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THE ANATOMICAL RECORD 246:305-316 (1996)
Ultrastructural Study of the Dorsal Lingual Epithelium of the
Soft-SheII TurtIe, Trionyx cartilagineus (CheIonia, Tr ionychidae)
SHIN-ICHI IWASAKI, TOMOICHIRO ASAMI, AND CHAITIP WANICHANON
Department of Histology IS.-IJ.) and Department of Anatomy ( T A . ) , The Nippon Dental
University School of Dentistry at Niigata, Niigata, Japan; Department of Anatomy, Faculty
of Science, Mahidol Uniuersity, Bangkok, Thailand (C.
W.)
ABSTRACT
Background: The soft-shellturtle, Trionyx cartilagineus, is
classified phylogenetically to the family Trionychidae, whose members live
in small rivers or ponds. The purpose of the present study was to examine
the ultrastructure of the dorsal epithelium of the tongue of the soft-shell
turtle and to compare the results of the observations with those reported
for the tongue of other freshwater turtles.
Methods: Light microscopy, transmission electron microscopy, and scanning electron microscopy were used to examine the dorsal epithelium of the
tongue of the soft-shell turtle.
Results: The tongue is triangular with a slightly round apex when viewed
dorsally but it appears flattened when viewed laterally. Lingual papillae
were visible on the dorsal surface of the tongue with some localized variations. Irregular, dome-shaped or ridge-like papillae were observed on the
anterior part of the dorsal lingual surface. Large, cylindrical papillae were
located along the midline of the posterior part of the tongue. Low, disk-like
papillae were located on both sides of the dorsal surface of the posterior
part of the tongue. Taste pores were recognizable in the center of the disklike papillae. At higher magnification, scanning electron microscopy revealed microridges on the surface of cells located on the outermost side of
the anterior part of the tongue, and the thickenings of cell margins were
clearly seen. Microvilli were distributed compactly over the entire posterior part of the tongue. Light microscopy revealed that the mucosal epithelium of the anterior part of the tongue was of the keratinized, stratified
squamous type, while the mucosal epithelium of the posterior part of the
tongue was of the nonkeratinized, stratified cuboidal type. In the lateroposterior part of the tongue, taste buds were recognized. Transmission
electron microscopy revealed that the epithelium of the anterior part of the
tongue was of a typical keratinized type. Small numbers of keratohyalin
granules and membrane-coating granules appeared in the cytoplasm of the
shallow intermediate layer. On the apical side of the lingual papillae located on the posterior side of the tongue, cells from the intermediate layer
to the surface layer of the non-keratinized epithelium contained many fine,
discoidal granules. A large part of the epithelium consisted of mucous cells
in the concave area on the posterior side.
Conclusions: The dorsal surface and epithelium of the tongue of the softshell turtle differed significantly from those of other freshwater turtles, in
spite of the similarity in terms of gross morphology among the tongues of
such turtles. o 1996 Wiley-Liss, Inc.
Key words: Soft-shell turtle, Tongue, Lingual papillae, Microridges, Microvilli, Ultrastructure, Epithelium, Keratinization
The soft-shell turtle, Trionyx cartilagineus, belongs
to the order Chelonia and the family Trionvchidae.
whose members live in small rivers or bonds. This spe:
Received December 1, 1995; accepted June 11 1996.
cies is widely distributed in tropical areas of Asia.
Address reprint requests to
Shin-Ichi Iwhaki,
Department of
These tuhles often dig into the mud and, in addition, Histology, The Nippon Dental University School of Dentistry at Niithey sometimes spend time on land near their fresh- gata, 1-8 Hamaura-cho, Niigata 951, Japan.
=,
0 1996 WILEY-LISS, INC.
306
S.-I. IWASAKI ET AL.
water habitat. They are, thus, adapted to terrestrial
life to some extent. However, they take small fishes,
frogs, shrimps, shellfishes, aquatic insects, and some
aquatic grasses as food from aquatic environment. This
feeding habitat is not very different from that of other
freshwater turtles distributed in the tropical areas of
Asia.
