Elsevier

Cretaceous Research

Volume 93, January 2019, Pages 275-284
Cretaceous Research

Aquatic adaptation in the skull of carnivorous dinosaurs (Theropoda: Spinosauridae) and the evolution of aquatic habits in spinosaurids

https://doi.org/10.1016/j.cretres.2018.06.013Get rights and content

Abstract

The Spinosauridae is a specialized group of theropod dinosaurs characterised by a long, narrow skull, robust forelimbs with a hooked thumb claw, and tall neural spines forming a dorsal sail. The ecology of these unusual dinosaurs has been debated since the original discovery of Spinosaurus aegyptiacus in 1912. Morphological similarities to crocodilians, including tooth shape and an elongated rostrum, indicate a piscivorous diet, and in the giant Spinosaurus, a long body and short limbs suggest semi-aquatic habits. However, the hypothesized aquatic habits of Spinosaurus have been called into question, and the distribution of aquatic habits within Spinosauridae remain unclear. Here, new spinosaurid specimens from the Kem Kem beds of Morocco reveal aquatic adaptations in the cranium. Elevated orbits and bending of the frontals placed the eyes atop the skull, as in semiaquatic animals such as crocodiles and hippos. Two morphologies are present, a smaller morph characterized by narrow, triangular frontals, and a larger morph characterized by broad, subrectangular frontals overlapping the prefrontals. The two morphs suggest two distinct spinosaurine taxa, and are tentatively referred to the spinosaurines Spinosaurus cf. aegyptiacus and Sigilmassasaurus brevicollis, respectively. Semiaquatic habits were widespread within the Spinosaurinae and at least two distinct aquatic spinosaurines inhabited the Cenomanian of North Africa, challenging previous assumptions that non-avian dinosaurs were solely terrestrial. The appearance of giant semiaquatic dinosaurs may have followed the disappearance of giant pholidosaurid crocodylomorphs, suggesting that the extinction of large crocodylomorphs was associated with the rise of dinosaurs as apex predators in the freshwater ecosystem in North Africa.

Introduction

The Spinosauridae is a specialised family of large theropod dinosaurs known from the mid-Cretaceous (Stromer, 1915a, Charig and Milner, 1997, Sereno et al., 1998, Sues et al., 2002). They are characterised by robust forelimbs with a massive thumb claw (Charig and Milner, 1997, Sereno et al., 1998), tall neural spines forming a dorsal sail (Sereno et al., 1998, Allain et al., 2012), and long skulls with conical teeth that are convergent with those of crocodylians (Sereno et al., 1998, Sues et al., 2002, Rayfield et al., 2007). Spinosaurids grew to enormous size, and at least one species, Spinosaurus aegyptiacus, grew as large or larger than Tyrannosaurus rex (dal Sasso et al., 2005). Spinosaurid ecology and feeding habits have been debated, but spinosaurids are thought to be piscivorous (Charig and Milner, 1997, Sereno et al., 1998, Ibrahim et al., 2014, Hone and Holtz, 2017) based on their piercing teeth (Sereno et al., 1998) and the morphology of the skull and jaws, which resemble those of piscivorous crocodilians (Sereno et al., 1998, Rayfield et al., 2007, Ibrahim et al., 2014). Consistent with this hypothesis, spinosaurids are abundant in fluvial and nearshore marine habitats (Benyoucef et al., 2015), where they occur alongside a rich fauna of freshwater fish including sharks, lungfish, and coelacanths (Cavin et al., 2010, Benyoucef et al., 2015), which they most likely fed on (Ibrahim et al., 2014).

Recently it was proposed that the spinosaurine Spinosaurus was not only piscivorous but semi-aquatic based on potential adaptations for aquatic locomotion (Ibrahim et al., 2014). These include reduction of the medullary cavity in the long bones, which increases bone density and reduces buoyancy (Ibrahim et al., 2014), reduction of the pelvic girdle (Ibrahim et al., 2014), and modification of the foot for aquatic propulsion (Ibrahim et al., 2014). Anterior positioning of the center of mass within the ribcage may have also enhanced balance during aquatic movement (Ibrahim et al., 2014). Semiaquatic habits are also suggested by the retracted nostrils (Ibrahim et al., 2014), which would have allowed the animal to breathe while partially submerged, and by stable isotope analyses of tooth enamel (Amiot et al., 2010). However, no complete skeleton is known for Spinosaurus. Reconstructions are based on specimens from different localities (Ibrahim et al., 2014) and possibly different species (Evers et al., 2015), complicating attempts to understand its functional morphology. Furthermore, the extent to which aquatic adaptations characterized other species is unclear, although recently, a tibia from the Aptian-Albian of Brazil was described as exhibiting pachyostosis (Aureliano et al., 2018). The hypothesis of aquatic habits has not, therefore, been universally accepted (Hone and Holtz, 2017).

