Vertebral pneumaticity is correlated with serial variation in vertebral shape in storks

Birds and their ornithodiran ancestors are unique among vertebrates in exhibiting air-filled sinuses in their postcranial bones, a phenomenon called postcranial skeletal pneumaticity. The factors that account for serial and interspecific variation in postcranial skeletal pneumaticity are poorly understood, although body size, ecology, and bone biomechanics have all been implicated as influencing the extent to which pneumatizing epithelia invade the skeleton and induce bone resorption. Here, I use high-resolution computed-tomography to holistically quantify vertebral pneumaticity in members of the neognath family Ciconiidae (storks), with pneumaticity measured as the relative volume of internal air space. These data are used to describe serial variation in extent of pneumaticity and to assess whether and how pneumaticity varies with the size and shape of a vertebra. Pneumaticity increases dramatically from the middle of the neck onwards, contrary to previous predictions that cervical pneumaticity should decrease toward the thorax to maintain structural integrity as the mass and bending moments of the neck increase. Although the largest vertebrae sampled are also the most pneumatic, vertebral size cannot on its own account for serial or interspecific variation in extent of pneumaticity. Vertebral shape, as quantified by three-dimensional geometric morphometrics, is found to be significantly correlated with extent of pneumaticity, with elongate vertebrae being less pneumatic than craniocaudally short and dorsoventrally tall vertebrae. Considered together, the results of this study are consistent with the hypothesis that shape- and position-specific biomechanics influence the amount of bone loss that can be safely tolerated. These results have potentially important implications for the evolution of vertebral morphology in birds and their extinct relatives.

Automated summary

The study reveals that air-filled sinuses in birds' vertebral bones vary with the position in the neck and are influenced by the shape of the vertebrae. The size of the vertebrae alone cannot explain the variation in pneumaticity. The results suggest that biomechanics related to shape and position play a role in determining the amount of bone loss that can be tolerated.