Estudio morfologico de la lengua de budgericar melopsittacus undulatus.
KEY WORDS: I. Lengua; 2. Epitelio; 3. Tejido conectivo: 4. Ave; 5. SEM.
Morphological study of the tongue of budgerigar (Melopsittacus undulatus)
SUMMARY: The tongue of the budgerigar was analyzed macroscopically and by scanning electron microscopy with conventional and NaoH maceration techniques. Macroscopic analysis showed a median sulcus along the medium to the posterior regions. Transverse sulcus were also observed. The dorsum of the tongue showed a relatively smooth surface lined by keratinized stratified squamous epithelium. Lingual papillae were not detect on the anterior and medium regions, only at the root of the tongue. These structures were curved and inclined posteriorly. Near to the larynges aditus numerous projections like lingual papillae were noted. The anterior and medium regions showed connective tissue protrusions with longitudinal and transversal arrangement. The surface of the protrusions presented connective tissue papillae with finger-like shape.
KEY WORDS: 1. Tongue; 2. Epithelium; 3. Connective Tissue; 4. Bird; 5. SEM.
The budgerigar are small birds with medium size of 17 cm belonging to the Psitaciforms Order which probably originated from Australia. The exotic specie are disseminated in captivity and represents high commercial value like pet animal. The original colors of these birds are green and blue; the first mutation that occurred in 17 century provided the yellow one and nowadays there are about 200 different colors.
The dorsum of the tongue of mammals presented a specialized mucous membrane with lingual papillae related to specific function of gustation. The anatomy, histology and ultrastructural details of these structures change according to the analyzed species as observed by Iwasaki & Miyata (1989); Kobayashi et al. (1989, 1998); Kobayashi (1992); Agungpriyono et al. (1995); Watanabe et al. (1992, 1997); Kumar et al. (1998) and Martinez et al. (1998, 2000). Iwasaki & Kumakura (1994) and Herrel et al. (1998) described the tongue of reptile and amphibians, respectively. On the other hand, few papers of the tongue of birds are available in the literature (Iwasaki, 1992, Iwasaki et al. 1997, Kobayashi et al. 1998).
Several methods of epithelium removal on various tissue types employing scanning electron microscope were developed in the last years (Klein-Szanto & Schroeder, 1977: Low & Mcclugage, 1984; Hull & Warfel, 1986; Kobayashi). One of these techniques is the NaOH maceration introduced by Ohtani (1992).
The objective of the present paper was to described the morphological features of the tongue of budgerigar, comparing it to other species of birds described in the literature.
MATERIAL AND METHOD
Six male adult budgerigar (Melopsittacus undulatus) were used in the present paper. After the birds sacrificed by ether inhalation, the tongues were washed with distilled water and dissected. For observations on the dorsum of the tongue it was used the conventional SEM method. For studies of the lamina propria, three tongues were fixed with modified Karnovsky solution, containing 2.5% glutaraldehyde, 2.0% paraformaldehyde in 0.1 M phosphate buffer, pH 7.2. The specimens were rinsed and immersed in a 10% aqueous solution of NaOH, for 3-6, at room temperature, according to the method of Ohtani. The samples were rinsed in distilled water and post-fixed with 1% osmium tetroxide solution, for 2 hrs. After immersion in a 1.0% aqueous solution of tannic acid for 1 hr and 30 minutes, they were rinsed again in distilled water for several hours and dehydrated in an increasing series of ethanol. The samples were dried in a critical point using C[O.sub.2] liquid (Balzers CPD-010), coated with gold ions in a SEM coating (Balzers MED-010) and examined under a Philips FEM-515 scanning electron microscope at 20 kV.
Macroscopic findings: The small tongue of budgerigar presented elongated shape with round tip and 0,7 mm of length. The width of the anterior region was 0,3 mm changing to the posterior region to 0,5 mm. Macroscopic analysis showed a median sulcus along the medium to the posterior regions. Transverse sulcus were also observed. Lingual papillae were not detect macroscopically on the dorsum of the tongue. The larynges aditus open close to the end of the posterior region of the tongue.
Scanning electron microscopy: The images of the dorsum of the tongue showed a relatively smooth surface lined by keratinized stratified squamous epithelium. However, at higher magnification several sulcus were seen in the anterior and medium regions. The anterior sulcus were disposed in the longitudinal axis while in the medium region the sulcus were transversal in the tongue.
The polygonal epithelial cells presented well-developed microridges widely distributed and clear cellular limit. Many desquamating cells were seen. Lingual papillae were not find in the anterior and medium regions. The posterior region presented numerous conical papillae. These structures were curved and inclined posteriorly. Desquamating polygonal cells were also observed in the conical papillae.