It has been shown that, together with variations in
the shape of the tongue itself, the form and the pattern
of distribution of the lingual papillae exhibit significant variations among different species of reptiles
(Iwasaki and Miyata, 1985; Robinowitz and Tandler,
1986; Schwenk, 1986; Iwasaki, 1990a, 1992; Mao et al.,
1991; Iwasaki et al., 1992; Iwasaki and Kumakura,
1994). There are also many differences in the nature of
the dorsal lingual epithelium in reptiles. These differences can be categorized phylogenetically and, at the
same time, they reflect the adaptation of reptiles to
their environments t o a certain extent. For example,
the lingual epithelium of completely terrestrial reptiles has a tendency to be keratinized (Mao et al., 1991;
Iwasaki and Kumakura, 1994), while that of the reptiles that live in or near ponds or small rivers has a
tendency to be nonkeratinized (Iwasaki, 1992; Iwasaki
et al., 1992). The tongues of reptiles that live under
amphibious circumstances tend to have both keratinized and nonkeratinized epithelium in different parts
of the tongue (Schwenk, 1988; Iwasaki, 1990a; Iwasaki
and Kobayashi, 1992).
The purpose of the present study was to examine the
histological and ultrastructural features of the lingual
epithelium of the soft-shell turtle by light microscopy,
scanning electron microscopy, and transmission electron microscopy and to compare the results of the observations with those reported for the tongues of other
reptiles, in particular, those of other freshwater turtles. The eventual goal of our comparative ultrastructural studies is to clarify the relationship between the
ultrastructural features of the lingual epithelium and
the lifestyles of turtles that live in different environments.
After rinsing in 0.1 M cacodylate buffer, some of the
samples for transmission electron microscopy were
postfixed in a phosphate-buffered solution (pH 7.4) of
1%osmium tetroxide a t 4°C for 1.5 hours. This procedure was followed by dehydration, epoxy-resin embedding, ultrathin sectioning, and double-staining with
lead citrate and uranyl acetate. The specimens were
then observed under a transmission electron microscope (JEM-1200 EX;JEOL, Tokyo).
Some of the specimens embedded in epoxy resin were
cut into semithin sections of 1 pm in thickness and
stained with Toluidine blue for examination by light
microscopy.
RESULTS
Scanning Electron Microscopy
The tongue of the soft-shell turtle, T. cartilagineus, is
triangular with a round apex when viewed dorsally,
but it appears flattened when viewed laterally. The
length of tongues of turtles varied from 4.8 to 5.5 mm,
and the width of the lingual radix varied from 7.1 to 7.8
mm. The radix was connected to the pharynx. Lingual
papillae were observed on the dorsal surface of the
tongue, with some local differences (Fig. 1).Irregular,
dome-shaped or ridge-like papillae were observed on
the anterior part of the dorsal lingual surface. Ridgelike papillae meandered over the surface, and protrusions of the desquamating epithelium were scattered
over the surface (Fig. 2).At higher magnification, microridges were clearly seen over the entire surface of each
superficial cell in this region. The thickening of cell
margins was also visible (Fig. 3).
Large, cylindrical papillae were located along the
midline of the posterior part of the tongue. The diameter of these papillae ranged from 150 to 450 pm, and
their height ranged from 200 to 600 pm (Fig. 4). The
outline of each cell on the outermost side of these papillae was clearly recognizable. These cells varied in
shape, but most of them were polygonal (Fig. 5). Higher
magnification revealed the compact distribution of microvilli on the free surface of the cells (Fig. 6).
Low, disk-like papillae were located on both sides of
MATERIALS AND METHODS
the dorsal surface of the posterior part of the tongue.
