Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-28T00:24:36.914Z Has data issue: false hasContentIssue false
  • English
  • Français

Anatomical, Histological, and Electron Microscopic Structures of Syrinx in Male Budgerigars (Melopsittacus undulatus)

Part of: Micrographia Collection

Published online by Cambridge University Press:  04 November 2020

Fatma M. Abdel-Maksoud Open the ORCID record for Fatma M. Abdel-Maksoud [Opens in a new window] ,
Marwa M. Hussein Open the ORCID record for Marwa M. Hussein [Opens in a new window] ,
Amira Hamdy  and
Ismail Abdel-Aziz Ibrahim
Fatma M. Abdel-Maksoud*
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, Assiut, Egypt
Marwa M. Hussein
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, Assiut, Egypt
Amira Hamdy
Affiliation:
Department of Anatomy, Faculty of Veterinary Medicine, New Valley University, New Valley, Egypt
Ismail Abdel-Aziz Ibrahim
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, Assiut, Egypt
*
*Author for correspondence: Fatma M. Abdel-Maksoud, E-mail: fatma.abdelmaksoud@vet.au.edu.eg
Get access

Abstract

The syrinx is the main source for phonation in birds, its function is analogous to the mammalian larynx. Birds have both a larynx and a syrinx, but they use only the latter to vocalize. The objective of this work to give a detailed description of the anatomical, histological, and ultrastructural of syrinx in male budgerigars as a model of a passerine bird. The syrinx in the current study was to be found as a tracheobronchial type, it consists of cranial (tympanum) part and caudal (bronchosyringeal) part and, additionally, there are lateral vibrating membranes. The tympanum is formed of the last six tracheal rings, histologically its lamina epithelialis is a pseudostratified ciliated columnar epithelium with goblet cells and interrupted by intraepithelial glands. The secretory acini appear oval and lined by pyramidal secretory cells. The lamina propria–submucosa contain numerous blood capillaries, immune cells, and telocytes (TCs). The electron microscopic examination revealed numerous blood capillaries surrounded by fibroblasts and numerous immune cells, including mast cells and wandering leukocytes, within the tympanum mucosa. Hence, this study provides a detailed knowledge about the syrinx in male budgerigars.

Keywords

budgerigarshistologicalsyrinxtympanum
Type
Micrographia
Information
Microscopy and Microanalysis , Volume 26 , Issue 6 , December 2020 , pp. 1226 - 1235
Copyright
Copyright © Microscopy Society of America 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

