Functional Design of the Mature Avian Respiratory System

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Abstract

The avian respiratory system is structurally exceptionally complex and functionally remarkably efficient. It comprises a lung that serves as the gas exchanger and air sacs that function as the ventilators. Topographically, the lung is located between two sets of air sacs, namely, a cranial and a caudal group. They continuously ventilate the lung in a craniocaudal direction by synchronized activities. The air sacs are delicate, transparent and compliant structures. Since they are avascular, they play no part in gas exchange. The lung is attached to the ribs and the vertebrae on the dorsolateral aspects and to the horizontal septum on the ventral one. It renders the lung practically rigid. This allows the exchange tissue (parenchyma) to be very intensely subdivided, resulting in minuscular terminal respiratory units, the air capillaries. That way, the respiratory surface area is increased. The bronchial system of the avian lung forms a continuous loop that consists of a three-tier system of airways. These are a primary bronchus, secondary bronchi and tertiary bronchi (parabronchi). The arrangement of the airways and the blood vessels in the lung determines where and how air and blood are distributed and the respiratory media exposed to each other for gas exchange. A cross-current system is formed by the essentially perpendicular disposition between the flow of air in the parabronchial lumen and that of venous blood in the exchange tissue; an auxiliary counter-current arrangement is formed by the relationship between the direction of the flow of air in the air capillaries and that of the blood in the blood capillaries, and a multicapillary serial arterialization system consists of the sequential interaction between the blood in the blood capillaries and the air in the capillaries in the parabronchus. In addition to these features, the bird lung has large capillary blood volume, extensive surface respiratory surface area and particularly thin blood-gas (tissue) barrier. The morphological specializations and the adaptive physiological features such as large tidal volume and cardiac output all together explain the exceptional gas exchange efficiency of the avian respiratory system, supporting the high metabolic capacity and energetic lifestyles of birds.

Keywords

Birds Lung Air sacs Gas exchange Parabronchus Air capillaries Blood capillaries 
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Notes

Acknowledgements

The preparation of this work was supported by the National Research Foundation (NRF) of South Africa. The views and opinions expressed here are, however, mine and not those of the NRF. To the many people that have collaborated with me over the years, I am eternally grateful for their ideas shared with me, giving me their time unreservedly, and particularly for their continued friendship.

References

  1. Abdalla MA. The blood supply to the lung. In: King AS, McLelland J, editors. Form and function in birds, vol. 4. London: Academic; 1989. p. 281–306.Google Scholar
  2. Abdalla MA, King AS. The functional anatomy of the pulmonary circulation of the domestic fowl. Respir Physiol. 1975;23:267–90.PubMedCrossRefGoogle Scholar
  3. Abdalla MA, King AS. Pulmonary arteriovenous anastomoses in the avian lung: do they exist? Respir Physiol. 1976a;27:187–91.PubMedCrossRefGoogle Scholar
  4. Abdalla MA, King AS. The functional anatomy of the bronchial circulation of the domestic fowl. J Anat. 1976b;121:537–50.PubMedPubMedCentralGoogle Scholar
  5. Abdalla MA, King AS. The avian bronchial arteries: species variations. J Anat. 1977;123:697–704.PubMedPubMedCentralGoogle Scholar
  6. Abdalla MA, Maina JN, King AS, King DZ, Henry J. Morphometrics of the avian lung. 1. The domestic fowl, Gallus domesticus. Respir Physiol. 1982;47:267–78.PubMedCrossRefGoogle Scholar
  7. Alonso C, Waring A, Zasadzinki JA. Keeping lung surfactant where it belongs: protein regulation of two-dimensional viscosity. Biophys J. 2005;89:266–73.PubMedPubMedCentralCrossRefGoogle Scholar
  8. Aschoff J, Pohl H. Rhythmic variations in energy metabolism. Fed Proc. 1970;29:1541–52.PubMedGoogle Scholar
  9. Bartholomew GA, Lighton JRB. Oxygen consumption during hover-feeding in free-ranging Anna hummingbirds. J Exp Biol. 1986;123:191–9.PubMedGoogle Scholar
  10. Bernhard W, Gerbert A, Vieten G, Rau G, Hollfield JM, Postle AD, Frenhorst J. Pulmonary surfactant in birds: coping with surface tension in a tubular lung. Am J Physiol Regul Intergr Comp Physiol. 2001;281:R327–37.Google Scholar