Five male and five female adults of Trionyx carti- The diameter of each disk-like papilla ranged from 250
Zugineus were purchased commercially in Bangkok, to 300 pm. Ridge-like folds occupied the area between
Thailand. The length of their carapaces ranged from these disk-like papillae. The width of these folds was
4.5 to 7.5 cm and the width ranged from 4.0 to 6.5 cm. almost constant. There was a small pore in the center
Under ether anesthesia, turtles were killed by decap- of each discoidal papilla (Fig. 7). At higher magnificaitation. Specimens were fixed in 2.5% glutaraldehyde tion, the outline of each cell was clearly visible, and
for 8 hours and transferred to 0.1 M phosphate buffer microvilli were distributed compactly on the free sur(pH 7.4) at Mahidol University. After the specimens face of the cells, as they were in the area along the
had been sent to the Nippon Dental University, Japan, midline of the posterior part of the tongue. The mithey were fixed in half-strength Karnovsky solution crovilli varied in length (Fig. 8).
that contained 2% paraformaldehyde and 2.5% gluLight Microscopy
taraldehyde (pH 7.4).After rinsing in 0.1 M cacodylate
Light microscopy revealed that the mucosal epithebuffer, samples for scanning electron microscopy were
post-fixed in a phosphate-buffered solution (pH 7.4) of lium of the anterior part of the tongue was of the strat1%osmium tetroxide at 37°C for 2 hours. These sam- ified squamous type. A lamina propria was located beples were then treated with 8 N hydrochloric acid at tween the mucosal epithelium and the lingual muscle.
60°C for 30 minutes in order t o remove the mucus from The connective tissue of the lamina propria seldom
the surface of the tissue. This procedure was followed formed papillae. A keratinized layer was clearly visible
by dehydration, freeze-drying in tertiary butanol and in the epithelium. In the basal layer and deep intermesputter-coating with platinum and palladium ions. The diate layer, the cells were almost spherical and their
specimens were examined with a scanning electron mi- nuclei were also spherical and relatively large. The
deep intermediate layer was composed of several layers
croscope (S-800; Hitachi, Tokyo).
Fig. 1. Scanning electron micrograph of the dorsal lingual surface.
Bo, lingual body; arrow, lingual apex. x 20.
Fig. 2. Scanning electron micrograph of the anterior part of the
dorsal lingual surface. x 58.
Fig. 3. Higher-magnfication scanning electron micrograph of the
epithelial surface of the anterior part of the tongue. Mr, microridges;
arrow, thickening of cell margins. X 3,500.
Fig. 4. Scanning electron micrograph of large, cylindrical papillae
(Cy) located along the midline of the posterior part of the tongue. x 58.
Fig. 5.Scanning electron micrograph of the surface of a large, cylindrical papilla. x 2,300.
Fig. 6.Higher-magnification scanning electron micrograph of the
superficial cells of the lingual epithelium of a large, cylindrical papilla. Mv,microvilli. x 5,800.
Fig. 7.Scanning electron micrograph of the surface of a low, disklike papilla located on the side of the dorsal surface of the posterior
part of the tongue. Arrow, a small pore. x 140.
Fig. 8.Higher-magnification scanning electron micrograph of the
superficial cells of the lingual epithelium of a low, disk-like papilla
located on the side of the dorsal surface of the posterior part of the
tongue. Mv, microvilli. x 8,000.
DORSAL LINGUAL EPITHELIUM OF T. CARTILAGINEUS
Fig. 9. Light micrograph of the dorsal mucosa of the anterior part
of the tongue. Ct, connective tissue of the lamina propria; Ep, lingual
epithelium. Epoxy resin embedding, Toluidine blue staining. X 340.
Fig. 10. Light micrograph of the mucosa of the apical part of a
large, cylindrical papilla located along the midline of the posterior
part of the tongue. Ct, connective tissue of the lamina propria; Ep,
lingual epithelium. Epoxy resin embedding, Toluidine blue staining.
x 340.
of cells. In the shallow intermediate layer, cells became
suddenly flattened, and there was a rapid transition to
the keratinized layer. A layer of desquamating cells on
the outermost side of the keratinized layer was also
noted (Fig. 9).
