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. 2008 Sep 30;3(9):e3303.
doi: 10.1371/journal.pone.0003303.

Evidence for avian intrathoracic air sacs in a new predatory dinosaur from Argentina

Paul C Sereno  1 , Ricardo N Martinez, Jeffrey A Wilson, David J Varricchio, Oscar A Alcober, Hans C E Larsson
Affiliations

Evidence for avian intrathoracic air sacs in a new predatory dinosaur from Argentina

Paul C Sereno et al. PLoS One. .

Abstract

Background: Living 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 findings: We 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/significance: We 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.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Cranial sinus and postcranial air sac systems in birds.
All pneumatic spaces are paired except the clavicular air sac, and the lungs are shaded. Abbreviations: aas, abdominal air sac; atas, anterior thoracic air sac; cas, cervical air sac; clas, clavicular air sac; hd, humeral diverticulum of the clavicular air sac; lu, lung; pns, paranasal sinus; ptas, posterior thoracic air sac; pts, paratympanic sinus; t, trachea.
Figure 2
Figure 2. Tooth of the theropod Aerosteon riocoloradensis.
Isolated crown from the maxillary or dentary series (MCNA-PV-3137; cast). (A)-Side view of crown. (B)-Enlarged view of crown tip. Scale bars equal 1 cm.
Figure 3
Figure 3. Postorbital of the theropod Aerosteon riocoloradensis.
Right postorbital (MCNA-PV-3137; cast) in right lateral (A), medial (B), anterior (C), posterior (D), and dorsal (E) views. Scale bar equals 5 cm. Abbreviations: af, articular surface for the frontal; aj, articular surface for the jugal; als, articular surface for the laterosphenoid; asq, articular surface for the squamosal; oru, orbital rugosity; stf, supratemporal fossa.
Figure 4
Figure 4. Quadrate of the theropod Aerosteon riocoloradensis.
Left quadrate (MCNA-PV-3137; cast) in left lateral (A), medial (B), anterior (C), posterior (D), dorsal (E), and ventral (F) views. Scale bar equals 5 cm. Abbreviations: aqj, articular surface for the quadratojugal; asq, articular surface for the squamosal; co, condyle; he, head; pnec, pneumatocoel; qf, quadrate foramen.
Figure 5
Figure 5. Anterior cervical vertebrae of the theropod Aerosteon riocoloradensis.
Atlas and cervical 3 centrum (MCNA-PV-3137; cast) in left lateral view. (A)-Atlas. (B)-Cervical 3 centrum. Scale bars equal 5 cm. Abbreviations: ic, intercentrum; na, neural arch; pa, parapophysis; pl, pleurocoel; pnec, pneumatocoel.
Figure 6
Figure 6. Mid cervical vertebrae of the theropod Aerosteon riocoloradensis.
Cervical vertebrae 4 and 6 (MCNA-PV-3137; cast) in left lateral view. (A)-Cervical 4. (B)-Cervical 6. Scale bar equals 5 cm. Abbreviations: pa, parapophysis; pl, pleurocoel; se, septum.
Figure 7
Figure 7. Anterior and mid dorsal vertebrae of the theropod Aerosteon riocoloradensis.
Dorsal vertebrae 1, 4 and 8 (MCNA-PV-3137; cast) in left lateral view. (A)-Dorsal 1. (B)-Dorsal 4. (C)-Dorsal 8. Scale bar equals 10 cm. Abbreviations: pa, parapophysis; pl, pleurocoel.
Figure 8
Figure 8. Posterior dorsal vertebrae of the theropod Aerosteon riocoloradensis.
Dorsal vertebrae 11 and 14 (MCNA-PV-3137; cast) in left lateral view. (A)-Dorsal 11. (B)-Dorsal 14. Scale bar equals 10 cm. Abbreviations: dipc, diapophyseal canal; hpo, hyposphene; pa, parapophysis; pl, pleurocoel; poz, postzygapophysis; prz, prezygapophysis; se, septum; tp, transverse process.
Figure 9
Figure 9. Caudal vertebrae of the theropod Aerosteon riocoloradensis.
Anterior and mid caudal centra (MCNA-PV-3137; cast) in left lateral view. (A)-Anterior caudal centrum. (B)-Mid caudal centrum. Scale bar equals 10 cm. Abbreviations: ach, articular surface for a chevron; pl, pleurocoel; se, septum.
Figure 10
Figure 10. Gastralia of the theropod Aerosteon riocoloradensis.
Coossified medial gastral elements from anterior end of cuirass (MCNA-PV-3137). (A)-Coossified gastralia (cast) in ventral view. (B)-Stereopairs of the medial portion of one gastralium showing the pneumatopore and lumen inside the shaft in ventrolateral view. Scale bars equal 10 cm in A and 5 cm in B. Abbreviations: afl, anterior flange; l, left; mge, medial gastral element; pfl, posterior flange; pnec, pneumatocoel; pnep, pneumatopore; r, right; su, suture.
