Nitrogen isotopes reveal independent origins of N2-fixing symbiosis in extant cycad lineages.

Cycads are ancient seed plants (gymnosperms) that emerged by the early Permian. Although they were common understory flora and food for dinosaurs in the Mesozoic, their abundance declined markedly in the Cenozoic. Extant cycads persist in restricted populations in tropical and subtropical habitats and, with their conserved morphology, are often called 'living fossils.' All surviving taxa receive nitrogen from symbiotic N2-fixing cyanobacteria living in modified roots, suggesting an ancestral origin of this symbiosis. However, such an ancient acquisition is discordant with the abundance of cycads in Mesozoic fossil assemblages, as modern N2-fixing symbioses typically occur only in nutrient-poor habitats where advantageous for survival. Here, we use foliar nitrogen isotope ratios-a proxy for N2 fixation in modern plants-to probe the antiquity of the cycad-cyanobacterial symbiosis. We find that fossilized cycad leaves from two Cenozoic representatives of extant genera have nitrogen isotopic compositions consistent with microbial N2 fixation. In contrast, all extinct cycad genera have nitrogen isotope ratios that are indistinguishable from co-existing non-cycad plants and generally inconsistent with microbial N2 fixation, pointing to nitrogen assimilation from soils and not through symbiosis. This pattern indicates that, rather than being ancestral within cycads, N2-fixing symbiosis arose independently in the lineages leading to living cycads during or after the Jurassic. The preferential survival of these lineages may therefore reflect the effects of competition with angiosperms and Cenozoic climatic change.

Palaeopathological evidence for intraspecific combat in ankylosaurid dinosaurs.

Ankylosaurid dinosaurs were heavily armoured herbivores with tails modified into club-like weapons. These tail clubs have widely been considered defensive adaptations wielded against predatory theropod dinosaurs. Here we argue instead that ankylosaurid tail clubs were sexually selected structures used primarily for intraspecific combat. We found pathological osteoderms (armour plates) in the holotype specimen of Zuul crurivastator, which are localized to the flanks in the hip region rather than distributed randomly across the body, consistent with injuries inflicted by lateral tail-swinging and ritualized combat. We failed to find convincing evidence for predation as a key selective pressure in the evolution of the tail club. High variation in tail club size through time, and delayed ontogenetic growth of the tail club further support the sexual selection hypothesis. There is little doubt that the tail club could have been used in defence when needed, but our results suggest that sexual selection drove the evolution of this impressive weapon. This changes the prevailing view of ankylosaurs, suggesting they were behaviorally complex animals that likely engaged in ritualized combat for social dominance as in other ornithischian dinosaurs and mammals.

The phylogenetic nomenclature of ornithischian dinosaurs.

Ornithischians form a large clade of globally distributed Mesozoic dinosaurs, and represent one of their three major radiations. Throughout their evolutionary history, exceeding 134 million years, ornithischians evolved considerable morphological disparity, expressed especially through the cranial and osteodermal features of their most distinguishable representatives. The nearly two-century-long research history on ornithischians has resulted in the recognition of numerous diverse lineages, many of which have been named. Following the formative publications establishing the theoretical foundation of phylogenetic nomenclature throughout the 1980s and 1990s, many of the proposed names of ornithischian clades were provided with phylogenetic definitions. Some of these definitions have proven useful and have not been changed, beyond the way they were formulated, since their introduction. Some names, however, have multiple definitions, making their application ambiguous. Recent implementation of the International Code of Phylogenetic Nomenclature (ICPN, or PhyloCode) offers the opportunity to explore the utility of previously proposed definitions of established taxon names. Since the Articles of the ICPN are not to be applied retroactively, all phylogenetic definitions published prior to its implementation remain informal (and ineffective) in the light of the Code. Here, we revise the nomenclature of ornithischian dinosaur clades; we revisit 76 preexisting ornithischian clade names, review their recent and historical use, and formally establish their phylogenetic definitions. Additionally, we introduce five new clade names: two for robustly supported clades of later-diverging hadrosaurids and ceratopsians, one uniting heterodontosaurids and genasaurs, and two for clades of nodosaurids. Our study marks a key step towards a formal phylogenetic nomenclature of ornithischian dinosaurs.

Tail Weaponry in Ankylosaurs and Glyptodonts: An Example of a Rare but Strongly Convergent Phenotype.

