Susannah C. R. Maidment

Systematics and phylogeny of Stegosauria (Dinosauria: Ornithischia)

Synopsis Stegosauria is a clade of ornithischian dinosaurs characterised by a bizarre array of dermal armour extending, in two parasagittal rows, from the cervical region to the end of the tail. Although Stegosaurus is one of the most familiar of all dinosaurs, little is known regarding the evolutionary history of this clade. Alpha‐level taxonomic revision of all proposed stegosaur taxa shows that 11 species of stego‐saur can be regarded as valid on the basis of autapomorphies. These are: Dacentrurus armatus and Loricatosaurus priscus (gen. nov.) from Europe; Kentrosaurus aethiopicus and Paranthodon afric‐anus from Africa; Tuojiangosaurus multispinus, Chungkingosaurus jiangbeiensis, Huayangosaurus taibaii, Gigantspinosaurus sichuanensis and Stegosaurus homheni (comb. nov.) from China; and Stegosaurus mjosi (comb. nov.) and Stegosaurus armatus from North America. A cladistic analysis of Stegosauria (the first to be based upon direct observation of all relevant specimens) is presented, which indicates that Tuojiangosaurus, Loricatosaurus and Paranthodon are sister taxa to Stegosaurus. Stegosaurinae can be defined as all stegosaurs more closely related to Stegosaurus than to Dacentrurus; Stegosauridae is defined as all stegosaurs more closely related to Stegosaurus than to Huayangosaurus; and Huayangosauridae can be defined as all stegosaurs more closely related to Huayangosaurus than to Stegosaurus. This study is also the first phylogenetic analysis to include Gigantspinosaurus, which is recovered as the most basal stegosaur.

Phylogeny of the ankylosaurian dinosaurs (Ornithischia: Thyreophora)

Ankylosauria is a diverse clade of quadrupedal ornithischian dinosaurs whose remains are known from Middle Jurassic to latest Cretaceous sediments worldwide. Despite a long history of research, ankylosaur interrelationships remain poorly resolved and existing cladistic analyses suffer from limited character and taxon sampling. Here, we present the most comprehensive phylogenetic analysis of the group attempted to date. The traditional ankylosaurid–nodosaurid dichotomy is maintained. Ankylosauridae forms a well-resolved clade, which includes Zhongyuansaurus, the first ankylosaurid known to lack a tail club. Nodosauridae includes a number of taxa that were resolved either as ‘polacanthids’ or basal ankylosaurids in previous analyses. The use of a broader character sample allows analysis of the interrelationships of all valid ankylosaur species; this has revealed several previously unrecognized relationships. Stegosauria is recovered as the sister taxon to Ankylosauria, while Scelidosaurus is found to be a basal thyreophoran. Dedicated methods for coding continuous characters could be used in future to improve the resolution of ankylosaur phylogeny, particularly in order to explore the relationships within the poorly resolved nodosaurid clade.

A new long-necked ‘sauropod-mimic’ stegosaur and the evolution of the plated dinosaurs

Stegosaurian dinosaurs have a quadrupedal stance, short forelimbs, short necks, and are generally considered to be low browsers. A new stegosaur, Miragaia longicollum gen. et sp. nov., from the Late Jurassic of Portugal, has a neck comprising at least 17 cervical vertebrae. This is eight additional cervical vertebrae when compared with the ancestral condition seen in basal ornithischians such as Scutellosaurus. Miragaia has a higher cervical count than most of the iconically long-necked sauropod dinosaurs. Long neck length has been achieved by ‘cervicalization’ of anterior dorsal vertebrae and probable lengthening of centra. All these anatomical features are evolutionarily convergent with those exhibited in the necks of sauropod dinosaurs. Miragaia longicollum is based upon a partial articulated skeleton, and includes the only known cranial remains from any European stegosaur. A well-resolved phylogeny supports a new clade that unites Miragaia and Dacentrurus as the sister group to Stegosaurus; this new topology challenges the common view of Dacentrurus as a basal stegosaur.

