, which differ in their classification, habitat and activity (lizard, Trachylepis vittata and the Long-eared hedgehog, Hemiechinus auritus) by using light microscope. The results show that the tongue of the two species is differ in size, color and shape, three parts are distinguished in the dorsal surface of the tongue, apex, body and root. Histologically, the entire dorsal surface of tongue in the two species is covered by lingual papillae which appear of many types. The filiform and fungiform papillae are main types of lingual papillae which are different among the two species in height, thickness and subtypes. There are distinct lingual papillae appeared in T. vittata that was cuboid papillae, also the circumvallate papillae appeared only in the H.auritus. The stratified squamous epithelium tissue surrounded tongue in the two species that is almost non keratinized in T.vittata but it is keratinized in H. auritus and contain a number of taste buds. The lamina propria in the two species is consisted of dense connective tissue which contained many structures that is different among the two species. The mucus glands appeared in T.vittata and absent in H. auritus. Histochemically, the tongue of the two species is positive for carbohydrates stains and negative with others histochemical stains. In conclusion, the tongue compounds of T.vittata are more appropriate to feeding manner on insects from that of H. auritus tongue.
... Current study also showed that the dorsal surface of the body and root of the tongue in Hemidactylus vlaviviridus are covered by various types of papillae, and these papillae are different in shape, size, number and distribution among different groups of vertebrates (1,14,28,35). Types of papillae on the dorsal surface of the body and root of the tongue like fungiform, filiform, long and short foliolate, conical and cuboidal, and that also appeared in some reptiles and other vertebrates (1,2,5,19,36). Moreover, this study described the demo shaped papillae which are correspond to the cubodial in Geko japonicas, Present results almost similar with (1,37) that found the apex without papillae in Hemidactylus Flaviviridis. ...
... This could be the reason of the dark color in the apex tongue in gecko. Stratified muscle fibers appeared in different arrangement and density, these muscles observed in all vertebrates studied and the muscular organization is helped the tongue on its movement, while the hyoglossus muscle appear clearly in the body and root of the tongue, this reported in other reptiles (1,19,28,36,37). The SEM examination revealed that the dorsal region of the tongue in gecko covered with various types of papillae that showed clearly differences between the body and root of tongue and this is agree with (6,24,26). ...
The aim of this study to investigate the tongue morphology and histology in house gecko Hemidactylus flaviviridis using light and scanning electron-microscopy (SEM) technique.The morphology result revealed the presence of three parts : apex , body and lingual root .The light microscopy result showed that the tongue is covered with mucous membrane composed of non keratinized stratified squamous epithelium based on lamina propria which contain bundles of striated muscles its fibers in different directions including connective tissue , blood vessels and nerves. The lingual mucosa of the dorsal surface is covered with different pattern of lingual papillae which are widely distributed all over the dorsal surface except the apex. Noticed on the dorsal surface different types of papillae were like fungiform, long and short folliolate, conical and cuboidal papillae. SEM examination showed that the tongue in Hemidactylus vlaviviridus appeared elongated with triangular shape and bifurcated free tip, also it is divided into three parts: apex, body and root; many types of papillae are distributed on the dorsal surface of the body and root of tongue. Fungiform papillae are widely distributed all over the dorsal surface of the tongue body .In the root of tongue, there are different types of papillae like filiform and foliate papillae , a lot of goblet cells have been showed in this region .
... Both studied species depend on a fast bite to seize their prey by using their jaws. Although their jaws provided with small teeth but it cannot penetrate the skin of the prey, thus these reptile species are using different strategies during catching their prey and continue by several protractionretraction motions of the tongue (Jamniczky, Russell, Johnson, Montuelle, & Bels, 2009). A. boskianus (Lizard) uses active search strategy, while P. guttatus (Gecko) uses sit-and-wait strategy to find their food (Saber et al., 1994). ...
... This may explain why the numerous of taste buds are observed along the two-third of the tongue of P. guttatus, while few restricted along the fore-tongue of A. boskianus (lizard) but increase on its mid-tongue. Jamniczky et al. (2009) noted that gekkota largely lack taste buds and concluded that this phenomenon may be phylogenetic and also may be a functional or adaptive significance to it. This view disagree with that mentioned by Bayoumi et al. (2011), who observed taste buds on the apical and lateral surfaces of the dome-shaped lingual papillae on the tip of P. guttatus, while they are completely absent on the papillae of A. boskianus tongue. ...
Abstract
The current observations focused on the ultrastructure comparison between the
tongue of two reptile species endemic the Egyptian fauna; Bosc's fringe-toed lizard
Acanthodactylus boskianus and Sinai fan-fingered gecko Ptyodactylus guttatus to
exhibit the relationship between the lingual epithelium and its function according to
their specific feeding strategy. A. boskianus possessed triangular elongated tongue
with bifurcated tapering apex and wide base while; the P. guttatus had a triangular
flattened tongue with conical shallow bifurcated apex and broad base. The ventral
surface of the lingual apex of A. boskianus had transverse while in P. guttatus had two
oval pads and median ventral groove. Both surfaces of the tongue of both examined
species are covered by stratified squamous epithelium with great variability of degree
of keratinization. The dorsal epithelium formed flattened and conical filiform papillae
in A. boskianus, while in P. guttatus formed cylindrical papillae, conical, and tall filiform
ones. Few taste buds are observed on the fore-tongue but increase on the midtongue
of A. boskianus, while in P. guttatus, numerous taste buds are distributed on
the fore-tongue and mid-tongue. Both surfaces of the laryngeal mound of both
examined species provided with numerous of cilia and orifices of laryngeal gland. The
present results confirmed that the tongue of A. boskianus acts as a chemoreceptor
organ to follow pheromone trails of prey and mates. While in P. guttatus the tongue
may play an important role in the feeding mechanism and act as a chemoreceptor
organ.
