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THE ANATOMICAL RECORD 247:149–163 (1997)
Ultrastructural Study of the Keratinization of the Dorsal
Epithelium of the Tongue of Middendorff’s Bean Goose,
Anser fabalis middendorffii (Anseres, Antidae)
SHIN-ICHI IWASAKI,1* TOMOICHIRO ASAMI,2 AND AKIRA CHIBA3
of Histology, The Nippon Dental University School of Dentistry at Niigata,
Niigata, Japan
2Department of Anatomy, The Nippon Dental University School of Dentistry at Niigata,
Niigata, Japan
3Department of Biology, The Nippon Dental University School of Dentistry at Niigata,
Niigata, Japan
1Department
ABSTRACT
Background: Comparative studies of ultrastructural features
of tongues allow deductions to be made about relationships between structure
and function, as reflected by an animal’s feeding habits. The present study was
performed to serve as a basis for further studies of avian feeding mechanisms
and of relationships between the fine structure of the lingual epithelium and
the development of the expression of keratins.
Methods: The light microscope, scanning electron microscope, and
transmission electron microscope were used.
Results: The dorsal surface of the tongue of Middendorff’s bean goose, Anser
fabalis middendorffii, has a distinctive anterior region that extends for
five-sixths of its length and has a clear posterior region. The anterior region,
when observed macroscopically and by scanning electron microscopy, is
distinguished along its forward half by a clear median line. The back half of the
anterior region has an indistinct median sulcus in some parts. There are no
lingual papillae on the entire dorsal surface of the anterior and posterior
regions. Giant conical papillae are located in a transverse row between the
anterior and posterior regions. On both lateral sides of the anterior region for
five-sixths of the length of the tongue, lingual hairs are compactly distributed,
and small numbers of large cylindrical papillae are arranged at almost regular
intervals between these lingual hairs. Examination of the dorsal lingual
epithelium by light and transmission electron microscopy provided histological and cytological criteria for distinguishing the anterior and posterior
regions, both of which were composed of stratified squamous epithelium.
Basal cells were similar throughout the dorsal epithelium. The intermediate
layer of cells in the anterior region contained numerous tonofibrils in electrondense bundles composed of tonofilaments of 10 nm in diameter. The outer
layer was composed of electron-dense, well-keratinized cells, with layers of
electron-lucent cells on the outermost surface. The cells in the intermediate
layer in the posterior region of the tongue were almost completely filled with
unbundled tonofilaments. The surface layer exhibited features of parakeratinization. In all of the giant conical papillae, the large cylindrical papillae, and
the lingual hairs, the epithelium was strongly keratinized.
Conclusions: The three-dimensional microanatomy and cytological features of the dorsal lingual epithelium of avians seem to be related to the
functional role and shape of the tongue of each species in feeding. Anat.
Rec. 247:149–163, 1997. r 1997 Wiley-Liss, Inc.
Key words: Middendorff’s bean goose; tongue; lingual papillae; epithelium; ultrastructure; keratinization
Most birds can fly but some cannot, and all are
adapted to their different environments with respect to
food sources, for example, the seashore, ponds, small
rivers, fields, or mountains. In a most extreme case,
penguins gather fish as food under the sea. Reflecting
r 1997 WILEY-LISS, INC.
Received 3 April 1996; accepted 12 September 1996.
*Correspondence to: Dr. Shin-ichi Iwasaki, Department of Histology, The Nippon Dental University School of Dentistry at Niigata, 1-8
Hamaura-cho, Niigata 951, Japan.
150
S.I. IWASAKI ET AL.
their different lifestyles, birds have different feeding
habits, with corresponding differences in the structures
of their bills and tongues.
Some studies (Zweers, 1974, 1982; Zweers et al.,
1977; Berkhoudt, 1985; Kooloos, 1986) have reported
synchronized interactions between the jaw and the
tongue during feeding and drinking in several avian
species. In addition, Homberger and Meyers (1989)
reported a more extensive examination of the biomechanical interactions of structural elements of the
lingual apparatus of Gallus gallus involved in feeding.
However, few data are available with respect to the
cytology of the lingual epithelium of birds.