The unusual clubbed tails of glyptodonts among mammals and ankylosaurines among dinosaurs most likely functioned as weapons of intraspecific combat or interspecific defense and are characterized by stiffening of the distal tail and, in some taxa, expansion of the distal tail tip. Although similarities in tail weaponry have been noted as a potential example of convergent evolution, this hypothesis has not been tested quantitatively, particularly with metrics that can distinguish convergence from long-term stasis, assess the relative strength of convergence, and identify potential constraints in the appearance of traits during the stepwise, independent evolution of these structures. Using recently developed metrics of convergence within a phylomorphospace framework, we document that convergence accounts for over 80% of the morphological evolution in traits associated with tail weaponry in ankylosaurs and glyptodonts. In addition, we find that ankylosaurs and glyptodonts shared an independently derived, yet constrained progression of traits correlated with the presence of a tail club, including stiffening of the distal tail as a precedent to expansion of the tail tip in both clades. Despite differences in the anatomical construction of the tail club linked to lineage-specific historical contingency, these lineages experienced pronounced, quantifiable convergent evolution, supporting hypotheses of functional constraints and shared selective pressures on the evolution of these distinctive weapons. Anat Rec, 303:988-998, 2020. © 2019 Wiley Periodicals, Inc.

A new leptoceratopsid dinosaur from Maastrichtian-aged deposits of the Sustut Basin, northern British Columbia, Canada.

A partial dinosaur skeleton from the Sustut Basin of northern British Columbia, Canada, previously described as an indeterminate neornithischian, is here reinterpreted as a leptoceratopsid ceratopsian, Ferrisaurus sustutensis, gen. et. sp. nov. The skeleton includes parts of the pectoral girdles, left forelimb, left hindlimb, and right pes. It can be distinguished from other named leptoceratopsids based on the proportions of the ulna and pedal phalanges. This is the first unique dinosaur species reported from British Columbia, and can be placed within a reasonably resolved phylogenetic context, with Ferrisaurus recovered as more closely related to Leptoceratops than Montanoceratops. At 68.2-67.2 Ma in age, Ferrisaurus falls between, and slightly overlaps with, both Montanoceratops and Leptoceratops, and represents a western range extension for Laramidian leptoceratopsids.

Puncture-and-Pull Biomechanics in the Teeth of Predatory Coelurosaurian Dinosaurs.

The teeth of putatively carnivorous dinosaurs are often blade-shaped with well-defined serrated cutting edges (Figure 1). These ziphodont teeth are often easily differentiated based on the morphology and density of the denticles [1, 2]. A tearing function has been proposed for theropod denticles in general [3], but the functional significance of denticle phenotypic variation has received less attention. In particular, the unusual hooked denticles found in troodontids suggest a different feeding strategy or diet compared to other small theropods. We used a two-pronged approach to investigate the function of denticle shape variation across theropods with both congruent body shapes and sizes (e.g., dromaeosaurids versus troodontids) and highly disparate body shapes and sizes (e.g., troodontids versus tyrannosaurids), using microwear and finite element analyses (Figure 1). We found that many toothed coelurosaurian theropods employed a puncture-and-pull feeding movement, in which parallel scratches form while biting down into prey and oblique scratches form as the head is pulled backward with the jaws closed. In finite element simulations, theropod teeth had the lowest stresses when bite forces were aligned with the oblique family of microwear scratches. Different denticle morphologies performed differently under a variety of simulated biting angles: Dromaeosaurus and Saurornitholestes were well-adapted for handling struggling prey, whereas troodontid teeth were more likely to fail at non-optimal bite angles. Troodontids may have favored softer, smaller, or immobile prey.

The evolution of tail weaponization in amniotes.

Weaponry, for the purpose of intraspecific combat or predator defence, is one of the most widespread animal adaptations, yet the selective pressures and constraints governing its phenotypic diversity and skeletal regionalization are not well understood. Here, we investigate the evolution of tail weaponry in amniotes, a rare form of weaponry that nonetheless evolved independently among a broad spectrum of life including mammals, turtles and dinosaurs. Using phylogenetic comparative methods, we test for links between morphology, ecology and behaviour in extant amniotes known to use the tail as a weapon, and in extinct taxa bearing osseous tail armaments. We find robust ecological and morphological correlates of both tail lashing behaviour and bony tail weaponry, including large body size, body armour and herbivory, suggesting these life-history parameters factor into the evolution of antipredator behaviours and tail armaments. We suggest that the evolution of tail weaponry is rare because large, armoured herbivores are uncommon in extant terrestrial faunas, as they have been throughout evolutionary history.

