Advertisement

Journal of Comparative Physiology B

, Volume 186, Issue 5, pp 541–552 | Cite as

Unidirectional pulmonary airflow in vertebrates: a review of structure, function, and evolution

  • Robert L. CieriEmail author
  • C. G. Farmer
Review

Abstract

Mechanisms explaining unidirectional pulmonary airflow in birds, a condition where lung gases flow in a consistent direction during both inspiration and expiration in some parts of the lung, were suggested as early as the first part of the twentieth century and unidirectional pulmonary airflow has been discovered recently in crocodilians and squamates. Our knowledge of the functional anatomy, fluid dynamics, and significance of this trait is reviewed. The preponderance of the data indicates that unidirectional airflow is maintained by means of convective inertia in inspiratory and expiratory aerodynamic valves in birds. The study of flow patterns in non-avian reptiles is just beginning, but inspiratory aerodynamic valving likely also plays an important role in controlling flow direction in these lungs. Although highly efficient counter and cross-current blood–gas exchange arrangements are possible in lungs with unidirectional airflow, very few experiments have investigated blood–gas exchange mechanisms in the bird lung and blood–gas arrangements in the lungs of non-avian reptiles are completely unknown. The presence of unidirectional airflow in non-volant ectotherms voids the traditional hypothesis that this trait evolved to supply the high aerobic demands of flight and endothermy, and there is a need for new scenarios in our understanding of lung evolution. The potential value of unidirectional pulmonary airflow for allowing economic lung gas mixing, facilitating lung gas washout, and providing for adequate gas exchange during hypoxic conditions is discussed.

Keywords

Unidirectional airflow Pulmonary Diapsid Lung Cardiogenic 

Notes

Acknowledgments

The authors thank Scott Echols for the computed tomography dataset used in Figs. 24a. This work was supported by the United States National Science Foundation (IOS 0818973 and IOS 1055080 to C.G.F., and a Graduate Research Fellowship to R.L.C).