In the present study, we describe the fine structure of
the dorsal lingual epithelium of the Middendorff ’s bean
goose. Our data can serve as a basis for further studies
of avian feeding mechanisms and of relationships between the fine structure of the lingual epithelium and
the development of the expression of keratin. Scanning
electron microscopy was used to examine relationships
between three-dimensional features and histological
structures observed in sections.
MATERIALS AND METHODS
Three Middendorff ’s bean geese (one adult male, one
adult female, and one young female), Anser fabalis
middendorffii, which is phylogenetically categorized to
the order Anseres and the family Antidae, were used in
this study. The birds weighed 5.0–5.6 kg in body weight
and had a wing span of 89.0–98.4 cm. All had been
found dead in a paddy field in winter in Toyosaka City,
Niigata Prefecture, Japan. Because the cadavers were
fresh but injured when they were found, they were
forwarded to us for macroscopic and microscopic examinations of physical condition and for estimation of the
causative factors of death.
After measurements of body size, visceral organs
including the tongue were quickly dissected out and
immersed in 10% formol for light microscopy or in
Karnovsky’s solution, which consisted of 5% glutaraldehyde and 4% paraformaldehyde in 0.1 M cacodylate
buffer (pH 7.4), for electron microscopy . After rinsing in
0.1 M cacodylate buffer, samples of tongues for transmission electron microscopy were postfixed in a phosphate
buffered solution of 1% osmium tetroxide at 4°C for 1.5
hr. This procedure was followed by dehydration and
epoxy resin embedding. The specimens were then observed under a transmission electron microscope (JEM1200 EX; JEOL, Tokyo). Semithin sections from the
blocks embedded in epoxy resin were stained with 0.2%
toluidine blue in 2.5% Na2CO3. Photomicrographs of
sections were taken under a light microscope.
After rinsing in 0.1 M cacodylate buffer, tongue
samples for scanning electron microscopy were postfixed in a phosphate buffered solution of 1% osmium
tetroxide at 37°C for 1.5 hr. These samples were then
treated with 8 N hydrochloric acid at 60°C for 20 min to
remove the mucus from the surface of the tissue. This
procedure was followed by dehydration, critical-point
drying, and platinum-palladium ion sputter coating.
The specimens were observed under a scanning electron microscope (S-800; Hitachi, Tokyo).
Fig.1. Macroscopic dorsal view of the tongue of Middendorff’s bean
goose, Anser fabalis middendorffii. Bo, lingual body; Pr, prominences
located on both sides of median line; Gp, giant conical papillae; Ra;
lingual radix; Lh, lingual hair; Ph, pharynx; Arrow, lingual apex. 30.8.
RESULTS
The cause of death of the three bean geese was
determined to be accidental. The tongues were analyzed as part of our ongoing studies of animal tongues,
with the following results. No significant differences
were observed between male and female or between
adult and young individual to the extent examined in
the present study.
Macroscopic Appearance
Each tongue was narrow and elongated in the anteroposterior direction, and the apical region of the tongue
was round. The width of the tongue was almost constant from the anterior region to the posterior region
but became slightly larger in the posterior direction.
The dorsal surface of the tongue had a distinctive
anterior region equal to five-sixths of its length, which
corresponds to the lingual body, and a posterior region
of one-sixth of its length, the lingual radix. The anterior
region of the lingual body was distinguished macroscopically along its forward half by a clear median sulcus.
The posterior half of the lingual body had an indistinct
median sulcus in some parts only. There were no
lingual papillae on the entire dorsal surface of the
lingual body and the lingual radix. Two anteroposteriorly elongated prominences, which meandered somewhat, were located on both sides of the median line.
Giant conical papillae were located in a transverse row
between the lingual body and the lingual radix. On both
lateral sides of the lingual body, lingual hairs were
compactly distributed, and small numbers of cylindri-
Fig. 2. Scanning electron micrograph of the lingual apex (arrow) and
the lingual body (Bo) of Middendorff’s bean goose, Anser fabalis
middendorffii. 318.5.
Fig. 3. Scanning electron micrograph of the dorsal surface of the
lingual body. Arrow, lingual sulcus. 322.5.
