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R E S E A R C H A R T I C L E
S alem S . B ay ou m i
A lm - E ld een A . A b d - E lh am eed E l- S h ar k aw y M . M oh am ed
C O M PAR AT I VE S TU D I ES O N T H E D O R SAL L I N GU AL S U R FAC E O F T W O EGYPTIAN SQU AMATE R EPTILES W ITH TW O D IFF EREN T FEEDIN G H ABITS
ABSTRACT:
Several studies are concerned to study the mammalian tongue f rom the morphological standpoint, using modern techniques, in order to propose a f unctional hypothesis on f ood- tongue relationship during the successive f eeding process. However, no enough data are available in the literature about the correlation between the tongue morphology and the f eeding habits of many of the Egyptian reptiles. Theref ore, the present study is conducted to clarif y the morphological and histological appearance of the dorsal lingual surf ace of two Egyptian squamate reptiles having two diff erent f eeding habits; the insectivorous gecko, Tarentola annularis and the Egyptian vegetarian spiny tail lizard, Uromastyx aegypticus. The dorsal tongue surf ace is examined morphologically and by light and scanning electron microscopy (SE M). The results revealed that the tongue in both species is macroscopically dif f erent. At SE M, the dorsal lingual surf aces of both species are rich in lingual papillae of various shapes and sizes. In gecko, three types of lingual papillae are recognized; dom e-shaped, leaf -shaped and broad scale-like papillae on the lingual apex, body and root of the tongue, respectively. In lizard, broad scale-like papillae are observed on the apex, m eanwhile transverse parallel f olds, broad and short f olds, and leaf -like papillae are detected on the tongue body. Moreover, f lattened scale- like lingual papillae are f ound on the lingual root. Histological examination revealed that the dorsal lingual epithelium in both species consists of stratified squamous type which is para-keratinized in gecko and non-keratinized in lizard. The present data indicated that the morphological and histological variations of both tongues may be related to their f eeding habits. These results can give a contribution to the knowledge of the tongue anatom y and histology in two widely dif f used species in Egypt.
KEY W ORDS:
Reptilia, Tongue, SE M, Light microscopy
CORRESPONDANCE:
S alem S . B ay ou m i
Zoology Department, Faculty of Science, Tanta University
E-m ail: s ihambayoumi@ yahoo.c om
Abeer A b d - E lh am eed Alm -El deen Marwa Moham ed El- Sharkawy
Zoology Depart m ent, Facul ty of Science, Tanta Universi ty
ARTICLE CODE: 23.01. 11
INTRODUCTION:
In terms of gross anatom y, tongue shows great variability throughout vertebrates. Despite such variation, the dorsal surf ace of the tongue is usually covered by one or more types of elevations; the lingual papillae (Iwasaki, 2002). Many studies have demonstrated that the dorsal surf ace of the reptilian tongue is rich with lingual papillae (Sm ith 1986; Delheusy et al., 1994; Iwasaki et al., 1996a,b&c; Beisser et al., 1998&2001;
Abbate et al., 2009&2010). They reported that the f orm and the pattern of distribution of these papillae exhibit signif icant variations among dif f erent species of reptiles. Only in some turtles and snakes, the lingual papillae are absent on the entire surf ace of the tongue (W inokur, 1988; Mao et al., 1991; Iwasaki and Kumakura, 1994).