Here, we describe new fossils that shed light on the ecology of these unusual dinosaurs. The new fossils consist of skull bones from the Kem Kem beds of Morocco (Fig. 1), a deposit that represents floodplain, river, and delta environments (Cavin et al., 2010). These fossils reveal adaptations for aquatic habits in the frontals of two different spinosaurines, which are here tentatively referred to Spinosaurus cf. aegyptiacus and Sigilmassasaurus brevicollis.

Institutional abbreviations: FSAC, Faculté des Science Aïn Chock, Casablanca; NHMUK, Natural History Museum, London.

Section snippets

Geological setting

The Kem Kem beds outcrop in eastern Morocco and comprise a series of sandstones, claystones, gypsum and limestones deposited in continental fluvial to deltaic paleoenvironments. The lower part of the Kem Kem beds have been assigned to the Ifezouane Formation, while the upper part of the Kem Kem has been assigned to the Aoufous Formation (Cavin et al., 2010).

The age of the Kem Kem beds is not known with certainty. On the basis of marine invertebrates, the overlying Akrabou Formation can be

Systematic palaeontology

  • Dinosauria Owen, 1842

  • Saurischia Seeley, 1888

  • Theropoda Marsh, 1881

  • Tetanurae Gauthier, 1986

  • Spinosauridae Stromer, 1915

  • Spinosaurinae Stromer, 1915

  • Spinosaurini new taxon

  • Spinosaurid Morph A = ? cf. Spinosaurus aegyptiacus Stromer, 1915

  • Material. FSAC-KK-3209 (Fig. 2A–D) left frontal with a partial right frontal; FSAC-KK-3210 (Fig. 2E–G) paired frontals and parietals.

  • Locality and horizon. Cenomanian Kem Kem beds, northeast Morocco. FSAC-KK-3209 comes from the Ifezouane Formation exposures at Begaa;

Phylogenetic analysis

We conducted a phylogenetic analysis based on a recent character taxon matrix (Evers et al., 2015). To this matrix we added a number of taxa, including a spinosaur from the Barremian of Portugal (Mateus et al., 2011), Siamosaurus from the Barremian-Aptian of Thailand (Buffetaut and Ingavat, 1986), an unnamed spinosaurid from the Eumeralla Formation of Australia (Barrett et al., 2011), Oxalaia from the Cenomanian of Brazil (Kellner et al., 2011), and a spinosaurid from the Albian of Gara Samani,

Affinities of the Kem Kem frontals

The following combination of characters, shared with Irritator, allow referral of the frontals described here to the Spinosauridae: triangular frontals, participation of frontals in the orbital margins, upturned orbital margins, frontal sagittal crest, strong posterior extension of nasals dorsally over the frontals, and frontals arched in lateral view. The frontals differ from Irritator, and resemble each other, in being fused medially and in having a strongly developed dorsal keel that rises

Conclusions

Frontals from the Kem Kem beds can be referred to Spinosauridae and furthermore represent two distinct taxa, tentatively identified as Spinosaurus cf. aegyptiacus and Sigilmassasaurus brevicollis. Arching of the frontals and upturning of the orbital margins result in the dorsal displacement of the orbits, here interpreted as an adaptation for aquatic habits. These features, along with the elongate body, short limbs, pachyostotic bones, and adaptations for piscivory, support the interpretation

Author contributions

NRL designed the project, TA, NRL, CGK and SZ wrote the manuscript; TA, CGK and NL prepared specimens, NL conducted the phylogenetic analysis, SZ assisted with logistics.

