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Journal of Ornithology

, Volume 156, Supplement 1, pp 41–63 | Cite as

The design of the avian respiratory system: development, morphology and function

  • John N. Maina
Review

Abstract

The avian respiratory apparatus is separated into a gas exchanger (the lung) and ventilators (the air sacs). Synchronized bellows-like movements of the cranial and caudal air sacs ventilate the lung continuously and unidirectionally in a caudocranial direction. With the lungs practically rigid, after their insertion into the ribs and the vertebrae and on attaching to the membranous horizontal septum, surface tension is not a constraining factor to the intensity that the gas exchange tissue can subdivide. Delicate, transparent, capacious and avascular, the air sacs are not directly involved in gas exchange. The airway system comprises of a three-tiered system of passageways, namely a primary bronchus, the secondary bronchi and the tertiary bronchi (parabronchi). The crosscurrent system is formed by the perpendicular arrangement between the mass (convective) air flow in the parabronchial lumen and the centripetal (inward) flow of the venous blood in the exchange tissue; the countercurrent system consists of the centrifugal (outward) flow of air from the parabronchial lumen into the air capillaries and the centripetal (inward) flow of blood in the blood capillaries, and; the multicapillary serial arterialization system is formed by the blood capillaries and the air capillaries where venous blood is oxygenated in succession at the infinite number of points where the respiratory units contact exchange tissue. Together with the aforementioned systems, features like large capillary blood volume, extensive respiratory surface area and thin blood-gas barrier accord high pulmonary diffusing capacity of O2 that supports the high metabolic capacities and energetic lifestyles of birds.

Keywords

Birds Lung Air sacs Respiration Development Flight Oxygen 

Notes

Acknowledgments

I am grateful to the National Research Foundation (NRF) of South Africa for funding the preparation of this work and the many colleagues who have collaborated with me over the years. I wish to thank the Organizing Committee of the 26th International Ornithological Congress, held in Tokyo (Japan) in August 2014, for inviting me to give a talk at the conference. This paper is based on that presentation. I would also like to thank two anonymous referees for suggestions and comments which greatly helped improve the manuscript.

