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Functional Morphology of the Tongue in the Domestic Goose (Anser Anser f. Domestica)

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THE ANATOMICAL RECORD 294:1574–1584 (2011)
Functional Morphology of the
Tongue in the Domestic Goose
(Anser Anser f. Domestica)
HANNA JACKOWIAK,1* KINGA SKIERESZ-SZEWCZYK,1 SZYMON GODYNICKI,1
SHIN-ICHI IWASAKI,2 AND WILFRIED MEYER3
1
Department of Histology and Embryology, Poznań University of Life Sciences,
Wojska Polskiego 71 C, 60-625 Poznań, Poland
2
Advanced Research Center, Department of Histology, The Nippon Dental University
School of Dentistry at Niigata, 1-8 Hamaura–cho, Niigata 951, Japan
3
Institute of Anatomy, University of Veterinary Medicine Hannover Foundation,
Bischofsholer Damm 15, 30173 Hannover, Germany
ABSTRACT
Using LM and SEM methods, the study describes microstructures in
particular areas of the tongue of the goose. A thick multilayered keratinized epithelium forms the ‘‘lingual nail’’ and covers small and giant conical papillae, whereby the first functions as an exoskeleton of the tongue
apex, and the latter are arranged along the lingual and well-developed
connective tissue cores, and together with the bill lamellae are involved
in cutting. The row of conical papillae on the lingual prominence prevents
regurgitation of transported food. In the area of the ‘‘lingual nail’’ and in
the anterior part of the lingual prominence, Herbst corpuscles are accumulated, which allow to recognize food position. Filiform papillae, as
widely distributed between the conical papillae of the body, are responsible for filtering. They can be explained as long keratinized processes of
the epithelium and are devoid of connective tissue cores. During food
transport, the flattened areas of the lingual body and the lingual prominence are protected by a parakeratinized epithelium, but the root is covered by a nonkeratinized epithelium. The presence of adipose tissue in
the tongue probably reduces pressure during food passage, but also promotes mucus evacuation from the lingual glands, thus facilitating food
transport. An entoglossal bone with a continuation as cartilage is the
stable structural basis of the tongue system. Anat Rec, 294:1574–1584,
C 2011 Wiley-Liss, Inc.
2011. V
Key words: tongue; epithelium; lingual papillae; lingual nail;
Herbst corpuscles; domestic goose
The type of food intake and processing of food in animals are important factors to affect the morphological diversity of structures on the surface of the tongue.
Previous investigations of the oral cavity in birds focused
on the position of the tongue in the beak cavity and
detailed macroanatomical and microanatomical features,
such as diversity of mechanical papillae, types of epithelium covering the lingual mucosa and modifications of
skeletal structures, including the hyoid apparatus. Moreover, several earlier studies included already aspects of
the rich relief of the tongue in Anseriformes (McLelland,
C 2011 WILEY-LISS, INC.
V
1975, 1979; Vollmerhaus and Sinowatz, 1992; König and
Liebich, 2001).
*Correspondence to: Dr. Hanna Jackowiak, Department of
Histology and Embryology, Poznań University of Life Sciences,
Wojska Polskiego 71 C, 60-625 Poznań, Poland. Fax: þ48-61848-7623. E-mail: hannaj@up.poznan.pl
Received 9 November 2009; Accepted 25 May 2011
DOI 10.1002/ar.21447
Published online 9 August 2011 in Wiley Online Library
(wileyonlinelibrary.com).
MICROSTRUCTURE OF GOOSE TONGUE
Von Preuss et al. (1969) pointed out that the tongue
in the duck is ‘‘fleshy,’’ as related to the lack of a
cartilage skeleton and abundant adipose tissue. Other
publications concentrated on the specific microstructure
of the tongue, as, for example, in the bean goose (Iwasaki, 1997). Homberger and Brush (1986) studied the adaptation of the fleshy tongue of the parrot for processing
seeds. In the chicken, feeding with grains, and in the
carnivorous white-tailed eagle, there are numerous conical papillae at the end of the lingual body, pointing backwards to prevent food from moving back before
swallowing (Iwasaki and Kobayashi, 1986; Jackowiak
and Godynicki, 2006). Special structures observed in the
nutcracker are two long keratinized plates, which grow
from the ventral surface of the lingual apex and are
used for extracting seeds from pine cones (Jackowiak
et al., 2010). In the white-tailed eagle, the duck, and the
bean goose, the median groove of the tongue is an important instrument to influence the direction of food transport (Iwasaki, 1997; Jackowiak and Godynicki, 2006).
