Long bone histology of Chersina angulata : Interelement variation and life history data

The current study deduced the growth pattern and lifestyle habits of Chersina angulata based on bone histology and cross-sectional geometry of limb bones. Femora, humeri, and tibiae of seven different-sized individuals representing different ontogenetic stages were assessed to determine the interelement and intraskeletal histological variation within and among the tortoises. The bone histology of adult propodials consists of a highly vascularized, uninterrupted fibrolamellar bone tissue with a woven texture in the perimedullary and midcortical regions suggesting overall fast early growth. However, later in ontogeny, growth was slow and even ceased periodically as suggested by slowly formed parallel-fibered bone tissue and several growth marks in the pericortical region. In juvenile individuals, fibrolamellar bone tissue is restricted to the perimedullary regions of propodials as remnants of bone formed during the earliest stages of ontogeny. The epipodials are characterized by having parallel-fibered bone tissue present in their cortices; however, periodic arrests in growth are recorded at various times. Remnants of fibrolamellar bone tissue formed during early ontogeny occur in the epipodials of only a few individuals. Interelement variation is evident, in terms of variation in the orientation of vascular canals between individuals and within the same diaphyseal cross-sections. Different elements show varying cross-sectional geometry, which appear to be correlated with the fossorial behavior of the species. Our results show that of all the long bones, the tibia is least remodeled during ontogeny and it is therefore the best element for skeletochronology.     

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 as deduced from bone microstructure of some selected neotherapsids with special emphasis on dicynodonts: Phylogenetic implications

Osteohistological analysis of the dicynodonts Endothiodon, Diictodon, Lystrosaurus and Wadiasaurus reveals distinctly different growth patterns within a framework of an overall fast growth. The late Permian endemic taxon from India, Endothiodon mahalanobisi and the South African Diictodon feliceps had periodic fast growth. The early Triassic Lystrosaurus murrayi and the middle Triassic Wadiasaurus indicus had an initial fast growth followed by a relatively slow growth later in ontogeny as is observed from the presence of peripheral parallel fibred bone. Although all examined dicynodont genera had an indeterminate growth strategy, the bone microstructure of Wadiasaurus suggests that its growth was much slower than that of other dicynodonts examined. Mapping of osetohistological character states on a cladogram depicting the inter-relationship between available neotherapsid genera shows that fibrolamellar bone tissue, overall fast growth and indeterminate growth strategy were plesiomorphic for the neotherapsids. A considerable reduction in developmental plasticity and evolution of apparently independent growth trajectories from environmental conditions are evident within the non-mammalian cynodonts, with the advanced tritylodontids achieving almost a mammalian growth trajectory.     

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.     

On the origin of high growth rates in archosaurs and their ancient relatives: Complementary histological studies on Triassic archosauriforms and the problem of a “phylogenetic signal” in bone histology

Three possible hypotheses could explain the polarity of the histological features of basal archosauriform and archosauromorph reptiles: either, the fibrolamellar complex is basal; or, the lamellar-zonal complex is basal or finally, the condition varied, and each complex evolved more than once in these early groups. The answer to this question would have broad implications for our understanding of the physiological, ecological, and behavioral features of the first archosaurs. To this end, we sampled the bone histology of various archosauriforms and basal archosaurs from the Triassic and Lower Jurassic: erythrosuchids, proterochampsids, euparkeriids, and basal ornithischian dinosaurs, including forms close to the origin of archosaurs but poorly assessed phylogenetically. The new data suggest that the possibility of reaching and maintaining very high growth rates through ontogeny could have been a basal characteristic of archosauriforms. This was partly retained (at least during early ontogeny) in most lineages of Triassic pseudosuchians, which nevertheless generally relied on lower growth rates to reach large body sizes. This trend to slower growth seems to have been further emphasized among Crocodylomorpha, which may thus have secondarily reverted toward more generalized reptilian growth strategies. Accordingly, their “typical ectothermic reptilian condition” may be a derived condition within archosauriforms, homoplastic to the generalized physiological condition of basal amniotes. On the other hand, ornithosuchians apparently retained and even enhanced the high growth rates of many basal archosauriforms during most of their ontogenetic trajectories. The Triassic may have been a time of “experimentation” in growth strategies for several archosauriform lineages, only one of which (ornithodirans) eventually stayed with the higher investment strategy successfully.     