KEYWORDS
Acanthodactylus boskianus, adaptation, histology, lingual epithelium, Ptyodactylus
guttatus, SEM
... Both studied species depend on a fast bite to seize their prey by using their jaws. Although their jaws provided with small teeth but it cannot penetrate the skin of the prey, thus these reptile species are using different strategies during catching their prey and continue by several protractionretraction motions of the tongue (Jamniczky, Russell, Johnson, Montuelle, & Bels, 2009). A. boskianus (Lizard) uses active search strategy, while P. guttatus (Gecko) uses sit-and-wait strategy to find their food (Saber et al., 1994). ...
... This may explain why the numerous of taste buds are observed along the two-third of the tongue of P. guttatus, while few restricted along the fore-tongue of A. boskianus (lizard) but increase on its mid-tongue. Jamniczky et al. (2009) noted that gekkota largely lack taste buds and concluded that this phenomenon may be phylogenetic and also may be a functional or adaptive significance to it. This view disagree with that mentioned by Bayoumi et al. (2011), who observed taste buds on the apical and lateral surfaces of the dome-shaped lingual papillae on the tip of P. guttatus, while they are completely absent on the papillae of A. boskianus tongue. ...
The current observations focused on the ultrastructure comparison between the tongue of two reptile species endemic the Egyptian fauna; Bosc's fringe-toed lizard Acanthodactylus boskianus and Sinai fan-fingered gecko Ptyodactylus guttatus to exhibit the relationship between the lingual epithelium and its function according to their specific feeding strategy. A. boskianus possessed triangular elongated tongue with bifurcated tapering apex and wide base while; the P. guttatus had a triangular flattened tongue with conical shallow bifurcated apex and broad base. The ventral surface of the lingual apex of A. boskianus had transverse while in P. guttatus had two oval pads and median ventral groove. Both surfaces of the tongue of both examined species are covered by stratified squamous epithelium with great variability of degree of keratinization. The dorsal epithelium formed flattened and conical filiform papillae in A. boskianus, while in P. guttatus formed cylindrical papillae, conical, and tall filiform ones. Few taste buds are observed on the fore-tongue but increase on the mid-tongue of A. boskianus, while in P. guttatus, numerous taste buds are distributed on the fore-tongue and mid-tongue. Both surfaces of the laryngeal mound of both examined species provided with numerous of cilia and orifices of laryngeal gland. The present results confirmed that the tongue of A. boskianus acts as a chemoreceptor organ to follow pheromone trails of prey and mates. While in P. guttatus the tongue may play an important role in the feeding mechanism and act as a chemoreceptor organ.
... These different papillae are overlapped, some of them has serrated ends and trenches in between. Similar kinds of lingual papillae are described by Jamniczky et al. (2009), in Eublepharis macularius, El-Sayyad et al. (2011) in Tarentola annularis , and El-Bakry and Hamdi (2016 in Tarentola annularis and Crocodylus niloticus . ...
... Some authors suggested that taste buds may play an important role in receiving chemical and mechanical information of food (Nasr et al., 2012). Other studies failed to establish the presence of taste buds in some lizard (Jamniczky et al., 2009) in Eublepharis macularius, Abbate et al. (2010) in Podarcis sicula, and Darwish (2012) in Ptyodactylus guttatus and Stenodactylus petrii . ...
The lingual morphology of the squamata is still
unknown in many species. The lake of detailed
description in specific species has hindered the
understanding of the functional morphology of
the squamata tongue. Therefore, the aim of the
study is designed to reveal the morphology of
the tongues of the insectivore Scincus scincus;
the herbivore Uromastyx ornate, and the
carnivore Psammophis schokari by using SEM.
The tongue consists of apex, body, and lingual
root in sequence. Morphologically, the tongues
of S. scincus and U. ornata is flattened dorsoventrally
with a triangle shape in S. scincus and
rectangular in U. ornata. The tip of the first
species is short furrow, while in the second it is
split. Where, the tongue of P. schokari, is slim,
thin, and narrow with bifurcated tip. A median
sulcus is deep in P. schokari, while shallow in
U. ornata and absent in S. scincus. The lingual
papillae are absent in the dorsal surface of the
tongue of P. schokari, while, they are acquired
with numerous shapes on the dorsal lingual
surface of S. scincus and U. ornata. Many
microfacets are seen on the apical dorsal
surface of the P. schokari tongue. The lingual
gland openings are noted only in the lingual
apex of U. ornata tongue. The taste buds occur
along the tongue of S. scincus and observed
only on the root part of the of U. ornata. In
contrast the taste buds are absent in P.
schokari tongue. From the obvious variation of
the dorsal lingual surface of the tongue of three
examined species we can concluded that these
differences may be reflect to their feeding habit.
... (Baeckens et al., 2017;Beisser, Lemell, & Weisgram, 2001;Heiss et al., 2011;Jamniczky, Russell, Johnson, Montuelle, & Bels, 2009;Koca, Oğuz, & Osanç, 2007;Lemell, Beisser, & Weisgram, 2000;Mouton, Flemming, & Broeckhoven, 2014;Putterill & Soley, 2004;Rehorek et al., 2014), and in some cases, as happens in snakes, its role is important only for the olfaction (Filoramo & Schwenk, 2009;Nishida, Yoshie, & Fujita, 2000). Several and peculiar different characteristics were observed in several vertebrates, including mammals (see for a review Iwasaki, 2002). ...
... The specific name "macularius" from the latin "macula" is referred to the presence of numerous spotted markings. Little is known, and little number of bibliographic data are present in literature about the lingual morphology of Lacertilia, tongue (Abbate et al., 2010(Abbate et al., , 2009Iwasaki, 1990;Schwenk, 2000) and only one paper is available on the Leopard Gecko correlated particularly to the context of drinking behaviour (Jamniczky et al., 2009). Therefore by scanning electron microscopy, light and confocal laser microscopy the morphological aspects of the lingual dorsal and ventral surface and the possible correlations with different functions will be considered. ...