Schwenk (1988) studied the tongue morphology and some behavioral characters in lizards and concluded that “phylogeny is a better predictor to tongues morphology than is ecology”. In this consequence, the author divided the lizards into two sister-groups;
iguanians (Iguanidae, Agam idae, and Chaneleontidae) and scleroglossans (other f amilies). Iwasaki et al. (1996a&b) categorized the dif f erences, which have been seen in the f eatures of the dorsal lingual epithelium in reptiles, phylogenetically and at the same time they f ound that this variation reflects the adaptation of reptiles to their
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consequence, previous histological structures on the tongues of dif f erent reptile species ref lected adaptations to a dry habitat or to seawater, although stratification and keratinization of the lingual epithelium are com mon f eatures (Iwasaki, 1990; Iwasaki &
Kumakura, 1994; Toubeau et al., 1994;
Iwasaki et al., 1996a,b&c). However, no enough data are so f ar available in the literature about the correlation of the tongue morphology and the f eeding habits of many of the Egyptian reptiles. Therefore, the aim of the present study is to investigate the anatom ical, morphological and histological dif f erences of the dorsal lingual surf aces of two Egyptian squamate reptiles with diff erent f eeding habits; the gecko, Tarentola annularis which is an insectivorous and the Egyptian spiny tail lizard, Uromastyx aegypticus which is a vegetarian. Moreover, a com parison will be made between the present results and the results described previously in other reptiles in order to elucidate the correlation between the morphological appearance and the histological structures of the tongue, as well as the f eeding habits in reptiles.
MATERIAL AND METHODS:
Tongue of the white spot or annulated gecko, Tarentola annularis (Geof f ory, 1823);
order squamata, suborder lacertalia, f amily gekkonidae, and that of the E gyptian spiny tail lizard, Uromastyx aegypticus (Froskal, 1775);
order squamata, suborder lacertalia, f amily agamidae, were used in the present study. 12 specimens of both sexes from both species, 6 each, were used. The animals were captured f rom Abou-Rawash, Giza province, Egypt. The animals were anaesthetized with diethyl ether and the tongues were caref ully removed and processed as f ollow:
For SE M, the tongues were immediately f ixed overnight in m odif ied K arnovsky solution (92% paraformaldehyde and 2.5% glutraldehyde containing 0.1 M phosphate-buffered solution, pH 7.4 at 4ºC (Karnovsky, 1965). Af ter rinsing in 0.1 M phosphate buf f er, the samples were postf ixed in phosphate-buf f ered solution (pH 7.4) of 1% osmium tetroxide at 4ºC f or 2 hours. The specimens were then washed in 0.1 M phosphate buf f er solution f or several times bef ore treating with 3N hydrochloric acid f or 20 min at 60ºC to remove extra cellular mucus f rom the lingual surf ace. The specimens were then washed in phosphate buf f er and dehydrated in a graded ethanol series to the critical-point of drying and gold coated. The specimens were then examined and photographed by a Joel 5300JSM SEM at the f aculty of science, Alexandria University, Egypt.
For light microscopy, small pieces of the tongues were f ixed in 10% buf f ered f ormalin f or at least 24 hours, dehydrated and
embedded in paraf f in wax. 5 Mm thick serial sections were cut transversely and stained with haematoxylin and eosin.
RESULTS:
Gecko:
The tongue of gecko is dorso-ventrally f lattened with lanceolate appearance, somewhat rounded tip and with inverted V- shaped end. The tongue is conf luent with the f loor of the buccal cavity f or its entire length and its posterior portion is in continuity with the hyoid musculature. It is about 1 cm in length and 0.3 cm width. The thickness of the tongue gradually increases towards the pharynx. Anatomically, the tongue consists of three parts; lingual apex, lingual body, and lingual root (Fig. 1).
Fig. 1. Phot ogr aph of the geck o t ongue showin g lingual Apex (LA), Lingual body (LB) and lingual r oot ( LR).
Scanning electron microscopic examination revealed that the tip of the lingual apex has a narrow and short f urrow (Fig. 2). The lingual papillae are com pactly distributed throughout the entire dorsal lingual surf ace. Morphologically, three types of lingual papillae with dif f erent sizes and shaped are determined. These papillae are dome-shaped, f an-shaped, and broad scale- like papillae.
Fig. 2. Sc anning electr on micr ogr aph of the dors al lingual surfac e of geck o showing furr ow lingual apex ( LA) and dome-s haped papillae ( DP).