References

  1. Abdalla MA (1989) The blood supply to the lung. In: King AS, McLelland J (eds) Form and function in birds, vol 4. Academic Press, London, pp 281–306Google Scholar
  2. Abdalla MA, King AS (1975) The functional anatomy of the pulmonary circulation of the domestic fowl. Respir Physiol 23:267–290PubMedCrossRefGoogle Scholar
  3. Abdalla MA, King AS (1976a) Pulmonary arteriovenous anastomoses in the avian lung: do they exist? Respir Physiol 27:187–191PubMedCrossRefGoogle Scholar
  4. Abdalla MA, King AS (1976b) The functional anatomy of the bronchial circulation of thedomestic fowl. J Anat 121:537–550PubMedPubMedCentralGoogle Scholar
  5. Abdalla MA, King AS (1977) The avian bronchial arteries: species variations. J Anat 123:697–704PubMedPubMedCentralGoogle Scholar
  6. Abdalla MA, Maina JN, King AS, King DZ, Henry J (1982) Morphometrics of the avian lung. 1. The domestic fowl, Gallus domesticus. Respir Physiol 47:267–278PubMedCrossRefGoogle Scholar
  7. Aschoff J, Pohl H (1970) Rhythmic variations in energy metabolism. Fed Proc 29:1541–1552PubMedGoogle Scholar
  8. Banzett RB, Nations CS, Wang N, Butler JP, Lehr JL (1992) Mechanical interdependence of wing beat and breathing in starlings. Respir Physiol 89:27–36PubMedCrossRefGoogle Scholar
  9. Black CP, Tenney SM (1980) Oxygen transport during progressive hypoxia in high altitude and sea level water-fowl. Respir Physiol 39:217–239PubMedCrossRefGoogle Scholar
  10. Bramwell CD (1971) Aerodynamics of Pteranodon. J Linn Soc Biol 3:313–328CrossRefGoogle Scholar
  11. Brown RE, Kovacs CE, Butler JP, Wang N, Lehr J, Banzett RB (1995) The avian lung: is there an aerodynamic expiratory valve? J Exp Biol 198:2349–2357PubMedGoogle Scholar
  12. Chen WT, Chen JM, Mueller SC (1986) Coupled expression and colocalization of 140 K cell adhesion molecules, fibronectin, and laminin during morphogenesis and cytodifferentiation of chick lung cells. J Cell Biol 103:1073–1090PubMedCrossRefGoogle Scholar
  13. Coitier V (1573) Cited by Campana (1875) Anatomia avium. In: Externum et internarum praecipalium humani corporis partium tabulae arque anatomicae exercitationes. Nuremberg, pp 1–253Google Scholar
  14. Cook RD, Vaillant CR, King AS (1987) The structure and innervation of the saccopleural membrane of the domestic fowl, Gallus gallus: an ultrastructural and immunohistochemical study. J Anat 150:1–9PubMedPubMedCentralGoogle Scholar
  15. De Beer G (1954) Archeopteryx lithographica. British Museum of Natural History, LondonGoogle Scholar
  16. Del Corral JPD (1995) Anatomy and histology of the lung and air sacs of birds. In: Pastor LM (ed) Histology, ultrastructure and immunohistochemistry of the respiratory organs in non-mammalian vertebrates. Publicaciones de la Universitatd de University of Murcia, Murcia (Spain), pp 179–233Google Scholar
  17. Dubach M (1981) Quantitative analysis of the respiratory system of the house sparrow, budgerigar, and violet-eared hummingbird. Respir Physiol 46:43–60PubMedCrossRefGoogle Scholar
  18. Dumont ER (2010) Bone density and the lightweight skeletons of birds. Proc R Soc B 277:2193–2198. doi: 10.1098/rspb.2010.0117 PubMedPubMedCentralCrossRefGoogle Scholar
  19. Duncker HR (1971) The lung-air sac system of birds. A contribution to the functional anatomy of the respiratory apparatus. Adv Anat Embryol Cell Biol 45:1–171Google Scholar
  20. Duncker HR (1972) Structure of the avian lung. Respir Physiol 14:4–63CrossRefGoogle Scholar
  21. Duncker HR (1974) Structure of the avian respiratory tract. Respir Physiol 22:1–34PubMedCrossRefGoogle Scholar
  22. Duncker H-R (1978) Development of the avian respiratory and circulatory systems. In: Piiper J (ed) Respiratory function in birds, adult and embryonic. Springer, Berlin, pp 260–273CrossRefGoogle Scholar
