Parallel-fibred Bone Research Articles

A new adult specimen of the basalmost ornithuromorph bird Archaeorhynchus spathula (Aves: Ornithuromorpha) and its implications for early avian ontogeny

Most living birds characteristically grow rapidly and reach adult size within a year. Nevertheless, little is known about how such an advanced developmental strategy evolved despite many discoveries of early fossil birds. Here we assess the long-bone histology from a new adult specimen of Archaeorhynchus spathula, the basalmost taxon of Ornithuromorpha. Ornithuromorpha is the most inclusive clade containing extant birds but not the Mesozoic Enantiornithes. Histological analysis reveals that the cortex is composed of parallel-fibred bone with three lines of arrested growth, indicative of slow and annually interrupted growth for this taxon. Such bone histology is significantly different from that of other known basal ornithuromorphs, but resembles that of enantiornithines, which leads us to suggest protracted slow growth in the common ancestor of Ornithuromorpha and Enantiornithes. The fusion sequence of the tarsometatarsus between Enantiornithes and Ornithuromorpha has long been hypothesized to be differen...

Bone histology, microanatomy, and growth of the nothosauroid Simosaurus gaillardoti (Sauropterygia) from the Upper Muschelkalk of southern Germany/Baden-Württemberg

Simosaurus gaillardoti was a large eosauropterygian (Sauropterygia), a group of diverse diapsid marine reptiles. Its occurrence correlates to transgression phases in the Germanic Basin and a former morphological study hypothesized that Simosaurus was capable of sustained swimming. Microanatomical analysis of five long bones revealed functional differences between the humerus and femur but did not confirm sustained swimming in Simosaurus. It had certain active swimming abilities but – based on microanatomy – it was a less efficient swimmer when compared to contemporaneously living nothosaurs. Simosaurus grew with well-vascularized coarse parallel-fibred bone tissue. Growth marks appear as broad zones and thin annuli. Two specimens show an external fundamental system in their outer cortex. For three samples the logistic growth model best describes growth in Simosaurus. The estimated ages at death range between 7 and 13 years, asymptotic masses range between 113 and 129kg and were reached after 10 up to 20 years. Maximum growth rates were between 44 and 69g per day, and higher than of an extant similar-sized reptile such as Varanus komodoensis, Alligator mississippiensis, and Caretta caretta, but are still consistent with the variability seen in extant reptiles. Growth of one femur followed the von Bertalanffy model but the model's biological reliability is questionable due to an unrealistic high hatchling mass.

Histology of the heterostracan dermal skeleton: Insight into the origin of the vertebrate mineralised skeleton

ABSTRACTLiving vertebrates are divided into those that possess a fully formed and fully mineralised skeleton (gnathostomes) versus those that possess only unmineralised cartilaginous rudiments (cyclostomes). As such, extinct phylogenetic intermediates of these living lineages afford unique insights into the evolutionary assembly of the vertebrate mineralised skeleton and its canonical tissue types. Extinct jawless and jawed fishes assigned to the gnathostome stem evidence the piecemeal assembly of skeletal systems, revealing that the dermal skeleton is the earliest manifestation of a homologous mineralised skeleton. Yet the nature of the primitive dermal skeleton, itself, is poorly understood. This is principally because previous histological studies of early vertebrates lacked a phylogenetic framework required to derive evolutionary hypotheses. Nowhere is this more apparent than within Heterostraci, a diverse clade of primitive jawless vertebrates. To this end, we surveyed the dermal skeletal histology of heterostracans, inferred the plesiomorphic heterostracan skeleton and, through histological comparison to other skeletonising vertebrate clades, deduced the ancestral nature of the vertebrate dermal skeleton. Heterostracans primitively possess a four‐layered skeleton, comprising a superficial layer of odontodes composed of dentine and enameloid; a compact layer of acellular parallel‐fibred bone containing a network of vascular canals that supply the pulp canals (L1); a trabecular layer consisting of intersecting radial walls composed of acellular parallel‐fibred bone, showing osteon‐like development (L2); and a basal layer of isopedin (L3). A three layered skeleton, equivalent to the superficial layer L2 and L3 and composed of enameloid, dentine and acellular bone, is possessed by the ancestor of heterostracans + jawed vertebrates. We conclude that an osteogenic component is plesiomorphic with respect to the vertebrate dermal skeleton. Consequently, we interpret the dermal skeleton of denticles in chondrichthyans and jawless thelodonts as independently and secondarily simplified. J. Morphol. 276:657–680, 2015. © 2015 The Authors Journal of Morphology Published by Wiley Periodicals, Inc.