Deceased

References

Al-Bishtue, AAH (2014). Anatomical investigations of the syrinx (voice box) of the adult male West African guinea fowl (Numida meleagris galeata) in the Al-Najaf Al-Ashraf province. Al-Qadisiya J Vet Med Sci 13, 100–105.Google Scholar
Arican, I, Yildiz, H & Yilmaz, B (2007). Morphometric studies on vocal organ of white Turkey. Indian Vet J 84, 964–966.Google Scholar
Bancroft, JD, Layton, C & Suvarna, SK (2013). Bancroft's Theory and Practice of Histological Techniques. London: Elsevier, Churchill Livingstone.Google Scholar
Baumel, JJ, King, AS, Breazile, JE, Evans, HE & Berge, JCV (1993). Handbook of Avian Anatomy: Nomina Anatomica Avium. Cambridge, MA: The Nuttall Ornithological Club No. 23.Google Scholar
Bayram, G & Liman, N (2000). A morphological investigation of the postnatal development of the syrinx in the quail. Turk J Vet Anim Sci 24, 381–392.Google Scholar
Burke, MR, Adkins-Regan, E & Wade, J (2007). Laterality in syrinx muscle morphology of the Japanese quail (Coturnix japonica). Physiol Behav 90, 682–686.CrossRefGoogle ScholarPubMed
Bustamante-Marin, XM & Ostrowski, LE (2018). Cilia and mucociliary clearance. Cold Spring Harb Perspect Biol 9, a028241.CrossRefGoogle Scholar
Cevik-Demirkan, A, Haziroglu, RM & Kurtul, I (2007). Gross morphological and histological features of larynx, trachea and syrinx in Japanese quail. Anat Histol Embryol 36, 215–219.CrossRefGoogle ScholarPubMed
Cevik-Demirkan, A & Ozdemir, V (2011). A study on anatomical structures of the larynx, trachea and syrinx in Eurasian eagle owl (Bubo bubo). J Anim Vet Adv 10, 3218–3224.Google Scholar
During, DN, Ziegler, A, Thompson, CK, Ziegler, A, Faber, C, Muller, J, Scharff, C & Elemans, CP (2013). The songbird syrinx morphome: A three-dimensional, high-resolution, interactive morphological map of the zebra finch vocal organ. BMC Biol 11, 1.CrossRefGoogle ScholarPubMed
Edwards, SV, Kingan, SB, Calkins, JD, Balakrishnan, CN, Jennings, WB, Swanson, WJ & Sorenson, MD (2005). Speciation in birds: Genes, geography, and sexual selection. Proc Natl Acad Sci USA 102(Suppl 1), 6550–6557.CrossRefGoogle ScholarPubMed
Erdogan, S, Sagsoz, H & Paulsen, F (2015). Functional anatomy of the syrinx of the chukar partridge (Galliformes: Alectoris chukar) as a model for phonation research. Anat Rec 298, 602–617.CrossRefGoogle Scholar
Evans, MJ, Van Winkle, LS, Fanucchi, MV & Plopper, CG (1999). The attenuated fibroblast sheath of the respiratory tract epithelial–mesenchymal trophic unit. Am J Respir Cell Mol Biol 21, 655–657.CrossRefGoogle ScholarPubMed
Fee, MS (2002). Measurement of the linear and non linear mechanical properties of the oscine syrinx: Implications for function. J Comp Physiol A 188, 829–839.CrossRefGoogle Scholar
Frank, T, Probst, A, Konig, HE & Walter, I (2007). The syrinx of the male mallard (Anas platyrhynchos): Special anatomical features. Anat Histol Embryol 36, 121–126.CrossRefGoogle ScholarPubMed
Frank, T, Walter, I, Probst, A & Konig, HE (2006). Histological aspects of the syrinx of the male mallard (Anas platyrhynchos). Anat Histol Embryol 35, 396–401.CrossRefGoogle ScholarPubMed
Gaban-Lima, R & Höfling, (2006). Comparative anatomy of the syrinx in the Tribe Arini (Aves: Psittacidae). Braz J Morphol Sci 23, 501–512.Google Scholar
Gaunt, AS & Gaunt, SLL (1977). Mechanics of the syrinx in Gallus gallus. II. Electromyographic studies of ad libitum vocalizations. J Morphol 152, 1–20.CrossRefGoogle ScholarPubMed