Fig. 4. Higher magnification scanning electron micrograph of the
surface of the lingual body. Mr, microridges; arrow, cell-margin
thickening. 35,500.
Fig. 5. Scanning electron micrograph of the lateral side of the lingual
body (Bo). Lh, lingual hairs; Cp, cylindrical papillae. 322.5.
KERATINIZATION OF THE DORSAL EPITHELIUM
Figs. 2–5.
151
152
S.I. IWASAKI ET AL.
Figs. 6–9.
KERATINIZATION OF THE DORSAL EPITHELIUM
cal papillae were arranged between these lingual hairs
(Fig. 1).
Scanning Electron Microscopy
Most of the dorsal surface of the lingual body was
relatively smooth, without any lingual papillae. The
epithelial surface of the region was slightly undulated
(Figs. 2, 3, 7, 8). The anterior region of the lingual body
was also distinguished along its forward half by a clear
median sulcus, except on the surface of the apex (Figs.
2, 3). Well-developed microridges were widely distributed on the cell surface of the dorsum of the lingual
body. Intercellular borders were clearly distinguishable
as cell-margin thickenings. The outline of each cell in
dorsal view was polygonal (Fig. 4). Scanning electron
microscopy clearly revealed, on both lateral sides of the
lingual body, compactly distributed lingual hairs and
small numbers of cylindrical papillae that were arranged at almost regular intervals between lingual
hairs (Fig. 5). Higher magnification scanning electron
microscopy indicated that the lingual hairs and the
cylindrical papillae had smooth surfaces with scattered
micropits and fine striations (Fig. 6). The hind half of
the lingual body had an indistinct median sulcus only
in some parts, as observed macroscopically. Two curved
anteroposteriorly elongated prominences were located
on both sides of the median line. Small dome-shaped
bulges were scattered on these prominences (Fig. 7).
The epithelium of the terminal end of the lingual body
had a very wrinkled surface (Figs. 8, 9). The desquamating cells could be easily recognized on the wrinkled
surface of the epithelium (Fig. 9). Well-developed, significant microridges adorned the surface of all the outer
epithelial cells in this area. Cell-margin thickening was
clearly visible, revealing the polygonal profile of each
cell (Fig. 10). Giant conical papillae were located in two
transverse rows between the lingual body and the
lingual radix (Figs. 1, 11). The structure of the outermost surface of these papillae was almost the same as
those of lingual hairs and cylindrical papillae; the
surface of the giant conical papillae tended to be
smooth, with scattered micropits and striations. However, relatively large numbers of desquamating cells
were seen on the surface of the giant conical papillae
(Fig. 12).
On the lingual radix, there were no lingual papillae,
apart from several giant conical papillae, on the entire
dorsal surface of the posterior region (Fig. 1). A median
sulcus was never observed. At lower and higher magnifications, the features of the epithelium of this area
were identical to these at the end of the lingual body.
Fig. 6. Higher magnification scanning electron micrograph of the
surface of a cylindrical papilla located on the lateral side of the lingual
body. Arrows, micropits. 3280.
Fig. 7. Scanning electron micrograph of two curved anteroposteriorly elongated prominences (Pr) that are located on both sides of the
median line. Bu, small bulges. 322.5.
Fig. 8. Scanning electron micrograph of the dorsal surface of the
proximal end of the lingual body (Bo). Gp, giant conical papilla. 322.5.
Fig. 9. Scanning electron micrograph of the epithelial surface of the
proximal end of the lingual body. 3110.
153
Light Microscopy
The epithelium of the entire lingual dorsum was of
the stratified squamous type. The connective tissue of
the lamina propria penetrated deeply into the epithelium, forming connective tissue papillae (Figs. 13–16).
In the lingual apex and the lingual body, apart from the
terminal end just in front of the giant conical papillae,
the stratified squamous epithelium was of the keratinized type. Penetration of the connective tissue was
clearly recognizable just beneath the keratinized layer,
implying the presence of very long rete pegs of the
epithelium (Figs. 13, 14). The cells of the basal layer
and the deep intermediate layer were round or elliptical, as were their nuclei (Fig. 13). From the deep
intermediate layer to the surface layer, the cells and
nuclei became gradually flattened. The cells were significantly flattened and strongly stained with toluidine
blue. Nuclei disappeared completely from the keratinized layer. These features are typical of orthokeratinization. Electron-lucent cells were on the outermost surface of the keratinized layer. These cells seemed to
coincide with desquamating cells (Fig. 14).