  23. Duncker HR, Guntert M (1985a) The quantitative design of the avian respiratory system: from hummingbird to the mute swan. In: Nachtigall W (ed) BIONA report No. 3. Gustav-Fischer, Stuttgart, pp 361-378Google Scholar
  24. Duncker HR, Guntert M (1985b) Morphometric analysis of the avian respiratory system. In: Duncker HR, G Fleischer G (eds) Vertebrate morphology. Gustav-Fischer, Stuttgart, pp 383–387Google Scholar
  25. Elkins N (1983) Weather and bird behaviour. T and AD Poyser, Stoke on TrentGoogle Scholar
  26. Ellington CE (1999) Limitations of animal flight performance. J Exp Biol 160:71–91Google Scholar
  27. Farjado RJ, Hernandez E, O’Connor PM (2007) Postcranial skeletal pneumaticity: a case study in the use of quantitative microCT to assess vertebral structure in birds. J Anat 211:138–147. doi: 10.1111/j.1469-7580.2007.00749.x CrossRefGoogle Scholar
  28. Farner DS (1970) Some glimpses of comparative avian physiology. Fed Proc 29:1649–1663PubMedGoogle Scholar
  29. Fedde MR (1980) The structure and gas flow pattern in the avian lung. Poult Sci 59:2642–2653PubMedCrossRefGoogle Scholar
  30. Fletcher OJ (1980) Pathology of the avian respiratory system. Poult Sci 59:2666–2679PubMedCrossRefGoogle Scholar
  31. Gehr P, Mwangi DK, Amman A, Maloiy GMO, Taylor CR, Weibel ER (1981) Design of the mammalian respiratory system. V. Scaling morphometric pulmonary diffusing capacity to body mass: wild and domestic animals. Respir Physiol 44:61–86PubMedCrossRefGoogle Scholar
  32. Goldin GV, Opperman LA (1980) Induction of supernumerary tracheal buds and the stimulation of DNA synthesis in the embryonic chick lung and trachea by epidermal growth factor. J Embryol Exp Morphol 60:235–243PubMedGoogle Scholar
  33. Grubb BR (1982) Cardiac output and stroke volume in exercising ducks and pigeons. J Appl Physiol 53:203–211CrossRefGoogle Scholar
  34. Gruson ES (1976) Checklist of birds of the world. William Collins, LondonGoogle Scholar
  35. Hacohen N, Kramer S, Sutherland D, Hiromi Y, Krasnow M (1998) Sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92:253–263PubMedCrossRefGoogle Scholar
  36. Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morph 88:49–92PubMedCrossRefGoogle Scholar
  37. Hogg DA (1984) The distribution of pneumatisation in the skeleton of the adult domestic fowl. J Anat 138:617–629PubMedPubMedCentralGoogle Scholar
  38. Holt EA, Miller SW (2011) Bioindicators: using organisms to measure environmental impacts. Nature Education Knowledge 3:8Google Scholar
  39. Jones AW, Radnor CJP (1972a) The development of the chick tertiary bronchus. I. general development and the mode of production of the osmiophilic inclusion body. J Anat 113:303–324PubMedPubMedCentralGoogle Scholar
  40. Jones AW, Radnor CJP (1972b) The development of the chick tertiary bronchus. II. The origin of the surface lining system. J Anat 113:325–340PubMedPubMedCentralGoogle Scholar
  41. Jones JH, Effmann EL, Schmidt-Nielsen K (1985) Lung volume changes during respiration in ducks. Respir Physiol 59:15–25PubMedCrossRefGoogle Scholar
  42. King AS (1966) Structural and functional aspects of the avian lung and its air sacs. Intern Rev Gen Exp Zool 2:171–267CrossRefGoogle Scholar
  43. King JR (1974) Seasonal allocation of time and energy resources in birds. In: Paynter RA (ed) Avian energetics. Nuttal Ornithological Club, Cambridge (MA), pp 4–85Google Scholar
  44. King AS (1979) Systema respiratorium. In: Baumel JJ, King AS, Lucas AM, Breazile JE, Evans HE (eds) Nomina anatomica avium. Academic Press, London, pp 227–265Google Scholar
  45. King AS, Molony V (1971) The anatomy of respiration. In: Bell DF, Freeman BM (eds) Physiology and biochemistry of the domestic fowl, vol 1. Academic Press, London, pp 347–384Google Scholar
  46. Lasiewski RC, Dawson WR (1967) A re-examination of the relation between standard metabolic rate and body weight in birds. Condor 69:13–23CrossRefGoogle Scholar
  47. Laybourne RC (1974) Collision between a vulture and an aircraft at an altitude of 37,000 ft. Wilson Bull 86:461–462Google Scholar
