Extreme postcranial pneumaticity in sauropod dinosaurs from South America
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- Cerda, I.A., Salgado, L. & Powell, J.E. Paläontol Z (2012) 86: 441. doi:10.1007/s12542-012-0140-6
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Birds are unique among living tetrapods in possessing pneumaticity of the postcranial skeleton, with invasion of bone by the lung and air-sac system. Postcranial skeletal pneumaticity (PSP) has been reported in numerous extinct archosaurs including pterosaurs and non-avian dinosaurs. Here we report a case of extreme PSP in a group of small-bodied, armored sauropod dinosaurs from the Upper Cretaceous of South America. Based on osteological data, we report an extensive invasion of pneumatic diverticula along the vertebral column, reaching the distal portion of the tail. Also, we provide evidence of pneumaticity in both pectoral and pelvic girdles. Our study reveals that the extreme PSP in archosaurs is not restricted to pterosaurs and theropod dinosaurs.
KeywordsSauropodaTitanosauriaUpper CretaceousAir-sac systemAppendicular pneumaticity
Vögel sind einzigartig innerhalb der lebenden Tetrapoden, da sie eine Pneumatisierung des Postkranialskeletts aufweisen, welche die Invasion von Knochen durch die Lunge und Luftsack-Systeme einschließt. Diese postkraniale Skelettpneumatisierung (PSP) ist bereits in zahlreichen ausgestorbenen Archosauriern, einschließlich Pterosauriern und Dinosauriern, die nicht der Vogellinie angehören, beschrieben worden. Hier berichten wir über einen Fall von extremer PSP in einer Gruppe von kleinwüchsigen, gepanzerten sauropoden Dinosauriern aus der Oberkreide von Südamerika. Basierend auf osteologischen Daten lässt sich eine umfangreiche Invasion von pneumatischen Divertikeln entlang der Wirbelsäule nachweisen, welche sich bis in die distalen Bereiche des Schwanzes erstreckt. Darüber hinaus zeigen sich Hinweise auf Pneumatisierung in beiden Brust- und Beckengürteln. Unsere Studie zeigt, dass diese extreme Form von PSP in Archosauriern nicht auf Flugsaurier und theropode Dinosaurier beschränkt ist.
Birds are the only extant group of vertebrates that possesses a pneumatic postcranial skeleton, which results from invasion of bone by extensions (diverticula) from the lung and air-sac system (Britt 1993; Duncker 1971). This feature has also been reported in numerous extinct archosaurs including pterosaurs and non-avian dinosaurs (Benson et al. 2011; Britt 1993; Buttler et al. 2009; Claessens et al. 2009; Janensch 1947; O’Connor 2006; Wedel 2003; Yates et al. 2012). In sauropod dinosaurs, the postcranial skeletal pneumaticity (PSP) has been commonly identified in the presacral axial skeleton (including dorsal ribs) and, in some groups, in the sacrum and the proximal and middle caudal vertebrae (Janensch 1947; Schwarz et al. 2007; Wedel et al. 2000; Wedel 2003, 2007, 2009). Pneumatization of the pelvic girdle has been proposed for some Neosauropoda taxa (Carvalho et al. 2003; Hocknull et al. 2009; Wedel 2009; Wilson and Upchurch 2009; Woodward and Lehman 2009; Xu et al. 2006), but based on non-conclusive evidence, and pneumaticity in the pectoral girdle has definitely never been reported in sauropodomorphs.
Several osteological correlates of PSP have been previously proposed for the determination of this feature in fossil groups (Britt 1993). However, recent studies on extant tetrapods have demonstrated that the correlation between many of these purported osteological features (i.e., blind fossae) with PSP is ambiguous (O’Connor 2006; O’Connor and Claessens 2005). The only unambiguous indicators of pneumaticity are large cortical openings (foramina) connected directly with large internal cavities (camerae or camellae) within the bone. Using this anatomical criterion, we study the PSP in a derived clade of titanosaurian sauropods from the Upper Cretaceous of South America [Saltasaurini (Salgado and Bonaparte 2007, Saltasaurinae sensu Salgado et al. 1997, Saltasaurinae sensu Powell 2003)], which actually includes Saltasaurus loricatus from Northwestern Argentina (Bonaparte and Powell 1980; Powell 2003) and Neuquensaurus australis and Rocasaurus muniozi from Northern Patagonia (Powell 2003; Salgado and Azpilicueta 2000).
APB: Museo de la Asociación Paleontológica de Bariloche, Río Negro Province, Argentina; MLP-CS, Museo de La Plata, Cinco Saltos Collection, La Plata, Argentina; MLP-Ly: Museo de La Plata, Lydekker’s Collection; PVL: Paleovertebrate collection of Instituto “Miguel Lillo”, Tucumán Province, San Miguel de Tucumán, Argentina. MPCA-Pv: Paleovertebrate Collection of Museo Provincial “Carlos Ameghino”, Cipolletti, Río Negro Province, Argentina; MCS-Pv, Paleovertebrate Collection of Museo Regional Cinco Saltos, Río Negro Province, Argentina.
