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

Abstract

Background Birds 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. Methods Here, 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. Results We 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.

The osteohistological variability in the evolution of basal avialans

“…However, as of the Ornithothoraces, the thickness of these marginal bone layer decreases considerably, in general rarely exceeding 35% of the total bone cortex in the case of the ICL and 15% in the case of the OCL (Figures 3‐7; Tables 3 and 4). The pattern for the marginal bone layers is similar to what is observed in the Neornithes, in general never exceeding 15 to 20% of the total bone cortex (Bourdon et al., 2009; Chinsamy, 1995; Dabee, 2013; de Margerie, 2002; McGuire et al., 2020; Ponton et al., 2004; Starck & Chinsamy, 2002). This decrease in the thickness of the ICL becomes more prominent in the non‐ornithurine euornithians and the extinct ornithurines exhibiting uninterrupted bone growth.…”

“…Our comparisons of the studied osteohistological features in basal avians indicate that the microstructure and formation observed in extant Neornithes for the ICL and OCL originated prior to the crown, specifically as of the Ornithothoraces. A potential explanation for this noticeable decrease of the thickness in these two marginal bone layers is probably the evolutionary increase in bone growth rates throughout the basal avians to reach values similar and/or equal to those observed in extant neornithines, which in general reach full somatic and sexual maturity in more or less a year (Figure 8; Brusatte et al., 2015; Chinsamy‐Turan, 2005; McGuire et al., 2020; Ponton et al., 2004; Prondvai et al., 2020; Starck & Ricklefs, 1998). In the case of the ICL, there is another reasonable explanation which is most likely associated with the increase in medullar resorption during the late ontogenetic stage prior to full somatic maturity (McGuire et al., 2020).…”

“…A potential explanation for this noticeable decrease of the thickness in these two marginal bone layers is probably the evolutionary increase in bone growth rates throughout the basal avians to reach values similar and/or equal to those observed in extant neornithines, which in general reach full somatic and sexual maturity in more or less a year (Figure 8; Brusatte et al., 2015; Chinsamy‐Turan, 2005; McGuire et al., 2020; Ponton et al., 2004; Prondvai et al., 2020; Starck & Ricklefs, 1998). In the case of the ICL, there is another reasonable explanation which is most likely associated with the increase in medullar resorption during the late ontogenetic stage prior to full somatic maturity (McGuire et al., 2020). This medullar resorption is, in the case of female birds, a mean to acquire minerals for the formation of calcium shells around their eggs.…”

A histological survey of avian post-natal skeletal ontogeny

“…Certainly, a larger sample size and additional sectioning of each element would provide a more rigorous test, but preliminary results indicate that laminar vascularity does not dominate the humerus in a majority, or even many, birds. This corroborates recent findings in homing pigeons (McGuire et al, 2020) and bats (Lee & Simons, 2015). Of particular note, McGuire et al ( 2020) observed a higher degree in laminarity in younger individuals, with vascular orientation becoming increasingly longitudinal with maturity.…”

“…Galloanseriforms understandably draw the attention of researchers because of their importance in the poultry industry, and because specimens are readily available since they are domestically bred and farmed. Comparatively few studies have investigated histological characteristics outside of these early-diverging clades (de Margerie et al, 2004;Watanabe, 2018;McGuire et al, 2020).…”