  48. Locy WA, Larsell O (1916) The embryology of the bird’s lung based on observations of the bronchial tree. Part I. Amer J Anat 19:447–504CrossRefGoogle Scholar
  49. Loscertales M, Mikels AJ, Hu JKH, Donahoe PK, Roberts DJ (2008) Chick pulmonary Wnt5a directs airway and vascular tubulogenesis. Development 135:1365–1376PubMedCrossRefGoogle Scholar
  50. Magnussen H, Willmer H, Scheid P (1976) Gas exchange in the air sacs: contribution to respiratory gas exchange in ducks. Respir Physiol 26:129–146PubMedCrossRefGoogle Scholar
  51. Maina JN (1982a) Stereological analysis of the paleopulmo and neopulmo respiratory regions of the avian lung (Streptopelia decaocto). IRCS Med Sci 10:328Google Scholar
  52. Maina JN (1982b) A scanning electron microscopic study of the air and blood capillaries of the lung of the Domestic fowl (Gallus domesticus). Experientia 35:614–616CrossRefGoogle Scholar
  53. Maina JN (1984) Morphometrics of the avian lung. 3. The structural design of the passerine lung. Respir Physiol 55:291–309PubMedCrossRefGoogle Scholar
  54. Maina JN (1987) Morphometrics of the avian lung. 4. The structural design of the charadriiform lung. Respir Physiol 68:99–119PubMedCrossRefGoogle Scholar
  55. Maina JN (1988) Scanning electron microscopic study of the spatial organization of the air- and blood conducting components of the avian lung (Gallus gallus domesticus). Anat Rec 222:145–153PubMedCrossRefGoogle Scholar
  56. Maina JN (1989) Morphometry of the avian lung. In: King AS, McLelland J (eds) Form and function in birds, vol 4. Academic Press, London, pp 307–368Google Scholar
  57. Maina JN (1993) Morphometries of the avian lung: the structural-functional correlations In the design of the lungs of birds. Comp Biochem Physiol 105A:397–410CrossRefGoogle Scholar
  58. Maina JN (1998) The gas exchangers: structure, function, and evolution of the respiratory processes. Springer, HeidelbergCrossRefGoogle Scholar
  59. Maina JN (2000) What it takes to fly: the novel respiratory structural and functional adaptations in birds and bats. J Exp Biol 203:3045–3064PubMedGoogle Scholar
  60. Maina JN (2002) Some recent advances on the study of the functional design of the avian lung: morphologic and morphometric perspectives. Biol Rev 77:97–152PubMedCrossRefGoogle Scholar
  61. Maina JN (2003a) 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 35:375–391PubMedCrossRefGoogle Scholar
  62. Maina JN (2003b) 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 207:119–134PubMedCrossRefGoogle Scholar
  63. Maina JN (2004a) A systematic study of hematopoiesis, vasculogenesis, and angiogensis in the developing avian lung, Gallus gallus variant domesticus. Tissue Cell 36:307–322PubMedCrossRefGoogle Scholar
  64. Maina JN (2004b) Morphogenesis of the laminated tripartite cytoarchitectural design of the blood-gas barrier of the avian lung: a systematic electron microscopic study of the domestic fowl, Gallus gallus variant domesticus. Tissue Cell 36:129–139PubMedCrossRefGoogle Scholar
  65. Maina JN (2005) The lung-air sac system of birds: development, structure, and function. Springer, HeidelbergGoogle Scholar
  66. Maina JN (2006) 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 81:545–579PubMedCrossRefGoogle Scholar
  67. Maina JN (2008) Functional morphology of the avian respiratory system, the lung-air sac system: efficiency built on complexity. Ostrich 79:117–132CrossRefGoogle Scholar
  68. Maina JN (2011) Bioengineering aspects in the design of gas exchangers: comparative evolutionary, morphological, functional, and molecular perspectives. Springer, HeidelbergGoogle Scholar
  69. Maina JN (2012) Comparative molecular developmental aspects of the mammalian- and the avian lungs, and the insectan tracheal system by branching morphogenesis: recent advances and future directions. Front Zool 2012(9):16CrossRefGoogle Scholar