The dome-shaped lingual papillae are scattered along both lateral edges, on the dorsal surface of the apex, and on the body of the tongue. The surfaces of the papillae are
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surfaces generally bear taste buds with their fine pores and residual mucous substance can be seen at the surface of the papillae (Figs 3&4). Flat leaf-shaped lingual papillae with pointed ends are compactly distributed over the wide area of the lingual body. They are directed posteriorly and are increasing in length backwardly (Fig. 5). Broad scale-like papillae are arranged in overlapping rows on the lingual root. They have wide bases and wide tips with some cracks on its free end. Taste pores can be noted on the surface of some papillae.
Moreover, desquamated cells are observed on the most of these papillae. These papillae are directed backwardly (Fig. 6).
Fig. 3. Higher magnification of (fig. 2) showing dome- shaped lingual papillae ( DP) and t aste por es (TB).
Fig. 4. Higher magnific at ion of (f ig.3) s howing taste bud ( TB), taste por e (TP) and r es idual of muc ous substanc e ( MS).
Fig. 5. Sc anning electron micr ogr aph of the lingual body of geck o t ongue s howing dome-s haped papillae (DP) and f lat fan- shap ed papillae ( FP).
Fig. 6. Sc anning electr on micr ogr aph of the lingual r oot of geck o tongue showing br oad sc ale- lik e papillae (BP), des quamat ed c ells ( arrows) and t ast e por es ( arr owhead).
Histological observations revealed that the dome-shaped lingual papillae have short stalks and broad f lat surf aces. Connective tissue core arises f rom the lamina propria and penetrates deep into the canters of these papillae. The epithelium that covers the papillae is a thin para-keratinized stratified squamous. A thin layer of squamous cells can be seen at the outer surf ace of the papillae.
Taste buds are located at the dorsal and lateral wall of the papillae as a small hill- shaped epithelial protrusion of the papillary surf ace. These buds are opened externally by taste pores. The cells of the taste buds that are chief ly spindle in shape, have elongated and basally located nuclei (Fig. 7).
Fig. 7. Photomicr ogr aph of a tr ans vers e s ection of the lingual ap ex of geck o tongue s howing dome- shaped papilla (DP), taste bud ( TB), taste por e (TP) and non- k er at inized squamous epit heliu m ( arrowhead).
The f lat f an-shaped lingual papillae have slightly bended point proj ection that directed backwardly. A narrow connective tissue core penetrates the papillae canters.
The surf aces of the papillae are covered by a thin layer of para-keratinized stratified squamous epithelium. Taste buds are absent (Fig. 8).
ISSN: 2090 - 0511 On Line ISSN: 2090 - 0503 http://www.egyseb. org Fig. 8. Photomicr ogr aph of a tr ans vers e s ection of
the lingual body of geck o t ongue showing flat f an-s haped lingual papilla (FP), c onnective tissue c or e ( CTC) and k er at inized epitheliu m ( arr owhead).
In the broad, scale-like lingual papillae, the papillae have a broad irregular surf ace, narrow base and long constricted stalk. The mucosa consists of an outermost thin para- keratinized stratified squamous epithelium, beneath which is a dense network of connective tissue called lamina propria, in which numerous blood capillaries are f ound.
The lamina propria is continuous with the connective tissue which penetrated deeply into the canters of the papillae. The connective tissue core is m uch wider than in other two papillae.
Fig. 9. Photomicr ogr aph of a tr ans vers e s ection of the lingual r oot of geck o t ongue s howing br oad scale-s haped lingual papilla ( BP) and k er at inized epithelium ( arrowhead).
Lizard:
The tongue of the lizard is triangle in shape and is f lattened dorso-ventrally with sharp apex and inverted U-shaped end. It is about 2.5 cm in length and 1.5 cm width. It is
f ixed f rom its posterior part in the f loor of the buccal cavity and its anterior part is free. No anatom ical or morphological demarcations can be observed between its parts; the apex, the body, and the lingual root (Fig. 10).
Fig. 10. Phot ogr aph of the lizar d t ongue showin g lingual ap ex ( LA), lingual body ( LB) and lingual r oot ( LR).
