Elsevier

Cretaceous Research

Volume 127, November 2021, 104925
Cretaceous Research

Vertebral pneumaticity of the paravian theropod Unenlagia comahuensis, from the Upper Cretaceous of Patagonia, Argentina

https://doi.org/10.1016/j.cretres.2021.104925Get rights and content

Highlights

  • Pneumatic features of the dorsal vertebrae of Unenlagia comahuensis are studied.

  • Lateral pneumatic foramina are in the centrum from anterior to posterior dorsals.

  • CT scans revealed camellate tissue in the vertebral centra.

  • Camellae are also observed in other unenlagiines, such as Unenlagia paynemili.

  • This study increases the knowledge of pneumaticity of non-avian theropods.

Abstract

Postcranial skeletal pneumaticity (PSP) characterizes extant birds. This feature is related to a series of air sacs connected to the lungs and prolonged in diverticula that invade bones internally. Previous works revealed that PSP was present along the line to birds, being distinctive of pterosaurs and saurischian dinosaurs. PSP is profuse in the vertebral column of sauropods and theropods and was very studied in sauropods, although scarcely in non-avian theropods. Here we analyze the vertebral pneumaticity of the unenlagiine theropod Unenlagia comahuensis, including the observation through CT scans. Unenlagiinae is a clade of southern dromaeosaurid theropods that is closely related to birds. The vertebral centra have lateral pneumatic foramina (lpf) within fossae (commonly termed ‘pleurocoels’) in middle and posterior dorsals, an unusual feature among extant birds and many non-avian theropods. Another possibly pneumatic fossa stands out at both sides of the neural spine base, which is not present in dorsals of other non-avian theropods, except the unenlagiine Unenlagia paynemili. CT scans revealed camellate tissue in the centra, consisting of small chambers separated by thin trabeculae. Camellae are also observed in the unenlagiines U. paynemili and Austroraptor cabazai, other dromaeosaurids, other coelurosaurs, and some non-coelurosaurian tetanurans. Instead, more primitive groups generally have camerae (larger chambers separated by scarce thick septa). Thus, a possible trend of the vertebral inner pneumaticity types is observed throughout non-avian theropod evolution, as indicated by previous authors. This study provides valuable information that helps to clarify this trend, not only in dromaeosaurids but also throughout theropod evolution.

Introduction

Dromaeosaurids are highly derived theropods related to birds. The first discoveries of dromaeosaurids began in the ‘20s of the last century, with Dromaeosaurus albertensis (Matthew and Brown, 1922) and Velociraptor mongoliensis (Osborn, 1924) in Canada and Mongolia, respectively. Since that time, all dromaeosaurid remains were found in the Northern Hemisphere, mostly in Asia and North America (Gianechini and Apesteguía, 2011).

The separation of the supercontinent Pangea into a northern Laurasia and a southern Gondwana, during the Jurassic, possibly generated a vicarious evolution event between the unenlagiines in the south and the remaining dromaeosaurids in the north (Makovicky et al., 2005; Novas and Pol, 2005).

In the ‘90s, a new theropod (Unenlagia comahuensis) with characters shared with dromaeosaurids and birds was found in Cretaceous outcrops of Argentina (Novas and Puerta, 1997). In later years, other theropod specimens were found in southern landmasses, which had common features with U. comahuensis. Bonaparte (1999) observed that U. comahuensis shares characters with the Malagascan taxon Rahonavis ostromi (Forster et al., 1998), and considered that they are members of the same family, which he established as Unenlagiidae. With the discovery and description of Buitreraptor gonzalezorum, new phylogenetic analyses clustered these taxa in a monophyletic group, within Dromaeosauridae, which they established as Unenlagiinae (Makovicky et al., 2005).

Among extant tetrapods, only birds have postcranial skeletal pneumaticity (Duncker, 1971; O'Connor, 2006), However, this feature is present in the evolutionary line of the ornithodirans, specifically in pterosaurs and saurischian dinosaurs, from the Late Triassic (Britt, 1997; Wedel, 2009; Benson et al., 2012). The pneumatic system consists of bone correlates, such as fossae, foramina, camellate tissue or camerae, and soft tissue (respiratory system), including the lungs and their nine air sacs. Epithelial extensions, called ‘diverticula’, are released from these air sacs, which penetrate the bones through foramina (King, 1966; Duncker, 1971).

In the case of non-avian theropods, postcranial pneumaticity is restricted to the axial skeleton and some scarce appendicular bones, and the location of foramina is similar to that of foramina in birds (O'Connor and Claessens, 2005; O'Connor, 2006; Benson et al., 2012).

