Histological Structure of the Tongue in Birds at Light and Scanning Electron Microscopic Level: A Review Study
Subject Areas : Journal of Animal Biology
Ali Parchami
1
(Department of Basic Sciences, Faculty of Veterinary Medicine, Shahrekord University, Shahrekord, Iran )
Keywords: Tongue, Birds, Light microscopy, Electron microscopy, Salivary glands,
Abstract :
The tongue in birds has many fundamental similarities with this organ in mammals and has three parts: tip, body, and root. Significant differences in the morphology of the tongue in birds may be caused by differences in the anatomical structure of the lower beak, type of diet, nutritional habits, lifestyle, environmental conditions, etc. The tongue and especially the tip of the organ can be seen in different forms in birds. In some species of birds, the median groove is found on the dorsal surface of the tongue. The papillary crest on the dorsal surface of the body consists of cone-like papillae, which show significant differences in different species from the point of view of distribution, number, appearance, manner of placement, and degree of evolution. The epithelium of the dorsal surface of the tongue in some birds shows differences in specific areas of the organ based on nutritional patterns, type of food, and animal's environment. In birds, taste buds are mainly found at the base of the tongue and on the floor or roof of the mouth. Salivary glands show obvious species differences and are generally much more developed in grain-eating birds. In prey birds, they have little development and in some birds, they are absent. Lingual salivary glands are found in alveolar, tubulo-alveolar, and tubular types and are of serous and seromucous type. In many birds, the lingual salivary glands are located in two anterior and posterior groups without any anatomical continuity, in some birds, the parin layer in the mucous membrane of the organ is filled with mucous glands whose pores open on the dorsal and ventral surfaces of the tongue. The way of distribution and the anatomical position of these glands in the connective tissue of the tongue show differences in different species of birds.
1. Abou-Zaid D.F.A. 2008. Comparative anatomical study on the dorsal surface structure of the tongue of two birds with different feeding habits. Egyptian Journal of Experimental Biology, 4:65-72.
2. Al-Taai S.A.H., Khalaf A.S. 2022. Histomorphological study of the tongue in adult starling birds (Sturnus valguris). Iranian Journal of Ichthyology, 9: 116-122.
3. Başak F., Atalgin Ş.H., Bozkurt E.Ü. 2017. Tongue and lingual salivary glands of the canary: scanning electron microscopy and histochemical study. Folia Morphologica, 76(3):348-354.
4. Beason R.C. 2003. Through a Bird's Eye - Exploring Avian Sensory Perception. Bird Strike Committee USA/Canada, 5th Joint Annual Meeting, Toronto, Internet Center for Wildlife Damage Management.
5. Bock W.J. 1999. Plenary03: Functional and evolutionary morphology of woodpeckers. Proc. 22 International Ornithology Congess, Durban: Ostrich, 70(1)23-31.
6. Crole M.R., Soley J.T. 2009. Morphology of the tongue of the emu (Dromaius novaehollandiae). I. Gross anatomical features and topography. Onderstepoort Journal of Veterinary Research, 76:335-345.
7. Crole M.R., Soley J.T. 2009. Morphology of the tongue of the emu (Dromaius novaehollandiae). II. histological features. Onderstepoort Journal of Veterinary Research, 76:347-361.
8. Crole M. R., Soley J. T. 2010. Surface morphology of the tongue of the emu (Dromaius novaehollandiae) Tongue. Anatomia Histologia Embryologia, 39:355-365.
9. del Hoyo J., Elliott A., Sargatal J. 2011. Handbook of the Birds of the World (Vol. 1-16). Barcelona: Lynx Edictions.
10. El-Bakary N.E. 2011. Surface Morphology of the Tongue of the Hoopoe (Upupa Epops). Journal of American Science: 7.
11. Elsheikh E.H., Al-Zahaby S.H.A. 2014. Light and scanning electron microscopic study of the tongue in the hooded crow (Aves: Corvus corone cornix). The Journal of Basic and Applied Zoology, 67:83-90.
12. Emura S. 2008. SEM studies on the lingual papillae and their connective tissue cores of the black kite (Milvus migrans) (in Japanese). Medicine and Biology, 152:43-47.