A new ankylosaurine dinosaur from the Judith River Formation of Montana, USA, based on an exceptional skeleton with soft tissue preservation.

The terrestrial Judith River Formation of northern Montana was deposited over an approximately 4 Myr interval during the Campanian (Late Cretaceous). Despite having been prospected and collected continuously by palaeontologists for over a century, few relatively complete dinosaur skeletons have been recovered from this unit to date. Here we describe a new genus and species of ankylosaurine dinosaur, Zuul crurivastator, from the Coal Ridge Member of the Judith River Formation, based on an exceptionally complete and well-preserved skeleton (ROM 75860). This is the first ankylosaurin skeleton known with a complete skull and tail club, and it is the most complete ankylosaurid ever found in North America. The presence of abundant soft tissue preservation across the skeleton, including in situ osteoderms, skin impressions and dark films that probably represent preserved keratin, make this exceptional skeleton an important reference for understanding the evolution of dermal and epidermal structures in this clade. Phylogenetic analysis recovers Zuul as an ankylosaurin ankylosaurid within a clade of Dyoplosaurus and Scolosaurus, with Euoplocephalus being more distantly related within Ankylosaurini. The occurrence of Z. crurivastator from the upper Judith River Formation fills a gap in the ankylosaurine stratigraphic and geographical record in North America, and further highlights that Campanian ankylosaurines were undergoing rapid evolution and stratigraphic succession of taxa as observed for Laramidian ceratopsids, hadrosaurids, pachycephalosaurids and tyrannosaurids.

A small azhdarchoid pterosaur from the latest Cretaceous, the age of flying giants.

Pterosaur fossils from the Campanian-Maastrichtian of North America have been reported from the continental interior, but few have been described from the west coast. The first pterosaur from the Campanian Northumberland Formation (Nanaimo Group) of Hornby Island, British Columbia, is represented here by a humerus, dorsal vertebrae (including three fused notarial vertebrae), and other fragments. The elements have features typical of Azhdarchoidea, an identification consistent with dominance of this group in the latest Cretaceous. The new material is significant for its size and ontogenetic stage: the humerus and vertebrae indicate a wingspan of ca 1.5 m, but histological sections and bone fusions indicate the individual was approaching maturity at time of death. Pterosaurs of this size are exceedingly rare in Upper Cretaceous strata, a phenomenon commonly attributed to smaller pterosaurs becoming extinct in the Late Cretaceous as part of a reduction in pterosaur diversity and disparity. The absence of small juveniles of large species-which must have existed-in the fossil record is evidence of a preservational bias against small pterosaurs in the Late Cretaceous, and caution should be applied to any interpretation of latest Cretaceous pterosaur diversity and success.

The furculae of the dromaeosaurid dinosaur Dakotaraptor steini are trionychid turtle entoplastra.

Dakotaraptor steini is a recently described dromaeosaurid dinosaur from the Upper Cretaceous (Maastrichtian) Hell Creek Formation of South Dakota. Included within the D. steini hypodigm are three elements originally identified as furculae, one of which was made part of the holotype specimen. We show that the elements described as D. steini 'furculae' are not theropod dinosaur furculae, but are rather trionychid turtle entoplastra referable to cf. Axestemys splendida. The hypodigm of D. steini should be adjusted accordingly.

Ankylosaurid dinosaur tail clubs evolved through stepwise acquisition of key features.

Ankylosaurid ankylosaurs were quadrupedal, herbivorous dinosaurs with abundant dermal ossifications. They are best known for their distinctive tail club composed of stiff, interlocking vertebrae (the handle) and large, bulbous osteoderms (the knob), which may have been used as a weapon. However, tail clubs appear relatively late in the evolution of ankylosaurids, and seemed to have been present only in a derived clade of ankylosaurids during the last 20 million years of the Mesozoic Era. New evidence from mid Cretaceous fossils from China suggests that the evolution of the tail club occurred at least 40 million years earlier, and in a stepwise manner, with early ankylosaurids evolving handle-like vertebrae before the distal osteoderms enlarged and coossified to form a knob.

A new ankylosaurid dinosaur from the Upper Cretaceous (Kirtlandian) of New Mexico with implications for ankylosaurid diversity in the Upper Cretaceous of western North America.

