New insights from bone microanatomy of the Late Triassic Hyperodapedon (Archosauromorpha,Rhynchosauria): implications for archosauromorph growth strategy

Bone microanatomy of multiple postcranial skeletal elements of several individuals of Hyperodapedon collected from India is reported. This reveals that fibrolamellar bone tissue is predominant in the mid‐ and inner cortices, whereas the peripheral region of the cortex is composed of either parallel‐fibred and/or lamellar bone. The pattern of primary osteons mostly ranges between laminar and subplexiform. Such predominance of fibrolamellar bone tissue in the cortex suggests an overall fast growth, which slowed down considerably later in ontogeny. Four distinct ontogenetic stages are identified based on the bone microstructure. During the juvenile stage, growth was fast and continuous, but it became punctuated during the early and late sub‐adult stages. In adult individuals, growth was slow and showed periodic interruption but did not stop completely, suggesting that Hyperodapedon had an indeterminate growth strategy. Interelemental histovariations affecting cortical thickness, organization of the vascular network, incidence of growth rings and extent of secondary reconstruction are noted. Throughout ontogeny, the femora show higher cortical thickness than humeri and tibiae, suggesting differential appositional growth rate between the skeletal elements. Differences in cortical thickness are noted in the ribs, which suggest differential functional constraints based on anatomical site‐specific occurrences. Although fibrolamellar bone tissue became progressively more dominant towards the archosaurs, there are considerable variations in the growth patterns of the archosauromorphs. This is exemplified by the bone microstructure of Hyperodapedon, which deviates from the generalized slow‐growth pattern proposed for all basal archosauromorphs, suggesting that rapid growth was already present in the archosauromorphs. The cortical thickness of various long bones of Hyperodapedon bears similarity with that of several extant terrestrial quadrupeds, suggesting that Hyperodapedon was essentially a terrestrial quadruped.     

GROWTH PATTERNS OF THRINAXODON LIORHINUS, A NON-MAMMALIAN CYNODONT FROM THE LOWER TRIASSIC OF SOUTH AFRICA

Abstract:  The growth dynamics of the Early Triassic non-mammalian cynodont Thrinaxodon liorhinus were assessed through bone histology. Several limb bones of various sizes were examined, revealing a rapidly deposited, uninterrupted, fibro-lamellar bone tissue. A region of slowly deposited parallel-fibred bone occurs peripherally in most skeletal elements studied, becoming more extensively developed in the larger limb bones. On the basis of the bone histology, it is proposed that Thrinaxodon liorhinus grew rapidly during early ontogeny, and at a slower rate with increasing age, possibly once sexual maturity was reached. Variation in bone tissue patterns at different stages of ontogeny is noted and discussed. Given that growth rings are generally absent from the skeletal elements studied, and that the environment was seasonal, it appears that Thrinaxodon liorhinus growth was unaffected by environmental fluctuations.     

LYSTROSAURUS MURRAYI (THERAPSIDA, DICYNODONTIA): BONE HISTOLOGY, GROWTH AND LIFESTYLE ADAPTATIONS

Abstract:  Examination of the bone microstructure of Lystrosaurus murrayi from India and South Africa reveals a predominance of fibrolamellar bone tissue, which suggests rapid periosteal osteogenesis and an overall fast growth. Four distinct ontogenetic stages have been identified based on tissue type, organization of the primary osteons, incidence of growth rings, secondary reconstruction and endosteal bone deposition. An indeterminate growth strategy is proposed for Lystrosaurus . Inter-elemental histovariability suggests differential growth rate of the skeletal elements within the same individual, and among different individuals. The high cortical thickness of the dorsal ribs, an extensive secondary reconstruction in the cortical region of different skeletal elements that resulted in erosionally enlarged channels from the perimedullary to the midcortical region, and trabecular infilling of the medullary region even in the diaphyseal sections of the limb bones suggest at least a semi-aquatic lifestyle for L. murrayi .     