In some birds that swallow their food without processing it, the tongue can be much shorter. For instance in
the cormorant, the tongue has been reduced to a small,
connective tissue structure and can be regarded as rudimentary (Jackowiak and Godynicki, 2006). In the ostrich, the short tongue has no mechanical papillae but
contains numerous mucous glands for moistening the
beak cavity, which may be an adaptation to semi-arid climatic conditions (Jackowiak and Ludwig, 2008).
Finally, behavioural observations confirm that in birds
living in the water but also on land, such as geese, ducks
or swans, both the beak and the tongue are remarkable
tools used for cutting grass, solid food intake, drinking
and filtering water (Kooloos, 1986; Zweers et al., 1997;
Van Der Leeuw et al., 2003; Glatz et al., 2006).
In view of all this information, this study concentrates
on the microstructure of the tongue mucosa in the
domestic goose for a better definition of the specific functions of particular tongue areas during the processes of
grazing, pecking, filter-feeding, and drinking.
MATERIAL AND METHODS
The study was conducted using five tongues of adult
females (9-month-old, average weight 5.5 kg) of the
domestic goose, collected from the local slaughterhouse.
Immediately after dissection, the tongues were fixed in
10% formalin and then documented with a digital camera. For the light microscopical observations (LM), samples from the lingual apex, body, prominence, and root of
the tongue were dehydrated in an ascending series of
ethanol (70–96%) and routinely embedded in paraplast.
Histological slides of a thickness of about 4 lm were
stained according to the Masson-Goldner trichrome
method. The results were documented with an Axioscope
2 plus light microscope (Zeiss, Germany). The morphometric data were obtained using a KS 400 computer
morphometric system (Zeiss).
For observations under the scanning electron microscope
(SEM), the samples were dehydrated in a series of ethanol
(70–100%) and acetone (96%-abs.), and subsequently dried
at critical point using CO2 (Critical Point Dryer K850,
Emitech). All specimens were mounted on aluminium
stubs covered with carbon tabs, sputtered with gold (Sputter Coater S 150B, Edwards) and observed under the LEO
435 VP (Zeiss) at an accelerating voltage of 10–15 kV.
1575
Fig. 1. Dorsal view on the tongue of domestic goose. Black arrow
shows median groove. White arrow shows a row of conical papillae of
the lingual prominence. Arrowhead shows elevation of root lingual mucosa with 3–4 cone-shaped papillae. Continuous line marks area with
small conical papillae. Dotted line marks area with giant conical papillae. A, apex; B, body; LP, lingual prominence; R, root; L, laryngeal
prominence. Scale bar-1 cm.
Fig. 2. Dorsal view of the anterior part of tongue and beak of
goose. Black arrow shows squamous ‘‘lingual nail.’’ Arrowheads mark
laminae of beak edge. Asterisk shows depression of the beak. A,
apex; B, body. Scale bar-5 mm.
RESULTS
Macroscopic Observation
The tongue of the domestic goose was narrow and
elongated, and attached to the bottom part of the beak
by a short lingual frenulum at the level of the beginning
of the lingual prominence. Apart from the depression in
the anterior part, it tightly fitted into the beak cavity,
with three parts that could be distinguished: the apex,
the body and the root (Figs. 1, 2). The tongue had a total
length of 7 cm, whereby the apex measured about 1 cm,
the body with the lingual prominence 5.5 cm and the
root 0.5 cm. The width of the tongue was 1.3 cm at the
apex, 2 cm at the body, 1.1–2.1 cm at the lingual prominence and 1.4 cm at the root.
The apex of the tongue of the domestic goose was
rounded, and no lingual papillae were found on its
smooth edge (Figs. 1–3). On the ventral surface of the
tongue, a flat, triangular and white scale, called the ‘‘lingual nail’’ (Fig. 2) could be detected that covered sheathlike the anterolateral border of the apex. On the flat dorsal surface of the tongue body a shallow median groove
1576
JACKOWIAK ET AL.
Fig. 3. Dorsal view of the apex of the tongue with ‘‘lingual nail’’ protruding out from the ventral surface of the tongue (Ln). Arrow shows
single exfoliated superficial cell. A, apex.