  11. Bernhard W, Haslam PL, Floros J. From birds to humans: new concepts on airways relative to alveolar surfactant. Am J Respir Cell Mol Biol. 2004;30:6–11.PubMedCrossRefGoogle Scholar
  12. Bezuidenhout AJ, Groenewald HB, Soley JT. An anatomical study of the respiratory air sacs in ostriches. Onderstepoort J Vet Res. 1999;66:317–25.PubMedGoogle Scholar
  13. Biggs PM, King AS. A new experimental approach to the problem of the air pathway within the avian lung. J Physiol Lond. 1957;138:282–99.PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bishop CM, Spivey RJ, Hawkes LA, Batbayar N, Chua B, Frappell PB, Milsom WK, et al. The roller coaster flight strategy of bar-headed geese conserves energy during Himalayan migrations. Science. 2015;347:250–4.PubMedCrossRefGoogle Scholar
  15. Brackenbury JH. Air flow dynamics in the avian lung as determined by direct and indirect methods. Respir Physiol. 1971;13:319–29.PubMedCrossRefGoogle Scholar
  16. Brackenbury JH, Akester AR. A model of the capillary zone of the avian tertiary bronchus. In: Piiper J, editor. Respiratory function in birds, adult and embryonic. Berlin: Springer; 1978. p. 109–63.Google Scholar
  17. Bramwell CD. Aerodynamics of Pteranodon. J Linn Soc Biol. 1971;3:313–28.CrossRefGoogle Scholar
  18. Carlson CW, Beggs EC. Ultrastructure of the abdominal air sac of the fowl. Res Vet Sci. 1973;14:148–50.PubMedGoogle Scholar
  19. Carpenter FL, Paton DC, Hixon MA. Weight gain and adjustment of feeding territory size in migrant hummingbirds. Proc Natl Acad Sci USA. 1983;80:7259–63.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Coiter V. Anatomie Avium. In: Externarum et internarum praecipalium humani corporis partium tabulae atque anatomicae exercitationes observationesque varieae. Norimbergae; 1573. p. 130–3Google Scholar
  21. Constable G. How things work: flight. Alexandria, Virginia: Time Life Books; 1990.Google Scholar
  22. Cook RD, King AS. Observations on the ultrastructure of the smooth muscle and its innervation in the avian lung. J Anat. 1970;106:273–83.PubMedPubMedCentralGoogle Scholar
  23. Cook RD, Vaillant CR, King AS. The structure and innervation of the saccopleural membrane of the domestic fowl, Gallus gallus: an ultrastructural and immunohistochemical study. J Anat. 1987;150:1–9.PubMedPubMedCentralGoogle Scholar
  24. Costa DP, Prince PA. Foraging energetics of grey-headed albatrosses, Diomedea chrysostoma at Bird Island, South Georgia. Ibis. 1987; 129:149–58.Google Scholar
  25. Daniels CB, Lopatkov OV, Orgeig S. Evolution of surface activity related functions of vertebrate pulmonary surfactant. Clin Exp Pharmacol Physiol. 2001;25:716–21.CrossRefGoogle Scholar
  26. Daniels CB, Orgeig S. The comparative biology of pulmonary surfactant: past, present and future. Comp Biochem Physiol A. 2001;129:9–36.CrossRefGoogle Scholar
  27. Daniels CB, Orgeig S, Wood PG, Sullivan LC, Lopatkov AK, Smits AW. The changing state of surfactant lipids: new insights from ancient animals. Am Zool. 1998;38:305–20.CrossRefGoogle Scholar
  28. de Beer G. Archeopteryx lithographica. London: British Museum (Natural History); 1954.Google Scholar
  29. Dubach M. Quantitative analysis of the respiratory system of the house sparrow, budgerigar, and violet-eared hummingbird. Respir Physiol. 1981;46:43–60.PubMedCrossRefGoogle Scholar
  30. Dubois A, Brody AW, Lewis DH, Burgess F. Oscillation mechanics of lungs and chest in man. J Appl Physiol. 1956;8:587–94.PubMedGoogle Scholar
  31. Duncker HR. The lung-air sac system of birds. A contribution to the functional anatomy of the respiratory apparatus. Ergeb Anat Entwicklungsgesch. 1971;45:1–171.Google Scholar
  32. Duncker HR. Structure of the avian lung. Respir Physiol. 1972;14:4–63.CrossRefGoogle Scholar
  33. Duncker HR. Structure of the avian respiratory tract. Respir Physiol. 1974;22:1–34.PubMedCrossRefGoogle Scholar
  34. Duncker HR. Development of the avian respiratory and circulatory systems. In: Piiper J, editor. Respiratory function in birds, adult and embryonic. Berlin: Springer; 1978. p. 260–73.CrossRefGoogle Scholar
  35. Duncker HR. General morphological principles of amniotic lungs. In: Piiper J, editor. Respiratory function in birds, adult and embryonic. Heidelberg: Springer; 1979. p. 1–15.Google Scholar
  36. Duncker HR. Vertebrate lungs: structure, topography and mechanics: a comparative perspective of the progressive integration of respiratory system, locomotor apparatus and ontogenetic development. Respir Physiol Neurobiol. 2004;144:111–24.PubMedCrossRefGoogle Scholar
  37. Duncker HR, Guntert M. The quantitative design of the avian respiratory system: from hummingbird to the mute swan. In: Nachtigall W, editor. BIONA Report No. 3. Stuttgart: Gustav-Fischer; 1985a. p. 361–78.Google Scholar