13. Emura S., Chen H. 2008. Scanning electron microscopic study of the tongue in the owl (Strix uralensis). Anatomia Histologia Embryologia, 37:475-478.
14. Emura S., Okumura T., Chen H. 2010. Comparative studies of the dorsal surface of the tongue in three avian species by scanning electron microscopy. Okajimas Folia Anatomica Japonica, 86(4):111-115.
15. Emura S., Okumura T., Chen H. 2009. Scanning electron microscopic study of the tongue in the Japanese Pygmi Woodpecker (Dendrocoposkizuki). Okajimas Folia Anatomica Japonica, 86:31-35.
16. Emura S., Okumura T., Chen H. 2008. Scanning electron microscopic study of the tongue in the peregrine falcon and common kestrel. Okajimas Folia Anatomica Japonica, 85:11-15.
17. Erdogan S., Alan A. 2012. Gross anatomical and scanning electron microscopic studies of the oropharyngeal cavity in the European magpie (Pica pica) and the common raven (Corvus corax). Microscopy Research Technique, 75:379-387.
18. Erdoğan S., Iwasaki S. 2014. Function-related morphological characteristic and specialized structures of the avian tongue. Annals of Anatomy, 196:75-87.
19. Erdogan S., Pérez W., Alan A. 2012. Anatomical and scanning electron microscopic investigations of the tongue and laryngeal entrance in the longlegged buzzard (Buteorufinus, Cretzschmar). Microscopy Resesarch and Technique, 75:1245-1252.
20. Erdoğan S., Sağsöz H., Akbalik M.E. 2012. Anatomical and histologi¬cal structure of the tongue and histochemical characteris¬tics of the lingual salivary glands in the Chukar partridge (Alectoris chukar). British Poultry Science, 53(3):307-315.
21. Ertas T.D., Erdogan S. 2019. Investigation of abou (Gallus domesticus) tongue by morphometric and scanning electron microscopic methods. Dicle Universitesi Veteriner Fakultesi Dergisi, 12:8-12.
22. Farouk S.M., Hassan S.A. 2015. Histochemical and ultrastructural characteristics of tongue of laughing dove (Stigmatopelia senegalensis). Journal of Cytology and Histology, 6:363-368.
23. Fatahian Dehkordi R. A., Parchami A., Bahadora, S. 2010. Light and scanning electron microscopic study of the tongue in the zebra finch (Carduelis carduelis) (Aves: Passeriformes: Fringillidae). Slovenian Veterinary Research, 47:139-144.
24. Gentle M.J. 1971. The lingual taste buds of Gallus domesticus. British Poultry Science, 12(2):245-248.
25. Gill F.B. 1994. Ornithology. 2nd edition. New York: W.H. Freeman and Company.
26. Grant V., Temeles E. J. 1992. Foraging ability of rufous humming birds on humming bird flowers and hawkmoth flowers. Proceedings of the National Academy of Sciences, USA, 89:9400-9404.
27. Hassan S.M., Moussa E.A., Cartwright A.L. 2010. Variations by Sex in Anatomical and Morphological Features of the Tongue of Egyptian Goose (Alopochen aegyptiacus). Cells Tissues Organs, 191:161-165.
28. Homberger D.C., Brush A.H. 1986. Functional morphological and biochemical correlations of the keratinized structures in the African grey parrot (Psittacus erithacus). Zoomorphology, 106:103-114.
29. Homberger D.G., Meyers R.A. 1989. Morphology of the Lingual Apparatus of the Domestic Chicken Gallus gallus, With Special Attention to the Structure of the Fasciae. The American Journal of Anatomy, 186:217-257.
30. Huang R., Zhi Q., Izpisua-Belmonte J., Christ B., Patel K. 1999. Origin and development of the avian tongue muscles. Anatomy and Embryology, 200:137-152.
31. Igwebuike U.M., Eze U.U. 2010. Anatomy of the oropharynx and tongue of the African Pied crow (Corvus albus). Veterinarski Arhiv, 80:523-531.
