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Introduction

The respiratory tract of birds has an elaborate series of pneumatic (air-filled) outgrowths that include sinuses within the head and neck and air sacs within the thorax (Figure 1). Sinuses often invade the bones enclosing the nasal cavity (paranasal sinuses) and ear region (paratympanic sinuses), forming membrane-lined, air-filled internal spaces. Air sacs also invade bone in the postcranial skeleton, although many remain free of bone so they can function as compliant bellows, shunting inspired air along a path through a pair of rigid lungs [1]–[4].

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.

doi:10.1371/journal.pone.0003303.g001

In this paper, we describe a new large-bodied theropod from the Late Cretaceous of Argentina, Aerosteon riocoloradensis gen. et sp. nov., characterized by cranial and postcranial bones that are exceptionally pneumatic. Some of its postcranial bones show pneumatic hollowing that can be linked to intrathoracic air sacs that are directly involved in lung ventilation. As a result of an extraordinary level of pneumatization, as well as the excellent state of preservation of much of the axial column and girdles, Aerosteon helps to constrain hypotheses for the evolution of avian-style respiration.

The new theropod is particularly interesting for another reason; it represents a previously unrecorded lineage of large-bodied predator in the early Late Cretaceous (Santonian, ca. 84 Ma) of South America. Most large-bodied Cretaceous theropods on southern continents (South America, Africa, Madagascar, India) pertain to one of three distinctive and contemporary clades: abelisaurids [5]–[7], spinosaurids [8], [9], or carcharodontosaurids [10]–[12]. This predatory triumvirate persisted for millions of years on both South America and Africa [13]. Although initially thought to be a late-surviving carcharodontosaurid [14], Aerosteon preserves cranial bones that bear none of the distinguishing features of carcharodontosaurids [13], [15]. Rather, Aerosteon represents a distinctive basal tetanuran lineage that has survived into the Late Cretaceous on South America and is possibly linked to the allosauroid radiation of the Jurassic.

The purpose of the present paper is not to determine the precise phylogenetic position of Aerosteon but rather to describe its most salient features, outline the range of its remarkable pneumatic spaces, and discuss their relevance to understanding the early evolution of avian air sacs and lung ventilation.

Avian Air Sacs

Avian air sacs arise directly from the lungs (Figure 1) and can be divided into cranial and caudal divisions [1]–[4], [16]–[22]. Within the cranial division, the paired cervical air sacs are not ventilated during respiration and often invade the centrum and neural arches of cervical and anterior thoracic vertebrae. The primary role of the cervical air sacs seems to be the reduction of bone mass, as shown by quantitative comparison of the extent of pneumatic hollowing of skeletal bone in volant and nonvolant birds [22].

The remaining air sacs are involved in lung ventilation and include the median clavicular air sac, the paired anterior and posterior thoracic air sacs, and the paired abdominal air sacs (Figure 1). In contrast to cervical air sacs, these operate as bellows, shunting inspired air along a unidirectional pathway through the lungs—a respiratory pattern unique to birds [1]–[4]. Whereas the anterior and posterior thoracic air sacs almost never invade bone in living birds, the clavicular and abdominal air sacs more commonly have diverticulae that invade axial or appendicular bone [16]–[22]. The intrathoracic location and form of these pneumatic invasions in living birds constitutes the available comparative evidence to allow their identification in fossils [23]. With the exception of evidence presented below, however, pneumatic invasion of appendicular skeletal bone within the thorax has not been reported on conclusive evidence outside crown birds (Neornithes).

Fossil Evidence

Cervical Air Sacs.

The cervical air sacs lie alongside the vertebral column in living birds and sometimes invade the vertebrae and ribs via pneumatopores of variable size. Invaginated pneumatic spaces that enter the lateral aspect of the centra, called pleurocoels, have been traced back in the fossil record to the Late Jurassic bird Archaeopteryx [23]–[25], to various saurischian dinosaurs [23], [26], [27], pterosaurs [23], [28], [29], and possibly to even more primitive, crocodilian relatives in the Triassic [30]. Although doubt was cast recently on the use of fossae as evidence of pneumaticity in basal archosaurs [31], a new basal suchian (distant crocodilian relative) has just been described with cervical pleurocoels [32].

