We present novel findings on sauropod bone histology that cast doubt on general palaeohistological concepts concerning the true nature of woven bone in primary cortical bone and its role in the rapid growth and giant body sizes of sauropod dinosaurs. By preparing and investigating longitudinal thin sections of sauropod long bones, of which transverse thin sections were published previously, we found that the amount of woven bone in the primary complex has been largely overestimated. Using comparative cellular and light-extinction characteristics in the two section planes, we revealed that the majority of the bony lamina consists of longitudinally organized primary bone, whereas woven bone is usually represented only by a layer a few cells thin in the laminae. Previous arguments on sauropod biology, which have been based on the overestimated amount, misinterpreted formation process and misjudged role of woven bone in the plexiform bone formation of sauropod dinosaurs, are thereby rejected. To explain the observed pattern in fossil bones, we review the most recent advances in bone biology concerning bone formation processes at the cellular and tissue levels. Differentiation between static and dynamic osteogenesis (SO and DO) and the revealed characteristics of SO- versus DO-derived bone tissues shed light on several questions raised by our palaeohistological results and permit identification of these bone tissues in fossils with high confidence. By presenting the methods generally used for investigating fossil bones, we show that the major cause of overestimation of the amount of woven bone in previous palaeohistological studies is the almost exclusive usage of transverse sections. In these sections, cells and crystallites of the longitudinally organized primary bone are cut transversely, thus cells appear rounded and crystallites remain dark under crossed plane polarizers, thereby giving the false impression of woven bone. In order to avoid further confusion in palaeohistological studies, we introduce new osteohistological terms as well as revise widely used but incorrect terminology. To infer the role of woven bone in the bone formation of fast-growing tetrapods, we review some aspects of the interrelationships between the vascularity of bone tissues, basal metabolic rate, body size and growth rate. By putting our findings into the context of osteogenesis, we provide a new model for the diametrical limb bone growth of sauropods and present new implications for the evolution of fast growth in vertebrates. Since biomechanical studies of bone tissues suggest that predominant collagen fibre orientation (CFO) is controlled by endogenous, functional and perhaps phylogenetic factors, the relationship between CFO and bone growth rate as defined by Amprino's rule, which has been the basis for the biological interpretation of several osteohistological features, must be revised. Our findings draw attention to the urgent need for revising widely accepted basic concepts of palaeohistological studies, and for a more integrativ...
Research on the bone histology of extant and extinct animals has a long scientific history and an accurate description of microstructural tissues is the cornerstone of the field. Ideally, terminology needs to convey as much information as possible about the structural, developmental, and functional aspects of bone tissues corresponding to the up-to-date knowledge of the time. However, current terms are not always consistent with new observations and advances in the field of bone biology. We provide a brief overview of some ambiguities and their origins, and suggest a new approach of bone tissue classification and description that is congruent with our current understanding of bone as a living tissue, emphasizing its developmental aspects. This approach requires the introduction of a new term, namely 'woven-parallel complex', for describing a broad range of complex bone tissue types, including intramembranous and endochondral bones, and different types of primary as well as secondary bone tissues. We reconsider the classical concept of fibrolamellar complex, which we place within the new developmental approach. Finally, using non-archosaurian archosauromorphs as an example group, we demonstrate how the new approach can be utilized in an evolutionary context. The present study demonstrates the relevance and constant evolution of technical terminology along with the advances of the field of science.