Near to the larynges aditus numerous projections like lingual papillae were note& This area were also lined with stratified epithelium.
After epithelial layer were removed with maceration method, the architecture of the lamina propria of the tongue was exposed. The anterior and medium regions showed several connective tissue protrusions with longitudinal and transversal arrangements according to the epithelial sulcus. The surface of the protrusions presented connective tissue papillae with finger-like shape. Around the larynges aditus were also observed small connective papillae. At higher magnification were showed that the collagen fibers presented an intrincated disposition composing a meshwork.
[FIGURE 1 OMITTED]
The tongue of birds presents numerous variability in form and size which may be related to feeding habits. The literature described different types of adaptation of the bird's tongue like for collecting food, for manipulating food and for swallowing. The characteristic of the tongue adapted to collect food is the developed hyobranchial apparatus, which permit large protrusions of the organ, while the tongue adapted to manipulate food is non-protrude organ with numerous sharp caudally-direct papillae. On the other hand, the tongue related to swallowing appears in many species with major capacity of procuring or cathing food. This organ presented papillae distributed at the root of the tongue (Harrison, 1964).
The budgerigar presented the tongue lined with keratinized stratified squamous epithelium similar to others birds and mammals. The superficial polygonal epithelial cells showed clear borders and several microridges. The same characteristics were described by (Watanabe et al. 1992: Agungpriyono el al. and Kobayashi el al. 1998). Andrews (1976) suggested that the microridges must protect the superficial cells keeping more quantity of mucous between adjacent cells.
Papillae were observed in the posterior region, at the root of the tongue of budgerigar. This characteristic may classified this bird in the third type of the classification of Harrison. Iwasaki et al. (1997) described the keratinization of the dorsal epitlielium of the tongue of Middendorff's bean goose. This bird did not present lingual papillae in the anterior and posterior regions. Giant conical papillae were located in a transverse row between these regions. Kobayashi et al. (1998) studied the fine structure of the tongue of penguin which presented the dorsal surface densely distributed with large spine-like lingual papillae. The chicken (Iwasaki & Kobayashi, 1986) and little tern (Iwasaki) presented papillae on the anterior region of the tongue. As we can see, the distribution of papillae ate related with the specie and their habit food.
[FIGURES 2-13 OMITTED]
The direct observation at scanning electron microscope permits to clarify the three-dimensional structure of the lamina propria. Several methods of maceration have been developed in the last years. Klein-Szanto & Schroeder used EDTA and Low & Mcclugage used boric acid. Kobayashi & Wanichacon (1992) employed HC1 treatment method at room temperature, exposing the true surface of the connective tissue papillae of the tongues. Otherwise, Ohtani introduced a cell-maceration method with NaOH aqueous solution. According to Ohtani, this treatment eliminates the cellular elements more effectively than any other method so far described. Our results showed the original architecture and disposition of the connective tissue papillae using the NaOH cell maceration.
Kobayashi et al. (1998) examined the structure of the tongue of penguin, which showed connective tissue core with similar morphology of the external papillae. The connective papillae revealed fine parallel striations running along the long axis of the papillae. The filiform-like papillae of the chick presented similar characteristics. The connective papillae distributed on the posterior region of the tongue of budgerigar were also similar in shape with the external papillae. In contrast, mammals connective tissue papillae usual demonstrated different morphology from the external shape. In conclusion, the morphology of the dorsum of the tongue of budgerigar seem to be related to the intrinsic aspects of the feeding habits of the species and the animal order also must be considered.
Received : 1712-2001
Agungpriyono, S.; Yamada, J.; Kitamura, N. Morphology of the dorsal lingual papillae in the lesser mouse deer, Tragulus javanicus. J. Anat., 187:635-40, 1995.
Andrews, P. M. Microplicae: characteristic ridge like folds plasmalema. J. Cell. Bio., 68:420-9, 1976.
Harrison, J. G. Tongue. In: (ed. By) A. L. Thomson: A new dictionary of birds. Nelson, London, 1964.
Herrel, A.; Timmermans, Jean-Pierre; De Vree, E Tongue flicking in agamid lizards: Morphology, kinematics, and muscle activity patterns. Anat. Rec., 252:102-16, 1998.
Hull, M. T. & Warfel, K.A. Basal lamina at the epithelial-connective tissue junction in the rat forestomach, esophagus, tongue and palate. Scanning electron microscopic study. Scanning Electron micros., 1:1395401, 1986.