References

  1. Banzett RB, Butler JP, Nations CS, Barnas GM, Lehr JL, Jones JH (1987) Inspiratory aerodynamic valving in goose lungs depends on gas density and velocity. Respir Physiol 70:287–300CrossRefPubMedGoogle Scholar
  2. Banzett RB, Nations CS, Wang N (1991) Pressure profiles show features essential to aerodynamic valving in geese. Respir Physiol 84:295–309CrossRefPubMedGoogle Scholar
  3. Barnas GM, Mather FB (1978) Response of avian intrapulmonary smooth muscle to changes in carbon dioxide concentration. Poult Sci 57(5):1400–1407CrossRefPubMedGoogle Scholar
  4. Bickler PE, Spragg RG, Hartman MT, White FN (1985) Distribution of ventilation in American alligator, alligator mississippiensis. Am J Physiol 249:R477–R481PubMedGoogle Scholar
  5. Brackenbury J (1971) Airflow dynamics in the avian lung as determined by direct and indirect methods. Respir Physiol 13(3):319–329CrossRefPubMedGoogle Scholar
  6. Brackenbury J (1972) Physical Determinants of Air Flow Pattern Within the Avian Lung. Respir Physiol 15:384–397CrossRefPubMedGoogle Scholar
  7. Brackenbury J (1979) Corrections to the Hazelhoff model of airflow in the avian lung. Respir Physiol 36:143–154CrossRefPubMedGoogle Scholar
  8. Brackenbury J (1989) Respiratory function in exercising fowl following occlusion of the thoracic air sacs. J Exp Biol 237:227–237Google Scholar
  9. Brackenbury J, Amaku J (1990a) Effects of combined abdominal and thoracic airsac occlusion on respiration in domestic fowl. J Exp Biol 152:93–100Google Scholar
  10. Brackenbury J, Amaku J (1990b) Respiratory responses of domestic fowl to hyperthermia following selective air sac occlusions. Exp Physiol 75:391–400CrossRefPubMedGoogle Scholar
  11. Bretz WL, Schmidt-Nielsen K (1971) Bird respiration: flow patterns in the duck lung. J Exp Biol 54:103–118PubMedGoogle Scholar
  12. Bretz WL, Schmidt-Nielsen K (1972) The movement of gas in the respiratory system of the duck. J Exp Biol 56:57–65Google Scholar
  13. Brown RE, Kovacs CK, 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
  14. Butler PJ, West NH, Jones DR (1977) Respiratory and cardiovascular responses of the pigeon to sustained, level flight in a wind-tunnel. J Exp Biol 71:7–26Google Scholar
  15. Butler JP, Banzett RB, Fredberg JJ (1988) Inspiratory valving in avian bronchi: aerodynamic considerations. Respir Physiol 72:241–255CrossRefPubMedGoogle Scholar
  16. Calder WA, Schmidt-Nielsen K (1966) Evaporative cooling and respiratory alkalosis in the pigeon. Proc Natl Acad Sci 55(4):750–756CrossRefPubMedPubMedCentralGoogle Scholar
  17. Carlson AJ, Luckhardt AB (1920) Studies on the visceral nervous system. III. Lung automatism and lung reflexes in Reptilia (turtles: Chrysemys elegans and Malacoclemmys lesueurii. snake: Eutenia elegans). Am J Physiol 54:261–306Google Scholar
  18. Cieri RL, Craven BA, Schachner ER, Farmer CG (2014) New insight into the evolution of the vertebrate respiratory system and the discovery of unidirectional airflow in iguana lungs. Proc Natl Acad Sci 111:17218–17223CrossRefPubMedPubMedCentralGoogle Scholar
  19. Davies D, Dutton RE (1975) Gas-blood PCO2, gradients during avian gas exchange. J Appl Physiol 39:405–410PubMedGoogle Scholar
  20. Dolphin WF (1987) Ventilation and dive patterns of humpback whales, Megaptera novaeangliae, on their Alaskan feeding grounds. Can J Zool 65:83–90CrossRefGoogle Scholar
  21. Dotterweich H (1936) Die atmung der vogel. Z Für Vgl Physiol 23:744–770Google Scholar
  22. Dubach M (1981) Quantitative analysis of the respiratory system of the house sparrow, budgerigar and violet-eared hummingbird. Respir Physiol 46:43–60CrossRefPubMedGoogle Scholar
  23. Farmer CG (2010) The provenance of alveolar and parabronchial lungs: insights from paleoecology and the discovery of cardiogenic, unidirectional airflow in the American alligator (Alligator mississippiensis). Physiol Biochem Zool 83:561–575CrossRefPubMedGoogle Scholar
  24. Farmer CG (2015a) The evolution of unidirectional pulmonary airflow. Physiol 30(4):260–272. doi: 10.1152/physiol.00056.2014 CrossRefPubMedGoogle Scholar
