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

Lee AH, Simons EL - PeerJ (2015)

Bottom Line: Our results show that humeri from bats across a wide phylogenetic and body size range do not contain any laminar bone.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Anatomy, Midwestern University , Glendale, AZ , USA.

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.

No MeSH data available.


Related in: MedlinePlus

Histology of humeri in sampled bats ordered by ascending body mass.Non-polarized imagery reveals avascular to poorly vascularized compacta. Representative views are from the anterior octant of (A) Rhinolophus lepidus, (B) Macrotus californicus, (C) Phyllostomus discolor, (D) Noctilio leporinus, (E) Rousettus leschenaultii, and (F) Pteropus vampyrus. Periosteal surface points up in each panel. Scale bar equals (A) 150 µm, (B) 200 µm, (C) 300 µm, (D & E) 400 µm, and (F) 800 µm. Digital slides are available at http://paleohistology.appspot.com.
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fig-2: Histology of humeri in sampled bats ordered by ascending body mass.Non-polarized imagery reveals avascular to poorly vascularized compacta. Representative views are from the anterior octant of (A) Rhinolophus lepidus, (B) Macrotus californicus, (C) Phyllostomus discolor, (D) Noctilio leporinus, (E) Rousettus leschenaultii, and (F) Pteropus vampyrus. Periosteal surface points up in each panel. Scale bar equals (A) 150 µm, (B) 200 µm, (C) 300 µm, (D & E) 400 µm, and (F) 800 µm. Digital slides are available at http://paleohistology.appspot.com.

Mentions: In most sections, the curvature of the periosteal surface means that the tangent line needed to measure circumferential and radial canals changes across the cortical octant. The repeated referencing of each canal to a variable periosteal tangent line is time-consuming and increases the likelihood of measurement error. We standardized the tangent line and thereby increased the throughput of canal measurement by uncurving each cortical octant relative to the periosteal surface using the “Straighten” function in ImageJ (1.49b, National Institutes of Health, USA). Once a cortical quadrant is “straightened”, the periosteal surface is aligned with the horizontal (Figs. 2 and 3) and a constant reference line is established. To assess the extent of image deformation on canal orientation, we overlaid a graphical layer containing known test angles relative to the periosteal surface and circular profiles prior to straightening. On average, image deformation is acceptable; test angles deviate no more than 5 degrees from their original values, and circular profiles maintain aspect ratios between 1.00–1.17. At least for the currently sampled bones with relatively thin cortices, the “Straighten” function preserves original orientation data.


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

Lee AH, Simons EL - PeerJ (2015)

Histology of humeri in sampled bats ordered by ascending body mass.Non-polarized imagery reveals avascular to poorly vascularized compacta. Representative views are from the anterior octant of (A) Rhinolophus lepidus, (B) Macrotus californicus, (C) Phyllostomus discolor, (D) Noctilio leporinus, (E) Rousettus leschenaultii, and (F) Pteropus vampyrus. Periosteal surface points up in each panel. Scale bar equals (A) 150 µm, (B) 200 µm, (C) 300 µm, (D & E) 400 µm, and (F) 800 µm. Digital slides are available at http://paleohistology.appspot.com.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4359045&req=5

fig-2: Histology of humeri in sampled bats ordered by ascending body mass.Non-polarized imagery reveals avascular to poorly vascularized compacta. Representative views are from the anterior octant of (A) Rhinolophus lepidus, (B) Macrotus californicus, (C) Phyllostomus discolor, (D) Noctilio leporinus, (E) Rousettus leschenaultii, and (F) Pteropus vampyrus. Periosteal surface points up in each panel. Scale bar equals (A) 150 µm, (B) 200 µm, (C) 300 µm, (D & E) 400 µm, and (F) 800 µm. Digital slides are available at http://paleohistology.appspot.com.
Mentions: In most sections, the curvature of the periosteal surface means that the tangent line needed to measure circumferential and radial canals changes across the cortical octant. The repeated referencing of each canal to a variable periosteal tangent line is time-consuming and increases the likelihood of measurement error. We standardized the tangent line and thereby increased the throughput of canal measurement by uncurving each cortical octant relative to the periosteal surface using the “Straighten” function in ImageJ (1.49b, National Institutes of Health, USA). Once a cortical quadrant is “straightened”, the periosteal surface is aligned with the horizontal (Figs. 2 and 3) and a constant reference line is established. To assess the extent of image deformation on canal orientation, we overlaid a graphical layer containing known test angles relative to the periosteal surface and circular profiles prior to straightening. On average, image deformation is acceptable; test angles deviate no more than 5 degrees from their original values, and circular profiles maintain aspect ratios between 1.00–1.17. At least for the currently sampled bones with relatively thin cortices, the “Straighten” function preserves original orientation data.

Bottom Line: Our results show that humeri from bats across a wide phylogenetic and body size range do not contain any laminar bone.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Anatomy, Midwestern University , Glendale, AZ , USA.

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.

No MeSH data available.


Related in: MedlinePlus