The leopard gecko is a crepuscular and insectivorous reptile. The role of the tongue in this reptile is fundamental for the prey capture and ingestion and is not related with eyes cleaning as usual in other geckos. The elongated tongue can be divided into a foretongue with a slightly bifurcated apex and a hindtongue. Scanning electron microscopy demonstrated that several different papillae are present on the dorsal surface, foliate and dome‐shaped in the foretongue, becoming thicker and stouter with reduced interpapillary spaces in the lateral parts. The hindtongue is characterised by wide foliate papillae with indented margins and deep fissures of the mucosa. Light microscopy showed the presence of a stratified slightly keratinized squamous epithelium in the apex of the foretongue, a stratified non‐keratinized squamous epithelium in the fore and in the hindtongue. In the foretongue, numerous muciparous caliciform cells were observed. Moreover, the presence of taste buds on the tongue ventral surface was demonstrated for the first time in this species and the confocal laser study revealed a strong immunoreactivity for the S‐100 protein in the sensory cells. Therefore, the results obtained could give a contribution to the knowledge of the tongue anatomy and are a basis for eventual further studies regarding the feeding habits in a reptile become a popular pet.
... Gustation is poorly developed in geckos (Schwenk 1985). There is no evidence of taste buds in leopard geckos (Schwenk 1985;Jamniczky et al. 2009). Therefore, the tongueflicking may be directly linked to vomerolfaction (Schwenk 1993). ...
... Oxoaldehyde may not have any aversive effect on leopard geckos because it is odourless. It seems that oxoaldehyde might be mediated by gustation, which is poorly developed in leopard geckos (Schwenk 1985;Jamniczky et al. 2009). ...
Chemical protection of Heteroptera is mostly based on repellent secretion,
which might signal the unpalatability of the bug to its potential predators or be
directly toxic to predators. The aversive reactions of leopard geckos (Eublepharis
macularius) were tested towards the major compounds of defensive secretion of
Graphosoma lineatum: (1) a mixture of three aldehydes: (E)-hex-2-enal, (E)-oct-2-
enal, (E)-dec-2-enal; (2) a mixture of three aldehydes and tridecane; (3) oxoaldehyde:
(E)-4-oxohex-2-enal; (4) extracted metathoracic scent-glands secretion of Graphosoma
lineatum adults and (5) hexane as a non-polar solvent. Additionally, (6) 2-isobutyl-3-
methoxypyrazine was used to exclude the effect of neophobia. All chemicals were
applied on a palatable food (Tenebrio molitor larvae). The aversive reactions of
leopard geckos towards the mealworms were evaluated by observing the approach
latencies, attack latencies and approach–attack intervals. Leopard geckos exhibited
aversive reactions to the mixture of three aldehydes and also to this mixture and
tridecane. Oxoaldehyde did not have any aversive effect. The whole metathoracic
scent-glands secretion clearly had an aversive effect on geckos. Furthemore, when a
living specimen of Graphosoma lineatum was offered to the geckos before the trials
with the mixture of three aldehydes, the impact of this mixture was enhanced, thus
acting as a potential signal of unpalatability.
... The Sinai fan-fingered gecko tongue has numerous taste buds along its twothirds lingual region, while the Bosc's fringe-toed lizard tongue has a small number on its foretongue but an increase in its midtongue [25]. Previous studies [29,40] found that gekkotan and blue-tongued lizard tongues primarily lack taste buds, suggesting it may be a phylogenetic, functional, or adaptive feature. This view disagrees with that mentioned by Bayoumi and Abd-Elhameed [11], who observed taste buds on the apical and lateral surfaces of the dome-shaped papillae on the lingual tip of P. guttatus, while they were completely absent from the papillae of A. boskianus tongue; meanwhile, Taha [41] observed the presence of a few taste buds in the epithelium of the three lingual parts of Trachylepis vittata. ...
The present study used light and scanning electron microscopy to describe the integrative morphological description of the tongue and laryngeal mound of Heremites vittatus, an endemic lizard of Saharan Africa. Additionally, ultrastructure, histology, histochemistry, and immunohistochemical approaches were used to characterize the lingual apparatus adaptations. In the present study, Heremites vittatus consisted of a complex lingual papillary system in which the ventral apical surface of the foretongue comprised conical papillae. The dorsal surface consisted of different filiform pa-pillary (papillae filiformes) types: the anterior section had two types (bifid and pointed), and the posterior section had four types (triangular, trifid, quadrifid, and pentafid) papillae. The dorsal midtongue surface exhibits scale-like, serrated filiform papillae with anterior gland openings. The hindtongue consisted of two overlapping filiform papillae: scale-like board-serrated papillae on the median portion and finger-like papillae on the wings. The dorsal surface of the laryngeal mound had 18 longitudinal folds with glandular openings. Histologically, the foretongue was covered by a slightly keratinized layer that was absent in the mid- and hindtongue. The lingual glands were absent from the foretongue but present in the interpapillary space in the mid- and hindtongues. We ob-served a few rounded taste buds in the conical papilla epithelium. Histochemical analysis revealed strong glandular Alcian Blue (AB)-positive and Periodic Acid–Schiff (PAS) positive reactions. Immunohistochemistry showed strong cytokeratin immunopositivity in all parts of the tongue. In conclusion, the obtained data about the lingual characterizations have been consistent with the active foraging behavior of the species and its environmental conditions.
... The mucosa of the posterior region consists of pseudostratified columnar epithelium provided with goblet cells containing secretory granules and dense microvilli. Jamniczky et al. described the presence of glandular goblet clusters on the exposed stalks of papillae in the middle and posterior tongue regions in Eublepharis macularius (Jamniczky et al., 2009). ...
Background
The tongue plays definite and important role in simplifying food intake and also, exhibits significant morphological distinctions to acclimatize the environment. This study aimed to investigate the variations in gross and microscopic anatomy of the tongue in two tetrapod classes Ptychadena mascareniensis from class: Amphibia and Hemidactylus turcicus from class: Reptilia to correlate the structure and functions of the tongue in relations to the habitat and feeding mechanisms.
Results
All the modifications perceived in the tongues of the premeditated animals explained the relationship between adaptation of each animal to its feeding habit and habitat. Amphibians which live in and nearby freshwater showed no keratinization in their lingual epithelium. However, reptiles, which live in terrestrial habitats, have shown keratinization and ideal forms of lingual papillae which considered the most remarkable feature of the histological structures of the reptilian tongues and reflect their adaptations to the dry habitat in which they live.