The features of cells in the epithelium from the basal
layer to the shallow intermediate layer were almost the
same at the proximal end of the lingual body as in the
rest of the lingual body (Figs. 15, 16). However, the
features of the outer surface of these two regions were
clearly different; at the proximal end of the lingual body
and in the lingual radix, the keratinized layer was very
thin and indistinct. Desquamating cell layers were also
recognizable on the outermost surface (Fig. 15).
The epithelium of the giant conical papillae, cylindrical papillae, and lingual hair was strongly keratinized.
The features of cells of the basal layer and the intermediate layer were almost the same as those of the lingual
body and the lingual radix. However, the epithelium
from the basal layer to the shallow intermediate layer
of these papillae was significantly thinner than that of
the anterior and posterior regions and lacked the
strongly developed rete pegs. By contrast, the keratinized layer of these papillae was rather thick (Fig. 17;
also see Fig. 18).
Transmission Electron Microscopy
The lingual body
The cells of the basal and deep intermediate layers of
the epithelium of the lingual body were round or
elliptical. A large elliptical nucleus was seen in the
central region of each epithelial cell. The basal lamina
was intercalated between the basal epithelial cells and
the lamina propria. Cell membranes were relatively
smooth all around the epithelial cells. Intercellular
spaces were narrow. The cytoplasm of these cells contained mitochondria, free ribosomes, rough endoplasmic reticulum, and bundles of tonofilaments. Heterochromatin was sparsely distributed in the nucleus of
each cell (Fig. 19). Desmosomes joined the cell membranes of adjacent cells from the basal layer to the
keratinized layer (Figs. 19–23).
The cells of the intermediate layer became abruptly
flattened, as did their nuclei. In the lower part of the
shallow intermediate layer, the cells were still elliptical. However, the nuclei were irregular in shape. Many
154
S.I. IWASAKI ET AL.
Fig. 10. Higher magnification scanning electron micrograph of the
cells at the outermost side of the epithelium of the proximal end of the
lingual body. Mr, microridges; arrow, cell-margin thickening. 35,500.
Fig. 11. Scanning electron micrograph of giant conical papillae (Gp)
located between the lingual body and the lingual radix. 328.
Fig. 12. Higher magnification scanning electron micrograph of the
epithelial surface of a giant conical papilla located between the
lingual body and the lingual radix. 3225.
KERATINIZATION OF THE DORSAL EPITHELIUM
155
Fig. 13. Light micrograph of the basal and the deep intermediate
layers of the dorsal epithelium (Ep) of the lingual body. Lp, lamina
propria; Ct, connective tissue papilla of the lamina propria. 3350.
Fig. 14. Light micrograph of the shallow intermediate (Sl) and the
keratinized (Kl) layers of the dorsal epithelium of the lingual body. Ct,
connective tissue papilla of the lamina propria. 3350.
bundles of tonofilaments occupied a large part of the
cytoplasm. Relatively large numbers of free ribosomes
and small numbers of mitochondria and rough endoplasmic reticulum were also seen in the cytoplasm. Keratohyalin granules were never observed. Cell borders were
irregular (Fig. 20). In the upper part of the shallow
intermediate layer, the cells and nuclei were flattened.
Most of the cytoplasm was filled with bundles of
tonofilaments. Relatively large numbers of free ribosomes were scattered among these bundles and tended
to be clustered. Small numbers of mitochondria were
still recognized. No keratohyalin granules were seen.
The cell membranes were slightly undulated. Intercellular spaces became narrower from the lower part of the
shallow intermediate layer to the upper part of the
shallow intermediate layer (Fig. 21). On the outermost
side of the shallow intermediate layer, just beneath the
keratinized layer, the cells became significantly flattened, and their nuclei had almost disappeared. Most of
the cytoplasm was filled with tonofibrils of medium
electron density. Very small numbers of coagulated
ribosomes were still recognizable among these tonofibrils, but no keratohyalin granules were ever observed.
