Torsional resistance as a principal component of the structural design of long bones: Comparative multivariate evidence in birds

Margerie, Emmanuel de; Sanchez, Sophie; Cubo, Jorge; Castanet, J.

doi:10.1002/ar.a.20141

Cited by 116 publications

(174 citation statements)

References 64 publications

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“…Instead, avian hindlimb bones have often been assumed to be loaded primarily in longitudinal bending, consistent with the parasagittal orientation of the lower limb (Alexander et al, 1979b;Biewener, 1982;Cubo and Casinos, 1998;de Margerie et al, 2005). However, as noted above, the results here show that the emu femur and TBT are predominantly loaded in torsion.…”

Section: Torsion Versus Axial Loading In Tetrapod Hindlimb Bonessupporting

confidence: 70%

Skeletal strain patterns and growth in the emu hindlimb during ontogeny

Main

Biewener

2007

Journal of Experimental Biology

154

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SUMMARY Most studies examining changes in mechanical performance in animals across size have typically focused on inter-specific comparisons across large size ranges. Scale effects, however, can also have important consequences in vertebrates as they increase in size and mass during ontogeny. The goal of this study was to examine how growth and development in the emu (Dromaius novaehollandiae) hindlimb skeleton reflects the demands placed upon it by ontogenetic changes in locomotor mechanics and body mass. Bone strain patterns in the femur and tibiotarsus (TBT) were related to ontogenetic changes in limb kinematics, ground reaction forces, and ontogenetic scaling patterns of the cross-sectional bone geometry, curvature and mineral ash content over a 4.4-fold increase in leg length and 65-fold increase in mass. Although the distribution of principal and axial strains remained similar in both bones over the ontogenetic size range examined, principal strains on the cranial femur and caudal femur and TBT increased significantly during growth. The ontogenetic increase in principal strains in these bones was likely caused by isometry or only slight positive allometry in bone cross-sectional geometry during growth, while relative limb loading remained similar. The growth-related increase in bone strain magnitude was likely mitigated by increased bone mineralization and decreased curvature. Throughout most of ontogeny, shear strains dominated loading in both bones. This was reflected in the nearly circular cross-sectional geometry of the femur and TBT, suggesting selection for resistance to high torsional loads, as opposed to the more eccentric cross-sectional geometries often associated with the bending common to tetrapods with parasagittal limb orientations, for which in vivobone strains have typically been measured to date.

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Section: Torsion Versus Axial Loading In Tetrapod Hindlimb Bonessupporting

confidence: 70%

Skeletal strain patterns and growth in the emu hindlimb during ontogeny

Main

Biewener

2007

Journal of Experimental Biology

154

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“…Bars ¼ 200 lm (a, d), 2 mm (b, c, e-g) posthatch development cannot be simply extrapolated to the embryonic TMT skeleton, and a relationship between bone porosity and deposition rates has still remained controversial (Starck and Chinsamy, 2002). However, because bone growth requires sufficient nutrient and mineral supplies from dense vascular network (de Ricqlés et al, 1991) and the porosity of bone reflects the degree of bone vascularization (de Margerie et al, 2005), it may be worth considering the relation of growth progression and three-dimensional orientation of channels in which vascular network resides. Our SEM observations showed that the formation of bony struts and trabeculae resulted in the layered arrays of channels in the cylindrical bone wall.…”

Section: Discussionmentioning

confidence: 99%

Development of the Tarsometatarsal Skeleton by the Lateral Fusion of Three Cylindrical Periosteal Bones in the Chick Embryo (Gallus gallus)