Conclusion
There were some variations reported in histological structure, gross anatomy and ultrastructure morphology of the tongue from the two tetrapod classes, the Amphibia ( Ptychadena mascareniensis ) and Reptilia ( Hemidactylus turcicus ). The present study is the first one in Egypt that deals with the tongue structures and functions in one of the amphibians Ptychadena mascareniensis. Concerning the lizard Hemidactylus turcicus.
... In vertebrates, the tongue supports the hyoid skeleton by acting as an integral part in facilitating the action of the tongue. The hyoid skeleton in reptiles has several morphological patterns depending upon the feeding habitats (Darwish, 2012;Jamniczky, Russell, Johnson, Montuelle, & Bels, 2009;Schwenk, 1995;Sherbrooke, Scardino, deNys, & Schwartzkopf, 2007). However, the hyolingual system for reptiles in general, which supports the posterior portion of the buccal floor with the larynx embedded, is importantly involved not only in drinking, food handling, and transport, but also in respiration (e.g., gular pumping and panting) and vocalization (Riede et al., 2015;Riede, Tokuda, & Farmer, 2011). ...
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.
... Nasr et al. (2012) mentioned that the presence of taste buds on the tongue tip of the rat may play an important role in receiving chemical and mechanical information of food. On other hand, some authors failed to detect taste buds in Eublepharis macularius (Jamniczky et al., 2009), in Podarcis sicula (Abbate et al., 2010), and in Ptyodactylus guttatus and Stenodactylus petrii (Darwish, 2012). ...
... Histochemically, results of present study showed that the tongue in the two present species T. annularis and C. niloticus, is strongly positive for carbohydrates stains (PAS, PAS-alcian reaction), indicates a considerable activity of this glands in the production of the mucous secretion containing glycoproteins. It has been referred that these substances are helping the tongue adhesion and swallowing of the food easily; this has been also documented in other vertebrates [6,24,41,49]. The tongue shows stronger reaction for protein stained with bromophenol technique in the lingual glands of C. niloticus compared with moderate reaction of T. annularis. ...
The present study deals with examined the morphological features, histological and histochemical aspect of the tongue of two reptilian species, Tarentola annularis (Family: Gekkonidae) and Crocodylus niloticus ( Family: Crocodylidea), with different habitats, feeding pattern and behavior by light and scanning electron microscope. It was observed, that the bifurcation of the tongue is more visible in Tarentola annularis. Conical and filamentous papillae are observed on the lingual body of Tarentola annularis, while in crocodylus niloticus a mechanical filiform and gustatory papillae appeared, both. The lingual mucosa in Tarentola annularis is covered by stratified squamous epithelium and keratinized but in crocodylus niloticus it is highly folded and more heavily keratinized in the folded region and have a localized thickenings structures resembling taste buds. Mucous glands appeared in Tarentola annularis and compound tubular glands in crocodylus niloticus. At SEM, abundant microridges and microvilli in both species were exhibited on papillae surface facilitated feeding habits. Histochemically, the tongue of two species is strongly positive for carbohydrate stain but with variable degree with others stains. In conclusion, there is a marked correlation between the structure of the tongue of the present reptilian species, habitats and feeding mechanism of the two species.
... In this case, the aversive effect could be mediated by gustation, which is also well developed in green lizards (Schwenk, 1985;Cooper, 1991). The absence of any aversive effect of oxoaldehyde on leopard geckos (Gregorovičová andČerníková, unpublished data) may be related to their poorly developed sense of gustation (Schwenk, 1985;Jamniczky et al., 2009). On the other hand, oxoaldehyde has a strong aversive effect on birds (Gregorovičová et al., unpublished data), presumably due to their relatively well developed gustatory sense (Mason and Clark, 2000). ...
The chemical defence of Heteroptera is primarily based on repellent secretions which signal the potential toxicity of the bug to its predators. We tested the aversive reactions of green lizards (Lacerta viridis) towards the major compounds of the defensive secretion of Graphosoma lineatum, specifically: (i) a mixture of three aldehydes: (E)-hex-2-enal, (E)-oct-2-enal, (E)-dec-2-enal; (ii) a mixture of these three aldehydes and tridecane; (iii) oxoaldehyde: (E)-4-oxohex-2-enal; (iv) secretion extracted from metathoracic scent glands of G. lineatum adults and (v) hexane as a non-polar solvent. All chemicals were presented on a palatable food (Tenebrio molitor larvae). The aversive reactions of the green lizards towards the mealworms were evaluated by observing the approach latencies, attack latencies and approach-attack intervals. The green lizards exhibited a strong aversive reaction to the mixture of three aldehydes. Tridecane reduced the aversive reaction to the aldehyde mixture. Oxoaldehyde caused the weakest, but still significant, aversive reaction. The secretion from whole metathoracic scent glands also clearly had an aversive effect on the green lizards. Moreover, when a living specimen of G. lineatum or Pyrrhocoris apterus (another aposematic red-and-black prey) was presented to the green lizards before the trials with the aldehyde mixture, the aversive effect of the mixture was enhanced. In conclusion, the mixture of three aldehydes had the strong aversive effect and could signal the potential toxicity of G. lineatum to the green lizards.
Copyright © 2015. Published by Elsevier GmbH.
... The tongue in reptiles, and in particular in lizards, presents regional variations in histological structure and specific functions in the process of drinking, food sensing and manipulation (Iwasaki et al., 1985;Iwasaki, 1990;Wassif, 2002;Jamniczky et al., 2009;El-Sayyad et al., 2011;Darwish, 2012). The apical region of the tongue is generally flatter and the papillae present in this region are either reduced or absent while keratinized layers are thicker than in the more proximal regions. ...
