Unidirectional pulmonary airflow patterns in the savannah monitor lizard

Abstract

The unidirectional airflow patterns in the lungs of birds have long been considered a unique and specialized trait associated with the oxygen demands of flying, their endothermic metabolism1 and unusual pulmonary architecture2,3. However, the discovery of similar flow patterns in the lungs of crocodilians indicates that this character is probably ancestral for all archosaurs—the group that includes extant birds and crocodilians as well as their extinct relatives, such as pterosaurs and dinosaurs4,5,6. Unidirectional flow in birds results from aerodynamic valves, rather than from sphincters or other physical mechanisms7,8, and similar aerodynamic valves seem to be present in crocodilians4,5,6. The anatomical and developmental similarities in the primary and secondary bronchi of birds and crocodilians suggest that these structures and airflow patterns may be homologous4,5,6,9. The origin of this pattern is at least as old as the split between crocodilians and birds, which occurred in the Triassic period10. Alternatively, this pattern of flow may be even older; this hypothesis can be tested by investigating patterns of airflow in members of the outgroup to birds and crocodilians, the Lepidosauromorpha (tuatara, lizards and snakes). Here we demonstrate region-specific unidirectional airflow in the lungs of the savannah monitor lizard (Varanus exanthematicus). The presence of unidirectional flow in the lungs of V. exanthematicus thus gives rise to two possible evolutionary scenarios: either unidirectional airflow evolved independently in archosaurs and monitor lizards, or these flow patterns are homologous in archosaurs and V. exanthematicus, having evolved only once in ancestral diapsids (the clade encompassing snakes, lizards, crocodilians and birds). If unidirectional airflow is plesiomorphic for Diapsida, this respiratory character can be reconstructed for extinct diapsids, and evolved in a small ectothermic tetrapod during the Palaeozoic era at least a hundred million years before the origin of birds.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Pulmonary anatomy and airflow patterns of Varanus exanthematicus.
Figure 2: Airflow recorded in vivo.
Figure 3: Phylogeny for Diapsida showing lungs of representative taxa.

References

  1. 1

    Maina, J. N. 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. Cambr. Phil. Soc. 81, 545–579 (2006)

    Article  Google Scholar 

  2. 2

    Brackenbury, J. H. Lung-air-sac anatomy and respiratory pressures in the bird. J. Exp. Biol. 57, 543–550 (1972)

    CAS  PubMed  Google Scholar 

  3. 3

    Maina, J. N. Spectacularly robust! Tensegrity principle explains the mechanical strength of the avian lung. Respir. Physiol. Neurobiol. 155, 1–10 (2007)

    ADS  CAS  Article  Google Scholar 

  4. 4

    Farmer, C. G. 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, 561–575 (2010)

    CAS  Article  Google Scholar 

  5. 5

    Farmer, C. G. & Sanders, K. Unidirectional airflow in the lungs of alligators. Science 327, 338–340 (2010)

    ADS  CAS  Article  Google Scholar 

  6. 6

    Schachner, E. R., Hutchinson, J. R. & Farmer, C. G. Pulmonary anatomy in the Nile crocodile and the evolution of unidirectional airflow in Archosauria. PeerJ http://dx.doi.org/10.7717/peerj.60 (2013)

  7. 7

    Butler, J. P., Banzett, R. B. & Fredberg, J. J. Inspiratory valving in avian bronchi: aerodynamic considerations. Respir. Physiol. 72, 241–255 (1988)

    CAS  Article  Google Scholar 

  8. 8

    Hazelhoff, E. H. Structure and function of the lung of birds. Poult. Sci. 30, 3–10 (1951)

    Article  Google Scholar 

  9. 9

    Sanders, R. K. & Farmer, C. G. The pulmonary anatomy of Alligator mississippiensis and its similarity to the avian respiratory system. Anat. Rec. 295, 699–714 (2012)

    Article  Google Scholar 

  10. 10

    Nesbitt, S. J. The early evolution of archosaurs: relationships and the origin of major clades. Bull. Am. Mus. Nat. Hist. 352, 1–292 (2011)

    Article  Google Scholar 

  11. 11

    Perry, S. F. in Biology of the Reptilia Vol. 19 (Morphology G) (eds Gans, C. & Gaunt, A. S. ) 1–92 (Society for the Study of Amphibians and Reptiles, 1998)

    Google Scholar 

  12. 12

    Conrad, J. L., Balcarcel, A. M. & Mehling, C. M. Earliest example of a giant monitor lizard (Varanus, Varanidae, Squamata). PLoS ONE 7, e41767 (2012)

    ADS  CAS  Article  PubMed Central  Google Scholar 

  13. 13

    Holmes, R. B., Murray, A. M., Attia, Y. S., Simons, E. L. & Chatrath, P. Oldest known Varanus (Squamata: Varanidae) from the Upper Eocene and Lower Oligocene of Egypt: support for an African origin of the genus. Palaeontology 53, 1099–1110 (2010)

