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Comparative Features of the Upper Alimentary Tract in the Domestic Fowl (Gallus gallus domesticus) and Kestrel (Falco tinnunculus): A Morphological, Histochemical, and Scanning Electron Microscopic Study

Published online by Cambridge University Press:  10 December 2020

Abdallah A. Alsanosy
Affiliation:
Histology and Cytology Department, Faculty of Veterinary Medicine, Damanhour University, Damanhour22511, Egypt
Ahmed E. Noreldin
Affiliation:
Histology and Cytology Department, Faculty of Veterinary Medicine, Damanhour University, Damanhour22511, Egypt
Yaser H. A. Elewa
Affiliation:
Histology and Cytology Department, Faculty of Veterinary Medicine, Zagazig University, Zagazig44519, Egypt Laboratory of Anatomy, Faculty of Veterinary Medicine, Basic Veterinary Sciences, Hokkaido University, Sapporo060-0818, Japan
Sahar F. Mahmoud
Affiliation:
Histology and Cytology Department, Faculty of Veterinary Medicine, Damanhour University, Damanhour22511, Egypt
Mohamed A. Elnasharty*
Affiliation:
Histology and Cytology Department, Faculty of Veterinary Medicine, Damanhour University, Damanhour22511, Egypt
Asmaa Aboelnour
Affiliation:
Histology and Cytology Department, Faculty of Veterinary Medicine, Damanhour University, Damanhour22511, Egypt
*
*Author for correspondence: Mohamed A. Elnasharty, E-mail: elnashartyeg@yahoo.com
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Abstract

The avian alimentary tract has evolved into different histologic structures to accommodate the physical and chemical features of several food types and flight requirements. We compared the esophagus, proventriculus, and gizzard of the domestic fowl, Gallus gallus domesticus (GGD) and kestrels, Falco tinnunculus (FT) using immunohistochemistry and scanning electron microscopy with various stains and lectins [Dolichos biflorus agglutinin (DBA) and Ricinus communis agglutinin I (RCA120)], and α-smooth muscle actin (α-SMA). The esophagus of GGD demonstrated thickened epithelium, muscularis mucosae, and inner circular longitudinal tunica muscularis layers; moderate outer longitudinal tunica muscularis layers; and a true crop. In contrast, the esophagus of FT showed a thin epithelium, no muscularis mucosae, moderate inner longitudinal and thick outer circular tunica muscularis layers, and no true crop. In the proventriculus, the nature of the secretion in GGD was neutral, but that of FT was acidic and neutral. In the gizzard, the muscle coat of GGD by α-SMA had no muscularis mucosae, unlike FT, which had muscularis mucosae. In summary, there are many histologic differences between GGD and FT to meet their different physiologic needs, such as feeding.

Type
Micrographia
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Abumandour, M (2013). Morphological studies of the stomach of falcon. Sci J Vet Adv 2(3), 3040.Google Scholar
Akester, A (1986). Structure of the glandular layer and koilin membrane in the gizzard of the adult domestic fowl (Gallus gallus domesticus). J Anat 147, 1.Google Scholar
Al-Nasser, A, Al-Khalaifa, H, Al-Saffar, A, Khalil, F, Albahouh, M, Ragheb, G, Al-Haddad, A & Mashaly, M (2007). Overview of chicken taxonomy and domestication. World's Poult Sci J 63(2), 285300.CrossRefGoogle Scholar
Al-Saffar, F & Al-Samawy, ER (2014). Microscopic study of the proventriculus and ventriculus of the striated scope Owl (Otus Scors brucei) in Iraq. Kufa J Vet Sci 5(2), 923.Google Scholar
Al-taee, AA (2017). Macroscopic and microscopic study of digestive tract of brown falcon Falco berigora in Iraq. JUBPAS 25(3), 915936.Google Scholar
Bancroft, JD & Layton, C (2013). The hematoxylin and eosin, connective and mesenchymal tissues with their stains. In Bancroft s Theory and Practice of Histological Techniques, Kim Suvarna, S, Layton, C & Bancroft, JD (Eds.), pp. 173186. Philadelphia: Churchill Livingstone.CrossRefGoogle Scholar
Batt, H (1924). A study of the normal histology of the fowl. Rep. of the Ontario Vet. Coll. pp. 21–31.Google Scholar
Bennett, T & Cobb, J (1969). Studies on the avian gizzard: The development of the gizzard and its innervation. Z Zellforsch Mikrosk Anat 98(4), 599621.CrossRefGoogle ScholarPubMed
