The evolution of maximum terrestrial body mass in sauropod dinosaurs.

The long-necked dinosaurs, sauropods, are famous for their extreme body sizes, evolving body masses several times greater than the next-heaviest terrestrial animals, elephant-like and rhinoceros- like mammals and 'duck-billed' dinosaurs. The pace of sauropod discovery has been exponential in recent decades, resulting in the recognition of sauropods as a global, ecologically diverse group of herbivorous dinosaurs comprising over 250 known species1. However, limitations due to missing data from their patchy fossil record have so far limited studies of sauropod body-size evolution to less than half their known diversity1. Here, I present models to confidently predict unknown limb-bone measurements in sauropods, resulting in a dataset 50% larger than previously assembled. Leveraging the emerging consilience among body mass estimation methods for fossil tetrapods, I then map sauropod body mass evolution through time in a phylogenetic context. Likelihood-based ancestral state reconstruction reveals that sauropods convergently surpassed maximum terrestrial mammalian body mass at least three dozen times over the course of 100 million years, on at least six landmasses and in at least five ecomorphologically disparate clades. Sauropod maximum body mass rapidly increased early in their evolutionary history from under 5,000 kg before levelling off around 40,000 kg (with notable exceptions)2, in a pattern similar to that observed in terrestrial mammals3.

Developmental strategies underlying gigantism and miniaturization in non-avialan theropod dinosaurs.

In amniotes, the predominant developmental strategy underlying body size evolution is thought to be adjustments to the rate of growth rather than its duration. However, most theoretical and experimental studies supporting this axiom focus on pairwise comparisons and/or lack an explicit phylogenetic framework. We present the first large-scale phylogenetic comparative analysis examining developmental strategies underlying the evolution of body size, focusing on non-avialan theropod dinosaurs. We reconstruct ancestral states of growth rate and body mass in a taxonomically rich dataset, finding that contrary to expectations, changes in the rate and duration of growth played nearly equal roles in the evolution of the vast body size disparity present in non-avialan theropods-and perhaps that of amniotes in general.

Evolution of amniote dentine apposition rates.

In amniotes, daily rates of dentine formation in non-ever-growing teeth range from less than 1 to over 25 µm per day. The latter value has been suggested to represent the upper limit of odontoblast activity in non-ever-growing teeth, a hypothesis supported by the lack of scaling between dentine apposition rates and body mass in Dinosauria. To determine the correlates and potential controls of dentine apposition rate, we assembled a dataset of apposition rates, metabolic rates and body masses for ca 80 amniote taxa of diverse ecologies and diets. We used phylogenetic regression to test for scaling relationships and reconstruct ancestral states of daily dentine apposition across Amniota. We find no relationship between body mass and daily dentine apposition rate (DDAR) for non-ever-growing teeth in Amniota as a whole or within major clades. Metabolic rate, the number of tooth generations, diet and habitat also do not predict or correspond with DDARs. Similar DDARs are found in large terrestrial mammals, dinosaurs and marine reptiles, whereas primates, cetaceans and some smaller marine reptiles independently evolved exceptionally slow rates. Life-history factors may explain the evolution of dentine apposition rates, which evolved rapidly at the origin of major clades.

Redescription of Brachiosaurid Sauropod Dinosaur Material From the Upper Jurassic Morrison Formation, Colorado, USA.

Like many long-standing dinosaur taxa, Brachiosaurus altithorax from the Upper Jurassic Morrison Formation of North America suffers from taxonomic issues stemming from a relatively incomplete holotype. Lack of anatomical overlap has precluded definitive referral of important specimens, including a mostly complete skull discovered in 1883. We redescribe this skull and some other significant brachiosaurid specimens based on new preparation and computed tomographic (CT) data. We argue that these elements are most parsimoniously referred to B. altithorax. Including these tentatively referred elements in a phylogenetic analysis does not alter the hypothesized relationships of B. altithorax, congruent with the presence of a single brachiosaurid taxon across western North America in the Late Jurassic. Based on CT data, we estimate that B. altithorax had a slower tooth replacement rate than Camarasaurus or the diplodocoids it shared Morrison Formation landscapes with, which suggests a difference in diet and/or feeding strategy. Anat Rec, 303:732-758, 2020. © 2019 Wiley Periodicals, Inc.

Correction: Evolution of high tooth replacement rates in theropod dinosaurs.

[This corrects the article DOI: 10.1371/journal.pone.0224734.].

Evolution of high tooth replacement rates in theropod dinosaurs.

