John R. Horner

LONG BONE HISTOLOGY OF THE HADROSAURID DINOSAUR MAIASAURA PEEBLESORUM: GROWTH DYNAMICS AND PHYSIOLOGY BASED ON AN ONTOGENETIC SERIES OF SKELETAL ELEMENTS

Abstract Ontogenetic changes in the bone histology of Maiasaura peeblesorum are revealed by six relatively distinct but gradational growth stages: early and late nestling, early and late juvenile, sub-adult, and adult. These stages are distinguished not only by relative size but by changes in the histological patterns of bones at each stage. In general, the earliest stages are marked by spongy bone matrix with large vascular canals. Through growth, the cortical bone differentiates into fibro-lamellar tissue that tends to become more regularly layered in the outer cortex. By the sub-adult stage, lines of arrested growth (LAGs) begin to appear regularly. Resorption lines and substantial Haversian substitution in many long bones also begin to appear at this stage, and the external cortex has a lamellar-zonal structure in some bones that indicates imminent cessation of growth. Judging by the rates of apposition of similar bone tissues in living amniotes, and by the number and placement of LAGs, these patterns suggest that young Maiasaura nestlings grew at very high rates, and at high and moderately high rates during later nestling, juvenile, and sub-adult stages, slowing to low and very low growth rates in adults (7–9 m total length). The nesting period would have lasted one to two months, late juvenile size (3.5 meters) would have been reached in one or two years, and adult size in six to eight years, depending on the basis for extrapolating bone growth rates. The histological tissues, patterns, and inferred growth rates of the bones of Maiasaura are completely different from those of living non-avian reptiles, generally similar to those of most other dinosaurs and pterosaurs for which data are available, and much like those of extant birds and mammals. No living reptiles (except birds) grow to adult size at these rates, nor do they show these histological patterns. We conclude that Maiasaura did not grow at all like living non-avian reptiles, which cannot be considered informative models for most aspects of dinosaurian growth (or physiology, to the extent that growth rates reflect metabolism). The use of lines of arrested growth (LAGs) to infer dinosaurian physiology has never been tested and is not supported by independent lines of evidence; their use in calculating age is also more complex than previously suggested and should not be based on single bones.

Dinosaurian growth rates and bird origins

Dinosaurs, like other tetrapods, grew more quickly just after hatching than later in life. However, they did not grow like most other non-avian reptiles, which grow slowly and gradually through life. Rather, microscopic analyses of the long-bone tissues show that dinosaurs grew to their adult size relatively quickly, much as large birds and mammals do today. The first birds reduced their adult body size by shortening the phase of rapid growth common to their larger theropod dinosaur relatives. These changes in timing were primarily related not to physiological differences but to differences in growth strategy.

Comparative osteohistology of some embryonic and perinatal archosaurs: developmental and behavioral implications for dinosaurs

Abstract Histologic studies of embryonic and perinatal longbones of living birds, non-avian dinosaurs, and other reptiles show a strong phylogenetic signal in the distribution of tissues and patterns of vascularization in both the shafts and the bone ends. The embryonic bones of basal archosaurs and other reptiles have thin-walled cortices and large marrow cavities that are sometimes subdivided by erosion rooms in early stages of growth. The cortices of basal reptiles are poorly vascularized, and osteocyte lacunae are common but randomly organized. Additionally, there is no evidence of fibrolamellar tissue organization around the vascular spaces. Compared with turtles, basal archosaurs show an increase in vascularization, better organized osteocytes, and some fibrolamellar tissue organization. In dinosaurs, including birds, vascularization is greater than in basal archosaurs, as is cortical thickness, and the osteocyte lacunae are more abundant and less randomly organized. Fibrolamellar tissues are evident around vascular canals and form organized primary osteons in older perinates and juveniles. Metaphyseal (“epiphyseal”) morphology varies with the acquisition of new features in derived groups. The cartilage cone, persistent through the Reptilia (crown-group reptiles, including birds), is completely calcified in ornithischian dinosaurs before it is eroded by marrow processes; cartilage canals, absent in basal archosaurs, are present in Dinosauria; a thickened calcified hypertrophy zone in Dinosauria indicates an acceleration of longitudinal bone growth. Variations in this set of histological synapomorphies overlap between birds and non-avian dinosaurs. In birds, these variations are strongly correlated with life-history strategies. This overlap, plus independent evidence from nesting sites, reinforces the hypothesis that variations in bone growth strategies in Mesozoic dinosaurs reflect different life-history strategies, including nesting behavior of neonates and parental care.