  70. Maina JN, King AS (1982) Thickness of the avian blood-gas barrier: qualitative and quantitative observations. J Anat 134:553–562PubMedPubMedCentralGoogle Scholar
  71. Maina JN, King AS (1984) The structural functional correlation in the design of the bat Lung: a morphometric study. J Exp Biol 111:43–63PubMedGoogle Scholar
  72. Maina JN, King AS (1987) A morphometric study of the lung of a humboldt penguin (Spheniscus humboldti). Zentralb Vet Med C, Anat Histol Embryol 16:293–297Google Scholar
  73. Maina JN, King AS (1989) The lung of the emu, Dromaius novaehollandiae: a microscopic and morphometric study. J Anat 163:67–74PubMedPubMedCentralGoogle Scholar
  74. Maina JN, Nathaniel C (2001) A qualitative and quantitative study of the lung of an ostrich, Struthio camelus. J Exp Biol 204:2313–2330PubMedGoogle Scholar
  75. Maina JN, West JB (2005) Thin but strong! the dilemma inherent in the structural design of the blood-water/gas barrier. Physiol Rev 85:811–844PubMedCrossRefGoogle Scholar
  76. Maina JN, Woodward JD (2009) Three-dimensional serial section computer reconstruction of the arrangement of the structural components of the parabronchus of the ostrich, Struthio camelus lung. Anat Rec 292:1685–1698CrossRefGoogle Scholar
  77. Maina JN, Abdalla MA, King AS (1982a) Light microscopic morphometry of the lungs of 19 avian species. Acta Anat 112:264–270PubMedCrossRefGoogle Scholar
  78. Maina JN, King AS, King DZ (1982b) A morphometric analysis of the lungs of a species of bat. Respir Physiol 50:1–11Google Scholar
  79. Maina JN, Howard CV, Scales L (1983) Length densities and maximum diameter distribution of the air capillaries of the paleopulmo and neopulmo regions of the avian lung. Acta Stereol 2:101–107Google Scholar
  80. Maina JN, King AS, Settle G (1989) An allometric study of the pulmonary morphometric parameters in birds, with mammalian comparison. Philos Trans R Soc London 326B:1–57CrossRefGoogle Scholar
  81. Maina JN, Thomas SP, Hyde DM (1991) A morphometric study of bats of different size: correlations between structure and function of the chiropteran lung. Philos Trans R Soc Lond B Biol Sci 333:31–50PubMedCrossRefGoogle Scholar
  82. Maina JN, Madan AK, Alison B (2003) Expression of fibroblast growth factor-2 (FGF-2) in early stages (days 3-11) of the development of the avian lung, Gallus gallus variant domesticus. J Anat Lond 203:505–512CrossRefGoogle Scholar
  83. Maina JN, Singh P, Moss EA (2009) Inspiratory aerodynamic valving occurs in the ostrich, Struthio camelus lung: computational fluid dynamics study under resting unsteady state inhalation. Respir Physiol Neurobiol 169:262–270PubMedCrossRefGoogle Scholar
  84. Makanya AN, Djonov V (2009) Parabronchial angioarchitecture in developing and adult chickens. J Appl Physiol 106:1959–1969PubMedCrossRefGoogle Scholar
  85. Makanya AN, Hlushchuk R, Duncker HR, Draeger A, Djonov V (2006) Epithelial transformations in the establishment of the blood-gas barrier in the developing chick embryo lung. Dev Dyn 235:68–81PubMedCrossRefGoogle Scholar
  86. Makanya AN, Hlushchuk R, Baum O, Velinov N, Ochs M, Djonov V (2007) Microvascular endowment in the developing chicken embryo lung. Am J Physiol Lung Cell Mol Physiol 292:L1136–L1146PubMedCrossRefGoogle Scholar
  87. Makanya AN, El-Darawish Y, Kavoi BM, Djonov V (2011a) Spatial and functional relationships between air conduits and blood capillaries in the pulmonary gas exchange tissue od adult and develoing chickens. Microsc Res Tech 74:159–169PubMedCrossRefGoogle Scholar
  88. Makanya AN, Hlushchuk R, Djonov V (2011b) The pulmonary blood-gas barrier in the embryo: inauguration, development and refinement. Respir Physiol Neurobiol 178:30–38PubMedCrossRefGoogle Scholar
  89. Makanya AN, Koller T, Hlushchuk R, Djonov V (2012) Pre-hatch lung development in the ostrich. Respir Physiol Neurolbiol 180:183–192CrossRefGoogle Scholar