The goal of this work is to present a study of the vertebral pneumaticity of Unenlagia comahuensis. This includes a detailed description of the fossae and foramina and a visualization of the internal pneumaticity using CT scans. These results will be compared with that seen in other dromaeosaurids, and especially in other unenlagiines.

Section snippets

Anatomical description and computed tomography scans

The holotype specimen of Unenlagia comahuensis (MCF-PVPH 78) was found in outcrops of the Portezuelo Formation (Turonian–Coniacian), in the Sierra de Portezuelo, center-east of Neuquén Province, Argentina (Novas and Puerta, 1997; Novas et al., 2021; Fig. 1). The materials here analyzed are part of the holotype and consist of three dorsal vertebrae (Fig. 2, Fig. 3, Fig. 4, Fig. 5, Fig. 6), which were interpreted as 8th, 10th and 13th in position (Novas et al., 2021). As the 13th vertebra is the

Description of the external vertebral pneumaticity

The anterior surface of the neural arches shows right and left centroprezygapophyseal fossae (cprf). These are bounded laterally by the centroprezygapophyseal lamina (cprl) and the prezygoparapophyseal lamina (prpl), dorsomedially by the intraprezygapophyseal lamina (tprl), medially by the neural canal, and dorsally by the prezygapophysis (Fig. 2). The cprf of the 13th vertebra are less developed. Inside each cprf of the 8th and 10th vertebrae, two foramina are observed, one of them is larger

Discussion

The presence of internal camellate tissue in the vertebrae of the unenlagiines is not unexpected, since it is a common trait in derived coelurosaurs (e.g. Britt, 1993; Sues and Averianov, 2016a; Forster et al., 2020; Smith et al., 2021; see below). U. comahuensis confirms that the lpf communicates with the internal camellae. Previous authors have explained that the only non-ambiguous evidence of pneumaticity in bones is the presence of internal chambers that are continuous with the exterior

Conclusions

The external and internal pneumaticity of the dorsal vertebrae of Unenlagia comahuensis were described in this work. Notable external pneumatic traits are the presence of well-developed lpf throughout the dorsal series along with the presence of a fossa (posdf) at both sides of the neural spine of the last (13th) dorsal, all of which have internal foramina that seem to communicate with the interior. The lpf are extended through the entire dorsal series in several groups of non-avian theropods,

Acknowledgments

The authors of this work thank Dr Rodolfo Coria and Ludmila Coria (MCF) for allowing us access to the material of Unenlagia comahuensis, and Daniel Cabaza (MML), Carlos Muñóz (MPCA), Jorge Calvo (MUCPv), Carl Mehling (AMNH), and Daniel Brinkman (YPM) for allowing access to the fossil collections under their care. We also want to especially thank Sanatorio Plaza Huincul for allowing us to perform the CT scans. Thanks to Mattia Baiano and Guillermo Windholz for assistance in the review of the

References (101)

  • C.T. Barker et al.

    A highly pneumatic middle Cretaceous theropod from the British Lower Greensand

    Papers in Palaeontology

    (2020)
  • R.B.J. Benson et al.

    Air-filled postcranial bones in theropod dinosaurs: physiological implications and the ‘reptile’-bird transition

    Biological Reviews

    (2012)
  • J.F. Bonaparte

    Tetrapod faunas from South America and India: a palaeobiogeographic interpretation

    Proceedings of the Indian Natural Sciences Academy

    (1999)
  • B.B. Britt

    Theropods of Dry Mesa Quarry (Morrison Formation, Late Jurassic), Colorado, with emphasis on the osteology of Torvosaurus tanneri

    Brigham Young University Geology Studies

    (1991)
  • B.B. Britt

    Pneumatic postcranial bones in dinosaurs and other archosaurs

    (1993)
  • B.B. Britt

    Postcranial pneumaticity

  • B.B. Britt et al.

    Postcranial pneumatization in Archaeopteryx

    Nature

    (1998)
  • C.A. Brochu

    Osteology of Tyrannosaurus Rex: insights from a nearly complete skeleton and high resolution computed tomographic analysis of the skull

    Journal of Vertebrate Paleontology

    (2003)
  • S.L. Brusatte et al.

    The osteology of Balaur bondoc, an island-dwelling dromaeosaurid (Dinosauria: Theropoda) from the Late Cretaceous of Romania

    Bulletin of the American Museum of Natural History

    (2013)
  • D.A. Burnham

    New information on Bambiraptor feinbergi (Theropoda: Dromaeosauridae) from the Late Cretaceous of Montana

  • J.O. Calvo et al.
    (2004)
  • K. Carpenter et al.

    Redescription of the small maniraptoran theropods Ornitholestes and Coelurus from the Upper Jurassic Morrison Formation of Wyoming

  • A. Cau et al.