Life history of Rhamphorhynchus inferred from bone histology and the diversity of pterosaurian growth strategies

Background

Rhamphorhynchus from the Solnhofen Limestones is the most prevalent long tailed pterosaur with a debated life history. Whereas morphological studies suggested a slow crocodile-like growth strategy and superprecocial volant hatchlings, the only histological study hitherto conducted on Rhamphorhynchus concluded a relatively high growth rate for the genus. These controversial conclusions can be tested by a bone histological survey of an ontogenetic series of Rhamphorhynchus.

Methodology/Principal Findings

Our results suggest that Bennett''s second size category does not reflect real ontogenetic stage. Significant body size differences of histologically as well as morphologically adult specimens suggest developmental plasticity. Contrasting the ‘superprecocial hatchling’ hypothesis, the dominance of fibrolamellar bone in early juveniles implies that hatchlings sustained high growth rate, however only up to the attainment of 30–50% and 7–20% of adult wingspan and body mass, respectively. The early fast growth phase was followed by a prolonged, slow-growth phase indicated by parallel-fibred bone deposition and lines of arrested growth in the cortex, a transition which has also been observed in Pterodaustro. An external fundamental system is absent in all investigated specimens, but due to the restricted sample size, neither determinate nor indeterminate growth could be confirmed in Rhamphorhynchus.

Conclusions/Significance

The initial rapid growth phase early in Rhamphorhynchus ontogeny supports the non-volant nature of its hatchlings, and refutes the widely accepted ‘superprecocial hatchling’ hypothesis. We suggest the onset of powered flight, and not of reproduction as the cause of the transition from the fast growth phase to a prolonged slower growth phase. Rapidly growing early juveniles may have been attended by their parents, or could have been independent precocial, but non-volant arboreal creatures until attaining a certain somatic maturity to get airborne. This study adds to the understanding on the diversity of pterosaurian growth strategies.     

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.     

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.     

The osteohistological variability in the evolution of basal avialans

Basal avialans have been the focus of numerous histological studies in the past decade, from which different osteohistological patterns have been described. In this review, we look at the osteohistology in selected specimens from the four major avian groups: the long-tailed Avialae (Archaeopteryx and Jeholornithiformes), basal Pygostylia, Enantiornithes and Euornithes. Developmental and evolutionary changes in the three major bone layers are observed throughout the bone cortex of the limbs, may it be interspecific or intraspecific. Most noteworthy is the adaptive change from the overall lamellar/parallel-fibered bone tissue to a fibrolamellar complex in the mid-cortex as of the basal Pygostylia, potentially even as of the Jeholornithiformes. This change is generally associated with an increase in the density and complexity of the neurovascular network. Another evolutionary-developmental feature is the progressive loss of post-natal growth marks as of the non-ornithurine Euornithes, indicative of uninterrupted bone growth as observed in extant Neornithes. Our comparisons of the osteohistological patterns allow us to better determine how and when specific features typical observed in the avian crown group developed, associated with external and internal factors, and how they lead to what is commonly observed in extant Neornithes.     

Osteomyelitis in a 265-million-year-old titanosuchid (Dinocephalia,Therapsida)

Abstract

Analytical palaeohistology techniques have allowed a better understanding of the microstructure of fossil bone, as well as of bone pathologies of extinct animals. Osteomyelitis is one of the oldest identified bone pathologies, occurring in Synapsida dating back as far as the Lower Permian. Here we show the presence of this pathology in the femur of Jonkeria parva, an omnivorous titanosuchid from the Tapinocephalus Assemblage Zone of the Karoo Basin of South Africa. The pathology is characterised by bony radial spicules growing perpendicular to the normal orientation of the unaffected fibrolamellar bone tissue, and shows localised increase in vascular canal size. Puncture marks on the femur suggests that an attack by a predator may have resulted in a bacterial infection that caused contiguous and subjacent osteomyelitis.     