  90. McLelland J (1989) Anatomy of the lungs and air sacs. In: King AS, McLelland J (eds) Form and function in birds, vol IV. Academic Press, London, pp 221–279Google Scholar
  91. Metzger RJ, Klein OD, Martin GR, Krasnov MA (2008) The branching programme of the mouse lung development. Nature Lond 453:745–750PubMedPubMedCentralCrossRefGoogle Scholar
  92. Miura T, Hartmann D, Kinboshi M, Komada M, Ishibashi M, Shiota K (2009) The cyst-branch difference in developing chick lung results from a different morphogen diffusion coefficient. Mech Dev 126:160–172PubMedCrossRefGoogle Scholar
  93. Morony JJ, Bock WJ, Farrand J (1975) Reference list of the birds of the world. American Museum of Natural History New York, Department of Ornithology, New YorkGoogle Scholar
  94. Moura RS, Coutinho-Borges JP, Pacheco AP, daMota PO, Correia-Pinto J (2011) FGF signaling pathway in the developing chick lung: expression and inhibition sites. PLoS One 6(3):e17660. doi: 10.1371/journal.pone.0017660 PubMedPubMedCentralCrossRefGoogle Scholar
  95. Muraoka RS, Bushdid PB, Brantley DM, Yull FE, Kerr LD (2000) Mesenchymal expression of nuclear factor-kappaβ inhibits epithelial growth and branching in the embryonic chick lung. Dev Biol 225:322–338PubMedCrossRefGoogle Scholar
  96. Norberg UM (1990) Vertebrate flight: mechanics, physiology, morphology, ecology and evolution. Springer, BerlinCrossRefGoogle Scholar
  97. Nudds RL, Bryant DM (2000) The energy cost of short flights in birds. J Exp Biol 203:1561–1582PubMedGoogle Scholar
  98. Pearson JT, Seymour RS, Baudinette RV, Runciman S (2002) Respiration and energetics of embryonic development in a large altricial bird, the Australian pelican, Pelecanus conspicillatus. J Exp Biol 205:2925–2933PubMedGoogle Scholar
  99. Piiper J, Scheid P (1973) Gas exchange in the avian lung: model and experimental evidence. In: Bolis L, Schmidt-Nielsen K, Maddrell SHP (eds) Comparative physiology. Elsevier, Amasterdam, pp 161–185Google Scholar
  100. Pohl HA (1962) Thermal feedback in countercurrent exchange columns. Ind Eng Chem Fundamen 2:73–78. doi: 10.1021/i160002a001 CrossRefGoogle Scholar
  101. Powell FL (1983) Respiration. In: Abs M (ed) Physiology and behaviours of the pigeon. Academic Press, New York, pp 73–95Google Scholar
  102. Powell FL, Scheid P (1989) Physiology of gas exchange in the avian respiratory system. In: King AS, McLelland J (eds) Form and function in birds, vol 4. Academic Press, London, pp 393–437Google Scholar
  103. Radu C, Radu L (1971) Le dispositif vasculaire du poumon chez les oiseaux domestiques (coq, dindon, oie, canard). Revue Med Vet 122:1219–1226Google Scholar
  104. Rawal UM (1976) Nerves in the avian air sacs. Pavo 14:57–60Google Scholar
  105. Romanoff AL (1960) The avian embryo. Macmillan, New YorkGoogle Scholar
  106. Runciman S, Seymour RS, Baudinette RV, Pearson JT (2005) An allometric study of the lung morphology during development in the Australian pelican, Pelicanus conspicillatus. J Anat 207:365–380PubMedPubMedCentralCrossRefGoogle Scholar
  107. Sakiyama J-I, Yamagishi A, Kuroiwa A (2003) Tbx-Fgf10 system controls lung bud formation during chicken embryonic development. Development 130:1225–1234PubMedCrossRefGoogle Scholar
  108. Salomonsen F (1967) Migratory movements of the Arctic tern (Sterna paradisea pontoppidan) in the Southern Ocean. Det Kgl Danske Vid Selsk Biol Med 24:1–37Google Scholar
  109. Scheid P (1979) Mechanisms of gas exchange in bird lungs. Rev Physiol Biochem Pharmacol 86:137–186PubMedGoogle Scholar
  110. Scheid P, Piiper J (1972) Cross-currrent gas exchange in the avian lungs: effects of reversed parabronchial air flow in ducks. Respir Physiol 16:304–312PubMedCrossRefGoogle Scholar
  111. Seymour RS, Runciman S, Baudinette RV, Pearson JT (2004) Developmental allometry of pulmonary structyre and function in the latricial Australian pelican, Pelecanus conspicillatus. J Exp Biol 207:2663–2669PubMedCrossRefGoogle Scholar
