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

Abstract

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.

Quantitative assessment of the vertebral pneumaticity in an anhanguerid pterosaur using micro-CT scanning

“…Unlike what we calculated for SNSB/BSPG 1991 I 27, the pneumaticity of the cervical vertebrae in storks increases posteriorly. These results suggest that the increase in pneumaticity may also be related to regions in which there is a reduction in the range of movement in some axes, and, consequently, the tensions that could exceed the limit of bone resistance also decrease 48 – 50 , contradicting previous hypotheses of bone reinforcement in this region of the vertebral column 36 . In the case of the vertebrae of SNSB/BSPG 1991 I 27, the higher degree of pneumaticity present in the mid-cervical vertebrae could be a reflection of their long length, resulting in a low range of movement and, consequently, a decrease of the tensions on this region of the neck.…”

“…The mean ASP for each vertebra of SNSB/BSPG 1991 I 27 varied between 68 and 72%. Furthermore, we observed here a reduction of the ASP and increase in the area occupied by trabecular bone in the cranio-caudal direction in the vertebral series of SNSB/BSPG 1991 I 27, which may be related to a biomechanical requirement of the vertebral column 36 , 37 , 48 – 50 . Within the same vertebra, ASP values in the neural arch were higher at mid-length and decreased towards the zygapophyses, indicating a probable need for a higher level of stiffness 44 .…”

“…In comparison to extant birds, the vertebral ASP of SNSB/BSPG 1991 I 27 is slightly lower than those of the posterior cervical vertebrae of extant storks (Ciconiidae), but higher than the ASP of the vertebrae of their first and second neck segments 48 . However, the ASP in birds was not estimated by cross-sections, but rather measured from the vertebral total volume 48 . Unlike what we calculated for SNSB/BSPG 1991 I 27, the pneumaticity of the cervical vertebrae in storks increases posteriorly.…”

“…The images were exported as DICOM files with the software Volume Graphics to visualise the individual slices. The grey balance of each image was enhanced using ImageJ 48 to observe the pneumatic cavities, for such the same brightness/contrast value was used for all analysed slices.…”

Postcranial skeletal pneumaticity innon‐aquaticneoavians: Insights from accipitrimorphae

“…Three now extinct groups (non-avian theropods, sauropodomorphs, and pterosaurs) exhibit robust osteological correlates associated with postcranial skeletal pneumaticity (Butler et al, 2009(Butler et al, , 2012O'Connor, 2006;O'Connor & Claessens, 2005;Wedel, 2003Wedel, , 2006. Focused research has begun to characterize expression patterns of postcranial pneumaticity in both neornithine birds (Gutherz & O'Connor, 2021;Moore, 2020;O'Connor, 2004O'Connor, , 2009Smith, 2012) and their now extinct relatives (e.g., non-avian theropod dinosaurs; Benson et al, 2012).…”