A new ankylosaurid (Ankylosauria: Dinosauria), Ziapelta sanjuanensis, gen. et sp. nov., is based on a complete skull, an incomplete first cervical half ring, a possible fragment of the second cervical half ring, and additional fragmentary osteoderms. The holotype specimen is from the Upper Cretaceous (Upper Campanian, Kirtlandian Land-Vertebrate Age) Kirtland Formation (De-na-zin Member) at Hunter Wash, San Juan Basin, in northwestern New Mexico, USA. Diagnostic characters of Ziapelta include: a large, prominent triangular median nasal caputegulum; a mixture of flat and bulbous frontonasal caputegulae; ventrolaterally oriented squamosal horns with a sharp, prominent dorsal keel; and the ventral surface of basicranium with three prominent anteroposteriorly oriented fossae. A phylogenetic analysis suggests that Ziapelta is not closely related to the other ankylosaurid from the De-na-zin Member, Nodocephalosaurus, but allies it to the northern North American ankylosaurids Ankylosaurus, Anodontosaurus, Euoplocephalus, Dyoplosaurus, and Scolosaurus.

A mummified duck-billed dinosaur with a soft-tissue cock's comb.

Among living vertebrates, soft tissues are responsible for labile appendages (combs, wattles, proboscides) that are critical for activities ranging from locomotion to sexual display [1]. However, soft tissues rarely fossilize, and such soft-tissue appendages are unknown for many extinct taxa, including dinosaurs. Here we report a remarkable "mummified" specimen of the hadrosaurid dinosaur Edmontosaurus regalis from the latest Cretaceous Wapiti Formation, Alberta, Canada, that preserves a three-dimensional cranial crest (or "comb") composed entirely of soft tissue. Previously, crest function has centered on the hypertrophied nasal passages of lambeosaurine hadrosaurids, which acted as resonance chambers during vocalization [2-4]. The fleshy comb in Edmontosaurus necessitates an alternative explanation most likely related to either social signaling or sexual selection [5-7]. This discovery provides the first view of bizarre, soft-tissue signaling structures in a dinosaur and provides additional evidence for social behavior. Crest evolution within Hadrosaurinae apparently culminated in the secondary loss of the bony crest at the terminal Cretaceous; however, the new specimen indicates that cranial ornamentation was in fact not lost but substituted in Edmontosaurus by a fleshy display structure. It also implies that visual display played a key role in the evolution of hadrosaurine crests and raises the possibility of similar soft-tissue structures among other dinosaurs.

Epidermal and dermal integumentary structures of ankylosaurian dinosaurs.

Ankylosaurian dinosaurs are most notable for their abundant and morphologically diverse osteoderms, which would have given them a spiky appearance in life. Isolated osteoderms are relatively common and provide important information about the structure of the ankylosaur dermis, but fossilized impressions of the soft-tissue epidermis of ankylosaurs are rare. Nevertheless, well-preserved integument exists on several ankylosaur fossils that shows osteoderms were covered by a single epidermal scale, but one or many millimeter-sized ossicles may be present under polygonal, basement epidermal scales. Evidence for the taxonomic utility of ankylosaurid epidermal scale architecture is presented for the first time. This study builds on previous osteological work that argues for a greater diversity of ankylosaurids in the Dinosaur Park Formation of Alberta than has been traditionally recognized and adds to the hypothesis that epidermal skin impressions are taxonomically relevant across diverse dinosaur clades.

Euoplocephalus tutus and the diversity of ankylosaurid dinosaurs in the Late Cretaceous of Alberta, Canada, and Montana, USA.

Few ankylosaurs are known from more than a single specimen, but the ankylosaurid Euoplocephalus tutus (from the Late Cretaceous of Alberta, Canada and Montana, USA) is represented by dozens of skulls and partial skeletons, and is therefore an important taxon for understanding intraspecific variation in ankylosaurs. Euoplocephalus is unusual compared to other dinosaurs from the Late Cretaceous of Alberta because it is recognized from the Dinosaur Park, Horseshoe Canyon, and Two Medicine formations. A comprehensive review of material attributed to Euoplocephalus finds support for the resurrection of its purported synonyms Anodontosaurus lambei and Scolosaurus cutleri, and the previously resurrected Dyoplosaurus acutosquameus. Anodontosaurus is found primarily in the Horseshoe Canyon Formation of Alberta and is characterized by ornamentation posterior to the orbits and on the first cervical half ring, and wide, triangular knob osteoderms. Euoplocephalus is primarily found in Megaherbivore Assemblage Zone 1 in the Dinosaur Park Formation of Alberta and is characterized by the absence of ornamentation posterior to the orbits and on the first cervical half ring, and keeled medial osteoderms on the first cervical half ring. Scolosaurus is found primarily in the Two Medicine Formation of Montana (although the holotype is from Dinosaur Provincial Park), and is characterized by long, back-swept squamosal horns, ornamentation posterior to the orbit, and low medial osteoderms on the first cervical half ring; Oohkotokia horneri is morphologically indistinguishable from Scolosaurus cutleri. Dyoplosaurus was previously differentiated from Euoplocephalus sensu lato by the morphology of the pelvis and pes, and these features also differentiate Dyoplosaurus from Anodontosaurus and Scolosaurus; a narrow tail club knob is probably also characteristic for Dyoplosaurus.

