Collagen fiber orientation pattern, osteon morphology and distribution, and presence of laminar histology do not distinguish torsion from bending in bat and pigeon wing bones

Abstract

Bone can adapt to its habitual load history at various levels of its hierarchical structural and material organization. However, it is unclear how strongly a bone's structural characteristics (e.g. cross‐sectional shape) are linked to microstructural characteristics (e.g. distributions of osteons and their vascular canals) or ultrastructural characteristics [e.g. patterns of predominant collagen fiber orientation (CFO)]. We compared the cross‐sectional geometry, microstructure and ultrastructure of pigeon (Columba livia domestica) humeri, and third metacarpals (B3M) and humeri of a large bat (Pteropus poliocephalus). The pigeon humerus is habitually torsionally loaded, and has unremodeled (‘primary’) bone with vessels (secondary osteons are absent) and high ‘laminarity’ because a large majority of these vessels course circularly with respect to the bone's external surface. In vivo data show that the bat humerus is also habitually torsionally loaded; this contrasts with habitual single‐plane bending of the B3M, where in vivo data show that it oscillates back and forth in the same direction. In contrast to pigeon humeri where laminar bone is present, the primary tissue of these bat bones is largely avascular, but secondary osteons are present and are usually in the deeper cortex. Nevertheless, the load history of humeri of both species is prevalent/predominant torsion, producing diffusely distributed shear stresses throughout the cross‐section. We tested the hypothesis that despite microstructural/osteonal differences in these pigeon and bat bones, they will have similar characteristics at the ultrastructural level that adapt each bone for its load history. We postulate that predominant CFO is this characteristic. However, even though data reported in prior studies of bones of non‐flying mammals suggest that CFO would show regional variations in accordance with the habitual ‘tension regions’ and ‘compression regions’ in the direction of unidirectional habitual bending, we hypothesized that alternating directions of bending within the same plane would obviate these regional/site‐specific adaptations in the B3M. Similarly, but for other reasons, we did not expect regional variations in CFO in the habitually torsionally loaded bat and pigeon humeri because uniformly oblique‐to‐transverse CFO is the adaptation expected for the diffusely distributed shear stresses produced by torsion/multidirectional loads. We analyzed transverse sections from mid‐diaphyses of adult bones for CFO, secondary osteon characteristics (size, shape and population density), cortical thickness in quadrants of the cortex, and additional measures of cross‐sectional geometry, including the degree of circular shape that can help distinguish habitual torsion from bending. Results showed the expected lack of regional CFO differences in quasi‐circular shaped, and torsionally loaded, pigeon and bat humeri. As expected, the B3M also lacked CFO variations between the opposing cortices along the plane of bending, and the quasi‐elliptical cross‐se...

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

“…Recent work on adult feral pigeons reveals “high” laminarity at least in the humerus ( Skedros & Doutré, 2019 ). The contrasting results suggest that laminarity in homing pigeons may not be as representative of the wild-type as assumed by the present study.…”

“…In adult birds, collagen fibers with oblique-to-transverse orientation (i.e., spiraling 45 -90 to the longitudinal axis) are especially abundant throughout the cortex of bones shaped to resist torsion (De Margerie et al, 2005). Similar collagen fiber orientation evolved independently in adult birds and at least one species of fruit bat (Skedros & Doutré, 2019) suggesting that it may be a fundamental adaptation of vertebrate flapping flight. If so, we expect collagen fiber obliquity and torsional rigidity of wing bones to increase with locomotor maturity.…”

The effects of growth rate and biomechanical loading on bone laminarity within the emu skeleton

“…Laminarity indices can be quite variable among individuals in some species. The pigeon humerus, which has been shown to experience large torsional loads, has been documented to exhibit both high and low laminarity in different individuals (Lee & Simons, 2015; Ourfalian, Ezell & Lee, 2016; Skedros & Doutré, 2019). Similarly, a pooled sample of humeri from eight Red-tailed hawks show LI values that range from 0.30–0.70 (Simons & O’Connor, 2012; Marelli & Simons, 2014).…”

“…In addition, the torsional resistance in bones may more likely be linked to the specific orientation of another histological feature: collagen fibers. Collagen fiber orientation (CFO) has been shown to reflect principal strain distributions (Riggs, Lanyon & Boyde, 1993; Skedros & Hunt, 2004; Skedros, Hunt & Bloebaum, 2004; Skedros & Doutré, 2019). Analysis of CFO is beyond the scope of the current study.…”

Mineralized Collagen Fibrils: An Essential Component in Determining the Mechanical Behavior of Cortical Bone

“…Observations in primate long bones suggest that the collagen fiber orientation is predominantly longitudinally aligned, indicating the possible adaptation process of collagen fiber to tensional loading . However, evidence to the contrary suggests that collagen fiber orientation in bat and pigeon humeri could not fully represent the torsional loading and bending history …”