Similarity of Crocodilian and Avian Lungs Indicates Unidirectional Flow Is Ancestral for Archosaurs

Patterns of airflow and pulmonary anatomy were studied in the American alligator (Alligator mississippiensis), the black caiman (Melanosuchus niger), the spectacled caiman (Caiman crocodilus), the dwarf crocodile (Osteolaemus tetraspis), the saltwater crocodile (Crocodylus porosus), the Nile crocodile (Crocodylus niloticus), and Morelet's crocodile (Crocodylus moreletii). In addition, anatomy was studied in the Orinoco crocodile (Crocodylus intermedius). Airflow was measured using heated thermistor flow meters and visualized by endoscopy during insufflation of aerosolized propolene glycol and glycerol. Computed tomography and gross dissection were used to visualize the anatomy. In all species studied a bird-like pattern of unidirectional flow was present, in which air flowed caudad in the cervical ventral bronchus and its branches during both lung inflation and deflation and craniad in dorsobronchi and their branches. Tubular pathways connected the secondary bronchi to each other and allowed air to flow from the dorsobronchi into the ventrobronchi. No evidence for anatomical valves was found, suggesting that aerodynamic valves cause the unidirectional flow. In vivo data from the American alligator showed that unidirectional flow is present during periods of breath-holding (apnea) and is powered by the beating heart, suggesting that this pattern of flow harnesses the heart as a pump for air. Unidirectional flow may also facilitate washout of stale gases from the lung, reducing the cost of breathing, respiratory evaporative water loss, heat loss through the heat of vaporization, and facilitating crypsis. The similarity in structure and function of the bird lung with pulmonary anatomy of this broad range of crocodilian species indicates that a similar morphology and pattern of unidirectional flow were present in the lungs of the common ancestor of crocodilians and birds. These data suggest a paradigm shift is needed in our understanding of the evolution of this character. Although conventional wisdom is that unidirectional flow is important for the high activity and basal metabolic rates for which birds are renowned, the widespread occurrence of this pattern of flow in crocodilians indicates otherwise. Furthermore, these results show that air sacs are not requisite for unidirectional flow, and therefore raise questions about the function of avian air sacs.