Very fine processes composed of cell membrane were
still observed. Intercellular spaces were almost absent
in this zone of the intermediate layer (Fig. 22).
A keratinized layer, which was located on the apical
side of the shallow intermediate layer and appeared
with an abrupt transition from the shallow intermediate layer, showed the most different appearance from
the surface layer of the lingual radix. The cells in the
keratinized layer were significantly flattened, and their
nuclei had disappeared completely. Most of the cytoplasm was filled with keratin filaments of high electron
density. Hardly any other organelles were visible. Very
fine processes composed of cell membrane were still
observed. These epithelial cells formed a cornified cell
envelope when they became keratinized. The cells
located on the extreme free surface side of the keratinized layer were of the desquamating type. In this layer
of desquamating cells, keratin filaments became looser,
and each filament was clearly distinguishable. The
villous-appearing surface of cell membranes coincided
with the microridges seen under the scanning electron
microscope (Fig. 23).
The lingual radix
The cells of the basal and suprabasal layers of the
dorsal epithelium of the lingual radix were fundamentally similar to those of the lingual body. However, the
cells in these layers were relatively elongated and
elliptical as compared with those in the anterior region.
A large and elongated elliptical nucleus was located in
the center of each cell. The cytoplasm contained mitochondria, rough endoplasmic reticulum, free ribosomes,
tonofibrils, and vacuoles. Cell membranes were relatively smooth (Fig. 24). Desmosomes were frequently
observed between adjacent cells from the basal layer to
the surface layer; the same features were noted in the
lingual body (Figs. 24–28).
In the deep intermediate layer, the cells and nuclei
were round toward the shallow intermediate layer.
Tonofibrils increased in number, and free ribosomes
were still abundant. Mitochondria and regions of rough
endoplasmic reticulum were fewer in number and
appeared to be deteriorating. Intercellular digitation
was well developed. Intercellular spaces were hardly
ever seen (Fig. 25). In the shallow intermediate layer,
156
S.I. IWASAKI ET AL.
Fig. 15. Light micrograph of the dorsal epithelium (Ep) of the lingual
radix. Lp, lamina propria. 3175.
Fig. 17. Light micrograph of the keratinized (Kl) layer of the
epithelium of a cylindrical papilla. 3700.
Fig. 16. Light micrograph of the basal and the deep intermediate
layers of the dorsal epithelium (Ep) of the lingual radix. Lp, lamina
propria. 3700.
Fig. 18. Light micrograph of the basal and the deep intermediate
layers of the epithelium (Ep) of a giant conical papilla. Lp, lamina
propria. 3350.
the cells and nuclei were flatter than those in the deep
intermediate layer. A large part of the cytoplasm was
occupied by tonofibrils, and free ribosomes were scattered among these bundles. These ribosomes tended to
be aggregated but did not form granular structures.
Intercellular digitations could be seen (Fig. 26).
In the surface layer, the cells were significantly
flattened, and in most the nucleus had disappeared.
However, a few cells in the lower part of this layer
contained a pyknotic and condensed nucleus (Figs. 27,
28). Almost all the cytoplasm of these cells was filled
with tonofibrils. The electron density of these tonofilaments was lower than that of keratin filaments. A few
aggregated ribosomes were still visible in this layer.
Intercellular digitations disappeared. Instead, the cell
membrane formed fine processes all around the cell
surface (Fig. 27). These features remained apparent
until the outermost side of the surface layer. Cell
membranes formed microridges on the free surface side
of cells (Fig. 28).
The lingual papillae
The basal and suprabasal layers of the epithelium of
the giant conical papillae, the large cylindrical papillae,
and the lingual hairs were almost the same as those of
the lingual body and the lingual radix. In the deep
intermediate layer of all three kinds of lingual papilla,
the cells became suddenly flattened, as did their nuclei.
Bundles of tonofibrils increased in number in the
cytoplasm, and free ribosomes were scattered among
these bundles. Hardly any other organelles were recog-
KERATINIZATION OF THE DORSAL EPITHELIUM
Fig. 19. Transmission electron micrograph of the basal layer of the
dorsal epithelium of the lingual body. N, nucleus; Bl, basal lamina; Lp,
lamina propria; arrow, desmosome. 36,000.