BackgroundRhabdodontid ornithopod dinosaurs are characteristic elements of Late Cretaceous European vertebrate faunas and were previously collected from lower Campanian to Maastrichtian continental deposits. Phylogenetic analyses have placed rhabdodontids among basal ornithopods as the sister taxon to the clade consisting of Tenontosaurus, Dryosaurus, Camptosaurus, and Iguanodon. Recent studies considered Zalmoxes, the best known representative of the clade, to be significantly smaller than closely related ornithopods such as Tenontosaurus, Camptosaurus, or Rhabdodon, and concluded that it was probably an island dwarf that inhabited the Maastrichtian Haţeg Island.Methodology/Principal FindingsRhabdodontid remains from the Santonian of western Hungary provide evidence for a new, small-bodied form, which we assign to Mochlodon vorosi n. sp. The new species is most similar to the early Campanian M. suessi from Austria, and the close affinities of the two species is further supported by the results of a global phylogenetic analysis of ornithischian dinosaurs. Bone histological studies of representatives of all rhabdodontids indicate a similar adult body length of 1.6–1.8 m in the Hungarian and Austrian species, 2.4–2.5 m in the subadults of both Zalmoxes robustus and Z. shqiperorum and a much larger, 5–6 m adult body length in Rhabdodon. Phylogenetic mapping of femoral lengths onto the results of the phylogenetic analysis suggests a femoral length of around 340 mm as the ancestral state for Rhabdodontidae, close to the adult femoral lengths known for Zalmoxes (320–333 mm).Conclusions/SignificanceOur analysis of body size evolution does not support the hypothesis of autapomorhic nanism for Zalmoxes. However, Rhabdodon is reconstructed as having undergone autapomorphic giantism and the reconstructed small femoral length (245 mm) of Mochlodon is consistent with a reduction in size relative to the ancestral rhabdodontid condition. Our results imply a pre-Santonian divergence between western and eastern rhabdodontid lineages within the western Tethyan archipelago.
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.
With their elongated forelimbs and variable aerial skills, paravian dinosaurs, a clade also comprising modern birds, are in the hotspot of vertebrate evolutionary research. Inferences on the early evolution of flight largely rely on bone and feather morphology, while osteohistological traits are usually studied to explore life-history characteristics. By sampling and comparing multiple homologous fore- and hind limb elements, we integrate for the first time qualitative and quantitative osteohistological approaches to get insight into the intraskeletal growth dynamics and their functional implications in five paravian dinosaur taxa, Anchiornis, Aurornis, Eosinopteryx, Serikornis, and Jeholornis. Our qualitative assessment implies a considerable diversity in allometric/isometric growth patterns among these paravians. Quantitative analyses show that neither taxa nor homologous elements have characteristic histology, and that ontogenetic stage, element size and the newly introduced relative element precocity only partially explain the diaphyseal histovariability. Still, Jeholornis, the only avialan studied here, is histologically distinct from all other specimens in the multivariate visualizations raising the hypothesis that its bone tissue characteristics may be related to its superior aerial capabilities compared to the non-avialan paravians. Our results warrant further research on the osteohistological correlates of flight and developmental strategies in birds and bird-like dinosaurs.
Thin fossil eggshell from Upper Cretaceous deposits of Europe, characterized by nodular ornamentation similar to modern gekkotan eggshell, has mostly been interpreted as gekkotan (=‘geckoid’) in origin. However, in some cases, as for the oogenus Pseudogeckoolithus, a theropod affinity has also been suggested. The true affinity of these fossil ‘geckoid’ eggshells has remained controversial due to the absence of analytical methods for identifying genuine gecko eggshell in the fossil record. In this study, we apply electron backscatter diffraction (EBSD) analysis to latest Cretaceous European ‘geckoid’ (including Pseudogeckoolithus) eggshell, in comparison with modern gekkotan and theropod (avian) eggshell. We found that Pseudogeckoolithus has a definite theropod eggshell‐like crystallographic configuration, in clear contrast to that seen in modern ‘gecko eggshells’. Furthermore, the crystallography of the nodular ornamentation in Pseudogeckoolithus is similar to that seen in megapode eggshell, but different from that of gecko eggshell, despite superficial morphological similarity. The remarkable morphological similarities between Pseudogeckoolithus and modern gecko eggshells are thus convergent, and the ‘gekkotan affinity’ hypothesis can be dismissed for Pseudogeckoolithus. This study provides a template for differentiating true gekkotan from dinosaurian eggshells in the fossil record. The potential functional significance of eggshell ornamentation, lost in most modern birds, requires further study, and experimental zoological approach may shed light on this issue. Finally, the present results suggest caution about the dangers of using potentially homoplastic eggshell characters in eggshell parataxonomy.
Ankylosaurian dinosaurs were low-browsing quadrupeds that were thought of as simple orthal pulpers exhibiting minimal tooth occlusion during feeding, as in many extant lizards. Recent
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