Osteohistological insight into the early stages of growth in Mussaurus patagonicus (Dinosauria,Sauropodomorpha)

Here, we describe the bone histology of juvenile specimens of the basal sauropodomorph Mussaurus patagonicus and interpret its significance in terms of the early growth dynamics of this taxon. Thin sections from three juvenile specimens (femur length, 111–120 mm) of Mussaurus were analysed. The sampled bones consist of multiple postcranial elements collected from the Late Triassic Laguna Colorada Formation (El Tranquilo Group, Patagonia). The cortical bone is composed of fibrolamellar bone tissue. Vascularisation is commonly laminar or plexiform in the long bones. Growth marks are absent in all the examined samples. The ‘epiphyses’ of long bones are all formed by well-developed hypertrophied calcified cartilage. The predominance of woven-fibred bone matrix in cortical bones indicates a fast growth rate in the individuals examined. Moreover, given the existence of growth marks in adult specimens of Mussaurus, as in other sauropodomorphs, and assuming that the first lines of arrested growth was formed during the first year of life, the absence of growth marks in all the bones suggest that the specimens died before reaching their first year of life. Compared with the African taxon Massospondylus carinatus (another basal sauropodomorph for which the bone histology has been previously studied), it appears that Mussaurus had a higher early growth rate than Massospondylus.     

Palaeohistology and external microanatomy of rauisuchian osteoderms (Archosauria: Pseudosuchia)

Abstract: The presence of postcranial dermal armour is plesiomorphic for Archosauria. Here, we survey the external microanatomy and histology of postcranial osteoderms (i.e. dorsal paramedian and caudal osteoderms) of rauisuchians, a widely distributed assemblage of extinct predatory pseudosuchians from the Triassic. The osteoderms of eight rauisuchian taxa were found to be rather compact bones, which usually lack significant bone remodelling or large areas of cancellous bone. The presence of highly vascularized woven or fibrolamellar bone tissue deposited in the core areas indicates higher growth rates during earlier life stages, whereas a more compact parallel‐fibred bone matrix indicates reduced growth rates in later development. This pattern of change corroborates earlier studies on long bone histology. With the exception of a bone tissue found in the sample of Batrachotomus kupferzellensis, which might be the result of metaplastic ossification, the general mode of skeletogenesis is comparable with intramembraneous ossification. The lack of cancellous bone tissue and remodelling processes associated with bone ornamentation, as well as the predominantly intramembraneous mode of ossification, indicates that rauisuchian osteoderm formation differs profoundly from that of the osteoderms of the only extant pseudosuchian lineage, the crocodylians.     

Long bone microstructure gives new insights into the life of pachypleurosaurids from the Middle Triassic of Monte San Giorgio,Switzerland/Italy

The long bone microstructure of four pachypleurosaurid taxa from Monte San Giorgio (Switzerland/Italy) was studied. Pachypleurosaurids are secondarily aquatic reptiles that lived during the Middle Triassic in varying marine environments of the Tethys. All four pachypleurosaurids show high compactness values in their long bones based on a thick cortex and a calcified cartilaginous core, which remains in the medullary region throughout the ontogeny. Parts or even the entire embryonic bone layer composed of a mixture of woven-fibered bone tissue and parallel-fibered bone tissue is preserved in both pachypleurosaurid genera. The rest of the cortex consists of lamellar-zonal bone tissue type. Differences in the microstructure of the bones between the pachypleurosaurids are reflected in the occurrence of remodelling processes, which, if present, affect the innermost growth marks of the cortex or the calcified cartilaginous core. Further variation is present in the spacing pattern of the growth cycles, as well as in the degree of vascularisation of the lamellar-zonal bone tissue type. Our data on the microstructure of the long bones support previous studies on morphology and facies distribution, which indicated different habitats and adaptation to a secondary aquatic lifestyle for each pachypleurosaurid taxon. Life history data furthermore reflect different longevities and ages at sexual maturity. The bone histological data of the stratigraphically youngest and oldest pachypleurosaurid species might indicate possible climate-dependant reproductive seasons similar to Recent lacertilian squamates.     

Growth dynamics of Australia's polar dinosaurs

Analysis of bone microstructure in ornithopod and theropod dinosaurs from Victoria, Australia, documents ontogenetic changes, providing insight into the dinosaurs' successful habitation of Cretaceous Antarctic environments. Woven-fibered bone tissue in the smallest specimens indicates rapid growth rates during early ontogeny. Later ontogeny is marked by parallel-fibered tissue, suggesting reduced growth rates approaching skeletal maturity. Bone microstructure similarities between the ornithopods and theropods, including the presence of LAGs in each group, suggest there is no osteohistologic evidence supporting the hypothesis that polar theropods hibernated seasonally. Results instead suggest high-latitude dinosaurs had growth trajectories similar to their lower-latitude relatives and thus, rapid early ontogenetic growth and the cyclical suspensions of growth inherent in the theropod and ornithopod lineages enabled them to successfully exploit polar regions.     