Fig. 20. Transmission electron micrograph of the deep intermediate
layer. N, nucleus; Tb, tonofibrils; R, free ribosomes; arrow, desmosome.
36,000.
157
Fig. 21. Transmission electron micrograph of the shallow intermediate layer. N, nucleus; Tb, bundles of tonofilaments; R, coagulated free
ribosomes; arrow, desmosome. 320,000.
158
S.I. IWASAKI ET AL.
Fig. 22. Transmission electron micrograph of the cytoplasm of cells
on the outermost side of the shallow intermediate layer. Tb, tonofibrils; R, coagulated free ribosomes; rER, rough endoplasmic reticulum; arrow, desmosome. 310,000.
Fig. 23. Transmission electron micrograph of the keratinized layers
that contain cells of desquamating type on the extreme free-surface
side. Kf, keratin fibers; Mr, microridge; arrow, desmosome. 36,000.
nizable. Cell membranes were relatively smooth (Fig.
29). Desmosomes were intercalated among membranes
of neighboring cells from the basal layer to the keratinized layer (Figs. 29–31).
In the shallow intermediate layer of the epithelium of
the giant conical papillae, nuclei were condensed or had
disappeared. The cells were significantly flattened, and
cell membranes were smooth. Bundles of tonofilaments
also increased in number, and free ribosomes decreased
in number (Fig. 30). A thick keratinized layer was
located on the apical side of the shallow intermediate
layer and appeared with an abrupt transition from the
159
KERATINIZATION OF THE DORSAL EPITHELIUM
Fig. 24. Transmission electron micrograph of the basal layer of the
dorsal epithelium of the lingual radix. N, nucleus; Tb, tonofibrils; R,
free ribosomes; arrow, desmosome. 320,000.
Fig. 25. Transmission electron micrograph of the deep intermediate
layer of the lingual radix. N, nucleus; Tb, tonofibrils; arrow, desmosome. 36,000.
shallow intermediate layer. The cells were flatter than
those in any other layer. No nuclei were visible in cells
in this layer. Almost all the cytoplasm of these cells was
filled with keratin fibers. At higher magnification,
transmission electron microscopy revealed that bundles
of keratin fibers crossed over each other in all directions. These fibers made a speckled pattern composed of
areas of higher and lower electron density (Fig. 31).
These features were almost same as those in layers of
the large cylindrical papillae and the lingual hairs.
DISCUSSION
This study was carried out as part of an effort to
clarify the relationships between feeding habits and the
160
S.I. IWASAKI ET AL.
Fig. 26. Transmission electron micrograph of the shallow intermediate layer of the lingual radix. N, nucleus; Tb, tonofibrils; R, free
ribosomes; arrow, desmosome. 310,000.
Fig. 27. Transmission electron micrograph of the transitional area
between the shallow intermediate layer and the surface layer of the
lingual radix. Tb, tonofibrils; R, coagulated free ribosomes; arrow,
desmosome. 36,000.
Fig. 28. Transmission electron micrograph of the surface layer of the
lingual radix. N, nucleus; Tb, tonofibrils; Mr, microridges; arrow,
desmosome. 36,000.
Fig. 30. Transmission electron micrograph of the shallow intermediate layer of the epithelium of a giant conical papilla. N, nucleus; Tb,
bundles of tonofilaments. 36,000.
Fig. 29. Transmission electron micrograph of the deep intermediate
layer of the epithelium of a giant conical papilla. N, nucleus; Tb,
bundles of tonofilaments; R, free ribosomes. 310,000.
Fig. 31. Higher magnification transmission electron micrograph of
the cytoplasm of a cell in the keratinized layer of the epithelium of a
giant conical papilla. Kf, keratin fibers. 345,000.
KERATINIZATION OF THE DORSAL EPITHELIUM
Figs. 28–31.
161
162
S.I. IWASAKI ET AL.
structural features of tongues. Middendorff’s bean goose,
the little tern (Iwasaki, 1992a), and the chicken (Iwasaki
and Kobayashi, 1986) were chosen for a series of studies
of lingual morphology because these three species live
in different circumstances and have different feeding
habits; Middendorff’s bean goose lives around marshes
and in rice fields, the little tern lives near the seashore,
and the chicken is a domestic fowl.