Ontogeny of postcanine tooth form in the ferret,Mustela putorius (Carnivora: Mammalia), and the evolution of dental diversity within the mustelidae

This study describes dental development within the ferret, Mustela putorius, through study of the form of the carnassial teeth and the upper first molar at progressive growth stages. Primordial teeth were serially sectioned in sagittal and transverse planes and three-dimensional reconstructions of tooth primordia were generated using MacReco software. Regional growth of the crown and asynchronous maturation of the dental tissues were observed in each tooth. The upper carnassial blade develops early and the tooth increases in length rapidly. Lingual growth of the upper carnassial is less pronounced and the protocone and its surrounding region mature late. The lower carnassial blade develops early and the talonid is late to mature. Development of the upper first molar differs from carnassial development in the early emphasis upon transverse growth and reduced lengthwise expansion. The early development of the carnassial blades in the ferret is shared with other carnivores, and may reflect the functional significance of this feature. Later stages of tooth ontogeny differ among carnivoran taxa and the specialized morphology of ferret teeth results from an apparently truncated period of late tooth ontogeny. This suggests that carnivoran species may share a common path of early development that specifies the ontogeny of homologous tooth features and that in later stages developmental differences result in species-specific tooth forms. J. Morphol. 237:69–90, 1998. © 1998 Wiley-Liss, Inc.     

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.     

Unlocking the ring: Occurrence and development of the uninterrupted intrabullar septum in Canidae

The maned wolf, Chrysocyon brachyurus, and some of the earliest canids are known for the peculiar ring-like shape of their intrabullar septum (an incomplete bony partition in the auditory bulla). In attempt to understand the origin of this character state, the auditory bullae in adult and juvenile dried skulls of 28 species of living Caninae were examined with a special emphasis on the occurrence of a ring-like (uninterrupted) septum. In addition to C. brachyurus, this morphology was invariably found in the bush dog, Speothos venaticus, what makes the presence of the uninterrupted septum the first osteological synapomorphy supporting the Chrysocyon–Speothos clade recently revealed by molecular systematics.The canine juvenile morphologies indicate that the intrabullar septum is ring-like at its early developmental stage. As ontogeny progresses, the septum resorbs differentially, depending on taxon, to become horseshoe- or crescent-like. By this transformation of the initially ring-like septum, Caninae seem to ontogenetically parallel a trend found in the phylogeny of Hesperocyoninae, an extinct canid group. The reverse recapitulation occurs, however, in the evolution of Caninae themselves, with their most-derived members having a least-resorbed septum. This implies that the ontogenetic criterion cannot be used for inference of the polarity of septal character states within the Caninae. The evolution of the canine intrabullar septum could have involved a series of heterochronies towards increasingly paedomorphic states in several lineages of the tribe Canini.New data were also obtained on the bone composition of the canid intrabullar septum. While the dorsal septum is entotympanic, the ventral one is in fact ectotympanic in adult Caninae. This compound structure results from penetration of the ventral entotympanic sinus into the ectotympanic.     

Bone surface texture as an ontogenetic indicator in long bones of the Canada goose Branta canadensis (Anseriformes: Anatidae)

