Evidence for Avian Intrathoracic Air Sacs in a New Predatory Dinosaur from Argentina

Abstract

BackgroundLiving birds possess a unique heterogeneous pulmonary system composed of a rigid, dorsally-anchored lung and several compliant air sacs that operate as bellows, driving inspired air through the lung. Evidence from the fossil record for the origin and evolution of this system is extremely limited, because lungs do not fossilize and because the bellow-like air sacs in living birds only rarely penetrate (pneumatize) skeletal bone and thus leave a record of their presence.Methodology/Principal FindingsWe describe a new predatory dinosaur from Upper Cretaceous rocks in Argentina, Aerosteon riocoloradensis gen. et sp. nov., that exhibits extreme pneumatization of skeletal bone, including pneumatic hollowing of the furcula and ilium. In living birds, these two bones are pneumatized by diverticulae of air sacs (clavicular, abdominal) that are involved in pulmonary ventilation. We also describe several pneumatized gastralia (“stomach ribs”), which suggest that diverticulae of the air sac system were present in surface tissues of the thorax.Conclusions/SignificanceWe present a four-phase model for the evolution of avian air sacs and costosternal-driven lung ventilation based on the known fossil record of theropod dinosaurs and osteological correlates in extant birds:(1) Phase I—Elaboration of paraxial cervical air sacs in basal theropods no later than the earliest Late Triassic.(2) Phase II—Differentiation of avian ventilatory air sacs, including both cranial (clavicular air sac) and caudal (abdominal air sac) divisions, in basal tetanurans during the Jurassic. A heterogeneous respiratory tract with compliant air sacs, in turn, suggests the presence of rigid, dorsally attached lungs with flow-through ventilation.(3) Phase III—Evolution of a primitive costosternal pump in maniraptoriform theropods before the close of the Jurassic.(4) Phase IV—Evolution of an advanced costosternal pump in maniraptoran theropods before the close of the Jurassic.In addition, we conclude:(5) The advent of avian unidirectional lung ventilation is not possible to pinpoint, as osteological correlates have yet to be identified for uni- or bidirectional lung ventilation.(6) The origin and evolution of avian air sacs may have been driven by one or more of the following three factors: flow-through lung ventilation, locomotory balance, and/or thermal regulation.

A new sauropod dinosaur from the Early Cretaceous of Tunisia with extreme avian-like pneumatization

“…ARTICLE surface of the ischium of Tataouinea does not differ in shape, depth and presence of clearly defined margins, from the pleurocoels in the axial skeleton and is interpreted as pneumatic in origin. Pneumatic invasion of the pelvic girdle has been reported in both theropods and neosauropods 18,26,28 , but all previous reports were limited to the ilium. Other sauropods show small internal chambers pneumatising the iliac blades but not invading the pubic peduncle 26 , whereas a large chamber hollowing the latter peduncle was reported only in theropods 28 .…”

“…Pneumatic invasion of the pelvic girdle has been reported in both theropods and neosauropods 18,26,28 , but all previous reports were limited to the ilium. Other sauropods show small internal chambers pneumatising the iliac blades but not invading the pubic peduncle 26 , whereas a large chamber hollowing the latter peduncle was reported only in theropods 28 . The distribution of the osteological correlates of pneumatic features among Rebbachisauridae shows a progressive expansion of the postcranial pneumatization along the lineage leading to nigersaurines (Fig.…”

“…A more conservative approach 28 considered axial pneumatization as ambiguous evidence of abdominal air sacs, and only pelvic pneumatization in areas removed from contact with the sacrum as unambiguous evidence of abdominal air sacs, to avoid potential confusion with extramural pneumatization by posterior expansions of the cervical air sacs. ONM DT 1-36 is the first sauropod where large pneumatic foramina penetrate pelvic bones removed from direct contact with the axial skeleton, and thus accords with the presence of abdominal air sacs even following the most conservative approach 28 .…”

Dinosaur Energetics: Setting the Bounds on Feasible Physiologies and Ecologies

“…It is possible that the respiration rate required to support such a metabolic rate was only possible because of the existence of avian-like air sacs, with the attendant possibility of a through-flow continuous ventilation system (Wedel 2003a, b;O'Connor and Claessens 2005;Sereno et al 2008;Tickle et al 2012). Among living amniotes, pneumatic postcranial bones are present only in birds, and they are the osteological correlates of the diverticular lungs and pulmonary air sacs (Wedel 2006).…”

Stratigraphy of the Neuquén Group, Upper Cretaceous of the Neuquén Basin (Argentina): new proposal for lithostratigraphic ordaining

“…De la región septentrional de la Cuenca Neuquina provienen algunos ejemplares de dinosaurios terópodos como Aucasaurus garridoi (Coria et al, 2002a) y Aeroston riocoloradensis (Sereno et al, 2008); así como dinosaurios saurópodos representados por el Pitekunsaurus macayai (Filippi & Garrido, 2008). Tal como lo indicaran Leanza et al (2004), el ejemplar de titanosaurio más completo conocido hasta el momento (Calvo et al, 1997) provendría de estos mismos depósitos.…”