Novel data on aetosaur (Archosauria,Pseudosuchia) osteoderm microanatomy and histology: palaeobiological implications

One of the most striking features of aetosaurs is the possession of an extensive bony armour composed of dorsal, ventral and appendicular osteoderms. With the purpose of establishing the main histological changes during ontogeny and the degree of histological variation within the armour, we analysed the bone histology of dorsal (paramedian and lateral), ventral and appendicular osteoderms from different taxa from the Late Triassic of South America, including Aetosauroides scagliai, Aetobarbakinoides brasiliensis and Neoaetosauroides engaeus. Histological data support an intramembranous origin for osteoderms. Nevertheless, evidence for metaplastic ossification (i.e. structural fibres) at advanced ontogenetic stages, in at least some elements, is also present. A variant type of parallel fibred bone, which we have named ‘crossed parallel fibred bone’, is characterized for aetosaurs. In this pseudosuchian group, osteoderms exhibit very important microstructural changes during ontogeny, which can be useful for determining ontogenetic stages from isolated elements. Histological data suggest a relatively early onset of sexual maturity among aetosaurs. Microanatomical analysis from different taxa reveal that having high values of compactness is the plesiomorphic condition for Aetosauria. The notably increased compactness of the osteoderms does not appear to be related to size, ontogeny, sex or reproductive status of the individuals. Although a high degree of compactness of osteoderms and other bones has been considered as evidence for an aquatic lifestyle in vertebrates, such an inference contradicts the current concept of a fully terrestrial lifestyle in aetosaurs.     

Palaeobiology of Triassic procolophonids,inferred from bone microstructure

Procolophonoidea represent the most successful radiation of Parareptilia that lived during the Permo-Triassic. They are one of the few vertebrate groups that survived the end-Permian extinction and are thus important for studying the recovery of the post-extinction terrestrial ecosystem. Here, we investigate the palaeobiology of three Triassic procolophonid parareptiles, namely Sauropareion anoplus, Procolophon trigoniceps and Teratophon spinigenis, from the Karoo Basin of South Africa, inferred from histological analyses of their limb bones. Results reveal that all three taxa exhibit parallel-fibered bone tissue. Growth rings are absent in the Early Triassic Sauropareion and Procolophon whereas annuli are present in the Middle Triassic Teratophon, even during early ontogeny, suggesting a difference in life histories. Morphology and bone histology imply fossorial lifestyles for all three taxa, suggesting that burrowing may have played an important role in their survival during the harsh post-extinction Triassic environment.     

Limb bone histology and growth in Placerias hesternus (Therapsida: Anomodontia) from the Upper Triassic of North America

Abstract: Patterns of bone deposition are reported and deduced from mid‐shaft sections of 21 limb bones of the dicynodont Placerias hesternus from the Placerias Quarry (Upper Triassic), Arizona, USA. All sampled elements of P. hesternus have a large medullary cavity completely filled with bony trabeculae surrounded by dense cortical bone. Dense Haversian bone extends from the perimedullary region to at least the mid‐cortex in all sampled bones. Primary bone in the outer cortex of limb elements of P. hesternus is generally zonal fibrolamellar with a peripheral layer of parallel‐fibred bone. These data suggest periodic rapid osteogenesis followed by slower growth. Among dicynodonts, this strategy is most similar to growth previously reported in other Triassic (Lystrosaurus, Wadiasaurus) and some Permian taxa (Oudenodon, Tropidostoma). An external fundamental system (EFS), suggesting complete or near complete cessation of appositional growth, is present in the largest tibia. This is the first report of EFS in dicynodonts and may represent the attainment of maximum size in P. hesternus. Slow‐growing peripheral bone was observed in elements of varying size in our sample and may support a differential growth pattern between P. hesternus individuals from this locality. A complete growth series of P. hesternus, analysis of Placerias specimens from other localities, and further sampling of other Upper Triassic dicynodonts are needed to better understand a more complete picture of the growth and remodelling patterns that we have initially investigated.     

