The anatomy of the domestic duck lung was studied macroscopically, by casting and by light, transmission, and scanning electron microscopy. The lung had four categories of secondary bronchi (SB), namely, the medioventral (MV, 4-5), laterodorsal (LD, 6–10), lateroventral (LV, 2–4), and posterior secondary bronchi (PO, 36–44). The neopulmonic parabronchi formed an intricate feltwork on the ventral third of the lung and inosculated those from the other SB. The lung parenchyma was organized into cylindrical parabronchi separated by thin septa containing blood vessels. Atria were shallow and well-fortified by epithelial ridges reinforced by smooth muscle bundles and gave rise to 2–6 elongate infundibulae. Air capillaries arose either directly from the atria or from infundibulae and were tubular or globular in shape with thin interconnecting branches. The newly described spatial disposition of the conducting air conduits closely resembles that of the chicken. This remarkable similarity between the categories, numbers, and 3D arrangement of the SB in the duck and chicken points to a convergence in function-oriented design. To illuminate airflow dynamics in the avian lung, precise directions of airflow in the various categories of SB and parabronchi need to be characterized. 1. Introduction It has long been known that airflow in the bird lung is mainly unidirectional [1, 2], and this has been attributed largely to the bellows-like action of the air sacs. In a recent report, it has been demonstrated that airflow in the alligator lung is unidirectional just like in birds, despite the absence of air sacs [3]. This has thrown more confusion into the already controversial descriptions of the avian lung structure and function. Over the years, the structure and function of the avian lung have intrigued scientists and the actual structural complexity is only beginning to come to light [4]. The seminal insights into the avian lung function such as the description of unidirectional air flow [2, 5] and cross-current gas exchange [6] were established in the duck lung. While several studies have attempted to elucidate the fine details of the avian lung structure, certain aspects that could be directly related to function still remain enigmatic and several techniques including 3D reconstruction have been attempted to resolve the spatial arrangement of the gas exchange tissue [7–9]. Furthermore, lung structure among vertebrates has been most refined in birds where the thinnest blood gas-barrier is encountered [10, 11]. Generally, the avian lung is reported to be noncompliant
References
[1]
E. H. Hazelhoff, “Structure and function of the lung of birds,” Poultry Science, vol. 30, pp. 3–10, 1951.
[2]
W. L. Bretz and K. Schmidt-Nielsen, “Bird respiration: flow patterns in the duck lung,” Journal of Experimental Biology, vol. 54, no. 1, pp. 103–118, 1971.
[3]
C. G. Farmer and K. Sanders, “Unidirectional airflow in the lungs of alligators,” Science, vol. 327, no. 5963, pp. 338–340, 2010.
[4]
A. N. Makanya and V. Djonov, “Development and spatial organization of the air conduits in the lung of the domestic fowl, gallus Gallus variant domesticus,” Microscopy Research and Technique, vol. 71, no. 9, pp. 689–702, 2008.
[5]
P. Scheid and J. Piiper, “Cross-current gas exchange in avian lungs: effects of reversed parabronchial air flow in ducks,” Respiration Physiology, vol. 16, no. 3, pp. 304–312, 1972.
[6]
P. Scheid, “Mechanisms of gas exchange in bird lungs,” Reviews of Physiology Biochemistry and Pharmacology, vol. 86, pp. 137–186, 1979.
[7]
P. Scheid, H. Slama, and H. Willmer, “Volume and ventilation of air sacs in ducks studied by inert gas wash out,” Respiration Physiology, vol. 21, no. 1, pp. 19–36, 1974.
[8]
J. N. Maina and J. D. Woodward, “Three-dimensional serial section computer reconstruction of the arrangement of the structural components of the parabronchus of the Ostrich, Struthio camelus lung,” Anatomical Record, vol. 292, no. 11, pp. 1685–1698, 2009.
[9]
J. D. Woodward and J. N. Maina, “Study of the structure of the air and blood capillaries of the gas exchange tissue of the avian lung by serial section three-dimensional reconstruction,” Journal of Microscopy, vol. 230, pp. 84–93, 2008.