  38. Duncker HR, Guntert M. Morphometric analysis of the avian respiratory system. In: Duncker HR, Fleischer G, editors. Vertebrate morphology. Stuttgart: Gustav-Fischer; 1985b. p. 383–7.Google Scholar
  39. Egevang C, Stenhouse IJ, Phillips RA, Petersen A, Fox JW, Silk JRD. Tracking of Arctic terns Sterna paradisaea reveals longest animal migration. Proc Natl Acad Sci USA. 2010;107:2078–81.PubMedPubMedCentralCrossRefGoogle Scholar
  40. Farner DS. Some glimpses of comparative avian physiology. Fed Proc. 1970;29:1649–63.PubMedGoogle Scholar
  41. Fedde MR. The structure and gas flow pattern in the avian lung. Poult Sci. 1980;59:2642–53.PubMedCrossRefGoogle Scholar
  42. Fedde MR. Relationship of structure and function of the avian respiratory system to disease susceptibility. Poult Sci. 1998;77:1130–8.PubMedCrossRefGoogle Scholar
  43. Fletcher OJ. Pathology of the avian respiratory system. Poult Sci. 1980;59:2666–79.PubMedCrossRefGoogle Scholar
  44. Foot NJ, Orgeig S, Daniels CB. The evolution of a physiological system: the pulmonary surfactant system in diving mammals. Respir Physiol Neurobiol. 2006;154:118–38.PubMedCrossRefGoogle Scholar
  45. Fujiwara T, Adams FH, Nozaki M, Dermer GB. Pulmonary surfactant phospholipids from Turkey lung: comparison with rabbit lung. Am J Phys. 1970;218:218–25.Google Scholar
  46. Fung YC. Biomechanics: mechanical properties of living tissues. 2nd ed. Berlin: Springer; 1993.CrossRefGoogle Scholar
  47. Gehr P, Mwangi DK, Amman A, Maloiy GMO, Taylor CR, Weibel ER. Design of the mammalian respiratory system. V. Scaling morphometric diffusing capacity to body mass: wild and domestic animals. Respir Physiol. 1981;44:41–86.CrossRefGoogle Scholar
  48. Gehr P, Sehovic S, Burri PH, Classen H, Weibel ER. The lung of shrews: morphometric estimation of diffusion capacity. Respir Physiol. 1980;44:61–86.CrossRefGoogle Scholar
  49. Geiser F. Ontogeny and phylogeny of endothermy and torpor in mammals and birds. Comp Biochem Physiol A Mol Integr Physiol. 2008;150:176–80.PubMedCrossRefGoogle Scholar
  50. Gier HT. The air sacs of the loon. Auk. 1952;69:40–9.CrossRefGoogle Scholar
  51. Grigg GC, Beard LA, Augee ML. The evolution of endothermy and its diversity in mammals and birds. Physiol Biochem Zool. 2004;77:982–97.PubMedCrossRefGoogle Scholar
  52. Groebbels FDV. Bau, Funktion, Lebenserscheinung, Einpassung, vol. 1. Berlin: Gebriider Borntraeger; 1932.Google Scholar
  53. Grubb BR. Cardiac output and stroke volume in exercising ducks and pigeons. J Appl Physiol. 1982;53:203–11.CrossRefGoogle Scholar
  54. Gruson ES. Checklist of birds of the world. London: Collins; 1976.Google Scholar
  55. Hawkes LA, Balachancran S, Batbayar N, Butler PJ, Frappell PB, Milsom WK, Tseveenmyadag S, Newman SH, et al. The trans-Himalayan flights of bar-headed geese (Anser indicus). Proc Natl Acad Sci USA. 2011;108:9516–9.PubMedPubMedCentralCrossRefGoogle Scholar
  56. Henk WG, Haldman JT. Microanatomy of the lung of the bowhead whale Balaena mysticetus. Anat Rec. 1990;226:187–97.PubMedCrossRefGoogle Scholar
  57. Hlastala MP, Berger AJ. Physiology of respiration. 1st ed. New York: Oxford University Press; 1996.Google Scholar
  58. Hlastala MP, Berger AJ. Physiology of respiration. 2nd ed. New York: Oxford University Press; 2001.Google Scholar
  59. Hochachka PW. Comparative intermediary metabolism. In: Prosser CL, editor. Comparative animal physiology. 3rd ed. Philadelphia: Saunders; 1973. p. 212–78.Google Scholar
  60. Holle JP, Heisler N, Scheid P. Blood flow distribution in the bird lung and its controls by respiratory gases. Am J Phys. 1978;234:R146–54.Google Scholar
  61. Hsia CW, Schimtz A, Lambertz M, Perry SF, Maina JN. Evolution of air breathing: oxygen homeostatsis and the transitions from water- to-land and sky. Compr Physiol. 2013;3:849–915.PubMedPubMedCentralGoogle Scholar
  62. Hughes GM, Weibel ER. Morphometry of fish lungs. In: Hughes GM, editor. Respiration of amphibious vertebrates. London: Academic; 1976. p. 213–32.Google Scholar
  63. Hunter P. The nature of flight: the molecules and mechanics of flight in animals. EMBO Rep. 2007;8:813. doi: 10.1038/sj.embor.7401050.Google Scholar
  64. Jammes Y, Bouverot P. Direct PCO2 measurement in the dorsobronchial gas of wake Pekin ducks: evidence for a physiological role of the neopulmo in respiratory gas exchanges. Comp Biochem Physiol. 1975;52A:635–7.CrossRefGoogle Scholar
  65. Jimoh SA, Maina JN. Immuno-localization of type-IV collagen in the blood-gas barrier and the epithelial cell connections of the avian lung. Biol Lett. 2013;9 doi: 10.1098/rsbl.2012.0951.
