Geometric analysis of airway trees shows that lung anatomy evolved to enable explosive ventilation and prevent barotrauma in cetaceans

Abstract

Two new biomechanical challenges faced cetacean lungs compared to their terrestrial ancestors. First, hydrostatic pressures encountered during deep dives are sufficient to cause nearly full lung collapse, risking substantial barotrauma during surfacing if air is trapped in the fragile smaller airways. Second, rapid ventilation in large cetaceans requires correspondingly high ventilatory flow rates. In order to investigate how airway geometry evolved in response to these challenges, we characterized airway geometry from 12 species of cetaceans that vary in common dive depth and ventilatory behavior and a domestic pig using computed tomography. After segmenting the major airways, we generated centerline networks models for the larger airways and computed geometric parameters for each tree including mean branching angle, percent volume fraction, and Strahler branching, diameter, and length ratios. When airway geometry was regressed against ventilatory and diving parameters with phylogenetic least squares, neither average branching angle, percent volume fraction, Strahler length ratio or Strahler branching ratio significantly varied with common ventilatory mode or common diving depth. Higher Strahler diameter ratios were associated with slower ventilation and deeper diving depth, suggesting that cetacean lungs have responded to biomechanical pressures primarily with changes in airway diameter. High Strahler diameter ratios lungs in deeper diving species may help to facilitate more complete collapse of the delicate terminal airways by providing for a greater incompressible volume for air storage at depth. On the other hand, lungs with low Strahler diameter ratios would be better for fast ventilation because the gradual decrease in diameter moving distally should keep peripheral flow resistance low, maximizing ventilatory flow rates.