Gaunt, AS & Gaunt, SLL (1985 a). Electromyographic studies of the syrinx in parrots (Aves, Psittacidae). Zoomorphology 105, 1–11.CrossRefGoogle Scholar
Gaunt, AS & Gaunt, SLL (1985 b). Syringeal Structure and Avian Phonation. In: Current Ornithology. New York: Plenum Press.CrossRefGoogle Scholar
Getty, R (1975). Anatomy of Domestic Animals. Philadelphia: W.B. Saunders Company.Google Scholar
Goller, F & Larsen, ON (1999). Role of syringeal vibrations in bird vocalizations. Proc R Soc Lond B 266, 1609–1615.Google Scholar
Gündemir, O & Alpak, H (2020). Macroanatomic examination of the Trachea and syrinx in Budgerigars and Canaries. Harran Üniv Vet Fak Derg 9, 19–23.CrossRefGoogle Scholar
Hiemstra, PS (2001). Epithelial antimicrobial peptides and proteins: Their role in host defence and inflammation. Paediatr Respir Rev 2, 306–310.Google ScholarPubMed
Ibrahim, IA, Hussein, MM, Hamdy, A & Abdel-Maksoud, FM (2020). Comparative morphological features of syrinx in male domestic fowl Gallus gallus domesticus and male domestic pigeon Columba livia domestica: A histochemical, ultrastructural, scanning electron microscopic and morphometrical study. Microsc Microanal 26(2), 1–22.CrossRefGoogle ScholarPubMed
Ince, NG, Pazvant, G & Alpak, H (2012). Anatomical features of the syrinx in sea gulls. Ankara Üniv Vet Fak Derg 59, 1–3.Google Scholar
Kabak, M, Orhan, IO & Haziroglu, RM (2007). The gross anatomy of larynx, trachea and syrinx in the long-legged buzzard (Buteo rufinus). Anat Histol Embryol 36, 27–32.CrossRefGoogle ScholarPubMed
Karunovsky, M (1965). A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27, 137A.Google Scholar
Keskin, N & Ili, P (2013). Glycohistochemistry of the lateral tympanic membrane in the syrinx of the Denizli cock. Turk J Vet Anim Sci 37, 414–418.CrossRefGoogle Scholar
Khaksar, Z, Kookhdan, ET & Parto, P (2012). A study on anatomy and histological structure of Larynx in male and female turkeys. World J Zool 7, 245–250.Google Scholar
King, AS (1975). Sisson and Grossman's the Anatomy of the Domestic Animals, Getty R (Ed.). Philadelphia: Saunders.Google Scholar
King, AS (1989). Functional anatomy of the syrinx. In Form and Function in Birds, King, AS & Meclelland, J (Eds.), London: Academic Press.Google Scholar
King, AS & Mclelland, J (1984). Birds Their Structure and Function. London: Bailiere Tindall.Google Scholar
Kriesell, HJ, Le bohec, C, Cerwenka, AF, Hertel, M, Robin, JP, Ruthensteiner, B, Gahr, M, Aubin, T & Düring, DN (2020). Vocal tract anatomy of king penguins: Morphological traits of two-voiced sound production. Front Zool 17, 5.CrossRefGoogle ScholarPubMed
Larsen, ON & Goller, F (1997). In situ biomechanics of the syrinx and sound generation in pigeons. J Exp Biol 200, 2165–2176.Google Scholar
Larsen, ON & Goller, F (2002). Direct observation of syringeal muscle function in songbirds and a parrot. J Exp Biol 205, 25–35.CrossRefGoogle Scholar
Marshall, JS & DawickI, W (2007). New and emerging roles for mast cells in host defence. Curr Opin Immunol 19, 31–38.Google Scholar
McNamara, PS, Flanagan, BF, Hart, CA & Smyth, RL (2005). Production of chemokines in the lungs of infants with severe respiratory syncytial virus bronchiolitis. J Infect Dis 191, 1225–1232.CrossRefGoogle ScholarPubMed
McNamara, PS, Flanagan, BF, Selby, AM, Hart, CA & Smyth, RL (2004). Pro-and anti-inflammatory responses in respiratory syncytial virus bronchiolitis. Eur Respir J 23, 106–112.CrossRefGoogle ScholarPubMed
