Locomotion in ornithischian dinosaurs: an assessment using three‐dimensional computational modelling

Abstract

Ornithischian dinosaurs were primitively bipedal with forelimbs modified for grasping, but quadrupedalism evolved in the clade on at least three occasions independently. Outside of Ornithischia, quadrupedality from bipedal ancestors has only evolved on two other occasions, making this one of the rarest locomotory transitions in tetrapod evolutionary history. The osteological and myological changes associated with these transitions have only recently been documented, and the biomechanical consequences of these changes remain to be examined. Here, we review previous approaches to understanding locomotion in extinct animals, which can be broadly split into form-function approaches using analogy based on extant animals, limb-bone scaling, and computational approaches. We then carry out the first systematic attempt to quantify changes in locomotor muscle function in bipedal and quadrupedal ornithischian dinosaurs. Using three-dimensional computational modelling of the major pelvic locomotor muscle moment arms, we examine similarities and differences among individual taxa, between quadrupedal and bipedal taxa, and among taxa representing the three major ornithischian lineages (Thyreophora, Ornithopoda, Marginocephalia). Our results suggest that the ceratopsid Chasmosaurus and the ornithopod Hypsilophodon have relatively low moment arms for most muscles and most functions, perhaps suggesting poor locomotor performance in these taxa. Quadrupeds have higher abductor moment arms than bipeds, which we suggest is due to the overall wider bodies of the quadrupeds modelled. A peak in extensor moment arms at more extended hip angles and lower medial rotator moment arms in quadrupeds than in bipeds may be due to a more columnar hindlimb and loss of medial rotation as a form of lateral limb support in quadrupeds. We are not able to identify trends in moment arm evolution across Ornithischia as a whole, suggesting that the bipedal ancestry of ornithischians did not constrain the development of quadrupedal locomotion via a limited number of functional pathways. Functional anatomy appears to have had a greater effect on moment arms than phylogeny, and the differences identified between individual taxa and individual clades may relate to differences in locomotor performance required for living in different environments or for clade-specific behaviours.

The evolution of ornithischian quadrupedality

“…3). Maidment et al (2014a) also found that the peak in femoral retractor moment arms occurred at more extended hip angles in quadrupedal ornithischians than in bipedal ornithischians (Fig. 4).…”

“…2). PIFI functioned to protract and abduct the femur (Bates et al 2012), and elongation of the preacetabular process in all groups of quadrupedal ornithischian increased the moment arm of this muscle for femoral protraction (Maidment et al 2014a; Fig. 3).…”

“…Similarly, hoof-like manual unguals are also involved in weight bearing (e.g. Norman 1980) and the lateral expansion of the ilium is associated with reorganisation of the hip musculature, which enables increased abduction moment arms that are required for limb stabilisation (Maidment et al 2014a;see below).…”

“…These changes can be related to muscle function and stance, and provide information on the modifications required to the musculoskeletal system that were essential for quadrupedality to evolve (Maidment et al 2014a). …”

“…The manus of bipedal dinosaurs was supinated to allow for grasping (the primitive condition: Sereno 1997), but became pronated during the evolution of quadrupedality to allow weight-bearing. The development of an anterolateral process on the proximal ulna is indicative of this change in both ornithischians and sauropodomorphs (Yates et al 2010;Maidment and Barrett 2014a). In taxa with an anterolateral process, the radius lies medial to the ulna, and the manus is pronated.…”