Tooth replacement rate is an important contributor to feeding ecology for polyphyodont animals. Dinosaurs exhibit a wide range of tooth replacement rates, mirroring their diverse craniofacial specializations, but little is known about broad-scale allometric or evolutionary patterns within the group. In the current broad but sparse dinosaurian sample, only three non-avian theropod tooth replacement rates have been estimated. We estimated tooth formation and replacement rates in three additional non-avian theropod dinosaurs, the derived latest Cretaceous abelisaurid Majungasaurus and the more generalized Late Jurassic Allosaurus and Ceratosaurus. We created the largest dental histological and CT dataset for any theropod dinosaur, sectioning and scanning over a dozen toothed elements of Majungasaurus and several additional elements from the other two genera. Using this large sample, we created models of tooth formation time that allow for theropod replacement rates to be estimated non-destructively. In contrast to previous results for theropods, we found high tooth replacement rates in all three genera, with Allosaurus and Ceratosaurus rates of ~100 days and 56 days for Majungasaurus. The latter rate is on par with those of derived herbivorous dinosaurs including some neosauropods, hadrosaurids, and ceratopsians. This elevated rate may be a response to high rates of tooth wear in Majungasaurus. Within Dinosauria, there is no relationship between body mass and tooth replacement rate and no trends in replacement rate over time. Rather, tooth replacement rate is clade-specific, with elevated rates in abelisaurids and diplodocoids and lower rates in coelurosaurs.

Scaling of statically derived osteocyte lacunae in extant birds: implications for palaeophysiological reconstruction.

Osteocytes are mature versions of osteoblasts, bone-forming cells that develop in two ways: via 'static' osteogenesis, differentiating and ossifying tissue in situ to form a scaffold upon which other bone can form, or 'dynamic' osteogenesis, migrating to infill or lay down bone around neurovasculature. A previous study regressed the volume of osteocyte lacunae derived from dynamic osteogenesis (DO) of a broad sample of extant bird species against body mass, the growth rate constant ( k), mass-specific metabolic rate, genome size, and erythrocyte size. There were significant relationships with body mass, growth rate, metabolic rate, and genome size, with the latter being the strongest. Using the same avian histological dataset, we measured over 3800 osteocyte lacunar axes derived from static osteogenesis (SO) in order to look for differences in the strength of form-function relationships inferred for DO-derived lacunae at the cellular and tissue levels. The relationship between osteocyte lacunar volume and body mass was stronger when measuring SO lacunae, whereas relationships between osteocyte lacunar volume versus growth rate and basal metabolic rate disappeared. The relationship between osteocyte lacuna volume and genome size remained significant and moderately strong when measuring SO lacunae, whereas osteocyte lacuna volume was still unrelated to erythrocyte size. Our results indicate that growth and metabolic rate signals are contained in avian DO but not SO osteocyte lacunae, suggesting that the former should be used in estimating these parameters in extinct animals.

A new fossil assemblage shows that large angiosperm trees grew in North America by the Turonian (Late Cretaceous).

The diversification of flowering plants and marked turnover in vertebrate faunas during the mid-Cretaceous transformed terrestrial communities, but the transition is obscured by reduced terrestrial deposition attributable to high sea levels. We report a new fossil assemblage from multiple localities in the Upper Cretaceous Ferron Sandstone Member of the Mancos Shale Formation in Utah. The fossils date to the Turonian, a severely underrepresented interval in the terrestrial fossil record of North America. A large silicified log (maximum preserved diameter, 1.8 m; estimated height, ca. 50 m) is assigned to the genus Paraphyllanthoxylon; it is the largest known pre-Campanian angiosperm and the earliest documented occurrence of an angiosperm tree more than 1.0 m in diameter. Foliage and palynomorphs of ferns, conifers, and angiosperms confirm the presence of mixed forest or woodland vegetation. Previously known terrestrial vertebrate remains from the Ferron Sandstone Member include fish teeth, two short dinosaur trackways, and a pterosaur; we report the first turtle and crocodilian remains and an ornithopod sacrum. Previous studies indicate that angiosperm trees were present by the Cenomanian, but this discovery demonstrates that angiosperm trees approaching 2 m in diameter were part of the forest canopies across southern North America by the Turonian (~92 million years ago), nearly 15 million years earlier than previously thought.

Precocity in a tiny titanosaur from the Cretaceous of Madagascar.