The mucosal epithelium along the midline of the posterior part of the tongue was of the stratified-cuboidal
type. The connective tissue of the lamina propria penetrated deeply into the center of each papilla. There
were some differences between the epithelium in the
309
Fig. 1 1. Light micrograph of the mucosa of the concave part at the
bottom of a large, cylindrical papilla located along the midline of the
posterior part of the tongue. Ct, connective tissue of the lamina propria; Ep, lingual epithelium. Epoxy resin embedding, Toluidine blue
staining. x 340.
Fig. 12. Light micrograph of the mucosa of the central part of a low
disk-like papilla located on the side of the dorsal surface of the posterior part of the tongue. Ct, connective tissue of the lamina propria;
Ep, lingual epithelium; Tb, taste bud. Epoxy resin embedding, Toluidine blue staining. x 340.
apical region and that in the basal region of each cylindrical papilla. Although, in both regions, most of the
cytoplasm of each superficial cell contained translucent
material, the thickness of the layer of these cells varied
significantly: that on the apical region of the papillae
was thinner than that on the basal region of the papillae. Therefore, this kind of cell on the apical region
formed only the surface layer, while these cells on the
basal region formed both the shallow intermediate
layer and the surface layer (Figs. 10,111. Furthermore,
310
S.-I.IWASAKI ET AL.
mucous cells increased in number closer to the basal
region (Fig. 11).
The mucosal epithelium of the low, disk-like papillae, which were located on both sides of the dorsal surface of the posterior part of the tongue, was almost the
same as that of the cylindrical papillae. However, the
surface layer of cells, the cytoplasm of which contained
translucent material, was relatively thin. The connective tissue of the lamina propria had the same profile
as the disk-like papillae themselves. A taste bud was
found in the center of each disk-like papilla on the
lateral sides of the posterior region of the tongue. The
location of each taste bud coincided exactly with that of
the individual pores observed by scanning electron microscopy. In the peripheral area of the disk-like papillae, the layer of cells with cytoplasm that contained
translucent material became somewhat thicker (Fig.
12).
Transmission Electron Microscopy
Transmission electron microscopy revealed that the
cells of the basal and deep intermediate layers of the
epithelium of the anterior part of the tongue were elliptical in shape, and a large elliptical nucleus was
seen in the central region of each epithelial cell. A
basement membrane lay between the basal cells of the
epithelium and the lamina propria. Hemidesmosomes
were found occasionally along the basal surfaces of the
basal cells. The epithelial cells extended fine cellular
processes in all directions, and desmosomes joined the
processes of adjacent cells. Intercellular spaces were
relatively wide (Fig. 13). The cytoplasm of these cells
contained mitochondria, free ribosomes, rough endoplasmic reticulum, and bundles of tonofibrils, and the
nucleus in each cell contained well-developed heterochromatin. A few Merkel cells were located between
keratiocytes (Figs. 13, 14).
The cells of the intermediate layer became abruptly
flattened, as did their nuclei. As shown in Figure 12,
the cells in the shallow intermediate layer were significantly flattened and their nuclei were condensed or
absent. The cytoplasm contained many bundles of
tonofibrils, a relatively large number of membranecoating granules, free ribosomes, rough endoplasmic
reticulum, and small numbers of small keratohyalin
granules. The cell membranes of the intermediatelayer cells were smooth in some cases and slightly undulated in others. Desmosomes frequently joined adjacent cells. Intercellular spaces became narrower as the
cells progressed from the deep intermediate layer to
the shallow intermediate layer. A keratinized layer
was located on the apical side of the shallow intermediate layer and appeared with an abrupt transition
from the shallow intermediate layer (Fig. 15).