Acknowledgements

Thanks to Mohammed Ben Sekkou for assistance in Morocco and to the people of Begaa, Taouz, and Erfoud. Thanks to the reviewers for comments that have improved this paper. Thanks to Oliver Rauhut for access to Irritator and Anneke van Heteren for access to skulls of extant mammals. Research was supported by the University of Bath (TA, NRL) and Fonds National de la Recherche, Luxembourg, AFR Grant 10142968 (CGK).

References (63)

  • P.M. Barrett et al.

    First spinosaurid dinosaur from Australia and the cosmopolitanism of Cretaceous dinosaur faunas

    Biology Letters

    (2011)
  • S.L. Brusatte et al.

    The first definitive carcharodontosaurid (Dinosauria: Theropoda) from Asia and the delayed ascent of tyrannosaurids

    Naturwissenschaften

    (2009)
  • S.L. Brusatte et al.

    The osteology of Shaochilong maortuensis, a carcharodontosaurid (Dinosauria: Theropoda) from the Late Cretaceous of Asia

    Zootaxa

    (2010)
  • E. Buffetaut et al.

    Unusual theropod dinosaur teeth from the Upper Jurassic of Phu Wiang, northeastern Thailand

    Revue de Paléobiologie

    (1986)
  • E. Buffetaut et al.

    An Early Cretaceous spinosaurid theropod from southern China

    Geological Magazine

    (2008)
  • E. Buffetaut et al.

    The giant crocodilian Sarcosuchus in the Early Cretaceous of Brazil and Niger

    Palaeontology

    (1977)
  • A. Cau et al.

    Evidence of a new carcharodontosaurid from the Upper Cretaceous of Morocco

    Acta Palaeontologica Polonica

    (2012)
  • L. Cavin et al.

    Taxonomic composition and trophic structure of the continental Bony fish assemblage from the Early Late Cretaceous of southeastern Morocco

    PLoS One

    (2015)
  • A.J. Charig et al.

    Baryonyx walkeri, a fish-eating dinosaur from the Wealden of Surrey

    Bulletin of the Natural History Museum of London (Geology)

    (1997)
  • A.A. Chiarenza et al.

    A large abelisaurid (Dinosauria, Theropoda) from Morocco and comments on the Cenomanian theropods from North Africa

    PeerJ

    (2016)
  • J.R. Corfield et al.

    Diversity in olfactory bulb size in birds reflects allometry, ecology, and phylogeny

    Frontiers in Neuroanatomy

    (2015)
  • A.R. Cuff et al.

    Feeding mechanics in spinosaurid theropods and extant crocodilians

    PLoS One

    (2013)
  • C. dal Sasso et al.

    New information on the skull of the enigmatic theropod Spinosaurus, with remarks on its size and affinities

    Journal of Vertebrate Paleontology

    (2005)
  • F.d.L. de Broin

    Elosuchus, a new genus of crocodile from the Cretaceous of the North of Africa

    Comptes Rendus Palevol

    (2002)
  • F. Debroin et al.

    Découverte dún Crocodilien nouveau dans le Crétacé inférieur du Sahara

    Comptes Rendus Hebdomadaires des Seances del Academie Des Sciences Serie D

    (1966)
  • 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)
  • E.S. Gaffney et al.

    Galianemys, a new side-necked turtle (Pelomedusoides: Bothremydidae) from the Late Cretaceous of Morocco

    American Museum Novitates

    (2002)
  • E.S. Gaffney et al.

    Evolution of the side-necked turtles: the families Bothremydidae, Euraxemydidae, and Araripemydidae

    Bulletin of the American Museum of Natural History

    (2006)
  • C. Hendrickx et al.

    Morphofunctional Analysis of the Quadrate of Spinosauridae (Dinosauria: Theropoda) and the Presence of Spinosaurus and a Second Spinosaurine Taxon in the Cenomanian of North Africa

    PLoS One

    (2016)
  • D.W.E. Hone et al.

    A century of Spinosaurus – a review and revision of the Spinosauridae with comments on their ecology

    Acta Geologica Sinica (English Edition)

    (2017)
  • D.A. Hooijer

    Pleistocene remains of hippopotamus from the Orange free State

    Navorsinge van die Nasionale Museum: Researches of the National Museum

    (1958)
  • Cited by (0)

    View full text