Fig. 4. Sagittal-cross section through the apex of the tongue. In the
thick dorsal epithelium (Epd) arrow shows the superficial cells layer an
intensely stained cytoplasm. Epv, ventral epithelium, Ln, ‘‘lingual nail,’’
Enc, entoglossal cartilage. Scale bar-250 lm.
divided the lingual mucosa into two equal parts (Fig. 1).
Mechanical conical papillae bordered linearly and symmetrically the marginal parts of the body and were lined
along the lamellae at the bottom part of the beak (Figs.
1, 6).
In the anterior part of the body, 11 pairs of small conical papillae could be seen, with pointed processes
directed sideways and slightly backwards (Fig. 1). In the
posterior part of the body, four pairs of giant conical papillae were obvious, with pointed processes adjusted to
the back of the tongue (Fig. 1). The last giant conical papilla, located near the lingual prominence, was composed
of two parts that differed in size: a larger lateral part
and a smaller median part. Among the conical papillae
of the body, very densely arranged filiform papillae were
conspicuous (Figs. 6–8) on the dorsal surface of the
tongue as another papilla type (Fig. 8). These hair-like
structures were organized in 3–4 rows along the giant
conical papillae of the body, forming long, single, twisted
Fig. 5. Cross section through the superficial layer of the ventral epithelium of the apex. Ln, lingual nail. Scale bar-50 lm.
Fig. 6. Lateral view of the body of the goose tongue. Black arrows
show openings of the lingual glands. White arrows show filiform papillae. Arrowheads mark giant conical papillae. B, body; LP, lingual
prominence. Scale bar-3 mm.
processes. Additionally, at the posterior dorsal tongue
surface, 6–15 papillae with blunt processes pointing to
the back of the tongue (Fig. 10) were obvious at both
sides of the median groove. At both sides of the smooth
lateral surface of the body and the lingual prominence,
19 glandular openings formed straight lines (Fig. 6). The
distance between the openings ranged between 0.9–1.8
mm. The lingual prominence above the body of the
tongue was a triangular structure, the basal part of
which facing the root (Fig. 1). Alike the body it was divided into two symmetrical parts by the median groove.
On the posterior border of the lingual prominence, 10
mechanical conical papillae could be seen (Fig. 1), and
their pointed processes slightly overlapped the smooth
surface of the root. These papillae were usually arranged
in a single row, however, in one specimen two rows were
observed.
The root was the shortest part of the tongue and connated with the laryngeal prominence (Fig. 1), whereby
its flat surface was situated lower than the surface of
MICROSTRUCTURE OF GOOSE TONGUE
1577
Fig. 7. View on the marginal part of the body with small conical
papillae (SCo) and filiform papillae (Fp) of the goose tongue.
Fig. 9. Higher magnification of the basal part of the filiform papillae
immersed in the epithelium (Fp). B, surface of the body; Ep, epithelium. Scale bar-100 lm.
Fig. 8. Dorsal view of the posterior marginal part of the body with
giant conical papillae (GCo), filiform papillae (Fp), and hair-like papillae
(Hp). Scale bar-1 mm.
Fig. 10. Dorsal view of the posterior part of the body of the tongue.
Arrows show symmetrical papillae with blunt processes. Dotted line
points middle line of the tongue at lingual prominence.
the latter tongue part. The dorsal surface of the root
also showed 2–3 glandular openings. The lateral surface
of the tongue was marked by two elevations of the lingual mucosa (Fig. 1). Each elevation was composed of an
oval basal part and 3–4 cone-shaped papillae protruding
from it.
was highly developed in the lingual prominence and the
posterior part of the body of the tongue, where it had a
thickness of 4 mm. In the anterior part of the body and
the root it was not very abundant, and with 1–2 mm
clearly thinner. Such adipose tissue was also found
directly below the conical papillae of the body.
In the multilayered epithelium of the lingual mucosa,
a basal, an intermediate and a superficial layer could be
distinguished. In all parts of the tongue, the cells of the
basal layer were elliptic, their nuclei occupying two third
parts of the cell volume and showing 1 or 2 nucleoli (Fig.
17). The cells flattened towards the surface of the epithelium and created the intermediate layer (Fig. 18). The
cells in the lower part of this layer type appeared polygonal, with round nuclei, several nucleoli and a light and
homogeneously stained cytoplasm. In the upper part of
the intermediate layer located above the papillae of the
connective tissue, the cells were flattened, with nuclei elliptical in shape retaining still nucleoli. The cytoplasm
Microscopic Observations
The LM observations revealed an entoglossal bone as
skeletal element of the tongue in the domestic goose,
that had its continuation as a cartilage reaching as far
as half of the apex length (Fig. 4). The entoglossal bone
and the cartilage were covered by the mucosa and its
multilayered epithelium.
