Rethinking the nature of fibrolamellar bone: an integrative biological revision of sauropod plexiform bone formation

Published on Feb 1, 2014in Biological Reviews10.288
· DOI :10.1111/brv.12041
Koen Stein10
Estimated H-index: 10
(University of Bonn),
Edina Prondvai5
Estimated H-index: 5
(MTA: Hungarian Academy of Sciences)
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 integrative approach to bone formation, biomechanics and bone microstructural features of extant and extinct vertebrates to infer life history traits of long extinct, iconic animals like dinosaurs. © 2013 Cambridge Philosophical Society.
  • References (110)
  • Citations (54)
📖 Papers frequently viewed together
412 Citations
38 Citations
4 Authors (Jorge Cubo, ..., Laëtitia Montes)
56 Citations
78% of Scinapse members use related papers. After signing in, all features are FREE.
#1Edwin Alberto Cadena Rueda (NCSU: North Carolina State University)H-Index: 11
#2Mary H. Schweitzer (NCSU: North Carolina State University)H-Index: 25
article i nfo Here we describe variations in osteocytes derived from each of the three bone layers that comprise the turtle shell. We examine osteocytes in bone from four extant turtle species to form a morphological 'baseline' ,a nd then compare these with morphologies of osteocytes preserved in Cenozoic and Mesozoic fossils. Two different morphotypes of osteocytes are recognized: flattened-oblate osteocytes (FO osteocytes), which are particularly abundant in the internal cortex and lamellae of...
20 CitationsSource
#1Nicole Klein (University of Bonn)H-Index: 20
#2P Martinsander (University of Bonn)H-Index: 32
Last. Eric Buffetaut (CNRS: Centre national de la recherche scientifique)H-Index: 37
view all 6 authors...
Background Long bone histology of the most derived Sauropoda, the Titanosauria suggests that titanosaurian long bone histology differs from the uniform bone histology of basal Sauropoda. Here we describe the long bone histology of the titanosaur Ampelosaurus atacis and compare it to that of basal neosauropods and other titanosaurs to clarify if a special titanosaur bone histology exists. Methodology/Principal Findings Ampelosaurus retains the laminar vascular organization of basal Sauropoda, but...
25 CitationsSource
#1Jorge Cubo (University of Paris)H-Index: 23
#2Nathalie Le Roy (University of Burgundy)H-Index: 9
Last. Laëtitia Montes (University of Paris)H-Index: 6
view all 4 authors...
The clade Archosauria contains two very different sister groups in terms of diversity (number of species) and disparity (phenotypic variation): Crurotarsi (taxa more closely related to crocodiles than to birds) and Ornithodira (pterosaurs and dinosaurs including birds). The extant species of Crurotarsi may constitute a biased sample of past biodiversity regarding growth patterns and metabolic rates. Bone histological characters can be conserved over hundreds of millions of years in the fossil re...
56 CitationsSource
#1Roger S. Seymour (University of Adelaide)H-Index: 44
#2Sarah L. Smith (University of Adelaide)H-Index: 1
Last. Daniela Schwarz-Wings (Humboldt University of Berlin)H-Index: 7
view all 5 authors...
The cross-sectional area of a nutrient foramen of a long bone is related to blood flow requirements of the internal bone cells that are essential for dynamic bone remodelling. Foramen area increases with body size in parallel among living mammals and non-varanid reptiles, but is significantly larger in mammals. An index of blood flow rate through the foramina is about 10 times higher in mammals than in reptiles, and even higher if differences in blood pressure are considered. The scaling of fora...
34 CitationsSource
#1Burcin Ekser (University of Pittsburgh)H-Index: 28
#2Edwin Klein (University of Pittsburgh)H-Index: 30
Last. Bruno Gridelli (ISMETT)H-Index: 34
view all 13 authors...
Orthotopic liver transplantation was carried out in baboons using wild-type (WT, n = 1) or genetically-engineered pigs (α1,3-galactosyltransferase gene-knockout, GTKO), n = 1; GTKO pigs transgenic for human CD46, n = 7) and a clinically-acceptable immunosuppressive regimen. Biopsies were obtained from the WT pig liver pre-Tx and at 30 min, 1, 2, 3, 4 and 5 h post-transplantation. Biopsies of genetically-engineered livers were obtained pre-Tx, 2 h after reperfusion and at necropsy (4–7 days after...
36 CitationsSource
#1Shaena Montanari (AMNH: American Museum of Natural History)H-Index: 10
#2Stephen L. Brusatte (AMNH: American Museum of Natural History)H-Index: 34
Last. Mark A. Norell (AMNH: American Museum of Natural History)H-Index: 60
view all 4 authors...
Recent studies have emphasized the ability to reconstruct genome sizes (C-values) of extinct organisms such as dinosaurs, using correlations between known genome sizes and bone cell (osteocyte lacunae) volumes. Because of the established positive relationship between cell size and genome size in extant vertebrates, osteocyte lacunae volume is a viable proxy for reconstructing C-values in the absence of any viable genetic material. However, intra-skeletal osteocyte lacunae size variation, which c...
10 CitationsSource
#1Darja Obradovic Wagner (FU: Free University of Berlin)H-Index: 2
#2Per Aspenberg (Linköping University)H-Index: 60
Bone is specific to vertebrates, and originated as mineralization around the basal membrane of the throat or skin, giving rise to tooth-like structures and protective shields in animals with a soft cartilage-like endoskeleton. A combination of fossil anatomy and genetic information from modern species has improved our understanding of the evolution of bone. Thus, even in man, there are still similarities in the molecular regulation of skin appendages and bone. This article gives a brief overview...