Previous molecular studies indicated that antimicrobial peptides in lizard are expressed in the skin and tongue among other epithelial organs. The present ultrastructural immunogold study aimed to detect the specific location of three broadly expressed antimicrobial peptides in the tongue of the lizard Anolis carolinensis. The immunocytochemical study indicated that beta-defensin-15, the likely main defensin of granulocytes and skin, is poorly expressed in some dense and medium-dense granules of glandular cells of the papillated tongue. Conversely beta-defensin-27 appears highly expressed in numerous pale and cribriform dense granules of glandular cells and is also secreted on the tongue surface. The immunostaining for cathelicidin-1 indicated a variable but however positive immunolabeling in numerous granules in the tongue glands, suggesting that this antimicrobial peptide previously found on the epidermal surface is also present in the tongue secretions and participates to the formation of the anti-microbial oral barrier. The study suggests that among the numerous beta-defensins and cathelicidins identified in the genome of this lizard is present a specific distribution of different peptide subtypes in various body regions, including the tongue, and that these peptides contribute to the formation of local antimicrobial barriers.
Copyright © 2015 Elsevier GmbH. All rights reserved.
... The lingual papillae consist of a dermal core covered with stratified squamous epithelium Chunhabundit et al., 1992;Emura et al., 2000aEmura et al., ,b, 2001. Many studies have demonstrated that the dorsal surface of the reptilian tongue is rich in lingual papillae (Jamniczky et al., 2009;Cizek et al., 2011). On the other hand, Iwasaki and Miyata (1985) reported that no lingual papillae are located on the surface of the anterior bifurcated area of the adult Japanese lizard tongue. ...
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.
... On the other hand, both iguanids and geckos evolved apomorphic lingual behaviors that may rely on increased joint stiffening for hyolingual muscles that a fused Meckel's cartilage may provide. Iguanids evolved translational tongue protrusion (Reilly and McBrayer, 2007) in which the tongue is projected out of the mouth toward prey items (Meyers and Nishikawa, 2000) whereas geckos engage in drinking behaviors in which the tongue is extended into aqueous substrates (Jamniczky et al., 2009). Both behaviors require extensible, hydrostatic hyolingual systems that differ significantly from the chemosensation-based tongue extension behavior evolved in anguimorphs and snakes. ...
Although the mandibular symphysis is a functionally and evolutionarily important feature of the vertebrate skull, little is known about the soft-tissue morphology of the joint in squamate reptiles. Lizards evolved a diversity of skull shapes and feeding behaviors, thus it is expected that the morphology of the symphysis will correspond with functional patterns. Here, we present new histological data illustrating the morphology of the joint in a number of taxa including iguanians, geckos, scincomorphs, lacertoids, and anguimorphs. The symphyses of all taxa exhibit dorsal and ventral fibrous portions of the joints that possess an array of parallel and woven collagen fibers. The middle and ventral portions of the joints are complemented by contributions of Meckel's cartilage. Kinetic taxa have more loosely built symphyses with large domains of parallel-oriented fibers whereas hard biting and akinetic taxa have symphyses primarily composed of dense, woven fibers. Whereas most taxa maintain unfused Meckel's cartilages, iguanians, and geckos independently evolved fused Meckel's cartilages; however, the joint's morphologies suggest different developmental mechanisms. Fused Meckel's cartilages may be associated with the apomorphic lingual behaviors exhibited by iguanians (tongue translation) and geckos (drinking). These morphological data shed new light on the functional, developmental, and evolutionary patterns displayed by the heads of lizards.
The aim of this study was to investigate the anatomical and histological structure of the tongue in ground squirrels. This animal is widely distributed all over the world, especially in the Middle East, but no study has been reported on its tongue structure. In this investigation, we studied five squirrels that were died due to the road accidents. The freshly samples were collected and fixed in 10% formalin solution and after being transferred to the laboratory, the tongue tissue was separated and was studied anatomically. Then, the samples entered the tissue passage stages, and 5-7 µm thick sections were prepared from the paraffin blocks and stained by the hematoxylin-eosin method. The results of this study showed that the surface of the tongue is covered by filiform papillae. Between this papillae, Fungiform papillae without taste buds were visible from the apex to root of the tongue. Three numbers of circumvallate papillae were also visible at the root of the tongue, which were the only chemical papillae of the tongue in this rodent. Most of the tongue structure was made up of skeletal muscles. Lingual glands were serous and mucous secretory units and could be seen only in root of tongue. According to the results of the present study, despite the unique differences in the tongue structure in the ground squirrel, it seems that in general, the tongue structure in this ground squirrel is similar to other squirrel families, especially the Iranian squirrel.
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. We advance the hypothesis that all lizards will conserve the basic means of tongue‐based water uptake and precisely directed intraoral fluid transport seen in the leopard gecko, although specializations for tongue‐based food capture and/or lingually based chemoreception may impact them. We selected the leopard gecko Eublepharis macularius to explore its drinking behaviour through high‐speed cinematography and cineradiography.
It is belong to the order Squamata, family, Chamaeleonidae. They have characteristic features of tongue protrusion during capturing prey attracts many research works and assay its velocity during protrusion. Yet little studies touched the anatomical and histological feature of the juvenile tongue and especially the middle tongue region involved in the tongue elongation, the present study aimed to focus on the histological structure of the mid-tongue and clarify its role in projection of the tongue as well as the glandular structure, keratinization of lingual epithelium and proliferation capacity of the fore-tongue region in relation with their feeding habits during the juvenile age. Juvenile Chameleo chameleon are collected from Abu Rawash, north of Giza Governorate, Egypt during summer 2015. Three juvenile developmental stages are used in the present study and categorized according to the gross morphological criteria of head, abdomen and limb lengths. The tongue and hyoid apparatus were removed and photographed. Histological, immunohistochemistry of cytokeratin and stem cell factor and scanning electronic microscopic investigations were carried out on the fore-tongue region, meanwhile only histological studies were done for the median tongue region. Morphometric assessments of number and length of lingual papillae and grades of cytokeratin and stem cell expression were done. Histologically, the dorsal lingual mucosa of the fore-tongue possessed different pattern of lingual papillae including finger-like, club, cubical, biforked and multi-branched papillae. The finger-like papillae are more abundant compared to the other types. The lamina propria of anterior median tongue pad are more glandular and exhibited abundant distribution of PAS-positive tubular glands and moderate alcian blue staining affinity of both alveolar and branched alveolar glands. There is no detected keratinization of the lingual epithelium. Stem cell factor appeared denser on the lingual mucosa and cell boundaries of glandular tissues. The mid-tongue region possessed a central cartilaginous core outlined by double layers of connective tissue coat and longitudinal and circular muscle fibers which give the power of protrusion of tongue. It is the first time to record the presence of cartilaginous elements in the mid-tongue region of chameleon. Finally the authors concluded that the juvenile stages of common chameleon exhibited striking cartilaginous inner compartment of the med-tongue and glandular fore-tongue adapted for capturing prey coincides with high proliferated activities and presence of different kinds of non-keratinized lingual papillae.