    Article  Google Scholar 

  14. 14

    Collar, D. C., Schulte, J. A., II & Losos, J. B. Evolution of extreme body size disparity in monitor lizards (Varanus). Evolution 65, 2664–2680 (2011)

    Article  Google Scholar 

  15. 15

    Pianka, E. R. Evolution of body size: varanid lizards as a model system. Am. Nat. 146, 398–414 (1995)

    Article  Google Scholar 

  16. 16

    Thompson, G. G. & Withers, P. C. Standard and maximal metabolic rates of goannas (Squamata: Varanidae). Physiol. Zool. 70, 307–323 (1997)

    CAS  Article  Google Scholar 

  17. 17

    Owerkowicz, T., Farmer, C. G., Hicks, J. W. & Brainerd, E. L. Contribution of the gular pump to ventilation. Science 284, 1661–1663 (1999)

    ADS  CAS  Article  Google Scholar 

  18. 18

    Becker, H.-O., Böhme, W. & Perry, S. F. Die Lungenmorphologie der Warane (Reptilia: Varanidae) und ihre systematisch-stammesgeschichtliche Bedeutung. Bonn. Zool. Beitr. 40, 27–56 (1989)

    Google Scholar 

  19. 19

    Burnell, A., Collins, S. & Young, B. A. The postpulmonary septum of Varanus salvator and its implication for Mosasaurian ventilation and physiology. Bull. Soc. Geol. Fr. 183, 159–169 (2012)

    Article  Google Scholar 

  20. 20

    Kirschfeld, U. Eine Bauplananalyse der Waranlunge. Zool. Beitr. Neue Folge 16, 401–440 (1970)

    Google Scholar 

  21. 21

    Maina, J. N., Maloiy, G. M. O., Warui, C. N., Njogu, E. K. & Kokwaro, E. D. Scanning electron microscope study of the morphology of the reptilian lung: the savanna monitor lizard Varanus exanthematicus and the Pancake Tortoise Malacochersus tornieri. Anat. Rec. 224, 514–522 (1989)

    CAS  Article  Google Scholar 

  22. 22

    Perry, S. F. & Duncker, H. R. Lung architecture, volume and static mechanics in five species of lizards. Respir. Physiol. 34, 61–81 (1978)

    CAS  Article  Google Scholar 

  23. 23

    Wallach, V. in Biology of the Reptilia Vol. 19 (Morphology G) (eds Gans, C. & Gaunt, A. S. ) 93–295 (Society for the Study of Amphibians and Reptiles, 1998)

    Google Scholar 

  24. 24

    Milani, A. Beiträge zur Kenntniss der Reptilienlunge. Zool. Jahrb. 7, 545–592 (1894)

    Google Scholar 

  25. 25

    Milani, A. Beiträge zur Kenntnis der Reptilienlunge. II. Zool. Jahrb. 10, 93–156 (1897)

    Google Scholar 

  26. 26

    Milsom, W. K. & Vitalis, T. Z. Pulmonary mechanics and the work of breathing in the lizard, Gekko gecko. J. Exp. Biol. 113, 187–202 (1984)

    Google Scholar 

Download references

Acknowledgements

We thank J. Dix (Reptile Rescue Service) for the donation of deceased varanid specimens, J. Bourke for assistance with Avizo, and D. Shafer for German translations. This work was supported by an American Association of Anatomists Postdoctoral Fellowship and an American Philosophical Society Franklin Research Grant to E.R.S., National Science Foundation grants to C.G.F. (IOS-1055080 and IOS-0818973) and a generous donation to the Farmer laboratory by S. Meyer.

Author information

Affiliations

Authors

Contributions

E.R.S. and R.L.C. conducted the in vivo surgeries. All authors collected data on excised lungs. E.R.S. acquired the CT scans and generated the three-dimensional digital models. C.G.F. and J.P.B. supervised and contributed ideas throughout the project. All authors contributed to the manuscript.

Corresponding authors

Correspondence to Emma R. Schachner or C. G. Farmer.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related audio

Supplementary information

3D model of the skeletal and pulmonary anatomy of Varanus exanthematicus

A volume rendered three dimensional skeleton and segmented surface of the lungs and bronchial tree (left craniolateral view) of a female Varanus exanthematicus generated from a CT scan. The bronchus in which in vivo unidirectional flow was measured is indicated. Abbreviations: cb, cervical bronchus; L1-L10, lateral bronchi 1-10; M1-M11, medial bronchi 1-11. (MP4 29060 kb)

Unidirectional movement of fluid through regions of the lung in V. exanthematicus

Microsphere infused saline flowing from lateral bronchus 10 to lateral bronchus 9 in an excised right lung during manual ventilation (60 cc syringe). The microspheres can be seen moving from right to left (caudal to cranial) during inspiration and expiration. Abbreviations: L9, lateral bronchus 9; L10, lateral bronchus 10. (MP4 27392 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Schachner, E., Cieri, R., Butler, J. et al. Unidirectional pulmonary airflow patterns in the savannah monitor lizard. Nature 506, 367–370 (2014). https://doi.org/10.1038/nature12871

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing