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International Journal of Morphology

versión On-line ISSN 0717-9502

Int. J. Morphol. v.21 n.2 Temuco  2003

http://dx.doi.org/10.4067/S0717-95022003000200004 

Int. J. Morphol., 21(2):117-122 2003.

MORPHOLOGICAL STUDY OF THE TONGUE OF BUDGERIGAR
(Melopsittacus undulatus)

ESTUDIO MORFOLÓGICO DE LA LENGUA DE BUDGERICAR Melopsittacus undulatus

*Martinez, M.; *Stefanini, M. A.; **Martinez. F. E.; ***Guida, H. L.;
**Pinheiro, P. F. F.; **Almeida, C. C. D.; **Segatelli, T. M. 

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. 


INTRODUCTION

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 CO2 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.

RESULTS

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.


Fig. 1 Macroscopic view of the tongue (*) and pharyngeal region (white *) of budgerigar. Note transverse and longitudinal sulcus on the dorsum of the tongue. X 4.5.

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.


Fig. 2. Scanning electron micrograph of the dorsum of the tongue of budgerigar. Shows longitudinal sulcus on the anterior area (*). X 90.
Fig. 3. SEM image of the medium area with distinct transverse sulcus (arrow) and desquamating cell (double arrow). X 95.
Fig. 4. SEM image of the posterior region of the tongue with conical papillae (arrow) and aditus larynges area (*) with papillae (arrow head). X 30.
Fig. 5. High magnification of the papillae of the posterior region of the tongue (*). Note that these structures were curved and inclined posteriorly. X 195.
Fig. 6. High magnification of the epithelial surface of the tongue. The polygonal epithelial cells presented distinct borders (arrows) and microridges (*). X 1570.
Fig. 7. SEM image from the pharyngeal region with papillae lined with stratified squamous epithelium (star). X 95.
Fig. 8. High magnification on the polygonal cells from the pharyngeal region of budgerigar. X 650.

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 noted. 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.


Fig. 9. NaOH treated tongue of budgerigar. Note the anterior (*) and medium (**) regions with several protru-sions on the lamina propria. X 20
Fig. 10. SEM image showing longitudinal and transversal arrangements (arrow head) of the lamina propria protru-sions. X 50.
Fig. 11. High magnification of the anterior region of the tongue. Shows connective papillae with finger-like shape from the longitudinal protrusions. X 195.
Fig. 12. SEM image from aditus larynges area (star). Note small papillae surro-unding the opening (arrow). X 45.
Fig. 13. High magnification showing the collagen meshwork on the lamina propria of the tongue. X 650.

DISCUSSION

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 et al. and Kobayashi et 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 epithelium 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 are related with the specie and their habit food.

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 HCl 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. 


SUMMARY: La lengua del budgericar fue analizada macroscópicamente y a través de miccroscopía electrónica de barrido con técnicas de maceración de NaOH. El análisis macroscópico mostró un surco mediano a lo largo de las regiones media y posterior. Surcos transversos también fueron observados. El dorso de la lengua mostró una superficie relativamente suave cubierta por epitelio queratinizado, escamoso, estratificado. No fueron detectadas papilas linguales en las regiones anterior y media, siendo solamente observadas en la raíz de la lengua. Estas estructuras se mostraron inclinadas posteriormente. Cerca del ádito de la laringe fueron observadas numerosas proyecciones de papilas linguales. Las regiones anterior y media mostraron protrusiones de tejido conectivo con disposiciones longitudinal y transversal. La superficie de las protrusiones presentaron papilas de tejido conectivo con forma de dedo.

KEY WORDS: 1. Lengua; 2. Epitelio; 3. Tejido conectivo; 4. Ave; 5. SEM. 


REFERENCES

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Correspondence to:
Dr. Marcelo Martinez
Departamento de Morfologia e Patologia
Universidade Federal de São Carlos
Rod. Washington Luís Km 235 s/n°
CEP: 13.565.905
São Carlos / São Paulo
BRASIL

Phone 55-16-2608330
Fax 55-16- 2608326

Email: martinez@power.ufscar.br

Received : 17-12-2001
Accepted: 05-02-2003 


* Department of Morphology and Pathology, Federal University of São Carlos (UFSCar), São Carlos/SP, Brazil.
** Department of Anatomy, Institute of Biosciences, State University of São Paulo (UNESP), Rubião Júnior, Botucatu/SP, Brazil.
*** Department of Phonoaudiology, State University of São Paulo (UNESP), Marília/SP, Brazil.

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