The macroscopic morphology of the tongue of these
three species differs significantly. The tongue of Middendorff’s bean goose is long in the anteroposterior direction, and its width is almost constant from the anterior
region to the posterior region. The tongue of the little
tern is also long but very narrow (Iwasaki, 1992a). The
tongue of the chicken is long in the anteroposterior
direction and triangular, with a pointed apex (Iwasaki
and Kobayashi, 1986). Kooloos (1986) pointed out, from
observations of the pecking mechanism of the mallard,
that all movements of epidermal structures can be
interpreted as causing the transportation of food. The
present study suggests that the shape of the tongue is
most important for performing this function.
The shape of the tongue of Middendorff’s bean goose
is somewhat similar to that of the mallard (Berkhoudt,
1977; Kooloos, 1986). The tongue of the African gray
parrot is also long in the anteroposterior direction but a
relatively rounded profile, which is very different from
the tongues of the other species cited in this study
(Homberger and Brush, 1986). The three-dimensional
microarchitecture of the dorsal surface of the tongue
also seems to be specific to each species. On the chicken
tongue (Iwasaki and Kobayashi, 1986), filiform papillae, which are distinct protrusions of the desquamating
epithelial cells, are widely distributed over the anterior
region. In view of the way chickens feed, the fluffy
surface of the lingual dorsum, coated with mucous fluid,
seems to be suitable for retaining various foods. On the
tongue of the little tern (Iwasaki, 1992a), median papillae are located in the anterior region, and protrusions of
desquamating epithelial cells are prominent. The
notched surface of the lingual dorsum seems to be suitable for retaining small fishes, which the birds usually
catch with their tapering bills. Middendorff’s bean
goose usually eats water chestnuts, roots of rice plants,
and other water plants, which are relatively hard.
Cornified teeth, which are useful for biting off such hard
pieces of plants, are located on both sides of the bill. The
lingual papillae, such as the lingual hairs and cylindrical papillae, are arranged on both sides of the anterior
part of the tongue, adjacent to the cornified teeth of the
bills. Therefore, these structures might cooperate with
the cornified teeth in biting off parts of plants. Strong
keratinization of the epithelium of these papillae suggests good adaptation with respect to performance of
these functions. Micropits on the surface of these papillae are also observed on the surface of strongly keratinized epithelium of the lingual papillae of mammals
(Iwasaki et al., 1987). The striations observed on the
surface of the cylindrical papilla of Middendorff’s bean
goose might be generated by hard food during feeding.
In Middendorff’s bean goose, the little tern (Iwasaki,
1992a), and the chicken (Iwasaki and Kobayashi, 1986),
scanning electron microscopy has shown that the dorsal
surface of the posterior end of the tongue is relatively
smooth. This structure seems to be adapted to the
smooth swallowing of foods. The ultrastructure of the
dorsal lingual surface and tongue shape are quite
suitable to the feeding habits of each species.
Giant conical papillae, called ‘‘lingual spikes’’ by
Kooloos (1986), are arranged on the dorsal surface
between the lingual body and the lingual radix of the
mallard (Berkhoudt, 1977; Kooloos, 1986), the chick
(Iwasaki and Kobayashi, 1986), the little tern (Iwasaki,
1992a), and Middendorff’s bean goose in almost the
same pattern. The degree of keratinization of these
papillae is significant, as is the case for the lingual
papillae of the mongoose, a mammal (Iwasaki and
Miyata, 1990). However, the functional significance of
these giant conical papillae is unknown.