32. İlgün R., Kuru N., Bölükbaş F., Gür F. M. 2020. Histological and Electron Microscopical Structure of Tongue and Lingual Papillae of Guinea Fowl (Numida meleagris) Pakistan Journal of Zoology, 52(3):949-956.
33. Iwasaki S. 2002. Evolution of the Structure and Function of the Vertebrate Tongue. Journal of Anatomy, 201:1–13.
34. Iwasaki S. 1992. Fine structure of the dorsal lingual epithelium of the little tern, Sterna albifrons Pallas (Aves, Lari). Journal of Morphology, 212(2):13-26.
35. Iwasaki S., Asami T., Chiba A. 1997. Ultrastructural study of the keratinization of the dorsal epithelium of the tongue of Middendorff’s bean goose, Anser fabalis middendorffii (Anseres, Antidae). The Anatomical Record, 247(2):149–163.
36. Iwasaki S., Kobayashi K. 1986. Scanning and transmission electron microscopical studies on the lingual dorsal epithelium of chickens. Acta Anatomica Nipponica, 61:83–96.
37. Jackowiak H., Andrzejewski W., Godynicki S. 2006. Light and scanning electron microscopic study of the tongue in the cormorant Phalacrocorax carbo (Phalacrocoracidae, aves). Zoological Science, 23:161-167.
38. Jackowiak H., Godynicki S. 2005. Light and scanning electron microscopic study of the tongue in the white tailed eagle (Haliaeetus albicilla, Accipitridae, Aves). Annals of Anatomy, 187:251-259.
39. Jackowiak H., Ludwig M. 2008. Light and scanning electron microscopic study of the ostrich (Strutio camelus) tongue. Zoological Science, 25:188-194.
40. Jackowiak H., Shieresz-Szewczyk K. 2011. Functional Morphology of the Tongue in the Domestic Goose (Anser Anser f. Domestica). The Anatomical Record, 294:1574-1584.
41. Jackowiak H., Skieresz-Szewczyk K., Kwiecinski Z., Trzielinska-Lorych J., Godynicki S. 2010. Functional Morphology of the Tongue in the Nutcracker (Nucifraga caryocatactes). Zoological Science, 27(7):589-594.
42. Kadhim K.K., AL-Timmemi H., Thamir A.A. 2013. Histomorphological and histochemical observations of the Common Myna (Acridotheres tristis) tongue. International Scholarly Research Notices, 2013:1-4.
43. Karadağ H., Nur İ. H. 2002. Systema digestorium. In: Anatomy of domestic birds (ed. N. Dursun). Medisan publication, Ankara, 55-56.
44. Kobayashi K., Kumakura M., Yoshimura K. 1998. Fine structure of the tongue and lingual papillae of the penguin. Archives of Histology and Cytology, 61:37-46.
45. Komarek V., Malinovesky L., Lemez L. 1986. Anatomia avium domesticarum embryologia galli. Priroda vedavatel’stvo knih a casoposov, Bratyslava.
46. Kullaa-Mikkonen A., Sorvari T. E. 1985. A scanning electron microscopic study of the dorsal surface of the human tongue. Acta Anatomica, 123:114-120.
47. Landsborough, S.A. 1964. A New Dictionary of Birds. New York: McGraw-Hill Book Company.
48. Lucas F.A. 1896. The Taxonomic Value of the Tongue in Birds. The Auk, Vol 13, No 2, 1896. The Tongues of Birds. U.S. National Museum for 1895, 1895:1001-1019.
49. Madkour F.A. 2018. Characteristic features of the pharyngeal cavity of the laughing dove (Strep-topelia senegalensis aegyptiaca) and Japanese quail (Coturnix coturnix). Assiut Veterinary Medical Journal, 64:52–59.
50. Marshall A.J. 1960. Biology and Comparative Physiology of Birds. New York and London: Academic Press.
51. Matsuo R. 2000. Role of saliva in the maintenance of taste sensitiv¬ity. Critical Reviews in Oral Biology and Medicine, 11(2):216–229.