[10]
A. Makanya, A. Anagnostopoulou, and V. Djonov, “Development and remodeling of the vertebrate blood-gas barrier,” BioMed Research International, vol. 2013, Article ID 101597, 15 pages, 2013.
[11]
J. N. Maina, “Structure, function and evolution of the gas exchangers: comparative perspectives,” Journal of Anatomy, vol. 201, no. 4, pp. 281–304, 2002.
[12]
M. R. Fedde, “Relationship of structure and function of the avian respiratory system to disease susceptibility,” Poultry Science, vol. 77, no. 8, pp. 1130–1138, 1998.
[13]
P. Scheid, “Estimation of effective parabronchial gas volume during intermittent ventilatory flow: theory and application in the duck,” Respiration Physiology, vol. 32, no. 1, pp. 1–14, 1978.
[14]
R. C. Lasewski, “Respiration function in birds,” in Avian Biology, D. S. Farner, J. R. King, and K. C. Parkes, Eds., pp. 287–343, Academic press, New York, NY, USA, 1972.
[15]
A. N. Makanya, Y. El-Darawish, B. M. Kavoi, and V. Djonov, “Spatial and functional relationships between air conduits and blood capillaries in the pulmonary gas exchange tissue of adult and developing chickens,” Microscopy Research and Technique, vol. 74, no. 2, pp. 159–169, 2011.
[16]
A. N. Makanya and V. G. Djonov, “Parabronchial angioarchitecture in developing and adult chickens,” Journal of Applied Physiology, vol. 106, no. 6, pp. 1959–1969, 2009.
[17]
T. Nasu, “Scanning electron microscopic study on the microarchitecture of the vascular system in the pigeon lung,” Journal of Veterinary Medical Science, vol. 67, pp. 1071–1074, 2005.
[18]
E. R. Schachner, J. R. Hutchinson, and C. Farmer, “Pulmonary anatomy in the Nile crocodile and the evolution of unidirectional airflow in Archosauria,” PeerJ, vol. 1, article e60, 2013.
[19]
P. Scheid, H. Slama, and J. Piiper, “Mechanisms of unidirectional flow in parabronchi of avian lungs: measurements in duck lung preparations,” Respiration Physiology, vol. 14, no. 1-2, pp. 83–95, 1972.
[20]
A. R. Akester, “The comparative anatomy of the respiratory pathways in the domestic fowl (Gallus domesticus), pigeon (Columbia livia) and domestic duck (Anas platyrhyncha),” Journal of anatomy, vol. 94, pp. 487–505, 1960.
[21]
H. R. Duncker, “The lung air sac system of birds. A contribution to the functional anatomy of the respiratory apparatus,” Ergebnisse der Anatomie und Entwicklungsgeschichte, vol. 45, no. 6, pp. 7–171, 1971.
[22]
J. Lopez, E. Gomez, and P. Sesma, “Anatomical study of the bronchial system and major blood vessels of the chicken lung (Gallus gallus) by means of a three-dimensional scale model,” Anatomical Record, vol. 234, no. 2, pp. 240–248, 1992.
[23]
D. O. Kuethe, “Fluid mechanical valving of air flow in bird lungs,” Journal of Experimental Biology, vol. 136, pp. 1–12, 1988.
[24]
R. Bulacio, M. H. Hazelhoff, and A. M. Torres, “Renal expression and function of oat1 and oat3 in rats with vascular calcification,” Pharmacology, vol. 90, pp. 66–77, 2012.
[25]
E. J. Eliason, “Alligators, like birds, breathe one way only,” The Journal of Experimental Biology, vol. 213, no. 11, 2010.
[26]
A. N. Makanya, R. Hlushchuk, and V. Djonov, “The pulmonary blood-gas barrier in the avian embryo: inauguration, development and refinement,” Respiratory Physiology & Neurobiology, vol. 178, pp. 30–38, 2011.
[27]
F. L. Powell, M. R. Fedde, R. K. Gratz, and P. Scheid, “Ventilatory response to CO2 in birds. I. Measurements in the unanesthetized duck,” Respiration Physiology, vol. 35, no. 3, pp. 349–359, 1978.