The cells in the surface layer were significantly flattened and their nuclei had completely disappeared.
Most of the cytoplasm was filled with keratin fibers
and high electron-density. Hardly any other organelles
were visible. Very fine, cellular processesjoined by desmosomes were still observed in this layer. Intercellular
spaces were relatively wide as compared to those of the
underlying shallow intermediate layer. The cells lying
on top of the keratinized layer were of the desquamating type. In this layer of desquamating cells, keratin
fibers became looser, and each fiber, which was some-
what thicker than the tonofibrils and tonofilaments,
was clearly distinguishable. The rugged surface of cell
membranes originated from cellular processes in the
underlying layer and coincided with the microridges.
Cementing substances, which were secreted from membrane-coating granules, were scattered in the intercellular spaces (Fig. 16).
Ultrastructural features of the epithelium of the cylindrical papillae and of the discoidal papillae of the
posterior part of the tongue were fundamentally similar except for small differences in the thickness of the
layer of cells that contained granules, as also noted by
light microscopy. As shown in Figures 17 and 18, the
cells of the basal and deep intermediate layers of the
epithelium of the posterior part of the tongue appeared
irregularly elliptical or somewhat flattened in shape;
the nucleus was large and irregularly elliptical, lying
in the central region of each epithelial cell. The cytoplasm of these cells contained mitochondria, free ribosomes, rough endoplasmic reticulum, glycogen granules, and bundles of tonofibrils. Cellular processes
extended in all directions and desmosomes joined the
processes of adjacent cells. Intercellular spaces were
relatively wide, and a basement membrane lay between the basal layer of the epithelium and the connective tissue of the lamina propria.
As shown in Figure 19, the cells in the shallow intermediate layer were elliptical, and their nuclei were
also elliptical and located centrally. Most of the cytoplasm contained fine, discoid granules. The electron
density of these granules varied. Small numbers of free
ribosomes, mitochondria, and glycogen granules were
scattered in the cytoplasm. In some cells of this layer,
well-developed, rough endoplasmic reticulum was observed. Cellular processes still extended in all directions; desmosomesjoined the processes of adjacent cells
and intercellular spaces were still relatively wide.
As shown in Figures 20 and 21, the cells of the surface layer were somewhat elongated in the basoapical
direction, and their nuclei were located basally. Most of
the cytoplasm was filled with fine, discoidal granules.
The electron density of these granules varied from medium to high, but usually it was high. Microvilli extended from the apical surfaces, while smaller and less
regularly shaped processes extended from the basolatera1 surfaces. Intercalated desmosomes were also seen.
Junctional complexes were well developed between the
apical half of the adjacent cells of the outermost side.
Intercellular spaces were narrow and neighboring cells
were in close contact with each other, as compared with
Fig. 13. Transmission electron micrograph of the basal and deep
intermediate layers of the epithelium of the anterior part of the
tongue. N, nucleus; Em, basement membrane;Ct, connective tissue of
the lamina propria; Cp, cellular processes; Me, Merkel cell. x 5,000.
Fig. 14. Transmission electron micrograph of the deep intermediate
layers of the epithelium of the anterior part of the tongue. N, nucleus;
R, free ribosomes;T, tonofibrils. x 10,000,
Fig. 15. Transmission electron micrograph of the shallow intermediate and keratinized (KI)layers of the epithelium of the anterior part
of the tongue. N, nucleus; T,tonofibrils; MCG, membrane-coating
granule. x 10,000.
Fig. 16. Transmission electron micrograph of the keratinized layer
(KI).Cs, cementing substance. x 15,000.
DORSAL LINGUAL EPITHELIUM O F T.CARTILAGINEUS
Figs. 13-16.