    The phylogenetic affinities of the bizarre Late Cretaceous Romanian theropod Balaur bondoc (Dinosauria, Maniraptora): dromaeosaurid or flightless bird?

    PeerJ

    (2015)
  • A. Cau et al.

    Synchrotron scanning reveals amphibious ecomorphology in a new clade of bird-like dinosaurs

    Nature

    (2017)
  • L.M. Chiappe

    Osteology of the flightless Patagopteryx deferrariisi from the Late Cretaceous of Patagonia (Argentina)

  • L.M. Chiappe et al.

    Skeletal morphology and systematics of the Cretaceous Euenantiornithes (Ornithothoraces: Enantiornithes)

  • L.M. Chiappe et al.

    Anatomy and systematics of the Confuciusornithidae (Theropoda: Aves) from the Late Mesozoic of northeastern China

    Bulletin of the American Museum of Natural History

    (1999)
  • L.M. Chiappe et al.

    New enantiornithine bird from the marine Upper Cretaceous of Alabama

    Journal of Vertebrate Paleontology

    (2002)
  • L.M. Chiappe et al.

    A new specimen of the Early Cretaceous bird Hongshanornis longicresta: insights into the aerodynamics and diet of a basal ornithuromorph

    PeerJ

    (2014)
  • P. Christiansen et al.

    Axial and appendicular pneumaticity in Archaeopteryx

    Proceedings of the Royal Society of London Series B

    (2000)
  • J.A. Clarke

    Morphology, phylogenetic taxonomy, and systematics of Ichthyornis and Apatornis (Avialae: Ornithurae)

    Bulletin of the American Museum of Natural History

    (2004)
  • P.J. Currie et al.

    New information on Cretaceous troodontids (Dinosauria, Theropoda) from the People‘s Republic of China

    Canadian Journal of Earth Sciences

    (2001)
  • H. Duncker

    Structure of avian lungs

    Respiration Physiology

    (1971)
  • A. Elzanowski

    Archaeopterygidae (Upper Jurassic of Germany)

  • S.W. Evers et al.

    A reappraisal of the morphology and systematic position of the theropod dinosaur Sigilmassasaurus from the “middle” Cretaceous of Morocco

    PeerJ

    (2015)
  • C.A. Forster et al.

    The theropod ancestry of birds: new evidence from the Late Cretaceous of Madagascar

    Nature

    (1998)
  • C.A. Forster et al.

    The osteology of the Late Cretaceous paravian Rahonavis ostromi from Madagascar

    Palaeontologia Electronica

    (2020)
  • F.A. Gianechini et al.

    Unenlagiinae revisited: dromaeosaurid theropods from South America

    Anais da Academia Brasileira de Ciências

    (2011)
  • G. Han et al.

    A new raptorial dinosaur with exceptionally long feathering provides insights into dromaeosaurid flight performance

    Nature Communications

    (2014)
  • B.P. Hedrick et al.

    The slothful claw: osteology and taphonomy of Nothronychus mckinleyi and N. graffami (Dinosauria: Theropoda) and anatomical considerations for derived therizinosaurids

    PloS One

    (2015)
  • S. Hope

    The Mesozoic radiation of Neornithes

  • D. Hu et al.

    A pre-Archaeopteryx troodontid theropod from China with long feathers on the metatarsus

    Nature

    (2009)
  • H. Hu et al.

    New anatomical information on the bohaiornithid Longusunguis and the presence of a plesiomorphic diapsid skull in Enantiornithes

    Journal of Systematic Palaeontology

    (2020)
  • S.H. Hwang et al.

    New specimens of Microraptor zhaoianus (Theropoda: Dromaeosauridae) from northeastern China

    American Museum Novitates

    (2002)
  • A.A. Karhu et al.

    A new family of Maniraptora (Dinosauria: Saurischia) from the Late Cretaceous of Mongolia

    Paleontological Journal

    (1996)
  • U. Lefèvre et al.

    A new long-tailed basal bird from the Lower Cretaceous of north-eastern China

    Biological Journal of the Linnean Society

    (2014)
  • U. Lefèvre et al.

    A new Jurassic theropod from China documents a transitional step in the macrostructure of feathers

    Science and Nature

    (2017)
  • N.R. Longrich et al.

    A microraptorine (Dinosauria–Dromaeosauridae) from the Late Cretaceous of North America

    Proceedings of the National Academy of Sciences of the United States of America

    (2009)
  • J.H. Madsen

    Allosaurus fragilis: a revised osteology

    Utah Geological and Mineral Survey, Bulletin

    (1976)
  • P.J. Makovicky et al.

    The earliest dromaeosaurid theropod from South America

    Nature

    (2005)
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