Biochemical analysis has demonstrated that a-keratins, found in 10-nm tonofilaments, are produced in the
epithelium of essentially all vertebrates (Franke et al.,
1978; Sun et al., 1979). In contrast, b-keratins, found in
3-nm cytoplasmic filaments, are detected only in specific epithelial tissue of birds and reptiles (Sawyer et al.,
1986; Landmann, 1986). Homberger and Brush (1986)
concluded that, in the parrot, b-keratins are expressed
exclusively in the anterior ventral region, whereas
a-keratins are detected in all parts of the lingual
epithelium. Furthermore, Carver and Sawyer (1989)
found that, in the chick, the anterior ventral epithelium
of the tongue contains a-keratin polypeptides characteristic of skin-type differentiation, whereas the epithelium
of the dorsal and posterior ventral regions contains
a-keratin polypeptides characteristic of esophageal differentiation (O’Guin et al., 1987). Moreover, b-keratins
appear to be produced only in the differentiated epithelial cells of the anterior ventral region of the tongue
(Carver and Sawyer, 1989). In contrast, in avian skin,
the appearance of keratohyalin granules is different in
the different regions examined. These granules are
present in epidermal cells of the inner surface and
hinge region of scutate scales or in generalized apteric
regions (Parakkal and Matoltsy, 1968; Matoltsy, 1969;
Parakkal and Alexander, 1972; Sawyer et al., 1974), but
they are not present in the epidermal cells of reticulate
scales (Sawyer and Borg, 1979).
In ultrastructural studies of the chick (Iwasaki and
Kobayashi, 1986), the little tern (Iwasaki, 1992a), and
Middendorff’s bean goose, no keratohyalin granules
were ever seen in any area of the dorsal lingual
epithelium, although the pattern of keratinization in
the surface layer of the anterior region of the tongue
clearly differed from that of the posterior region. Therefore, a mechanism for the control of epithelial keratinization of the tongue, which is different from that
proposed for mammals (Iwasaki, 1990a; Iwasaki and
Miyata, 1989, 1990), might be operative in the avian
lingual epithelium. The possibility, however, that droplet-shaped keratohyalin granules that have been found
in the lingual epithelium of mammals might affect
keratinization should not be completely ignored.
The present results indicate that terminal modifications of the squamous epithelial cells are different in
the lingual body and the lingual radix of Middendorff’s
bean goose, as is also the case in the little tern (Iwasaki,
1992a). Cytological features of surface-layer cells are
also different in the two regions of these species. In the
chicken tongue (Iwasaki and Kobayashi, 1986), terminal modifications of the dorsal epithelium are more
KERATINIZATION OF THE DORSAL EPITHELIUM
distinctly different in the anterior and posterior regions. Our ultrastructural observations may contribute
to the clarification of the relationship between structural features and feeding and, with biochemical analyses, may help us to clarify the mechanisms of local
differentiation of the lingual epithelium. We may ask
whether or not the environmental characteristics of an
animal’s life have any effect on the differentiation of its
oral mucosa, for example, on the keratinization of the
lingual epithelial tissue. In this connection, it would be
of interest to compare birds that live mainly in inland
areas with those that live mainly on the seashore or on
damp ground. From this point of view, the similarities
in keratinization of the lingual epithelium of Middendorff’s bean goose and the little tern seem to be strongly
related to the similarities in the habitats of the two
species. At the same time, the differences in the degree
of keratinization of the lingual epithelium between
these two species and the chicken seem to be based on
differences in habitat: the chicken lives in a habitat
much drier than that of Middendorff’s bean goose and
the little tern. Even clearer examples are provided by
reptiles. For example, the lingual epithelium of snakes,
which are adapted to dry terrestrial life, is strongly
keratinized (Mao et al., 1991; Iwasaki and Kumakura,
1994), whereas that of freshwater turtles, which are
adapted to aquatic life, is nonkeratinized (Iwasaki,
1992b; Iwasaki et al., 1992). The lingual epithelium of
lizards, which are adapted to an intermediate habitat,
exhibits intermediate levels of keratinization (Rabinowitz and Tandler, 1986; Schwenk, 1988; Iwasaki, 1990b;
Iwasaki and Kobayashi, 1992). In birds, the degree of
keratinization of the lingual epithelium seems to a
certain extent to reflect differences in lifestyle.
In conclusion, the three-dimensional microanatomy
and cytological features of the dorsal lingual epithelium
of avians seem to be related to the functional role and
shape of the tongue of each species in feeding.
ACKNOWLEDGMENTS
We are grateful to Dr. Ryuhei Honma, Environmental Analysis Center of Niigata Prefecture, for his generous supply of materials.
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