Functional Morphology of the Tongue in the Domestic Goose (Anser Anser f. Domestica)код для вставкиСкачать
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: firstname.lastname@example.org 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 1578 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. LITERATURE CITED Alibardi L. 2004. Immunocytochemical and autoradiographic studies on the process of keratinization in avian epidermis suggests absence of keratohyalin. J Morphol 259:238–253. 1583 Alibardi L. 2006. 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