  66. Jones JH, Effmann EL, Schmidt-Nielsen K. Lung volume changes during respiration in ducks. Respir Physiol. 1985;59:15–25.PubMedCrossRefGoogle Scholar
  67. Juillet A. Recherches anatomiques, embryologiques, histologiques et comparatives sur le poumon des oiseaux. Arch Zool Exp Gen. 1912;IX:207–371.Google Scholar
  68. Karasov WH, Phan D, Diamond JM, Carpenter FL. Food passage and intestinal nutrient absorption in hummingbirds. Auk. 1986;103:453–64.Google Scholar
  69. Kardong KV. Vertebrates: comparative anatomy, function, and evolution. 5th ed. New York: McGraw-Hill; 2009.Google Scholar
  70. Kellog RH. Laws of physics pertaining to gas exchange. In: Farhi LE, Tenney SM, editors. Handbook of physiology, section 3, the respiratory system, vol. IV: gas exchange. Bethesda, MD: American Physiological Society; 1987. P. 13–21.Google Scholar
  71. King AS. Structural and functional aspects of the avian lung and its air sacs. Intern Rev Gen Exp Zool. 1966;2:171–267.CrossRefGoogle Scholar
  72. King JR. Seasonal allocation of time and energy resources in birds. In: Paynter RA, editor. Avian energetics. Cambridge, MA: Nuttall Ornithological Club; 1974. p. 4–85.Google Scholar
  73. King AS. Systema respiratorium. In: Baumel JJ, King AS, Lucas AM, Breazile JE, Evans HE, editors. Nomina anatomica avium. London: Academic; 1979. p. 227–65.Google Scholar
  74. King AS, Atherton JD. The identity of the air sacs of the Turkey (Melleagris gallopavo). Acta Anat. 1970;77:78–91.PubMedCrossRefGoogle Scholar
  75. King AS, King DZ. Avian morphology. In: King AS, McLelland J, editors. Form and function in birds, vol. 1. London: Academic; 1979. p. 1–38.Google Scholar
  76. King AS, Molony V. The anatomy of respiration. In: Bell DF, Freeman BM, editors. Physiology and biochemistry of the domestic fowl, vol. 1. London: Academic; 1971. p. 347–84.Google Scholar
  77. Klika E, Scheuermann DW, De Groodt-Lassel MHA, Bazantova I, Switka A. Anchoring and support system of pulmonary gas exchange tissue in four bird species. Acta Anat. 1997;159:30–41.PubMedCrossRefGoogle Scholar
  78. Köppen U, Yakoview A, Barth R, Kaatz M, Berthold P. Seasonal migrations of four individual bar-headed geese, Anser indicus from Kyrgyzstan followed by satellite telemetry. J Ornithol. 2010;151:703–12.CrossRefGoogle Scholar
  79. Koteja P. The evolution of concepts on the evolution of endothermy in birds and mammals. Physiol Biochem Zool. 2004;77:1043–50.PubMedCrossRefGoogle Scholar
  80. Krebs JR, Harvey PH. Busy doing nothing—efficiently. Nature. 1986;320:18–9.CrossRefGoogle Scholar
  81. Laplace PS. A philosophical essay on probabilities (translated from the 6th French edition by Truscott FW, Emory FL). New York: Wiley; 1902.Google Scholar
  82. Lasiewski RC. The energetics of migrating hummingbirds. Condor. 1962;64:324.CrossRefGoogle Scholar
  83. Lasiewski RC, Dawson WR. A re-examination of the relation between standard metabolic rate and body weight in birds. Condor. 1967;69:13–23.CrossRefGoogle Scholar
  84. Laybourne RC. Collision between a vulture and an aircraft at an altitude of 37,000 ft. Wilson Bull. 1974;86:461–2.Google Scholar
  85. Li J. Processing, stability and interactions of lung surfactant protein C. Stockholm: Karolinska Institutet University Press; 2005.Google Scholar
  86. Locy WA, Larsell O. The embryology of the bird’s lung based on observations of the bronchial tree. Part I. Am J Anat. 1916a;19:447–504.CrossRefGoogle Scholar
  87. Locy WA, Larsell O. The embryology of the bird’s lung based on observations of the domestic fowl. Part II. Am J Anat. 1916b;20:1–44.CrossRefGoogle Scholar
  88. Macklem P, Bouverot P, Scheid P. Measurement of the distensibility of the parabronchi in duck lungs. Respir Physiol. 1979;33:23–35.CrossRefGoogle Scholar
  89. Magnussen H, Willmer H, Scheid P. Gas exchange in the air sacs: contribution to respiratory gas exchange in ducks. Respir Physiol. 1976;26:129–46.PubMedCrossRefGoogle Scholar
  90. Maina JN. Morphometrics of the avian lung. 3. The structural design of the passerine lung. Respir Physiol. 1984;55:291–309.PubMedCrossRefGoogle Scholar
  91. Maina JN. Scanning electron microscopic study of the spatial organization of the air- and blood conducting components of the avian lung (Gallus gallus domesticus). Anat Rec. 1988;222:145–53.PubMedCrossRefGoogle Scholar
  92. Maina JN. The morphometry of the avian lung. In: King AS, McLelland J, editors. Form and function in birds, vol. 4. London: Academic; 1989. p. 307–68.Google Scholar
  93. Maina JN. Morphometries of the avian lung: the structural-functional correlations in the design of lungs of birds. Comp Biochem Physiol. 1993;105:397–410.CrossRefGoogle Scholar
  94. Maina JN. The gas exchangers: structure, function, and evolution of the respiratory processes. Berlin: Springer; 1998.CrossRefGoogle Scholar
  95. Maina JN. What it takes to fly: the novel respiratory structural and functional adaptations in birds and bats. J Exp Biol. 2000a;203:3045–64.PubMedGoogle Scholar
  96. Maina JN. Is the sheet-flow design a ‘frozen core’ (a Bauplan) of the gas exchangers? Comparative functional morphology of the respiratory microvascular systems: illustration of the geometry and rationalization of the fractal properties. Comp Biochem Physiol. 2000b;126A:491–515.CrossRefGoogle Scholar
  97. Maina JN. Some recent advances of the study and understanding of the functional design of the avian lung: morphological and morphometric perspectives. Biol Rev. 2002;77:97–152.PubMedCrossRefGoogle Scholar
  98. Maina JN. A systematic study of the development of the airway (bronchial) system of the avian lung from days 3 to 26 of embryogenesis: a transmission electron microscopic study on the domestic fowl, Gallus gallus variant domesticus. Tissue Cell. 2003a;35:375–91.PubMedCrossRefGoogle Scholar
