Abstract

BackgroundDinosaurs are unique among terrestrial tetrapods in their body sizes, which range from less than 3 gm in hummingbirds to 70,000 kg or more in sauropods. Studies of the microstructure of bone tissue have indicated that large dinosaurs, once believed to be slow growing, attained maturity at rates comparable to or greater than those of large mammals. A number of structural criteria in bone tissue have been used to assess differences in rates of osteogenesis in extinct taxa, including counts of lines of arrested growth and the density of vascular canals.Methodology/Principal FindingsHere, we examine the density of the cytoplasmic surface of bone-producing cells, a feature which may set an upper limit to the rate of osteogenesis. Osteocyte lacunae and canaliculi, the cavities in bone containing osteocytes and their extensions, were measured in thin-sections of primary (woven and parallel fibered) bone in a diversity of tetrapods. The results indicate that bone cell surfaces are more densely organized in the Saurischia (extant birds, extinct Mesozoic Theropoda and Sauropodomorpha) than in other tetrapods, a result of denser branching of the cell extensions. The highest postnatal growth rates among extant tetrapods occur in modern birds, the only surviving saurischians, and the finding of exceptional cytoplasmic surface area of the cells that produce bone in this group suggests a relationship with bone growth rate. In support of this relationship is finding the lowest cell surface density among the saurischians examined in Dinornis, a member of a group of ratites that evolved in New Zealand in isolation from mammalian predators and show other evidence of lowered maturation rates.

Highlights

  • Structural Organization and GrowthSkeletal bone provides the framework supporting the body and the mechanism for locomotion, making its strength and rate of maturation vital to each individual

  • Our results show that cell bodies of smaller diameter allow larger cell surface areas if the cell interspaces are filled with a greater abundance of densely branching cell processes

  • Saurischian dinosaurs have, in their fastest forming types of bone tissue, the most densely organized bone cell cytoplasm of any of the tetrapod groups examined. This higher density results from more profuse branching of the cell processes and is first seen in late Triassic basal saurischians. This increased density appears to have been initiated by reduction in the size of the cell bodies because smaller cell perimeters limit the number of branches that can emerge directly from the cell body

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Summary

Introduction

Structural Organization and GrowthSkeletal bone provides the framework supporting the body and the mechanism for locomotion, making its strength and rate of maturation vital to each individual. At a higher level of structural organization, fibrolamellar (plexiform) bone [5]–[7] is a vascular based tissue that increases the diametric rate of bone growth by enlarging the surface areas on which new bone can simultaneously form. In this tissue, trabeculae of rapidly formed woven or parallel-fibered bone are extended outward from the growing surface, leaving unfilled spaces around the vascular canals which are subsequently filled with slower forming but stronger lamellar tissue to form primary osteons [8], [9]. A number of structural criteria in bone tissue have been used to assess differences in rates of osteogenesis in extinct taxa, including counts of lines of arrested growth and the density of vascular canals.

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