Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-22T19:46:16.518Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Part of: Micrographia Collection

Published online by Cambridge University Press:  31 January 2020

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

Abstract

Many studies have been carried out to investigate the morphological structure of the syrinx in many bird species. However, the cellular organization of the syrinx in the fowls and pigeons is still unclear. The current study revealed that in fowl and pigeon, the syrinx is formed of three main parts including tympanum (cranial) part, intermediate syringeal part, and bronchosyringeal (caudal) part, in addition to pessulus and tympaniform membranes. A great variation in the structural characteristics of syrinx of fowl and pigeon was recorded. In fowl, the tympaniform membranes showed a characteristic distribution of elastic and collagen fibers which increase the elasticity of tympaniform membranes. Moreover, the bony pessulus helps the medial tympaniform membranes to be stiffer, vibrate more strongly so that louder sound will be generated. In pigeon, the lateral tympaniform membrane is of greater thickness so that the oscillation of this membrane is reduced and the amplitude is lower. Moreover, the pessulus is smaller in size and is formed mainly of connective tissue core (devoid of cartilaginous or bony plates), resulting in the failure of stretching and vibrating of the medial tympaniform membranes, that leads to the generation of deeper sound. Electron microscopic examination of the syringes of fowls and pigeons revealed numerous immune cells including dendritic cells, plasma cells, mast cells, and lymphocytes distributed within syringeal mucosa and invading the syringeal epithelium. Telocytes were first recorded in the syrinx of fowls and pigeons in this study. They presented two long telopodes that made up frequent close contacts with other neighboring telocytes, immune cells, and blood capillaries.

Keywords

dendritic reticular cellsimmune cellssyrinxtelocytestympaniform membranes
Type
Micrographia
Information
Microscopy and Microanalysis , Volume 26 , Issue 2 , April 2020 , pp. 326 - 347
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.)