  99. Maina JN. Developmental dynamics of the bronchial (airway)- and air sac systems of the avian respiratory system from days 3 to 26 of life: a scanning electron microscopic study of the domestic fowl, Gallus gallus variant domesticus. Anat Embryol. 2003b;1207:119–34.CrossRefGoogle Scholar
  100. Maina JN. The design of the lung-air sac system of birds: development, structure, and function. Heidelberg: Springer; 2005.Google Scholar
  101. Maina JN. Development, structure, and function of a novel respiratory organ, the lung-air sac system of birds: to go where no other vertebrate has gone. Biol Rev. 2006;81:545–79.PubMedCrossRefGoogle Scholar
  102. Maina JN. Minutialization at its extreme best! The underpinnings of the remarkable strengths of the air and the blood capillaries of the avian lung: a conundrum. Respir Physiol Neurobiol. 2007a;159:141–5.PubMedCrossRefGoogle Scholar
  103. Maina JN. Spectacularly robust! Tensegrity principle explains the mechanical strength of the avian lung. Respir Physiol Neurobiol. 2007b;155:1–10.PubMedCrossRefGoogle Scholar
  104. Maina JN. Structural and biomechanical properties of the exchange tissue of the avian lung. Anat Rec. 2015a;298:1673–88.CrossRefGoogle Scholar
  105. Maina JN. The design of the avian respiratory system: development, morphology and function. J Ornithol. 2015b;156:41–63.CrossRefGoogle Scholar
  106. Maina JN. Morphological and morphometric properties of the blood-gas barrier: comparative perspectives. In: Makanya AN, editor. The vertebrate blood-gas barrier in health and disease. New York: Springer; 2015c. p. 15–38.CrossRefGoogle Scholar
  107. Maina JN. Pivotal debates and controversies on the structure and function of the avian respiratory system: setting the record straight. Biol Rev. 2016a; doi: 10.1111/brv.12292.PubMedGoogle Scholar
  108. Maina JN. Critical appraisal of some factors pertinent to the functional designs of the gas exchangers. Cell Tissue Res. 2016b; doi: 10.1007/s00441-016-2549-9.PubMedGoogle Scholar
  109. Maina JN, Abdalla MA, King AS. Light microscopic morphometry of the lungs of 19 avian species. Acta Anat. 1982;112:264–70.PubMedCrossRefGoogle Scholar
  110. Maina JN, Howard CV, Scales L. Length densities and maximum diameter distribution of the air capillaries of the paleopulmo and neopulmo region of the avian lung. Acta Stereol. 1983;2:101–7.Google Scholar
  111. Maina JN, Jimoh SA. Structural failures of the blood-gas barrier and the epithelial-epithelial cell connections in the different vascular regions of the lung of the domestic fowl, Gallus gallus variant domesticus, at rest and during exercise. Biol Open. 2013;2:267–76.PubMedPubMedCentralCrossRefGoogle Scholar
  112. Maina JN, Jimoh SA, Hosie M. Implicit mechanistic role of the collagen-, smooth muscle, and elastic tissue components in strengthening the air- and the blood capillaries of the avian lung. J Anat. 2010;217:597–608.PubMedPubMedCentralCrossRefGoogle Scholar
  113. Maina JN, King AS. The thickness of the avian blood-gas barrier: qualitative and quantitative observations. J Anat. 1982;134:553–62.PubMedPubMedCentralGoogle Scholar
  114. Maina JN, King AS. The structural functional correlation in the design of the bat lung. A morphometric study. J Exp Biol. 1984;111:43–63.PubMedGoogle Scholar
  115. Maina JN, King AS. A morphometric study of the lung of a Humboldt penguin (Spheniscus humboldti). Zentralb Vet Med C Anat Histol Embryol. 1987;16:293–7.Google Scholar
  116. Maina JN, King AS. The lung of the emu, Dromaius novaehollandiae: a microscopic and morphometric study. J Anat. 1989;163:67–74.PubMedPubMedCentralGoogle Scholar
  117. Maina JN, King AS, Settle G. An allometric study of the pulmonary morphometric parameters in birds, with mammalian comparison. Phil Trans R Soc. 1989;326B:1–57.CrossRefGoogle Scholar
  118. Maina JN, Nathaniel C. A qualitative and quantitative study of the lung of an ostrich, Struthio camelus. J Exp Biol. 2001;204:2313–30.PubMedGoogle Scholar
  119. Maina JN, Sikiru AJ. Study of stress induced failure of the blood-gas barrier and the epithelial-epithelial cells connections of the lung of the domestic fowl, Gallus gallus variant domesticus after vascular perfusion. Biomed Eng Comput Biol. 2013;5:77–88.PubMedPubMedCentralCrossRefGoogle Scholar
  120. Maina JN, Thomas SP, Dallas DM. A morphometric study of bats of different size: correlations between structure and function of the chiropteran lung. Phil Trans R Soc Lond B. 1991;333:31–50.CrossRefGoogle Scholar
  121. Maina JN, van Gils P. Morphometric characterization of the airway and vascular systems of the lung of the domestic pig, Sus scrofa: comparison of the airway, arterial, and venous systems. Comp Biochem Physiol. 2001;130A:781–98.CrossRefGoogle Scholar
  122. Maina JN, West JB. Thin and strong! The bioengineering dilemma in the structural and functional design of the blood-gas barrier. Physiol Rev. 2005;85:811–44.PubMedCrossRefGoogle Scholar
  123. Maina JN, Woodward JD. Three-dimensional serial section computer reconstruction of the arrangement of the structural components of the parabronchus of the ostrich, Struthio camelus lung. Anat Rec. 2009;291:1685–98.CrossRefGoogle Scholar
  124. Makanya AN, Djonov V. Development and spatial organization of the air conduits in the lung of the domestic fowl, Gallus gallus variant domesticus. Microsc Res Tech. 2008;71:689–702.PubMedCrossRefGoogle Scholar
  125. Makanya AN, El-Darawish Y, Kavoi BM, Djonov V. Spatial and functional relationships between air conduits and blood capillaries in the pulmonary gas exchange tissue of adult and developing chickens. Microsc Res Tech. 2011;74:159–69.PubMedCrossRefGoogle Scholar
  126. Makanya AN, Kavoi BM, Djonov V. Three dimensional structure and disposition of the air conducting and gas exchange conduits of the avian lung: the domestic duck (Cairina moschata). ISRN Anat. 2014. Doi:org/ 10.1155/2014/621982.