Growth in small dinosaurs and pterosaurs: the evolution of archosaurian growth strategies

Abstract Histological evidence of the bones of pterosaurs and dinosaurs indicates that the typically large forms of these groups grew at rates more comparable to those of birds and mammals than to those of other living reptiles. However, Scutellosaurus, a small, bipedal, basal thyreophoran ornithischian dinosaur of the Early Jurassic, shows histological features in its skeletal tissues that suggest relatively lower growth rates than in those of larger dinosaurs. In these respects Scutellosaurus, like other small dinosaurs such as Orodromeus and some basal birds, is more like young, rapidly growing crocodiles than larger, more derived ornithischians (hadrosaurs) and all saurischians (sauropods and theropods). Similar patterns can be seen in small, mostly basal pterosaurs such as Eudimorphodon and Rhamphorhynchus. However, superficial similarities to crocodile bone growth belie some important differences, which are most usefully interpreted in phylogenetic and ontogenetic contexts. Large size evolved secondarily in several dinosaurian and pterosaurian lineages. We hypothesize that this larger size was made possible by rapid growth strategies that are reflected by characteristic highly vascularized fibro-lamellar bone tissues that comprise most of the cortex. Dinosaurs and pterosaurs, like other tetrapods, generally grew more quickly in early stages and more slowly as growth neared completion. As in other vertebrate groups, taxa of small adult size may have grown at lower rates or for shorter durations than larger taxa did. Phylogenetic patterns suggest that by themselves, the low vascularity and inferred low growth rates seen in small dinosaurs and pterosaurs are not good indicators of thermometabolic regime, because they are correlated so strongly with size. They may reflect mechanical exigencies of small size rather than especially lower growth rates, tied to the process of deposition of particular kinds of bone tissues. The evolution of life history strategies in dinosaurs and pterosaurs, as they relate to rates of growth and adult body sizes, will be better understood as more complete histological studies place these data into phylogenetic and ontogenetic contexts.

Biomolecular characterization and protein sequences of the Campanian hadrosaur B. canadensis.

The Birds and the Dinosaurs The extent to which primary tissues are preserved in ancient fossils remains controversial. Schweitzer et al. (p. 626; see the news story by Service) describe well-preserved tissues and primary collagen sequences from the femur of an 80-million-year-old hadrosaur. The fossil preserved structures resembling primary bone tissues and vessels. Both extracts and tissue pieces were analyzed in multiple laboratories by mass spectrometry, which revealed ancient collagen sequences that support a close relation between birds and dinosaurs. Analysis of well-preserved tissues from an 80-million-year-old hadrosaur supports the dinosaur-bird relationship. Molecular preservation in non-avian dinosaurs is controversial. We present multiple lines of evidence that endogenous proteinaceous material is preserved in bone fragments and soft tissues from an 80-million-year-old Campanian hadrosaur, Brachylophosaurus canadensis [Museum of the Rockies (MOR) 2598]. Microstructural and immunological data are consistent with preservation of multiple bone matrix and vessel proteins, and phylogenetic analyses of Brachylophosaurus collagen sequenced by mass spectrometry robustly support the bird-dinosaur clade, consistent with an endogenous source for these collagen peptides. These data complement earlier results from Tyrannosaurus rex (MOR 1125) and confirm that molecular preservation in Cretaceous dinosaurs is not a unique event.