Osteohistology of hyperodapedontine rhynchosaurs (Diapsida, Archosauromorpha) from the Upper Triassic of Southern Brazil.

The first osteohistological study focused exclusively on rhynchosaurs (non-archosauriform archosauromorphs), based on the hyperodapedontines Teyumbaita sulcognathus and Hyperodapedon sp., from the Upper Triassic of Southern Brazil, indicates a relatively rapid growth rate in early ontogeny shown by the fibrolamellar complex, with a change to slow intermittent growth during late ontogeny represented by parallel-fibred bone with several growth marks. Contrary to previous studies, which described a typical non-archosaur reptilian bone tissue pattern for rhynchosaurs, with growth marks extending across the entire cortex, we demonstrate that, in both studied taxa, the initial growth rate was faster in comparison to the later. This suggests that the ability of rapid growth at high rates was already present in basal non-archosauriform archosauromorphs.

A histological study of a femur of Plagiosuchus, a Middle Triassic temnospondyl amphibian from southern Germany, using thin sections and micro-CT scanning

AbstractThe histology of a femur of Plagiosuchus, a Middle Triassic temnospondyl amphibian, is described on the basis of two supplementary methods: classic thin sectioning and micro-CT scanning. In addition, the effectiveness of high-resolution micro-CT scanning for histological analysis is assessed. A classic, mid-shaft thin section of the femur was prepared, but prior to slicing two micro-CT scans were made. One of these has an image stack of a total of 1,024 images in the horizontal plane and a slice thickness of 87.8 μm, so that the entire bone could be captured, while the second was at mid-shaft region only, yet with a higher resolution of 28.3 μm and an image stack of 787 images in the horizontal plane. The classic thin section shows a very small medullary region which is surrounded by a layer of endosteal bone. The thick cortex is highly porous with numerous large, mainly longitudinal, vascular canals arranged in layers. In the deepest cortex woven bone occurs and primary osteons had locally started to form (incipient fibro-lamellar bone), which gradually passes into parallel-fibred bone and more lamellar bone close to the outer surface. Remains of a Kastschenko line were identified, enabling a reconstruction of the entire growth record. Five Lines of Arrested Growth (LAG) could be counted. The micro-CT scan enabled observations of the ontogenetic growth stages and calculation of growth rate on the basis of a single specimen. The micro-CT scan permitted a reconstruction of the ontogenetic development and the exact deposition rate per annum. Moreover, at higher resolution the micro-CT scan revealed data on micro-anatomical characters, such as porosity and skeletochronology (growth mark count). In conclusion, micro-CT scans do provide an alternative in cases where thin sectioning of the original bone is not possible.

Osteoderm microstructure of “rauisuchian” archosaurs from South America

In this contribution we analyze and discuss the microanatomy and histology of postcranial osteoderms of a number of “rauisuchians” from different localities of South America (Argentina and Brazil). The studied sample includes osteoderms of Fasolasuchus tenax, Prestosuchus chiniquensis, Saurosuchus galilei and an undetermined rauisuchian from Brazil. The bone microanatomy of the osteoderms is variable: whereas some specimens have a rather compact structure, others show a diploe architecture with a central cancellous core bordered by two compact cortices. Both external and basal cortices are mainly composed of poorly vascularized, fine and coarse parallel-fibred bone and networks of interwoven and mineralized fiber bundles. The internal region of the non-remodeled specimens consists of a well-vascularized core in which the intrinsic fibers exhibit important variations (even in the same specimen), ranging from coarse, parallel-fibred to woven-fibred bone tissues. Lines of arrested growth (LAGs) are well recorded in both basal and external cortices. Differences in the bone microstructure (compact vs. diploe) could be related to the age, sex and reproductive status of the sampled individuals. Hence, age estimation based on the count of LAGs in rauisuchian osteoderms appears to be reliable only in the early stages of ontogeny. The bone microstructure suggests that rauisuchian osteoderms were originated through a mechanism that involves both intramembranous and metaplastic ossifications.

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 FindingsOur 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/SignificanceThe 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.