Materials and methods
The examined material of Saltasaurus includes all the specimens referred to by Powell (2003) and identified as PVL 4017 and PVL 4740 (see Powell 2003 for a complete list of the specimens). The material was collected from the Upper Cretaceous (?upper Campanian-Maastrichtian) sediments of the Lecho Formation at the locality of El Brete (south of Salta Province, Argentina) (Bonaparte and Powell 1980; Powell 2003). The specimens of Neuquensaurus were recovered from the localities of Cinco Saltos and Lago Pellegrini (Río Negro Province, Argentina), from sediments of the Anacleto Formation (lower Campanian) (Powell 2003; Salgado et al. 2005; Otero 2010). We examined postcranial elements assigned to Neuquensaurus identified as MCS-Pv 5 (Salgado et al. 2005), MLP-Ly and MLP-CS (see Powell 2003 for a complete list of the materials housed in Museo de La Plata). The assignment of the studied specimens to Neuquensaurus has been previously discussed by several authors (McIntosh 1990; Powell 2003; Wilson and Upchurch 2003; Salgado et al. 2005; Otero 2010). The Rocasaurus material includes the holotype (MPCA-Pv 46) and all the referred material (MPCA-Pv 47-51, MPCA-Pv 56-60 and APB 2887). These specimens were collected from sediments of the Allen Formation (middle Campanian-lower Maastrichtian) of the locality of Salitral Moreno (Río Negro Province, Argentina) (Salgado and Azpilicueta 2000).
The internal structure of the examined bones was studied by observation of: fortuitous breaks in specimens (all the three taxa); mechanical sections (Saltasaurus) and non-destructive computed tomography (CT) (vertebrae of Neuquensaurs and Rocasaurus). Obtaining images by CT scanning was not possible for Saltasaurus, because of the prevalent heavy elements in its sedimentary matrix. The CT scanning of the different bones was conducted on a Pro Speed helicoidal scanner (99783 Pro Gp serie) housed at Policlínico Neuquén (Neuquén Province, Argentina). Vertebral laminae and fossae terminology follows Wilson (2000) and Wilson et al. (2011). Pneumatic structure nomenclature follows Britt (1993) and Wedel et al. (2000).
Among sauropod dinosaurs, internal cavities (camerae and camellae) have been previously reported in the pelvic girdle (ilia) of several taxa, including: Euhelopus zdanskyi (Wilson and Upchurch 2009; Wiman 1929), Lirainosaurus astibiae (Sanz et al. 1999), Amazonsaurus maranhensis (Carvalho et al. 2003), Sonidosaurus saihangaobiensis (Xu et al. 2006), Diamantinasaurus matildae (Hocknull et al. 2009) and Alamosaurussanjuanensis (Woodward and Lehman 2009). These cavities have been interpreted by some authors as pneumatic (Carvalho et al. 2003; Hocknull et al. 2009; Wedel 2009; Wilson and Upchurch 2009; Woodward and Lehman 2009; Xu et al. 2006). However, at present, there are no reports in sauropodomorphs of cortical foramina communicating with the internal cavities of the ilia. As has been previously stated, the only unambiguous indicators of pneumaticity are large foramina connected directly with large internal cavities (camerae or camellae) within the bone (O’Connor 2006; O’Connor and Claessens 2005). Our finding gives the first report of a cortical foramen communicated with internal cavities in the ilium and supports the previous hypothesis of the invasion of pneumatic diverticula in the pelvic girdle in some Neosauropoda taxa. We note that in several badly damaged Saltasaurini bones (e.g., Saltasaurus scapula PVL 4017-153, Neuquensaurus ilium MLP-CS 1259, Rocasaurus ilium MPCA-Pv 46-13), the camellate tissue is present but the pneumatic foramina could not be found. We infer that the pneumatic foramina were actually present but obscured by the poor preservation of the bones. The same explanation could be applied to those non-Saltasaurini sauropods for which camellate tissue has been reported in the ilium. Hence, as has been previously proposed by Wedel (2003, 2005, 2009), the invasion of pneumatic diverticulae in the ilium appears to be an extended character within derived neosauropod dinosaurs.
With regard to the pneumatic invasion in the pectoral girdle of Saltasaurus and Neuquensaurus, there are no previous reports of internal cavities in this portion of the skeleton of sauropodomorph dinosaurs. Thus, Saltasaurini titanosaurs are the only known group of sauropodomorph dinosaurs with this character. Given that the scapular girdle is not preserved in Rocasaurus, it is not possible to determine if pneumatic features in this element are present by direct observation. However, since Neuquensaurus is the sister group of the clade formed by Rocasaurus + Saltasaurus (Calvo et al. 2007a, b; González Riga et al. 2009), we hypothesize that camellate tissue and cortical foramina were actually present in the scapula and coracoides of Rocasaurus.