Scanning electron microscopic examination revealed that the apex of the tongue has a bif urcated tip. This bif urcation is deep and wide. Lingual papillae are widely distributed all over the dorsal surf ace of the tongue except the tip that covered with desquamated epithelial cells (Fig. 11). Broad scale-like lingual papillae are arranged in parallel transverse rows j ust behind the desquamated lingual tip. The apical surf ace of these papillae is broad and smooth while neither taste buds nor taste pores are f ound (Fig. 12).
Fig. 11. Sc anning electr on micr ogr aph of the dors al surfac e of the ap ex lizar d tongue showin g bifurc at ed lingual apex (LA) and br oad sc ale- lik e papillae ( BP) desquamated epit helial c ells ( arr ow).
Fig. 12. Sc anning electr on micr ogr aph of th e anter ior part of t he lingual ap ex of lizar d t ongu e showing br oad sc ale- like papillae ( BP).
ISSN: 2090 - 0511 On Line ISSN: 2090 - 0503 http://www.egyseb. org At the anterior part of the lingual body,
numerous transverse parallel f olds are observed. At higher magnif ication, numerous and com pactly protrusions-like short microvilli are detected over the whole surf ace of these f olds (Fig. 13). At the middle region of the lingual body, the mucosal surf ace is decorated with densely broad and short f olds.
These f olds are semicircular structure with rounded tip; their surf aces are irregular due to the presence of small protrusions and their basal surf aces that appear to be com posed of com pactly small bulges. In addition, these f olds are rich with the taste pores (Fig. 14). At the dorsal surf ace of the posterior part of the body of the tongue, leaf -like papillae are scattered. These papillae are flattened dorso- ventrally, broad basally, and pointed posteriorly. Its surf ace is covered with squamous epithelial cells and rich with taste pores (Fig. 15).
Fig. 13. Sc anning electr on micr ogr aph of the anter ior part of the lingual body of lizar d showin g tr ans vers e par allel folds (TF). Note th e pr otr us ions lik e m icr ovilli ( arr ows).
Fig. 14. Sc anning electr on micr ogr aph of the middle part of t he lingual body of lizar d s howing br oad and short f olds (BF), s mall bulges ( B) at t h e bas al part of the papillae.
Fig. 15. Sc anning electr on micr ogr aph of th e poster ior part of t he lingual body of lizar d showing leaf-lik e papillae (LP) and small bulges (B) at their basal parts and t ast e pores ( arr ows).
The dorsal surf ace of the root of the tongue is covered by broad, f lattened and scale-like papillae. These papillae are backwardly directed and most of them are branched dorsally into two or more broad process (Fig. 16).
Fig. 16. Sc anning electron micr ogr aph of the lingual r oot of lizard showing f lat f an-shaped papillae (FP).
Histological observations of the mucosa of the apex region revealed that broad scale- like lingual papillae have broad straight surf aces with somewhat narrow bases and long constricted stalk. Connective tissue core arises f rom the lamina propria and penetrates deep into the canters of these papillae. The epithelium that covers the papillae is of a non- keratinized stratif ied squamous type (Fig. 17).
Fig. 17. Photomicr ogr aph of a tr ans vers e s ection of the lingual apex of t he lizard s howing br oad scale- lik e papillae (Bp) and non- k er at inized strat if ied squamous epit helium (arrowhead).
In the middle region of the body tongue the mucosal membrane is thrown into well developed, leaf -like papillae. These papillae are covered with non-keratinized stratified squamous epithelium (Fig. 18). Beneath the epithelium a well pronounced lamina propria which is continuous with connective tissue and penetrates the core of the f olds.
ISSN: 2090 - 0511 On Line ISSN: 2090 - 0503 http://www.egyseb. org Fig. 18. Photomicr ogr aph of a tr ans vers e s ection of
the poster ior part of the lingual body of th e lizar d showing leaf-lik e papillae ( LP) and non- k er at inized strat if ied squamous epit heliu m ( arr owhead).
The broad, f lat f an-shaped lingual papillae are observed at the dorsal surf ace of the root of the tongue. The connective tissue penetrated deeply into their centres. The apical surf ace of these papillae is divided into several processes (Fig. 19).