  25. Farmer CG (2015b) Similarity of crocodilian and avian lungs indicates unidirectional flow is ancestral for archosaurs. Integr Comp Biol pp 1–10Google Scholar
  26. Farmer CG (2015c) Unidirectional flow in lizard lungs: a paradigm shift in our understanding of lung evolution in Diapsida. Zoology 118(5):299–301CrossRefPubMedGoogle Scholar
  27. Farmer CG, Sanders K (2010) Unidirectional airflow in the lungs of alligators. Science 327:338–340CrossRefPubMedGoogle Scholar
  28. Fedde MR, Orr JA, Shams H, Scheid P (1989) Cardiopulmonary function in exercising bar-headed geese during normoxia and hypoxia. Respir Physiol 77:239–252CrossRefPubMedGoogle Scholar
  29. Figueroa D, Olivares R, Salaberry M, Sabat P, Canals M (2007) Interplay between the morphometry of the lungs and the mode of locomotion in birds and mammals. Biol Res 40:193–201CrossRefPubMedGoogle Scholar
  30. Harvey EP, Ben-Tal A (2016) Robust unidirectional airflow through avian lungs: new insights from a piecewise linear mathematical model. PLoS Comput Biol 12(2):e1004637CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hazelhoff EH (1943) Bouw en Functie van de Vogellong. Versl Gewone Vergad Afd Naturk K ned Akad Wet 52:391–400Google Scholar
  32. Hazelhoff EH (1951) Structure and function of the lung of birds. Poult Sci 30(1):3–10CrossRefGoogle Scholar
  33. Hicks JW, White FN (1992) Pulmonary gas exchange during intermittent ventilation in the American alligator. Respir Physiol 88:23–36CrossRefPubMedGoogle Scholar
  34. Jones DR, Holeton GF (1972) Cardiovascular and respiratory responses of ducks to progressive hypocapnic hypoxia. J Exp Biol 56:657–666PubMedGoogle Scholar
  35. Jones JH, Effmann EL, Schmidt-Nielsen K (1981) Control of air flow in bird lungs: radiographic studies. Respir Physiol 45:121–131CrossRefPubMedGoogle Scholar
  36. Jones JH, Effmann EL, Schmidt-Nielsen K (1985) Lung volume changes during respiration in ducks. Respir Physiol 59:15–25CrossRefPubMedGoogle Scholar
  37. King A (1966) Structural and functional aspects of the avian lungs and air sacs. In: Felts WJL, Harrison RJ (eds) International review of general and experimental zoology, Vol 2, Academic Press, New York, London, pp 171–267Google Scholar
  38. King A, Cowie A (1969) The functional anatomy of the bronchial muscle of a bird. J Anat 105(2):323–336PubMedPubMedCentralGoogle Scholar
  39. Kuethe DO (1988) Fluid mechanical valving of air flow in bird lungs. J Exp Biol 136:1–12PubMedGoogle Scholar
  40. Mackelprang R, Goller F (2013) Ventilation patterns of the songbird lung/air sac system during different behaviors. J Exp Biol 216:3611–3619CrossRefPubMedPubMedCentralGoogle Scholar
  41. Maina JN (2000) What it takes to fly: the structural and functional respiratory refinements in birds and bats. J Exp Biol 203:3045–3064PubMedGoogle Scholar
  42. 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 Camb Philos Soc 81:545–579CrossRefPubMedGoogle Scholar
  43. Maina JN (2015a) Structural and biomechanical properties of the exchange tissue of the avian lung. Anat Rec 298:1673–1688. doi: 10.1002/ar.23162 CrossRefGoogle Scholar
  44. Maina JN (2015b) The design of the avian respiratory system: development, morphology and function. J Ornithol 156(suppl 1):41–63 CrossRefGoogle Scholar
  45. Maina JN, Africa M (2000) Inspiratory aerodynamic valving in the avian lung: functional morphology of the extrapulmonary primary bronchus. J Exp Biol 203:2865–2876PubMedGoogle Scholar
  46. Maina JN, Singh P, Moss E (2009) Inspiratory aerodynamic valving occurs in the ostrich, Struthio camelus lung: a computational fluid dynamics study under resting unsteady state inhalation. Respir Physiol Neurobiol 169:262–270CrossRefPubMedGoogle Scholar
  47. Meyer M, Worth H, Scheid P (1976) Gas-blood CO2 equilibration in parabronchial lungs of birds. J Appl Physiol 41(3):302–309PubMedGoogle Scholar
  48. Milani A (1894a) Beiträge zur Kenntniss der Reptilienlunge I. Lacertilia. Zool Jahrb X Abtha f Morph 10:93–146Google Scholar
  49. Milani A (1894b) Beiträge zur Kenntniss der Reptilienlunge II Theil. Zool Jahrb X Abtha f Morph 7:545–592Google Scholar
  50. Milsom WK (1991) Intermittent breathing in vertebrates. Annu Rev Physiol 53:87–105CrossRefPubMedGoogle Scholar