52. McLelland J. 1990. A Color Atlas of Avian Anatomy. Wolfe Publishing Ltd.
53. McLelland J. 1979. Systema digestorium. In: Baumel, J. J., King, A. S., Lucas, A. M., Breazile, J. E., Evans, H. E. (Eds.), Nomina anatomica avium. Academic Press, New York, pp. 307-309.
54. Nickel R., Schummer A., Seiferle E. 1977. Anatomy of the domestic birds, Verlag Paul Parey, Berlin, 45-46.
55. Olsen P., Joseph L. 2011. Stray Feathers: Reflections on the Structure, Behavior and Evolution of Birds. Collingwood VIC 3066: CSIRO Publishing.
56. Onuk B., Tütüncü S., Kabak M., Alan A. 2015. Macroanatomic, light microscopic, and scanning electron microscopic studies of the tongue in the Seagull (Larus fuscus) and common buzzard (Buteo buteo). Acta Zoologica, 96:60-66.
57. Parchami A., Dehkordi R.F. 2011. Lingual structure in the domestic pigeon (Columba livia domestica): A light and scanning electron microscopic study. World Applied Science Journal, 12:1517-1522.
58. Parchami A., Fatahian Dehkordi R. F., Bahadoran S. 2010. Scanning electron microscopy of the tongue in the golden eagle Aquila chrysaetos (Aves: Falconiformes). World Journal of Zoology, 5:257-263.
59. Parchami A., Fatahian Dehkordi R.F., Bahadoran S. 2010. Fine Structure of the Dorsal Lingual Epithelium of the Common Quail (Coturnix coturnix). World Applied Sciences Journal, 10:1185-1189.
60. Parchami A., Fatahian Dehkordi R.A. 2013. Light and electron microscopic study of the tongue in the White-eared bulbul (Pycnonotus leucotis). Iranian Journal of Veterinary Research, 2013(14):9-14.
61. Parchami A., Salimi M. 2017. Light and scanning electron microscopic study of the lingual structure in the budgerigar (Melopsittacus undulatus). Iranian Journal of Veterinary Medicine, 11(1):97-104.
62. Portman A. 1961. Sensory Organs: Skin, Taste and Olfaction. In Biology and Comparative Physiology of Birds, Vol. II, by A.J. Marshall. New York and London: Academic Press, 37-48.
63. Pourlis A.F. 2014. Morphological features of the tongue in the quail (Coturnix coturnix japonica). Journal of Morphology, 31:177-181.
64. Proctor N.S., Lynch P.J. 1993. Manual of Ornithology. New Haven and London: Yale University Press.
65. Rico-Guevara A., Rubega M.A. 2011. The hummingbird tongue is a fluid trap, not a capillary tube. PNAS, 2011.
66. Salem S.B. 1990. Comparative morpho-histology of the tongue of birds in relation to the feeding habits. Delta Journal of Science, 14(4):1586-1614.
67. Schwenk K. 1989. Functional and evolutionary morphology of lingual feeding in squamate reptiles: phylogenetics and kinematics. Journal of Zoology, 219:153-175.
68. Skieresz-Szewczyk K., Jackowiak H., Ratajczak M. 2014. LM and TEM study of the orthokeratinized and parakeratinized epithelium of the tongue in the domestic duck (Anas platyrhynchos f. domestica). Micron, 67:117-124.
69. Susi F.R. 1969. Keratinization in the mucosa of the ventral surface of the chicken tongue. Journal of anatomy, 105: 477-486
70. Tabasi M., Mohammadpour A.A. 2019. Light and scanning electron microscopic study of the tongue in the guinea fowl (Numida meleagris). Comparative Clinical Pathology, 28:613-619.
71. Uppal V., Bansal N., Anuradha Pathak D., Singh A. 2014. Light and scanning electron microscopy studies of tongues. Avian Biology Research, 7:167-171.
72. Vollmerhaus B., Sinowatz F. 1992. Verdauungsapparat. In: Nickel, R., Schummer, E., Seiferle, E. (Eds.), Anatomie der Vogel Bd. 5, Lehrbuch der Anatomie der Haustiere. Parey, Berlin.
73. Whittow G.C. 2000. Sturkie’s Avian Physiology. Academic press, NewYork, London, USA, 97-107.