  127. Marshall AJ. Cited in King and King 1979. Avian morphology. In: King AS, McLelland J, editors. Form and function in birds, vol. 1. London: Academic; 1962. P. 1–38.Google Scholar
  128. Martinez del Rio C. Dietary, phylogenetic and ecological correlates of intestinal sucrase and maltase activity in birds. Physiol Zool. 1990;63:987–1011.Google Scholar
  129. Mathieu-Costello O, Szewczak JM, Logermann RB, Agey PJ. Geometry of blood-tissue exchange in bat flight muscle compared with bat hindlimb and rat soleus muscle. Am J Phys. 1992;262:R955–65.Google Scholar
  130. McLelland J. Anatomy of the lungs and air sacs. In: King AS, McLelland J, editors. Form and function in birds, vol. 4. London: Academic; 1989. p. 221–79.Google Scholar
  131. Meban C. Thicknesses of the air-blood barriers in vertebrate lungs. J Anat. 1980;131:299–307.PubMedPubMedCentralGoogle Scholar
  132. Miller DN, Bondurant S. Surface characteristics of vertebrate lung extracts. J Appl Physiol. 1961;16:1075–7.PubMedGoogle Scholar
  133. Miura T, Hartmann D, Kinboshi M, Komada M, Ishibashi M, Shiota K. The cyst-branch difference in developing chick lung results from a different morphogen diffusion coefficient. Mech Dev. 2009;126:160–72.PubMedCrossRefGoogle Scholar
  134. Morony JJ, Bock WJ, Farrand J. Reference list of the birds of the world. New York: American Museum of Natural History, Department of Ornithology; 1975.Google Scholar
  135. Moura RS, Coutinho-Borges JP, Pacheco AP, daMota PO, Correia-Pinto J. FGF signaling pathway in the developing chick lung: expression and inhibition sites. PLoS One. 2011;6(3):e17660. doi: 10.1371/journal.pone.0017660.PubMedPubMedCentralCrossRefGoogle Scholar
  136. Moura RS, Silva-Gonçalves C, Vaz-Cunha P. Expression analysis of Shh signaling members in early stages of chick lung development. Histochem Cell Biol. 2016; doi: 10.1007/s00418-016-1448-1.PubMedGoogle Scholar
  137. Müller B. The air sacs of the pigeon. Smithson misc Colls. 1908;50:365–414.Google Scholar
  138. Nudds RL, Bryant DM. The energy cost of short flights in birds. J Exp Biol. 2000;203:1561–82.PubMedGoogle Scholar
  139. Ostrom JH. The origin of birds. Annu Rev Earth Planet Sci. 1975;3:55–77.CrossRefGoogle Scholar
  140. Pattle RE. Lung surfactant and lung lining in birds. In: Piiper J, editor. Respiratory function in birds, adult and embryonic. Berlin: Springer; 1978. p. 23–32.CrossRefGoogle Scholar
  141. Perry SF. Quantitative anatomy of the lungs of the red-eared turtle, Pseudemys script elegans. Respir Physiol. 1978;35:245–62.PubMedCrossRefGoogle Scholar
  142. Perry SF. Mainstreams in the evolution of vertebrate respiratory structures. In: King AS, McLelland J, editors. Form and function in birds, vol. V. London: Academic; 1989a. p. 1–67.Google Scholar
  143. Perry SF. Structure and function of the reptilian respiratory system. In: Wood SC, editor. Comparative pulmonary physiology: current concepts. New York: Marcel Dekker; 1989b. p. 193–236.Google Scholar
  144. Perry SF. Gas exchange strategies in reptiles and the origin of the avian lung. In: Wood SC, Weber RE, Hargens AR, Millard RW, editors. Physiological adaptations in vertebrates: respiration, circulation, and metabolism. New York: Marcel Dekker; 1992. p. 149–67.Google Scholar
  145. Piiper J. Origin of carbon dioxide in caudal air sacs of birds. In: Piiper J, editor. Respiratory function in birds, adult and embryonic. Berlin: Springer; 1978. p. 221–48.CrossRefGoogle Scholar
  146. Piiper J, Scheid P. Gas exchange in the avian lung: model and experimental evidence. In: Bolis L, Schmidt-Nielsen K, Maddrell SHP, editors. Comparative physiology. Amasterdam: Elsevier; 1973. p. 161–85.Google Scholar
  147. Pough FH, Heiser JB, McFarland WN. Vertebrate life. 3rd ed. New York: Macmillan; 1989.Google Scholar
  148. Powell FL. Respiration. In: Abs M, editor. Physiology and behaviours of the pigeon. New York: Academic; 1983. p. 73–95.Google Scholar
  149. Powell FL. Respiration. In: Whittow GC, editor. Sturkie’s Avian Physiology. 5th ed. San Diego, CA: Academic; 2000. p. 233–64.Google Scholar