Q: How do geckos walk across ceilings? A: Millions of hair-like setae on each foot. Q: Where do geckos come from? A: Throughout the world. Usually where it's warm. Q: How many species of geckos are there? A: Close to 1,500 and counting! Q: What do they eat? A: Insects mostly. Discover the biology, natural history, and diversity of geckos-the acrobatic little lizards made famous by a car insurance ad campaign. Lizard biologist and gecko expert Aaron Bauer answers deceptively simple questions with surprising and little-known facts. Readers can explore color photographs that reveal the natural wonder and beauty of the gecko form and are further informed by images of how geckos live in their natural habitats. Although written for nonexperts, Geckos also provides a carefully selected bibliography and a new list of all known species that will be of interest to herpetologists. Anyone who owns a gecko, has seen them in the wild, or has wondered about them will appreciate this gem of a book. © 2013 The Johns Hopkins University Press. All rights reserved.
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.
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.
Scanning electron microscopy was employed to investigate the ultrastructure of oral epithelialcells of the lizard, Takydromus tachydromoides. The specimens were prepared by a methodinvolving osmium postfixation and acid treatment to remove extracellular attached material.Bump-shaped protuberances were arranged symmetrically on both sides of the median line of thepalate. Epithelial surfaces besides the bump-shaped protuberances were widely covered with fine folds.At higher magnification, a network pattern of microridges was closely distributed over the entiresurface of the palate, and each cell marginal thickening was clear. The protuberances were alsoobserved in the latero-posterior region of the floor of the mouth. A number of nicks were arrangedsymmetrically on both sides along the median line of the fore-region of the floor. Taste buds werescattered in the epithelial surfaces between nicks. At higher magnification, microvilli as well as microridgeswere observed on the epithelial cell surfaces of the floor. There were no papillar structures onthe ventral tongue surface. Fine pits were densely distributed over the entire epithelial cellsurface. The cell margin was clearly distinguishable as a depressed line. The epithelial surface ofthe laryngeal part of the pharynx was entirely covered with ciliated cells. Taste buds were alsoscattered on the inner gingival epithelial surfaces of the upper and lower jaws along the dentalarches. Relatively indistinct microridges were widely distributed on the gingival epithelial cell surfaceof the upper jaw. Scrollwork and network patterns of microridges were clearly observed on the gin -gival epithelial surface of the lower jaw.
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.
The Australian thorny devil, Moloch horridus Gray, 1841, and the Texas horned lizard, Phrynosoma cornutum Harlan, 1825, have the remarkable ability to rapidly move water through interscalar spaces on their skin’s surface to their
mouth for drinking. The morphology of these scale hinges has not been studied. We used histological and SEM techniques to
examine and compare the scale hinges of both species. Additional taxa in their respective lineages were examined in order
to evaluate the potential that convergent evolution has occurred. In the two species that transport water, each scale hinge
has a basally expanded and semi-enclosed channel formed by the hinge joint that is interconnected with all scale hinges on
the body. We hypothesize that it is within this semi-tubular channel system of hinge joints, where the β-layer keratin of
the integument is very thin, that water is transported. Hinge joint walls are covered by a complex topography of fractured
surfaces that greatly expand the channel’s surface area and probably enhance capillary transport of water. In addition, we
note differing morphology of scale surfaces at the rear of the jaws of both species. We hypothesize that capillary forces
fill the scale-hinge system and additional forces, generated within the mouth by observed motions during drinking, depress
local water-pressure to pull water through the channels of the hinge-joint system. We conclude that the combined features
in the two species, semi-tubular hinge-joint channels with convoluted walls and a jaw-buccal cavity pumping-mechanism, have
convergently evolved for capture, transport, and drinking of water from sporadic rainfall.
Three different types of lingual papilla were observed by scanning electron microscopy on the dorsal lingual epithelium of the lizard Gekko japonicus. Dome-shaped lingual papillae were located at the apex. Flat, fan-shaped lingual papillae were seen in the widest area of the lingual body. Long, scale-like lingual papillae were arranged on the latero-posterior dorsal surface. At higher magnification, microvilli and microridges were seen to be widely distributed over the surface of the papillae. By light microscopy, the epithelium of the dome-shaped papillae was composed of single, columnar epithelial cells filled with secretory granules. The tip of the epithelium of the fan-shaped and scale-like papillae was composed of stratified squamous epithelial cells without granules. The major part of the epithelium of these two types of papilla, except the tip area, was also composed of single, columnar epithelial cells with secretory granules. By transmission electron microscopy, a nucleus without a defined shape was seen to be located in the basal part of each of the single, columnar epithelial cells. Rough-surfaced endoplasmic reticulum and Golgi apparatus were well developed around the nucleus. The other, major part of the cytoplasm was filled with the spherical secretory granules, a large number of which had very electron-dense cores and moderately electron-dense peripheral regions. In the stratified squamous epithelium, a nucleus, which tended to be condensed on the free-surface side, was located in the center of each cell. Mitochondria, endoplasmic reticulum, and vesicles were observed in the cytoplasm.