Diversity of cortical bone morphology in anuran amphibians

The cortical bones of mammals, birds, and reptiles are composed of a complex of woven bone and lamellar bone (fibrolamellar bone) organized into a variety of different patterns; however, it remains unclear whether amphibians possess similar structures. Importantly, to understand the evolutionary process of limb bones in tetrapods, it is necessary to compare the bone structure of amphibians (aquatic to terrestrial) with that of amniotes (mostly terrestrial). Therefore, this study compared the cortical bones in the long bones of several frog species before and after metamorphosis. Using micro-computed tomography (CT), we found that the cortical bones in the fibrolamellar bone of Xenopus tropicalis (Pipoidea superfamily) and Lithobates catesbeianus (Ranoidea superfamily) froglets are dense, whereas those of Ceratophrys cranwelli (Hyloidea superfamily) are porous. To clarify whether these features are common to their superfamily or sister group, four other frog species were examined. Histochemical analyses revealed porous cortical bones in C. ornata and Lepidobatrachus laevis (belonging to the same family, Ceratophryidae, as C. cranwelli). However, the cortical bones of Dryophytes japonicus (Hylidae, a sister group of Ceratophryidae in the Hyloidea superfamily), Microhyla okinavensis (Microhylidae, independent of the Hyloidea superfamily), and Pleurodeles waltl, a newt as an outgroup of anurans, are dense with no observed cavities. Our findings demonstrate that at least three members of the Ceratophryidae family have porous cortical bones similar to those of reptiles, birds, and mammals, suggesting that the process of fibrolamellar bone formation arose evolutionarily in amphibians and is conserved in the common ancestor of amniotes.     

Osteohistology of the non-mammaliaform traversodontids Protuberum cabralense and Exaeretodon riograndensis from southern Brazil

Abstract

The current study presents a detailed analysis of the osteohistology of the Triassic non-mammaliaform traversodontid cynodonts Protuberum cabralense and Exaeretodon riograndesis. The data provided here adds new information on the growth patterns of South American traversodontids. A single subadult individual of P. cabralense revealed bone tissues comprising uninterrupted fibrolamellar bone. Patches of slower growing lamellar bone at the periphery of one of the elements suggests a transition to overall slower growth in later ontogeny. The bone tissues of E. riograndensis also exhibit uninterrupted fibrolamellar bone during early ontogeny, but growth became cyclical from mid-ontogeny. The early rapid, sustained growth observed in these taxa is similar to that seen in other traversodontids, and may be related to the achievement of large body size in the derived members of the clade.     

四川自贡大山铺中侏罗世蜀龙和峨眉龙长骨骨组织结构的初步研究

通过对四川自贡大山铺恐龙动物群中两种主要蜥脚类恐龙—李氏蜀龙和天府峨眉龙肱骨和尺骨的骨组织结构观察,并与我国晚白垩世的几种恐龙长骨进行对比,结果发现:1)恐龙的长骨都具有快速的后生生长速率;2)恐龙的生长方式属于非限定生长,即在成年后并不停止生长;3)不同类型的恐龙到了成年以后,其骨沉积速率可能有较大差异;4)不同类型的恐龙在长骨的生长改建过程中,骨组织内部的重吸收作用有较大差异;5)生长轮结构在不同部位的骨骼中或在骨骼的生长发育过程中可能也有较大差异。     

Long bone histology of Ophiacodon reveals the geologically earliest occurrence of fibrolamellar bone in the mammalian stem lineage

Shared histological characteristics have been observed in the bone matrix and vascularity between Ophiacodontidae and the later therapsids (Synapsida). Historically, this coincidence has been explained as simply a reflection of the presumed aquatic lifestyle of Ophiacodon or even a sign of immaturity. Here we show, by histologically sampling an ontogenetic series of Ophiacodon humeri, as well as additional material, the existence of fibrolamellar bone (FLB) in the postcranial bones of a pelycosaur. Our findings have reaffirmed what previous studies first described as fast growing tissue, and by proxy, have disproven that the highly vascularized cortex is simply a reflection of young age. This tissue demonstrates the classic histological characteristics of true FLB. The cortex consists of primary osteons in a woven bone matrix and remains highly vascularized throughout ontogeny, providing evidence for fast skeletal growth. Overall, the FLB tissue we have described in Ophiacodon is more advanced or “mammal-like” in terms of the osteonal development, bone matrix, and skeletal growth than what has been described thus far for any other pelycosaur taxon. With regards to the histological record, our results remain inconclusive as to the preferred ecology of Ophiacodon due to a similar cortical vascularity pattern exhibited by other carnivorous pelycosaurs. Our findings have set the evolutionary origins of FLB and high skeletal growth rates back approximately 20 million years to the Early Permian, and by phylogenetic extension perhaps the Late Carboniferous.     