The characteristic morphological feature of the tongue
was yellow adipose tissue beneath the lamina propria of
the mucosa at the surface of the lingual body, the lingual
prominence and the root (Fig. 20). This specific structure
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JACKOWIAK ET AL.
Fig. 11. Higher magnification of the epithelium on the dorsal surface of the body. Arrow shows single exfoliated superficial cell.
Fig. 13. Higher magnification of the superficial layer of the epithelium of the dorsal surface of the body. Arrows show strongly stained
cells with flat and elongated cell nuclei. Scale bar-10 lm.
Fig. 12. Cross section through the epithelium (Ep) of the dorsal surface of the body. Arrow shows the continuous layer of intensely
stained cytoplasm of the superficial cells. Lp, lamina propria. Scale
bar-60 lm.
around the nuclei appeared darker than near to the nuclear membrane. The structure of the superficial layer of
the epithelium was very diverse, with superficial cells on
the apex and the body of the tongue, containing highly
condensed nuclei (Fig. 13). These cells formed continuous layers (Figs. 4, 12), whereby their cytoplasm stained
intensely red. In the superficial epithelial cells covering
the lingual prominence and the root, the nuclei were
small or absent. The less intense red color of the cytoplasm created the impression of single, noncontinuous
Fig. 14. Higher magnification of the epithelium on the dorsal surface of the lingual prominence. Arrow shows a single exfoliated cell.
Scale bar-20 lm.
strands (Figs. 15, 19, 24). SEM of the epithelium showed
the superficial cells to be exfoliated as single scales
(Figs. 3, 11, 14). The architecture of the superficial layer
covering the mechanical papillae was different, and
included a horny layer. Nevertheless, highly condensed
nuclei without nucleoli were still present in the cytoplasm (Fig. 21).
The results of the epithelial measurements revealed
differences between the three parts of the tongue. The
MICROSTRUCTURE OF GOOSE TONGUE
1579
Fig. 15. Cross section through the parakeratinized epithelium on
the surface of the lingual prominence (Ep). Arrow shows noncontinuous strands of the superficial cells with less intensely cytoplasm. Lp,
lamina propria. Scale bar-100 lm.
Fig. 17. Higher magnification of the basal layer of the parakeratinized epithelium on the lingual prominence. Arrow shows a rounded
cell nucleus with nucleoli. Lp, lamina propria. Scale bar-10 lm.
Fig. 16. Cross section through the mucosa of the lingual prominence with subepithelial Herbst corpuscles (H). Ep, epithelium. Scale
bar-50 lm.
average thickness of the epithelium at the dorsal surface
of the apex was 1,246 lm, at the body 420 lm, and at
the lingual prominence 557 lm. The root was covered by
an epithelium with a thickness of about 300 lm.
The mechanical papillae at the lingual surface of the
domestic goose had a well-developed core composed of
Fig. 18. Higher magnification of the intermediate layer of the parakeratinized epithelium on the lingual prominence. Black arrow shows
an oval cell nucleus in the lower part of the intermediate layer. White
arrow shows flattened cell nuclei, black arrow the intensely stained
cytoplasm around a cell nucleus in the upper part of the intermediate
layer. Scale bar-10 lm.
1580
JACKOWIAK ET AL.
Fig. 19. Higher magnification of the superficial layer of the parakeratinized epithelium on the lingual prominence. Black arrow shows two
strongly stained cells. In some epithelial cells, the cytoplasm is light
and flat nucleus are present (white arrows). Scale bar-10 lm.
Fig. 21. Cross section through the keratinized epithelium covered
conical papilla of the lingual prominence. Arrows show highly condensed nuclei in the keratinized layer (K). B, basal layer; I, intermediate layer; Lp, lamina propria. Scale bar-50 lm.