  112. Stabellini G, Locci P, Calvitti M, Evangelisti R, Marinucci L, Bodo M, Carusio A, Canaider S, Carinci P (2001) Epithelial-mesenchymal interactions and lung branching morphogenesis, role of polyamines and transforming growth factor beta1. Eur J Histochem 45:151–162PubMedGoogle Scholar
  113. Starck JM (1998) Structural variants and invariants in avian embryonic postnatal development. In: Starck JM, Ricklefs RE (eds) Avian growth and developments. Oxford University Press, New York, pp 59–88Google Scholar
  114. Stanislaus M (1937) Untersuchungen an der Kolibrilunge. Zeits Morphol Tiere 33:261–289CrossRefGoogle Scholar
  115. Swan LW (1961) The ecology of the high Himalayas. Sci Am 205:67–78CrossRefGoogle Scholar
  116. Tenney SM, Tenney JB (1970) Quantitative morphology of cold-blooded lungs: amphibia and Reptilia. Respir Physiol 9:197–215PubMedCrossRefGoogle Scholar
  117. Thomas SP (1987) The physiology of bat flight. In: Fenton MB, Racey P, Rayner JMV (eds) Recent advances in the study of bats. Cambridge University Press, Cambridge, pp 75–99Google Scholar
  118. Thomas SP, Follette DB, Thomas GS (1995) Metabolic and ventilatory adjustments and tolerance of the bat Pteropus poliocephalus to acute hypoxic stress. Comp Biochem Physiol 112A:43–54CrossRefGoogle Scholar
  119. Timmwood KI, Hyde DM, Plopper CG (1987) Lung growth of the turkey, Meleagris gallopavo. I. morphological and morphometric description. Am J Anat 178:144–157PubMedCrossRefGoogle Scholar
  120. Tobalske BW, Hedrik TL, Dial KP, Biewener AA (2003) Comparative power curves in bird flight. Nature 421:363–366PubMedCrossRefGoogle Scholar
  121. Trampel DW, Fletcher OJ (1980) Ring-stabilizing technique for collection of avian air sacs. Am J Vet Res 14:1730–1734Google Scholar
  122. Vos HJ (1937) Über das Fehlen der rekurrenten Bronchien beim Pinguin und bei den Reptilien. Zool Anz 117:176–181Google Scholar
  123. Walsh C, McLelland J (1974) The ultrastructure of the avian extrapulmonary respiratory epithelium. Acta Anat 89:412–422PubMedCrossRefGoogle Scholar
  124. Warburton D, El-Hashash A, Carraro G, Tiozzo C, Sala F et al (2010) Lung organogenesis. Curr Top Dev Biol 90:73–158PubMedPubMedCentralCrossRefGoogle Scholar
  125. Weibel ER (1970/1971) Morphometric estimation of pulmonary diffusion capacity. I. model and method. Respir Physiol 11:54–75Google Scholar
  126. Weibel ER, Knight BW (1964) A morphometric study on the thickness of the pulmonary air-blood barrier. J Cell Biol 21:367–384PubMedPubMedCentralCrossRefGoogle Scholar
  127. Wells DJ (1993) Muscle performance in hovering hummingbirds. J Exp Biol 178:39–57Google Scholar
  128. West NH, Bamford OS, Jones DR (1977) A scanning electron microscope study of the microvasculature of the avian lung. Cell Tiss Res 176:553–564CrossRefGoogle Scholar
  129. Wigglesworth VB (1972) The principles of insect physiology, 7th edn. Chapman and Hall, LondonGoogle Scholar
  130. Winter Y (1999) Flight speed and body mass of nectar-feeding bats (glossophaginae) during foraging. J Exp Biol 202:1917–1930PubMedGoogle Scholar
  131. Woodward JD, Maina JN (2005) A 3-D digital reconstruction of the components of the gas exchange tissue of the lung of the Muscovy duck, Cairina moschata. J Anat Lond 206:477–492CrossRefGoogle Scholar
  132. Woodward JD, Maina JN (2008) 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. J Microsc 230:84–93PubMedCrossRefGoogle Scholar
  133. Yalden DW, Morris PA (1975) The lives of bats. The New York Times Book Co., New YorkGoogle Scholar

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© Dt. Ornithologen-Gesellschaft e.V. 2015

Authors and Affiliations

  1. 1.Department of ZoologyUniversity of JohannesburgJohannesburgSouth Africa

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