References

Al-aameli, MH & Kadhim, K (2017). Histomorphological study of syrinx of black francolin (Francolinus francolinus) in Iraq. Adv Anim Vet Sci 5(2), 92–99.CrossRefGoogle Scholar
Bancroft, JD, Layton, C & Suvarna, SK (2013). Bancroft's Theory and Practice of Histological Techniques, 7th ed.London: Elsevier/Churchill Livingstone.Google Scholar
Barbara, H, Vulsteke, C, Peter, D, Anthony, VB, Stefan, H, Denis, W, Ximena, EK, Elisabeth, VE & Filip, A (2018). Quality of care in oncology: Quality indicators in testicular cancer: A hospital-based approach. Acta Clinica Belgica 73(1), 29–33. doi:10.1080/17843286.2017.1331814CrossRefGoogle ScholarPubMed
Baumel, JJ, King, AS, Breazile, JE, Evans, HE & Berge, JCV (1993). Handbook of Avian Anatomy: Nomina Anatomica Avium, 2nd ed.Cambridge, MA: The Nuttall Ornithological Club. No: 23.Google Scholar
Bei, Y, Zhou, Q, Fu, S, Lv, D, Chen, P, Chen, Y, Wang, F & Xiao, J (2015). Cardiac telocytes and fibroblasts in primary culture: Different morphologies and immunophenotypes. PLoS ONE 10(2), e0115991. doi:10.1371/journal.pone.0115991CrossRefGoogle ScholarPubMed
Bell, DJ & Freeman, BM (1971). Physiology and Biochemistry of the Domestic Fowl, 2nd ed.London: UK Academic Press.Google Scholar
Brackenbury, JH (1980). Control of sound production in the syrinx of the fowl Gallus gallus. J Exp Biol 85, 239–251.Google 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(3), 215–219. doi:10.1111/j.1439-0264.2007.00758.xCrossRefGoogle ScholarPubMed
Constable, PD, Gohar, HM, Morin, DE & Thurmon, JC (1996). Use of hypertonic saline-dextran solution to resuscitate hypovolemic calves with diarrhea. Am J Vet Res 57(1), 97–104.Google ScholarPubMed
Cover, MS (1953). Cross and microscopic anatomy of the respiratory system of the turkey. Am J Vet Res April, 230–238.Google Scholar
Cretoiu, SM & Popescu, LM (2014). Telocytes revisited. Biomol Concepts 5(5), 353–369.CrossRefGoogle ScholarPubMed
Dyce, KM, Sack, WO & Wensing, CJG (1987). Textbook of Veterinary Anatomy. London, UK: W. B. Saunders Company.Google Scholar
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(3), 602–617.CrossRefGoogle ScholarPubMed
Erle, DJ & Pabst, R (2000). Intraepithelial lymphocytes in the lung. A neglected lymphocyte population. Am J Respir Cell Mol Biol 22, 398–400.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(6), 655–657.CrossRefGoogle ScholarPubMed
Frank, T, Probst, A, Konig, HE & Walter, I (2007). The syrinx of the male mallard (Anas platyrhynchos): Special anatomical features. Anat Histol Embryo 36(2), 121–126. doi:10.1111/j.1439-0264.2006.00737.xCrossRefGoogle ScholarPubMed
Frank, T, Walter, I, Probst, A & Konig, HE (2006). Histological aspects of the syrinx of the male mallard (Anas platyrhynchos). Anat Histol Embryo 35(6), 396–401. doi:10.1111/j.1439-0264.2006.00701.xCrossRefGoogle Scholar
Freeman, B (1983). Physiology and Biochemistry of the Domestic Fowl, 234–256. New York: Academic Press.Google Scholar
Gaban-lima, R & Höfling, E (2006). Comparative anatomy of the syrinx in the Tribe Arini (Aves: Psittacidae). Braz J Morphol Sci 23(3–4), 501–512.Google Scholar
Galli, SJ, Maurer, M & Lantz, CS (1999). Mast cells as sentinels of innate immunity. Curr Opin Immunol 11(1), 53–59.CrossRefGoogle ScholarPubMed
Gaunt, AS & Gaunt, SLL (1977). Mechanics of the syrinx in Gallus gallus. II. Electromyographic studies of ad libitum vocalizations. J Morphol 152(1), 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, vol. 2. Johnston, Richard F (Ed.), New York, NY: Plenum Press.Google Scholar
Gaunt, AS, Gaunt, SLL & Casey, RM (1982). Syringeal mechanics reassessed: Evidence from Streptopelia. The Auk 99(3), 474–494.Google Scholar
Getty, R (1975). Anatomy of Domestic Animals. Philadelphia, PA: W.B. Saunders Company.Google Scholar