Bradley, OC & Grahame, T (1960). The Structure of the Fowl. Edinburgh.Oliver and Boyd.Google Scholar
Calhoun, ML (1954). Microscopic anatomy of the digestive system of the chicken. Iowa, USA.The Iowa State College Press.Google Scholar
Caviedes-Vidal, E & Karasov, WH (2001). Developmental changes in digestive physiology of nestling house sparrows, Passer domesticus. Physiol Biochem Zool 74(5), 769782.CrossRefGoogle ScholarPubMed
Cheah, P & Ramachandran, K (1994). Alterations in mucin type: An indicator for suspicion of malignant gastric transformation. Malays J Pathol 16(1), 3942.Google ScholarPubMed
Chikilian, M & de Speroni, NB (1996). Comparative study of the digestive system of three species of tinamou. I. Crypturellus tataupa, Nothoprocta cinerascens, and Nothura maculosa (Aves: Tinamidae). J Morphol 228(1), 7788.3.0.CO;2-M>CrossRefGoogle Scholar
Del Rio, CM, Baker, H & Baker, I (1992). Ecological and evolutionary implications of digestive processes: Bird preferences and the sugar constituents of floral nectar and fruit pulp. Experientia 48(6), 544551.CrossRefGoogle Scholar
del Rio, CM & Karasov, WH (1990). Digestion strategies in nectar-and fruit-eating birds and the sugar composition of plant rewards. Am Nat 136(5), 618637.CrossRefGoogle Scholar
Denbow, DM (2015). Chapter 14 -Gastrointestinal Anatomy and Physiology. In Sturkie'sAvian Physiology (Sixth Edition), Scanes, CG (Ed.), pp. 337366. SanDiego: Academic Press.Google Scholar
Duke, GE (1997). Gastrointestinal physiology and nutrition in wild birds. Proc Nutr Soc 56(3), 10491056.CrossRefGoogle ScholarPubMed
Eurell, JA & Frappier, BL (2013). Dellmann's Textbook of Veterinary Histology. Hoboken, New Jersey: Wiley-Blackwell.Google Scholar
Ford, S (2010). Raptor gastroenterology. J Exot Pet Med 19(2), 140150.CrossRefGoogle Scholar
Gabius, HJ (2001). Glycohistochemistry: The why and how of detection and localization of endogenous lectins. Anat Histol Embryol 30(1), 331.CrossRefGoogle ScholarPubMed
Goldstein, I & Poretz, RD (2012. Isolation, physicochemical characterization, and carbohydrate-bindingspecificity of Iectins. In The lectins.Properties, functions, and applications in biology and medicine, Irvin E., Liener, Nathan, Sharon & Liener, I (Eds.), pp. 233247. SanDiego: AcademicPress.Google Scholar
Goldstein, IJ & Hayes, CE (1978). The lectins: Carbohydrate-binding proteins of plants and animals. Adv Carbohydr Chem Biochem 35, 127340.CrossRefGoogle ScholarPubMed
Hamdi, H, El-Ghareeb, A-W, Zaher, M & AbuAmod, F (2013). Anatomical, histological and histochemical adaptations of the avian alimentary canal to their food habits: II - Elanus caeruleus. Int J Sci Eng Res 4(10), 1355.Google Scholar
Hassan, SA & Moussa, EA (2012). Gross and microscopic studies on the stomach of domestic duck (Anas platyrhynchos) and domestic pigeon (Columba livia domestica). J Vet Anat 5(2), 105127.CrossRefGoogle Scholar
Hodges, RD (1974). The Histology of the Fowl. San Diego: Academic Press.Google Scholar
Hume, I (1998). Optimization in designof the digestive system. In Principles of animal design, Weibel, ER, Taylor, CR & Bolis, L (Eds.), pp. 212219. Cambridge, UK: Cambridge University Press.Google Scholar
Kadhim, K, Zuki, A, Noordin, M & Babjee, S (2011 a). Histomorphology of the stomach, proventriculus and ventriculus of the red jungle fowl. Anat Histol Embryol 40(3), 226233.CrossRefGoogle ScholarPubMed
Kadhim, KK, Zuki, A, Noordin, M, Babjee, S & Zamri-Saad, M (2011 b). Activities of amylase, trypsin and chymotrypsin of pancreas and small intestinal contents in the red jungle fowl and broiler breed. Afr J Biotechnol 10(1), 108115.Google Scholar
Kent, GC & Miller, L (1997). Comparative Anatomy of the Vertebrates. Dubuque, IA: Wm. C. Brown.Google Scholar
Klasing, KC (1999).Avian gastrointestinal anatomy and physiology. Seminarsin Avian and Exotic Pet Medicine.8(2), 4250.CrossRefGoogle Scholar
Layton, C & Bancroft, JD (2013). Carbohydrates. In Bancroft S Theory and Practice of Histological Techniques, Kim suvarna, S, Layton, C & Bancroft, JD (Eds.), pp. 215238. Philadelphia: Churchill Livingstone.CrossRefGoogle Scholar
Leznicka, B (1971). The effect of diet on the histological structure of the oesophagus and glandular stomach in the coot (Fulicaatra). Zool Poioniae 3(21), 263280.Google Scholar