Structure and Growth Pattern of Pseudoteeth in Pelagornis mauretanicus (Aves,Odontopterygiformes, Pelagornithidae)

The extinct Odontopterygiformes are the sole birds known to possess strong and sharp bony pseudoteeth, the shape and location of which are closely mimetic of real teeth. The structure of the pseudoteeth is investigated here in a late Pliocene/early Pleistocene species, Pelagornis mauretanicus, using X-ray microtomography and thin sections. The results are interpreted with regard to the pseudotooth mode of growth, and have implications concerning aspects of Pelagornis ecology. The larger pseudoteeth are hollow and approximately cone-shaped, and the smaller ones are rostro-caudally constricted. The walls of pseudoteeth are composed of bone tissue of the fibro-lamellar type, which is intensively remodeled by Haversian substitution. The jaw bones display the same structure as the pseudoteeth, but their vascular canals are oriented parallel to the long axis of the bones, whereas they are perpendicular to this direction in the pseudoteeth. There is no hiatus or evidence of a fusion between the pseudoteeth and the jaw bones. Two possible models for pseudotooth growth are derived from the histological data. The most plausible model is that pseudotooth growth began after the completion of jaw bone growth, as a simple local protraction of periosteal osteogenic activity. Pseudotooth development thus occurred relatively late during ontogeny. The highly vascularized structure and the relative abundance of parallel-fibered bone tissue in the pseudoteeth suggest poor mechanical capabilities. The pseudoteeth were most likely covered and protected by the hardened, keratinized rhamphotheca in the adult during life. The late development of the pseudoteeth would involve a similarly late and/or partial hardening of the rhamphotheca, as displayed by extant Anseriformes, Apterygiformes and some Charadriiformes. This would add support to the hypothesis of a close phylogenetic relationship between Odontopterygiformes and Anseriformes. The late maturation of the Pelagornis feeding apparatus, and hence the delayed capability for efficient prey catching, suggests that Pelagornis was altricial.     

Evolutionary Patterns of Bone Histology and Bone Compactness in Xenarthran Mammal Long Bones

Bone microstructure reflects physiological characteristics and has been shown to contain phylogenetic and ecological signals. Although mammalian long bone histology is receiving increasing attention, systematic examination of the main clades has not yet been performed. Here we describe the long bone microstructure of Xenarthra based on thin sections representing twenty-two species. Additionally, patterns in bone compactness of humeri and femora are investigated. The primary bone tissue of xenarthran long bones is composed of a mixture of woven, parallel-fibered and lamellar bone. The vascular canals have a longitudinal, reticular or radial orientation and are mostly arranged in an irregular manner. Concentric rows of vascular canals and laminar organization of the tissue are only found in anteater bones. The long bones of adult specimens are marked by dense Haversian bone, a feature that has been noted for most groups of mammals. In the long bones of armadillos, secondary osteons have an oblique orientation within the three-dimensional bone tissue, thus resulting in their irregular shape when the bones are sectioned transversely. Secondary remodeling is generally more extensive in large taxa than in small taxa, and this could be caused by increased loading. Lines of arrested growth are assumed to be present in all specimens, but they are restricted to the outermost layer in bones of armadillos and are often masked by secondary remodeling in large taxa. Parameters of bone compactness show a pattern in the femur that separates Cingulata and Pilosa (Folivora and Vermilingua), with cingulates having a lower compactness than pilosans. In addition, cingulates show an allometric relationship between humeral and femoral bone compactness.     

The ontogenetic osteohistology of Tenontosaurus tilletti

Tenontosaurus tilletti is an ornithopod dinosaur known from the Early Cretaceous (Aptian-Albian) Cloverly and Antlers formations of the Western United States. It is represented by a large number of specimens spanning a number of ontogenetic stages, and these specimens have been collected across a wide geographic range (from central Montana to southern Oklahoma). Here I describe the long bone histology of T. tilletti and discuss histological variation at the individual, ontogenetic and geographic levels. The ontogenetic pattern of bone histology in T. tilletti is similar to that of other dinosaurs, reflecting extremely rapid growth early in life, and sustained rapid growth through sub-adult ontogeny. But unlike other iguanodontians, this dinosaur shows an extended multi-year period of slow growth as skeletal maturity approached. Evidence of termination of growth (e.g., an external fundamental system) is observed in only the largest individuals, although other histological signals in only slightly smaller specimens suggest a substantial slowing of growth later in life. Histological differences in the amount of remodeling and the number of lines of arrested growth varied among elements within individuals, but bone histology was conservative across sampled individuals of the species, despite known paleoenvironmental differences between the Antlers and Cloverly formations. The bone histology of T. tilletti indicates a much slower growth trajectory than observed for other iguanodontians (e.g., hadrosaurids), suggesting that those taxa reached much larger sizes than Tenontosaurus in a shorter time.