Figure 11
Figure 11. Furcula of the theropod Aerosteon riocoloradensis.
Furcula (MCNA-PV-3137; cast) in anterior (A) and posterior (B) views. Scale bar equals 10 cm. Abbreviations: ep, epicleideum; pnec, pneumatocoel.
Figure 12
Figure 12. Furcula of the theropod Aerosteon riocoloradensis and magpie goose Anseranas semiplamata.
(A)-Stereopairs of the furcula of Aerosteon riocoloradensis (MCNA-PV-3137) in posterodorsal view. (B)-Stereopairs of the furcula of Anseranas semiplamata (FMNH 338808) in posterodorsal view. Scale bars equal 10 cm in A and 2 cm in B.
Figure 13
Figure 13. Ilium of the theropod Aerosteon riocoloradensis.
Left ilium (MCNA-PV-3137; cast) in left lateral (A) and medial (B) views. Scale bar equals 20 cm. Abbreviations: bfo, brevis fossa; isped, ischial peduncle; poap, postacetabular process; pped, pubic peduncle; prap, preacetabular process.
Figure 14
Figure 14. Pneumatopores on the left ilium of the theropod Aerosteon riocoloradensis.
Detail views of the left ilium (MCNA-PV-3137). (A)-Pneumatopores on the base of the preacetabular process in lateral view. (B)-Pneumatopores on the central iliac blade in medial view. (C)-Stereopairs of the pubic peduncle in lateral view showing pneumatopore complex. (D)-Pneumatopores on the brevis fossa of the postacetabular process in ventral view; largest pneumatopore (4 cm in transverse diameter) opens posteriorly (to the right) just posterior to five smaller ventrally-facing pneumatopores (marked). A, B, and D are from a cast of MCNA-PV-3137 to reduce color distraction. Scale bars equal 5 cm in A and 10 cm in B, C and D. Arrows point to pneumatopores.
Figure 15
Figure 15. Pubes of the theropod Aerosteon riocoloradensis.
Pubes (MCNA-PV-3137; cast) in left lateral (A) and anterior (B) views. Scale bar equals 20 cm. Abbreviations: ac, acetabulum; f, foot; fe, fenestra; iped, iliac peduncle; isped, ischial peduncle; pvo, pelvic outlet.
Figure 16
Figure 16. Summary of pneumatic features of the theropod Aerosteon riocoloradensis.
(A)-Silhouette reconstruction in left lateral view showing preserved bones of the holotype and referred specimens (MCNA-PV-3137-3139); body length approximately 9-10 m. (B)-Left quadrate in posterior view. (C)-Dorsal 14 in left lateral view with enlarged cross-sections of the neural spine and transverse process. (D)-Furcula in anterior view with sagittal cross-section. (E)-Cross-section of medial gastral element from the anterior end of the cuirass showing pneumatocoel. (F)-Left ilium in lateral view with enlarged cross-section of pubic peduncle. Scale bars equal 5 cm in B, 10 cm (3 cm for cross-sections) in C, 10 cm (same for cross-section) in D, 2 cm in E, and 20 cm (6 cm for cross-section) in F. Abbreviations: aqj, articular surface for the quadratojugal; asq, articular surface for the squamosal; bfo, brevis fossa; ca, canal; dipc, diapophyseal canal; ep, epicleideum; hpo, hyposphene; ilb, iliac blade; isped, ischial peduncle; ns, neural spine; pa, parapophysis; pc, pleurocoel; pnec, pneumatocoel; pned, pneumatic depression; pnep, pneumatopore; poap, postacetabular process; poz, postzygapophysis; pped, pubic peduncle; prap, preacetabular process; prz, prezygapophysis; ptfl, pterygoid flange; qc, quadrate condyles; qf, quadrate foramen; qh, quadrate head; se, septum; tp, transverse process.
Figure 17
Figure 17. Cladogram of Dinosauria showing the four-phase model for evolution of avian air sacs and lung ventilation within Theropoda.
Phase I (Theropoda), variable posterior extension of paraxial cervical air sacs. Phase II (Tetanurae), elaboration of cranial (clavicular) and caudal (abdominal) intrathoracic air sac divisions and subcutaneous diverticulae. Phase III (Maniraptoriformes), primitive costosternal ventilatory pump. Phase IV (Maniraptora), advanced costosternal ventilatory pump. Abbreviations: aas, abdominal air sac; cas, cervical air sac; caas, caudal air sacs; clas, clavicular air sac; cor, coracoid; cras, cranial air sacs; lu, lung; sr, sternal rib; st, sternum; up, uncinate process; vr, vertebral rib. Bold arrow on lung indicates flow-through lung ventilation; question mark indicates uncertainty in the direction of air flow (uni- or bidirectional).
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