López-Calleja, MV, Bozinovic, F & del Rio, CM (1997). Effects of sugar concentration on hummingbird feeding and energy use. Comp Biochem Phys A: Physiol 118(4), 12911299.CrossRefGoogle Scholar
Marshall, AJ (2013). Biology and Comparative Physiology of Birds. San Diego: Academic Press.Google Scholar
Menzies, G & Fisk, A (1963). Observations on the oxyntico-peptic cells in the proventricular mucosa of Gallus domesticus. J Cell Sci 3(66), 207215.Google Scholar
Naya, DE, Ebensperger, LA, Sabat, P & Bozinovic, F (2008). Digestive and metabolic flexibility allows female degus to cope with lactation costs. Physiol Biochem Zool 81(2), 186194.CrossRefGoogle ScholarPubMed
Onouchi, S, Ichii, O, Otsuka, S, Hashimoto, Y & Kon, Y (2013). Analysis of duodenojejunal flexure formation in mice: Implications for understanding the genetic basis for gastrointestinal morphology in mammals. J Anat 223(4), 385398.CrossRefGoogle ScholarPubMed
Penry, D & Jumars, P (1986). Chemical reactor theory and optimal digestion. BioScience 36, 310315.CrossRefGoogle Scholar
Perry-Gal, L, Erlich, A, Gilboa, A & Bar-Oz, G (2015). Earliest economic exploitation of chicken outside East Asia: Evidence from the Hellenistic Southern Levant. Proc Natl Acad Sci USA 112(32), 98499854.CrossRefGoogle ScholarPubMed
Rajabi, E & Nabipour, A (2009). Histological study on the oesophagus and crop in various species of wild bird. Avian Biol Res 2(3), 161164.CrossRefGoogle Scholar
Riegert, J, Lövy, M & Fainová, D (2009). Diet composition of common kestrels Falco tinnunculus and long-eared owls Asio otus coexisting in an urban environment. Ornis Fenn 86(4), 123130.Google Scholar
Romanoff, AL (1960). The Avian Embryo: Structural and Functional Development. New York, USA.MacMillian Co.Google Scholar
Roth, J (1996). Protein glycosylation in the endoplasmic reticulum and the Golgi apparatus and cell type-specificity of cell surface glycoconjugate expression: Analysis by the protein A-gold and lectin-gold techniques. Histochem Cell Biol 106(1), 7992.CrossRefGoogle ScholarPubMed
Sabat, P & Veloso, C (2003). Ontogenic development of intestinal disaccharidases in the precocial rodent Octodon degus (Octodontidae). Comp Biochem Phys A: Mol Integr Physiol 134(2), 393397.CrossRefGoogle Scholar
Sassi, PL, Borghi, CE & Bozinovic, F (2007). Spatial and seasonal plasticity in digestive morphology of cavies (Microcavia australis) inhabiting habitats with different plant qualities. J Mammal 88(1), 165172.CrossRefGoogle Scholar
Selvan, PS, Ushakumary, S & Ramesh, G (2008). Studies on the histochemistry of the proventriculus and gizzard of post-hatch Guinea fowl (Numida meleagris). Int J Poult Sci 7(11), 11121116.Google Scholar
Spicer, S (1992). Diversity of cell glycoconjugates shown histochemically: A perspective. J Histochem Cytochem 40, 138.CrossRefGoogle ScholarPubMed
Toner, PG (1963). The fine structure of resting and active cells in the submucosal glands of the fowl proventriculus. J Anat 97(Pt 4), 575.Google ScholarPubMed
Topfer-Petersen, E (1999). Carbohydrate-based interactions on the route of a spermatozoon to fertilization. Hum Reprod Update 5(4), 314329.CrossRefGoogle Scholar
Varghese, F, Bukhari, AB, Malhotra, R & De, A (2014). IHC profiler: An open source plugin for the quantitative evaluation and automated scoring of immunohistochemistry images of human tissue samples. PLoS One 9(5), e96801.CrossRefGoogle ScholarPubMed
Yamada, K & Shimizu, S (1977). The histochemistry of galactose residues of complex carbohydrates as studied by peroxidase-labeled Ricinus communis agglutinin. Histochemistry 53(2), 143156.CrossRefGoogle ScholarPubMed
Zaher, M, El-Ghareeb, A-W, Hamdi, H & AbuAmod, F (2012). Anatomical, histological and histochemical adaptations of the avian alimentary canal to their food habits: I - Coturnix coturnix. Life Sci J 9(3), 253275.Google Scholar
Zhu, L (2015 a). Histological and histochemical study on the stomach (proventriculus and gizzard) of black-tailed crake (Porzana bicolor). Pak J Zool 47(3), 607616.Google Scholar
Zhu, L (2015 b). Histological study of the oesophagus and stomach in grey-backed shrike (Lanius tephronotus). Int J Morphol 33(2), 459464.CrossRefGoogle Scholar