Goller, F & Larsen, ON (1999). Role of syringeal vibrations in bird vocalizations. Proc R Soc Lond B: Biol Sci 266(1429), 1609–1615.Google Scholar
Goller, F & Suthers, RA (1996). Role of syringeal muscles in gating airflow and sound production in singing brown thrashers. J Neurophysiol 75, 867–876.CrossRefGoogle ScholarPubMed
Hartley, RS & Suthers, RA (1990). Lateralization of syringeal function during song production in the canary. J Neurobiol 21, 1236–1248.CrossRefGoogle ScholarPubMed
Hiemstra, PS (2001). Epithelial antimicrobial peptides and proteins: Their role in host defence and inflammation. Paediatr Respir Rev 2(4), 306–310. doi:10.1053/prrv.2001.0165Google ScholarPubMed
Hogg, DA (1982). Ossification of the laryngeal tracheal and syringeal cartilages in the domestic fowl. J Anat 134, 57–71.Google ScholarPubMed
Hussein, MM & Mokhtar, DM (2018). The roles of telocytes in lung development and angiogenesis: An immunohistochemical, ultrastructural, scanning electron microscopy and morphometrical study. Dev Biol 443(2), 137–152.CrossRefGoogle ScholarPubMed
Kang, Y, Zhu, Z, Zheng, Y, Wan, W, Manole, CG & Zhang, Q (2015). Skin telocytes versus fibroblasts: Two distinct dermal cell populations. J Cell Mol Med 19(11), 2530–2539. doi:10.1111/jcmm.12671CrossRefGoogle 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(4), 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(3), 245–250.Google Scholar
King, AS (1989). Functional anatomy of the syrinx. In Form and Function in Birds, vol. 4. King, AS & McLelland, J (Eds.), New York, NY: Academic Press.Google Scholar
King, AS & Mclelland, J (1975). Outlines of Avian Anatomy, 1st ed.London: Bailiere and Tindall.Google Scholar
King, AS & Mclelland, J (1984). Birds Their Structure and Function, 2nd ed.London: Bailiere Tindall.Google Scholar
Koch, T (1973). Anatomy of the Chicken and Domestic Birds, 1st ed.Iowa City, IA: The Iowa State University Press.Google Scholar
Konig, HE & Liebich, HG (2001). Anatomie und Propadeutik des Geflugels. Stuttgart: Schattaver.Google Scholar
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(Pt 1), 25–35.Google Scholar
Larsen, ON, Goller, F & van Leeuwen, JL (2006). Aspects of syringeal mechanics in avian phonation. Acta Zool Sin 52(Suppl. 1), 478–481.Google Scholar
Levin, M (2012). Molecular bioelectricity in developmental biology: New tools and recent discoveries: Control of cell behavior and pattern formation by transmembrane potential gradients. Bioessays 34(3), 205–217.CrossRefGoogle ScholarPubMed
Marshall, JS & Dawicki, W (2007). New and emerging roles for mast cells in host defence. Curr Opin Immunol 19(1), 31–38.Google Scholar
Mclelland, J (1990). A colour Atlas of Avian Anatomy. London: Wolfe Publishing Ltd.Google Scholar
McNamara, PS, Flanagan, BF, Selby, AM, Hart, C & Smyth, RL (2004). Proandanti-inflammatory responses in respiratory syncytial virus bronchiolitis. Eur Respir J 23, 106–112.CrossRefGoogle ScholarPubMed
McNamara, PS, Flanagan, BF, Hart, CA & Smyth, RL (2005). Production ofchemokines in the lungs of infants with severe respiratory syncytialvirus bronchiolitis. J Infect Dis 191, 1225–1232.CrossRefGoogle Scholar
Meclelland, J (1990). A colour Atlas of Avian Anatomy. London: Wolfe Publishing Ltd.Google Scholar
Merad, M, Sathe, P, Helft, J, Miller, J & Mortha, A (2013). The dendritic cell lineage: Ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Ann Rev Immunol 31, 563–604.CrossRefGoogle ScholarPubMed
Mokhtar, DM, Hussein, MT, Hussein, MM, Abd-Elhafez, EA & Kamel, G (2019). New insight into the development of the respiratory Acini in rabbits: Morphological, electron microscopic studies, and TUNEL assay. Microsc Microanal 25(3), 769–785.CrossRefGoogle ScholarPubMed
Mokhtar, DM & Hussien, MH (2019). Cellular elements organization in the trachea of mallard (Anas platyrhynchos) with a special reference to its local immunological role Protoplasma. https://doi.org/10.1007/s00709-019-01444-5CrossRefGoogle Scholar