Miller, EH, Seneviratne, SS, Jones, IL, Robertson, GJ & Wilhelm, SI (2008). Syringeal anatomy and allometry in murres (Alcidae: Uria). J Ornithol 149, 545–554.CrossRefGoogle Scholar
Mohamed, R (2017 a). Gross anatomical syringeal structures of goose (Anser anser domesticus). J Adv Vet Anim Res 4, 343–347.CrossRefGoogle Scholar
Mohamed, R (2017 b). Sexual dimorphism in the anatomical features of the syrinx in the white Pekin Ducks (Anas platyrhynchos). Int J Agric Sci Vet Med 5, 78–85.Google Scholar
Myers, JA (1917). Studies on the syrinx of Gallus domesticus. J Morphol 20, 165–215.CrossRefGoogle Scholar
Nicholas, B, Skipp, P, Mould, R, Rennard, S, Davies, DE, O'Connor, CD & Djukanović, R (2006). Shotgun proteomic analysis of human-induced sputum. Proteomics 6, 4390–4401.CrossRefGoogle ScholarPubMed
Nickel, R, Schummer, A & Seiferle, E (1977). Anatomy of the Domestic Birds. Berlin, Germany: Verlag Paul Parey.Google Scholar
Nottebohm, F (1976). Phonation in the orange-winghed Amazon parrot (Amazona amazonica). J Comp Physiol 108, 157–170.CrossRefGoogle Scholar
Onuk, B, Haziroglu, RM & Kabak, M (2010). The gross anatomy of larynx, trachae and syrinx in goose (Anser anser domesticus). Kafkas Univ Vet Fak Derg 16, 443–450.Google Scholar
Ozudogru, Z, Balkaya, H, Kara, A & Ozdemir, D (2015). A study of the morphological structure of the syrinx of the Sparrowhawk (Accipiter nisus). Israel J Vet Med 70, 46–50.Google Scholar
Paulsen, K (1970). The principle of voice production. HNO 18, 1.Google ScholarPubMed
Ragab, AS, Reem, RT, Rezk, MH & Nora, AS (2016). The gross anatomy of the syrinx of the Turkey. Int J Adv Res Biol Sci 3, 82–90.Google Scholar
Reynolds, ES (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17, 208.CrossRefGoogle ScholarPubMed
Riede, T & Olson, CR (2020). The vocal organ of hummingbirds shows convergence with songbirds. Sci Rep 10, 1–14.CrossRefGoogle ScholarPubMed
Rodríguez, JRG & Fabila, GS (2010). Descripción anatómica del esqueleto de los tractos respiratorios superiores del periquito australiano (Melopsittacus undulatus). Int J Morphol 28, 85–92.Google Scholar
Spurr, AR (1969). A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26, 31–43.CrossRefGoogle ScholarPubMed
Stein, RC (1968). Modulation in bird sounds. The Auk 85, 229–243.CrossRefGoogle Scholar
Tabler, JM, Rigney, MM, Berman, GJ, Gopalakrishnan, S, Heude, E, Al-Lami, HA, Yannakoudakis, BZ, Fitch, RD, Carter, C, Vokes, S, Liu, KJ, Tajbakhsh, S, Egnor, SR & Wallingford, JB (2017). Cilia-mediated Hedgehog signaling controls form and function in the mammalian larynx. Elife 6, 1–26.CrossRefGoogle ScholarPubMed
Taşbaş, M, Hazıroğlu, RM, Çakır, A & Özer, M (1994). Morphological investigations of the respiratory system of the Denizli cock. II. Laryx, trachea, syrinx. Ankara Univ Vet Fak Derg 41, 135–153.Google Scholar
Warner, RW (1972). The anatomy of the syrinx in passerine birds. J Zool Lond 168, 381–393.CrossRefGoogle Scholar
Yildiz, H, Bahadir, A & Akkoc, A (2003). A study on the morphological structure of syrinx in ostriches (Struthio camelus). Anat Histol Embryol 32, 187–191.CrossRefGoogle Scholar
Yildiz, H, Yilmaz, B & Arican, I (2005). Morphological structure of the syrinx in the Bursa roller pigeon. Bull Vet Inst Pulawy 49, 323–327.Google Scholar
Yilmaz, B, Yilmaz, R, Arican, I & Yildiz, H (2012). Anatomical structure of the syrinx in the mallard (Anas platyrhynchos). Harran Univ Vet Fak Derg 1, 111–116.Google Scholar