This study employed light microscopic (LM), scanning electron microscopic (SEM), and transmission electron microscopic (TEM) methods to provide detailed morphological information on the histological and ultrastructural features of the dorsal tongue epithelium of Rhinoclemmys pulcherrima incisa. SEM revealed columnar papillae laterally, as well as papillae, which tend to have a ridge-like appearance in the center of the tongue. LM and TEM showed three different zones of lingual epithelium: a stratified apical area with serous cells at the top of the papillae, a stratified lateral area with both serous and mucus cells, and an unstratified glandular area consisting of distinct glandular ducts with mucus cells. Comparison with morphological data from other turtles shows that the lingual epithelial structure in R. p. incisa is in accordance with that observed for other generalized omnivores which prefer a terrestrial lifestyle, thus matching the ecological information about this species.
The tongue is often considered a key innovation in the evolution of a terrestrial lifestyle as it allows animals to transport food items through the oral cavity in air, a medium with low density and viscosity. The tongue has been secondarily coopted for a wide diversity of functions, including prey capture, drinking, breathing, and defensive behaviors. Within basal lizard groups, the tongue is used primarily for the purpose of prey capture and transport. In more derived groups, however, the tongue appears specialized for chemoreceptive purposes. Here we examine the tongue structure and morphology in lacertid lizards, a group of lizards where the tongue is critical to both food transport and chemoreception. Because of the different mechanical demands imposed by these different functions, regional morphological specializations of the tongue are expected. All species of lacertid lizards examined here have relatively light tongue muscles, but a well developed hyobranchial musculature that may assist during food transport. The intrinsic musculature, including verticalis, transversalis, and longitudinalis groups, is well developed and may cause the tongue elongation and retraction observed during chemoreception and drinking. The papillary morphology is complex and shows clear differences between the tongue tips and anterior fore-tongue, and the more posterior parts of the tongue. Our data show a subdivision between the fore- and hind-tongue in both papillary structure and muscular anatomy likely allowing these animals to use their tongues effectively during both chemoreception and prey transport. Moreover, our data suggest the importance of hyobranchium movements during prey transport in lacertid lizards.
Background:
The ability to detect chemical cues is highly developed in Scleroglossa, and particularly in anguid lizards. This ability was predicted because anguids possess a well-developed vomeronasal organ (VNO) (or Jacobson's organ) and rely largely on chemical cues in various behaviours as other active foragers. In this work, we have investigated the possible functional association between tongue flicking and the VNO in the lizard Anguis fragilis.
Methods:
The morphology of the tongue and the buccal cavity was investigated by light and scanning electron microscopy. The kinematics of tongue and jaw movements was studied by high speed cinematography.
Results:
The epithelial cells of the ventral aspect of the tongue tips show microstructures (microridges, microfacets, micropores) which are not present on other areas of the mouth. Beneath the tongue, the floor of the buccal cavity shows two concave-like elevations suggesting a structural analogy with the anterior processes described in snakes. The apex and the internal margin of these processes bear parallel oblique ridges. Taste buds occur anteriorly on the buccal floor and on the palate and are abundant on the internal side and on the edge on the anterior processes. The tongue showed three modes of tongue flicking: simple downward extension, single oscillation, and multiple oscillations. At each tongue flick, the ventral surface of the tips was observed contacting the substratum. Immediately after the tongue retraction, the buccal floor moved slightly upward. The observation of tongue flicking with the mouth open showed that the anterior processes moved upward when the tongue was retracted.
Conclusions:
These observations suggest that following: 1) during tongue flicking the ventral surface of the tongue tips invariably makes contact with the substratum; 2) the microstructures of the tongue tips and the ridges of the anterior processes might be helpful for collecting and receiving, respectively, chemicals during tongue flicking; 3) the anterior processes may be apposed on the roof of the mouth next to the ducts of VNOs when the buccal floor is fully elevated; 4) due to their localization, the taste buds could be equally stimulated by the molecules transferred during tongue flicking.
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.
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.
Based on regional differences in surface morphology, the dorsum of the tongue of Anolis carolinensis can be subdivided into four distinct zones. The first quarter of the tongue is relatively smooth, whereas the second and fourth quarters are festooned with closely packed cylindriform papillae, which are covered by typical parakeratotic stratified squamous epithelium. The third quarter of the tongue is covered by papillae of novel morphology that we have named "plumose papillae." These are composed of a slender connective tissue core covered by stratified squamous epithelium from whose surface numerous elongated cells radiate. These "plume cells" are about 30-40 microns long and have an extremely irregular nucleus in their expanded terminus. Their stalks are affixed by desmosomes to the deeper cells of the epithelium, and their free surfaces are covered by intricately patterned microplications. Their cytosol contains a dense web of 100-A cytofilaments that may be involved in maintaining the peculiar morphology of the cells. Regardless of type, all lingual papillae of A. carolinensis contain a single longitudinally oriented skeletal muscle fiber that originates from the underlying lingual muscles, raising the possibility that the papillae can be moved at will. The plumose papillae and their retinue of plume cells are unique morphological structures that may be important in mastication and deglutition of food.
The anatomy of the hyo-lingual apparatus in the iguanid lizard Oplurus cuvieri has been studied by light microscopy and scanning electron microscopy. Four areas were observed on the dorsal lingual epithelium of the lizard. Tongue tips are covered with a smooth epithelium. Closely packed flattened and cylindriform papillae cover the foretongue. The surface of the midtongue bears an unpapillose epithelium. Short conical papillae are arranged on the two lateral posterior bundles of the tongue. At high magnification, microvilli and microridges are widely distributed over the surface of the papillae. The epithelium of the papillae is composed of cells filled with secretory granules. Each surface plays successive roles during food ingestion, intra-buccal transport, and swallowing. The mucous interpapillary spaces would serve the adherence between the tongue and the food, the smooth epithelium of the midtongue should facilitate movements of the prey toward the pharynx, and conical papillae of the hindtongue present a rough surface which should act on the prey during the swallowing phase. The intrinsic morphology of the tongue is rather similar to that previously described for iguanids, but fibers of M. verticalis encircles ventrally the lingual process. These fibers could act in tongue protrusion as previously suggested for agamids. The morphology and function of the extrinsic tongue musculature and the hyoid musculature, analysed by electrical stimulations, are similar to the previous descriptions in iguanids and agamids either for feeding or displaying functions.
