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