Fig. 20. Cross section of the posterior part of the lingual prominence with conical papillae (Co). Black arrow shows anterior mucous
glands surrounded by the adipose tissue (At). Arrowhead points excretory duct. Ep, keratinized epithelium. Scale bar-250 lm.
collagen-rich connective tissue (Fig. 20). The small conical papillae of the body of the tongue were 3.5 mm in
height, while the big conical papillae amounted 4.3 mm
(Figs. 7, 8). The thickness of the epithelium covering the
papillae of the body varied between 311 lm on the lateral surface and 525 lm on the top surface of the papillae. The thickness of the horny layer varied between 197
lm on the lateral surface and 396 lm on the top surface
of the papillae. The height of the conical papillae at the
lingual prominence amounted to 3 mm, with a width of
1.3 mm (Fig. 22). The average thickness of the epithelium covering the lateral surface was 266 and 489 lm at
the top surface of the papillae. The average thickness of
the horny layer at the lateral surface was 111 and 266
lm at the top surface of the papillae. The filiform papillae were different in structure, because as keratinized
processes of the epithelium they did not contain connective tissue cores (Figs. 7–9). The average length of the
filiform papillae was 2.5 mm and their diameter varied
between 65 and 87 lm. The length of these hair-like
structures amounted to 2.1 mm, with a diameter varying
between 102 and 130 lm.
Mucous glands were found in the lamina propria of
the lingual mucosa. Depending on their location, they
could be divided into three types: glands of the body, the
lingual prominence, and the root of the tongue. The
glands of the body and the lingual prominence were
located deeply below the epithelium on both sides of the
entoglossal cartilage, with single secretory units surrounded only by adipose tissue (Fig. 20). The glands of
the root were located directly below the epithelium and,
as opposed to the glands of the body and the lingual
MICROSTRUCTURE OF GOOSE TONGUE
1581
Fig. 23. Cross section of the middle part of the root of the tongue
with opening of the posterior lingual glands (arrow). Ep, parakeratinized epithelium; Lp, lamina propria; Gl, secretory units of mucous
glands. Scale bar–100 lm.
Fig. 22. Higher magnification of the conical papilla of the lingual
prominence. Arrow shows single exfoliated cell. Scale bar-30 lm.
prominence; they were surrounded by collagen fibre bundles of the connective tissue (Fig. 23).
The epithelium at the ventral surface of the apex
formed a ‘‘lingual nail’’ (Figs. 4, 5). The total thickness of
this epithelium was 198 lm, and its horny layer
amounted up to 103 lm.
Lamellar Herbst corpuscles were distributed as characteristic subepithelial structures in the lamina propria
of the mucosa of the apex near the ‘‘lingual nail,’’ in the
front part of lingual prominence and below the conical
papillae of the body. These round mechanoreceptors with
an average diameter of 32 lm appeared as single structures or in groups of 3–4 corpuscles. The largest accumulation composed of five corpuscles was observed at
the anterior part of the lingual prominence (Fig. 16).
DISCUSSION
The tongues of the Anseriformes are important tools
used during several actions, such as collecting solid food,
filtering food from the water or drinking water. In this
context it appears that the most important factors influencing a remarkable variety of lingual structures in
birds are the kind of food taken and/or the type of food
intake (Iwasaki, 2002; Van Der Leeuw et al., 2003; Glatz
et al., 2006). For example, the tongue of the domestic
goose is characterized by a long body with numerous
papillae, which are pointed at the lateral tongue parts
and the triangular lingual prominence. These morpho-
Fig. 24. Higher magnification of the superficial layer of parakeratinized epithelium of the root. Arrow shows noncontinuous layer of less
intense stained cytoplasm of the superficial cells. Scale bar-50 lm.
logical features resemble those of the bean goose belonging to the Anserinae subfamily (Iwasaki, 1997).
However, in the domestic goose, the dorsal surface of the
body and of the lingual prominence showed a median
groove, whereas in the bean goose (Iwasaki, 1997) and
in the white-tailed eagle (Jackowiak and Godynicki,
2005) such structure was only present at the body of the
tongue.
Behavioral observations carried out in the laboratory
environment by Van Der Leeuw et al. (2003) demonstrated that four types of food intake, called grazing,
pecking, drinking, and filter-feeding, are used in the
Anseriformes. This finding also revealed differences in
food transportation between the subfamilies Anatinae
and Anserinae resulting from different diets. The diet of
the Anatinae subfamily comprised a wide spectrum of
1582
JACKOWIAK ET AL.
food, ranging from species feeding on grains and plants
to species that are specialized in feeding on bivalves,
other molluscs and fish. At the same time, species
belonging to the Anserinae, such as the goose and the
swan, feed mainly on the vegetative parts of plants.