Analyzing taphonomic deformation of ankylosaur skulls using retrodeformation and finite element analysis.

Taphonomic deformation can make the interpretation of vertebrate fossil morphology difficult. The effects of taphonomic deformation are investigated in two ankylosaurid dinosaur taxa, Euoplocephalus tutus (to investigate effects on our understanding of intraspecific variation) and Minotaurasaurus ramachandrani (to investigate the validity of this genus). The ratio of orbit maximum rostrocaudal length to perpendicular height is used as a strain ellipse, which can be used to determine if ankylosaur skull fossils have been dorsoventrally compacted during fossilization and diagenesis. The software program Geomagic is used to retrodeform three-dimensional (3D) digital models of the ankylosaur skulls. The effects of sediment compaction are modeled using finite element analysis, and the resulting strain distributions are compared with the retrodeformed models as a test of the retrodeformation method. Taphonomic deformation can account for a large amount of intraspecific variation in Euoplocephalus, but finite element analysis and retrodeformation of Minotaurasaurus shows that many of its diagnostic features are unlikely to result from deformation.

The internal cranial morphology of an armoured dinosaur Euoplocephalus corroborated by X-ray computed tomographic reconstruction.

Internal cranial anatomy is a challenging area to study in fossilized skulls because of small sample sizes and varied post-mortem preservational alterations. This difficulty has led to the lack of correspondence between results obtained from direct osteological observation and from more indirect reconstruction methods. This paper presents corroborating evidence from direct osteological observation and from reconstruction based on computed X-ray tomography (CT) on the internal cranial anatomy of the ankylosaurid dinosaur Euoplocephalus tutus. A remarkable specimen of Euoplocephalus preserves rarely observed internal cranial structures such as vascular impressions in the nasal cavity, olfactory turbinates and possible impressions of conchae. Comparison with fossils and CT models of other taxa and other Euoplocephalus specimens adds osteological evidence for the previously reconstructed nasal cavity in this dinosaur and revises the previously described braincase morphology. A new interpretation of the ethmoidal homology identifies a mesethmoid, sphenethmoid and ectethmoid. These ethmoidal ossifications are continuous with the mineralized walls of the nasal cavity. The location of the olfactory fenestra provides further evidence that the olfactory regions of the nasal cavity are pushed to the sides of the main airway. This implies that the function of the vascular impressions in the nasal cavity and the looping of the cavity are not related to olfaction. A byproduct of the elongate, looping airway is a dramatic increase in surface area of the nasal respiratory mucosa, which in extant species has been linked to heat and water balance. A role in vocalization as a resonating chamber is another possible function of the looping and elongation of the nasal cavity. Olfaction remains as a possible function for the enlarged olfactory region, suggesting that multiple functions account for different parts of the ankylosaurid nasal cavity that underwent substantial modification. Cranial endocasts show negligible variation within Euoplocephalus, which lends some confidence to interspecific comparisons of endocranial morphology.

Finite element analyses of ankylosaurid dinosaur tail club impacts.

Ankylosaurid dinosaurs have modified distal caudal vertebrae (the handle) and large terminal caudal osteoderms (the knob) that together form a tail club. Three-dimensional digital models of four tail clubs referred to Euoplocephalus tutus were created from computed tomography scans of fossil specimens. We propose to use finite element modeling to examine the distribution of stress in simulated tail club impacts in order to determine the biological feasibility of hypothesized tail clubbing behavior. Results show that peak stresses were artificially high at the rigid constraint. The data suggest that tail clubs with small and average-sized knobs were unlikely to fail during forceful impacts, but large clubs may have been at risk of fracture cranial to the knob. The modified handle vertebrae were capable of supporting the weight of even very large knobs. Long prezygapophyses and neural spines in the handle vertebrae helped distribute stress evenly along the handle. We conclude that tail swinging-behavior may have been possible in Euoplocephalus, but more sophisticated models incorporating flexible constraints are needed to support this hypothesis.