Breathing with floating ribs: XROMM analysis of lung ventilation in savannah monitor lizards

Abstract

The structures and functions of the vertebrate lung and trunk are linked through the act of ventilation, but the connections between these structures and functions are poorly understood. We used X-ray reconstruction of moving morphology (XROMM) to measure rib kinematics during lung ventilation in three savannah monitor lizards (Varanus exanthematicus). All of the dorsal ribs, including the floating ribs, contributed to ventilation; the magnitude and kinematic pattern showed no detectable cranial-to-caudal gradient. The true ribs acted as two rigid bodies connected by flexible cartilage, with the vertebral rib and ventromedial shaft of each sternal rib remaining rigid and the cartilage between them forming a flexible intracostal joint. Rib rotations can be decomposed into bucket handle rotation around a dorsoventral axis, pump handle rotation around a mediolateral axis and caliper motion around a craniocaudal axis. Dorsal rib motion was dominated by roughly equal contributions of bucket and pump rotation in two individuals and by bucket rotation in the third individual. The recruitment of floating ribs during ventilation in monitor lizards is strikingly different from the situation in iguanas, where only the first few true ribs contribute to breathing. This difference may be related to the design of the pulmonary system and life history traits in these two species. Motion of the floating ribs may maximize ventilation of the caudally and ventrolaterally positioned compliant saccular chambers in the lungs of varanids, while restriction of ventilation to a few true ribs may maximize crypsis in iguanas.

Locomotor rib kinematics in two species of lizards and a new hypothesis for the evolution of aspiration breathing in amniotes

“…6). Caliper rotation contributes little to lung ventilation in these species 11,12 , and was variable among individuals during locomotion (Fig. 2c), so will not be considered further.…”

“…Modern lepidosaurs retain this locomotor mode [4][5][6][7][8][9] , but detailed 3D axial undulatory kinematics have not been measured in these animals. Motion of the axial skeleton and ribs has received considerable attention during lung ventilation [10][11][12][13][14] , but in what way do the vertebrae and ribs ( Fig. 1) move during locomotion, if they move at all?…”

“…Costal kinematics are deceptively complex, especially in squamates because they have unicapitate ribs articulating with the vertebral column via shallow ball-and-socket joints that permit unrestrained rotation 15 . Three-dimensional rib rotations can be decomposed into three components, often defined relative to the animal's body axes: bucket-handle rotation around a dorsoventral axis, caliper rotation around a craniocaudal axis, and pump-handle rotation around a mediolateral axis [10][11][12][13][14] . These motions can best be studied with X-ray Frame from null hypothesis (movie s3) showing lateral flexion at every intervertebral joint and no motion at the costovertebral joints.…”

“…monitor lizards and Argentine black and white tegus. We then compared these results from locomotion with costovertebral joint motions measured previously during lung ventilation (Cieri et al, 2018;Capano et al, 2019) in the same six individual lizards (three individuals from each species).…”

Computational Fluid Dynamics Reveals a Unique Net Unidirectional Pattern of Pulmonary Airflow in the Savannah Monitor Lizard (Varanus exanthematicus)

“…Lung morphology and costal mobility during ventilation. The lung CFD model placed into anatomical position with ribs scaled by percentage to the most mobile rib as measured by with X‐ray reconstruction of moving morphology analysis (Cieri et al, ).…”