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.
Light microscopical (LM) and scanning (SEM) and transmission (TEM) electron microscopical methods were used.
SEM 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.
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.
The kinematics of feeding in the gekkotan lizard Phelsuma madagascariensis (Scleroglossa) was investigated using high-speed cinematography (200-300 frames s(-)(1)) and X-ray films (64 frames s(-)(1)). Qualitative kinematic analysis of the head and jaw displacement of the prey to (capture) and within (reduction, transport, swallowing, licking) the buccal cavity are compared for two types of prey (crickets and mealworms) in 30 feeding sequences from four individuals. Maximal displacement of structures and timing of events are compared statistically to assess the differences among the phases and the prey using analysis of variance. P. madagascariensis uses its jaws only to capture the two types of prey item, and the capture jaw cycle is divided into fast-opening (FO), fast-closing (FC) and slow-closing (SC) stages only. As in iguanians and other scleroglossans, the reduction and transport cycles always involve a slow opening (SOI and SOII) stage before the FO stage, followed by FC and SC stages: this last stage was not easily identified in all feeding phase. Transport of the prey was followed by a large number of licking cycles. Our data show (i) that the capture profile in gekkotans is similar to that observed for other scleroglossans and different from that described for iguanians (e.g. the absence of an SO stage); (ii) that the kinematics of jaw and related hyo-lingual cycles of intraoral manipulation (reduction and transport) are similar in lizards with a very different hyo-lingual system (Iguania, Gekkota and Scincomorpha), suggesting a basic mechanism of feeding cycles in squamates, transformed in varanids and snakes; and (iii) that prey type affects the kinematics of capture and manipulation, although the high level of variation among lizards suggests a possible individual modulation of feeding mechanism. A principal components analysis was performed to compare capture and transport cycles in this study of P. madagascariensis (Gekkota) and a previous study of Oplurus cuvieri (Iguania). This analysis separated the capture cycle of each species, but the transport cycles were not completely separated. These results demonstrate the complexity of the modulation and evolution of feeding process in squamates.
Studies of the comparative morphology of the tongues of living vertebrates have revealed how variations in the morphology and function of the organ might be related to evolutional events. The tongue, which plays a very important role in food intake by vertebrates, exhibits significant morphological variations that appear to represent adaptation to the current environmental conditions of each respective habitat. This review examines the fundamental importance of morphology in the evolution of the vertebrate tongue, focusing on the origin of the tongue and on the relationship between morphology and environmental conditions. Tongues of various extant vertebrates, including those of amphibians, reptiles, birds and mammals, were analysed in terms of gross anatomy and microanatomy by light microscopy and by scanning and transmission electron microscopy. Comparisons of tongue morphology revealed a relationship between changes in the appearance of the tongue and changes in habitat, from a freshwater environment to a terrestrial environment, as well as a relationship between the extent of keratinization of the lingual epithelium and the transition from a moist or wet environment to a dry environment. The lingual epithelium of amphibians is devoid of keratinization while that of reptilians is keratinized to different extents. Reptiles live in a variety of habitats, from seawater to regions of high temperature and very high or very low humidity. Keratinization of the lingual epithelium is considered to have been acquired concomitantly with the evolution of amniotes. The variations in the extent of keratinization of the lingual epithelium, which is observed between various amniotes, appear to be secondary, reflecting the environmental conditions of different species.
The return of Atlantic salmon (Salmon salar) to their home river for spawning coincides with drastic skeletal alterations in both sexes. Most prominent is the development of a kype (hook) at the tip of the lower jaw in males. Salmon that survive spawning have to cope with the kype throughout their life, unless it disappears after spawning, as was suggested in the early literature. To understand the fate of the kype skeleton, we compared morphological and histological features of kypes from pre-spawned mature anadromous males (grilse) with post-spawned males (kelts). The kype of male grilse is supported by fast-growing skeletal needles that differ from regular dentary bone. In kelts, growth of the kype skeleton has stopped and skeletal needles are resorbed apically by osteoclasts. Simultaneously, and despite the critical physiological condition of the animals, proximal parts of the kype skeleton are remodelled and converted into regular dentary bone. Apical resorption of the skeleton explains reports of a decrease of the kype in kelts. The conversion of basal kype skeleton into regular dentary bone contributes to the elongation of the dentary and probably also to the development of a larger kype in repetitive spawning males.
Feeding in lepidosaurs Feeding: Form, function and evolution in tetrapod vertebrates (pp. 175–291) Functional morphology of the scale hinges used to transport water: Convergent drinking adaptations in desert lizards
- K Schwenk
- W C Sherbrooke
- A J Scardino
- R De Nys
- L Schwartzkopf
Schwenk, K. (2000). Feeding in lepidosaurs. In K. Schwenk (Ed.), Feeding: Form, function and evolution in tetrapod vertebrates (pp. 175–291). San Diego: Academic Press. Sherbrooke, W. C., Scardino, A. J., de Nys, R., & Schwartzkopf, L. (2007). Functional morphology of the scale hinges used to transport water: Convergent drinking adaptations in desert lizards (Moloch horridus and Phrynosoma cornutum). Zoomor-phology, 126, 89–102.
Ueber die Zungendrusen von Anguis, Pseudopus und Lacerta. Arch Fur Mikrosk Anat
- Von Seiler
von Seiler, R. F. (1891). Ueber die Zungendrusen von Anguis, Pseudopus und Lacerta. Arch Fur Mikrosk Anat, 38, 177–265.
The reptiles of the Indo-Australian archipelago
- N De Rooij
Gekko behavioral trait: Tongue wiping spectacle
- H R Bustard
- HR Bustard
Evaluating the complexity of the trophic system in Reptilia
- V L Bels
- VL Bels
Feeding in lepidosaurs Feeding: Form, function and evolution in tetrapod vertebrates
- K Schwenk
Die Zungendriisen von Lacerta
- R F Von Seiler
Australian reptiles in colour
- H G Cogger
- HG Cogger
Ueber die Zungendrusen von Anguis
- R F Von Seiler
- RF Seiler von
- N Rooij de