Sauropod dinosaurs exhibit the largest ontogenetic size range among terrestrial vertebrates, but a dearth of very young individuals has hindered understanding of the beginning of their growth trajectory. A new specimen of Rapetosaurus krausei sheds light on early life in the smallest stage of one of the largest dinosaurs. Bones record rapid growth rates and hatching lines, indicating that this individual weighed ~3.4 kilograms at hatching. Just several weeks later, when it likely succumbed to starvation in a drought-stressed ecosystem, it had reached a mass of ~40 kilograms and was ~35 centimeters tall at the hip. Unexpectedly, Rapetosaurus limb bones grew isometrically throughout their development. Cortical remodeling, limb isometry, and thin calcified hypertrophic metaphyseal cartilages indicate an active, precocial growth strategy.

Osteology of Huabeisaurus allocotus (Sauropoda: Titanosauriformes) from the Upper Cretaceous of China.

BACKGROUND: The Late Cretaceous titanosauriform sauropod Huabeisaurus allocotus Pang and Cheng is known from teeth and much of the postcranial skeleton. Its completeness makes it an important taxon for integrating and interpreting anatomical observations from more fragmentary Cretaceous East Asian sauropods and for understanding titanosauriform evolution in general. METHODOLOGY/PRINCIPAL FINDINGS: We present a detailed redescription of Huabeisaurus allocotus and a suite of anatomical comparisons with other titanosauriforms that demonstrate its validity via autapomorphies (e.g., division of some presacral vertebral laminae, reduced development of caudal ribs, the development of fossae relative to one another in caudal vertebral neural arches, high tibia-to-femur ratio). Huabeisaurus shares many features with other Cretaceous East Asian sauropods (e.g., pendant cervical ribs, anterior-middle caudal vertebrae with a nearly flat anterior centrum face and a concave posterior centrum face) that are absent in sauropods from other landmasses and strata, suggesting a close relationship among many of these forms within the clade Somphospondyli. CONCLUSIONS/SIGNIFICANCE: Restudy of Huabeisaurus provides further evidence for the existence of a clade of somphospondylans--Euhelopodidae--mainly found in the Cretaceous of East Asia. Euhelopodidae represents a fourth example of the evolution of narrow crowns within Sauropoda, along with diplodocoids, brachiosaurids, and advanced titanosaurs (lithostrotians). Despite being known from fewer species than Diplodocoidea, Brachiosauridae, or Lithostrotia, euhelopodids possessed a broader range of tooth shapes than any of these clades, suggesting that euhelopodids exemplified a comparably broad range of feeding strategies and perhaps diets.

Measurement, variation, and scaling of osteocyte lacunae: a case study in birds.

Basic issues surrounding osteocyte biology are still poorly understood, including the variability of osteocyte morphology within and among bones, individuals, and species. Several studies have suggested that the volume or shape of osteocytes (or their lacunae) is related to bone and/or organismal growth rate or metabolism, but the nature of this relationship, if any, is unclear. Furthermore, several studies have linked osteocyte lacuna volume with genome size or growth rate and suggested that osteocyte lacuna volume is unrelated to body size. Herein the scaling of osteocyte lacuna volume with body mass, growth and basal metabolic rates, genome size, and red blood cell size is examined using a broad sample of extant birds within a phylogenetic framework. Over 12,000 osteocyte lacuna axes were measured in a variety of bones from 34 avian and four non-avian dinosaur species. Osteocyte lacunae in parallel-fibered bone are scalene ellipsoids; their morphology and volume cannot be reliably estimated from any single thin section, and using a prolate ellipsoid model to estimate osteocyte lacuna volume results in a substantial (ca. 2-7 times) underestimate relative to true lacunar volume. Orthogonal thin sections reveal that in birds, even when only observing parallel-fibered, primary, cortical bone, intra-skeletal variation in osteocyte lacuna volume and shape is very high (volumes vary by a factor of 5.4 among different bones), whereas variation among homologous bones of the same species is low (1.2-44%; mean=12%). Ordinary and phylogenetically informed bivariate and multiple regressions demonstrate that in birds, osteocyte volume scales significantly but weakly with body mass and mass-specific basal metabolic rate and moderately with genome size, but not with erythrocyte size. Avian whole-body growth rate and osteocyte lacuna volume are weakly and inversely related. Finally, we present the first three-dimensionally calculated osteocyte volumes for several non-avian dinosaurs, which are much larger than previously reported values and smaller than those of large extant avians. Osteocyte volumes estimated from a single transverse section and assuming prolate morphology, as done in previous studies, are relative underestimates in theropod dinosaurs compared to sauropod dinosaurs, raising the possibility that no major change in osteocyte volumes (and genome size) occurred within Theropoda on the lineage leading to birds. Osteocyte volume is intertwined with several organismal attributes whose relative importance varies at a number of hierarchical levels.

Evolution of high tooth replacement rates in sauropod dinosaurs.

