Wing bone laminarity is not an adaptation for torsional resistance in bats

Abstract

Torsional loading is a common feature of skeletal biomechanics during vertebrate flight. The importance of resisting torsional loads is best illustrated by the convergence of wing bone structure (e.g., long with thin walls) across extant bats and birds. Whether or not such a convergence occurs at the microstructural level is less clear. In volant birds, the humeri and ulnae often contain abundant laminar bony tissue in which primary circumferential vascular canals course concentrically about the long axis of the bone. These circumferential canals and the matrix surrounding them presumably function to resist the tissue-level shear stress caused by flight-induced torsion. Here, we assess whether or not laminar bone is a general adaptive feature in extant flying vertebrates using a histological analysis of bat bones. We sampled the humeri from six adult taxa representing a broad phylogenetic and body size range (6–1,000 g). Transverse thick sections were prepared from the midshaft of each humerus. Bone tissue was classified based on the predominant orientation of primary vascular canals. Our results show that humeri from bats across a wide phylogenetic and body size range do not contain any laminar bone. Instead, humeri are essentially avascular in bats below about 100 g and are poorly vascularized with occasional longitudinal to slightly radial canals in large bats. In contrast, humeri from birds across a comparable size range (40–1,000 g) are highly vascularized with a wide range in bone laminarity. Phylogenetically-informed scaling analyses reveal that the difference in vascularity between birds and bats is best explained by higher somatic relative growth rates in birds. The presence of wing bone laminarity in birds and its absence in bats suggests that laminar bone is not a necessary biomechanical feature in flying vertebrates and may be apomorphic to birds.

Interpreting the three‐dimensional orientation of vascular canals and cross‐sectional geometry of cortical bone in birds and bats

“…Previous studies have noted that bats tend to be poorly vascularized or avascular (Foote & Hrdlicka, ; Enlow & Brown, ; de Ricqlès et al. ; Bennett & Forwood, ; Lee & Simons, ). Monitor lizards are also known to have inconsistent vascularization, with cortices that can be completely free of vascular canals.…”

“…; de Boef et al. ; Marelli & Simons, ; Lee & Simons, ) creates a laminarity index based on the proportion of circumferential canal area out of total canal area. In a histological slice, the area of longitudinal canals measured is underestimated, as only a small cross‐section of the canal is measured, as opposed to a transverse section of circumferential or radial canals.…”

“…We chose the largest locally accessible species of bats and birds because bones below a certain size often have fewer canals (de Buffrénil et al. ; Lee & Simons, ). The bat specimens were borrowed from the Department of Natural History – Mammology at the Royal Ontario Museum (Toronto, Canada).…”

“…Most birds experience very rapid growth, as they need to acquire flight quickly to feed themselves (Erickson et al. ); bats, however, experience slower growth (Kunz & Stern, ; Lee & Simons, ). Skedros & Hunt () found a significantly higher laminarity index in adult turkey ulnae than in sub‐adult bones.…”

Inspiration for wing design: how forelimb specialization enables active flight in modern vertebrates

“…At the micro-level, laminar bones enable better torsional resistance [33]. Bird wing bones are frequently highly laminar with circular canals [28,34] (figure 2c), whereas bat wing bones lack this laminarity [35].…”