The long bone histology of Ceresiosaurus (Sauropterygia, Reptilia) in comparison to other eosauropterygians from the Middle Triassic of Monte San Giorgio (Switzerland/Italy)

Ceresiosaurus is a secondarily marine reptile that lived during the Middle Triassic (Ladinian–Anisian) in a subtropical lagoonal environment with varying open marine influences. The genus comprises two species, Ceresiosaurus calcagnii and C. lanzi, and represents one of the largest vertebrate of up to 3-m snout-tail length from the UNESCO World Heritage site Monte San Giorgio, which is settled along the Swiss–Italian border. Earlier morphological studies identified this genus as basal sauropterygian still possessing many similarities with the plesiomorphic ancestral terrestrial condition. Interspecific morphological variation was interpreted as indicator for different habit(at) preferences by ascribing two locomotion types for each of the species. In this study, detailed data on the microstructure of the long bones are given and findings were put into a palaeoecological and phylogenetic context in comparison to other sauropterygians from Monte San Giorgio. Results showed that both Ceresiosaurus species retain a calcified cartilaginous core in the medullary region in at least young individuals. They both exhibit cyclical bone growth of lamellar to parallel-fibred bone matrices with undulating incremental growth marks and low to moderate vascularisation (lamellar-zonal bone tissue type). Interspecific variation comprises differences in the distribution of differently organised bone matrices and the size, orientation and number of vascularisation. The vascularisation pattern (abundance and orientation of the canals) of the pachyosteosclerotic long bones of C. calcagnii mostly resembles the histotype of the stratigraphically youngest pachypleurosaurid from Monte San Giorgio, Neusticosaurus edwardsii (except for the presence of primary osteons in the cortex of the former). The bone sample of C. lanzi is only osteosclerotic and most similar to young Nothosaurus (except for the irregular presence of fibrolamellar bone in the latter). The slightly different growth pattern already at young ontogenetic stages might be linked to a different mode of life within the restricted lagoonal basin for Ceresiosaurus, which supports previous studies on the morphological data that ascribed two different locomotion types.

The palaeohistology of the basal ichthyosaur Mixosaurus (Ichthyopterygia, Mixosauridae) from the Middle Triassic: Palaeobiological implications

Here, we provide the first bone histological examination of an ontogenetic series of the basal ichthyosaur Mixosaurus encompassing postnatal to large adult specimens. Growth marks are present in sampled humeri, a femur, a fibula, as well as in other skeletal elements (gastral ribs). Ontogenetic changes are traceable throughout stylo- and zeugopodial development, but interior remodelling and resorption deleted part of the internal growth record in the primary cortex. Mixosaurus humeri started as flat structures consisting of a core of endochondral woven bone and residual calcified cartilage, whereas growth continued by deposition of periosteal fibrolamellar and parallel-fibred bone. Unlike the fast-growing post-Triassic ichthyosaurs that lack growth marks, microstructural and life history data are now becoming available for a basal ichthyosaur. The high growth rate of Mixosaurus may indicate that higher metabolic rates characterised small, non-thunniform ichthyosaurs, as had been suggested already for post-Triassic, cruising forms.

Dermal armour histology of aetosaurs (Archosauria: Pseudosuchia), from the Upper Triassic of Argentina and Brazil

Cerda, I.A. & Desojo, J.B. 2010: Dermal armour histology of aetosaurs (Archosauria: Pseudosuchia), from the Upper Triassic of Argentina and Brazil. Lethaia, Vol. 44, pp. 417–428. One of the most striking features documented in aetosaurs is the presence of an extensive bony armour composed of several osteoderms. Here, we analyse the bone microstructure of these elements in some South American Aetosaurinae aetosaurs, including Aetosauroides scagliai. In general terms, Aetosaurinae osteoderms are compact structures characterized by the presence of three tissue types: a basal cortex of poorly vascularized parallel-fibred bone tissue, a core of highly vascularized fibro-lamellar bone, and an external cortex of rather avascular lamellar bone tissue. Sharpey’s fibres are more visible at the internal core, toward the lateral margins and aligned parallel to the major axis of the dermal plate. No evidence of metaplastic origin is reported in the osteoderms, and we hypothesize an intramembranous ossification for these elements. The bone tissue distribution reveals that the development of the osteoderm in Aetosaurinae starts in a position located medial to the plate midpoint, and the main sites of active osteogenesis occur towards the lateral and medial edges of the plate. The osteoderm ornamentation is originated and maintained by a process of resorption and redeposition of the external cortex, which also includes preferential bone deposition in some particular sites. Given that no secondary reconstruction occurs in the osteoderms, growth marks are well preserved and they provide very important information regarding the relative age and growth pattern of Aetosaurinae aetosaurs. □Aetosauria, Aetosauroides, Archosauria, bone microstructure, integumentary skeleton, osteoderm.