  150. Powell FL, Hastings RH, Mazzone RW. Pulmonary vascular resistance during unilateral pulmonary artery occlusion in ducks. Am J Phys. 1985;249:R34–43.Google Scholar
  151. Powell FL, Scheid P. Physiology of gas exchange in the avian respiratory system. In: King AS, McLelland J, editors. Form and function of the avian lung, vol. 4. London: Academic; 1989. p. 393–437.Google Scholar
  152. Powers DR, Naggy KA. Field metabolic rate and food consumption by free-living Anna’s hummingbirds (Calypte anna). Physiol Zool. 1988;61:500–6.CrossRefGoogle Scholar
  153. Radu C, Radu L. Le dispositif vasculaire du poumon chez les oiseaux domestiques (coq, dindon, oie, canard). Rev Med Vet. 1971;122:1219–26.Google Scholar
  154. Rawal UM. Nerves in the avian air sacs. Pavo. 1976;14:57–60.Google Scholar
  155. Romanoff AL. The avian embryo. New York: Macmillan; 1960.Google Scholar
  156. Scheid P. Mechanisms of gas exchange in bird lungs. Rev Physiol Biochem Pharmacol. 1979;86:137–86.PubMedGoogle Scholar
  157. Scheid P. The use of models in physiological studies. In: Feder ME, Bennett AF, Burggrenn WW, Huey RB, editors. New direction in ecological physiology. Cambridge: Cambridge University Press; 1987. p. 275–88.Google Scholar
  158. Scheid P, Piiper J. Cross-currrent gas exchange in the avian lungs: effects of reversed parabronchial air flow in ducks. Respir Physiol. 1972;16:304–12.PubMedCrossRefGoogle Scholar
  159. Scheid P, Piiper J. Respiratory mechanics and air flow in birds. In: King AS, McLelland J, editors. Form and function in birds, vol. 4. London: Academic; 1989. p. 364–91.Google Scholar
  160. Scheuermann DW, Klika E, Lasseel DG, Bazantova I, Switka A. An electron microscopic study of the parabronchial epithelium in the mature lung of four bird species. Anat Rec. 1997;249:213–25.PubMedCrossRefGoogle Scholar
  161. Scheuermann DW, Klika E, Lasseel DG, Bazantova I, Switka A. Lamellar inclusions and trilaminar substance in the parabronchial epithelium of the quail (Coturnix coturnix). Ann Anat. 2000;182:221–33.PubMedCrossRefGoogle Scholar
  162. Scott GR, Hawkes LA, Frappel PB, Butler PJ, Bishop CM, Milsom WK. How bar-headed geese fly over the Himalayas. Physiology. 2014;30:107–15.CrossRefGoogle Scholar
  163. Seeherman HJ, Taylor CR, Maloiy GMO, Armstrong RB. Design of the mammalian respiratory system. II. Measuring maximum aerobic capacity. Respir Physiol. 1981;44:11–23.PubMedCrossRefGoogle Scholar
  164. Spragg RS. Surfactant for acute lung injury. Am J Respir Cell Mol Biol. 2007;37:377–8.PubMedCrossRefGoogle Scholar
  165. Stanislaus M. Untersuchungen an der Kolibrilunge. Z Morphol Tiere. 1937;33:261–89.CrossRefGoogle Scholar
  166. Suarez RK. Hummingbird flight: sustaining the highest mass-specific metabolic rates among vertebrates. Experientia. 1992;48:565–70.PubMedCrossRefGoogle Scholar
  167. Suarez RK, Brown GS, Hochachka PW. Mitochondrial respiration in hummingbird muscles. Am J Phys. 1986;251:R537–42.Google Scholar
  168. Suarez RK, Lighton JRB, Brown GS, Mathieu-Costello O. Mitochondrial respiration in hummingbird flight muscles. Proc Natl Acad Sci USA. 1991;87:9207–10.CrossRefGoogle Scholar
  169. Thomas SP. The physiology of bat flight. In: Fenton MB, Racey P, Rayner JMV, editors. Recent advances in the study of bats. Cambridge: Cambridge University Press; 1987. p. 75–99.Google Scholar
  170. Tobalske BW, Hedrik TL, Dial KP, Biewener AA. Comparative power curves in bird flight. Nature. 2003;421:363–6.PubMedCrossRefGoogle Scholar
  171. Trampel DW, Fletcher OJ. Ring-stabilizing technique for collection of avian air sacs. Am J Vet Res. 1980;14:1730–4.Google Scholar
  172. Tucker V. Respiratory physiology of house sparrows in relation to high altitude flight. J Exp Biol. 1968;48:55–66.PubMedGoogle Scholar
  173. Tucker VA. Energetics of natural avian flight. In: Paynter RA, editor. Avian energetics. Cambridge, MA: Nuttall Ornithological Club; 1974. p. 298–333.Google Scholar
  174. Tzschentke B, Rumpf M. Embryonic development of endothermy. Respir Physiol Neurobiol. 2011;178:97–107.PubMedCrossRefGoogle Scholar
  175. Videler JJ. Avian flight. Oxford: Oxford University Press; 2006.CrossRefGoogle Scholar