Fig. 19. Photomicr ogr aph of a tr ans vers e s ection of the lingual r oot of lizard s howing br oad sc ale- lik e papilla ( BP), and non- k er at inized strat ified squamous epit helium (arr owhead).
DISCUSSION:
The present study is carried out as a part of an ef f ort to clarif y the relationship between the f eeding habits and the morphological and histological f eatures of the vertebrates tongue. The tongues of two
Egyptian squamates; the gecko (insectivorous reptile) and the lizard (vegetarian reptile) are used in the present study. The results revealed that the tongues in the studied reptiles are macroscopically dif f erent. The tongue of the gecko is f lattened dorso-ventrally with lanceolate appearance and somewhat rounded tip with a narrow and shallow f urrow. The tongue of the lizard is also f lattened dorso-ventrally but it is triangle in shape and has pointed tip with wide and deep bif urcation. The presence of the bif urcation in the lingual tip of the investigated species agrees with m any other reptilian species that have dif f erent f eeding habits as in Takydromua takydromoides (Iwasaki and Miyata, 1985), in Gekko japonicas (Iwasaki, 1990), in Am erican chameleon (Rabinowitz and Tandler, 1991), in Oplurus cuvieri (Delheusy et al., 1994), and in Pogona vitticeps (Schaerlaeken et al., 2007).
The present results together with the previous studies indicated that there is no a signif icant ef f ect on the diff erence of the diet on the presence of this bif urcation.
Theref ore, it seems to be a phylogenetic structure in reptiles. This agrees with Estes and Pregill (1988) and Schewenk (1988) who used the lingual characters to build phylogenic relationships between lizards that show large concordances with that obtained f rom other morphological characters. The most important prediction of Schwenk’s study (1988) is that tongue morphology is related to phylogeny, and does not vary with ecological f actors (i.e. diet, habitat, water availability) of the niche occupied by each species. However, the dif f erence in the morphological structure of this bif urcation in the investigated species revealed that it might be related to the f eeding habits. W ide and deep bif urcation in herbivores lizard’s tongue may help in cutting and wounding dif f erent kinds of herbs while narrow and shallow bif urcation in the insectivores gecko’s tongue ref lect that the insects may be swallowed without any processing in the buccal cavity.
The present results indicated that the dorsal lingual surf aces of both gecko and lizard are rich in lingual papillae displaying various shapes and sizes. In gecko, three types of lingual papillae are recognized. These are dome-shaped, f lat leaf -shaped, and broad scale-like papillae on the lingual apex, body and root, respectively. In lizard, broad scale- like papillae are located on the lingual apex, whereas, transverse parallel f olds, broad short f olds, and leaf -like papillae are detected throughout the dorsal surf ace of the lingual body. In addition, broad, f lat and fan- shaped papillae are distributed on the dorsal surf ace of the lingual root. These results indicated that the same kinds of the lingual papillae are detected on the dorsal lingual
ISSN: 2090 - 0511 On Line ISSN: 2090 - 0503 http://www.egyseb. org surf ace of both species although their
arrangement is dif f erent. The presence of such kinds of the lingual papillae agree with many authors in diff erent reptiles (Rabinowitz and Tandler, 1986) in Am erican chameleon, Anolis carolinensis, (Sm ith, 1986) in varanus, (Delheusy et al., 1994) in the Collared iguanid lizard, Oplurus cuvieri, (Beisser et al., 1998&2001) ) in the Af rican mud turtle Pelusios castaneus and the red-eared slider Trachemys scripta elegans, and (Abbate et al., 2009&2010) in blue-tongue skink and Italian lizard. They reported that "based on the regional dif f erences in surf ace morphology, the dorsum of the tongue of can be subdivided into several distinct zones".
On the contrary, some reptiles, as some turtles and snakes, have no lingual papillae on the entire dorsal lingual surf ace (W inokur, 1988; Mao et al., 1991; Iwasaki and Kumakura, 1994). McDowell (1972) and Gillingham and Clark (1981) reported that snake's tongue does not appear to be important f or the direct intake of f ood but might be used exclusively f or olf action in co- operation with Jacobson's vomeronasal organs. The f licking of a snake's tongue is thought to be a way of adsorbing odorants in the air (Halpern et al., 1986).