311
312
S.-I.IWASAKI ET AL.
sea turtle (Iwasaki et al., 1996). In the freshwater turtles G . reevesii (Iwasaki, 1992) and C . japonica
(Iwasaki et al., 1992), for example, ridge-like lingual
papillae, on which dome-shaped bulges or cells are
compactly distributed, are located over the entire dorsal lingual surface. In the soft-shell turtle, by contrast,
three types of lingual papillae with different shapes
were observed on the dorsal lingual surface. The reasons for such differences were not identified in the
present study. More observations of different turtles
that belong to different families and live in different
habitats are necessary.
Microridges are widely observed on the dorsal lingual surface of mammals, in particular on the interpapillary surface. They disappear with the progression
of keratinization (Iwasaki et al., 1987, 1988; Iwasaki
and Miyata, 1989,1990; Iwasaki, 1990b).Microvilli are
predominantly located on the dorsal lingual surface of
G . japonicus (Iwasaki, 1990a), G . reevesii (Iwasaki,
1992), and C . japonica (Iwasaki et al., 1992) although
the development of microridges is less pronounced than
in T. tachydromoides (Iwasaki and Miyata, 1985). As
DISCUSSION
pointed out by Sperry and Wassersug (19761, microStudies of the gross morphology and ultrastructure ridges might play a role in the retention and spreading
of reptilian tongues are of interest because such of mucus on the epithelial cell surface. Microvilli on the
tongues are highly variable (Goin and Goin, 1962; Patt surface of the oral epithelial cells are also thought to
and Patt, 1969). The Reptilia, as a paraphyletic unit, have a function similar to that of microridges. Furtherinclude taxa that differ radically in terms of the his- more, it is assumed that, as in the case of lingual patology of the lingual epithelium, as for example, in the pillae, both microvilli and microridges function as supTestudines (Iwasaki, 1992; Iwasaki et al., 1992) and porting structures for the uptake of food, which is more
Lepidosauria (Morgan and Heidt, 1978; Rabinowitz easily attached to a rough surface covered with mucus
and Tandler, 1986; Schwenk, 1986, 1988; Iwasaki, than to a smooth surface.
1990a; Smith and Mackay, 1990; Mao et al., 1991;
The lingual epithelium of the freshwater turtle is
Iwasaki and Kobayashi, 1992). Ultrastructural studies entirely of the nonkeratinized, stratified, cuboidal type,
of the tongues of some species of squamates, namely, but that of the soft-shell turtle consists both of the keraColeonyx variegata, Gymnophutalumus lineatus, tinized, stratified, squamous type and the nonkeratiAmeiva bifrontuta, Cnemidophorus tigris, and Lygo- nized, stratified, cuboidal type, depending on the region
s o m sp. (Schwenk, 1988), Takydromus tachydro- of the lingual dorsum. These features of the soft-shell
moides (Iwasaki and Miyata, 1983, and Gekko japoni- turtle are also different from those of lizards (Iwasaki
cus (Iwasaki, 1990a), have revealed that lingual scales and Miyata, 1985; Rabinowitz and Tandler, 1986;
and lingual plicae are widely distributed on the dorsal Schwenk, 1988; Smith, 1988; Iwasaki, 1990a) and
lingual surface. Other species of squamates have very snakes (Ma0 et al., 1991; Iwasaki and Kumakura,
different types of lingual papilla. For example, fila- 1994). The dorsal lingual epithelium of the latter is
mentous or cylindriform papillae are found in Anolis mostly or entirely of the keratinized type. Thus, the
carolinensis (Rabinowitz and Tandler, 1986; Schwenk, epithelium of the soft-shell turtle seems to be interme1988) and Sphenodon punctatus (Schwenk, 1986) and diate between those of freshwater turtles, which are
reticular papillae are found in Goniocephalus grandis aquatic, and those of the lizard and snakes, which are
(Schwenk, 1988). By contrast, the tongues of the rat terrestrial. The lifestyle of the soft-shell turtle also
snakes, Elaphe quadrivirgata (Iwasaki and Kumakura, seems intermediate between those of aquatic and ter1994) and Elaphe climacophora (Iwasaki et al., 1996) restrial reptiles.
