Differing trabecular bone architecture in dinosaurs and mammals contribute to stiffness and limits on bone strain.

Trevor G Aguirre,Aniket Ingrole,Luca Fuller,Anthony R Fiorillo,Seth W Donahue,Tim W Seek,Joseph J W Sertich,Deepak Vashishth

doi:10.1371/journal.pone.0237042

Abstract

The largest dinosaurs were enormous animals whose body mass placed massive gravitational loads on their skeleton. Previous studies investigated dinosaurian bone strength and biomechanics, but the relationships between dinosaurian trabecular bone architecture and mechanical behavior has not been studied. In this study, trabecular bone samples from the distal femur and proximal tibia of dinosaurs ranging in body mass from 23-8,000 kg were investigated. The trabecular architecture was quantified from micro-computed tomography scans and allometric scaling relationships were used to determine how the trabecular bone architectural indices changed with body mass. Trabecular bone mechanical behavior was investigated by finite element modeling. It was found that dinosaurian trabecular bone volume fraction is positively correlated with body mass similar to what is observed for extant mammalian species, while trabecular spacing, number, and connectivity density in dinosaurs is negatively correlated with body mass, exhibiting opposite behavior from extant mammals. Furthermore, it was found that trabecular bone apparent modulus is positively correlated with body mass in dinosaurian species, while no correlation was observed for mammalian species. Additionally, trabecular bone tensile and compressive principal strains were not correlated with body mass in mammalian or dinosaurian species. Trabecular bone apparent modulus was positively correlated with trabecular spacing in mammals and positively correlated with connectivity density in dinosaurs, but these differential architectural effects on trabecular bone apparent modulus limit average trabecular bone tissue strains to below 3,000 microstrain for estimated high levels of physiological loading in both mammals and dinosaurs.

Highlights

Terrestrial dinosaurs were massive animals that placed exceptional mechanical demands on their bones, but it is unknown how trabecular bone architecture helped meet those demands
Previous studies of extant mammalian and avian species found no correlation between trabecular bone volume fraction and body mass in animals ranging in body mass from mouse to elephant [8, 9]
This result is surprising since animals with greater mass require stiffer bone structures to support larger gravitational loads and apparent elastic modulus is positively correlated with bone volume fraction [10]

Summary

Introduction

Terrestrial dinosaurs were massive animals that placed exceptional mechanical demands on their bones, but it is unknown how trabecular bone architecture helped meet those demands. The physiological process of bone remodeling helps achieve a balance between bone weight and mechanical competence, repairs and limits the accumulation of fatigue damage [3], and adapts to limit strains [4]. It is noteworthy that trabecular bone volume fraction does not scale with body mass in mammalian and avian long bones. This is surprising because it is well documented that the mechanical properties of trabecular bone positively correlate with volume fraction [10]. It is possible that trabecular bone volume fraction does not increase with body mass because the bones would become too heavy and too metabolically expensive to maintain and transport

Methods

Results

Conclusion