For more than a century, paleontologists have agreed on the existence of cervical air sacs, or some comparable pneumatic structure, in saurischian dinosaurs on the basis of pleurocoels which closely resemble those in some living birds. The longstanding question is the fossil record of noncervical air sacs—sacs that are involved in avian lung ventilation.

Ventilatory Air Sacs.

Ventilatory air sacs, unfortunately, are the least likely to leave evidence of their presence in skeletal bone. Paleontologists and comparative anatomists, as a result, have focused on axial pneumaticity, and opinion has split as to the meaning of observed patterns. In extant birds, pneumatic invasion by cervical air sacs is usually restricted to the cervical and anterior thoracic vertebrae and their respective ribs [1], [16]–[22]. The posterior thoracic, synsacral, and caudal vertebrae, in contrast, are pneumatized by diverticulae extending directly from the lung or from abdominal air sacs [1], [16], [19], [21], [22]. Some authors have concluded, therefore, that the lung and abdominal air sacs must also be responsible for pneumaticity in the posterior half of the axial column in nonavian dinosaurs and, on this basis, have packed the thoracic cavity of theropods with a full complement of avian ventilatory air sacs [33]. An opposing view is that the continuous series of pleurocoels observed in many nonavian dinosaurs suggests that the nonventilatory, paraxial cervical air sacs extended posteriorly along the column [26], [34].

We are inclined to support the latter, more conservative interpretation that pleurocoels in nonavian dinosaurs are a product of paraxial cervical air sacs and provide, at best, ambiguous evidence for intrathoracic ventilatory air sacs. First, pleurocoels are rare in birds, and no living bird has an unbroken cervical-to-caudal series of pleurocoels as occurs in some nonavian dinosaurs, including the one we describe below [31]. As Wedel [26] has underscored, pleurocoels extend posteriorly in the axial column of saurischian dinosaurs to a variable extent, but neither adults nor juveniles of any species show an apneumatic gap. Allotting an unbroken series of pleurocoels of graded form, as in the case we describe below, to three different pneumatic sources (cervical air sacs, lung diverticulae, abdominal air sacs) is difficult to defend. Drawing a direct analogy based on birds for the source(s) of pneumaticity in the posterior axial column in nonavian dinosaurs [22], [31], [33], thus, is problematic.

Second, cervical air sacs have been observed extending to the posterior end of the vertebral column in birds. Several authors have described cervical air sacs extending posteriorly beyond the abdominal air sacs in the ostrich (Struthio camelus) [21], [36]. Ratites have relatively smaller abdominal sacs than in other birds and, as nonvolant basal avians, serve as better analogs for nonavian saurischians than volant neognaths [37].

Finally, the posterior portion of the avian axial skeleton is completely transformed by extensive coossification of vertebrae and girdle bone and by posterolateral rotation of the pubes away from the midline, which allows unobstructed distal extension of the viscera and abdominal air sac under the synsacrum and caudal vertebrae. The pelvic space in nonavian saurischians, in contrast, is not nearly as open and continuous with the thoracic cavity, offering comparably less space for these air sacs [37].

More conclusive evidence of intrathoracic ventilatory air sacs in fossils, in sum, will require an osteological signature of pneumatic structures in nonaxial (appendicular) bones, which that cannot be dismissed as an elaboration of the paraxial cervical air sacs. We now turn attention to previous reports of such pneumaticity in the appendicular skeleton of nonavian dinosaurs.

Previous Reports of Appendicular Pneumaticity.

Appendicular pneumaticity in nonavian dinosaurs is poorly documented. An ilium of the Middle Jurassic theropod Piatnitzkysaurus was shown with two small foramina, one above the pubic peduncle and another above the acetabulum [38: fig. 22]. These small foramina were described as pneumatic and associated with internal space and likened to other supposedly pneumatic foramina in the femur, tibia and metatarsals. The small foramen figured on the shaft of the tibia has elsewhere been described as a neurovascular foramen. Were such long bones also pneumatic, this would constitute an extraordinary condition, as none of the limb bones in Archaeopteryx nor those in other basal avians outside Ornithothoraces (Enantiornithes + Euornithes) has ever been shown to be pneumatic.