27 CitationsSource
#1Holly N. Woodward (MSU: Montana State University)H-Index: 10
#2John R. Horner (MSU: Montana State University)H-Index: 44
Last. James O. Farlow (Purdue University)H-Index: 27
view all 3 authors...
Abstract An external fundamental system (EFS) is a form of bone microstructure present in the outermost cortex of long bones in animals that have attained skeletal maturity. It indicates an effective cessation of any significant periosteal growth (i.e., growth in circumference or girth). Although an EFS has been noted in several reptile taxa, the idea that reptiles grow continually throughout their lives remains popular. Examination of femoral bone microstructure from captive American Alligators...
62 CitationsSource
#1Timothy G. BromageH-Index: 33
#2Yusuf M. Juwayeyi (LIU: Long Island University)H-Index: 7
Last. John Chisi (UNIMA: University of Malawi)H-Index: 8
view all 6 authors...
Mammalian teeth exhibit incremental structures representing successive forming fronts of enamel at varying time scales, including a short daily increment called a cross striation and a long period cal
15 CitationsSource
#1Michael Kerschnitzki (MPG: Max Planck Society)H-Index: 15
#2Wolfgang Wagermaier (MPG: Max Planck Society)H-Index: 13
Last. Peter Fratzl (MPG: Max Planck Society)H-Index: 86
view all 8 authors...
Bone is a dynamic tissue that is continually undergoing a process of remodeling – an effect due to the interplay between bone resorption by osteoclasts and bone formation by osteoblasts. When new bone is deposited, some of the osteoblasts are embedded in the mineralizing collagen matrix and differentiate to osteocytes, forming a dense network throughout the whole bone tissue. Here, we investigate the extent to which the organization of the osteocyte network controls the collagen matrix arrangeme...
120 CitationsSource
Cited By54
#1Emma R. Schachner (LSU Health Sciences Center New Orleans)H-Index: 13
#2Randall B. Irmis (UofU: University of Utah)H-Index: 23
Last. Sterling J. Nesbitt (VT: Virginia Tech)H-Index: 31
view all 6 authors...
Poposaurus gracilis is a bipedal pseudosuchian archosaur that has been poorly understood since the discovery of the holotype fragmentary partial postcranial skeleton in 1915. Poposaurus. gracilis is a member of Poposauroidea, an unusually morphologically divergent clade of pseudosuchians containing taxa that are bipedal, quadrupedal, toothed, edentulous, and some individuals with elongated thoracic neural spines (i.e., sails). In 2003, a well preserved, fully articulated, and nearly complete pos...
#1Thomas M. Cullen (FMNH: Field Museum of Natural History)H-Index: 6
#2D. Jade Simon (U of T: University of Toronto)
Last. David C. Evans (U of T: University of Toronto)H-Index: 23
view all 4 authors...
#1Benjamin Jentgen-Ceschino (Vrije Universiteit Brussel)H-Index: 1
#2Koen Stein (Vrije Universiteit Brussel)H-Index: 10
Last. Valentin Fischer (University of Liège)H-Index: 15
view all 3 authors...
The histology of sauropod long bones often appears uniform and conservative along their evolutionary tree. One of the main aspects of their bone histology is to exhibit a fibrolamellar complex in t...
#1Donald Davesne (University of Oxford)H-Index: 4
#2Armin D. Schmitt (University of Oxford)H-Index: 1
Last. Sophie Sanchez (Uppsala University)H-Index: 16
view all 5 authors...
Osteocytes, cells embedded within the bone mineral matrix, inform on key aspects of vertebrate biology. In particular, a relationship between volumes of the osteocytes and bone growth and/or genome size has been proposed for several tetrapod lineages. However, the variation in osteocyte volume across different scales is poorly characterised, and mostly relies on incomplete, two-dimensional information. In this study, we propose to characterise the variation of osteocyte volumes in ray-finned fis...
#1Mathieu G. Faure‐Brac (University of Paris)
#2François Pelissier (University of Paris)
Last. Jorge Cubo (University of Paris)H-Index: 23
view all 3 authors...
#1Elizaveta A. Boitsova (SPbU: Saint Petersburg State University)H-Index: 2
#2Pavel P. Skutschas (SPbU: Saint Petersburg State University)H-Index: 13
Last. Olga A MasuytinaH-Index: 1
view all 6 authors...
1 CitationsSource
#1Jorge Cubo (University of Paris)H-Index: 23
#2Nour-Eddine Jalil (University of Paris)H-Index: 3
1 CitationsSource
#1GrunmeierOrvil (Adelphi University)H-Index: 1
#2Michael D. D'Emic (Adelphi University)H-Index: 15
Osteocytes are mature versions of osteoblasts, bone-forming cells that develop in two ways: via ‘static’ osteogenesis, differentiating and ossifying tissue in situ to form a scaffold upon which oth...
2 CitationsSource
#1Christopher T. Griffin (VT: Virginia Tech)H-Index: 4
#2Lauren S. Bano (VT: Virginia Tech)H-Index: 1
Last. Sterling J. Nesbitt (VT: Virginia Tech)H-Index: 31
view all 6 authors...
1 CitationsSource
#1Roberto Toni (Tufts University)H-Index: 11