Armand de Ricqlès

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.

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.

Ontogenetic evolution of bone structurein Late Cretaceous Plesiosauria from New Zealand

Abstract Histological observations of homologous bones (vertebrae, ribs, humerus, phalanges) among conspecific juvenileand adult Upper Cretaceous plesiosaurs from New Zealand (elasmosaurs and pliosaurs) demonstrates a unique “ontogenetic trajectory” of skeletal histogenesis in these animals. While juveniles demonstrate a “pachyosteosclerotic” condition of the skeleton, adults have a very light “osteoporotic-like” bone structure. Until now, one or the other of these histological specializations was known among aquatic tetrapods, adapted along contrasting pathways to this environment, either by ballasting (pachyosteosclerosis; e.g. sirenians) or by lightening (osteoporotic-like adaptation: e.g. modern cetaceans) of the skeleton. The successive occurrence of these constrasting conditions during ontogenesis of a single organism had never been reported, as far as we know, but could well be an ontogenetic characteristic of Plesiosaurs sensu lato . The significance of these findings are discussed in various phylogenetical, functional and paleoecological contexts. The ontogenetic trajectory of the plesiosaur skeleton is interpreted within the general framework of developmental heterochrony. Specifically, it suggests that juvenile plesiosaurs kept a conservative (plesiomorphic) ecology for sauropterygians, as poorly mobile, lagoon or shore dwellers while, in contrast, the adults would shift towards much more active locomotory behaviors in the open sea.

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.

Jaw growth and tooth replacement in Captorhinus aguti (Reptilia: Captorhinomorpha): a morphological and histological analysis

ABSTRACT We here report the results of a primarily histological study of jaw growth and tooth replacement in the Early Permian captorhinomorph reptile Captorhinus aguti. Preliminary histological examination shows that “drift” of teeth from the lingual to the labial side of the jaw apparently occurred through a combination of bone growth + remodelling. Simple graphical analysis of proportional changes in the C. aguti skull and jaws over a threefold span of size increase demonstrates that growth was essentially isometric. This fact and our preliminary histological observations are combined into a model of jaw growth plus tooth replacement, in which the positions and relative ages of teeth are described in terms of the Zahnreihen of Edmund (1960). Detailed histological observations are then used to test the model, which is confirmed in all essentials but shown to be incomplete as first formulated. With incorporation of the fact that during growth the older, smaller parts of the dentary and maxilla were progr...

Comparative Long Bone Histology and Growth of the “Hypsilophodontid” Dinosaurs Orodromeus makelai, Dryosaurus altus, and Tenontosaurus tillettii (Ornythlschla: Euornithopoda)

ABSTRACT The long bone histology of the “hypsilophodontid” dinosaurs Orodromeus makelai, Dryosaurus altus, and Tenontosaurus tilletti, was examined from perinate to largest available ontogenetic stages. These ontogenies were compared with each other, and to those of other dinosaurs, notably hadrosaurids such as Maiasaura and Hypacrosaurus. Orodromeus is a small dinosaur, and its more moderate growth trajectory is consistent with those generally observed for relatively small dinosaurs and other small ornithosuchians. Tenontosaurus achieves a relatively larger adult size, and its bone histology through ontogeny is similar to those of hadrosaurs, although reflective of slightly lower growth rates. Dryosaurus is thought to be a small dinosaur, but in its largest recognized ontogenetic stages it does not display the “adult” histological features of other ornithopod adults, although it does suggest growth rates comparable to those of larger ornithopods, including hadrosaurs. Determinate growth is observed in Orodromeus, Tenontosaurus, and hadrosaurs, so we infer that the adult stage of Dryosaurus has not yet been recognized. Dinosaurs continued to grow slowly after reaching adult size, so the largest known specimens of most taxa are not maxima.

Bone growth marks reveal protracted growth in New Zealand kiwi (Aves, Apterygidae)

The presence of bone growth marks reflecting annual rhythms in the cortical bone of non-avian tetrapods is now established as a general phenomenon. In contrast, ornithurines (the theropod group including modern birds and their closest relatives) usually grow rapidly in less than a year, such that no annual rhythms are expressed in bone cortices, except scarce growth marks restricted to the outer cortical layer. So far, cyclical growth in modern birds has been restricted to the Eocene Diatryma, the extant parrot Amazona amazonica and the extinct New Zealand (NZ) moa (Dinornithidae). Here we show the presence of lines of arrested growth in the long bones of the living NZ kiwi (Apteryx spp., Apterygidae). Kiwis take 5–6 years to reach full adult body size, which indicates a delayed maturity and a slow reproductive cycle. Protracted growth probably evolved convergently in moa and kiwi sometime since the Middle Miocene, owing to the severe climatic cooling in the southwest Pacific and the absence of mammalian predators.