Previous studies have documented the existence of pneumatic features in the anterior and even in the middle caudal vertebrae of some Neosauropoda taxa (Janensch 1947; Salgado et al. 2006; Wedel 2009). However, pneumaticity in the distal portion of the tail as described here for Saltasaurini titanosaurs has not been previously reported in sauropodomorph dinosaurs. Our data reveal an unexpected caudal extension of the pneumatic diverticula from the respiratory system, only comparable to some lineages of non-avian theropods (Benson et al. 2011).
Body size and postcranial pneumaticity
Since the development of PSP is thought to have been very important in the achievement of giant size in sauropodomorph dinosaurs (Sander et al. 2011), the extreme pneumaticity in Saltasaurini is rather unexpected. Saltasaurini titanosaurs represent one of the few cases of phylogenetic decrease in body size among dinosaurs (Wilson 2005). This group has been considered as the “smallest of the giants,” with body lengths that probably did not exceed 7 m. Our data reveal that one of the smallest sauropod clades actually has the most developed PSP. In this sense, although body size seems to be important in the development of PSP in sauropod dinosaurs (Britt 1993; Wedel 2003), this is not the only factor governing the evolution of pneumaticity. A detailed analysis on a larger data set, including species-level information, is necessary to elucidate which are the main factors involved in the development of PSP in sauropod dinosaurs.
Structure of respiratory system
Although the presence of PSP is indicative of air sacs and diverticula, the lack of pneumaticity does not indicate the absence of such pulmonary specializations (O’Connor 2006; Wedel 2003, 2007, 2009). Hence, it is very plausible that the clavicular air sac was actually present in a more inclusive clade of sauropodomorph dinosaurs, but its osteological correlates were only present in Saltasaurini titanosaurs. A similar hypothesis has been proposed for the cervical and abdominal air sacs in basal sauropodomorph dinosaurs, for which unambiguous correlates of PSP are absent or poorly documented (Butler et al. 2012; Wedel 2007, 2009; Yates et al. 2012).
Since PSP has been recorded in different lineages of ornithodiran archosaurs (pterosaurs, sauropodomorph and non-avian theropod dinosaurs), several authors have proposed that the presence of a heterogeneously partitioned pulmonary system is primitive for ornithodiran archosaurs (Benson et al. 2011; Britt 1993; Butler et al. 2012; Wedel 2003, 2007; Yates et al. 2012). The extreme PSP reported here for Saltasaurini titanosaurs, with evidence of cervical, abdominal and clavicular air sacs, reinforces this idea. The independent acquisition of appendicular pneumaticity in pterosaurs (Claessens et al. 2009) and dinosaurs (theropods and derived sauropodomorphs) (Benson et al. 2011; Wedel 2009) emphasizes the tendency for ornithodirans to extensively pneumatize the postcranial skeleton (Benson et al. 2011; Butler et al. 2012).
Osteological features of the axial and appendicular skeleton in Saltasaurini titanosaurs reveal extreme pneumaticity that is unparalleled in other sauropodomorph dinosaurs, with invasion of pneumatic diverticula in the pectoral girdle and the distal portion of the tail. Our result indicates that, besides pterosaurs and theropod dinosaurs, extensive pneumaticity was also reached independently in Sauropodomorpha. Our data also strengthen the hypothesis for the presence of posterior abdominal air sacs in sauropodomorph dinosaurs and provide the first evidence for a clavicular air sac in this lineage. Finally, the record of extreme PSP in Saltasaurini titanosaurs contributes to the growing evidence of widespread, repeated evolution of appendicular and posterior axial skeletal pneumaticity in ornithodiran archosaurs, which in turn indicates that a heterogeneously partitioned pulmonary system is primitive for this group.
We thank Marcelo Reguero, Lucas Pomi, Carlos Muñoz, Norma Brugni and all the staff of Comision Amigos del Museo of Cinco Saltos for access to the specimens under their care, Maia Quintili, Silvia Fasano, Juan José Perazzolo and the authorities of the Policlinico Neuquén for CT scans, Brooks Britt for access to his unpublished PhD thesis, Rodrigo Pellegrini for reading the text and useful comments, Torsten Scheyer for translating the abstract into German and Jorge González for the skeletal reconstruction of Saltasaurus in Fig. 2. The quality of is work has been substantially improved by the useful comments and critical reviews of Roger Benson, Paul Upchurch and Richard Butler. This work was supported by Conicet (PIP 6455 to L.S) and Agencia de Promoción Científica y Técnica (PICT 357 to L.S.).