On the other hand, carnivorous turtles, which live permanently in water, use suction f eeding f or intra-oral f ood transport, where water is drawn into the oral cavity by suddenly lowering the f loor of the mouth, so that water movement is the main m echanism of intraoral f ood transport (Bram ble and W ake, 1985; Beisser et al., 1998).
Generally, based on the absence of the lingual papillae on the entire dorsal lingual surf ace of the turtles, W inokur (1988) pointed out that the presence or f ormation of the lingual papillae is correlated with the adaptation of species to their habitat, diet, or f eeding behaviour. On the other side, Schwenk (1988) reported that tongue morphology is related to phylogeny, and does not vary with ecological f actors.
However, the dif f erences in the type and the arrangement of the dorsal lingual papillae in the present two Egyptian squamate reptiles that have dif f erent f eeding habits ref lect the impact of the f eeding mechanism on the morphological structures of the tongues in reptiles. In this consequence, Iwasaki (2002) reported that the shape and structure of the tongue dif f er signif icantly among reptiles, ref lecting the various f unctions of each respective tongue.
The present investigation revealed that dome-shaped lingual papillae and some taste buds are observed on the apical or lateral surf aces on the bif urcated lingual apex of the gecko. However, neither lingual papillae nor taste buds are noticed on the lingual bif urcated tip of the lizard. The pattern of
distribution of the lingual papillae on the lingual apex of gecko is similar to that of, Takydromus tachydromoides and Gekko japonicus (Iwasaki and Miyata, 1985;
Iwasaki, 1990). On the other side, the smooth lingual tip of the lizard is similar to what observed in Am erican chameleon (Rbinowitz and Tandler, 1986) and the iguanid lizard (Delheusy et al., 1994).
Schwenk (1985) assumed that in all iguanids, the taste buds are abundant on the papillae of the f ore-tongue. He explained that the role of such taste buds is to test the palatability of the prey when contacts with the tongue occur during capture. This may explain why taste buds are observed on the apical and lateral surf aces of the dome- shaped lingual papillae on the tip of gecko tongue while they are com pletely absent on the papillae of lizard tongue.
The present histological observations demonstrated that the dorsal lingual epithelium of the gecko and the lizard consists of stratif ied squamous type. In the gecko, there is a thin layer of keratin on the outer most surf ace while this layer is absent in the lizard. The keratinisation of the gecko tongue is in consistent with Iwasaki (1990) in lizard, Iwasaki and Kumakura (1994) in rat snake, and Toubeau et al. (1994) in lizard.
They reported that stratification and keratinisation of the lingual epithelium is a com mon f eature in reptiles. They explained this f eature as a ref lection of the dry f ood they eat. However, the absence of the keratin layer of the lizard tongue is in consistent with the tongue of turtle which eat herbs (Iwasaki et al., 1992; Beisser et al., 1995& 1998).
In lizards, similar dif f erences with respect to the histological structure of the lingual epithelium have been reported among species (Schwenk, 1985&1986; Sm ith, 1988;
Schwenk and Throckm orton 1989; Iwasaki, 1990; Toubeau et al., 1994). They f ound that the most signif icant dif f erences are f ound in the degree and extent of keratinisation of the lingual epithelium. The present study clarif ies that the dif f erence in the keratinisation pattern of the dorsal lingual epithelium in both species m ay be related to the f eeding habits.
In conclusion, morphological and histological f eatures of the dorsal lingual surf aces of two Egyptian squamate reptiles;
the gecko, Tarentola annularis and the Egyptian spiny tail lizard, Uromastyx aegypticus showed many dif f erences. These dif f erences ref lected the adaptation of these two species to their f eeding habits to a certain extent. These results could give a contribution to the knowledge of the tongue morphology and histology in these widely dif f used two species in Egypt.
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