The locomotor musculature of basal ornithischian dinosaurs

ABSTRACT The earliest ornithischian dinosaurs were small bipeds that possessed the derived, retroverted pubis that is synapomorphic for the clade. Their forelimbs were modified for grasping. Subsequently, ornithischians radiated into numerous body shapes and sizes. Three lineages independently evolved large size and quadrupedality, requiring profound changes to the osteology and myology of the locomotor apparatus. Using comparisons with extinct archosaurian outgroups, as well as extant birds and crocodilians, we reconstruct basal ornithischian limb musculature in order to determine the sequence of musculoskeletal changes that occurred prior to and during the early evolution of Ornithischia. The musculoskeletal anatomy of basal ornithischian forelimbs was probably more similar to that of the crown group archosaur common ancestor and crocodilians than it was to birds. Reduction or loss of the clavicle resulted in migration of the clavicular deltoid onto the proximal scapula and development of a distinct acromial process. The coracobrachialis brevis and supracoracoideus probably protracted the humerus, whereas the scapulohumeralis caudalis and deltoideus scapularis probably retracted it. The deltoideus clavicularis was likely a humeral abductor. In the hind limb, the elongate preacetabular process indicates lateral migration of important femoral protractors to the ilium from an inferred ancestral location on the dorsal vertebrae. The puboischiofemoralis externus was greatly reduced or possibly lost due to pubic retroversion. The reconstruction of basal ornithischian myology provides a baseline for determining the musculoskeletal changes associated with different locomotor modes in ornithischians, and a foundation for biomechanical studies of dinosaur locomotion.

Fibres and cellular structures preserved in 75-million–year-old dinosaur specimens

Exceptionally preserved organic remains are known throughout the vertebrate fossil record, and recently, evidence has emerged that such soft tissue might contain original components. We examined samples from eight Cretaceous dinosaur bones using nano-analytical techniques; the bones are not exceptionally preserved and show no external indication of soft tissue. In one sample, we observe structures consistent with endogenous collagen fibre remains displaying ∼67 nm banding, indicating the possible preservation of the original quaternary structure. Using ToF-SIMS, we identify amino-acid fragments typical of collagen fibrils. Furthermore, we observe structures consistent with putative erythrocyte remains that exhibit mass spectra similar to emu whole blood. Using advanced material characterization approaches, we find that these putative biological structures can be well preserved over geological timescales, and their preservation is more common than previously thought. The preservation of protein over geological timescales offers the opportunity to investigate relationships, physiology and behaviour of long extinct animals.

Osteological Correlates for Quadrupedality in Ornithischian Dinosaurs

The evolution of quadrupedality from bipedal ancestors is an exceptionally rare transition in tetrapod evolution, but it has occurred several times within the herbivorous dinosaur clade Ornithischia. Stegosauria, Ankylosauria, and Ceratopsidae are all uncontroversially quadrupedal, while basal ornithischians and basal ornithopods are uncontroversially bipedal. However, stance in iguanodontian ornithopods, including the hadrosaurs, and in non-ceratopsid ceratopsians is debated because robust osteological correlates of quadrupedality have not been identified. We examine a suite of characteristics that have been previously proposed as osteological correlates for bipedality or quadrupedality in dinosaurs. These include both discrete anatomical features, which we assess as correlates for quadrupedality using character optimization onto a composite cladogram, and proportional ratios, which we assess as correlates by reconstructing nodal ancestral states using squared-change parsimony, followed by optimization. We also examine the correlation of these features with body size. An anterolateral process on the proximal ulna, hoof-shaped manual unguals, a transversely broadened ilium, a reduced fourth trochanter and a femur longer than the tibia are found to be robust correlates of quadrupedality in ornithischian dinosaurs. Along the ceratopsid “stem” lineage, quadrupedal characters were acquired in a stepwise fashion, with forelimb characters developing prior to changes in the hind limb. In contrast, iguanodontid ornithopods display a mosaic of character states, indicating varying degrees of facultative quadrupedality that probably arose for a variety of different reasons. Hadrosaurs are found to possess all character states associated with quadrupedality and were probably predominantly quadrupedal. In general, quadrupedal ornithischians do not appear to have been constrained by their bipedal ancestry to a particular order of character acquisition.

Limb-Bone Scaling Indicates Diverse Stance and Gait in Quadrupedal Ornithischian Dinosaurs

Background The most primitive ornithischian dinosaurs were small bipeds, but quadrupedality evolved three times independently in the clade. The transition to quadrupedality from bipedal ancestors is rare in the history of terrestrial vertebrate evolution, and extant analogues do not exist. Constraints imposed on quadrupedal ornithischians by their ancestral bipedal bauplan remain unexplored, and consequently, debate continues about their stance and gait. For example, it has been proposed that some ornithischians could run, while others consider that none were cursorial. Methodology/Principal Findings Drawing on biomechanical concepts of limb bone scaling and locomotor theory developed for extant taxa, we use the largest dataset of ornithischian postcranial measurements so far compiled to examine stance and gait in quadrupedal ornithischians. Differences in femoral midshaft eccentricity in hadrosaurs and ceratopsids may indicate that hadrosaurs placed their feet on the midline during locomotion, while ceratopsids placed their feet more laterally, under the hips. More robust humeri in the largest ceratopsids relative to smaller taxa may be due to positive allometry in skull size with body mass in ceratopsids, while slender humeri in the largest stegosaurs may be the result of differences in dermal armor distribution within the clade. Hadrosaurs are found to display the most cursorial morphologies of the quadrupedal ornithischian cades, indicating higher locomotor performance than in ceratopsids and thyreophorans. Conclusions/Significance Limb bone scaling indicates that a previously unrealised diversity of stances and gaits were employed by quadrupedal ornithischians despite apparent convergence in limb morphology. Grouping quadrupedal ornithischians together as a single functional group hides this disparity. Differences in limb proportions and scaling are likely due to the possession of display structures such as horns, frills and dermal armor that may have affected the center of mass of the animal, and differences in locomotor behaviour such as migration, predator escape or home range size.

