Abstract
Uniquely among extant vertebrates, birds possess complex respiratory systems characterised by the combination of small, rigid lungs, extensive pulmonary air sacs that possess diverticula that invade (pneumatise) the postcranial skeleton, unidirectional ventilation of the lungs, and efficient crosscurrent gas exchange. Crocodilians, the only other living archosaurs, also possess unidirectional lung ventilation, but lack true air sacs and postcranial skeletal pneumaticity (PSP). PSP can be used to infer the presence of avian-like pulmonary air sacs in several extinct archosaur clades (non-avian theropod dinosaurs, sauropod dinosaurs and pterosaurs). However, the evolution of respiratory systems in other archosaurs, especially in the lineage leading to crocodilians, is poorly documented. Here, we use µCT-scanning to investigate the vertebral anatomy of Triassic archosaur taxa, from both the avian and crocodilian lineages as well as non-archosaurian diapsid outgroups. Our results confirm previous suggestions that unambiguous evidence of PSP (presence of internal pneumatic cavities linked to the exterior by foramina) is found only in bird-line (ornithodiran) archosaurs. We propose that pulmonary air sacs were present in the common ancestor of Ornithodira and may have been subsequently lost or reduced in some members of the clade (notably in ornithischian dinosaurs). The development of these avian-like respiratory features might have been linked to inferred increases in activity levels among ornithodirans. By contrast, no crocodile-line archosaur (pseudosuchian) exhibits evidence for unambiguous PSP, but many of these taxa possess the complex array of vertebral laminae and fossae that always accompany the presence of air sacs in ornithodirans. These laminae and fossae are likely homologous with those in ornithodirans, which suggests the need for further investigation of the hypothesis that a reduced, or non-invasive, system of pulmonary air sacs may be have been present in these taxa (and secondarily lost in extant crocodilians) and was potentially primitive for Archosauria as a whole.
Highlights
Birds are the most speciose extant terrestrial vertebrates, and their success has frequently been suggested to be associated with high metabolic rates and flight
Other extant tetrapods including crocodilians lack postcranial pneumatization and air sacs [7,15], crocodilians possess sac-like chambers with a low density of parenchyma [3,7,16,17,18] that are analogous to true air sacs, which provide a foundation for the evolution of pneumatisation [7], and which have been inferred to have been present in the ancestral archosaur [18]
postcranial skeletal pneumaticity (PSP) has been used as a key source of evidence in investigations of the early evolution of the avian air sac system, with cervical and abdominal air sacs and an avian-style aspiration pump inferred to have been present in theropod dinosaurs and pterosaurs [6,11]
Summary
Birds are the most speciose extant terrestrial vertebrates, and their success has frequently been suggested to be associated with high metabolic rates and flight Linked to these key innovations is the presence of an extensive system of air sacs in the thorax and abdomen, which form important components of the exceptionally efficient avian respiratory system [1,2,3,4]. PSP has been used as a key source of evidence in investigations of the early evolution of the avian air sac system, with cervical and abdominal air sacs and an avian-style aspiration pump inferred to have been present in theropod dinosaurs and pterosaurs [6,11] These inferences have been made largely based on the observation that particular regions of the vertebral column are invariably pneumatised by particular air sacs in extant birds ([6], contra [24]). In spite of the high level of interest in PSP and the evolution of the avian lung, the timing of the origin(s) of PSP in archosaurs is not well constrained, and the distribution of pneumaticity among early archosaurs and closely related taxa (Archosauriformes) remains controversial and poorly known
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