Growth series of femora, tibiotarsi, and humeri of the Canada goose Branta canadensis were examined to evaluate whether bone surface textures are reliable indicators of relative age and skeletal maturity in this taxon. The relationship between surface texture and skeletal maturity was analysed by comparing element texture types with both size-based and size-independent maturity estimates. A subsample of hindlimb elements was thin sectioned to observe histological structures underlying various surface textures. Three relative age classes of elements are identifiable based on surface texture. Juvenile and subadult bone textures have fibrous and/or porous areas on the bone shaft and are distinguished by the presence (in juveniles) or absence (in subadults) of coarse longitudinal striations in proximal and/or distal regions. Adult bone texture lacks surface porosity. Immature textures are caused by channels in fibrolamellar bone intersecting the bone surface; the presence or absence of striations is determined by channel orientation. Mature textures may be underlain by fibrolamellar bone with little to no surface exposure of channels, or by lamellar bone deposited after rapid growth ceases. The utility of the textural ageing method appears intimately related to the uninterrupted determinate growth regime of Branta . This suggests that bone surface textures may prove useful as skeletal maturity indicators in both modern and fossil taxa with similar growth regimes, but may not necessarily be reliable for taxa with interrupted and/or indeterminate growth.  © 2006 The Linnean Society of London, Zoological Journal of the Linnean Society , 2006, 148 , 133–168.     

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.     

Long Bone Histology of Sauropterygia from the Lower Muschelkalk of the Germanic Basin Provides Unexpected Implications for Phylogeny

Background

Sauropterygia is an abundant and successful group of Triassic marine reptiles. Phylogenetic relationships of Triassic Sauropterygia have always been unstable and recently questioned. Although specimens occur in high numbers, the main problems are rareness of diagnostic material from the Germanic Basin and uniformity of postcranial morphology of eosauropterygians. In the current paper, morphotypes of humeri along with their corresponding bone histologies for Lower to Middle Muschelkalk sauropterygians are described and interpreted for the first time in a phylogenetic context.

Methodology/Principal Findings

Nothosaurus shows a typical plesiomorphic lamellar-zonal bone type, but varying growth patterns and the occurrence of a new humerus morphotype point to a higher taxonomic diversity than was known. In contrast to the enormous morphological variability of eosauropterygian humeri not assigned to Nothosaurus, their long bone histology is relatively uniform and can be divided into two histotypes. Unexpectedly, both of these histotypes reveal abundant fibrolamellar bone throughout the cortex. This pushes the origin of fibrolamellar bone in Sauropterygia back from the Cretaceous to the early Middle Triassic (early Anisian). Histotype A is assigned to Cymatosaurus, a basal member of the Pistosauroidea, which includes the plesiosaurs as derived members. Histotype B is related to the pachypleurosaur Anarosaurus. Contrary to these new finds, the stratigraphically younger pachypleurosaur Neusticosaurus shows the plesiomorphic lamellar-zonal bone type and an incomplete endochondral ossification, like Nothosaurus.

Conclusions/Significance

Histological results hypothetically discussed in a phylogenetical context have a large impact on the current phylogenetic hypothesis of Sauropterygia, leaving the pachypleurosaurs polyphyletic. On the basis of histological data, Neusticosaurus would be related to Nothosaurus, whereas Anarosaurus would follow the pistosaur clade. Furthermore, the presence of fibrolamellar bone, which is accompanied with increased growth rates and presumably even with increased metabolic rates, already in Anarosaurus and Cymatosaurus can explain the success of the Pistosauroidea, the only sauropterygian group to survive into the Jurassic and give rise to the pelagic plesiosaur radiation.     

EARLY GAMETOPHYTE ONTOGENY OF GLEICHENIA BIFIDA (WILLD.) SPRENG.: PHYLOGENETIC AND ECOLOGICAL IMPLICATIONS

Past investigation of gametophyte ontogeny in Gleichenia bifida indicated that there was considerable plasticity in early developmental stages (spore germination to initiation of two-dimensional growth). Recent examination has shown that this early ontogeny is not so plastic and can be defined by a characteristic series of developmental stages. Cell divisions following germination result in a three-dimensional mass of cells which secondarily initiates the two-dimensional thallus. Early development as a three-dimensional mass correlates with other gametophyte and sporophyte features which indicate Gleichenia to be phylogenetically primitive. This pattern of early ontogeny may also be of adaptive significance in enabling the gametophytes to survive the environmental fluctuations of the exposed, bare-soil habitats which they colonize.