A deep depression on the brevis shelf on an ilium of the Cretaceous carcharodontosaurid theropod Mapusaurus, likewise, was labeled “pneumatic diverticulae” of the ilium of [12: fig 26]. The structure, however, was described in the text as a site of origin of powerful hind limb retractor musculature. Whether the ilium in Mapusaurus is actually pneumatized, however, cannot be determined on available information.

Recently, the furcula in the Early Cretaceous dromaeosaurid Buitreraptor was described as “pneumatic” with “trabeculae spanning its interior” [39:1008]. Most of the interior of the bone is hollowed, which does suggest pneumatic invasion, although the pair of potential pneumatopores near the midline are particularly small (P. Makovicky, pers. comm.).

“Cancellous” bone was described in the ilia of the titanosaurs Epachthosaurus [40] and Lirainosaurus [41], although no further claim was made regarding its pneumatic status. The titanosauriform Euhelopus also has a bone texture of larger cells that may be pneumatic (J. Wilson, personal observation). At present there are no reports of appendicular bones among sauropodomorphs with pneumatopores that lead to bone texture than is demonstrably pneumatic.

In sum, the evidence currently documenting the presence of nonaxial pneumatic structures in nonavian dinosaurs is poorly established. Several years ago, we reported the pneumatic spaces in the furcula and ilium described below [14]. The pneumatic status of these and other structures we describe below is quite evident and will add important new evidence for the identity and distribution of air sacs in nonavian theropods.

Methods

Preparation

The holotypic and referred specimens were prepared using pin vice, pneumatic air scribe, and air abrasive. The white-colored bones are embedded in a fine-grained, poorly sorted, hematitic siltstone matrix that in places was very hard. To reduce color distractions in photographic images between the white bone and red-brown matrix, some bones were molded and cast in matt grey-colored casting epoxy.

Imaging

Computed tomography of the furcula, gastral elements, and ilium was undertaken to observe internal pneumatic spaces using a Philips Brilliance 64-slice scanner at 80 Kv in the University of Chicago Hospitals.

Terminology

We employed traditional, or “Romerian,” anatomical and directional terms over veterinarian alternatives [42] and followed recent recommendations regarding the identification of vertebral laminae [43]. “Anterior” and “posterior,” for example, are used as directional terms rather than the veterinarian alternatives “rostral” or “cranial” and “caudal,” except when referring to cranial and caudal air sac divisions in birds.

Institutional abbreviations:

Results

Systematic Paleontology

Systematic hierarchy:

Dinosauria Owen, 1842

Theropoda Marsh, 1881

Tetanurae Gauthier, 1986

Allosauroidea Marsh, 1878

Aerosteon gen. nov.

Etymology.

Aeros, air (Greek); osteon, bone (Greek). Named for the extreme development of pneumatic spaces in skeletal bone.

Type Species.

Aerosteon riocoloradensis.

Aerosteon riocoloradensis sp. nov.

Figures 2–11, 12A, 13–16

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.

doi:10.1371/journal.pone.0003303.g002

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.

doi:10.1371/journal.pone.0003303.g003

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.

doi:10.1371/journal.pone.0003303.g004

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.

doi:10.1371/journal.pone.0003303.g005

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.

doi:10.1371/journal.pone.0003303.g006

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.

doi:10.1371/journal.pone.0003303.g007

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.

doi:10.1371/journal.pone.0003303.g008

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.

doi:10.1371/journal.pone.0003303.g009

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.

doi:10.1371/journal.pone.0003303.g010

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.

doi:10.1371/journal.pone.0003303.g011

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.

doi:10.1371/journal.pone.0003303.g012

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.

doi:10.1371/journal.pone.0003303.g013

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.

doi:10.1371/journal.pone.0003303.g014

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.

doi:10.1371/journal.pone.0003303.g015

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, art