Thus, it is assumed that the geese are more adapted to
the terrestrial style of life than to the aquatic one (Kear,
1966; Van Der Leeuw et al., 2003). Due to the fact of living predominantly on land, these birds, unlike ducks,
are considered to be nonspecialist filter feeders (Van Der
Leeuw et al., 2003). Farm-bred, domestic geese are
mostly fed with grass, chickweed, rape, clover, carrottops, dandelions, and chopped vegetables; grains are
supplied as oats, rye, wheat, and maize (Kear, 1966).
Based on the findings of this study, we presume that
the microstructures detected at the particular parts of
the goose tongue are related to specific food intake functions (see e.g., Van Der Leeuw et al., 2003; Glatz et al.,
2006). The intake of solid food in geese occurs in two different ways: grazing and pecking. During grazing the
goose uses the lateral rims of the beak to grab the leaves
of grass, which are then broken off, swallowed, and
transported to the oesophagus. The blades of grass are
hold by pressing the lingual prominence to the palate.
Pecking, the second way of solid food intake, starts
with grabbing the grains by the front part of the beak.
The structures directly linked to the process of grazing
in the domestic goose are the small and large conical
papillae (or mechanical receptors) of the body of the
tongue. They are located at the lateral parts of the
tongue and compatible to the lamellae in the bottom
part of the beak. Based on a thick protective horny layer
and well developed connective tissue cores, the papillae,
together with the beak, may, additionally, help to cut
plants effectively and to prepare the latter for intraoral
transport. In pecking, mostly the apex and the lingual
prominence are involved, which change their location to
enable the transport of grains to the oesophagus.
During the transport of collected grains, the ‘‘lingual
nail’’ plays an important role. As previously reported for
the parrot, chicken, and white-tailed eagle (Homberger
and Brush, 1986; Homberger and Meyer, 1989; Jackowiak and Godynicki, 2005), the epithelium of the ‘‘lingual nail’’ shows a strong or hard keratinization. In the
domestic goose, the ‘‘lingual nail’’ has a unique shape,
because it ensheathes the apex of the tongue and pierces
the apex edges. The anterior part of the tongue does not
contain the entoglossal cartilage, so the well keratinized
‘‘lingual nail’’ can be emphasized as an important element of the external frame of the apex. According to
Homberger and Brush (1986), this hard and resistible
structure has is flexible enough that it can be stretched,
and in the domestic goose, as in other birds, may function as a spoon for lifting grains.
Furthermore, other important methods of food intake
in geese are drinking and filter-feeding. According to
Van Der Leeuw et al. (2003), the mechanism of drinking
is based on the immersion of an open beak, when water
fills the frontal part of the beak cavity. Then the beak is
closed and the water flows along the surface of the
tongue. During filter-feeding, the movement of the lingual prominence causes that the water is expelled from
the oral cavity, whereas small parts of food are hold
inside. The mucosal structures of the tongue of the
domestic goose taking part in food filtration are the fili-
form papillae. They fill the spaces between the conical
papillae, where the food is trapped. Our histological examination revealed that these papillae are keratinized
processes of the epithelium without a subepithelial connective tissue core that can undergo renewal in cases of
destruction. Van Der Leeuw et al. (2003) found that filter-feeding in the goose is less effective than in the
duck. In our opinion this results from a species–specific
distribution of the filiform papillae. In the duck, these
long and fine structures completely cover the short conical papillae like a dense bristle, whereas in the domestic
goose the filiform papillae are much shorter and on the
same level of height or length as conical papillae. Such
arrangement of the filiform papillae in geese probably
indicates an adaptation to terrestrial conditions, as compared to ducks.
Food transportation on the dorsal surface of the
tongue is performed by coordinated movements of the
tongue and the beak (Van Der Leeuw et al., 2003). The
elevation and/or pressing down of the apex and the lingual prominence have an influence on the mucosal structure, especially on the epithelium of the tongue. This
epithelium generally covering the tongue in vertebrates,
is multilayered and partially keratinized (Iwasaki,
2002). It is an adaptation to terrestrial life and also connected with protective functions. Our study of such epithelium in the domestic goose revealed three types:
parakeratinized at the apex and the body, orthokeratinized at the mechanical papillae, and nonkeratinized at
the root of the tongue. Such classification is adapted
from previous research on the process of keratinization
in mammals (Alibardi, 2009). In birds, it is difficult to
determine such types of epithelia precisely, particularly
because of the fact that numerous intermediate forms
can be observed (Alibardi, 2006, 2009). In this context it
is of interest that, according to our findings, cell nuclei
remain in the horny layer, thus indicating that the keratinization mechanism in birds may be somewhat different from that one in mammals. In the latter group, the
keratinization process is characterized by the presence
of keratohyalin granules in the spinous layer, followed
by the production of the horny layer. Regarding birds,
such granules have not been demonstrated in the epidermis or during feather production (Alibardi, 2004). Summarizing all aspects, it appears that the mechanism of
epithelial keratinization in the oral cavity of birds has
still to be clarified.