Morphological and histological changes of dermal scales during the fish-to-tetrapod transition

Witzmann F. (2011). Morphological and histological changes of dermal scales during the fish-to-tetrapod transition. —Acta Zoologica (Stockholm) 92: 281–302. The gastral scales of limbed tetrapodomorphs evolved from the ‘elpistostegid’-type of scale by an enlargement and differentiation of the articulation facets and a shortening and broadening of the keel. These changes caused a tighter connection between gastral scales within a scale row and a greater overlap between the rows. Dorsal round scales of limbed tetrapodomorphs developed from a gastral scale-type by an alteration of the ontogenetic pathway. The posterolateral direction of scale rows in ‘elpistostegids’ was retained in the gastral scalation of most limbed tetrapodomorphs, whereas the arrangement of round dorsal scales is modified to a transverse orientation. Both gastral and dorsal scales of limbed tetrapodomorphs consist solely of parallel-fibred bone with circumferential growth marks. The proportionally larger overlap surfaces of gastral scales and their mode of articulation in the ventral midline indicate that the body of limbed tetrapodomorphs might have been more flexible than that of their finned relatives. The alteration of dermal scales was one of the most rapid morphological changes during the fish-to-tetrapod transition. Once established, gastral and dorsal scales were retained as a conservative character in different lineages of basal tetrapods, in both the amphibian and the amniote lineages.

Conserved bone microstructure in the shells of long-necked and short-necked chelid turtles (Testudinata, Pleurodira)

<strong class="journal-contentHeaderColor">Abstract.</strong> Extant and fossil chelids are restricted to South America and Australasia. Based on morphological data, long-necked and short-necked chelids are hypothesised to form natural groups respectively, whereas molecular and serological data indicate South American and Australasian chelids are monophyletic, regardless of neck-length. Here I provide shell bone histological and microanatomical data and character mapping of seven chelid taxa and the Late Jurassic stem-pleurodiran <i>Platychelys oberndorferi</i> Wagner, 1853 to test both competing hypotheses. The chelid shells show conserved bone microstructures, many of which are plesiomorphic for all turtles. Part of the variation among chelid shell microstructures could be attributed to functional aspects associated with the ecology of the taxa, i.e. adaptation to an aquatic lifestyle. The character mapping further indicates that the hypothesis of clades based on neck length is supported by two synapomorphies (i.e., parallel-fibred bone grading into lamellar bone in internal cortex and vascularisation of internal cortex) and one less tree step (16 instead of 17) in contrast to the molecular-based separation based on geographic distribution. <br><br> doi:<a href="http://dx.doi.org/10.1002/mmng.200800009" target="_blank">10.1002/mmng.200800009</a>

Conserved bone microstructure in the shells of long-necked and short-necked chelid turtles (Testudinata, Pleurodira)

Extant and fossil chelids are restricted to South America and Australasia. Based on morphological data, long-necked and short-necked chelids are hypothesised to form natural groups respectively, whereas molecular and serological data indicate South American and Australasian chelids are monophyletic, regardless of neck-length. Here I provide shell bone histological and microanatomical data and character mapping of seven chelid taxa and the Late Jurassic stem-pleurodiran &lt;i&gt;Platychelys oberndorferi&lt;/i&gt; Wagner, 1853 to test both competing hypotheses. The chelid shells show conserved bone microstructures, many of which are plesiomorphic for all turtles. Part of the variation among chelid shell microstructures could be attributed to functional aspects associated with the ecology of the taxa, i.e. adaptation to an aquatic lifestyle. The character mapping further indicates that the hypothesis of clades based on neck length is supported by two synapomorphies (i.e., parallel-fibred bone grading into lamellar bone in internal cortex and vascularisation of internal cortex) and one less tree step (16 instead of 17) in contrast to the molecular-based separation based on geographic distribution. &lt;br&gt;&lt;br&gt; doi:&lt;a href="http://dx.doi.org/10.1002/mmng.200800009" target="_blank"&gt;10.1002/mmng.200800009&lt;/a&gt;

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.