have no recognizable lingual papillae of any type on
the dorsal surface. Winokur (1988) determined, from
Fig. 17. Transmission electron micrograph of the basal layer of the
macroscopic and histological observations of eight spe- epithelium of the posterior part of the tongue. N, nucleus; Bm, basecies that represented all twelve families of extant tur- ment membrane; ct, connective tissue of the lamina propria; Cp, celtles, that the tongues of aquatic species have small lular processes. x 10,000.
lingual papillae or lack such papillae entirely, while
Fig. 18. Transmission electron micrograph of the deep intermediate
terrestrial species have tongues with numerous glan- layer of the epithelium of the posterior part of the tongue. N, nucleus;
dular papillae. Recently, fine-structural aspects of the Cp, cellular processes. x 6,000.
lingual epithelium of a few species of turtles have been
Fig. 19. Transmission electron micrograph of the shallow intermereported by Iwasaki (1992) and Iwasaki et al. (1992, diate layer of the epithelium of the posterior part of the tongue. N,
nucleus; G, fine, discoid granules; M, mitochondria;rER, rough endo1996).
In three dimensions, the fine structure of the lingual plasmic reticulum; Cp, cellular processes. X 6,000.
dorsal surface reveals clear differences between the
Fig. 20. Transmission electron micrograph of the surface layer of the
soft-shell turtle, other freshwater turtles in the family epithelium of the posterior part of the tongue. G, tine, dimoid granEmydidae (Iwasaki, 1992,Iwasaki et al., 19921,and the ules; Mu, mucous cell; Mv, microvilli. x 6,000.
the cells of the underlying layer (Fig. 20). In the most
superficial cells, fine, discoidal granules were present
in the apical region of the cytoplasm. Large, round nuclei were located basally in the cells. In the cytoplasm
between the nucleus and the discoidal granules, Golgi
apparatus, mitochondria, and rough endoplasmic reticulum were visible. On the basal side of the nucleus,
well-developed rough endoplasmic reticulum filled the
cytoplasm (Figs. 21,221. Some cells secreted these discoidal granules into the oral cavity. In such cases, each
granule was secreted successively and the secretion
seemed to be of the merocrine type (Fig. 23). As observed by light microscopy, mucous cells were present
in relatively large numbers in the basal areas of cylindrical papillae and in the concavities between disk-like
papillae. In the mucous cells found in the superficial
layer of the epithelium, almost spherical granules with
various degrees of electron-density occupied most of the
cytoplasm, and other organelles were hardly visible. A
small nucleus was seen in the basal region of each cell
(Figs. 24, 25).
DORSAL LINGUAL EPITHELIUM O F T. CARTILAGINEUS
Figs. 17-20,
313
314
S.-I. IWASAKI ET AL.
Fig. 21. Transmission electron micrograph of a cell containing fine,
discoidal granules in the surface layer of the epithelium of the posterior part of the tongue. N, nucleus; G, fine, discoidal granules; Ga,
Golgi apparatus; Cp, cellular processes; Mv, microvilli. x 8,000.
Fig. 22. Higher-magnificationtransmission electron micrograph of
the apical side of the nucleus of a cell that contains fine, discoidal
granules in the surface layer of the epithelium of the posterior part of
the tongue. N, nucleus; G, origin of fine, discoidal granules; rER,
rough endoplasmic reticulum. x 20,000.
Fig. 23.Higher-magnification transmission electron micrograph of
the apical side of a cell that contains fine, discoidal granules in the
surface layer of the epithelium of the posterior part of the tongue. G,
fine, discoidal granules; Mv, microvilli. x 20,000.
DORSAL LINGUAL EPITHELIUM OF 2'. CARTILAGINEUS
Fig. 24. Transmission electron micrograph of the basal side of mu-
(Mu) in the surface layer of the epithelium of the posterior
part of the tongue. N, nucleus; Cp, cellular processes. x 5,000.