Iwasaki, S. & Kobayashi, K. Scanning and transmission electron microscopical studies on the lingual dorsal epithelium of chickens. Acta Anat. Nippon., 61:83-96, 1986.
Iwasaki, S. & Miyata, K. Fine structure of the filiform papilla of beagle dogs. J. Morphol., 201:235-49, 1989.
Iwasaki, S. Fine structure of the dorsal lingual epithelium of the little tern, Stena albifrons Palias (Avis, Lari). J. Morphol., 212:13-26, 1992.
Iwasaki, S. & Kumakura, M. An ultrastructural study of the dorsal lingual epithelium of the rat snake, Elaphe quadrivirgata. Ann. Anat., 176:455-62, 1994.
Iwasaki, S.; Tomoichiro, A. & Akira. C. Ultrastructural study of the keratinization of the dorsal epithelium of the tongue of Middendorff's Bean Goose, Anser fabalis middendorffii (Anseres, Antidae). Anat. Rec., 247: 149-63, 1997.
Klein-Szanto, A. J. P. & Schroeder, H. E. Architecture and density of the connective tissue papillae of the human oral mucosa. J. Anat., 123:93-109, 1977.
Kobayashi, K. Stereo architecture of the interface of the epithelial cell layer and connective tissue core of the folliate papilla in the rabbit tongue. Acta Anat., 143: 109-17, 1992.
Kobayashi, K.; Miyata, K. & Asami, T. Three-dimensional structure of the connective tissue core of the lingual papillae in the crab-eating macaque. Shigaku., 77:130-817, 1989.
Kobayashi, K. &Wanichacon, C. Stereo architecture of the connective tissue cores of the lingual papillae in the treeshrew (Tttpaia glis). Anat Embriol., 186:511-8, 1992.
Kobayashi, K.: Kumakura, M.: Yoshimura, K.: Inatomi, M. & Asami, T. Fine structure of the tongue and lingual papillae of the penguin. Arch. Hist. Cytol., 61:37-46, 1998.
Kumar, P.; Kumar. S. & Singh, Y. Tongue papillae in goat: a scanning electron-microscopic study. Anat. Histol. Embryol., 27:355-7, 1998.
Low, F. N. & Mclugage, S.G. Microdissection by ultrasonication: Scanning electron microscopy study of the epithelial basal lamina of the alimentary canal in the rat. Amet: J. Anat., 169:137-47, 1984.
Martinez, M.: Martinez, F. E.; Pinheiro, P. F. F: Almeida, C. C. D: Guida, H. L. & Watanabe, I. Scanning electron microscopic study of the vallate papillae of the opossum (Didelphis albiventris). Rev: Chil. Anat., 16:67-73,1998.
Martinez, M.; Martinez, F. E.; Pinheiro, P.F. F.; Almeida, C. C. D.; Segatelli, T. M. & Watanabe, I. Scanning electron microscopio study of the tongue of chinchila (Chinchila laniger). Rev: Chil. Anat., 18(1):53-59, 2000.
Ohtani, O. The maceration technique in scanning electron microscopy ofcollagen fiber frameworks. It's application in the study of human livers. Arch. Histol. cytol., 55:225-32, 1992.
Watanabe, I; Morais, J. O. R; Yokoyama, R; Inokuchi, T. & Hamasaki, M. Three-dimensional structure of the subepithelial connective tissue papillae of the armadillo (Dasypus novemcinctus) tongue. Rey. Ch il. Anat., 10:97-103, 1992.
Watanabe, I.; Ogawa, K.; Cavalcanti, F. L. & Lopes, R. A. Scanning electron microscopio study of the Von Ebner's glands of the Cebbus apella tongue. Bras. J. Morphol. Sci., 14:275-79, 1997.
Dr. Marcelo Martinez
Departamento de Morfologia e Patologia
Universidade Federal de Sao Carlos
Rod. Washington Luis Km 235 s/no
Sao Carlos / Sao Paulo
* Martinez, M.; * Stefanini, M. A.; ** Martinez. F. E.; *** Guida, H. L.; * Pinheiro, P. F. F.; ** Almeida, C. C. D.; ** Segatelli, T. M.
* Department of Morphology and Pathology, Federal University of Sao Carlos (UFSCar), Sao Carlos/SP, Brazil.
** Department of Anatomy, Institute of Biosciences, State University of Silo Paulo (UNESP), Rubiao Junior, Botucatu/SP, Brazil.
*** Department of Phonoaudiology, State University of Sao Paulo (UNESP), Marilia/SR Brazil.