Bone histological correlates for air sacs and their implications for understanding the origin of the dinosaurian respiratory system

Abstract

Air sacs are an important component of the avian respiratory system, and corresponding structures also were crucial for the evolution of sauropod dinosaur gigantism. Inferring the presence of air sacs in fossils so far is restricted to bones preserving internal pneumatic cavities and foramina as osteological correlates. We here present bone histological correlates for air sacs as a new potential identification tool for these elements of the respiratory system. The analysis of several avian and non-avian dinosaur samples revealed delicate fibres in secondary trabecular and secondary endosteal bone that in the former case (birds) is known or in the latter (non-avian dinosaurs) assumed to have been in contact with air sacs, respectively. The bone histology of this 'pneumosteal tissue' is markedly different from those regions where muscles attached presenting classical Sharpey's fibres. The pneumatized bones of several non-dinosaurian taxa do not exhibit the characteristics of this 'pneumosteum'. Our new histology-based approach thus can be instrumental in reconstructing the origin of air sacs among dinosaurs and hence for our understanding of this remarkable evolutionary novelty of the respiratory system.

Histology and pneumaticity of Aoniraptor libertatem (Dinosauria, Theropoda), an enigmatic mid‐sized megaraptoran from Patagonia

“…The histological features of the vertebrae of Aoniraptor resemble the sauropods Europasaurus holgeri and Diplodocus sp., because of the presence of a surface not composed of cortical bone but rather of secondary trabecular bone. In all cases, the secondary trabecular bone shows a pneumosteal tissue (Lambertz et al ., 2018). Similar observations in the sauropod Urebatitan corroborate the presence of pneumosteum in this taxon (Aureliano et al ., 2019).…”

“…However, postcranial pneumaticity is not unique to birds, being observed in non‐avian dinosaurs (Britt, 1993; Wedel, 2003; O´Connor, 2006, 2007; O’Connor and Claessens, 2006; Sereno et al ., 2008; Makovicky and Zanno, 2011; Benson et al ., 2012; Xu et al ., 2014; Watanabe et al ., 2015; Lambertz et al ., 2018) as well as pterosaurs (Britt, 1993; Butler et al ., 2009; Claessens et al ., 2009; Martin and Palmer, 2014). The presence of this condition in non‐volant taxa indicates that the interaction between postcranial pneumaticity and flight capability was secondarily acquired and suggests that the main function of postcranial pneumatization is not flight.…”

“…Recently, a few works (Lambertz et al ., 2018; Aureliano et al ., 2019) reveal that the presence of an air‐sac system could be inferred from the presence of pneumosteal tissue. This gives another tool for recognizing and improving knowledge of the distribution and evolution of the pneumaticity within Dinosauria.…”

“…This gives another tool for recognizing and improving knowledge of the distribution and evolution of the pneumaticity within Dinosauria. A correlation between air‐sac system invasion and its histological signal in bones has been proposed (Lambertz et al ., 2018). Within non‐avian dinosaurs, pneumosteal tissue has been found in the sauropods Europasaurus holgeri , Diplodocus sp.…”

“…Within non‐avian dinosaurs, pneumosteal tissue has been found in the sauropods Europasaurus holgeri , Diplodocus sp. (Lambertz et al ., 2018) and Uberabatitan ribeiroi (Aureliano et al ., 2019). We expand here the occurrence of pneumosteum to non‐avian theropod dinosaurs by identification of this tissue in the caudal vertebrae and chevron in Aoniraptor libertatem .…”