Modelling the three-dimensional elastic constants of parallel-fibred and lamellar bone

The complex hierarchical structure of lamellar bone makes understanding structure–mechanical function relations, very difficult. We approach the problem by first using the relatively simple structure of parallel-fibred bone to construct a mathematical model for calculating Young's moduli in three-dimensions. Parallel-fibred bone is composed essentially of arrays of mineralized collagen fibrils, which are also the basic structural motif of the individual lamellae of lamellar bone. Parallel-fibred bone structure has orthotropic symmetry. As the sizes and shapes of crystals in bone are not well known, the model is also used to compare the cases of platelet-, ribbon- and sheet-reinforced composites. The far more complicated rotated plywood structure of lamellar bone results in the loss of the orthotropic symmetry of individual lamellae. The mathematical model used circumvents this problem by sub-dividing the lamellar unit into a thin lamella, thick lamella, transition zone between them, and the recently observed “back-flip” lamella. Each of these is regarded as having orthotropic symmetry. After the calculation of their Young's moduli they are rotated in space in accordance with the rotated plywood model, and then the segments are combined to present the overall modulus values in three-dimensions. The calculated trends compare well with the trends in microhardness values measured for circumferential lamellar bone. Microhardness values are, as yet, the only measurements available for direct comparison. Although the model is not directly applicable to osteonal bone, which is composed of many hollow cylinders of lamellar bone, the range of calculated modulus values and the trends observed for off-axis calculations, compare well with measured values. © 1998 Chapman & Hall

Histological identification of osteocytes in the allegedly acellular bone of the sea breams Acanthopagrus australis, Pagrus auratus and Rhabdosargus sarba (Sparidae, Perciformes, Teleostei)

The bone of advanced teleost fishes such as those of the family Sparidae is said to lack osteocytes or to be acellular. Acellularity has been determined by apparent lack of osteocyte lacunae. This study questions the validity of this criterion. Scanning electron and light microscopy of paraffin and resin sections were used to show that the sides of sea bream mandibles consist of laminar parallel-fibred bone that we call tubular bone, because it contains tubules, and localised regions of Sharpey fibre bone. Osteocytes lie along the walls of tubules that also contain collagen fibril bundles (T-fibres), or in the lumens of tubules that do not contain T-fibres. We show that the osteocytes are derived from osteoblasts. The T-fibre system is different from other fibre systems that have been described. The tubules enclose wide T-fibres (lenticular in cross-section, maximum width about 8 microns) that taper at their ends and continue as thin T-fibres (round in cross-section, about 2 microns wide). The T-fibres originate in the periosteum. In mature tubular bone, spaces of increasing size develop around the osteocytes. Osteocytes are released from the bone matrix and become postosteocytes or bone-lining cells. Secondary bone lines the largest spaces. In Sharpey fibre bone, small osteocytes in small lacunae (about 2 microns wide) are found in columns parallel to the Sharpey fibres. Large osteocytes are found in large round spaces and are much larger than comparable osteocytes in lacunae in the bone of the salmon Salmo salar. We conclude that an absence of visible or conventional osteocyte lacunae does not mean that the cells themselves are absent. There are cells and two types of collagen fibre bundle in the tubules. The cells are osteocytes derived from osteoblasts, and these osteocytes apparently resorb bone with the result that large amounts of bone are destroyed. "Acellular" tubular and Sharpey fibre bone are types of cellular bone that differ from each other and from conventional cellular bone.

Morphological study of intercellular junctions during osteocyte differentiation

Ultrastructural studies were carried out on intercellular relationships during osteocyte differentiation in primary parallel-fibred bone of newborn rabbit. It was found that throughout the whole differentiative process preosteocytes are in close relationship with the neighboring cells (osteoblasts, osteocytes) by means of variously-shaped intercellular contacts (invaginated finger-like, side-to-side, and end-to-end) and two types of specialized junctions: gap and adherens. The pivotal role played by these contacts and junctions in osteocyte differentiation and activity is considered in the context of their particular functional significance.

Osteocyte Differentiation in the Tibia of Newborn Rabbit: An Ultrastructural Study of the Formation of Cytoplasmic Processes

The morphological changes undergone by the osteoblast at the ultrastructural level, during its differentiation into osteocyte, were studied in the primary parallel-fibred bone of the newborn rabbit by means of incomplete three-dimensional reconstruction from partially serial-sectioned preosteocytes. The findings obtained suggest that the formation of osteocyte cytoplasmic processes is an asynchronous and asymmetrical phenomenon that seems to precede the mineralization of the organic matrix and to give rise to an asymmetrical mature osteocyte. The functions of cytoplasmic processes as regards bone formation, cell nutrition and osteoblast modulation are discussed. The mechanism by which the osteoblast 'enters' the bone matrix is hypothesized.