Development of limb bone laminarity in the homing pigeon (Columba livia).

Rylee S Mcguire,Andrew H Lee,Kelly Ezell,Raffi Ourfalian

doi:10.7717/peerj.9878

Abstract

BackgroundBirds show adaptations in limb bone shape that are associated with resisting locomotor loads. Whether comparable adaptations occur in the microstructure of avian cortical bone is less clear. One proposed microstructural adaptation is laminar bone in which the proportion of circumferentially-oriented vascular canals (i.e., laminarity) is large. Previous work on adult birds shows elevated laminarity in specific limb elements of some taxa, presumably to resist torsion-induced shear strain during locomotion. However, more recent analyses using improved measurements in adult birds and bats reveal lower laminarity than expected in bones associated with torsional loading. Even so, there may still be support for the resistance hypothesis if laminarity increases with growth and locomotor maturation.MethodsHere, we tested that hypothesis using a growth series of 17 homing pigeons (15–563 g). Torsional rigidity and laminarity of limb bones were measured from histological sections sampled from midshaft. Ontogenetic trends in laminarity were assessed using principal component analysis to reduce dimensionality followed by beta regression with a logit link function.ResultsWe found that torsional rigidity of limb bones increases disproportionately with growth, consistent with rapid structural compensation associated with locomotor maturation. However, laminarity decreases with maturity, weakening the hypothesis that high laminarity is a flight adaptation at least in the pigeon. Instead, the histological results suggest that low laminarity, specifically the relative proportion of longitudinal canals aligned with peak principal strains, may better reflect the loading history of a bone.

Highlights

Laminar bone is a form of fibrolamellar bony tissue in which the primary vascular canal network is organized into concentric interconnected layers (Francillon-Vieillot et al, 1990)
While walking, chickens and emus generate large torsional loads in the femur and tibiotarsus (Biewener, Swartz & Bertram, 1986; Carrano & Biewener, 1999; Main & Biewener, 2007). If these loading patterns are similar across birds, the elevated laminarity observed in humeri, ulnae, femora, and tibiotarsi of many avian species may be a general feature of limb bones loaded habitually in torsion (De Margerie et al, 2005)
At mid-diaphysis, the cortical bone in the limbs of the sampled pigeons become increasingly compact with growth (Tables S2–S6)

Summary

Introduction

Laminar bone is a form of fibrolamellar bony tissue in which the primary vascular canal network is organized into concentric interconnected layers (Francillon-Vieillot et al, 1990). Theoretical modeling suggests that these limb bones experience locomotor-induced torsion (i.e., by flapping in the humerus and ulna and by walking in the femur and tibiotarsus) (Pennycuick, 1967). While walking, chickens and emus generate large torsional loads in the femur and tibiotarsus (Biewener, Swartz & Bertram, 1986; Carrano & Biewener, 1999; Main & Biewener, 2007) If these loading patterns are similar across birds, the elevated laminarity observed in humeri, ulnae, femora, and tibiotarsi of many avian species may be a general feature of limb bones loaded habitually in torsion (De Margerie et al, 2005). The histological results suggest that low laminarity, the relative proportion of longitudinal canals aligned with peak principal strains, may better reflect the loading history of a bone

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Discussion

Conclusion