  176. Vos HJ. Über das Fehlen der rekurrenten Bronchien beim Pinguin und bei den Reptilien. Zool Anz. 1937;117:176–81.Google Scholar
  177. Walsh C, McLelland J. The ultrastructure of the avian extrapulmonary respiratory epithelium. Acta Anat. 1974;89:412–22.PubMedCrossRefGoogle Scholar
  178. Ward S, Bishop CM, Woakes AJ, Butler PJ. Heart rate and the rate of oxygen consumption of flying and walking barnacle geese (Branta leucopsis) and bar-headed geese (Anser indicus). J Exp Biol. 2002;205:47–3356.Google Scholar
  179. Watson RR, Fu Z, West JB. Morphometry of the extremely thin pulmonary blood-gas barrier in the chicken lung. Am J Physiol Lung Cell Mol Physiol. 2007;292:L769–77.PubMedCrossRefGoogle Scholar
  180. Watson RR, Fu Z, West JB. Minimal distensibility of pulmonary capillaries in avian lungs compared with mammalian lungs. Respir Physiol Neurobiol. 2008;160:208–14.PubMedCrossRefGoogle Scholar
  181. Weibel ER. Morphometry of the human lung. Berlin: Springer; 1963.CrossRefGoogle Scholar
  182. Weibel ER. Morphological basis of the alveolar-capillary gas exchange. Physiol Rev. 1973;53:419–95.PubMedGoogle Scholar
  183. Weibel ER. The pathways for oxygen. Harvard, MA: Harvard University Press; 1984.Google Scholar
  184. Weibel ER, Knight BW. A morphometric study on the thickness of the pulmonary air-blood barrier. J Cell Biol. 1964;21:367–84.PubMedPubMedCentralCrossRefGoogle Scholar
  185. Wells DJ. Muscle performance in hovering hummingbirds. J Exp Biol. 1993;178:39–57.Google Scholar
  186. Welty JC. The life of birds. 2nd ed. Philadelphia: Saunders; 1979.Google Scholar
  187. West NH, Bamford OS, Jones DR. A scanning electron microscope study of the microvasculature of the avian lung. Cell Tissue Res. 1977;176:553–64.PubMedCrossRefGoogle Scholar
  188. West JB, Fu Z, Deerinck TJ, Mackey MR, Obayashi JT, Ellsman MH. Structure-function studies of blood- and air capillaries in chicken lung using 3-D electron microscopy. Respir Physiol Neurobiol. 2010;170:202–9.PubMedCrossRefGoogle Scholar
  189. West JB, Watson RR, Fu Z. The honeycomb-like structure of the bird lung allows a uniquely thin blood-gas barrier. Respir Physiol Neurobiol. 2006;152:115–8.PubMedCrossRefGoogle Scholar
  190. West JB, Watson RR, Fu Z. Major differences in the pulmonary circulation between birds and mammals. Respir Physiol Neurobiol. 2007a;157:382–90.PubMedCrossRefGoogle Scholar
  191. West JB, Watson RR, Fu Z. Support of pulmonary capillaries in avian lung: letter to the editor. Respir Physiol Neurobiol. 2007b;159:146.PubMedPubMedCentralCrossRefGoogle Scholar
  192. West JB, Watson RR, Fu Z. The human lung: did evolution get it wrong? Eur Respir J. 2007c;29:11–7.PubMedCrossRefGoogle Scholar
  193. West B, Zhou BW. Did chickens go North? New evidence for domestication. J Archeol Sci. 1988;15:515–33.CrossRefGoogle Scholar
  194. Wetherbee DK. Air sacs in the English sparrow. Auk. 1951;68:242–4.CrossRefGoogle Scholar
  195. Wigglesworth VB. The principles of insect physiology. 7th ed. London: Chapman & Hall; 1972.Google Scholar
  196. Woodward JD, Maina JN. A 3-D digital reconstruction of the components of the gas exchange tissue of the lung of the Muscovy duck, Cairina moschata. J Anat. 2005;206:477–92.PubMedPubMedCentralCrossRefGoogle Scholar
  197. Woodward JD, Maina JN. Study of the structure of the air- and the blood capillaries of the gas exchange tissue of the avian lung by serial section three-dimensional reconstruction. J Microsc. 2008;230:84–93.PubMedCrossRefGoogle Scholar
  198. Yalden DW, Morris PA. The lives of bats. New York: The New York Times; 1975.Google Scholar
  199. Yapp WB. The life and organization of birds. London: Edward Arnold; 1970.Google Scholar
  200. Zuo YY, Veldhuizen RA, Neumann AW, Ptersen NO, Possmeyer F. Current perspectives in pulmonary surfactant inhibition, enhancement and evaluation. Biochim Biophys Acta. 2008;1778:1947–77.PubMedCrossRefGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of ZoologyUniversity of JohannesburgJohannesburgSouth Africa

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