Age and growth dynamics of Tyrannosaurus rex

Tyrannosaurus rex is the most commonly found North American latest Cretaceous theropod, but until the 1980s only five specimens had been discovered, and no more than six have received a full description. Consequently there has been little information on how old Tyrannosaurus specimens were at maturity or death. Histological analysis of seven individuals provided, for the first time, an opportunity to assess the age represented by the bone cortex, to estimate the average individual age of these skeletons, to determine whether they represented fully grown individuals, and to predict their individual longevity. Though a range of ages (15–25 years) was found for the specimens studied, the seven individuals demonstrate that T. rex reached effectively full size in less than 20 years. The growth rate of T. rex was comparable to that of the African elephant, which has a similar mass and time to maturity. Some of the known specimens of T. rex did not quite reach full size; others do not seem to have survived long after achieving it.

Extreme Cranial Ontogeny in the Upper Cretaceous Dinosaur Pachycephalosaurus

Background Extended neoteny and late stage allometric growth increase morphological disparity between growth stages in at least some dinosaurs. Coupled with relatively low dinosaur density in the Upper Cretaceous of North America, ontogenetic transformational representatives are often difficult to distinguish. For example, many hadrosaurids previously reported to represent relatively small lambeosaurine species were demonstrated to be juveniles of the larger taxa. Marginocephalians (pachycephalosaurids + ceratopsids) undergo comparable and extreme cranial morphological change during ontogeny. Methodology/Principal Findings Cranial histology, morphology and computer tomography reveal patterns of internal skull development that show the purported diagnostic characters for the pachycephalosaurids Dracorex hogwartsia and Stygimoloch spinifer are ontogenetically derived features. Coronal histological sections of the frontoparietal dome of an adult Pachycephalosaurus wyomingensis reveal a dense structure composed of metaplastic bone with a variety of extremely fibrous and acellular tissue. Coronal histological sections and computer tomography of a skull and frontoparietal dome of Stygimoloch spinifer reveal an open intrafrontal suture indicative of a subadult stage of development. These dinosaurs employed metaplasia to rapidly grow and change the size and shape of their horns, cranial ornaments and frontoparietal domes, resulting in extreme cranial alterations during late stages of growth. We propose that Dracorex hogwartsia, Stygimoloch spinifer and Pachycephalosaurus wyomingensis are the same taxon and represent an ontogenetic series united by shared morphology and increasing skull length. Conclusions/Significance Dracorex hogwartsia (juvenile) and Stygimoloch spinifer (subadult) are reinterpreted as younger growth stages of Pachycephalosaurus wyomingensis (adult). This synonymy reduces the number of pachycephalosaurid taxa from the Upper Cretaceous of North America and demonstrates the importance of cranial ontogeny in evaluating dinosaur diversity and taxonomy. These growth stages reflect a continuum rather than specific developmental steps defined by “known” terminal morphologies.

On the bone histology of some Triassic pseudosuchian archosaurs and related taxa

Abstract The long bone histology of some major groups of extinct Triassic crocodile relatives (phytosaurs, aetosaurs, poposaurs) is generally similar to that of living and fossil crocodylomorphs. Early deposition of more or less fibro-lamellar, fast-growing tissue gives way to cycles of deposition of a layer of less well-vascularized, predominantly parallel-fibered bone, followed by an annulus of nearly avascular bone and a line of arrested growth (LAG). These cycles, forming the so-called lamellar-zonal pattern of bone tissue suggesting slow growth, differ from the situation in most ornithosuchians (pterosaurs and dinosaurs), in which the pattern is generally that of fast-growing fibro-lamellar tissue throughout, that may become less vascular and eventually avascular only as full size is reached. LAGs are common, but annuli are not. Although the pseudosuchian pattern is presumed primitive for archosaurs, erythrosuchians (non-archosaurian Archosauriformes) apparently grew much like dinosaurs did, so the pseudosuchian pattern may not necessarily be primitive for Archosauriformes. Moreover, the histological patterns of the basal crocodylomorph Terrestrisuchus suggest elevated growth rates compared to typical crocodiles, though not as high as those of dinosaurs and pterosaurs. In general, there is a clear difference in histological tissue types, and hence in growth regimes and rates, between pseudosuchians and ornithosuchians, which extends back to the separation of these two archosaurian lineages at least by the Middle Triassic.