  51. Paré M, Ludders JW, Erb HN (2013) Association of partial pressure of carbon dioxide in expired gas and arterial blood at three different ventilation states in apneic chickens (Gallus domesticus) during air sac insufflation anesthesia. Vet Anaesth Analg 40:245–256CrossRefPubMedGoogle Scholar
  52. Perry SF (1990) Gas exchange strategy in the Nile crocodile: a morphometric study. J Comp Physiol B 156(6):761–769Google Scholar
  53. Perry SF, Duncker H-R (1978) Lung architecture, volume and static mechanics in five species of lizards. Respir Physiol 34:61–81CrossRefPubMedGoogle Scholar
  54. Piiper J, Drees F, Scheid P (1970) Gas exchange in the domestic fowl during spontaneous breathing and artificial ventilation. Respir Physiol 9:234–245CrossRefPubMedGoogle Scholar
  55. Powell FL (2015) Respiration. In: Scanes C (ed) Sturkie’s Avian Physiology, 6th edn. Elsevier, San Diego, pp 301–336Google Scholar
  56. Powell FL, Geiser J, Gratz RK, Scheid P (1981) Airflow in the avian respiratory tract: variations of O2 and CO2 concentrations in the bronchi of the duck. Respir Physiol 44:195–213CrossRefPubMedGoogle Scholar
  57. Sanders RK, Farmer CG (2012) The pulmonary anatomy of Alligator mississippiensis and its similarity to the avian respiratory system. Anat Rec 295:699–714CrossRefGoogle Scholar
  58. Schachner ER, Cieri RL, Butler JP, Farmer CG (2013) Unidirectional pulmonary airflow patterns in the savannah monitor lizard. Nature 506:367–370CrossRefPubMedGoogle Scholar
  59. Scheid P (1979) Mechanisms of gas exchange in bird lungs. Rev Physiol Biochem Pharmacol 86:137–186PubMedGoogle Scholar
  60. Scheid P, Piiper J (1970) Analysis of gas exchange in the avian lung: theory and experiments in the domestic fowl. Respir Physiol 9:246–262CrossRefPubMedGoogle Scholar
  61. Scheid P, Piiper J (1971) Direct measurement of the pathway of respired gas in duck lungs. Respir Physiol 11:308–314CrossRefPubMedGoogle Scholar
  62. Scheid P, Piiper J (1972) Cross-current gas exchange in avian lungs: effects of reversed parabronchial air flow in ducks. Respir Physiol 16:304–312CrossRefPubMedGoogle Scholar
  63. Scheid P, Piiper J (1980) Blood/gas equilibrium of carbon dioxide in lungs. A critical review. Respir Physiol 39(1):1–31CrossRefPubMedGoogle Scholar
  64. Scheid P, Slama H, Piiper J (1972) Mechanisms of unidirectional flow in parabronchi of avian lungs: measurements in duck lung preparations. Respir Physiol 14:83–95CrossRefPubMedGoogle Scholar
  65. Scheid P, Slama H, Willmer H (1974) Volume and ventilation of air sacs in ducks studied by inert gas wash-out. Respir Physiol 21:19–36CrossRefPubMedGoogle Scholar
  66. Scheid P, Kuhlmann WD, Fedde MR (1977) Intrapulmonary receptors in the Tegu lizard: II. Functional characteristics and localization. Respir Physiol 29:49–62CrossRefPubMedGoogle Scholar
  67. Schmidt-Nielsen K, Kanwisher J, Lasiewski RC, Cohn JE, Bretz WL (1969) Temperature regulation and respiration in the ostrich. The Condor 71(4):341–352CrossRefGoogle Scholar
  68. Thomas SP, Lust MR, van Riper HJ (1984) Ventilation and oxygen extraction in the bat Phyllostomus hastatus during rest and steady flight. Physiol Zool 57:237–250CrossRefGoogle Scholar
  69. 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 A Physiol 112:43–54CrossRefPubMedGoogle Scholar
  70. Tucker VA (1968) Respiratory exchange and evaporative water loss in the flying budgerigar. J Exp Biol 48:67–87Google Scholar
  71. Urushikubo A, Nakamura M, Hirahara H (2013) Effects of the air sac compliances on flow in the parabronchi: computational fluid dynamics using an anatomically simplified model of an avian respiratory system. J Biomed Sci Eng 6:483–492CrossRefGoogle Scholar
  72. Wang N, Banzett RB, Butler JP, Fredberg JJ (1988) Bird lung models show that convective inertia effects inspiratory aerodynamic valving. Respir Physiol 73:111–124CrossRefPubMedGoogle Scholar
  73. Wang N, Banzett RB, Nations CS, Jenkins FA (1992) An aerodynamic valve in the avian primary bronchus. J Exp Biol 262:441–445Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of BiologyUniversity of UtahSalt Lake CityUSA

Personalised recommendations