Myers, JA (1917). Studies on the syrinx of Gallus domesticus. J Morphol 20, 165–215.CrossRefGoogle Scholar
Nickel, R, Schummer, A & Seiferle, E (1977). Anatomy of the Domestic Birds, 2nd ed.Berlin: Verlag Paul Parey.Google Scholar
Nottebohm, F (1976). Phonation in the orange-winged 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(3), 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). Isr J Vet Med 70(4), 46–50.Google Scholar
Piperno, E & Peirone, S (1975). Morphological characteristics and mutual relationships of the tracheal cartilaginous rings in Gallus gallus. Anat Histol Embryol 4, 172–178.CrossRefGoogle ScholarPubMed
Popescu, LM & Faussone-Pellegrini, MS (2010). TELOCYTES – a case of serendipity: The winding way from Interstitial Cells of Cajal (ICC), via Interstitial Cajal-Like Cells (ICLC) to TELOCYTES. J Cell Mol Med 14(4), 729–740.CrossRefGoogle Scholar
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(6), 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 & Goller, F (2010). Functional morphology of the sound-generating labia in the syrinx of two songbird species. J Anat 216(1), 23–36.CrossRefGoogle ScholarPubMed
Seller, TJ (1987). Bird Respiration, vol. 1, 1st ed.Boca Raton, FL: CRC Press.Google Scholar
Smythies, J & Edelstein, L (2014). Telocytes, exosomes, gap junctions and the cytoskeleton: The makings of a primitive nervous system? Front Cell Neurosci 7, 278.CrossRefGoogle ScholarPubMed
Spurr, AR (1969). A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26(1–2), 31–43.CrossRefGoogle ScholarPubMed
Suthers, RA (2001). Peripheral vocal mechanisms in birds: Are songbirds special? Neth J Zool 51, 217–242.CrossRefGoogle Scholar
Suthers, RA, Goller, F & Hartley, RS (1994). Motor dynamics of song production by mimic thrushes. J Neurobiol 25(8), 917–936.CrossRefGoogle ScholarPubMed
Suthers, RA & Zollinger, SA (2004). Producing song. The vocal apparatus. Ann NY Acad Sci 1016, 109–129.CrossRefGoogle ScholarPubMed
Taşbaş, M, Hazıroğlu, RM, Çakır, A & Özer, M (1994). Morphological investigations of the respiratory system of the Denizli cock. II. Larynx, trachea, syrinx. Ankara Univ Vet Fak Derg 41, 135–153.Google Scholar
Turley, SJ, Inaba, K, Garrett, WS, Ebersold, M, Unternaehrer, J, Steinman, RM & Mellman, I (2000). Transport of peptide-MHC class II complexes in developing dendritic cells. Science 288(5465), 522–527.CrossRefGoogle ScholarPubMed
Warner, RW (1971). The structural basis of the organ of voice in the genera Anas and Aythya (Ayes). J Zool 164, 197–207.CrossRefGoogle Scholar
Warner, RW (1972 a). The anatomy of the syrinx in passerine birds. J Zool Lond 168, 381–393.CrossRefGoogle Scholar
Warner, RW (1972 b). The syrinx in family Columbidea. J Zool 166, 385–390.CrossRefGoogle Scholar
Warren, DK, Patterson, DK & Pepperberg, IM (1996). Mechanisms of American English vowel production in a grey parrot (Psittacus erithacus). The Auk 113, 41–58.Google Scholar
West, MA, Lucocq, JM & Watts, C (1994). Antigen processing and class II MHC peptide-loading compartments in human B-lymphoblastoid cells. Nature 369(6476), 147–151.CrossRefGoogle ScholarPubMed
Witczak, P & Brzezińska-Błaszczyk, E (2012). Mast cells in viral infections. Postepy Hig Med Dosw 66, 231–241.CrossRefGoogle ScholarPubMed
Yang, P, Wang, S, Gandahi, JA, Bian, X, Wu, L, Liu, Y, Zhang, L, Zhang, Q & Chen, Q (2012). Ultrastructural identification of different subtypes of interstitial cells of Cajal in the chicken ileum. Poult Sci 91(8), 1936–1940.CrossRefGoogle ScholarPubMed
Yildiz, H, Bahadir, A & Akkoc, A (2003). A study on the morphological structure of syrinx in ostriches (Struthio camelus). Anat Histol Embryo 32(3), 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(2), 111–116.Google Scholar