CQUS cells
Fig. 25. Transmission electron micrograph of the apical side of a
mucous cell (Mu) in the surface layer of the epithelium on the poste-
In mammals, the tongue functions mainly as an organ for the uptake of food and sensing of taste (Graziadei, 1969). Salivary glands that discharge secretions
into the oral cavity are also well developed. The three
pairs of large extraoral glands are known as the major
salivary glands. Numerous small glands are widely
distributed in the mucosa and submucosa of the oral
cavity. These small glands are known as the minor
salivary glands and are composed of parenchymal elements invested in and supported by connective tissue.
The parenchymal elements are derived from the oral
epithelium and consist of terminal secretory units that
lead into ducts that eventually open into the oral cavity
(Hand, 1980). Several salivary glands are generally located around the oral cavity in various species of reptile. The location of the salivary glands in turtles is
unknown. However, aquatic turtles only have lingual
glands as salivary glands (Kochva, 1978). In addition,
previous studies (Schwenk, 1986; Iwasaki, 1990a,
1991; Iwasaki et al., 1992) support the present observations that the lingual epithelium contains numerous
cells with secretory granules. These results suggest
that, in reptiles, the tongue is an important organ for
secretion of granules or fluid into the oral cavity and
that this moist tongue is useful for catching food, just
as it is in frogs. However, the epithelium is clearly
315
rior part of the tongue. G, fine, discoidal granules of a neighboring cell
without mucous granules; M, mitochondriaof a neighboring cell without mucous granules; rER, rough endoplasmic reticulum of a neighbring cell without mucous granules; Mv, microvilli of a neighboring
cell without mucous granules. x 10,000.
different from that of the salivary glands of mammals
because it does not form a glandular structure. Most of
the epithelial cells of G . japonicus contain granules
with a bipartite structure (Iwasaki, 1990a). In the dorsal lingual epithelium two different types of granular
cell have been documented in three species of turtles,
T. curtilagineus, G . reeuesii (Iwasaki, 19921, and C.
juponica (Iwasaki et al., 1992), and both types of cell
are morphologically distinguishable from the granular
cells in G . juponicus: one type is the typical mucous
cell; the other type of cell contains numerous, round,
fine granules. The present and previous studies
(Iwasaki, 1992; Iwasaki et al., 1992) indicate that the
lingual epithelium of freshwater turtles contains mucous cells, as does that of lizards. "he fine, discoidal
granules are very similar in shape in T. curtilagineus,
G . reeuesii (Iwasaki, 1992), and C. juponicu (Iwasaki et
al., 1992). From the results of the present study, it
appears that the fine, discoidal granules are secretory
granules. However, their nature is unclear and remains to be determined by histochemical studies.
The present study indicated that taste buds were located in the dorsal epithelium of the tongue. Taste buds
have been observed on the tongues of some species of
turtles (Pevzner and Tikhonova, 1979; Spindel et al.,
1987; Korte, 1980) but not of others such as snakes
316
S.-I. IWASAKI ET AL.
(Iwasaki and Kumakura, 1994; Iwasaki et al., 1996).
The reason for this discrepancy remains to be explained.
In conclusion, the nature of the lingual epithelium of
the soft-shell turtle is intermediate between that of
other freshwater turtles in Emydidae and that of the
terrestrial lizard, in spite of the similarities in the
gross morphology of the tongue between the other
freshwater turtles and the soft-shell turtle. The differences seem to reflect the phylogenetic differences between the soft-shell turtle and turtles in the Emydidae
and/or the differences in lifestyle of the various turtles.
ACKNOWLEDGMENTS
The authors are grateful to Mr. M. Kumakura, Department of Anatomy, School of Dentistry at Niigata,
The Nippon Dental University, for his technical assistance.
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