Computational modelling of locomotor muscle moment arms in the basal dinosaur Lesothosaurus diagnosticus: assessing convergence between birds and basal ornithischians

Ornithischia (the ‘bird‐hipped’ dinosaurs) encompasses bipedal, facultative quadrupedal and quadrupedal taxa. Primitive ornithischians were small bipeds, but large body size and obligate quadrupedality evolved independently in all major ornithischian lineages. Numerous pelvic and hind limb features distinguish ornithischians from the majority of other non‐avian dinosaurs. However, some of these features, notably a retroverted pubis and elongate iliac preacetabular process, appeared convergently in maniraptoran theropods, and were inherited by their avian descendants. During maniraptoran/avian evolution these pelvic modifications led to significant changes in the functions of associated muscles, involving alterations to the moment arms and the activation patterns of pelvic musculature. However, the functions of these features in ornithischians and their influence on locomotion have not been tested and remain poorly understood. Here, we provide quantitative tests of bipedal ornithischian muscle function using computational modelling to estimate 3D hind limb moment arms for the most complete basal ornithischian, Lesothosaurus diagnosticus. This approach enables sensitivity analyses to be carried out to explore the effects of uncertainties in muscle reconstructions of extinct taxa, and allows direct comparisons to be made with similarly constructed models of other bipedal dinosaurs. This analysis supports some previously proposed qualitative inferences of muscle function in basal ornithischians. However, more importantly, this work highlights ambiguities in the roles of certain muscles, notably those inserting close to the hip joint. Comparative analysis reveals that moment arm polarities and magnitudes in Lesothosaurus, basal tetanuran theropods and the extant ostrich are generally similar. However, several key differences are identified, most significantly in comparisons between the moment arms of muscles associated with convergent osteological features in ornithischians and birds. Craniad migration of the iliofemoralis group muscles in birds correlates with increased leverage and use of medial femoral rotation to counter stance phase adduction moments at the hip. In Lesothosaurus the iliofemoralis group maintains significantly higher moment arms for abduction, consistent with the hip abduction mode of lateral limb support hypothesized for basal dinosaurs. Sensitivity analysis highlights ambiguity in the role of musculature associated with the retroverted pubis (puboischiofemoralis externus group) in ornithischians. However, it seems likely that this musculature may have predominantly functioned similarly to homologous muscles in extant birds, activating during the swing phase to adduct the lower limb through lateral rotation of the femur. Overall the results suggest that locomotor muscle leverage in Lesothosaurus (and by inference basal ornithischians in general) was more similar to that of other non‐avian dinosaurs than the ostrich, representing what was probably the basal dinosaur condition. This work thereby contradicts previous hypotheses of ornithischian–bird functional convergence.

A review of the Late Jurassic stegosaurs (Dinosauria, Stegosauria) from the People's Republic of China

Seven genera of stegosaurian dinosaur have been named on the basis of material from the Upper Jurassic of China, and this represents a diversity of stegosaurs unparalleled around the world at this time. However, many of the original specimens used to diagnose and describe these species are currently unavailable, and the original descriptions and figures are often inadequate. The Chinese stegosaurs have proven ‘unstable’ in the few cladistic analyses of Stegosauria that have been carried out, causing a loss of resolution in cladograms. Supplementary data on previously described specimens are presented here along with a taxonomic revision. Only Tuojiangosaurus multispinus, Chungkingosaurus jiangbeiensis and Gigantspinosaurus sichuanensis are considered to be valid taxa, with autapomorphies pertaining to features of the ilio-sacral blocks and dermal armour in all cases. The holotype specimen of ‘Chialingosaurus kuani’ is a juvenile, bearing no diagnostic characters, and ‘Monkonosaurus lawulacus’ is based on fragmentary and undiagnostic material. ‘Changtusaurus’ and ‘Yingshanosaurus’ have never been described or figured and their whereabouts are unknown, so they are regarded as nomina nuda. This taxonomic revision significantly reduces known stegosaurian diversity worldwide, and shows that the Chinese diversity was similar to that of Europe and North America in the Upper Jurassic. Previously, it had been suggested that the diversity of Chinese stegosaurs indicated an Asian origin for the clade, a claim that cannot now be upheld.

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

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.