Embryos and eggs for the Cretaceous theropod dinosaur Troodon formosus

Abstract Elongate and asymmetric eggs of the oospecies Prismatoolithus levis occur regularly in the Upper Cretaceous Two Medicine Formation of western Montana. These eggs had previously been assigned to the ornithischian Orodromeus makelai, for both juvenile and adult remains are typically associated with these eggs. Reexamination of the embryos shows them to exhibit at least 24 apomorphies of the clades Dinosauria, Theropoda and Paraves. The embryos also display a pneumatic quadrate, closely placed basal tubera, a high tooth count, a metatarsal II much narrower than IV and a strongly constricted metatarsal III, all possible synapomorphies of the Troodontidae. Presence of large basal tubera and a broadly rounded anterior border of the maxillary fenestra permit assignment to Troodon formosus. Most but not all bones appear ossified, suggesting a developmental level comparable to stages 35–38 of avian embryos and a time approaching hatching. Embryos show a consistent level of development from one egg to another indicating synchronous hatching of the clutch. Embryonic Troodon exhibit long distal segments and radically different hindlimb proportions in comparison to adults. Orodromeus and other small vertebrate remains associated with Troodon egg horizons may represent prey of the adults during egg-laying and brooding. Troodon eggs show several aspects either shared or convergent with some birds, and further demonstrate the close relationship of Troodontidae and Aves. These features include: asymmetric egg form, non-branching angusticanaliculate pores, distinct structural differentiation of the mammillary and overlying prismatic layer, barrel-shaped mammillary cones with a blocky calcite cleavage, and prismatic structure visible throughout the second structural layer.

The evolution and function of thyreophoran dinosaur scutes: implications for plate function in stegosaurs

Abstract The evolution of scutes in thyreophoran dinosaurs, based on Scutellosaurus, Scelidosaurus, Stegosaurus, and several ankylosaurs, began with small rounded or ovoid structures that typically had slight, anteroposteriorly oriented keels. These scutes were elaborated in two general and overlapping ways: they could flare laterally and asymmetrically beneath the keels that mark the anteroposterior axis, and they could be hypertrophied in their distal growth to produce plates, spikes, and other kinds of ornamentation. Stegosaurus plates and spikes are thus primarily hypertrophied keels of primitive thyreophoran scutes, sometimes with elaboration of dermal bone around their pustulate bases. Histologically, most thyreophoran scute tissues comprise secondary trabecular medullary bone that is sandwiched between layers of compact primary bone. Some scutes partly or mostly comprise anatomically metaplastic bone, that is, ossified fibrous tissue that shows incremental growth. The “plumbing” of Stegosaurus plates was not apparently built to support a “radiator” system of internal blood vessels that communicated with the outside of the plates and coursed along their external surfaces to return heated or cooled blood to the body core. Possibly a purely external system supported this function but there is no independent evidence for it. On the other hand, many of the vascular features in stegosaurian plates and spikes reflect bautechnisches artifacts of growth and production of bone. Surface vascular features likely supported bone growth and remodeling, as well as the blood supply to a keratinous covering. When the gross and microstructural features of the plates and spikes are viewed in phylogenetic context, no clear pattern of thermoregulatory function emerges, though an accessory role cannot be eliminated in certain individual species. It seems more likely, as in other groups of dinosaurs, that the variation of dermal armor form in stegosaurs was primarily linked to species individuation and recognition, perhaps secondarily to inter- and intraspecific display, and rarely to facultative thermoregulation.