Namba

Yamazaki

Yuguchi

et al. 2010

The Anatomical Record

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An avian tarsometatarsal (TMT) skeleton spanning from the base of toes to the intertarsal joint is a compound bone developed by elongation and lateral fusion of three cylindrical periosteal bones. Ontogenetic development of the TMT skeleton is likely to recapitulate the changes occurred during evolution but so far has received less attention. In this study, its development has been examined morphologically and histologically in the chick, Gallus gallus. Three metatarsal cartilage rods radiating distally earlier in development became aligned parallel to each other by embryonic day 8 (ED8). Calcification initiated at ED8 in the midshaft of cartilage propagated cylindrically along its surface. Coordinated radial growth by fabricating bony struts and trabeculae resulted in the formation of three independent bone cylinders, which further became closely apposed with each other by ED13 when the periosteum began to fuse in a back-to-back orientation. Bone microstructure, especially orientation of intertrabecular channels in which blood vasculature resides, appeared related to the observed rapid longitudinal growth. Differential radial growth was considered to delineate eventual surface configurations of a compound TMT bone, but its morphogenesis preceded the fusion of bone cylinders. Bony trabeculae connecting adjacent cylinders emerged first at ED17 in the dorsal and ventral quarters of intervening tissue at the mid-diaphyseal level. Posthatch TMT skeleton had a seemingly uniform mid-diaphysis, although the septa persisted between original marrow cavities. These findings provide morphological and histological bases for further cellular and molecular studies on this developmental process. Anat Rec, 293:1527Rec, 293: -1535

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“…Because locomotion is one of the most frequent and demanding behaviors in which limbs are used (Biewener, 1990;Biewener, 1993), this diversity in limb design is frequently attributed to variation in the mechanical loads that bones experience during locomotion (Currey, 1984;Bertram and Biewener, 1988;Blob, 2001;Currey, 2002;Lieberman et al, 2004;de Margerie et al, 2005). Damage or fracture of bones during locomotion could have serious, even fatal, consequences for animals.…”

Section: Introductionmentioning

confidence: 99%

Loading mechanics of the femur in tiger salamanders (Ambystoma tigrinum) during terrestrial locomotion

Sheffield

Blob

2011

Journal of Experimental Biology

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SUMMARYSalamanders are often used as representatives of the basal tetrapod body plan in functional studies, but little is known about the loads experienced by their limb bones during locomotion. Although salamanders' slow walking speeds might lead to low locomotor forces and limb bone stresses similar to those of non-avian reptiles, their highly sprawled posture combined with relatively small limb bones could produce elevated limb bone stresses closer to those of avian and mammalian species. This study evaluates the loads on the femur of the tiger salamander (Ambystoma tigrinum) during terrestrial locomotion using threedimensional measurements of the ground reaction force (GRF) and hindlimb kinematics, as well as anatomical measurements of the femur and hindlimb muscles. At peak stress (29.8±2.0% stance), the net GRF magnitude averaged 0.42body weights and was directed nearly vertically for the middle 20-40% of the contact interval, essentially perpendicular to the femur. Although torsional shear stresses were significant (4.1±0.3MPa), bending stresses experienced by the femur were low compared with other vertebrate lineages (tensile: 14.9±0.8MPa; compressive: -18.9±1.0MPa), and mechanical property tests indicated yield strengths that were fairly standard for tetrapods (157.1±3.7MPa). Femoral bending safety factors (10.5) were considerably higher than values typical for birds and mammals, and closer to the elevated values calculated for reptilian species. These results suggest that high limb bone safety factors may have an ancient evolutionary history, though the underlying cause of high safety factors (e.g. low limb bone loads, high bone strength or a combination of the two) may vary among lineages.

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Torsional resistance as a principal component of the structural design of long bones: Comparative multivariate evidence in birds

Cited by 116 publications

References 64 publications

Skeletal strain patterns and growth in the emu hindlimb during ontogeny

Skeletal strain patterns and growth in the emu hindlimb during ontogeny

Development of the Tarsometatarsal Skeleton by the Lateral Fusion of Three Cylindrical Periosteal Bones in the Chick Embryo (Gallus gallus)

Loading mechanics of the femur in tiger salamanders (Ambystoma tigrinum) during terrestrial locomotion

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