Naturwissenschaften DOI 10.1007/s00114-014-1239-2 ORIGINAL PAPER What drove reversions to quadrupedality in ornithischian dinosaurs? Testing hypotheses using centre of mass modelling Susannah C. R. Maidment & Donald M. Henderson & Paul M. Barrett Received: 22 April 2014 /Revised: 5 August 2014 /Accepted: 4 September 2014 # Springer-Verlag Berlin Heidelberg 2014 Abstract The exceptionally rare transition to quadrupedalism evolutionary pathways to convergent quadrupedal from bipedal ancestors occurred on three independent occa- morphology. sions in ornithischian dinosaurs. The possible driving forces behind these transitions remain elusive, but several hypothe- Keywords Ornithischia . Quadrupedality . 3D mathematical ses—including the development of dermal armour and the slicing . Centre of mass expansion of head size and cranial ornamentation—have been proposed to account for this major shift in stance. We modelled the position of the centre of mass (CoM) in several Introduction exemplar ornithischian taxa and demonstrate that the anterior shifts in CoM position associated with the development of an Ornithischia was a diverse dinosaur clade that dominated the enlarged skull ornamented with horns and frills for display/ terrestrial herbivorous vertebrate niche throughout much of defence may have been one of the drivers promoting ceratop- the Mesozoic. Early forms were small (~1 m long) animals sian quadrupedality. A posterior shift in CoM position coin- (Butler et al. 2008), but they diversified into a variety of small cident with the development of extensive dermal armour in and large quadrupedal and bipedal megaherbivores. All major thyreophorans demonstrates this cannot have been a primary ornithischian subclades (Thyreophora, Ornithopoda, causative mechanism for quadrupedality in this clade. Marginocephalia) include members that developed a variety Quadrupedalism developed in response to different selective of elaborate cranial or dermal structures, including pressures in each ornithischian lineage, indicating different hypertrophied osteoderms in thyreophorans, cranial horns and frills in ceratopsians (Marginocephalia), and elaborate Communicated by: Robert R. Reisz nasal crests in hadrosaurids (Ornithopoda), that were likely related to display, defence or intraspecific behaviours (Fig. 1; Electronic supplementary material The online version of this article (doi:10.1007/s00114-014-1239-2) contains supplementary material, Ostrom 1962; Galton 1970a;Hopson1975;Farlowand which is available to authorized users. Dodson 1975; Farlow et al. 1976; Molnar 1977; Coombs 1979;Thulborn1993). S. C. R. Maidment : P. M. Barrett Department of Earth Sciences, The Natural History Museum, Quadrupedality evolved at least three times within Cromwell Road, London SW7 5BD, UK Ornithischia: once in Thyreophora (in the common ancestor P. M. Barrett of Scelidosaurus, stegosaurs and ankylosaurs), once in e-mail: [email protected] Marginocephalia (at some point on the ‘stem lineage’ to ceratopsids) and at least once in Ornithopoda (once in * S. C. R. Maidment ( ) hadrosaurids, and possibly in some non-hadrosaurid Department of Earth Science and Engineering, South Kensington Campus, Imperial College, London SW7 2AZ, UK iguanodontians; Fig. 1 [Maidment and Barrett 2012, 2014]). e-mail: [email protected] The evolution of quadrupedality from a bipedal ancestor is an exceptionally rare transition in the history of tetrapod evolu- D. M. Henderson tion, having only occurred in the sauropodomorph sauris- Royal Tyrrell Museum, Highway 838, Midland Provincial Park, Drumheller, AB T0J 0Y0, Canada chians (Bonnan 2003; Yates et al. 2010) and the silesaurid e-mail: [email protected] dinosauriformes (Nesbitt et al. 2010) outside of Ornithischia. Naturwissenschaften Fig. 1 Ornithischian relationships Psittacosaurus Scelidosaurus Scutellosaurus The repeated evolution of quadrupedality from bipedal ances- Triceratops (Hatcher et al. 1907), which possessed some of tors within Ornithischia is therefore unprecedented, but the the largest heads among vertebrates, measured either abso- subject has received little attention, and the evolutionary lutely or relative to trunk length (Sereno et al. 2007). For drivers that led to the recurrent adoption of quadrupedality example, the ceratopsid Pentaceratops has a skull+ in Ornithischia remain elusive. Determining the possible se- parietosquamosal frill length that is 118 % of trunk length lection pressures that drove bipedal taxa to revert to a quadru- (measured as the distance between the shoulder glenoid and pedal condition is therefore of interest in terms of understand- acetabulum). Sereno et al. (2007) suggested that a head length ing the full pattern of tetrapod locomotory and biomechanical greater than 40 % of trunk length would only be possible in a evolution. quadrupedal animal. Thyreophoran dinosaurs are characterized by an array of We aim to examine quantitatively the effects of previously postcranial dermal armour extending from the neck to the tip proposed morphological drivers on ornithischian stance, of the tail. Basal members of Thyreophora (Scutellosaurus based on the assumption that any measurable causative mech- [Colbert 1981]; Emausaurus [Haubold 1990]) have numerous anism for reversion to quadrupedality must result in an ante- small osteoderms on all body regions, and these are rior movement of the centre of mass (CoM). We also take the hypertrophied in more derived thyreophorans. Ankylosaurs opportunity to model the CoM in a hadrosaurid ornithopod to possess a variety of large conical, flat and spike-like examine stance in this clade. The stance of iguanodontian osteoderms, and smaller polygonal plates that sometimes fuse ornithopods, and particularly of hadrosaurids, has always been to form mosaic-like pavements covering the dorsal surface of controversial (e.g. review in Norman 1980). Galton (1970b) the body (as well as osteoderms associated with the skull and argued that hadrosaurids were bipedal on the basis of their mandible), whereas stegosaurs possess plate-like or spinose osteology, while others have presented evidence from track- osteoderms that extend in two parasagittal rows along the ways (Lockley and Wright 2001), limb proportions (Dilkes back. On the basis of his work on the basal thyreophoran 2001) and soft tissues (Sellers et al. 2009) that they may have Scutellosaurus, Colbert (1981) suggested that primitive been at least facultatively quadrupedal. Maidment and Barrett thyreophorans might have been facultatively quadrupedal (2014) suggested that hadrosaurids possessed a number of due to the need to provide additional support to resist the osteological correlates indicative of habitual quadrupedality. weight of this armour. In a bipedal animal, CoM must be located above the hind Some ceratopsian dinosaurs possess cranial ornamentation feet in order for the animal to balance in equilibrium. A such as a frill (composed of elongated squamosals and parie- quadruped is not constrained in this regard, and the CoM tals) and horns (which are located dorsal to the orbit, on the can lie further anteriorly so that body mass is distributed jugal and projecting dorsally from the nasal). These features between the fore- and hind limbs. A CoM located anterior to are present incipiently in neoceratopsians (e.g. Protoceratops the foot can only occur in an animal that is an obligate [Brown and Schlaikjer 1940]), but are developed to their quadruped. However, a CoM located over the hind foot does greatest extent in the ceratopsids, such as Chasmosaurus and not necessarily indicate bipedality. In contrast, it could occur Naturwissenschaften in a quadrupedal animal that has evolved quadrupedality for Stegosaurus and Euoplocephalus are universally reconstruct- reasons other than an anterior shift in CoM, such as a prefer- ed as quadrupedal (Gilmore 1914;Coombs1978). ence for low browse. ThedistributionofarmouronScelidosaurus, Stegosaurus Herein, we mathematically model the CoMs of various and Euoplocephalus is known because several specimens ornithischian dinosaurs to test the following hypotheses: preserve the armour in situ (NHMUK R1111; USNM [Na- tional Museum of Natural History, Smithsonian Institution, 1. Thyreophorans became quadrupedal because the addi- Washington D.C., U.S.A.] 4934; NHMUK R5161); however, tional mass of dermal armour forced their CoM to move the armour of Scutellosaurus was not found in situ, and so its anteriorly. distribution on the body is conjectural. The reconstruction of 2. Ceratopsians became quadrupedal because the additional the armour of Scutellosaurus was based on that of Colbert mass of extensive cranial ornamentation forced their CoM (1981) with additional information from the position of ar- to move anteriorly. mour in ankylosaurs and stegosaurs. 3. CoM location in hadrosaurids would have allowed them The basal ceratopsian Psittacosaurus is known from many to exploit both bipedal and quadrupedal locomotion. complete and partially complete skeletons (Osborn 1923; Sereno 2010) and was chosen to represent the basal ceratop- sian condition. Psittacosaurus lacks morphological indicators of quadrupedality (Maidment and Barrett 2014), although Methods evidence from limb bone scaling suggests that juveniles of this taxon may have been quadrupedal (Zhao et al. 2013). The Taxon selection In order to investigate changes in CoM asso- chasmosaurine ceratopsid Chasmosaurus was chosen to rep- ciated with reversions to quadrupedality, basal and derived resent a derived ceratopsian.