Morphometric analysis of the parakeratinized epithelium of the goose tongue confirmed that parts of the latter, for example the apex, have developed a very thick
epithelium by actively contacting food, which to a certain extent may compensate for the lack of the horny
layer. Our observations also showed a reduction in thickness of the parakeratinized epithelium of more than 50%
at the lingual prominence and 70% at the body, which
may be related to the fact that these parts of the tongue
are less involved in collecting food. The thin nonkeratinized epithelium at the root of the goose tongue seems
to be an exception within birds. The lack of a horny
layer obviously results from a weak contact with food,
because during swallowing the lingual prominence is
depressed and its conical papillae overlap the root of the
tongue.
The elevation and pressing of the lingual prominence
up to the palate region during grazing and filter-feeding,
MICROSTRUCTURE OF GOOSE TONGUE
causes pressure on the surface of the prominence, that
is received by the mass of the yellow adipose tissue. As
we learned from our study, adipose tissue also surrounds
the lingual glands, and thus, movements of the tongue
may bring about mechanic stimuli, causing mucus
release from the glandular secretory units and ducts.
The distribution of such glands and their openings so far
studied in birds revealed that the anterior lingual glands
have their openings at both sides of the tongue and posterior lingual glands at the surface of the root (Iwasaki
and Kobayashi, 1986; Kobayashi et al., 1998; Liman
et al., 2001; Jackowiak and Godynicki, 2005; Rossi et al.,
2005). Our observations in the domestic goose corroborate the findings of most of the latter authors. However,
it should be noted that the number of glandular openings was much higher in the goose than in other bird
groups. The mucus secreted covers the whole beak sulcus and the tongue surface, which decreases friction during food collection and moistens the beak cavity during
food transport.
For birds and mammals, three types of sensory receptors
have been described as present in the skin and lingual mucosa of the mouth cavity and the beak: Grandry corpuscles,
Merkel corpuscles, and Herbst corpuscles. Merkel and
Herbst corpuscles are characteristic of water birds and nonwater birds (Toyoshima et al., 1992; Halata and Grim,
1993; Toyoshima et al., 1993; del Valle et al., 1995); Grandry
corpuscles are only found in water birds (Gottschaldt and
Lausmann, 1974; Leitner and Roumy, 1974; Toyoshima,
1993; Kumamoto et al., 1995; Halata et al., 2003). Our findings include the observation of subepithelial lamellar
mechanoreceptors (Herbst corpuscles), which react during
a mechanical deformation of the mucosa when the food is
connecting with the tongue. The distribution pattern of
mechanoreceptors is important for the choice of food, the
identification of the food position on the tongue, and the
execution of correct movements of the latter, which promotes effective food transport into the oesophagus. Previous studies on touch sensitivity within the beak of the goose
revealed a high concentration of Grandry and Herbst corpuscles in the anterior parts of the beak skin and the mucosa of the beak cavity, where they form the ‘‘bill tip organ’’
(Gottschaldt and Lausmann, 1974; Gentle and Breward,
1986). Our findings emphasize that accumulations of
Herbst corpuscles are present in the mucosa near the ‘‘lingual nail,’’ in front of the lingual prominence, and less sensory corpuscles in the lamina propria below the conical
papillae of the body. In this way, during feeding in the
domestic goose, mechanical stimuli about food positioning
could be received at the front part of the beak cavity, as well
as the apex and the area in front of the lingual prominence
of the tongue. So the tongue can be regarded as an important element of the ‘‘bill-tongue organ.’’
In conclusion, our study demonstrated that the tongue of
the domestic goose is a highly specialized organ in cutting
the vegetative parts of plants as well as in taking solid food
in the form of seeds, which may be closely related to their
terrestrial style of life. Nevertheless, the tongue of geese is
still adapted to food filtration to a certain extent.
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