BACKGROUND: Tooth replacement rate can be calculated in extinct animals by counting incremental lines of deposition in tooth dentin. Calculating this rate in several taxa allows for the study of the evolution of tooth replacement rate. Sauropod dinosaurs, the largest terrestrial animals that ever evolved, exhibited a diversity of tooth sizes and shapes, but little is known about their tooth replacement rates. METHODOLOGY/PRINCIPAL FINDINGS: We present tooth replacement rate, formation time, crown volume, total dentition volume, and enamel thickness for two coexisting but distantly related and morphologically disparate sauropod dinosaurs Camarasaurus and Diplodocus. Individual tooth formation time was determined by counting daily incremental lines in dentin. Tooth replacement rate is calculated as the difference between the number of days recorded in successive replacement teeth. Each tooth family in Camarasaurus has a maximum of three replacement teeth, whereas each Diplodocus tooth family has up to five. Tooth formation times are about 1.7 times longer in Camarasaurus than in Diplodocus (315 vs. 185 days). Average tooth replacement rate in Camarasaurus is about one tooth every 62 days versus about one tooth every 35 days in Diplodocus. Despite slower tooth replacement rates in Camarasaurus, the volumetric rate of Camarasaurus tooth replacement is 10 times faster than in Diplodocus because of its substantially greater tooth volumes. A novel method to estimate replacement rate was developed and applied to several other sauropodomorphs that we were not able to thin section. CONCLUSIONS/SIGNIFICANCE: Differences in tooth replacement rate among sauropodomorphs likely reflect disparate feeding strategies and/or food choices, which would have facilitated the coexistence of these gigantic herbivores in one ecosystem. Early neosauropods are characterized by high tooth replacement rates (despite their large tooth size), and derived titanosaurs and diplodocoids independently evolved the highest known tooth replacement rates among archosaurs.

Sauropod dinosaur osteoderms from the Late Cretaceous of Madagascar.

Osteoderms are bones embedded within the dermis, and are common to select members of most major tetrapod lineages. The largest known animals that bear osteoderms are members of Titanosauria, a diverse clade of sauropod dinosaurs. Here we report on two titanosaur osteoderms recovered from the Upper Cretaceous Maevarano Formation of Madagascar. Each osteoderm was discovered in association with a partial skeleton representing a distinct ontogenetic stage of the titanosaur Rapetosaurus krausei. Combined, these specimens provide novel insights into the arrangement and function of titanosaur osteoderms. Taphonomic data confirm that Rapetosaurus developed only limited numbers of osteoderms in its integument. The adult-sized osteoderm is the most massive integumentary skeletal element yet discovered, with an estimated volume of 9.63 litres. Uniquely, this specimen possesses an internal cavity equivalent to more than half its total volume. Large, hollow osteoderms may have functioned as mineral stores in fecund, rapidly growing titanosaurs inhabiting stressed environments.

A nomenclature for vertebral fossae in sauropods and other saurischian dinosaurs.

BACKGROUND: The axial skeleton of extinct saurischian dinosaurs (i.e., theropods, sauropodomorphs), like living birds, was pneumatized by epithelial outpocketings of the respiratory system. Pneumatic signatures in the vertebral column of fossil saurischians include complex branching chambers within the bone (internal pneumaticity) and large chambers visible externally that are bounded by neural arch laminae (external pneumaticity). Although general aspects of internal pneumaticity are synapomorphic for saurischian subgroups, the individual internal pneumatic spaces cannot be homologized across species or even along the vertebral column, due to their variability and absence of topographical landmarks. External pneumatic structures, in contrast, are defined by ready topological landmarks (vertebral laminae), but no consistent nomenclatural system exists. This deficiency has fostered confusion and limited their use as character data in phylogenetic analysis. METHODOLOGY/PRINCIPAL FINDINGS: We present a simple system for naming external neural arch fossae that parallels the one developed for the vertebral laminae that bound them. The nomenclatural system identifies fossae by pointing to reference landmarks (e.g., neural spine, centrum, costal articulations, zygapophyses). We standardize the naming process by creating tripartite names from "primary landmarks," which form the zygodiapophyseal table, "secondary landmarks," which orient with respect to that table, and "tertiary landmarks," which further delineate a given fossa. CONCLUSIONS/SIGNIFICANCE: The proposed nomenclatural system for lamina-bounded fossae adds clarity to descriptions of complex vertebrae and allows these structures to be sourced as character data for phylogenetic analyses. These anatomical terms denote potentially homologous pneumatic structures within Saurischia, but they could be applied to any vertebrate with vertebral laminae that enclose spaces, regardless of their developmental origin or phylogenetic distribution.